\\n\\n
Released this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\\n\\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
Note: Edited in March 2021
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'IntechOpen is proud to announce that 191 of our authors have made the Clarivate™ Highly Cited Researchers List for 2020, ranking them among the top 1% most-cited.
\n\nThroughout the years, the list has named a total of 261 IntechOpen authors as Highly Cited. Of those researchers, 69 have been featured on the list multiple times.
\n\n\n\nReleased this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\n\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
Note: Edited in March 2021
\n'}],latestNews:[{slug:"intechopen-signs-new-contract-with-cepiec-china-for-distribution-of-open-access-books-20210319",title:"IntechOpen Signs New Contract with CEPIEC, China for Distribution of Open Access Books"},{slug:"150-million-downloads-and-counting-20210316",title:"150 Million Downloads and Counting"},{slug:"intechopen-secures-indefinite-content-preservation-with-clockss-20210309",title:"IntechOpen Secures Indefinite Content Preservation with CLOCKSS"},{slug:"intechopen-expands-to-all-global-amazon-channels-with-full-catalog-of-books-20210308",title:"IntechOpen Expands to All Global Amazon Channels with Full Catalog of Books"},{slug:"stanford-university-identifies-top-2-scientists-over-1-000-are-intechopen-authors-and-editors-20210122",title:"Stanford University Identifies Top 2% Scientists, Over 1,000 are IntechOpen Authors and Editors"},{slug:"intechopen-authors-included-in-the-highly-cited-researchers-list-for-2020-20210121",title:"IntechOpen Authors Included in the Highly Cited Researchers List for 2020"},{slug:"intechopen-maintains-position-as-the-world-s-largest-oa-book-publisher-20201218",title:"IntechOpen Maintains Position as the World’s Largest OA Book Publisher"},{slug:"all-intechopen-books-available-on-perlego-20201215",title:"All IntechOpen Books Available on Perlego"}]},book:{item:{type:"book",id:"1940",leadTitle:null,fullTitle:"Bio-Inspired Computational Algorithms and Their Applications",title:"Bio-Inspired Computational Algorithms and Their Applications",subtitle:null,reviewType:"peer-reviewed",abstract:"Bio-inspired computational algorithms are always hot research topics in artificial intelligence communities. 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D. degrees in intellectual information systems and Innovative life science from University of Toyama, Toyama, Japan in 2008 and 2011, respectively. From 2005 to 2006, he was a technical support engineer in Wicrosoft Co. Ltd., Shanghai, China. He has received the Outstanding Academic Performance Award of IEICE Hokuriku Branch in 2008, the Outstanding Self-financed Students Abroad Award of Chinese Government from China Scholarship Council in 2009, the Outstanding Academic Achievement Award of IPSJ Hokuriku Branch in 2011, and the Outstanding Doctoral Award of University of Toyama in 2011. He is currently an associate research fellow at the Key Laboratory of Embedded System and Service Computing, Ministry of Education, Tongji University, Shanghai 200092, China. 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In more than 100 years, the Brazilian industries have covered most of the regions of their country and have developed various areas of the civil society. But today, it is not possible to approximate and explain the role of entrepreneurship toward the practice of innovation, since many entrepreneurs still come to the market with similar ideas, creating some wealth, despite most of them are still not innovating [1]. However, Drucker [2] has suggested that innovation is directly related to the economic or social potential of entrepreneurship change, which consists in creating and using new products, processes, organizations or production systems. It represents the key to competitiveness and knowledge development [3], but it still occurs in very few Brazilian organizations [1].
In [4], Brazil is ranked in the 69th position among 128 countries, behind the economies of Panama, Colombia, Mongolia, South Africa and others. The Global Innovation Index assists in adapting policies for long-term development to increase productivity and generate employment. According to Ref. [4], the growth forecasts for 2016 were not optimistic as well as the economic recovery slowed down even in high-income countries like the United States, Japan and some European countries. At the same time, low- and middle-income countries face lower growth expectations than they were 2 years ago. Africa, Latin America and the Caribbean have reduced their growth rates to levels considered modest by the report, and for Brazil, this impact was mainly felt by the fall in commodity prices, which increases the economic fragility of the country. In this scenario, innovation is distant, since there is no wealth for investment in research and development [4]. The Central Bank of Brazil reports that, since 1980, the country has followed a sinusoidal trajectory with its economic growth (Figure 1), considering that the past 3 years are with negative results.
Brazil’s economic growth (1980–2014). Source: [
This reality has become a fact, since this country of Latin America has not evolved beyond its GDP, demonstrating that Brazilian organizations do not invest in innovation. It is important to note that Brazilian companies, research institutions and government are making an effort to keep on their agenda the generation of innovation. However, at a moment where Brazil has entered in a period of economic turbulence, it has become necessary for the country to overcome the short-term constraints and to stick to the commitments that generate results with innovation. An interaction and a stronger cooperation within Latin America could perhaps contribute to the recovery of the economy and consequently reach a higher level of innovations in the country [4]. An Innovation Survey (PINTEC) highlights that for the period of 2012–2014, Brazil had 132,529 innovation intense companies (industry and services). Those companies seek competitiveness and an improvement in financial performance, suffering a constant pressure on normative issues and legal impositions [6]. Still facing economic, social, political and environmental problems, the Brazilian industry has been declining nowadays. According to data released by the Brazilian Institute of Geography and Statistics (IBGE) in February 2017, the Brazilian industrial production fell by 6.6% in 2016 compared to 2015. In this context, the effort of companies to invest and generate innovations stayed at a minimum level of investment, due to the lack of both sustainability and expansion in productive capacity.
So, in a Brazilian context, what would be the link between a centenary background of entrepreneurship activity and an almost inexistent rate of consistent innovation intensity?
The investigation of the dynamics between the entrepreneurial reality, sustainability and innovations in the leading organizations of Serra Gaúcha (RS), Brazil constitutes the main mandate of the Multidisciplinary Research Group in Innovation and Competitiveness [7], in partnership with the Nucleus of Innovation, Entrepreneurship and Sustainability [8]. Both Groups are associated to the MSc and Doctorate Programs in Administration of the University of Caxias do Sul (RS), Brazil, and focus on the development of new research paths based on integration and interdisciplinary. One of their objectives is to develop new evaluation tools on the potential of Brazilian companies to allow a better recognition of business realities in terms of entrepreneurial development, sustainability and innovation in organizations.
As introduced by Schumpeter in 1934, the concept of entrepreneurship is considered as the main generator of companies’ competitiveness as well as a guarantor for their development [9]. It constitutes the elements for the local leading organizations to generate the development of a region and to improve the quality of life of a community [10]. In that perspective, the Brazilian entrepreneurs know how to take advantage of the opportunities of the local business dynamic, by improving their organizational characteristics that allow their development and competitiveness. However, data on the issues of entrepreneurship and innovation development in Brazil are contradictory, and no scientific link has yet been scientifically established [1]. However, the importance of innovation for business growth and the economic development of the regions is already recognized in the literature and is of common interest to all actors in a society of organizations [11, 12]. Porter [13], in his book “The Competitive Advantage of Nations,” examines why some nations achieve success in international competition and others fail. The author reports that business success is based on its economic environment, the relevance of its government policies and the presence and efficiency of its support institutions. In this context, innovations have assumed a fundamental role in all the advanced economies of the world and are considered as essential for the growth and the development of a nation. However, since it is not possible to directly insert the practice of innovation into entrepreneurship and, since the Brazilian entrepreneurs do undertake action and also create wealth despite of not innovating [1]; why cannot we directly link entrepreneurship to innovation in most of the Brazilian economy?
A prosperous path to economic growth starts by enhancing the existing entrepreneurial potential in a country through support mechanisms that allow the economic development of the organizations [13]. The search for innovation is to ensure, if not enlarge, a market share of a company and to trigger impacts beyond the simple economic sphere. In this sense, and according to Lundvall [14], the innovation is the key to development and constitutes the economic and social advance of a region or a nation. Thus, the literature demonstrates that innovation can strongly contribute to the socio-economic development of a region, but does not guarantee its specific sustainable development [1]. In a strategic perspective, it is necessary for an organization to generate innovations as a part of its growth strategy, since it represents a basic standard for sustainable and innovative behavior toward its own development [15]. Through such dilemma, how to link the entrepreneurial effort to success in innovation? In that context, the results generated by sustainability could lead to a new and different level of innovation that generates organizational competitiveness and stability. Consequently, both sustainability and innovation can become critical to ensuring the competitiveness of organizations in the global context [16].
Concerns about sustainability and innovation are shown to managers as a new business strategy, since it provides a competitive differential, attracting the most demanding and frequent segments of society [17]. In order to ensure a “posture for innovation,” a society of organizations [18] seeks to implement mechanisms of sustainable management, involving the commitment of the actors themselves, aligned with a corporate strategy [19]. In such scenario, a logic emerges between entrepreneurship and the actions focused on change and innovation [16, 20]. Any innovative management strategies implemented in a leading organization envision a sustainable endogenous action. It then confirms their activities and actions toward a sustainable growth, which generates a variety of direct and indirect impacts within and outside the organization, and ranging from the consumers and employees to the regional community [21, 22].
Nevertheless, such action is limited to the organization’s own environment and does not grow in a socio-economic context. The Brazilian organizations innovate in isolation with no perspective of open diffusion [23, 24]. Who innovates does not divulge. Whoever undertakes imitates but does not innovate. Considering the socio-economic reality of Brazil and from the relevance of the issues related to entrepreneurship and organizational innovation in the country, the importance of sustainability for the organizations could become a solution for the integration of entrepreneurship with innovation. Such is our premise.
There is an extensive theoretical basis produced on the economic approach to entrepreneurship, and the foundations are related to the various schools of economic thought, such as the works of Schumpeter, Kirzner and Knight. According to Schumpeter [9], the entrepreneur is the one who destroys the existing economic order by introducing new products and services, by creating new forms of organizations or by exploiting new resources and materials. According to the economist, the entrepreneur is considered as an engine of the economic system who perceives the essence of entrepreneurship in the use of new business opportunities and by associating this concept with innovation [25]. Such a view leads to a trend toward economic growth and a value system peculiar to it, by creating an environment for product consumption, profit, competitiveness and organizational development [26].
The work of the economists has demonstrated a tendency to concentrate on issues such as wealth, commerce and social welfare. However, some authors like McClelland [27], Stevenson and Gumpert [28] and Gartner [29] introduced new perspectives of study on entrepreneurship. McClelland [27] postulates that the psychological approach considers that the entrepreneur has specific characteristics and behavior. Stevenson and Gumpert [28] believe that entrepreneurship research should focus on what the entrepreneur does and not on what he is, since the entrepreneurial process can be considered as a set of behaviors that the entrepreneur develops. Gartner [29] postulates that an entrepreneurial organization may be driven by the perception of the opportunities and the oriented actions, where the actions of the entrepreneur must be the starting point for theorizing about entrepreneurship.
The social approach to entrepreneurship proposes different levels of analysis that are above the individual entrepreneur. It looks into the interpersonal network, the organizational structure, the population, as well as the institutional environment [30]. Thus, such approach aggregates the traditional focus given to financial and market conditions, by introducing the issue of socio-economic sustainability. Pirich et al. [31] postulate that to encounter innovation actions in conjunction with an entrepreneurship reality, three key elements must be met: (1) the economic antecedents and an incentive of open business behavior; (2) a sophistication and efficiency in spreading knowledge generation and (3) an adequate capacity of the organizations, their employees and the individuals in general. Therefore, since researches tend to explain and define the “entrepreneur” by using axioms from different disciplines [27], the field of entrepreneurship can be studied through economic, psychological, social and organizational theories [29, 32, 33]. Consequently, the entrepreneurial perspectives of research include the study of the socio-economic forces that interfere in a regional economic development perspective, through certain axioms coming from the field of psychology, social sciences and organizational studies.
On one hand, a globalized and competitive market demands an increasingly strategic position, where companies are induced to establish defined strategies to maintain competitive advantage. On the other hand, consumers are pressing for quality, safety and different new products. In order to meet the pressures set by the consumers and the business world, companies are starting to pay attention to sustainability as a solution for growth. The role of the organizations in the development is an upward movement in an entire social system. It is characterized not only by endogenous economic and non-economic factors but also by induced and implemented exogenous elements, such as government policies and laws [34]. The idea of development is multidimensional and involves the economic, environmental, cultural, social and political dimensions [35, 36].
The concept of sustainability related to the use of available resources, whether natural, capital or human, has a process of historical construction that has resulted in indicators used by the various nations. In Brazil, “sustainable development” indicators are part of a series of international efforts to achieve the ideas and the principles formulated at the United Nations Conference on Environment and Development (UNCED), held in Rio de Janeiro in 1992 [37]. The publication of “Indicators of Sustainable Development – Brazil 2015,” from IBGE, brings data on the Brazilian reality through environmental, social, economic and institutional perspectives [37]. In this context, the economic effects are relatively easy to predict due to the important amount of developed instruments, but the social and environmental effects are more difficult to assess in advance because they involve many more variables, uncertainties and interactions. According to Schot and Geels [38], sustainable development requires the combination of technical and social changes, since they are deeply related. Therefore, the authors raise the necessity to transform the conventional understanding on sustainability, by incorporating new axioms of study that may facilitate the understanding on sustainability and its implications [39].
More recently, the concept of economic sustainability has appeared in the development of growth models. Until the 1970s, economic analyses only included the axioms of monetary flow and economic growth and relegating the limits of the natural environment to the background [40]. In 1971, Georgescu-Roegen [41] presented the idea that the economy must consider the law of entropy in the process of growth, given the fact that the expansion of the countries occurs by increasing the use of energy. Martine [42] analyzes the effects of energy consumption per capita, per country and relates it to the growth in population. The study concludes that the production and the consumption patterns of industrial economies continue to have a greater participation in their quality of life compared to the demographic growth of the developing countries. According to [43], one of the greatest challenges the world will face in this new millennium will be to make the organizations protective and improve the quality of the environment. The author postulates on the necessity to establish performance standards based on a judicious use of economic instruments and harmonious framework regulatory policies, since the organizations that will take the lead on the environmental issue will have to cover high risks to get significant competitive advantages in the market.
Today, the Brazilian economy experiences an internal crisis of frightening socio-economic size. The International Monetary Fund has presented negative economic data for the last 18 months and foresees a downturn for the entire South American continent. IMF [44] reported that “[…as the global recovery continues to struggle to gain its footing, growth in Latin America and the Caribbean has been marked down further and is likely to contract for the second consecutive year in 2016].” A further deterioration of the situation in Brazil could lead to a reduction in the demand for exports between trading partners in the region and an increase in the perception of risk, which could create more difficulties for the leading companies and become more vulnerable in an already fragile global market [44]. According to data from such survey, Brazil has shown the third worst growth performance projection in Latin America for 2015, 2016 and 2017, after Ecuador and Venezuela. Nevertheless, the situation is expected to improve in 2017, considering the proposed changes and measures by the Brazilian Government to boost fiscal sustainability, as well as the measures taken to liberalize and open the economy in order to significantly enhance the country’s competitiveness. IMF [44] also mentioned that growth in Latin America and the Caribbean is expected to remain below historical trends for a near future. In that context, it becomes relevant to rethink the dimensions of study about the companies, their economic performance and their real capacity to innovate.
In the literature, the debates about the environmental dimension of sustainability mainly consider the aspects that touch on the renewable natural resources, the impacts caused in the environment and the environmental actions used by the organizations [6, 45, 46]. For many years, the environmental issue has been understood as something that was not part of the organizational context. Companies were seen as economic institutions that were concerned with resolving economic problems (what they produce, how to produce and to whom to produce for). The environmental problems were perceived as outside threats to corporate profitability and established business practices. By the mid-1990s, a new phase of integration of environmental issues began to be implemented in the organizations. It proposes (1) the progressive introduction of a sustainability perspective; (2) the proliferation of collective engagements; (3) a greater interaction between the public and private spheres and (4) a greater involvement of the organized civil society. This scenario postulates that companies begin to focus their activities and actions toward sustainable development. The premise is that everything that is done inside an organization generates a variety of direct and indirect impacts inside and outside of its core competence, affecting consumers, community collaborators and the environment [22].
Given the evolution of society toward an environmental conscience, the organizations started to adopt a different posture than the original one aimed at achieving a maximum profit [43]. Thus, since it was essential for the organizations to not only maintain the role of producers of goods and services but also to become responsible for the environment in which they are inserted [47], new managerial tools and the adaptation of the existing management systems were developed to give a more effective approach to the problem. From that moment, the environmental issue became strategic within the organizations [48]. According to Fisher [47], the concept of environmental responsibility as an organizational strategic vector has recently gained ground. The author postulates that the companies start to realize that the respect for the environment and the valorization of man are among the main factors that directly reflect their success as a way to gain competitive advantage in the market. The environmental dimension emerges as a viable alternative, allowing economistic objectives to be maintained and incorporating environmental issues into the economic model of development [48]. Accordingly, the environmental dimension can become a new business strategy, as it provides a competitive edge and attracts the most demanding and environmentally conscious segments of society.
The social sustainability dimension, historically referred to as “social responsibility,” emerged as a way for the wealthiest to help the most in need [49]. The idea to let the organizations re-route some profit to “invest” in social development projects began to win support after World War II. It represented a new and stronger concept of the society of the organizations and it was socially making sense [18]. According to Melo Neto and Froes [50], social responsibility is a collective action aimed at fostering civility. The author postulates that social responsibility focuses on the “civic duty” of the organizations, which requires management, periodicity and systematization [47]. Considered as the “Father of Social Responsibility,” Bowen [51], in his book “Social Responsibilities of the Businessman,” initiated the modern era of the literature on social responsibility [52, 53].
A global movement of non-governmental organizations (NGOs) in search of values such as ethics, solidarity and trust has generated interest among various actors like the civil society, governments, investors, financiers, insurance companies, consumers and the media [54]. The diffusion of the concept of social responsibility in the organizations has occurred with greater scope with the creation of entities that disseminate and support companies in their actions of social responsibility. Generating profits for shareholders is no longer the sole concern of companies. Environmental, social, legal and ethical concerns have penetrated the strategic core of the companies, which have undergone a transition period in their way to re-think their strategies and their mission [55]. Any socially responsible company implements ethical practices with its established relationships, including the shareholders, clients, employees, suppliers or with the whole community. According to [56, p. 118], “[…a socially responsible company is the one that can generate profit as well as be beneficial for society.].”
Social responsibility actions enable the organizations to stand out from their environment. In addition, customers, suppliers, shareholders and stakeholders of the organization perceive those actions as a competitive edge, which makes them stand out from other competitors [57]. When a company is socially responsible, it attracts consumers and increases sales potential, generating greater profits for shareholders. Socio-economic sustainability is becoming a factor of differentiation in organizational management, being characterized as a business opportunity [48]. According to [58], being socially responsible is one of the cornerstones of business sustainability and must be considered as important as the concepts of quality, technology and the capacity for innovation.
The movement for sustainable development seems to be one of the most important social movements of this century. There are many voluntary initiatives related to sustainable development subscribed by the organizations. By committing themselves to sustainable development, entrepreneurs must necessarily change their way of acting in order to achieve economic sustainability and social sustainability, in a neoclassical perspective, in order to reduce their negative social impacts arising from a purely economic perspective. This requires a new way of looking at innovation, which leads to the idea of “innovation intensity” because of the implementation and the presence of sustainability [39].
Schumpeter [9] emphasizes the importance of innovations for the development of the economy of a country. The author postulates that the innovations introduced by innovative entrepreneurs constitute the main stimulus for the generation of a new economic cycle. Consequently, the innovation process is aimed at discovering, experimenting, developing, adopting new products, new production processes and new organizational forms [59, 60]. According to Drucker [2], innovation is the specific instrument of the entrepreneurial spirit. Dosi [60] postulates that the innovation is the search, the discovery, the experimentation and the adoption of new products, new processes and new organizational forms. Therefore, companies that want to increase their competitiveness feel the need to invest in practices aimed at the systematic development of new technologies, by seeking new ways to develop their activities, through the creation of new products, services or processes [61, 62].
In principle, innovation can be characterized as a type of change that introduces new organizational practices and they can be classified into four categories. The first one refers to products or services innovation, which represents the changes of a product or a service offered by an organization. The second one refers to process innovation, which represents the changes in the way products or services are created and distributed in an organization. The concept of management of innovation refers to the adaptations in the underlying mental models that shape the core competence of an organization. Finally, the concept of marketing innovation (competitive position) represents the changes in the context that the products or services are introduced in the market [12, 63]. Oslo Manual [64] introduces four main categories in its model: product, process, marketing and organization. According to Gallouj [65], the classification of Oslo Manual [64] brings the analysis of the restrictive definitions to the industrial sector, in addition to focus on technology innovations. However, considering the sectoral scope proposed and interpreted by Oslo Manual [64], innovations can occur in any sector of the economy. The adoption of an innovation respects a process where the deciders act to use innovation as the best available option. Rogers [23] points out the internal environment of the organization as one of the determinants that can contribute to the success or the failure of adopting a technology innovation. However, recent researches have linked social matters with the concept of innovation; denominated as social innovation. It poses its focus on the structures, the objects and their effects, the initiative capacity of the individuals, the organizations, the communities and their social movements. Those researches allow a new discussion about the process of innovation transfer and its role on the public policy institutions [57].
A sustainable, innovative organization “is not one that introduces novelty of any kind, but novelties that addresses the multiple dimensions of sustainability on a systematic basis and that reaches out positive results for society and the environment” [66, p. 105]. The current sustainability phenomenon generates an increasing capacity to differentiate products and services [24] and to aggregate the contexts of work and life environment [57]. Such differentiation search passes through the process of innovation [2, 57, 60, 67, 68]. Consequently, it only makes sense to postulate that entrepreneurs will begin to incorporate issue on sustainability for strategy arguments because of societal pressure as an alternative to develop growth through innovation. Based on this, it seems obvious to foresee a new perspective of research that integrates the theories of entrepreneurship, sustainability and innovation.
The objective of this research is to highlight the relevance of sustainability for organizations as a way to trigger the integration of entrepreneurship toward innovation in the Brazilian context. Various exploratory and descriptive researches on the dynamics of entrepreneurship, innovation and sustainability in the main organizations of the Serra Gaúcha (RS), Brazil was carried out through the Multidisciplinary Research Group on Innovation and Competitiveness [7], in partnership with a research Nucleus on Innovation, Entrepreneurship and Sustainability [8]. Evidenced among the following concepts: entrepreneurship, sustainability and innovation, the approach of this research was qualitative and the method used was documentary research because it articulated subjects where the theoretical dimensions and bases are unknown [69]. That is, highlighted the relevance of sustainability for organizations as a way to make a solution of integration to entrepreneurship for innovation in the Brazilian context exemplifying one or more trends in the behavior of a given phenomenon.
In the first 12 years of activities of the research Group, 40 Master’s and Doctoral dissertations were finalized, which offered a more concise and comprehensive look at the concepts of entrepreneurship, sustainability and innovation. The Group developed national and international academic and research activities, which have contributed to a clearer understanding of those themes. The object of the studies mainly focuses on leading sectors of the Brazilian economy, through the study of organizations situated in the southern region of Brazil. The researches refer to 11 sectors of the Brazilian economy (Figure 2).
Distribution of the GMIC/NIES researches in the Brazilian economy. Source: The authors.
The studies include the sectors of health, the metal-mechanic industry, technology, education, services, the furniture industry, the textile industry, the food and beverage industry (wine), the transportation and the energy industries and the MSE sectors. Most of the researches had a qualitative-exploratory character, with some key quantitative-descriptive ones. It generated the production of numerous articles in indexed journals and conferences and books chapters from international publishers. In general, the recurrent research objectives focus on identifying, describing and analyzing the dimensions of the entrepreneurial reality and the characteristics of innovation and sustainability adopted by the leading organizations of the Serra Gaúcha, Brazil.
The Group’s research activities were developed in three specific moments. The first period refers to the research activities related to the themes of entrepreneurship and innovation. The axiom of entrepreneurship was studied, based on Schumpeter’s [9] concept of innovation and through three aspects: the profile, processes and systems, seen as reactive or proactive entrepreneurial realities. The second period, from 2010, coincides with the integration of the PhD course with the MSc program, where research on innovation has taken a different strand. In addition to studying innovation as a proactive entrepreneurial dimension, the Group has been researching innovation through its process, by integrating the causes and stages, indicators and process models, and finally the study of innovation as a system. During the third period, a concentration of internal innovations in the organizations, in a restricted scale, emerges from the research results in several areas of economic activity, but without demonstrating a sustainable effect. This lack of sustained diffusion of innovations, coupled with a high degree of entrepreneurial activity, has led to question the very essence of the concepts of entrepreneurship and sustainability as structuring elements for the generation of innovation. Porter [13] reports that business success is based on its economic environment, where innovation has assumed a fundamental role in all the economies of the world and is considered essential for the growth and development of companies and nations. Nevertheless, the author is lacking in explaining how to establish the link between entrepreneurship and innovation.
The conceptual framework brings an integration of the axioms of entrepreneurship, sustainability and innovation and is supported by its economic, environmental and social relevance. The concept figure must dimension the cause-effect connections that may exist from one dimension to the other [70]. Figure 3 introduces the integrated context of the researches carried out.
Representation of the axioms of entrepreneurship, sustainability and innovation. Source: The authors.
The classification of the entrepreneurial axioms is contextualized in four dimensions: (1) economic [9, 61, 71], (2) social [72, 73], (3) organizational [2, 73] and (4) psychological [2, 27]. In order to study the question of sustainability, the (1) economic [74, 75], (2) environmental [13, 48] and (3) social [43, 54] dimensions were addressed. Finally, the study about innovations in the leading organizations of Serra Gaúcha uses the categories listed according to Oslo Manual [64]: (1) products (services) innovation; (2) process innovation; (3) organizational management innovation and (4) marketing innovation, considering that those categories have a greater proximity to the research objectives.
It is important to note that for the organizations, both sustainability and innovation can become critical to ensuring competitiveness in a global context. Not only to innovate constantly but also to innovate considering the social and economic dimensions of sustainability [37, 39]. The application to those dimensions makes the innovation process more sophisticated and demanding, which requires any organization to make a greater effort to meet such requirement. This leads to new perspectives in management of innovation.
The identification, the description and the analysis of the dimensions of the entrepreneurial reality, the characteristics of innovation and sustainability adopted by the leading organizations of the Serra Gaúcha present an eclectic panorama in terms of results.
In the health sector, studies demonstrate a structural shift from a technology-based economy to an “entrepreneurial health service” society. The results consider knowledge as a central resource, which is reflected by changes in the innovation process. Therefore, the innovation process is seen as a learning method to generate or to acquire new knowledge from the analysis of the local environment, where knowledge, skills and attitudes constitute the key elements in the identification and the execution of social and communicational actions. In a hospital context, the preponderant element for linking the dynamics of the innovations resides in the management of the environmental residues that constitute a stimulus to the improvement of the quality attributes of the health services. The surveys clearly show the presence of entrepreneurial activities, the employees’ concerns and their relevant actions toward the application of sustainability standards and the application of strategies and the creation and implementation of innovations to improve the quality of services to the population [76].
Researches in the metal-mechanical sector have demonstrated a relationship between the concepts of entrepreneurship, innovation and sustainability, both in historical and cultural contexts. The results show that the actions of the entrepreneurs are a demonstration of the strength of the attributes of the individuals, through the enhancement of opportunities and the use of the conditions that promote the economic development of the region, making it become one of the most dynamic sectors of the Brazilian economy [33]. In the region of Caxias do Sul, all entrepreneurs act either in micro, small, medium or large companies. The region represents the second metal-mechanical pole of Brazil, precisely because of this entrepreneurial force in the Serra Gaúcha region. The results identified the implantation of product and process innovations, which were all of incremental type and internal to each company. Large companies have sophisticated organizational innovation schemes, but they do not even represent 1% of the organizational population. The research corroborated with such position, considering that innovation is a new product or service, a new structure or administrative system, a new technological production process, a new plan or a program related to the members of the organization [77]. The research also pointed out the presence of environmental sustainability schemes, but exclusively within the large companies of the region. In addition, by having the duty to comply with the Brazilian environmental and capitalization laws, larger companies have developed strategies with a sustainability scheme to maintain a continuous flow of innovation, from the generation of ideas to internal applied research schemes [6, 21].
In technology development environments, the main results reveal a series of elements that preceded and influenced the constitution of the innovation environments and gave rise to different models, with their own characteristics. One main aspect that arises from the results is the entrepreneurial nature of the people who study, research and create new companies within the reality of a technology environment [78]. In addition, the researchers identified and analyzed the roles played by the university, the government and the business sector, as proposed in Etzkowitz’s [79] model. In that context, it was possible to evidence a new determinant in the constitution of the Brazilian science parks and technology incubators: leadership. It is considered as a new dimension of analysis to the triple helix model. Such concept emerges from empirical, spontaneous and endogenous movements of development and resides in any university management teams that generate a favorable environment for the promotion of entrepreneurship and innovation capable of creating and developing the necessary conditions for the implementation and the consolidation of scientific and technology environments [80]. The question of sustainability was identified as being present in the incubation and technology development environments in an incremental and discontinued way.
In the higher education sector, the researchers did not show an entrepreneurial specificity due to the nature of the economic branch and the rules and conditions that govern higher education institutions in Brazil [81, 82]. In terms of innovation, the dimension of innovation processes was evidenced through results that show antecedents for organizational learning, which impact as the outputs on the performance of the courses in the national education evaluation system [83, 84]. The most relevant aspects of the research show parity between the teaching practices and the practices of single and double learning cycles; through the informal relationships between the teachers and the outcomes of the course assessments and on the links between the companies, the non-academic professionals and student performance. Such reality is re-enforced through a pedagogical model that enhances such convergence [85]. From a sustainability perspective, the surveys did not present relevant data to identify a differentiated model.
In the service sector, the entrepreneurial issue occupied and demonstrated positive results with the proposed theories. Such convergence allowed verifying the presence of characteristics on the profile of the entrepreneurs, such as resilience [86]. The concept of innovation was identified in the study as a perspective for economic growth. The axiom of leadership appeared as a key element, considering the difficulties, the weaknesses and the socio-economic scarcities that Brazil encounters. The results showed the absence of a system of innovation in the creative industry in State of Rio Grande do Sul [87], which supports the idea that the entrepreneurial axiom is omnipresent in the Brazilian economic reality, but the concepts of innovation and sustainability for the services sector are almost inexistent. The research carried out in the Province of Quebec, Canada, in collaboration with the Ministry of Science, Innovation and Technology Development of the State of Rio Grande do Sul, shows a complete system of innovation and sustainability. The study allowed the Brazilian Ministry to confirm the absence of a system of innovation [10] and the necessity to have a structural perspective at the situation. The Canadian research has shown that the issue of sustainability is a key element in creating innovation environments and processes in a given region, through partnerships and by linking business creativity to the production of scientific knowledge and the economic development of the State [88].
In the furniture sector, research has demonstrated an entrepreneurial reality with industrial leaders and regionalism with this phenomenon. In terms of innovation, the results point out links between the use of specific resources (information system, people, knowledge management, alliance) and product innovation. It demonstrates that product innovation is the result of the use of specific resources, which constitutes the antecedents for innovation. The enterprises in the furniture industry have a joint research entity that look for information regarding the use of strategic resources, which extends their “innovative capabilities.” Nevertheless, the business community has not yet consolidated integrated sustainability schemes for the advancement and the development of innovations [89]. Only the greater companies pretended to realize innovations, but only in an exclusive internal way. Such pattern shows that the companies do not use schemes capable of producing innovations that impact on global performance.
In the food and beverages industry, more specifically in the Brazilian wine industry, researchers have shown the formulation of strategies from both entrepreneurial and innovative perspectives, involving processes and ecosystems. The wine production in the southern region of Brazil presents a high level of associative and family entrepreneurship, with a large number of wineries that were established and are operated as a family business or as the result of regional association schemes [90]. In such entrepreneurial ecosystem, the wineries create connections through their association and develop entrepreneurial and innovative strategies with the actors involved and with different intensities of the local society. The associations serve as bridges between wineries, institutes, class entities and with local governments [91]. The study allowed observing that the oldest wineries are developing a structuring entrepreneurial process, aiming at the certification for “Appellation d’origine contrôlée,” in search of a quality brand based on the certification of Geographical Origin Indication. Such initiative corroborates with Schumpeter’s [9] vision, where the entrepreneur innovates to differentiate itself and conquer new markets. The study of the ecosystems allowed the identification of the actors that compose and interact in the associations, by using the association as a link between the wineries and all the government actors. Through the association schemes, the wineries strengthen their positioning and competitiveness in terms of sustainability. Being small and limited, the group manages to innovate because it has achieved a certain degree of internal sustainability.
In the textile sector, research results show that the entire industrial activity is the result of entrepreneurial action. In this context, researchers establish that innovations include incremental changes in procedures, techniques, materials and dissemination, according to Oslo Manual [64]. It can be considered that the rectilinear knitting sector presents innovations that allow characterizing an environment of change, which aims at the improvement and the qualification of the products and services offered to the customers. The study of the process innovations shows significant changes in machinery, production layout, software that aid in production control, production scheduling and techniques were highlighted [92, 93]. Innovations in marketing showed that more and more companies are willing to disclose their products through direct dissemination to customers. The organizational innovations that happen are incremental and internal to an organization, confirming that this sector of the economy do not present perspectives of sustainability.
Research in the transportation sector refer to the port and logistics matters, which are recognized as global entrepreneurial activities, coped with the presence of process innovations [94, 95]. Considering the frequency of innovations occurring in the sector, the requirement of the Agência Nacional de Transportes Aquaviários do Brasil—ANTAQ, which regulates the implementation of the country’s environmental agenda, generated a high number of innovations, mainly related to process innovations. This position confirms the presence of sustainability caused by the application of the National laws and regulations.
Research in the energy field presents opposing scenarios in terms of entrepreneurship and innovation. The omnipresence of laws and regulations does not allow room for creativity and change. The concern and position from the energy managers are to achieve a high degree of accuracy in their decision process. The research shows a greater determinant for the use of forecasting model in their decision process, which contributes to companies that improve a forecasting strategy as a process innovation and consider the possibility of reaching forecast results that are closer to reality, to create an edge in such competitive market [96]. The behavior and trends that arise in the complex equation of the decision process and by predictive models presuppose a permanent search for sustainability to offer a permanent quality service to the community.
The MSE sector represents 93% of the private organizations in Brazil [97], being a crucial subject for studies. The Schumpeterian view argues that entrepreneurial action is the driving force behind the activities of all those companies and is the basis of the country’s economy. In such context, research shows that most of the companies surveyed use performance indicators to monitor business management. The companies that had the highest sales increase are those that, in addition to the indicators have a clear definition of the business, have established goals and have information about the industry and the competition [98]. In terms of innovation and sustainability, research has shown the absence of both dimensions. Innovation is restricted to larger companies and is limited to an internal environment. The absence of sustainability demonstrates that there is a relationship between the two concepts.
The researches on various sectors of the Brazilian Serra Gaúcha economy allow to point out the existence of a relationship between the concepts of entrepreneurship, innovation and sustainability through individual, social, cultural process and system perspectives. By using historical and cultural panoramas, it was possible to observe the manifestations of the entrepreneurs of the region of Serra Gaúcha and to assert that the attributes and the actions of those entrepreneurs constitute a demonstration of the strength for the potential of the opportunities and the use of the conditions that promoted the economic development of region. The presence of “entrepreneurship intensity” in this specific region and the concern for sustainability lead to a more “coherent” understanding of the innovation process, which is in fact still very poorly achieved in Brazil and little understood by the country’s institutional leaders. The key elements of the researches also converged on the issues of the entrepreneurs’ actions, considering that innovation represents the success of a business community that leads in terms of entrepreneurship and sustainability. In Brazil, innovation could generate new and differentiated organisations that could have a positive socio-economic impact in a fragmented and closed business society. Such results demonstrate the limitation of Chesbrough’s [24] model to explain open innovation in the Brazilian reality. The identification, the description and the analysis of the conceptual trilogy are exposed through the region’s own history, and the main results reveal a series of elements, events that preceded and influenced the constitution of the industrialization of the Serra Gaúcha region and gave rise to different models with their own specific particularities.
The positioning and the distribution of the results on entrepreneurship (Figure 4 – on a scale 1–3–5) based on a “Etzkowitzian” perspective show peculiar private-public realities by sector of the Brazilian economy in relation to entrepreneurship intensity.
Public-private realities [
Figure 4 presents two theoretically already known phenomena, but little considered in the Brazilian scientific community. First, the connection between the private-public nature of the organizations and the entrepreneurial intensity phenomenon. Second, the connection between the social nature of the organizations and the level of entrepreneurial intensity. The research confirms the link between entrepreneurial intensity and the private sector organizational nature, but does not exclude specific sectors of development, such as the health and transportation sectors. History may sustain the reasons why both these sectors show entrepreneurial intensity, whereas the education and energy sectors present other results. These issues are related to the Brazilian public sphere, where the management processes are highly bureaucratic and the methods of supervision do not encourage entrepreneurship intensity. Thus, their cases can be explained, not by the country’s legislation but by the control on the governance and processes in the organizations of each sector, which reinforce the idea of including a fourth Helix to aggregate Dorion et al.’s [78] model.
To understand the matter of the organizations and sustainability, the practices of entrepreneurship adopted were pointed out in a historical perspective. According to the authors, many entrepreneurs from the industry have developed an entrepreneurial behavior because they were attentive to perceive the opportunities of the market. However, they did not know how to cooperate with each other, by sharing risks and learning from their mistakes. The results show their capacity to enhance skilful and firm behavior regarding issues involving their relationship with public power. This dimension raises the question of sustainability, considering that the actors did not go beyond business issues and became agents of economic development by their individual and collective actions that led to the development of the region in a peculiar way. The Brazilian Serra Gaúcha region managed to excel due to endogenous entrepreneurial intensity issues, nor for sustainability.
Figure 5 proposes a rationale between the issue of territorial coverage and sustainability intensity, on a scale 1–3–5. Researches in the health and energy sectors show the presence of intra-organizational sustainability schemes at the regional level. The metal-mechanic industry, the technology development environments, the sectors of education, services, furniture, food and beverages, textile and transport point out the question of sustainability as an internal strategic element of the organizations. Researches in the metal-mechanic sector have demonstrated that cleaner production methods and environmental management practices are tools that aim at the efficiency of the production process, the use of its inputs and the generation of industrial waste. The furniture and textile sectors point out isolated process and product innovation actions and economic and environmental sustainability cases. Since entrepreneurship constitutes the engine of the sector, the creative industry sector did not show the presence of sustainability, but only some innovation actions in isolated initiatives.
Territory (scale) and sustainability intensity. Source: The authors.
There is consensus in the researches about the fact that entrepreneurship appears in all sectors of the studied activities, but with different intensities. Sustainability does contribute to the business innovations, but still it is not possible to explain to what extent and in what specific way. Each sector has its own rationale profile on entrepreneurship, sustainability and innovation. A trend radar shows opposite and convergent results among the sectors of the Brazilian economy.
The rationale between the concepts of entrepreneurship, sustainability and innovation, as presented in Figure 6, brings some reflections that can more clearly contextualize and explain those issues in Brazil. The sectors that most presented evidence of innovations refer to health, technology development and transportation environments, which all belong to the public sphere. Then, a higher degree of innovation intensity demonstrates a drive for economic, environmental and social improvements and growth. Based on a sustainable process of combining and recombining the capacities and preferences of the different agents integrated into a regional organizational reality; it is possible to design regional structural schemes on innovation that would give the necessary sustainability edge to make them survive through time. Such mobilization would allow a continuous development effort that produce regeneration patterns, necessary for regional long-term development schemes. Therefore, innovation becomes a learning process that generates or acquires new knowledge from the analysis of a specific sustainable environment.
Entrepreneurship, sustainability and innovation intensities. Source: The authors.
The sectors of such Brazilian regional economy that presented less “innovation intensity” are characterized by internal organizational activities of innovation, preventing them to become “regional systems of innovation,” which presupposes the lack of sustainability. Those limitations can be characterized as “innovation ghettos” in order to establish the intensity necessary to generate innovation activities within a specific territory. Ghettos, as explained by its etymology, refer to the conditions of survival of a population, in a limited and a highly concentrated scale. In that logic, the researchers have also demonstrated the presence of “ghettos of sustainability, ghettos of innovation, and therefore, ghettos of sustainability and innovation” in the sectors of this Brazilian regional economy, but in differentiated and restricted perspectives.
Finally and in a managerial perspective, considering the trilogy of entrepreneurship, sustainability and innovation, the organizations may seek a sustainable competitive advantage to generate monopoly through a regional logic. In turbulent organizational environments such as Brazil, a regional perspective may present some structural advantages for business activity. Nevertheless, only the generation of entrepreneurial initiatives with the aim for innovation through sustainability will favor regional development. In that regard, to better understand the logic of regional development and its organizational reality, more researches need to be accomplished.
To maintain hemostasis, new blood cells must be constantly generated to replace those lost through injury, disease, or age. Hematopoiesis, is the process where hematopoietic stem cells (HSC) differentiate into mature blood cells and is tightly regulated by the bone marrow (BM) micro-environment (or stem cell niche; reviewed in [1]), signal transduction pathways (reviewed in [2]), cytokines (reviewed in [3]), transcription factors (reviewed in [4]), epigenetics, (reviewed in [5]) and metabolic pathways (reviewed in [6]). HSCs are rare, constituting only 0.001% of peripheral blood (PB) and 0.05% of BM cells, but are responsible for producing a lifetime supply of blood cells. HSCs are cells that able to durably self-renew whilst also being multipotent. This differentiation is generally considered to occur via several intermediate progenitor cells, ultimately terminating in the specific mature blood cell through a process termed fate restriction or lineage commitment.
The compartmentalization of HSC, their progenitors and terminally differentiated blood cells, into different stages of differentiation, is traditionally based on the expression of cell surface proteins (Figure 1). The recent emergence of single cell technologies such as fluorescent in situ hybridization, high-throughput single-cell quantitative PCR, single cell mass spectrometry and mass cytometry however, have led to re-analysis of these models of hematopoietic differentiation [7]. Discrete progenitor cell populations, as determined by cell surface markers, have been shown to consist of heterogenous populations with different fates [8]. Recently, a study by Velten
Human hematopoiesis. Schematic diagram showing classical model of hematopoietic lineage commitment, with phenotypical cell surface markers (red), transcription factors determining differentiation (green box) and growth factors involved in myelopoiesis (blue). Hematopoietic stem cell (HSC), cluster of differentiation (CD), hematopoietic progenitor cell (HPC), common myeloid progenitor (CMP), common lymphoid progenitor (CLP), interleukin (IL), granulocyte macrophage (GM) colony-stimulating-factor (CSF), stem cell factor (SCF), thrombopoietin (TPO), erythropoietin (EPO), granulocyte myeloid progenitor (GMP), runt-related transcription factor 1 (RUNX1), transcription factor stem cell leukemia (SCL), ccaat enhancer binding proteins (C/EBP), friend of GATA protein 1 (FOG-1).
Regardless of provenance, leukemogenesis is characterized by a block in differentiation and an accumulation of immature white blood cell blasts with a rapid increase in these blasts, characteristic of the acute leukemias. Acute lymphoblastic leukemia (ALL) and acute myeloid leukemia (AML) are heterogenous diseases with a block in lymphoid or myeloid differentiation, respectively. They occur due to one or more genetic insults. Whilst ALL is predominantly a disease of children (80%), with a greater than 90% 5 y survival rate [10], in adults long term survival stands at only 30–40% [11]. AML in contrast is primarily a disease of the elderly, and like adult ALL it’s 5 y survival rate is around 30%, however this falls in the over 60’s to a particularly bleak 10% [12]. In ALL, recent advances for example in the use of tyrosine kinase inhibitors and CAR-T cell therapy, have started to suggest improvements to overall survival [10]. However, in patients fit enough to tolerate chemotherapy, the standard treatment for AML since 1973 has been a seven-day continuous intravenous infusion of cytarabine (Ara-C) (100–200 mg/m2) and 3 daily doses of daunorubicin (45–90 mg/m2), sometimes followed by allogeneic or autologous stem cell transplantation, and despite some recent advances (reviewed in [13, 14]), current treatments appear to have reached their efficacious limits and new therapies are required.
One potential therapeutic opportunity involves exploiting the metabolic differences that exist between malignant and non-malignant cells [15]. Differences that, in AML at least, appear exacerbated by cellular levels of reactive oxygen species (ROS) [16].
ROS is the collective term for several oxygen containing free radicals and other reactive molecules, such as hydrogen peroxide (H2O2). Physiologically, ROS are initially generated via the univalent reduction of molecular oxygen which generates superoxide (O2•−). Superoxide (t1/2 = 1 μs) subsequently dismutates to H2O2 (t1/2 = 1 ms) [17], either spontaneously or via the catalytic action of the enzyme superoxide dismutase (SOD), or reacts with other ROS molecules, forming a variety of other ROS (Figure 2). Functionally, ROS is important in innate immunity, protein folding in the endoplasmic reticulum and as a cell signalling molecule involved in cellular proliferation, survival, differentiation and gene expression [18].
Formation of reactive oxygen species (ROS). Diatomic oxygen (O2) is univalently reduced by peroxisomes (PO), xanthine oxidase (XO), the electron transport chain (ETC), or NADPH oxidase (NOX) to generate superoxide (O2•−). PO may also reduce O2 directly to form H2O2. O2•− may then dismutate to H2O2 either spontaneously or through the enzymatic action of superoxide dismutase (SOD). Hydroxyl radicals (OH•) may then be formed from H2O2 via the formation of hypochlorous radical (HOCl) in the PO, or via Fenton chemistry. Reactive nitrogen species (RNS) may also be formed through the reaction of nitric oxide radical (NO•) with O2•−.
There are several sources of cellular ROS, including the mitochondria, the nicotinamide adenine dinucleotide phosphate (NADPH) oxidase family of enzymes (NOX), the cytochrome P450 enzymes, peroxisomes and the metabolic enzyme xanthine oxidase (XO).
Generation of ROS by the mitochondria is primarily a function of ‘electron leakage’ from the electron transport chain (ETC), however, mitochondrial ROS may also be generated as a result of numerous enzymes including monoamine oxidase, cytochrome b5 reductase, glycerol-3-phosphate dehydrogenase, aconitase, pyruvate dehydrogenase and α-ketoglutarate dehydrogenase (reviewed in [19]). Mitochondrial ROS production resulting from the ETC generates O2•−, and is thought to occur as result of one of three mechanisms. The first mechanism is a consequence of a high NADH/NAD+ ratio, and results from oxygen interacting with fully reduced FMN. Mitochondrial ROS generated by this mechanism has been observed due to mitochondrial mutation, physiological damage such as ischemia or aging, and only small amounts of ROS are thought to be generated via these mechanisms in normally respiring cells [20]. The second mechanism occurs when there is a high level of reduced co-enzyme Q (CoQH2) in complex II, which in the presence of a high proton motive force generated by the proton pump, force electrons back into complex I in a process known as reverse electron transport (RET). Whilst RET generated ROS has also been implicated in diseases such as ischemia, it is now also thought to be involved as a cell signalling molecule in metabolic adaptation, myeloid differentiation and response to bacterial infection [21]. The third mechanism of ROS generation by the ETC occurs at complex III and has also been implicated in ROS signalling. The formation of O2•− occurs at the ubiquinol oxidation centre (Qo) site of the cytochrome bc1 complex, in which fully oxidized CoQ supports formation of O2•−, through the transfer of electrons from reduced heme b1 to molecular oxygen [22]. Generation of O2•− by complex I and II occurs exclusively in the mitochondrial matrix, whereas O2•− generated by complex III also occurs in the intermembrane space. O2•− generated in the mitochondrial matrix is rapidly converted to H2O2 by mitochondrial SOD (Mn-SOD), whereas O2•− generated in the intermembrane space travels through the outer mitochondrial membrane prior to conversion to H2O2 by cytosolic SOD (Cu/Zn-SOD).
Whilst mitochondrial oxidative phosphorylation is a major source of intracellular ROS, the main source of extracellular ROS involves the nicotinamide adenine dinucleotide phosphate (NADPH) oxidase family of enzymes (NOX). The NOX family of enzymes comprise of seven members, NOX1–5 and dual oxidase (DUOX) 1 and 2. NOX enzymes are transmembrane proteins that transfer electrons from NADPH to molecular oxygen, generating O2•− (or H2O2), which can then be converted to other forms of ROS. Different NOX isoforms share conserved structural features comprising of six helical transmembrane domains (TM) (with helix III and helix V containing two heme-binding histidines), and a C-terminus cytosolic domain (DH), which allows binding of FAD and NADPH (Figure 3). Difficulties in obtaining suitable levels of NOX proteins mean that to date relatively little crystal structure data is available. However, a recently published report [23], has elucidated the structure of the TM and DH domains (common to all NOX isoforms) of
Generation of superoxide (O2•−) by NADPH Oxidase (NOX). Schematic diagram showing the major structural features of NOX2, it’s activation by phosphorylation (P) of p67phoxand p47phox and the assembly of the major subunits of the NOX complex, and the generation of superoxide via electron transfer from NADPH to flavin adenine dinucleotide (FAD) to heme groups to diatomic oxygen. Guanosine triphosphate (GTP), guanosine diphosphate (GDP), homology domain (DH), RAS-related C3 botulinum toxin substrate 2 (Rac2).
From a metabolic perspective, one source of NOX2 activation results when cells experience intermittent hypoxia. Under this condition activation of the metabolic enzyme XO, an enzyme important in the catabolism of purines and a major source of cellular ROS, occurs [24]. XO activation leads to increased ROS, which induces Ca2+ activation of protein kinase C, an enzyme important in cell signalling, migration of p47phox and p67phox to the cell membrane, resulting in activation of the NOX2 complex (Figure 3). Finally it is important to note, from a cell signalling perspective, that extracellular H2O2 (which is rapidly formed from O2•−) is readily transported across the cell membrane via the transmembrane water permeable channel protein family of aquaporins [25, 26].
ROS has been implicated in both HSC quiescence and hematopoietic differentiation. HSC reside in the bone marrow and their quiescence is known to be negatively regulated by ROS. Forkhead box O (FOXO) transcription factors are involved in cell-cycle arrest and apoptosis and are activated in response to oxidative stress whereupon they translocate to the nucleus [27]. Translocation of FOXO4 to the nucleus has been shown to be a function of redox signalling, where oxidation of cys-239 by ROS mediates the formation of disulphide bonds with nuclear import receptor transportin-1, which in turn allows nuclear localization [28]. FOXO deactivation occurs as a result of phosphorylation in response to activation of the regulatory cell cycle PI3K/AKT/mTOR pathway, resulting in their export from the nucleus and subsequent degradation in the cytoplasm [29]. Studies in murine HSC have shown that deletion of FOXO3a, which upregulates transcription of Mn-SOD [30], results in decreased HSC renewal [31] which is mediated by the tumor suppressor protein ataxia-telangiectasia mutated (ATM) and is accompanied by elevated ROS levels and myeloid lineage expansion [32]. Deletion of ATM in mice resulted in BM failure which was restored following treatment with antioxidants [33]. In a different study, isolation of murine HSC into ROS high and ROS low populations showed that the ROS low population maintained self-renewal capacity following serial transplantations, whilst the self-renewal capacity of the ROS high population was exhausted following the third serial transplantation. Treatment of the ROS high HSC with the antioxidant N-acetyl cysteine (NAC), the p38 inhibitor SB203508 or rapamycin (a mTOR inhibitor), restored self-renewal activity [34]. Interestingly, the ROS high population in this study also exhibited a decreased ability to adhere to cells containing calcium sensing receptors, whilst NOX generated ROS has additionally been implicated in osteoclast differentiation in human mesenchymal cells, further emphasizing a potential regulatory role of ROS, in the BM niche [35].
Whilst these increased ROS levels are associated with HSC losing quiescence, it has also been shown, in the human megakaryocytic cell line MO7e, that hematopoietic cytokines, such as granulocyte macrophage-colony stimulating factor, interleukin-3, stem cell factor and thrombopoietin all increase ROS levels [36]. In megakaryopoiesis, ROS has been shown to increase platelet production and maturation in the chronic myeloid leukemia (CML) cell line MEG-01 and primary human megakaryocytes [37], which in murine models is mediated by the transcription factor NF-E2 [38]. Following lineage commitment, megakaryocyte progenitors undergo endomitosis (chromosomal replication in the absence of cell division), which in murine cells is potentially mediated by NOX1-derived ROS [39]. In human HSC, NOX-derived ROS has also been shown to be crucial for megakaryocyte differentiation via activation of ERK, AKT and JAK2 signalling pathways [40], whilst another study revealed the importance of cytochrome P450 2E1-generated ROS in megakaryocyte differentiation in human HSC [41]. As noted above, increased ROS in HSC has been associated with expanded myelopoiesis. Interestingly, a recent study using murine CMP, showed that higher levels of ROS impeded megakaryopoiesis, instead directing differentiation of CMP into GMP [42]. Finally, ROS has also been shown to induce differentiation of the promonocytic cell line, U937, into macrophages [43], and the differentiation of primary human monocytes into dendritic cells [44].
One of the first studies implicating ROS in carcinogenesis was performed in mice subcutaneously injected with C3H mouse fibroblasts, that had been previously cultured
In leukemia, a study which collected blood samples from ALL and CML patients samples and compared them with normal blood samples showed elevated levels of ROS in both ALL and CML patients [52], whilst elevated levels of NOX generated ROS, are observed, alongside increased proliferation in both AML models and AML patient samples when compared with healthy controls [53]. Reactions of ROS with DNA can generate numerous oxidised bases, including 8-hydroxy-2-deoxyguanosine (8-OHdG) which causes G:C to T:A DNA transversions (reviewed in [54]). Increased levels of 8-OHdG have been observed in patients with breast cancer [55], gastric carcinomas [56], lung cancer [57] and colorectal cancer [58]. In leukemia, a study of 116 Chinese children with either ALL or AML revealed significantly elevated levels of 8-OHdG, whilst 8-OHdG levels were also significantly elevated in relapsed AML adult patients [59].
As a signalling molecule, ROS can lead to hyperactivation of the PI3K pathway, a common feature of many cancers, resulting in increased cell survival, VEGF production, secretion of MMP (reviewed in [60]) and inactivation of FOXO [32]. In AML, constitutive activation of the PI3K/AKT pathway is frequently observed [61, 62], however the role of FOXO is less clear. A recent study revealed that FOXO1 expression in osteoblasts mediated β-catenin initiated AML [63], whilst a study of AML patient samples showed that 40% exhibited FOXO activation, that upon inhibition resulted in myeloid differentiation and AML cell death [64]. Additionally, in both CML and AML the BCR-ABL fusion protein and FMS-like tyrosine kinase receptor 3 internal tandem duplications (FLT3-ITD) have been shown to lead to phosphorylation of AKT resulting in increased activation of NOX, and increased ROS production (reviewed in [65]), which may in turn reinforce PI3K/AKT activation.
Broadly defined, cellular metabolism involves a series of catabolic or anabolic chemical reactions which generate or use energy as part of this process. In chemotrophs this energy is obtained through the oxidation of nutrients, with the energy typically stored in the form of ATP. Whilst in higher organisms a plethora of enzymatically catalyzed metabolic reactions occur, which are all part of different interconnecting metabolic pathways with multitudinous feedback mechanisms. These pathways are evolutionarily highly conserved with the citric acid cycle, for example, essentially a feature in all terrestrial life. There are three main classes of molecules involved in metabolism; carbohydrates, proteins and lipids that are either catabolized to generate energy or energy stores or used by anabolic pathways in the synthesis of, for example, nucleotides and structural molecules such as cell membranes. In mammals, a triumvirate of glycolysis, citric acid cycle and the ETC are central to the generation of ATP, with glycolysis and the citric acid cycle contributing 2 ATP molecules each and the ETC generating up to 34 ATP molecules in a process collectively termed aerobic respiration (reviewed in [66]).
Given the skew towards ATP production in the ETC, Otto Warburg’s observation in 1956 that aerobic glycolysis was a hallmark feature of cancer cells [15], was initially attributed to being the result of defective mitochondria in malignant cells, and initially raised little interest. However, this hypothesis is now known in most cases to be incorrect (reviewed in [67]) and instead, it has been shown that mitochondrial respiration is often necessary in tumorigenesis [68]. However, given its ubiquity and despite its inefficiency when compared with ETC, it is clear that the phenomenon of increased aerobic glycolysis (eponymously titled ‘The Warburg Effect’), must offer cancer cells some competitive advantage, although its exact ontology remains unclear. One hypothesis contends that whilst inefficient, aerobic glycolysis generates ATP at a rate 10–100 times faster than oxidative phosphorylation, therefore supplying cancer cells with energy at a faster rate. This increased glycolytic flux could then, potentially generate more nucleotides, amino acids and lipids for biosynthesis as well as generating the reducing agent NADPH, to deal with the increased levels of ROS common in many cancer cells [69]. Alternatively, increases in excreted lactate as a result of aerobic glycolysis would likely generate a more acidic microenvironment, breaking down stromal membrane structures and potentially increasing cancer cell motility and metastasis [70].
It has been shown that activation of the tumor suppressor protein ATM by ROS promotes glucose-6-phosphate dehydrogenase (G-6-PD) activity, the first step of the pentose phosphate pathway (PPP), which in turn generates NADPH [71]. Given that major cellular antioxidant systems, ultimately rely on NADPH to provide their reducing power, it is perhaps not surprising that ROS in both normal and aberrant cellular processes is inextricably linked with metabolism. In the cytosol, NADPH is primarily generated through the PPP, whilst a number of mechanisms exist for mitochondrial NADPH generation [72], which include the serine synthesis pathway (SSP) (via the folate cycle) [73] and the action of the citric acid cycle enzyme isocitrate dehydrogenase (IDH). IDH1 and IDH2 are commonly mutated in AML [74], although in this context NADPH is consumed, and the D-2-hydroxyglutarate generated leads to stabilization of the hypoxia regulator, hypoxia inducible factor alpha (HIF-1α) [75].
HIF-1α as a target of ROS is controversial [76], however it is overexpressed in many cancers where it induces expression of numerous glycolytic genes. The ROS regulated transcription factor nuclear-related factor 2 (NRF2) has also been shown to modulate metabolism in lung cancer cell lines, through the upregulation of enzymes involved in the NADPH production, notably G-6-PD, IDH1 and malic enzyme 1 [77] and high NRF2 levels have previously been reported in AML [78]. Furthermore, the tumor suppressor protein TP53 is also important in regulating metabolism. Homozygous deletion of TP53 in mice results in decreased oxygen consumption arising from decreased mitochondrial respiration [79]. TP53 expression has been shown to inhibit, both glucose transporter (GLUT) 1 and 4 and the glycolytic enzyme phosphoglycerate mutase (PGAM) (reviewed in [80]) leading to decreased glycolysis and potentially increased metabolism via the PPP and SSP. Finally, TP53 also upregulates the apoptosis regulator (TIGAR) an enzyme which has an active domain similar to 6-Phosphofructo-2-kinase/fructoste-2,6-bisphosphatase (PFKFB). TIGAR catalyzes the reaction of fructose-2,6-bisphosphate (F-2,6-BP) to fructose-6-phosphate (F-6-P), which inhibits glycolysis, redirects metabolites into the PPP, generating NADPH [81].
Changes of cellular ROS levels in both normal signalling as well cell signalling following cellular transformation result in changes in numerous signalling pathways controlling multiple cellular functions including growth, proliferation and differentiation. A number of these signalling pathways, exercise regulatory control over various metabolic pathways, which in turn modulate ROS levels via several feedback mechanisms (Figure 4). In leukemia, mutations in the
Regulation of metabolic pathways. Schematic illustration outlining some of the regulatory mechanism involved in glycolysis and other key metabolic pathways. Transcription factors are in pink and signalling pathways in blue. Reactive oxygen species (ROS), forkhead box O (FOXO), pyruvate kinase muscle 2 (PKM2), signal transducer and activator of transcription (STAT), nuclear factor kappa-light-chain-enhancer of activated B-cells (NF-κB), glucose transporter (GLUT) hypoxia inducible factor-1 alpha (HIF-1α), tumour suppressor protein 53 (TP53), glycogen synthase kinase 3β (GSK-3β), isocitrate dehydrogenase (IDH), succinate dehydrogenase (SDH), fumarate hydratase (FH), protein kinase B (AKT), mammalian target of rapamycin (mTOR), phosphoinositide 3-kinase (PI3K), synthesis of cytochrome c oxidase 2 (SCO2) and prolyl-hydroxylase domain (PHD).
Nuclear localization of the glycolytic enzyme pyruvate kinase muscle 2 (PKM2) is also ROS mediated, where it acts as a co-factor in the activation of the transcription factor, c-MYC. RAS also activates c-MYC which is overexpressed in greater than 50% of human cancers and c-MYC has been shown to activate glycolysis via the upregulation of GLUT, the glycolytic enzymes hexokinase (HK), phosphoglucose isomerase (PGI), phosphofructokinase (PFK), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), phosphoglycerate kinase (PGK), PKM2, as well as lactate dehydrogenase A (LDHA), pyruvate dehydrogenase kinase 1 (PDK1) and PFKFB3 (reviewed in [87]). Increased glutaminolysis is also a target of c-MYC, which upregulates the glutamine transporter ASCT2 and a key enzyme glutaminase. Additionally, c-MYC was shown to upregulate both phosphoglycerate dehydrogenase (PHGDH) which catalyzes the first step of the SSP, serine hydroxymethyltransferase, part of the folate cycle as well as several genes involved in fatty acid metabolism and the citric acid cycle (reviewed in [67]). In contrast TP53 is known to inhibit glycolysis through inhibition of GLUT1, GLUT4 and PGAM and through activation of TIGAR and synthesis of cytochrome c oxidase 2 (SCO2). Inhibition of glycolysis also occurs due to the regulatory role of miRNA. For example, miR-195-5p inhibits GLUT3, miR-143 inhibits HK2 and miR-155 inhibits HIF-1α. Furthermore, TP53 induces miR-34a which suppresses HK1, HK2, GPI and PDK1, as well as sirtuin 1, which activates FOXO1, NF-κB and in a positive feedback loop TP53 (reviewed in [80]).
Given the role that ROS plays in regulating metabolism, it is not surprising that expression of nearly all enzymes associated with glycolysis have been shown to be altered in solid tumors, a pattern also observed in leukemia. In ALL, micro-array analysis showed significant upregulation of PFK as well as the glucose transporters GLUT1 and GLUT4 in pediatric B-ALL samples [88], whilst deletion of GLUT1 in primary human B-ALL cells suppressed leukemic progression
The citric acid cycle is a series of metabolic reactions involving oxidation/reduction reactions, which generate nicotinamide adenine dinucleotide (NAD)H and flavin adenine dinucleotide (FAD)H via the transfer of hydride ions, thus providing electrons for the ETC which is a major source of cellular ROS (reviewed in [106]). Mutations of IDH, which catalyzes the decarboxylation of isocitrate to alpha-ketoglutarate are frequently reported in AML (reviewed in [107]). Characterization of the inhibitor AG-221, which has been shown to inhibit mutant IDH2 in AML cells
The SSP branches from the glycolytic pathway at the glycolytic intermediate 3-PG, where it is converted into 3-phosphohydroxypyruvate by the enzyme PHGDH, followed by conversion to phosphoserine by phosphoserine aminotransferase 1 and finally to serine by the action of the enzyme phosphoserine phosphatase (reviewed in [73]). Regulation of the SSP is achieved through 2-phosphoglycerate (2-PG) which activates PHGDH whilst serine activates the tetrameric form of PKM2 leading to increased glycolysis and decreased levels of 2-PG. Importantly serine can enter the folate cycle, which provides another route for the generation of NADPH, which has been shown to contribute to tumor growth
The PPP generate nucleotides for biosynthesis and is a major source of cellular NADPH, an important cellular antioxidant. The first step involves the dehydrogenation of G-6-P to 6-phosphogluconolactone (6-PG) catalyzed by G-6-PD and the conversion of NADP+ to [115]. Gluconolactonase catalyzes the hydrolysis of 6-PG to 6-phosphogluconate, which is then catalyzed by 6-phosphogluconate dehydrogenase (6-PGD) to ribulose-5-phosphate (Ru-5-P) alongside the generation of a second NADPH. Ru-5-P can then be converted into ribose-5-phosphate (R-5-P) by the enzymatic action of ribulose-5-phosphate isomerase. R-5-P can then be used in the synthesis of nucleotides. Alternatively, where redox homeostasis and not nucleotide synthesis is the major requirement of the cell Ru-5-P can be catalyzed by ribulose-5-phosphate epimerase, into xyulose-5-phosphate (X-5-P) and via a series of further metabolic reactions back into the glycolytic intermediates F-6-P and glyceraldehyde-3-phosphate. G-6-PD is the rate limiting step of the PPP and is regulated by the NADP+/NADPH ratio, RAS/PI3K signalling and phosphorylation by Src, whilst 6-PGD is inhibited by 3-PG [99]. In cancer, aberrant RAS signalling or activation of Src can promote activation of the PPP. In AML, a recent study showed upregulation of
Lipid metabolism has also been shown to be dysregulated in both solid tumors and hematological malignancies (reviewed in [120]). Increased fatty acid oxidation (FAO) allows cancer cells to overcome metabolic and oxidative stress through the generation of ATP and NADPH. Significant changes to lipid metabolite levels are seen in AML patient samples with either high levels or low levels of ROS [16], whilst suppression of NOX2 has also been shown to increase FAO [121]. Furthermore, inhibition of the FAO using Avocatin B results in decreased NADPH levels and ROS dependent cell death in primary human AML samples but not normal mononuclear cells [122]. In ALL, use of L-asparaginase has been shown to increase FAO activity as a metabolic escape mechanism, however use of the FAO inhibitor etomoxir in combination with L-asparaginase has been shown to increase sensitivity of both leukemic cell lines and patient samples [123].
In the last twenty years, it has become increasingly clear that ROS play a significant role in cellular signalling, particularly pathways associated with growth, differentiation and survival, whilst its roles in HSC quiescence and normal hematopoiesis have started to be delineated. In many cancers including hematological malignancies, ROS levels have been shown to be elevated, leading to aberrant signalling in these pathways. Previously, arguments for both the use of anti-oxidant and pro-oxidant treatments in leukemia have been made (reviewed in [124]). Despite the transformation of survival rates in patients with acute promyelocytic leukemia using arsenic trioxide [125] cancer cells often upregulate the production of antioxidants, and downregulate pro-apoptotic pathways such as TP53, as a response to high ROS, allowing them to escape apoptosis. In addition, it has been shown that both cancer stem cells [126, 127] and leukemic stem cells [128] exhibit low ROS levels, suggesting that even if treatment with pro-oxidants eliminates the bulk of cancer cells, cancer/leukemic stem cells may survive and relapse occur. Conversely, studies involving the use of antioxidants in treatment and epidemiological studies of antioxidant use, have shown mixed results (reviewed in [129, 130]). Increasingly it is becoming apparent that increased levels of ROS are leading to changes in signalling pathways directly or indirectly controlling metabolism, as a mechanism for managing oxidative stress. Whilst, it has long been known that cancer cells exhibit greatly altered metabolism, only recently have the purposes behind this altered metabolism, started to be elucidated. Consequently, synergistic treatments involving the use of metabolic inhibitors, alongside classical treatments for leukemias are being explored. Future work, elucidating the intricate mechanisms governing the interplay between ROS and metabolism, alongside new and more specific metabolic inhibitors provide much promise for the future treatment of leukemia.
We are grateful to Blood Cancer UK for programmatic funding and to Tenovus Cancer Care for funding Andrew Robinson. We are grateful to Wellcome ISSF for funding aspects of ROS research. We are grateful for support from the NCRI AML trials cell bank and the AML patients for providing primary samples used in several of our studies.
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\\n"}]'},components:[{type:"htmlEditorComponent",content:'Publishing with IntechOpen means that your scientific publications already meet these basic requirements. It also means that through our utilization of open licensing, our publications are also able to be copied, shared, searched, linked, crawled, and mined for text and data, optimizing our authors' compliance as suggested by the European Commission.
\n\nMetadata for all publications is also automatically deposited in IntechOpen's OAI repository, making them available through the Open Access Infrastructure for Research in Europe's (OpenAIRE) search interface further establishing our compliance.
\n\nIn other words, publishing with IntechOpen guarantees compliance.
\n\nRead more about Open Access in Horizon 2020 here.
\n\nWhich scientific publication to choose?
\n\nWhen choosing a publication, Horizon 2020 grant recipients are encouraged to provide open access to various types of scientific publications including monographs, edited books and conference proceedings.
\n\nIntechOpen publishes all of the aforementioned formats in compliance with the requirements and criteria established by the European Commission for the Horizon 2020 Program.
\n\nAuthors requiring additional information are welcome to send their inquiries to funders@intechopen.com
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