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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
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The process of teaching and learning enhanced by technology is commonly known as e-learning. The virtual campus is the fundamental element on which a virtual education project is based. If it is an accessible virtual campus, it must be ensured that all functionality can be used by any user, including users with disabilities.
There are several challenges associated with the implementation of effective learning outcomes via e-learning within a virtual campus. In this chapter in particular, the considerations on the use of e-learning to reach students with disabilities and the barriers [1–5] that they may have will be analyzed, providing the basic knowledge to prepare an accessible virtual campus.
This chapter is structured as follows: A state of the art on accessibility related to virtual campuses, highlighting studies related to the application of accessibility standards to improve the e-learning systems is presented in the first section. The first section explores on the main accessibility requirements for an e-learning campus. Then a review on the basic knowledge that the stakeholders involved in e-learning education should have in order to preserve and promote accessibility is presented. In particular, the authors propose an evaluation guideline on accessibility for virtual campus administrators. Finally, the considerations on the accessibility requirements of learning objects (LOs) are presented using the IMS Access for all v3.0 specification, the main objective of which is to simplify the definition of the accessibility metadata for learning objects and the preferences and needs of the users of these objects tracing them to students’ related disabilities.
A virtual campus is an environment based on a web technology that provides facilities for the development, management, and publication of content that contribute to the process of teaching and learning. In this work, a virtual campus will be also referred as e-learning system and learning management system (LMS). In terms on legislation related to students with disabilities in e-learning, Edmonds [6] explored the different laws available and highlights the legal and technical concerns for education institutions. International legislation in terms of technological evolution related to e-learning is reflected on the Convention on the Rights of Persons with Disabilities (CRPD) in Article 9 (points 2.g an 2.h) [7]. The CRPD highlights the importance of promoting access to information and communications technology (ICT) for people with disabilities (PWD) and specially producing accessible content in early stages at minimum costs. Related to education, the (CRPD) in Article 24 recognizes the right to education. Countries that signed the CRPD must make sure that students with disabilities are able to get access not only to general education but also to tertiary education, vocational training, adult education, and lifelong learning without discrimination and on an equal basis with others.
In terms of accessibility, the International Organization for Standardization (ISO) defines accessibility as “the usability of a product, service, environment or facility by people with the widest range of capabilities” [8]. The World Wide Web Consortium (W3C), the organization in charge of developing web standards, created the Web Accessibility Initiative (WAI) with the aim of studying the problems of accessibility and propose solutions. One of its most known results is the Web Content Accessibility Guidelines (WCAG) 2.0 that establishes four principles that give the foundation of web accessibility: web content must be perceivable, understandable, operable, and robust [8].
In terms on learning objects accessibility, it is important to take into consideration the standard ISO/IEC 24751 [9–11] to describe the process of using an accessible online educational system, which takes into account the needs and preferences of the student and contains accessibility metadata of the learning objects. This chapter will explore also on the metadata for the learning objects using the IMS Access for All v3.0 specification [12], the main objective of which is to simplify the definition of the accessibility metadata for learning objects and the preferences and needs of the users of these objects.
Learning management systems (LMS) are mainly based on web technologies through a client–server model, with an interface prepared to work base on HTML markup and presented in a web browser. For this type of systems, accessibility requirements should be followed, especially guidelines provided by the Web Accessibility Initiative (WAI) [13] part of the World Wide Web Consortium (W3C). These guidelines are summarized as follows:
Authoring Tool Accessibility Guidelines (ATAG) [14]—guidelines intended to software used to create web sites and content
User Agent Accessibility Guidelines (UAAG) [15]—addresses web browsers and media players, and especially related to assistive technologies interaction
Web Content Accessibility Guidelines (WCAG) [8]—guidelines intended to improve information on a web site, including text, images, videos, etc.
Accessible Rich Internet Applications (WAI-ARIA) [16]—defines a way to make dynamic web content and web applications based on new interactive technologies as Ajax, HTML5 more accessible
Learning management systems (LMS) work with web technology, so their user interfaces can be evaluated based on the basic principles for creating accessible web content as presented in WCAG 2.0. The universality of these guidelines is evidenced by the fact that it was approved in 2012 as an international standard: ISO/IEC DIS 40500 [8]. WCAG 2.0 identifies twelve guidelines and numerous compliance criteria (“
Perceivable: This principle is related to how information and user interface components must be presentable to users in ways they can perceive without limitations. This means that users must be able to perceive the content and information available in a web, the information presented in any part of the web must be visible to all of their senses.
Operable: This principle is based on the fact that user interface components and navigation through a web must be operable. This is important so that users must be able to operate the interface, avoiding to ask the user some interaction that she cannot perform.
Understandable: This means that users must be able to understand the information as well as the operation of the user interface without more details provided.
Robust: Content presented in a web must be really robust, in a way that it can be interpreted easily by a wide variety of user agents, especially software and hardware prepared as assistive technologies. This means in other works that users must be able to access the content independently as technologies advance and evolve.
Under each of the four principles, there is a list of guidelines that address the principle. There are a total of 12 guidelines. One of the key objectives of the guidelines is to ensure that content is directly accessible to as many people as possible. There are success criteria related to each guideline, which describe specifically what must be achieved in order to conform to the WCAG 2.0 standard [8]. Each success criterion is written as a statement that will be either true or false when specific web content is tested against it. Table 1 presents the 12-guideline part of the standard.
\n\t\t\t\t | \n\t\t\t\n\t\t\t\t | \n\t\t
Perceivable | \n\t\t\t1.1 Provide text alternatives for any non-text content so that it can be changed into other forms people need, such as large print, Braille, speech or simpler language. 1.2 Provide alternatives for time-based media. 1.3 Create content that can be presented in different ways (for example, simpler layout) without losing information or structure. 1.4 Make it easier for users to see and hear content, including separating foreground from background. | \n\t\t
Operable | \n\t\t\t2.1 Make all functionality available from a keyboard. 2.2 Provide users enough time to read and use content. 2.3 Do not design content in a way that is known to cause seizures. 2.4 Provide ways to help users navigate, find content, and determine where they are. | \n\t\t
Understandable | \n\t\t\t3.1 Make text content readable and understandable. 3.2 Make web pages appear and operate in predictable ways. 3.3 Help users avoid and correct mistakes. | \n\t\t
Robust | \n\t\t\t4.1 Maximize compatibility with current and future user agents, including assistive technologies. | \n\t\t
Accessibility guidelines for web content WCAG 2.0
The group of principles, guidelines, and success criteria based on WCAG 2.0 [8] are applicable to any web pages and digital content. In the case of e-learning systems (e.g., LMS), these systems are a group of web pages and educational digital content so WCAG 2.0 can be applied to each element. As a summary, the following six basic accessibility principles should be included in every e-learning system [17]:
Allow users to customize their portal based on their preferences.
Provide equivalents to every time-based media and visual elements.
Use different ways to present information in an interface.
Provide information appropriate compatible with assistive technologies.
Allow access to all functionalities via keyboard.
Provide background information and status and location information to the user at all times.
From WCAG 2.0 [8] guidelines and different accessibility related laws, in terms of basic functionality, e-learning systems (learning content management systems) should have the following basic characteristics:
Structure
Absence of markup code errors in pages (HTML, CSS)
Setting of accessibility preferences as default configuration, available for user personalization
Accessibility check for content creators (HTML editors) and images selectors (e.g., alternative texts for each image)
Summary of last activity within the system
Keyboard navigation
Definition of a logical order to display tab indicators, provide a visual place mark to identify where the user is in a particular moment
Provide links to jump to main content
Functionality to simplify configuration to minimize secondary content pages and menus
Functionality to select options using a simple combination of keys
Provide complete access to all functionality via keyword, including HTML editors, controls in multimedia viewers, and Web 2.0 functionalities (e.g., Drag and drop”)
Enable keyboard shortcuts (hotkeys) and provide a definition page with all combinations
Provide a complete sitemap structure for navigation in all systems
If a key is pressed by mistake, provide the ability to undo and return to previous state
Magnification of screen size and functionality to change colors contrast
Provide a standard design of the interface through all systems in order to find similar functionality on all tools
Provide integration for assistive technologies
Provide a selector to change style sheets for user personalization
Avoid the communication of system information based on colors (e.g., buttons with a specific color and meaning)
Provide the ability to change user preferences to change font size and style
Maximize compatibility with assistive technologies
Compliance-oriented design to improve interoperability with assistive technologies
Consistent and unique design of headings, links, buttons and images description
Provide descriptive forms including support for errors correction. Identification of the location of the users when filling a form
Minimal use of frames, appropriate use of title in frames, provide adoption of ARIA standard attributes and navigational marks (“role landmarks”), structural tags, and alerts
Multimedia (audio) functionalities
Authoring tools are software and services included in e-learning systems (LMS), used for teachers and students to produce web content as educational material. Authoring tools related to LMS include desktop applications, multimedia authoring tools, and mainly HTML editors (e.g., what-you-see-is-what-you-get WYSIWIG editors). These tools should follow the Authoring Tool Accessibility Guidelines (ATAG) 2.0 [14].
The Authoring Tool Accessibility Guidelines (ATAG) explain to developers how to make and adapt the authoring tools to be accessible so that people with disabilities can access and create educational content. The guidelines explain how to help authors (teachers and students) to create more accessible web content (learning material) with inline validators, forms with hints and reminders.
Accessibility, from the perspective of authoring tools, is related to content creators and then for final users (especially people with disabilities). Thus, ATAG [14] is divided into two parts, each reflecting a key aspect of accessibility with respect to authoring tools. Part A “Make the authoring tool user interface accessible” relates to the accessibility of authoring tool user interfaces to authors with disabilities. Part B “Support the production of accessible content” relates to support by authoring tools for the creation, by any author (teachers and students, not just those with disabilities), of web content that is more accessible to end users with disabilities.
Besides general authoring tools, which are referred by ATAG, it is important to keep in mind that in the field of e-Learning, educational resources are usually packaged in containers for interoperability and reusability. Following ATAG [14] recommendations, tools used to prepare educational containers should take into account the accessibility requirements.
The format most commonly used is Sharable Content Object Reference Model (SCORM). This is a set of standards and specifications for creating structured teaching objects [18]. With SCORM, it is possible to create content that can be imported into different learning management systems providing SCORM compatibility. Based on the original definition of SCORM (ADL) [18], it is important to mention the six motivations of the standards: accessibility, adaptability, affordability, durability, interoperability, and reusability. In this chapter, Section 4 will elaborate on two aspects: accessibility and adaptability for the learning objects, building blocks for this standard.
The users of an e-learning campus use different tools as media players, web browsers, and assistive technologies to be part of the educational process. These tools are known as user agents. The User Agent Accessibility Guidelines (UAAG) [15] explain how to make user agents accessible to people with disabilities, particularly to increase accessibility to web content, a basic building block for educational material in a virtual campus. As described in the working draft of UAAG Guidelines, in addition to helping developers of browsers and media players, UAAG 2.0 benefits developers of assistive technologies because it explains what types of information and control an assistive technology may expect from a user agent that follows UAAG 2.0. Assistive technologies not addressed directly by UAAG 2.0 [15] (e.g., Braille rendering) are still essential to ensuring web access for some users with disabilities.
UAAG is organized in guidelines, principles, and success criteria elements. There are five principles: “perceivable, operable, understandable, programmatic access, and specification and conventions.” Following the principles, there are 27 guidelines [15].
Nowadays, web applications, in our work the case of virtual campuses based on learning management systems, are increasingly using more advanced and complex user interface controls such as tree controls for site navigation, drag-and-drop functionality, or technologies developed with Ajax or DHTML. To prevent accessibility issues, the Web Accessibility Initiative (WAI) [13] proposed a recommendation called “Accessible Rich Internet Applications,” usually known as WAI-ARIA [16]. This suite of recommendations defines a way to make web content and web applications more accessible to people with disabilities. It especially helps with dynamic content and advanced user interface controls developed with Ajax, HTML, JavaScript, and related technologies.
More specifically, WAI-ARIA provides a framework for adding attributes to identify features for user interaction, giving hints on how they relate to each other, and their current state. The WAI-ARIA framework [16] identifies innovative navigation techniques to mark regions and common web structures as menus, primary content, secondary content, banner information, and other types of web structures. As a working example for developers, with WAI-ARIA, it is possible to identify regions of pages and enable keyboard users to easily move among regions rather than having to press the tab key many times.
WAI-ARIA also includes technologies to map controls, Ajax live regions, and events to accessibility application programming interfaces (APIs), including custom controls used for rich Internet applications. WAI-ARIA [16] techniques apply to widgets such as buttons, drop-down lists, calendar functions, tree controls (for example, expandable menus), and others usually available in virtual campuses so it is important that LMS administrators.
Once a virtual campus reaches an acceptable level of accessibility, this accessibility must be constantly maintained. The content and learning material published by the teachers and administrators will be periodically updated, and it is important to teach stakeholders on how to create and adapt learning content to be accessible following most used guidelines. Among the actions to be carried out periodically to maintain accessibility in a virtual campus are the following:
Training for teachers and students in techniques for creating accessible digital contents
Training for teachers in Universal Learning Design techniques
Providing in the virtual campus the functionality of online accessibility checkers when final users work with basic actions such as uploading images and alternative text, providing context information for links, validating information in content editors, etc.
It is important to take into consideration that when digital content is created by teachers or students in any type of format (textual, graphic, audio, or multimedia), it is necessary to keep in mind that final users of such content may be people with physical, sensory, or cognitive limitations, who could find barriers to access the information. In fact, at some point in our lives, we all probably will have limitations that can affect our access to digital content. Among the difficulties that teachers are facing when preparing learning content in digital format is the diversity of authoring tools available to create the content. In [19], a collection of the basic considerations to create accessible digital content are presented and for diversity, the Accessible Digital Office Document (ADOD) initiative [20] prepared different recommendations based on the content creator used.
The Accessible Digital Office Documents (ADOD) Project [20] is an initiative created to provide guidelines on the accessibility of office documents, office document formats, and office applications independent of the tool used to create the content. ADOD provides both an “ADOD Assessment Framework” and a suite of practical guidance documents that are intended to help stakeholders in the educational process to make decisions about office applications. Currently, ADOD is based primarily on the WCAG and ATAG recommendations presented in Section 2.
The recommendations provided for office tools are also applicable to PDF documents. Among the recommendations to create accessible PDF documents with learning content, based on WCAG 2.0 guidelines [21], are the following:
Check that all nontext elements should include alternative text.
Check for background color and foreground contrast.
Specify the text language in all documents to help assistive technologies.
Check if hyperlinks are correctly formatted and functional.
Provide labeling of elements and correct use of styles.
Provide alternative texts and contextual information for hyperlinks.
Provide information for abbreviations and acronyms.
Check for language changes in the text if more than one language is used.
Identify decorative elements in headers and footers.
Add markers (bookmarks) that allow the user to jump to a specific part of the document.
Verify that the default reading order, according to the structure of tags, makes sense and is consistent.
Check for the proper security settings, avoiding sharing a document with password.
If the PDF contains an image from a scanned document, an OCR process has to be prepared to provide the text as background alternative for assistive technologies.
In case the PDF contains a form, the fields properties should have a detailed description to help the user to fill in the requested information.
Besides the ADOD project and the recent book [19], other initiatives and guidelines for creating electronic documents accessible are found in [22–24].
As an alternative, authors can export a document in DAISY format, which is a good way to ensure that a document is accessible. DAISY is a multimedia format that maintains and promotes a system of Access to standard printed documents for blind, low vision or other problems. The format was developed by the DAISY consortium in 1996 and is currently based on the definition of ANSI/NISO Z39.86-2005 standard [25].
The text content can be exported in DAISY format with plug-ins for Word processors as Microsoft Office Word and LibreOffice Writer. This format can be tested with a DAISY complaint software, for example, the AMIS software (http:/www.daisy.org/amis). Exporting content to DAISY [25] format allows authors to check the accessibility of a document to a person with vision problems because the software prepares and audio book based on the content.
Administrators for a virtual campus based on learning management systems (LMS) should not assume that the users (e.g., teacher, instructor, tutor, student, etc.) have all the knowledge concerning WCAG guidelines or principles of Universal Learning Design. It is important to incorporate and provide descriptive aid in the different interfaces and provide validators to allow users to know whether the content is accessible based on the minimal requirements established by the educational institution.
Examples of basic functionality to be included to help final users creating contents are as follows:
Basic code validator (HTML) included in WYSIWYG content editors usually used in application for discussion forums, wikis, information box, etc. (e.g., AChecker plug-in (www.achecker.ca) for ATutor LMS)
Validator for images and alternative text aids for users editing content
Validator for accessibility in equation writer editors
The evaluation of the accessibility of a virtual campus and its contents is performed in two main phases.
Automatic analysis with validation tools
Manual analysis/heuristic evaluation by experts and end users
The first phase is proposed to use an online automatic validator based on the WCAG guidelines. Some of the identified tools available online are as follows:
Examinator (based on WCAG 2.0 guidelines) (www.examinator.ws)
AChecker (based on WCAG 2.0, HTML y CSS) (www.achecker.ca)
TAW (based on WCAG 2.0) (www.tawdis.net)
CynthiaSays (based on WCAG 2.0) (www.cynthia-says.com)
Tingtun (based on WCAG 2.0) (accessibility.tingtun.no)
HERA (based on WCAG 1.0) (www.sidar.com/hera)
WebAim (Web Accessibility Evaluation Tool) (http://wave.webaim.org)
HTML validator (http://validator.w3.org/)
CSS validator (http://jigsaw.w3.org/css-validator/)
The assessment of accessibility should identify a simple of pages related to the main actions from users within the virtual campus. The main actions to be evaluated are as follows:
Start using the virtual campus.
Visit the homepage of the educational institution.
Visit the accessibility information for the educational institution.
Pages that the user needs to visit to reach the virtual campus login pages.
Registration, enrollment, and log into the virtual campus.
Change the personal settings and preferences for the user.
Follow the steps to visit a course page.
Use basic functionality for students.
Find and review content within a course, including multimedia content.
Contribute to course content assigned to the student (wiki tool or upload a file form).
Find, check, and submit and assessment.
Find a questionnaire, read the instructions, answer all questions, and send the completed questionnaire (quiz).
Find and check the gradebook.
Read news and announcements published by the teacher.
Find, publish, and interact in a course blog.
Find the discussion forums application and be part of a conversation.
Use basic functionality for teachers.
Create and publish content in a course page.
Create content on the course with conditional availability (hide and enable content).
Create a task assignment.
Create a questionnaire with different types of questions.
Reorganize and sort items in the course menu.
Copy items from one section of the course to another section.
Login and manage the student gradebook.
Evaluate and comment a student assignment.
The pages included in the virtual campus (dynamic content and login required pages) usually cannot be verified easily by automatic analysis tools. To perform this analysis, it is possible to use installed tools as plug-ins (e.g., WAVE tool) or download the pages to be evaluated as static content.
The second phase of the evaluation is the heuristic evaluation by experts and end users. Automatic validation tools offer a partial view on the accessibility, but it is important to have a group of accessibility experts and final users with disabilities to test the main functions and have a contrasted opinion and recommendations to improve the accessibility of the virtual campus.
Learning objects (LOs) are the minimum unit in which educational content is organized so that it can be easily published for a better understanding. One of the most popular definitions of LO is that offered by Wiley “as any digital resource that can be reused to support learning” [26].
The main goal of an LO is their reuse in more than one training activity. To do this, it is necessary that the LO can be found in a simple manner. To achieve this, we need to describe the LO’s characteristics, including their metadata, which are a set of fields that provide information about the LO such as, for example, its title, its description, the language in which it is written, or its scope. There are some specifications and standards commonly used to define the LO metadata for their correct description. The most popular are Dublin Core [27] and LOM [28].
LOs, besides regular metadata, must have associated accessibility metadata that describe their accessibility characteristics and that make them accessible to all people. These metadata are the fields used for searching accessible LOs.
Repositories are used to store LOs and to facilitate their search and therefore their reuse. Search operations are performed based on their metadata, hence the importance of clearly and correctly describing the resources, which provides more precise searches. One of the most known repositories is Merlot [29], which have an interesting advanced search function.
When users need to perform a training activity, they use these repositories to find the learning objects that better adapt to that training, thus drawing up a new course from the learning objects found in the repository or repositories to they can access.
Metadata should be inserted in an XML (extensible markup language) file [30], composed of each of the fields (each field corresponds to a metadata) described following one of the standards published for this purpose, such as, for example, learning object metadata (LOM) [28]. This work is provided by metadata editors such as, for example, LomPad, known for being one of the most used [31].
LomPad editor.
As shown in Figure 1, the LomPad editor allows completing the LOM metadata fields. Once all data have been inserted, an XML file containing all information is generated.
The process for sharing content and distributing it among different information systems is to pack it in a compressed file composed of the content and metadata that describe it. In this scope, there are two specifications widely used, such as Sharable Content Object Reference Model (SCORM) [18] and IMS Common Cartridge [32]. Just as there are editors to help content authors to describe the metadata, there are also editors that help to pack this content along with metadata. One of the most known editors is Reload Editor [33].
Reload not only allows packing content based on SCORM specification but also allows to describe resources with metadata (analogously to LomPad) and to organize the sequencing of these resources.
IMS AfA v3.0 specification [12] is a way to add accessible metadata to a learning object. Using this, we can describe what is the best sensory form to access the learning object. The specification is created with the aim of simplifying the ISO/IEC 24751 standard [9–11] due to the difficulties encountered when putting it into practice. Both standard and specification in version 3.0 cover the entire process from reading the user needs to the search mechanism needed to find the LO that meets those needs or preferences. The main objectives of IMS AfA v3.0 specification are as follows [12]:
Being simple and easy to understand
Facilitating its modification to suit the needs of the organizations requiring some parts of the model
Facilitating integration with other metadata and specifications
Allowing integration with devices’ properties standards for accessibility
Allowing integration with user agents, accessibility APIs, and productivity-oriented accessibility standards
Allowing inclusion in accessibility frameworks and tools
It has two metadata models to describe the following:
Personal needs and preferences (PNP): description model of the users’ needs and preferences to access and interact with the digital resources
Digital resource description (DRD): description model of the accessibility metadata for the digital training resources
With the AfA DRD, the accessible metadata of the learning objects are described and with the AfA PNP the students can provide their personal needs (or those due to disability environments). The goal is to find the learning objects that best match user needs and preferences in an automated way, solving the metadata similarities between PNP and DRD.
AfA DRD defines the accessibility metadata of a resource that will be used for searching and using the most adequate learning resource to each user according to his or her PNPs.
The adaptation of a learning object occurs when we produce one with the same training content but with a different form of access. To achieve this, two types of LOs must exist: original and adapted. An original resource corresponds to a primary resource, while an adapted resource presents the same educational information than the original resource, for example, a PDF format file as the original resource and an audio description of its content as an adapted resource. The first one presents textual access, while the adaptation presents auditory access to the same educational content.
Original resources may have any number of adaptations, which may be total or partial, i.e., or they are adaptations of the whole educational content or they are just a part of this.
Digital resource description (DRD) properties.
Figure 2 shows the accessibility properties or metadata of a resource and how they relate to each other, as IMS AfA v3.0 specification presents them. As seen in the figure, in order to simplify as much as possible the data model, the metadata have been organized in two clearly distinguished levels:
Those belonging to a basic core (Core Profile), containing the most important metadata, necessary for a proper description of the resource
Those belonging to the full specification, which extent and complement the basic core information
The specification shows a common information model to define and describe the student’s or user’s PNPs with a different sensory perception mode or who is in a disability context. The user’s PNPs may be environmental (for example, “in the dark”), may be related to the communications technology or the available and specific information services (for example, “when a Braille device is available”), or may relate to social situations (for example, “when my nurse is present”) or other scenarios.
The recommended method to generate the student’s PNPs is the presentation of a form with various options (like aforementioned or preferred sensory mode). The PNPs will be generated from students’ responses to these questions.
The declaration of PNPs is associated to one person. In turn, one person can generate several sets of PNPs for being used in the environment he or she is at each moment (for example, in the dark or in a noisy area). Like any software application, user’s PNPs should be easily modified by editing the user profile and by allowing its extension, replacement, or removal.
Personal needs and preferences (PNP) properties.
Figure 3 shows the user’s accessibility properties and how they relate to each other. In the same manner as specification AfA DRD, there are properties belonging to the basic profile (Core Profile) and those belonging to the full specification.
In this section, a scenario of use of IMS AfA v3.0 specification [12] is described in addition to other e-learning specifications and standards previously explained, describing all stages for getting an accessible learning object.
First, a content author plans to carry out a learning resource that contains a video tutorial (original resource) of an educational course. An alternative content (adapted resource) is created to provide access to this resource to the students with disabilities (especially those with visual problems). This resource consists of an audio description (audio file that describes the images containing meaningful information).
The content author uses LomPad [31] or Reload [33] to describe the LOM metadata of the video tutorial, thus describing the educational material so that it can be located and reused in different training activities.
Then it is necessary to include the accessibility metadata of the original resource; thus, the type of sensorial perception is described, which is needed to understand the training content. As this is a video, both the visual and the auditory senses are needed. For inserting the accessibility metadata by following IMS AfA specification, the author can use LomPad-AfA tool [34], as shown in Figure 4, whose ultimate goal is to generate the XML file, as shown in Figure 5. LomPad-AFA allows the content authors and the learning platform users to insert accessibility metadata of LOs (DRDs) and students’ PNPs, respectively, generating both XML format files. This tool allows to complete the properties of DRDs and PNPs graphically and to generate the corresponding XML file following the IMS AfA v3.0 specification.
In the XML file generated, which is shown in Figure 5, it is described that the original resource has two access modes: visual and auditory. It has one adaptation: OR_1_A1, and it can be controlled using the keyboard and mouse.
The following step will be creating the description for the adapted resource, which contains the audio description. Using LomPad-AfA, the accessibility metadata are filled and the XML file is generated (Figure 6).
Original resource’s DRD XML (afadrdv3p0_OR_1.xml).
In the XML file generated, which is shown in Figure 6, it is described that the adapted resource has an auditory access mode, and it adapts a visual one. More details about the type of adaptation are given through property “adaptation type,” and it is specified that it is an audio description. It has full control by keyboard and mouse. It is an adaptation of the original resource OR_1, and it is a partial adaptation. Finally, it states that the audio is recorded using a human voice.
Once the resources are created and the metadata are defined in their corresponding XML files, a package containing all information and following SCORM specification will be created. As shown in Figure 7, the SCORM package will be composed of two resources (the original and the adaptation) and their metadata files. The original resource will have associated two metadata files, one with its LOM metadata and another one with the IMS AfA metadata. Adapted resource only needs the IMS AfA metadata since the adapted resource contains the same learning information as the original.
Adapted resource’s A1 DRD XML (afadrdv3p0_OR_1_A1.xml).
LomPad-AfA resource DRD properties.
LomPad-AfA user PNP properties.
Furthermore, LomPad-AfA tool allows generating XML files containing the users’ PNPs. For example, if a blind person or a person with visual problem wants to describe his or her preferences, he or she has to fill the metadata, as shown in Figure 8, and generate the XML file, as shown in Figure 9.
SCORM content.
User PNP XML (afapnpv3p0_USR1.xml).
In the XML file generated, as shown in Figure 9, it is described that, for visual content, the user prefers adapted resources that have an auditory or textual access mode. By means of property “adaptation type required,” more details about the type of desired adaptation for visual content are given, and it is specified that they should contain audio description or long description. A learning system (educational platform, learning object repository, etc.) that is able to understand the PNP defined above and whose user is interested in learning the educational resource of the video tutorial, which represents the original resource, should show the adaptations that are associated with it.
The accessibility of a virtual campus should be ensured at two levels: (1) the accessibility of the learning management system (LMS) that supports the campus and (2) the accessibility of the learning materials published on the platform. A virtual campus with an LMS platform that meets the criteria under different guidelines as described in WCAG 2.0 will be accessible, but when new content is published, the accessibility could be lost, and students with disabilities could face barriers to achieve the learning objectives. Thus, it is important to maintain a continuous process of training for stakeholders involved in the virtual campus.
The main principles that an accessible virtual campus should provide are as follows: (1) allow users to customize their portal based on their preferences, (2) provide equivalents to every time-based media and visual elements, (3) use different ways to present information in an interface, (4) provide information appropriate compatible with assistive technologies, (5) allow access to all functionalities via keyboard, and (6) provide background information and status and location information to the user at all times.
Training for users of virtual campus, publishing learning content is an ongoing process that should primarily include the following components: (1) training teachers and students in techniques for creating accessible documents, (2) training teachers on universal learning design techniques, and (3) training LMS administrators to maintain the accessibility and configure the LMS to provide validators of accessibility in content editors, to ease the process of learning objects publication.
IMS AfA v3.0 specification presents to the content authors and developers the technical way to follow for achieving an accessible online teaching. According to ISO/IEC 24751-2-3 standard and IMS AfA v3.0 specification, the basic steps in developing an accessible online course are as follows: creating accessible learning objects (LOs), both original and adapted, by means of inserting the accessibility metadata; reading the users’ personal needs and preferences (PNP); and searching and presentation of LOs meeting those PNPs.
For an LO that can be used in an educational platform, it is necessary to pack all files shaping the LO with the files containing its metadata, including the accessibility ones, and following the standards established. There is a great lack of technical applications and human resources to provide assistance in developing accessible resources.
This work is funded by the University of Alcalá (Spain) and Galileo University (Guatemala) (grant ESVIAL project). Authors also want to acknowledge support from the Master in Software Engineering for the Web and the TIFyC research group.
There is much evidence that significant changes in the body and fat weight in men with metabolic disorders, such as severe obesity and type 2 diabetes mellitus (DM2), and with long-term fasting can lead to the alteration in the hypothalamic-pituitary-gonadal (HPG) axis, as illustrated by the changed secretion of gonadotropin-releasing hormone (GnRH) and gonadotropins, the reduced testosterone (T) production by Leydig cells and the impaired spermatogenesis. The alterations in the HPG axis, as a result, lead to infertility [1, 2, 3]. The relationship between the fat content and androgens level has been demonstrated in animals with obesity and DM2, as well as in fasting conditions [4, 5, 6]. All this indicates that adipocyte-produced factors can play an important role in controlling the HPG axis and in regulating the steroidogenesis in Leydig cells. Among these factors, the most interesting are adipokines, such as leptin, adiponectin, resistin and visfatin [3, 7, 8]. It is well known that in metabolic disorders, the plasma levels of these adipokines and the functional activity of adipokines-regulated signaling systems in the target tissues undergo significant changes, which can be considered to be one of the key causes of abnormalities in the HPG axis and androgen deficiency [9, 10, 11].
\nThe regulatory effects of the plasma, pituitary and testicular leptin on the male HPG axis and the testosterone synthesis in the testes in the norm and in the metabolic disorders. Abbreviations: p-Lep and t-Lep, the pituitary and testicular leptin; LepR, leptin receptor; GnRH, gonadotropin-releasing hormone; GnRH-R, receptor of GnRH; LH, luteinizing hormone; T, testosterone; AMPK, AMP-activated protein kinase; CREB, cAMP response element-binding protein; Nur77, c-Jun, c-Fos and Sf1, transcription factors Nur77, c-Jun, c-Fos and Sf1; SREBP1, sterol regulatory element-binding protein-1; cAMP-PDE, cAMP-specific phosphodiesterase; StAR, steroidogenic acute regulatory protein; P450scc and P450c17, cytochromes P450scc (P450 cholesterol side chain cleavage enzyme) and P450c17; 3β-HSD, 3β-hydroxysteroid dehydrogenase; α-MSH, α-melanocyte-stimulating hormone; AgRP, agouti-related peptide; NPY, neuropeptide Y; BBB, blood-brain barrier; BTB, blood-testicular barrier.
The regulatory effects of adiponectin circulating in the blood and adiponectin synthesized in the pituitary and testes on the activity of the male HPG axis and the testosterone production. Abbreviations: AdipoR1 and AdipoR2, adiponectin receptors of the types 1 and 2; ERK1/2, extracellular signal-regulated kinases 1/2; Sp1, transcription factor Sp1. The other abbreviations are the same as in
There is evidence that adipokines affect the different components of the male HPG axis. Transferred to the brain through the blood-brain barrier (BBB), adipokines act on the activity of hypothalamic GnRH-expressing neurons, thus changing the GnRH-stimulated production of luteinizing hormone (LH), the main regulator of T synthesis, by pituitary gonadotrophs [12, 13]. The adipokines can directly affect the gonadotrophs producing LH, and in this regulation both the adipokines circulating in the bloodstream and the adipokines synthesized within the pituitary can be involved [14, 15]. Some adipokines can also directly affect the functions of Leydig cells, as indicated by a high level of adipokines expression in the testes, as well as detection of the main components of the adipokine signaling, including adipokine-specific receptors, in testicular cells, including Leydig cells [16, 17, 18, 19]. The study of the effects of leptin, adiponectin and other adipokines on the male HPG axis and their role in the regulation of steroidogenesis is a major problem of clinical endocrinology and reproductive medicine. The solution of this problem will allow developing the new approaches for restoring the reproductive functions and androgen status in men with endocrine and metabolic disorders, which is based on the normalization of the adipokine signaling in the CNS and at the periphery.
\nThis review presents the comprehensive analysis of the involvement of leptin, adiponectin, resistin and visfatin in the regulation of the male HPG axis and steroidogenesis, as well as of the possible mechanisms of this regulation. The role of adipokines in the dysregulation of the male reproductive system and the impaired steroidogenic activity in the testes in obesity and DM2 are also discussed.
\nLeptin, a 167-amino acid polypeptide hormone encoded by the
The regulatory effects of leptin are realized due to its specific interaction with leptin receptors (Ob-R) that are generated by alternative splicing and include at least six isoforms [26]. The full-length isoform Ob-Rb is active and expressed in the hypothalamus with high intensity [27, 28]. The truncated isoforms, Ob-Ra, Ob-Rc, Ob-Rd and Ob-Rf are inactive, but retain the ability to bind to leptin at its excess. It is assumed that they carry out the receptor-mediated transport of leptin through the BBB and, possibly, through other tissue barriers [29, 30]. In the arcuate nuclei (ARC) of hypothalamus, leptin binds to Ob-Rb receptor, which leads to the phosphorylation of JAK2, a non-receptor tyrosine kinase, that phosphorylates the Tyr985, Tyr1077 and Tyr1138 residues located within the intracellular domain of Ob-Rb, each responsible for the activation of certain signaling cascade [23]. It has been shown that the phospho-Tyr985 is responsible for activation of Src Homology 2 domain-containing protein tyrosine phosphatase 2 (SHP-2) and the mitogen-activated protein kinases (MAPK), such as extracellular signal-related kinases-1/2 (ERK1/2), c-Jun amino-terminal kinases (JNK) and p38-MAPK, which are involved in the regulation of cell growth and differentiation. The targets of MAPK are different transcription factors, including c-Fos, c-Jun and cAMP response element-binding protein (CREB), which control the expression of a large number of genes [3, 31]. The phospho-Tyr1138 is responsible for activation of the transcription factor STAT3 (signal transducer and activator of transcription-3) regulating the expression of genes involved in metabolic and growth processes. In turn, phospho-Tyr1077 induces the activation of the transcription factor STAT5, responsible for the regulation of energy metabolism and endocrine system [23, 32].
\nAnother mechanism of leptin action is the activation of 3-phosphoinositide pathway, which involves phosphatidylinositol-3-kinase (PI3K) and Akt kinase controlling the activity of the multi-component kinase mTOR complex 1. Since Akt-mediated inhibition of this complex in the hypothalamic ARC leads to a decrease in the expression of the
In the recent years, the evidence has been obtained that leptin plays a very important role in the control of male reproductive functions and puberty, which is based on leptin-mediated regulation of the HPG axis [8, 37]. The
A survey of men from Slovenia, Macedonia and Serbia with three different mononucleotide mutations within the
The mutations within the
The effects of leptin on the male HPG axis can be carried out at the level of hypothalamic neurons, pituitary gonadotrophs and testicular cells. It is important to note that the response of the HPG axis to leptin depends on the dose of this adipokine and the duration of treatment, the metabolic and hormonal status, as well as the functional state of the leptin signaling system in the target tissues. This is well illustrated by the data on the influence of leptin on the hypothalamic structures. It is shown that a single i.c.v. administration of leptin to ovariectomized female rats under starvation conditions, when the leptin level was reduced, led to a rapid increase in the plasma LH level, which demonstrates leptin-mediated stimulation of secretory activity of the GnRH-neurons [12, 46]. At the same time, under conditions of prolonged administration of leptin, an increase in LH level [47] or lack of leptin effect on LH secretion [48] were detected, which may be assumed to be due to varying degrees of leptin resistance in the case of long-term action of leptin on hypothalamic neurons. This was supported by the fact that the action of low, nanomolar concentrations of leptin on the ARC and the ventromedial nuclei of the hypothalamus led to an increase in the GnRH secretion, while high, micromolar leptin concentrations did not cause this effect [5, 37]. The i.c.v. administration of leptin to fasting cows led to an increase of both basal and GnRH-stimulated LH secretion, while the administration of leptin to fed animals with the increased leptin level did not induce significant changes in LH level [49, 50]. Thus, the stimulating effect of leptin on the HPG axis at the hypothalamic level was largely dependent on eating behavior, and was the main mechanism that mediates the relationship between the satiety and metabolic status, on the one hand, and the gonadotropins levels and activity of the steroidogenesis system, on the other.
\nThe central effects of leptin on the HPG axis are mediated through its interaction with leptin receptors located on hypothalamic ARC neurons expressing either pro-opiomelanocortin (POMC) or agouti-related peptide (AgRP) and neuropeptide Y (NPY). Due to activation of these neurons by leptin, the positive (POMC-neurons) or negative (AgRP/NPY-neurons) regulation of GnRH-neurons occurs, especially since these neurons themselves do not contain the receptor Ob-Rb and, therefore, can not be target for leptin (Figure 1).
\nLeptin-induced activation of ObRb located on the POMC-neurons leads to an increase in the production of POMC-derived melanocortin peptides, primarily α-melanocyte-stimulating hormone (α-MSH), an agonist of types 3 and 4 melanocortin receptors (MC3R and MC4R) [51]. The α-MSH binds to MC3/4R located on GnRH-neurons, and stimulates the GnRH secretion by them. In favor of this mechanism, there is evidence that the administration of leptin to the preoptic area of the hypothalamus leads simultaneously to an increase in α-MSH level and a stimulation of GnRH secretion [52]. The MC3/4R agonists, such as α-MSH and its analogue melanotan-II are also effective, increasing GnRH release [53, 54]. It should be noted that at least 70% of GnRH-neurons are activated by α-MSH [53]. Both MC3R and MC4R are involved in the effects of melanocortin peptides on GnRH-neurons, since mice lacking only one type of MCR remain capable of reproduction [55, 56].
\nAnother mechanism for leptin regulation of GnRH secretion, in which the melanocortin peptides also participate, is more complex. In accordance with this, in the first stage the melanocortin peptides secreted by POMC-neurons interact with MCR located on the KNDy-neurons. Kisspeptin released from KNDy-neurons binds to the kisspeptin receptors located on GnRH-neurons and stimulates GnRH secretion [57]. In the hypothalamic ARC, the outgrowths of POMC-neurons form the contacts with the bodies of KNDy-neurons, and a release of α-MSH by POMC-neurons causes a rapid depolarization of KNDy-neurons. Pharmacological inhibition of MC3R and MC4R by the antagonist SHU9119 decreases the expression of kisspeptin by 45%. The stimulating effect of melanotan-II on LH production in mice lacking the kisspeptin receptor GPR54 was reduced significantly [57].
\nThe AgRP, the endogenous MC3/4R antagonist, and NPY, both produced by the AgRP/NPY-neurons, mediate the inhibitory effect of leptin on LH production by pituitary gonadotrophs. However, the degradation of AgRP/NPY-neurons and the knockout of the
Leptin can stimulate LH production, acting directly on gonadotrophs (Figure 1). Unlike the hypothalamus, where leptin is mainly transferred from the bloodstream, its source in gonadotrophs can be either the plasma leptin or pituitary leptin synthesized by gonadotrophs [67, 68]. There is a good reason to believe that pituitary leptin functions as a paracrine and autocrine regulator controlling the survival and functional activity of gonadotrophs, since the plasma leptin can not mediate the complex pattern of pituitary hormone secretion [69]. This assumption is supported by the data obtained in mice with tissue-specific knockout of the
The functions of the autonomous leptin system in the pituitary, its participation in gonadotropins production and the relationship between the activity of this system and the physiological state of the HPG axis are supported by the following facts. The
Currently, there is evidence that leptin not only indirectly affects the steroidogenesis in Leydig cells through the regulation of the HPG axis but is also capable of directly affecting the activity of steroidogenesis system [3, 8]. The following facts support this: (1) the transport of leptin circulating in the bloodstream through the blood-testicular barrier (BTB) and the synthesis of leptin in the testicular cells; (2) the expression of leptin receptors and the presence of effector components of the leptin signaling in Leydig cells and (3) the results of the
In 1999, Banks and coauthors showed that leptin circulating in the blood was transported through the BTB, and the permeability was higher than in the case of the BBB [75]. Based on high rate of leptin transport through the BTB and high permeability of this barrier to other proteins, it was concluded that the mechanisms of leptin transport through the BBB and BTB differ significantly. However, taking into account the high density of the truncated isoform Ob-Ra of leptin receptor on the surface of endothelial cells forming the BTB, there is reason to believe that, like the BBB, leptin transport through the BTB is also a receptor-dependent [37]. In this case, one should expect its dependence on the activity of the leptin signaling system at the periphery and its decrease in the conditions of leptin resistance. Another source of intratesticular leptin was its synthesis in the testes of adult men and animals. The highest level of the
The effectors, whose activity is regulated by leptin through the activated forms of Ob-Rb and JAK2, control the activity of the transcription factors regulating the expression of steroidogenesis genes in different ways [3]. Leptin-induced stimulation of Akt-kinase and MAPK results in the phosphorylation and activation of the transcription factor CREB that is also activated by gonadotropins via cAMP-dependent pathways [81]. The activation of p38-MAPK and JNK leads to the stimulation of the transcription factors Nur77 and c-Jun [82, 83]. The main targets for these factors are the genes encoding StAR protein responsible for transport of cholesterol into the mitochondria and P450 cholesterol side chain cleavage enzyme (cytochrome P450scc) converting cholesterol to pregnenolone [84] (Figure 1). Along with this, the activation of MAPK cascade results in an increase in the expression of Sf-1 factor, the coactivator of expression of the gene encoding StAR and the genes
Leptin activation of the STAT3 and STAT5, as well as leptin-induced ERK1/2-dependent activation of the factor c-Fos lead to the opposite effect and suppress steroidogenesis in Leydig cells. An increase in ERK1/2 activity may be due to the prolonged leptin effect on the system Ob-Rb/JAK2 and, as a result, the activation of SHP-2 phosphatase, which affects the activity of MAPK cascade [89]. A decrease in T production by Leydig cells can be the result of AMPK activation, which suppresses the activity of sterol regulatory element-binding protein-1 (SREBP1) [90]. As is well known, SREBP1 positively regulates the
In addition to direct leptin effect on the expression of steroidogenesis genes, this adipokine can modulate the gonadotropin signaling pathways in Leydig cells, inducing an increase in gonadotropin-stimulated T production. It is well known that LH and human chorionic gonadotropin (hCG) specifically bind to LH/hCG receptors located on Leydig cells and stimulate the activity of adenylyl cyclase catalyzing cAMP synthesis, which leads to the activation of protein kinase A and CREB. Further, the level of intracellular cAMP is reduced due to its hydrolysis by cAMP-specific phosphodiesterases (cAMP-PDE), which leads to the attenuation of signal transduction generated by gonadotropins and inhibits their stimulating effect on steroidogenesis. Leptin suppresses the cAMP-PDE activity, maintaining the increased level of intracellular cAMP and thereby potentiates steroidogenic effect of gonadotropins (Figure 1). This is supported by the data that leptin enhances the stimulating effect of hCG on the cAMP level in rat Leydig cells [77].
\nAlong with the regulation of T synthesis in Leydig cells, leptin controls the mass and size of the testes, diameter of the seminiferous tubules and spermatogenesis and affects the survival of Leydig cells and other testicular cells [26, 93]. Leptin also regulates steroidogenesis in the ovaries and adrenal glands, and the mechanisms of its regulatory effect are believed to be similar to those in Leydig cells [37, 94].
\nIn men with obesity, metabolic syndrome and DM2, the activity of the male HPG axis and the T production are decreased, which lead to androgen deficiency [95, 96, 97]. Along with this, in diabetic men the plasma level of estrogens and the ratio of estrogen/T are significantly increased, which due to the increased activity of aromatase and the altered production of sex hormone-binding globulin [98, 99, 100, 101]. The elevated concentrations of reactive oxygen species and inflammatory factors lead to the damage in Leydig cells and reduce their steroidogenic activity [97, 102].
\nIn obesity and DM2, the plasma leptin level is significantly increased [103, 104], which leads to leptin resistance. As a result, the receptor-mediated transport of leptin through the BBB is reduced, which leads to a decrease in the intrahypothalamic leptin level and to a weakening of the regulatory effects of leptin on hypothalamic neurons and GnRH secretion (Figure 1). It is also not possible to exclude the possibility of reducing leptin transport through the BTB, although such data have not yet been obtained.
\nThe detailed study of the relationships between the leptin signaling and androgen deficiency in men with obesity and DM2 are not currently available. In rats with diet-induced obesity, severe hyperleptinemia and leptin resistance was associated with a decrease in the number of Leydig cells by 30%. This can be caused by the reduced intratesticular levels of leptin or the decreased sensitivity of testicular cells to this adipokine that participates in the regulation of survival and proliferation of Leydig cells (Figure 1). Although the plasma T level in obese male rats did not change, in the testes of animals it decreased by 25%, which was associated with a decrease in the expression of the
The deterioration of reproductive functions was found in mice with a knockout of the gene encoding the catalytic p110α-subunit of PI3K in the adipose tissue [106]. In the testes of 30-day knockout mice with severe hyperleptinemia, the expression of the gene encoding leptin was increased, while the expression of the genes encoding StAR and P450scc was reduced. Adult knockout mice had a severe form of hyperleptinemia, obesity, hepatic steatosis and the impaired glucose tolerance, and were infertile. It was quite unexpected that in the testes of knockout animals the expression of the
Polypeptide hormone adiponectin is produced mainly by the adipose tissue [109, 110], but despite this, the plasma adiponectin level is negatively correlated with the body mass index and the reserves of adipose tissue [111]. The plasma level of adiponectin is characterized by gender specificity and significantly lowers in males, which is true for humans and rodents [112]. Adiponectin can be synthesized not only by the adipose tissue but also by the brain, pituitary, testes and others [17, 113]. Adiponectin is consists of a variable N-terminal domain, a large globular C-terminal domain and a collagenous domain located between them, containing 22 collagenous Gly-XY repeats [114, 115, 116]. Using the collagenous repeats, adiponectin molecules interact with each other to form the homotrimeric complexes that aggregate into the hexamers and high-molecular complexes similar to those in the case of tumor necrosis factor-α (TNF-α) [117]. To form the trimeric complex, hydroxylation of the proline and lysine residues in the collagenous repeats is necessary, since the lack of this modification does not allow the formation of such complex and leads to a loss in the adiponectin activity [118, 119]. High-molecular complexes of adiponectin are stabilized by disulfide bonds formed between the trimers [120]. The trimeric, hexameric and high-molecular complexes are present in the bloodstream, while the monomeric forms are found in trace amounts [115, 121, 122, 123]. Post-translational modifications of adiponectin and its oligomerization significantly affect the bioavailability, binding characteristics and pattern of specific activity of adiponectin [115, 120, 123, 124, 125].
\nThe tissues, the targets of adiponectin, express the adiponectin receptors AdipoR1 and AdipoR2, which bind specifically to various forms of adiponectin with different affinity [111, 125, 126, 127]. Despite the fact that both these receptors seven times penetrate the plasma membrane, like classical G protein-coupled receptors, they differ significantly from them in membrane topology, having the extracellular C-terminal domain and the intracellular N-terminal domain. In addition, the adiponectin receptors interact with APPL proteins (adaptor protein, phosphotyrosine interacting with plekstrin-homologous domain and leucine zipper), but not with heterotrimeric G-proteins. The AdipoR1 binds with a high affinity to the truncated globular form of adiponectin and with a low affinity with the oligomeric and high-molecular forms of full-length adiponectin, while AdipoR2 binds with an intermediate affinity to both the full-length and globular forms. The both receptors interact with two isoforms of the APPL proteins, APPL-1 and APPL-2 [128, 129]. The interaction of adiponectin-activated AdipoR1 with APPL-1 leads to the activation of AMPK and the 3-phosphoinositide and MAPK cascades. The APPL-2 forms a complex with APPL-1 and prevents APPL-1-mediated regulations. When adiponectin binds to AdipoR1, the APPL-1/APPL-2 complex dissociates, resulting in the release of APPL-1 to interact with the downstream effector proteins [116, 130].
\nAdiponectin is able to control steroidogenic function in the testes directly, acting on Leydig cells, and indirectly, acting on the HPG axis at the hypothalamic and pituitary levels. To interact with hypothalamic neurons, the main target of adiponectin in the CNS, it is necessary to transport adiponectin into the brain through the BBB. It is suggested that the receptor-mediated transport of adiponectin through the BBB can be carried out through the AdipoR1 and AdipoR2 receptors located on the endothelium of cerebral vessels (Figure 2). In addition, a large number of adiponectin receptors and the components of adiponectin-regulated signaling pathways have been identified in the ARC and paraventricular nuclei of the hypothalamus [131, 132, 133, 134] and in other brain areas [13]. Adiponectin is easily transferred from the bloodstream to the brain and cerebrospinal fluid (CSF), although its concentration in the CSF is low, being only 0.1% of that in the blood [132, 133, 134, 135]. In obesity, which was characterized by the reduced plasma level of adiponectin [134, 136, 137], its concentration in the brain areas was also decreased [134]. It should be noted that, as in the case of circulating adiponectin, a negative correlation was found between the adiponectin level in the CSF and the body mass [133, 134]. Thus, unlike leptin, intracerebral adiponectin deficiency in obesity is caused by a reduced level of this adipokine in the blood. Although there is evidence that adiponectin can be synthesized in the CNS [17, 113], the greatest, if not all, amount of this adipokine comes from the periphery, and the intracerebral level of adiponectin depends on the activity of adiponectin-transporting system of the brain.
\nUpon binding to adiponectin receptors in neurons of the paraventricular nuclei and the periventricular region of the hypothalamus, adiponectin activates AMPK [13, 138], decreases the activity of ERK1/2 [13], causes a weakening of the calcium-dependent signaling pathways and inhibits the hyperpolarization-activated cationic currents responsible for pacemaker activity of GnRH-neurons [139]. It is important to note that the inhibition of ERK1/2 activity is due to an increase in AMPK activity [13]. The main result of adiponectin action on GnRH-neurons is a decrease in the synthesis and secretion of GnRH and, as a consequence, a decreased LH production by gonadotrophs [13, 139] (Figure 2).
\nAdiponectin also interacts with the KNDy-neurons expressing kisspeptin. Adiponectin-induced increase in AMPK activity in these neurons results in the inhibition of AMPK-dependent transport of the transcription factor SP1 into the nucleus, which is illustrated by SP1 accumulation in the cytoplasm. As a result, the expression of the
The inhibitory effect of adiponectin on LH production can be carried out at the pituitary level, since both adiponectin receptors were detected in the LH-expressing gonadotrophs of human and rats [14, 142, 143]. In addition, the expression of the
As noted above, the expression of the
The main regulators of the
The AdipoR2 was located on the surface of Leydig cells, while AdipoR1 was found in the epithelium of the seminiferous tubules. In spermatozoa there are both types of the adiponectin receptors [17, 148, 149]. The
All of the above indicates that adiponectin positively regulates the T synthesis (Figure 2). Indeed, treatment of the MA-10 Leydig cells with adiponectin at the concentrations of 50–5000 ng/mL resulted in an increase in the production of progesterone, a precursor of T, which was associated with cAMP-dependent activation of StAR and cytochrome P450scc [151]. In the earlier studies, it was shown that adiponectin, acting on the testes, suppressed both the basal and hCG-stimulated T production, although the expression of the steroidogenesis enzymes, such as cytochrome P450scc and dehydrogenases 3β-HSD and 17β-HSD3, did not change [17, 148]. The mechanisms of adiponectin action on Leydig cells include the stimulation of PI3K and Akt kinase, which results in the changed expression of Akt-dependent genes, as well as the regulation of ERK1/2, whose activity decreases at low concentrations of adiponectin and increases at its high concentrations [148]. It can be assumed that the dependence of adiponectin effect on ERK1/2 on its concentration, as well as a set of the effector components of MAPK cascade regulated by adiponectin are responsible for the different mode of the regulation of steroidogenesis by this adipokine. The treatment of Leydig cells with adiponectin did not affect the expression of LH receptor, and this indicates the preservation of the sensitivity of these cells to gonadotropins [148].
\nVisfatin produced by the adipose tissue is a multifunctional protein that functions as a signal molecule and as a nicotinamide phosphoribosyltransferase (NAMPT) catalyzing the synthesis of nicotinamide adenine mononucleotide from nicotinamide and 5-phosphoribosyl-1-pyrophosphate [152, 153, 154]. In humans, visfatin includes 491 amino acids and forms a functionally active homodimer complex [10, 155, 156]. Paradoxically, the receptor for visfatin has not yet been found. It is known that the main targets of visfatin, as in the case of most other adipokines, are the MAPK and PI3K/Akt pathway, and the activation of Akt kinase occurs 5 min after treatment of cells with visfatin [156, 157, 158].
\nThe highest concentration of visfatin is detected in the white adipose tissue. In obesity and DM2, the plasma visfatin level is steadily increased, and the degree of this increase varies greatly, due to both the individual characteristics of patients and the various approaches to measure the visfatin concentration [2, 155]. The visfatin level is also increases in women with a polycystic ovary syndrome, for which obesity and insulin resistance are characteristic [155]. Despite an increase in the plasma level of visfatin, its concentration in the CSF decreases, and this is probably due to the impaired transport of visfatin through the BBB. These data suggest that, as in the case of leptin and insulin, the transport of visfatin into the brain can be receptor-mediated, and decreases in the conditions of visfatin resistance.
\nThe data on the involvement of visfatin in regulation of the reproductive system are mainly related to the female HPG axis, folliculogenesis and steroidogenesis in the ovaries [7]. There is a positive correlation between the visfatin level in follicular fluid and the quantity and quality of the follicles [159]. It is assumed that the effect of visfatin on the ovarian steroidogenesis system can be realized via the mechanisms that lead to an increase in the production of insulin-like growth factor-1 (IGF-1), a stimulator of steroidogenesis [138]. In this case, the effects of visfatin are characterized by species specificity. The introduction of recombinant human visfatin into chicken did not stimulate, but, on the contrary, suppressed the basal and IGF-1-stimulated expression of the
In the case of the male reproductive axis, the targets for visfatin may be all of its components. Information on the central mechanisms of action of visfatin is limited to its effect on the hypothalamic neurons responsible for control of glucose homeostasis [160]. However, the fact that visfatin, like leptin, affects the activity of 3-phosphoinositide pathway, supports its possible participation in the regulation of GnRH-neurons activity. The evidences were obtained in favor of the regulation of LH-expressing pituitary gonadotrophs by visfatin. Firstly, the mRNA for visfatin was detected in gonadotrophs, which indicates its synthesis in them and the role of visfatin in the autocrine and paracrine regulation of the anterior pituitary. Secondly, visfatin stimulates the AMPK activity in the cultured murine gonadotroph-like cells LβT2, resulting in a decrease in LH secretion [161].
\nThe ability of visfatin to influence the testicular functions and the T synthesis is supported by the following data. Visfatin is expressed in Leydig cells, spermatocytes and spermatozoa [19], and its level in the seminal fluid is much higher than in the blood [162]. When exposed to Leydig cells, visfatin increases the T production, and the maximal effect of visfatin is achieved at its concentration of 10−6 M [163]. The inhibitor of Raf-1 kinase reduces the stimulating effect of visfatin on steroidogenesis, while the inhibitors of the protein kinases A and C have a little influence on this effect. It is assumed that the effects of visfatin on steroidogenesis may be due to activation of insulin receptors [163], which are widely represented in Leydig cells, especially since previously it has been reported that insulin receptor can interact with visfatin [154, 164]. However, despite the similarity of regulatory effects of insulin and visfatin, in the recent years the ability of visfatin specifically binds to insulin receptor has been questioned [157].
\nResistin is a polypeptide with a molecular mass of 12.5 kDa, which forms a homodimer stabilized by disulfide bonds [138]. Although resistin is mainly secreted by adipocytes of the white and brown adipose tissues and macrophages [165, 166], its expression is also shown in the testes in the Sertoli and Leydig cells, which indicates the participation of resistin in the autocrine and paracrine regulation of testicular cells [16]. The expression of the
The level of resistin in the bloodstream, from which it is able to be transported to the testes, varies greatly depending on the metabolic status, gender and species. Fasting leads to a decrease in the plasma resistin level and the
Using the primary culture of pituitary cells of rhesus monkey it was shown that resistin activates a number of signaling pathways, including cAMP-dependent and 3-phosphoinositide cascades regulating the cell survival and secretory activity. Resistin affects the secretion of growth hormone and adrenocorticotropic hormone, although LH secretion remains unchanged. It should be noted, however, that the treatment of pituitary cells with leptin and adiponectin also did not affect LH secretion, which is probably due to the peculiarities of cultured cells used in the experiment [174].
\nResistin was found in the brain and CSF, and although its concentration was much lower than in the bloodstream, it can be assumed that resistin affects the activity of hypothalamic neurons controlling GnRH secretion [116, 133]. One of the mechanisms of this may be the influence of resistin on the adiponectin signaling in hypothalamic neurons. A prolonged i.c.v. administration of resistin into rats and mice results in a decrease in the expression of both types of adiponectin receptors, AdipoR1 and AdipoR2, and also reduces the functional activity of APPL-1 protein, thereby weakening the APPL-1-mediated adiponectin signaling. There is reason to believe that this effect of resistin is implemented through the receptor TLR4, since the inhibiting effect of resistin on the adiponectin signaling was not detected in mice lacking TLR4 [175].
\nThe
The regulation of the male gonadal axis by adipokines can be carried out both through the changes in the plasma level and bioavailability of adipokines produced (a systemic regulation) and through the changes in the expression and specific activity of adipokines in the target tissues, the components of the HPG axis, such as the hypothalamus, pituitary and testes (an autonomous regulation). In the case of systemic adipokines regulation, the changes in the plasma level of adipokines that are associated with feeding behavior, physiological conditions, and also with an imbalance of adipokines and a resistance to them in obesity, DM2 and other metabolic disorders directly affect the functional activity of the male HPG axis and T production. Of great importance is the activity of the adipokine-transporting system, which transfers the adipokines through the BBB into the brain, where they regulate the GnRH- and KNDy-neurons involved in GnRH secretion, and also through the BTB into the testes, where they control the steroidogenesis system and the synthesis of T, the main effector hormone of the male HPG axis. In the case of autonomous regulation, the adipokines synthesized in the pituitary and testes function as the autocrine and paracrine factors and to a large extent determine functional activity of the components of the HPG axis. On the one hand, they regulate proliferation and survival of gonadotrophs and testicular cells, primarily Leydig cells, and on the other, affect their ability to produce gonadotropins and steroid hormones. It is important to note that between the systemic and autonomous adipokine-mediated regulation of the male HPG axis there are the complex integrative relationships and interactions that are realized at different levels of this axis. As a consequence, the changes in the pattern and levels of adipokines in the bloodstream can be differently associated with activity of the hypothalamic, pituitary and testicular components of the HPG axis, since in this case it is necessary to take into account the functional state of autonomous adipokine systems. The ratio of different adipokines in the blood and in the tissues, the components of the HPG axis, contributes significantly to the resulting effects of adipokines on the reproductive system, since their effects on the male HPG axis, including the testicular steroidogenesis system, may be synergistic or antagonistic.
\nThe study of the role of adipokines in the regulation of the male HPG axis is of great interest, since it will allow in the future to develop the effective approaches for monitoring functional activity of the male reproductive system and correcting the dysfunctions in this system in metabolic and endocrine disorders, including obesity and DM2. The adipokines and their analogues, as well as regulators and modulators of their signaling cascades in the hypothalamic neurons and testes, can be used as potential drugs to improve the reproductive functions and to normalize the steroidogenesis in men. It is also important how the treatment of men with GnRH analogous, gonadotropins with LH-like activity and androgens will affect the systemic and autonomic regulation of the GPH axis by adipokines. This should be taken into account when developing the approaches to improve metabolic status in obese and diabetic patients and in elderly men with an androgen deficiency using the activators of the HPG axis and androgens. The study of the interaction between the male HPG axis and the adipokine system will allow us to decipher the fundamental mechanisms that determine the relationships between the eating behavior, hunger and satiety, on the one hand, and the sexual behavior and aggression, on the other.
\nThis work was supported by the Russian Foundation of Basic Investigations (project No 18-515-45004 IND-a).
\nConflicts of interest are absent.
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',metaTitle:"Horizon 2020 Compliance",metaDescription:"General requirements for Open Access to Horizon 2020 research project outputs are found within Guidelines on Open Access to Scientific Publication and Research Data in Horizon 2020. The guidelines, in their simplest form, state that if you are a Horizon 2020 recipient, you must ensure open access to your scientific publications by enabling them to be downloaded, printed and read online. Additionally, said publications must be peer reviewed. ",metaKeywords:null,canonicalURL:null,contentRaw:'[{"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.
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I am also a member of the team in charge for the supervision of Ph.D. students in the fields of development of silicon based planar waveguide sensor devices, study of inelastic electron tunnelling in planar tunnelling nanostructures for sensing applications and development of organotellurium(IV) compounds for semiconductor applications. I am a specialist in data analysis techniques and nanosurface structure. 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After obtaining a Master's degree in Mechanical Engineering, he continued his PhD studies in Robotics at the Vienna University of Technology. Here he worked as a robotic researcher with the university's Intelligent Manufacturing Systems Group as well as a guest researcher at various European universities, including the Swiss Federal Institute of Technology Lausanne (EPFL). During this time he published more than 20 scientific papers, gave presentations, served as a reviewer for major robotic journals and conferences and most importantly he co-founded and built the International Journal of Advanced Robotic Systems- world's first Open Access journal in the field of robotics. Starting this journal was a pivotal point in his career, since it was a pathway to founding IntechOpen - Open Access publisher focused on addressing academic researchers needs. Alex is a personification of IntechOpen key values being trusted, open and entrepreneurial. Today his focus is on defining the growth and development strategy for the company.",institutionString:null,institution:{name:"TU Wien",country:{name:"Austria"}}},{id:"19816",title:"Prof.",name:"Alexander",middleName:null,surname:"Kokorin",slug:"alexander-kokorin",fullName:"Alexander Kokorin",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/19816/images/1607_n.jpg",biography:"Alexander I. Kokorin: born: 1947, Moscow; DSc., PhD; Principal Research Fellow (Research Professor) of Department of Kinetics and Catalysis, N. Semenov Institute of Chemical Physics, Russian Academy of Sciences, Moscow.\r\nArea of research interests: physical chemistry of complex-organized molecular and nanosized systems, including polymer-metal complexes; the surface of doped oxide semiconductors. He is an expert in structural, absorptive, catalytic and photocatalytic properties, in structural organization and dynamic features of ionic liquids, in magnetic interactions between paramagnetic centers. The author or co-author of 3 books, over 200 articles and reviews in scientific journals and books. He is an actual member of the International EPR/ESR Society, European Society on Quantum Solar Energy Conversion, Moscow House of Scientists, of the Board of Moscow Physical Society.",institutionString:null,institution:{name:"Semenov Institute of Chemical Physics",country:{name:"Russia"}}},{id:"62389",title:"PhD.",name:"Ali Demir",middleName:null,surname:"Sezer",slug:"ali-demir-sezer",fullName:"Ali Demir Sezer",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/62389/images/3413_n.jpg",biography:"Dr. Ali Demir Sezer has a Ph.D. from Pharmaceutical Biotechnology at the Faculty of Pharmacy, University of Marmara (Turkey). 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Focus of his research activity is drug delivery, physico-chemical characterization and biological evaluation of biopolymers micro and nanoparticles as modified drug delivery system, and colloidal drug carriers (liposomes, nanoparticles etc.).",institutionString:null,institution:{name:"Marmara University",country:{name:"Turkey"}}},{id:"61051",title:"Prof.",name:"Andrea",middleName:null,surname:"Natale",slug:"andrea-natale",fullName:"Andrea Natale",position:null,profilePictureURL:"//cdnintech.com/web/frontend/www/assets/author.svg",biography:null,institutionString:null,institution:null},{id:"100762",title:"Prof.",name:"Andrea",middleName:null,surname:"Natale",slug:"andrea-natale",fullName:"Andrea Natale",position:null,profilePictureURL:"//cdnintech.com/web/frontend/www/assets/author.svg",biography:null,institutionString:null,institution:{name:"St David's Medical Center",country:{name:"United States of America"}}},{id:"107416",title:"Dr.",name:"Andrea",middleName:null,surname:"Natale",slug:"andrea-natale",fullName:"Andrea Natale",position:null,profilePictureURL:"//cdnintech.com/web/frontend/www/assets/author.svg",biography:null,institutionString:null,institution:{name:"Texas Cardiac Arrhythmia",country:{name:"United States of America"}}},{id:"64434",title:"Dr.",name:"Angkoon",middleName:null,surname:"Phinyomark",slug:"angkoon-phinyomark",fullName:"Angkoon Phinyomark",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/64434/images/2619_n.jpg",biography:"My name is Angkoon Phinyomark. I received a B.Eng. degree in Computer Engineering with First Class Honors in 2008 from Prince of Songkla University, Songkhla, Thailand, where I received a Ph.D. degree in Electrical Engineering. My research interests are primarily in the area of biomedical signal processing and classification notably EMG (electromyography signal), EOG (electrooculography signal), and EEG (electroencephalography signal), image analysis notably breast cancer analysis and optical coherence tomography, and rehabilitation engineering. I became a student member of IEEE in 2008. During October 2011-March 2012, I had worked at School of Computer Science and Electronic Engineering, University of Essex, Colchester, Essex, United Kingdom. In addition, during a B.Eng. I had been a visiting research student at Faculty of Computer Science, University of Murcia, Murcia, Spain for three months.\n\nI have published over 40 papers during 5 years in refereed journals, books, and conference proceedings in the areas of electro-physiological signals processing and classification, notably EMG and EOG signals, fractal analysis, wavelet analysis, texture analysis, feature extraction and machine learning algorithms, and assistive and rehabilitative devices. I have several computer programming language certificates, i.e. Sun Certified Programmer for the Java 2 Platform 1.4 (SCJP), Microsoft Certified Professional Developer, Web Developer (MCPD), Microsoft Certified Technology Specialist, .NET Framework 2.0 Web (MCTS). 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