Senescence markers.
\\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
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The imbalance of oxidative stress within the endothelium promotes the activation of cellular senescence processes, altering the biological functions of endothelial cells [1] and favoring CVD development. Indeed, chronologic aging or premature senescence (caused by pathologic environment) is significantly associated with CVD development [2].
\nCellular senescence is an irreversible biological phenomenon triggered by potentially harmful stimuli which can damage the cell genome. During this process, the cell interrupts the division process, entering a state of cell cycle arrest and becoming quiescent. Senescence is a protective mechanism which affects the major part of the cells within the organism, including the vascular cells [3, 4]. It is considered indispensable to prevent tumor development, although turns to be pathologic when senescent cells extensively accumulate in tissues as a consequence of aging.
\nCell senescence can be triggered prematurely due to aging-associated pathologies such as CVD or chronic kidney disease (CKD). In fact, several studies confirm that CKD patients manifest premature aging in several tissues, including those in the cardiovascular system [5]. This is partly explained because CKD patients show “classic” cardiovascular risk factors (age, lifestyle, left ventricular hypertrophy, dyslipidemia, hypertension and diabetes mellitus). Kidney failure leads to the accumulation of circulating uremic toxins in the blood of those patients, causing stress and damage to the endothelium and activating endothelial cells senescence. Furthermore, CKD patients often show subclinical chronic inflammation associated with an immunosenescence process, which seems to be induced by the uremic toxins and other factors [6]. The renal replacement therapies may have a significant role in this process, as they induce the activation of immunocompetent cells [7].
\nTaken together, these concepts show that blood circulating toxins cause endothelial cells to become senescent leading to the appearance of several CVD. For example, some studies have proved that, at least in atherosclerotic processes, the pathogenic basis by which the CVD is developed is endothelial senescence [8, 9]. When endothelial cells become senescent, their imbalanced functionality may lead to the loss of the vascular structure. Moreover, the senescent endothelium cannot regulate correctly the repairing and regenerative activity of endothelial progenitor cells (EPCs), which increases the harmful effect in the vascular bed [10]. It is easy to understand in this context that endothelial senescence acts as the first element in the development of CVD.
\nRecently, microvesicles (MVs) have been proposed as endothelial response elements that can take part both in damaging and repairing processes in the endothelium [10, 11, 12]. There is certain knowledge, yet scarce, about the mechanisms underlying the participation of MVs in endothelial homeostasis, although the implication of those MVs in endothelial senescence remains an unresolved question.
\nTherefore, to understand and characterize the mechanisms by which the senescent endothelial cells show an imbalanced functionality, it is necessary to identify early biomarkers and to design therapeutic targets for CVD.
\nEndothelial dysfunction is an earlier pathophysiologic stage in CVD development. Ross in 1976 published his theory of response to damage, where he hypothesized that the initial event in atherogenesis is the endothelial injury, followed by the proliferation of smooth muscle cells [13]. Over the past years, this theory has been consolidated as endothelial damage is shown to be decisive in the promotion of vascular diseases. Indeed, diverse pharmacologic and dietetic interventions are intended to prevent the imbalance of the endothelial function, trying to interfere with the development of atherosclerosis and its clinical consequences [14, 15].
\nThe endothelium is a thin monocellular layer that covers the inner surface of blood vessels, separating the circulating blood from the interstitial fluid [16]. The endothelium is not an inert organ, as it can respond to physical or chemical stimuli by liberating the adequate regulatory substance to keep the correct vasomotor equilibrium and homeostasis [17]. The endothelium acts as an autocrine, paracrine and endocrine gland. Endothelial cells produce vasodilating, antiproliferative, antithrombotic and antiadherent mediators, like nitric oxide (NO), prostacyclin, the endothelium-derived hyperpolarizing factor (EDHF) and the natriuretic peptide, type C (CNP). The actions of those molecules are compensated by the release of substances with the opposing effect, as endothelin 1, thromboxane A2, prostaglandin H2 and the superoxide anion. Thus, endothelium regulates the tone of the smooth muscle cells of the vessel wall, causing its relaxation or contraction and conditioning the vasodilation or vasoconstriction processes. Also, it regulates hemostasis by controlling the production of prothrombotic or antithrombotic molecules, as well as fibrinolytic and antifibrinolytic substances. Endothelium takes part in inflammatory and immune processes by regulating proliferation and cell migration, as well as adherence and leukocytes activation. It is capable of producing cytokines and adhesion molecules that regulate the inflammatory process, contributing to the defensive function of the organism by the activation of neutrophils and macrophages [18].
\nCardiovascular risk factors provoke an oxidative stress which alter the function of the endothelial cells and provoke endothelial dysfunction by reducing the ability of the endothelium to maintain the homeostasis and concluding with the development of vascular diseases [19]. The term “endothelial dysfunction” has been used to define diverse syndromes which include a change of the endothelial phenotype from a “basal” to an active state. It is a complex disorder which includes alterations in the vasomotor and antithrombotic responses, in the vascular permeability, the leukocytes recruitment and the proliferation of endothelial cells [20, 21]. In the progress of endothelial dysfunction, the presence of pathologic conditions can contribute accelerating CVD development [22, 23].
\nAmong the cardiovascular risk factors, the age arises as a critical factor. It is associated with damage and endothelial dysfunction, as well with atherosclerosis development which will lead to vascular pathologies [24]. Epidemiologic studies have demonstrated that aging is the most important risk factor for the development of CVD, mainly atherosclerotic [23]. During the gradual aging, the incidence and prevalence of atherothrombotic and coronary diseases and cerebrovascular accidents increases. For that reason, there must be a causal relationship between the age-associated changes and vascular damage. It has been demonstrated that, during aging, the vasculature of healthy subjects suffers several changes, as endothelial dysfunction [21], the arterial wall thickening and remodeling [25], angiogenesis alterations, incorrect vascular repair [26] and increased atherosclerosis prevalence [27]. The relationship between the development of these disorders and the aging process remain poorly understood, but it is possible that throughout the physiologic aging of the organisms some similar changes occur, comparable to those in the vascular diseases and sharing common cellular mechanisms.
\nOne of the mechanisms that have been postulated as a possible pathophysiological participant is the cellular senescence of the endothelium. Cellular senescence is an irreversible process typical for all cells in which cells leave the cycle division as a consequence of the cellular damage associated with diseases [28] and aging [29]. Cell senescence processes appear to be involved in physiological processes of control such as cancer protection, biological developmental processes, tissue repair in aging situations and age-related disorders. Although their involvement in the aging process was postulated by Shay and Wright (Hayflick limit) [30], the absence of specific markers of senescence has hampered efforts to characterize senescent cells that accumulate
Mechanisms by which endothelial cells become senescent and their characteristics. GF, growth factors; MMPs, matrix metalloproteinases; SASP, senescence-associated secretory phenotype; EMVs, endothelial microvesicles; ROS, reactive oxidative species.
Characteristics | \nMarkers | \nRegulation | \nTechniques | \nReferences | \n
---|---|---|---|---|
DNA replication (senescent cells decline in DNA replication) | \nBrdU | \n↓ | \nFluorescence microscope | \n[31] | \n
3H-dT | \n↓ | \nIncorporation of radioactivity | \n||
PCNA | \n↓ | \nImmunostaining/Western blot | \n||
Ki-67 | \n↓ | \nImmunostaining/Western blot | \n||
SA-β-gal activity (the SA-β-gal derives from the lysosomal β-galactosidase and reflects the increased lysosomal biogenesis) | \nX-gal substrate | \n↑ | \nLight microscopy (production of blue precipitate) | \n[41, 42] | \n
C12FDG (fluorogenic substrate) | \n↑ | \nFluorescence microscopy (production of green fluorogenic color) | \n||
Cell cycle arrest proteins (early markers of DNA damage-induced senescence) | \np16 | \n↑ | \nWestern blot/immunostaining | \n[43, 44, 45] | \n
p21 | \n[29, 46] | \n|||
p53 | \n||||
Cyclin D1 | \n[38] | \n|||
Lamin B1 | \n↓ | \n[39] | \n||
SAHFs (reorganization of chromatin into discrete foci) | \nDNA dyes: DAPI | \n↑ Presence of certain heterochromatin-associated histone modifications | \nFluorescence microscopy | \n[31, 47] | \n
SDF (different DNA repair proteins) | \nγ-H2AX: marker of DNA double strand breaks and genomic instability | \n↑ | \nFluorescence microscopy/Western blot | \n[31] | \n
53BP1: protein associated with DNA damage | \n↑ | \nFluorescence microscopy | \n
Senescence markers.
BrdU, 5-bromodeoxyuridine; 3H-dT, 3Hthymidine; PCNA, Proliferating cell nuclear antigen; SA-β-gal, Senescence-associated β-galactosidase; X-gal substrate, 5-bromo-4-chloro-3-indolyl-D-galactoside; C12FDG, 5-dodecanoylaminofluorescein di-β-D-galactopyranoside; SAHFs, senescence-associated heterochromatin foci; DAPI, 4′,6-diamidino-2-phenylindole; SDF, senescence-associated DNA damage foci; γ-H2AX; phosphorylated histone H2AX; 53BP1, p53-binding protein-1.
The use of all these elements to define senescent cells has provided convincing evidence that these senescent cells accumulate in tissues of humans, primates and rodents with advanced age, as well as in sites of tissue injury and remodeling. The most prominent feature of the senescent cells is a cell cycle arrest, which permanently withholds replication and the resistance to apoptosis. An important fact to note is that the cells with senescent characteristics are found in damaged tissues of patients with chronic diseases such as osteoarthritis, pulmonary fibrosis, atherosclerosis, Alzheimer’s disease or CKD [40].
\nCKD is known to promote cellular senescence and an accelerated aging. It is caused by the accumulation of toxins in the internal medium, and the consequence is the development of elderly associated pathologies, mainly CVD [48]. CKD-associated CVD show similar characteristics to the natural CVD in elderly, and for this reason, several authors propose that the biggest challenge in the treatment of CVD may be to understand why CKD promote the premature aging of the cardiovascular system [49].
\nEven though the progress in the last few years in the renal replacement therapy is substantial, the mortality of terminal CKD patients remains excessively high, with an incidence between 10 and 20-fold over the general population [50].
\nUremic patients have higher rates of cardiovascular morbidity and mortality than would be predicted by Framingham risk factors [50, 51, 52]. However, the presence of those factors is not enough to explain the significant increment of the cardiovascular risk in those patients. CKD patients show additional factors associated with uremia that could explain this increased CVD risk [53]. The presence of microalbumin and uremic toxins in blood, hyperhomocysteinemia, anemia, the abnormal calcium/phosphate metabolism, parathyroid hormone (PTH) level alterations, the treatment with vitamin D derived substances, the volume overload, the electrolytic imbalance, oxidative stress, inflammation, malnutrition, thrombogenic factors and the imbalance of NO/endothelin are risk factors intrinsically associated to CKD [54]. The valuation and modulation of those factors are of high importance in CKD patients, as some are variable and the correct treatment may prevent the progression of the pathology.
\nIn CKD patients, the endothelium is exposed to an additional stress because of the presence of factors related to the uremic state. This state can be modified depending on the conservative treatment or renal transplantation, but it has been demonstrated that it relies on a persistent microinflammatory state directly related to endothelial damage, partaking in atherosclerosis processes [7, 55, 56]. Under this hostile uremic-associated state, the endothelium loses its integrity. Some damage substances and molecules will be released as a reflection of the harmful stimuli [56, 57].
\nAmong several inflammatory factors, the subpopulation of monocytes habitually augmented in elderly, increases in the peripheral blood. The contribution of monocytes in inflammation and the CVD development has been widely studied by several groups, including ours [58]. Peripheral blood monocytes show a significant heterogeneity, reflected by the differential expression of the lipopolysaccharide binding receptor (CD14) at their surface and the low-affinity receptor Fc, FcγRIII (CD16). In the last years, monocytes have been divided into three populations or subsets based on the intensity of CD14 and CD16 expression (cell surface marker phenotype) being functionally differentiated in: classical monocytes (CD14++/CD16−), present mainly in healthy patients; intermediate monocytes (CD14++/CD16+) and non-classical monocytes (CD14+/CD16++). A possible causal role in the development of atherosclerosis in general population and CKD patients has been attributed to intermediate monocytes (CD14++/CD16+) [59]. CD14+/CD16++ monocytes are inflammatory senescent cells characterized by their increased capacity to produce proinflammatory cytokines and because of their strong function as dendritic cells [60]. CD14+/CD16++ can be differentiated
In addition to the activity of the immune cells in endothelial damage, some other factors could be involved, as some specific molecules are known to be increased in the peripheral blood of CKD. In different models, it has been shown that endothelial cells activated pathologically with uremic serum or uremic toxins enter into a premature senescent state. Also, they reduce their proliferative capability and show shortened telomeres, augmenting the expression of β-gal [69]. Another possible factor in the development of the CKD-associated CVD is the incorrect repair of the damaged endothelium by EPCs. This failure occurs mainly due to two factors: a decreased number of EPCs or their imbalanced function. In our studies, we demonstrated that in CKD patients there is a decrease in the number of EPCs and that this number is considerably lower in severe patients with, for example, vascular calcifications [10, 70]. Also, it has been demonstrated that EPCs lose their angiogenic capability, generally needed in the process of regeneration of harmed vascular structures (vasculogenesis). In this regard, the association between some diseases such as CKD-associated CVD and both number and function of EPCs, accelerate the processes of EPCs senescence and therefore damage in endothelial cells harboring.
\nThe endothelial MVs (EMVs) are extracellular vesicles produced by endothelial cells whose essential role is to act as a signaling system between the elements involved in the function and homeostasis of the vessel [71].
\nIn general, the extracellular vesicles can be found in many body fluids, including plasma and urine. They have a variable size, between 0.05 and 5 μm [71], and are involved in physiological and pathophysiological processes, participating as mediators in intercellular communication. They can act directly on the target cells by binding to ligands, cell surface receptors and/or membrane-associated enzymes, delivering or releasing their contents directly into the cytoplasm. Extracellular vesicles are elevated in patients with neurodegenerative, metabolic, pulmonary, autoimmune and vascular diseases, chronic inflammation and cancer [72]. The use of extracellular vesicles as markers for the prediction, diagnosis and prognosis of the disease is increasingly interesting, as well as their potential as new therapeutic targets [73]. There are several types of extracellular vesicles: exosomes, the MVs or microparticles and the apoptotic bodies, which are produced by different mechanisms [65]. The MVs are a heterogeneous population of up 2 μm diameter, which are formed from the cell membrane in a regulated active process, dependent on enzyme activity and calcium.
\nRecently, it has been demonstrated that MVs may play an essential role in cellular senescence processes [74] since they have been proposed as elements of an endothelial response that can participate in the damaging and repair processes of the endothelium [10, 11, 12]. MVs generated from different cell types can induce endothelial dysfunction because they are responsible for increasing oxidative stress, reducing the bioavailability of NO and producing cardiovascular inflammation. The knowledge about their formation and release represent an attractive therapeutic goal to limit MVs levels, but the mechanisms underlying the release are not fully elucidated. On the other hand, a direct or indirect inhibition of the effect of MVs is a more effective proposal [75]. The effect of certain drugs that are used to decrease cardiovascular risk have been shown to affect the MVs plasma levels, suggesting that the beneficial effects of these drugs could, at least in part, be mediated through a reduction of the concentration of MVs [76]. Moreover, different authors have highlighted the importance of diet on MVs release, being perhaps one of the mechanisms involved in the role of diet in the development of CVD [14, 77].The process of identification and separation of extracellular vesicles is complicated due to their extensive variability. In fact, currently, the absolute separation of exosomes, apoptotic bodies and MVs is not possible because their size ranges may overlap. The most common method for the separation and isolation of extracellular vesicles is the serial centrifugation. In the majority of the studies, a first centrifugation is performed at 200–1500 × g to remove cells and cell debris. Extracellular vesicles more than 100 nm are pelleted at 10,000–20,000 × g and small vesicles of 100 nm at 100,000–200,000 × g [78]. Following these protocols, we can obtain EMVs from supernatants of mature endothelial cells cultures, cellular debris and exosomes-free. The EMVs might also be obtained from plasma by similar processes, but would be found mixed with other MVs derived from other circulating cells.
\nThe most common methods to study single MVs are flow cytometry (FC), tunable resistive pulse sensing (TRPS), dynamic light scattering (DLS) and nanoparticle tracking analysis (NTA) [79]. To date, FC is the method most used to establish the cellular origin and the phenotype of the MVs and is based on the detection of light scatter and fluorescence intensity of the labeled MVs [80, 81, 82]. To characterize their cellular origin, different antigens expressed on the membrane of the MVs are identified. For this purpose, monoclonal antibodies (mAb) labeled with different fluorochromes that define the phenotype are used. To identify EMVs, specific fluorescent antibodies against endothelial cell can be used to characterize the phenotype. Some markers used to describe EMVs are CD144, CD105 and CD146. Moreover, the phospholipids are a class of lipids that are a major component of all biological membranes and in MVs are externalized. For this reason, these phospholipids present in the MVs membrane have also been used for EMVs detection and characterization [83]. The combination of several mAb simultaneously can facilitate the identification of the origin and the state of activation or apoptosis of the cell from which the MVs originate [84]. The EMVs determination protocol includes some preliminary steps designed to identify sizes, with beads that allow adjustments to the equipment, before the introduction of the samples. However, this method has limitations in identifying the smallest MVs that are below the detection limit of conventional FC equipment (diameter size lower 300 nm) [79]. Recent studies have shown that FC equipment with high sensitivity can amplify the forward scatter parameter capacity, which is used to identify the size of the MVs [85]. On the other hand, it is very helpful to provide information regarding functional activity of the extracellular vesicles [86, 87, 88, 89].
\nIn this regard, novel instruments including NTA or DLS have shown their advantages in the analysis of extracellular vesicles. NTA measures the distribution of the absolute size of the vesicles that range from 50 nm to 1 μm [90]. The vesicles in suspension are illuminated by a laser that produces light scattering or fluorescence. A microscope determines the position of individual vesicles, which are continuously moving due to Brownian motion [91]. When a fluorescent marker is used, NTA can also be used to determine the size of a subgroup of vesicles [92]. The principal advantage of this method is the detection of particles below 100 nm in diameter. In contrast, the limitation of this technique, the low resolution, therefore, NTA is incapable of distinguishing MVs from particles in suspension (debris) with the same size [79]. DLS, also known as photon correlation spectroscopy, measures the size distribution of vesicles between 1 nm and 6 μm. However, the absolute concentration of the vesicles cannot be determined by DLS because the average amplitude of the signal depends on the diameter, concentration and the refractive index of the vesicles [93, 94, 95].
\nThe last method TRPS consists in the movement of the MVs through tunable nanopores which are capable of registering MVs between 80 and 1000 nm [96]. Particles passing the pore generate a change in the electric resistance, thus providing information on diameter, surface charge and concentration of single particles. The major disadvantage of TRPS is that it cannot distinguish between MVs and similarly sized particles [79]. Independently of the method used to study of the MVs, it has been recommended to confirm the presence of MVs by measuring them at least with two different techniques.
\nIn addition, enzyme-linked immunosorbent assay (ELISA), Western blot or quantitative real-time PCR (qPCR) are useful tools for the detection of proteins or RNA in preparations of purified MVs. Electron microscopy can provide information concerning the vesicular morphology, size and the presence of markers. Moreover, proteomic analysis and profiles of RNA/microRNA (miRNA) may help to determine the composition of the MVs.
\nIn the absence of pathology, the EMVs are involved in the maintenance of vascular homeostasis, participating in the metabolism of the vascular environment [97]. The EMVs can act on the vascular wall, at the endothelial level, and on smooth muscle cells [98], regulating both vasomotor reactivity and angiogenesis. In fact, the formation of EMVs and their elimination seems to reflect a balance between activation and cell damage, cell survival/apoptosis and angiogenesis. Endothelial responses may be immediate; releasing various factors or can be delayed, modulating the expression of genes involved in regulating the structure and function of the vascular system (Figure 2). In
Mechanisms of endothelial microvesicles (MVs) action upon target cells. SMCs, smooth muscle cells; ECs, endothelial cells.
MVs concentration in blood from healthy subjects is clinically irrelevant. However, in patients with cardiovascular risk factors and after cardiovascular events, EMVs concentrations are increased significantly [10, 102]. In fact, in patients with CVD, an association between the number of circulating EMVs and the Framingham risk score has been shown [72]. In particular, high levels of EMVs in diseases associated with vascular injury seem to reflect an inflammatory and prothrombotic process. EMVs may participate in the development and amplification of CVD through both cardiac and vascular cells. On the other hand, numerous studies have emphasized the effect of cardioprotective drugs on reducing concentrations of extracellular vesicles [73] which reinforces the evidence about the possible correlation of EMVs and vascular injury.
\nEMVs, and in general all extracellular vesicles, carry a specific load that is capable of delivering to other cells, even in remote locations. Extracellular vesicles share characteristics with their parental cells such as cell surface receptors, integral membrane proteins, cytosolic molecules, organelles, mRNAs, miRNAs or small amounts of DNA and proteins, including transcription factors, cytokines and growth factors [103]. Cell receptors and transmembrane proteins can help in the identification of EMVs, and also are indicative of the ability of vesicles to interact directly with receptors on the surface of target cells, resulting in an intracellular signal transmission. In addition to its effect on specific receptors, it has been shown that EMVs may be fused to the target cell and transfer its contents directly inside as a vehicle for transfer of genetic information [11, 67, 104, 105]. Extracellular vesicles are considered as the main source of miRNAs, released into the bloodstream during cell activation or apoptosis [106]. In fact, most miRNAs are associated with extracellular vesicles and only small amounts of them can be found free in plasma. It is thought that extracellular vesicles are necessary to protect circulating miRNAs from degradation by RNases, transferring safely functional miRNAs from the parental cells receptor cells. miRNAs act as regulatory molecules in endothelial cells, vascular smooth muscle cells, platelets and inflammatory cells that contribute to modulate the initiation and progression of atherosclerosis. It is known that the release of miRNAs does not occur randomly but they are produced and released by controlled mechanisms [107, 108]. It has been described that there are several miRNAs involved in the regulation of vascular function and repair. It is expected that in the future, a better understanding of these molecules provides new options both diagnostic and therapeutic in the vascular pathology.
\nThe MVs from different sources such as endothelial cells, monocytes and lymphocytes can promote oxidative stress in the endothelium through processes that may involve several enzymatic systems [109]. The MVs can regulate the production of reactive oxygen species (ROS), although there are some discrepancies regarding ROS generation systems affected. These contradictory results may be due to the fact that MVs populations studied are from different sources or produced by different stimuli [105, 110]. From the biological point of view, these differences in the production of MVs have a significant for the potential to define MVs populations with different biological activities.
\nOne of the best-provided properties of MVs is its ability to promote coagulation [98]. In fact, the MVs are elevated in hypercoagulative disorders probably as a result of their active participation [98]. It is not clear how far MVs contribute to the
Chronic inflammation is a crucial factor in the development of atherosclerosis, and the effects of EMVs in inflammatory processes have been the subject of numerous studies since they may represent both a cause and a consequence of inflammation [12]. The MVs isolated from human atherosclerotic plaques can transfer intercellular adhesion molecule-1 (ICAM-1) to endothelial cells and could increase the ability to recruit inflammatory cells in a manner dependent of phosphatidylserine, which may increase the progression of the atherosclerotic plaque. The most conclusive evidence of a proinflammatory role for EMVs is that the administration of exogenous EMVs to rats is associated with acute lung injury, with increased levels of proinflammatory cytokines (IL-1β and TNF-α) and neutrophil infiltration on histological lesion perivascular space [111].
\nDifferent studies have described a role of MVs in the regulation of angiogenesis [112]. Platelet-derived MVs were first involved in the angiogenesis process since platelets contain at least 20 factors that regulate angiogenesis. Platelet-derived MVs stimulate proliferation, survival, migration, and formation of capillary-like structures in endothelial cells
In addition to being a potent stimulus for the formation of MVs, apoptosis can also be a consequence of MVs signaling [112]. Monocyte, erythrocytes, platelets and endothelial cells-derived MVs contain caspase-3. It is thought that the content of caspases may be a mechanism directed to control the apoptosis, suggesting that MVs could release caspase-3 into the target cells, participating in the induction of apoptosis. In addition, caspase-3 is implicated in numerous cellular processes, so the release of this protein could have an even more significant impact on the target cell.
\nThe MVs contain proteolytic enzymes, and then some of its effects could be attributed to alterations in the extracellular matrix or proteolytic cleavage of various signaling molecules. For example, the microvasculature-derived EMVs containing MMP-1, MMP-2, MMP-13 and MMP-7, which degrade fibronectin
Initially, proliferation and migration of adjacent endothelial cells have been identified as a factor of endothelial repair, and subsequent studies have shown that the maintenance of the endothelial structure is associated with EPCs and their ability to differentiate and repair damaged endothelial tissue. Due to the importance of this repair mechanism in the maintenance of vascular homeostasis, it is logical to think about the existence of close communication between damaged endothelial cells and EPCs. Previous studies performed by our group suggest that plasma EMVs, both of healthy subjects and patients with CKD; participate in the activity of the EPCs [10]. Our hypothesis is that EMVs can be an essential and necessary physiological mechanism of signaling to initiate the recruitment of EPCs from bone marrow. In
Vascular calcification is an increasingly constant process in developed countries and can contribute significantly to increased cardiovascular risk. The processes and mechanisms involved in the formation of vascular calcifications are poorly understood and are needed to develop new therapeutic strategies to prevent or avoid calcification. Patients CKD have a higher incidence of vascular calcification, and our group has shown that EMVs are increased in patients with an elevated degree of calcification [10]. In
MVs have also been associated with endothelial senescence. As we said before, senescent cells release characteristic molecules and substances composing the SASP. However, some of those substances which are known to be part of this SASP cannot be released as soluble molecules due to their nature, as some transmembrane proteins [119]. It is known that the premature induction of cellular senescence
CVD seem to begin as a consequence of a damaging process and endothelial dysfunction, and there are pieces of evidence implying cellular senescence in the functional imbalance of the endothelium. Cellular senescence is a physiological mechanism which occurs as a consequence of aging, but under different pathologic conditions, its regulation is modified, as in CVD or CKD. Senescent endothelial cells change their morphological and functional characteristics (Figure 3) and cannot correctly regulate the repairing and regenerative activity of EPCs. In the endothelial senescence context, the role of EMVs appears to be important. EMVs are considered as biomarkers of endothelial injury and are associated with an inflammatory and prothrombotic state. However, the perspectives of their study are beyond their role as biomarkers, as they are capable of transmitting biologic information in several physiologic and physiopathologic processes. EMVs are increased in elderly, but also in patients with CVD and CKD. Many questions remain unresolved to understand the role of EMVs in the endothelial function and damage. To comprehend and characterize the mechanisms by which the senescent endothelial cells show an imbalanced functionality is of great interest, opening new perspectives to increase our knowledge and to identify useful biomarkers in the timely diagnostics and to design therapeutic objectives in CVD.
\nDifferent characteristics of young and senescent endothelial cells. Senescent cells undergo distinctive phenotypic, morphological alterations and senescence-associated secretory phenotype (SASP). The number of endothelial microvesicles (EMVs) of the senescent cells is greater than those derived from young cells. Also, the reactive oxygen species (ROS) production is higher in senescent endothelial cells compared with young endothelial cells. Moreover, the secretion of growth factors (GF) and proinflammatory cytokines (infl. cytokines) from senescent endothelial cells are reduced.
This work was supported by Plan Nacional Proyectos de Investigación en Salud of Instituto de Salud Carlos III (ISCIII) Fondos Feder European Grants (PI14/00806 and PI17/01029); Red de Investigación Renal (REDinREN; RD16/0009/0034) Junta de Andalucía Grants, P12-CTS-7352 and Santander Universidad Complutense de Madrid PR41/17-20964. Matilde Alique is a fellow of the program “Ayuda Postdoctoral Programa Propio” from Universidad de Alcalá, Madrid, Spain. Rafael Ramírez-Carracedo is a fellow of the program FPI (Formación de Personal Universitario) from Universidad Francisco de Vitoria, Madrid, Spain”.
\nHoney is a compound widely used as a medicine and food source for thousands of years [1]. Several natural products that have been used as medicine have been replaced by modern pharmaceuticals, but recently they have returned to the world stage due to the growing public interest [2]. In ancient Egypt, beekeeping has been practiced for more than 4000 years, and honey has been used as a medicine in the treatment of wounds, ulcers, burns, abscesses, gastrointestinal diseases, inflammations, rigid joints, and even as a contraceptive method [1, 3]. In Asia, honey is recognized for its medicinal value since 2000 BC [1]. There are also references to different uses of honey in the bible and in the Qur’an [1]. The ancient Greek Hippocrates, known as the father of modern medicine, used honey to clean wounds, gastrointestinal diseases, and ulcers [1, 3]. In Ancient Rome, honey was also prescribed alone or in combinations, often used to treat throat problems, pneumonia, and even snake bites [1].
\nThe main components of honey are sugars, among which are predominantly fructose and glucose [4, 5]. However, there are other compounds in smaller quantities and very variable depending on the type of each honey, from the floral source where the bee collects the nectar, such as water and free amino acids [4, 5]. Among them, the most found is proline [4, 6]. Some specific enzymes are also found, the main enzymes of honey are invertase, amylase, and glucose oxidase, but other enzymes such as catalase and phosphatase [6, 7, 8]. Honey is also composed of organic acids that contribute to its characteristic flavor and are responsible for the excellent stability of honey against micro-organisms, for example, formic, acetic, butyric, oxalic, lactic, succinic, folic, malic, citric, and glycolic [6, 7]. Gluconic acid is considered one of the most important organic acids in honey; it is the product of catalytic oxidation of glucose oxidase, in this oxidation, hydrogen peroxide is also formed, which has a strong antibacterial effect [4, 5, 6, 7].
\nHoney may still have some mineral substances, such as potassium, magnesium, sodium, calcium, phosphorus, iron, manganese, cobalt, and copper; studies show that honey can contain several types of minerals, but potassium is the most abundant in various types of honey [6, 8, 9, 10]. Carotenoids, flavones, and anthocyanins can still be found, which contribute to the antioxidant action of honey [6]. About 80 aromatic compounds have been detected in honey, including carboxylic acids, aldehydes, ketones, alcohols, hydrocarbons, and phenols [6]. These compounds also contribute to the organoleptic properties of honey. The appearance of honey varies from almost colorless to dark brown; it can be liquid, viscous, or solid. Its flavor, aroma, and composition vary enormously, depending on the floral source in which the honeybee collects the nectar. However, some environmental factors can strongly influence honey composition, such as temperature and humidity [6, 7, 11].
\nHoney is a food that contains high energy carbohydrates, being that 95–99% of the total solids are composed by sugars, which are easily digestible, since they are similar to many fruits [7, 12]. Proteins and enzymes in honey often have no significant nutritional value, as they are usually not present in sufficient amounts [7]. Several of the essential vitamins are present in honey, such as vitamin K, B1, B2, B6, and C, but generally at insignificant levels [7, 8, 13]. The mineral content of honey is variable, usually darker honeys have significant amounts of minerals, but honey can be considered a nutritive sweetener, mainly due to its high fructose content [7, 13].
\nIn addition to its food value, honey has great potential in medicine; it has been used for thousands of years, and has now been widely studied as an alternative medicine. Honey is not a suitable medium for bacteria, since it is very acidic and has a very high sugar content. This causes an osmotic effect that prevents the growth of bacteria, this effect works literally drying the bacteria [7, 13]. Another type of antibacterial property of honey was called inhibition in 1940 by Dold [7]. And in 1963, Jonathan White proposed that this inhibitory effect described in 1940 was due to the hydrogen peroxide produced and accumulated in the diluted honey, which we know today, is a by-product of the formation of gluconic acid by the enzyme glucose oxidase [5, 7, 11].
\nHistorically, honey has been used for various medical purposes; and recent research has confirmed the effectiveness in the treatment of several diseases due to its components and its properties antibacterial, anti-inflammatory, antioxidants, antiviral, and others that will be addressed in this chapter.
\nInflammation is nothing more than a defense response of the body to a tissue that has suffered a certain damage, which consists of the recruitment of leucocytes and plasma proteins of the blood [14, 15]. This damage can be caused by physical, chemical, or even microbial agents; inflammation is characterized by edema, erythema, pain, and increased temperature [15, 16].
\nIt is well known that propolis, another product from honeybee colony, has potential anti-inflammatory properties, including
Gastric ulcers are among the most common diseases affecting humans, a study demonstrated that the use of honey in conjunction with other compounds may promote gastroprotection. Later, a recent study investigated the effect of gastric protection using only honey against gastric ulcers induced by ethanol in rats and also suggested this effect as gastroprotection [21, 22]. Manuka honey significantly decreased the ulcer, completely protected the mucus of the lesions and preserved the gastric mucus glycoprotein, significantly increased the mucus levels of gastric nitric oxide, reduced glutathione, glutathione peroxidase, and superoxide dismutase, and also decreased lipid peroxidation of the mucus and tumor necrosis factor-α, interleukins-1β, and concentrations of interleukins-6 [21]. Honey has been shown to be efficient in other types of ulcers, and this Manuka honey exerted an antiulcer effect, keeping enzymes and antioxidants, non-enzymatic and inflammatory cytokines reduced [21, 23].
\nIn addition to the Manuka honey and the Tualang honey, the anti-inflammatory effect of Malaysia’s Gelam honey was also studied, which is associated with anti-inflammatory effects on tissues [24, 25]. Malaysia Gelam honey was tested in rats induced by inflammation [25]. Paw edema was induced by a subplantar injection and the rats were treated with either the anti-inflammatory drug Indomethacin or Gelam honey. Results showed that Gelam honey can reduce dose-dependent edema in inflamed rat paws, decrease the production of nitric oxide, prostaglandin, tumor necrosis factor-α, and interleukin-6 in plasma, and suppress expression of synthase inducible nitric oxide, cyclooxygenase-2, tumor necrosis factor-α, and interleucine-6 in paw tissue [25]. The oral pre-treatment of Gelam honey at 2 g/kg body weight at two times (1 and 7 days) showed a decreased production of proinflammatory cytokines, which was similar to the effect of the anti-inflammatory indomethacin, both in plasma and in the tissue, and Gelam honey has anti-inflammatory effects and is potentially useful for the treatment of inflammatory conditions [25]. Another study demonstrated that different types of honey promoted increased release of TNF-α, IL-1β, and IL-6 from monocytes, which are cells that assist in healing [26].
\nWe can also compare the anti-inflammatory activity of honey with another herbal remedy in a study carried out in 2012 to test the activity of honey and brown sugar, surgically treated guinea pigs that were treated with honey, brown sugar, and a control group treated with saline solution, it is already known that sugar can help healing [27, 28]. The honey group showed a decrease in the area of the wound and the formation of granulation tissue before the brown sugar group and control; the honey group was still the only one that presented no crust in any wound and promoted a faster healing by stimulating the faster formation of granulation tissue and re-epithelization [28]. In addition, honey showed a higher antibacterial effect in relation to brown sugar and control group [28]. Another study had the same result, honey was effective in reducing bacterial contamination and wound healing [29].
\nRecent studies proved the anti-inflammatory activity of honey; different types of honey, different regions and different floral sources, were studied and both showed anti-inflammatory responses [17, 21, 25, 28]. Treatment with Tualang honey and Gelam honey showed similar responses to conventional anti-inflammatories used for specific treatments [17, 25]. Honey still has a better anti-inflammatory activity than brown sugar, promoting faster healing [28]. Also, honey is a relatively cheap and easily accessible anti-inflammatory compound that needs to be further studied and later applied in modern medicine [17, 21, 25, 28].
\nOne of the advances of modern medicine has been the development of antibiotics; these antibiotics can be bactericidal, which kill the micro-organisms directly, or bacteriostatic, which prevent the growth of micro-organisms [30]. However, micro-organisms are increasingly developing resistance to these antibiotics, which is a major concern. In addition to antibiotics, the prevention of bacterial diseases can be carried out with the use of vaccines and with basic sanitary methods [30, 31].
\nMany different micro-organisms can cause disease and be transmitted even by contaminated water, and among the major aquatic pathogens are
The bacteria
Salmonellosis is a gastrointestinal disease caused by eating food contaminated with
Another form of food poisoning is caused by enterotoxins produced by Gram-positive bacteria, such as
\n
Honey has an excellent antibacterial effect against different types of bacteria, as previously mentioned; honey is very acidic and has a very high sugar content, which does not serve as a suitable medium for bacteria [4, 5, 6, 7]. Moreover, in some honeys, the peroxide of hydrogen is found, which has a strong antibacterial effect [4, 5, 6, 7]. Remavil® honeys, Manuka honey, Tualang honey, and Gelam honey were tested with different types of bacteria and had positive results [34, 36, 41, 42]. The bacteria tested and susceptible to some of these honeys were
Of all human infectious diseases, the most prevalent and difficult to treat are those that are caused by viruses, because viruses usually remain infectious in dry mucus for a long time [14]. Also, viruses need a host cells to occur its replication; so killing the virus means killing your host cell as well. Hence, vaccination is the most efficient way to prevent these diseases [14, 46].
\nChickenpox is caused by the varicella-zoster virus and it is a very common childhood disease that usually does not cause many problems; but when it affects the elderly, it can be easily fatal [14, 47]. Varicella-zoster is highly contagious and is transmitted by infectious droplets, which results in a systemic rash on the skin [14]. As honey can be conveniently applied to the skin, it is easily found and relatively inexpensive, it can be considered an excellent remedy against Zoster rash, especially in developing countries, or in countries where antiviral drugs are relatively expensive and difficult to access. Therefore, a study determined
Respiratory syncytial virus is the most common cause of viral respiratory infections in infants and young children, also seriously affects adults, the elderly and immunocompromised, causing deaths mainly in the elderly [50, 51]. The antiviral activity of honey was tested for its action against the respiratory syncytial virus. A variety of tests using cell culture was developed to assess the susceptibility of respiratory syncytial virus to honey. The results confirmed that treatment with honey promoted inhibition of viral replication [50]. Attempts to isolate the antiviral component in honey demonstrated that sugar was not responsible for the inhibition of respiratory syncytial virus, but could be methylglyoxal; this component of honey may play a role in the increased potency of Manuka honey against respiratory syncytial virus [50]. Thus, honey may be an alternative and effective antiviral treatment for the therapy of respiratory viral infections, such as respiratory syncytial virus; however, other measures, such as an effective vaccine, are still necessary for the control of this disease [50, 52].
\nInfluenza is a highly infectious respiratory disease of viral origin that causes even more deaths than the respiratory syncytial virus at all ages, except in children less than a year old [14, 51]. Influenza viruses are transmitted from person to person through the air, especially from droplets expelled during coughing and sneezing and are a serious threat to human health, and there is an urgent need for the development of new drugs against these viruses. Therefore, the anti-influenza virus activity of honey from several sources was studied [53]. The results showed that honey, in general, and particularly Manuka honey, has potent inhibitory activity against the influenza virus, demonstrating a potential medicinal value [53]. In addition to honey, propolis has also been studied against the influenza virus and appears to decrease the activity of the influenza virus [54].
\nHoney, especially Manuka honey, has strong antiviral properties. Studies show that honey has action against the varicella-zoster virus, the respiratory syncytial virus, and also has anti-influenza activity [47, 50, 53]. New studies on this property of honey are necessary, mainly with other types of honey.
\nMost people associate fungi with organic matter decomposition or superficial fungal infections, but fungi can cause various human diseases, from mild to firmly established systemic diseases; the most serious infections can even be fatal [14]. The incidence of
As previously stated, honey has antifungal properties and may act against
In addition to the antifungal activity of honey against
\n
Besides the antibacterial and antiviral properties, some honeys also have antifungal properties [56, 57, 59, 61]. Recent studies showed some honey have properties against
In 2016, the cancer mortality rate has dropped 23% since 1991 [65]. Despite this progress, mortality rates are increasing for liver, pancreatic, and uterine cancers; and cancer is now the leading cause of death in 21 states from United States, lung cancer is still the most lethal, followed by breast cancer [65, 66]. The advance for cancer treatment needs more clinical and basic research [65].
\nMany scientists have focused on the antioxidant property of honey. Studies indicate that ingestion of honeybee products, such as honey, can prevent cancer [67, 68]. Through the use of human renal cancer cells, the antiproliferative activities, apoptosis, and the antitumor activity of honey were investigated [67]. Honey decreased cell viability in malignant cells regardless of concentration and time [67]. Honey induced apoptosis of human renal cancer cells according to honey concentration, and apoptosis plays an important role, most of the drugs used in the treatment of cancer are apoptotic inducers, so the apoptotic nature of honey is considered vital [67].
\nThe anticancer activity of honey samples was extracted from three different Egyptian floral sources and was tested against colon, breast, and liver tumor lineage [69]. Cassia honey showed moderate cytotoxic activity against colon cancer and breast cancer, with the weakest cytotoxic activity against liver cancer; Citrus honey exhibited the highest cytotoxic activity against breast cancer; and Ziziphus honey showed potent efficiency against colon, liver, and breast cancer [69]. Breast cancer, which is the type of cancer that most affects and kills women, was also tested for another type of honey, the Manuka honey, and the results showed that it is cytotoxic to MCF-7 breast cancer cells
The phytochemical content and antioxidant activity of melon honey and Manuka honey and their cytotoxic properties were tested against human and metastatic colon adenocarcinoma. The ability to induce apoptosis in colon cancer cells depends on the concentration of honey and type of cell line, in addition to having a great relation with the phenolic content and residues of tryptophan. Honey was analyzed for phenolic, flavonoid, amino acid, and protein contents, as well as their free radical scavenging activities [71, 72]. Melon honey presented the highest amount of phenolics, flavonoids, amino acids, and proteins, as well as antioxidant capacity in relation to Manuka honey [71]. Both melon honey and Manuka honey induced cytotoxicity and cell death independently of dose and time in human and metastatic colon adenocarcinoma cells [71]. Melon honey showed to be more efficient in concentrations [71]. The results indicate that melon honey and Manuka honey can induce inhibition of cell growth and the generation of reactive oxygen species in colon adenocarcinoma and metastatic cells, which may be due to the presence of phytochemicals with antioxidant properties. These results suggest a potential chemo-preventive agent against colon cancer; in addition, honey can improve the functioning of other substances already used in cancer treatment [71, 73].
\nResearch on cancer control has shown the importance of adjuvant therapies [74].
Several types of honey have been studied because of their anticancer properties [65, 67, 69, 70, 71, 74]. Currently, cancer is one of the world’s leading diseases, requiring further studies [65]. Some honey have already been tested against colon, breast, and liver tumor, as well as human kidney cancer and Ehrlich ascites carcinoma cell lines, where most have weak to strong cytotoxic activity depending on the type of honey tested and depending on the dose of honey [67, 69, 70, 71]. The effect of
Antioxidants, which are present in large amounts of honey, making it a food with great antioxidative potential, are free radical scavengers that reduce the formation or neutralize free radicals [11, 78]. A comparative analysis of total phenolic content and antioxidant potential of commercially available common honey was performed along with Malaysia’s Tualang honey. Biochemical analyzes revealed a significantly high phenolic content in Tualang honey [78]. In addition, the antioxidant capacity of Tualang honey was higher than that of common honey; these data suggested that the high activity of elimination of free radicals and antioxidant activity observed in Tualang honey were due to the increase in the level of phenolic compounds, it was also observed that the antioxidant activity of honey depends on its botanical origin [78, 79]. Therefore, the favorable antioxidant properties of Tualang honey can be important for nutrition and human health [78].
\nType 2 diabetes consists of progressive hyperglycemia, insulin resistance, and β-pancreatic cell failure, which may result from glucose toxicity, inflammatory cytokines, and oxidative stress, and is responsible for 90–95% of all cases of diabetes [80, 81]. A study investigated the effect of pre-treatment with Gelam honey, and the individual flavonoid components chrysin, luteolin, and quercetin on the production of reactive oxygen species, cell viability, lipid peroxidation, and insulin in hamster pancreatic cells, cultured under normal conditions and hyperglycemic, the pre-treatment of cells with Gelam honey extract or flavonoid components showed a significant decrease in the production of reactive oxygen species, glucose-induced lipid peroxidation, and a significant increase in insulin content and viability of cultured cells under hyperglycemic conditions. The results indicated the
Honey contains antioxidants, such as phenolic compounds that prevent cellular oxidative damage that leads to aging, disease such as cancer, metabolic disturbances, cardiovascular dysfunction and even death [83, 84]. The antioxidant effect of honey in young and middle-aged rats was compared, the rats were fed with pure water (control), those supplemented with 2.5 and 5.0 g/kg of Gelam honey for 30 days. Results showed that Gelam honey supplementation reduced DNA damage, plasma malondialdehyde level, and glutathione peroxidase. Liver activity superoxide dismutase also decreased in young rats supplemented with 5 g/kg of Gelam honey [84]. Gelam honey reduces the oxidative damage of young and middle-aged rats by modulating the activities of the antioxidant enzymes that were more prominent in higher concentration compared to the lower concentration [84]. Another study indicates that honey has these antioxidant and free radical sequestering properties, mainly due to its phenolic compounds [85].
\nHoney has antioxidant properties that can be further explored and studied, because antioxidants reduce free radicals and oxidative stress, which can help to promote and maintain health [80, 82, 84]. Besides the previously described, the antioxidant effect of honey can be an important property to help in the anticancer effect [67, 71].
\nSeveral studies have proven the effectiveness of honey as an alternative medicine; some have even shown that honey is as good a medicine as conventional medicine. Use of different types of honeys showed anti-inflammatory effect very similar to the conventional drug and that can be used as an alternative medicine in the treatment of diseases or inflammations. Honey can also be used as an antimicrobial agent anti-inflammatory, antibacterial, antivirals, antifungal, anticancer, and antioxidants. However, there is still a need to increase research on honey, especially in its potential as a medicine and also a dissemination of this knowledge to the population and the medical community, so an increase in the use of this powerful compound will be possible.
\nThe authors declare that there is no conflict of interest.
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