Abstract
The vascular endothelium is a protective barrier between the bloodstream and the vasculature that may be disrupted by different factors such as the presence of diseased states. Diseases like diabetes and obesity pose a great risk toward endothelial cell inflammation and oxidative stress, leading to endothelial cell dysfunction and thereby cardiovascular complications such as atherosclerosis. Sirtuins are NAD+-dependent histone deacetylases that are implicated in the pathophysiology of cardiovascular diseases, and they have been identified to be important regulators of endothelial cell function. A handful of recent studies suggest that disbalance in the regulation of endothelial sirtuins, mainly sirtuin 1 (SIRT1), contributes to endothelial cell dysfunction. Herein, we summarize how SIRT1 and other sirtuins may contribute to endothelial cell function and how presence of diseased conditions may alter their expressions to cause endothelial dysfunction. Moreover, we discuss how the beneficial effects of exercise on the endothelium are dependent on SIRT1. These mainly include regulation of signaling pathways related to endothelial nitric oxide synthase phosphorylation and nitric oxide production, mitochondrial biogenesis and mitochondria-mediated apoptotic pathways, oxidative stress and inflammatory pathways. Sirtuins as modulators of the adverse conditions in the endothelium hold a promising therapeutic potential for health conditions related to endothelial dysfunction and vascular ageing.
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References
Ahmed FW, Rider R, Glanville M, Narayanan K, Razvi S, Weaver JU (2016) Metformin improves circulating endothelial cells and endothelial progenitor cells in type 1 diabetes: MERIT study. Cardiovasc Diabetol 15:116. https://doi.org/10.1186/s12933-016-0413-6
Arunachalam G, Samuel SM, Marei I, Ding H, Triggle CR (2014) Metformin modulates hyperglycaemia-induced endothelial senescence and apoptosis through SIRT1. Br J Pharmacol 171:523–535. https://doi.org/10.1111/bph.12496
Arunachalam G, Lakshmanan AP, Samuel SM, Triggle CR, Ding H (2016) Molecular interplay between microRNA-34a and Sirtuin1 in hyperglycemia-mediated impaired angiogenesis in endothelial cells: effects of metformin. J Pharmacol Exp Ther 356:314–323. https://doi.org/10.1124/jpet.115.226894
Balestrieri ML et al (2008) High glucose downregulates endothelial progenitor cell number via SIRT1. Biochim Biophys Acta 1784:936–945. https://doi.org/10.1016/j.bbapap.2008.03.004
Balestrieri ML et al (2015) Sirtuin 6 expression and inflammatory activity in diabetic atherosclerotic plaques: effects of incretin treatment. Diabetes 64:1395–1406. https://doi.org/10.2337/db14-1149
Boily G et al (2008) SirT1 regulates energy metabolism and response to caloric restriction in mice. PLoS ONE 3:e1759–e1759. https://doi.org/10.1371/journal.pone.0001759
Boini KM, Hussain T, Li PL, Koka S (2017) Trimethylamine-N-oxide instigates NLRP3 inflammasome activation and endothelial dysfunction. Cell Physiol Biochem 44:152–162. https://doi.org/10.1159/000484623
Boocock DJ et al (2007) Phase I dose escalation pharmacokinetic study in healthy volunteers of resveratrol, a potential cancer chemopreventive agent. Cancer Epidemiol Biomarkers Prev 16:1246–1252. https://doi.org/10.1158/1055-9965.EPI-07-0022
Brown VA et al (2010) Repeat dose study of the cancer chemopreventive agent resveratrol in healthy volunteers: safety, pharmacokinetics, and effect on the insulin-like growth factor axis. Cancer Res 70:9003–9011. https://doi.org/10.1158/0008-5472.CAN-10-2364
Cacicedo JM, Gauthier MS, Lebrasseur NK, Jasuja R, Ruderman NB, Ido Y (2011) Acute exercise activates AMPK and eNOS in the mouse aorta. Am J Physiol Heart Circ Physiol 301:H1255–1265. https://doi.org/10.1152/ajpheart.01279.2010
Cao W, Dou Y, Li A (2018) Resveratrol boosts cognitive function by targeting SIRT1. Neurochem Res 43:1705–1713. https://doi.org/10.1007/s11064-018-2586-8
Cardus A, Uryga AK, Walters G, Erusalimsky JD (2013) SIRT6 protects human endothelial cells from DNA damage, telomere dysfunction, and senescence. Cardiovasc Res 97:571–579. https://doi.org/10.1093/cvr/cvs352
Cazzaniga A, Locatelli L, Castiglioni S, Maier JAM (2019) The dynamic adaptation of primary human endothelial cells to simulated microgravity. FASEB J 33:5957–5966. https://doi.org/10.1096/fj.201801586RR
Chalkiadaki A, Guarente L (2012) High-fat diet triggers inflammation-induced cleavage of SIRT1 in adipose tissue to promote metabolic dysfunction. Cell Metab 16:180–188. https://doi.org/10.1016/j.cmet.2012.07.003
Chan S-H et al (2018a) Exercise intervention attenuates hyperhomocysteinemia-induced aortic endothelial oxidative injury by regulating SIRT1 through mitigating NADPH oxidase/LOX-1 signaling. Redox Biol 14:116–125. https://doi.org/10.1016/j.redox.2017.08.016
Chan SH et al (2018b) Exercise intervention attenuates hyperhomocysteinemia-induced aortic endothelial oxidative injury by regulating SIRT1 through mitigating NADPH oxidase/LOX-1 signaling. Redox Biol 14:116–125. https://doi.org/10.1016/j.redox.2017.08.016
Cheang WS et al (2019) Resveratrol ameliorates endothelial dysfunction in diabetic and obese mice through sirtuin 1 and peroxisome proliferator-activated receptor delta. Pharmacol Res 139:384–394. https://doi.org/10.1016/j.phrs.2018.11.041
Chen J et al (2012) Cathepsin cleavage of sirtuin 1 in endothelial progenitor cells mediates stress-induced premature senescence. Am J Pathol 180:973–983. https://doi.org/10.1016/j.ajpath.2011.11.033
Chen Y, Fu LL, Wen X, Wang XY, Liu J, Cheng Y, Huang J (2014a) Sirtuin-3 (SIRT3), a therapeutic target with oncogenic and tumor-suppressive function in cancer. Cell Death Dis 5:e1047–e1047. https://doi.org/10.1038/cddis.2014.14
Chen Y, Wang H, Luo G, Dai X (2014b) SIRT4 inhibits cigarette smoke extracts-induced mononuclear cell adhesion to human pulmonary microvascular endothelial cells via regulating NF-κB activity. Toxicol Lett 226:320–327. https://doi.org/10.1016/j.toxlet.2014.02.022
Chen Z et al (2015) Oxidative stress activates endothelial innate immunity via sterol regulatory element binding protein 2 (SREBP2) transactivation of microRNA-92a. Circulation 131:805–814. https://doi.org/10.1161/CIRCULATIONAHA.114.013675
Chen Y, Liu H, Zhang H, Liu E, Xu C-B, Su X (2016) The sirt1/NF-kB signaling pathway is involved in regulation of endothelin type B receptors mediated by homocysteine in vascular smooth muscle cells. Biomed Pharmacother 84:1979–1985. https://doi.org/10.1016/j.biopha.2016.11.011
Cheng J, Luo X, Huang Z, Chen L (2019) Apelin/APJ system: a potential therapeutic target for endothelial dysfunction-related diseases. J Cell Physiol 234:12149–12160. https://doi.org/10.1002/jcp.27942
Cheung TM, Yan JB, Fu JJ, Huang J, Yuan F, Truskey GA (2015) Endothelial cell senescence increases traction forces due to age-associated changes in the glycocalyx and SIRT1. Cell Mol Bioeng 8:63–75. https://doi.org/10.1007/s12195-014-0371-6
Chu H et al (2018) Resveratrol protects late endothelial progenitor cells from TNF-alpha-induced inflammatory damage by upregulating Kruppel-like factor-2. Mol Med Rep 17:5708–5715. https://doi.org/10.3892/mmr.2018.8621
Civitarese AE et al (2007) Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Med 4:e76–e76. https://doi.org/10.1371/journal.pmed.0040076
Coletta C et al (2012) Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc Natl Acad Sci USA 109:9161–9166. https://doi.org/10.1073/pnas.1202916109
Costa CdS et al (2010) SIRT1 transcription is decreased in visceral adipose tissue of morbidly obese patients with severe hepatic steatosis. Obes Surg 20:633–639. https://doi.org/10.1007/s11695-009-0052-z
D’Onofrio N, Vitiello M, Casale R, Servillo L, Giovane A, Balestrieri ML (2015) Sirtuins in vascular diseases: emerging roles and therapeutic potential. Biochim Biophys Acta 1852:1311–1322. https://doi.org/10.1016/j.bbadis.2015.03.001
D'Onofrio N, Servillo L, Balestrieri ML (2018) SIRT1 and SIRT6 signaling pathways in cardiovascular disease protection. Antioxid Redox Signal 28:711–732. https://doi.org/10.1089/ars.2017.7178
Dai H, Sinclair DA, Ellis JL, Steegborn C (2018) Sirtuin activators and inhibitors: promises, achievements, and challenges. Pharmacol Ther 188:140–154. https://doi.org/10.1016/j.pharmthera.2018.03.004
Das A et al (2018) Impairment of an endothelial NAD+-H2S signaling network is a reversible cause of vascular aging. Cell 173:74–89.e20. https://doi.org/10.1016/j.cell.2018.02.008
Delmas D, Aires V, Limagne E, Dutartre P, Mazué F, Ghiringhelli F, Latruffe N (2011) Transport, stability, and biological activity of resveratrol. Ann N Y Acad Sci 1215:48–59. https://doi.org/10.1111/j.1749-6632.2010.05871.x
Ding M et al (2015) SIRT1 protects against myocardial ischemia-reperfusion injury via activating eNOS in diabetic rats. Cardiovasc Diabetol 14:143–143. https://doi.org/10.1186/s12933-015-0299-8
Eilken HM et al (2017) Pericytes regulate VEGF-induced endothelial sprouting through VEGFR1. Nat Commu 8:1574. https://doi.org/10.1038/s41467-017-01738-3
Fernandes GFS, Silva GDB, Pavan AR, Chiba DE, Chin CM, Dos Santos JL (2017) Epigenetic regulatory mechanisms induced by resveratrol. Nutrients 9:1201. https://doi.org/10.3390/nu9111201
Förstermann U, Li H (2011) Therapeutic effect of enhancing endothelial nitric oxide synthase (eNOS) expression and preventing eNOS uncoupling. Br J Pharmacol 164:213–223. https://doi.org/10.1111/j.1476-5381.2010.01196.x
Förstermann U, Münzel T (2006) Endothelial nitric oxide synthase in vascular disease. Circulation 113:1708–1714. https://doi.org/10.1161/CIRCULATIONAHA.105.602532
Fourny N, Lan C, Seree E, Bernard M, Desrois M (2019) Protective effect of resveratrol against ischemia-reperfusion injury via enhanced high energy compounds and eNOS-SIRT1 expression in type 2 diabetic female rat heart. Nutrients. https://doi.org/10.3390/nu11010105
Gambini J et al (2015) Properties of resveratrol: in vitro and in vivo studies about metabolism, bioavailability, and biological effects in animal models and humans. Oxid Med Cell Longev 2015:837042–837042. https://doi.org/10.1155/2015/837042
Gao J et al (2018) Loss of histone deacetylase 2 inhibits oxidative stress induced by high glucose via the HO-1/SIRT1 pathway in endothelial progenitor cells. Gene 678:1–7. https://doi.org/10.1016/j.gene.2018.07.072
Gerhardt H et al (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161:1163–1177. https://doi.org/10.1083/jcb.200302047
Gescher AJ, Steward WP (2003) Relationship between mechanisms, bioavailibility, and preclinical chemopreventive efficacy of resveratrol: a conundrum. Cancer Epidemiol Biomarkers Prev 12:953–957
Ghosh A, Gao L, Thakur A, Siu PM, Lai CWK (2017) Role of free fatty acids in endothelial dysfunction. J Biomed Sci 24:50. https://doi.org/10.1186/s12929-017-0357-5
Gomes BAQ et al (2018) Neuroprotective mechanisms of resveratrol in Alzheimer's disease: role of SIRT1. Oxid Med Cell Long 2018:8152373. https://doi.org/10.1155/2018/8152373
Gorenne I, Kumar S, Gray K, Figg N, Yu H, Mercer J, Bennett M (2013) Vascular smooth muscle cell sirtuin 1 protects against DNA damage and inhibits atherosclerosis. Circulation 127:386–396. https://doi.org/10.1161/CIRCULATIONAHA.112.124404
Grabowska W, Sikora E, Bielak-Zmijewska A (2017) Sirtuins, a promising target in slowing down the ageing process. Biogerontology 18:447–476. https://doi.org/10.1007/s10522-017-9685-9
Guarente L (2013) Calorie restriction and sirtuins revisited. Genes Dev 27:2072–2085. https://doi.org/10.1101/gad.227439.113
Guo Y et al (2018) Endothelial SIRT1 prevents age-induced impairment of vasodilator responses by enhancing the expression and activity of soluble guanylyl cyclase in smooth muscle cells. Cardiovasc Res. https://doi.org/10.1093/cvr/cvy212
Guo J et al (2019) Endothelial SIRT6 is vital to prevent hypertension and associated cardiorenal injury through targeting Nkx3.2-GATA5. Signal Circ Res 124:1448–1461. https://doi.org/10.1161/circresaha.118.314032
Harsha N et al (2017) CR6-interacting factor 1 deficiency impairs vascular function by inhibiting the Sirt1-endothelial nitric oxide synthase pathway. Antioxid Redox Signal 27:234–249. https://doi.org/10.1089/ars.2016.6719
Hashimoto-Komatsu A, Hirase T, Asaka M, Node K (2011) Angiotensin II induces microtubule reorganization mediated by a deacetylase SIRT2 in endothelial cells. Hypertens Res 34:949–956. https://doi.org/10.1038/hr.2011.64
He X, Zeng H, Roman RJ, Chen J-X (2018) Inhibition of prolyl hydroxylases alters cell metabolism and reverses pre-existing diastolic dysfunction in mice. Int J Cardiol 272:281–287. https://doi.org/10.1016/j.ijcard.2018.08.065
He X, Zeng H, Chen J-X (2019a) Emerging role of SIRT3 in endothelial metabolism, angiogenesis, and cardiovascular disease. J Cell Physiol 234:2252–2265. https://doi.org/10.1002/jcp.27200
He Y et al (2019b) Sitagliptin inhibits vascular inflammation via the SIRT6-dependent signaling pathway. Int Immunopharmacol 75:105805. https://doi.org/10.1016/j.intimp.2019.105805
Heath JM, Fernandez Esmerats J, Khambouneheuang L, Kumar S, Simmons R, Jo H (2018) Mechanosensitive microRNA-181b regulates aortic valve endothelial matrix degradation by targeting TIMP3. Cardiovasc Eng Technol 9:141–150. https://doi.org/10.1007/s13239-017-0296-z
Heilbronn LK, Ravussin E (2003) Calorie restriction and aging: review of the literature and implications for studies in humans. Am J Clin Nutr 78:361–369. https://doi.org/10.1093/ajcn/78.3.361
Herman AB, Autieri MV (2018) Cardiovascular disease, inflammation, and mRNA stability. Aging 10:3046–3047. https://doi.org/10.18632/aging.101619
Higashi Y, Yoshizumi M (2004) Exercise and endothelial function: role of endothelium-derived nitric oxide and oxidative stress in healthy subjects and hypertensive patients. Pharmacol Ther 102:87–96. https://doi.org/10.1016/j.pharmthera.2004.02.003
Hsu PY, Lin WY, Lin RT, Juo SHH (2018) MicroRNA let-7g inhibits angiotensin II-induced endothelial senescence via the LOX-1-independent mechanism. Int J Mol Med 41:2243–2251. https://doi.org/10.3892/ijmm.2018.3416
Huang B, Zhang W, Wei L, Chen S, Wang T, Fu R (2018) Resveratrol down-regulates endothelin type B receptors in vascular smooth muscle cells via Sirt1/ERK1/2/NF-кB signaling pathways. Eur J Pharmacol 840:44–49. https://doi.org/10.1016/j.ejphar.2018.09.022
Incalza MA, D'Oria R, Natalicchio A, Perrini S, Laviola L, Giorgino F (2018) Oxidative stress and reactive oxygen species in endothelial dysfunction associated with cardiovascular and metabolic diseases. Vascul Pharmacol 100:1–19. https://doi.org/10.1016/j.vph.2017.05.005
Jaffe EA (1987) Cell biology of endothelial cells. Hum Pathol 18:234–239. https://doi.org/10.1016/S0046-8177(87)80005-9
Jang IA et al (2018) Effects of resveratrol on the renin-angiotensin system in the aging kidney. Nutrients. https://doi.org/10.3390/nu10111741
Jannin B, Menzel M, Berlot J-P, Delmas D, Lançon A, Latruffe N (2004) Transport of resveratrol, a cancer chemopreventive agent, to cellular targets: plasmatic protein binding and cell uptake. Biochem Pharmacol 68:1113–1118. https://doi.org/10.1016/j.bcp.2004.04.028
Jesko H, Strosznajder RP (2016) Sirtuins and their interactions with transcription factors and poly(ADP-ribose) polymerases. Folia Neuropathol 54:212–233
Jęśko H, Wencel P, Strosznajder RP, Strosznajder JB (2017) Sirtuins and their roles in brain aging and neurodegenerative disorders. Neurochem Res 42:876–890. https://doi.org/10.1007/s11064-016-2110-y
Jiang T, Jiang D, Zhang L, Ding M, Zhou H (2019) Anagliptin ameliorates high glucose-induced endothelial dysfunction via suppression of NLRP3 inflammasome activation mediated by SIRT1. Mol Immunol 107:54–60. https://doi.org/10.1016/j.molimm.2019.01.006
Joshi S, Kar S, Kavdia M (2017) Computational analysis of interactions of oxidative stress and tetrahydrobiopterin reveals instability in eNOS coupling. Microvasc Res 114:114–128. https://doi.org/10.1016/j.mvr.2017.07.001
Karasawa T, Takahashi M (2017) Role of NLRP3 inflammasomes in atherosclerosis. J Atheroscler Thromb 24:443–451. https://doi.org/10.5551/jat.RV17001
Kassan M et al (2017) Sirtuin1 protects endothelial Caveolin-1 expression and preserves endothelial function via suppressing miR-204 and endoplasmic reticulum stress. Sci Rep 7:42265. https://doi.org/10.1038/srep42265
Kato R et al (2016) Sirt1 expression is associated with CD31 expression in blood cells from patients with chronic obstructive pulmonary disease. Respir Res 17:139. https://doi.org/10.1186/s12931-016-0452-2
Kaur I, Rawal P, Rohilla S, Bhat MH, Sharma P, Siddiqui H, Kaur S (2018) Endothelial progenitor cells from aged subjects display decreased expression of sirtuin 1, angiogenic functions, and increased senescence. Cell Biol Int 42:1212–1220. https://doi.org/10.1002/cbin.10999
Ke Y et al (2018) Gut flora-dependent metabolite trimethylamine-N-oxide accelerates endothelial cell senescence and vascular aging through oxidative stress. Free Radical Biol Med 116:88–100. https://doi.org/10.1016/j.freeradbiomed.2018.01.007
Kida Y, Goligorsky MS (2016) Sirtuins, cell senescence, and vascular aging. Can J Cardiol 32:634–641. https://doi.org/10.1016/j.cjca.2015.11.022
Kim MY et al (2012) The PPARδ-mediated inhibition of angiotensin II-induced premature senescence in human endothelial cells is SIRT1-dependent. Biochem Pharmacol 84:1627–1634. https://doi.org/10.1016/j.bcp.2012.09.008
Kim DJ, Martinez-Lemus LA, Davis GE (2013) EB1, p150Glued, and Clasp1 control endothelial tubulogenesis through microtubule assembly, acetylation, and apical polarization. Blood 121:3521–3530. https://doi.org/10.1182/blood-2012-11-470179
Kim JS et al (2015) Shear stress-induced mitochondrial biogenesis decreases the release of microparticles from endothelial cells. Am J Physiol Heart Circ Physiol 309:H425–433. https://doi.org/10.1152/ajpheart.00438.2014
Konukoglu D, Uzun H (2017) Endothelial dysfunction and hypertension. In: Islam MS (ed) Hypertension: from basic research to clinical practice. Springer, Cham, pp 511–540
Kuhnle G et al (2000) Resveratrol is absorbed in the small intestine as resveratrol glucuronide. Biochem Biophys Res Commun 272:212–217. https://doi.org/10.1006/bbrc.2000.2750
Kukkemane K, Jagota A (2019) Therapeutic effects of curcumin on age-induced alterations in daily rhythms of clock genes and Sirt1 expression in the SCN of male Wistar rats. Biogerontology 20:405–419. https://doi.org/10.1007/s10522-018-09794-y
Kuno A, Tanno M, Horio Y (2015) The effects of resveratrol and SIRT1 activation on dystrophic cardiomyopathy. Ann N Y Acad Sci 1348:46–54. https://doi.org/10.1111/nyas.12812
Kutryb-Zajac B, Koszalka P, Slominska EM, Smolenski RT (2018) The effects of pro- and anti-atherosclerotic factors on intracellular nucleotide concentration in murine endothelial cells. Nucleosides Nucleotides Nucleic Acids. https://doi.org/10.1080/15257770.2018.1498513
Lai WK, Kan MY (2015) Homocysteine-induced endothelial dysfunction. Ann Nutr Metab 67:1–12. https://doi.org/10.1159/000437098
Lamalice L, Le Boeuf F, Huot J (2007) Endothelial cell migration during angiogenesis. Circ Res 100:782–794. https://doi.org/10.1161/01.RES.0000259593.07661.1e
Lamichane S et al (2019) MHY2233 attenuates replicative cellular senescence in human endothelial progenitor cells via SIRT1 signaling. Oxid Med Cell Longev 2019:6492029–6492029. https://doi.org/10.1155/2019/6492029
Lee H-M, Kim J-J, Kim HJ, Shong M, Ku BJ, Jo E-K (2013) Upregulated NLRP3 inflammasome activation in patients with type 2 diabetes. Diabetes 62:194–204. https://doi.org/10.2337/db12-0420
Lee S-H, Lee J-H, Lee H-Y, Min K-J (2019a) Sirtuin signaling in cellular senescence and aging. BMB Rep 52:24–34. https://doi.org/10.5483/BMBRep.2019.52.1.290
Lee SJ, Baek SE, Jang MA, Kim CD (2019b) SIRT1 inhibits monocyte adhesion to the vascular endothelium by suppressing Mac-1 expression on monocytes. Exp Mol Med 51:47. https://doi.org/10.1038/s12276-019-0239-x
Lemarie CA et al (2011) Mthfr deficiency induces endothelial progenitor cell senescence via uncoupling of eNOS and downregulation of SIRT1. Am J Physiol Heart Circ Physiol 300:H745–753. https://doi.org/10.1152/ajpheart.00321.2010
Li L et al (2011) SIRT1 inhibits angiotensin II-induced vascular smooth muscle cell hypertrophy. Acta Biochim Biophys Sin 43:103–109. https://doi.org/10.1093/abbs/gmq104
Li W et al (2015a) Silent information regulator 1 (SIRT1) promotes the migration and proliferation of endothelial progenitor cells through the PI3K/Akt/eNOS signaling pathway. Int J Clin Exp Pathol 8:2274–2287
Li Z, Margariti A, Wu Y, Yang F, Hu J, Zhang L, Chen T (2015b) MicroRNA-199a induces differentiation of induced pluripotent stem cells into endothelial cells by targeting sirtuin. Mol Med Rep. https://doi.org/10.3892/mmr.2015.3845
Li Q et al (2016a) P66Shc-induced microRNA-34a causes diabetic endothelial dysfunction by downregulating Sirtuin1. Arterioscler Thromb Vasc Biol 36:2394–2403. https://doi.org/10.1161/atvbaha.116.308321
Li Y et al (2016b) SIRT1 inhibits inflammatory response partly through regulation of NLRP3 inflammasome in vascular endothelial cells. Mol Immunol 77:148–156. https://doi.org/10.1016/j.molimm.2016.07.018
Liao YC, Wang YS, Guo YC, Lin WL, Chang MH, Juo SH (2014) Let-7g improves multiple endothelial functions through targeting transforming growth factor-beta and SIRT-1 signaling. J Am Coll Cardiol 63:1685–1694. https://doi.org/10.1016/j.jacc.2013.09.069
Lipphardt M, Dihazi H, Muller GA, Goligorsky MS (2018a) Fibrogenic secretome of sirtuin 1-deficient endothelial cells: Wnt, Notch and Glycocalyx. Rheostat Front Physiol 9:7. https://doi.org/10.3389/fphys.2018.01325
Lipphardt M, Dihazi H, Müller GA, Goligorsky MS (2018b) Fibrogenic secretome of sirtuin 1-deficient endothelial cells: Wnt, Notch and Glycocalyx Rheostat. Front Physiol. https://doi.org/10.3389/fphys.2018.01325
Liu TF, Vachharajani VT, Yoza BK, McCall CE (2012) NAD+-dependent sirtuin 1 and 6 proteins coordinate a switch from glucose to fatty acid oxidation during the acute inflammatory response. J Biol Chem 287:25758–25769. https://doi.org/10.1074/jbc.M112.362343
Liu JN, Wu X, Wang X, Zhang Y, Bu PL, Zhang QY, Jiang F (2013) Global gene expression profiling reveals functional importance of Sirt2 in endothelial cells under oxidative stress. Int J Mol Sci 14:5633–5649. https://doi.org/10.3390/ijms14035633
Liu R, Liu H, Ha Y, Tilton RG, Zhang W (2014) Oxidative stress induces endothelial cell senescence via downregulation of Sirt6. Biomed Res Int 2014:902842. https://doi.org/10.1155/2014/902842
Liu Z, Wang J, Huang X, Li Z, Liu P (2016) Deletion of sirtuin 6 accelerates endothelial dysfunction and atherosclerosis in apolipoprotein E-deficient mice. Transl Res 172:18–29.e12. https://doi.org/10.1016/j.trsl.2016.02.005
Liu P et al (2018) Sirtuin 3-induced macrophage autophagy in regulating NLRP3 inflammasome activation. Biochim Biophys Acta (BBA) 1864:764–777. https://doi.org/10.1016/j.bbadis.2017.12.027
Liu C et al (2019) Targeting pericyte-endothelial cell crosstalk by circular RNA-cPWWP2A inhibition aggravates diabetes-induced microvascular dysfunction. Proc Natl Acad Sci USA 116:7455–7464. https://doi.org/10.1073/pnas.1814874116
Lu Y et al (2018) Protective effects of Danzhi jiangtang capsule on vascular endothelial damages induced by high-fat diet and palmitic acid. Biomed Pharmacother 107:1631–1640. https://doi.org/10.1016/j.biopha.2018.08.129
Luo X, Hu Y, He S, Ye Q, Lv Z, Liu J, Chen X (2019a) Dulaglutide inhibits high glucose-induced endothelial dysfunction and NLRP3 inflammasome activation. Arch Biochem Biophys 671:203–209. https://doi.org/10.1016/j.abb.2019.07.008
Luo Y, Lu S, Ai Q, Zhou P, Qin M, Sun G, Sun X (2019b) SIRT1/AMPK and Akt/eNOS signaling pathways are involved in endothelial protection of total aralosides of Aralia elata (Miq) Seem against high-fat diet-induced atherosclerosis in ApoE-/- mice. PTR Phytotherapy Res. https://doi.org/10.1002/ptr.6269
Marier J-F, Vachon P, Gritsas A, Zhang J, Moreau J-P, Ducharme MP (2002) Metabolism and disposition of resveratrol in rats: extent of absorption, glucuronidation, and enterohepatic recirculation evidenced by a linked-rat model. J Pharmacol Exp Ther 302:369–373. https://doi.org/10.1124/jpet.102.033340
Marton O et al (2010) Aging and exercise affect the level of protein acetylation and SIRT1 activity in cerebellum of male rats. Biogerontology 11:679–686. https://doi.org/10.1007/s10522-010-9279-2
Masaki T, Sawamura T (2006) Endothelin and endothelial dysfunction. Proc Jpn Acad Series B 82:17–24
Mattagajasingh I et al (2007) SIRT1 promotes endothelium-dependent vascular relaxation by activating endothelial nitric oxide synthase. Proc Natl Acad Sci 104:14855–14860. https://doi.org/10.1073/pnas.0704329104
Mercken EM et al (2014) SIRT1 but not its increased expression is essential for lifespan extension in caloric-restricted mice. Aging Cell 13:193–196. https://doi.org/10.1111/acel.12151
Miksits M et al (2005) Sulfation of resveratrol in human liver: evidence of a major role for the sulfotransferases SULT1A1 and SULT1E1. Xenobiotica 35:1101–1119. https://doi.org/10.1080/00498250500354253
Ming G-f, Wu K, Hu K, Chen Y, Xiao J (2016) NAMPT regulates senescence, proliferation, and migration of endothelial progenitor cells through the SIRT1 AS lncRNA/miR-22/SIRT1 pathway. Biochem Biophys Res Commun 478:1382–1388. https://doi.org/10.1016/j.bbrc.2016.08.133
Miyashita H et al (2012) Angiogenesis inhibitor vasohibin-1 enhances stress resistance of endothelial cells via induction of SOD2 and SIRT1. PLoS ONE 7:12. https://doi.org/10.1371/journal.pone.0046459
Moriya J, Minamino T (2017) Angiogenesis, cancer, and vascular aging. Front Cardiovasc Med. https://doi.org/10.3389/fcvm.2017.00065
Mortuza R, Feng B, Chakrabarti S (2015) SIRT1 reduction causes renal and retinal injury in diabetes through endothelin 1 and transforming growth factor β1. J Cell Mol Med 19:1857–1867. https://doi.org/10.1111/jcmm.12557
Mudau M, Genis A, Lochner A, Strijdom H (2012) Endothelial dysfunction: the early predictor of atherosclerosis. Cardiovasc J Afr 23:222–231. https://doi.org/10.5830/CVJA-2011-068
Nafisa A et al (2018) Endothelial function and dysfunction: impact of metformin. Pharmacol Ther 192:150–162. https://doi.org/10.1016/j.pharmthera.2018.07.007
Nakagawa T, Lomb DJ, Haigis MC, Guarente L (2009) SIRT5 Deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle. Cell 137:560–570. https://doi.org/10.1016/j.cell.2009.02.026
Ong AT, Aoki J, Kutryk MJ, Serruys PW (2005) How to accelerate the endothelialization of stents. Arch Mal Coeur Vaiss 98:123–126
Ota H, Akishita M, Eto M, Iijima K, Kaneki M, Ouchi Y (2007) Sirt1 modulates premature senescence-like phenotype in human endothelial cells. J Mol Cell Cardiol 43:571–579. https://doi.org/10.1016/j.yjmcc.2007.08.008
Ota H et al (2010) Induction of endothelial nitric oxide synthase, SIRT1, and catalase by statins inhibits endothelial senescence through the Akt pathway. Arterioscler Thromb Vasc Biol 30:2205–2211. https://doi.org/10.1161/atvbaha.110.210500
Pacholec M et al (2010) SRT1720, SRT2183, SRT1460, and resveratrol are not direct activators of SIRT1. J Biol Chem 285:8340–8351. https://doi.org/10.1074/jbc.M109.088682
Pan F et al (2016) MicroRNA-200a is up-regulated in aged rats with erectile dysfunction and could attenuate endothelial function via SIRT1 inhibition. Asian J Androl 18:74–79. https://doi.org/10.4103/1008-682x.154991
Peltz L et al (2012) Resveratrol exerts dosage and duration dependent effect on human mesenchymal stem cell development. PLoS ONE 7:e37162–e37162. https://doi.org/10.1371/journal.pone.0037162
Piao S et al (2018) CR6 interacting factor 1 deficiency promotes endothelial inflammation by SIRT1 downregulation. PLoS ONE 13:16. https://doi.org/10.1371/journal.pone.0192693
Piqueras L et al (2007) Activation of PPARβ/δ; induces endothelial cell proliferation and angiogenesis. Arterioscler Thromb Vasc Biol 27:63–69. https://doi.org/10.1161/01.ATV.0000250972.83623.61
Qiu Y, Lai H, Huang Y, Hong L, Wang H, Tao Y (2016) Effect of shear force on SIRT4 in LPS-injured human umbilical vein endothelial cells. Int J Clin Exp Pathol 9:4921–4930
Redman LM, Smith SR, Burton JH, Martin CK, Il'yasova D, Ravussin E (2018) Metabolic slowing and reduced oxidative damage with sustained caloric restriction support the rate of living and oxidative damage theories of aging. Cell Metab 27:805–815.e804. https://doi.org/10.1016/j.cmet.2018.02.019
Rocha B et al (2018) Energy restriction, exercise and atorvastatin treatment improve endothelial dysfunction and inhibit miRNA-155 in the erectile tissue of the aged rat. Nutr Metab 15:12. https://doi.org/10.1186/s12986-018-0265-z
Rokutanda T, Izumiya Y, Araki S, Hanatani S, Bober E, Braun T, Ogawa H (2012) Abstract 10980: Sirt7 regulates endothelial cell functions and promotes angiogenic response in mice model of hindlimb ischemia. Circulation 126:A10980–A10980. https://doi.org/10.1161/circ.126.suppl_21.A10980
Salani D, Taraboletti G, Rosanò L, Di Castro V, Borsotti P, Giavazzi R, Bagnato A (2000) Endothelin-1 induces an angiogenic phenotype in cultured endothelial cells and stimulates neovascularization in vivo. Am J Pathol 157:1703–1711. https://doi.org/10.1016/S0002-9440(10)64807-9
Salmito FTS, de Oliveira Neves FM, Meneses GC, de Almeida LR, Martins AMC, Libório AB (2015) Glycocalyx injury in adults with nephrotic syndrome: association with endothelial function. Clin Chim Acta 447:55–58. https://doi.org/10.1016/j.cca.2015.05.013
Sidorova-Darmos E et al (2014) Differential expression of sirtuin family members in the developing, adult, and aged rat brain. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2014.00333
Sieve I, Münster-Kühnel AK, Hilfiker-Kleiner D (2018) Regulation and function of endothelial glycocalyx layer in vascular diseases. Vascul Pharmacol 100:26–33. https://doi.org/10.1016/j.vph.2017.09.002
Smoliga JM, Blanchard O (2014) Enhancing the delivery of resveratrol in humans: if low bioavailability is the problem, what is the solution? Molecules 19:17154–17172. https://doi.org/10.3390/molecules191117154
Smoliga JM, Colombo ES, Campen MJ (2013) A healthier approach to clinical trials evaluating resveratrol for primary prevention of age-related diseases in healthy populations. Aging (Albany NY) 5:495–506. https://doi.org/10.18632/aging.100579
Someya S et al (2010) Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell 143:802–812. https://doi.org/10.1016/j.cell.2010.10.002
Song X, Yang B, Qiu F, Jia M, Fu G (2017) High glucose and free fatty acids induce endothelial progenitor cell senescence via PGC-1alpha/SIRT1 signaling pathway. Cell Biol Int 41:1146–1159. https://doi.org/10.1002/cbin.10833
Sorrentino SA et al (2007) Oxidant stress impairs in vivo reendothelialization capacity of endothelial progenitor cells from patients with type 2 diabetes mellitus: restoration by the peroxisome proliferator-activated receptor-gamma agonist rosiglitazone. Circulation 116:163–173. https://doi.org/10.1161/circulationaha.106.684381
Sosnowska B, Mazidi M, Penson P, Gluba-Brzózka A, Rysz J, Banach M (2017) The sirtuin family members SIRT1, SIRT3 and SIRT6: their role in vascular biology and atherogenesis. Atherosclerosis 265:275–282. https://doi.org/10.1016/j.atherosclerosis.2017.08.027
Stocco B, Toledo K, Salvador M, Paulo M, Koyama N, Torqueti Toloi MR (2012) Dose-dependent effect of resveratrol on bladder cancer cells: chemoprevention and oxidative stress. Maturitas 72:72–78. https://doi.org/10.1016/j.maturitas.2012.02.004
Summerhill V, Karagodin V, Grechko A, Myasoedova V, Orekhov A (2018) Vasculoprotective role of olive oil compounds via modulation of oxidative stress in atherosclerosis. Front Cardiovasc Med. https://doi.org/10.3389/fcvm.2018.00188
Sun L, Bai Y, Du G (2009) Endothelial dysfunction: an obstacle of therapeutic angiogenesis. Ageing Res Rev 8:306–313. https://doi.org/10.1016/j.arr.2009.04.003
Sun S et al (2020) Vascular endothelium-targeted Sirt7 gene therapy rejuvenates blood vessels and extends life span in a Hutchinson-Gilford progeria model. Sci Adv. https://doi.org/10.1126/sciadv.aay5556
Takizawa Y et al (2013) Up-regulation of endothelial nitric oxide synthase (eNOS), silent mating type information regulation 2 homologue 1 (SIRT1) and autophagy-related genes by repeated treatments with resveratrol in human umbilical vein endothelial cells. Br J Nutr 110:2150–2155. https://doi.org/10.1017/S0007114513001670
Tang X, Chen XF, Chen HZ, Liu DP (2017) Mitochondrial sirtuins in cardiometabolic diseases. Clin Sci (London, England) 131:2063–2078. https://doi.org/10.1042/cs20160685
Tao Y, Huang C, Huang Y, Hong L, Wang H, Zhou Z, Qiu Y (2015) SIRT4 suppresses inflammatory responses in human umbilical vein endothelial cells. Cardiovasc Toxicol 15:217–223. https://doi.org/10.1007/s12012-014-9287-6
Tao Y, Yu S, Chao M, Wang Y, Xiong J, Lai H (2019) SIRT4 suppresses the PI3K/Akt/NF-κB signaling pathway and attenuates HUVEC injury induced by oxLDL. Mol Med Rep 19:4973–4979. https://doi.org/10.3892/mmr.2019.10161
Tasatargil A, Tanriover G, Barutcigil A, Turkmen E (2018) Protective effect of resveratrol on methylglyoxal-induced endothelial dysfunction in aged rats. Aging Clin Exp Res. https://doi.org/10.1007/s40520-018-0986-x
Tennen RI, Berber E, Chua KF (2010) Functional dissection of SIRT6: Identification of domains that regulate histone deacetylase activity and chromatin localization. Mech Ageing Dev 131:185–192. https://doi.org/10.1016/j.mad.2010.01.006
Thangjam GS et al (2016) Hsp90 inhibition suppresses NF-kappa B transcriptional activation via Sirt-2 in human lung microvascular endothelial cells. Am J Physiol-Lung Cell Mol Physiol 310:L964–L974. https://doi.org/10.1152/ajplung.00054.2016
Thompson AM, Wagner R, Rzucidlo EM (2014) Age-related loss of SirT1 expression results in dysregulated human vascular smooth muscle cell function. Am J Physiol Heart Circ Physiol 307:H533–H541. https://doi.org/10.1152/ajpheart.00871.2013
Toiber D, Sebastian C, Mostoslavsky R (2011) Characterization of nuclear sirtuins: molecular mechanisms and physiological relevance. Handb Exp Pharmacol 206:189–224. https://doi.org/10.1007/978-3-642-21631-2_9
Trujillo-Gonzalez I et al (2018) microRNA-129-5p is regulated by choline availability and controls EGF receptor synthesis and neurogenesis in the cerebral cortex. FASEB J. https://doi.org/10.1096/fj.201801094RR
Urpí-Sardà M, Jáuregui O, Lamuela-Raventós RM, Jaeger W, Miksits M, Covas M-I, Andres-Lacueva C (2005) Uptake of diet resveratrol into the human low-density lipoprotein. Identification and quantification of resveratrol metabolites by liquid chromatography coupled with tandem mass spectrometry. Anal Chem 77:3149–3155. https://doi.org/10.1021/ac0484272
Vachharajani VT, Liu T, Wang X, Hoth JJ, Yoza BK, McCall CE (2016) Sirtuins Link Inflammation and Metabolism. J Immunol Res 2016:10. https://doi.org/10.1155/2016/8167273
Vanhoutte PM (1997) Endothelial dysfunction and atherosclerosis. Eur Heart J 18:19–29. https://doi.org/10.1093/eurheartj/18.suppl_E.19
Vassallo PF et al (2014) Accelerated senescence of cord blood endothelial progenitor cells in premature neonates is driven by SIRT1 decreased expression. Blood 123:2116–2126. https://doi.org/10.1182/blood-2013-02-484956
Vikram A, Kim YR, Kumar S, Li Q, Kassan M, Jacobs JS, Irani K (2016) Vascular microRNA-204 is remotely governed by the microbiome and impairs endothelium-dependent vasorelaxation by downregulating Sirtuin1. Nat Commun 7:12565. https://doi.org/10.1038/ncomms12565
Villalba JM, Alcaín FJ (2012) Sirtuin activators and inhibitors. BioFactors (Oxford, England) 38:349–359. https://doi.org/10.1002/biof.1032
Voghel G et al (2010) Endogenous oxidative stress prevents telomerase-dependent immortalization of human endothelial cells. Mech Ageing Dev 131:354–363. https://doi.org/10.1016/j.mad.2010.04.004
Walle T, Walle UK, Sedmera D, Klausner M (2006) Benzo[A]pyrene-induced oral carcinogenesis and chemoprevention: studies in bioengineered human tissue. Drug Metab Dispos 34:346–350. https://doi.org/10.1124/dmd.105.007948
Wallerath T, Deckert G, Ternes T, Anderson H, Li H, Witte K, Förstermann U (2002) Resveratrol, a polyphenolic phytoalexin present in red wine, enhances expression and activity of endothelial nitric oxide synthase. Circulation 106:1652–1658. https://doi.org/10.1161/01.cir.0000029925.18593.5c
Wan Y-Z et al (2014) SIRT1-mediated epigenetic downregulation of plasminogen activator inhibitor-1 prevents vascular endothelial replicative senescence. Aging Cell 13:890–899. https://doi.org/10.1111/acel.12247
Wang W et al (2019) Hydroxytyrosol NO regulates oxidative stress and NO production through SIRT1 in diabetic mice and vascular endothelial cells. Phytomedicine 52:206–215. https://doi.org/10.1016/j.phymed.2018.09.208
Wątroba M, Szukiewicz D (2016) The role of sirtuins in aging and age-related diseases. Adv Med Sci 61:52–62. https://doi.org/10.1016/j.advms.2015.09.003
Wenzel E, Somoza V (2005) Metabolism and bioavailability of trans-resveratrol. Mol Nutr Food Res 49:472–481. https://doi.org/10.1002/mnfr.200500010
Winnik S, Auwerx J, Sinclair DA, Matter CM (2015) Protective effects of sirtuins in cardiovascular diseases: from bench to bedside. Eur Heart J 36:3404–3412. https://doi.org/10.1093/eurheartj/ehv290
Wu H, Chen Z, Chen JZ, Xie J, Xu B (2018) Resveratrol improves tube formation in AGE-induced late endothelial progenitor cells by suppressing syndecan-4 shedding. Oxid Med Cell Long 2018:9045976. https://doi.org/10.1155/2018/9045976
Xia N et al (2010) Resveratrol reverses endothelial nitric-oxide synthase uncoupling in apolipoprotein E knockout mice. J Pharmacol Exp Therap 335:149–154. https://doi.org/10.1124/jpet.110.168724
Xia N et al (2013) Role of SIRT1 and FOXO factors in eNOS transcriptional activation by resveratrol. Nitric Oxide 32:29–35. https://doi.org/10.1016/j.niox.2013.04.001
Xia N, Forstermann U, Li H (2014a) Resveratrol and endothelial nitric oxide. Molecules (Basel, Switzerland) 19:16102–16121. https://doi.org/10.3390/molecules191016102
Xia N, Förstermann U, Li H (2014b) Resveratrol and endothelial nitric oxide. Molecules 19:16102–16121. https://doi.org/10.3390/molecules191016102
Xia N, Daiber A, Forstermann U, Li H (2017) Antioxidant effects of resveratrol in the cardiovascular system. Br J Pharmacol 174:1633–1646. https://doi.org/10.1111/bph.13492
Xing S-S, Li J, Chen L, Yang Y-F, He P-L, Li J, Yang J (2018) Salidroside attenuates endothelial cellular senescence via decreasing the expression of inflammatory cytokines and increasing the expression of SIRT3. Mech Ageing Dev 175:1–6. https://doi.org/10.1016/j.mad.2017.12.005
Xu Z, Zhang L, Fei X, Yi X, Li W, Wang Q (2014) The miR-29b–Sirt1 axis regulates self-renewal of mouse embryonic stem cells in response to reactive oxygen species. Cell Signal 26:1500–1505. https://doi.org/10.1016/j.cellsig.2014.03.010
Xu S et al (2016) SIRT6 protects against endothelial dysfunction and atherosclerosis in mice. Aging 8:1064–1082. https://doi.org/10.18632/aging.100975
Yang F et al (2019) Metformin Inhibits the NLRP3 Inflammasome via AMPK/mTOR-dependent effects in diabetic cardiomyopathy. Int J Biol Sci 15:1010–1019. https://doi.org/10.7150/ijbs.29680
Yang J, Wang N, Li J, Zhang J, Feng P (2010) Effects of resveratrol on NO secretion stimulated by insulin and its dependence on SIRT1 in high glucose cultured endothelial cells. Endocrine 37:365–372. https://doi.org/10.1007/s12020-010-9314-8
Yang N-C, Song T-Y, Chang Y-Z, Chen M-Y, Hu M-L (2015) Up-regulation of nicotinamide phosphoribosyltransferase and increase of NAD+ levels by glucose restriction extend replicative lifespan of human fibroblast Hs68 cells. Biogerontology 16:31–42. https://doi.org/10.1007/s10522-014-9528-x
Yao F et al (2019) The protective effect of hydroxytyrosol acetate against inflammation of vascular endothelial cells partly through the SIRT6-mediated PKM2 signaling pathway. Food Funct 10:5789–5803. https://doi.org/10.1039/c9fo00586b
Yin W-L, Yin W-G, Huang B-S, Wu L-X (2019) LncRNA SNHG12 inhibits miR-199a to upregulate SIRT1 to attenuate cerebral ischemia/reperfusion injury through activating AMPK signaling pathway. Neurosci Lett 690:188–195. https://doi.org/10.1016/j.neulet.2018.08.026
Yu B-B et al (2019) Mitochondrial dysfunction-mediated decline in angiogenic capacity of endothelial progenitor cells is associated with capillary rarefaction in patients with hypertension via downregulation of CXCR4/JAK2/SIRT5 signaling. EBioMedicine 42:64–75. https://doi.org/10.1016/j.ebiom.2019.03.031
Yuan Q et al (2014) Regulation of endothelial progenitor cell differentiation and function by dimethylarginine dimethylaminohydrolase 2 in an asymmetric dimethylarginine-independent manner. Cell Biol Int 38:1013–1022. https://doi.org/10.1002/cbin.10288
Yuan Y, Cruzat VF, Newsholme P, Cheng J, Chen Y, Lu Y (2016) Regulation of SIRT1 in aging: roles in mitochondrial function and biogenesis. Mech Ageing Dev 155:10–21. https://doi.org/10.1016/j.mad.2016.02.003
Zhai J, Qu X, Zhang Y, Gao H, Tao L, Song Y, Zhang S (2019) Salvianolic acid inhibits the effects of high glucose on vascular endothelial dysfunction by modulating the Sirt1-eNOS pathway. J Biochem Mol Toxicol 33:e22245
Zhang L et al (2014) MiR-132 inhibits expression of SIRT1 and induces pro-inflammatory processes of vascular endothelial inflammation through blockade of the SREBP-1c metabolic pathway. Cardiovasc Drugs Ther 28:303–311. https://doi.org/10.1007/s10557-014-6533-x
Zhang E, Guo Q, Gao H, Xu R, Teng S, Wu Y (2015) Metformin and resveratrol inhibited high glucose-induced metabolic memory of endothelial senescence through SIRT1/p300/p53/p21 pathway. PLoS ONE 10:e0143814–e0143814. https://doi.org/10.1371/journal.pone.0143814
Zhang J, Wang C, Nie H, Wu D, Ying W (2016) SIRT2 plays a significant role in maintaining the survival and energy metabolism of PIEC endothelial cells. Int J Physiol Pathophysiol Pharmacol 8:120–127
Zhang H-n, Xu Q-q, Thakur A, Alfred MO, Chakraborty M, Ghosh A, Yu X-b (2018a) Endothelial dysfunction in diabetes and hypertension: role of microRNAs and long non-coding RNAs Life. Sciences 213:258–268. https://doi.org/10.1016/j.lfs.2018.10.028
Zhang X, Sun D, Song JW, Zullo J, Lipphardt M, Coneh-Gould L, Goligorsky MS (2018b) Endothelial cell dysfunction and glycocalyx: a vicious circle Matrix. Biology 71–72:421–431. https://doi.org/10.1016/j.matbio.2018.01.026
Zhang C, Abdukerim M, Abilailieti M, Tang L, Ling Y, Pan S (2019) The protective effects of orexin a against high glucose-induced activation of NLRP3 inflammasome in human vascular endothelial cells. Arch Biochem Biophys. https://doi.org/10.1016/j.abb.2019.07.017
Zhao T, Li J, Chen AF (2010) MicroRNA-34a induces endothelial progenitor cell senescence and impedes its angiogenesis via suppressing silent information regulator 1. Am J Physiol Endocrinol Metab 299:E110–E116. https://doi.org/10.1152/ajpendo.00192.2010
Zhao Y, Vanhoutte PM, Leung SWS (2015) Vascular nitric oxide: beyond eNOS. J Pharmacol Sci 129:83–94. https://doi.org/10.1016/j.jphs.2015.09.002
Zu Y et al (2010) SIRT1 promotes proliferation and prevents senescence through targeting LKB1 in primary porcine aortic endothelial cells. Circ Res 106:1384–1393. https://doi.org/10.1161/CIRCRESAHA.109.215483
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This work is funded by the Natural Science Foundation of Zhejiang Province (LQ20H310003 to Y.X.B.), and Wu Jieping Medical Foundation (320675019088-19 to Z.C.H.).
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Zhang, Hn., Dai, Y., Zhang, Ch. et al. Sirtuins family as a target in endothelial cell dysfunction: implications for vascular ageing. Biogerontology 21, 495–516 (2020). https://doi.org/10.1007/s10522-020-09873-z
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DOI: https://doi.org/10.1007/s10522-020-09873-z