Эндотелий и старение: механизмы формирования сенесцентного фенотипа эндотелиальных клеток
https://doi.org/10.24884/1682-6655-2023-22-3-19-33
Аннотация
Проблема клеточного старения является ключевой в определении механизмов старения организма в целом и развития возраст-ассоциированных заболеваний. Изучение факторов, вызывающих активацию программы клеточного старения эндотелия, является важным аспектом расширения превентивных anti-age технологий, направленных на замедление данного процесса и снижения риска развития заболеваний сердечно-сосудистой системы. В данном обзоре освещены современные представления о факторах старения эндотелиальных клеток с акцентом на роль эндогенных изменений гомеостаза эндотелиальных клеток, их предшественниц и микроокружения. В качестве предполагаемых механизмов старения эндотелия рассмотрены дисрегуляция клеточного цикла, митохондриальная дисфункция, изменение гомеостаза белков, истощение пула эндотелиальных клеток-предшественников, а также изменение регуляции программ апоптоза и аутофагии.
Об авторах
Т. И. ВласоваРоссия
Власова Татьяна Ивановна – д-р мед. наук, доцент, зав. кафедрой нормальной и патологической физиологии
430000, г. Саранск, ул. Большевистская, д. 68
Н. Н. Петрищев
Россия
Петрищев Николай Николаевич – д-р мед. наук, профессор, профессор кафедры патофизиологии с курсом клинической патофизиологии
197022, Санкт-Петербург, ул. Льва Толстого, д. 6-8
Т. Д. Власов
Россия
Власов Тимур Дмитриевич – д-р мед. наук, профессор, зав. кафедрой патофизиологии с курсом клинической патофизиологии
197022, Санкт-Петербург, ул. Льва Толстого, д. 6-8
Список литературы
1. Ставровская А.В., Воронков Д.Н., Шестакова Е.А. и др. Моделирование возраст-зависимых заболеваний: связь нервной и эндокринной систем // Анналы клин. и эксперим. неврол. – 2018; – Т. 12, № 5S. – С. 79–86. Doi: 10.25692/ ACEN.2018.5.10.
2. Cohen C, Le Goff O, Soysouvanh F, Vasseur F, Tanou M, Nguyen C, Amrouche L, Le Guen J, Saltel-Fulero O, Meunier T, Nguyen-Khoa T, Rabant M, Nochy D, Legendre C, Friedlander G, Childs BG, Baker DJ, Knebelmann B, Anglicheau D, Milliat F, Terzi F. Glomerular endothelial cell senescence drives age-related kidney disease through PAI-1 // EMBO Mol Med. 2021;13(11):e14146. Doi: 10.15252/emmm.202114146.
3. Jia G, Aroor AR, Jia C, Sowers JR. Endothelial cell senescence in aging-related vascular dysfunction // Biochim Biophys Acta Mol Basis Dis. 2019;1865(7):1802–1809. Doi: 10.1016/j.bbadis.2018.08.008.
4. Bloom SI, Islam MT, Lesniewski LA, Donato AJ. Mechanisms and consequences of endothelial cell senescence // Nat Rev Cardiol. 2023;20(1):38–51. Doi: 10.1038/s41569- 022-00739-0.
5. Gasek NS, Kuchel GA, Kirkland JL et al. Strategies for targeting senescent cells in human disease // Nat Aging. 2021; 1:870–879. Doi: 10.1038/s43587-021-00121-8.
6. “Cоциальная жизнь” стареющих клеток: что такое SASP и зачем его изучать? / Бородкина А.В., Дерябин П.И., Грюкова А.А., Никольский Н.Н. // Acta Naturae (русскоязычная версия). – 2018. – Т. 10, № 1(36). – С. 4–14.
7. Carrel A. On the permanent life of tissues outside of the organism // J Exp Med. 1912;15(5):516–28. Doi: 10.1084/ jem.15.5.516.
8. Rodier F, Campisi J. Four faces of cellular senescence // J Cell Biol. 2011;192(4):547–556. Doi: 10.1083/jcb.201009094.
9. Franceschi C, Campisi J. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases // J Gerontol A Biol Sci Med Sci. 2014;69(Suppl 1): S4–S9. Doi: 10.1093/gerona/glu057.
10. de Keizer PL. The Fountain of Youth by Targeting Senescent Cells? // Trends Mol Med. 2017;23(1):6–17. Doi: 10.1016/j.molmed.2016.11.006.
11. Gorgoulis V, Adams PD, Alimonti A, Bennett DC, Bischof O, Bishop C, Campisi J, Collado M, Evangelou K, Ferbeyre G, Gil J, Hara E, Krizhanovsky V, Jurk D, Maier AB, Narita M, Niedernhofer L, Passos JF, Robbins PD, Schmitt CA, Sedivy J, Vougas K, von Zglinicki T, Zhou D, Serrano M, Demaria M. Cellular Senescence: Defining a Path Forward // Cell. 2019;179(4):813–827. Doi: 10.1016/j.cell.2019.10.005.
12. Hohensinner PJ, Kaun C, Buchberger E, Ebenbauer B, Demyanets S, Huk I, Eppel W, Maurer G, Huber K, Wojta J. Age intrinsic loss of telomere protection via TRF1 reduction in endothelial cells // Biochim Biophys Acta. 2016;1863(2):360– 367. Doi: 10.1016/j.bbamcr.2015.11.034.
13. Jia G et al. Vascular stiffness in insulin resistance and obesity // Frontiers Physiol. 2015;6:231. Doi: 10.3389/fphys. 2015.00231.
14. Власов Т.Д., Петрищев Н.Н., Лазовская О.А. Дисфункция эндотелия. Правильно ли мы понимаем этот термин? // Вестн. анестезиол. и реаниматол. – 2020. – Т. 17, № 2. – С. 76–84. Doi: 10.21292/2078- 5658-2020-17-2-76-84.
15. Власова Т.И., Петрищев Н.Н., Власов Т.Д. Дисфункция эндотелия как типовое патологическое состояние // Регионарное кровообращение и микроциркуляция. – 2022. – Т. 21, № 2. – С. 4–15. Doi: 10.24884/1682-6655-2022- 21-2-4-15.
16. Aird WC. Endothelial cell heterogeneity // Cold Spring Harb Perspect Med. 2012;2(1):a006429. Doi: 10.1101/cshperspect.a006429.
17. Васина Л.В., Власов Т.Д., Петрищев Н.Н. Функциональная гетерогенность эндотелия (обзор) // Артериальная гипертензия. – 2017. – Т. 23, № 2. – С. 88–102. Doi: 10.18705/1607-419X2017-23-2-88-102.
18. Inverso D, Shi J, Lee KH, Jakab M, Ben-Moshe S, Kulkarni SR, Schneider M, Wang G, Komeili M, Vélez PA, Riedel M, Spegg C, Ruppert T, Schaeffer-Reiss C, Helm D, Singh I, Boutros M, Chintharlapalli S, Heikenwalder M, Itzkovitz S, Augustin HG. A spatial vascular transcriptomic, proteomic, and phosphoproteomic atlas unveils an angiocrine Tie-Wnt signaling axis in the liver // Dev Cell. 2021;56(11):1677–1693. e10. Doi: 10.1016/j.devcel.2021.05.001.
19. Dight J, Zhao J, Styke C, Khosrotehrani K, Patel J. Resident vascular endothelial progenitor definition and function: the age of reckoning // Angiogenesis. 2022;25(1):15–33. Doi: 10.1007/s10456-021-09817-2.
20. Davies PF, Civelek M, Fang Y, Fleming I. The atherosusceptible endothelium: endothelial phenotypes in complex haemodynamic shear stress regions in vivo // Cardiovasc Res. 2013;99(2):315–327. Doi: 10.1093/cvr/cvt101.
21. Hobson B, Denekamp J. Endothelial proliferation in tumours and normal tissues: continuous labelling studies // Br J Cancer. 1984;49(4):405–413. Doi: 10.1038/bjc.1984.66.
22. Kliche K, Jeggle P, Pavenstädt H, Oberleithner H. Role of cellular mechanics in the function and life span of vascular endothelium // Pflugers Arch. 2011;462(2):209–217. Doi: 10.1007/s00424-011-0929-2.
23. DeLeve LD. Liver sinusoidal endothelial cells and liver regeneration // J Clin Invest. 2013;123(5):1861–1866. Doi: 10.1172/JCI66025.
24. He L, Huang X, Kanisicak O, Li Y, Wang Y, Li Y, Pu W, Liu Q, Zhang H, Tian X, Zhao H, Liu X, Zhang S, Nie Y, Hu S, Miao X, Wang Q-D, Wang F, Chen T, Xu Q, Lui KO, Molkentin JD, Zhou B. Preexisting endothelial cells mediate cardiac neovascularization after injury // J Clin Investig. 2017;127(8):2968–2981. Doi: 10.1172/JCI93868.
25. Wakabayashi T, Naito H, Suehiro JI, Lin Y, Kawaji H, Iba T, Kouno T, Ishikawa-Kato S, Furuno M, Takara K, Muramatsu F, Weizhen J, Kidoya H, Ishihara K, Hayashizaki Y, Nishida K, Yoder MC, Takakura N. CD157 marks tissue-resident endothelial stem cells with homeostatic and regenerative properties // Cell Stem Cell. 2018;22:384–397.e6. Doi: 10.1016/j.stem.2018.01.010.
26. Li Z, Solomonidis EG, Meloni M, Taylor RS, Duffin R, Dobie R, Magalhaes MS, Henderson BEP, Louwe PA, D’Amico G, Hodivala-Dilke KM, Shah AM, Mills NL, Simons BD, Gray GA, Henderson NC, Baker AH, Brittan M. Single-cell transcriptome analyses reveal novel targets modulating cardiac neovascularization by resident endothelial cells following myocardial infarction // Eur Heart J. 2019;40(30):2507–2520. Doi: 10.1093/eurheartj/ehz305.
27. Schupp JC, Adams TS, Cosme C Jr, Raredon MSB, Yuan Y, Omote N, Poli S, Chioccioli M, Rose KA, Manning EP, Sauler M, DeIuliis G, Ahangari F, Neumark N, Habermann AC, Gutierrez AJ, Bui LT, Lafyatis R, Pierce RW, Meyer KB, Nawijn MC, Teichmann SA, Banovich NE, Kropski JA, Niklason LE, Pe’er D, Yan X, Homer RJ, Rosas IO, Kaminski N. Integrated Single-Cell Atlas of Endothelial Cells of the Human Lung // Circulation. 2021;144(4):286–302. Doi: 10.1161/CIRCULATIONAHA.120.052318.
28. Rafii S, Butler JM, Ding BS. Angiocrine functions of organ-specific endothelial cells // Nature. 2016;529(7586):316– 325. Doi: 10.1038/nature17040.
29. Yoder MC. Endothelial stem and progenitor cells (stem cells): (2017 Grover conference series) // Pulm Circ. 2018;8(1):2045893217743950. Doi: 10.1177/ 2045893217 743950.
30. Harb R, Xie G, Lutzko C, Guo Y, Wang X, Hill CK et al. Bone marrow progenitor cells repair rat hepatic sinusoidal endothelial cells after liver injury // Gastroenterology. 2009; 137(2):704–712. Doi: 10.1053/j.gastro.2009.05.009.
31. Poisson J, Lemoinne S, Boulanger C, Durand F, Moreau R, Valla D, Rautou PE. Liver sinusoidal endothelial cells: Physiology and role in liver diseases // J Hepatol. 2017; 66(1):212–227. Doi: 10.1016/j.jhep.2016.07.009.
32. Wang L, Wang X, Xie G, Wang L, Hill CK, DeLeve LD. Liver sinusoidal endothelial cell progenitor cells promote liver regeneration in rats // J Clin Invest. 2012;122(4):1567–1573. Doi: 10.1172/JCI58789.
33. Chen C, Dai P, Nan L, Lu R, Wang X, Tian Y, Zhang X, Gao Y, Zheng S, Zhang Y. Isolation and characterization of endothelial progenitor cells from canine bone marrow // Biotech Histochem. 2021;96(2):85–93. Doi: 10.1080/10520295. 2020.1762001.
34. Ricottini E, Madonna R, Grieco D, Zoccoli A, Stampachiacchiere B, Patti G, Tonini G, De Caterina R, Di Sciascio G. Effect of high-dose atorvastatin reload on the release of endothelial progenitor cells in patients on long-term statin treatment who underwent percutaneous coronary intervention (from the ARMYDA-EPC Study) // Am J Cardiol. 2016;117(2):165–171. Doi: 10.1016/j.amjcard.2015.10.043.
35. Medina RJ, Barber CL, Sabatier F, Dignat-George F, Melero-Martin JM, Khosrotehrani K, Ohneda O, Randi AM, Chan JKY, Yamaguchi T, Van Hinsbergh VWM, Yoder MC, Stitt AW. Endothelial Progenitors: A Consensus Statement on Nomenclature // Stem Cells Transl Med. 2017;6(5):1316–1320. Doi: 10.1002/sctm.16-0360.
36. Evans CE, Iruela-Arispe ML, Zhao YY. Mechanisms of Endothelial Regeneration and Vascular Repair and Their Application to Regenerative Medicine // Am J Pathol. 2021; 191(1):52–65. Doi: 10.1016/j.ajpath.2020.10.001.
37. Wang T, Zang G, Zhang L, Sun Z, Liu J, Hou L, Wang Z. Role of Pericytes in Diabetic Angiogenesis // J Cardiovasc Pharmacol. 2022;79(1):e1–e10. Doi: 10.1097/FJC. 0000000000001147.
38. Felmeden DC, Blann AD, Lip GY. Angiogenesis: basic pathophysiology and implications for disease // Eur Heart J. 2003;24(7):586–603. Doi: 10.1016/s0195-668x(02)00635-8.
39. Minoshima A, Kabara M, Matsuki M et al. Pericyte-specific Ninjurin1 deletion attenuates vessel maturation and blood flow recovery in hind limb ischemia // Arterioscler Thromb Vasc Biol. 2018;38(10):2358–2370. Doi: 10.1161/ ATVBAHA.118.311375.
40. Špiranec Spes K, Hupp S, Werner F et al. Natriuretic peptides attenuate retinal pathological neovascularization via cyclic guanosine monophosphate signaling in pericytes and astrocytes // Arterioscler Thromb Vasc Biol. 2020;40(1):159– 174. Doi: 10.1161/ATVBAHA.119.313400.
41. He S, Sharpless NE. Senescence in Health and Disease // Cell. 2017;169(6):1000–1011. Doi: 10.1016/j.cell.2017.05.015.
42. Ritschka B, Storer M, Mas A, Heinzmann F, Ortells MC, Morton JP, Sansom OJ, Zender L, Keyes WM. The senescence-associated secretory phenotype induces cellular plasticity and tissue regeneration // Genes Dev. 2017;31(2):172– 183. Doi: 10.1101/gad.290635.116.
43. Schmitt CA, Wang B, Demaria M. Senescence and cancer – role and therapeutic opportunities. Nat Rev Clin Oncol. 2022;19(10):619–636. Doi: 10.1038/s41571-022-00668-4.
44. Ferrucci L, Kuchel GA. Heterogeneity of Aging: Individual Risk Factors, Mechanisms, Patient Priorities, and Outcomes // J Am Geriatr Soc. 2021;69(3):610–612. Doi: 10.1111/jgs.17011.
45. Martínez-Zamudio RI, Robinson L, Roux PF, Bischof O. SnapShot: Cellular Senescence in Pathophysiology // Cell. 2017;170(5):1044–1044.e1. Doi: 10.1016/j.cell.2017.08.025.
46. Uryga AK, Bennett MR. Ageing induced vascular smooth muscle cell senescence in atherosclerosis // J Physiol. 2016;8(594):2115–2124. Doi: 10.1113/JP270923.
47. Nagane M, Yasui H, Kuppusamy P, Yamashita T, Inanami O. DNA damage response in vascular endothelial senescence: Implication for radiation-induced cardiovascular diseases // J Radiat Res. 2021;62(4):564–573. Doi: 10.1093/ jrr/rrab032.
48. Kress JM, Dio LD, Heck L, Pulliero A, Izzotti A, Laarmann K, Fritz G, Kaina B. Human primary endothelial cells are impaired in nucleotide excision repair and sensitive to benzo[a]pyrene compared with smooth muscle cells and pericytes // Sci Rep. 2019;9(1):13800. Doi: 10.1038/s41598-019- 49953-w.
49. Nepali PR, Haimovitz-Friedman A. Chemotherapeutic Agents-Induced Ceramide-Rich Platforms (CRPs) in Endothelial Cells and Their Modulation // Methods Mol Biol. 2021;2187:215–221. Doi: 10.1007/978-1-0716-0814-2_12.
50. Brunt VE, Gioscia-Ryan RA, Richey JJ, Zigler MC, Cuevas LM, Gonzalez A, Vázquez-Baeza Y, Battson ML, Smithson AT, Gilley AD, Ackermann G, Neilson AP, Weir T, Davy KP, Knight R, Seals DR. Suppression of the gut microbiome ameliorates age-related arterial dysfunction and oxidative stress in mice // J Physiol. 2019;597(9):2361–2378. Doi: 10.1113/ JP277336.
51. Jia G, Habibi J, Aroor AR, Hill MA, DeMarco VG, Lee LE, Ma L, Barron BJ, Whaley-Connell A, Sowers JR. Enhanced endothelium epithelial sodium channel signaling prompts left ventricular diastolic dysfunction in obese female mice // Metabolism. 2018;78:69–79. Doi: 10.1016/j.metabol. 2017.08.008.
52. Abbas M, Jesel L, Auger C, Amoura L, Messas N, Manin G, Rumig C, Leon-Gonzalez AJ, Ribeiro TP, Silva GC, AbouMerhi R, Hamade E, Hecker M, Georg Y, Chakfe N, Ohlmann P, Schini-Kerth VB, Toti F, Morel O. Endothelial Microparticles From Acute Coronary Syndrome Patients Induce Premature Coronary Artery Endothelial Cell Aging and Thrombogenicity: Role of the Ang II/AT1 Receptor/NADPH Oxidase-Mediated Activation of MAPKs and PI3-Kinase Pathways // Circulation. 2017;135(3):280–296. Doi: 10.1161/CIRCULATIONAHA.116.017513.
53. Franceschi C, Campisi J. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases // J Gerontol A Biol Sci Med Sci. 2014;69(Suppl 1):S4–S9. Doi: 10.1093/gerona/glu057.
54. Rodriguez JE, Naigeon M, Goldschmidt V, Roulleaux Dugage M, Seknazi L, Danlos FX, Champiat S, Marabelle A, Michot JM, Massard C, Besse B, Ferrara R, Chaput N, Baldini C. Immunosenescence, inflammaging, and cancer immunotherapy efficacy // Expert Rev Anticancer Ther. 2022;22(9):915– 926. Doi: 10.1080/14737140.2022.2098718.
55. Coppé JP, Desprez PY, Krtolica A, Campisi J. The senescence-associated secretory phenotype: the dark side of tumor suppression // Annu Rev Pathol. 2010;5:99–118. Doi: 10.1146/annurev-pathol-121808-102144.
56. Власов Т.Д., Нестерович И.И., Шиманьски Д.А. Эндотелиальная дисфункция: от частного к общему. Возврат к «старой парадигме»? // Регионарное кровообращение и микроциркуляция. – 2019. – Т. 18, № 2. – С. 19– 27. Doi: 10.24884/1682- 6655-2019-18-2-19-27.
57. Khan SY, Awad EM, Oszwald A, Mayr M, Yin X, Waltenberger B, Stuppner H, Lipovac M, Uhrin P, Breuss JM. Premature senescence of endothelial cells upon chronic exposure to TNFα can be prevented by N-acetyl cysteine and plumericin // Sci Rep. 2017;7:39501. Doi: 10.1038/srep39501.
58. Gu Y, Vorburger R, Scarmeas N, Luchsinger JA, Manly JJ, Schupf N, Mayeux R, Brickman AM. Circulating inflammatory biomarkers in relation to brain structural measurements in a non-demented elderly population // Brain Behav Immun. 2017;65:150–160. Doi: 10.1016/j.bbi.2017.04.022.
59. Graves SI, Baker DJ. Implicating endothelial cell senescence to dysfunction in the ageing and diseased brain // Basic Clin Pharmacol Toxicol. 2020;127(2):102–110. Doi: 10.1111/bcpt.13403.
60. Villacorta L, Chang L. The role of perivascular adipose tissue in vasoconstriction, arterial stiffness, and aneurysm // Horm Mol Biol Clin Investig. 2015;21(2):137–147. Doi: 10.1515/hmbci-2014-0048.
61. Chaudhary K, Malhotra K, Sowers J, Aroor A. Uric Acid - key ingredient in the recipe for cardiorenal metabolic syndrome // Cardiorenal Med. 2013;3(3):208–220. Doi: 10.1159/000355405.
62. Canepa M, Viazzi F, Strait JB, Ameri P, Pontremoli R, Brunelli C, Studenski S, Ferrucci L, Lakatta EG, AlGhatrif M. Longitudinal Association Between Serum Uric Acid and Arterial Stiffness: Results From the Baltimore Longitudinal Study of Aging // Hypertension. 2017;69(2):228–235. Doi: 10.1161/ HYPERTENSIONAHA.116.08114.
63. Aroor AR, Jia G, Habibi J, Sun Z, Ramirez-Perez FI, Brady B, Chen D, Martinez-Lemus LA, Manrique C, Nistala R, Whaley-Connell AT, Demarco VG, Meininger GA, Sowers JR. Uric acid promotes vascular stiffness, maladaptive inflammatory responses and proteinuria in western diet fed mice // Metabolism. 2017;74:32–40. Doi: 10.1016/j.metabol.2017.06.006.
64. Shosha E, Xu Z, Narayanan SP, Lemtalsi T, Fouda AY, Rojas M, Xing J, Fulton D, Caldwell RW, Caldwell RB. Mechanisms of Diabetes-Induced Endothelial Cell Senescence: Role of Arginase 1 // Int J Mol Sci. 2018;19(4):1215. Doi: 10.3390/ ijms19041215.
65. Wang G, Han B, Zhang R, Liu Q, Wang X, Huang X, Liu D, Qiao W, Yang M, Luo X, Hou J, Yu B. C1q/TNF-Related Protein 9 Attenuates Atherosclerosis by Inhibiting Hyperglycemia-Induced Endothelial Cell Senescence Through the AMPKα/KLF4 Signaling Pathway // Front Pharmacol. 2021;12:758792. Doi: 10.3389/fphar.2021.758792.
66. Kim MY, Kang ES, Ham SA, Hwang JS, Yoo TS, Lee H, Paek KS, Park C, Lee HT, Kim JH, Han CW, Seo HG. The PPARδ-mediated inhibition of angiotensin II-induced premature senescence in human endothelial cells is SIRT1-dependent // Biochem Pharmacol. 2012;84(12):1627–1634. Doi: 10.1016/j.bcp.2012.09.008.
67. de Cavanagh EM, Piotrkowski B, Basso N, Stella I, Inserra F, Ferder L, Fraga CG. Enalapril and losartan attenuate mitochondrial dysfunction in aged rats // FASEB J. 2003; 17(9):1096–1098. Doi: 10.1096/fj.02-0063fje.
68. Basso N, Paglia N, Stella I, de Cavanagh EM, Ferder L, del Rosario Lores Arnaiz M, Inserra F. Protective effect of the inhibition of the renin-angiotensin system on aging // Regul Pept. 2005;128(3):247–252. Doi: 10.1016/j. regpep.2004.12.027.
69. Kusche-Vihrog K, Jeggle P, Oberleithner H. The role of ENaC in vascular endothelium // Pflugers Arch. 2014; 466(5):851–859. Doi: 10.1007/s00424-013-1356-3.
70. Rossman MJ, Kaplon RE, Hill SD, McNamara MN, Santos-Parker JR, Pierce GL, Seals DR, Donato AJ. Endothelial cell senescence with aging in healthy humans: prevention by habitual exercise and relation to vascular endothelial function // Am J Physiol Heart Circ Physiol. 2017;313(5):H890– H895. Doi: 10.1152/ajpheart.00416.2017.
71. Okuda K, Khan MY, Skurnick J, Kimura M, Aviv H, Aviv A. Telomere attrition of the human abdominal aorta: relationships with age and atherosclerosis // Atherosclerosis. 2000; 152(2):391–398. Doi: 10.1016/s0021-9150(99)00482-7.
72. Martínez-Zamudio RI, Robinson L, Roux PF, Bischof O. SnapShot: Cellular Senescence Pathways // Cell. 2017; 170(4):816–816.e1. Doi: 10.1016/j.cell.2017.07.049.
73. Bhayadia R, Schmidt BM, Melk A, Hömme M. Senescence-Induced Oxidative Stress Causes Endothelial Dysfunction // J Gerontol A Biol Sci Med Sci. 2016;71(2):161–169. Doi: 10.1093/gerona/glv008.
74. Holdt LM, Sass K, Gäbel G, Bergert H, Thiery J, Teupser D. Expression of Chr9p21 genes CDKN2B (p15(INK4b)), CDKN2A (p16(INK4a), p14(ARF)) and MTAP in human atherosclerotic plaque // Atherosclerosis. 2011;214(2):264–270. Doi: 10.1016/j.atherosclerosis.2010.06.029.
75. Morgan RG, Ives SJ, Lesniewski LA, Cawthon RM, Andtbacka RH, Noyes RD, Richardson RS, Donato AJ. Age-related telomere uncapping is associated with cellular senescence and inflammation independent of telomere shortening in human arteries // Am J Physiol Heart Circ Physiol. 2013;305(2):H251–H258. Doi: 10.1152/ajpheart. 00197.2013.
76. Sung JY, Lee KY, Kim JR, Choi HC. Interaction between mTOR pathway inhibition and autophagy induction attenuates adriamycin-induced vascular smooth muscle cell senescence through decreased expressions of p53/p21/p16 // Exp Gerontol. 2018;109:51–58. Doi: 10.1016/j.exger.2017.08.001.
77. Yue Z, Rong J, Ping W, Bing Y, Xin Y, Feng LD, Yaping W. Gene expression of the p16(INK4a)-Rb and p19(Arf)- p53-p21(Cip/Waf1) signaling pathways in the regulation of hematopoietic stem cell aging by ginsenoside Rg1 // Genet Mol Res. 2014;13(4):10086–10096. Doi: 10.4238/2014.
78. Beekman M, Blanché H, Perola M, Hervonen A, Bezrukov V, Sikora E, Flachsbart F, Christiansen L, De Craen AJ, Kirkwood TB, Rea IM, Poulain M, Robine JM, Valensin S, Stazi MA, Passarino G, Deiana L, Gonos ES, Paternoster L, Sørensen TI, Tan Q, Helmer Q, van den Akker EB, Deelen J, Martella F, Cordell HJ, Ayers KL, Vaupel JW, Törnwall O, Johnson TE, Schreiber S, Lathrop M, Skytthe A, Westendorp RG, Christensen K, Gampe J, Nebel A, Houwing-Duistermaat JJ, Slagboom PE, Franceschi C; GEHA consortium. Genome-wide linkage analysis for human longevity: Genetics of Healthy Aging Study // Aging Cell. 2013;12(2):184–193. Doi: 10.1111/acel.12039.
79. Mun GI, Lee SJ, An SM, Kim IK, Boo YC. Differential gene expression in young and senescent endothelial cells under static and laminar shear stress conditions // Free Radic Biol Med. 2009;47(3):291–299. Doi: 10.1016/j.freeradbiomed. 2009.04.032.
80. Yamaga M, Takemoto M, Shoji M, Sakamoto K, Yamamoto M, Ishikawa T, Koshizaka M, Maezawa Y, Kobayashi K, Yokote K. Werner syndrome: a model for sarcopenia due to accelerated aging // Aging (Albany NY). 2017;9(7):1738–1744. Doi: 10.18632/aging.101265.
81. Martinet W, Knaapen MW, De Meyer GR, Herman AG, Kockx MM. Elevated levels of oxidative DNA damage and DNArepair enzymes in human atherosclerotic plaques // Circulation. 2002;106(8):927–932. Doi: 10.1161/01.cir.0000026393. 47805.21.
82. Okuda K, Khan MY, Skurnick J, Kimura M, Aviv H, Aviv A. Telomere attrition of the human abdominal aorta: relationships with age and atherosclerosis // Atherosclerosis. 2000;152(2):391–398. Doi: 10.1016/s0021-9150 (99)00482-7.
83. Carracedo J, Merino A, Briceno C, Soriano S, Buendia P,Calleros L, Rodriguez M, Martin-Malo A, Aljama P &Ramirez R (2011). Carbamylated low-density lipoprotein induces oxidative stress and accelerated senescence in human endothelial progenitor cells // FASEB J. 2011;25(4):1314– 1322. Doi: 10.1096/fj.10-173377.
84. Minamino T, Miyauchi H, Yoshida T, Ishida Y, Yoshida H, Komuro I. Endothelial cell senescence in human atherosclerosis: role of telomere in endothelial dysfunction // Circulation. 2002;105(13):1541–1544. Doi: 10.1161/01. cir.0000013836.85741.17.
85. Matrone G, Thandavarayan RA, Walther BK, Meng S, Mojiri A, Cooke JP. Dysfunction of iPSC-derived endothelial cells in human Hutchinson-Gilford progeria syndrome // Cell Cycle. 2019;18(19):2495–2508. Doi: 10.1080/ 15384101.2019.1651587.
86. Eitan E, Tichon A, Gazit A, Gitler D, Slavin S, Priel E. Novel telomerase-increasing compound in mouse brain delays the onset of amyotrophic lateral sclerosis // EMBO Mol Med. 2012;4(4):313–329. Doi: 10.1002/emmm.201200212.
87. Tripathi V, Shen Z, Chakraborty A, Giri S, Freier SM, Wu X, Zhang Y, Gorospe M, Prasanth SG, Lal A, Prasanth KV. Long noncoding RNA MALAT1 controls cell cycle progression by regulating the expression of oncogenic transcription factor B-MYB // PLoS Genet. 2013;9(3):e1003368. Doi: 10.1371/ journal.pgen.1003368.
88. Bianchessi V, Badi I, Bertolotti M, Nigro P, D’Alessandra Y, Capogrossi MC, Zanobini M, Pompilio G, Raucci A, Lauri A. The mitochondrial lncRNA ASncmtRNA-2 is induced in aging and replicative senescence in Endothelial Cells // J Mol Cell Cardiol. 2015;81:62–70. Doi: 10.1016/j. yjmcc.2015.01.012.
89. Ghebre YT, Yakubov E, Wong WT, Krishnamurthy P, Sayed N, Sikora AG, Bonnen MD. Vascular Aging: Implications for Cardiovascular Disease and Therapy // Transl Med (Sunnyvale). 2016;6(4):183. Doi: 10.4172/2161-1025.1000183.
90. Boon RA, Seeger T, Heydt S, Fischer A, Hergenreider E, Horrevoets AJ, Vinciguerra M, Rosenthal N, Sciacca S, Pilato M, van Heijningen P, Essers J, Brandes RP, Zeiher AM, Dimmeler S. MicroRNA-29 in aortic dilation: implications for aneurysm formation // Circ Res. 2011;109(10):1115–1119. Doi: 10.1161/CIRCRESAHA.111.255737.
91. Fraineau S, Palii CG, Allan DS, Brand M. Epigenetic regulation of endothelial-cell-mediated vascular repair // FEBS J. 2015;282(9):1605–1629. Doi: 10.1111/febs.13183.
92. Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development // Cell. 1999;99(3):247– 257. Doi: 10.1016/s0092-8674(00)81656-6.
93. Cencioni C, Spallotta F, Martelli F, Valente S, Mai A, Zeiher AM, Gaetano C. Oxidative stress and epigenetic regulation in ageing and age-related diseases // Int J Mol Sci. 2013;14(9):17643–17663. Doi: 10.3390/ijms140917643.
94. Lagarkova MA, Volchkov PY, Philonenko ES, Kiselev SL. Efficient differentiation of hESCs into endothelial cells in vitro is secured by epigenetic changes // Cell Cycle. 2008; 7(18):2929–2935. Doi: 10.4161/cc.7.18.6700.
95. Zeng L, Xiao Q, Margariti A, Zhang Z, Zampetaki A, Patel S, Capogrossi MC, Hu Y, Xu Q. HDAC3 is crucial in shear- and VEGF-induced stem cell differentiation toward endothelial cells // J Cell Biol. 2006;174(7):1059–1069. Doi: 10.1083/jcb.200605113.
96. Illi B, Scopece A, Nanni S, Farsetti A, Morgante L, Biglioli P, Capogrossi MC, Gaetano C. Epigenetic histone modification and cardiovascular lineage programming in mouse embryonic stem cells exposed to laminar shear stress // Circ Res. 2005;96(5):501–508. Doi: 10.1161/01.RES.0000159181. 06379.63.
97. Ungvari Z, Labinskyy N, Gupte S, Chander PN, Edwards JG, Csiszar A. Dysregulation of mitochondrial biogenesis in vascular endothelial and smooth muscle cells of aged rats // Am J Physiol Heart Circ Physiol. 2008;294(5):H2121– H2128. Doi: 10.1152/ajpheart.00012.2008.
98. Scull CM, Tabas I. Mechanisms of ER stress-induced apoptosis in atherosclerosis // Arterioscler Thromb Vasc Biol. 2011;31(12):2792–2797. Doi: 10.1161/ATVBAHA.111.224881.
99. Laurindo FR, Araujo TL, Abrahão TB. Nox NADPH oxidases and the endoplasmic reticulum // Antioxid Redox Signal. 2014;20(17):2755–2775. Doi: 10.1089/ars.2013.5605.
100. Wan YZ, Gao P, Zhou S, Zhang ZQ, Hao DL, Lian LS, Li YJ, Chen HZ, Liu DP. SIRT1-mediated epigenetic downregulation of plasminogen activator inhibitor-1 prevents vascular endothelial replicative senescence // Aging Cell. 2014; 13(5):890–899. Doi: 10.1111/acel.12247.
101. Navarro-González JF, Donate-Correa J, Muros de Fuentes M, Pérez-Hernández H, Martínez-Sanz R, Mora-Fernández C. Reduced Klotho is associated with the presence and severity of coronary artery disease // Heart. 2014; 100(1):34–40. Doi: 10.1136/heartjnl-2013-304746.
102. Kurosu H, Yamamoto M, Clark JD, Pastor JV, Nandi A, Gurnani P, McGuinness OP, Chikuda H, Yamaguchi M, Kawaguchi H, Shimomura I, Takayama Y, Herz J, Kahn CR, Rosenblatt KP, Kuro-o M. Suppression of aging in mice by the hormone Klotho // Science. 2005;309(5742):1829–1833. Doi: 10.1126/science.1112766.
103. Wang XM, Xiao H, Liu LL, Cheng D, Li XJ, Si LY. FGF21 represses cerebrovascular aging via improving mitochondrial biogenesis and inhibiting p53 signaling pathway in an AMPK-dependent manner // Exp Cell Res. 2016; 346(2):147–156. Doi: 10.1016/j.yexcr.2016.06.020.
104. Савицкий Д.В., Линькова Н.С., Кветной И.М. и др. Cекреторный фенотип эндотелиоцитов человека, ассоциированный с репликативным и индуцированным старением // Успехи геронтол. – 2022. – Т. 35, № 4. – С. 478– 484.
105. Jerafi-Vider A, Bassi I, Moshe N, Tevet Y, Hen G, Splittstoesser D, Shin M, Lawson ND, Yaniv K. VEGFC/ FLT4-induced cell-cycle arrest mediates sprouting and differentiation of venous and lymphatic endothelial cells // Cell Rep. 2021;35(11):109255. Doi: 10.1016/j.celrep.2021.109255.
106. Chan GH, Chan E, Kwok CT, Leung GP, Lee SM, Seto SW. The role of p53 in the alternation of vascular functions // Front Pharmacol. 2022;13:981152. Doi: 10.3389/fphar. 2022.981152.
107. Baar MP, Brandt RMC, Putavet DA, Klein JDD, Derks KWJ, Bourgeois BRM, Stryeck S, Rijksen Y, van Willigenburg H, Feijtel DA, van der Pluijm I, Essers J, van Cappellen WA, van IJcken WF, Houtsmuller AB, Pothof J, de Bruin RWF, Madl T, Hoeijmakers JHJ, Campisi J, de Keizer PLJ. Targeted Apoptosis of Senescent Cells Restores Tissue Homeostasis in Response to Chemotoxicity and Aging // Cell. 2017;169(1):132–147.e16. Doi: 10.1016/j. cell.2017.02.031.
108. Lin JR, Shen WL, Yan C, Gao PJ. Downregulation of dynamin-related protein 1 contributes to impaired autophagic flux and angiogenic function in senescent endothelial cells // Arterioscler Thromb Vasc Biol. 2015;35(6):1413–1422. Doi: 10.1161/ATVBAHA.115.305706.
109. Tai H, Wang Z, Gong H, Han X, Zhou J, Wang X, Wei X, Ding Y, Huang N, Qin J, Zhang J, Wang S, Gao F, Chrzanowska-Lightowlers ZM, Xiang R, Xiao H. Autophagy impairment with lysosomal and mitochondrial dysfunction is an important characteristic of oxidative stress-induced senescence // Autophagy. 2017;13(1):99–113. Doi: 10.1080/ 15548627.2016.1247143.
110. Heiss C, Keymel S, Niesler U, Ziemann J, Kelm M, Kalka C. Impaired progenitor cell activity in age-related endothelial dysfunction // J Am Coll Cardiol. 2005;45(9):1441– 1448. Doi: 10.1016/j.jacc.2004.12.074.
111. Coppé JP, Patil CK, Rodier F, Sun Y, Muñoz DP, Goldstein J, Nelson PS, Desprez PY, Campisi J. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor // PLoS Biol. 2008;6(12):2853–2868. Doi: 10.1371/journal. pbio.0060301.
112. González-Gualda E, Baker AG, Fruk L, Muñoz-Espín D. A guide to assessing cellular senescence in vitro and in vivo // FEBS J. 2021;288(1):56–80. Doi: 10.1111/febs.15570.
113. Yamazaki Y, Baker DJ, Tachibana M, Liu CC, van Deursen JM, Brott TG, Bu G, Kanekiyo T. Vascular Cell Senescence Contributes to Blood-Brain Barrier Breakdown // Stroke. 2016;47(4):1068–1077. Doi: 10.1161/STROKEAHA.115.010835.
114. Elahy M, Jackaman C, Mamo JC, Lam V, Dhaliwal SS, Giles C, Nelson D, Takechi R. Blood-brain barrier dysfunction developed during normal aging is associated with inflammation and loss of tight junctions but not with leukocyte recruitment // Immun Ageing. 2015;12:2. Doi: 10.1186/ s12979-015-0029-9.
115. Parikh SM. The Angiopoietin-Tie2 Signaling Axis in Systemic Inflammation // J Am Soc Nephrol. 2017;28(7):1973– 1982. Doi: 10.1681/ASN.2017010069.
116. Wagatsuma A. Effect of aging on expression of angiogenesis-related factors in mouse skeletal muscle // Exp Gerontol. 2006;41(1):49–54. Doi: 10.1016/j.exger.2005.10.003.
117. Zhao L, Chen R, Qiu J, Huang Y, Lian C, Zhu X, Cui J, Wang S, Wang S, Hu Z, Wang J. CircCRIM1 Ameliorates Endothelial Cell Angiogenesis in Aging through the miR-455- 3p/Twist1/VEGFR2 Signaling Axis // Oxid Med Cell Longev. 2022;2022:2062885. Doi: 10.1155/2022/2062885.
118. Zhang M, Jiang L. Oxidized low-density lipoprotein decreases VEGFR2 expression in HUVECs and impairs angiogenesis // Exp Ther Med. 2016;12(6):3742–3748. Doi: 10.3892/etm.2016.3823.
119. Li Y, Kračun D, Dustin CM, El Massry M, Yuan S, Goossen CJ, DeVallance ER, Sahoo S, St Hilaire C, Gurkar AU, Finkel T, Straub AC, Cifuentes-Pagano E, Pagano PJ. Forestalling age-impaired angiogenesis and blood flow by targeting NOX: Interplay of NOX1, IL-6, and SASP in propagating cell senescence // Proc Natl Acad Sci U S A. 2021; 118(42):e2015666118. Doi: 10.1073/pnas.2015666118.
120. Piper B, Bogamuwa S, Hossain T, Farkas D, Rosas L, Green A, Newcomb G, Sun N, Horowitz JC, Bhagwani AR, Yang H, Kudryashova TV, Rojas M, Mora AL, Yan P, Mallampalli RK, Goncharova EA, Eckmann DM, Farkas L. RAB7 deficiency impairs pulmonary artery endothelial function and promotes pulmonary hypertension // bioRxiv [Preprint]. 2023;2023.02.03.526842. Doi: 10.1101/2023.02.03.526842.
121. Arrigoni C, Ostano P, Bersini S, Crippa M, Colombo MV, Gilardi M, Zagra L, Mello-Grand M, Gregnanin I, Ghilardi C, Bani MR, Candrian C, Chiorino G, Moretti M. Differential angiogenesis of bone and muscle endothelium in aging and inflammatory processes // Commun Biol. 2023; 6(1):126. Doi: 10.1038/s42003-023-04515-9.
122. Alavi P, Rathod AM, Jahroudi N. Age-Associated Increase in Thrombogenicity and Its Correlation with von Willebrand Factor // J Clin Med. 2021;10(18):4190. Doi: 10.3390/ jcm10184190.
123. Sepúlveda C, Palomo I, Fuentes E. Mechanisms of endothelial dysfunction during aging: Predisposition to thrombosis // Mech Ageing Dev. 2017;164:91–99. Doi: 10.1016/j. mad.2017.04.011.
124. Akrivou D, Perlepe G, Kirgou P, Gourgoulianis KI, Malli F. Pathophysiological Aspects of Aging in Venous Thromboembolism: An Update // Medicina (Kaunas). 2022; 58(8):1078. Doi: 10.3390/medicina58081078.
125. Gleerup G, Winther K. The effect of ageing on platelet function and fibrinolytic activity. Angiology. 1995;46(8):715– 718. Doi: 10.1177/000331979504600810.
126. Donato AJ, Morgan RG, Walker AE, Lesniewski LA. Cellular and molecular biology of aging endothelial cells // J Mol Cell Cardiol. 2015;89(Pt B):122–135. Doi: 10.1016/j. yjmcc.2015.01.021.
127. Schlaudecker J, Becker R. Inflammatory response and thrombosis in older individuals // Semin Thromb Hemost. 2014;40(6):669–674. Doi: 10.1055/s-0034-1387882.
128. McCafferty C, Busuttil-Crellin X, Cai T, Monagle P, Goldenberg NA, Ignjatovic V. Plasma Proteomic Analysis Reveals Age-Specific Changes in Platelet- and Endothelial Cell-Derived Proteins and Regulators of Plasma Coagulation and Fibrinolysis // J Pediatr. 2020;221S:S29-S36. Doi: 10.1016/j.jpeds.2020.01.051.
129. Bochenek ML, Schütz E, Schäfer K. Endothelial cell senescence and thrombosis: Ageing clots // Thromb Res. 2016; 147:36–45. Doi: 10.1016/j.thromres.2016.09.019.
130. Somanath PR, Podrez EA, Chen J, Ma Y, Marchant K, Antoch M, Byzova TV. Deficiency in core circadian protein Bmal1 is associated with a prothrombotic and vascular phenotype // J. Cell Physiol. 2011;226:132–140. Doi: 10.1002/jcp. 22314.
131. Dmitrieva NI, Burg MB. Secretion of von Willebrand factor by endothelial cells links sodium to hypercoagulability and thrombosis // Proc Natl Acad Sci U S A. 2014; 111(17):6485–6490. Doi: 10.1073/pnas.1404809111.
132. Pal PB, Sonowal H, Shukla K, Srivastava SK, Ramana KV. Aldose Reductase Mediates NLRP3 Inflammasome-Initiated Innate Immune Response in Hyperglycemia-Induced Thp1 Monocytes and Male Mice. Endocrinology. 2017;158(10): 3661–3675. Doi: 10.1210/en.2017-00294.
133. Barcena ML, Aslam M, Pozdniakova S, Norman K, Ladilov Y. Cardiovascular Inflammaging: Mechanisms and Translational Aspects // Cells. 2022;11(6):1010. Doi: 10.3390/ cells11061010.
134. Duong L, Radley-Crabb HG, Gardner JK, Tomay F, Dye DE, Grounds MD, Pixley FJ, Nelson DJ, Jackaman C. Macrophage depletion in elderly mice improves response to tumor immunotherapy, increases anti-tumor T cell activity and reduces treatment-induced cachexia // Front Genet. 2018;9: 526. Doi: 10.3389/fgene.2018.00526.
135. Xu M, Pirtskhalava T, Farr JN, Weigand BM, Palmer AK, Weivoda MM, Inman CL, Ogrodnik MB, Hachfeld CM, Fraser DG, Onken JL, Johnson KO, Verzosa GC, Langhi LGP, Weigl M, Giorgadze N, LeBrasseur NK, Miller JD, Jurk D, Singh RJ, Allison DB, Ejima K, Hubbard GB, Ikeno Y, Cubro H, Garovic VD, Hou X, Weroha SJ, Robbins PD, Niedernhofer LJ, Khosla S, Tchkonia T, Kirkland JL. Senolytics improve physical function and increase lifespan in old age // Nat Med. 2018;24(8):1246–1256. Doi: 10.1038/s41591-018-0092-9.
136. Grosse L, Wagner N, Emelyanov A, Molina C, Lacas-Gervais S, Wagner KD, Bulavin DV. Defined p16High Senescent Cell Types Are Indispensable for Mouse Healthspan // Cell Metab. 2020;32(1):87–99.e6. Doi: 10.1016/j.cmet.2020. 05.002.
137. Yegorov YE, Poznyak AV, Nikiforov NG, Starodubova AV, Orekhov AN. Role of Telomeres Shortening in Atherogenesis: An Overview // Cells. 2021;10(2):395. Doi: 10.3390/ cells10020395.
138. Mojiri A, Walther BK, Jiang C, Matrone G, Holgate R, Xu Q, Morales E, Wang G, Gu J, Wang R, Cooke JP. Telomerase therapy reverses vascular senescence and extends lifespan in progeria mice // Eur Heart J. 2021;42(42):4352–4369. Doi: 10.1093/eurheartj/ehab547.
139. Vinci MC, Carulli E, Rurali E, Rinaldi R, Damiano G, Raucci A, Pompilio G, Genovese S. The Long Telling Story of “Endothelial Progenitor Cells”: Where Are We at Now? // Cells. 2022;12(1):112. Doi: 10.3390/cells12010112.
140. Li S, Sun J, Yang J, Yang Y, Ding H, Yu B, Ma K, Chen M. Gelatin methacryloyl (GelMA) loaded with concentrated hypoxic pretreated adipose-derived mesenchymal stem cells(ADSCs) conditioned medium promotes wound healing and vascular regeneration in aged skin // Biomater Res. 2023; 27(1):11. Doi: 10.1186/s40824-023-00352-3.
141. Zhou H, Yang D, Cheng HS, McCoy MG, Pérez-Cremades D, Haemmig S, Wong D, Chen L, Feinberg MW. miR181b regulates vascular endothelial aging by modulating an MAP3K3 signaling pathway // FASEB J. 2022;36(6):e22353. Doi: 10.1096/fj.202200046R.
142. Donato AJ, Morgan RG, Walker AE, Lesniewski LA. Cellular and molecular biology of aging endothelial cells // J Mol Cell Cardiol. 2015;89(Pt B):122–135. Doi: 10.1016/j. yjmcc.2015.01.021.
Рецензия
Для цитирования:
Власова Т.И., Петрищев Н.Н., Власов Т.Д. Эндотелий и старение: механизмы формирования сенесцентного фенотипа эндотелиальных клеток. Регионарное кровообращение и микроциркуляция. 2023;22(3):19-33. https://doi.org/10.24884/1682-6655-2023-22-3-19-33
For citation:
Vlasova T.I., Petrishchev N.N., Vlasov T.D. Endothelium and aging: mechanisms for formation of senescence associated phenotype of endothelial cells. Regional blood circulation and microcirculation. 2023;22(3):19-33. (In Russ.) https://doi.org/10.24884/1682-6655-2023-22-3-19-33