A relationship exists between replicative senescence and cardiovascular health

Springer Science and Business Media LLC - Tập 2 - Trang 1-13 - 2013
Maria E Karavassilis1, Richard Faragher
1School of Medicine, The Commonwealth Building, The Hammersmith Hospital, Imperial College London, London, UK

Tóm tắt

A growing body of evidence demonstrates that the accumulation of senescent cells is a plausible ageing mechanism. It has been proposed that the senescence of vascular cells plays a causal role in the development of cardiovascular pathologies. A key prediction arising from this hypothesis is that cultures of cells derived from donors with cardiovascular disease will show reduced in vitro replicative capacities compared to those derived from disease-free controls. Accordingly, we carried out a formal review of the relationship among donor age, cardiovascular health status and maximum population doubling level attained in vitro by cultures of vascular smooth muscle and endothelial cells. Data were available to us on a total of 202 independent cell cultures. An inverse relationship was found to exist between replicative capacity and donor age in both endothelial and vascular smooth muscle cells. Cultures derived from donors with cardiovascular disease showed a lower overall replicative potential than age-matched healthy controls. In general the replicative potential at the start of the lifespan was found to be higher in those individuals without disease than those with disease and the difference in average cumulative population doublings (CPDs) in age-matched individuals in the two groups remained roughly constant throughout the lifetime. These results are consistent with the model in which the inherited replicative capacity of vascular cells is a stronger determinant of the onset of cardiovascular disease later in life, than wear-and-tear throughout the life course.

Tài liệu tham khảo

Yang DG, Liu L, Zheng XY: Cyclin-dependent kinase inhibitor p16(INK4a) and telomerase may co-modulate endothelial progenitor cells senescence. Ageing Res Rev. 2008, 7: 137-146. 10.1016/j.arr.2008.02.001. Minamino T, Komuro I: Vascular aging: insights from studies on cellular senescence, stem cell aging, and progeroid syndromes. Nat Clin Pract Cardiovasc Med. 2008, 5: 637-648. 10.1038/ncpcardio1324. Matthews C, Gorenne I, Scott S, Figg N, Kirkpatrick P, Ritchie A, Goddard M, Bennett M: Vascular smooth muscle cells undergo telomere-based senescence in human atherosclerosis: effects of telomerase and oxidative stress. Circ Res. 2006, 99: 156-164. 10.1161/01.RES.0000233315.38086.bc. Burton DG, Giles PJ, Sheerin AN, Smith SK, Lawton JJ, Ostler EL, Rhys-Williams W, Kipling D, Faragher RG: Microarray analysis of senescent vascular smooth muscle cells: a link to atherosclerosis and vascular calcification. Exp Gerontol. 2009, 44: 659-665. 10.1016/j.exger.2009.07.004. Baker DJ, Wijshake T, Tchkonia T, LeBrasseur NK, Childs BG, van de Sluis B, Kirkland JL, van Deursen JM: Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature. 2011, 479: 232-236. 10.1038/nature10600. Martin GM, Sprague CA, Epstein CJ: Replicative lifespan of cultivated human cells. Effects of donor's age, tissue and genotype. Lab Invest. 1970, 23: 86-92. Schneider EL, Mitsui Y: The relationship between in vitro cellular aging and in vivo human age. Proc Natl Acad Sci U S A. 1976, 73: 3584-3588. 10.1073/pnas.73.10.3584. Goldstein S, Moerman EJ, Soeldner JS, Gleason RE, Barnett DM: Chronologic and physiologic age affect replicative life-span of fibroblasts from diabetic, prediabetic, and normal donors. Science. 1978, 199: 781-782. 10.1126/science.622567. Cristofalo VJ, Allen RG, Pignolo RJ, Martin BG, Beck JC: Relationship between donor age and the replicative lifespan of human cells in culture: a reevaluation. Proc Natl Acad Sci U S A. 1998, 95: 10614-10619. 10.1073/pnas.95.18.10614. Maier AB, Westendorp RG: Relation between replicative senescence of human fibroblasts and life history characteristics. Ageing Res Rev. 2009, 8: 237-243. 10.1016/j.arr.2009.01.004. Maier AB, le Cessie S, de Koning-Treurniet C, Blom J, Westendorp RG, van Heemst D: Persistence of high-replicative capacity in cultured fibroblasts from nonagerians. Aging Cell. 2007, 6: 27-33. 10.1111/j.1474-9726.2006.00263.x. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O: A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A. 1995, 92: 9363-9367. 10.1073/pnas.92.20.9363. Herbig U, Ferreira M, Condel L, Carey D, Sedivy JM: Cellular senescence in aging primates. Science. 2006, 311: 1257-10.1126/science.1122446. Li Y, Yan Q, Wolf NS: Long-term caloric restriction delays age-related decline in proliferation capacity of murine lens epithelial cells in vitro and in vivo. Invest Ophthalmol Vis Sci. 1997, 38: 100-107. Fenton M, Barker S, Kurz DJ, Erusalimsky JD: Cellular senescence after single and repeated balloon catheter denudations of rabbit carotid arteries. Arterioscler Thromb Vasc Biol. 2001, 21: 220-226. 10.1161/01.ATV.21.2.220. Aviv H, Khan MY, Skurnick J, Okuda K, Kimura M, Gardner J, Priolo L, Aviv A: Age dependent aneuploidy and telomere length of the human vascular endothelium. Atherosclerosis. 2001, 159: 281-287. 10.1016/S0021-9150(01)00506-8. Bennet MR, Evan GI, Schwartz SM: Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atherosclerotic plaques. J Clin Invest. 1995, 95: 2266-2274. 10.1172/JCI117917. Moyer CF, Sajuthi D, Tulli H, Williams JK: Synthesis of IL-1 alpha and IL-1 beta by arterial cells in atherosclerosis. Am J Pathol. 1991, 138: 951-960. Schneiderman J, Sawdey MS, Keeton MR, Bordin GM, Bernstein EF, Dilley RB, Loskutoff DJ: Increased type 1 plasminogen activator inhibitor gene expression in atherosclerotic human arteries. Proc Natl Acad Sci U S A. 1992, 89: 6998-7002. 10.1073/pnas.89.15.6998. van der Wal AC, Das PK, Tigges AJ, Becker AE: Adhesion molecules on the endothelium and mononuclear cells in human atherosclerotic lesions. Am J Pathol. 1992, 141: 1427-1433. Burton DG, Matsubara H, Ikeda K: Pathophysiology of vascular calcification: Pivotal role of cellular senescence in vascular smooth muscle cells. Exp Gerontol. 2010, 45: 819-824. 10.1016/j.exger.2010.07.005. Chang E, Harley CB: Telomere length and replicative aging in human vascular tissues. Proc Natl Acad Sci U S A. 1995, 92: 11190-11194. 10.1073/pnas.92.24.11190. Slagboom PE, Droog S, Boomsma DI: Genetic determination of telomere size in humans: a twin study of three age groups. Am J Hum Genet. 1994, 55: 876-882. Brouilette SW, Moore JS, McMahon AD, Thompson JR, Ford I, Shepherd J, Packard CJ, Samani NJ, West of Scotland Coronary Prevention Study Group: Telomere length, risk of coronary heart disease, and statin treatment in the West of Scotland Primary Prevention Study: a nested case–control study. Lancet. 2007, 369: 107-114. 10.1016/S0140-6736(07)60071-3. Cawthon R, Smith KR, O'Brien E, Sivatchenko A, Kerber RA: Association between telomere length in blood and mortality in people aged 60 years or older. Lancet. 2003, 361: 393-395. 10.1016/S0140-6736(03)12384-7. Ben-Porath I, Weinberg RA: The signals and pathways activating cellular senescence. Int J Biochem Cell Biol. 2005, 37: 961-976. 10.1016/j.biocel.2004.10.013. Toussaint O, Medrano EE, von Zglinicki T: Cellular and molecular mechanisms of stress-induced premature senescence (SIPS) of human diploid fibroblasts and melanocytes. Exp Gerontol. 2000, 35: 927-945. 10.1016/S0531-5565(00)00180-7. Eisenberg DT, Salpea KD, Kuzawa CW, Hayes MG, Humphries SE, European Atherosclerosis Research Study II Group: Substantial variation in qPCR measured mean blood telomere lengths in young men from eleven European countries. Am J Hum Biol. 2011, 23: 228-231. 10.1002/ajhb.21126. Hunt SC, Chen W, Gardner JP, Kimura M, Srinivasan SR, Eckfeldt JH, Berenson GS, Aviv A: Leukocyte telomeres are longer in African Americans than in whites: the National Heart, Lung, and Blood Institute Family Heart Study and the Bogalusa Heart Study. Aging Cell. 2008, 7: 451-458. 10.1111/j.1474-9726.2008.00397.x. Demerath E, Cameron N, Gillman MW, Towne B, Siervogel RM: Telomeres and telomerase in the fetal origins of cardiovascular disease: a review. Hum Biol. 2004, 76: 127-146. 10.1353/hub.2004.0018. Epel ES, Blackburn EH, Lin J, Dhabhar FS, Adler NE, Morrow JD, Cawthon RM: Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci U S A. 2004, 101: 17312-17315. 10.1073/pnas.0407162101. Kimura M, Cherkas LF, Kato BS, Demissie S, Hjelmborg JB, Brimacombe M, Cupples A, Hunkin JL, Gardner JP, Lu X, Cao X, Sastrasinh M, Province MA, Hunt SC, Christensen K, Levy D, Spector TD, Aviv A: Offspring’s Leukocyte telomere length, paternal age, and telomere elongation in sperm. PLoS Genet. 2008, 4: e37-10.1371/journal.pgen.0040037. Hayflick L: The limited in vitro lifetime of human diploid cell strains. Exp Cell Res. 1965, 37: 614-636. 10.1016/0014-4827(65)90211-9. Arking R: The Biology of Aging: Observations and Principles. 1998, Sunderland, MA, USA: Sinauer Associates, Inc, 2 Nakano-Kurimoto R, Ikeda K, Uraoka M, Nakagawa Y, Yutaka K, Koide M, Takahashi T, Matoba S, Yamada H, Okigaki M, Matsubara H: Replicative senescence of vascular smooth muscle cells enhances the calcification through initiating the osteoblastic transition. Am J Physiol Heart Circ Physiol. 2009, 297: H1673-1684. 10.1152/ajpheart.00455.2009. Hampel B, Fortschegger K, Ressler S, Chang MW, Unterluggauer H, Breitwieser A, Sommergruber W, Fitzky B, Lepperdinger G, Jansen-Dürr P, Voglauer R, Grillari J: Increased expression of extracellular proteins as a hallmark of human endothelial cell in vitro senescence. Exp Gerontol. 2006, 41: 474-481. 10.1016/j.exger.2006.03.001. Vogel G, Thorin-Trescases N, Farhat N, Nguyen A, Villeneuve L, Mamarbachi AM, Fortier A, Perrault LP, Carrier M, Thorin E: Cellular senescence in endothelial cells from atherosclerotic patients is acceleration by oxidative stress associated with cardiovascular risk factors. Mech Ageing Dev. 2007, 128: 662-671. 10.1016/j.mad.2007.09.006. Hastings R, Qureshi M, Verma R, Lacy PS, Williams B: Telomere attrition and accumulation of senescent cells in cultured human endothelial cells. Cell Prolif. 2004, 37: 317-324. 10.1111/j.1365-2184.2004.00315.x. Garton KJ, Ferri N, Raines EW: Efficient expression of exogenous genes in primary vascular cells using IRES-based retroviral vectors. Biotechniques. 2002, 32: 830-834. Holley RW, Kiernan JA: Control of the initiation of DNA synthesis in 3T3 cells: Low-molecular-weight nutrients. Proc Nat Acad Sci U S A. 1974, 71: 2942-2945. 10.1073/pnas.71.8.2942. Watkins MT, Sharefkin JB, Zajtchuk R, Maciag TM, D'Amore PA, Ryan US, Van Wart H, Rich NM: Adult human saphenous vein endothelial cells: assessment of their reproductive capacity for Use in endothelial seeding of vascular prostheses. J Surg Res. 1983, 36: 588-596. Fukai N, Aoyagi M, Yamamoto M, Sakamoto H, Ogami K, Matsushima Y, Yamamoto K: Human arterial smooth muscle cell strains derived from patients with moyamoya disease: changes in biological characteristics and proliferative response during cellular ageing in vitro. Mech Ageing Dev. 1994, 75: 21-33. 10.1016/0047-6374(94)90025-6. Roach MR, Smith NB: Does high shear stress induced by blood flow lead to atherosclerosis?. Perspect Biol Med. 1983, 26: 287-303. Nerem RM, Levesque MJ: Fluid dynamics as a factor in the localization of atherogenesis. Ann N Y Acad Sci. 1983, 416: 709-710. 10.1111/j.1749-6632.1983.tb35222.x. Davies PF: Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat Clin Pract Cardiovasc Med. 2009, 6: 16-26. 10.1038/ncpcardio1397. 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: 391-398. 10.1016/S0021-9150(99)00482-7. Eskin SG, Sybers HD, Lester JW, Navarro LT, Gotto AM, DeBakey ME: Human smooth muscle cells cultured from atherosclerotic plaques and uninvolved vessel wall. In Vitro. 1981, 17: 713-718. 10.1007/BF02628408. Hoshi H, Kan M, Chen J, McKeehan W: Comparative endocrinology-paracrinology-autocrinology of human adult large vessel endothelial and smooth muscle cells. In Vitro Cell Dev Biol. 1987, 24: 309-320. Bierman EL: The effect of donor Age on the in vitro life span of cultured human arterial smooth-muscle cells. In Vitro. 1978, 14: 951-955. 10.1007/BF02616126. Hoshi H, McKeehan WL: Isolation, growth requirements, cloning, prostacyclin production and life-span of human adult endothelial cells in low serum culture medium. In Vitro Cell Dev Biol. 1986, 22: 51-56. 10.1007/BF02623441. Glassberg MK, Bern MM, Coughlin SR, Haudenschild CC, Hoyer L, Antoniades HN, Zetter BR: Cultured endothelial cells derived from the human iliac arteries. In Vitro. 1982, 18: 859-866. 10.1007/BF02796327. Johnson TE, Umbenhauer DR, Hill R, Bradt C, Mueller SN, Levine EM, Nichols WW: Karyotypic and phenotypic changes during in vitro aging of human endothelial cells. J Cell Physiol. 1992, 150: 17-27. 10.1002/jcp.1041500104. Maciag T, Hoover GA, Stemerman MB, Weinstein R: Serial propagation of human endothelial cells in vitro. J Cell Biol. 1981, 91: 420-426. 10.1083/jcb.91.2.420. Nobuhiko H, Yamamoto M, Imamura T, Mitsui Y, Yamamoto K: Evaluation of long-term cultured endothelial cells as a model system for studying vascular ageing. Mech Ageing Dev. 1988, 46: 111-123. 10.1016/0047-6374(88)90119-4. Vogel G, Thorin-Trescases N, Farhat N, Mamarbachi AM, Villeneuve L, Fortier A, Perrault LP, Carrier M, Thorin E: Chronic treatment with N-acetyl-cystein delays cellular senescence in endothelial cells isolated from a subgroup of atherosclerotic patients. Mech Ageing Dev. 2008, 129: 261-270. 10.1016/j.mad.2008.01.004.