Angiotensin II-mediated oxidative DNA damage accelerates cellular senescence in cultured human vascular smooth muscle cells via telomere-dependent and independent pathways

Circulation Research

Volumn 102, Issue 2, 2008, Pages 201-208

  Herbert, Karl E ^a   Mistry, Yogita ^a   Hastings, Richard ^a   Poolman, Toryn ^a   Niklason, Laura ^b   Williams, Bryan ^a,c  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b YALE UNIVERSITY   (United States)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Angiotensin II; DNA damage; Reactive oxygen species; Senescence; Vascular smooth muscle cell

Indexed keywords

2 BUTYL 4 CHLORO 1 [[2' (1H TETRAZOL 5 YL) 4 BIPHENYLYL]METHYL] 5 IMIDAZOLECARBOXYLIC ACID; ANGIOTENSIN II; BETA GALACTOSIDASE; CATALASE; PROTEIN P53; REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL AGING; COMET ASSAY; DNA DAMAGE; HUMAN; HUMAN CELL; LONG TERM EXPOSURE; OXIDATIVE STRESS; PRIORITY JOURNAL; SOUTHERN BLOTTING; STAINING; TELOMERE; VASCULAR SMOOTH MUSCLE; CELL CULTURE; CYTOLOGY; METABOLISM; PHYSIOLOGY;

ANGIOTENSIN II; CELL AGING; CELLS, CULTURED; DNA DAMAGE; HUMANS; MUSCLE, SMOOTH, VASCULAR; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; TELOMERE;

EID: 41149139491     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.107.158626     Document Type: Article

References (57)

1. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res. 1994;74:1141-1148.
2. Zafari AM, Ushio-Fukai M, Akers M, Yin Q, Shah A, Harrison DG, Taylor WR, Griendling KK. Role of NADH/NADPH oxidase-derived H2O2 in angiotensin II-induced vascular hypertrophy. Hypertension. 1998;32:488-495.
3. Cai H, Griendling KK, Harrison DG. The vascular NAD(P)H oxidases as therapeutic targets in cardiovascular diseases. Trends Pharmacol Sci. 2003;24:471-478.
4. Mehta PK, Griendling KK. Angiotensin II Cell Signaling: Physiological and Pathological Effects in the Cardiovascular System. Am J Physiol Cell Physiol. 2007;292:C82-C97.
5. Ushio-Fukai M, Alexander RW, Akers M, Griendling KK. p38 Mitogen-activated protein kinase is a critical component of the redox-sensitive signaling pathways activated by angiotensin II. Role in vascular smooth muscle cell hypertrophy. J Biol Chem. 1998;273:15022-15029.
6. Griendling KK, Sorescu D, Lassegue B, Ushio-Fukai M. Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiology and pathophysiology. Arterioscler Thromb Vasc Biol. 2000;20:2175-2183.
7. 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.
8. 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;105:1541-1544.
9. 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. von Zglinicki T. Oxidative stress shortens telomeres. Trends Biochem Sci. 2002;27:339-344.
11. Allsopp RC, Vaziri H, Patterson C, Goldstein S, Younglai EV, Futcher AB, Greider CW, Harley CB. Telomere length predicts replicative capacity of human fibroblasts. Proc Natl Acad Sci U S A. 1992;89:10114-10118.
12. d'Adda di Fagagna F, Reaper PM, Clay-Farrace L, Fiegler H, Carr P, Von Zglinicki T, Saretzki G, Carter NP, Jackson SP. A DNA damage checkpoint response in telomere-initiated senescence. Nature. 2003;426:194-198.
13. Minamino T, Miyauchi H, Yoshida T, Tateno K, Kunieda T, Komuro I. Vascular cell senescence and vascular aging. J Mol Cell Cardiol. 2004;36:175-183.
14. Minamino T, Komuro I. Vascular cell senescence: contribution to atherosclerosis. Circ Res. 2007;100:15-26.
15. Gorenne I, Kavurma M, Scott S, Bennett M. Vascular smooth muscle cell senescence in atherosclerosis. Cardiovasc Res. 2006;72:9-17.
16. Ballard VL, Edelberg JM. Stem cells and the regeneration of the aging cardiovascular system. Circ Res. 2007;100:1116-1127.
17. Ross R, Wight TN, Strandness E, Thiele B. Human atherosclerosis. I. Cell constitution and characteristics of advanced lesions of the superficial femoral artery. Am J Pathol. 1984;114:79-93.
18. Bennett MR, Macdonald K, Chan SW, Boyle JJ, Weissberg PL. Cooperative interactions between RB and p53 regulate cell proliferation, cell senescence, and apoptosis in human vascular smooth muscle cells from atherosclerotic plaques. Circ Res. 1998;82:704-712.
19. Liao S, Curci JA, Kelley BJ, Sicard GA, Thompson RW. Accelerated replicative senescence of medial smooth muscle cells derived from abdominal aortic aneurysms compared to the adjacent inferior mesenteric artery. J Surg Res. 2000;92:85-95.
20. 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.
21. Cawthon RM, 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.
22. Brouilette S, Singh RK, Thompson JR, Goodall AH, Samani NJ. White cell telomere length and risk of premature myocardial infarction. Arterioscler Thromb Vasc Biol. 2003;23:842-846.
23. O'Callaghan CJ, Williams B. Mechanical strain-induced extracellular matrix production by human vascular smooth muscle cells: role of TGF-beta(1). Hypertension. 2000;36:319-324.
24. McKee JA, Banik SS, Boyer MJ, Hamad NM, Lawson JH, Niklason LE, Counter CM. Human arteries engineered in vitro. EMBO Rep. 2003;4:633-638.
25. Klinger RY, Blum JL, Hearn B, Lebow B, Niklason LE. Relevance and safety of telomerase for human tissue engineering. Proc Natl Acad Sci U S A. 2006;103:2500-2505.
26. Collins AR, Dusinska M, Gedik CM, Stetina R. Oxidative damage to DNA: do we have a reliable biomarker? Environ Health Perspect. 1996;104 Suppl 3:465-469.
27. 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.
28. 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.
29. Touyz RM, Chen X, Tabet F, Yao G, He G, Quinn MT, Pagano PJ, Schiffrin EL. Expression of a functionally active gp91phox-containing neutrophil-type NAD(P)H oxidase in smooth muscle cells from human resistance arteries: regulation by angiotensin II. Circ Res. 2002;90:1205-1213.
30. Kunieda T, Minamino T, Nishi J, Tateno K, Oyama T, Katsuno T, Miyauchi H, Orimo M, Okada S, Takamura M, Nagai T, Kaneko S, Komuro I. Angiotensin II induces premature senescence of vascular smooth muscle cells and accelerates the development of atherosclerosis via a p21-dependent pathway. Circulation. 2006;114:953-960.
31. Imanishi T, Hano T, Nishio I. Angiotensin II accelerates endothelial progenitor cell senescence through induction of oxidative stress. J Hypertens. 2005;23:97-104.
32. Sharpless NE, DePinho RA. Telomeres, stem cells, senescence, and cancer. J Clin Invest. 2004;113:160-168.
33. Kurz DJ, Decary S, Hong Y, Trivier E, Akhmedov A, Erusalimsky JD. Chronic oxidative stress compromises telomere integrity and accelerates the onset of senescence in human endothelial cells. J Cell Sci. 2004;117:2417-2426.
34. Oikawa S, Kawanishi S. Site-specific DNA damage at GGG sequence by oxidative stress may accelerate telomere shortening. FEBS Lett. 1999;453:365-368.
35. Henle ES, Han Z, Tang N, Rai P, Luo Y, Linn S. Sequence-specific DNA cleavage by Fe2-mediated fenton reactions has possible biological implications. J Biol Chem. 1999;274:962-971.
36. von Zglinicki T, Pilger R, Sitte N. Accumulation of single-strand breaks is the major cause of telomere shortening in human fibroblasts. Free Radic Biol Med. 2000;28:64-74.
37. Minamino T, Mitsialis SA, Kourembanas S. Hypoxia extends the life span of vascular smooth muscle cells through telomerase activation. Mol Cell Biol. 2001;21:3336-3342.
38. Chen Q, Ames BN. Senescence-like growth arrest induced by hydrogen peroxide in human diploid fibroblast F65 cells. Proc Natl Acad Sci U S A. 1994;91:4130-4134.
39. Dumont P, Burton M, Chen QM, Gonos ES, Frippiat C, Mazarati JB, Eliaers F, Remacle J, Toussaint O. Induction of replicative senescence biomarkers by sublethal oxidative stresses in normal human fibroblast. Free Radic Biol Med. 2000;28:361-373.
40. Frippiat C, Dewelle J, Remacle J, Toussaint O. Signal transduction in H2O2-induced senescence-like phenotype in human diploid fibroblasts. Free Radic Biol Med. 2002;33:1334-1346.
41. Chen JH, Ozanne SE, Hales CN. Heterogeneity in premature senescence by oxidative stress correlates with differential DNA damage during the cell cycle. DNA Repair (Amst). 2005;4:1140-1148.
42. Zdanov S, Debacq-Chainiaux F, Toussaint O. Knocking down p53 with siRNA does not affect the overexpression of p21WAF-1 after exposure of IMR-90 hTERT fibroblasts to a sublethal concentration of H2O2 leading to premature senescence. Ann N Y Acad Sci. 2007;1100:316-322.
43. Naka K, Tachibana A, Ikeda K, Motoyama N. Stress-induced premature senescence in hTERT-expressing ataxia telangiectasia fibroblasts. J Biol Chem. 2004;279:2030-2037.
44. Gorbunova V, Seluanov A, Pereira-Smith OM. Expression of human telomerase (hTERT) does not prevent stress-induced senescence in normal human fibroblasts but protects the cells from stress-induced apoptosis and necrosis. J Biol Chem. 2002;277:38540-38549.
45. Yamada T, Horiuchi M, Dzau VJ. Angiotensin II type 2 receptor mediates programmed cell death. Proc Natl Acad Sci U S A. 1996;93:156-160.
46. Yamada T, Akishita M, Pollman MJ, Gibbons GH, Dzau VJ, Horiuchi M. Angiotensin II type 2 receptor mediates vascular smooth muscle cell apoptosis and antagonizes angiotensin II type 1 receptor action: an in vitro gene transfer study. Life Sci. 1998;63:PL289-PL295.
47. Akishita M, Nagai K, Xi H, Yu W, Sudoh N, Watanabe T, Ohara-Imaizumi M, Nagamatsu S, Kozaki K, Horiuchi M, Toba K. Renin-angiotensin system modulates oxidative stress-induced endothelial cell apoptosis in rats. Hypertension. 2005;45:1188-1193.
48. Li Y, Song YH, Mohler J, Delafontaine P. ANG II induces apoptosis of human vascular smooth muscle via extrinsic pathway involving inhibition of Akt phosphorylation and increased FasL expression. Am J Physiol Heart Circ Physiol. 2006;290:H2116-H2123.
49. Fuster JJ, Andres V. Telomere biology and cardiovascular disease. Circ Res. 2006;99:1167-1180.
50. Minamino T, Yoshida T, Tateno K, Miyauchi H, Zou Y, Toko H, Komuro I. Ras induces vascular smooth muscle cell senescence and inflammation in human atherosclerosis. Circulation. 2003;108:2264-2269.
51. Ogami M, Ikura Y, Ohsawa M, Matsuo T, Kayo S, Yoshimi N, Hai E, Shirai N, Ehara S, Komatsu R, Naruko T, Ueda M. Telomere shortening in human coronary artery diseases. Arterioscler Thromb Vasc Biol. 2004;24:546-550.
52. Chang E, Harley CB. Telomere length and replicative aging in human vascular tissues. Proc Natl Acad Sci U S A. 1995;92:11190-11194.
53. 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.
54. Fitzpatrick AL, Kronmal RA, Gardner JP, Psaty BM, Jenny NS, Tracy RP, Walston J, Kimura M, Aviv A. Leukocyte telomere length and cardiovascular disease in the cardiovascular health study. Am J Epidemiol. 2007;165:14-21.
55. Basso N, Cini R, Pietrelli A, Ferder L, Terragno NA, Inserra F. Protective effect of long-term angiotensin II inhibition. Amer J Physiol Heart Circ Physiol. 2007;293:1351-1358.
56. Touyz RM, Schiffrin EL. Ang II-stimulated superoxide production is mediated via phospholipase D in human vascular smooth muscle cells. Hypertension. 1999;34:976-982.
57. Dikalov S, Griendling KK, Harrison DG. Measurement of reactive oxygen species in cardiovascular studies. Hypertension. 2007;49:717-727.