Assessment and consequences of cell senescence in atherosclerosis

Current Opinion in Lipidology

Volumn 27, Issue 5, 2016, Pages 431-438

  Garrido, Abel Martin ^a   Bennett, Martin ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Atherosclerosis; Cell death; Cell senescence; DNA damage

Indexed keywords

BETA GALACTOSIDASE; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 2A; DNA; LAMIN; LAMIN B1; SECRETORY PROTEIN; UNCLASSIFIED DRUG;

ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CELL AGING; ENZYME ACTIVITY; HETEROCHROMATIN; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; REVIEW; TELOMERE SHORTENING; VASCULAR DISEASE; ANIMAL; GENETICS; METABOLISM; PATHOLOGY;

ANIMALS; ATHEROSCLEROSIS; CELLULAR SENESCENCE; DNA; HUMANS;

EID: 84973333868     PISSN: 09579672     EISSN: 14736535     Source Type: Journal    
DOI: 10.1097/MOL.0000000000000327     Document Type: Review

References (84)

1. Campisi J, Robert L. Cell senescence: Role in aging and age-related diseases. Interdiscip Top Gerontol 2014; 39:45-61.
2. Serrano M, Hannon GJ, Beach D. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 1993; 366:704-707.
3. Serrano M, Lin AW, McCurrach ME, et al. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 1997; 88:593-602.
4. Johnson DG, Schwarz JK, Cress WD, et al. Expression of transcription factor E2F1 induces quiescent cells to enter S phase. Nature 1993; 365:349-352.
5. Chellappan SP, Hiebert S, Mudryj M, et al. The E2F transcription factor is a cellular target for the RB protein. Cell 1991; 65:1053-1061.
6. Sharpless NE, Sherr CJ. Forging a signature of in vivo senescence. Nat Rev Cancer 2015; 15:397-408.
7. Baker DJ, Wijshake T, Tchkonia T, et al. Clearance of p16Ink4a-positive senescent cells delays ageing-Associated disorders. Nature 2011; 479:232-236.
8. Baker DJ, Childs BG, Durik M, et al. Naturally occurring p16-positive cells shorten healthy lifespan. Nature 2016; 530:184-189.
9. Matthews C, Gorenne I, Scott S, et al. Vascular smooth muscle cells undergo telomere-based senescence in human atherosclerosis: Effects of telomerase and oxidative stress. Circ Res 2006; 99:156-164.
10. Motterle A, Pu X, Wood H, et al. Functional analyses of coronary artery disease associated variation on chromosome 9p21 in vascular smooth muscle cells. Hum Mol Genet 2012; 21:4021-4029.
11. Holdt LM, Sass K, Gabel G, et al. Expression of Chr9p21 genes CDKN2B (p15(INK4b)), CDKN2A (p16(INK4a), p14(ARF)) and MTAP in human atherosclerotic plaque. Atherosclerosis 2011; 214:264-270.
12. Allahverdian S, Chehroudi AC, McManus BM, et al. Contribution of intimal smooth muscle cells to cholesterol accumulation and macrophage-like cells in human atherosclerosis. Circulation 2014; 129:1551-1559.
13. Shankman LS, Gomez D, Cherepanova OA, et al. KLF4-dependent phenotypic modulation of smooth muscle cells has a key role in atherosclerotic plaque pathogenesis. Nat Med 2015; 21:628-637.
14. Sawicka M, Pawlikowski J, Wilson S, et al. The specificity and patterns of staining in human cells and tissues of p16INK4a antibodies demonstrate variant antigen binding. PLoS One 2013; 8:e53313.
15. Alcorta DA, Xiong Y, Phelps D, et al. Involvement of the cyclin-dependent kinase inhibitor p16 (INK4a) in replicative senescence of normal human fibroblasts. Proc Natl Acad Sci USA 1996; 93:13742-13747.
16. el-Deiry WS, Tokino T, Velculescu VE, et al. WAF1, a potential mediator of p53 tumor suppression. Cell 1993; 75:817-825.
17. Stein GH, Drullinger LF, Soulard A, Dulic V. Differential roles for cyclindependent kinase inhibitors p21 and p16 in the mechanisms of senescence and differentiation in human fibroblasts. Mol Cell Biol 1999; 19:2109-2117.
18. Herbig U, Jobling WA, Chen BP, et al. Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol Cell 2004; 14:501-513.
19. d'Adda di Fagagna F, Reaper PM, Clay-Farrace L, et al. A DNA damage checkpoint response in telomere-initiated senescence. Nature 2003; 426:194-198.
20. Beausejour CM, Krtolica A, Galimi F, et al. Reversal of human cellular senescence: Roles of the p53 and p16 pathways. EMBO J 2003; 22:4212-4222.
21. Ihling C, Menzel G, Wellens E, et al. Topographical association between the cyclin-dependent kinases inhibitor p21, p53 accumulation, and cellular proliferation in human atherosclerotic tissue. Arterioscler Thromb Vasc Biol 1997; 17:2218-2224.
22. Tanner FC, Yang ZY, Duckers E, et al. Expression of cyclin-dependent kinase inhibitors in vascular disease. Circ Res 1998; 82:396-403.
23. Kunieda T, Minamino T, Nishi J, et al. 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.
24. Rowland BD, Peeper DS. KLF4, p21 and context-dependent opposing forces in cancer. Nature Reviews Cancer 2006; 6:11-23.
25. Blackburn EH, Gall JG. A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J Mol Biol 1978; 120:33-53.
26. Griffith JD, Comeau L, Rosenfield S, et al. Mammalian telomeres end in a large duplex loop. Cell 1999; 97:503-514.
27. de Lange T. Shelterin: The protein complex that shapes and safeguards human telomeres. Genes Dev 2005; 19:2100-2110.
28. von Zglinicki T. Oxidative stress shortens telomeres. Trends Biochem Sci 2002; 27:339-344.
29. Karlseder J, Broccoli D, Dai Y, et al. p53-And ATM-dependent apoptosis induced by telomeres lacking TRF2. Science 1999; 283:1321-1325.
30. Celli GB, de Lange T. DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion. Nat Cell Biol 2005; 7:712- 718.
31. Fumagalli M, Rossiello F, Clerici M, et al. Telomeric DNA damage is irreparable and causes persistent DNA-damage-response activation. Nat Cell Biol 2012; 14:355-365.
32. Hewitt G, Jurk D, Marques FD, et al. Telomeres are favoured targets of a persistent DNA damage response in ageing and stress-induced senescence. Nat Commun 2012; 3:708.
33. Okuda K, Khan MY, Skurnick J, et al. Telomere attrition of the human abdominal aorta: Relationships with age and atherosclerosis. Atherosclerosis 2000; 152:391-398.
34. Chang E, Harley CB. Telomere length and replicative aging in human vascular tissues. Proc Natl Acad Sci USA 1995; 92:11190-11194.
35. Wang J, Uryga AK, Reinhold J, et al. Vascular smooth muscle cell senescence promotes atherosclerosis and features of plaque vulnerability. Circulation 2015; 132:1909-1919.
36. Huzen J, Peeters W, de Boer RA, et al. Circulating leukocyte and carotid atherosclerotic plaque telomere length: interrelation, association with plaque characteristics, and restenosis after endarterectomy. Arterioscler Thromb Vasc Biol 2011; 31:1219-1225.
37. Canela A, Klatt P, Blasco MA. Telomere length analysis. Methods Mol Biol 2007; 371:45-72.
38. Lallemand-Breitenbach V, de The H. PML nuclear bodies. Cold Spring Harb Perspect Biol 2010; 2:a000661.
39. Ferbeyre G, de Stanchina E, Querido E, et al. PML is induced by oncogenic ras and promotes premature senescence. Genes Dev 2000; 14:2015- 2027.
40. Pearson M, Carbone R, Sebastiani C, et al. PML regulates p53 acetylation and premature senescence induced by oncogenic Ras. Nature 2000; 406:207-210.
41. Bischof O, KirshO, Pearson M, et al. Deconstructing PML-induced premature senescence. EMBO J 2002; 21:3358-3369.
42. Vernier M, Bourdeau V, Gaumont-Leclerc MF, et al. Regulation of E2Fs and senescence by PML nuclear bodies. Genes Dev 2011; 25:41-50.
43. Talluri S, Isaac CE, Ahmad M, et al. A G1 checkpoint mediated by the retinoblastoma protein that is dispensable in terminal differentiation but essential for senescence. Mol Cell Biol 2010; 30:948-960.
44. Gurrieri C, Capodieci P, Bernardi R, et al. Loss of the tumor suppressor PML in human cancers of multiple histologic origins. J Natl Cancer Inst 2004; 96:269-279.
45. Mudryj M, Devoto SH, Hiebert SW, et al. Cell cycle regulation of the E2F transcription factor involves an interaction with cyclin A. Cell 1991; 65:1243- 1253.
46. Narita M, Nuñez S, Heard E, et al. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 2003; 113:703-716.
47. Zhang R, Poustovoitov MV, Ye X, et al. Formation of MacroH2A-containing senescence-Associated heterochromatin foci and senescence driven by ASF1a and HIRA. Developmental Cell 2005; 8:19-30.
48. Banumathy G, Somaiah N, Zhang R, et al. Human UBN1 is an ortholog of yeast Hpc2p and has an essential role in the HIRA/ASF1a chromatinremodeling pathway in senescent cells. Mol Cell Biol 2009; 29: 758-770.
49. Rai TS, Puri A, McBryan T, et al. Human CABIN1 is a functional member of the human HIRA/UBN1/ASF1a histone H3.3 chaperone complex. Mol Cell Biol 2011; 31:4107-4118.
50. Sadaie M, Salama R, Carroll T, et al. Redistribution of the Lamin B1 genomic binding profile affects rearrangement of heterochromatic domains and SAHF formation during senescence. Genes Dev 2013; 27:1800-1808.
51. Narita M, Narita M, Krizhanovsky V, et al. A novel role for high-mobility group a proteins in cellular senescence and heterochromatin formation. Cell 2006; 126:503-514.
52. Adams PD. Remodeling of chromatin structure in senescent cells and its potential impact on tumor suppression and aging. Gene 2007; 397:84-93.
53. Di Micco R, Sulli G, Dobreva M, et al. Interplay between oncogene-induced DNA damage response and heterochromatin in senescence and cancer. Nature Cell Biol 2011; 13:292-302.
54. Ye X, Zerlanko B, Zhang R, et al. Definition of pRB-And p53-dependent and - independent steps in HIRA/ASF1a-mediated formation of senescence-Associated heterochromatin foci. Mol Cell Biol 2007; 27:2452-2465.
55. Collado M, Gil J, Efeyan A, et al. Tumour biology: senescence in premalignant tumours. Nature 2005; 436:642-1642.
56. Herbig U, Ferreira M, Condel L, et al. Cellular senescence in aging primates. Science 2006; 311:1257-11257.
57. Jeyapalan JC, Ferreira M, Sedivy JM, Herbig U. Accumulation of senescent cells in mitotic tissue of aging primates. Mechanisms of ageing and development 2007; 128:36-44.
58. Coppé J-P, Desprez P-Y, Krtolica A, Campisi J. The senescence-Associated secretory phenotype: The dark side of tumor suppression. Annual Rev Pathol 2010; 5:99-118.
59. Kang T-W, Yevsa T, Woller N, et al. Senescence surveillance of premalignant hepatocytes limits liver cancer development. Nature 2011; 479:547-551.
60. Krizhanovsky V, Yon M, Dickins RA, et al. Senescence of activated stellate cells limits liver fibrosis. Cell 2008; 134:657-667.
61. Xue W, Zender L, Miething C, et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007; 445:656-660.
62. Iannello A, Thompson TW, Ardolino M, et al. p53-dependent chemokine production by senescent tumor cells supports NKG2D-dependent tumor elimination by natural killer cells. J Exp Med 2013; 210:2057- 2069.
63. Acosta JC, O'Loghlen A, Banito A, et al. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 2008; 133:1006-1018.
64. Kuilman T, Michaloglou C, Vredeveld LC, et al. Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 2008; 133:1019-1031.
65. Coppé J-P, Kauser K, Campisi J, Beausé jour CM. Secretion of vascular endothelial growth factor by primary human fibroblasts at senescence. J Biol Chem 2006; 281:29568-29574.
66. Coppé J-P, Patil CK, Rodier F, et al. Senescence-Associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 2008; 6:e301.
67. Freund A, Patil CK, Campisi J. p38MAPK is a novel DNA damage responseindependent regulator of the senescence-Associated secretory phenotype. EMBO J 2011; 30:1536-1548.
68. Kang C, Xu Q, Martin TD, et al. The DNA damage response induces inflammation and senescence by inhibiting autophagy of GATA4. Science 2015; 349:aaa5612.
69. Rodier F, Coppé J-P, Patil CK, et al. Persistent DNA damage signalling triggers senescence-Associated inflammatory cytokine secretion. Nature Cell Biol 2009; 11:973-979.
70. Coppé J-P, Rodier F, Patil CK, et al. Tumor suppressor and aging biomarker p16INK4a induces cellular senescence without the associated inflammatory secretory phenotype. J Biol Chem 2011; 286:36396-36403.
71. Gardner SE, Humphry M, Bennett MR, Clarke MC. Senescent vascular smooth muscle cells drive inflammation through an Interleukin-1alpha-dependent senescence-Associated secretory phenotype. Arterioscler Thromb Vasc Biol 2015; 35:1963-1974.
72. Dechat T, Adam SA, Taimen P, et al. Nuclear lamins. Cold Spring Harb Perspect Biol 2010; 2:a000547.
73. Shimi T, Butin-Israeli V, Adam SA, et al. The role of nuclear lamin B1 in cell proliferation and senescence. Genes Dev 2011; 25:2579-2593.
74. Dreesen O, Chojnowski A, Ong PF, et al. Lamin B1 fluctuations have differential effects on cellular proliferation and senescence. J Cell Biol 2013; 200:605-617.
75. Freund A, Laberge R-M, Demaria M, Campisi J. Lamin B1 loss is a senescence-Associated biomarker. Mol Biol Cell 2012; 23:2066- 2075.
76. Dimri GP, Lee X, Basile G, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 1995; 92:9363-9367.
77. Lee BY, Han JA, Im JS, et al. Senescence-Associated b-galactosidase is lysosomal b-galactosidase. Aging Cell 2006; 5:187-195.
78. Krishna DR, Sperker B, Fritz P, Klotz U. Does pH 6 b-galactosidase activity indicate cell senescence? Mech Ageing Dev 1999; 109:113-123.
79. Aviv H, Khan MY, Skurnick J, et al. Age dependent aneuploidy and telomere length of the human vascular endothelium. Atherosclerosis 2001; 159:281- 287.
80. Vasile E, Tomita Y, Brown LF, et al. Differential expression of thymosin beta-10 by early passage and senescent vascular endothelium is modulated by VPF/VEGF: Evidence for senescent endothelial cells in vivo at sites of atherosclerosis. FASEB J 2001; 15:458-466.
81. Minamino T, Miyauchi H, Yoshida T, et al. Endothelial cell senescence in human atherosclerosis: Role of telomere in endothelial dysfunction. Circulation 2002; 105:1541-1544.
82. Rajapakse AG, Yepuri G, Carvas JM, et al. Hyperactive S6K1 mediates oxidative stress and endothelial dysfunction in aging: inhibition by resveratrol. PLoS One 2011; 6:e19237.
83. Yepuri G, Velagapudi S, Xiong Y, et al. Positive crosstalk between arginase-II and S6K1 in vascular endothelial inflammation and aging. Aging Cell 2012; 11:1005-1016.
84. Wu Z, Yu Y, Liu C, et al. Role of p38 mitogen-Activated protein kinase in vascular endothelial aging: interaction with Arginase-II and S6K1 signaling pathway. Aging (Albany NY) 2015; 7:70-81.