Molecular mechanisms of replicative senescence in endothelial cells

Experimental Gerontology

Volumn 38, Issue 11-12, 2003, Pages 1251-1257

  Foreman, Kimberly E ^a   Tang, Jun ^a  

^a LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Atherosclerosis; Endothelial cells; Senesence; Vascular integrity

Indexed keywords

ACIDIC FIBROBLAST GROWTH FACTOR; ADENOSINE A2A RECEPTOR; ADENOSINE TRIPHOSPHATASE; BRAIN DERIVED NEUROTROPHIC FACTOR; CANCER GROWTH FACTOR; COLLAGEN TYPE 3; CYCLIN A; CYCLIN B1; CYTOCHROME B; FIBROBLAST GROWTH FACTOR RECEPTOR; FIBRONECTIN; FOLLISTATIN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEAT SHOCK PROTEIN 70; INTERCELLULAR ADHESION MOLECULE 1; METALLOTHIONEIN I; ONCOPROTEIN; PROSTAGLANDIN DERIVATIVE; PROTEIN KINASE; PROTEIN P16; PROTEIN P21; PROTEIN P27; PROTEIN P53; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; RIBOSOME RNA; SOMATOMEDIN BINDING PROTEIN 6; SYNAPSIN I; TELOMERASE; TENASCIN; THYMIDYLATE SYNTHASE;

AGING; APOPTOSIS; ATHEROSCLEROSIS; CELL ACTIVITY; CELL AGING; CELL DIVISION; DISEASE COURSE; DNA SEQUENCE; ENDOTHELIUM CELL; GENE EXPRESSION; GENE INDUCTION; HUMAN; MOLECULAR MECHANICS; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SENESCENCE;

EID: 0347416785     PISSN: 05315565     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exger.2003.09.005     Document Type: Article

References (67)

1. Alani R.M., Hasskarl J., Grace M., Hernandez M.C., Israel M.A., Munger K. Immortalization of primary human keratinocytes by the helix-loop-helix protein, Id-1. Proc. Natl Acad. Sci. USA. 96:1999;9637-9641.
2. Albrecht E.W., Stegeman C.A., Heeringa P., Henning R.H., van Goor H. Protective role of endothelial nitric oxide synthase. J. Pathol. 199:2003;8-17.
3. An W.G., Chuman Y., Fojo T., Blagosklonny M.V. Inhibitors of transcription, proteasome inhibitors, and DNA-damaging drugs differentially affect feedback of p53 degradation. Exp. Cell Res. 244:1998;54-60.
4. An W.G., Kanekal M., Simon M.C., Maltepe E., Blagosklonny M.V., Neckers L.M. Stabilization of wild-type p53 by hypoxia-inducible factor 1alpha. Nature. 392:1998;405-408.
5. Aviv H., Khan M.Y., Skurnick J., Okuda K., Kimura M., Gardner J., Priolo L., Aviv A. Age dependent aneuploidy and telomere length of the human vascular endothelium. Atherosclerosis. 159:2001;281-287.
6. Benezra R., Davis R.L., Lockshon D., Turner D.L., Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell. 61:1990;49-59.
7. Bodnar A.G., Ouellette M., Frolkis M., Holt S.E., Chiu C.P., Morin G.B., Harley C.B., Shay J.W., Lichtsteiner S., Wright W.E. Extension of life-span by introduction of telomerase into normal human cells. Science. 279:1998;349-352.
8. Burrig K.F. The endothelium of advanced arteriosclerotic plaques in humans. Arterioscler. Thromb. 11:1991;1678-1689.
9. Campisi J. Cancer, aging and cellular senescence. In Vivo. 14:2000;183-188.
10. Campisi J. Cellular senescence as a tumor-suppressor mechanism. Trends Cell Biol. 11:2001;S27-S31.
11. Campisi J., Kim S.H., Lim C.S., Rubio M. Cellular senescence, cancer and aging: the telomere connection. Exp. Gerontol. 36:2001;1619-1637.
12. Cavallaro U., Castelli V., Del Monte U., Soria M.R. Phenotypic alterations in senescent large-vessel and microvascular endothelial cells. Mol. Cell. Biol. Res. Commun. 4:2000;117-121.
13. Challah M., Nadaud S., Philippe M., Battle T., Soubrier F., Corman B., Michel J.B. Circulating and cellular markers of endothelial dysfunction with aging in rats. Am. J. Physiol. 273:1997;H1941-H194H.
14. Chang E., Harley C.B. Telomere length and replicative aging in human vascular tissues. Proc. Natl Acad. Sci. USA. 92:1995;11190-11194.
15. Chiu C.P., Harley C.B. Replicative senescence and cell immortality: the role of telomeres and telomerase. Proc. Soc. Exp. Biol. Med. 214:1997;99-106.
16. Cohen J.I., Arnett E.N., Kolodny A.L., Roberts W.C. Cardiovascular features of the Werner syndrome. Am. J. Cardiol. 59:1987;493-495.
17. Comi P., Chiaramonte R., Maier J.A. Senescence-dependent regulation of type 1 plasminogen activator inhibitor in human vascular endothelial cells. Exp. Cell Res. 219:1995;304-308.
18. Cziraki A., Horvath I.G., Papp L. Endothelial function studies in pulmonary vascular disease: determination of angiotensin converting enzyme activity in humans. Int. J. Mol. Med. 9:2002;317-325.
19. Desprez P.Y., Lin C.Q., Thomasset N., Sympson C.J., Bissell M.J., Campisi J. A novel pathway for mammary epithelial cell invasion induced by the helix-loop-helix protein Id-1. Mol. Cell Biol. 18:1998;4577-4588.
20. Fenton M., Barker S., Kurz D.J., Erusalimsky J.D. Cellular senescence after single and repeated balloon catheter denudations of rabbit carotid arteries. Arterioscler. Thromb. Vasc. Biol. 21:2001;220-226.
21. Foreman K.E., Vaporciyan A.A., Bonish B.K., Jones M.L., Johnson K.J., Glovsky M.M., Eddy S.M., Ward P.A. C5a-induced expression of P-selectin in endothelial cells. J. Clin. Invest. 94:1994;1147-1155.
22. Grillari J., Hohenwarter O., Grabherr R.M., Katinger H. Subtractive hybridization of mRNA from early passage and senescent endothelial cells. Exp. Gerontol. 35:2000;187-197.
23. Hara E., Yamaguchi T., Nojima H., Ide T., Campisi J., Okayama H., Oda K. Idrelated genes encoding helix-loop-helix proteins are required for G1 progression and are repressed in senescent human fibroblasts. J. Biol. Chem. 269:1994;2139-2145.
24. Hayflick L., Moorehead P.S. The serial cultivation of human diploid cell strains. Exp. Cell Res. 25:1961;585-621.
25. Hoffmann J., Haendeler J., Aicher A., Rossig L., Vasa M., Zeiher A.M., Dimmeler S. Aging enhances the sensitivity of endothelial cells toward apoptotic stimuli: important role of nitric oxide. Circ. Res. 89:2001;709-715.
26. Kalashnik L., Bridgeman C.J., King A.R., Francis S.E., Mikhalovsky S., Wallis C., Denyer S.P., Crossman D., Faragher R.G. A cell kinetic analysis of human umbilical vein endothelial cells. Mech. Aging Dev. 120:2000;23-32.
27. Kreider B.L., Benezra R., Rovera G., Kadesch T. Inhibition of myeloid differentiation by the helix-loop-helix protein Id. Science. 255:1992;1700-1702.
28. Kumazaki T., Sakano T., Yoshida T., Hamada K., Sumida H., Teranishi Y., Nishiyama M., Mitsui Y. Enhanced expression of mitochondrial genes in senescent endothelial cells and fibroblasts. Mech. Aging Dev. 101:1998;91-99.
29. de Lange T. Activation of telomerase in a human tumor. Proc. Natl Acad. Sci. USA. 91:1994;2882-2885.
30. Levine A.J. p53, the cellular gatekeeper for growth and division. Cell. 88:1997;323-331.
31. Lin K., Hsu P.P., Chen B.P., Yuan S., Usami S., Shyy J.Y., Li Y.S., Chien S. Molecular mechanism of endothelial growth arrest by laminar shear stress. Proc. Natl Acad. Sci. USA. 97:2000;9385-9389.
32. Lovec H., Sewing A., Lucibello F.C., Muller R., Moroy T. Oncogenic activity of cyclin D1 revealed through cooperation with Ha-ras: link between cell cycle control and malignant transformation. Oncogene. 9:1994;323-326.
33. Maier J.A., Statuto M., Ragnotti G. Senescence stimulates U937-endothelial cell interactions. Exp. Cell Res. 208:1993;270-274.
34. Matsushita H., Chang E., Glassford A.J., Cooke J.P., Chiu C.P., Tsao P.S. eNOS activity is reduced in senescent human endothelial cells: preservation by hTERT immortalization. Circ. Res. 89:2001;793-798.
35. 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. 105:2002;1541-1544.
36. Nickoloff B.J., Chaturvedi V., Bacon P., Qin J.Z., Denning M.F., Diaz M.O. Id-1 delays senescence but does not immortalize keratinocytes. J. Biol. Chem. 275:2000;27501-27504.
37. Norton J.D. ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J. Cell Sci. 113:2000;3897-3905.
38. Okuda K., Khan M.Y., Skurnick J., Kimura M., Aviv H., Aviv A. Telomere attrition of the human abdominal aorta: relationships with age and atherosclerosis. Atherosclerosis. 152:2000;391-398.
39. Ranganathan S., Joseph J., Mehta J.L. Aspirin inhibits human coronary artery endothelial cell proliferation by upregulation of p53. Biochem. Biophys. Res. Commun. 301:2003;143-146.
40. Rao K.M., Cohen H.J. The role of the cytoskeleton in aging. Exp. Gerontol. 25:1990;7-22.
41. Rao K.M., Cohen H.J. Actin cytoskeletal network in aging and cancer. Mutat. Res. 256:1991;139-148.
42. Rivard A., Fabre J.E., Silver M., Chen D., Murohara T., Kearney M., Magner M., Asahara T., Isner J.M. Age-dependent impairment of angiogenesis. Circulation. 99:1999;111-120.
43. Ross R. The pathogenesis of atherosclerosis-an update. N. Engl. J. Med. 314:1986;488-500.
44. Ross R., Wight T.N., Strandness E., Thiele B. Human atherosclerosis I. Cell constitution and characteristics of advanced lesions of the superficial femoral artery. Am. J. Pathol. 114:1984;79-93.
45. Sato I., Morita I., Kaji K., Ikeda M., Nagao M., Murota S. Reduction of nitric oxide producing activity associated with in vitro aging in cultured human umbilical vein endothelial cell. Biochem. Biophys. Res. Commun. 195:1993;1070-1076.
46. Satoh T., Sasatomi E., Yamasaki F., Ishida H., Wu L., Tokunaga O. Multinucleated variant endothelial cells (MVECs) of human aorta: expression of tumor suppressor gene p53 and relationship to atherosclerosis and aging. Endothelium. 6:1998;123-132.
47. Serrano M., Gomez-Lahoz E., DePinho R.A., Beach D., Bar-Sagi D. Inhibition of rasinduced proliferation and cellular transformation by p16INK4. Science. 267:1995;249-252.
48. Serrano M., Lee H., Chin L., Cordon-Cardo C., Beach D., DePinho R.A. Role of the INK4a locus in tumor suppression and cell mortality. Cell. 85:1996;27-37.
49. Serrano M., Lin A.W., McCurrach M.E., Beach D., Lowe S.W. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell. 88:1997;593-602.
50. Shelton D.N., Chang E., Whittier P.S., Choi D., Funk W.D. Microarray analysis of replicative senescence. Curr. Biol. 9:1999;939-945.
51. Spyridopoulos I., Isner J.M., Losordo D.W. Oncogenic ras induces premature senescence in endothelial cells: role of p21(Cip1/Waf1). Basic Res. Cardiol. 97:2002;117-124.
52. Starkebaum G., Harlan J.M. Endothelial cell injury due to copper-catalyzed hydrogen peroxide generation from homocysteine. J. Clin. Invest. 77:1986;1370-1376.
53. Stempien-Otero A., Karsan A., Cornejo C.J., Xiang H., Eunson T., Morrison R.S., Kay M., Winn R., Harlan J. Mechanisms of hypoxia-induced endothelial cell death. Role of p53 in apoptosis. J. Biol. Chem. 274:1999;8039-8045.
54. Sugrue M.M., Shin D.Y., Lee S.W., Aaronson S.A. Wild-type p53 triggers a rapid senescence program in human tumor cells lacking functional p53. Proc. Natl Acad. Sci. USA. 94:1997;9648-9653.
55. Suschek C.V., Krischel V., Bruch-Gerharz D., Berendji D., Krutmann J., Kroncke K.D., Kolb-Bachofen V. Nitric oxide fully protects against UVA-induced apoptosis in tight correlation with Bcl-2 up-regulation. J. Biol. Chem. 274:1999;6130-6137.
56. Tang J., Gordon G.M., Nickoloff B.J., Foreman K.E. The helix-loop-helix protein id-1 delays onset of replicative senescence in human endothelial cells. Lab. Invest. 82:2002;1073-1079.
57. Tang J., Gordon G.M., Müller M.G., Dahiya M., Foreman K.E. The KSHV latency associated nuclear antigen (LANA) induces expression of the helix-loop-helix protein, Id-1, in human endothelial cells. J. Virol. 77:2003;5975-5984.
58. Thomson J.A., Kalishman J., Golos T.G., Durning M., Harris C.P., Becker R.A., Hearn J.P. Isolation of a primate embryonic stem cell line. Proc. Natl. Acad. Sci. USA. 92:1995;7844-7848.
59. Tokunaga O., Fan J.L., Watanabe T. Atherosclerosis- and age-related multinucleated variant endothelial cells in primary culture from human aorta. Am. J. Pathol. 135:1989;967-976.
60. Vasa M., Breitschopf K., Zeiher A.M., Dimmeler S. Nitric oxide activates telomerase and delays endothelial cell senescence. Circ. Res. 87:2000;540-542.
61. Wagner M., Hampel B., Bernhard D., Hala M., Zwerschke W., Jansen-Durr P. Replicative senescence of human endothelial cells in vitro involves G1 arrest, polyploidization and senescence-associated apoptosis. Exp. Gerontol. 36:2001;1327-1347.
62. Wang E. Senescent human fibroblasts resist programmed cell death, and failure to suppress bcl2 is involved. Cancer Res. 55:1995;2284-2292.
63. Xu D., Neville R., Finkel T. Homocysteine accelerates endothelial cell senescence. Fed. Eur. Biol. Soc. Lett. 470:2000;20-24.
64. Xu H.J., Zhou Y., Ji W., Perng G.S., Kruzelock R., Kong C.T., Bast R.C., Mills G.B., Li J., Hu S.X. Reexpression of the retinoblastoma protein in tumor cells induces senescence and telomerase inhibition. Oncogene. 15:1997;2589-2596.
65. Yang J., Chang E., Cherry A.M., Bangs C.D., Oei Y., Bodnar A., Bronstein A., Chiu C.P., Herron G.S. Human endothelial cell life extension by telomerase expression. J. Biol. Chem. 274:1999;26141-26148.
66. von Zglinicki T., Saretzki G., Docke W., Lotze C. Mild hyperoxia shortens telomeres and inhibits proliferation of fibroblasts: a model for senescence? Exp. Cell Res. 220:1995;186-193.
67. Zhang Y., Griffith E.C., Sage J., Jacks T., Liu J.O. Cell cycle inhibition by the antiangiogenic agent TNP-470 is mediated by p53 and p21WAF1/CIP1. Proc. Natl Acad. Sci. USA. 97:2000;6427-6432.