The role of replicative senescence in cancer and human ageing: Utility (or otherwise) of murine models

Cytogenetic and Genome Research

Volumn 105, Issue 2-4, 2004, Pages 455-463

  Smith, S K ^a   Kipling, D ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; CANCER; CANCER INHIBITION; CARCINOGENESIS; CELL CYCLE; CELL DIVISION; DISEASE MODEL; GROWTH RATE; HUMAN; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REPLICATIVE SENESCENCE; REVIEW; SENESCENCE; TELOMERE;

AGING; ANIMALS; CELL AGING; CELL CULTURE TECHNIQUES; CELL CYCLE; CELL DIVISION; CYCLIN-DEPENDENT KINASE INHIBITOR P16; HUMANS; MICE; MODELS, ANIMAL; NEOPLASMS; TELOMERE; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA; MURINAE;

EID: 3242752701     PISSN: 14248581     EISSN: None     Source Type: Journal    
DOI: 10.1159/000078219     Document Type: Review

References (106)

1. Alcorta DA, Xiong Y, Phelps D, Hannon G, Beach D, Barrett JC: Involvement of the cyclin-dependent kinase inhibitor p16 (INK4a) in replicative senescence of normal human fibroblasts. Proc Natl Acad Sci USA 93:13742-13747 (1996).
2. Allsopp RC, Harley CB: Evidence for a critical telomere length in senescent human fibroblasts. Exp Cell Res 219:130-136 (1995).
3. Allsopp RC, Chang E, Kashefi-Aazam M, Rogaev EI, Piatyszek MA, Shay JW, Harley CB: Telomere shortening is associated with cell division in vitro and in vivo. Exp Cell Res 220:194-200 (1995).
4. Artandi SE, Alson S, Tietze MK, Sharpless NE, Ye S, Greenberg RA, Castrillon DH, Horner JW, Weiler SR, Carrasco RD, DePinho RA: Constitutive telomerase expression promotes mammary carcinomas in aging mice. Proc Natl Acad Sci USA 99:8191-8196 (2002).
5. Beausejour CM, Krtolica A, Galimi F, Narita M, Lowe SW, Yaswen P, Campisi J: Reversal of human cellular senescence: roles of the p53 and p16 pathways. EMBO J 22:4212-4222 (2003).
6. Blasco MA, Lee HW, Hande MP, Samper E, Lansdorp PM, DePinho RA,Greider C W: Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91:25-34 (1997).
7. Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, Morin GB, Harley CB, Shay JW, Lichtsteiner S, Wright WE: Extension of life-span by introduction of telomerase into normal human cells. Science 279:349-352 (1998).
8. Bond JA, Wyllie FS, Wynford-Thomas D: Escape from senescence in human diploid fibroblasts induced directly by mutant p53. Oncogene 9:1885-1889 (1994).
9. Bond J, Haughton M, Blaydes J, Gire V, Wynford-Thomas D, Wyllie F: Evidence that transcriptional activation by p53 plays a direct role in the induction of cellular senescence. Oncogene 13:2097-2104 (1996).
10. Bond JA, Haughton MF, Rowson JM, Smith PJ, Gire V, Wynford-Thomas D, Wyllie FS: Control of replicative life span in human cells: barriers to clonal expansion intermediate between M1 senescence and M2 crisis. Mol Cell Biol 19:3103-3114 (1999).
11. Brenner AJ, Stampfer MR, Aldaz CM: Increased p16 expression with first senescence arrest in human mammary epithelial cells and extended growth capacity with p16 inactivation. Oncogene 17:199-205 (1998).
12. Bryan TM, Reddel RR: SV40-induced immortalization of human cells. Crit Rev Oncog 5:331-357 (1994).
13. Bryan TM, Englezou A, Dalla-Pozza L, Dunham MA, Reddel RR: Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat Med 3:1271-1274 (1997).
14. Campisi J: The biology of replicative senescence. Eur J Cancer 33:703-709 (1997).
15. Campisi J: Cellular senescence as a tumor-suppressor mechanism. Trends Cell Biol 11:S27-31 (2001).
16. Chen Q, Ames BN: Senescence-like growth arrest induced by hydrogen peroxide in human diploid fibroblast F65 cells. Proc Natl Acad Sci USA 91:4130-4134 (1994).
17. Collins CJ, Sedivy JM: Involvement of the INK4a/Arf gene locus in senescence. Aging Cell 2:145-150 (2003).
18. Condon J, Yin S, Mayhew B, Word RA, Wright WE, Shay JW, Rainey WE: Telomerase immortalization of human myometrial cells. Biol Reprod 67:506-514 (2002).
19. Counter CM, Hahn WC, Wei W, Caddle SD, Beijersbergen RL, Lansdorp PM, Sedivy JM, Weinberg RA: Dissociation among in vitro telomerase activity, telomere maintenance and cellular immortalization. Proc Natl Acad Sci USA 95:14723-14728 (1998).
20. Di Leonardo A, Linke SP, Clarkin K, Wahl GM: DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cip1 in normal human fibroblasts. Genes Dev 8:2540-2551 (1994).
21. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O, Peacocke M, Campisi J: A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 92:9363-9367 (1995).
22. Egan CA, Savre-Train I, Shay JW, Wilson SE, Bourne WM: Analysis of telomere lengths in human corneal endothelial cells from donors of different ages. Invest Ophthalmol Vis Sci 39:648-653 (1998).
23. Espejel S, Blasco MA: Identification of telomere-dependent "senescence-like" arrest in mouse embryonic fibroblasts. Exp Cell Res 276:242-248 (2002).
24. Evans RJ, Wyllie FS, Wynford-Thomas D, Kipling D, Jones CJ: A P53-dependent telomere-independent proliferative life span barrier in human astrocytes consistent with the molecular genetics of glioma development. Cancer Res 63:4854-4861 (2003).
25. Faragher RG: Cell senescence and human aging: where's the link? Biochem Soc Trans 28:221-226 (2000).
26. Faragher RG, Kipling D: How might replicative senescence contribute to human ageing? Bioessays 20:985-991 (1998).
27. Farwell DG, Shera KA, Koop JI, Bonnet GA, Matthews CP, Reuther GW, Coltrera MD, McDougall JK, Klingelhutz AJ: Genetic and epigenetic changes in human epithelial cells immortalized by telomerase. Am J Pathol 156:1537-1547 (2000).
28. Ferbeyre G, de Stanchina E, Lin AW, Querido E, McCurrach ME, Hannon GJ, Lowe SW: Oncogenic ras and p53 cooperate to induce cellular senescence. Mol Cell Biol 22:3497-3508 (2002).
29. Forsyth NR, Evans AP, Shay JW, Wright WE: Developmental differences in the immortalization of lung fibroblasts by telomerase. Aging Cell 2:235-243 (2003).
30. Foster SA, Galloway DA: Human papillomavirus type 16 E7 alleviates a proliferation block in early passage human mammary epithelial cells. Oncogene 12:1773-1779 (1996).
31. Gire V, Wynford-Thomas D: Reinitiation of DNA synthesis and cell division in senescent human fibroblasts by microinjection of anti-p53 antibodies. Mol Cell Biol 18:1611-1621 (1998).
32. Halvorsen TL, Beattie GM, Lopez AD, Hayek A, Levine F: Accelerated telomere shortening and senescence in human pancreatic islet cells stimulated to divide in vitro. J Endocrinol 166:103-109 (2000).
33. Hara E, Smith R, Parry D, Tahara H, Stone S, Peters G: Regulation of p16CDKN2 expression and its implications for cell immortalization and senescence. Mol Cell Biol 16:859-867 (1996).
34. Harley CB, Futcher AB, Greider CW: Telomeres shorten during ageing of human fibroblasts. Nature 345:458-460 (1990).
35. Hayflick L: The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 37:614-636 (1965).
36. Hayflick L, Moorhead PS: The serial cultivation of human diploid cell strains. Exp Cell Res 25:585-621 (1961).
37. Hemann MT, Strong MA, Hao LY, Greider CW: The shortest telomere not average telomere length is critical for cell viability and chromosome stability. Cell 107:67-77 (2001).
38. Huot TJ, Rowe J, Harland M, Drayton S, Brookes S, Gooptu C, Purkis P, Fried M, Bataille V, Hara E, Newton-Bishop J, Peters G: Biallelic mutations in p16(INK4a) confer resistance to Ras- and Ets-induced senescence in human diploid fibroblasts. Mol Cell Biol 22:8135-8143 (2002).
39. Huschtscha LI, Noble JR, Neumann AA, Moy EL, Barry P, Melki JR, Clark SJ, Reddel RR: Loss of p16INK4 expression by methylation is associated with lifespan extension of human mammary epithelial cells. Cancer Res 58:3508-3512 (1998).
40. Itahana K, Zou Y, Itahana Y, Martinez JL, Beausejour C, Jacobs JJ, Van Lohuizen M, Band V, Campisi J, Dimri GP: Control of the replicative life span of human fibroblasts by p16 and the polycomb protein Bmi-1. Mol Cell Biol 23:389-401 (2003).
41. Iwasa H, Han J, Ishikawa F: Mitogen-activated protein kinase p38 defines the common senescence-signalling pathway. Genes Cells 8:131-144 (2003).
42. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M: The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397:164-168 (1999).
43. Jiang H, Chou HS, Zhu L: Requirement of cyclin E-Cdk2 inhibition in p16(INK4a)-mediated growth suppression. Mol Cell Biol 18:5284-5290 (1998).
44. Jiang XR, Jimenez G, Chang E, Frolkis M, Kusler B, Sage M, Beeche M, Bodnar AG, Wahl GM, Tlsty TD, Chiu CP: Telomerase expression in human somatic cells does not induce changes associated with a transformed phenotype. Nat Genet 21:111-114 (1999).
45. Jones CJ, Kipling D, Morris M, Hepburn P, Skinner J, Bounacer A, Wyllie FS, Ivan M, Bartek J, Wynford-Thomas D, Bond JA: Evidence for a telomere-independent "clock" limiting RAS oncogene-driven proliferation of human thyroid epithelial cells. Mol Cell Biol 20:5690-5699 (2000).
46. Kamijo T, van de Kamp E, Chong MJ, Zindy F, Diehl JA, Sherr CJ, McKinnon PJ: Loss of the ARF tumor suppressor reverses premature replicative arrest but not radiation hypersensitivity arising from disabled atm function. Cancer Res 59:2464-2469 (1999).
47. Karlseder J, Smogorzewska A, de Lange T: Senescence induced by altered telomere state not telomere loss. Science 295:2446-2449 (2002).
48. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, Coviello GM, Wright WE, Weinrich SL, Shay JW: Specific association of human telomerase activity with immortal cells and cancer. Science 266:2011-2015 (1994).
49. Kipling D: Mammalian telomerase: catalytic subunit and knockout mice. Hum Mol Genet 6:1999-2004 (1997).
50. Kipling D: Telomeres replicative senescence and human ageing. Maturitas 38:25-37 (2001).
51. Kipling D, Cooke HJ: Hypervariable ultra-long telomeres in mice. Nature 347:400-402 (1990).
52. Kiyono T, Foster SA, Koop JI, McDougall JK, Galloway DA, Klingelhutz AJ: Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells. Nature 396:84-88 (1998).
53. Li GZ, Eller MS, Firoozabadi R, Gilchrest BA: Evidence that exposure of the telomere 3′ overhang sequence induces senescence. Proc Natl Acad Sci USA 100:527-531 (2003).
54. 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 38:100-107 (1997).
55. Lumpkin CK, Knepper JE, Butel JS, Smith JR, Pereira-Smith OM: Mitogenic effects of the proto-oncogene and oncogene forms of c-H-ras DNA in human diploid fibroblasts. Mol Cell Biol 6:2990-2993 (1986).
56. Martens UM, Chavez EA, Poon SS, Schmoor C, Lansdorp PM: Accumulation of short telomeres in human fibroblasts prior to replicative senescence. Exp Cell Res 256:291-299 (2000).
57. Martin JA, Mitchell CJ, Klingelhutz AJ, Buckwalter JA: Effects of telomerase and viral oncogene expression on the in vitro growth of human chondrocytes. J Gerontol A Biol Sci Med Sci 57:B48-53 (2002).
58. Mathon NF, Lloyd AC: Cell senescence and cancer. Nat Rev Cancer 1:203-213 (2001).
59. McConnell BB, Gregory FJ, Stott FJ, Hara E, Peters G: Induced expression of p16(INK4a) inhibits both CDK4- and CDK2-associated kinase activity by reassortment of cyclin-CDK-inhibitor complexes. Mol Cell Biol 19:1981-1989 (1999).
60. Melk A, Kittikowit W, Sandhu I, Halloran KM, Grimm P, Schmidt BM, Halloran PF: Cell senescence in rat kidneys in vivo increases with growth and age despite lack of telomere shortening. Kidney Int 63:2134-2143 (2003).
61. Migliaccio E, Giorgio M, Mele S, Pelicci G, Reboldi P, Pandolfi PP, Lanfrancone L, Pelicci PG: The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature 402:309-313 (1999).
62. Morales CP, Holt SE, Ouellette M, Kaur KJ, Yan Y, Wilson KS, White MA, Wright WE, Shay JW: Absence of cancer-associated changes in human fibroblasts immortalized with telomerase. Nat Genet 21:115-118 (1999).
63. Morales CP, Gandia KG, Ramirez RD, Wright WE, Shay JW, Spechler SJ: Characterisation of telomerase immortalised normal human oesophageal squamous cells. Gut 52:327-333 (2003).
64. Narita M, Nunez S, Heard E, Lin AW, Hearn SA, Spector DL, Hannon GJ, Lowe SW: Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 113:703-716 (2003).
65. Niida H, Matsumoto T, Satoh H, Shiwa M, Tokutake Y, Furuichi Y, Shinkai Y: Severe growth defect in mouse cells lacking the telomerase RNA component. Nat Genet 19:203-206 (1998).
66. Ohtani N, Zebedee Z, Huot TJ, Stinson JA, Sugimoto M, Ohashi Y, Sharrocks AD, Peters G, Hara E: Opposing effects of Ets and Id proteins on p16INK4a expression during cellular senescence. Nature 409:1067-1070 (2001).
67. Paramio JM, Segrelles C, Ruiz S, Martin-Caballero J, Page A, Martinez J, Serrano M, Jorcano JL: The ink4a/arf tumor suppressors cooperate with p21cip1/waf in the processes of mouse epidermal differentiation senescence and carcinogenesis. J Biol Chem 276:44203-44211 (2001).
68. Parkinson EK, Newbold RF, Keith WN: The genetic basis of human keratinocyte immortalisation in squamous cell carcinoma development: the role of telomerase reactivation. Eur J Cancer 33:727-734 (1997).
69. Parrinello S, Samper E, Krtolica A, Goldstein J, Melov S, Campisi J: Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat Cell Biol 5:741-747 (2003).
70. Ramirez RD, Morales CP, Herbert BS, Rohde JM, Passons C, Shay JW, Wright WE: Putative telomere-independent mechanisms of replicative aging reflect inadequate growth conditions. Genes Dev 15:398-403 (2001).
71. Reddel RR: A reassessment of the telomere hypothesis of senescence. Bioessays 20:977-984 (1998).
72. Rheinwald JG, Hahn WC, Ramsey MR, Wu JY, Guo Z, Tsao H, De Luca M, Catricala C, O'Toole KM: A two-stage p16(INK4A)- and p53-dependent keratinocyte senescence mechanism that limits replicative potential independent of telomere status. Mol Cell Biol 22:5157-5172 (2002).
73. Ruas M, Peters G: The p16INK4a/CDKN2A tumor suppressor and its relatives. Biochim Biophys Acta 1378:F115-177 (1998).
74. Serrano M, Lee H, Chin L, Cordon-Cardo C, Beach D, DePinho RA: Role of the INK4a locus in tumor suppression and cell mortality. Cell 85:27-37 (1996).
75. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW: Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88:593-602 (1997).
76. Severino J, Allen RG, Balin S, Balin A, Cristofalo VJ: Is beta-galactosidase staining a marker of senescence in vitro and in vivo? Exp Cell Res 257:162-171 (2000).
77. Shay JW, Pereira-Smith OM, Wright WE: A role for both RB and p53 in the regulation of human cellular senescence. Exp Cell Res 196:33-39 (1991a).
78. Shay JW, Wright WE, Werbin H: Defining the molecular mechanisms of human cell immortalization. Biochim Biophys Acta 1072:1-7 (1991b).
79. Shay JW, Wright WE, Brasiskyte D, Van der Haegen BA: E6 of human papillomavirus type 16 can overcome the M1 stage of immortalization in human mammary epithelial cells but not in human fibroblasts. Oncogene 8:1407-1413 (1993).
80. Shelton DN, Chang E, Whittier PS, Choi D, Funk WD: Microarray analysis of replicative senescence. Curr Biol 9:939-945 (1999).
81. Sherr CJ: Cancer cell cycles. Science 274:1672-1677 (1996).
82. Sherr CJ: The Pezcoller lecture: cancer cell cycles revisited. Cancer Res 60:3689-3695 (2000).
83. Sherr CJ: Parsing Ink4a/Arf: "pure" p16-null mice. Cell 106:531-534 (2001).
84. Sherr CJ, Roberts JM: CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13:1501-1512 (1999).
85. Simonsen JL, Rosada C, Serakinci N, Justesen J, Stenderup K, Rattan SI, Jensen TG, Kassem M: Telomerase expression extends the proliferative life-span and maintains the osteogenic potential of human bone marrow stromal cells. Nat Biotechnol 20:592-596 (2002).
86. Smogorzewska A, de Lange T: Different telomere damage signaling pathways in human and mouse cells. EMBO J 21:4338-4348 (2002).
87. Southern SA, Herrington CS: Disruption of cell cycle control by human papillomaviruses with special reference to cervical carcinoma. Int J Gynecol Cancer 10:263-274 (2000).
88. Stein GH, Drullinger LF, Robetorye RS, Pereira-Smith OM, Smith JR: Senescent cells fail to express cdc2 cycA and cycB in response to mitogen stimulation. Proc Natl Acad Sci USA 88:11012-11016 (1991).
89. Stein GH, Drullinger LF, Soulard A, Dulic V: Differential roles for cyclin-dependent kinase inhibitors p21 and p16 in the mechanisms of senescence and differentiation in human fibroblasts. Mol Cell Biol 19:2109-2117 (1999).
90. Steinert S, White DM, Zou Y, Shay JW, Wright WE: Telomere biology and cellular aging in nonhuman primate cells. Exp Cell Res 272:146-152 (2002).
91. Trimarchi JM, Lees JA: Sibling rivalry in the E2F family. Nat Rev Mol Cell Biol 3:11-20 (2002).
92. Vaziri H, Benchimol S: Reconstitution of telomerase activity in normal human cells leads to elongation of telomeres and extended replicative life span. Curr Biol 8:279-282 (1998).
93. Vaziri H, Squire JA, Pandita TK, Bradley G, Kuba RM, Zhang H, Gulyas S, Hill RP, Nolan GP, Benchimol S: Analysis of genomic integrity and p53-dependent G1 checkpoint in telomerase-induced extended-life-span human fibroblasts. Mol Cell Biol 19:2373-2379 (1999).
94. Vogt M, Haggblom C, Yeargin J, Christiansen-Weber T, Haas M: Independent induction of senescence by p16INK4a and p21CIP1 in spontaneously immortalized human fibroblasts. Cell Growth Differ 9:139-146 (1998).
95. 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 220:186-193 (1995).
96. Wang E: Senescent human fibroblasts resist programmed cell death and failure to suppress bcl2 is involved. Cancer Res 55:2284-2292 (1995).
97. Wang J, Hannon GJ, Beach DH: Risky immortalization by telomerase. Nature 405:55-756 (2000).
98. Watanabe Y, Lee SW, Detmar M, Ajioka I, Dvorak HF: Vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) delays and induces escape from senescence in human dermal microvascular endothelial cells. Oncogene 14:2025-2032 (1997).
99. Wazer DE, Liu XL, Chu Q, Gao Q, Band V: Immortalization of distinct human mammary epithelial cell types by human papilloma virus 16 E6 or E7. Proc Natl Acad Sci USA 92:3687-3691 (1995).
100. Webley K, Bond JA, Jones CJ, Blaydes JP, Craig A, Hupp T, Wynford-Thomas D: Posttranslational modifications of p53 in replicative senescence overlapping but distinct from those induced by DNA damage. Mol Cell Biol 20:2803-2808 (2000).
101. Wei W, Hemmer RM, Sedivy JM: Role of p14(ARF) in replicative and induced senescence of human fibroblasts. Mol Cell Biol 21:6748-6757 (2001).
102. Wynford-Thomas D: Cellular senescence and cancer. J Pathol 187:100-111 (1999).
103. Wynford-Thomas D, Kipling D: Telomerase Cancer and the knockout mouse. Nature 389:551-552 (1997).
104. Xin Z, Broccoli D: Manipulating mouse telomeres: models of tumorigenesis and aging. Cytogenet Genome Res 105:471-478 (2004).
105. Yang J, Chang E, Cherry AM, Bangs CD, Oei Y, Bodnar A, Bronstein A, Chiu CP, Herron GS: Human endothelial cell life extension by telomerase expression. J Biol Chem 274:26141-26148 (1999).
106. Zalvide J, DeCaprio JA: Role of pRb-related proteins in simian virus 40 large-T-antigen-mediated transformation. Mol Cell Biol 15:5800-5810 (1995).