Regulation of a senescence checkpoint response by the E2F1 transcription factor and p14(ARF) tumor suppressor

Molecular and Cellular Biology

Volumn 20, Issue 1, 2000, Pages 273-285

  Dimri, Goberdhan P ^a   Itahana, Koji ^a   Acosta, Meileen ^a   Campisi, Judith ^a  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2F;

ARTICLE; CELL AGING; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 0033989829     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.1.273-285.2000     Document Type: Article

References (77)

1. Afshari, C. A., P. J. Vojta, L. A. Annab, P. A. Futreal, T. B. Willard, and J. C. Barrett. 1993. Investigation of the role of G1/S cell cycle mediators in cellular senescence. Exp. Cell Res. 209:231-237.
2. Alcorta, D. A., Y. Xiong, D. Phelps, G. Hannon, D. Beach, and J. C. Barrett. 1996. Involvement of the cyclin-dependent kinase inhibitor p16 (INK4a) in replicative senescence of normal human fibroblasts. Proc. Natl. Acad. Sci. USA 93:13742-13747.
3. Atadja, P., H. Wong, I. Garkavstev, C. Veillette, and K. Riabowol. 1995. Increased activity of p53 in senescing fibroblasts. Proc. Natl. Acad. Sci. USA 92:8348-8352.
4. Bates, S., A. C. Phillips, P. A. Clark, F. Stott, G. Peters, R. L. Ludwig, and K. H. Voudsen. 1998. p14ARF links the tumor suppressors RB and p53. Nature 395:124-125.
5. Blattner, C., A. Sparks, and D. Lane. 1999. Transcription factor E2F-1 is upregulated in response to DNA damage in a manner analogous to that of p53. Mol. Cell. Biol. 19:3704-3713.
6. Bodnar, A. G., M. Ouellette, M. Frolkis, S. E. Holt, C. P. Chiu, G. B. Morin, C. B. Harley, J. W. Shay, S. Lichtsteiner, and W. E. Wright. 1998. Extension of life span by introduction of telomerase into normal human cells. Science 279:349-352.
7. Campisi, J. 1997. Aging and cancer: the double-edged sword of replicative senescence. J. Am. Geriatrics Soc. 45:1-6.
8. Campisi, J. 1996. Replicative senescence: an old lives tale? Cell 84:497-500.
9. Campisi, J., G. P. Dimri, and E. Hara. 1996. Control of replicative senescence, p. 121-149. In E. Schneider, and J. Rowe (ed.), Handbook of the biology of aging, 4th ed. Academic Press, New York, N.Y.
10. 2-induced senescent-like growth arrest in normal human fibroblasts: p53 and Rb control G(1) arrest but not cell replication. Biochem. J. 332:43-50.
11. 1/S regulatory genes. Mol. Cell. Biol. 15:4215-4224.
12. DeGregori, J., G. Leone, A. Miron, L. Jakoi, and J. R. Nevins. 1997. Distinct roles for E2F proteins in cell growth control and apoptosis. Proc. Natl. Acad. Sci. USA 94:7245-7250.
13. DiLeonardo, A., S. P. Linke, K. Clarkin, and G. M. Wahl. 1994. DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cip1 in normal human fibroblasts. Genes Dev. 8:2540-2551.
14. Dimri, G. P., J. Campisi, and Cold Spring Harbor Press. 1994. Molecular and cell biology of replicative senescence. Mol. Gen. Cancer 59:67-73.
15. Dimri, G. P., E. E. Kara, and J. Campisi. 1994. Regulation of two E2F-related genes in presenescent and senescent human fibroblasts. J. Biol. Chem. 269:16180-16186.
16. Dimri, G. P., X. Lee, G. Basile, M. Acosta, G. Scott, C. Roskelley, E. E. Medrano, M. Linskens, I. Rubelj, O. M. Pereira-Smith, M. Peacocke, and J. Campisi. 1995. A novel biomarker identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 92:9363-9367.
17. Dimri, G. P., M. Nakanishi, P. Y. Desprez, J. R. Smith, and J. Campisi. 1996. Inhibition of E2F activity by the p21 inhibitor of cyclin dependent protein kinases in cells expressing or lacking a functional retinoblastoma protein. Mol. Cell. Biol. 16:2987-2997.
18. Dimri, G. P., A. Testori, M. Acosta, and J. Campisi. 1996. Replicative senescence, aging and growth regulatory transcription factors. Biol. Signals 5:154-162.
19. Dyson, N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev. 12:2245-2262.
20. El-Deiry, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. M. Trent, D. Lin, W. E. Mercer, K. W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
21. Field, S. J., F. Y. Tsai, F. Kuo, A. M. Zubiaga, W. G. Kaelin, D. M. Livingston, S. H. Orkin, and M. E. Greenberg. 1996. E2F1 functions in mice to promote apoptosis and suppress proliferation. Cell 85:549-561.
22. Freedman, D. A., L. Wu, and A. J. Levine. 1999. Functions of the MDM2 oncoprotein. Mol. Life Sci. 55:96-107.
23. Halbert, C. L., G. W. Demes, and D. A. Galloway. 1992. The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J. Virol. 66:2125-2134.
24. Hara, E., R. Smith, D. Parry, H. Tahara, S. Stone, and G. Peters. 1996. Regulation of p16/CDKN2 expression and its implications for cell immortalization and senescence. Mol. Cell. Biol. 16:859-867.
25. Harley, C. B. 1991. Telomere loss: mitotic clock or genetic time bomb? Mutat. Res. 256:271-282.
26. Hayflick, L. 1965. The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 37:614-636.
27. Helin, K. 1997. Regulation of cell proliferation by E2F transcription factors. Curr. Opin. Genet. Dev. 8:28-35.
28. Helin, K., J. A. Lees, M. Vidal, N. Dyson, E. Harlow, and A. Fattaey. 1992. A cDNA encoding a pRB binding protein with properties of the transcription factor E2F. Cell 70:337-350.
29. Hofferer, M., C. Wirbelauer, B. Humar, and W. Kerk. 1999. Increased levels of E2F1 dependent DNA binding activity after UV-or gamma-irradiation. Nucleic Acids Res. 15:491-495.
30. Jacobs, J. J., K. Kieboom, S. Marino, R. A. DePinho, and M. van Lohuizen. 1999. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397:164-168.
31. Johnson, D. G., J. K. Schwarz, W. D. Cress, and J. R. Nevins. 1993. Expression of transcription factor E2F1 induces quiescent cells to enter S phase. Nature 365:349-352.
32. Kamijo, T., F. Zindy, M. F. Roussel, D. E. Quelle, R A. Downing, G. Ashmun, G. Grosveld, and C. J. Sherr. 1997. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91:649-659.
33. Klingelhutz, A., S. A. Foster, and J. K. McDougall. 1996. Telomerase activation by the E6 gene product of human papillomavirus type 16. Nature 380:79-83.
34. Lin, A. W., M. Barradas, J. C. Stone, L. van Aelst, M. Serrano, and S. W. Lowe. 1998. Premature senescence involving p53 and p16 is activated in response to constitutive MEK/MAPK mitogenic signaling. Genes Dev. 12: 3008-3019.
35. McConnell, B. B., M. Starborg, S. Brookes, and G. Peters. 1998. Inhibitors of cyclin-dependent kinases induce features of replicative senescence in early passage human diploid fibroblasts. Curr. Biol. 8:351-354.
36. Melillo, R. M., K. Helin, D. R. Lowy, and J. T. Schiller. 1994. Positive and negative regulation of cell proliferation by E2F1: influence of protein level and human papilloma virus oncoproteins. Mol. Cell. Biol. 14:8241-8249.
37. Merlin, A. B., V. L. Gabai, J. Yaglom, V. I. Shifrin, and M. Y. Sherman. 1998. Proteasome inhibitors activate stress kinases and induce Hsp72. J. Biol. Chem. 273:6373-6379.
38. Miller, A. D., and G. J. Rosman. 1989. Improved retroviral vectors for gene transfer and expression. BioTechniques 7:980-988.
39. Millis, A. J. T., M. Hoyle, H. M. McCue, and H. Martini. 1992. Differential expression of metalloproteinase and tissue inhibitor of metalloproteinase genes in diploid human fibroblasts. Exp. Cell Res. 201:373-379.
40. Mishima. K., J. T. Handa, A. Aotaki-Keen, G. A. Lutty, L. S. Morse, and L. M. Hjelmeland. 1999. Senescence-associated beta-galactosidase histochemistry for the primate eye. Invest. Ophthalmol. Vis. Sci. 40:1590-1593.
41. Morgenstern, J. P., and H. Land. 1990. Advanced mammalian gene transfer: high titer retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18:3587-3596.
42. Neuman, E., E. K. Flemington, W. R. Sellers, and W. G. Kaelin, Jr. 1994. Transcription of the E2F-1 gene is rendered cell cycle dependent by E2F DNA-binding sites within its promoter. Mol. Cell. Biol. 14:6607-6615.
43. Nevins, J. R. 1998. Toward an understanding of the functional complexity of the E2F and retinoblastoma families. Nat. Genet. 9:585-593.
44. Noda, A., Y. Ning, S. F. Venable, O. M. Pereira-Smith, and J. Smith. 1994. Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp. Cell Res. 21:90-98.
45. Ogryzko, V. V., T. H. Hirai, V. R. Russanova, D. A. Barbie, and B. H. Howard. 1996. Human fibroblast commitment to a senescence-like state in response to histone deacetylase inhibitors is cell cycle dependent. Mol. Cell. Biol. 16:5210-5218.
46. Oswald, F., H. Lovec, T. Moroy, and M. Lipp. 1994. E2F dependent regulation of human MYC: transactivation by cyclins D1 and A overrides tumor suppressor protein functions. Oncogene 9:2029-2036.
47. Pan, H., C. Yin, N. J. Dyson, E. Harlow, L. Yamasaki, and T. van Dyke. 1998. Key roles for E2F1 in signaling p53-dependent apoptosis and in cell division within developing tumors. Mol. Cell 2:283-292.
48. Pear, W. S., G. P. Nolan, M. L. Scott, and D. Baltimore. 1993. Production of high titer helper free retroviruses by transient transfection. Proc. Natl. Acad. Sci. USA 90:8392-8396.
49. Pendergrass, W. R., M. A. Lane, N. L. Bodkin, B. C. Hansen, D. K. Ingram, G. S. Roth, L. Yi, H. Bin, and N. S. Wolf. 1999. Cellular proliferation potential during aging and caloric restriction in rhesus monkeys (Macaca mulatta). J. Cell. Physiol. 180:123-130.
50. Pierce, A. M., I. B. Gimenez-Conti, R. Schneider-Broussard, L. A. Martinez, C. J. Conti, and D. G. Johnson. 1998. Increased E2F1 activity induces skin tumors in mice heterozygous and nullizygous for p53. Proc. Natl. Acad. Sci. USA 95:8858-8863.
51. Pomerantz, J., N. Schreiber-Agus, N. J. Liegeois, A. Silverman, L. Alland, L. Chin, J. Potes, K. Chen, I. Orlow, H. W. Lee, C. Cordon-Cardo, and R. A. DePinho. 1998. The Ink4a tumor suppressor gene product. p19Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell 92:713-723.
52. Qin, X. Q., D. M. Livingston, W. G. Kaelin, and P. D. Adams. 1994. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. USA 91:10918-10922.
53. Rapp, L., and J. J. Chen. 1998. The papillomavirus E6 proteins. Biochim. Biophys. Acta 1378:F1-F19.
54. Robertson, K. D., and P. A. Jones. 1998. The human ARF cell cycle regulatory gene promoter is a CpG island which can be silenced by DNA methylation and down-regulated by wild-type p53. Mol. Cell. Biol. 18:6457-6473.
55. Rubles, S. J., and G. R. Adami. 1998. Agents that cause DNA double strand breaks lead to p16INK4a enrichment and the premature senescence of normal fibroblasts. Oncogene 16:1113-1123.
56. Sager, R. 1991. Senescence as a mode of tumor suppression. Environ. Health Perspect. 93:59-62.
57. Saito, M., K. Helin, M. B. Valentine, B. B. Griffith, C. L. Willman, E. Harlow, and A. T. Look. 1995. Amplification of the E2F1 transcription factor gene in the HEL erythroleukemia cell line. Genomics 25:130-138.
58. Saunders, N. A., R. J. Smith, and A. M. Jetten. 1994. Regulation of proliferation-specific and differentiation-specific genes during senescence of human epidermal keratinocytes and mammary epithelial cells. Biochem. Biophys. Res. Commun. 197:46-54.
59. Scheffner, M., B. A. Werness, J. M. Huibregtse, A. J. Levine, and P. M. Howley. 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129-1136.
60. Sedivy, J. M. 1998. Can ends justify the means? Telomeres and the mechanisms of replicative senescence and immortalization in mammalian cells. Proc. Natl. Acad. Sci. USA 95:9078-9081.
61. Serrano, M., A. W. Lin, M. E. McCurrach, D. Beach, and S. W. Lowe. 1997. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and P16INK4a. Cell 88:593-602.
62. Shan, B., T. Durfee, and W. H. Lee. 1996. Disruption of RB/E2F-1 interaction by single point mutations in E2F-1 enhances S-phase entry and apoptosis. Proc. Natl. Acad. Sci. USA 93:679-684.
63. Shan, B., and W. H. Lee. 1994. Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol. Cell. Biol. 14:8166-8173.
64. Sherr, C. J. 1998. Tumor surveillance via the ARF-p53 pathway. Genes Dev. 12:2984-2981.
65. Smith, J. R., and O. M. Pereira-Smith. 1996. Replicative senescence: implications for in vivo aging and tumor suppression. Science 273:63-67.
66. Stein, G. H., L. F. Drullinger, A. Soulard, and V. Dulic. 1999. 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.
67. Stott, F. J., S. Bates, M. C. James, B. B. McConnell, M. Starborg, S. Brookes, I. Palmero, K. Ryan, E. Hara, K. H. Vousden, and G. Peters. 1998. The alternative product from the human CDKN2A locus, p14(ARF), participates in a regulatory feedback loop with p53 and MDM2. EMBO J. 17:5001-5014.
68. Tao, W., and A. J. Levine. 1999. P19 (ARF) stabilizes p53 by blocking nucleo-cytoplasmic shuttling of Mdm2. Proc. Natl. Acad. Sci. USA 96:6937-6941.
69. Tsai, K. Y., Y. Hu, K. F. Macleod, D. Crowley, L. Yamasaki, and T. Jacks. 1998. Mutation of E2F-1 suppresses apoptosis and inappropriate S phase entry and extends survival of Rb-deficient mouse embryos. Mol. Cell 2:293-304.
70. West, M. D., O. M. Pereira-Smith, and J. R. Smith. 1989. Replicative senescence of human skin fibroblasts correlates with a loss of regulation and overexpression of collagenase activity. Exp. Cell Res. 184:138-147.
71. Wright, W. E., and J. W. Shay. 1996. Mechanism of escaping senescence in human diploid cells, p. 153-167. In N. J. Holbrook, G. R. Martin, and R. A. Lockshin (ed.), Modern cell biology series. Cellular aging and cell death. Wiley & Sons, Inc., New York, N.Y.
72. Wu, X., and A. J. Levine. 1994. P53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. USA 91:3601-3606.
73. Yamasaki, L., R. Bronson, B. O. Williams, N. J. Dyson, E. Harlow, and T. Jacks. 1998. Loss of E2F-1 reduces tumorigenesis and extends the lifespan of Rb1(+/-) mice. Nat. Genet. 18:360-364.
74. Yamasaki, L., T. Jacks, R. Bronson, E. Goillot, E. Harlow, and N. J. Dyson. 1996. Tumor induction and tissue atrophy in mice lacking E2F-1. Cell 85: 537-548.
75. Zhang, Y., Y. Xiong, and W. G. Yarbrough. 1998. ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppressor pathways. Cell 92:725-734.
76. Zhu, J., D. Woods, M. McMahon, and J. M. Bishop. 1998. Senescence of human fibroblasts induced by oncogenic raf. Genes Dev. 12:2997-3007.
77. Zindy, F., C. M. Eischen, D. Randle, T. Kamijo, J. L. Cleveland, C. J. Sherr, and M. F. Roussel. 1998. Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev. 12: 2424-2434.