A G1 checkpoint mediated by the retinoblastoma protein that is dispensable in terminal differentiation but essential for senescence

Molecular and Cellular Biology

Volumn 30, Issue 4, 2010, Pages 948-960

  Talluri, Srikanth ^a   Isaac, Christian E ^a   Ahmad, Mohammad ^b,c   Henley, Shauna A ^a   Francis, Sarah M ^a   Martens, Alison L ^a   Bremner, Rod ^b,c   Dick, Frederick A ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F;

ANIMAL CELL; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CHROMATIN; DNA REPLICATION; GENE EXPRESSION; GENE REPRESSION; GENOTOXICITY; HETEROCHROMATIN; MITOSIS; MOUSE; MUSCLE CELL; MUTATION; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; SENESCENCE; ANIMAL; CELL AGING; CELL LINE; CYTOLOGY; FIBROBLAST; GENETIC TRANSCRIPTION; GENETICS; HUMAN; METABOLISM; MOUSE MUTANT;

ANIMALS; CELL AGING; CELL DIFFERENTIATION; CELL LINE; DNA REPLICATION; E2F TRANSCRIPTION FACTORS; FIBROBLASTS; G1 PHASE; HETEROCHROMATIN; HUMANS; MICE; MICE, KNOCKOUT; MUTATION; PROMOTER REGIONS, GENETIC; RETINOBLASTOMA PROTEIN; TRANSCRIPTION, GENETIC;

EID: 75749111377     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01168-09     Document Type: Article

References (58)

1. Ait-Si-Ali, S., V. Guasconi, L. Fritsch, R. Yahi, I. Sekhri, I. Naguibneva, P. Robin, F. Cabon, A. Polesskaya, and A. Harel-Bellan. 2004. A Suv39hdependent mechanism for silencing S-phase genes in differentiating but not cycling cells. EMBO J. 23:605-616.
2. Aparicio, O., J. V. Geisberg, E. Sekinger, E. Yang, Z. Moqtaderi, and K. Struhl. 2005. Chromatin immunoprecipitation for determining the association of proteins with specific genomic sequences in vivo, p. 21.3.1-21.3.33. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. E. Struhl (ed.), Current protocols in molecular biology. Greene Publishing Associates & Wiley-Interscience, New York, NY.
3. Blais, A., C. J. van Oevelen, R. Margueron, D. Acosta-Alvear, and B. D. Dynlacht. 2007. Retinoblastoma tumor suppressor protein-dependent methylation of histone H3 lysine 27 is associated with irreversible cell cycle exit. J. Cell Biol. 179:1399-1412.
4. 1 progression in C. elegans. Development 128:4349-4359.
5. Bracken, A. P., D. Kleine-Kohlbrecher, N. Dietrich, D. Pasini, G. Gargiulo, C. Beekmean, K. Theilgaard-Monch, S. Minucci, B. T. Porse, J. C. Marine, K. H. Hansen, and K. Helin. 2007. The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells. Genes Dev. 21:525-530.
6. Braig, M., S. Lee, C. Loddenkemper, C. Rudolph, A. H. Peters, B. Schlegelberger, H. Stein, B. Dorken, T. Jenuwein, and C. A. Schmitt. 2005. Oncogene-induced senescence as an initial barrier in lymphoma development. Nature 436:660-665.
7. Brehm, A., and T. Kouzarides. 1999. Retinoblastoma protein meets chromatin. Trends Biochem. Sci. 24:142-145.
8. Burkhart, D. L., and J. Sage. 2008. Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat. Rev. Cancer 8:671-682.
9. Buttitta, L., and B. Edgar. 2007. Mechanisms controlling cell cycle exit upon terminal differentiation. Curr. Opin. Cell Biol. 19:697-704.
10. Buttitta, L., A. Katzaroff, C. Perez, A. de la Cruz, and B. Edgar. 2007. A double-assurance mechanism controls cell cycle exit upon terminal differentiation in Drosophila. Dev. Cell 12:631-643.
11. Camarda, G., F. Siepi, D. Pajalunga, C. Bernardini, R. Rossi, A. Montecucco, E. Meccia, and M. Crescenzi. 2004. A pRb-independent mechanism preserves the postmitotic state in terminally differentiated skeletal muscle cells. J. Cell Biol. 167:417-423.
12. Campisi, J., and F. d'Adda di Fagagna. 2007. Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell Biol. 8:729-740.
13. Chen, D., I. Livne-bar, J. Vanderluit, R. S. Slack, M. Agochiya, and R. Bremner. 2004. Cell-specific effects of RB or RB/p107 loss on retinal development implicate an intrinsically death-resistant cell-of-origin in retinoblastoma. Cancer Cell 5:539-551.
14. Classon, M., and E. Harlow. 2002. The retinoblastoma tumour suppressor in development and cancer. Nat. Rev. Cancer 2:910-917.
15. Classon, M., S. R. Salama, C. Gorka, R. Mulloy, P. Braun, and E. E. Harlow. 2000. Combinatorial roles for pRB, p107 and p130 in E2F-mediated cell cycle control. Proc. Natl. Acad. Sci. U. S. A. 97:10820-10825.
16. Collado, M., M. Blasco, and M. Serrano. 2007. Cellular senescence in cancer and aging. Cell 130:223-233.
17. 1 control causing immortalization and increased cell turnover under growth-restricting conditions. Genes Dev. 14:3051-3064.
18. de Bruin, A., L. Wu, H. I. Saavedra, P. Wilson, Y. Yang, T. J. Rosol, M. Weinstein, M. L. Robinson, and G. Leone. 2003. Rb function in extraembryonic lineages suppresses apoptosis in the CNS of Rb-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 100:6546-6551.
19. Donehower, L., M. Harvey, B. Slagle, M. McArthur, C. Montgomery, J. Butel, and A. Bradley. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215-221.
20. Dunaief, J. L., B. E. Strober, S. Guha, P. A. Khavari, K. Alin, J. Luban, M. Begemann, G. R. Crabtree, and S. P. Goff. 1994. The retinoblastoma protein and BRG1 form a complex and cooperate to induce cell cycle arrest. Cell 79:119-130.
21. Ferguson, K., J. Vanderluit, J. Hébert, W. McIntosh, E. Tibbo, J. Mac-Laurin, D. Park, V. Wallace, M. Vooijs, S. McConnell, and R. Slack. 2002. Telencephalon-specific Rb knockouts reveal enhanced neurogenesis, survival and abnormal cortical development. EMBO J. 21:3337-3346.
22. Firth, L., and N. Baker. 2005. Extracellular signals responsible for spatially regulated proliferation in the differentiating Drosophila eye. Dev. Cell 8:541-551.
23. Francis, S. M., J. Bergseid, C. H. Coschi, C. E. Isaac, C. V. Hojilla, S. Chakrabarti, G. E. DiMattia, R. Khoka, J. Y. J. Wang, and F. A. Dick. 2009. A functional connection between pRB and TGFbeta in growth arrest and mammary gland development. Mol. Cell. Biol. 29:4455-4466.
24. Funayama, R., M. Saito, H. Tanobe, and F. Ishikawa. 2006. Loss of linker histone H1 in cellular senescence. J. Cell Biol. 175:869-880.
25. Harbour, J. W., and D. C. Dean. 2000. Chromatin remodeling and Rb activity. Curr. Opin. Cell Biol. 12:685-689.
26. Huh, M. S., M. H. Parker, A. Scime, R. Parks, and M. A. Rudnicki. 2004. Rb is required for progression through myogenic differentiation but not maintenance of terminal differentiation. J. Cell Biol. 166:865-876.
27. Hurford, R., D. Cobrinik, M.-H. Lee, and N. Dyson. 1997. pRB and p107/ p130 are required for the regulated expression of different sets of E2F responsive genes. Genes Dev. 11:1447-1463.
28. Isaac, C. E., S. M. Francis, A. L. Martens, L. M. Julian, L. A. Seifried, N. Erdmann, U. K. Binne, L. Harrington, P. Sicinski, N. J. Dyson, and F. A. Dick. 2006. The retinoblastoma protein regulates pericentric heterochromatin. Mol. Cell. Biol. 26:3659-3671.
29. Korenjak, M., and A. Brehm. 2005. E2F-Rb complexes regulating transcription of genes important for differentiation and development. Curr. Opin. Genet. Dev. 15:520-527.
30. Kotake, Y., R. Cao, P. Viatour, J. Sage, Y. Zhang, and Y. Xiong. 2007. pRB family proteins are required for H3K27 trimethylation and Polycomb repression complexes binding to and silencing p16INK4A tumor suppressor gene. Genes Dev. 21:49-54.
31. Krimpenfort, P., K. C. Quon, W. J. Mooi, A. Loonstra, and A. Berns. 2001. Loss of p16Ink4a confers susceptibility to metastatic melanoma in mice. Nature 413:83-86.
32. Krizhanovsky, V., M. Yon, R. Dickins, S. Hearn, J. Simon, C. Miething, H. Yee, L. Zender, and S. Lowe. 2008. Senescence of activated stellate cells limits liver fibrosis. Cell 134:657-667.
33. Lin, H. K., S. Bergmann, and P. P. Pandolfi. 2004. Cytoplasmic PML function in TGF-beta signalling. Nature 431:205-211.
34. MacLeod, K. 2008. The role of the RB tumour suppressor pathway in oxidative stress responses in the haematopoietic system. Nat. Rev. Cancer 8:769-781.
35. MacPherson, D., J. Sage, T. Kim, D. Ho, M. E. McLaughlin, and T. Jacks. 2004. Cell type-specific effects of Rb deletion in the murine retina. Genes Dev. 18:1681-1694.
36. Magnaghi-Jaulin, L., R. Groisman, I. Naguibneva, P. Robin, S. Lorain, J. P. Le Villain, F. Troalen, D. Trouche, and A. Harel-Bellan. 1998. Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature 391:601-604.
37. Mason-Richie, N. A., M. J. Mistry, C. A. Gettler, A. Elayyadi, and K. A. Wikenheiser-Brokamp. 2008. Retinoblastoma function is essential for establishing lung epithelial quiescence after injury. Cancer Res. 68:4068-4076.
38. Mayhew, C. N., E. E. Bosco, S. R. Fox, T. Okaya, P. Tarapore, S. J. Schwemberger, G. F. Babcock, A. B. Lentsch, K. Fukasawa, and E. S. Knudsen. 2005. Liver-specific pRB loss results in ectopic cell cycle entry and aberrant ploidy. Cancer Res. 65:4568-4577.
39. McClellan, K., V. Ruzhynsky, D. Douda, J. Vanderluit, K. Ferguson, D. Chen, R. Bremner, D. Park, G. Leone, and R. Slack. 2007. Unique requirement for Rb/E2F3 in neuronal migration: evidence for cell cycle-independent functions. Mol. Cell. Biol. 27:4825-4843.
40. McClellan, K., and R. S. Slack. 2007. Specific in vivo roles for E2Fs in differentiation and development. Cell Cycle 6:2917-2927.
41. Mulligan, G. J., J. Wong, and T. Jacks. 1998. p130 is dispensable in peripheral T lymphocytes: evidence for functional compensation by p107 and p130. Mol. Cell. Biol. 18:206-220.
42. Narita, M., S. Nunez, E. Heard, M. Narita, A. W. Lin, S. A. Hearn, D. L. Spector, G. J. Hannon, and S. W. Lowe. 2003. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 113:703-716.
43. Nielsen, S. J., R. Schneider, U. M. Bauer, A. J. Bannister, A. Morrison, D. O'Carroll, R. Firestein, M. Cleary, T. Jenuwein, R. E. Herrera, and T. Kouzarides. 2001. Rb targets histone H3 methylation and HP1 to promoters. Nature 412:561-565.
44. 2 phases of the cell cycle. J. Cell Biol. 135:441-456.
45. Panteleeva, I., S. Boutillier, V. See, D. Spiller, C. Rouaux, G. Almouzni, D. Bailly, C. Maison, H. Lai, J. Loeffler, and A. Boutillier. 2007. HP1alpha guides neuronal fate by timing E2F-targeted genes silencing during terminal differentiation. EMBO J. 26:3616-3628.
46. Peeper, D., J. Dannenberg, S. Douma, H. teRiele, and R. Bernards. 2001. Escape from premature senescence is not sufficient for oncogenic transformation by ras. Nat. Cell Biol. 3:198-203.
47. Regha, K., M. A. Sloane, R. Huang, F. M. Pauler, K. E. Warczok, B. Melikant, M. Radolf, J. H. Martens, G. Schotta, T. Jenuwein, and D. P. Barlow. 2007. Active and repressive chromatin are interspersed without spreading in an imprinted gene cluster in the mammalian genome. Mol. Cell 27:353-366.
48. Robertson, K. D., S. Ait-Si-Ali, T. Yokochi, P. A. Wade, P. L. Jones, and A. P. Wolffe. 2000. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat. Genet. 25:338-342.
49. Rowland, B. D., S. G. Denissov, S. Douma, H. G. Stunnenberg, R. Bernards, and D. S. Peeper. 2002. E2F transcriptional repressor complexes are critical downstream targets of p19arf/p53-induced proliferative arrest. Cancer Cell 2:55-65.
50. 1 control and immortalization. Genes Dev. 14:3037-3050.
51. Serrano, M., A. W. Lin, M. E. McCurrach, D. Beach, and S. W. Lowe. 1997. Oncogenic ras provokes premature senescence associated with accumulation of p53 and p16. Cell 88:593-602.
52. Sharpless, N. E., N. Bardeesy, K. H. Lee, D. Carrasco, D. H. Castrillon, A. J. Aguirre, E. A. Wu, J. W. Horner, and R. A. DePinho. 2001. Loss of p16Ink4a with retention of p19Arf predisposes mice to tumorigenesis. Nature 413: 86-91.
53. Singh, P., J. Coe, and W. Hong. 1995. A role for retinoblastoma protein in potentiating transcriptional activation by the glucocorticoid receptor. Nature 374:562-565.
54. Steer, C. J. 1995. Liver regeneration. FASEB J. 9:1396-1400.
55. Todaro, G. J., and H. Green. 1963. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17:299-313.
56. Zacksenhaus, E., Z. Jiang, D. Chung, J. D. Marth, R. A. Phillips, and B. L. Gallie. 1996. pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev. 10:3051-3064.
57. Zhang, J., J. Gray, L. Wu, G. Leone, S. Rowan, C. L. Cepko, X. Zhu, C. M. Craft, and M. A. Dyer. 2004. Rb regulates proliferation and rod photoreceptor development in the mouse retina. Nat. Genet. 36:351-360.
58. Zhang, R., W. Chen, and P. Adams. 2007. Molecular dissection of formation of senescence-associated heterochromatin foci. Mol. Cell. Biol. 27:2343-2358.