Role of the retinoblastoma tumor suppressor protein in cellular differentiation

Journal of Cellular Biochemistry

Volumn 94, Issue 5, 2005, Pages 870-879

  Nguyen, Don X ^a,b   McCance, Dennis J ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Cellular differentiation; Rb; Tumor suppressor

Indexed keywords

HISTONE DEACETYLASE; MYOD PROTEIN; PROTEIN MDM2; PROTEIN P107; PROTEIN P130; PROTEIN P16INK4A; PROTEIN P300; PROTEIN RB105; RETINOBLASTOMA PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

CANCER; CARCINOGENESIS; CELL CYCLE; CELL DIFFERENTIATION; GENE MUTATION; HUMAN; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; RETINOBLASTOMA; REVIEW; TISSUE DIFFERENTIATION; ANIMAL; NEOPLASM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; HUMANS; NEOPLASMS; RETINOBLASTOMA PROTEIN;

EID: 24344507918     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcb.20375     Document Type: Review

References (71)

1. Balsitis SJ, Sage J, Duensing S, Munger K, Jacks T, Lambert PF. 2003. Recapitulation of the effects of the human papillomavirus type 16 E7 oncogene on mouse epithelium by somatic Rb deletion and detection of pRb-independent effects of E7 in vivo. Mol Cell Biol 23:9094-9103.
2. Bavner A, Johansson L, Toresson G, Gustafsson JA, Treuter E. 2002. A transcriptional inhibitor targeted by the atypical orphan nuclear receptor SHP. EMBO Rep 3:478-484.
3. Chan HM, Krstic-Demonacos M, Smith L, Demonacos C, La Thangue NB. 2001. Acetylation control of the retinoblastoma tumour-suppressor protein. Nat Cell Biol 3:667-674.
4. Chau BN, Wang JY. 2003. Coordinated regulation of life and death by RB. Nat Rev Cancer 3:130-138.
5. Chen PL, Riley DJ, Chen Y, Lee WH. 1996. Retinoblastoma protein positively regulates terminal adipocyte differentiation through direct interaction with C/EBPs. Genes Dev 10:2794-2804.
6. Chen D, Livne-Bar I, Vanderluit JL, Slack RS, Agochiya M, Bremner R. 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.
7. Chin L, Pomerantz J, DePinho RA. 1998. The INK4a/ARF tumor suppressor: One gene-two products-two pathways. Trends Biochem Sci 23:291-296.
8. Clarke AR, Maandag ER, van Roon M, van der Lugt NM, van der Valk M, Hooper ML, Berns A, te Riele H. 1992. Requirement for a functional Rb-1 gene in murine development. Nature 359:328-330.
9. Classon M, Dyson N. 2001. p107 and p130: Versatile proteins with interesting pockets. Exp Cell Res 264:135-147.
10. Classon M, Harlow E. 2002. The retinoblastoma tumour suppressor in development and cancer. Nat Rev Cancer 2:910-917.
11. Cobrinik D, Lee MH, Hannon G, Mulligan G, Bronson RT, Dyson N, Harlow E, Beach D, Weinberg RA, Jacks T. 1996. Shared role of the pRB-related p130 and p107 proteins in limb development. Genes Dev 10:1633-1644.
12. Dannenberg JH, van Rossum A, Schuijff L, te Riele H. 2000. Ablation of the retinoblastoma gene family deregulates G(1) control causing immortalization and increased cell turnover under growth-restricting conditions. Genes Dev 14:3051-3064.
13. Davis RL, Cheng PF, Lassar AB, Weintraub H. 1990. The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell 60:733-746.
14. Durfee T, Becherer K, Chen PL, Yeh SH, Yang Y, Kilburn AE, Lee WH, Elledge SJ. 1993. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev 7:555-569.
15. Dyson N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev 12:2245-2262.
16. Ganguli G, Wasylyk B. 2003. p53-independent functions of MDM2. Mol Cancer Res 1:1027-1035.
17. Gu W, Schneider JW, Condorelli G, Kaushal S, Mahdavi V, Nadal-Ginard B. 1993. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell 72:309-324.
18. Halevy O, Novitch BG, Spicer DB, Skapek SX, Rhee J, Hannon GJ, Beach D, Lassar AB. 1995. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science 267:1018-1021.
19. Hanahan D, Weinberg RA. 2000. The hallmarks of cancer. Cell 100:57-70.
20. Harbour JW, Dean DC. 2000a. Rb function in cell-cycle regulation and apoptosis. Nat Cell Biol 2:E65-E67.
21. Harbour JW, Dean DC. 2000b. The Rb/E2F pathway: Expanding roles and emerging paradigms. Genes Dev 14:2393-2409.
22. Harris H. 2004. Tumour suppression: Putting on the brakes. Nature 427:201.
23. Hinds PW, Mittnacht S, Dulic V, Arnold A, Reed SI, Weinberg RA. 1992. Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell 70:993-1006.
24. Iezzi S, Di Padova M, Serra C, Caretti G, Simone C, Maklan E, Minetti G, Zhao P, Hoffman EP, Puri PL, Sartorelli V. 2004. Deacetylase inhibitors increase muscle cell size by promoting myoblast recruitment and fusion through induction of follistatin. Dev Cell 6:673-684.
25. Iyer NG, Ozdag H, Caldas C. 2004. p300/CBP and cancer. Oncogene 23:4225-4231.
26. Jacks T, Fazeli A, Schmitt EM, Bronson RT, Goodell MA, Weinberg RA. 1992. Effects of an Rb mutation in the mouse. Nature 359:295-300.
27. Lassar AB, Buskin JN, Lockshon D, Davis RL, Apone S, Hauschka SD, Weintraub H. 1989. MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell 58:823-831.
28. LeCouter JE, Kablar B, Hardy WR, Ying C, Megeney LA, May LL, Rudnicki MA. 1998a. Strain-dependent myeloid hyperplasia, growth deficiency, and accelerated cell cycle in mice lacking the Rb-related p107 gene. Mol Cell Biol 18:7455-7465.
29. LeCouter JE, Kablar B, Whyte PF, Ying C, Rudnicki MA. 1998b. Strain-dependent embryonic lethality in mice lacking the retinoblastoma-related p130 gene. Development 125:4669-4679.
30. Lee EY, Chang CY, Hu N, Wang YC, Lai CC, Herrup K, Lee WH, Bradley A. 1992. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359:288-294.
31. Lee C, Chang JH, Lee HS, Cho Y. 2002. Structural basis for the recognition of the E2F transactivation domain by the retinoblastoma tumor suppressor. Genes Dev 16:3199-3212.
32. Lees JA, Buchkovich KJ, Marshak DR, Anderson CW, Harlow E. 1991. The retinoblastoma protein is phosphorylated on multiple sites by human cdc2. Embo J 10:4279-4290.
33. Li FQ, Coonrod A, Horwitz M. 2000. Selection of a dominant negative retinoblastoma protein (RB) inhibiting satellite myoblast differentiation implies an indirect interaction between MyoD and RB. Mol Cell Biol 20:5129-5139.
34. Lin BT, Gruenwald S, Morla AO, Lee WH, Wang JY. 1991. Retinoblastoma cancer suppressor gene product is a substrate of the cell cycle regulator cdc2 kinase. Embo J 10:857-864.
35. Lipinski MM, Jacks T. 1999. The retinoblastoma gene family in differentiation and development. Oncogene 18:7873-7882.
36. Lipinski MM, Macleod KF, Williams BO, Mullaney TL, Crowley D, Jacks T. 2001. Cell-autonomous and non-cell-autonomous functions of the Rb tumor suppressor in developing central nervous system. Embo J 20:3402-3413.
37. Ludlow JW, Glendening CL, Livingston DM, DeCarprio JA. 1993. Specific enzymatic dephosphorylation of the retinoblastoma protein. Mol Cell Biol 13:367-372.
38. Lukas J, Parry D, Aagaard L, Mann DJ, Bartkova J, Strauss M, Peters G, Bartek J. 1995. Retinoblastoma-protein-dependent cell-cycle inhibition by the tumour suppressor p16. Nature 375:503-506.
39. MacLellan WR, Xiao G, Abdellatif M, Schneider MD. 2000. A novel Rb- and p300-binding protein inhibits transactivation by MyoD. Mol Cell Biol 20:8903-8915.
40. MacPherson D, Sage J, Crowley D, Trumpp A, Bronson RT, Jacks T. 2003. Conditional mutation of Rb causes cell cycle defects without apoptosis in the central nervous system. Mol Cell Biol 23:1044-1053.
41. MacPherson D, Sage J, Kim T, Ho D, McLaughlin ME, Jacks T. 2004. Cell type-specific effects of Rb deletion in the murine retina. Genes Dev 18:1681-1694.
42. McKinsey TA, Zhang CL, Olson EN. 2001. Control of muscle development by dueling HATs and HDACs. Curr Opin Genet Dev 11:497-504.
43. Medema RH, Herrera RE, Lam F, Weinberg RA. 1995. Growth suppression by p16ink4 requires functional retinoblastoma protein. Proc Natl Acad Sci USA 92:6289-6293.
44. Miyake S, Sellers WR, Safran M, Li X, Zhao W, Grossman SR, Gan J, DeCaprio JA, Adams PD, Kaelin WG, Jr. 2000. Cells degrade a novel inhibitor of differentiation with E1A-like properties upon exiting the cell cycle. Mol Cell Biol 20:8889-8902.
45. Mulligan G, Jacks T. 1998. The retinoblastoma gene family: Cousins with overlapping interests. Trends Genet 14:223-229.
46. Nguyen DX, Baglia LA, Huang SM, Baker CM, McCance DJ. 2004. Acetylation regulates the differentiation-specific functions of the retinoblastoma protein. Embo J 23:1609-1618.
47. Novitch BG, Mulligan GJ, Jacks T, Lassar AB. 1996. Skeletal muscle cells lacking the retinoblastoma protein display defects in muscle gene expression and accumulate in S and G2 phases of the cell cycle. J Cell Biol 135:441-456.
48. Novitch BG, Spicer DB, Kim PS, Cheung WL, Lassar AB. 1999. pRb is required for MEF2-dependent gene expression as well as cell-cycle arrest during skeletal muscle differentiation. Curr Biol 9:449-459.
49. Parker SB, Eichele G, Zhang P, Rawls A, Sands AT, Bradley A, Olson EN, Harper JW, Elledge SJ. 1995. p53-independent expression of p21Cip1 in muscle and other terminally differentiating cells. Science 267:1024-1027.
50. Puri PL, Iezzi S, Stiegler P, Chen TT, Schiltz RL, Muscat GE, Giordano A, Kedes L, Wang JY, Sartorelli V. 2001. Class I histone deacetylases sequentially interact with MyoD and pRb during skeletal myogenesis. Mol Cell 8:885-897.
51. Robanus-Maandag E, Dekker M, van der Valk M, Carrozza ML, Jeanny JC, Dannenberg JH, Berns A, te Riele H. 1998. p107 is a suppressor of retinoblastoma development in pRb-deficient mice. Genes Dev 12:1599-1609.
52. Ross JF, Liu X, Dynlacht BD. 1999. Mechanism of transcriptional repression of E2F by the retinoblastoma tumor suppressor protein. Mol Cell 3:195-205.
53. Ruiz S, Santos M, Segrelles C, Leis H, Jorcano JL, Berns A, Paramio JM, Vooijs M. 2004. Unique and overlapping functions of pRb and p107 in the control of proliferation and differentiation in epidermis. Development 131:2737-2748.
54. Sabourin LA, Girgis-Gabardo A, Seale P, Asakura A, Rudnicki MA. 1999. Reduced differentiation potential of primary MyoD-/- myogenic cells derived from adult skeletal muscle. J Cell Biol 144:631-643.
55. Sage J, Mulligan GJ, Attardi LD, Miller A, Chen S, Williams B, Theodorou E, Jacks T. 2000. Targeted disruption of the three Rb-related genes leads to loss of G(1) control and immortalization. Genes Dev 14:3037-3050.
56. Saunders N, Dicker A, Popa C, Jones S, Dahler A. 1999. Histone deacetylase inhibitors as potential anti-skin cancer agents. Cancer Res 59:399-404.
57. Schneider JW, Gu W, Zhu L, Mahdavi V, Nadal-Ginard B. 1994. Reversal of terminal differentiation mediated by pl07 in Rb-/- muscle cells. Science 264:1467-1471.
58. Sellers WR, Novitch BG, Miyake S, Heith A, Otterson GA, Kaye FJ, Lassar AB, Kaelin WG, Jr. 1998. Stable binding to E2F is not required for the retinoblastoma protein to activate transcription, promote differentiation, and suppress tumor cell growth. Genes Dev 12:95-106.
59. Shapiro GI, Edwards CD, Kobzik L, Godleski J, Richards W, Sugarbaker DJ, Rollins BJ. 1995. Reciprocal Rb inactivation and p16INK4 expression in primary lung cancers and cell lines. Cancer Res 55:505-509.
60. Sherr CJ. 2004. Principles of tumor suppression. Cell 116:235-246.
61. Stevaux O, Dyson NJ. 2002. A revised picture of the E2F transcriptional network and RB function. Curr Opin Cell Biol 14:684-691.
62. Takahashi Y, Rayman JB, Dynlacht BD. 2000. Analysis of promoter binding by the E2F and pRB families in vivo: Distinct E2F proteins mediate activation and repression. Genes Dev 14:804-816.
63. Thomas DM, Carty SA, Piscopo DM, Lee JS, Wang WF, Forrester WC, Hinds PW. 2001. The retinoblastoma protein acts as a transcriptional coactivator required for osteogenic differentiation. Mol Cell 8:303-316.
64. Tsai KY, Hu Y, Macleod KF, Crowley D, Yamasaki L, Jacks T. 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.
65. Vooijs M, Berns A. 1999. Developmental defects and tumor predisposition in Rb mutant mice. Oncogene 18:5293-5303.
66. Wells J, Boyd KE, Fry CJ, Bartley SM, Farnham PJ. 2000. Target gene specificity of E2F and pocket protein family members in living cells. Mol Cell Biol 20:5797-5807.
67. Wu L, de Bruin A, Saavedra HI, Starovic M, Trimboli A, Yang Y, Opavska J, Wilson P, Thompson JC, Ostrowski MC, Rosol TJ, Woollett LA, Weinstein M, Cross JC, Robinson ML, Leone G. 2003. Extra-embryonic function of Rb is essential for embryonic development and viability. Nature 421:942-947.
68. Yamasaki L, Bronson R, Williams BO, Dyson NJ, Harlow E, Jacks T. 1998. Loss of E2F-1 reduces tumorigenesis and extends the lifespan of Rb1 (+/-) mice. Nat Genet 18:360-364.
69. Zacksenhaus E, Jiang Z, Chung D, Marth JD, Phillips RA, Gallie BL. 1996. pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev 10:3051-3064.
70. Zhang HS, Dean DC. 2001. Rb-mediated chromatin structure regulation and transcriptional repression. Oncogene 20:3134-3138.
71. Zhang J, Gray J, Wu L, Leone G, Rowan S, Cepko CL, Zhu X, Craft CM, Dyer MA. 2004. Rb regulates proliferation and rod photoreceptor development in the mouse retina. Nat Genet 29:29.