The cell cycle and development: Redundant roles of cell cycle regulators

Current Opinion in Cell Biology

Volumn 11, Issue 6, 1999, Pages 655-662

  Zhang, Pumin ^a  

^a NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE; PROTEIN P27; RETINOBLASTOMA PROTEIN;

CELL CYCLE; CELL PROLIFERATION; DEVELOPMENT; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

EID: 0032707409     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(99)00032-0     Document Type: Review

References (65)

1. Weinberg R.A. The retinoblastoma protein and cell cycle control. Cell. 81:1995;323-330.
2. Harper J.W., Elledge S.J. Cdk inhibitors in development and cancer. Curr Opin Genet Dev. 6:1996;56-64.
3. Geng Y, Eaton E.N., Picon M., Roberts J.M., Lundberg A.S., Gifford A., Sardet C., Weinberg R.A. Regulation of cyclin E transcription by E2Fs and retinoblastoma protein. Oncogene. 12:1996;1173-1180.
4. Botz J., Zerfass-Thome K., Spitkovsky D., Delius H., Vogt B., Eilers M., Hatzigeorgiou A., Jansen-Durr P. Cell cycle regulation of the murine cyclin E gene depends on an E2F binding site in the promoter. Mol Cell Biol. 16:1996;3401-3409.
5. Ohtani K., DeGregori J, Nevins J.R. Regulation of the cyclin E gene by transcription factor E2F1. Proc Natl Acad Sci USA. 92:1995;12146-12150.
6. Dyson N. The regulation of E2F by pRb-family proteins. Genes Dev. 12:1998;2245-2262. This is an in depth review of function of E2F and its regulation by pRb family proteins.
7. •], this paper shows that pRb is capable of recruiting histone deacetylase (HDAC) to E2F. Therefore, pRb suppresses E2F's transcriptional activation activity not only through masking E2F's activation domain but also through modifying chromatin structure via HDAC.
8. •].
9. •].
10. Grunstein M. Histone acetylation in chromatin structure and transcription. Nature. 389:1997;349-352.
11. Gu W., Schneider J.W., Condorelli G., Kaushal S., Mahdavi V., Nadal-Ginard B. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell. 72:1993;309-324.
12. Novitch B.G., Mulligan G.J., Jacks T., Lassar A.B. 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. 135:1996;441-456.
13. Nead M.A., Baglia L.A., Antinore M.J., Ludlow J.W., McCance D.J. Rb binds c-Jun and activates transcription. EMBO J. 17:1998;2342-2352.
14. Chen P.L., Riley D.J., Chen Y., Lee W.H. Retinoblastoma protein positively regulates terminal adipocyte differentiation through direct interaction with C/EBPs. Genes Dev. 10:1996;2794-2804.
15. Sellers W.R., Novitch B.G., Miyake S., Heith A., Otterson G.A., Kaye F.J., Lassar A.B., Kaelin W.G. Jr. Stable binding to E2F is not required for the retinoblastoma protein to activate transcription promote differentiation and suppress tumor cell growth. Genes Dev. 12:1998;95-106. Some mutant forms of pRb isolated from human tumors or generated through site-directed mutagenesis were shown to have lost E2F-binding ability but to have retained the ability to stimulate differentiation (i.e. they were still capable of activating the expression of genes associated with differentiated phenotypes). This result indicates that transcriptional repressor and activator functions of pRb are separable and are likely to be unrelated. Interestingly these human pRb mutants are associated with a low risk of retinoblastoma suggesting that the tumor suppressing function of pRb also relies at least partially on its ability to promote differentiation.
16. Dunaief J.L., Strober B.E., Guha S., Khavari P.A., Alin K., Luban J., Begemann M., Crabtree G.R., Goff S.P. The retinoblastoma protein and BRG1 form a complex and cooperate to induce cell cycle arrest. Cell. 79:1994;119-130.
17. Strober B.E., Dunaief J.L., Guha Goff S.P. Functional interactions between the hBRM/hBRG1 transcriptional activators and the pRB family of proteins. Mol Cell Biol. 16:1996;1576-1583.
18. Singh P., Coe J., Hong W. A role for retinoblastoma protein in potentiating transcriptional activation by the glucocorticoid receptor. Nature. 374:1995;562-565.
19. Shao Z., Ruppert S., Robbins P.D. The retinoblastoma-susceptibility gene product binds directly to the human TATA-binding protein-associated factor TAFII250. Proc Natl Acad Sci USA. 92:1995;3115-3119.
20. Ruppert S., Wang E.H., Tjian R. Cloning and expression of human TAFII250: a TBP-associated factor implicated in cell-cycle regulation. Nature. 362:1993;175-179.
21. Mizzen C.A., Yang X.J., Kokubo T., Brownell J.E., Bannister A.J., Owen-Hughes T., Workman J., Wang L., Berger S.L., Kouzarides T.et al. The TAF(II) 250 subunit of TFIID has histone acetyltransferase activity. Cell. 87:1996;1261-1270.
22. Cobrinik D., Lee M-H., Hannon G., Mulligan G., Bronson R.T., Dyson N., Harlow E., Beach D., Weinberg R.A., Jacks T. Shared role of the pRB-related p130 and p107 proteins in limb development. Genes Dev. 10:1996;1633-1644.
23. Lee M-H., Williams B.O., Mulligan G., Mukai S., Bronson R.T., Dyson N., Harlow E., Jacks T. Targeted disruption of p107: functional overlap between p107 and Rb. Genes Dev. 10:1996;1621-1632.
24. Clarke A.R., Maandag E.R., van Roon M., van der Lugt N.M., van der Valk M., Hooper M.L., Berns A., te Riele H. Requirement for a functional Rb-1 gene in murine development. Nature. 359:1992;328-330.
25. Jacks T., Fazeli A., Schmitt E.M., Bronson R.T., Goodell M.A., Weinberg R.A. Effects of an Rb mutation in the mouse. Nature. 359:1992;295-300.
26. Lee E.Y., Chang C.Y., Hu N., Wang Y.C., Lai C.C., Herrup K., Lee W.H., Bradley A. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature. 359:1992;288-294.
27. Zacksenhaus E., Jiang Z., Chung D., Marth J.D., Phillips R.A., Gallie B.L. pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev. 10:1996;3051-3064.
28. Tsai K.Y., Hu Y., Macleod K.F., Crowley D., Yamasaki L., Jacks T. Mutation of E2F-1 suppresses apoptosis and inappropriate S phase entry and extends survival of Rb-deficient mouse embryos. Mol Cell. 2:1998;293-304. This paper demonstrates that increased rates of proliferation and apoptosis in Rb-null embryos are largely owing to unrestrained E2F-1 activity. Many other developmental defects persist in the Rb and E2F-1 double mutant, however, highlighting the developmental importance of functions of pRb other than controlling E2F-1.
29. Novitch B.G., Spicer D.B., Kim P.S., Cheung W.L., Lassar A.B. pRb is required for MEF2-dependent gene expression as well as cell-cycle arrest during skeletal muscle differentiation. Curr Biol. 9:1999;449-459. It has been known for some time that pRb is required for proper skeletal muscle differentiation, but which myogenic transcription factors require pRb activity remains elusive. Apparently it is not MyoD, despite the demonstration that MyoD interacts with pRb directly, since early events of skeletal muscle differentiation such as expression of p21 and myogenin proceed normally in the absence of pRb. This paper identifies MEF2 proteins as critical transcription factors that require the function of pRb in myogenesis, particularly for the expression of later differentiation markers such as myosin heavy chain.
30. Molkentin J.D., Black B.L., Martin J.F., Olson E.N. Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell. 83:1995;1125-1136.
31. Cip1 in muscle and other terminally differentiating cells. Science. 267:1995;1024-1027.
32. Halevy O., Novitch B.G., Spicer D.B., Skapek S.X., Rhee J., Hannon G.J., Beach D., Lassar A.B. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science. 267:1995;1018-1021.
33. Guo K., Wang J., Andres V., Smith R.C., Walsh K. MyoD-induced expression of p21 inhibits cyclin-dependent kinase activity upon myocyte terminal differentiation. Mol Cell Biol. 15:1995;3823-3829.
34. CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell. 82:1995;675-684.
35. Brugarolas J., Chandrasekaran C., Gordon J.I., Beach D., Jacks T., Hannon G.J. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature. 377:1995;552-557.
36. KIP2 is parallel but independent, suggesting that, in response to differentiation signals, these proteins are coordinately regulated to trigger both cell cycle exit and a dependent muscle-specific program of gene expression in order to initiate myoblast terminal differentiation and muscle formation.
37. CIP1 Cdk inhibitor family, is a candidate tumor suppressor gene. Genes Dev. 9:1995;650-662.
38. KIP2indicates a role in Beckwith-Wiedemann syndrome. Nature. 387:1997;151-158.
39. Kip2 results in increased apoptosis and delayed differentiation during mouse development. Genes Dev. 11:1997;973-983.
40. Venuti J.M., Morris J.H., Vivian J.L., Olson E.N., Klein W.H. Myogenin is required for late but not early aspects of myogenesis during mouse development. J Cell Biol. 128:1995;563-576.
41. -/- muscle cells. Science. 264:1994;1467-1471.
42. Cip1/WAF1in differentiation of primary mouse keratinocytes independent of cell cycle control. Science. 280:1998;1069-1072.
43. Zhang J.M., Wei Q., Zhao X., Paterson B.M. Coupling of the cell cycle and myogenesis through the cyclin D1-dependent interaction of MyoD with Cdk4. EMBO J. 18:1999;926-933.
44. Morgenbesser S.D., Williams B.O., Jacks T., DePinho R.A. p53-dependent apoptosis produced by Rb-deficiency in the developing mouse lens. Nature. 371:1994;72-74.
45. Piatigorsky J. Lens differentiation in vertebrates. A review of cellular and molecular features. Differentiation. 19:1981;134-153.
46. McAvoy J.W. Induction of the eye lens. Differentiation. 17:1980;137-149.
47. DeGregori J., Leone G., Miron A., Jakoi L., Nevins J. Distinct roles for E2F proteins in cell growth control and apoptosis. Proc Natl Acad Sci USA. 94:1999;7245-7250.
48. Quelle D.E., Zindy F., Ashmun R.A., Sherr C.J. Alternative reading frames of the INK4A tumour supressor gene encode two unrelated proteins capable of inducing cell cycle arrest. Cell. 83:1995;993-1000.
49. Pomerantz J., Schreiber-Agus N., Liegeois N.J., Silverman A., Alland L., Chin L., Potes J., Chen K., Orlow I., Lee H.W., Cordon-Cardo C., DePinho R.A. The Ink4a tumour suppressor gene product, p19Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell. 92:1998;713-723.
50. Zhang Y., Xiong Y., Yarbrough W.G. ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumour suppression pathways. Cell. 92:1992;725-734.
51. KIP2 deficiency.
52. Kip1-deficient mice. Cell. 85:1996;733-744.
53. Kip1. Cell. 85:1996;721-732.
54. Kip1 display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell. 85:1996;707-720.
55. INK4c is uniquely required for the proliferation control of B- and T- cells.
56. Sherr C.J. Cancer cell cycles. Science. 274:1996;1672-1677.
57. Ohtsubo M, Theodoras A.M., Schumacher J., Roberts J.M., Pagano M. Human cyclin E, a nuclear protein essential for the G1-to-S phase transition. Mol Cell Biol. 15:1995;2612-2624.
58. Lacey K.R., Jackson P.K., Stearns T. Cyclin-dependent kinase control of centrosome duplication. Proc Natl Acad Sci USA. 96:1999;2817-2822.
59. Matsumoto Y., Hayashi K., Nishida E. Cyclin-dependent kinase 2 (Cdk2) is required for centrosome duplication in mammalian cells. Curr Biol. 9:1999;429-432.
60. Hinchcliffe E.H., Li C., Thompson E.A., Maller J.L., Sluder G. Requirement of Cdk2-cyclin E activity for repeated centrosome reproduction in Xenopus egg extracts. Science. 283:1999;851-854.
61. Sicinski P., Donaher J.L., Parker S.B., Li T., Fazeli A., Gardner H., Haslam S.Z., Bronson R.T., Elledge S.J., Weinberg R.A. Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell. 82:1995;621-630.
62. KIP1.
63. Draetta G.F. Mammalian G1 cyclins. Curr Opin Cell Biol. 6:1994;842-846.
64. Rane S.G., Dubus P., Mettus R.V., Galbreath E.J., Boden G., Reddy E.P., Barbacid M. Loss of Cdk4 expression causes insulin-deficient diabetes and Cdk4 activation results in beta-islet cell hyperplasia. Nat Genet. 22:1999;44-52. It is shown here that Cdk4 is dispensable for embryonic development in mice, indicating its function is either not required or is compensated for by other Cdks, most likely Cdk6. Cdk4 is essential for postnatal development, however, as mice null for Cdk4 grow much slower than their wild type littermates and achieve less body weight by adulthood. Furthermore, Cdk4 inactivation not only causes a global deficiency in proliferation but also has particular impact on the development of pancreas β-islet cells and reproductive systems. As a result, Cdk4-null mice are diabetic owing to insulin insufficiency and both males and females are infertile.
65. Sicinski P., Donaher J.L., Geng Y., Parker S.B., Gardner H., Park M.Y., Robker R.L., Richards J.S., McGinnis L.K., Biggers J.D.et al. Cyclin D2 is an FSH-responsive gene involved in gonadal cell proliferation and oncogenesis. Nature. 384:1996;470-474.