Control of pRB phosphorylation

Current Opinion in Genetics and Development

Volumn 8, Issue 1, 1998, Pages 21-27

  Mittnacht, Sibylle ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; CYCLIN E; CYCLINE; GROWTH FACTOR; RETINOBLASTOMA PROTEIN;

CELL CYCLE; DEPHOSPHORYLATION; ENZYME ACTIVATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

EID: 0031935648     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(98)80057-9     Document Type: Article

References (69)

1. Hall M, Peters G. Genetic alterations of cyclins, cyclin-dependent kinases, and Cdk inhibitors in human cancer. Adv Cancer Res. 68:1996;67-108.
2. Palmero I, Peters G. Perturbation of cell cycle regulators in human cancer. Cancer Surv. 27:1996;351-367.
3. 1 cyclin-dependent kinases. Genes Dev. 9:1995;1149-1163.
4. Bartek J, Bartkova J, Lukas J. The retinoblastoma protein pathway and the restriction point. Curr Opin Cell Biol. 8:1996;805-814.
5. 1 restriction point. Crit Rev Oncogenesis. 7:1996;127-142.
6. Sanchez I, Dynlacht BD, tiTranscriptional control of the cell cycle. Curr Opin Cell Biol. 8:1996;318-324.
7. Mittnacht S, Lees JA, Desai D, Harlow E, Morgan DO, Weinberg RA. Distinct sub-populations of the retinoblastoma protein show a distinct pattern of phosphorylation. EMBO J. 13:1994;118-127.
8. 1/S phosphorylation of the retinoblastoma protein is associated with an altered affinity for the nuclear compartment. Cell. 65:1991;381-393.
9. Buchkovich K, Duffy LA, Harlow E. The retinoblastoma protein is phosphorylated during specific phases of the cell cycle. Cell. 58:1989;1097-1105.
10. DeCaprio JA, Ludlow JW, Lynch D, Furukawa Y, Griffin J, Piwnica WH, Huang CM, Livingston DM. The product of the retinoblastoma susceptibility gene has properties of a cell cycle regulatory element. Cell. 58:1989;1085-1095.
11. Chen PL, Scully P, Shew JY, Wang JY, Lee WH. Phosphorylation of the retinoblastoma gene product is modulated during the cell cycle and cellular differentiation. Cell. 58:1989;1193-1198.
12. Ludlow JW, Shon J, Pipas JM, Livingston DM, DeCaprio JA. The retinoblastoma susceptibility gene product undergoes cell cycle-dependent dephosphorylation and binding to and release from SV40 large T. Cell. 60:1990;387-396.
13. Mittnacht S, Hinds PW, Dowdy SF, Weinberg RA. Modulation of retinoblastoma protein activity during the cell cycle. Cold Spring Harb Symp Quant Biol. 56:1991;197-209.
14. Weinberg RA. The retinoblastoma protein and cell cycle control. Cell. 81:1995;323-330.
15. Nelson DA, Krucher NA, Ludlow JW. High molecular weight protein phosphatase type 1 dephosphorylates the retinoblastoma protein. J Biol Chem. 272:1997;4528-4535.
16. Kwon YG, Lee SY, Choi Y, Greengard P, Nairn AC. Cell cycle-dependent phosphorylation of mammalian protein phosphatase 1 by cdc2 kinase. Proc Natl Acad Sci USA. 94:1997;2168-2173.
17. Puntoni F, Villa ME. Phosphorylation of protein phosphatase-1 isoforms by cdc2-cyclin B in vitro. Mol Cell Biochem. 171:1997;115-120.
18. 1 arrest in human cancer cells. Curr Biol. 7:1997;375-386.
19. Dohadwala M, da Ce SE, Hall FL, Williams RT, Carbonaro HD, Nairn AC, Greengard P, Berndt N. Phosphorylation and inactivation of protein phosphatase 1 by cyclin-dependent kinases. Proc Natl Acad Sci USA. 91:1994;6408-6412.
20. Ludlow JW, Nelson DA. Control and activity of type-1 serine/threonine protein phosphatase during the cell cycle. Semin Cancer Biol. 6:1995;195-202.
21. 1 restriction point fails to halt cell cycle progression. Oncogene. 15:1997;337-345.
22. 2 phases during hypoxic stress. Exp Cell Res. 227:1996;106-115.
23. Haapajarvi T, Kivinen L, Pitkanen K, Laiho M. Cell cycle dependent effects of UV-radiation on p53 expression and retinoblastoma protein phosphorylation. Oncogene. 11:1995;151-159.
24. 2 during the process of induced cell differentiation. Exp Cell Res. 214:1994;250-257.
25. Lin BT, Gruenwald S, Morla AO, Lee WH, Wang JY. Retinoblastoma cancer suppressor gene product is a substrate of the cell cycle regulator cdc2 kinase. EMBO J. 10:1991;857-864.
26. Lees JA, Buchkovich KJ, Marshak DR, Anderson CW, Harlow E. The retinoblastoma protein is phosphorylated on multiple sites by human cdc2. EMBO J. 10:1991;4279-4290.
27. DeCaprio JA, Furukawa Y, Ajchenbaum F, Griffin JD, Livingston DM. The retinoblastoma-susceptibility gene product becomes phosphorylated in multiple stages during cell cycle entry and progression. Proc Natl Acad Sci USA. 89:1992;1795-1798.
28. Kitagawa M, Higashi H, Jung HK, Suzuki-Takahashi I, Ikeda M, Tamai K, Kato JY, Segawa K, Yoshida E, Nishimura S, et al. The consensus motif for phosphorylation by cyclin D1 - Cdk4 is different from that for phosphorylation by cyclin A/E-Cdk2. of special interest EMBO J. 15:1996;7060-7069 This paper demonstrates that S780 in human pRB is specifically phosphorylated by Cyclin D/cdk4 and Cyclin D/cdk6 and that site specificity for these kinases may be determined by the immediately surrounding amino acid sequence.
29. Zarkowska T, Harlow E, Mittnacht S. Monoclonal antibodies specific for underphosphorylated retinoblastoma protein identify a cell cycle regulated phosphorylation site targeted by CDKs. of special interest Oncogene. 14:1997;249-254 This paper provides evidence for the first time that pRB may be phosphorylated differentially by different cyclin-dependent kinase in vitro, thus raising the possibility that pRB's phosphorylation by different members of this kinase family may have distinct biochemical consequences.
30. 1/S cyclin-dependent kinases. of special interest J Biol Chem. 272:1997;12738-12746 This paper demonstrates that different cyclin-dependent kinases phosphorylate a distinct (but overlapping) set of sites on pRB, perhaps explaining the differential ability of these kinases to dissociate preformed pRB/T antigen complexes.
31. Gu Y, Rosenblatt J, Morgan DO. Cell cycle regulation of CDK2 activity by phosphorylation of Thr160 and Tyr15. EMBO J. 11:1992;3995-4005.
32. Matsuoka M, Kato JY, Fisher RP, Morgan DO, Sherr CJ. Activation of cyclin-dependent kinase 4 (cdk4) by mouse MO15-associated kinase. Mol Cell Biol. 14:1994;7265-7275.
33. Perez RI, Solomon DL, Sewing A, Land H. Myc activation of cyclin E/Cdk2 kinase involves induction of cyclin E gene transcription and inhibition of p27(Kip1) binding to newly formed complexes. Oncogene. 14:1997;2373-2381.
34. Matsushime H, Quelle DE, Shurtleff SA, Shibuya M, Sherr CJ, Kato JY. D-type cyclin-dependent kinase activity in mammalian cells. Mol Cell Biol. 14:1994;2066-2076.
35. Massagué J, Polyak K. Mammalian antiproliferative signals and their targets. Curr Opin Genet Dev. 5:1995;91-96.
36. Polyak K, Kato JY, Solomon MJ, Sherr CJ, Massagué J, Roberts JM, Koff A. p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-β and contact inhibition to cell cycle arrest. Genes Dev. 8:1994;9-22.
37. Li JM, Nichols MA, Chandrasekharan S, Xiong Y, Wang XF. Transforming growth factor-β activates the promoter of cyclin-dependent kinase inhibitor p15INK4B through an Sp1 consensus site. J Biol Chem. 270:1995;26750-26753.
38. Chin YE, Kitagawa M, Su WC, You ZH, Iwamoto Y, Fu XY. Cell growth arrest and induction of cyclin-dependent kinase inhibitor p21 WAF1/CIP1 mediated by STAT1. Science. 272:1996;719-722.
39. Harvat BL, Seth P, Jetten AM. The role of p27Kip1 in gamma interferon-mediated growth arrest of mammary epithelial cells and related defects in mammary carcinoma cells. Oncogene. 14:1997;2111-2122.
40. Kuniyasu H, Yasui W, Kitahara K, Naka K, Yokozaki H, Akama Y, Hamamoto T, Tahara H, Tahara E. Growth inhibitory effect of interferon-beta is associated with the induction of cyclin-dependent kinase inhibitor p27Kip1 in a human gastric carcinoma cell line. Cell Growth Differ. 8:1997;47-52.
41. Sangfelt O, Erickson S, Einhorn S, Grander D. Induction of Cip/Kip and Ink4 cyclin dependent kinase inhibitors by interferon-alpha in hematopoietic cell lines. Oncogene. 14:1997;415-423.
42. 1 in mammalian cells: inhibition of cyclin E-dependent kinase by TGF-β Science. 260:1993;536-539.
43. Reynisdottir I, Polyak K, Iavarone A, Massagué J. Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-β Genes Dev. 9:1995;1831-1845.
44. Iavarone A, Massagué J. Repression of the CDK activator Cdc25A and cell-cycle arrest by cytokine TGF-β in cells lacking the CDK inhibitor p15. Nature. 387:1997;417-422.
45. Tiefenbrun N, Melamed D, Levy N, Resnitzky D, Hoffman I, Reed SI, Kimchi A. Alpha interferon suppresses the cyclin D3 and cdc25A genes, leading to a reversible G0-like arrest. Mol Cell Biol. 16:1996;3934-3944.
46. Peeper DS, Upton TM, Ladha MH, Neuman E, Zalvide J, Bernards R, DeCaprio JA, Ewen ME. Ras signalling linked to the cell-cycle machinery by the retinoblastoma protein. of outstanding interest Nature. 386:1997;177-181 This paper, along with [47], shows that Ras signalling is not required in cells that lack pRB expression or ectopically express Cyclin D, suggesting that Ras function is required for pRB inactivation and operates through activation of Cyclin D kinase.
47. Mittnacht S, Paterson H, Olson MF, Marshall CJ. Ras signalling is required for inactivation of the tumour suppressor pRb cell-cycle control protein. of outstanding interest Curr Biol. 7:1997;219-221 This paper demonstrates that cells lacking pRB expression or expression of the CDK-Inhibitor p16INK4b have a reduced requirement for Ras signalling, suggesting (along with [46]) the Ras is required for pRB inactivation via activation of Cyclin D kinase.
48. Filmus J, Robles AI, Shi W, Wong MJ, Colombo LL, Conti CJ. Induction of cyclin D1 overexpression by activated ras. Oncogene. 9:1994;3627-3633.
49. 1 progression in NIH 3T3 cells. Mol Cell Biol. 15:1995;3654-3663.
50. Albanese C, Johnson J, Watanabe G, Eklund N, Vu D, Arnold A, Pestell RG. Transforming p21ras mutants and c-Ets-2 activate the cyclin D1 promoter through distinguishable regions. J Biol Chem. 270:1995;23589-23597.
51. Lavoie JN, L'Allemain G, Brunet A, Muller R, Pouyssegur J. Cyclin D1 expression is regulated positively by the p42/p44MAPK and negatively by the p38/HOGMAPK pathway. J Biol Chem. 271:1996;20608-20616.
52. 1 cyclin - cdk complexes. EMBO J. 14:1995;4814-4826.
53. Vlach J, Hennecke S, Alevizopoulos K, Conti D, Amati B. Growth arrest by the cyclin-dependent kinase inhibitor p27Kip1 is abrogated by c-Myc. EMBO J. 15:1996;6595-6604.
54. Galaktionov K, Chen X, Beach D. Cdc25 cell-cycle phosphatase as a target of c-myc. Nature. 382:1996;511-517.
55. 1 phase of the human cell cycle. Science. 257:1992;1689-1694.
56. Sheaff RJ, Groudine M, Gordon M, Roberts JM, Clurman BE. Cyclin E - CDK2 is a regulator of p27Kip1. Genes Dev. 11:1997;1464-1478.
57. 1 to S phase in growth-stimulated rat FRTL-5 cells. J Biol Chem. 272:1997;13-16.
58. Rodriguez VP, Warne PH, Dhand R, Vanhaesebroeck B, Gout I, Fry MJ, Waterfield MD, Downward J. Phosphatidylinositol-3-OH kinase as a direct target of Ras [see comments]. Nature. 370:1994;527-532.
59. Ridley AJ. Signal transduction through the GTP-binding proteins Rac and Rho. J Cell Sci. 18:1994;127-131. (Suppl).
60. 1 arrest upon microinjection into SAOS2 cells. This indicates that phosphorylation by the two kinases is not equivalent.
61. Hinds PW, Mittnacht S, Dulic V, Arnold A, Reed SI, Weinberg RA. Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell. 70:1992;993-1006.
62. Ewen ME, Sluss HK, Sherr CJ, Matsushime H, Kato J, Livingston DM. Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell. 73:1993;487-497.
63. Knudsen ES, Wang JY. Differential regulation of retinoblastoma protein function by specific Cdk phosphorylation sites. of special interest J Biol Chem. 271:1996;8313-8320 This paper provides evidence, for the first time, that different sets of pRB phosphorylation sites regulate the interaction of pRB with different ligands. These observations support a hypothesis whereby distinctly phosphorylated pRB forms would regulate different pRB effector pathways.
64. Leone G, DeGregori J, Sears R, Jakoi L, Nevins JR. Myc and Ras collaborate in inducing accumulation of active cyclin E/Cdk2 and E2F. of special interest Nature. 387:1997;422-426 This paper demonstrates that c-Myc and oncogenic Ras co-operate to induce cell cycle progression in REF 52 cells in the absence of Cyclin D activation and pRB hyperphosphorylation, and thus would seem to support a notion whereby these oncoproteins may not operate as effectors of pRB phosphorylation but, instead, trigger cell cycle progression through events that operate downstream of or parallel to those controlled by pRB.
65. Alevizopoulos K, Vlach J, Hennecke S, Amati B. Cyclin E and c-Myc promote cell proliferation in the presence of p16INK4a and of hypophosphorylated retinoblastoma family proteins. of outstanding interest EMBO J. 16:1997;5322-5333 This paper demonstrates that both Cyclin E and c-Myc overcome a block by INK proteins and trigger the continuous proliferation of cells without inactivating pRB's ability to bind to E2F. These findings support the notion that Cyclin E synthesis is a key target of the Cyclin D/pRB phosphorylation pathway. Significantly (and along with the results presented in [66]) they challenge the notion that Cyclin E kinase is a bone fide upstream effector of pRB phosphorylation.
66. Lukas J, Herzinger T, Hansen K, Moroni MC, Resnitzky D, Helin K, Reed SI, Bartek J. Cyclin E-induced S phase without activation of the pRb/E2F pathway. of outstanding interest Genes Dev. 11:1997;1479-1492 This paper demonstrates that Cyclin E expression can trigger S phase entry in cells expressing phosphorylation defective pRB and that it does so without activating of E2F. It provides the most direct support for a notion whereby Cyclin E promotes cell cycle progression through pathways other than pRB phosphorylation.
67. Hurford RJ, Cobrinik D, Lee MH, Dyson N. pRB and p107/p130 are required for the regulated expression of different sets of E2F responsive genes. Genes Dev. 11:1997;1447-1463.
68. Geng Y, Eaton EN, Picon M, Roberts JM, Lundberg AS, Gifford A, Sardet C, Weinberg RA. Regulation of cyclin E transcription by E2Fs and retinoblastoma protein. Oncogene. 12:1996;1173-1180.
69. White RJ. Regulation of RNA polymerases I and III by the retinoblastoma protein: a mechanism for growth control? Tr Biochem Sci. 22:1997;77-80.