102
Views
763
CrossRef citations to date
0
Altmetric
Cell Growth and Development

Functional Inactivation of the Retinoblastoma Protein Requires Sequential Modification by at Least Two Distinct Cyclin-cdk Complexes

&
Pages 753-761 | Received 05 Jun 1997, Accepted 31 Oct 1997, Published online: 28 Mar 2023

REFERENCES

  • Buchkovich, K., L. A. Duffy, and E. Harlow 1989. The retinoblastoma protein is phosphorylated during specific phases of the cell cycle. Cell 58: 1097–1105.
  • Chellappan, S. P., S Hiebert, M. Mudryj, J. M. Horowitz, and J. R. Nevins 1991. The E2F transcription factor is a cellular target for the RB protein. Cell 65: 1053–1061.
  • Chen, C., and H. Okayama 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7: 2745–2752.
  • Chen, P. L., P. Scully, J. Y. Shew, J. Y. Wang, and W. H. Lee 1989. Phosphorylation of the retinoblastoma gene product is modulated during the cell cycle and cellular differentiation. Cell 58: 1193–1198.
  • Chen, W. D., G. A. Otterson, S. Lipkowitz, S. N. Khleif, A. B. Coxon, and F. J. Kaye 1997. Apoptosis is associated with cleavage of a 5 kDa fragment from RB which mimics dephosphorylation and modulates E2F binding. Oncogene 14: 1243–1248.
  • Connell-Crowley, L., J. W. Harper, and D. W. Goodrich 1997. Cyclin D1/cdk4 regulates retinoblastoma protein-mediated cell cycle arrest by site-specific phosphorylation. Mol. Biol. Cell 8: 287–301.
  • De Caprio, J. A., Y. Furukawa, F. Ajchenbaum, J. D. Griffin, and D. M. Livingston 1992. The retinoblastoma-susceptibility gene product becomes phosphorylated in multiple stages during cell cycle entry and progression. Proc. Natl. Acad. Sci. USA 89: 1795–1798.
  • De Caprio, J. A., J. W. Ludlow, D. Lynch, Y. Furukawa, J. Griffin, H. Piwnica-Worms, C. M. Huang, and D. M. Livingston 1989. The product of the retinoblastoma susceptibility gene has properties of a cell cycle regulatory element. Cell 58: 1085–1095.
  • Dimri, G. P., M. Nakanishi, P. Y. Desprez, J. R. Smith, and J. Campisi 1996. Inhibition of E2F activity by the cyclin-dependent protein kinase inhibitor p21 in cells expressing or lacking a functional retinoblastoma protein. Mol. Cell. Biol. 16: 2987–2997.
  • Dowdy, S. F., P. W. Hinds, K. Louie, S. I. Reed, A. Arnold, and R. A. Weinberg 1993. Physical interaction of the retinoblastoma protein with human D cyclins. Cell 73: 499–511.
  • Dulic, V., E. Lees, and S. I. Reed 1992. Association of human cyclin E with a periodic G1-S phase protein kinase. Science 257: 1958–1961.
  • Duronio, R. J., P. H. O’Farrell, J. E. Xie, A. Brook, and N. Dyson 1995. The transcription factor E2F is required for S phase during Drosophila embryogenesis. Genes Dev. 9: 1445–1455.
  • Dynlacht, B. D., O. Flores, J. A. Lees, and E. Harlow 1994. Differential regulation of E2F transactivation by cyclin/cdk2 complexes. Genes Dev. 8: 1772–1786.
  • Ewen, M. E., H. K. Sluss, C. J. Sherr, H. Matsushime, J. Kato, and D. M. Livingston 1993. Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell 73: 487–497.
  • Geng, Y., E. N. Eaton, M. Picon, J. M. Roberts, A. S. Lundberg, A. Gifford, C. Sardet, and R. A. Weinberg 1996. Regulation of cyclin E transcription by E2Fs and retinoblastoma protein. Oncogene 12: 1173–1180.
  • Girard, F., U. Strausfeld, A. Fernandez, and N. J. Lamb 1991. Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell 67: 1169–1179.
  • Hamel, P. A., B. L. Cohen, L. M. Sorce, B. L. Gallie, and R. A. Phillips 1990. Hyperphosphorylation of the retinoblastoma gene product is determined by domains outside the simian virus 40 large-T-antigen-binding regions. Mol. Cell. Biol. 10: 6586–6595.
  • Hamel, P. A., R. M. Gill, R. A. Phillips, and B. L. Gallie 1992. Regions controlling hyperphosphorylation and conformation of the retinoblastoma gene product are independent of domains required for transcriptional repression. Oncogene 7: 693–701.
  • Hatakeyama, M., J. A. Brill, G. R. Fink, and R. A. Weinberg 1994. Collaboration of G1 cyclins in the functional inactivation of the retinoblastoma protein. Genes Dev. 8: 1759–1771.
  • Hengstschlager, M., E. Hengstschlager-Ottnad, O. Pusch, and E. Wawra 1996. The role of p16 in the E2F-dependent thymidine kinase regulation. Oncogene 12: 1635–1643.
  • Hinds, P. W., S. Mittnacht, V. Dulic, A. Arnold, S. I. Reed, and R. A. Weinberg 1992. Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell 70: 993–1006.
  • Hofmann, F., and D. M. Livingston 1996. Differential effects of cdk2 and cdk3 on the control of pRb and E2F function during G1 exit. Genes Dev. 10: 851–861.
  • Horton, L. E., Y. Qian, and D. J. Templeton 1995. G1 cyclins control the retinoblastoma gene product growth regulation activity via upstream mechanisms. Cell Growth Differ. 6: 395–407.
  • Janicke, R. U., P. A. Walker, X. Y. Lin, and A. G. Porter 1996. Specific cleavage of the retinoblastoma protein by an ICE-like protease in apoptosis. EMBO J. 15: 6969–6978.
  • Jiang, W., S. M. Kahn, P. Zhou, Y. J. Zhang, A. M. Cacace, A. S. Infante, S. Doi, R. M. Santella, and I. B. Weinstein 1993. Overexpression of cyclin D1 in rat fibroblasts causes abnormalities in growth control, cell cycle progression and gene expression. Oncogene 8: 3447–3457.
  • Kato, J., H. Matsushime, S. W. Hiebert, M. E. Ewen, and C. J. Sherr 1993. Direct binding of cyclin D to the retinoblastoma gene product (pRb) and pRb phosphorylation by the cyclin D-dependent kinase CDK4. Genes Dev. 7: 331–342.
  • Kitagawa, M., H. Higashi, H. K. Jung, I. Suzuki-Takahashi, M. Ikeda, K. Tamai, J. Kato, K. Segawa, E. Yoshida, S. Nishimura, and Y. Taya 1996. The consensus motif for phosphorylation by cyclin D1-Cdk4 is different from that for phosphorylation by cyclin A/E-Cdk2. EMBO J. 15: 7060–7069.
  • Knudsen, E. S., and J. Y. Wang 1996. Differential regulation of retinoblastoma protein function by specific Cdk phosphorylation sites. J. Biol. Chem. 271: 8313–8320.
  • Koff, A., A. Giordano, D. Desai, K. Yamashita, J. W. Harper, S. Elledge, T. Nishimoto, D. O. Morgan, B. R. Franza, and J. M. Roberts 1992. Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle. Science 257: 1689–1694.
  • Koh, J., G. H. Enders, B. D. Dynlacht, and E. Harlow 1995. Tumour-derived p16 alleles encoding proteins defective in cell-cycle inhibition. Nature 375: 506–510.
  • Krek, W., D. M. Livingston, and S. Shirodkar 1993. Binding to DNA and the retinoblastoma gene product promoted by complex formation of different E2F family members. Science 262: 1557–1560.
  • La Thangue, N. B. 1994. DRTF1/E2F: an expanding family of heterodimeric transcription factors implicated in cell-cycle control. Trends Biochem. Sci. 19: 108–114.
  • Lees, J. A., K. J. Buchkovich, D. R. Marshak, C. W. Anderson, and E. Harlow 1991. The retinoblastoma protein is phosphorylated on multiple sites by human cdc2. EMBO J. 10: 4279–4290.
  • Leone, G., J. De Gregori, R. Sears, L. Jakoi, and J. R. Nevins 1997. Myc and Ras collaborate in inducing accumulation of active cyclin E/Cdk2 and E2F. Nature 387: 422–426.
  • Lew, D. J., V. Dulic, and S. I. Reed 1991. Isolation of three novel human cyclins by rescue of G1 cyclin (Cln) function in yeast. Cell 66: 1197–1206.
  • Lin, B. T., S. Gruenwald, A. O. Morla, W. H. Lee, and J. Y. Wang 1991. Retinoblastoma cancer suppressor gene product is a substrate of the cell cycle regulator cdc2 kinase. EMBO J. 10: 857–864.
  • Matsushime, H., M. F. Roussel, R. A. Ashmun, and C. J. Sherr 1991. Colony-stimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell 65: 701–713.
  • Medema, R. H., R. E. Herrera, F. Lam, and R. A. Weinberg 1995. Growth suppression by p16ink4 requires functional retinoblastoma protein. Proc. Natl. Acad. Sci. USA 92: 6289–293.
  • Meyerson, M., and E. Harlow 1994. Identification of G1 kinase activity for cdk6, a novel cyclin D partner. Mol. Cell. Biol. 14: 2077–2086.
  • Mihara, K., X. R. Cao, A. Yen, S. Chandler, B. Driscoll, A. L. Murphree, A. T’Ang, and Y. K. Fung 1989. Cell cycle-dependent regulation of phosphorylation of the human retinoblastoma gene product. Science 246: 1300–1303.
  • Minshull, J., R. Golsteyn, C. S. Hill, and T. Hunt 1990. The A- and B-type cyclin associated cdc2 kinases in Xenopus turn on and off at different times in the cell cycle. EMBO J. 9: 2865–2875.
  • Mittnacht, S., J. A. Lees, D. Desai, E. Harlow, D. O. Morgan, and R. A. Weinberg 1994. Distinct sub-populations of the retinoblastoma protein show a distinct pattern of phosphorylation. EMBO J. 13: 118–127.
  • Mittnacht, S., and R. A. Weinberg 1991. G1/S phosphorylation of the retinoblastoma protein is associated with an altered affinity for the nuclear compartment. Cell 65: 381–393.
  • Moberg, K., M. A. Starz, and J. A. Lees 1996. E2F-4 switches from p130 to p107 and pRB in response to cell cycle reentry. Mol. Cell. Biol. 16: 1436–1449.
  • Ohtsubo, M., A. M. Theodoras, J. Schumacher, J. M. Roberts, and M. Pagano 1995. Human cyclin E, a nuclear protein essential for the G1-to-S phase transition. Mol. Cell. Biol. 15: 2612–2624.
  • Pines, J., and T. Hunter 1990. Human cyclin A is adenovirus E1A-associated protein p60 and behaves differently from cyclin B. Nature 346: 760–763.
  • Qian, Y., C. Luckey, L. Horton, M. Esser, and D. J. Templeton 1992. Biological function of the retinoblastoma protein requires distinct domains for hyperphosphorylation and transcription factor binding. Mol. Cell. Biol. 12: 5363–5372.
  • Quelle, D. E., R. A. Ashmun, S. A. Shurtleff, J. Y. Kato, D. Bar-Sagi, M. F. Roussel, and C. J. Sherr 1993. Overexpression of mouse D-type cyclins accelerates G1 phase in rodent fibroblasts. Genes Dev. 7: 1559–1571.
  • Resnitzky, D., M. Gossen, H. Bujard, and S. I. Reed 1994. Acceleration of the G1/S phase transition by expression of cyclins D1 and E with an inducible system. Mol. Cell. Biol. 14: 1669–1679.
  • Roach, P. J. 1990. Control of glycogen synthase by hierarchal protein phosphorylation. FASEB J. 4: 2961–2968.
  • Schulze, A., K. Zerfass, D. Spitkovsky, B. Henglein, and P. Jansen-Durr 1994. Activation of the E2F transcription factor by cyclin D1 is blocked by p16INK4, the product of the putative tumor suppressor gene MTS1. Oncogene 9: 3475–3482.
  • Serrano, M., G. J. Hannon, and D. Beach 1993. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 366: 704–707.
  • Sherr, C. J. 1994. G1 phase progression: cycling on cue. Cell 79: 551–555.
  • Tam, S. W., A. M. Theodoras, J. W. Shay, G. F. Draetta, and M. Pagano 1994. Differential expression and regulation of Cyclin D1 protein in normal and tumor human cells: association with Cdk4 is required for Cyclin D1 function in G1 progression. Oncogene 9: 2663–2674.
  • Tan, X., S. J. Martin, D. R. Green, and J. Y. J. Wang 1997. Degradation of retinoblastoma protein in tumor necrosis factor- and CD95-induced cell death. J. Biol. Chem. 272: 9613–9616.
  • Taya, Y., H. Yasuda, M. Kamijo, K. Nakaya, Y. Nakamura, Y. Ohba, and S. Nishimura 1989. In vitro phosphorylation of the tumor suppressor gene RB protein by mitosis-specific histone H1 kinase. Biochem. Biophys. Res. Commun. 164: 580–586.
  • Templeton, D. J., S. H. Park, L. Lanier, and R. A. Weinberg 1991. Nonfunctional mutants of the retinoblastoma protein are characterized by defects in phosphorylation, viral oncoprotein association, and nuclear tethering. Proc. Natl. Acad. Sci. USA 88: 3033–3037.
  • van den Heuvel, S., and E. Harlow 1993. Distinct roles for cyclin-dependent kinases in cell cycle control. Science 262: 2050–2054.
  • Weinberg, R. A. 1995. The retinoblastoma protein and cell cycle control. Cell 81: 323–330.
  • Whyte, P., K. J. Buchkovich, J. M. Horowitz, S. H. Friend, M. Raybuck, R. A. Weinberg, and E. Harlow 1988. Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product. Nature 334: 124–129.
  • Wu, C. L., M. Classon, N. Dyson, and E. Harlow 1996. Expression of dominant-negative mutant DP-1 blocks cell cycle progression in G1. Mol. Cell. Biol. 16: 3698–3706.
  • Zarkowska, T., and S. Mittnacht 1997. Differential Phosphorylation of the retinoblastoma protein by G1/S cyclin-dependent kinases. J. Biol. Chem. 19: 112738–12746.
  • Zarkowska, T., S. U. E. Harlow, and S. Mittnacht 1997. Monoclonal antibodies specific for underphosphorylated retinoblastoma protein identify a cell cycle regulated phosphorylation site targeted by CDKs. Oncogene 14: 249–254.
  • Zerfass-Thome, K., A. Schulze, W. Zwerschke, B. Vogt, K. Helin, J. Bartek, B. Henglein, and P. Jansen-Durr 1997. p27KIP1 blocks cyclin E-dependent transactivation of cyclin A gene expression. Mol. Cell. Biol. 17: 407–415.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.