Abstract
We previously showed that C2 myoblasts transformed by simian virus 40 large T antigen (SVLT) stop the myogenic process after the induction of myogenin and of high Rb levels; the induced Rb, however, becomes notably phosphorylated. We have analyzed the protein levels and activities of cyclin-dependent kinases (cdks) in untransformed C2 cells and in transformants of either SVLT or the cytoplasmic mutant NKT1 (which permits differentiation) upon a shift from growth medium (GM) to mitogen-poor differentiation medium (DM). After the shift, cdk4 levels remained constant and cdk6 levels decreased in all cell types; cdk2 minimally increased only in SVLT cells. Cyclin D1 was downregulated in DM in all cell types, and cyclin D3 was upregulated (albeit less strongly in SVLT cells than in the others). In contrast, a dramatic difference between SVLT cells and the other cells was observed for cyclins E and A, which essentially disappeared (as protein and RNA) in normal C2 and NKT1 cells upon the shift from GM to DM, whereas they increased in SVLT cells. Concurrently, cdk2 activity ceased in C2 and NKT1 cells in DM, whereas it persisted at 20% of the GM level in SVLT cells. cdk4 activity was detectable in all cells only in GM. Cyclin E and A induction thus appeared to sustain enough Rb phosphorylation to interfere with tissue-specific expression, with cdk activity not high enough to activate cyclin self-regulation. In DM, cdk2 complexed to D3 was underphosphorylated in all cells, and SVLT allowed strong inductions of p21 and p27 without affecting their complexes with cdks.
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- Adamczewski J. P., Gannon J. V., Hunt T. Simian virus 40 large T antigen associates with cyclin A and p33cdk2. J Virol. 1993 Nov;67(11):6551–6557. doi: 10.1128/jvi.67.11.6551-6557.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Alemà S., Tatò F. Oncogenes and muscle differentiation: multiple mechanisms of interference. Semin Cancer Biol. 1994 Apr;5(2):147–156. [PubMed] [Google Scholar]
- Aprelikova O., Xiong Y., Liu E. T. Both p16 and p21 families of cyclin-dependent kinase (CDK) inhibitors block the phosphorylation of cyclin-dependent kinases by the CDK-activating kinase. J Biol Chem. 1995 Aug 4;270(31):18195–18197. doi: 10.1074/jbc.270.31.18195. [DOI] [PubMed] [Google Scholar]
- Bader D., Masaki T., Fischman D. A. Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J Cell Biol. 1982 Dec;95(3):763–770. doi: 10.1083/jcb.95.3.763. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baldin V., Lukas J., Marcote M. J., Pagano M., Draetta G. Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev. 1993 May;7(5):812–821. doi: 10.1101/gad.7.5.812. [DOI] [PubMed] [Google Scholar]
- Bernards R., Shackleford G. M., Schackleford G. M., Gerber M. R., Horowitz J. M., Friend S. H., Schartl M., Bogenmann E., Rapaport J. M., McGee T. Structure and expression of the murine retinoblastoma gene and characterization of its encoded protein. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6474–6478. doi: 10.1073/pnas.86.17.6474. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buchberger A., Ragge K., Arnold H. H. The myogenin gene is activated during myocyte differentiation by pre-existing, not newly synthesized transcription factor MEF-2. J Biol Chem. 1994 Jun 24;269(25):17289–17296. [PubMed] [Google Scholar]
- Buckingham M. Molecular biology of muscle development. Cell. 1994 Jul 15;78(1):15–21. doi: 10.1016/0092-8674(94)90568-1. [DOI] [PubMed] [Google Scholar]
- Cao L., Faha B., Dembski M., Tsai L. H., Harlow E., Dyson N. Independent binding of the retinoblastoma protein and p107 to the transcription factor E2F. Nature. 1992 Jan 9;355(6356):176–179. doi: 10.1038/355176a0. [DOI] [PubMed] [Google Scholar]
- Cobrinik D., Whyte P., Peeper D. S., Jacks T., Weinberg R. A. Cell cycle-specific association of E2F with the p130 E1A-binding protein. Genes Dev. 1993 Dec;7(12A):2392–2404. doi: 10.1101/gad.7.12a.2392. [DOI] [PubMed] [Google Scholar]
- Coppola J. A., Lewis B. A., Cole M. D. Increased retinoblastoma gene expression is associated with late stages of differentiation in many different cell types. Oncogene. 1990 Nov;5(11):1731–1733. [PubMed] [Google Scholar]
- Davis R. L., Weintraub H., Lassar A. B. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell. 1987 Dec 24;51(6):987–1000. doi: 10.1016/0092-8674(87)90585-x. [DOI] [PubMed] [Google Scholar]
- DeCaprio J. A., Furukawa Y., Ajchenbaum F., Griffin J. D., Livingston D. M. The retinoblastoma-susceptibility gene product becomes phosphorylated in multiple stages during cell cycle entry and progression. Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1795–1798. doi: 10.1073/pnas.89.5.1795. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeGregori J., Kowalik T., Nevins J. R. Cellular targets for activation by the E2F1 transcription factor include DNA synthesis- and G1/S-regulatory genes. Mol Cell Biol. 1995 Aug;15(8):4215–4224. doi: 10.1128/mcb.15.8.4215. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dynlacht B. D., Flores O., Lees J. A., Harlow E. Differential regulation of E2F transactivation by cyclin/cdk2 complexes. Genes Dev. 1994 Aug 1;8(15):1772–1786. doi: 10.1101/gad.8.15.1772. [DOI] [PubMed] [Google Scholar]
- Dyson N., Dembski M., Fattaey A., Ngwu C., Ewen M., Helin K. Analysis of p107-associated proteins: p107 associates with a form of E2F that differs from pRB-associated E2F-1. J Virol. 1993 Dec;67(12):7641–7647. doi: 10.1128/jvi.67.12.7641-7647.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Edmondson D. G., Cheng T. C., Cserjesi P., Chakraborty T., Olson E. N. Analysis of the myogenin promoter reveals an indirect pathway for positive autoregulation mediated by the muscle-specific enhancer factor MEF-2. Mol Cell Biol. 1992 Sep;12(9):3665–3677. doi: 10.1128/mcb.12.9.3665. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Endo T., Goto S. Retinoblastoma gene product Rb accumulates during myogenic differentiation and is deinduced by the expression of SV40 large T antigen. J Biochem. 1992 Oct;112(4):427–430. doi: 10.1093/oxfordjournals.jbchem.a123916. [DOI] [PubMed] [Google Scholar]
- Endo T. SV40 large T inhibits myogenic differentiation partially through inducing c-jun. J Biochem. 1992 Sep;112(3):321–329. doi: 10.1093/oxfordjournals.jbchem.a123899. [DOI] [PubMed] [Google Scholar]
- Geng Y., Eaton E. N., Picón 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. 1996 Mar 21;12(6):1173–1180. [PubMed] [Google Scholar]
- Giordano A., Whyte P., Harlow E., Franza B. R., Jr, Beach D., Draetta G. A 60 kd cdc2-associated polypeptide complexes with the E1A proteins in adenovirus-infected cells. Cell. 1989 Sep 8;58(5):981–990. doi: 10.1016/0092-8674(89)90949-5. [DOI] [PubMed] [Google Scholar]
- Graña X., Reddy E. P. Cell cycle control in mammalian cells: role of cyclins, cyclin dependent kinases (CDKs), growth suppressor genes and cyclin-dependent kinase inhibitors (CKIs). Oncogene. 1995 Jul 20;11(2):211–219. [PubMed] [Google Scholar]
- 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. 1993 Feb 12;72(3):309–324. doi: 10.1016/0092-8674(93)90110-c. [DOI] [PubMed] [Google Scholar]
- Guo K., Wang J., Andrés V., Smith R. C., Walsh K. MyoD-induced expression of p21 inhibits cyclin-dependent kinase activity upon myocyte terminal differentiation. Mol Cell Biol. 1995 Jul;15(7):3823–3829. doi: 10.1128/mcb.15.7.3823. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haider S. R., Wang W., Kaufman S. J. SV40 T antigen inhibits expression of MyoD and myogenin, up-regulates Myf-5, but does not affect early expression of desmin or alpha 7 integrin during muscle development. Exp Cell Res. 1994 Feb;210(2):278–286. doi: 10.1006/excr.1994.1040. [DOI] [PubMed] [Google Scholar]
- 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. 1995 Feb 17;267(5200):1018–1021. doi: 10.1126/science.7863327. [DOI] [PubMed] [Google Scholar]
- Harper J. W., Elledge S. J., Keyomarsi K., Dynlacht B., Tsai L. H., Zhang P., Dobrowolski S., Bai C., Connell-Crowley L., Swindell E. Inhibition of cyclin-dependent kinases by p21. Mol Biol Cell. 1995 Apr;6(4):387–400. doi: 10.1091/mbc.6.4.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hasty P., Bradley A., Morris J. H., Edmondson D. G., Venuti J. M., Olson E. N., Klein W. H. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature. 1993 Aug 5;364(6437):501–506. doi: 10.1038/364501a0. [DOI] [PubMed] [Google Scholar]
- Herrera R. E., Sah V. P., Williams B. O., Mäkelä T. P., Weinberg R. A., Jacks T. Altered cell cycle kinetics, gene expression, and G1 restriction point regulation in Rb-deficient fibroblasts. Mol Cell Biol. 1996 May;16(5):2402–2407. doi: 10.1128/mcb.16.5.2402. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hollenberg S. M., Cheng P. F., Weintraub H. Use of a conditional MyoD transcription factor in studies of MyoD trans-activation and muscle determination. Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):8028–8032. doi: 10.1073/pnas.90.17.8028. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hunter T. Cooperation between oncogenes. Cell. 1991 Jan 25;64(2):249–270. doi: 10.1016/0092-8674(91)90637-e. [DOI] [PubMed] [Google Scholar]
- Iujvidin S., Fuchs O., Nudel U., Yaffe D. SV40 immortalizes myogenic cells: DNA synthesis and mitosis in differentiating myotubes. Differentiation. 1990 Jun;43(3):192–203. doi: 10.1111/j.1432-0436.1990.tb00446.x. [DOI] [PubMed] [Google Scholar]
- Jahn L., Sadoshima J., Izumo S. Cyclins and cyclin-dependent kinases are differentially regulated during terminal differentiation of C2C12 muscle cells. Exp Cell Res. 1994 Jun;212(2):297–307. doi: 10.1006/excr.1994.1147. [DOI] [PubMed] [Google Scholar]
- Kato J. Y., Matsuoka M., Strom D. K., Sherr C. J. Regulation of cyclin D-dependent kinase 4 (cdk4) by cdk4-activating kinase. Mol Cell Biol. 1994 Apr;14(4):2713–2721. doi: 10.1128/mcb.14.4.2713. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kiess M., Gill R. M., Hamel P. A. Expression and activity of the retinoblastoma protein (pRB)-family proteins, p107 and p130, during L6 myoblast differentiation. Cell Growth Differ. 1995 Oct;6(10):1287–1298. [PubMed] [Google Scholar]
- Kiess M., Gill R. M., Hamel P. A. Expression of the positive regulator of cell cycle progression, cyclin D3, is induced during differentiation of myoblasts into quiescent myotubes. Oncogene. 1995 Jan 5;10(1):159–166. [PubMed] [Google Scholar]
- Kitagawa M., Higashi H., Suzuki-Takahashi I., Segawa K., Hanks S. K., Taya Y., Nishimura S., Okuyama A. Phosphorylation of E2F-1 by cyclin A-cdk2. Oncogene. 1995 Jan 19;10(2):229–236. [PubMed] [Google Scholar]
- Krek W., Ewen M. E., Shirodkar S., Arany Z., Kaelin W. G., Jr, Livingston D. M. Negative regulation of the growth-promoting transcription factor E2F-1 by a stably bound cyclin A-dependent protein kinase. Cell. 1994 Jul 15;78(1):161–172. doi: 10.1016/0092-8674(94)90582-7. [DOI] [PubMed] [Google Scholar]
- Lees J. A., Buchkovich K. J., Marshak D. R., Anderson C. W., Harlow E. The retinoblastoma protein is phosphorylated on multiple sites by human cdc2. EMBO J. 1991 Dec;10(13):4279–4290. doi: 10.1002/j.1460-2075.1991.tb05006.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lin S. Y., Black A. R., Kostic D., Pajovic S., Hoover C. N., Azizkhan J. C. Cell cycle-regulated association of E2F1 and Sp1 is related to their functional interaction. Mol Cell Biol. 1996 Apr;16(4):1668–1675. doi: 10.1128/mcb.16.4.1668. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lukas J., Müller H., Bartkova J., Spitkovsky D., Kjerulff A. A., Jansen-Dürr P., Strauss M., Bartek J. DNA tumor virus oncoproteins and retinoblastoma gene mutations share the ability to relieve the cell's requirement for cyclin D1 function in G1. J Cell Biol. 1994 May;125(3):625–638. doi: 10.1083/jcb.125.3.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maione R., Fimia G. M., Amati P. Inhibition of in vitro myogenic differentiation by a polyomavirus early function. Oncogene. 1992 Jan;7(1):85–93. [PubMed] [Google Scholar]
- Mal A., Poon R. Y., Howe P. H., Toyoshima H., Hunter T., Harter M. L. Inactivation of p27Kip1 by the viral E1A oncoprotein in TGFbeta-treated cells. Nature. 1996 Mar 21;380(6571):262–265. doi: 10.1038/380262a0. [DOI] [PubMed] [Google Scholar]
- Manfredi J. J., Prives C. The transforming activity of simian virus 40 large tumor antigen. Biochim Biophys Acta. 1994 May 27;1198(1):65–83. doi: 10.1016/0304-419x(94)90006-x. [DOI] [PubMed] [Google Scholar]
- Martelli F., Cenciarelli C., Santarelli G., Polikar B., Felsani A., Caruso M. MyoD induces retinoblastoma gene expression during myogenic differentiation. Oncogene. 1994 Dec;9(12):3579–3590. [PubMed] [Google Scholar]
- Mayol X., Graña X., Baldi A., Sang N., Hu Q., Giordano A. Cloning of a new member of the retinoblastoma gene family (pRb2) which binds to the E1A transforming domain. Oncogene. 1993 Sep;8(9):2561–2566. [PubMed] [Google Scholar]
- Moberg K., Starz M. A., Lees J. A. E2F-4 switches from p130 to p107 and pRB in response to cell cycle reentry. Mol Cell Biol. 1996 Apr;16(4):1436–1449. doi: 10.1128/mcb.16.4.1436. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morgan D. O. Principles of CDK regulation. Nature. 1995 Mar 9;374(6518):131–134. doi: 10.1038/374131a0. [DOI] [PubMed] [Google Scholar]
- Mudrak I., Ogris E., Rotheneder H., Wintersberger E. Coordinated trans activation of DNA synthesis- and precursor-producing enzymes by polyomavirus large T antigen through interaction with the retinoblastoma protein. Mol Cell Biol. 1994 Mar;14(3):1886–1892. doi: 10.1128/mcb.14.3.1886. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ohkubo Y., Kishimoto T., Nakata T., Yasuda H., Endo T. SV40 large T antigen reinduces the cell cycle in terminally differentiated myotubes through inducing Cdk2, Cdc2, and their partner cyclins. Exp Cell Res. 1994 Sep;214(1):270–278. doi: 10.1006/excr.1994.1258. [DOI] [PubMed] [Google Scholar]
- Ohtani K., DeGregori J., Nevins J. R. Regulation of the cyclin E gene by transcription factor E2F1. Proc Natl Acad Sci U S A. 1995 Dec 19;92(26):12146–12150. doi: 10.1073/pnas.92.26.12146. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Olson E. N. Interplay between proliferation and differentiation within the myogenic lineage. Dev Biol. 1992 Dec;154(2):261–272. doi: 10.1016/0012-1606(92)90066-p. [DOI] [PubMed] [Google Scholar]
- Olson E. N., Perry M., Schulz R. A. Regulation of muscle differentiation by the MEF2 family of MADS box transcription factors. Dev Biol. 1995 Nov;172(1):2–14. doi: 10.1006/dbio.1995.0002. [DOI] [PubMed] [Google Scholar]
- Pagano M., Tam S. W., Theodoras A. M., Beer-Romero P., Del Sal G., Chau V., Yew P. R., Draetta G. F., Rolfe M. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science. 1995 Aug 4;269(5224):682–685. doi: 10.1126/science.7624798. [DOI] [PubMed] [Google Scholar]
- Parker S. B., Eichele G., Zhang P., Rawls A., Sands A. T., Bradley A., Olson E. N., Harper J. W., Elledge S. J. p53-independent expression of p21Cip1 in muscle and other terminally differentiating cells. Science. 1995 Feb 17;267(5200):1024–1027. doi: 10.1126/science.7863329. [DOI] [PubMed] [Google Scholar]
- Peeper D. S., Keblusek P., Helin K., Toebes M., van der Eb A. J., Zantema A. Phosphorylation of a specific cdk site in E2F-1 affects its electrophoretic mobility and promotes pRB-binding in vitro. Oncogene. 1995 Jan 5;10(1):39–48. [PubMed] [Google Scholar]
- Peterson S. R., Gadbois D. M., Bradbury E. M., Kraemer P. M. Immortalization of human fibroblasts by SV40 large T antigen results in the reduction of cyclin D1 expression and subunit association with proliferating cell nuclear antigen and Waf1. Cancer Res. 1995 Oct 15;55(20):4651–4657. [PubMed] [Google Scholar]
- Polyak K., Lee M. H., Erdjument-Bromage H., Koff A., Roberts J. M., Tempst P., Massagué J. Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell. 1994 Jul 15;78(1):59–66. doi: 10.1016/0092-8674(94)90572-x. [DOI] [PubMed] [Google Scholar]
- Poon R. Y., Hunter T. Dephosphorylation of Cdk2 Thr160 by the cyclin-dependent kinase-interacting phosphatase KAP in the absence of cyclin. Science. 1995 Oct 6;270(5233):90–93. doi: 10.1126/science.270.5233.90. [DOI] [PubMed] [Google Scholar]
- Poon R. Y., Toyoshima H., Hunter T. Redistribution of the CDK inhibitor p27 between different cyclin.CDK complexes in the mouse fibroblast cell cycle and in cells arrested with lovastatin or ultraviolet irradiation. Mol Biol Cell. 1995 Sep;6(9):1197–1213. doi: 10.1091/mbc.6.9.1197. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rao S. S., Chu C., Kohtz D. S. Ectopic expression of cyclin D1 prevents activation of gene transcription by myogenic basic helix-loop-helix regulators. Mol Cell Biol. 1994 Aug;14(8):5259–5267. doi: 10.1128/mcb.14.8.5259. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rao S. S., Kohtz D. S. Positive and negative regulation of D-type cyclin expression in skeletal myoblasts by basic fibroblast growth factor and transforming growth factor beta. A role for cyclin D1 in control of myoblast differentiation. J Biol Chem. 1995 Feb 24;270(8):4093–4100. doi: 10.1074/jbc.270.8.4093. [DOI] [PubMed] [Google Scholar]
- Resnitzky D., Reed S. I. Different roles for cyclins D1 and E in regulation of the G1-to-S transition. Mol Cell Biol. 1995 Jul;15(7):3463–3469. doi: 10.1128/mcb.15.7.3463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sala A., Nicolaides N. C., Engelhard A., Bellon T., Lawe D. C., Arnold A., Graña X., Giordano A., Calabretta B. Correlation between E2F-1 requirement in the S phase and E2F-1 transactivation of cell cycle-related genes in human cells. Cancer Res. 1994 Mar 15;54(6):1402–1406. [PubMed] [Google Scholar]
- Sardet C., Vidal M., Cobrinik D., Geng Y., Onufryk C., Chen A., Weinberg R. A. E2F-4 and E2F-5, two members of the E2F family, are expressed in the early phases of the cell cycle. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2403–2407. doi: 10.1073/pnas.92.6.2403. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schneider J. W., Gu W., Zhu L., Mahdavi V., Nadal-Ginard B. Reversal of terminal differentiation mediated by p107 in Rb-/- muscle cells. Science. 1994 Jun 3;264(5164):1467–1471. doi: 10.1126/science.8197461. [DOI] [PubMed] [Google Scholar]
- Schwarz J. K., Devoto S. H., Smith E. J., Chellappan S. P., Jakoi L., Nevins J. R. Interactions of the p107 and Rb proteins with E2F during the cell proliferation response. EMBO J. 1993 Mar;12(3):1013–1020. doi: 10.1002/j.1460-2075.1993.tb05742.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sherr C. J. G1 phase progression: cycling on cue. Cell. 1994 Nov 18;79(4):551–555. doi: 10.1016/0092-8674(94)90540-1. [DOI] [PubMed] [Google Scholar]
- Sherr C. J., Roberts J. M. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 1995 May 15;9(10):1149–1163. doi: 10.1101/gad.9.10.1149. [DOI] [PubMed] [Google Scholar]
- Shin E. K., Shin A., Paulding C., Schaffhausen B., Yee A. S. Multiple change in E2F function and regulation occur upon muscle differentiation. Mol Cell Biol. 1995 Apr;15(4):2252–2262. doi: 10.1128/mcb.15.4.2252. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Slack R. S., Hamel P. A., Bladon T. S., Gill R. M., McBurney M. W. Regulated expression of the retinoblastoma gene in differentiating embryonal carcinoma cells. Oncogene. 1993 Jun;8(6):1585–1591. [PubMed] [Google Scholar]
- Spitkovsky D., Steiner P., Lukas J., Lees E., Pagano M., Schulze A., Joswig S., Picard D., Tommasino M., Eilers M. Modulation of cyclin gene expression by adenovirus E1A in a cell line with E1A-dependent conditional proliferation. J Virol. 1994 Apr;68(4):2206–2214. doi: 10.1128/jvi.68.4.2206-2214.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Suzuki-Takahashi I., Kitagawa M., Saijo M., Higashi H., Ogino H., Matsumoto H., Taya Y., Nishimura S., Okuyama A. The interactions of E2F with pRB and with p107 are regulated via the phosphorylation of pRB and p107 by a cyclin-dependent kinase. Oncogene. 1995 May 4;10(9):1691–1698. [PubMed] [Google Scholar]
- Tam S. W., Shay J. W., Pagano M. Differential expression and cell cycle regulation of the cyclin-dependent kinase 4 inhibitor p16Ink4. Cancer Res. 1994 Nov 15;54(22):5816–5820. [PubMed] [Google Scholar]
- Tedesco D., Caruso M., Fischer-Fantuzzi L., Vesco C. The inhibition of cultured myoblast differentiation by the simian virus 40 large T antigen occurs after myogenin expression and Rb up-regulation and is not exerted by transformation-competent cytoplasmic mutants. J Virol. 1995 Nov;69(11):6947–6957. doi: 10.1128/jvi.69.11.6947-6957.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tedesco D., Fischer-Fantuzzi L., Vesco C. Limits of transforming competence of SV40 nuclear and cytoplasmic large T mutants with altered Rb binding sequences. Oncogene. 1993 Mar;8(3):549–557. [PubMed] [Google Scholar]
- Toyoshima H., Hunter T. p27, a novel inhibitor of G1 cyclin-Cdk protein kinase activity, is related to p21. Cell. 1994 Jul 15;78(1):67–74. doi: 10.1016/0092-8674(94)90573-8. [DOI] [PubMed] [Google Scholar]
- Vairo G., Livingston D. M., Ginsberg D. Functional interaction between E2F-4 and p130: evidence for distinct mechanisms underlying growth suppression by different retinoblastoma protein family members. Genes Dev. 1995 Apr 1;9(7):869–881. doi: 10.1101/gad.9.7.869. [DOI] [PubMed] [Google Scholar]
- Wang J., Nadal-Ginard B. Regulation of cyclins and p34CDC2 expression during terminal differentiation of C2C12 myocytes. Biochem Biophys Res Commun. 1995 Jan 5;206(1):82–88. doi: 10.1006/bbrc.1995.1012. [DOI] [PubMed] [Google Scholar]
- Weinberg R. A. The retinoblastoma protein and cell cycle control. Cell. 1995 May 5;81(3):323–330. doi: 10.1016/0092-8674(95)90385-2. [DOI] [PubMed] [Google Scholar]
- Weintraub H. The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell. 1993 Dec 31;75(7):1241–1244. doi: 10.1016/0092-8674(93)90610-3. [DOI] [PubMed] [Google Scholar]
- Wright W. E., Binder M., Funk W. Cyclic amplification and selection of targets (CASTing) for the myogenin consensus binding site. Mol Cell Biol. 1991 Aug;11(8):4104–4110. doi: 10.1128/mcb.11.8.4104. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xiong Y., Hannon G. J., Zhang H., Casso D., Kobayashi R., Beach D. p21 is a universal inhibitor of cyclin kinases. Nature. 1993 Dec 16;366(6456):701–704. doi: 10.1038/366701a0. [DOI] [PubMed] [Google Scholar]
- Xu M., Sheppard K. A., Peng C. Y., Yee A. S., Piwnica-Worms H. Cyclin A/CDK2 binds directly to E2F-1 and inhibits the DNA-binding activity of E2F-1/DP-1 by phosphorylation. Mol Cell Biol. 1994 Dec;14(12):8420–8431. doi: 10.1128/mcb.14.12.8420. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yaffe D., Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 1977 Dec 22;270(5639):725–727. doi: 10.1038/270725a0. [DOI] [PubMed] [Google Scholar]