Abstract
We have investigated the mechanism by which the simian virus 40 large T antigen (SVLT) interferes with the differentiation of C2 myoblasts. SVLT mutants, defective either in the Rb binding site, near the N-terminal end, in a region that affects binding to p53, or in the nuclear transport signal, were also employed to determine whether the interference was especially dependent on these functional domains. It was found that wild-type (wt) SVLT strongly inhibited the terminal differentiation of mouse C2 myoblasts, but this arrest occurred only after the synthesis of myogenin, an initial step in biochemical differentiation. Neither the synthesis nor some basic activities of MyoD appeared to be affected by wt SVLT. In these transformants, mitogen depletion elicited an increase in the Rb level comparable to that in normal C2 cells; wt SVLT, however, promoted the phosphorylation of a large part of the induced Rb. Mutations affecting nuclear transport were far more critical for the ability to interfere with myogenic differentiation than were those affecting the transforming potential; cytoplasmic SVLT expression was fully compatible with the terminal differentiation of C2 cells, despite enabling them to grow in semisolid medium, thus showing that the myogenesis-inhibiting property can be dissociated from transforming competence. The remaining SVLT mutants presented different degrees of ability to inhibit differentiation (as shown by the expression of tissue-specific markers in transformants). The inhibiting mutants, including the Rb binding site mutant, were able to promote a higher state of Rb phosphorylation than that observed in either normal cells or cytoplasmic-SVLT transformants.
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- Alemà S., Tatò F. Oncogenes and muscle differentiation: multiple mechanisms of interference. Semin Cancer Biol. 1994 Apr;5(2):147–156. [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]
- Bengal E., Ransone L., Scharfmann R., Dwarki V. J., Tapscott S. J., Weintraub H., Verma I. M. Functional antagonism between c-Jun and MyoD proteins: a direct physical association. Cell. 1992 Feb 7;68(3):507–519. doi: 10.1016/0092-8674(92)90187-h. [DOI] [PubMed] [Google Scholar]
- Birnbaum M., Shainberg A., Salzberg S. Infection with Moloney murine sarcoma virus inhibits myogenesis and alters the myogenic-associated (2'-5')oligoadenylate synthetase expression and activity. Virology. 1993 Jun;194(2):865–869. doi: 10.1006/viro.1993.1332. [DOI] [PubMed] [Google Scholar]
- Blochlinger K., Diggelmann H. Hygromycin B phosphotransferase as a selectable marker for DNA transfer experiments with higher eucaryotic cells. Mol Cell Biol. 1984 Dec;4(12):2929–2931. doi: 10.1128/mcb.4.12.2929. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Braun T., Bober E., Arnold H. H. Inhibition of muscle differentiation by the adenovirus E1a protein: repression of the transcriptional activating function of the HLH protein Myf-5. Genes Dev. 1992 May;6(5):888–902. doi: 10.1101/gad.6.5.888. [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]
- Caruso M., Martelli F., Giordano A., Felsani A. Regulation of MyoD gene transcription and protein function by the transforming domains of the adenovirus E1A oncoprotein. Oncogene. 1993 Feb;8(2):267–278. [PubMed] [Google Scholar]
- Chaney W. G., Howard D. R., Pollard J. W., Sallustio S., Stanley P. High-frequency transfection of CHO cells using polybrene. Somat Cell Mol Genet. 1986 May;12(3):237–244. doi: 10.1007/BF01570782. [DOI] [PubMed] [Google Scholar]
- Chellappan S., Kraus V. B., Kroger B., Munger K., Howley P. M., Phelps W. C., Nevins J. R. Adenovirus E1A, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the retinoblastoma gene product. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4549–4553. doi: 10.1073/pnas.89.10.4549. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen S., Paucha E. Identification of a region of simian virus 40 large T antigen required for cell transformation. J Virol. 1990 Jul;64(7):3350–3357. doi: 10.1128/jvi.64.7.3350-3357.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chittenden T., Livingston D. M., Kaelin W. G., Jr The T/E1A-binding domain of the retinoblastoma product can interact selectively with a sequence-specific DNA-binding protein. Cell. 1991 Jun 14;65(6):1073–1082. doi: 10.1016/0092-8674(91)90559-h. [DOI] [PubMed] [Google Scholar]
- 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. 1992 Sep 24;359(6393):328–330. doi: 10.1038/359328a0. [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]
- Crescenzi M., Crouch D. H., Tatò F. Transformation by myc prevents fusion but not biochemical differentiation of C2C12 myoblasts: mechanisms of phenotypic correction in mixed culture with normal cells. J Cell Biol. 1994 Jun;125(5):1137–1145. doi: 10.1083/jcb.125.5.1137. [DOI] [PMC free article] [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]
- DeCaprio J. A., Ludlow J. W., Figge J., Shew J. Y., Huang C. M., Lee W. H., Marsilio E., Paucha E., Livingston D. M. SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene. Cell. 1988 Jul 15;54(2):275–283. doi: 10.1016/0092-8674(88)90559-4. [DOI] [PubMed] [Google Scholar]
- Donehower L. A., Bradley A. The tumor suppressor p53. Biochim Biophys Acta. 1993 Aug 23;1155(2):181–205. doi: 10.1016/0304-419x(93)90004-v. [DOI] [PubMed] [Google Scholar]
- Dornreiter I., Höss A., Arthur A. K., Fanning E. SV40 T antigen binds directly to the large subunit of purified DNA polymerase alpha. EMBO J. 1990 Oct;9(10):3329–3336. doi: 10.1002/j.1460-2075.1990.tb07533.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dyson N., Buchkovich K., Whyte P., Harlow E. The cellular 107K protein that binds to adenovirus E1A also associates with the large T antigens of SV40 and JC virus. Cell. 1989 Jul 28;58(2):249–255. doi: 10.1016/0092-8674(89)90839-8. [DOI] [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]
- Enkemann S. A., Konieczny S. F., Taparowsky E. J. Adenovirus 5 E1A represses muscle-specific enhancers and inhibits expression of the myogenic regulatory factor genes, MyoD1 and myogenin. Cell Growth Differ. 1990 Aug;1(8):375–382. [PubMed] [Google Scholar]
- Ewen M. E., Xing Y. G., Lawrence J. B., Livingston D. M. Molecular cloning, chromosomal mapping, and expression of the cDNA for p107, a retinoblastoma gene product-related protein. Cell. 1991 Sep 20;66(6):1155–1164. doi: 10.1016/0092-8674(91)90038-z. [DOI] [PubMed] [Google Scholar]
- Falcone G., Alemà S., Tatò F. Transcription of muscle-specific genes is repressed by reactivation of pp60v-src in postmitotic quail myotubes. Mol Cell Biol. 1991 Jun;11(6):3331–3338. doi: 10.1128/mcb.11.6.3331. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fanning E., Knippers R. Structure and function of simian virus 40 large tumor antigen. Annu Rev Biochem. 1992;61:55–85. doi: 10.1146/annurev.bi.61.070192.000415. [DOI] [PubMed] [Google Scholar]
- Fischer-Fantuzzi L., Vesco C. Cell-dependent efficiency of reiterated nuclear signals in a mutant simian virus 40 oncoprotein targeted to the nucleus. Mol Cell Biol. 1988 Dec;8(12):5495–5503. doi: 10.1128/mcb.8.12.5495. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gossett L. A., Zhang W., Olson E. N. Dexamethasone-dependent inhibition of differentiation of C2 myoblasts bearing steroid-inducible N-ras oncogenes. J Cell Biol. 1988 Jun;106(6):2127–2137. doi: 10.1083/jcb.106.6.2127. [DOI] [PMC free article] [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]
- 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]
- 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]
- 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]
- Kalderon D., Roberts B. L., Richardson W. D., Smith A. E. A short amino acid sequence able to specify nuclear location. Cell. 1984 Dec;39(3 Pt 2):499–509. doi: 10.1016/0092-8674(84)90457-4. [DOI] [PubMed] [Google Scholar]
- Kierstead T. D., Tevethia M. J. Association of p53 binding and immortalization of primary C57BL/6 mouse embryo fibroblasts by using simian virus 40 T-antigen mutants bearing internal overlapping deletion mutations. J Virol. 1993 Apr;67(4):1817–1829. doi: 10.1128/jvi.67.4.1817-1829.1993. [DOI] [PMC free article] [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]
- Konieczny S. F., Drobes B. L., Menke S. L., Taparowsky E. J. Inhibition of myogenic differentiation by the H-ras oncogene is associated with the down regulation of the MyoD1 gene. Oncogene. 1989 Apr;4(4):473–481. [PubMed] [Google Scholar]
- La Rocca S. A., Crouch D. H., Gillespie D. A. c-Myc inhibits myogenic differentiation and myoD expression by a mechanism which can be dissociated from cell transformation. Oncogene. 1994 Dec;9(12):3499–3508. [PubMed] [Google Scholar]
- Lanford R. E., Wong C., Butel J. S. Differential ability of a T-antigen transport-defective mutant of simian virus 40 to transform primary and established rodent cells. Mol Cell Biol. 1985 May;5(5):1043–1050. doi: 10.1128/mcb.5.5.1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lassar A. B., Thayer M. J., Overell R. W., Weintraub H. Transformation by activated ras or fos prevents myogenesis by inhibiting expression of MyoD1. Cell. 1989 Aug 25;58(4):659–667. doi: 10.1016/0092-8674(89)90101-3. [DOI] [PubMed] [Google Scholar]
- Levine A. J. The tumor suppressor genes. Annu Rev Biochem. 1993;62:623–651. doi: 10.1146/annurev.bi.62.070193.003203. [DOI] [PubMed] [Google Scholar]
- Li L., Chambard J. C., Karin M., Olson E. N. Fos and Jun repress transcriptional activation by myogenin and MyoD: the amino terminus of Jun can mediate repression. Genes Dev. 1992 Apr;6(4):676–689. doi: 10.1101/gad.6.4.676. [DOI] [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]
- Maione R., Fimia G. M., Holman P., Schaffhausen B., Amati P. Retinoblastoma antioncogene is involved in the inhibition of myogenesis by polyomavirus large T antigen. Cell Growth Differ. 1994 Feb;5(2):231–237. [PubMed] [Google Scholar]
- Mallein-Gerin F., Olsen B. R. Expression of simian virus 40 large T (tumor) oncogene in mouse chondrocytes induces cell proliferation without loss of the differentiated phenotype. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3289–3293. doi: 10.1073/pnas.90.8.3289. [DOI] [PMC free article] [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]
- Minty A. J., Caravatti M., Robert B., Cohen A., Daubas P., Weydert A., Gros F., Buckingham M. E. Mouse actin messenger RNAs. Construction and characterization of a recombinant plasmid molecule containing a complementary DNA transcript of mouse alpha-actin mRNA. J Biol Chem. 1981 Jan 25;256(2):1008–1014. [PubMed] [Google Scholar]
- Ogryzko V. V., Hirai T. H., Shih C. E., Howard B. H. Dissociation of retinoblastoma gene protein hyperphosphorylation and commitment to enter S phase. J Virol. 1994 Jun;68(6):3724–3732. doi: 10.1128/jvi.68.6.3724-3732.1994. [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]
- 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]
- Oshima J., Steinmann K. E., Campisi J., Schlegel R. Modulation of cell growth, p34cdc2 and cyclin A levels by SV-40 large T antigen. Oncogene. 1993 Nov;8(11):2987–2993. [PubMed] [Google Scholar]
- Quartin R. S., Cole C. N., Pipas J. M., Levine A. J. The amino-terminal functions of the simian virus 40 large T antigen are required to overcome wild-type p53-mediated growth arrest of cells. J Virol. 1994 Mar;68(3):1334–1341. doi: 10.1128/jvi.68.3.1334-1341.1994. [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]
- Richon V. M., Rifkind R. A., Marks P. A. Expression and phosphorylation of the retinoblastoma protein during induced differentiation of murine erythroleukemia cells. Cell Growth Differ. 1992 Jul;3(7):413–420. [PubMed] [Google Scholar]
- Rudnicki M. A., Schnegelsberg P. N., Stead R. H., Braun T., Arnold H. H., Jaenisch R. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell. 1993 Dec 31;75(7):1351–1359. doi: 10.1016/0092-8674(93)90621-v. [DOI] [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]
- Shirodkar S., Ewen M., DeCaprio J. A., Morgan J., Livingston D. M., Chittenden T. The transcription factor E2F interacts with the retinoblastoma product and a p107-cyclin A complex in a cell cycle-regulated manner. Cell. 1992 Jan 10;68(1):157–166. doi: 10.1016/0092-8674(92)90214-w. [DOI] [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]
- Sompayrac L., Danna K. J. An amino-terminal fragment of SV40 T antigen transforms REF52 cells. Virology. 1992 Nov;191(1):439–442. doi: 10.1016/0042-6822(92)90206-5. [DOI] [PubMed] [Google Scholar]
- Srinivasan A., Peden K. W., Pipas J. M. The large tumor antigen of simian virus 40 encodes at least two distinct transforming functions. J Virol. 1989 Dec;63(12):5459–5463. doi: 10.1128/jvi.63.12.5459-5463.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Strohmeyer T., Reissmann P., Cordon-Cardo C., Hartmann M., Ackermann R., Slamon D. Correlation between retinoblastoma gene expression and differentiation in human testicular tumors. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6662–6666. doi: 10.1073/pnas.88.15.6662. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Symonds H. S., McCarthy S. A., Chen J., Pipas J. M., Van Dyke T. Use of transgenic mice reveals cell-specific transformation by a simian virus 40 T-antigen amino-terminal mutant. Mol Cell Biol. 1993 Jun;13(6):3255–3265. doi: 10.1128/mcb.13.6.3255. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Szekely L., Jiang W. Q., Bulic-Jakus F., Rosen A., Ringertz N., Klein G., Wiman K. G. Cell type and differentiation dependent heterogeneity in retinoblastoma protein expression in SCID mouse fetuses. Cell Growth Differ. 1992 Mar;3(3):149–156. [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]
- Thompson D. L., Kalderon D., Smith A. E., Tevethia M. J. Dissociation of Rb-binding and anchorage-independent growth from immortalization and tumorigenicity using SV40 mutants producing N-terminally truncated large T antigens. Virology. 1990 Sep;178(1):15–34. doi: 10.1016/0042-6822(90)90375-2. [DOI] [PubMed] [Google Scholar]
- Vogelstein B., Kinzler K. W. p53 function and dysfunction. Cell. 1992 Aug 21;70(4):523–526. doi: 10.1016/0092-8674(92)90421-8. [DOI] [PubMed] [Google Scholar]
- Wang H. G., Draetta G., Moran E. E1A induces phosphorylation of the retinoblastoma protein independently of direct physical association between the E1A and retinoblastoma products. Mol Cell Biol. 1991 Aug;11(8):4253–4265. doi: 10.1128/mcb.11.8.4253. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Webster K. A., Muscat G. E., Kedes L. Adenovirus E1A products suppress myogenic differentiation and inhibit transcription from muscle-specific promoters. Nature. 1988 Apr 7;332(6164):553–557. doi: 10.1038/332553a0. [DOI] [PubMed] [Google Scholar]
- Weintraub H., Davis R., Tapscott S., Thayer M., Krause M., Benezra R., Blackwell T. K., Turner D., Rupp R., Hollenberg S. The myoD gene family: nodal point during specification of the muscle cell lineage. Science. 1991 Feb 15;251(4995):761–766. doi: 10.1126/science.1846704. [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]
- Weydert A., Daubas P., Lazaridis I., Barton P., Garner I., Leader D. P., Bonhomme F., Catalan J., Simon D., Guénet J. L. Genes for skeletal muscle myosin heavy chains are clustered and are not located on the same mouse chromosome as a cardiac myosin heavy chain gene. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7183–7187. doi: 10.1073/pnas.82.21.7183. [DOI] [PMC free article] [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]
- Yaciuk P., Carter M. C., Pipas J. M., Moran E. Simian virus 40 large-T antigen expresses a biological activity complementary to the p300-associated transforming function of the adenovirus E1A gene products. Mol Cell Biol. 1991 Apr;11(4):2116–2124. doi: 10.1128/mcb.11.4.2116. [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]
- Zhou J., Olson E. N. Dimerization through the helix-loop-helix motif enhances phosphorylation of the transcription activation domains of myogenin. Mol Cell Biol. 1994 Sep;14(9):6232–6243. doi: 10.1128/mcb.14.9.6232. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu J. Y., Abate M., Rice P. W., Cole C. N. The ability of simian virus 40 large T antigen to immortalize primary mouse embryo fibroblasts cosegregates with its ability to bind to p53. J Virol. 1991 Dec;65(12):6872–6880. doi: 10.1128/jvi.65.12.6872-6880.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu J. Y., Rice P. W., Chamberlain M., Cole C. N. Mapping the transcriptional transactivation function of simian virus 40 large T antigen. J Virol. 1991 Jun;65(6):2778–2790. doi: 10.1128/jvi.65.6.2778-2790.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu J., Rice P. W., Gorsch L., Abate M., Cole C. N. Transformation of a continuous rat embryo fibroblast cell line requires three separate domains of simian virus 40 large T antigen. J Virol. 1992 May;66(5):2780–2791. doi: 10.1128/jvi.66.5.2780-2791.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu L., van den Heuvel S., Helin K., Fattaey A., Ewen M., Livingston D., Dyson N., Harlow E. Inhibition of cell proliferation by p107, a relative of the retinoblastoma protein. Genes Dev. 1993 Jul;7(7A):1111–1125. doi: 10.1101/gad.7.7a.1111. [DOI] [PubMed] [Google Scholar]