Abstract
We have investigated p53-E1b 58-kilodalton (kDa) protein complex formation during permissive and semipermissive infections with adenovirus type 5 (Ad5) dl309. While metabolic labeling studies easily detected p53-E1b 58-kDa protein complexes in transformed rat cells (XhoI-C), the same methods have not revealed complexes during infection of either human osteosarcoma cells (permissive) or normal rat kidney cells (semipermissive). Complexes were not detectable at any stage during the replicative cycle of Ad5 dl309 in osteosarcoma cells, and they could not be stabilized by using an in vivo cross-linking agent. In addition, using the E4-defective mutant Ad5 dl355, no complexes were observed either. Thus, the lack of p53-E1b 58-kDa protein complex formation during infection is not due to competition from the E4 34-kDa protein. In vitro association experiments showed that in vitro-translated mouse and human p53 could form complexes with E1b 58-kDa antigen expressed during infection. Thus, such E1b proteins are competent to form complexes. The converse experiment, in which in vitro-translated E1b 58-kDa protein was mixed with lysates of osteosarcoma cells, showed little or no p53-E1b 58-kDa protein association, even though the in vitro E1b 58-kDa protein could associate stably with p53 from cells containing endogenous p53-E1b 58-kDa protein complex. These data suggest that competence to form p53-E1b 58-kDa protein complexes resides in some property of p53.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Benchimol S., Pim D., Crawford L. Radioimmunoassay of the cellular protein p53 in mouse and human cell lines. EMBO J. 1982;1(9):1055–1062. doi: 10.1002/j.1460-2075.1982.tb01296.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Braithwaite A. W., Murray J. D., Bellett A. J. Alterations to controls of cellular DNA synthesis by adenovirus infection. J Virol. 1981 Aug;39(2):331–340. doi: 10.1128/jvi.39.2.331-340.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Braithwaite A. W., Sturzbecher H. W., Addison C., Palmer C., Rudge K., Jenkins J. R. Mouse p53 inhibits SV40 origin-dependent DNA replication. Nature. 1987 Oct 1;329(6138):458–460. doi: 10.1038/329458a0. [DOI] [PubMed] [Google Scholar]
- Burger C., Fanning E. Specific DNA binding activity of T antigen subclasses varies among different SV40-transformed cell lines. Virology. 1983 Apr 15;126(1):19–31. doi: 10.1016/0042-6822(83)90459-2. [DOI] [PubMed] [Google Scholar]
- Calabretta B., Kaczmarek L., Selleri L., Torelli G., Ming P. M., Ming S. C., Mercer W. E. Growth-dependent expression of human Mr 53,000 tumor antigen messenger RNA in normal and neoplastic cells. Cancer Res. 1986 Nov;46(11):5738–5742. [PubMed] [Google Scholar]
- Crawford L. V., Pim D. C., Gurney E. G., Goodfellow P., Taylor-Papadimitriou J. Detection of a common feature in several human tumor cell lines--a 53,000-dalton protein. Proc Natl Acad Sci U S A. 1981 Jan;78(1):41–45. doi: 10.1073/pnas.78.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cutt J. R., Shenk T., Hearing P. Analysis of adenovirus early region 4-encoded polypeptides synthesized in productively infected cells. J Virol. 1987 Feb;61(2):543–552. doi: 10.1128/jvi.61.2.543-552.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eliyahu D., Raz A., Gruss P., Givol D., Oren M. Participation of p53 cellular tumour antigen in transformation of normal embryonic cells. Nature. 1984 Dec 13;312(5995):646–649. doi: 10.1038/312646a0. [DOI] [PubMed] [Google Scholar]
- Fukui Y., Saito I., Shiroki K., Shimojo H. Isolation of transformation-defective, replication-nondefective early region 1B mutants of adenovirus 12. J Virol. 1984 Jan;49(1):154–161. doi: 10.1128/jvi.49.1.154-161.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Graham F. L., Smiley J., Russell W. C., Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol. 1977 Jul;36(1):59–74. doi: 10.1099/0022-1317-36-1-59. [DOI] [PubMed] [Google Scholar]
- Grand R. J., Gallimore P. H. Adenovirus type 12 early region 1 proteins: a study of their subcellular localization and protein-protein interactions. J Gen Virol. 1984 Dec;65(Pt 12):2149–2166. doi: 10.1099/0022-1317-65-12-2149. [DOI] [PubMed] [Google Scholar]
- Halbert D. N., Cutt J. R., Shenk T. Adenovirus early region 4 encodes functions required for efficient DNA replication, late gene expression, and host cell shutoff. J Virol. 1985 Oct;56(1):250–257. doi: 10.1128/jvi.56.1.250-257.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Harlow E., Crawford L. V., Pim D. C., Williamson N. M. Monoclonal antibodies specific for simian virus 40 tumor antigens. J Virol. 1981 Sep;39(3):861–869. doi: 10.1128/jvi.39.3.861-869.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hérissé J., Rigolet M., de Dinechin S. D., Galibert F. Nucleotide sequence of adenovirus 2 DNA fragment encoding for the carboxylic region of the fiber protein and the entire E4 region. Nucleic Acids Res. 1981 Aug 25;9(16):4023–4042. doi: 10.1093/nar/9.16.4023. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jenkins J. R., Chumakov P., Addison C., Stürzbecher H. W., Wade-Evans A. Two distinct regions of the murine p53 primary amino acid sequence are implicated in stable complex formation with simian virus 40 T antigen. J Virol. 1988 Oct;62(10):3903–3906. doi: 10.1128/jvi.62.10.3903-3906.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jenkins J. R., Rudge K., Chumakov P., Currie G. A. The cellular oncogene p53 can be activated by mutagenesis. 1985 Oct 31-Nov 6Nature. 317(6040):816–818. doi: 10.1038/317816a0. [DOI] [PubMed] [Google Scholar]
- Jenkins J. R., Rudge K., Currie G. A. Cellular immortalization by a cDNA clone encoding the transformation-associated phosphoprotein p53. Nature. 1984 Dec 13;312(5995):651–654. doi: 10.1038/312651a0. [DOI] [PubMed] [Google Scholar]
- Jenkins J. R., Rudge K., Redmond S., Wade-Evans A. Cloning and expression analysis of full length mouse cDNA sequences encoding the transformation associated protein p53. Nucleic Acids Res. 1984 Jul 25;12(14):5609–5626. doi: 10.1093/nar/12.14.5609. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones N., Shenk T. Isolation of deletion and substitution mutants of adenovirus type 5. Cell. 1978 Jan;13(1):181–188. doi: 10.1016/0092-8674(78)90148-4. [DOI] [PubMed] [Google Scholar]
- Kessler S. W. Rapid isolation of antigens from cells with a staphylococcal protein A-antibody adsorbent: parameters of the interaction of antibody-antigen complexes with protein A. J Immunol. 1975 Dec;115(6):1617–1624. [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Lane D. P., Crawford L. V. T antigen is bound to a host protein in SV40-transformed cells. Nature. 1979 Mar 15;278(5701):261–263. doi: 10.1038/278261a0. [DOI] [PubMed] [Google Scholar]
- Linzer D. I., Levine A. J. Characterization of a 54K dalton cellular SV40 tumor antigen present in SV40-transformed cells and uninfected embryonal carcinoma cells. Cell. 1979 May;17(1):43–52. doi: 10.1016/0092-8674(79)90293-9. [DOI] [PubMed] [Google Scholar]
- Mak I., Mak S., Benchimol S. Expression of the cellular p53 protein in cells transformed by adenovirus 12 and viral DNA fragments. Virology. 1988 Mar;163(1):201–204. doi: 10.1016/0042-6822(88)90248-6. [DOI] [PubMed] [Google Scholar]
- Matlashewski G., Banks L., Pim D., Crawford L. Analysis of human p53 proteins and mRNA levels in normal and transformed cells. Eur J Biochem. 1986 Feb 3;154(3):665–672. doi: 10.1111/j.1432-1033.1986.tb09449.x. [DOI] [PubMed] [Google Scholar]
- Mercer W. E., Avignolo C., Baserga R. Role of the p53 protein in cell proliferation as studied by microinjection of monoclonal antibodies. Mol Cell Biol. 1984 Feb;4(2):276–281. doi: 10.1128/mcb.4.2.276. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mercer W. E., Nelson D., DeLeo A. B., Old L. J., Baserga R. Microinjection of monoclonal antibody to protein p53 inhibits serum-induced DNA synthesis in 3T3 cells. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6309–6312. doi: 10.1073/pnas.79.20.6309. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oren M., Maltzman W., Levine A. J. Post-translational regulation of the 54K cellular tumor antigen in normal and transformed cells. Mol Cell Biol. 1981 Feb;1(2):101–110. doi: 10.1128/mcb.1.2.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Parada L. F., Land H., Weinberg R. A., Wolf D., Rotter V. Cooperation between gene encoding p53 tumour antigen and ras in cellular transformation. Nature. 1984 Dec 13;312(5995):649–651. doi: 10.1038/312649a0. [DOI] [PubMed] [Google Scholar]
- Pilder S., Moore M., Logan J., Shenk T. The adenovirus E1B-55K transforming polypeptide modulates transport or cytoplasmic stabilization of viral and host cell mRNAs. Mol Cell Biol. 1986 Feb;6(2):470–476. doi: 10.1128/mcb.6.2.470. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pinhasi-Kimhi O., Michalovitz D., Ben-Zeev A., Oren M. Specific interaction between the p53 cellular tumour antigen and major heat shock proteins. Nature. 1986 Mar 13;320(6058):182–184. doi: 10.1038/320182a0. [DOI] [PubMed] [Google Scholar]
- Reich N. C., Levine A. J. Growth regulation of a cellular tumour antigen, p53, in nontransformed cells. Nature. 1984 Mar 8;308(5955):199–201. doi: 10.1038/308199a0. [DOI] [PubMed] [Google Scholar]
- Reich N. C., Oren M., Levine A. J. Two distinct mechanisms regulate the levels of a cellular tumor antigen, p53. Mol Cell Biol. 1983 Dec;3(12):2143–2150. doi: 10.1128/mcb.3.12.2143. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rogel A., Popliker M., Webb C. G., Oren M. p53 cellular tumor antigen: analysis of mRNA levels in normal adult tissues, embryos, and tumors. Mol Cell Biol. 1985 Oct;5(10):2851–2855. doi: 10.1128/mcb.5.10.2851. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sarnow P., Hearing P., Anderson C. W., Halbert D. N., Shenk T., Levine A. J. Adenovirus early region 1B 58,000-dalton tumor antigen is physically associated with an early region 4 25,000-dalton protein in productively infected cells. J Virol. 1984 Mar;49(3):692–700. doi: 10.1128/jvi.49.3.692-700.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sarnow P., Ho Y. S., Williams J., Levine A. J. Adenovirus E1b-58kd tumor antigen and SV40 large tumor antigen are physically associated with the same 54 kd cellular protein in transformed cells. Cell. 1982 Feb;28(2):387–394. doi: 10.1016/0092-8674(82)90356-7. [DOI] [PubMed] [Google Scholar]
- Simanis V., Lane D. P. An immunoaffinity purification procedure for SV40 large T antigen. Virology. 1985 Jul 15;144(1):88–100. doi: 10.1016/0042-6822(85)90308-3. [DOI] [PubMed] [Google Scholar]
- Stürzbecher H. W., Chumakov P., Welch W. J., Jenkins J. R. Mutant p53 proteins bind hsp 72/73 cellular heat shock-related proteins in SV40-transformed monkey cells. Oncogene. 1987 May;1(2):201–211. [PubMed] [Google Scholar]
- Tainsky M. A., Shamanski F. L., Blair D., Vande Woude G. Human recipient cell for oncogene transfection studies. Mol Cell Biol. 1987 Mar;7(3):1280–1284. doi: 10.1128/mcb.7.3.1280. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thomas R., Kaplan L., Reich N., Lane D. P., Levine A. J. Characterization of human p53 antigens employing primate specific monoclonal antibodies. Virology. 1983 Dec;131(2):502–517. doi: 10.1016/0042-6822(83)90516-0. [DOI] [PubMed] [Google Scholar]
- Wade-Evans A., Jenkins J. R. Precise epitope mapping of the murine transformation-associated protein, p53. EMBO J. 1985 Mar;4(3):699–706. doi: 10.1002/j.1460-2075.1985.tb03686.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zantema A., Schrier P. I., Davis-Olivier A., van Laar T., Vaessen R. T., van der EB A. J. Adenovirus serotype determines association and localization of the large E1B tumor antigen with cellular tumor antigen p53 in transformed cells. Mol Cell Biol. 1985 Nov;5(11):3084–3091. doi: 10.1128/mcb.5.11.3084. [DOI] [PMC free article] [PubMed] [Google Scholar]