Home LiteratureArticle Details
PMID: 2642977 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Mutation is required to activate the p53 gene for cooperation with the ras oncogene and transformation.

Journal of virology ·Vol. 63 ·No. 2 ·1989-02-00 ·Pages 739-46

Hinds P, Finlay C, Levine AJ

Abstract

Previous experiments have brought into question which amino acid sequence of the p53 oncogene product should be considered wild type and whether the normal protein is capable of cooperating with the ras oncogene to transform cells in culture. To address these questions, a series of p53 cDNA-genomic hybrid clones have been compared for the ability to cooperate with the ras oncogene in transformation assays. From these experiments, it has become clear that the amino acid alanine at position 135, in either the genomic clone or the cDNA clone, failed to produce a p53 protein that cooperated with the ras oncogene and transformed cells. Replacing alanine with valine at this position in either the genomic or the cDNA clone activated for transformation in this assay. Using restriction enzyme polymorphisms in the p53 gene, it was shown that normal mouse DNA encodes alanine at position 135 in the p53 protein. Thus, mutation is required to activate the p53 protein for cooperation with the ras oncogene. After cotransfection with the activated ras gene, the genomic p53 DNA clone always produced more transformed cell foci (1.7-fold) than similar cDNA clones and these foci were more readily cloned (3.6-fold) into permanent cell lines. A series of deletion mutants of the genomic p53 clone were employed to show that the presence of intron 4 in the p53 gene was sufficient to provide much enhanced clonability of transformed foci from culture dishes. The presence of introns in the p53 gene constructions also resulted in elevated levels of p53 protein in the p53-plus-ras-transformed cell lines. Thus, qualitative changes in the p53 protein are required to activate p53 for transformation with the oncogene ras. Quantitative improvements of transformation frequencies are associated with the higher expression levels of altered p53 protein that are provided by having one of the p53 introns in the transforming plasmid.

MeSH Terms
Amino Acid Sequence Animals Antigens, Polyomavirus Transforming/physiology Cell Transformation, Neoplastic/genetics Cells, Cultured DNA/genetics Fibroblasts Introns Mice Mice, Inbred BALB C/genetics Neoplasm Proteins/genetics,physiology Oncogenes Phosphoproteins/genetics,physiology Proto-Oncogene Proteins/physiology Proto-Oncogene Proteins p21(ras) Rats Tumor Suppressor Protein p53
Chemicals
Antigens, Polyomavirus Transforming Neoplasm Proteins Phosphoproteins Proto-Oncogene Proteins Tumor Suppressor Protein p53 DNA Proto-Oncogene Proteins p21(ras)
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Hinds P
Department of Molecular Biology, Princeton University, New Jersey 08544.
Finlay C
Levine A J
References (29)
29 references, click to expand
  1. The induction of ovalbumin and conalbumin mRNA by estrogen and progesterone in chick oviduct explant cultures.
    Cell. 1978 Jun;14(2):403-13 PMID: 566622
  2. T antigen is bound to a host protein in SV40-transformed cells.
    Nature. 1979 Mar 15;278(5701):261-3 PMID: 218111
  3. 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 PMID: 222475
  4. Sequencing end-labeled DNA with base-specific chemical cleavages.
    Methods Enzymol. 1980;65(1):499-560 PMID: 6246368
  5. Abelson murine leukemia virus-induced tumors elicit antibodies against a host cell protein, P50.
    J Virol. 1980 Nov;36(2):547-55 PMID: 6159484
  6. p53 transformation-related protein: detection by monoclonal antibody in mouse and human cells.
    Proc Natl Acad Sci U S A. 1981 Mar;78(3):1695-9 PMID: 6940183
  7. 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):41-5 PMID: 6264441
  8. Monoclonal antibodies specific for simian virus 40 tumor antigens.
    J Virol. 1981 Sep;39(3):861-9 PMID: 6169844
  9. 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):387-94 PMID: 6277513
  10. Isolation and preliminary characterization of a human transforming gene from T24 bladder carcinoma cells.
    Nature. 1982 Apr 1;296(5856):404-9 PMID: 7063039
  11. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity.
    Anal Biochem. 1983 Jul 1;132(1):6-13 PMID: 6312838
  12. A single gene and a pseudogene for the cellular tumour antigen p53.
    Nature. 1983 Dec 8-14;306(5943):594-7 PMID: 6646235
  13. Two distinct mechanisms regulate the levels of a cellular tumor antigen, p53.
    Mol Cell Biol. 1983 Dec;3(12):2143-50 PMID: 6318085
  14. Cloning and expression analysis of full length mouse cDNA sequences encoding the transformation associated protein p53.
    Nucleic Acids Res. 1984 Jul 25;12(14):5609-26 PMID: 6379601
  15. Analysis of the gene coding for the murine cellular tumour antigen p53.
    EMBO J. 1984 Sep;3(9):2179-83 PMID: 6092064
  16. Use of adeno-associated virus as a mammalian DNA cloning vector: transduction of neomycin resistance into mammalian tissue culture cells.
    Proc Natl Acad Sci U S A. 1984 Oct;81(20):6466-70 PMID: 6093102
  17. Participation of p53 cellular tumour antigen in transformation of normal embryonic cells.
    Nature. 1984 Dec 13-19;312(5995):646-9 PMID: 6095116
  18. Cooperation between gene encoding p53 tumour antigen and ras in cellular transformation.
    Nature. 1984 Dec 13-19;312(5995):649-51 PMID: 6390217
  19. Precise epitope mapping of the murine transformation-associated protein, p53.
    EMBO J. 1985 Mar;4(3):699-706 PMID: 2408882
  20. Overproduction of p53 antigen makes established cells highly tumorigenic.
    Nature. 1985 Jul 11-17;316(6024):158-60 PMID: 3892307
  21. The amino acid sequence of murine p53 determined from a c-DNA clone.
    Virology. 1984 Apr 30;134(2):477-82 PMID: 6400059
  22. Monoclonal antibody analysis of p53 expression in normal and transformed cells.
    J Virol. 1986 Aug;59(2):444-52 PMID: 2426467
  23. Identification of the p53 protein domain involved in formation of the simian virus 40 large T-antigen-p53 protein complex.
    J Virol. 1986 Sep;59(3):574-83 PMID: 3016321
  24. p53 cellular tumor antigen: analysis of mRNA levels in normal adult tissues, embryos, and tumors.
    Mol Cell Biol. 1985 Oct;5(10):2851-5 PMID: 3915536
  25. Immunologically distinct p53 molecules generated by alternative splicing.
    Mol Cell Biol. 1986 Sep;6(9):3232-9 PMID: 3023970
  26. Immunological evidence for the association of p53 with a heat shock protein, hsc70, in p53-plus-ras-transformed cell lines.
    Mol Cell Biol. 1987 Aug;7(8):2863-9 PMID: 3313006
  27. Post-translational regulation of the 54K cellular tumor antigen in normal and transformed cells.
    Mol Cell Biol. 1981 Feb;1(2):101-10 PMID: 6100960
  28. Activating mutations for transformation by p53 produce a gene product that forms an hsc70-p53 complex with an altered half-life.
    Mol Cell Biol. 1988 Feb;8(2):531-9 PMID: 2832726
  29. Immortalization of rat embryo fibroblasts by the cellular p53 oncogene.
    Oncogene. 1988 May;2(5):445-52 PMID: 3287278
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1989-02-00
Pages
739-46
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC247745
Subset
IM
Grants
NCI NIH HHS · P01-CA41086-03 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]