Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1985 Jun;82(12):4198–4201. doi: 10.1073/pnas.82.12.4198

Rates of evolution of the retroviral oncogene of Moloney murine sarcoma virus and of its cellular homologues.

T Gojobori, S Yokoyama
PMCID: PMC397963  PMID: 2987967

Abstract

A method is proposed for computing the rates of nucleotide substitution for an oncogene of a retrovirus (v-onc), its cellular homologue (c-onc), and the retrovirus genome simultaneously. The method has been applied to DNA sequences of the v-mos gene of Moloney murine sarcoma virus (Mo-MuSV) and the c-mos and gag genes of Mo-MuSV and Moloney murine leukemia virus (Mo-MuLV). The rates of nucleotide substitution for c-mos, the gag gene, and v-mos are estimated to be 1.71 X 10(-9), 6.3 X 10(-4), and 1.31 X 10(-3) per site per year, respectively. The rate of evolution of c-mos is comparable to that of many functional genes in DNA genomes, suggesting some important biological function played by cellular oncogenes. The rates of nucleotide substitution in the v-mos and gag genes are very high and are similar to those of RNA viral genes such as the hemagglutinin and neuraminidase genes in the influenza A virus. Thus, oncogenes seem to exemplify a general feature of genome evolution: the rate of evolution of RNA genomes can be more than a million times greater than that of DNA genomes because of a high mutation rate in the RNA genome.

Full text

PDF
4198

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abelson H. T., Rabstein L. S. Influence of prednisolone on Moloney leukemogenic virus in BALB-c mice. Cancer Res. 1970 Aug;30(8):2208–2212. [PubMed] [Google Scholar]
  2. Air G. M. Sequence relationships among the hemagglutinin genes of 12 subtypes of influenza A virus. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7639–7643. doi: 10.1073/pnas.78.12.7639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Battula N., Loeb L. A. The infidelity of avian myeloblastosis virus deoxyribonucleic acid polymerase in polynucleotide replication. J Biol Chem. 1974 Jul 10;249(13):4086–4093. [PubMed] [Google Scholar]
  4. Bishop J. M. Cellular oncogenes and retroviruses. Annu Rev Biochem. 1983;52:301–354. doi: 10.1146/annurev.bi.52.070183.001505. [DOI] [PubMed] [Google Scholar]
  5. Darlix J. L., Spahr P. F. High spontaneous mutation rate of Rous sarcoma virus demonstrated by direct sequencing of the RNA genome. Nucleic Acids Res. 1983 Sep 10;11(17):5953–5967. doi: 10.1093/nar/11.17.5953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Efstratiadis A., Posakony J. W., Maniatis T., Lawn R. M., O'Connell C., Spritz R. A., DeRiel J. K., Forget B. G., Weissman S. M., Slightom J. L. The structure and evolution of the human beta-globin gene family. Cell. 1980 Oct;21(3):653–668. doi: 10.1016/0092-8674(80)90429-8. [DOI] [PubMed] [Google Scholar]
  7. Gojobori T. Codon substitution in evolution and the "saturation" of synonymous changes. Genetics. 1983 Dec;105(4):1011–1027. doi: 10.1093/genetics/105.4.1011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gojobori T., Ishii K., Nei M. Estimation of average number of nucleotide substitutions when the rate of substitution varies with nucleotide. J Mol Evol. 1982;18(6):414–423. doi: 10.1007/BF01840889. [DOI] [PubMed] [Google Scholar]
  9. Heldin C. H., Westermark B. Growth factors: mechanism of action and relation to oncogenes. Cell. 1984 May;37(1):9–20. doi: 10.1016/0092-8674(84)90296-4. [DOI] [PubMed] [Google Scholar]
  10. Holland J., Spindler K., Horodyski F., Grabau E., Nichol S., VandePol S. Rapid evolution of RNA genomes. Science. 1982 Mar 26;215(4540):1577–1585. doi: 10.1126/science.7041255. [DOI] [PubMed] [Google Scholar]
  11. Kelly K., Cochran B. H., Stiles C. D., Leder P. Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor. Cell. 1983 Dec;35(3 Pt 2):603–610. doi: 10.1016/0092-8674(83)90092-2. [DOI] [PubMed] [Google Scholar]
  12. Kimura M. Estimation of evolutionary distances between homologous nucleotide sequences. Proc Natl Acad Sci U S A. 1981 Jan;78(1):454–458. doi: 10.1073/pnas.78.1.454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Krystal M., Buonagurio D., Young J. F., Palese P. Sequential mutations in the NS genes of influenza virus field strains. J Virol. 1983 Feb;45(2):547–554. doi: 10.1128/jvi.45.2.547-554.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Li W. H., Gojobori T., Nei M. Pseudogenes as a paradigm of neutral evolution. Nature. 1981 Jul 16;292(5820):237–239. doi: 10.1038/292237a0. [DOI] [PubMed] [Google Scholar]
  15. Mark G. E., Rapp U. R. Primary structure of v-raf: relatedness to the src family of oncogenes. Science. 1984 Apr 20;224(4646):285–289. doi: 10.1126/science.6324342. [DOI] [PubMed] [Google Scholar]
  16. Martínez C., del Rio L., Portela A., Domingo E., Ortín J. Evolution of the influenza virus neuraminidase gene during drift of the N2 subtype. Virology. 1983 Oct 30;130(2):539–545. doi: 10.1016/0042-6822(83)90108-3. [DOI] [PubMed] [Google Scholar]
  17. Moloney J. B. A virus-induced rhabdomyosarcoma of mice. Natl Cancer Inst Monogr. 1966 Sep;22:139–142. [PubMed] [Google Scholar]
  18. Papkoff J., Lai M. H., Hunter T., Verma I. M. Analysis of transforming gene products from Moloney murine sarcoma virus. Cell. 1981 Nov;27(1 Pt 2):109–119. doi: 10.1016/0092-8674(81)90365-2. [DOI] [PubMed] [Google Scholar]
  19. Perler F., Efstratiadis A., Lomedico P., Gilbert W., Kolodner R., Dodgson J. The evolution of genes: the chicken preproinsulin gene. Cell. 1980 Jun;20(2):555–566. doi: 10.1016/0092-8674(80)90641-8. [DOI] [PubMed] [Google Scholar]
  20. Reddy E. P., Smith M. J., Aaronson S. A. Complete nucleotide sequence and organization of the Moloney murine sarcoma virus genome. Science. 1981 Oct 23;214(4519):445–450. doi: 10.1126/science.6170110. [DOI] [PubMed] [Google Scholar]
  21. Reddy E. P., Smith M. J., Srinivasan A. Nucleotide sequence of Abelson murine leukemia virus genome: structural similarity of its transforming gene product to other onc gene products with tyrosine-specific kinase activity. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3623–3627. doi: 10.1073/pnas.80.12.3623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Shinnick T. M., Lerner R. A., Sutcliffe J. G. Nucleotide sequence of Moloney murine leukaemia virus. Nature. 1981 Oct 15;293(5833):543–548. doi: 10.1038/293543a0. [DOI] [PubMed] [Google Scholar]
  23. Stanton L. W., Watt R., Marcu K. B. Translocation, breakage and truncated transcripts of c-myc oncogene in murine plasmacytomas. Nature. 1983 Jun 2;303(5916):401–406. doi: 10.1038/303401a0. [DOI] [PubMed] [Google Scholar]
  24. Takahata N., Kimura M. A model of evolutionary base substitutions and its application with special reference to rapid change of pseudogenes. Genetics. 1981 Jul;98(3):641–657. doi: 10.1093/genetics/98.3.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Temin H. M. The cellular and molecular biology of RNA tumor viruses, especially avian leukosis-sarcoma viruses, and their relatives. Adv Cancer Res. 1974;19(0):47–104. doi: 10.1016/s0065-230x(08)60052-4. [DOI] [PubMed] [Google Scholar]
  26. Van Beveren C., Galleshaw J. A., Jonas V., Berns A. J., Doolittle R. F., Donoghue D. J., Verma I. M. Nucleotide sequence and formation of the transforming gene of a mouse sarcoma virus. Nature. 1981 Jan 22;289(5795):258–262. doi: 10.1038/289258a0. [DOI] [PubMed] [Google Scholar]
  27. Van Beveren C., van Straaten F., Galleshaw J. A., Verma I. M. Nucleotide sequence of the genome of a murine sarcoma virus. Cell. 1981 Nov;27(1 Pt 2):97–108. doi: 10.1016/0092-8674(81)90364-0. [DOI] [PubMed] [Google Scholar]
  28. Varmus H. E. Form and function of retroviral proviruses. Science. 1982 May 21;216(4548):812–820. doi: 10.1126/science.6177038. [DOI] [PubMed] [Google Scholar]
  29. Wang J. Y., Ledley F., Goff S., Lee R., Groner Y., Baltimore D. The mouse c-abl locus: molecular cloning and characterization. Cell. 1984 Feb;36(2):349–356. doi: 10.1016/0092-8674(84)90228-9. [DOI] [PubMed] [Google Scholar]
  30. Watson D. K., Psallidopoulos M. C., Samuel K. P., Dalla-Favera R., Papas T. S. Nucleotide sequence analysis of human c-myc locus, chicken homologue, and myelocytomatosis virus MC29 transforming gene reveals a highly conserved gene product. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3642–3645. doi: 10.1073/pnas.80.12.3642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Watson R., Oskarsson M., Vande Woude G. F. Human DNA sequence homologous to the transforming gene (mos) of Moloney murine sarcoma virus. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4078–4082. doi: 10.1073/pnas.79.13.4078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Zarling D. A., Temin H. M. High spontaneous mutation rate of an avian sarcoma virus. J Virol. 1975 Jan;17(1):74–84. doi: 10.1128/jvi.17.1.74-84.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. van der Hoorn F. A., Firzlaff J. Complete c-mos (rat) nucleotide sequence: presence of conserved domains in c-mos proteins. Nucleic Acids Res. 1984 Feb 24;12(4):2147–2156. doi: 10.1093/nar/12.4.2147. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES