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. 1981 Jan;37(1):36–47. doi: 10.1128/jvi.37.1.36-47.1981

Protein-coding potential of mouse mammary tumor virus genome RNA as examined by in vitro translation.

C Dickson, G Peters
PMCID: PMC170979  PMID: 6260988

Abstract

The protein-coding capacity of the mouse mammary tumor virus genome has been examined by in vitro translation of genome length and polyadenylated subgenomic fragments of viral RNA. Intact genome RNA of about 35S programmed synthesis of the Pr77gag, Pr110gag and Pr160gag/pol precursors seen in infected cells in vivo. Polyadenylated RNA fragments of 18 to 28S encoded products whose tryptic peptide maps resembled those of the nonglycosylated precursor to the envelope glycoproteins, confirming the gene order 5'-gag-pol-env-3'. Translation of polyadenylated RNA fragments smaller than 18S yielded a series of related proteins whose peptide maps bore no resemblance to any of the virion structural proteins. Thus, a region of the mouse mammary tumor virus genome distal to the env gene appears to have an open reading frame sufficient to encode at least 36,000 daltons of protein as of yet unknown function.

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Selected References

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

  1. Atkins J. F., Gesteland R. F., Reid B. R., Anderson C. W. Normal tRNAs promote ribosomal frameshifting. Cell. 1979 Dec;18(4):1119–1131. doi: 10.1016/0092-8674(79)90225-3. [DOI] [PubMed] [Google Scholar]
  2. Austen B. M. Predicted secondary structures of amino-terminal extension sequences of secreted proteins. FEBS Lett. 1979 Jul 15;103(2):308–313. doi: 10.1016/0014-5793(79)81351-4. [DOI] [PubMed] [Google Scholar]
  3. Baltimore D. Tumor viruses: 1974. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 2):1187–1200. doi: 10.1101/sqb.1974.039.01.137. [DOI] [PubMed] [Google Scholar]
  4. Brugge J. S., Erikson R. L. Identification of a transformation-specific antigen induced by an avian sarcoma virus. Nature. 1977 Sep 22;269(5626):346–348. doi: 10.1038/269346a0. [DOI] [PubMed] [Google Scholar]
  5. Coffin J. M., Billeter M. A. A physical map of the Rous sarcoma virus genome. J Mol Biol. 1976 Jan 25;100(3):293–318. doi: 10.1016/s0022-2836(76)80065-4. [DOI] [PubMed] [Google Scholar]
  6. Collett M. S., Erikson E., Purchio A. F., Brugge J. S., Erikson R. L. A normal cell protein similar in structure and function to the avian sarcoma virus transforming gene product. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3159–3163. doi: 10.1073/pnas.76.7.3159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Collett M. S., Erikson R. L. Protein kinase activity associated with the avian sarcoma virus src gene product. Proc Natl Acad Sci U S A. 1978 Apr;75(4):2021–2024. doi: 10.1073/pnas.75.4.2021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dahl H. H., Dickson C. Cell-free synthesis of mouse mammary tumor virus Pr77 from virion and intracellular mRNA. J Virol. 1979 Mar;29(3):1131–1141. doi: 10.1128/jvi.29.3.1131-1141.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dickson C., Atterwill M. Composition, arrangement and cleavage of the mouse mammary tumor virus polyprotein precursor Pr77gag and p110gag. Cell. 1979 Aug;17(4):1003–1012. doi: 10.1016/0092-8674(79)90339-8. [DOI] [PubMed] [Google Scholar]
  10. Dickson C., Atterwill M. Polyproteins related to the major core protein of mouse mammary tumor virus. J Virol. 1978 Jun;26(3):660–672. doi: 10.1128/jvi.26.3.660-672.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dickson C., Atterwill M. Structure and processing of the mouse mammary tumor virus glycoprotein precursor pr73env. J Virol. 1980 Aug;35(2):349–361. doi: 10.1128/jvi.35.2.349-361.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dickson C., Puma J. P., Nandi S. Identification of a precursor protein to the major glycoproteins of mouse mammary tumor virus. J Virol. 1975 Jan;17(1):275–282. doi: 10.1128/jvi.17.1.275-282.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Eiden J. J., Nichols J. L. Characterization of poly(riboadenylic acid) segments in L-cell messenger ribonucleic acid. Biochemistry. 1973 Sep 25;12(20):3951–3956. doi: 10.1021/bi00744a026. [DOI] [PubMed] [Google Scholar]
  14. Erikson E., Collett M. S., Erikson R. L. In vitro synthesis of a functional avian sarcoma virus transforming-gene product. Nature. 1978 Aug 31;274(5674):919–921. doi: 10.1038/274919a0. [DOI] [PubMed] [Google Scholar]
  15. Fine D. L., Plowman J. K., Kelley S. P., Arthur L. O., Hillman E. A. Enhanced production of mouse mammary tumor virus in dexamethasone-treated, 5-iododeoxyuridine-stimulated mammary tumor cell cultures. J Natl Cancer Inst. 1974 Jun;52(6):1881–1886. doi: 10.1093/jnci/52.6.1881. [DOI] [PubMed] [Google Scholar]
  16. Furuichi Y., Shatkin A. J., Stavnezer E., Bishop J. M. Blocked, methylated 5'-terminal sequence in avian sarcoma virus RNA. Nature. 1975 Oct 16;257(5527):618–620. doi: 10.1038/257618a0. [DOI] [PubMed] [Google Scholar]
  17. Groner B., Hynes N. E., Diggelmann H. Identification of mouse mammary tumor virus-specific mRNA. J Virol. 1979 Apr;30(1):417–420. doi: 10.1128/jvi.30.1.417-420.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hilgers J., Bentvelzen P. Interaction between viral and genetic factors in murine mammary cancer. Adv Cancer Res. 1978;26:143–195. doi: 10.1016/s0065-230x(08)60087-1. [DOI] [PubMed] [Google Scholar]
  19. Jamjoom G. A., Naso R. B., Arlinghaus R. B. Further characterization of intracellular precursor polyproteins of Rauscher leukemia virus. Virology. 1977 May 1;78(1):11–34. doi: 10.1016/0042-6822(77)90075-7. [DOI] [PubMed] [Google Scholar]
  20. Keith J., Fraenkel-Conrat H. Identification of the 5' end of Rous sarcoma virus RNA. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3347–3350. doi: 10.1073/pnas.72.9.3347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kerr I. M., Olshevsky U., Lodish H. F., Baltimore D. Translation of murine leukemia virus RNA in cell-free systems from animal cells. J Virol. 1976 May;18(2):627–635. doi: 10.1128/jvi.18.2.627-635.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kopchick J. J., Jamjoom G. A., Watson K. F., Arlinghaus R. B. Biosynthesis of reverse transcriptase from Rauscher murine leukemia virus by synthesis and cleavage of a gag-pol read-through viral precursor polyprotein. Proc Natl Acad Sci U S A. 1978 Apr;75(4):2016–2020. doi: 10.1073/pnas.75.4.2016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Laskey R. A., Mills A. D. Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography. Eur J Biochem. 1975 Aug 15;56(2):335–341. doi: 10.1111/j.1432-1033.1975.tb02238.x. [DOI] [PubMed] [Google Scholar]
  25. Levinson A. D., Oppermann H., Levintow L., Varmus H. E., Bishop J. M. Evidence that the transforming gene of avian sarcoma virus encodes a protein kinase associated with a phosphoprotein. Cell. 1978 Oct;15(2):561–572. doi: 10.1016/0092-8674(78)90024-7. [DOI] [PubMed] [Google Scholar]
  26. Martin G. S. Rous sarcoma virus: a function required for the maintenance of the transformed state. Nature. 1970 Sep 5;227(5262):1021–1023. doi: 10.1038/2271021a0. [DOI] [PubMed] [Google Scholar]
  27. Nusse R., Asselbergs F. A., Salden M. H., Michalides R. J., Bloemendal H. Translation of mouse mammary tumor virus RNA: precursor polypeptides are phosphorylated during processing. Virology. 1978 Nov;91(1):106–115. doi: 10.1016/0042-6822(78)90359-8. [DOI] [PubMed] [Google Scholar]
  28. Oppermann H., Bishop J. M., Varmus H. E., Levintow L. A joint produce of the genes gag and pol of avian sarcoma virus: a possible precursor of reverse transcriptase. Cell. 1977 Dec;12(4):993–1005. doi: 10.1016/0092-8674(77)90164-7. [DOI] [PubMed] [Google Scholar]
  29. Oppermann H., Levinson A. D., Varmus H. E., Levintow L., Bishop J. M. Uninfected vertebrate cells contain a protein that is closely related to the product of the avian sarcoma virus transforming gene (src). Proc Natl Acad Sci U S A. 1979 Apr;76(4):1804–1808. doi: 10.1073/pnas.76.4.1804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Papkoff J., Hunter T., Beemon K. In vitro translation of virion RNA from Moloney murine sarcoma virus. Virology. 1980 Feb;101(1):91–103. doi: 10.1016/0042-6822(80)90486-9. [DOI] [PubMed] [Google Scholar]
  31. Pelham H. R., Jackson R. J. An efficient mRNA-dependent translation system from reticulocyte lysates. Eur J Biochem. 1976 Aug 1;67(1):247–256. doi: 10.1111/j.1432-1033.1976.tb10656.x. [DOI] [PubMed] [Google Scholar]
  32. Philipson L., Andersson P., Olshevsky U., Weinberg R., Baltimore D., Gesteland R. Translation of MuLV and MSV RNAs in nuclease-treated reticulocyte extracts: enhancement of the gag-pol polypeptide with yeast suppressor tRNA. Cell. 1978 Jan;13(1):189–199. doi: 10.1016/0092-8674(78)90149-6. [DOI] [PubMed] [Google Scholar]
  33. Racevskis J., Sarkar N. H. Synthesis and processing of precursor polypeptides to murine mammary tumor virus structural proteins. J Virol. 1978 Jan;25(1):374–383. doi: 10.1128/jvi.25.1.374-383.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Ringold G. M., Yamamoto K. R., Shank P. R., Varmus H. E. Mouse mammary tumor virus DNA in infected rat cells: characterization of unintegrated forms. Cell. 1977 Jan;10(1):19–26. doi: 10.1016/0092-8674(77)90135-0. [DOI] [PubMed] [Google Scholar]
  35. Ringold G., Lasfargues E. Y., Bishop J. M., Varmus H. E. Production of mouse mammary tumor virus by cultured cells in the absence and presence of hormones: assay by molecular hybridization. Virology. 1975 May;65(1):135–147. doi: 10.1016/0042-6822(75)90014-8. [DOI] [PubMed] [Google Scholar]
  36. Robertson D. L., Varmus H. E. Structural analysis of the intracellular RNAs of murine mammary tumor virus. J Virol. 1979 May;30(2):576–589. doi: 10.1128/jvi.30.2.576-589.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schochetman G., Long C. W., Oroszlan S., Arthur L., Fine D. L. Isolation of separate precursor polypeptides for the mouse mammary tumor virus glycoproteins and nonglycoproteins. Virology. 1978 Mar;85(1):168–174. doi: 10.1016/0042-6822(78)90421-x. [DOI] [PubMed] [Google Scholar]
  38. Sefton B. M., Beemon K., Hunter T. Comparison of the expression of the src gene of Rous sarcoma virus in vitro and in vivo. J Virol. 1978 Dec;28(3):957–971. doi: 10.1128/jvi.28.3.957-971.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sefton B. M., Hunter T., Beemon K. Product of in vitro translation of the Rous sarcoma virus src gene has protein kinase activity. J Virol. 1979 Apr;30(1):311–318. doi: 10.1128/jvi.30.1.311-318.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sen G. C., Smith S. W., Marcus S. L., Sarkar N. H. Identification of the messenger RNAs coding for the gag and env gene products of the murine mammary tumor virus. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1736–1740. doi: 10.1073/pnas.76.4.1736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Shank P. R., Cohen J. C., Varmus H. E., Yamamoto K. R., Ringold G. M. Mapping of linear and circular forms of mouse mammary tumor virus DNA with restriction endonucleases: evidence for a large specific deletion occurring at high frequency during circularization. Proc Natl Acad Sci U S A. 1978 May;75(5):2112–2116. doi: 10.1073/pnas.75.5.2112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Shields A., Goff S., Paskind M., Otto G., Baltimore D. Structure of the Abelson murine leukemia virus genome. Cell. 1979 Dec;18(4):955–962. doi: 10.1016/0092-8674(79)90208-3. [DOI] [PubMed] [Google Scholar]
  43. Varmus H. E., Ringold G., Yamamoto K. R. Regulation of mouse mammary tumor virus gene expression by glucocorticoid hormones. Monogr Endocrinol. 1979;12:253–278. doi: 10.1007/978-3-642-81265-1_14. [DOI] [PubMed] [Google Scholar]
  44. Wang L. H., Duesberg P. Properties and location of poly(A) in Rous sarcoma virus RNA. J Virol. 1974 Dec;14(6):1515–1529. doi: 10.1128/jvi.14.6.1515-1529.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wang L., Galehouse D., Mellon P., Duesberg P., Mason W. S., Vogt P. K. Mapping oligonucleotides of Rous sarcoma virus RNA that segregate with polymerase and group-specific antigen markers in recombinants. Proc Natl Acad Sci U S A. 1976 Nov;73(11):3952–3956. doi: 10.1073/pnas.73.11.3952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Weiss S. R., Hackett P. B., Oppermann H., Ullrich A., Levintow L., Bishop J. M. Cell-free translation of avian sarcoma virus RNA: suppression of the gag termination codon does not augment synthesis of the joint gag/pol product. Cell. 1978 Oct;15(2):607–614. doi: 10.1016/0092-8674(78)90029-6. [DOI] [PubMed] [Google Scholar]
  47. Závada J., Dickson C., Weiss R. Pseudotypes of vesicular stomatitis virus with envelope antigens provided by murine mammary tumor virus. Virology. 1977 Oct 1;82(1):221–231. doi: 10.1016/0042-6822(77)90045-9. [DOI] [PubMed] [Google Scholar]

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