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. 1979 Jul;31(1):53–62. doi: 10.1128/jvi.31.1.53-62.1979

Diversity of mammary tumor viral genes within the genus Mus, the species Mus musculus, and the strain C3H.

W Drohan, J Schlom
PMCID: PMC353421  PMID: 228059

Abstract

Proviral sequences complementary to the C3H mouse mammary tumor virus RNA genome are present in the DNA of early occurring mammary tumors of C3H/HeN mice and are absent from apparently normal C3H/HeN tissues; these sequences are non-germ line transmitted in C3H/HeN mice and have been termed tumor-associated sequences; (W. Drohan et al., J. Virol. 21:986-995, 1977). We report here that tumor-associated sequences are present in the DNA of spontaneous mammary tumors that occur early in the life of several inbred, high-tumor-incidence mouse strains but are absent in mammary tumors that occur later in life in low- and moderate-tumor-incidence strains. These sequences are also absent in apparently normal organs tested from numerous laboratory mouse strains, feral mice, Mus musculus subspecies, and other Mus species. Sequences represented in tumor-associated sequence RNA, however, are present as endogenous provirus in GR mice (at approximately four copies per haploid genome) and in two of five substrains of C3H mice tested (at approximately one copy per haploid genome). The two substrains of C3H mice positive for endogenous tumor-associated sequence provirus were recently (circa 1930) separated from the negative substrains of C3H mice. The results may be explained by the unlikely chance segregation of proviral sequences or by the recent integration of viral genes (within the last few decades). Whereas radioactively labeled mouse mammary tumor virus 60-70S RNA or complementary DNA detected mouse mammary tumor virus-related proviral information in all laboratory mouse strains, feral mice, subspecies of M. musculus, and other species of Mus, the use of tumor-associated sequence RNA clearly revealed the genetic diversity that may exist between different colonies or substrains of "inbred" laboratory mice commonly used in cancer research.

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Selected References

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

  1. Baluda M. A., Drohan W. N. Distribution of deoxyribonucleic acid complementary to the ribonucleic acid of avian myeloblastosis virus in tissues of normal and tumor-bearing chickens. J Virol. 1972 Nov;10(5):1002–1009. doi: 10.1128/jvi.10.5.1002-1009.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bedigian H. G., Meier H. Isolation of an endogenous C-type RNA virus from Mus musculus molossinus. J Natl Cancer Inst. 1975 Oct;55(4):1007–1010. doi: 10.1093/jnci/55.4.1007. [DOI] [PubMed] [Google Scholar]
  3. Benveniste R. E., Callahan R., Sherr C. J., Chapman V., Todaro G. J. Two distinct endogenous type C viruses isolated from the asian rodent Mus cervicolor: conservation of virogene sequences in related rodent species. J Virol. 1977 Mar;21(3):849–862. doi: 10.1128/jvi.21.3.849-862.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Callahan R., Benveniste R. E., Sherr C. J., Schidlovsky G., Todaro G. J. A new class of genetically transmitted retravirus isolated from Mus cervicolor. Proc Natl Acad Sci U S A. 1976 Oct;73(10):3579–3583. doi: 10.1073/pnas.73.10.3579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Callahan R., Sherr C. J., Todaro G. J. A new class of murine retroviruses: immunological and biochemical comparison of novel isolates from Mus cervicolor and Mus caroli. Virology. 1977 Jul 15;80(2):401–406. doi: 10.1016/s0042-6822(77)80015-9. [DOI] [PubMed] [Google Scholar]
  6. Colcher D., Drohan W., Schlom Mason-Pfizer virus RNA genome: relationship to the RNA of morphologically similar isolates and other oncornaviruses. J Virol. 1976 Mar;17(3):705–712. doi: 10.1128/jvi.17.3.705-712.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Drohan W., Colcher D., Schlom J. The use of standard and relaxed hybridization conditions to detect two classes of sequences related to type-D retroviruses in the DNAs of primates. Biochim Biophys Acta. 1978 Nov 21;521(1):1–15. doi: 10.1016/0005-2787(78)90244-7. [DOI] [PubMed] [Google Scholar]
  8. Drohan W., Kettmann R., Colcher D., Schlom J. Isolation of the mouse mammary tumor virus sequences not transmitted as germinal provirus in the C3H and RIII mouse strains. J Virol. 1977 Mar;21(3):986–995. doi: 10.1128/jvi.21.3.986-995.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Drohan W., Schlom J. Differential distribution of mouse mammary tumor virus-related sequences in the DNA's of rats. J Natl Cancer Inst. 1979 May;62(5):1279–1286. doi: 10.1093/jnci/62.5.1279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. GROSS L. Susceptibility of suckling-infant, and resistance of adult, mice of the C3H and of the C57 lines to inoculation with Ak leukemia. Cancer. 1950 Nov;3(6):1073–1087. doi: 10.1002/1097-0142(1950)3:6<1073::aid-cncr2820030618>3.0.co;2-5. [DOI] [PubMed] [Google Scholar]
  11. Gross L. Viral etiology of leukemia and lymphomas in mice. A brief historical survey and present status. Zentralbl Bakteriol Orig A. 1972 May;220(1):57–65. [PubMed] [Google Scholar]
  12. Howard D. K., Colcher D., Teramoto Y. A., Young J. M., Schlom J. Characterization of mouse mammary tumor viruses propagated in heterologous cells. Cancer Res. 1977 Aug;37(8 Pt 1):2696–2704. [PubMed] [Google Scholar]
  13. Jaenisch R. Germ line integration and Mendelian transmission of the exogenous Moloney leukemia virus. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1260–1264. doi: 10.1073/pnas.73.4.1260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jaenisch R. Germ line integration of moloney leukemia virus: effect of homozygosity at the m-mulV locus. Cell. 1977 Nov;12(3):691–696. doi: 10.1016/0092-8674(77)90269-0. [DOI] [PubMed] [Google Scholar]
  15. Martinson H. G., Wagenaar E. B. Thermal elution chromatography of nucleic acids on hydroxyapatite. Biochim Biophys Acta. 1977 Feb 3;474(3):445–455. doi: 10.1016/0005-2787(77)90273-8. [DOI] [PubMed] [Google Scholar]
  16. McGrath C. M., Marineau E. J., Voyles B. A. Changes in MuMTV DNA and RNA levels in Balb/c mammary epithelial cells during malignant transformation by exogenous MuTV and by hormones. Virology. 1978 Jun 15;87(2):339–353. doi: 10.1016/0042-6822(78)90139-3. [DOI] [PubMed] [Google Scholar]
  17. Michalides R., Schlom J. Relationship in nucleic acid sequences between mouse mammary tumor virus variants. Proc Natl Acad Sci U S A. 1975 Nov;72(11):4635–4639. doi: 10.1073/pnas.72.11.4635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Morris V. L., Medeiros E., Ringold G. M., Bishop J. M., Varmus H. E. Comparison of mouse mammary tumor virus-specific DNA in inbred, wild and Asian mice, and in tumors and normal organs from inbred mice. J Mol Biol. 1977 Jul;114(1):73–91. doi: 10.1016/0022-2836(77)90284-4. [DOI] [PubMed] [Google Scholar]
  19. Owens R. B., Hackett A. J. Tissue culture studies of mouse mammary tumor cells and associated viruses. J Natl Cancer Inst. 1972 Nov;49(5):1321–1332. [PubMed] [Google Scholar]
  20. Schlom J., Colcher D., Drohan W., Kettmann R., Michalides R., Vlahakis G., Young J. Differences in mouse mammary tumor viruses. Relationship to early and late occurring mammary tumors. Cancer. 1977 Jun;39(6 Suppl):2727–2733. doi: 10.1002/1097-0142(197706)39:6<2727::aid-cncr2820390660>3.0.co;2-p. [DOI] [PubMed] [Google Scholar]
  21. Schochetman G., Schlom J. Independent polypeptide chain initiation sites for the synthesis of different classes of proteins for an RNA tumor virus: mouse mammary tumor virus. Virology. 1976 Sep;73(2):431–441. doi: 10.1016/0042-6822(76)90404-9. [DOI] [PubMed] [Google Scholar]
  22. Shoyab M., Evans R. M., Baluda M. A. Presence in leukemic cells of avian myeloblastosis virus-specific DNA sequences absent in normal chicken cells. J Virol. 1974 Jul;14(1):47–49. doi: 10.1128/jvi.14.1.47-49.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Smith G. H. Role of the milk agent in disappearance of mammary cancer in C3H/StWi mice. J Natl Cancer Inst. 1966 Apr;36(4):685–701. doi: 10.1093/jnci/36.4.685. [DOI] [PubMed] [Google Scholar]
  24. Strong L C. The Establishment of the C(3)H Inbred Strain of Mice for the Study of Spontaneous Carcinoma of the Mammary Gland. Genetics. 1935 Nov;20(6):586–591. doi: 10.1093/genetics/20.6.586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Taylor B. A., Bedigian H. G., Meier H. Genetic studies of the Fv-1 locus of mice: linkage with Gpd-1 in recombinant inbred lines. J Virol. 1977 Jul;23(1):106–109. doi: 10.1128/jvi.23.1.106-109.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Taylor J. M., Illmensee R., Summers J. Efficeint transcription of RNA into DNA by avian sarcoma virus polymerase. Biochim Biophys Acta. 1976 Sep 6;442(3):324–330. doi: 10.1016/0005-2787(76)90307-5. [DOI] [PubMed] [Google Scholar]
  27. Teramoto Y. A., Kufe D., Schlom J. Type-specific antigenic determinants on the major external glycoprotein of high- and low-oncogenic murine mammary tumor viruses. J Virol. 1977 Nov;24(2):525–533. doi: 10.1128/jvi.24.2.525-533.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Teramoto Y. A., Schlom J. Radioimmunoassays that demonstrate type-specific and group-specific antigenic reactivities for the major internal structural protein of murine mammary tumor viruses. Cancer Res. 1978 Jul;38(7):1990–1995. doi: 10.1203/00006450-199501000-00002. [DOI] [PubMed] [Google Scholar]
  29. Varmus H. E., Bishop J. M., Nowinski R. C., Sarker N. H. Mammary tumour virus specific nucleotide sequences in mouse DNA. Nat New Biol. 1972 Aug 9;238(84):189–191. doi: 10.1038/newbio238189a0. [DOI] [PubMed] [Google Scholar]

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