Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1977 Mar;21(3):849–862. doi: 10.1128/jvi.21.3.849-862.1977

Two distinct endogenous type C viruses isolated from the asian rodent Mus cervicolor: conservation of virogene sequences in related rodent species.

R E Benveniste, R Callahan, C J Sherr, V Chapman, G J Todaro
PMCID: PMC515622  PMID: 66330

Abstract

The cocultivation of a lung cell line from the Southeast Asian mouse Mus cervicolor with cells from heterologous species has resulted in the isolation of two new distinct type C viruses. Both viruses are endogenous to M. cervicolor and are present in multiple copies in the cellular DNA of these mice. One of the viruses, designated M. cervicolor type CI, replicates readily in the SIRC rabbit cell line and is antigenically related to the infectious primate type C viruses isolated from a woolly monkey (simian sarcoma-associated virus) and gibbon apes (gibbon ape leukemia virus). This virus is also closely related by both immunological and nucleic acid hybridization criteria to a type C virus previously isolated from a second Asian murine species, Mus caroli. The isolation of the M. cervicolor type C I virus thus provides further evidence that the infectious primate type C viruses originated by trans-species infection of primates by an endogenous virus of mice. The second virus, designated M. cervicolor type C II, replicates well in various cell lines derived from the laboratory mouse Mus musculus. While antigenically related to type C viruses derived from M. musculus, the M. cervicolor type C II virus isolate can be readily distinguished from standard murine leukemia viruses. Both new type C viruses from M. cervicolor are unrelated to the previously described retrovirus (M432) isolated from the same Mus species. The DNA of M. cervicolor therefore contains multiple copies of at least three distinct classes of endogenous viral genes. An examination of the cellular DNA of other rodent species for nucleic acid sequences related to the genomes of both M. cervicolor type C I and II reveals that both viruses have been highly conserved evolutionarily, and that other species of rodents, such as laboratory mice and rats, contain endogenous virogenes related to those in the DNA of M. cervicolor.

Full text

PDF
849

Selected References

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

  1. Aaronson S. A., Hartley J. W., Todaro G. J. Mouse leukemia virus: "spontaneous" release by mouse embryo cells after long-term in vitro cultivation. Proc Natl Acad Sci U S A. 1969 Sep;64(1):87–94. doi: 10.1073/pnas.64.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aaronson S. A., Stephenson J. R. Independent segregation of loci for activation of biologically distinguishable RNA C-type viruses in mouse cells. Proc Natl Acad Sci U S A. 1973 Jul;70(7):2055–2058. doi: 10.1073/pnas.70.7.2055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ando T. A nuclease specific for heat-denatured DNA in isolated from a product of Aspergillus oryzae. Biochim Biophys Acta. 1966 Jan 18;114(1):158–168. doi: 10.1016/0005-2787(66)90263-2. [DOI] [PubMed] [Google Scholar]
  4. Benveniste R. E., Heinemann R., Wilson G. L., Callahan R., Todaro G. J. Detection of baboon type C viral sequences in various primate tissues by molecular hybridization. J Virol. 1974 Jul;14(1):56–67. doi: 10.1128/jvi.14.1.56-67.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Benveniste R. E., Lieber M. M., Todaro G. J. A distinct class of inducible murine type-C viruses that replicates in the rabbit SIRC cell line. Proc Natl Acad Sci U S A. 1974 Mar;71(3):602–606. doi: 10.1073/pnas.71.3.602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Benveniste R. E., Scolnick E. M. RNA in mammalian sarcoma virus transformed nonproducer cells homologous to murine leukemia virus RNA. Virology. 1973 Feb;51(2):370–382. doi: 10.1016/0042-6822(73)90436-4. [DOI] [PubMed] [Google Scholar]
  7. Benveniste R. E., Sherr C. J., Todaro G. J. Evolution of type C viral genes: origin of feline leukemia virus. Science. 1975 Nov 28;190(4217):886–888. doi: 10.1126/science.52892. [DOI] [PubMed] [Google Scholar]
  8. Benveniste R. E., Todaro G. J. Evolution of C-type viral genes: inheritance of exogenously acquired viral genes. Nature. 1974 Dec 6;252(5483):456–459. doi: 10.1038/252456a0. [DOI] [PubMed] [Google Scholar]
  9. Benveniste R. E., Todaro G. J. Evolution of type C viral genes: I. Nucleic acid from baboon type C virus as a measure of divergence among primate species. Proc Natl Acad Sci U S A. 1974 Nov;71(11):4513–4518. doi: 10.1073/pnas.71.11.4513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Benveniste R. E., Todaro G. J. Evolution of type C viral genes: evidence for an Asian origin of man. Nature. 1976 May 13;261(5556):101–108. doi: 10.1038/261101a0. [DOI] [PubMed] [Google Scholar]
  11. Benveniste R. E., Todaro G. J. Evolution of type C viral genes: preservation of ancestral murine type C viral sequences in pig cellular DNA. Proc Natl Acad Sci U S A. 1975 Oct;72(10):4090–4094. doi: 10.1073/pnas.72.10.4090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Benveniste R. E., Todaro G. J. Homology between type-C viruses of various species as determined by molecular hybridization. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3316–3320. doi: 10.1073/pnas.70.12.3316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Benveniste R. E., Todaro G. J. Multiple divergent copies of endogenous C-type virogenes in mammalian cells. Nature. 1974 Nov 8;252(5479):170–173. doi: 10.1038/252170a0. [DOI] [PubMed] [Google Scholar]
  14. Bittner J. J. SOME POSSIBLE EFFECTS OF NURSING ON THE MAMMARY GLAND TUMOR INCIDENCE IN MICE. Science. 1936 Aug 14;84(2172):162–162. doi: 10.1126/science.84.2172.162. [DOI] [PubMed] [Google Scholar]
  15. Britten R. J., Kohne D. E. Repeated sequences in DNA. Hundreds of thousands of copies of DNA sequences have been incorporated into the genomes of higher organisms. Science. 1968 Aug 9;161(3841):529–540. doi: 10.1126/science.161.3841.529. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. GROSS L. "Spontaneous" leukemia developing in C3H mice following inoculation in infancy, with AK-leukemic extracts, or AK-embrvos. Proc Soc Exp Biol Med. 1951 Jan;76(1):27–32. [PubMed] [Google Scholar]
  18. Hartley J. W., Rowe W. P. Naturally occurring murine leukemia viruses in wild mice: characterization of a new "amphotropic" class. J Virol. 1976 Jul;19(1):19–25. doi: 10.1128/jvi.19.1.19-25.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kawakami T. G., Buckley P. M. Antigenic studies on gibbon type-C viruses. Transplant Proc. 1974 Jun;6(2):193–196. [PubMed] [Google Scholar]
  20. Kawakami T. G., Huff S. D., Buckley P. M., Dungworth D. L., Synder S. P., Gilden R. V. C-type virus associated with gibbon lymphosarcoma. Nat New Biol. 1972 Feb 9;235(58):170–171. doi: 10.1038/newbio235170a0. [DOI] [PubMed] [Google Scholar]
  21. Kohne D. E. Evolution of higher-organism DNA. Q Rev Biophys. 1970 Aug;3(3):327–375. doi: 10.1017/s0033583500004765. [DOI] [PubMed] [Google Scholar]
  22. LIEBERMAN M., KAPLAN H. S. Leukemogenic activity of filtrates from radiation-induced lymphoid tumors of mice. Science. 1959 Aug 14;130(3372):387–388. doi: 10.1126/science.130.3372.387. [DOI] [PubMed] [Google Scholar]
  23. Levy J. A. Xenotropic viruses: murine leukemia viruses associated with NIH Swiss, NZB, and other mouse strains. Science. 1973 Dec 14;182(4117):1151–1153. doi: 10.1126/science.182.4117.1151. [DOI] [PubMed] [Google Scholar]
  24. Lieber M. M., Benveniste R. E., Livingston D. M., Todaro G. J. Mammalian cells in culture frequently release type C viruses. Science. 1973 Oct 5;182(4107):56–59. doi: 10.1126/science.182.4107.56. [DOI] [PubMed] [Google Scholar]
  25. Lieber M. M., Sherr C. J., Todaro G. J., Benveniste R. E., Callahan R., Coon H. G. Isolation from the asian mouse Mus caroli of an endogenous type C virus related to infectious primate type C viruses. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2315–2319. doi: 10.1073/pnas.72.6.2315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lieber M. M., Sherr C. J., Todaro G. J. S-tropic murine type-C viruses: frequency of isolation from continuous cell lines, leukemia virus preparations and normal spleens. Int J Cancer. 1974 May 15;13(5):587–598. doi: 10.1002/ijc.2910130503. [DOI] [PubMed] [Google Scholar]
  27. Lieber M., Sherr C., Potter M., Todaro G. Isolation of type-C viruses from the Asian feral mouse Mus musculus molossinus. Int J Cancer. 1975 Feb 15;15(2):211–220. doi: 10.1002/ijc.2910150206. [DOI] [PubMed] [Google Scholar]
  28. McCarthy B. J., Farquhar M. N. The rate of change of DNA in evolution. Brookhaven Symp Biol. 1972;23:1–43. [PubMed] [Google Scholar]
  29. McConaughy B. L., McCarthy B. J. Related base sequences in the DNA of simple and complex organisms. VI. The extent of base sequence divergence among the DNAs of various rodents. Biochem Genet. 1970 Jun;4(3):425–446. doi: 10.1007/BF00485758. [DOI] [PubMed] [Google Scholar]
  30. Rasheed S., Gardner M. B., Chan E. Amphotropic host range of naturally occuring wild mouse leukemia viruses. J Virol. 1976 Jul;19(1):13–18. doi: 10.1128/jvi.19.1.13-18.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rice N. R. Change in repeated DNA in evolution. Brookhaven Symp Biol. 1972;23:44–79. [PubMed] [Google Scholar]
  32. Ringold G. M., Blair P. B., Bishop J. M., Varmus H. E. Nucleotide sequence homologies among mouse mammary tumor viruses. Virology. 1976 Apr;70(2):550–553. doi: 10.1016/0042-6822(76)90297-x. [DOI] [PubMed] [Google Scholar]
  33. Scolnic E. M., Goldberg R. J., Parks W. P. A biochemical and genetic analysis of mammalian RNA-containing sarcoma viruses. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 2):885–895. doi: 10.1101/sqb.1974.039.01.103. [DOI] [PubMed] [Google Scholar]
  34. Scolnick E. M., Parks W. P., Livingston D. M. Radioimmunoassay of mammalian type C viral proteins. I. Species specific reactions of murine and feline viruses. J Immunol. 1972 Sep;109(3):570–577. [PubMed] [Google Scholar]
  35. Scolnick E. M., Parks W., Kawakami T., Kohne D., Okabe H., Gilden R., Hatanaka M. Primate and murine type-C viral nucleic acid association kinetics: analysis of model systems and natural tissues. J Virol. 1974 Feb;13(2):363–369. doi: 10.1128/jvi.13.2.363-369.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sherr C. J., Benveniste R. E., Lieber M. M., Todaro G. J. Type C viruses from Kirsten sarcoma-transformed mink cells co-cultivated with primate cells and expressing p30 antigens related to feline leukemia virus. J Virol. 1976 Aug;19(2):346–358. doi: 10.1128/jvi.19.2.346-358.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sherr C. J., Fedele L. A., Benveniste R. E., Todaro G. J. Interspecies antigenic determinants of the reverse transcriptases and p30 proteins of mammalian type C viruses. J Virol. 1975 Jun;15(6):1440–1448. doi: 10.1128/jvi.15.6.1440-1448.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sherr C. J., Todaro G. J. Radioimmunoassay of the major group specific protein of endogenous baboon type C viruses: relation to the RD-114-CCC group and detection of antigen in normal baboon tissues. Virology. 1974 Sep;61(1):168–181. doi: 10.1016/0042-6822(74)90252-9. [DOI] [PubMed] [Google Scholar]
  39. Theilen G. H., Gould D., Fowler M., Dungworth D. L. C-type virus in tumor tissue of a woolly monkey (Lagothrix spp.) with fibrosarcoma. J Natl Cancer Inst. 1971 Oct;47(4):881–889. [PubMed] [Google Scholar]
  40. Todaro G. J., Arnstein P., Parks W. P., Lennette E. H., Huebner R. J. A type-C virus in human rhabdomyosarcoma cells after inoculation into NIH Swiss mice treated with antithymocyte serum. Proc Natl Acad Sci U S A. 1973 Mar;70(3):859–862. doi: 10.1073/pnas.70.3.859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Todaro G. J., Benveniste R. E., Callahan R., Lieber M. M., Sherr C. J. Endogenous primate and feline type C viruses. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 2):1159–1168. doi: 10.1101/sqb.1974.039.01.133. [DOI] [PubMed] [Google Scholar]
  42. Todaro G. J., Lieber M. M., Benveniste R. E., Sherr C. J. Infectious primate type C viruses: Three isolates belonging to a new subgroup from the brains of normal gibbons. Virology. 1975 Oct;67(2):335–343. doi: 10.1016/0042-6822(75)90435-3. [DOI] [PubMed] [Google Scholar]
  43. Todaro G. J., Sherr C. J., Benveniste R. E., Lieber M. M., Melnick J. L. Type C viruses of baboons: isolation from normal cell cultures. Cell. 1974 May;2(1):55–61. doi: 10.1016/0092-8674(74)90008-7. [DOI] [PubMed] [Google Scholar]
  44. Todaro G. J. Spontaneous release of type C viruses from clonal lines of spontaneously transformed Blab-3T3 cells. Nat New Biol. 1972 Nov 29;240(100):157–160. doi: 10.1038/newbio240157a0. [DOI] [PubMed] [Google Scholar]
  45. Wolfe L. G., Deinhardt F., Theilen G. H., Rabin H., Kawakami T., Bustad L. K. Induction of tumors in marmoset monkeys by simian sarcoma virus, type 1 (Lagothrix): a preliminary report. J Natl Cancer Inst. 1971 Nov;47(5):1115–1120. [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES