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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
. 1977 Jul;74(7):2953–2957. doi: 10.1073/pnas.74.7.2953

Segregation of genetic information for a B-tropic leukemia virus with the structural locus for BALB:virus-1.

K C Robbins, C D Cabradilla, J R Stephenson, S A Aaronson
PMCID: PMC431361  PMID: 197526

Abstract

A B-tropic type-C RNA virus isolatable from lymphoreticular tumors of the inbred BALB/c mouse strain has previously been shown to be leukemogenic in its natural host. This virus is not chemically inducible from BALB/c embryo cells or from embryo lines containing segregating inducibility loci for two known endogenous type-C viruses of BALB/c cells. Molecular hybridization and type-specific immunologic assays demonstrate a high degree of genetic homology between the B-tropic leukemia virus and BALB:virus-1, an N-tropic endogenous virus of BALB/c cells. Genetic sequences specific for BALB:virus-1 are shown to segregate with the locus for BALB:virus-1 induction in genetic crosses between BALB/c and the noninducible NIH Swiss strain. Thus, if the information of the B-tropic virus is encoded in the genome of the animal, it must be closely linked to the structural locus for BALB:virus-1. The evidence is consistent with a mechanism by which a small genetic alteration in BALB:virus-1 leads to a virus, whose growth is unrestricted, and subsequently to the development of neoplasia.

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Selected References

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

  1. Aaronson S. A., Stephenson J. R. Endogenous type-C RNA viruses of mammalian cells. Biochim Biophys Acta. 1976 Dec 23;458(4):323–354. doi: 10.1016/0304-419x(76)90006-8. [DOI] [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. Aaronson S. A., Todaro G. J. Development of 3T3-like lines from Balb-c mouse embryo cultures: transformation susceptibility to SV40. J Cell Physiol. 1968 Oct;72(2):141–148. doi: 10.1002/jcp.1040720208. [DOI] [PubMed] [Google Scholar]
  4. Aaronson S. A., Todaro G. J., Scolnick E. M. Induction of murine C-type viruses from clonal lines of virus-free BALB-3T3 cells. Science. 1971 Oct 8;174(4005):157–159. doi: 10.1126/science.174.4005.157. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Buchhagen D. L., Stutman O., Fleissner E. Chromatographic Separation and Antigenic Analysis of Proteins of the Oncornaviruses IV. Biochemical Typing of Murine Viral Proteins. J Virol. 1975 May;15(5):1148–1157. doi: 10.1128/jvi.15.5.1148-1157.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cabradilla C. D., Robbins K. C., Aaronson S. A. Induction of mouse type-C virus by translational inhibitors: evidence for transcriptional derepression of a specific class of endogenous virus. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4541–4545. doi: 10.1073/pnas.73.12.4541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Callahan R., Benveniste R. E., Lieber M. M., Todaro G. J. Nucleic acid homology of murine type-C viral genes. J Virol. 1974 Dec;14(6):1394–1403. doi: 10.1128/jvi.14.6.1394-1403.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chattopadhyay S. K., Lowy D. R., Teich N. M., Levine A. S., Rowe W. P. Evidence that the AKR murine-leukemia-virus genome is complete in DNA of the high-virus AKR mouse and incomplete in the DNA of the "virus-negative" NIH mouse. Proc Natl Acad Sci U S A. 1974 Jan;71(1):167–171. doi: 10.1073/pnas.71.1.167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chattopadhyay S. K., Rowe W. P., Teich N. M., Lowy D. R. Definitive evidence that the murine C-type virus inducing locus Akv-1 is viral genetic material. Proc Natl Acad Sci U S A. 1975 Mar;72(3):906–910. doi: 10.1073/pnas.72.3.906. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Duesberg P. H., Canaani E. Complementarity between Rous sarcoma virus (RSV) RNA and the in vitro-synthesized DNA of the virus-associated DNA polymerase. Virology. 1970 Nov;42(3):783–788. doi: 10.1016/0042-6822(70)90325-9. [DOI] [PubMed] [Google Scholar]
  12. GREENWOOD F. C., HUNTER W. M., GLOVER J. S. THE PREPARATION OF I-131-LABELLED HUMAN GROWTH HORMONE OF HIGH SPECIFIC RADIOACTIVITY. Biochem J. 1963 Oct;89:114–123. doi: 10.1042/bj0890114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gelb L. D., Milstien J. B., Martin M. A., Aaronson S. A. Characterization of murine leukaemia virus-specific DNA present in normal mouse cells. Nat New Biol. 1973 Jul 18;244(133):76–79. doi: 10.1038/newbio244076a0. [DOI] [PubMed] [Google Scholar]
  14. Greenberger J. S., Stephenson J. R., Moloney W. C., Aaronson S. A. Different hematological diseases induced by type C viruses chemically activated from embryo cells of different mouse strains. Cancer Res. 1975 Jan;35(1):245–252. [PubMed] [Google Scholar]
  15. Hartley J. W., Rowe W. P., Capps W. I., Huebner R. J. Isolation of naturally occurring viruses of the murine leukemia virus group in tissue culture. J Virol. 1969 Feb;3(2):126–132. doi: 10.1128/jvi.3.2.126-132.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hartley J. W., Rowe W. P. Clonal cells lines from a feral mouse embryo which lack host-range restrictions for murine leukemia viruses. Virology. 1975 May;65(1):128–134. doi: 10.1016/0042-6822(75)90013-6. [DOI] [PubMed] [Google Scholar]
  17. Hartley J. W., Rowe W. P., Huebner R. J. Host-range restrictions of murine leukemia viruses in mouse embryo cell cultures. J Virol. 1970 Feb;5(2):221–225. doi: 10.1128/jvi.5.2.221-225.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hino S., Stephenson J. R., Aaronson S. A. Radiommunoassays for the 70,000-molecular-weight glycoproteins of endogenous mouse type C viruses: viral antigen expression in normal mouse tissues and sera. J Virol. 1976 Jun;18(3):933–941. doi: 10.1128/jvi.18.3.933-941.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hopkins N., Traktman P., Whalen K. N-Tropic variants obtained after co-infection with N- and B-tropic murine leukemia viruses. J Virol. 1976 Apr;18(1):324–331. doi: 10.1128/jvi.18.1.324-331.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Huang A. S., Besmer P., Chu L., Baltimore D. Growth of pseudotypes of vesicular stomatitis virus with N-tropic murine leukemia virus coats in cells resistant to N-tropic viruses. J Virol. 1973 Sep;12(3):659–662. doi: 10.1128/jvi.12.3.659-662.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jainchill J. L., Aaronson S. A., Todaro G. J. Murine sarcoma and leukemia viruses: assay using clonal lines of contact-inhibited mouse cells. J Virol. 1969 Nov;4(5):549–553. doi: 10.1128/jvi.4.5.549-553.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Jolicoeur P., Baltimore D. Effect of Fv-1 gene product on proviral DNA formation and integration in cells infected with murine leukemia viruses. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2236–2240. doi: 10.1073/pnas.73.7.2236. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Klement V., Rowe W. P., Hartley J. W., Pugh W. E. Mixed culture cytopathogenicity: a new test for growth of murine leukemia viruses in tissue culture. Proc Natl Acad Sci U S A. 1969 Jul;63(3):753–758. doi: 10.1073/pnas.63.3.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Krontiris T. G., Soeiro R., Fields B. N. Host restriction of Friend leukemia virus. Role of the viral outer coat. Proc Natl Acad Sci U S A. 1973 Sep;70(9):2549–2553. doi: 10.1073/pnas.70.9.2549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Leong J. A., Garapin A. C., Jackson N., Fanshier L., Levinson W., Bishop J. M. Virus-specific ribonucleic acid in cells producing rous sarcoma virus: detection and characterization. J Virol. 1972 Jun;9(6):891–902. doi: 10.1128/jvi.9.6.891-902.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Lilly F., Duran-Reynals M. L., Rowe W. P. Correlation of early murine leukemia virus titer and H-2 type with spontaneous leukemia in mice of the BALB/c times AKR cross: a genetic analysis. J Exp Med. 1975 Apr 1;141(4):882–889. [PMC free article] [PubMed] [Google Scholar]
  28. Lowy D. R., Rowe W. P., Teich N., Hartley J. W. Murine leukemia virus: high-frequency activation in vitro by 5-iododeoxyuridine and 5-bromodeoxyuridine. Science. 1971 Oct 8;174(4005):155–156. doi: 10.1126/science.174.4005.155. [DOI] [PubMed] [Google Scholar]
  29. Madison R. M., Rabstein L. S., Bryan W. R. Mortality rate and spontaneous lesions found in 2,928 untreated BALB/cCr mice. J Natl Cancer Inst. 1968 Apr;40(4):683–685. [PubMed] [Google Scholar]
  30. Peters R. L., Hartley J. W., Spahn G. J., Rabstein L. S., Whitmire C. E., Turner H. C., Huebner R. J. Prevalence of the group-specific (gs) antigen and infectious virus expressions of the murine C-type RNA viruses during the life span of BALB-cCr mice. Int J Cancer. 1972 Sep 15;10(2):283–289. doi: 10.1002/ijc.2910100208. [DOI] [PubMed] [Google Scholar]
  31. Peters R. L., Spahn G. J., Rabstein L. S., Kelloff G. J., Huebner R. J. Murine C-type RNA virus from spontaneous neoplasms: in vitro host range and oncogenic potential. Science. 1973 Aug 17;181(4100):665–667. doi: 10.1126/science.181.4100.665. [DOI] [PubMed] [Google Scholar]
  32. Pincus T., Hartley J. W., Rowe W. P. A major genetic locus affecting resistance to infection with murine leukemia viruses. I. Tissue culture studies of naturally occurring viruses. J Exp Med. 1971 Jun 1;133(6):1219–1233. doi: 10.1084/jem.133.6.1219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rowe W. P., Hartley J. W., Bremner T. Genetic mapping of a murine leukemia virus-inducing locus of AKR mice. Science. 1972 Nov 24;178(4063):860–862. doi: 10.1126/science.178.4063.860. [DOI] [PubMed] [Google Scholar]
  34. Rowe W. P. Studies of genetic transmission of murine leukemia virus by AKR mice. I. Crosses with Fv-1 n strains of mice. J Exp Med. 1972 Nov 1;136(5):1272–1285. doi: 10.1084/jem.136.5.1272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Stephension J. R., Reynolds R. K., Tronick S. R., Aaronson S. A. Distribution of three classes of endogenous type-C RNA viruses among inbred strains of mice. Virology. 1975 Oct;67(2):404–414. doi: 10.1016/0042-6822(75)90442-0. [DOI] [PubMed] [Google Scholar]
  36. Stephenson J. R., Aaronson S. A., Arnstein P., Huebner R. J., Tronick S. R. Demonstration of two immunologically distinct xenotropic type C RNA viruses of mouse cells. Virology. 1974 Sep;61(1):56–63. doi: 10.1016/0042-6822(74)90241-4. [DOI] [PubMed] [Google Scholar]
  37. Stephenson J. R., Aaronson S. A. Segregation of loci for C-type virus induction in strains of mice with high and low incidence of leukemia. Science. 1973 May 25;180(4088):865–866. doi: 10.1126/science.180.4088.865. [DOI] [PubMed] [Google Scholar]
  38. Taylor B. A., Meier H., Myers D. D. Host-gene control of C-type RNA tumor virus: inheritance of the group-specific antigen of murine leukemia virus. Proc Natl Acad Sci U S A. 1971 Dec;68(12):3190–3194. doi: 10.1073/pnas.68.12.3190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]

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