Skip to main content
PMC 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
. 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.

Full text

PDF

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]

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