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
. 1974 Jan;71(1):167–171. doi: 10.1073/pnas.71.1.167

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

Sisir K Chattopadhyay *, Douglas R Lowy *,*, Natalie M Teich *, Arthur S Levine †, Wallace P Rowe *
PMCID: PMC387958  PMID: 4359326

Abstract

The AKR mouse has a high titer of murine leukemia virus early in life, and virus-negative cells derived from embryos of this mouse strain can be activated to yield murine leukemia virus by treatment with 5-iododeoxyuridine. In contrast to this high-virus strain, the NIH Swiss mouse has a low incidence of leukemia and no murine leukemia virus has been isolated from it (virus-negative). We have investigated this difference between AKR and NIH mice by examining the sequences specific for murine leukemia virus in nucleic acids of these mice. A single-stranded viral-DNA probe synthesized in vitro using murine-leukemia-virus from the AKR mouse contains at least 87% of the sequences present in the 70S viral RNA; most of these sequences are in proportions similar to their content in the 70S RNA. Using this probe in nucleic acid hybridization experiments, we have shown that NIH-mouse-cell DNA and AKR-mouse-cell DNA differ with respect to sequences specific for AKR murine-leukemia-virus: NIH-mouse-cell DNA lacks some of the virus-specific sequences present in AKR-mouse-cell DNA, and there are two distinct sets of virus-specific sequences in AKR-mouse-cell DNA, whereas there is only one set in NIH-mouse-cell DNA.

RNA from virus-negative AKR-mouse cells grown in tissue culture contains some, but not all, virus-specific RNA sequences; however, within 48 hr after initiating treatment of these cells with 5-iododeoxyuridine, the complete viral genome is represented in cellular RNA.

Keywords: mouse leukemia virus, AKR and NIH mouse DNA and RNA, IdU activation, reassociation kinetics

Full text

PDF
167

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. 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]
  2. 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]
  3. Baluda M. A. Widespread presence, in chickens, of DNA complementary to the RNA genome of avian leukosis viruses. Proc Natl Acad Sci U S A. 1972 Mar;69(3):576–580. doi: 10.1073/pnas.69.3.576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Benveniste R. E., Todaro G. J., Scolnick E. M., Parks W. P. Partial transcription of murine type C viral genomes in BALB c cell lines. J Virol. 1973 Oct;12(4):711–720. doi: 10.1128/jvi.12.4.711-720.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Garapin A. C., Varmus H. E., Faras A. J., Levinson W. E., Bishop J. M. RNA-directed DNA synthesis by virions of Rous sarcoma virus: further characterization of the templates and the extent of their transcription. Virology. 1973 Mar;52(1):264–274. doi: 10.1016/0042-6822(73)90414-5. [DOI] [PubMed] [Google Scholar]
  8. Gelb L. D., Aaronson S. A., Martin M. A. Heterogeneity of murine leukemia virus in vitro DNA; detection of viral DNA in mammalian cells. Science. 1971 Jun 25;172(3990):1353–1355. doi: 10.1126/science.172.3990.1353. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Hartley J. W., Rowe W. P., Capps W. I., Huebner R. J. Complement fixation and tissue culture assays for mouse leukemia viruses. Proc Natl Acad Sci U S A. 1965 May;53(5):931–938. doi: 10.1073/pnas.53.5.931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kohne D. E. Isolation and characterization of bacterial ribosomal RNA cistrons. Biophys J. 1968 Oct;8(10):1104–1118. doi: 10.1016/S0006-3495(68)86542-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Levin M. J., Oxman M. N., Diamandopoulos G. T., Levine A. S., Henry P. H., Enders J. F. Virus-specific nucleic acids in SV40-exposed hamster embryo cell lines: correlation with S and T antigens. Proc Natl Acad Sci U S A. 1969 Feb;62(2):589–596. doi: 10.1073/pnas.62.2.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Neiman P. E. Measurement of endogenous leukosis virus nucleotide sequences in the DNA of normal avian embryos by RNA-DNA hybridization. Virology. 1973 May;53(1):196–203. doi: 10.1016/0042-6822(73)90478-9. [DOI] [PubMed] [Google Scholar]
  15. Robinson W. S., Pitkanen A., Rubin H. The nucleic acid of the Bryan strain of Rous sarcoma virus: purification of the virus and isolation of the nucleic acid. Proc Natl Acad Sci U S A. 1965 Jul;54(1):137–144. doi: 10.1073/pnas.54.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Rowe W. P., Hartley J. W., Lander M. R., Pugh W. E., Teich N. Noninfectious AKR mouse embryo cell lines in which each cell has the capacity to be activated to produce infectious murine leukemia virus. Virology. 1971 Dec;46(3):866–876. doi: 10.1016/0042-6822(71)90087-0. [DOI] [PubMed] [Google Scholar]
  17. Rowe W. P., Hartley J. W. Studies of genetic transmission of murine leukemia virus by AKR mice. II. Crosses with Fv-1 b strains of mice. J Exp Med. 1972 Nov 1;136(5):1286–1301. doi: 10.1084/jem.136.5.1286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rowe W. P., Pincus T. Quantitative studies of naturally occurring murine leukemia virus infection of AKR mice. J Exp Med. 1972 Feb 1;135(2):429–436. doi: 10.1084/jem.135.2.429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Sutton W. D. A crude nuclease preparation suitable for use in DNA reassociation experiments. Biochim Biophys Acta. 1971 Jul 29;240(4):522–531. doi: 10.1016/0005-2787(71)90709-x. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Varmus H. E., Bishop J. M., Vogt P. K. Appearance of virus-specific DNA in mammalian cells following transformation by Rous sarcoma virus. J Mol Biol. 1973 Mar 15;74(4):613–626. doi: 10.1016/0022-2836(73)90052-1. [DOI] [PubMed] [Google Scholar]
  23. Varmus H. E., Weiss R. A., Friis R. R., Levinson W., Bishop J. M. Detection of avian tumor virus-specific nucleotide sequences in avian cell DNAs (reassociation kinetics-RNA tumor viruses-gas antigen-Rous sarcoma virus, chick cells). Proc Natl Acad Sci U S A. 1972 Jan;69(1):20–24. doi: 10.1073/pnas.69.1.20. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wetmur J. G., Davidson N. Kinetics of renaturation of DNA. J Mol Biol. 1968 Feb 14;31(3):349–370. doi: 10.1016/0022-2836(68)90414-2. [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