Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1983 Oct;48(1):102–109. doi: 10.1128/jvi.48.1.102-109.1983

Evidence for a new form of retroviral env transcript in leukemic and normal mouse lymphoid cells.

M Boccara, M Souyri, C Magarian, E Stavnezer, E Fleissner
PMCID: PMC255326  PMID: 6193284

Abstract

Murine leukemia virus-related RNA species were examined in a set of radiation-induced T-cell leukemias from BALB/c mice. No evidence was found for linkage of viral long terminal repeat-derived (U5) sequences to information of host origin. A novel class of 2-kilobase (kb) env-related transcripts, about 1kb shorter than normal viral env messenger, was found in all the leukemias. All of the 2-kb transcripts contained sequences homologous to the xenotropic virus-related env sequences in the Friend spleen focus-forming virus, representing the N-terminal portion of gp70. In two of the leukemias, these transcripts were found to contain both ecotropic p15E and U3 sequences in addition to the xenotropic gp70-related sequence. These two leukemias, but not others in which ecotropic sequences were absent from the 2-kb RNA, harbored several copies of a specific class of env recombinant proviruses. These proviruses possessed full-size env genes and were submethylated, as shown by SmaI and XmaI digests of proviral DNA. Low levels of 2-kb RNA were found in normal thymocytes from strains BALB/c, AKR, and 129 but not from congenic 129 GIX- mice. It is possible that the 2-kb RNA may originate by a novel splicing step that removes portions of the gp70 and p15E sequences from full-length env transcripts.

Full text

PDF
102

Images in this article

103Image
on p.103
104Image
on p.104
104Image
on p.104
105Image
on p.105
106Image
on p.106
107Image
on p.107
107Image
on p.107

Selected References

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

  1. Chattopadhyay S. K., Cloyd M. W., Linemeyer D. L., Lander M. R., Rands E., Lowy D. R. Cellular origin and role of mink cell focus-forming viruses in murine thymic lymphomas. Nature. 1982 Jan 7;295(5844):25–31. doi: 10.1038/295025a0. [DOI] [PubMed] [Google Scholar]
  2. Ellis R. W., Hopkins N., Fleissner E. Biochemical analysis of murine leukemia viruses isolated from radiation-induced leukemias of strain BALB/c. J Virol. 1980 Feb;33(2):661–670. doi: 10.1128/jvi.33.2.661-670.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ellis R. W., Stockert E., Fleissner E. Association of endogenous retroviruses with radiation-induced leukemias of BALB/c mice. J Virol. 1980 Feb;33(2):652–660. doi: 10.1128/jvi.33.2.652-660.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Famulari N. G. Murine leukemia viruses with recombinant env genes: a discussion of their role in leukemogenesis. Curr Top Microbiol Immunol. 1983;103:75–108. doi: 10.1007/978-3-642-68943-7_4. [DOI] [PubMed] [Google Scholar]
  5. Fischinger P. J., Thiel H. J., Ihle J. N., Lee J. C., Elder J. H. Detection of a recombinant murine leukemia virus-related glycoprotein on virus-negative thymoma cells. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1920–1924. doi: 10.1073/pnas.78.3.1920. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fleissner E., Snyder H. W., Jr Oncoviral proteins as cellular antigens. Curr Top Microbiol Immunol. 1982;98:37–80. doi: 10.1007/978-3-642-68369-5_5. [DOI] [PubMed] [Google Scholar]
  7. Gross-Bellard M., Oudet P., Chambon P. Isolation of high-molecular-weight DNA from mammalian cells. Eur J Biochem. 1973 Jul 2;36(1):32–38. doi: 10.1111/j.1432-1033.1973.tb02881.x. [DOI] [PubMed] [Google Scholar]
  8. Hartley J. W., Wolford N. K., Old L. J., Rowe W. P. A new class of murine leukemia virus associated with development of spontaneous lymphomas. Proc Natl Acad Sci U S A. 1977 Feb;74(2):789–792. doi: 10.1073/pnas.74.2.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hayward W. S., Neel B. G., Astrin S. M. Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature. 1981 Apr 9;290(5806):475–480. doi: 10.1038/290475a0. [DOI] [PubMed] [Google Scholar]
  10. Herr W., Gilbert W. Somatically acquired recombinant murine leukemia proviruses in thymic leukemias of AKR/J mice. J Virol. 1983 Apr;46(1):70–82. doi: 10.1128/jvi.46.1.70-82.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hoffmann J. W., Steffen D., Gusella J., Tabin C., Bird S., Cowing D., Weinberg R. A. DNA methylation affecting the expression of murine leukemia proviruses. J Virol. 1982 Oct;44(1):144–157. doi: 10.1128/jvi.44.1.144-157.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kelly M., Holland C. A., Lung M. L., Chattopadhyay S. K., Lowy D. R., Hopkins N. H. Nucleotide sequence of the 3' end of MCF 247 murine leukemia virus. J Virol. 1983 Jan;45(1):291–298. doi: 10.1128/jvi.45.1.291-298.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kirschmeier P., Gattoni-Celli S., Dina D., Weinstein I. B. Carcinogen- and radiation-transformed C3H 10T1/2 cells contain RNAs homologous to the long terminal repeat sequence of a murine leukemia virus. Proc Natl Acad Sci U S A. 1982 May;79(9):2773–2777. doi: 10.1073/pnas.79.9.2773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Levy D. E., Lerner R. A., Wilson M. C. A genetic locus regulates the expression of tissue-specific mRNAs from multiple transcription units. Proc Natl Acad Sci U S A. 1982 Oct;79(19):5823–5827. doi: 10.1073/pnas.79.19.5823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Linemeyer D. L., Menke J. G., Ruscetti S. K., Evans L. H., Scolnick E. M. Envelope gene sequences which encode the gp52 protein of spleen focus-forming virus are required for the induction of erythroid cell proliferation. J Virol. 1982 Jul;43(1):223–233. doi: 10.1128/jvi.43.1.223-233.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lung M. L., Hartley J. W., Rowe W. P., Hopkins N. H. Large RNase T1-resistant oligonucleotides encoding p15E and the U3 region of the long terminal repeat distinguish two biological classes of mink cell focus-forming type C viruses of inbred mice. J Virol. 1983 Jan;45(1):275–290. doi: 10.1128/jvi.45.1.275-290.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. McMaster G. K., Carmichael G. G. Analysis of single- and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4835–4838. doi: 10.1073/pnas.74.11.4835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Montandon P. E., Montandon F., Fan H. Methylation state and DNase I sensitivity of chromatin containing Moloney murine leukemia virus DNA in exogenously infected mouse cells. J Virol. 1982 Nov;44(2):475–486. doi: 10.1128/jvi.44.2.475-486.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Neel B. G., Hayward W. S., Robinson H. L., Fang J., Astrin S. M. Avian leukosis virus-induced tumors have common proviral integration sites and synthesize discrete new RNAs: oncogenesis by promoter insertion. Cell. 1981 Feb;23(2):323–334. doi: 10.1016/0092-8674(81)90128-8. [DOI] [PubMed] [Google Scholar]
  20. Old L. J., Stockert E. Immunogenetics of cell surface antigens of mouse leukemia. Annu Rev Genet. 1977;11:127–160. doi: 10.1146/annurev.ge.11.120177.001015. [DOI] [PubMed] [Google Scholar]
  21. Payne G. S., Bishop J. M., Varmus H. E. Multiple arrangements of viral DNA and an activated host oncogene in bursal lymphomas. Nature. 1982 Jan 21;295(5846):209–214. doi: 10.1038/295209a0. [DOI] [PubMed] [Google Scholar]
  22. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  23. Roblin R., Young J. M., Mural R. J., Bell T. E., Ihle J. N. Molecular cloning and characterization of murine leukemia virus-related DNA sequences from C3H/HeN mouse DNA. J Virol. 1982 Jul;43(1):113–126. doi: 10.1128/jvi.43.1.113-126.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Saule S., Roussel M., Lagrou C., Stehelin D. Characterization of the oncogene (erb) of avian erythroblastosis virus and its cellular progenitor. J Virol. 1981 May;38(2):409–419. doi: 10.1128/jvi.38.2.409-419.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Seed B. Diazotizable arylamine cellulose papers for the coupling and hybridization of nucleic acids. Nucleic Acids Res. 1982 Mar 11;10(5):1799–1810. doi: 10.1093/nar/10.5.1799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  27. Steffen D. L., Mural R., Cowing D., Mielcarz J., Young J., Roblin R. Most of the murine leukemia virus sequences in the DNA of NIH/swiss mice consist of two closely related proviruses, each repeated several times. J Virol. 1982 Jul;43(1):127–135. doi: 10.1128/jvi.43.1.127-135.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Stockert E., Boyse E. A., Obata Y., Ikeda H., Sarkar N. H., Hoffman H. A. New mutant and congenic mouse stocks expressing the murine leukemia virus-associated thymocyte surface antigen GIX. J Exp Med. 1975 Aug 1;142(2):512–517. doi: 10.1084/jem.142.2.512. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Stockert E., Old L. J., Boyse E. A. The G-IX system. A cell surface allo-antigen associated with murine leukemia virus; implications regarding chromosomal integration of the viral genome. J Exp Med. 1971 Jun 1;133(6):1334–1355. doi: 10.1084/jem.133.6.1334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tress E., Pierotti M., DeLeo A. B., O'Donnell P. V., Fleissner E. Endogenous murine leukemia virus-encoded proteins in radiation leukemias of BALB/c mice. Virology. 1982 Feb;117(1):207–218. doi: 10.1016/0042-6822(82)90520-7. [DOI] [PubMed] [Google Scholar]
  31. Troxler D. H., Yuan E., Linemeyer D., Ruscetti S., Scolnick E. M. Helper-independent mink cell focus-inducing strains of Friend murine type-C virus: potential relationship to the origin of replication-defective spleen focus-forming virus. J Exp Med. 1978 Sep 1;148(3):639–653. doi: 10.1084/jem.148.3.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tung J. S., Shen F. W., Viamontes G., Palladino M., Fleissner E. The same genetic locus directs differentiation-linked expression of endogenous retrovirus gp70 on thymocytes and spleen cells in the mouse. Immunogenetics. 1982 Jan;15(1):103–108. doi: 10.1007/BF00375507. [DOI] [PubMed] [Google Scholar]

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

RESOURCES