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. 1981 Sep;39(3):777–791. doi: 10.1128/jvi.39.3.777-791.1981

Genomes of murine leukemia viruses isolated from wild mice.

S K Chattopadhyay, A I Oliff, D L Linemeyer, M R Lander, D R Lowy
PMCID: PMC171310  PMID: 6270351

Abstract

The genomes of murine leukemia viruses (MuLV) isolated from wild mice have been studied. Detailed restriction endonuclease maps of the 8.8-kilobase (kb) unintegrated linear viral DNAs were derived for five ecotropic and five amphotropic MuLV's from California field mice, for Friend MuLV, and for one ecotropic and one xenotropic MuLV from Mus musculus castaneus. In general, the California MuLV's were similar in their leftward 6 kb (corresponding to the leftward long terminal repeat [LTR], gag, and pol) and rightward 1 kb (7.8 to 8.8 kb, corresponding to p15E and the rightward LTR). For the region spanning 6.0 to 7.7 kb (which includes the sequences that encode gp70) the amphotropic MuLV's shared few enzyme sites with the ecotropic MuLV's, although the California ecotropic MuLV's were highly related to each other in this region, as were the amphotropic MuLV's. Cross-hybridization studies between amphotropic and California ecotropic MuLV DNAs indicated that they were not homologous in the region 6.3 to 7.6 kb; the California ecotropic viral DNAs cross-hybridized in this region to AKR ecotropic MuLV. When the California viral DNAs were compared with AKR ecotropic viral DNA, many differences in enzyme sites were noted throughout the genome. The U3 regions of the wild mouse LTRs showed partial homology to this region in AKR MuLV. The LTR of Moloney MuLV was highly related to that of the California MuLV's, whereas the LTR of Friend MuLV appeared to be a recombinant between the two types of LTRs. The M. musculus castaneus isolates were most closely related to ecotropic and xenotropic MuLV's isolated from inbred mice. One amphotropic MuLV DNA was cloned from supercoiled viral DNA at its unique EcoRI site in pBR322. Viral DNAs with one and two LTRs were isolated. After digestion with EcoRI, DNAs of both types were infectious. It is concluded that ecotropic and amphotropic MuLV's differ primarily in the region which encodes gp70.

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  1. Barbacid M., Robbins K. C., Aaronson S. A. Wild mouse RNA tumor viruses. A nongenetically transmitted virus group closely related to exogenous leukemia viruses of laboratory mouse strains. J Exp Med. 1979 Jan 1;149(1):254–266. doi: 10.1084/jem.149.1.254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barbacid M., Stephenson J. R., Aaronson S. A. gag Gene of mammalian type-C RNA tumour viruses. Nature. 1976 Aug 12;262(5569):554–559. doi: 10.1038/262554a0. [DOI] [PubMed] [Google Scholar]
  3. Berns A. J., Lai M. H., Bosselman R. A., McKennett M. A., Bacheler L. T., Fan H., Maandag E. C., van der Putten H. V., Verma I. M. Molecular cloning of unintegrated and a portion of integrated moloney murine leukemia viral DNA in bacteriophage lambda. J Virol. 1980 Oct;36(1):254–263. doi: 10.1128/jvi.36.1.254-263.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bryant M. L., Pal B. K., Gardner M. B., Elder J. H., Jensen F. C., Lerner R. A. Structural analysis of the major envelope glycoprotein (gp70) of the amphotropic and ecotropic type C viruses of wild mice. Virology. 1978 Feb;84(2):348–358. doi: 10.1016/0042-6822(78)90254-4. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Chattopadhyay S. K., Hartley J. W., Lander M. R., Kramer B. S., Rowe W. P. Biochemical characterization of the amphotropic group of murine leukemia viruses. J Virol. 1978 Apr;26(1):29–39. doi: 10.1128/jvi.26.1.29-39.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chattopadhyay S. K., Lander M. R., Rands E., Lowy D. R. Structure of endogenous murine leukemia virus DNA in mouse genomes. Proc Natl Acad Sci U S A. 1980 Oct;77(10):5774–5778. doi: 10.1073/pnas.77.10.5774. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chattopadhyay S. K., Lander M. R., Rowe W. P. Close similarity between endogenous ecotropic virus of Mus musculus molossinus and AKR virus. J Virol. 1980 Nov;36(2):499–505. doi: 10.1128/jvi.36.2.499-505.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Clewell D. B. Nature of Col E 1 plasmid replication in Escherichia coli in the presence of the chloramphenicol. J Bacteriol. 1972 May;110(2):667–676. doi: 10.1128/jb.110.2.667-676.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cohen S. N., Chang A. C., Hsu L. Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA. Proc Natl Acad Sci U S A. 1972 Aug;69(8):2110–2114. doi: 10.1073/pnas.69.8.2110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dhar R., McClements W. L., Enquist L. W., Vande Woude G. F. Nucleotide sequences of integrated Moloney sarcoma provirus long terminal repeats and their host and viral junctions. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3937–3941. doi: 10.1073/pnas.77.7.3937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Donoghue D. J., Rothenberg E., Hopkins N., Baltimore D., Sharp P. A. Heteroduplex analysis of the nonhomology region between Moloney MuLV and the dual host range derivative HIX virus. Cell. 1978 Aug;14(4):959–970. doi: 10.1016/0092-8674(78)90350-1. [DOI] [PubMed] [Google Scholar]
  13. Elder J. H., Jensen F. C., Bryant M. L., Lerner R. A. Polymorphism of the major envelope glycoprotein (gp70) of murine C-type viruses: virion associated and differentiation antigens encoded by a multi-gene family. Nature. 1977 May 5;267(5606):23–28. doi: 10.1038/267023a0. [DOI] [PubMed] [Google Scholar]
  14. FRIEND C. Cell-free transmission in adult Swiss mice of a disease having the character of a leukemia. J Exp Med. 1957 Apr 1;105(4):307–318. doi: 10.1084/jem.105.4.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gardner M. B. Type C viruses of wild mice: characterization and natural history of amphotropic, ecotropic, and xenotropic MuLv. Curr Top Microbiol Immunol. 1978;79:215–259. doi: 10.1007/978-3-642-66853-1_5. [DOI] [PubMed] [Google Scholar]
  16. Gilboa E., Goff S., Shields A., Yoshimura F., Mitra S., Baltimore D. In vitro synthesis of a 9 kbp terminally redundant DNA carrying the infectivity of Moloney murine leukemia virus. Cell. 1979 Apr;16(4):863–874. doi: 10.1016/0092-8674(79)90101-6. [DOI] [PubMed] [Google Scholar]
  17. Graham F. L., van der Eb A. J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973 Apr;52(2):456–467. doi: 10.1016/0042-6822(73)90341-3. [DOI] [PubMed] [Google Scholar]
  18. Green N., Hiai H., Elder J. H., Schwartz R. S., Khiroya R. H., Thomas C. Y., Tsichlis P. N., Coffin J. M. Expression of leukemogenic recombinant viruses associated with a recessive gene in HRS/J mice. J Exp Med. 1980 Aug 1;152(2):249–264. doi: 10.1084/jem.152.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hager G. L., Chang E. H., Chan H. W., Garon C. F., Israel M. A., Martin M. A., Scolnick E. M., Lowy D. R. Molecular cloning of the Harvey sarcoma virus closed circular DNA intermediates: initial structural and biological characterization. J Virol. 1979 Sep;31(3):795–809. doi: 10.1128/jvi.31.3.795-809.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Highfield P. E., Rafield L. F., Gilmer T. M., Parsons J. T. Molecular cloning of avian sarcoma virus closed circular DNA: structural and biological characterization of three recombinant clones. J Virol. 1980 Oct;36(1):271–279. doi: 10.1128/jvi.36.1.271-279.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol. 1967 Jun 14;26(2):365–369. doi: 10.1016/0022-2836(67)90307-5. [DOI] [PubMed] [Google Scholar]
  24. Jamjoom G. A., Naso R. B., Arlinghaus R. B. Further characterization of intracellular precursor polyproteins of Rauscher leukemia virus. Virology. 1977 May 1;78(1):11–34. doi: 10.1016/0042-6822(77)90075-7. [DOI] [PubMed] [Google Scholar]
  25. Karshin W. L., Arcement L. J., Naso R. B., Arlinghaus R. B. Common precursor for Rauscher leukemia virus gp69/71, p15(E), and p12(E). J Virol. 1977 Sep;23(3):787–798. doi: 10.1128/jvi.23.3.787-798.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lander M. R., Moll B., Rowe W. P. A procedure for culture of cells from mouse tail biopsies: brief communication. J Natl Cancer Inst. 1978 Feb;60(2):477–478. [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. Linemeyer D. L., Ruscetti S. K., Menke J. G., Scolnick E. M. Recovery of biologically active spleen focus-forming virus from molecularly cloned spleen focus-forming virus-pBR322 circular DNA by cotransfection with infectious type C retroviral DNA. J Virol. 1980 Sep;35(3):710–721. doi: 10.1128/jvi.35.3.710-721.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lowy D. R. Infectious murine leukemia virus from DNA of virus-negative AKR mouse embryo cells. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5539–5543. doi: 10.1073/pnas.75.11.5539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lowy D. R., Rands E., Chattopadhyay S. K., Garon C. F., Hager G. L. Molecular cloning of infectious integrated murine leukemia virus DNA from infected mouse cells. Proc Natl Acad Sci U S A. 1980 Jan;77(1):614–618. doi: 10.1073/pnas.77.1.614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lowy D. R., Rands E., Scolnick E. M. Helper-independent transformation by unintegrated Harvey sarcoma virus DNA. J Virol. 1978 May;26(2):291–298. doi: 10.1128/jvi.26.2.291-298.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Lung M. L., Hering C., Hartley J. W., Rowe W. P., Hopkins N. Analysis of the genomes of mink cell focus-inducing murine type-C viruses: a progress report. Cold Spring Harb Symp Quant Biol. 1980;44(Pt 2):1269–1274. doi: 10.1101/sqb.1980.044.01.138. [DOI] [PubMed] [Google Scholar]
  34. Maniatis T., Jeffrey A., Kleid D. G. Nucleotide sequence of the rightward operator of phage lambda. Proc Natl Acad Sci U S A. 1975 Mar;72(3):1184–1188. doi: 10.1073/pnas.72.3.1184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Oliff A. I., Hager G. L., Chang E. H., Scolnick E. M., Chan H. W., Lowy D. R. Transfection of molecularly cloned Friend murine leukemia virus DNA yields a highly leukemogenic helper-independent type C virus. J Virol. 1980 Jan;33(1):475–486. doi: 10.1128/jvi.33.1.475-486.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Oliff A., Linemeyer D., Ruscetti S., Lowe R., Lowy D. R., Scolnick E. Subgenomic fragment of molecular cloned Friend murine leukemia virus DNA contains the gene(s) responsible for Friend murine leukemia virus-induced disease. J Virol. 1980 Sep;35(3):924–936. doi: 10.1128/jvi.35.3.924-936.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rands E., Lowy D. R., Lander M. R., Chattopadhyay S. K. Restriction endonuclease mapping of ecotropic murine leukemia viral DNAs: size and sequence heterogeneity of the long terminal repeat. Virology. 1981 Jan 30;108(2):445–452. doi: 10.1016/0042-6822(81)90451-7. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Rothenberg E., Donoghue D. J., Baltimore D. Analysis of a 5' leader sequence on murine leukemia virus 21S RNA: heteroduplex mapping with long reverse transcriptase products. Cell. 1978 Mar;13(3):435–451. doi: 10.1016/0092-8674(78)90318-5. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. Stephenson J. R., Tronick S. R., Aaronson S. A. Analysis of type specific antigenic determinants of two structural polypeptides of mouse RNA C-Type viruses. Virology. 1974 Mar;58(1):1–8. doi: 10.1016/0042-6822(74)90135-4. [DOI] [PubMed] [Google Scholar]
  42. Strand M., August J. T. Structural proteins of mammalian oncogenic RNA viruses: multiple antigenic determinants of the major internal protein and envelope glycoprotein. J Virol. 1974 Jan;13(1):171–180. doi: 10.1128/jvi.13.1.171-180.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sutcliffe J. G., Shinnick T. M., Verma I. M., Lerner R. A. Nucleotide sequence of Moloney leukemia virus: 3' end reveals details of replications, analogy to bacterial transposons, and an unexpected gene. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3302–3306. doi: 10.1073/pnas.77.6.3302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. 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]
  45. 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]
  46. Yoshimura F. K., Weinberg R. A. Restriction endonuclease cleavage of linear and closed circular murine leukemia viral DNAs: discovery of a smaller circular form. Cell. 1979 Feb;16(2):323–332. doi: 10.1016/0092-8674(79)90009-6. [DOI] [PubMed] [Google Scholar]

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