Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1977 Mar;21(3):965–973. doi: 10.1128/jvi.21.3.965-973.1977

Mechanism of restriction of ecotropic and xenotropic murine leukemia viruses and formation of pseudotypes between the two viruses.

P Besmer, D Baltimore
PMCID: PMC515635  PMID: 191655

Abstract

Ecotropic and xenotropic murine leukemia viruses (MuLV's) constitute separate interference groups; within each group there is cross-interference, but between the groups there is no detectable interference. Interference is manifest against pseudotypes in which the vesicular stomatitis virus genome is contained within the coat of one of the murine leukemia viruses. The pseudotypes display the cell specificity of the leukemia viruses: pseudotypes with an ecotropic MuLV coat infect mouse cells but not rabbit or mink cells; pseudotypes with a xenotropic MuLV coat infect rabbit or mink cells well but mouse cells very poorly. Efficient pseudotype formation also occurs between the two MuLV classes, and both the interference patterns and the cell specificity of these pseudotypes are entirely determined by their envelope. Using these pseudotypes, ecotropic MuLV infection could be established in xenogeneic cells, and the resulting progeny could be scored by using a conventional XC cell assay. Also, xenotropic MuLV infection could be established in a mouse cell, showing that no absolute intracellular barrier against xenotropic virus growth exists in murine cells. The major barriers against both xenotropic and ecotropic MuLV therefore are cell surface barriers. Xenogeneic cells probably lack receptors for ecotropic MuLV, but murine cells may either lack receptors for xenotropic MuLV or have receptors that are blocked by endogenous expression of the glycoprotein of endogenous xenotropic MuLV.

Full text

PDF
965

Selected References

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

  1. Aaronson S. A. Common genetic alterations of RNA tumour viruses grown in human cells. Nature. 1971 Apr 16;230(5294):445–447. doi: 10.1038/230445a0. [DOI] [PubMed] [Google Scholar]
  2. Aaronson S. A., Stephenson J. R. Differential cellular regulation of three distinct classes of type C RNA viruses endogenous to mouse cells. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 2):1129–1137. doi: 10.1101/sqb.1974.039.01.129. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Ablashi D. V., Turner W., Armstrong G. R., Bass L. R. Characterization of murine Rauscher leukemia virus propagated in human cells. J Natl Cancer Inst. 1972 Mar;48(3):615–621. [PubMed] [Google Scholar]
  5. Benveniste R. E., Lieber M. M., Todaro G. J. A distinct class of inducible murine type-C viruses that replicates in the rabbit SIRC cell line. Proc Natl Acad Sci U S A. 1974 Mar;71(3):602–606. doi: 10.1073/pnas.71.3.602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Besmer P., Smotkin D., Haseltine W., Fan H., Wilson A. T., Paskind M., Weinberg R., Baltimore D. Mechanism of induction of RNA tumor viruses by halogenated pyrimidines. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 2):1103–1107. doi: 10.1101/sqb.1974.039.01.125. [DOI] [PubMed] [Google Scholar]
  7. Callahan R., Lieber M. M., Todaro G. J. Nucleic acid homology of murine xenotropic type C viruses. J Virol. 1975 Jun;15(6):1378–1384. doi: 10.1128/jvi.15.6.1378-1384.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. DeLarco J., Todaro G. J. Membrane receptors for murine leukemia viruses: characterization using the purified viral envelope glycoprotein, gp71. Cell. 1976 Jul;8(3):365–371. doi: 10.1016/0092-8674(76)90148-3. [DOI] [PubMed] [Google Scholar]
  9. Fan H., Besmer P. RNA metabolism of murine leukemia virus II. Endogenous virus-specific RNA in the uninfected BALB/c cell line JLS-V9. J Virol. 1975 Apr;15(4):836–842. doi: 10.1128/jvi.15.4.836-842.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fan H., Paskind M. Measurement of the sequence complexity of cloned Moloney murine leukemia virus 60 to 70S RNA: evidence for a haploid genome. J Virol. 1974 Sep;14(3):421–429. doi: 10.1128/jvi.14.3.421-429.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fischinger P. J., Blevins C. S., Nomura S. Simple, quantitative assay for both xenotropic murine leukemia and ecotropic feline leukemia viruses. J Virol. 1974 Jul;14(1):177–179. doi: 10.1128/jvi.14.1.177-179.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fischinger P. J., Nomura S., Blevins C. S., Bolognesi D. P. Two levels of restriction by mouse or cat cells of murine sarcoma virus coated by endogenous xenotropic oncornavirus. J Gen Virol. 1975 Oct;29(1):51–62. doi: 10.1099/0022-1317-29-1-51. [DOI] [PubMed] [Google Scholar]
  13. Gazdar A. F., Russell E. K., Minna J. D. Replication of mouse-tropic and xenotropic strains of murine leukemia virus in human x mouse hybrid cells. Proc Natl Acad Sci U S A. 1974 Jul;71(7):2642–2645. doi: 10.1073/pnas.71.7.2642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Henderson I. C., Lieber M. M., Todaro G. J. Mink cell line Mv 1 Lu (CCL 64). Focus formation and the generation of "nonproducer" transformed cell lines with murine and feline sarcoma viruses. Virology. 1974 Jul;60(1):282–287. doi: 10.1016/0042-6822(74)90386-9. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. Huu Duc-Nguyen, Rosenblum E. N., Zeigel R. F. Persistent infection of a rat kidney cell line with Rauscher murine leukemia virus. J Bacteriol. 1966 Oct;92(4):1133–1140. doi: 10.1128/jb.92.4.1133-1140.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. Jolicoeur P., Baltimore D. Effect of the Fv-1 locus on the titration of murine leukemia viruses. J Virol. 1975 Dec;16(6):1593–1598. doi: 10.1128/jvi.16.6.1593-1598.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Levy J. A. Host range of murine xenotropic virus: replication in avian cells. Nature. 1975 Jan 10;253(5487):140–142. doi: 10.1038/253140a0. [DOI] [PubMed] [Google Scholar]
  24. Levy J. A., Kazan P., Varnier O., Kleiman H. Murine xenotropic type C viruses I. Distribution and further characterization of the virus in NZB mice. J Virol. 1975 Oct;16(4):844–853. doi: 10.1128/jvi.16.4.844-853.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Levy J. A., Pincus T. Demonstration of biological activity of a murine leukemia virus of New Zealand black mice. Science. 1970 Oct 16;170(3955):326–327. doi: 10.1126/science.170.3955.326. [DOI] [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. Meuth M., Green H. Induction of a deoxycytidineless state in cultured mammalian cells by bromodeoxyuridine. Cell. 1974 Jun;2(2):109–112. doi: 10.1016/0092-8674(74)90099-3. [DOI] [PubMed] [Google Scholar]
  28. Parkman R., Levy J. A., Ting R. C. Murine sarcoma virus: the question of defectiveness. Science. 1970 Apr 17;168(3929):387–389. doi: 10.1126/science.168.3929.387. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Pincus T., Rowe W. P., Lilly F. A major genetic locus affecting resistance to infection with murine leukemia viruses. II. Apparent identity to a major locus described for resistance to friend murine leukemia virus. J Exp Med. 1971 Jun 1;133(6):1234–1241. doi: 10.1084/jem.133.6.1234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rowe W. P., Pugh W. E., Hartley J. W. Plaque assay techniques for murine leukemia viruses. Virology. 1970 Dec;42(4):1136–1139. doi: 10.1016/0042-6822(70)90362-4. [DOI] [PubMed] [Google Scholar]
  32. SVOBODA J., CHYLE P., SIMKOVIC D., HILGERT I. Demonstration of the absence of infectious Rous virus in rat tumour XC, whose structurally intact cells produce Rous sarcoma when transferred to chicks. Folia Biol (Praha) 1963 Apr;9:77–81. [PubMed] [Google Scholar]
  33. Sarma P. S., Cheong M. P., Hartley J. W., Huebner R. J. A viral interference test for mouse leukemia viruses. Virology. 1967 Sep;33(1):180–184. doi: 10.1016/0042-6822(67)90111-0. [DOI] [PubMed] [Google Scholar]
  34. Scolnick E. M., Parks W. P. Host range studies on xenotropic type C viruses in somatic cell hybrids. Virology. 1974 May;59(1):168–178. doi: 10.1016/0042-6822(74)90213-x. [DOI] [PubMed] [Google Scholar]
  35. Stampfer M., Baltimore D., Huang A. S. Absence of interference during high-multiplicity infection by clonally purified vesicular stomatitis virus. J Virol. 1971 Mar;7(3):409–411. doi: 10.1128/jvi.7.3.409-411.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Stampfer M., Baltimore D., Huang A. S. Ribonucleic acid synthesis of vesicular stomatitis virus. I. Species of ribonucleic acid found in Chinese hamster ovary cells infected with plaque-forming and defective particles. J Virol. 1969 Aug;4(2):154–161. doi: 10.1128/jvi.4.2.154-161.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Steck F. T., Rubin H. The mechanism of interference between an avian leukosis virus and Rous sarcoma virus. I. Establishment of interference. Virology. 1966 Aug;29(4):628–641. doi: 10.1016/0042-6822(66)90287-x. [DOI] [PubMed] [Google Scholar]
  38. Steck F. T., Rubin H. The mechanism of interference between an avian leukosis virus and Rous sarcoma virus. II. Early steps of infection by RSV of cells under conditions of interference. Virology. 1966 Aug;29(4):642–653. doi: 10.1016/0042-6822(66)90288-1. [DOI] [PubMed] [Google Scholar]
  39. 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]
  40. 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]
  41. Ware L. M., Axelrad A. A. Inherited resistance to N- and B-tropic murine leukemia viruses in vitro: evidence that congenic mouse strains SIM and SIM.R differ at the Fv-1 locus. Virology. 1972 Nov;50(2):339–348. doi: 10.1016/0042-6822(72)90385-6. [DOI] [PubMed] [Google Scholar]
  42. Weiss R. A., Boettiger D., Love D. N. Phenotypic mixing between vesicular stomatitis virus and avian RNA tumor viruses. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 2):913–918. doi: 10.1101/sqb.1974.039.01.106. [DOI] [PubMed] [Google Scholar]
  43. Wright B. S., Korol W. Infection of human embryonic cell cultures with the Rauscher murine leukemia virus. Cancer Res. 1969 Oct;29(10):1886–1888. [PubMed] [Google Scholar]
  44. Wright B. S., O'Brien P. A., Shibley G. P., Mayyasi S. A., Lasfargues J. C. Infection of an established mouse bone marrow cell line (JLS-V9) with Rauscher and Moloney murine leukemia viruses. Cancer Res. 1967 Sep;27(9):1672–1677. [PubMed] [Google Scholar]
  45. Závada J. Pseudotypes of vesicular stomatitis virus with the coat of murine leukaemia and of avian myeloblastosis viruses. J Gen Virol. 1972 Jun;15(3):183–191. doi: 10.1099/0022-1317-15-3-183. [DOI] [PubMed] [Google Scholar]
  46. Závada J. VSV pseudotype particles with the coat of avian myeloblastosis virus. Nat New Biol. 1972 Nov 22;240(99):122–124. doi: 10.1038/newbio240122a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES