Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1986 Jan;57(1):389–393. doi: 10.1128/jvi.57.1.389-393.1986

Analysis of two strains of Friend murine leukemia viruses differing in ability to induce early splenomegaly: lack of relationship with generation of recombinant mink cell focus-forming viruses.

M Sitbon, L Evans, J Nishio, K Wehrly, B Chesebro
PMCID: PMC252743  PMID: 3001361

Abstract

Friend murine leukemia helper viruses (F-MuLV) 57 and B3 were indistinguishable by genomic structural analyses with RNase T1-resistant oligonucleotide fingerprinting and by antigenic reactivity with a panel of 31 monoclonal antibodies directed against murine leukemia viruses. Nevertheless, F-MuLV 57 and B3 had strikingly different virulences. Approximately 2 months after inoculation, IRW and NFS/N mice inoculated as newborns with F-MuLV 57 had gross splenomegaly caused by erythroid proliferation. In contrast, an equivalent dose of F-MuLV B3 induced spleen or lymph node enlargement 4 to 13 months after inoculation. Although most cases of spleen enlargement in F-MuLV B3-inoculated mice were due to erythroid proliferation, lymphoid or myeloid proliferation was also frequently observed. The replication of both F-MuLV 57 and B3 was equally efficient, and both viruses generated recombinant dual-tropic mink cell focus-forming (MCF) viruses with the same kinetics and efficiency. Moreover, MCF viruses induced by F-MuLV 57 and B3 had the same antigenic patterns. Therefore, the ability of F-MuLV to induce early splenomegaly did not correlate with the generation of recombinant MCF viruses.

Full text

PDF
392

Images in this article

Selected References

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

  1. Carter R. L., Chesterman F. C., Rowson K. E., Salaman M. H., Wedderburn N. Induction of lymphoma in BALB-c mice by Rowson-Parr virus (RPV). Int J Cancer. 1970 Sep 15;6(2):290–303. doi: 10.1002/ijc.2910060217. [DOI] [PubMed] [Google Scholar]
  2. Chatis P. A., Holland C. A., Hartley J. W., Rowe W. P., Hopkins N. Role for the 3' end of the genome in determining disease specificity of Friend and Moloney murine leukemia viruses. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4408–4411. doi: 10.1073/pnas.80.14.4408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chatis P. A., Holland C. A., Silver J. E., Frederickson T. N., Hopkins N., Hartley J. W. A 3' end fragment encompassing the transcriptional enhancers of nondefective Friend virus confers erythroleukemogenicity on Moloney leukemia virus. J Virol. 1984 Oct;52(1):248–254. doi: 10.1128/jvi.52.1.248-254.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Chesebro B., Britt W., Evans L., Wehrly K., Nishio J., Cloyd M. Characterization of monoclonal antibodies reactive with murine leukemia viruses: use in analysis of strains of friend MCF and Friend ecotropic murine leukemia virus. Virology. 1983 May;127(1):134–148. doi: 10.1016/0042-6822(83)90378-1. [DOI] [PubMed] [Google Scholar]
  6. Chesebro B., Portis J. L., Wehrly K., Nishio J. Effect of murine host genotype on MCF virus expression, latency, and leukemia cell type of leukemias induced by Friend murine leukemia helper virus. Virology. 1983 Jul 15;128(1):221–233. doi: 10.1016/0042-6822(83)90332-x. [DOI] [PubMed] [Google Scholar]
  7. Chesebro B., Wehrly K., Cloyd M., Britt W., Portis J., Collins J., Nishio J. Characterization of mouse monoclonal antibodies specific for Friend murine leukemia virus-induced erythroleukemia cells: friend-specific and FMR-specific antigens. Virology. 1981 Jul 15;112(1):131–144. doi: 10.1016/0042-6822(81)90619-x. [DOI] [PubMed] [Google Scholar]
  8. Chesebro B., Wehrly K., Nishio J., Evans L. Leukemia induction by a new strain of Friend mink cell focus-inducing virus: synergistic effect of Friend ecotropic murine leukemia virus. J Virol. 1984 Jul;51(1):63–70. doi: 10.1128/jvi.51.1.63-70.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dawson P. J., Tacke R. B., Fieldsteel A. H. Relationship between Friend virus and an associated lymphatic leukaemia virus. Br J Cancer. 1968 Sep;22(3):569–576. doi: 10.1038/bjc.1968.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. DesGroseillers L., Jolicoeur P. Mapping the viral sequences conferring leukemogenicity and disease specificity in Moloney and amphotropic murine leukemia viruses. J Virol. 1984 Nov;52(2):448–456. doi: 10.1128/jvi.52.2.448-456.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Evans L. H., Cloyd M. W. Friend and Moloney murine leukemia viruses specifically recombine with different endogenous retroviral sequences to generate mink cell focus-forming viruses. Proc Natl Acad Sci U S A. 1985 Jan;82(2):459–463. doi: 10.1073/pnas.82.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Evans L. H., Cloyd M. W. Generation of mink cell focus-forming viruses by Friend murine leukemia virus: recombination with specific endogenous proviral sequences. J Virol. 1984 Mar;49(3):772–781. doi: 10.1128/jvi.49.3.772-781.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fischinger P. J., Nomura S., Bolognesi D. P. A novel murine oncornavirus with dual eco- and xenotropic properties. Proc Natl Acad Sci U S A. 1975 Dec;72(12):5150–5155. doi: 10.1073/pnas.72.12.5150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Ishimoto A., Adachi A., Sakai K., Matsuyama M. Long terminal repeat of Friend-MCF virus contains the sequence responsible for erythroid leukemia. Virology. 1985 Feb;141(1):30–42. doi: 10.1016/0042-6822(85)90180-1. [DOI] [PubMed] [Google Scholar]
  16. Lander M. R., Chattopadhyay S. K. A Mus dunni cell line that lacks sequences closely related to endogenous murine leukemia viruses and can be infected by ectropic, amphotropic, xenotropic, and mink cell focus-forming viruses. J Virol. 1984 Nov;52(2):695–698. doi: 10.1128/jvi.52.2.695-698.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. MacDonald M. E., Mak T. W., Bernstein A. Erythroleukemia induction by replication-competent type C viruses cloned from the anemia- and polycythemia-inducing isolates of Friend leukemia virus. J Exp Med. 1980 Jun 1;151(6):1493–1503. doi: 10.1084/jem.151.6.1493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Oliff A., Ruscetti S., Douglass E. C., Scolnick E. Isolation of transplantable erythroleukemia cells from mice infected with helper-independent Friend murine leukemia virus. Blood. 1981 Aug;58(2):244–254. [PubMed] [Google Scholar]
  21. Oliff A., Signorelli K., Collins L. The envelope gene and long terminal repeat sequences contribute to the pathogenic phenotype of helper-independent Friend viruses. J Virol. 1984 Sep;51(3):788–794. doi: 10.1128/jvi.51.3.788-794.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Portis J. L., McAtee F. J., Cloyd M. W. Monoclonal antibodies to xenotropic and MCF murine leukemia viruses derived during the graft-versus-host reaction. Virology. 1982 Apr 15;118(1):181–190. doi: 10.1016/0042-6822(82)90331-2. [DOI] [PubMed] [Google Scholar]
  23. Portis J. L., McAtee F. J. Monoclonal antibodies derived during graft-versus-host reaction. II. Antibodies detect unique determinants common to many MCF viruses. Virology. 1983 Apr 15;126(1):96–105. doi: 10.1016/0042-6822(83)90464-6. [DOI] [PubMed] [Google Scholar]
  24. Ruscetti S., Davis L., Feild J., Oliff A. Friend murine leukemia virus-induced leukemia is associated with the formation of mink cell focus-inducing viruses and is blocked in mice expressing endogenous mink cell focus-inducing xenotropic viral envelope genes. J Exp Med. 1981 Sep 1;154(3):907–920. doi: 10.1084/jem.154.3.907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ruscetti S., Feild J., Davis L., Oliff A. Factors determining the susceptibility of NIH swiss mice to erythroleukemia induced by Friend murine leukemia virus. Virology. 1982 Mar;117(2):357–365. doi: 10.1016/0042-6822(82)90475-5. [DOI] [PubMed] [Google Scholar]
  26. Silver J. E., Fredrickson T. N. A new gene that controls the type of leukemia induced by Friend murine leukemia virus. J Exp Med. 1983 Aug 1;158(2):493–505. doi: 10.1084/jem.158.2.493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Silver J. E., Fredrickson T. N. Susceptibility to Friend helper virus leukemias in CXB recombinant inbred mice. J Exp Med. 1983 Nov 1;158(5):1693–1702. doi: 10.1084/jem.158.5.1693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sitbon M., Nishio J., Wehrly K., Chesebro B. Pseudotyping of dual-tropic recombinant viruses generated by infection of mice with different ecotropic murine leukemia viruses. Virology. 1985 Jan 15;140(1):144–151. doi: 10.1016/0042-6822(85)90453-2. [DOI] [PubMed] [Google Scholar]
  29. Sitbon M., Nishio J., Wehrly K., Lodmell D., Chesebro B. Use of a focal immunofluorescence assay on live cells for quantitation of retroviruses: distinction of host range classes in virus mixtures and biological cloning of dual-tropic murine leukemia viruses. Virology. 1985 Feb;141(1):110–118. doi: 10.1016/0042-6822(85)90187-4. [DOI] [PubMed] [Google Scholar]
  30. Steeves R. A., Eckner R. J., Bennett M., Mirand E. A., Trudel P. J. Isolation and characterization of a lymphatic leukemia virus in the Friend virus complex. J Natl Cancer Inst. 1971 Jun;46(6):1209–1217. [PubMed] [Google Scholar]
  31. Troxler D. H., Scolnick E. M. Rapid leukemia induced by cloned friend strain of replicating murine type-C virus. Association with induction of xenotropic-related RNA sequences contained in spleen focus-forming virus. Virology. 1978 Mar;85(1):17–27. doi: 10.1016/0042-6822(78)90408-7. [DOI] [PubMed] [Google Scholar]

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

RESOURCES