Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1983 Jun;40(3):977–984. doi: 10.1128/iai.40.3.977-984.1983

T and B lymphocyte susceptibility to murine leukemia virus moloney.

D D Isaak, J Cerny
PMCID: PMC348147  PMID: 6602095

Abstract

The susceptibility of T and B lymphocytes to productive infection and transformation by murine leukemia virus Moloney was determined by enumeration of cells producing infectious virus after in vitro infection of mitogen-stimulated, isolated cell populations and by in vivo infection of euthymic BALB/c and thymus-deficient (nude) mice. Our in vitro results demonstrated that the majority of splenic T cells and thymocytes are resistant to productive infection in vitro; a specific subpopulation of susceptible nylon-adherent splenic T cells was identified, however. Similarly, surface immunoglobulin-positive B cells also represent susceptible targets in vitro; mature B cells, however, did not represent the principal target for transformation in the in vivo experiments. Infected euthymic mice expressed increasing titers of murine leukemia virus and uniformly developed fatal T-cell lymphomas at 10 to 12 weeks postinfection; nude mice, in contrast, maintained high, stable levels of viremia throughout the 28 weeks of observation. Infected nude mice remained free of malignancy or developed either granulocytic leukemias or, in one case, reticulum cell sarcoma. Collectively, the results indicate that while the majority of T cells are resistant to productive infection, they represent the principle targets for transformation; B cells, however, represent permissive targets for virus replication, but are resistant to transformation.

Full text

PDF
977

Selected References

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

  1. Asjö B., Fenyö E. M., Spira J., Klein G. Appearance and distribution of virally determined antigens in lymphoid organs of mice during leukemogenesis by Moloney leukemia virus. Leuk Res. 1980;4(1):89–103. doi: 10.1016/0145-2126(80)90049-1. [DOI] [PubMed] [Google Scholar]
  2. Baird S., Raschke W., Weissman I. L. Evidence that MuLV-induced thymic lymphoma cells possess specific cell membrane binding sites for MuLV. Int J Cancer. 1977 Mar 15;19(3):403–413. doi: 10.1002/ijc.2910190319. [DOI] [PubMed] [Google Scholar]
  3. Bassin R. H., Tuttle N., Fischinger P. J. Rapid cell culture assay technic for murine leukaemia viruses. Nature. 1971 Feb 19;229(5286):564–566. doi: 10.1038/229564b0. [DOI] [PubMed] [Google Scholar]
  4. Boyer B., Gisselbrecht S., Debre P., McKenzie I., Levy J. P. Genetic control of sensitivity to Moloney leukemia virus in mice. IV. Phenotypic heterogeneity of the leukemic mice. J Immunol. 1980 Oct;125(4):1415–1420. [PubMed] [Google Scholar]
  5. Celada F., Asjö B., Klein G. The presence of Moloney virus induced antigen on antibody-producing cells. Clin Exp Immunol. 1970 Mar;6(3):317–323. [PMC free article] [PubMed] [Google Scholar]
  6. Cerny J., Fistel S. H., Hensgen P. A. Interactions of murine leukemia virus (MuLV) with isolated lymphocytes. I. Virus replication in lymphocytes infected with Friend virus and cultures in diffusion chambers in vivo. Int J Cancer. 1976 Aug 15;18(2):176–188. doi: 10.1002/ijc.2910180207. [DOI] [PubMed] [Google Scholar]
  7. Cerny J., Hensgen P. A., Fistel S. H., Demler L. M. Interactions of murine leukemia virus (MuLV) with isolated lymphocytes. II. Infections of B and T cells with Friend virus complex indiffusion chambers and in vitro: effect of polyclonal mitogens. Int J Cancer. 1976 Aug 15;18(2):189–196. doi: 10.1002/ijc.2910180208. [DOI] [PubMed] [Google Scholar]
  8. Cerny J., Stiller R. A. Immunosuppression by spleen cells from Moloney leukemia. Comparison of the suppressive effect on antibody response and on mitogen-induced response. J Immunol. 1975 Oct;115(4):943–949. [PubMed] [Google Scholar]
  9. Cremer N. E., Taylor D. O., Lennette E. H. Localization of immunoglobulin and viral antigen in rats infected with Moloney virus. J Natl Cancer Inst. 1969 May;42(5):695–707. [PubMed] [Google Scholar]
  10. DUNN T. B., MOLONEY J. B., GREEN A. W., ARNOLD B. Pathogenesis of a virus-induced leukemia in mice. J Natl Cancer Inst. 1961 Jan;26:189–221. [PubMed] [Google Scholar]
  11. Fischinger P. J., Ihle J. N., de Noronha F., Bolognesi D. P. Oncogenic and immunogenic potential of cloned HIX virus in mice and cats. Med Microbiol Immunol. 1977;164(1-3):119–129. doi: 10.1007/BF02121308. [DOI] [PubMed] [Google Scholar]
  12. Haas M., Sher T., Smolinsky S. Leukemogenesis in vitro induced by thymus epithelial reticulum cells transmitting murine leukemia viruses. Cancer Res. 1977 Jun;37(6):1800–1807. [PubMed] [Google Scholar]
  13. Handwerger B. S., Schwartz R. H. Separation of murine lymphoid cells using nylon wool columns. Recovery of the B cell-enriched population. Transplantation. 1974 Dec;18(6):544–548. doi: 10.1097/00007890-197412000-00013. [DOI] [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. Horak I., Enjuanes L., Lee J. C., Ihle J. N. Resistance of cultures of normal T cells to infection with murine type C viruses. J Virol. 1981 Jan;37(1):483–487. doi: 10.1128/jvi.37.1.483-487.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ihle J. N. Experimental models and conceptual approaches to studies of lymphomas and leukemia: etiology, biology, and control. Semin Hematol. 1978 Apr;15(2):95–115. [PubMed] [Google Scholar]
  17. Isaak D. D., Cerny J. Target cell heterogeneity in murine leukemia virus infection. II. Demonstration of Friend leukemia-virus-permissive and non-permissive subsets of splenic T cells. Int J Cancer. 1981;27(4):505–512. doi: 10.1002/ijc.2910270414. [DOI] [PubMed] [Google Scholar]
  18. Isaak D. D., Price J. A., Reinisch C. L., Cerny J. Target cell heterogeneity in murine leukemia virus infection. I. Differences in susceptibility to infection with Friend leukemia virus between B lymphocytes from spleen, bone marrow and lymph nodes. J Immunol. 1979 Oct;123(4):1822–1828. [PubMed] [Google Scholar]
  19. Jaenisch R., Fan H., Croker B. Infection of preimplantation mouse embryos and of newborn mice with leukemia virus: tissue distribution of viral DNA and RNA and leukemogenesis in the adult animal. Proc Natl Acad Sci U S A. 1975 Oct;72(10):4008–4012. doi: 10.1073/pnas.72.10.4008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. KAPLAN H. S., BROWN M. B. Development of lymphoid tumors in nonirradiated thymic grafts in thymectomized irradiated mice. Science. 1954 Apr 2;119(3092):439–440. doi: 10.1126/science.119.3092.439. [DOI] [PubMed] [Google Scholar]
  21. Katz I. R., Asofsky R., Thorbecke G. J. Suppression of spontaneous reticulum cell sarcoma development and of syngeneic stimulator cell by anti-mu treatment of SJL/J mice. J Immunol. 1980 Sep;125(3):1355–1359. [PubMed] [Google Scholar]
  22. Kumar V., Caruso T., Bennett M. Mechanisms of genetic resistance to Friend virus leukemia. III. Susceptibility of mitogen-responsive lymphocytes mediated by T cells. J Exp Med. 1976 Apr 1;143(4):728–740. doi: 10.1084/jem.143.4.728. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. MOLONEY J. B. Biological studies on a lymphoid-leukemia virus extracted from sarcoma 37. I. Origin and introductory investigations. J Natl Cancer Inst. 1960 Apr;24:933–951. [PubMed] [Google Scholar]
  24. Nowinski R. C., Hays E. F. Oncogenicity of AKR endogenous leukemia viruses. J Virol. 1978 Jul;27(1):13–18. doi: 10.1128/jvi.27.1.13-18.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Oshiro L. S., Cremer N. E., Taylor D. O., Lennette E. H. Electron microscopic studies on the localization of antibodies in rat lymph node cells producing moloney virus. J Natl Cancer Inst. 1969 Nov;43(5):1109–1118. [PubMed] [Google Scholar]
  26. Proffitt M. R., Hirsch M. S., McKenzie I. F., Gheridian B., Black P. H. Immunological mechanisms in the pathogenesis of virus-induced murine leukemia. II. Characterization of autoreactive thymocytes. Int J Cancer. 1975 Feb 15;15(2):230–240. doi: 10.1002/ijc.2910150208. [DOI] [PubMed] [Google Scholar]
  27. Reddy E. P., Dunn C. Y., Aaronson S. A. Different lymphoid cell targets by transformation by replication-competent Moloney and Rauscher mouse leukemia viruses. Cell. 1980 Mar;19(3):663–669. doi: 10.1016/s0092-8674(80)80043-2. [DOI] [PubMed] [Google Scholar]
  28. Ricciardi-Castagnoli P., Lieberman M., Finn O., Kaplan H. S. T-cell lymphoma induction by radiation leukemia virus in athymic nude mice. J Exp Med. 1978 Nov 1;148(5):1292–1310. doi: 10.1084/jem.148.5.1292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schlossman S. F., Hudson L. Specific purification of lymphocyte populations on a digestible immunoabsorbent. J Immunol. 1973 Jan;110(1):313–319. [PubMed] [Google Scholar]
  30. Schrader J. W., Battye F., Scollay R. Expression of Thy-1 antigen is not limited to T cells in cultures of mouse hemopoietic cells. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4161–4165. doi: 10.1073/pnas.79.13.4161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Shevach E. M., Stobo J. D., Green I. Immunoglobulin and theta-bearing murine leukemias and lymphomas. J Immunol. 1972 May;108(5):1146–1151. [PubMed] [Google Scholar]
  32. 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 Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES