Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1993 Jun;67(6):3665–3670. doi: 10.1128/jvi.67.6.3665-3670.1993

Increased hematopoiesis in mice soon after infection by Friend murine leukemia virus.

T Mitchell 1
PMCID: PMC237722  PMID: 8497076

Abstract

Friend murine leukemia virus (F-MuLV), an erythroleukemogenic replication-competent retrovirus, induces leukemia in its host after a long latency. However, the early effects of infection may determine the pathway that eventually leads to malignant transformation. To determine how F-MuLV affects host cell proliferation soon after infection, BALB/c mice were inoculated with virus and then were assayed for susceptibility to appropriately pseudotyped spleen focus-forming virus (SFFV) as an indicator of erythropoietic activity. Twelve-week-old mice exposed to F-MuLV for 9 days were more susceptible (by a factor of 30) to superinfection by SFFV than were nonviremic mice. To test whether increased susceptibility was the result of increased hematopoietic activity, hematopoietic progenitors from the spleens of F-MuLV-infected mice were enumerated with a clonal culture assay. Nine days after inoculation with F-MuLV, the numbers of colony-forming progenitors increased by a factor of 4. Morphological analysis of the cultured colonies showed that erythroid, granulocytic, monocytic, and mixed granulocytic-monocytic progenitors all had increased. Thus, F-MuLV more rapidly induced a generalized increase in hematopoiesis than has previously been reported. The splenic hyperplasia induced by F-MuLV soon after infection may explain its ability to accelerate leukemogenesis in mice also infected by the polytropic Friend mink cell focus-forming virus.

Full text

PDF
3665

Images in this article

Selected References

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

  1. AXELRAD A. A., STEEVES R. A. ASSAY FOR FRIEND LEUKEMIA VIRUS: RAPID QUANTITATIVE METHOD BASED ON ENUMERATION OF MACROSCOPIC SPLEEN FOCI IN MICE. Virology. 1964 Nov;24:513–518. doi: 10.1016/0042-6822(64)90199-0. [DOI] [PubMed] [Google Scholar]
  2. Amanuma H., Katori A., Obata M., Sagata N., Ikawa Y. Complete nucleotide sequence of the gene for the specific glycoprotein (gp55) of Friend spleen focus-forming virus. Proc Natl Acad Sci U S A. 1983 Jul;80(13):3913–3917. doi: 10.1073/pnas.80.13.3913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Davis B. R., Brightman B. K., Chandy K. G., Fan H. Characterization of a preleukemic state induced by Moloney murine leukemia virus: evidence for two infection events during leukemogenesis. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4875–4879. doi: 10.1073/pnas.84.14.4875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Doig D., Chesebro B. Anti-Friend virus antibody is associated with recovery from viremia and loss of viral leukemia cell-surface antigens in leukemic mice. Identification of Rfv-3 as a gene locus influencing antibody production. J Exp Med. 1979 Jul 1;150(1):10–19. doi: 10.1084/jem.150.1.10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Earl P. L., Moss B., Morrison R. P., Wehrly K., Nishio J., Chesebro B. T-lymphocyte priming and protection against Friend leukemia by vaccinia-retrovirus env gene recombinant. Science. 1986 Nov 7;234(4777):728–731. doi: 10.1126/science.3490689. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. 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]
  10. 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]
  11. Holland C. A., Anklesaria P., Sakakeeny M. A., Greenberger J. S. Enhancer sequences of a retroviral vector determine expression of a gene in multipotent hematopoietic progenitors and committed erythroid cells. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8662–8666. doi: 10.1073/pnas.84.23.8662. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hopkins N., Besmer P., DeLeo A. B., Law L. W. High-frequency cotransfer of the transformed phenotype and a tumor-specific transplantation antigen by DNA from the 3-methylcholanthrene-induced Meth A sarcoma of BALB/c mice. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7555–7559. doi: 10.1073/pnas.78.12.7555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kost T. A., Koury M. J., Krantz S. B. Mature erythroid burst-forming units are target cells for Friend virus-induced erythroid bursts. Virology. 1981 Jan 30;108(2):309–317. doi: 10.1016/0042-6822(81)90439-6. [DOI] [PubMed] [Google Scholar]
  14. Li J. P., Baltimore D. Mechanism of leukemogenesis induced by mink cell focus-forming murine leukemia viruses. J Virol. 1991 May;65(5):2408–2414. doi: 10.1128/jvi.65.5.2408-2414.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Li J. P., D'Andrea A. D., Lodish H. F., Baltimore D. Activation of cell growth by binding of Friend spleen focus-forming virus gp55 glycoprotein to the erythropoietin receptor. Nature. 1990 Feb 22;343(6260):762–764. doi: 10.1038/343762a0. [DOI] [PubMed] [Google Scholar]
  16. Li Q. X., Fan H. Bone marrow depletion by 89Sr complements a preleukemic defect in a long terminal repeat variant of Moloney murine leukemia virus. J Virol. 1991 Aug;65(8):4442–4448. doi: 10.1128/jvi.65.8.4442-4448.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Metcalf D., Johnson G. R. Production by spleen and lymph node cells of conditioned medium with erythroid and other hemopoietic colony-stimulating activity. J Cell Physiol. 1978 Jul;96(1):31–42. doi: 10.1002/jcp.1040960105. [DOI] [PubMed] [Google Scholar]
  19. Mitchell T., Risser R. Interference established in mice by infection with Friend murine leukemia virus. J Virol. 1992 Sep;66(9):5696–5702. doi: 10.1128/jvi.66.9.5696-5702.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Rein A. Interference grouping of murine leukemia viruses: a distinct receptor for the MCF-recombinant viruses in mouse cells. Virology. 1982 Jul 15;120(1):251–257. doi: 10.1016/0042-6822(82)90024-1. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Runnels J., Serunian L., Thursby M., Rosenberg N. Moloney leukemia virus immortalizes B lymphocytes in vitro. J Virol. 1991 Oct;65(10):5549–5552. doi: 10.1128/jvi.65.10.5549-5552.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ruscetti S., Wolff L. Biological and biochemical differences between variants of spleen focus-forming virus can be localized to a region containing the 3' end of the envelope gene. J Virol. 1985 Dec;56(3):717–722. doi: 10.1128/jvi.56.3.717-722.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sitbon M., Ellerbrok H., Pozo F., Nishio J., Hayes S. F., Evans L. H., Chesebro B. Sequences in the U5-gag-pol region influence early and late pathogenic effects of Friend and Moloney murine leukemia viruses. J Virol. 1990 May;64(5):2135–2140. doi: 10.1128/jvi.64.5.2135-2140.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sitbon M., Sola B., Evans L., Nishio J., Hayes S. F., Nathanson K., Garon C. F., Chesebro B. Hemolytic anemia and erythroleukemia, two distinct pathogenic effects of Friend MuLV: mapping of the effects to different regions of the viral genome. Cell. 1986 Dec 26;47(6):851–859. doi: 10.1016/0092-8674(86)90800-7. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. Storch T. G., Arnstein P., Manohar V., Leiserson W. M., Chused T. M. Proliferation of infected lymphoid precursors before Moloney murine leukemia virus-induced T-cell lymphoma. J Natl Cancer Inst. 1985 Jan;74(1):137–143. [PubMed] [Google Scholar]
  30. 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]
  31. Tsichlis P. N., Bear S. E. Infection by mink cell focus-forming viruses confers interleukin 2 (IL-2) independence to an IL-2-dependent rat T-cell lymphoma line. Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):4611–4615. doi: 10.1073/pnas.88.11.4611. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES