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. 1989 Oct;63(10):4434–4437. doi: 10.1128/jvi.63.10.4434-4437.1989

Splenic accumulation of interleukin-3-dependent hematopoietic cells in Friend erythroleukemia.

C Spiro 1, B C Gliniak 1, D Kabat 1
PMCID: PMC251064  PMID: 2789294

Abstract

Interleukin-3-dependent hematopoietic stem cells commonly accumulate in spleens of mice infected with leukemia viruses. To study their origins, a molecularly tagged helper-free Friend spleen focus-forming virus was used to produce erythroleukemias. Uninfected interleukin-3-dependent basophil-mast cell progenitors coproliferated amidst the spleen focus-forming virus-infected leukemic cells. Splenic proliferation of normal stem cells is apparently a host response to leukemogenesis, and we propose that it may contribute to certain retroviral diseases.

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Selected References

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  1. Berger S. A., Sanderson N., Bernstein A., Hankins W. D. Induction of the early stages of Friend erythroleukemia with helper-free Friend spleen focus-forming virus. Proc Natl Acad Sci U S A. 1985 Oct;82(20):6913–6917. doi: 10.1073/pnas.82.20.6913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bestwick R. K., Hankins W. D., Kabat D. Roles of helper and defective retroviral genomes in murine erythroleukemia: studies of spleen focus-forming virus in the absence of helper. J Virol. 1985 Dec;56(3):660–664. doi: 10.1128/jvi.56.3.660-664.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Dresler S., Ruta M., Murray M. J., Kabat D. Glycoprotein encoded by the Friend spleen focus-forming virus. J Virol. 1979 May;30(2):564–575. doi: 10.1128/jvi.30.2.564-575.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Hara H., Ogawa M. Erthropoietic precursors in mice with phenylhydrazine-induced anemia. Am J Hematol. 1976;1(4):453–458. doi: 10.1002/ajh.2830010410. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Hobom-Schnegg B., Robinson H. L., Robinson W. S. Replication of Rous sarcoma virus in synchronized cells. J Gen Virol. 1970;7(2):85–93. doi: 10.1099/0022-1317-7-2-85. [DOI] [PubMed] [Google Scholar]
  8. Ihle J. N., Enjuanes L., Lee J. C., Keller J. The immune response to C-type viruses and its potential role in leukemogenesis. Curr Top Microbiol Immunol. 1982;101:31–49. doi: 10.1007/978-3-642-68654-2_2. [DOI] [PubMed] [Google Scholar]
  9. Ihle J. N., Weinstein Y. Immunological regulation of hematopoietic/lymphoid stem cell differentiation by interleukin 3. Adv Immunol. 1986;39:1–50. doi: 10.1016/s0065-2776(08)60347-8. [DOI] [PubMed] [Google Scholar]
  10. Lee J. C., Ihle J. N. Chronic immune stimulation is required for Moloney leukaemia virus-induced lymphomas. Nature. 1981 Jan 29;289(5796):407–409. doi: 10.1038/289407a0. [DOI] [PubMed] [Google Scholar]
  11. Lee J. C., Ihle J. N. Increased responses to lymphokines are correlated with preleukemia in mice inoculated with Moloney leukemia virus. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7712–7716. doi: 10.1073/pnas.78.12.7712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. McGrath M. S., Weissman I. L. AKR leukemogenesis: identification and biological significance of thymic lymphoma receptors for AKR retroviruses. Cell. 1979 May;17(1):65–75. doi: 10.1016/0092-8674(79)90295-2. [DOI] [PubMed] [Google Scholar]
  13. Nagao K., Yokoro K., Aaronson S. A. Continuous lines of basophil/mast cells derived from normal mouse bone marrow. Science. 1981 Apr 17;212(4492):333–335. doi: 10.1126/science.7209531. [DOI] [PubMed] [Google Scholar]
  14. Oliff A., Agranovsky O., McKinney M. D., Murty V. V., Bauchwitz R. Friend murine leukemia virus-immortalized myeloid cells are converted into tumorigenic cell lines by Abelson leukemia virus. Proc Natl Acad Sci U S A. 1985 May;82(10):3306–3310. doi: 10.1073/pnas.82.10.3306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Oliff A., Oliff I., Schmidt B., Famulari N. Isolation of immortal cell lines from the first stage of murine leukemia virus-induced leukemia. Proc Natl Acad Sci U S A. 1984 Sep;81(17):5464–5467. doi: 10.1073/pnas.81.17.5464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Paskind M. P., Weinberg R. A., Baltimore D. Dependence of Moloney murine leukemia virus production on cell growth. Virology. 1975 Sep;67(1):242–248. doi: 10.1016/0042-6822(75)90421-3. [DOI] [PubMed] [Google Scholar]
  17. Pierce J. H., Di Fiore P. P., Aaronson S. A., Potter M., Pumphrey J., Scott A., Ihle J. N. Neoplastic transformation of mast cells by Abelson-MuLV: abrogation of IL-3 dependence by a nonautocrine mechanism. Cell. 1985 Jul;41(3):685–693. doi: 10.1016/s0092-8674(85)80049-0. [DOI] [PubMed] [Google Scholar]
  18. Pinter A., Honnen W. J. The mature form of the Friend spleen focus-forming virus envelope protein, gp65, is efficiently secreted from cells. Virology. 1985 Jun;143(2):646–650. doi: 10.1016/0042-6822(85)90406-4. [DOI] [PubMed] [Google Scholar]
  19. Rapp U. R., Cleveland J. L., Brightman K., Scott A., Ihle J. N. Abrogation of IL-3 and IL-2 dependence by recombinant murine retroviruses expressing v-myc oncogenes. Nature. 1985 Oct 3;317(6036):434–438. doi: 10.1038/317434a0. [DOI] [PubMed] [Google Scholar]
  20. Ruta M., Kabat D. Plasma membrane glycoproteins encoded by cloned Rauscher and Friend spleen focus-forming viruses. J Virol. 1980 Sep;35(3):844–853. doi: 10.1128/jvi.35.3.844-853.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sherton C. C., Evans L. H., Polonoff E., Kabat D. Relationship of Friend murine leukemia virus production to growth and hemoglobin synthesis in cultured erythroleukemia cells. J Virol. 1976 Jul;19(1):118–125. doi: 10.1128/jvi.19.1.118-125.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sonoda Y., Yang Y. C., Wong G. G., Clark S. C., Ogawa M. Analysis in serum-free culture of the targets of recombinant human hemopoietic growth factors: interleukin 3 and granulocyte/macrophage-colony-stimulating factor are specific for early developmental stages. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4360–4364. doi: 10.1073/pnas.85.12.4360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Spiro C., Gliniak B., Kabat D. A tagged helper-free Friend virus causes clonal erythroblast immortality by specific proviral integration in the cellular genome. J Virol. 1988 Nov;62(11):4129–4135. doi: 10.1128/jvi.62.11.4129-4135.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Varmus H. E., Padgett T., Heasley S., Simon G., Bishop J. M. Cellular functions are required for the synthesis and integration of avian sarcoma virus-specific DNA. Cell. 1977 Jun;11(2):307–319. doi: 10.1016/0092-8674(77)90047-2. [DOI] [PubMed] [Google Scholar]
  26. Wolff L., Ruscetti S. Malignant transformation of erythroid cells in vivo by introduction of a nonreplicating retrovirus vector. Science. 1985 Jun 28;228(4707):1549–1552. doi: 10.1126/science.2990034. [DOI] [PubMed] [Google Scholar]
  27. Wolff L., Tambourin P., Ruscetti S. Induction of the autonomous stage of transformation in erythroid cells infected with SFFV: helper virus is not required. Virology. 1986 Jul 15;152(1):272–276. doi: 10.1016/0042-6822(86)90393-4. [DOI] [PubMed] [Google Scholar]
  28. Yam L. T., Li C. Y., Crosby W. H. Cytochemical identification of monocytes and granulocytes. Am J Clin Pathol. 1971 Mar;55(3):283–290. doi: 10.1093/ajcp/55.3.283. [DOI] [PubMed] [Google Scholar]
  29. Yung Y. P., Eger R., Tertian G., Moore M. A. Long-term in vitro culture of murine mast cells. II. Purification of a mast cell growth factor and its dissociation from TCGF. J Immunol. 1981 Aug;127(2):794–799. [PubMed] [Google Scholar]

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