Retrovirus-mediated transfer and expression of the interleukin-3 gene in mouse hematopoietic cells result in a myeloproliferative disorder (original) (raw)
Abstract
A high-titer, recombinant retroviral vector produced in psi 2 packaging cells has been used to introduce the murine interleukin-3 (IL-3) gene into mouse hematopoietic cells. Integration and expression of the IL-3 gene was observed in spleen foci from which could be derived factor-independent, continuously proliferating cell lines. Irradiated or genetically anemic W/Wv recipients of infected hematopoietic cells developed a myeloproliferative syndrome characterized by a marked elevation in leukocyte count, bone marrow hyperplasia, and enlargement of the liver and spleen. The syndrome reflected proliferation of one or more stem cell clones, the progeny of which were capable of repopulating secondary recipients. One animal developed the syndrome primarily by a paracrine mechanism. Endogenous IL-3 production caused amplification of hematopoietic cells but did not appear to alter the maturational or self-renewal potential of these cells.
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- Armentano D., Yu S. F., Kantoff P. W., von Ruden T., Anderson W. F., Gilboa E. Effect of internal viral sequences on the utility of retroviral vectors. J Virol. 1987 May;61(5):1647–1650. doi: 10.1128/jvi.61.5.1647-1650.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barker J. E., Keenan M. A., Raphals L. Development of the mouse hematopoietic system. II. Estimation of spleen and liver "stem" cell number. J Cell Physiol. 1969 Aug;74(1):51–56. doi: 10.1002/jcp.1040740107. [DOI] [PubMed] [Google Scholar]
- 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]
- Ben-Neriah Y., Daley G. Q., Mes-Masson A. M., Witte O. N., Baltimore D. The chronic myelogenous leukemia-specific P210 protein is the product of the bcr/abl hybrid gene. Science. 1986 Jul 11;233(4760):212–214. doi: 10.1126/science.3460176. [DOI] [PubMed] [Google Scholar]
- Bishop J. M. The molecular genetics of cancer. Science. 1987 Jan 16;235(4786):305–311. doi: 10.1126/science.3541204. [DOI] [PubMed] [Google Scholar]
- Browder T. M., Abrams J. S., Wong P. M., Nienhuis A. W. Mechanism of autocrine stimulation in hematopoietic cells producing interleukin-3 after retrovirus-mediated gene transfer. Mol Cell Biol. 1989 Jan;9(1):204–213. doi: 10.1128/mcb.9.1.204. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Champlin R. E., Golde D. W. Chronic myelogenous leukemia: recent advances. Blood. 1985 May;65(5):1039–1047. [PubMed] [Google Scholar]
- Chung S. W., Ruscetti S., Wong P. M. Formation of factor-independent hematopoietic multilineage colonies after Abelson virus infection. Blood. 1988 Apr;71(4):973–977. [PubMed] [Google Scholar]
- Chung S. W., Wong P. M., Shen-Ong G., Ruscetti S., Ishizaka T., Eaves C. J. Production of granulocyte-macrophage colony-stimulating factor by Abelson virus-induced tumorigenic mast cell lines. Blood. 1986 Nov;68(5):1074–1081. [PubMed] [Google Scholar]
- Dick J. E., Magli M. C., Huszar D., Phillips R. A., Bernstein A. Introduction of a selectable gene into primitive stem cells capable of long-term reconstitution of the hemopoietic system of W/Wv mice. Cell. 1985 Aug;42(1):71–79. doi: 10.1016/s0092-8674(85)80102-1. [DOI] [PubMed] [Google Scholar]
- Eaves C. J., Eaves A. C. Erythropoietin (Ep) dose-response curves for three classes of erythroid progenitors in normal human marrow and in patients with polycythemia vera. Blood. 1978 Dec;52(6):1196–1210. [PubMed] [Google Scholar]
- Griffin J. D., Rambaldi A., Vellenga E., Young D. C., Ostapovicz D., Cannistra S. A. Secretion of interleukin-1 by acute myeloblastic leukemia cells in vitro induces endothelial cells to secrete colony stimulating factors. Blood. 1987 Oct;70(4):1218–1221. [PubMed] [Google Scholar]
- Griffin J. D., Young D. C. The role of colony stimulating factors in leukaemogenesis. Clin Haematol. 1986 Nov;15(4):995–1002. [PubMed] [Google Scholar]
- Hapel A. J., Vande Woude G., Campbell H. D., Young I. G., Robins T. Generation of an autocrine leukaemia using a retroviral expression vector carrying the interleukin-3 gene. Lymphokine Res. 1986 Fall;5(4):249–254. [PubMed] [Google Scholar]
- Hapel A. J., Young I. G. Abnormal expression of interleukin-3 and leukaemia. Anticancer Res. 1987 Jul-Aug;7(4A):661–667. [PubMed] [Google Scholar]
- Harrison D. E. Competitive repopulation: a new assay for long-term stem cell functional capacity. Blood. 1980 Jan;55(1):77–81. [PubMed] [Google Scholar]
- Heard J. M., Roussel M. F., Rettenmier C. W., Sherr C. J. Multilineage hematopoietic disorders induced by transplantation of bone marrow cells expressing the v-fms oncogene. Cell. 1987 Nov 20;51(4):663–673. doi: 10.1016/0092-8674(87)90135-8. [DOI] [PubMed] [Google Scholar]
- Lang R. A., Metcalf D., Cuthbertson R. A., Lyons I., Stanley E., Kelso A., Kannourakis G., Williamson D. J., Klintworth G. K., Gonda T. J. Transgenic mice expressing a hemopoietic growth factor gene (GM-CSF) develop accumulations of macrophages, blindness, and a fatal syndrome of tissue damage. Cell. 1987 Nov 20;51(4):675–686. doi: 10.1016/0092-8674(87)90136-x. [DOI] [PubMed] [Google Scholar]
- Lang R. A., Metcalf D., Gough N. M., Dunn A. R., Gonda T. J. Expression of a hemopoietic growth factor cDNA in a factor-dependent cell line results in autonomous growth and tumorigenicity. Cell. 1985 Dec;43(2 Pt 1):531–542. doi: 10.1016/0092-8674(85)90182-5. [DOI] [PubMed] [Google Scholar]
- Lemischka I. R., Raulet D. H., Mulligan R. C. Developmental potential and dynamic behavior of hematopoietic stem cells. Cell. 1986 Jun 20;45(6):917–927. doi: 10.1016/0092-8674(86)90566-0. [DOI] [PubMed] [Google Scholar]
- Ley T. J., Anagnou N. P., Pepe G., Nienhuis A. W. RNA processing errors in patients with beta-thalassemia. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4775–4779. doi: 10.1073/pnas.79.15.4775. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mann R., Mulligan R. C., Baltimore D. Construction of a retrovirus packaging mutant and its use to produce helper-free defective retrovirus. Cell. 1983 May;33(1):153–159. doi: 10.1016/0092-8674(83)90344-6. [DOI] [PubMed] [Google Scholar]
- Metcalf D., Begley C. G., Johnson G. R., Nicola N. A., Lopez A. F., Williamson D. J. Effects of purified bacterially synthesized murine multi-CSF (IL-3) on hematopoiesis in normal adult mice. Blood. 1986 Jul;68(1):46–57. [PubMed] [Google Scholar]
- Metcalf D., Begley C. G., Nicola N. A., Johnson G. R. Quantitative responsiveness of murine hemopoietic populations in vitro and in vivo to recombinant multi-CSF (IL-3). Exp Hematol. 1987 Mar;15(3):288–295. [PubMed] [Google Scholar]
- Metcalf D. The molecular biology and functions of the granulocyte-macrophage colony-stimulating factors. Blood. 1986 Feb;67(2):257–267. [PubMed] [Google Scholar]
- Naparstek E., Wagner K., Harrison D., Greenberger J. S. Hematopoietic effects of continuous intravenous infusion of mice with growth factors produced by the WEHI-3 cell line. Acta Haematol. 1987;77(1):1–5. doi: 10.1159/000205939. [DOI] [PubMed] [Google Scholar]
- Prchal J. F., Adamson J. W., Murphy S., Steinmann L., Fialkow P. J. Polycythemia vera. The in vitro response of normal and abnormal stem cell lines to erythropoietin. J Clin Invest. 1978 Apr;61(4):1044–1047. doi: 10.1172/JCI109003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ross R., Raines E. W., Bowen-Pope D. F. The biology of platelet-derived growth factor. Cell. 1986 Jul 18;46(2):155–169. doi: 10.1016/0092-8674(86)90733-6. [DOI] [PubMed] [Google Scholar]
- Russell E. S. Hereditary anemias of the mouse: a review for geneticists. Adv Genet. 1979;20:357–459. [PubMed] [Google Scholar]
- Schrader J. W., Leslie K. B., Ziltener H. J., Schrader S. Autostimulatory mechanisms in myeloid leukemogenesis. J Cell Biochem. 1987 May;34(1):39–46. doi: 10.1002/jcb.240340106. [DOI] [PubMed] [Google Scholar]
- Sporn M. B., Roberts A. B. Autocrine growth factors and cancer. 1985 Feb 28-Mar 6Nature. 313(6005):745–747. doi: 10.1038/313745a0. [DOI] [PubMed] [Google Scholar]
- TILL J. E., McCULLOCH E. A. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res. 1961 Feb;14:213–222. [PubMed] [Google Scholar]
- Weaver S., Haigwood N. L., Hutchison C. A., 3rd, Edgell M. H. DNA fragments of the Mus musculus beta globin haplotypes Hbbs and Hbbd. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1385–1389. doi: 10.1073/pnas.76.3.1385. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Whitney J. B., 3rd Simplified typing of mouse hemoglobin (Hbb) phenotypes using cystamine. Biochem Genet. 1978 Aug;16(7-8):667–672. doi: 10.1007/BF00484723. [DOI] [PubMed] [Google Scholar]
- Wong P. M., Chung S. W., Nienhuis A. W. Retroviral transfer and expression of the interleukin-3 gene in hemopoietic cells. Genes Dev. 1987 Jun;1(4):358–365. doi: 10.1101/gad.1.4.358. [DOI] [PubMed] [Google Scholar]
- Wong P. M., Chung S. W., White J. S., Reicheld S. M., Patterson M., Clarke B. J., Chui D. H. Adult hemoglobins are synthesized in murine fetal hepatic erythropoietic cells. Blood. 1983 Dec;62(6):1280–1288. [PubMed] [Google Scholar]
- Wong P. M., Humphries R. K., Chen T. R., Eaves C. J. Evidence for a multistep pathogenesis in the generation of tumorigenic cell lines from hemopoietic colonies exposed to Abelson virus in vitro. Exp Hematol. 1987 Mar;15(3):280–287. [PubMed] [Google Scholar]
- 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]
- Yoshida K., Seki M., Hayata I., Niwa O., Tadokoro K., Tada N. Myeloproliferative disorder due to abnormal production of hematopoietic stimulators. Leuk Res. 1987;11(7):621–627. doi: 10.1016/0145-2126(87)90034-8. [DOI] [PubMed] [Google Scholar]
- Young D. C., Griffin J. D. Autocrine secretion of GM-CSF in acute myeloblastic leukemia. Blood. 1986 Nov;68(5):1178–1181. [PubMed] [Google Scholar]
- Young D. C., Wagner K., Griffin J. D. Constitutive expression of the granulocyte-macrophage colony-stimulating factor gene in acute myeloblastic leukemia. J Clin Invest. 1987 Jan;79(1):100–106. doi: 10.1172/JCI112769. [DOI] [PMC free article] [PubMed] [Google Scholar]