Induction of macrophage colony-stimulating factor-dependent growth and differentiation after introduction of the murine c-fms gene into FDC-P1 cells (original) (raw)

Abstract

A system has been established for analyzing the functions of the c-fms/macrophage colony-stimulating factor (M-CSF) receptor gene product in hematopoietic growth and differentiation. The murine c-fms gene was introduced into the factor-dependent murine hematopoietic cell line FDC-P1 by retroviral infection, and conversion to M-CSF-dependent growth was assayed in agar cultures. Expression of the c-fms gene in FDC-P1 cells, which normally do not express this gene, resulted in the conversion of resultant FD(c-fms) cells to M-CSF-dependent growth. Stimulation of FD(c-fms) cells by M-CSF led to the formation of colonies of altered morphology and produced reversible morphological changes suggestive of myeloid differentiation. M-CSF also induced expression of mature myeloid surface marker proteins in the FD(c-fms) cells. Neither multi-CSF nor granulocyte-macrophage CSF induced similar phenotypic changes but remained able to stimulate the proliferation of undifferentiated FD(c-fms) cells. These results indicate that the c-fms gene was expressed functionally in FDC-P1 cells and transmitted signals for growth. Also, the interaction of M-CSF with the c-fms gene product generated an additional signal for myeloid differentiation but did not irreversibly commit FD(c-fms) cells to terminal differentiation. This system can be used for molecular analysis of the growth- and differentiation-promoting activities of the c-fms proto-oncogene.

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Selected References

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  1. Austyn J. M., Gordon S. F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur J Immunol. 1981 Oct;11(10):805–815. doi: 10.1002/eji.1830111013. [DOI] [PubMed] [Google Scholar]
  2. Basch R. S., Berman J. W. Thy-1 determinants are present on many murine hematopoietic cells other than T cells. Eur J Immunol. 1982 May;12(5):359–364. doi: 10.1002/eji.1830120502. [DOI] [PubMed] [Google Scholar]
  3. Besmer P., Lader E., George P. C., Bergold P. J., Qiu F. H., Zuckerman E. E., Hardy W. D. A new acute transforming feline retrovirus with fms homology specifies a C-terminally truncated version of the c-fms protein that is different from SM-feline sarcoma virus v-fms protein. J Virol. 1986 Oct;60(1):194–203. doi: 10.1128/jvi.60.1.194-203.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bowtell D. D., Cory S., Johnson G. R., Gonda T. J. Comparison of expression in hemopoietic cells by retroviral vectors carrying two genes. J Virol. 1988 Jul;62(7):2464–2473. doi: 10.1128/jvi.62.7.2464-2473.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Burgess A. W., Metcalf D. Characterization of a serum factor stimulating the differentiation of myelomonocytic leukemic cells. Int J Cancer. 1980 Nov 15;26(5):647–654. doi: 10.1002/ijc.2910260517. [DOI] [PubMed] [Google Scholar]
  6. Byrne P. V., Guilbert L. J., Stanley E. R. Distribution of cells bearing receptors for a colony-stimulating factor (CSF-1) in murine tissues. J Cell Biol. 1981 Dec;91(3 Pt 1):848–853. doi: 10.1083/jcb.91.3.848. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Coussens L., Van Beveren C., Smith D., Chen E., Mitchell R. L., Isacke C. M., Verma I. M., Ullrich A. Structural alteration of viral homologue of receptor proto-oncogene fms at carboxyl terminus. Nature. 1986 Mar 20;320(6059):277–280. doi: 10.1038/320277a0. [DOI] [PubMed] [Google Scholar]
  8. Dexter T. M., Garland J., Scott D., Scolnick E., Metcalf D. Growth of factor-dependent hemopoietic precursor cell lines. J Exp Med. 1980 Oct 1;152(4):1036–1047. doi: 10.1084/jem.152.4.1036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Di Fiore P. P., Pierce J. H., Fleming T. P., Hazan R., Ullrich A., King C. R., Schlessinger J., Aaronson S. A. Overexpression of the human EGF receptor confers an EGF-dependent transformed phenotype to NIH 3T3 cells. Cell. 1987 Dec 24;51(6):1063–1070. doi: 10.1016/0092-8674(87)90592-7. [DOI] [PubMed] [Google Scholar]
  10. Di Fiore P. P., Pierce J. H., Kraus M. H., Segatto O., King C. R., Aaronson S. A. erbB-2 is a potent oncogene when overexpressed in NIH/3T3 cells. Science. 1987 Jul 10;237(4811):178–182. doi: 10.1126/science.2885917. [DOI] [PubMed] [Google Scholar]
  11. Downing J. R., Rettenmier C. W., Sherr C. J. Ligand-induced tyrosine kinase activity of the colony-stimulating factor 1 receptor in a murine macrophage cell line. Mol Cell Biol. 1988 Apr;8(4):1795–1799. doi: 10.1128/mcb.8.4.1795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Greaves M. F., Chan L. C., Furley A. J., Watt S. M., Molgaard H. V. Lineage promiscuity in hemopoietic differentiation and leukemia. Blood. 1986 Jan;67(1):1–11. [PubMed] [Google Scholar]
  13. Hampe A., Gobet M., Sherr C. J., Galibert F. Nucleotide sequence of the feline retroviral oncogene v-fms shows unexpected homology with oncogenes encoding tyrosine-specific protein kinases. Proc Natl Acad Sci U S A. 1984 Jan;81(1):85–89. doi: 10.1073/pnas.81.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hapel A. J., Warren H. S., Hume D. A. Different colony-stimulating factors are detected by the "interleukin-3"-dependent cell lines FDC-Pl and 32D cl-23. Blood. 1984 Oct;64(4):786–790. [PubMed] [Google Scholar]
  15. 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]
  16. Holmes K. L., Morse H. C., 3rd Murine hematopoietic cell surface antigen expression. Immunol Today. 1988 Nov;9(11):344–350. doi: 10.1016/0167-5699(88)91335-7. [DOI] [PubMed] [Google Scholar]
  17. Hudziak R. M., Schlessinger J., Ullrich A. Increased expression of the putative growth factor receptor p185HER2 causes transformation and tumorigenesis of NIH 3T3 cells. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7159–7163. doi: 10.1073/pnas.84.20.7159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hynes R. O. Integrins: a family of cell surface receptors. Cell. 1987 Feb 27;48(4):549–554. doi: 10.1016/0092-8674(87)90233-9. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Lee S. H., Starkey P. M., Gordon S. Quantitative analysis of total macrophage content in adult mouse tissues. Immunochemical studies with monoclonal antibody F4/80. J Exp Med. 1985 Mar 1;161(3):475–489. doi: 10.1084/jem.161.3.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lyman S. D., Park L., Rohrschneider L. R. Colony stimulating factor-1 induced growth stimulation of v-fms transformed fibroblasts. Oncogene. 1988 Oct;3(4):391–395. [PubMed] [Google Scholar]
  22. Lyman S. D., Rohrschneider L. R. Analysis of functional domains of the v-fms-encoded protein of Susan McDonough strain feline sarcoma virus by linker insertion mutagenesis. Mol Cell Biol. 1987 Sep;7(9):3287–3296. doi: 10.1128/mcb.7.9.3287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Muller-Sieburg C. E., Whitlock C. A., Weissman I. L. Isolation of two early B lymphocyte progenitors from mouse marrow: a committed pre-pre-B cell and a clonogenic Thy-1-lo hematopoietic stem cell. Cell. 1986 Feb 28;44(4):653–662. doi: 10.1016/0092-8674(86)90274-6. [DOI] [PubMed] [Google Scholar]
  24. Nichols E. J., Manger R., Hakomori S., Herscovics A., Rohrschneider L. R. Transformation by the v-fms oncogene product: role of glycosylational processing and cell surface expression. Mol Cell Biol. 1985 Dec;5(12):3467–3475. doi: 10.1128/mcb.5.12.3467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pierce J. H., Ruggiero M., Fleming T. P., Di Fiore P. P., Greenberger J. S., Varticovski L., Schlessinger J., Rovera G., Aaronson S. A. Signal transduction through the EGF receptor transfected in IL-3-dependent hematopoietic cells. Science. 1988 Feb 5;239(4840):628–631. doi: 10.1126/science.3257584. [DOI] [PubMed] [Google Scholar]
  26. REIF A. E., ALLEN J. M. SPECIFICITY OF ISOANTISERA AGAINST LEUKAEMIC AND THYMIC LYMPHOCYTES. Nature. 1963 Dec 28;200:1332–1333. doi: 10.1038/2001332b0. [DOI] [PubMed] [Google Scholar]
  27. Regenstreif L. J., Rossant J. Expression of the c-fms proto-oncogene and of the cytokine, CSF-1, during mouse embryogenesis. Dev Biol. 1989 May;133(1):284–294. doi: 10.1016/0012-1606(89)90319-9. [DOI] [PubMed] [Google Scholar]
  28. Rohrschneider L. R., Rothwell V. M., Nicola N. A. Transformation of murine fibroblasts by a retrovirus encoding the murine c-fms proto-oncogene. Oncogene. 1989 Aug;4(8):1015–1022. [PubMed] [Google Scholar]
  29. Rothwell V. M., Rohrschneider L. R. Murine c-fms cDNA: cloning, sequence analysis and retroviral expression. Oncogene Res. 1987 Sep-Oct;1(4):311–324. [PubMed] [Google Scholar]
  30. Sanchez-Madrid F., Simon P., Thompson S., Springer T. A. Mapping of antigenic and functional epitopes on the alpha- and beta-subunits of two related mouse glycoproteins involved in cell interactions, LFA-1 and Mac-1. J Exp Med. 1983 Aug 1;158(2):586–602. doi: 10.1084/jem.158.2.586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sarma P. S., Sharar A. L., McDonough S. The SM strain of feline sarcoma virus. Biologic and antigenic characterization of virus. Proc Soc Exp Biol Med. 1972 Sep;140(4):1365–1368. doi: 10.3181/00379727-140-36675. [DOI] [PubMed] [Google Scholar]
  32. Sherr C. J., Rettenmier C. W., Sacca R., Roussel M. F., Look A. T., Stanley E. R. The c-fms proto-oncogene product is related to the receptor for the mononuclear phagocyte growth factor, CSF-1. Cell. 1985 Jul;41(3):665–676. doi: 10.1016/s0092-8674(85)80047-7. [DOI] [PubMed] [Google Scholar]
  33. Smith L. J., Curtis J. E., Messner H. A., Senn J. S., Furthmayr H., McCulloch E. A. Lineage infidelity in acute leukemia. Blood. 1983 Jun;61(6):1138–1145. [PubMed] [Google Scholar]
  34. Stanley E. R., Guilbert L. J. Methods for the purification, assay, characterization and target cell binding of a colony stimulating factor (CSF-1). J Immunol Methods. 1981;42(3):253–284. doi: 10.1016/0022-1759(81)90156-3. [DOI] [PubMed] [Google Scholar]
  35. Stanley E. R., Guilbert L. J., Tushinski R. J., Bartelmez S. H. CSF-1--a mononuclear phagocyte lineage-specific hemopoietic growth factor. J Cell Biochem. 1983;21(2):151–159. doi: 10.1002/jcb.240210206. [DOI] [PubMed] [Google Scholar]
  36. Stern D. F., Hare D. L., Cecchini M. A., Weinberg R. A. Construction of a novel oncogene based on synthetic sequences encoding epidermal growth factor. Science. 1987 Jan 16;235(4786):321–324. doi: 10.1126/science.3492043. [DOI] [PubMed] [Google Scholar]
  37. Taylor G. R., Reedijk M., Rothwell V., Rohrschneider L., Pawson T. The unique insert of cellular and viral fms protein tyrosine kinase domains is dispensable for enzymatic and transforming activities. EMBO J. 1989 Jul;8(7):2029–2037. doi: 10.1002/j.1460-2075.1989.tb03611.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tushinski R. J., Oliver I. T., Guilbert L. J., Tynan P. W., Warner J. R., Stanley E. R. Survival of mononuclear phagocytes depends on a lineage-specific growth factor that the differentiated cells selectively destroy. Cell. 1982 Jan;28(1):71–81. doi: 10.1016/0092-8674(82)90376-2. [DOI] [PubMed] [Google Scholar]
  39. Velu T. J., Beguinot L., Vass W. C., Willingham M. C., Merlino G. T., Pastan I., Lowy D. R. Epidermal-growth-factor-dependent transformation by a human EGF receptor proto-oncogene. Science. 1987 Dec 4;238(4832):1408–1410. doi: 10.1126/science.3500513. [DOI] [PubMed] [Google Scholar]
  40. Walker F., Nicola N. A., Metcalf D., Burgess A. W. Hierarchical down-modulation of hemopoietic growth factor receptors. Cell. 1985 Nov;43(1):269–276. doi: 10.1016/0092-8674(85)90032-7. [DOI] [PubMed] [Google Scholar]
  41. Wheeler E. F., Askew D., May S., Ihle J. N., Sherr C. J. The v-fms oncogene induces factor-independent growth and transformation of the interleukin-3-dependent myeloid cell line FDC-P1. Mol Cell Biol. 1987 May;7(5):1673–1680. doi: 10.1128/mcb.7.5.1673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wheeler E. F., Roussel M. F., Hampe A., Walker M. H., Fried V. A., Look A. T., Rettenmier C. W., Sherr C. J. The amino-terminal domain of the v-fms oncogene product includes a functional signal peptide that directs synthesis of a transforming glycoprotein in the absence of feline leukemia virus gag sequences. J Virol. 1986 Aug;59(2):224–233. doi: 10.1128/jvi.59.2.224-233.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Williams L. T. Signal transduction by the platelet-derived growth factor receptor. Science. 1989 Mar 24;243(4898):1564–1570. doi: 10.1126/science.2538922. [DOI] [PubMed] [Google Scholar]
  44. Woolford J., McAuliffe A., Rohrschneider L. R. Activation of the feline c-fms proto-oncogene: multiple alterations are required to generate a fully transformed phenotype. Cell. 1988 Dec 23;55(6):965–977. doi: 10.1016/0092-8674(88)90242-5. [DOI] [PubMed] [Google Scholar]
  45. Woolford J., Rothwell V., Rohrschneider L. Characterization of the human c-fms gene product and its expression in cells of the monocyte-macrophage lineage. Mol Cell Biol. 1985 Dec;5(12):3458–3466. doi: 10.1128/mcb.5.12.3458. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. von Rüden T., Wagner E. F. Expression of functional human EGF receptor on murine bone marrow cells. EMBO J. 1988 Sep;7(9):2749–2756. doi: 10.1002/j.1460-2075.1988.tb03129.x. [DOI] [PMC free article] [PubMed] [Google Scholar]