Skip to main content
SpringerLink
Log in

Transcriptional regulation of c-fms gene expression

  • Original Article
  • Published:
Cell Biochemistry and Biophysics Aims and scope Submit manuscript

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

References

  1. Crocker, P. R. and Gordon, S. (1985) Isolation and characterization of resident stromal macrophages and haemopoietic cell clusters from mouse bone marrow. J. Exp. Med. 162, 993–1014.

    Article  PubMed  CAS  Google Scholar 

  2. Denkers, I. A. M., Beelen, R. H. J., Ossenkoppele, G. J., and Langenhuysen, M. M. A. C. (1992) Differences of cellular composition and adhension molecule expression in “leukemic” as compared with “normal” human long-term bone marrow cultures. Ann. Hematol. 64, 210–216.

    Article  PubMed  CAS  Google Scholar 

  3. Fibbe, W. E., van Damme, J., Billiau, A., Voogt, P. J., Duinkerken, N., Kluck, P. M., and Falkenburg, J. H. (1986) Interleukin-1 (22-K factor) induces release of granulocyte-macrophage colony-stimulating activity from human mononuclear phagocytes. Blood 68, 1316–1321.

    PubMed  CAS  Google Scholar 

  4. Vogt, C., Pentz, S., and Rich, I. N. (1989) A role for the macrophage in normal hemopoiesis: III. In vitro and in vivo erythropoietin gene expression in macrophages detected by in situ hybridization. Exp. Hematol. 17, 391–397.

    PubMed  CAS  Google Scholar 

  5. van den Heuvel, R., Mathieu, E., Schoeters, G., Leppens, H., and Vanderborght, O. (1991) Stromal cells from murine developing hemopoietic organs: comparison of colony-forming unit of fibroblasts and long-term cultures. Int. J. Dev. Biol. 35, 33–41.

    PubMed  Google Scholar 

  6. Metcalf, D. (1985) Multi-CSF-dependent colony formation by cells of a murine hemopoietic cell line: specificity and action of multi-CSF. Blood 65, 357–362.

    PubMed  CAS  Google Scholar 

  7. Metcalf, D. (1989) The molecular control of cell division, differentiation, commitment and motivation in haemopoietic cells. Nature 339, 27–30.

    Article  PubMed  CAS  Google Scholar 

  8. Dinarello, C. A. (1994) The biological properties of interleukin-1. Eur. Cytokine Netw. 5, 517–531.

    PubMed  CAS  Google Scholar 

  9. Broxmeyer, H. E., Maze, R., Miyazawa, K., Carow, C., Hendrie, P. C., Cooper, S., Hangoc, G., Vadhan-Raj, S., and Lu, L. (1991) The kit receptor and its ligand, steel factor, as regulators of hemopoiesis. Cancer Cells 3, 480–487.

    PubMed  CAS  Google Scholar 

  10. Breen, F. N., Hume, D. A., and Weidemann, M. J. (1990) The effects of interleukin 3 (IL3) on cells responsive to macrophage colony-stimulating factor (CSF-1) in liquid bone marrow culture. Br. J. Haematol. 74, 138–147.

    PubMed  CAS  Google Scholar 

  11. Breen, F. N., Hume, D. A., and Weidemann, M. J. (1991) Interactions between granulocyte-macrophage colony-stimulating factor, macrophage colony-stimulating factor and gamma interferon lead to enhanced proliferation of murine macrophage progenitor cells. J. Immunol. 147, 1542–1547.

    PubMed  CAS  Google Scholar 

  12. Bartelmez, S. H., Bradley, T. R., Bertoncello, I., Mochizuki, D. Y., Tushinski, R. J., Stanley, E. R., Hapel, A. J., Young, I. G., Kriegler, A. B., and Hodgson, G. S. (1989) Interleukin 1 plus interleukin 3 plus colony-stimulating factor 1 are essential for clonal proliferation of primitive myeloid bone marrow cells. Exp. Hematol. 17, 240–245.

    PubMed  CAS  Google Scholar 

  13. Warren, M. K., and Vogel, S. N. (1985) Bone marrow-derived macrophages: development and regulation of differentiation markers by colony-stimulating factor and interferons. J. Immunol. 134, 982–989.

    PubMed  CAS  Google Scholar 

  14. Roth, P., and Stanley, E. R. (1992) The biology of CSF-1 and its receptor. Curr. Top. Microbiol. Immunol. 181, 141–167.

    PubMed  CAS  Google Scholar 

  15. Wiktor-Jedrzejczak, W., Bartocci, A., Ferrante, A. J., Ahmed, A. A., Sell, K. W., Pollard, J. W., and Stanley, E. R. (1990) Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc. Natl. Acad. Sci. USA 87, 4828–4832.

    Article  PubMed  CAS  Google Scholar 

  16. Yoshida, H., Hayashi, S., Kunisada, T., Ogawa, M., Nishikawa, S., Okamura, H., Sudo, T., Shultz, L. D., and Nishikawa, S. (1990) The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 345, 442–444.

    Article  PubMed  CAS  Google Scholar 

  17. Felix, R., Cecchini, M. G., Hofstetter, W., Elford, P. R., Stutzer, A., and Fleisch, H. (1990) Impairment of macrophage colony-stimulating factor production and lack of resident bone marrow macrophages in the osteopetrotic op/op mouse. J. Bone Miner. Res. 5, 781–789.

    Article  PubMed  CAS  Google Scholar 

  18. Wiktor-Jedrzejczak, W., Ratajczak, M. Z., Ptasznik, A., Sell, K. W., Ahmed-Ansari, A., and Ostertag, W. (1992) CSF-1 deficiency in the op/op mouse has differential effects on macrophage populations and differentiation stages. Exp. Hematol. 20, 1004–1010.

    PubMed  CAS  Google Scholar 

  19. Cecchini, M. G., Dominguez, M. G., Mocci, S., Wetterwald, A., Felix, R., Fleisch, H., Chisholm, O., Hofstetter, W., Pollard, J. W., and Stanley, E. R. (1994) Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development 120, 1357–1372.

    PubMed  CAS  Google Scholar 

  20. Begg, S. K., Radley, J. M., Pollard, J. W., Chisholm, O. T., Stanley, E. R., and Bertoncello, I. (1993) Delayed hematopoietic development in osteopetrotic (op/op) mice. J. Exp. Med. 177, 237–242.

    Article  PubMed  CAS  Google Scholar 

  21. Witmer-Pack, M. D., Hughes, D. A., Schuler, G., Lawson, L., McWilliam, A., Inaba, K., Steinman, R. M., and Gordon, S. (1993) Identification of macrophages and dendritic cells in the osteopetrotic (op/op) mouse. J. Cell. Sci. 104, 1021–1029.

    PubMed  Google Scholar 

  22. Hume, D. A., Monkley, S. J., and Wainwright, B. J. (1995) Detection of c-fms protooncogene in early mouse embryos by whole mount in situ hybridization indicates roles for macrophages in tissue remodelling. Br. J. Haematol. 90, 939–942.

    PubMed  CAS  Google Scholar 

  23. Takatsuka, H., Umezu, H., Hasegawa, G., Usuda, H., Ebe, Y., Naito, M., and Shultz, L. D. (1998) Bone remodeling and macrophage differentiation in osteopetrosis (op) mutant mice defective in the production of macrophage colony-stimulating factor. J. Submicrosc. Cytol. Pathol. 30, 239–247.

    PubMed  CAS  Google Scholar 

  24. Niida, S., Kaku, M., Amano, H., Yoshida, H., Kataoka, H., Nishikawa, S., Tanne, K., Maeda, N., Nishikawa, S., and Kodama, H. (1999) Vascular endothelial growth factor can substitute for macrophage colony-stimulating factor in the support of osteoclastic bone resorption. J. Exp. Med. 190, 293–298.

    Article  PubMed  CAS  Google Scholar 

  25. Reddy, M. A., Yang, B. S., Xie, Y., Barnett, C. J., Ross, I. L., Sweet, M. J., Hume, D. A., and Ostrowski, M. C. (1994) Opposing actions of c-ets/PU.1 and c-myb protooncogene products in regulating the macrophage-specific promoters of the human and mouse colony-stimulating factor-1 receptor (c-fms) genes. J. Exp. Med. 180, 2309–2319.

    Article  PubMed  CAS  Google Scholar 

  26. Weber, B., Horiguchi, J., Luebbers, R., Sherman, M., and Kufe, D. (1989) Posttranscriptional stabilization of c-fms mRNA by a labile protein during human monocytic differentiation. Mol. Cell. Biol. 9, 769–775.

    PubMed  CAS  Google Scholar 

  27. Gliniak, B. C. and Rohrschneider, L. R. (1990) Expression of the M-CSF receptor is controlled posttranscriptionally by the dominant actions of GM-CSF or multi-CSF. Cell 63, 1073–1083.

    Article  PubMed  CAS  Google Scholar 

  28. Gusella, G. L., Ayroldi, E., Espinoza-Delgado, I., and Varesio, L. (1990) Lipopolysaccharide, but not IFN-gamma, down-regulates c-fms mRNA proto-oncogene expression in murine macrophages. J. Immunol. 144, 3574–3580.

    PubMed  CAS  Google Scholar 

  29. Stone, R. M., Imamura, K., Datta, R., Sherman, M. L., and Kufe, D. W. (1990) Inhibition of phorbol ester-induced monocytic differentiation and c-fms gene expression by dexamethasone: potential involvement of arachidonic acid metabolites. Blood 76, 1225–1232.

    PubMed  CAS  Google Scholar 

  30. Sapi, E., Flick, M. B., Gilmore-Hebert, M., Rodov, S., and Kacinski, B. M. (1995) Transcriptional regulation of the c-fms (CSF-1R) proto-oncogene in human breast carcinoma cells by glucocorticoids. Oncogene 10, 529–542.

    PubMed  CAS  Google Scholar 

  31. Chambers, S. K., Gilmore-Hebert, M., Wang, Y., Rodov, S., Benz, E. J. Jr., and Kacinski, B. M. (1993) Posttranscriptional regulation of colony-stimulating factor-1 (CSF-1) and CSF-1 receptor gene expression during inhibition of phorbol-ester-induced monocytic differentiation by dexamethasone and cyclosporin A: potential involvement of a destabilizing protein. Exp. Hematol. 21, 1328–1334.

    PubMed  CAS  Google Scholar 

  32. Myers, M. J., Ghildyal, N., and Schook, L. B. (1995) Endotoxin and interferon-gamma differentially regulate the transcriptional levels of proto-oncogenes and cytokine genes during the differentiation of colony-stimulating factor type-1-derived macrophages. Immunology 85, 318–324.

    PubMed  CAS  Google Scholar 

  33. Biskobing, D. M., Fan, D., and Rubin, J. (1997) c-fms mRNA is regulated posttranscriptionally by 1,25(OH)2D3 in HL-60 cells. Calcif. Tissue Int. 61, 205–209.

    Article  PubMed  CAS  Google Scholar 

  34. Arceci, R. J., Pampfer, S., and Pollard, J. W. (1992) Expression of CSF-1 / c-fms and SF/c-kit mRNA during preimplantation mouse development. Dev. Biol. 151, 1–8.

    Article  PubMed  CAS  Google Scholar 

  35. Regenstreif, L. J., and Rossant, J. (1989) Expression of the c-fms proto-oncogene and of the cytokine, CSF-1, during mouse embryogenesis. Dev. Biol. 133, 284–294.

    Article  PubMed  CAS  Google Scholar 

  36. Arceci, R. J., Shanahan, F., Stanley, E. R., and Pollard, J. W. (1989) Temporal expression and location of colony-stimulating factor 1 (CSF-1) and its receptor in the female reproductive tract are consistent with CSF-1-regulated placental development. Proc. Natl. Acad. Sci. USA 86, 8818–8822.

    Article  PubMed  CAS  Google Scholar 

  37. Azuma, C., Saji, F., Kimura, T., Tokugawa, Y., Takemura, M., Miki, M., Ono, M., and Tanizawa, O. (1991) The gene expression of macrophage colony-stimulating factor (MCSF) and MCSF receptor in the human myometrium during pregnancy: regulation by sex steroid hormone. J. Steroid Biochem. Mol. Biol. 39, 883–888.

    Article  PubMed  CAS  Google Scholar 

  38. Azuma, C., Saji, F., Kimura, T., Tokugawa, Y., Takemura, M., Samejima, Y., and Tanizawa, O. (1990) Steroid hormones induce macrophage colony-stimulating factor (MCSF) and MCSF receptor mRNAs in the human endometrium. J. Mol. Endocrinol. 5, 103–108.

    Article  PubMed  CAS  Google Scholar 

  39. Pampfer, S., Daiter, E., Barad, D., and Poliard, J. W. (1992) Expression of the colony-stimulating factor-1 receptor (c-fms proto-oncogene product) in the human uterus and placenta. Biol. Reprod. 46, 48–57.

    Article  PubMed  CAS  Google Scholar 

  40. Jokhi, P. P., Chumbley, G., King, A., Gardner, L., and Loke, Y. W. (1993) Expression of the colony stimulating factor-1 receptor (c-fms product) by cells at the human uteroplacental interface. Lab. Invest. 68, 308–320.

    PubMed  CAS  Google Scholar 

  41. Saji, F., Azuma, C., Kimura, T., Koyama, M., Ohashi, K., and Tanizawa, O. (1990) Gene expression of macrophage colony-stimulating factor and its receptor in human placenta and decidua. Am. J. Reprod. Immunol. 24, 99–104.

    PubMed  CAS  Google Scholar 

  42. Marks, S. C. Jr., and Lane, P. W. (1976) Osteopetrosis, a new recessive skeletal mutation on chromosome 12 of the mouse. J. Hered. 67, 11–18.

    PubMed  Google Scholar 

  43. Pollard, J. W., Hunt, J. S., Wiktor-Jedrzejczak, W., and Stanley, E. R. (1991) A pregnancy defect in the osteopetrotic (op/op) mouse demonstrates the requirement for CSF-1 in female fertility. Dev. Biol. 148, 273–283.

    Article  PubMed  CAS  Google Scholar 

  44. Lichanska, A. M., Browne, C. M., Henkel, G. W., Murphy, K. M., Ostrowski, M. C., McKercher, S. R., Maki, R. A., and Hume, D. A. (1999) Differentiation of the embryonic mononuclear phagocyte system. The role of transcription factor PU.1. Blood, in press.

  45. Morris, L., Graham, C. F., and Gordon, S. (1991) Macrophages in the haemopoietic and other tissues of the developing mouse detected by monoclonal antibody F4/80. Development 112, 517–526.

    PubMed  CAS  Google Scholar 

  46. Aperlo, C., Sevilla, L., Guerin, S., Pognonec, P., and Boulukos, K. E. (1998) Synergistic effects of colony-stimulating factor 1 and leukemia inhibitory factor in inducing early myeloid cell differentiation. Cell Growth Differ. 9, 929–937.

    PubMed  CAS  Google Scholar 

  47. Hass, R., Prudovsky, I., and Kruhoffer, M. (1997) Differential effects of phorbol ester on signaling and gene expression in human leukemia cells. Leuk. Res. 21, 589–594.

    Article  PubMed  CAS  Google Scholar 

  48. Byrne, P. V., Guilbert, L. J., and Stanley, E. R. (1981) Distribution of cells bearing receptors for a colony-stimulating factor (CSF-1) in murine tissues. J. Cell. Biol. 91, 848–853.

    Article  PubMed  CAS  Google Scholar 

  49. Guilbert, L. J. and Stanley, E. R. (1980) Specific interaction of murine colony-stimulating factor with mononuclear phagocytic cells. J. Cell. Biol. 85, 153–159.

    Article  PubMed  CAS  Google Scholar 

  50. Cohen, P. E., Nishimura, K., Zhu, L., and Pollard, J. W. (1999) Macrophages: important accessory cells for reproductive function. J. Leukoc. Biol. 66, 765–772.

    PubMed  CAS  Google Scholar 

  51. Hofstetter, W., Wetterwald, A., Cecchini, M. C., Felix, R., Fleisch, H., and Mueller, C. (1992) Detection of transcripts for the receptor for macrophage colony-stimulating factor, c-fms, in murine osteoclasts. Proc. Natl. Acad. Sci. USA 89, 9637–9641.

    Article  PubMed  CAS  Google Scholar 

  52. Yang, S., Zhang, Y., Rodriguiz, R. M., Ries, W. L., and Key, L. L. Jr. (1996) Functions of the M-CSF receptor on osteoclasts. Bone 18, 355–360.

    Article  PubMed  CAS  Google Scholar 

  53. Tanaka, S., Takahashi, N., Udagawa, N., Tamura, T., Akatsu, T., Stanley, E. R., Kurokawa, T., and Suda, T. (1993) Macrophage colony-stimulating factor is indispensable for both proliferation and differentiation of osteoclast progenitors. J. Clin. Invest. 91, 257–263.

    PubMed  CAS  Google Scholar 

  54. Cecchini, M. G., Hofstetter, W., Halasy, J., Wetterwald, A., and Felix, R. (1997) Role of CSF-1 in bone and bone marrow development. Mol. Reprod. Dev. 46, 75–83.

    Article  PubMed  CAS  Google Scholar 

  55. Felix, R., Hofstetter, W., Wetterwald, A., Cecchini, M. G., and Fleisch, H. (1994) Role of colony-stimulating factor-1 in bone metabolism. J. Cell. Biochem. 55, 340–349.

    Article  PubMed  CAS  Google Scholar 

  56. Quinn, J. M., Elliott, J., Gillespie, M. T., and Martin, T. J. (1998) A combination of osteoclast differentiation factor and macrophage-colony stimulating factor is sufficient for both human and mouse osteoclast formation in vitro. Endocrinology 139, 4424–4427.

    Article  PubMed  CAS  Google Scholar 

  57. Nagai, M. and Sato, N. (1999) Reciprocal gene expression of osteoclastogenesis inhibitory factor and osteoclast differentiation factor regulates osteoclast formation. Biochem. Biophys. Res. Commun. 257, 719–723.

    Article  PubMed  CAS  Google Scholar 

  58. Edwards, M., Sarma, U., and Flanagan, A. M. (1998) Macrophage colony-stimulating factor increases bone resorption by osteoclasts disaggregated from human fetal long bones. Bone 22, 325–329.

    Article  PubMed  CAS  Google Scholar 

  59. Baker, A. H., Ridge, S. A., Hoy, T., Cachia, P. G., Culligan, D., Baines, P., Whittaker, J. A., Jacobs, A., and Padua, R. A. (1993) Expression of the colony-stimulating factor 1 receptor in B lymphocytes. Oncogene 8, 371–378.

    PubMed  CAS  Google Scholar 

  60. Murase, S. and Hayashi, Y. (1998) Expression pattern and neurotrophic role of the c-fms proto-oncogene M-CSF receptor in rodent Purkinje cells. J. Neurosci. 18, 10,481–10,492.

    CAS  Google Scholar 

  61. Perry, V. H., Hume, D. A., and Gordon, S. (1985) Immunohistochemical localisation of macrophages and microglia in the developing mouse brain. Neuroscience 173, 313–326.

    Article  Google Scholar 

  62. Sawada, M., Suzumura, A., Yamamoto, H., and Marunouchi, T. (1990) Activation and proliferation of the isolated microglia by colony stimulating factor-1 and possible involvement of protein kinase C. Brain Res. 509, 119–124.

    Article  PubMed  CAS  Google Scholar 

  63. Sawada, M., Itoh, Y., Suzumura, A., and Marunouchi, T. (1993) Expression of cytokine receptors in cultured neuronal and glial cells. Neurosci. Lett. 160, 131–134.

    Article  PubMed  CAS  Google Scholar 

  64. Sapi, E., Flick, M. B., Rodov, S., Carter, D., and Kacinski, B. M. (1998) Expression of CSF-I and CSF-I receptor by normal lactating mammary epithelial cells. J. Soc. Gynecol. Investig. 5, 94–101.

    Article  PubMed  CAS  Google Scholar 

  65. Pollard, J. W. and Hennighausen, L. (1994) Colony stimulating factor 1 is required for mammary gland development during pregnancy. Proc. Natl. Acad. Sci. USA 91, 9312–9316.

    Article  PubMed  CAS  Google Scholar 

  66. Rambaldi, A., Wakamiya, N., Vellenga, E., Horiguchi, J., Warren, M. K., Kufe, D., and Griffin, J. D. (1988) Expression of the macrophage colony-stimulating factor and c-fms gene in human acute myeloblastic leukemia cells. J. Clin. Invest. 81, 1030–1035.

    Article  PubMed  CAS  Google Scholar 

  67. Kacinski, B. M., Carter, D., Mittal, K., Yee, L. D., Scata, K. A., Donofrio, L., Chambers, S. K., Wang, K. I., Yang-Feng, T., Rohrschneider, L. R., and Rothwell, V. M. (1990) Ovarian adenocarcinomas express fms-complementary transcripts and fms antigen, often with coexpression of CSF-1. Am. J. Pathol. 137, 135–147.

    PubMed  CAS  Google Scholar 

  68. Kacinski, B. M., Scata, K. A., Carter, D., Yee, L. D., Sapi, E., King, B. L., Chambers, S. K., Jones, M. A., Pirro, M. H., Stanley, E. R., and Rohrschneider, L. R. (1991) Fms (CSF-1 receptor) and CSF-1 transcripts and protein are expressed by human breast carcinomas in vivo and in vitro. Oncogene 6, 941–952.

    PubMed  CAS  Google Scholar 

  69. Paietta, E., Racezskis, J., Stanley, E. R., Andreeff, M., Papenhausen, P., and Wiernik, P. (1990) Expression of the macrophage growth factor, CSF-1 and its receptor c-fms by a Hodgkin’s disease-derived cell line and its variants. Cancer Res. 50, 2049–2055.

    PubMed  CAS  Google Scholar 

  70. Baiocchi, G., Kavanagh, J. J., Talpaz, M., Wharton, J. T., Gutterman, J. U., and Kurzrock, R. (1991) Expression of the macrophage colony-stimulating factor and its receptor in gynecologic malignancies. Cancer 67, 990–996.

    Article  PubMed  CAS  Google Scholar 

  71. Storga, D., Pecina-Slaus, N., Pavelic, J., Pavelic, Z. P., and Pavelic, K. (1992) c-fms is present in primary tumours as well as in their metastases in bone marrow. Int. J. Exp. Pathol. 73, 527–533.

    PubMed  CAS  Google Scholar 

  72. Leiserowitz, G. S., Harris, S. A., Subramaniam, M., Keeney, G. L., Podratz, K. C., and Spelsberg, T. C. (1993) The proto-oncogene c-fms is overexpressed in endometrial cancer. Gynecol Oncol. 49, 190–196.

    Article  PubMed  CAS  Google Scholar 

  73. Till, K. J., Lopez, A., Slupsky, J., and Cawley, J. C. (1993) C-fms protein expression by B-cells, with particular reference to the hairy cells of hairy-cell leukaemia. Br. J. Haematol. 83, 223–231.

    PubMed  CAS  Google Scholar 

  74. Burthem, J., Baker, P. K., Hunt, J. A., and Cawley, J. C. (1994) The function of c-fms in hairy-cell leukemia: macrophage colony-stimulating factor stimulates hairy-cell movement. Blood 83, 1381–1389.

    PubMed  CAS  Google Scholar 

  75. Keshava, N., Gubba, S., and Tekmal, R. R. (1999) Overexpression of macrophage colony-stimulating factor (CSF-1) and its receptor, c-fms, in normal ovarian granulosa cells leads to cell proliferation and tumorigenesis. J. Soc. Gynecol. Invest. 6, 41–49.

    Article  CAS  Google Scholar 

  76. Tang, R., Beuvon, F., Ojeda, M., Mosseri, V., Pouillart, P., and Scholl, S. (1992) M-CSF (monocyte colony stimulating factor) and M-CSF receptor expression by breast tumour cells: M-CSF mediated recruitment of tumour infiltrating monocytes? J. Cell. Biochem. 50, 350–356.

    Article  PubMed  CAS  Google Scholar 

  77. Scholl, S. M., Pallud, C., Beuvon, F., Hacene, K., Stanley, E. R., Rohrschneider, L., Tang, R., Pouillart, P., and Lidereau, R. (1994) Anticolony-stimulating factor-1 antibody staining in primary breast adenocarcinomas correlates with marked inflammatory cell infiltrates and prognosis. J. Natl. Cancer Inst. 86, 120–126.

    Article  PubMed  CAS  Google Scholar 

  78. Bruckner, A., Filderman, A. E., Kirchheimer, J. C., Binder, B. R., and Remold, H. G. (1992) Endogenous receptor-bound urokinase mediates tissue invasion of the human lung carcinoma cell lines A549 and Calu-1. Cancer Res. 52, 3043–3047.

    PubMed  CAS  Google Scholar 

  79. Filderman, A. E., Bruckner, A., Kacinski, B. M., Deng, N., and Remold, H. G. (1992) Macrophage colony-stimulating factor (CSF-1) enhances invasiveness in CSF-1 receptor-positive carcinoma cell lines. Cancer Res. 52, 3661–3666.

    PubMed  CAS  Google Scholar 

  80. Rettenmier, C. W., Roussel, M. F., Ashmun, R. A., Ralph, P., Price, K., and Sherr, C. J. (1987) Synthesis of membrane-bound colony-stimulating factor 1 (CSF-1) and downmodulation of CSF-1 receptor in NIH3T3 cells transformed by cotransfection of the human CSF-1 and c-fms (CSF-1 receptor) genes. Mol. Cell. Biol. 7, 2378–2387.

    PubMed  CAS  Google Scholar 

  81. Roussel, M. F., Dull, T. J., Rettenmier, C. W., Ralph, P., Ullrich, A., and Sherr, C. J. (1987) Transforming potential of the c-fms proto-oncogene (CSF-1 receptor). Nature. 325, 549–552.

    Article  PubMed  CAS  Google Scholar 

  82. van der Geer, P. and Hunter, T. (1993) Mutation of Tyr697, a GRB2-binding site, and Tyr721, a PI 3-kinase binding site, abrogates signal transduction by the murine CSF-1 receptor expressed in Rat-2 fibroblasts. EMBO J. 12, 5161–5172.

    PubMed  Google Scholar 

  83. Favot, P., Xie, Y., and Hume, D. A. (1995) Regulation of the c-fms promoter in murine tumour cell lines. Oncogene 11, 1371–1381.

    PubMed  CAS  Google Scholar 

  84. Roberts, W. M., Shapiro, L. H., Ashmun, R. A., and Look, A. T. (1992) Transcription of the human colony-stimulating factor-1 receptor gene is regulated by separate tissue-specific promoters. Blood 79, 586–593.

    PubMed  CAS  Google Scholar 

  85. Xie, Y., Favot, P., Dunn, T. L., Cassady, A. I., and Hume, D. A. (1993) Expression of mRNA encoding the macrophage colony-stimulating factor receptor (c-fms) is controlled by aconstitutive promoter and tissue-specific transcription elongation. Mol. Cell. Biol. 13, 3191–3201.

    Google Scholar 

  86. Visvader, J. and Verma, I. M. (1989) Differential transcription of exon 1 of the human c-fms gene in placental trophoblasts and monocytes. Mol. Cell. Biol. 9, 1336–1341.

    PubMed  CAS  Google Scholar 

  87. Sapi, E. and Kacinski, B. M. (1999) The role of CSF-1 in normal and neoplastic breast physiology. Proc. Soc. Exp. Biol. Med. 220, 1–8.

    Article  PubMed  CAS  Google Scholar 

  88. Sapi, E., Flick, M. B., and Kacinski, B. M. (1994) The first intron of human c-fms proto-oncogene contains a processed pseudogene (RPL7P) for ribosomal protein L7. Genomics 22, 641–645.

    Article  PubMed  CAS  Google Scholar 

  89. Zhang, D. E., Hetherington, C. J., Chen, H. M., and Tenen, D. G. (1994) The macrophage transcription factor PU.1 directs tissue-specific expression of the macrophage colony-stimulating factor receptor. Mol. Cell. Biol. 14, 373–381.

    PubMed  CAS  Google Scholar 

  90. Ross, I. L., Dunn, T. L., Xie, Y., Roy, S., Barnett, C. J., and Hume, D. A. (1994) Comparison of the expression and function of the transcription factor PU.1 (Spi-1 proto-oncogene) between murine macrophages and B lymphocytes. Oncogene 9, 121–132.

    PubMed  CAS  Google Scholar 

  91. Ross, I. L., Xie, Y., Ostrowski, M. C., and Hume, D. A. (1998) Interaction between PU.1 and another Ets family transcription factor promotes macrophage-specific basal transcription initiation. J. Biol. Chem. 273, 6662–6669.

    Article  PubMed  CAS  Google Scholar 

  92. Helftenbein, G., Krusekopf, K., Just, U., Cross, M., Ostertag, W., Niemann, H., and Tamura, T. (1996) Transcriptional regulation of the c-fms proto-oncogene mediated by granulocyte/macrophage colony-stimulating factor (GM-CSF) in murine cell lines. Oncogene 12, 931–935.

    PubMed  CAS  Google Scholar 

  93. Collart, M. A., Tourkine, N., Belin, D., Vassalli, P., Jeanteur, P., and Blanchard, J. M. (1991) c-fos gene transcription in murine macrophages is modulated by a calcium-dependent block to elongation in intron 1. Mol. Cell. Biol. 11, 2826–2831.

    PubMed  CAS  Google Scholar 

  94. Bentley, D. L., and Groudine, M. (1986) A block to elongation is largely responsible for decreased transcription of c-myc in differentiated HL60 cells. Nature 321, 702–706.

    Article  PubMed  CAS  Google Scholar 

  95. Bender, T. P., Thompson, C. B., and Kuehl, W. M. (1987) Differential expression of c-myb mRNA in murine B lymphomas by a block to transcription elongation. Science 237, 1473–1476.

    Article  PubMed  CAS  Google Scholar 

  96. Watson, R. J. (1988) A transcriptional arrest mechanism involved in controlling constitutive levels of mouse c-myb mRNA. Oncogene 2, 267–272.

    PubMed  CAS  Google Scholar 

  97. Haley, J. D. and Waterfield, M. D. (1991) Contributory effects of de novo transcription and premature transcript termination in the regulation of human epidermal growth factor receptor proto-oncogene RNA synthesis. J. Biol. Chem. 266, 1746–1753.

    PubMed  CAS  Google Scholar 

  98. Chen, Z., Harless, M. L., Wright, D. A., and Kellems, R. E. (1990) Identification and characterization of transcriptional arrest sites in exon 1 of the human adenosine deaminase gene. Mol. Cell. Biol. 10, 4555–4564.

    PubMed  CAS  Google Scholar 

  99. Gisselbrecht, S., Fichelson, S., Sola, B., Bordereaux, D., Hampe, A., Andre, C., Galibert, F., and Tambourin, P. (1987) Frequent c-fms activation by proviral insertion in mouse myeloblastic leukaemias. Nature 329, 259–261.

    Article  PubMed  CAS  Google Scholar 

  100. Moorwood, K., Charles, A. K., Salpekar, A., Wallace, J. I., Brown, K. W., and Malik, K. (1998) Antisense WT1 transcription parallels sense mRNA and protein expression in fetal kidney and can elevate protein levels in vitro. J. Pathol. 185, 352–359.

    Article  PubMed  CAS  Google Scholar 

  101. Felgner, J., Kreipe, H., Heidorn, K., Jaquet, K., Heuss, R., Zschunke, F., Radzun, H. J., and Parwaresch, M. R. (1992) Lineage-specific methylation of the c-fms gene in blood cells and macrophages. Leukemia 6, 420–425.

    PubMed  CAS  Google Scholar 

  102. Bird, A. P. and Southern, E. M. (1978) Use of restriction enzymes to study eukaryotic DNA methylation: I. The methylation pattern in ribosomal DNA from Xenopus laevis. J. Mol. Biol. 118, 27–47.

    Article  PubMed  CAS  Google Scholar 

  103. Lubbert, M., Henschler, R., Kreutz, M., Andreesen, R., Mertelsmann, R., and Herrmann, F. (1997) The human lysozyme gene undergoes stepwise demethylation during phagocyte maturation. Leukemia 11, 990–997.

    Article  PubMed  CAS  Google Scholar 

  104. Felgner, J., Heidorn, K., Korbacher, D., Frahm, S. O., and Parwaresch, R. (1999) Cell lineage specificity in G-CSF receptor gene methylation. Leukemia 13, 530–534.

    Article  PubMed  CAS  Google Scholar 

  105. Jin, D. I., Jameson, S. B., Reddy, M. A., Schenkman, D., and Ostrowski, M. C. (1995) Alterations in differentiation and behavior of monocytic phagocytes in transgenic mice that express dominant suppressors of ras signaling. Mol. Cell. Biol. 15, 693–703.

    PubMed  CAS  Google Scholar 

  106. Pahl, H. L., Scheibe, R. J., Zhang, D. E., Chen, H. M., Galson, D. L., Maki, R. A., and Tenen, D. G. (1993) The proto-oncogene PU.1 regulates expression of the myeloid-specific CD11b promoter. J. Biol. Chem. 268, 5014–5020.

    PubMed  CAS  Google Scholar 

  107. Rosmarin, A. G., Caprio, D. G., Kirsch, D. G., Handa, H., and Simkevich, C. P. (1995a) GABP and PU.1 compete for binding, yet cooperate to increase CD18 (beta 2 leukocyte integrin) transcription. J. Biol. Chem. 270, 23,627–23,633.

    CAS  Google Scholar 

  108. Rosmarin, A. G., Caprio, D., Levy, R., and Simkevich, C. (1995b) CD18 (beta 2 leukocyte integrin) promoter requires PU.1 transcription factor for myeloid activity. Proc. Natl. Acad. Sci. USA 92, 801–805.

    Article  PubMed  CAS  Google Scholar 

  109. Bottinger, E. P., Shelley, C. S., Farokhzad, O. C., and Arnaout, M. A. (1994) The human beta 2 integrin CD18 promoter consists of two inverted Ets cis elements. Mol. Cell. Biol. 14, 2604–2615.

    PubMed  CAS  Google Scholar 

  110. Perez, C., Coeffier, E., Moreau-Gachelin, F., Wietzerbin, J., and Benech, P. D. (1994) Involvement of the transcription factor PU.1/Spi-1 in myeloid cell-restricted expression of an interferon-inducible gene encoding the human high-affinity Fc gamma receptor. Mol. Cell. Biol. 14, 5023–5031.

    PubMed  CAS  Google Scholar 

  111. Eichbaum, Q. G., Iyer, R., Raveh, D. P., Mathieu, C., and Ezekowitz, R. A. (1994) Restriction of interferon gamma responsiveness and basal expression of the myeloid human Fc gamma R1b gene is mediated by a functional PU.1 site and a transcription initiator consensus. J. Exp. Med. 179, 1985–1996.

    Article  PubMed  CAS  Google Scholar 

  112. Feinman, R., Qiu, W. Q., Pearse, R. N., Nikolajczyk, B. S., Sen, R., Sheffery, M., and Ravetch, J. V. (1994) PU.1 and an HLH family member contribute to the myeloid-specific transcription of the Fc gamma RIIIA promoter. EMBO J. 13, 3852–3860.

    PubMed  CAS  Google Scholar 

  113. Hohaus, S., Petrovick, M. S., Voso, M. T., Sun, Z., Zhang, D. E., and Tenen, D. G. (1995) PU.1 (Spi-1) and C/EBP alpha regulate expression of the granulocyte-macrophage colony-stimulating factor receptor alpha gene. Mol. Cell. Biol. 15, 5830–5845.

    PubMed  CAS  Google Scholar 

  114. Heydemann, A., Juang, G., Hennessy, K., Parmacek, M. S., and Simon, M. C. (1996) The myeloid-cell-specific c-fes promoter is regulated by Sp1, PU.1, and a novel transcription factor. Mol. Cell. Biol. 16, 1676–1686.

    PubMed  CAS  Google Scholar 

  115. Moulton, K. S., Semple, K., Wu, H., and Glass, C. K. (1994) Cell-specific expression of the macrophage scavenger receptor gene is dependent on PU.1 and a composite AP-1/ets motif. Mol. Cell. Biol. 14, 4408–4418.

    PubMed  CAS  Google Scholar 

  116. Kistler, B., Pfisterer, P., and Wirth, T. (1995) Lymphoid-and myeloid-specific activity of the PU.1 promoter is determined by the combinatorial action of octamer ets transcription factors. Oncogene 11, 1095–1106.

    PubMed  CAS  Google Scholar 

  117. Chen, H., Ray-Gallet, D., Zhang, P., Hetherington, C. J., Gonzalez, D. A., Zhang, D. E., Moreau-Gachelin, F., and Tenen, D. G. (1995) PU.1 (Spi-1) autoregulates its expression in myeloid cells. Oncogene 11, 1549–1560.

    PubMed  CAS  Google Scholar 

  118. Rehli, M., den Elzen, N., Cassady, A. I., Ostrowski, M. C., and Hume, D. A. (1999) Cloning and characterisation of the murine genes for bHLH-ZIP factors TFEC and TFEB reveals a common gene organisation for all MiT-subfamily members. Genomics 56, 111–120.

    Article  PubMed  CAS  Google Scholar 

  119. Moreau-Gachelin, F. (1994) Spi-1/PU.1: an oncogene of the Ets family. Biochim. Biophys. Acta 1198, 149–163.

    PubMed  Google Scholar 

  120. Klemsz, M. J., McKercher, S. R., Celada, A., van Beveren, C., and Maki, R. A. (1990) The macrophage and B cell-specific transcription factor PU.1 is related to the ets oncogene. Cell 61, 113–124.

    Article  PubMed  CAS  Google Scholar 

  121. Hromas, R., Orazi, A., Neiman, R. S., Maki, R., van Beveran, C., Moore, J., and Klemsz, M. (1993) Hematopoietic lineage-and stage-restricted expression of the ETS oncogene family member PU.1. Blood 82, 2998–3004.

    PubMed  CAS  Google Scholar 

  122. Scott, E. W., Simon, M. C., Anastasi, J., and Singh, H. (1994) Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 265, 1573–1577.

    Article  PubMed  CAS  Google Scholar 

  123. McKercher, S. R., Torbett, B. E., Anderson, K. L., Henkel, G. W., Vestal, D. J., Baribault, H., Klemsz, M., Feeney, A. J., Wu, G. E., Paige, C. J., and Maki, R. A. (1996) Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J. 15, 5647–5658.

    PubMed  CAS  Google Scholar 

  124. Anderson, K. L., Smith, K. A., Conners, K., McKercher, S. R., Maki, R. A., and Torbett, B. E., (1998) Myeloid development is selectively disrupted in PU.1 null mice. Blood 91, 3702–3710.

    PubMed  CAS  Google Scholar 

  125. DeKoter, R. P., Walsh, J. C., and Singh H. (1998) PU.1 regulates both cytokine-dependent proliferation and differentiation of granulocyte/macrophage progenitors. EMBO J. 17, 4456–4468.

    Article  PubMed  CAS  Google Scholar 

  126. Olson, M. C., Scott, E. W., Hack, A. A., Su, G. H., Tenen, D. G., Singh, H., and Simon, M. C. (1995) PU.1 is not essential for early myeloid gene expression but is required for terminal myeloid differentiation. Immunity 3, 703–714.

    Article  PubMed  CAS  Google Scholar 

  127. Fowles, L. F., Martin, M. L., Nelsen, L., Stacey, K. J., Redd, D., Clark, Y. M., Nagamine, Y., McMahon, M., Hume, D. A., and Ostrowski, M. C. (1998) Persistent activation of mitogen-activated protein kinases p42 and p44 and ets-2 phosphorylation in response to colony-stimulating factor 1/c-fms signaling. Mol. Cell. Biol. 18, 5148–5156.

    PubMed  CAS  Google Scholar 

  128. Yang, B. S., Hauser, C. A., Henkel, G., Colman, M. S., van Beveren, C., Stacey, K. J., Hume, D. A., Maki, R. A., and Ostrowski, M. C. (1996) Ras-mediated phosphorylation of a conserved threonine residue enhances the transactivation activities of c-Ets1 and c-Ets2. Mol. Cell. Biol. 16, 538–547.

    PubMed  CAS  Google Scholar 

  129. Stacey, K. J., Fowles, L. F., Colman, M. S., Ostrowski, M. C., and Hume, D. A. (1995) Regulation of urokinase-type plasminogen activator gene transcription by macrophage colony-stimulating factor. Mol. Cell. Biol. 15, 3430–3441.

    PubMed  CAS  Google Scholar 

  130. Hagemeier, C., Bannister, A. J., Cook, A., and Kouzarides, T. (1993) The activation domain of transcription factor PU.1 binds the retinoblastoma (RB) protein and the transcription factor TFIID in vitro: RB shows sequence similarity to TFIID and TFIIB. Proc Natl Acad Sci USA 90, 1580–1584.

    Article  PubMed  CAS  Google Scholar 

  131. Nuchprayoon, I., Meyers, S., Scott, L. M., Suzow, J., Hiebert, S., and Friedman, A. D. (1994) PEBP2/CBF, the murine homolog of the human myeloid AML1 and PEBP2 beta/CBF beta proto-oncoproteins, regulates the murine myeloperoxidase and neutrophil elastase genes in immature myeloid cells. Mol. Cell. Biol. 14, 5558–5568.

    PubMed  CAS  Google Scholar 

  132. Zhang, D. E., Hetherington, C. J., Meyers, S., Rhoades, K. L., Larson, C. J., Chen, H. M., Hiebert, S. W., and Tenen, D. G. (1996) CCAAT enhancer-binding protein (C/EBP) and AML1 (CBF alpha2) synergistically activate the macrophage colony-stimulating factor receptor promoter. Mol. Cell. Biol. 16, 1231–1240.

    PubMed  CAS  Google Scholar 

  133. Petrovick, M. S., Hiebert, S. W., Friedman, A. D., Hetherington, C. J., Tenen, D. G., and Zhang, D. E. (1998) Multiple functional domains of AML1: PU.1 and C/EBP alpha synergize with different regions of AML1. Mol. Cell. Biol. 18, 3915–3925.

    PubMed  CAS  Google Scholar 

  134. Xie, Y., Ross, I. L., Browne, C. M., Lichanska, A., Favot, P., Ostrowski, M. C., and Hume, D. A. (1996) Transcriptional control of the expression of the c-fms gene encoding the receptor for macrophage colony-stimulating (CSF-1). Immunobiology 195, 461–476.

    Google Scholar 

  135. Natsuka, S., Akira, S., Nishio, Y., Hashimoto, S., Sugita, T., Isshiki, H., and Kishimoto, T. (1992) Macrophage differentiation-specific expression of NF-IL6, a transcription factor for interleukin-6. Blood 79, 460–466.

    PubMed  CAS  Google Scholar 

  136. Lowenstein, C. J., Alley, E. W., Raval, P., Snowman, A. M., Snyder, S. H., Russell, S. W., and Murphy, W. J. (1993) Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon gamma and lipopolysaccharide. Proc. Natl. Acad. Sci. USA 90, 9730–9734.

    Article  PubMed  CAS  Google Scholar 

  137. Bretz, J. D., Williams, S. C., Baer, M., Johnson, P. F., and Schwartz, R. C., (1994) C/EBP-related protein 2 confers lipopolysaccharide-inducible expression of interleukin 6 and monocyte chemoattractant protein 1 to a lymphoblastic cell line. Proc. Natl. Acad. Sci. USA 91, 7306–7310.

    Article  PubMed  CAS  Google Scholar 

  138. Tanaka, T., Akira, S., Yoshida, K., Umemoto, M., Yoneda, Y., Shirafuji, N., Fujiwara, H., Suematsu, S., Yoshida, N., and Kishimoto, T. (1995) Targeted disruption of the NF-IL6 gene discloses its essential role in bacteria killing and tumor cytotoxicity by macrophages. Cell 80, 353–361.

    Article  PubMed  CAS  Google Scholar 

  139. Hsu, W., Kerppola, T. K., Chen, P. L., Curran, T., and Chen-Kiang, S. (1994) Fos and Jun repress transcription activation by NF-IL6 through association at the basic zipper region. Mol. Cell. Biol. 14, 268–276.

    PubMed  CAS  Google Scholar 

  140. Landschulz, W. H., Johnson, P. F., and McKnight, S. L. (1989) The DNA binding domain of the rat liver nuclear protein C/EBP is bipartite. Science 243, 1681–1688.

    Article  PubMed  CAS  Google Scholar 

  141. Vinson, C. R., Sigler, P. B., and McKnight, S. L. (1989) Scissors-grip model for DNA recognition by a family of leucine zipper proteins. Science 246, 911–916.

    Article  PubMed  CAS  Google Scholar 

  142. Chen, P. L., Riley, D. J., Chen-Kiang, S., and Lee, W. H. (1996) Retinoblastoma protein directly interacts with and activates the transcription factor NF-IL6. Proc. Natl. Acad. Sci. USA 93, 465–469.

    Article  PubMed  CAS  Google Scholar 

  143. LeClair, K. P., Blanar, M. A., and Sharp, P. A. (1992) The p50 subunit of NF-kappa B associates with the NF-IL6 transcription factor. Proc. Natl. Acad. Sci. USA 89, 8145–8149.

    Article  PubMed  CAS  Google Scholar 

  144. Mink, S., Kerber, U., and Klempnauer, K. H. (1996) Interaction of C/EBPbeta and v-Myb is required for synergistic activation of the mim-1 gene. Mol. Cell. Biol. 16, 1316–1325.

    PubMed  CAS  Google Scholar 

  145. Stein, B., Cogswell, P. C., and Baldwin, A. S. Jr. (1993) Functional and physical associations between NF-kappa B and C/EBP family members: a Rel domain-bZIP interaction. Mol. Cell. Biol. 13, 3964–3974.

    PubMed  CAS  Google Scholar 

  146. Nagulapalli, S., Pongubala, J. M., and Atchison, M. L. (1995) Multiple proteins physically interact with PU.1. Transcriptional synergy with NF-IL6 beta (C/EBP delta, CRP3). J. Immunol. 155, 4330–4338.

    PubMed  CAS  Google Scholar 

  147. Voellmy, R. (1994) Transduction of the stress signal and mechanisms of transcriptional regulation of heat shock/stress protein gene expression in higher eukaryotes. Crit. Rev. Eukaryot. Gene. Expr. 4, 357–401.

    PubMed  CAS  Google Scholar 

  148. Wu, C. (1995) Heat shock transcription factors: structure and regulation. Annu. Rev. Cell. Dev. Biol. 11, 441–469.

    Article  PubMed  CAS  Google Scholar 

  149. Sato, M., Morii, E., Takebayashi-Suzuki, K., Yasui, N., Ochi, T., Kitamura, Y., and Nomura, S. (1999) Microphthalmia-associated transcription factor interacts with PU.1 and c-Fos: determination of their subcellular localization. Biochem Biophys. Res. Commun. 254, 384–387.

    Article  PubMed  CAS  Google Scholar 

  150. Behre, G., Whitmarsh, A. J., Coghlan, M. P., Hoang, T., Carpenter, C. L., Zhang, D. E., Davis, R. J., and Tenen, D. G. (1999) c-Jun is a JNK-independent coactivator of the PU.1 transcription factor. J. Biol. Chem. 274, 4939–4346.

    Article  PubMed  CAS  Google Scholar 

  151. Li, A. C., Guidez, F. R., Collier, J. G., and Glass, C. K. (1998) The macrosialin promoter directs high levels of transcriptional activity in macrophages dependent on combinatorial interactions between PU.1 and c-Jun. J. Biol. Chem. 273, 5389–5399.

    Article  PubMed  CAS  Google Scholar 

  152. Rehli, M., Lichanska, A., den Elzen, N., Ostrowski, M. C., and Hume, D. A. (1999) TFEC is a macrophage-restricted member of the MiT-subfamily of bHLH-ZIP transcription factors. J. Immunol. 162, 1559–1565.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Adult Oncology, Dana Farber Cancer Institute, USA

    Yue Xie

  2. Laboratory of Molecular and Cellular Biology, Beth Israel Deaconess Medical Center, Harvard Medical School, 44 Binney Street, 02115, Boston, MA

    Changmin Chen

  3. Departments of Microbiology and Biochemistry and Centre for Molecular and Cellular Biology, University of Queensland, 4072, Brisbane, Australia

    David A. Hume

Authors
  1. Yue Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Changmin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David A. Hume
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xie, Y., Chen, C. & Hume, D.A. Transcriptional regulation of c-fms gene expression. Cell Biochem Biophys 34, 1–16 (2001). https://doi.org/10.1385/CBB:34:1:001

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1385/CBB:34:1:001

Keywords

Search

Navigation