Abstract
Colony stimulating factor 1 (CSF-1) is a functionally versatile, circulating homodimeric growth factor that stimulates the survival, proliferation, and differentiation of mononuclear phagocytic cells, the differentiation of osteoclast progenitor cells and that regulates cells of the female reproductive tract. CSF-1 is also expressed in the central nervous system where it may regulate the differentiation and activation of microglia. The diverse forms of CSF-1 are all encoded by a single gene. Alternative posttranscriptional splicing and posttranslational cleavage determines whether CSF-1 will be produced as a secreted proteoglycan, secreted glycoprotein, or as a cell-surface glycoprotein that may be involved in cell-cell interactions. CSF-1 is expressed in glioblastoma cell-lines, normal human astrocytes, and in operative specimens of human glioma. The CSF-1 receptor, encoded by the c-fms proto-oncogene, is also expressed in human gliomas. We conclude that coexpression of CSF-1 and its receptor in some human gliomas hints at a possible autocrine or paracrine growth stimulatory role for CSF-1; however, its function in the mammalian CNS remains to be elucidated.
Similar content being viewed by others
References
Alterman R. L., Morrison R.S., Goodrich J. T., Papenhausen P., and Moskal J. R. (1991) A primary encephalocele culture yields a pure population of human astrocytes.Brain Res. 550, 319–323.
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.
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.
Bishop J. M. (1987) The molecular genetics of cancer.Science 235, 305–311.
Cockram C. S. (1990) Growth factors, astrocytes and astrocytomas.Seminars in Developmental Biology 1, 421–435.
Cross M. and Dexter T. M. (1991) Growth factors in development, transformation, and tumorigenesis.Cell 64, 271–280.
Das S. K., Stanley E. R., Guilbert L. J., and Forman L. W. (1981) Human colony stimulating factor (CSF-1) radioimmunoassy: resolution of three subclasses of human colony stimulating factors.Blood 58, 630–641.
Das S. K. and Stanley E. R. (1982) Structure-function studies of a colony stimulating factor (CSF-1).J. Biol. Chem. 257, 13,679–13,684.
Downing J. R., Rettenmeier C. W., and Sherr C. J. (1988) Ligand induced tyrosine kinase activity of the colony stimulating factor-1 receptor in a murine macrophage cell line.Mol. Cell. Biol. 8, 1795–1799.
Felix R., Cecchini M. G., and Fleisch H. (1990) Macrophage colony simulating factor restores in vivo bone resorption in the op/op osteopetrotic mouse.Endocrinology 127, 2592–2594.
Folkman J. and Klagsbrun M. (1987) Angiogenic factors.Science 235, 442–447.
Gilbert H. S., Praloran V., and Stanley E. R. (1989) Increased circulating CSF-1 (M-CSF) in myeloproliferative disease: association with myeloid metaplasia and peripheral bone marrow extension.Blood 74, 1231–1234.
Gross J. L., Behrens D. L., Mullins D. E., Kornblith P. L., and Dexter D. L. (1988) Plasminogen activator and inhibitor activity in human glioma cells and modulation by sodium butyrate.Cancer Res. 48, 291–296.
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.
Guilbert L. J., and Stanley E. R. (1986) The interaction of125I- colony stimulating factor 1 with bone marrow-derived macrophages.J. Biol. Chem. 261, 4024–4032.
Hao C., Guilbert L. J., and Federoff S. J. (1990) Production of colony stimulating factor I (CSF-1) by mouse astroglia in vitro.J. Neurosci. Res. 27, 314–323.
Horiguchi J. M., Sherman M. L., Sampson-Johannes B. L., Weber B. L., and Kufe D. W. (1988) CSF-1 and c-fms expression in human carcinoma cell lines.Biochem. Biophys. Res. Commun. 157, 395–401.
Hulkower K. L., Brosnan C. F., and Berman J. W. (1991) Cytokine gene expression in the central nervous system of rats with experimental autoimmune encephalomyelitis (EAE).FASEB J. 5, A8184.
Janowska-Wieczorek A., Belch A. R., Jacobs A., Bowen D., Padua R-A., Paietta E., and Stanley E. R. (1991) Increased circulating colony stimulating factor 1 in patients with preleukemia, leukemia and lymphoid malignancies.Blood 77, 1796–1803.
Kacinski B. M., Carter D., Mittal K., Kohorn E. I., Bloodgood R. S., Donahue J., Donofrio L., Edwards R., Schwartz P. E., Chambers J. T., and Chambers S. K. (1988) High level expression of fms proto-oncogene mRNA is observed in clinically aggressive human endometrial adenocarcinomas.Int. J. Radiat. Oncol. Biol. Phys. 15, 823–829.
Kacinski B. M., Bloodgood R. S., Schwartz P. E., Carter D., and Stanley E. R. (1989a) The macrophage colony stimulating factor CSF-1 is produced by human ovarian and endometrial carcinoma-derived cell lines and is present at abnormally high levels in the plasma of ovarian carcinoma patients with active disease.Cold Spring Harb. Symp. Quant. Biol. Cancer Cells 7, 333–337.
Kacinski B. M., Stanley E. R., Carter D., Chambers J. T., Chambers J. T., Kohorn E. I., and Schwartz P. E. (1989b) Circulating levels of CSF-1 (M-CSF) a lymphohematopoietic cytokine may be a useful marker of disease status in patients with malignant ovarian neoplasms.Int. J. Radiat. Oncol. Biol. Phys. 17, 159–164.
Kacinski B. M., Chambers S. K., Carter D., Filderman A. E., and Stanley E. R. (1990) The macrophage colony stimulating factor CSF-1, an auto- and paracrine tumor cytokine is also a circulating “tumor marker” in patients with ovarian, endometrial, and pulmonary neoplasms.Prog. Leuk. Biol. 108, 393–400.
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.
Kawasaki E. S., Ladner M. B., Wang A. M., Van Arsdell J., Warren M. K., Coyne M. Y., Schweikart V. L., Lee M. T., Wilson K. J., Boosman A., Stanley E. R., Ralph P., Mark D. F. (1985) Molecular cloning of a complementary DNA encoding human macrophage specific colony stimulating factor (CSF-1).Science 230, 291–296.
Ladner M. B., Martin G. A., Noble J. A., Nikoloff D. M., Tal R., Kawasaki E. S., and White T. J. (1987) Human CSF-1: gene structure and alternative splicing of mRNA precursors.EMBO J. 6, 2693–2698.
Li W. and Stanley E. R. (1991) Role of dimerization and modification of the CSF-1 receptor in its activation and internalization during the CSF-1 response.EMBO J. 10, 277–288.
Morrison R. S., Gross J. L., Herblin W. F., Reilly T. M., LaSala P. A., Alterman R. L., Moskal J. R., Kornblith P. L., and Dexter D. L. (1990) Basic fibroblast growth factor-like activity and receptors are expressed in a human glioma cell lines.Cancer Res. 50, 2524–2529.
Nakamura M., Merchav S., Carter A., Ernst T. J., Demetri G. D., Furukawa Y., Anderson K., Freeman A. S., and Griffin J. D. (1989) Expression of a novel 3.5 kb macrophage colony stimulating factor transcript in human myeloma cells.J. Immunol. 143, 3543–3547.
Paietta E., Racevskis J., Stanley E. R., Andreeff M., Papenhausen P., and Wiernik P. M. (1990) Expression of the macrophage growth factor, CSF-1 and its receptor, C-FMS, by a Hodgkins disease derived cell-line and its variants.Cancer Res. 50, 2049–2055.
Pollard J. W., Bartocci A., Arceci R., Orlofsky A., Ladner M. B., and Stanley E. R. (1987) Apparent role of the macrophage growth factor, CSF-1, in placental development.Nature 330, 484–486.
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.
Price L. K. H., Choi H. U., Rosenberg L., and Stanley E. R. (1992) The predominant form of secreted colony stimulating factor 1 is a proteoglycan.J. Biol. Chem. 267, 2190–2199.
Rambaldi A., Wakamiya I. V., Vellenga E., Horiguchi J., Warren M. K., Kufe D., and Griffin J. D. (1988) Expression of the macrophage colony stimulating factor and c-fms genes in human acute myeloblastic leukemia cells.J. Clin. Invest. 81, 1030–1035.
Salcman M. (1990) Epidemiology and factors affecting survival, inMalignant Cerebral Glioma (Apuzzo M. L. J., ed.), American Association of Neurological Surgeons, Park Ridge, IL.
Sengupta A., Liu W-K, Yeung Y. G., Yeung D. C. Y., Frackelton Jr., A. R., and Stanley E. R. (1988) Identification and subcellular localization of proteins that are rapidly phosphorylated in tyrosine in response to colony stimulating factor 1.Proc. Natl. Acad. Sci. USA 85, 8062–8066.
Shafit-Zagardo B., Sharma N., Berman J. W., and Brosnan C. F. (1991) IL-1 and TNF upregulate CSF-1 expression in rat astrocyte cultures.J. Cell. Biol. 115, 2450a.
Sherr C. J., Rettenmier C. W., Sacca R., Roussel M., Look A. T., and Stanley E. R. (1985) The c-fms proto-oncogene product is related to the receptor for the mononuclear phagocyte growth factor, CSF-1.Cell 41, 665–676.
Stanley E. R. (1990) Role of colony stimulating factor 1 in monocytopoiesis and placental development, inGenetics of Pattern Formation and Growth Control, Wiley-Liss, pp. 165–180.
Stanley E. R., Guilbert L. J., Tushinski R. J. and Bartelmez S. H. (1983) CSF-1 —a mononuclear phagocyte lineage-specific hemopoietic growth factor.J. Cell. Biochem. 21, 151–159.
Stein J., Borzillo G. V., and Rettenmeier C. W. (1990) Direct stimulation of cells expressing receptors for macrophage colony stimulating factor (CSF-1) by a plasma membrane-bound precursor of human CSF-1.Blood 76, 1308–1314.
Takahashi J. A., Fukumoto M., Igarashi K., Oda Y., Kikuchi H., and Hatanaka M. (1992) Correlation of basic fibroblast growth factor expression levels with the degree of malignancy and vascularity in human gliomas.J. Neurosurg. 76, 792–798.
Thery C., Hetier E., Evrard C., and Mallat M. (1990) Expression of macrophage colony stimulating factor gene in the mouse brain during development.J. Neurosci. Res. 26, 129–133.
Thery C., Stanley E. R., and Mallat M. (1992) Interleukin 1 and tumor necrosis factor alpha stimulate the production of colony stimulating factor 1 by murine astrocytes.J. Neurosci. Res., in press.
Tushinski R. J. and Stanley E. R. (1985) The regulation of mononuclear phagocyte entry into S phase by the colony stimulating factor CSF-1.J. Cell Physiol. 116, 67–75.
Ulrich A. and Schlessinger J. (1990) Signal transduction by receptors with tyrosine kinase activity.Cell 61, 203–212.
Wiktor-Jedrzejczak W., Bartocci A., Ferrante A. W., Jr., Ahmed-Ansari 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.
Wong A. J., Bigner S. H., Bigner D. D., Kinzler K. W., Hamilton S. R., and Vogelstein B. (1987) Increased expression of the epidermal growth factor receptor gene in malignant gliomas is invariably associated with gene amplication.Proc. Natl. Acad. Sci. USA 84, 6899–6903.
Wu M. and Yunis A. A. (1980) Common pattern of two distinct types of colony stimulating factor in human tissues and cultured cells.J. Clin. Invest. 65, 772–776.
Yeung Y. G., Jubinsky P. T., Sengupta A., Yeung D. C. Y., and Stanley E. R. (1987) Purification of the colony stimulating factor 1 receptor and demonstration of its tyrosine kinase activity.Proc. Natl. Acad. Sci. USA 84, 1268–1271, 1987.
Yoshida H., Hayashi S-I, Kunisada T., Ogawa M., Nishikawa S., Okomura H., Sudo T., Shultz L. D., and Nishikawa S-I (1990) The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene.Nature 345, 422–424.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Alterman, R.L., Stanley, E.R. Colony stimulating factor-1 expression in human glioma. Molecular and Chemical Neuropathology 21, 177–188 (1994). https://doi.org/10.1007/BF02815350
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF02815350