Cancer Cell Biology
Expression of emmprin (CD147), a cell surface inducer of matrix metalloproteinases, in normal human brain and gliomas
Tetsuro Sameshima,
Kazuki Nabeshima,
Bryan P. Toole,
Kiyotaka Yokogami,
Yasunori Okada,
Tomokazu Goya,
Masashi Koono,
Shinichiro Wakisaka,
Corresponding Author
Tetsuro Sameshima
Department of Neurosurgery, Miyazaki Medical College, Kiyotake, Miyazaki, Japan
Department of Neurosurgery, Miyazaki Medical College, 5200 Kihara, Kiyotake, Miyazaki 889-1692, Japan. Fax: (81)-985-84-4571Search for more papers by this authorKazuki Nabeshima
Department of Pathology, Miyazaki Medical College, Kiyotake, Miyazaki, Japan
Search for more papers by this authorBryan P. Toole
Department of Anatomy and Cellular Biology, Tufts University School of Medicine, Boston, Massachusetts, USA
Search for more papers by this authorKiyotaka Yokogami
Department of Neurosurgery, Miyazaki Medical College, Kiyotake, Miyazaki, Japan
Search for more papers by this authorYasunori Okada
Department of Pathology, Keio University School of Medicine, Tokyo, Japan
Search for more papers by this authorTomokazu Goya
Department of Neurosurgery, Miyazaki Medical College, Kiyotake, Miyazaki, Japan
Search for more papers by this authorMasashi Koono
Department of Pathology, Miyazaki Medical College, Kiyotake, Miyazaki, Japan
Search for more papers by this authorShinichiro Wakisaka
Department of Neurosurgery, Miyazaki Medical College, Kiyotake, Miyazaki, Japan
Search for more papers by this authorTetsuro Sameshima,
Kazuki Nabeshima,
Bryan P. Toole,
Kiyotaka Yokogami,
Yasunori Okada,
Tomokazu Goya,
Masashi Koono,
Shinichiro Wakisaka,
Corresponding Author
Tetsuro Sameshima
Department of Neurosurgery, Miyazaki Medical College, Kiyotake, Miyazaki, Japan
Department of Neurosurgery, Miyazaki Medical College, 5200 Kihara, Kiyotake, Miyazaki 889-1692, Japan. Fax: (81)-985-84-4571Search for more papers by this authorKazuki Nabeshima
Department of Pathology, Miyazaki Medical College, Kiyotake, Miyazaki, Japan
Search for more papers by this authorBryan P. Toole
Department of Anatomy and Cellular Biology, Tufts University School of Medicine, Boston, Massachusetts, USA
Search for more papers by this authorKiyotaka Yokogami
Department of Neurosurgery, Miyazaki Medical College, Kiyotake, Miyazaki, Japan
Search for more papers by this authorYasunori Okada
Department of Pathology, Keio University School of Medicine, Tokyo, Japan
Search for more papers by this authorTomokazu Goya
Department of Neurosurgery, Miyazaki Medical College, Kiyotake, Miyazaki, Japan
Search for more papers by this authorMasashi Koono
Department of Pathology, Miyazaki Medical College, Kiyotake, Miyazaki, Japan
Search for more papers by this authorShinichiro Wakisaka
Department of Neurosurgery, Miyazaki Medical College, Kiyotake, Miyazaki, Japan
Search for more papers by this authorFirst published: 23 August 2000
Citations: 117
Abstract
EMMPRIN (extracellular matrix metalloproteinase inducer), also called CD147, basigin or M6 in the human, is a member of the immunoglobulin superfamily that is present on the surface of tumor cells and stimulates adjacent fibroblasts to produce matrix metalloproteinases (MMPs). In our study, we investigated expression of EMMPRIN in human normal brain and gliomas, since mouse basigin and chicken HT7, the species homologues of human EMMPRIN, are associated with neuronal interactions and normal blood-brain barrier function, respectively. EMMPRIN expression was detected in all samples of non-neoplastic brain and glioma tissues examined. However, expression levels of EMMPRIN mRNA and protein were significantly higher in gliomas than in non-neoplastic brain. Moreover, levels of mRNA expression and immunohistochemical staining correlated with tumor progression in gliomas: They were highest in the most malignant form of glioma, glioblastoma multiforme, followed by anaplastic astrocytoma and then low-grade astrocytoma. Also, immunolocalization revealed quite different distributions in non-neoplastic brain and glioma: EMMPRIN was demonstrated only in vascular endothelium in non-neoplastic regions of the brain, whereas it was present in tumor cells but not in proliferating blood vessels in malignant gliomas. These data indicate that an MMP inducer molecule EMMPRIN is differently expressed in human normal brain and gliomas and could be associated with astrocytoma progression. Possible mechanisms whereby glioma cell EMMPRIN could influence tumor progression will be discussed. Int. J. Cancer 88:21–27, 2000. © 2000 Wiley-Liss, Inc.
REFERENCES
- Albrecht, U., Seulberger, H., Schwarz, H. and Risau, W., Correlation of blood-brain barrier function and HT7 protein distribution in chick brain circumventricular organs. Brain Res., 535, 49-61 (1990).
- Basset, P., Bellocq, J.P., Wolf, C., Stoll, I., Hutin, P., Limacher, J.M., Podhajcer, O.L., Chenard, M.P., Rio, M.C. and Chambon, P., A novel metalloproteinase specifically expressed in stromal cells of breast carcinomas. Nature, 348, 699-704 (1990).
- Biswas, C., Tumor cell stimulation of collagenase production by fibroblasts. Biochem. Biophys. Res. Commun., 109, 1026-1034 (1982).
-
Biswas, C. and
Toole, B.P.,
Modulation of the extracellular matrix by tumor cell-fibroblast interactions. In:
E. Elson,
W. Frazier and
L. Glaser, editors,
Cell membranes: methods and reviews, pp. 341-363,
Plenum Publishing,
New York
1987).
10.1007/978-1-4613-1915-3_7 Google Scholar
- Biswas, C., Zhang, Y., DeCastro, R., Guo, H., Nakamura, T., Kataoka, H. and Nabeshima, K., The human tumor cell-derived collagenase stimulatory factor (renamed EMMPRIN) is a member of the immunoglobulin superfamily. Cancer Res., 55, 43 4-439 (1995).
- Burger, P.C. and Scheithauer, B.W. Tumours of the central nervous system. Armed Forces Institute of Pathology, Washington, D.C. 1994).
- Dabbous, M.K., El-Torky, M., Haney, L., Brinkley, B. and Sobhy, N., Collagenase activity in rabbit carcinoma: cell source and cell interactions. Int. J. Cancer, 31, 357-364 (1983).
- Ellis, S.M., Nabeshima, K. and Biswas, C., Monoclonal antibody preparation and purification of a tumor cell collagenase-stimulatory factor. Cancer Res., 49, 3385-3391 (1989).
- Fossum, S., Mallett, S. and Barclay, A.N., The MRC OX-47 antigen is a member of the immunoglobulin superfamily with an unusual transmembrane sequence. Europ. J. Immunol., 21, 671-679 (1991).
- Giese, A. and Westphal, M., Glioma invasion in the central nervous system. Neurosurgery, 39, 235-252 (1996).
- Goslen, J.B., Eisen, A.Z. and Bauer, E.A., Stimulation of skin fibroblast collagenase production by a cytokine derived from basal cell carcinoma. J. Invest. Dermatol., 85, 161-164 (1985).
- Gray, F. and Nordmann, P., Bacterial infections. In: D.I. Graham and P.L. Lantos, editors. Greenfield's neuropathology, 6th ed., pp. 113-129, Oxford University Press, New York 1997).
- Gray, S.T., Wilkins, R.J. and Yun, K., Interstitial collagenase gene expression in oral squamous cell carcinoma. Amer. J. Pathol., 141, 301-306 (1992).
- Guo, H., Zucker, S., Gordon, M.K., Toole, B.P. and Biswas, C., Stimulation of matrix metalloproteinase production by recombinant extracellular matrix metalloproteinase inducer from transfected chinese hamster ovary cells. J. biol. Chem., 272, 24-27 (1997).
- Heppner, K.J., Matrisian, L.M., Jensen, R.A. and Williams, W.H., Expression of most matrix metalloproteinase family members in breast cancer represents a tumor-induced host response. Amer. J. Pathol., 149, 273-282 (1996).
- Heussen, C. and Dowdle, E.B., Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrates. Anal. Biochem., 102, 196-202 (1980).
- Himelstein, B.P., Canete-Soler, R., Bernhard, E.J. and Muschel, R.J., Induction of fibroblast 92 kDa gelatinase/type IV collagenase expression by direct contact with metastatic tumor cells. J. Cell Sci., 107, 477-486 (1994).
- Hiraoka, N., Allen, E., Apel, I.J., Gyetko, M.R. and Weiss, S.J., Matrix metalloproteinases regulate neovascularization by acting as pericellular fibrinolysins. Cell, 95, 365-377 (1998).
- Ito, A., Nakajima, S., Sasaguri, Y., Nagase, H. and Mori, Y., Co-culture of human breast adenocarcinoma MCF-7 cells and human dermal fibroblasts enhances the production of matrix metalloproteinases 1, 2, and 3 in fibroblasts. Brit. J. Cancer, 71, 1039-1045 (1995).
- Itoh, T., Tanioka, M., Yoshida, H., Yoshioka, T., Nishimoto, H. and Itohara, S., Reduced angiogenesis and tumor progression in gelatinase A-deficient mice. Cancer Res., 58, 1048-1051, 1998).
- Kasinrerk, W., Fiebiger, E., Stefanova, I., Baumruker, T., Knapp, W. and Stockinger, H., Human leukocyte activation antigen M6, a member of the Ig superfamily, is the species homologue of rat OX-47, mouse basigin, and chicken HT7 molecule. J. Immunol., 149, 847-854 (1992).
- Kataoka, H., DeCastro, R., Zucker, S. and Biswas, C., Tumor cell-derived collagenase-stimulatory factor increases expression of interstitial collagenase, stromelysin, and 72-kDa gelatinase. Cancer Res., 53, 3154-3158 (1993).
-
Kleihues, P.,
Burger, P.C. and
Scheithauer, B.W.,
Histological typing of tumours of the central nervous system. In:
International Histological Classification of Tumours.
World Health Organization,
Geneva
1993).
10.1007/978-3-642-84988-6 Google Scholar
-
Kurogi, T.,
Nabeshima, K.,
Kataoka, H.,
Okada, Y. and
Koono, M.,
Stimulation of gelatinase B and tissue inhibitors of metalloproteinase (TIMP) production in co-culture of human osteosarcoma cells and human fibroblasts: gelatinase B production was stimulated via up-regulation of fibroblast growth factor (FGF) receptor.
Int. J. Cancer,
66,
82-90
(1996).
10.1002/(SICI)1097-0215(19960328)66:1<82::AID-IJC15>3.0.CO;2-D CAS PubMed Web of Science® Google Scholar
- Lampert, K., Machein, U., Machein, M.R., Conca, W., Peter, H.H. and Volk, B., Expression of matrix metalloproteinases and their tissue inhibitors in human brain tumors. Amer. J. Pathol., 153, 429-437 (1998).
- Liotta, L.A., Steeg, P.S. and Stetler-Stevenson, W.G., Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell, 64, 327-336 (1991).
- Majmudar, G., Nelson, B.R., Jensen, T.C. and Johnson, T.M., Increased expression of matrix metalloproteinase-3 (stromelysin-1) in cultured fibroblasts and basal cell carcinomas of nevoid basal cell carcinoma syndrome. Mol. Carcinog., 11, 29-33 (1994).
- Masson, R., Lefebvre, O., Noël, A., El Fahime, M., Chenard, M.P., Wendling, C., Kebers, F., LeMeur, M., Dierich, A., Foidart, J.M., Basset, P. and Rio, M.C., In vivo evidence that the stromelysin-3 metalloproteinase contributes in a paracrine manner to epithelial cell malignancy. J. Cell Biol., 140, 1535-1541 (1998).
- Miyauchi, T., Masuzawa, Y. and Muramatsu, T., The basigin group of the immunoglobulin superfamily: complete conservation of a segment in and around transmembrane domains of human and mouse basigin and chicken HT7 antigen. J. Biochem., 110, 770-774 (1991).
- Moriyama, T., Kataoka, H., Seguchi, K., Nabeshima, K., Kawano, H., Goya, T., Wakisaka, S. and Koono, M., Establishment and characterization of a new human glioblastoma cell line (MGM-1) with highly motile phenotype. Hum. Cell, 10, 105-110 (1997).
- Muraoka, K., Nabeshima, K., Murayama, T., Biswas, C. and Koono, M., Enhanced expression of a tumor-cell-derived collagenase-stimulatory factor in urothelial carcinoma: its usefulness as a tumor marker for bladder cancers. Int. J. Cancer, 55, 19-26 (1993).
- Nabeshima, K., Kishi, J., Kurogi, T., Komada, N., Kataoka, H., Okada, Y. and Koono, M., Stimulation of TIMP-1 and metalloproteinase production in co-cultures of human tumor cells and human fibroblasts. Cancer Lett., 78, 133-140 (1994).
- Nabeshima, K., Lane, W.S. and Biswas, C., Partial sequencing and characterization of the tumor cell-derived collagenase stimulatory factor. Arch. Biochem. Biophys., 285, 90-96 (1991).
- Nabeshima, K., Shimao, Y., Sato, S., Kataoka, H., Moriyama, T., Kawano, H., Wakisaka, S. and Koono, M., Expression of c-Met correlates with grade of malignancy in human astrocytic tumours: an immunohistochemical study. Histopathology, 31, 436-443 (1997).
- Nakada, M., Nakamura, H., Ikeda, E., Fujimoto, N., Yamashita, J., Sato, H., Seiki, M. and Okada, Y., Expression and tissue localization of membrane-types 1, 2 and 3 matrix metalloproteinases in human astrocytic tumors. Amer. J. Pathol., 154, 417-428 (1999).
- Nakano, A., Tani, E., Miyazaki, K., Yamamoto, Y. and Furuyama, J., Matrix metalloproteinases and tissue inhibitors of metalloproteinases in human gliomas. J. Neurosurg., 83, 298-307 (1995).
- Noël, A.C., Polette, M., Lewalle, J.M., Munaut, C., Emonard, H.P., Birembaut, P. and Foidart, J.M., Coordinate enhancement of gelatinase A mRNA and activity levels in human fibroblasts in response to breast-adenocarcinoma cells. Int. J. Cancer, 56, 331-336 (1994).
- Noël, A., Hajitou, A., L'Hoir, C., Maquoi, E., Baramova, E., Lewalle, J.M., Remacle, A., Kebers, F., Brown, P., Calberg-Bacq, C.M. and Foidart, J.M., Inhibition of stromal matrix metalloproteinases: effects of breast-tumor promotion by fibroblasts. Int. J. Cancer, 76, 267-273 (1998).
- Okada, A., Bellocq, J.P., Rouyer, N., Chenard, M.P., Rio, M.C., Chambon, P. and Basset, P., Membrane-type matrix metalloproteinase (MT-MMP) gene is expressed in stromal cells of human colon, breast and head and neck carcinomas. Proc. nat. Acad. Sci. Wash., 92, 2730-2734 (1995).
- Overall, C.M. and Sodek, J., Concanavalin A produces a matrix-degradative phenotype in human fibroblasts. J. biol. Chem., 265, 21141-21151 (1990).
- Polette, M., Gilles, C., Marchand, V., Lorenzato, M., Toole, B.P., Tournier, J.M., Zucker, S. and Birembaut, P., Tumor collagenase stimulatory factor (TCSF) expression and localization in human lung and breast cancers. J. Histochem. Cytochem., 45, 703-709 (1997).
- Poulsom, R., Hanby, A.M., Pignatelli, M., Jeffery, R.E., Longcroft, J.M., Rogers, L. and Stamp, G.W., Expression of gelatinase A and TIMP-2 mRNAs in desmoplastic fibroblasts in both mammary carcinomas and basal cell carcinoma of the skin. J. Clin. Pathol., 46, 429-436 (1993).
- Poulsom, R., Pignatelli, M., Stetler-Stevenson, W.G., Liotta, L.A., Wright, P.A., Jeffery, R.E., Longcroft, J.M., Rogers, L. and Stamp, G.W.H., Stromal expression of 72 kDa type IV collagenase (MMP-2) and TIMP-2 mRNAs in colorectal neoplasia. Amer. J. Pathol., 141, 389-396 (1992).
- Prescott, J., Troccoli, N. and Biswas, C., Coordinate increase in collagenase mRNA and enzyme levels in human fibroblasts treated with the tumor cell factor, TCSF. Biochem. Int., 19, 257-266 (1989).
- Pyke, C., Ralfkiaer, E., Huhtala, P., Hurskainen, T., Dano, K. and Tryggvason, K., Localization of messenger RNA for Mr 72000 and 92000 type IV collagenases in human skin cancers by in situ hybridization. Cancer Res., 52, 1336-1341 (1992).
- Sawaya, R.E., Yamamoto, M., Gokaslan, Z.L., Wang, S.W., Mohanam, S., Fuller, G.N., McCutcheon, I.E., Stetler-Stevenson, W.G., Nicolson, G.L. and Rao, J.S., Expression and localization of 72 kDa type IV collagenase (MMP-2) in human malignant gliomas in vitro. Clin. Exp. Metastasis, 14, 35-42 (1996).
- Schlosshauer, B. and Herzog, K.H., Neurothelin: inducible cell surface glycoprotein of blood-brain barrier-specific endothelial cells and distinct neurons. J. Cell Biol., 110, 1261-1274 (1990).
- Seulberger, H., Lottspeich, F. and Risau, W., The inducible blood-brain barrier specific molecule HT7 is a novel immunoglobulin-like cell surface glycoprotein. EMBO J., 9, 2151-2158 (1990).
- Uhm, J.H., Dooley, N.P., Villemure, J.G. and Young, V.W., Glioma invasion in vitro: regulation by matrix metalloprotease-2 and protein kinase C. Clin. Exp. Metastasis, 14, 421-433 (1996).
- Yamamoto, M., Mohanam, S., Sawaya, R., Fuller, G.N., Seiki, M., Sato, H., Gokaslan, Z.L., Liotta, L.A., Nicolson, G.L. and Rao, J.S., Differential expression of membrane-type matrix metalloproteinase and its correlation with gelatinase A activation in human malignant brain tumors in vivo and in vitro. Cancer Res., 56, 384-392 (1996).
- Zhang, H.F., Ong, W.Y., Leong, S.K. and Garey, L.J., Ultrastructural characteristics of blood vessels in the infant and adult human cerebral cortex. Histol. Histopathol., 12, 85-97 (1997).
Citing Literature
