Summary
The immunohistochemical distribution of tenascin (TN), fibronectin (FN), and laminin (LN) was investigated in 56 human gliomas (8 astrocytomas, 15 anaplastic astrocytomas, and 33 glioblastomas) with regards to the histological degree of malignancy and the degree of tumor cell differentiation evaluated by the staining of glial fibrillary acidic protein (GFAP). In 8 anaplastic astrocytomas and 28 glioblastomas, TN was predominantly immunolocalized in the basement membrane zone of the proliferating tumor vessels; sections of all astrocytomas were negative for TN staining. FN was localized in the basement membrane zone of the vessels in all astrocytomas, 12 anaplastic astrocytomas, and 22 glioblastomas. In 7 anaplastic astrocytomas and 19 glioblastomas, both TN and FN were expressed to various degrees in the tumor vessels. However, most of the TN-positive vessels did not express FN, and most of the FN-positive vessels were negative for TN staining. Furthermore, in 6 anaplastic astrocytomas and 12 glioblastomas, either TN of FN, but not both, were expressed in any area on serial sections. Most of the tumor cells around TN-positive, FN-negative tumor vessels did not express GFAP. On the other hand, GFAP was present in most tumor cells around TN-negative, FN-positive vessels. LN was detected in all vascular and pial-glial basement membrane zone of the tissues examined. These findings indicate that the degree of histological malignancy and the degree of cell dedifferentiation of human gliomas correlate well with the expression of TN, but are inversely correlated with the expression of FN. We postulate that the expression of TN, but not of FN, plays a role in the promotion of angiogenesis in malignant gliomas.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anbazhagan R, Sakakura T, Gusterson BA (1990) The distribution of immuno-reactive tenascin in the epithelialmesenchymal junktional areas of benign and malignant squamous epithelia. Virchows Arch [B] 59:59–63
Aufderheide E, Ekblom P (1988) Tenascin during gut development: appearance in the measenchyme, shift in molecular forms, and dependence on epithelial-mesenchymal interactions. J Cell Biol 107:2341–2349
Aufderheide E, Chiquet-Ehrismann R, Ekblom P (1987) Epithelial-mesenchymal interactions in the developing kidney lead to expression of tenascin in the mesenchyme. J Cell Biol 105:599–608
Bellon G, Caulet T, Cam Y, Pluot M, Poulin G, Pytlinska M, Bernard MH (1985) Immunohistochemical localisation of macromolecules of the basement membrane and extracellular matrix of human gliomas and meningiomas. Acta Neuropathol (Berl) 66:245–252
Bourdon MA, Ruoslahti E (1989) Tenascin mediates cell attachment through and RGD-dependent receptor. J Cell Biol 108:1149–1155
Bourdon MA, Wikstrand CJ, Furthmayr H, Matthews TJ, Bigner DD (1983) Human glioma-mesenchymal extracellular matrix antigen defined by monoclonal antibody. Cancer Res 43:2796–2805
Bronner-Fraser M (1988) Distribution and function of fenascin during cranial neural crest development in the chick. J Neurosci Res 21:135–147
Chiquet-Ehrismann R, Mackie EJ, Pearson CA, Sakakura T (1986) Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell 47:131–139
Chiquet-Ehrismann R, Kalla P, Pearson CA, Beck K, Chiquet M (1988) Tenascin interferes with fibronectin action. Cell 53:383–390
Crossin KL, Hoffman S, Grumet M, Thiery JP, Edelman GM (1986) Site-restricted expression of cytotactin during development of the chicken embryo. J Cell Biol 102:1917–1930
Erickson HP, Bourdon MA (1989) Tenascin: an extracellular matrix protein prominent in specialized embryonic tissue and tumors. Annu Rev Cell Biol 5:71–92
Fagan JB, Sobel ME, Yamada KM, de Crombrugghe B, Pastan I (1981) Effects of transformation on fibronectin gene expression using cloned fibronectin cDNA. J Biol Chem 256:520–525
Fulling KH, Garcia DM (1985) Anaplastic astrocytoma of the adult cerebrum. Prognostic value of histologic features. Cancer 55:928–931
Grant JW, Steart PV, Aguzzi A, Jones DB, Gallagher PJ (1989) Gliosarcoma: an immunohistochemical study. Acta Neuropatho 79:305–309
Grumet M, Hoffman S, Crossin KL, Edelman GM (1985) Cytotactin, an extracellular matrix protein of neural and non-neural tissue that mediates glia-neuron interaction. Proc Natl Acad Sci USA 82:8075–8079
Higuchi M, Ohnishi T, Arita N, Hiraga S, Iwasaki H, Hayakawa T, Mori S (1991) Immunohistochemical localization of fibronectin, laminin and fibronectin-receptor in human malignant gliomas: in relation to tumor invasion. Brain Nerve (Tokyo) 43:17–23
Hølund B, Clausen PP, Clemensen I (1981) The influence of fixation and tissue preparation on the immunohistochemical demonstration of fibronectin in human tissue. Histochemistry 72:291–299
Jones FS, Burgoon MP, Hoffman S, Crossin KL, Cunningham BA, Edelman GM (1988) A cDNA clone for cytotactin contains sequences similar to epidermal growth factor-like repeats segments of fibronectin and fibrinogen. Proc Natl Acad Sci USA 85:2186–2190
Jones TR, Bigner SH, Schold SC, Eng LF, Bigner DD (1981) Anaplastic human gliomas grown in athymic mice. Morphology and glial fibrillary acidic protein expression. Am J Pathol 105:315–327
Koukoulis GK, Gould VE, Bhattacharyya A, Gould JE, Howeedy AA, Virtanen I (1991) Tenascin in normal, reactive, hyperplastic, and neoplastic tissues: Biologic and pathologic implications. Hum Pathol 22:636–643
Laywell ED, Dorries U, Bartsch U, Faissner A, Schachner M, Steindler DA (1992) Enhanced expression of the developmentally regulated extracellular matrix molecule tenascin following adult brain injury. Proc Natl Acad Sci USA 89:2634–2638
Lightner VA, Gumkowski F, Bigner DD, Erickson HP (1989) Tenascin/hexabrachion in human skin: biochemical identification and localization by light and electron microscopy. J Cell Biol 108:2483–2493
Lotz MM, Burdsal CA, Erckson HP, McClay DR (1989) Cell adhesion to fibronectin and tenascin: quantitative measurements of initial binding and subsequent strengthening response. J Cell Biol 109, 1795–1805
Mackie EJ, Chiquet-Ehrismann R, Pearson CA, Inaguma Y, Taya K, Kawarada Y, Sakakura T (1987) Tenascin is a stromal marker for epithelial malignancy in the mammary gland. Proc Natl Acad Sci USA 84:4621–4625
Mackie EJ, Thesleff I, Chiquet-Ehrismann R (1987) Tenascin is associated with chondrogenic and osteogenic differentiation in vivo and promotes chondrogenesis in vitro. J Cell Biol 105:2569–2579
Mackie EJ, Halfter W, Liverani D (1988) Induction of tenascin in healing wounds. J Cell Biol 107:2757–2767
Mauro A, Bertolotto A, Germano J, Giaccone G, Giordana MT, Migheli A, Schiffer D (1984) Collagenase in the immunohistochemical demonstration of laminin, fibronectin and factor VIII/RAg in nervous tissue after fixation. Histochemistry 80:157–163
McComb RD, Bigner DD (1985) Immunolocalization of monoclonal antibody-defined extracellular matrix antigens in human brain tumors. J Neurooncol 3:181–186
McComb RD, Miller KA (1990) Developmental and reactive expression of tenascin (TN) in the human cerebellum. J Neuropathol Exp Neurol 49:344
Ohnishi T, Arita N, Hiraga S, Higuchi M, Hayakawa T (1991) Human malignant glioma cells migrate to fibronectin and laminin: role of extracellular matrix components in glioma cell invasion. In: Tabuchi K (ed) Biological aspects of brain tumors. Springer-Verlag, Tokyo, pp408–415
Paulus W, Sage EH, Liszka U, Iruela-Arispe ML, Jellinger K (1991) Increased levels of type VIII collagen in human brain tumours compared to normal brain tissue and non-neoplastic cerebral disorders.
Russell DS, Rubinstein LJ (1989) Tumours of central neuroepithelial origin. In: Pathology of tumours of the nervous system. 5th edn. Edward Arnold, London, pp 83–350
Rutka JT, Mayatt CA, Giblin JR, Davis RL, Rosenblum ML (1987) Distribution of extracellular matrix proteins in primary human brain tumours: an immunohistochemical analysis. Can J Neurol Sci 14:25–30
Schiffer D (1991) Patterns of tumor growth. In: Salcman M (ed) Neurobiology of brain tumors. Williams & Wilkins, Baltimore, pp 102–135
Schiffer D, Giordana MT, Mauro A, Migheli A (1984) GFAP, FVIII/RAg, laminin, and fibronectin in gliosarcomas: an immunohistochemcial study. Acta Neuropathol (Berl) 63:108–116
Shi ZR, Itzkowitz SH, Kim YS (1988) A comparison of three immunoperoxidase techniques for antigen detection in colorectal carcinoma tissues. J Histochem Cytochem 36:317–322
Spring J, Beck K, Chiquet-Ehrisman R (1989) Two contrary function of tenascin: dissection of the active sites by recombinant tenascin fragments. Cell 59:325–334
Thesleff I, Mackie E, Vainio S, Chiquet-Ehrismann R (1987) Change in the distribution of tenascin during tooth development. Development 101:289–296
Vaheri A, Ruoslahti E (1974) Disappearance of a major cell-type specific surface glycoprotein antigen (SF) after transformation of fibroblasts by Rous sarcoma virus. Int J Cancer 13:579–586
Zülch KJ (1979) Histologic typing of tumors of the central nervous system. International classification of tumors. World Health Organization Geneva, No. 21
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Higuchi, M., Ohnishi, T., Arita, N. et al. Expression of tenascin in human gliomas: its relation to histological malignancy, tumor dedifferentiation and angiogenesis. Acta Neuropathol 85, 481–487 (1993). https://doi.org/10.1007/BF00230486
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00230486