Abstract
Rabbit antisera against tenascin, a large extracellular matrix protein, in conjunction with monoclonal antibodies of mouse origin against versican, a large hyaluronate-binding proteoglycan, were used to make a comparative study of the distribution of the two antigens in the same cryostat sections by double immunofluorescence. In the central nervous system, tenascin was invariably associated with versican, but the reverse was not true, in that versican was also found where tenascin was not detectable, particularly in gray matter. There were major species differences in the distribution of tenascin in the central nervous system. In the cow, tenascin was found in cerebral and spinal cord white matter and in the granule cell layer of the cerebellum. In the human brain, tenascin was found in cerebral white matter but not in the cerebellum. In the rat, tenascin was mainly confined to brain periventricular layer and spinal cord white matter. During the development of the cerebellum of the rat, the tenascin immunoreactivity decreased, and a lower molecular weight band appeared (J1-160/180/restrictin?) and persisted throughout adulthood. Tenascin expression was a relatively late event in the development of the rat central nervous system, immunoreactivity being first observed after birth. In the rat embryo, tenascin was found to co-localize with versican in precartilaginous mesenchyme and in connective tissue underlying epithelia. The colocalization of versican with tenascin suggests that versican may be the tenascin (cytotactin)-associated proteoglycan reported in the literature.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Asher R, Perides G, Vanderhaeghen J-J, Bignami A (1991) The extracellular matrix of central nervous system white matter: demonstration of an hyaluronate-protein complex. J Neurosci Res 28:410–421
Aukhil I, Slemp CC, Lightner VA, Nishimura K, Briscoe G, Erickson HP (1990) Purification of hexabrachion (tenascin) from cell culture conditioned medium, and separation from a cell adhesion factor. Matrix 10:98–111
Bartsch S, Bartsch U, Dörries U, Faissner A, Weller A, Ekblom P, Schachner M (1992) Expression of tenascin in the developing and adult cerebellar cortex. J Neurosci 12:736–749
Bignami A, Asher R (1992) Some observations on the localization of hyaluronic acid in adult, newborn and embryonal rat brain. Int J Dev Neurosci 10:45–58
Bignami A, Dahl D (1986a) Brain-specific hyaluronate-binding protein: an immunohistological study with monoclonal antibodies of human and bovine CNS. Proc Natl Acad Sci USA 83:3518–3522
Bignami A, Dahl D (1986b) Brain-specific hyaluronate-binding protein. A product of white matter astrocytes? J Neurocytol 15:671–679
Bignami A, Asher R, Perides G, Rahemtulla F (1992) The extracellular matrix of cerebral gray matter: Golgi's pericellular net and Nissl's nervöses Grau revisited. Int J Dev Neurosci 10:291–299
Bignami A, Perides G, Rahemtulla F (1993) Versican, a hyaluronate-binding proteoglycan of embryonal precartilaginous mesenchyma, is mainly expressed postnatally in rat brain. J Neurosci Res 34:97–106
Bratt P, Anderson MM, Månsson-Rahemtulla B, Stevens JW, Zhou C, Rahemtulla F (1992) Isolation and characterization of bovine gingival proteoglycans versican and decorin. Int J Biochem 24:1573–1583
Chiquet M (1989) Tenascin/J1/cytotactin: the potential function of hexabrachion proteins in neural development. Dev Neurosci 11:266–275
Chiquet M, Fambrough DM (1984) Chick myotendinous antigen Il. A novel extracellular matrix glycoprotein complex consisting of large disulfide-linked subunits. J Cell Biol 98:1937–1946
Chuong C-M, Crossin KL, Edelman GM (1987) Sequential expression and differential function of multiple adhesion molecules during the formation of cerebellar cortical layers. J Cell Biol 104:331–342
Dahl D, Grossi M, Bignami A (1984) Masking of epitopes in tissue sections. A study of glial fibrillary acidic (GFA) protein with antisera and monoclonal antibodies. Histochemistry 81:525–531
Edelman GM, Jones FS (1992) Cytotactin: a morphoregulatory molecule and a target for regulation by homeobox gene products. Trends Biochem Sci 17:228–232
Erickson HP (1993) Tenascin-C, tenascin-R, and tenascin X — a family of talented proteins in search of functions. Curr Opin Cell Biol (in press)
Erickson HP, Bourdon MA (1989) Tenascin: an extracellular matrix protein prominent in specialized embryonic tissues and tumors. Ann Rev Cell Biol 5:71–92
Faissner A, Kruse J, Chiquet-Ehrismann R, Mackie E (1988) The high-molecular-weight J1 glycoproteins are immunochemically related to tenascin. Differentiation 37:104–11
Fryer HGL, Kelly GM, Molinaro L, Hockfield S (1992) The high molecular weight Cat-301 chondroitin sulfate proteoglycan from brain is related to the large aggregating proteoglycan from cartilage, aggrecan. J Biol Chem 267:9874–9883
Hoffman S, Edelman GM (1987) A proteoglycan with HNK-1 antigenic determinants is a neuron-associated ligand for cytotactin. Proc Natl Acad Sci USA 84:2523–2527
Hoffman S, Crossin KL, Edelman GM (1988) Molecular forms, binding functions and developmental expression patterns of cytotactin and cytotactin-binding proteoglycan, an interactive pair of extracellular matrix molecules. J Cell Biol 106:519–532
Husmann K, Faissner A, Schachner M (1992) Tenascin promotes cerebellar granule cell migration and neurite outgrowth by different domains in the fibronectin type III repeats. J Cell Biol 116:1475–1486
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
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
Miragall F, Kadmon G, Faissner A, Antonicek H, Schachner M (1990) Retention of J1/tenascin and the polysialylated form of the neural cell adhesion molecule (N-CAM) in the adult olfactory bulb. J Neurocytol 19:899–914
Nörenberg U, Wille H, Wolff JM, Frank R, Rathjen FG (1992) The chicken neural extracellular matrix molecule restrictin: similarity with EFG, fibronectin type-III, and fibrinogen-like motifs. Neuron 8:849–864
Perides G, Lane WS, Andrews D, Dahl D, Bignami A (1989) Isolation and partial characterization of a glial hyaluronatebinding protein. J Biol Chem 264:5981–5987
Perides G, Rahemtulla F, Lane WS, Asher RA, Bignami A (1992) Isolation of a large aggregating proteoglycan from human brain. J Biol Chem 267:23883–23887
Prieto AL, Jones FS, Cunningham BA, Crossin KL, Edelman GM (1990) Localization during development of alternative spliced forms of cytotactin mRNA by in situ hybridization. J Cell Biol 111:685–698
Rettig WJ, Garin-Chesa P, Beresford HR, Melamed MR, Old LJ (1988) Definition of an extracellular protein in rostral portions of the human central nervous system. Brain Res 438:315–322
Rettig WJ, Hoffman S, Su SL, Garin-Chesa P (1992) Species diversity of neuronectin and cytotactin expression patterns in the vertebrate central nervous system. Brain Res 590:219–228
Saga Y, Yagi T, Ikawa Y, Sakakura T, Aizawa S (1992) Mice develop normally without tenascin. Genes Dev 6:1821–1831
Shinomura T, Jensen KL, Yamagata M, Kimata K, Solursh M (1990) The distribution of mesenchyma proteoglycan (PG-M) during wing bud outgrowth. Anat Embryol 181:227–233
Shinomura T, Nishida Y, Kimata K (1992) A large chondroitin sulfate protelgycan (PG-M) and cartilage differentiation. In: Kuetner K et al. (eds) Articular cartilage and osteoarthritis. Raven Press, New York, pp 35–44
Steindler DA, Cooper NGF, Faissner A, Schachner M (1989) Boundaries defined by adhesion molecules during development of the cerebral cortex: the J1/tenascin glycoprotein in the mouse somatosensory cortical barrel field. Dev Biol 131:243–260
Taylor HC, Lightner VA, Beyer WF Jr, McCashin D, Briscoe G, Erickson HP (1989) Biochemical and structural studies of tenascin/hexabrachion proteins. J Cell Biochem 41:71–90
Towbin H, Stehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedures and some applications. Proc Natl Acad Sci USA 76:4350–4354
Vaughan L, Huker S, Chiquet M, Winterhalter KH (1987) A major six armed glycoprotein from embryonic cartilage. EMBO J 6:349–353
Zimmermann DR, Ruoslahti E (1989) Multiple domains of the large fibroblast proteoglycan, versican. EMBO J 8:2975–2981
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Perides, G., Erickson, H.P., Rahemtulla, F. et al. Colocalization of tenascin with versican, a hyaluronate-binding chondroitin sulfate proteoglycan. Anat Embryol 188, 467–479 (1993). https://doi.org/10.1007/BF00190141
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00190141