Abstract
The extracellular matrix molecule tenascin has been implicated in neuron-glia recognition in the developing central and peripheral nervous system and in regeneration. In this study, its role in Bergmann glial process-mediated neuronal migration was assayed in vitro using tissue explants of the early postnatal mouse cerebellar cortex. Of the five mAbs reacting with nonoverlapping epitopes on tenascin, mAbs J1/tn1, J1/tn4, and J1/tn5, but not mAbs J1/tn2 and J1/tn3 inhibited granule cell migration. Localization of the immunoreactive domains by EM of rotary shadowed tenascin molecules revealed that the mAbs J1/tn4 and J1/tn5, like the previously described J1/tn1 antibody, bound between the third and fifth fibronectin type III homologous repeats and mAb J1/tn3 bound between the third and fifth EGF-like repeats. mAb J1/tn2 had previously been found to react between fibronectin type III homologous repeats 10 and 11 of the mouse molecule (Lochter, A., L. Vaughan, A. Kaplony, A. Prochiantz, M. Schachner, and A. Faissner. 1991. J. Cell Biol. 113:1159-1171). When postnatal granule cell neurons were cultured on tenascin adsorbed to polyornithine, both the percentage of neurite-bearing cells and the length of outgrowing neurites were increased when compared to neurons growing on polyornithine alone. This neurite outgrowth promoting effect of tenascin was abolished only by mAb J1/tn2 or tenascin added to the culture medium in soluble form. The other antibodies did not modify the stimulatory or inhibitory effects of the molecule. These observations indicate that tenascin influences neurite outgrowth and migration of cerebellar granule cells by different domains in the fibronectin type III homologous repeats.
Full Text
The Full Text of this article is available as a PDF (2.0 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Antonicek H., Persohn E., Schachner M. Biochemical and functional characterization of a novel neuron-glia adhesion molecule that is involved in neuronal migration. J Cell Biol. 1987 Jun;104(6):1587–1595. doi: 10.1083/jcb.104.6.1587. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Aufderheide E., Ekblom P. Tenascin during gut development: appearance in the mesenchyme, shift in molecular forms, and dependence on epithelial-mesenchymal interactions. J Cell Biol. 1988 Dec;107(6 Pt 1):2341–2349. doi: 10.1083/jcb.107.6.2341. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bourdon M. A., Wikstrand C. J., Furthmayr H., Matthews T. J., Bigner D. D. Human glioma-mesenchymal extracellular matrix antigen defined by monoclonal antibody. Cancer Res. 1983 Jun;43(6):2796–2805. [PubMed] [Google Scholar]
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
- Bronner-Fraser M. Distribution and function of tenascin during cranial neural crest development in the chick. J Neurosci Res. 1988 Oct-Dec;21(2-4):135–147. doi: 10.1002/jnr.490210206. [DOI] [PubMed] [Google Scholar]
- Burgoon M. P., Grumet M., Mauro V., Edelman G. M., Cunningham B. A. Structure of the chicken neuron-glia cell adhesion molecule, Ng-CAM: origin of the polypeptides and relation to the Ig superfamily. J Cell Biol. 1991 Mar;112(5):1017–1029. doi: 10.1083/jcb.112.5.1017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chiquet-Ehrismann R., Kalla P., Pearson C. A., Beck K., Chiquet M. Tenascin interferes with fibronectin action. Cell. 1988 May 6;53(3):383–390. doi: 10.1016/0092-8674(88)90158-4. [DOI] [PubMed] [Google Scholar]
- Chiquet-Ehrismann R., Mackie E. J., Pearson C. A., Sakakura T. Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell. 1986 Oct 10;47(1):131–139. doi: 10.1016/0092-8674(86)90374-0. [DOI] [PubMed] [Google Scholar]
- Chiquet M., Fambrough D. M. Chick myotendinous antigen. I. A monoclonal antibody as a marker for tendon and muscle morphogenesis. J Cell Biol. 1984 Jun;98(6):1926–1936. doi: 10.1083/jcb.98.6.1926. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chiquet M., Fambrough D. M. Chick myotendinous antigen. II. A novel extracellular glycoprotein complex consisting of large disulfide-linked subunits. J Cell Biol. 1984 Jun;98(6):1937–1946. doi: 10.1083/jcb.98.6.1937. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chuong C. M., Crossin K. L., Edelman G. M. Sequential expression and differential function of multiple adhesion molecules during the formation of cerebellar cortical layers. J Cell Biol. 1987 Feb;104(2):331–342. doi: 10.1083/jcb.104.2.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Collins F. Induction of neurite outgrowth by a conditioned-medium factor bound to the culture substratum. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5210–5213. doi: 10.1073/pnas.75.10.5210. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Crossin K. L., Hoffman S., Tan S. S., Edelman G. M. Cytotactin and its proteoglycan ligand mark structural and functional boundaries in somatosensory cortex of the early postnatal mouse. Dev Biol. 1989 Dec;136(2):381–392. doi: 10.1016/0012-1606(89)90264-9. [DOI] [PubMed] [Google Scholar]
- Crossin K. L., Prieto A. L., Hoffman S., Jones F. S., Friedlander D. R. Expression of adhesion molecules and the establishment of boundaries during embryonic and neural development. Exp Neurol. 1990 Jul;109(1):6–18. doi: 10.1016/s0014-4886(05)80004-4. [DOI] [PubMed] [Google Scholar]
- Daniloff J. K., Crossin K. L., Pinçon-Raymond M., Murawsky M., Rieger F., Edelman G. M. Expression of cytotactin in the normal and regenerating neuromuscular system. J Cell Biol. 1989 Feb;108(2):625–635. doi: 10.1083/jcb.108.2.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Epperlein H. H., Halfter W., Tucker R. P. The distribution of fibronectin and tenascin along migratory pathways of the neural crest in the trunk of amphibian embryos. Development. 1988 Aug;103(4):743–756. doi: 10.1242/dev.103.4.743. [DOI] [PubMed] [Google Scholar]
- Erickson H. P., Bourdon M. A. Tenascin: an extracellular matrix protein prominent in specialized embryonic tissues and tumors. Annu Rev Cell Biol. 1989;5:71–92. doi: 10.1146/annurev.cb.05.110189.000443. [DOI] [PubMed] [Google Scholar]
- Erickson H. P., Inglesias J. L. A six-armed oligomer isolated from cell surface fibronectin preparations. Nature. 1984 Sep 20;311(5983):267–269. doi: 10.1038/311267a0. [DOI] [PubMed] [Google Scholar]
- Faissner A., Kruse J., Chiquet-Ehrismann R., Mackie E. The high-molecular-weight J1 glycoproteins are immunochemically related to tenascin. Differentiation. 1988;37(2):104–114. doi: 10.1111/j.1432-0436.1988.tb00802.x. [DOI] [PubMed] [Google Scholar]
- Faissner A., Kruse J. J1/tenascin is a repulsive substrate for central nervous system neurons. Neuron. 1990 Nov;5(5):627–637. doi: 10.1016/0896-6273(90)90217-4. [DOI] [PubMed] [Google Scholar]
- Fischer G. Cultivation of mouse cerebellar cells in serum free, hormonally defined media: survival of neurons. Neurosci Lett. 1982 Mar 5;28(3):325–329. doi: 10.1016/0304-3940(82)90079-9. [DOI] [PubMed] [Google Scholar]
- Fischer G., Künemund V., Schachner M. Neurite outgrowth patterns in cerebellar microexplant cultures are affected by antibodies to the cell surface glycoprotein L1. J Neurosci. 1986 Feb;6(2):605–612. doi: 10.1523/JNEUROSCI.06-02-00605.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Friguet B., Djavadi-Ohaniance L., Pages J., Bussard A., Goldberg M. A convenient enzyme-linked immunosorbent assay for testing whether monoclonal antibodies recognize the same antigenic site. Application to hybridomas specific for the beta 2-subunit of Escherichia coli tryptophan synthase. J Immunol Methods. 1983 Jun 10;60(3):351–358. doi: 10.1016/0022-1759(83)90292-2. [DOI] [PubMed] [Google Scholar]
- Fujita S. Quantitative analysis of cell proliferation and differentiation in the cortex of the postnatal mouse cerebellum. J Cell Biol. 1967 Feb;32(2):277–287. doi: 10.1083/jcb.32.2.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fuss B., Pott U., Fischer P., Schwab M. E., Schachner M. Identification of a cDNA clone specific for the oligodendrocyte-derived repulsive extracellular matrix molecule J1-160/180. J Neurosci Res. 1991 Jul;29(3):299–307. doi: 10.1002/jnr.490290305. [DOI] [PubMed] [Google Scholar]
- Gloor S., Antonicek H., Sweadner K. J., Pagliusi S., Frank R., Moos M., Schachner M. The adhesion molecule on glia (AMOG) is a homologue of the beta subunit of the Na,K-ATPase. J Cell Biol. 1990 Jan;110(1):165–174. doi: 10.1083/jcb.110.1.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grumet M., Hoffman S., Crossin K. L., Edelman G. M. Cytotactin, an extracellular matrix protein of neural and non-neural tissues that mediates glia-neuron interaction. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8075–8079. doi: 10.1073/pnas.82.23.8075. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Halfter W., Chiquet-Ehrismann R., Tucker R. P. The effect of tenascin and embryonic basal lamina on the behavior and morphology of neural crest cells in vitro. Dev Biol. 1989 Mar;132(1):14–25. doi: 10.1016/0012-1606(89)90200-5. [DOI] [PubMed] [Google Scholar]
- Hatten M. E., Liem R. K., Mason C. A. Two forms of cerebellar glial cells interact differently with neurons in vitro. J Cell Biol. 1984 Jan;98(1):193–204. doi: 10.1083/jcb.98.1.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Houck D. W., Loken M. R. Simultaneous analysis of cell surface antigens, bromodeoxyuridine incorporation and DNA content. Cytometry. 1985 Nov;6(6):531–538. doi: 10.1002/cyto.990060607. [DOI] [PubMed] [Google Scholar]
- Jhaveri S., Erzurumlu R. S., Crossin K. Barrel construction in rodent neocortex: role of thalamic afferents versus extracellular matrix molecules. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4489–4493. doi: 10.1073/pnas.88.10.4489. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones F. S., Hoffman S., Cunningham B. A., Edelman G. M. A detailed structural model of cytotactin: protein homologies, alternative RNA splicing, and binding regions. Proc Natl Acad Sci U S A. 1989 Mar;86(6):1905–1909. doi: 10.1073/pnas.86.6.1905. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kaplony A., Zimmermann D. R., Fischer R. W., Imhof B. A., Odermatt B. F., Winterhalter K. H., Vaughan L. Tenascin Mr 220,000 isoform expression correlates with corneal cell migration. Development. 1991 Jun;112(2):605–614. doi: 10.1242/dev.112.2.605. [DOI] [PubMed] [Google Scholar]
- Kearney J. F., Radbruch A., Liesegang B., Rajewsky K. A new mouse myeloma cell line that has lost immunoglobulin expression but permits the construction of antibody-secreting hybrid cell lines. J Immunol. 1979 Oct;123(4):1548–1550. [PubMed] [Google Scholar]
- Keilhauer G., Faissner A., Schachner M. Differential inhibition of neurone-neurone, neurone-astrocyte and astrocyte-astrocyte adhesion by L1, L2 and N-CAM antibodies. Nature. 1985 Aug 22;316(6030):728–730. doi: 10.1038/316728a0. [DOI] [PubMed] [Google Scholar]
- Kruse J., Keilhauer G., Faissner A., Timpl R., Schachner M. The J1 glycoprotein--a novel nervous system cell adhesion molecule of the L2/HNK-1 family. Nature. 1985 Jul 11;316(6024):146–148. doi: 10.1038/316146a0. [DOI] [PubMed] [Google Scholar]
- Kruse J., Mailhammer R., Wernecke H., Faissner A., Sommer I., Goridis C., Schachner M. Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature. 1984 Sep 13;311(5982):153–155. doi: 10.1038/311153a0. [DOI] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Lagenaur C., Sommer I., Schachner M. Subclass of astroglia in mouse cerebellum recognized by monoclonal antibody. Dev Biol. 1980 Oct;79(2):367–378. doi: 10.1016/0012-1606(80)90122-0. [DOI] [PubMed] [Google Scholar]
- Lawler J. The structural and functional properties of thrombospondin. Blood. 1986 May;67(5):1197–1209. [PubMed] [Google Scholar]
- Lehmann S., Kuchler S., Theveniau M., Vincendon G., Zanetta J. P. An endogenous lectin and one of its neuronal glycoprotein ligands are involved in contact guidance of neuron migration. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6455–6459. doi: 10.1073/pnas.87.16.6455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lindner J., Guenther J., Nick H., Zinser G., Antonicek H., Schachner M., Monard D. Modulation of granule cell migration by a glia-derived protein. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4568–4571. doi: 10.1073/pnas.83.12.4568. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lindner J., Orkand P. M., Schachner M. Histotypic pattern formation in cerebellar reaggregate cultures in the presence of antibodies to L1 cell surface antigen. Neurosci Lett. 1985 Apr 9;55(2):145–149. doi: 10.1016/0304-3940(85)90010-2. [DOI] [PubMed] [Google Scholar]
- Lindner J., Rathjen F. G., Schachner M. L1 mono- and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. 1983 Sep 29-Oct 5Nature. 305(5933):427–430. doi: 10.1038/305427a0. [DOI] [PubMed] [Google Scholar]
- Lochter A., Vaughan L., Kaplony A., Prochiantz A., Schachner M., Faissner A. J1/tenascin in substrate-bound and soluble form displays contrary effects on neurite outgrowth. J Cell Biol. 1991 Jun;113(5):1159–1171. doi: 10.1083/jcb.113.5.1159. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lotz M. M., Burdsal C. A., Erickson H. P., McClay D. R. Cell adhesion to fibronectin and tenascin: quantitative measurements of initial binding and subsequent strengthening response. J Cell Biol. 1989 Oct;109(4 Pt 1):1795–1805. doi: 10.1083/jcb.109.4.1795. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MIALE I. L., SIDMAN R. L. An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp Neurol. 1961 Oct;4:277–296. doi: 10.1016/0014-4886(61)90055-3. [DOI] [PubMed] [Google Scholar]
- Mackie E. J., Tucker R. P., Halfter W., Chiquet-Ehrismann R., Epperlein H. H. The distribution of tenascin coincides with pathways of neural crest cell migration. Development. 1988 Jan;102(1):237–250. doi: 10.1242/dev.102.1.237. [DOI] [PubMed] [Google Scholar]
- Martini R., Schachner M., Faissner A. Enhanced expression of the extracellular matrix molecule J1/tenascin in the regenerating adult mouse sciatic nerve. J Neurocytol. 1990 Aug;19(4):601–616. doi: 10.1007/BF01257247. [DOI] [PubMed] [Google Scholar]
- Moonen G., Grau-Wagemans M. P., Selak I. Plasminogen activator-plasmin system and neuronal migration. Nature. 1982 Aug 19;298(5876):753–755. doi: 10.1038/298753a0. [DOI] [PubMed] [Google Scholar]
- Nies D. E., Hemesath T. J., Kim J. H., Gulcher J. R., Stefansson K. The complete cDNA sequence of human hexabrachion (Tenascin). A multidomain protein containing unique epidermal growth factor repeats. J Biol Chem. 1991 Feb 15;266(5):2818–2823. [PubMed] [Google Scholar]
- O'Shea K. S., Rheinheimer J. S., Dixit V. M. Deposition and role of thrombospondin in the histogenesis of the cerebellar cortex. J Cell Biol. 1990 Apr;110(4):1275–1283. doi: 10.1083/jcb.110.4.1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Persohn E., Schachner M. Immunoelectron microscopic localization of the neural cell adhesion molecules L1 and N-CAM during postnatal development of the mouse cerebellum. J Cell Biol. 1987 Jul;105(1):569–576. doi: 10.1083/jcb.105.1.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pesheva P., Spiess E., Schachner M. J1-160 and J1-180 are oligodendrocyte-secreted nonpermissive substrates for cell adhesion. J Cell Biol. 1989 Oct;109(4 Pt 1):1765–1778. doi: 10.1083/jcb.109.4.1765. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Poltorak M., Sadoul R., Keilhauer G., Landa C., Fahrig T., Schachner M. Myelin-associated glycoprotein, a member of the L2/HNK-1 family of neural cell adhesion molecules, is involved in neuron-oligodendrocyte and oligodendrocyte-oligodendrocyte interaction. J Cell Biol. 1987 Oct;105(4):1893–1899. doi: 10.1083/jcb.105.4.1893. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rakic P. Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study in Macacus Rhesus. J Comp Neurol. 1971 Mar;141(3):283–312. doi: 10.1002/cne.901410303. [DOI] [PubMed] [Google Scholar]
- Rakic P. Principles of neural cell migration. Experientia. 1990 Sep 15;46(9):882–891. doi: 10.1007/BF01939380. [DOI] [PubMed] [Google Scholar]
- Rathjen F. G. A neurite outgrowth-promoting molecule in developing fiber tracts. Trends Neurosci. 1988 May;11(5):183–184. doi: 10.1016/0166-2236(88)90116-6. [DOI] [PubMed] [Google Scholar]
- Rathjen F. G., Schachner M. Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J. 1984 Jan;3(1):1–10. doi: 10.1002/j.1460-2075.1984.tb01753.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Riou J. F., Shi D. L., Chiquet M., Boucaut J. C. Exogenous tenascin inhibits mesodermal cell migration during amphibian gastrulation. Dev Biol. 1990 Feb;137(2):305–317. doi: 10.1016/0012-1606(90)90256-i. [DOI] [PubMed] [Google Scholar]
- Sanes J. R. Extracellular matrix molecules that influence neural development. Annu Rev Neurosci. 1989;12:491–516. doi: 10.1146/annurev.ne.12.030189.002423. [DOI] [PubMed] [Google Scholar]
- Schuch U., Lohse M. J., Schachner M. Neural cell adhesion molecules influence second messenger systems. Neuron. 1989 Jul;3(1):13–20. doi: 10.1016/0896-6273(89)90111-6. [DOI] [PubMed] [Google Scholar]
- Siri A., Carnemolla B., Saginati M., Leprini A., Casari G., Baralle F., Zardi L. Human tenascin: primary structure, pre-mRNA splicing patterns and localization of the epitopes recognized by two monoclonal antibodies. Nucleic Acids Res. 1991 Feb 11;19(3):525–531. doi: 10.1093/nar/19.3.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spring J., Beck K., Chiquet-Ehrismann R. Two contrary functions of tenascin: dissection of the active sites by recombinant tenascin fragments. Cell. 1989 Oct 20;59(2):325–334. doi: 10.1016/0092-8674(89)90294-8. [DOI] [PubMed] [Google Scholar]
- Steindler D. A., Cooper N. G., Faissner A., Schachner M. Boundaries defined by adhesion molecules during development of the cerebral cortex: the J1/tenascin glycoprotein in the mouse somatosensory cortical barrel field. Dev Biol. 1989 Jan;131(1):243–260. doi: 10.1016/s0012-1606(89)80056-9. [DOI] [PubMed] [Google Scholar]
- Steindler D. A., O'Brien T. F., Laywell E., Harrington K., Faissner A., Schachner M. Boundaries during normal and abnormal brain development: in vivo and in vitro studies of glia and glycoconjugates. Exp Neurol. 1990 Jul;109(1):35–56. doi: 10.1016/s0014-4886(05)80007-x. [DOI] [PubMed] [Google Scholar]
- Stern C. D., Norris W. E., Bronner-Fraser M., Carlson G. J., Faissner A., Keynes R. J., Schachner M. J1/tenascin-related molecules are not responsible for the segmented pattern of neural crest cells or motor axons in the chick embryo. Development. 1989 Oct;107(2):309–319. doi: 10.1242/dev.107.2.309. [DOI] [PubMed] [Google Scholar]
- Stitt T. N., Hatten M. E. Antibodies that recognize astrotactin block granule neuron binding to astroglia. Neuron. 1990 Nov;5(5):639–649. doi: 10.1016/0896-6273(90)90218-5. [DOI] [PubMed] [Google Scholar]
- Tan S. S., Crossin K. L., Hoffman S., Edelman G. M. Asymmetric expression in somites of cytotactin and its proteoglycan ligand is correlated with neural crest cell distribution. Proc Natl Acad Sci U S A. 1987 Nov;84(22):7977–7981. doi: 10.1073/pnas.84.22.7977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vaughan L., Huber S., Chiquet M., Winterhalter K. H. A major, six-armed glycoprotein from embryonic cartilage. EMBO J. 1987 Feb;6(2):349–353. doi: 10.1002/j.1460-2075.1987.tb04761.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wehrle B., Chiquet M. Tenascin is accumulated along developing peripheral nerves and allows neurite outgrowth in vitro. Development. 1990 Oct;110(2):401–415. doi: 10.1242/dev.110.2.401. [DOI] [PubMed] [Google Scholar]
- Weller A., Beck S., Ekblom P. Amino acid sequence of mouse tenascin and differential expression of two tenascin isoforms during embryogenesis. J Cell Biol. 1991 Jan;112(2):355–362. doi: 10.1083/jcb.112.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]