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The glia-derived extracellular matrix glycoprotein tenascin-C promotes embryonic and postnatal retina axon outgrowth via the alternatively spliced fibronectin type III domain TNfnD

Published online by Cambridge University Press:  10 June 2009

Sonia Siddiqui ,
Andrea Horvat-Bröcker  and
Andreas Faissner
Sonia Siddiqui
Affiliation:
Department of Cell Morphology and Molecular Neurobiology, Ruhr-University, Bochum, Germany International Graduate School of Neuroscience (IGSN), Ruhr-University, Germany
Andrea Horvat-Bröcker
Affiliation:
Department of Cell Morphology and Molecular Neurobiology, Ruhr-University, Bochum, Germany
Andreas Faissner*
Affiliation:
Department of Cell Morphology and Molecular Neurobiology, Ruhr-University, Bochum, Germany
*
Correspondence should be addressed to: Andreas Faissner, Ruhr-University, Department of Cell Morphology and Molecular Neurobiology, Building NDEF 05/594 Universitaetsstr. 150, D-44801 Bochum, Germany phone: +49234 3223851 email: andreas.faissner@ruhr-uni-bochum.de
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Abstract

Tenascin-C (Tnc) is an astrocytic multifunctional extracellular matrix (ECM) glycoprotein that potentially promotes or inhibits neurite outgrowth. To investigate its possible functions for retinal development, explants from embryonic day 18 (E18) rat retinas were cultivated on culture substrates composed of poly-d-lysine (PDL), or PDL additionally coated with Tnc or laminin (LN)-1, which significantly increased fiber length. When combined with LN, Tnc induced axon fasciculation that reduced the apparent number of outgrowing fibers. In order to circumscribe the stimulatory region, Tnc-derived fibronectin type III (TNfn) domains fused to the human Ig-Fc-fragment TNfnD6-Fc, TNfnBD-Fc, TNFnA1A2-Fc and TNfnA1D-Fc were studied. The fusion proteins TNfnBD-Fc and to a lesser degree TNfnA1D-Fc were stimulatory when compared with the Ig-Fc-fragment protein without insert. In contrast, the combination TNfnA1A2-Fc reduced fiber outgrowth beneath the values obtained for the Ig-Fc domain, indicating potential inhibitory properties. The monoclonal J1/tn2 antibody (clone 578) that is specific for domain TNfnD blocked the stimulatory properties of the TNfn-Fc fusions. When postnatal day 7 retinal ganglion cells were used rather that explants, Tnc and Tnc-derived proteins proved permissive for neurite outgrowth. The present study highlights a strong retinal axon growth-promoting activity of the Tnc domain TNfnD, which is modulated by neighboring domains.

Keywords

Extracellular matrixneuron–glia interactionsretinal explanttenascin-gene familyaxon guidance by glia
Type
Research Article
Information
Neuron Glia Biology , Volume 4 , Issue 4 , November 2008 , pp. 271 - 283
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Barres, B.A., Silverstein, B.E., Corey, D.P. and Chun, L.L. (1988) Immunological, morphological, and electrophysiological variation among retinal ganglion cells purified by panning. Neuron 1, 791–803.CrossRefGoogle ScholarPubMed
Bartsch, S., Husmann, K., Schachner, M. and Bartsch, U. (1995) The extracellular matrix molecule tenascin: expression in the developing chick retinotectal system and substrate properties for retinal ganglion cell neurites in vitro. European Journal of Neuroscience 7, 907–916.CrossRefGoogle ScholarPubMed
Bartsch, U., Bartsch, S., Dorries, U. and Schachner, M. (1992) Immunohistological localization of tenascin in the developing and lesioned adult mouse optic nerve. European Journal of Neuroscience 4, 338–352.CrossRefGoogle ScholarPubMed
Becker, C.G., Becker, T., Meyer, R.L. and Schachner, M. (1999) Tenascin-R inhibits the growth of optic fibers in vitro but is rapidly eliminated during nerve regeneration in the salamander Pleurodeles waltl. Journal of Neuroscience 19, 813–827.CrossRefGoogle ScholarPubMed
Becker, C.G., Schweitzer, J., Feldner, J., Becker, T. and Schachner, M. (2003) Tenascin-R as a repellent guidance molecule for developing optic axons in zebrafish. Journal of Neuroscience 23, 6232–6237.CrossRefGoogle ScholarPubMed
Becker, C.G., Schweitzer, J., Feldner, J., Schachner, M. and Becker, T. (2004) Tenascin-R as a repellent guidance molecule for newly growing and regenerating optic axons in adult zebrafish. Molecular and Cellular Neuroscience 26, 376–389.CrossRefGoogle ScholarPubMed
Becker, T., Anliker, B., Becker, C.G., Taylor, J., Schachner, M., Meyer, R.L. et al. (2000) Tenascin-R inhibits regrowth of optic fibers in vitro and persists in the optic nerve of mice after injury. Glia 29, 330–346.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Biehlmaier, O., Makhankov, Y. and Neuhauss, S.C. (2007) Impaired retinal differentiation and maintenance in zebrafish laminin mutants. Investigative Ophthalmology & Visual Science 48, 2887–2894.CrossRefGoogle ScholarPubMed
Cai, D., Qiu, J., Cao, Z., McAtee, M., Bregman, B.S. and Filbin, M.T. (2001) Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate. Journal of Neuroscience 21, 4731–4739.CrossRefGoogle ScholarPubMed
Camand, E., Morel, M.P., Faissner, A., Sotelo, C. and Dusart, I. (2004) Long-term changes in the molecular composition of the glial scar and progressive increase of serotoninergic fibre sprouting after hemisection of the mouse spinal cord. European Journal of Neuroscience 20, 1161–1176.CrossRefGoogle ScholarPubMed
Chalasani, S.H., Sabelko, K.A., Sunshine, M.J., Littman, D.R. and Raper, J.A. (2003) A chemokine, SDF-1, reduces the effectiveness of multiple axonal repellents and is required for normal axon pathfinding. Journal of Neuroscience 23, 1360–1371.CrossRefGoogle ScholarPubMed
Colamarino, S.A. and Tessier-Lavigne, M. (1995) The role of the floor plate in axon guidance. Annual Review of Neuroscience 18, 497–529.CrossRefGoogle ScholarPubMed
Doherty, P. and Walsh, F.S. (1994) Signal transduction events underlying neurite outgrowth stimulated by cell adhesion molecules. Current Opinion in Neurobiology 4, 49–55.CrossRefGoogle ScholarPubMed
Dorries, U. and Schachner, M. (1994) Tenascin mRNA isoforms in the developing mouse brain. Journal of Neuroscience Research 37, 336–347.CrossRefGoogle ScholarPubMed
Engelsberg, K. and Ghosh, F. (2007) Transplantation of cultured adult porcine full-thickness retina. Cell Transplantation 16, 31–39.CrossRefGoogle ScholarPubMed
Evans, A.R., Euteneuer, S., Chavez, E., Mullen, L.M., Hui, E.E., Bhatia, S.N. et al. (2007) Laminin and fibronectin modulate inner ear spiral ganglion neurite outgrowth in an in vitro alternate choice assay. Developmental Neurobiology 67, 1721–1730.CrossRefGoogle Scholar
Faissner, A. (1997) The tenascin gene family in axon growth and guidance. Cell and Tissue Research 290, 331–341. Review.CrossRefGoogle ScholarPubMed
Faissner, A. and Kruse, J. (1990) J1/tenascin is a repulsive substrate for central nervous system neurons. Neuron 5, 627–637.CrossRefGoogle ScholarPubMed
Garcion, E., Faissner, A. and Ffrench-Constant, C. (2001) Knockout mice reveal a contribution of the extracellular matrix molecule tenascin-C to neural precursor proliferation and migration. Development 128, 2485–2496.CrossRefGoogle ScholarPubMed
Garwood, J., Garcion, E., Dobbertin, A., Heck, N., Calco, V., Ffrench-Constant, C. et al. (2004) Auto crine expression of tenascin-c by oligodendrocyte precursor cells affects maturation rate and cell survival. European Journal of Neuroscience 20, 2524–24440.CrossRefGoogle Scholar
Gogia, P. and Schneeweis, D. (2004) Neurite extension from rod bipolar cells in retinal cell and explant cultures. Conference Proceedings IEEE Engineering in Medicine and Biological Society 6, 4229–4232.Google Scholar
Götz, B., Scholze, A., Clement, A., Joester, A., Schütte, K., Wigger, F. et al. (1996) Tenascin-C contains distinct adhesive, anti-adhesive, and neurite outgrowth promoting sites for neurons. Journal of Cell Biology 132, 681–699.CrossRefGoogle ScholarPubMed
Gotz, M., Bolz, J., Joester, A. and Faissner, A. (1997) Tenascin-C synthesis and influence on axonal growth during rat cortical development. European Journal of Neuroscience 9, 496–506.CrossRefGoogle ScholarPubMed
Haupt, C. and Huber, A.B. (2008) How axons see their way – axonal guidance in the visual system. Frontiers in Bioscience 13, 3136–3149.CrossRefGoogle ScholarPubMed
Hopker, V.H., Shewan, D., Tessier-Lavigne, M., Poo, M. and Holt, C. (1999) Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 401, 69–73.CrossRefGoogle ScholarPubMed
Huang, W., Fileta, J., Guo, Y. and Grosskreutz, C.L. (2006) Downregulation of Thy1 in retinal ganglion cells in experimental glaucoma. Current Eye Research 31, 265–271.CrossRefGoogle ScholarPubMed
Hynds, D.L. and Snow, D.M. (2001) Fibronectin and laminin elicit differential behaviors from SH-SY5Y growth cones contacting inhibitory chondroitin sulfate proteoglycans. Journal of Neuroscience Research 66, 630–642.CrossRefGoogle ScholarPubMed
Ivins, J.K., Parry, M.K. and Long, D.A. (2004) A novel cAMP-dependent pathway activates neuronal integrin function in retinal neurons. Journal of Neuroscience 24, 1212–1216.CrossRefGoogle ScholarPubMed
Joester, A. and Faissner, A. (1999) Evidence for combinatorial variability of tenascin-C isoforms and developmental regulation in the mouse central nervous system. Journal of Biological Chemistry 274, 17144–17151.CrossRefGoogle ScholarPubMed
Joester, A. and Faissner, A. (2001) The structure and function of tenascins in the nervous system. Matrix Biology 20, 13–22.CrossRefGoogle ScholarPubMed
Jones, F.S. and Jones, P.L. (2000) The tenascin family of ECM glycoproteins: structure, function, and regulation during embryonic development and tissue remodeling. Developmental Dynamics 218, 235–259.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Koch, T., Brugger, T., Bach, A., Gennarini, G. and Trotter, J. (1997) Expression of the immunoglobulin superfamily cell adhesion molecule F3 by oligodendrocyte-lineage cells. Glia 19, 199–212.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Lang, D.M., Monzon-Mayor, M., Del Mar Romero-Aleman, M., Yanes, C., Santos, E. and Pesheva, P. (2008) Tenascin-R and axon growth-promoting molecules are up-regulated in the regenerating visual pathway of the lizard (Gallotia galloti). Developmental Neurobiology 68, 899–916.CrossRefGoogle ScholarPubMed
Liu, H.Y., Nur-E-Kamal, A., Schachner, M. and Meiners, S. (2005) Neurite guidance by the FnC repeat of human tenascin-C: neurite attraction vs. neurite retention. European Journal of Neuroscience 22, 1863–1872.CrossRefGoogle ScholarPubMed
Lochter, A., Vaughan, L., Kaplony, A., Prochiantz, A., Schachner, M. and Faissner, A. (1991) J1/tenascin in substrate-bound and soluble form displays contrary effects on neurite outgrowth. Journal of Cell Biology 113, 1159–1171.CrossRefGoogle ScholarPubMed
Maseruka, H., Ridgway, A., Tullo, A. and Bonshek, R. (2000) Developmental changes in patterns of expression of tenascin-C variants in the human cornea. Investigative Ophthalmology & Visual Science 41, 4101–4107.Google ScholarPubMed
Meiners, S. and Mercado, M.L. (2003) Functional peptide sequences derived from extracellular matrix glycoproteins and their receptors: strategies to improve neuronal regeneration. Molecular Neurobiology 27, 177–196.CrossRefGoogle ScholarPubMed
Meiners, S., Nur-e-Kamal, M.S. and Mercado, M.L. (2001) Identification of a neurite outgrowth-promoting motif within the alternatively spliced region of human tenascin-C. Journal of Neuroscience 21, 7215–7225.CrossRefGoogle ScholarPubMed
Meiners, S., Powell, E.M. and Geller, H.M. (1995) A distinct subset of tenascin/CS-6-PG-rich astrocytes restricts neuronal growth in vitro. Journal of Neuroscience 15, 8096–8108.CrossRefGoogle ScholarPubMed
Meiners, S., Powell, E.M. and Geller, H.M. (1999) Neurite outgrowth promotion by the alternatively spliced region of tenascin-C is influenced by cell-type specific binding. Matrix Biology 18, 75–87.CrossRefGoogle ScholarPubMed
Mercado, M.L., Nur-e-Kamal, A., Liu, H.Y., Gross, S.R., Movahed, R. and Meiners, S. (2004) Neurite outgrowth by the alternatively spliced region of human tenascin-C is mediated by neuronal alpha7beta1 integrin. Journal of Neuroscience 24, 238–247.CrossRefGoogle ScholarPubMed
Meyer-Franke, A., Kaplan, M.R., Pfrieger, F.W. and Barres, B.A. (1995) Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron 15, 805–819.CrossRefGoogle ScholarPubMed
Nishio, T., Kawaguchi, S., Yamamoto, M., Iseda, T., Kawasaki, T. and Hase, T. (2005) Tenascin-C regulates proliferation and migration of cultured astrocytes in a scratch wound assay. Neuroscience 1, 87–102.CrossRefGoogle Scholar
Orend, G. and Chiquet-Ehrismann, R. (2006) Tenascin-C induced signaling in cancer. Cancer Letters 244, 143–163.CrossRefGoogle ScholarPubMed
Perez, R.G. and Halfter, W. (1993) Tenascin in the developing chick visual system: distribution and potential role as a modulator of retinal axon growth. Developmental Biology 156, 278–292.CrossRefGoogle ScholarPubMed
Properzi, F., Asher, R.A. and Fawcett, J.W. (2003) Chondroitin sulphate proteoglycans in the central nervous system: changes and synthesis after injury. Biochemical Society Transactions 31, 335–336. Review.CrossRefGoogle ScholarPubMed
Qiu, J., Cai, D., Dai, H., McAtee, M., Hoffman, P.N., Bregman, B.S. et al. (2002) Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34, 895–903.CrossRefGoogle ScholarPubMed
Rauch, U., Clement, A., Retzler, C., Frohlich, L., Fassler, R., Gohring, W. et al. (1997) Mapping of a defined neurocan binding site to distinct domains of tenascin-C. Journal of Biological Chemistry 272, 26905–26912.CrossRefGoogle ScholarPubMed
Rhodes, K.E., Moon, L.D. and Fawcett, J.W. (2003) Inhibiting cell proliferation during formation of the glial scar: effects on axon regeneration in the CNS. Neuroscience 120, 41–56.CrossRefGoogle ScholarPubMed
Rigato, F., Garwood, J., Calco, V., Heck, N., Faivre-Sarrailh, C. and Faissner, A. (2002) Tenascin-C promotes neurite outgrowth of embryonic hippocampal neurons through the alternatively spliced fibronectin type III BD domains via activation of the cell adhesion molecule F3/contactin. Journal of Neuroscience 22, 6596–6609.CrossRefGoogle ScholarPubMed
Rodger, J., Goto, H., Cui, Q., Chen, P.B. and Harvey, A.R. (2005) cAMP regulates axon outgrowth and guidance during optic nerve regeneration in goldfish. Molecular and Cellular Neuroscience 30, 452–464.CrossRefGoogle ScholarPubMed
Rowan, S., Chen, C.M., Young, T.L., Fisher, D.E. and Cepko, C.L. (2004) Transdifferentiation of the retina into pigmented cells in ocular retardation mice defines a new function of the homeodomain gene Chx10. Development 131, 5139–5152.CrossRefGoogle ScholarPubMed
Saga, T., Endo, K., Akiyama, T., Sakahara, H., Koizumi, M., Watanabe, Y. et al. (1991) Scintigraphic detection of overexpressed c-erbB-2 protooncogene products by a class-switched murine anti-c-erbB-2 protein monoclonal antibody. Cancer Research 51, 990–994.Google ScholarPubMed
Saito, Y., Imazeki, H., Miura, S., Yoshimura, T., Okutsu, H., Harada, Y. et al. (2007) A peptide derived from tenascin-C induces 1 integrin activation through syndecan-4. Journal of Biological Chemistry 282, 34929–34937 Epub 32007 Sep 34926.CrossRefGoogle ScholarPubMed
Shearer, M.C., Niclou, S.P., Brown, D., Asher, R.A., Holtmaat, A.J., Levine, J.M. et al. (2003) The astrocyte/meningeal cell interface is a barrier to neurite outgrowth which can be overcome by manipulation of inhibitory molecules or axonal signalling pathways. Molecular and Cellular Neuroscience 24, 913–925.CrossRefGoogle ScholarPubMed
Shewan, D., Dwivedy, A., Anderson, R. and Holt, C.E. (2002) Age-related changes underlie switch in netrin-1 responsiveness as growth cones advance along visual pathway. Nature Neuroscience 5, 955–962.CrossRefGoogle ScholarPubMed
Siddiqui, S., Horvat-Broecker, A. and Faissner, A. (2009) Comparative screening of glial cell types reveals extracellular matrix that inhibits retinal axon growth in a chondroitinase ABC-resistant fashion. Glia Epub 25 Feb, doi:10.1002/glia.20860.CrossRefGoogle Scholar
Song, H.J., Ming, G.L. and Poo, M.M. (1997) cAMP-induced switching in turning direction of nerve growth cones. Nature 6639, 275–279. Erratum in:1997 Sep 1925;1389(6649):1412.CrossRefGoogle Scholar
Stuermer, C.A. and Bastmeyer, M. (2000) The retinal axon's pathfinding to the optic disk. Progress in Neurobiology 62, 197–214.CrossRefGoogle Scholar
von Holst, A., Egbers, U., Prochiantz, A. and Faissner, A. (2007) Neural stem/progenitor cells express 20 tenascin C isoforms that are differentially regulated by Pax6. Journal of Biological Chemistry 282, 9172–9181.CrossRefGoogle ScholarPubMed
Weller, R.E., Steele, G.E. and Cusick, C.G. (1991) Cortical connections of dorsal cortex rostral to V II in squirrel monkeys. The Journal of Comparative Neurology 306, 521–537.CrossRefGoogle Scholar
Wolman, M.A., Regnery, A.M., Becker, T., Becker, C.G. and Halloran, M.C. (2007) Semaphorin3D regulates axon axon interactions by modulating levels of L1 cell adhesion molecule. Journal of Neuroscience 27, 9653–9663.CrossRefGoogle ScholarPubMed
Zelina, P., Avci, H.X., Thelen, K. and Pollerberg, G.E. (2005) The cell adhesion molecule NrCAM is crucial for growth cone behaviour and pathfinding of retinal ganglion cell axons. Development 132, 3609–3618.CrossRefGoogle ScholarPubMed
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