Abstract
In vitro and in vivo studies on the role of tenascins have shown that the two paradigmatic glycoproteins of the tenascin family, tenascin-C (TnC) and tenascin-R (TnR) play important roles in cell proliferation and migration, fate determination, axonal pathfinding, myelination, and synaptic plasticity. As components of the extracellular matrix, both molecules show distinct, but also overlapping dual functions in inhibiting and promoting cell interactions depending on the cell type, developmental stage and molecular microenvironment. They are expressed by neurons and glia as well as, for TnC, by cells of the immune system. The functional relationship between neural and immune cells becomes relevant in acute and chronic nervous system disorders, in particular when the blood brain and blood peripheral nerve barriers are compromised. In this review, we will describe the functional parameters of the two molecules in cell interactions during development and, in the adult, in synaptic activity and plasticity, as well as regeneration after injury, with TnC being conducive for regeneration and TnR being inhibitory for functional recovery. Although not much is known about the role of tenascins in neuroinflammation, we will describe emerging knowledge on the interplay between neural and immune cells in autoimmune diseases, such as multiple sclerosis and polyneuropathies. We will attempt to point out the directions of experimental approaches that we envisage would help gaining insights into the complex interplay of TnC and TnR with the cells that express them in pathological conditions of nervous and immune systems.
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Abu El-Asrar AM, Meersschaert A, Al-Kharashi SA, Missotten L, Geboes K (2003) Immuno-histochemical evaluation of conjunctival remodelling in vernal keratoconjunctivitis. Eye (Lond) 17:767–771
Agrawal SM, Yong VW (2006) Immunopathogenesis of multiple sclerosis. Int Rev Neurobiol 79:99–126
Aloisi F, Borsellino G, Samoggia P, Testa U, Chelucci C, Russo G, Peschle C, Levi G (1992) Astrocyte cultures from human embryonic brain: characterization and modulation of surface molecules by inflammatory cytokines. J Neurosci Res 32:494–506
Angelov DN, Walther M, Streppel M, Guntinas-Lichius O, Neiss WF, Probstmeier R, Pesheva P (1998) Tenascin-R is antiadhesive for activated microglia that induce downregulation of the protein after peripheral nerve injury: a new role in neuronal protection. J Neurosci 18:6218–6229
Ankeny DP, Popovich PG (2009) Mechanisms and implications of adaptive immune responses after traumatic spinal cord injury. Neuroscience 158:1112–1121
Apostolova I, Irintchev A, Schachner M (2006) Tenascin-R restricts posttraumatic remodeling of motoneuron innervation and functional recovery after spinal cord injury in adult mice. J Neurosci 26:7849–7859
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
Barnea G, Grumet M, Milev P, Silvennoinen O, Levy JB, Sap J, Schlessinger J (1994) Receptor tyrosine phosphatase beta is expressed in the form of proteoglycan and binds to the extracellular matrix protein tenascin. J Biol Chem 269:14349–14352
Bartholomäus I, Kawakami N, Odoardi F, Schläger C, Miljkovic D, Ellwart JW, Klinkert WE, Flügel-Koch C, Issekutz TB, Wekerle H, Flügel A (2009) Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature 462:94–98
Bartsch U (1996) The extracellular matrix molecule tenascin-C: expression in vivo and functional characterization in vitro. Prog Neurobiol 49:145–168
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
Bartsch U, Pesheva P, Raff M, Schachner M (1993) Expression of janusin (J1–160/180) in the retina and optic nerve of the developing and adult mouse. Glia 9:57–69
Bartsch U, Faissner A, Trotter J, Dörries U, Bartsch S, Mohajeri H, Schachner M (1994) Tenascin demarcates the boundary between the myelinated and nonmyelinated part of retinal ganglion cell axons in the developing and adult mouse. J Neurosci 14:4756–4768
Bartsch S, Husmann K, Schachner M, 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. Eur J Neurosci 7:907–916
Becker T, Becker CG, Niemann U, Naujoks-Manteuffel C, Bartsch U, Schachner M, Roth G (1995) Immunohistological localization of tenascin-C in the developing and regenerating retinotectal system of two amphibian species. J Comp Neurol 360:643–657
Becker T, Anliker B, Becker CG, Taylor J, Schachner M, Meyer RL, Bartsch U (2000) Tenascin-R inhibits regrowth of optic fibers in vitro and persists in the optic nerve of mice after injury. Glia 29:330–346
Becker CG, Schweitzer J, Feldner J, Becker T, Schachner M (2003) Tenascin-R as a repellent guidance molecule for developing optic axons in zebrafish. J Neurosci 23:6232–6237
Bourdon MA, Ruoslahti E (1989) Tenascin mediates cell attachment through an RGD-dependent receptor. J Cell Biol 108:1149–1155
Bradbury EJ, Carter LM (2011) Manipulating the glial scar: chondroitinase ABC as a therapy for spinal cord injury. Brain Res Bull 84:306–316
Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636–640
Brenneke F, Bukalo O, Dityatev A, Lie AA (2004) Mice deficient for the extracellular matrix glycoprotein tenascin-r show physiological and structural hallmarks of increased hippocampal excitability, but no increased susceptibility to seizures in the pilocarpine model of epilepsy. Neuroscience 124:841–855
Bristow J, Tee MK, Gitelman SE, Mellon SH, Miller WL (1993) Tenascin-X: a novel extracellular matrix protein encoded by the human XB gene overlapping P450c21B. J Cell Biol 122:265–278
Brodkey JA, Laywell ED, O’Brien TF, Faissner A, Stefansson K, Dörries HU, Schachner M, Steindler DA (1995) Focal brain injury and upregulation of a developmentally regulated extracellular matrix protein. J Neurosurg 82:106–112
Brown MC, Staniszewska I, Lazarovici P, Tuszynski GP, Del Valle L, Marcinkiewicz C (2008) Regulatory effect of nerve growth factor in alpha9beta1 integrin-dependent progression of glioblastoma. Neuro Oncol 10:968–980
Brückner G, Grosche J, Schmidt S, Härtig W, Margolis RU, Delpech B, Seidenbecher CI, Czaniera R, Schachner M (2000) Postnatal development of perineuronal nets in wild-type mice and in a mutant deficient in tenascin-R. J Comp Neurol 428:616–629
Bukalo O, Schachner M, Dityatev A (2001) Modification of extracellular matrix by enzymatic removal of chondroitin sulfate and by lack of tenascin-R differentially affects several forms of synaptic plasticity in the hippocampus. Neuroscience 104:359–369
Catalán V, Gómez-Ambrosi J, Rodríguez A, Ramírez B, Rotellar F, Valentí V, Silva C, Gil MJ, Salvador J, Frühbeck G (2012) Increased tenascin C and toll-like receptor 4 levels in visceral adipose tissue as a link between inflammation and extracellular matrix remodeling in obesity. J Clin Endocrinol Metab 97:E1880–E1889
Celio MR, Blümcke I (1994) Perineuronal nets—a specialized form of extracellular matrix in the adult nervous system. Brain Res Brain Res Rev 19:128–145
Celio MR, Chicquet-Ehrismann R (1993) ‘Perineuronal nets’ around cortical interneurons expressing parvalbumin are rich in tenascin. Neurosci Lett 162:37–40
Chen J, Joon Lee H, Jakovcevski I, Shah R, Bhagat N, Loers G, Liu HY, Meiners S, Taschenberger G, Kügler S, Irintchev A, Schachner M (2010) The extracellular matrix glycoprotein tenascin-C is beneficial for spinal cord regeneration. Mol Ther 18:1769–1777
Chilosi M, Lestani M, Benedetti A, Montagna L, Pedron S, Scarpa A, Menestrina F, Hirohashi S, Pizzolo G, Semenzato G (1993) Constitutive expression of tenascin in T-dependent zones of human lymphoid tissues. Am J Pathol 143:1348–1355
Chiquet M, Fambrough DM (1984) Chick myotendinous antigen. II. A novel extracellular glycoprotein complex consisting of large disulfide-linked subunits. J Cell Biol 98:1937–1946
Chiquet-Ehrismann R (1991) Anti-adhesive molecules of the extracellular matrix. Curr Opin Cell Biol 3:800–804
Chung CY, Erickson HP (1994) Cell surface annexin II is a high affinity receptor for the alternatively spliced segment of tenascin-C. J Cell Biol 126:539–548
Chung CY, Zardi L, Erickson HP (1995) Binding of tenascin-C to soluble fibronectin and matrix fibrils. J Biol Chem 270:29012–29017
Chung CY, Murphy-Ullrich JE, Erickson HP (1996) Mitogenesis, cell migration, and loss of focal adhesions induced by tenascin-C interacting with its cell surface receptor, annexin II. Mol Biol Cell 7:883–892
Clark RA, Erickson HP, Springer TA (1997) Tenascin supports lymphocyte rolling. J Cell Biol 137:755–765
Cleek RL, Rege AA, Denner LA, Eskin SG, Mikos AG (1997) Inhibition of smooth muscle cell growth in vitro by an antisense oligodeoxynucleotide released from poly(DL-lactic-co-glycolic acid) microparticles. J Biomed Mater Res 35:525–530
Conway JF, Parry DA (1991) Three-stranded alpha-fibrous proteins: the heptad repeat and its implications for structure. Int J Biol Macromol 13:14–16
Cowan KN, Jones PL, Rabinovitch M (2000) Elastase and matrix metalloproteinase inhibitors induce regression, and tenascin-C antisense prevents progression, of vascular disease. J Clin Invest 105:21–34
Crossin KL (1991) Cytotactin binding: inhibition of stimulated proliferation and intracellular alkalinization in fibroblasts. Proc Natl Acad Sci USA 88:11403–11407
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
Crossin KL, Hoffman S, Tan SS, Edelman GM (1989) Cytotactin and its proteoglycan ligand mark structural and functional boundaries in somatosensory cortex of the early postnatal mouse. Dev Biol 136:381–392
David S, Kroner A (2011) Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci 12:388–399
Deckner M, Lindholm T, Cullheim S, Risling M (2000) Differential expression of tenascin-C, tenascin-R, tenascin/J1, and tenascin-X in spinal cord scar tissue and in the olfactory system. Exp Neurol 166:350–362
Deller T, Haas CA, Naumann T, Joester A, Faissner A, Frotscher M (1997) Up-regulation of astrocyte-derived tenascin-C correlates with neurite outgrowth in the rat dentate gyrus after unilateral entorhinal cortex lesion. Neuroscience 81:829–846
Devanathan V, Jakovcevski I, Santuccione A, Li S, Lee HJ, Peles E, Leshchyns’ka I, Sytnyk V, Schachner M (2010) Cellular form of prion protein inhibits Reelin-mediated shedding of Caspr from the neuronal cell surface to potentiate Caspr-mediated inhibition of neurite outgrowth. J Neurosci 30:9292–9305
DiProspero NA, Meiners S, Geller HM (1997) Inflammatory cytokines interact to modulate extracellular matrix and astrocytic support of neurite outgrowth. Exp Neurol 148:628–639
Dityatev A, Schachner M (2003) Extracellular matrix molecules and synaptic plasticity. Nat Rev Neurosci 4:456–468
Dityatev A, Schachner M, Sonderegger P (2010a) The dual role of the extracellular matrix in synaptic plasticity and homeostasis. Nat Rev Neurosci 11:735–746
Dityatev A, Seidenbecher CI, Schachner M (2010b) Compartmentalization from the outside: the extracellular matrix and functional microdomains in the brain. Trends Neurosci 33:503–512
Doerries U, Taylor J, Xiao Z, Lochter A, Montag D, Schachner M (1996) Distinct effects of recombinant tenascin-C domains on neuronal cell adhesion, growth cone guidance, and neuronal polarity. J Neurosci Res 43:420–438
Dörries U, Schachner M (1994) Tenascin mRNA isoforms in the developing mouse brain. J Neurosci Res 37:336–347
Faissner A (1997) The tenascin gene family in axon growth and guidance. Cell Tissue Res 290:331–341
Faissner A, Kruse J (1990) J1/tenascin is a repulsive substrate for central nervous system neurons. Neuron 5:627–637
Faissner A, Steindler D (1995) Boundaries and inhibitory molecules in developing neural tissues. Glia 13:233–254
Faissner A, Scholze A, Götz B (1994) Tenascin glycoproteins in developing neural tissues: only decoration? Perspect Dev Neurobiol 2:53–66
Fruttiger M, Schachner M, Martini R (1995) Tenascin-C expression during Wallerian degeneration in C57BL/Wld(S) mice: Possible implications for axonal regeneration. J Neurocytol 24:1–14
Fuss B, Pott U, Fischer P, Schwab ME, Schachner M (1991) Identification of a cDNA clone specific for the oligodendrocyte-derived repulsive extracellular matrix molecule J1–160/180. J Neurosci Res 29:299–307
Fuss B, Wintergerst ES, Bartsch U, Schachner M (1993) Molecular characterization and in situ mRNA localization of the neural recognition molecule J1–160/180: a modular structure similar to tenascin. J Cell Biol 120:1237–1249
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
Goh FG, Piccinini AM, Krausgruber T, Udalova IA, Midwood KS (2010) Transcriptional regulation of the endogenous danger signal tenascin-C: a novel autocrine loop in inflammation. J Immunol 184:2655–2662
Götz B, Scholze A, Clement A, Joester A, Schütte K, Wigger F, Frank R, Spiess E, Ekblom P, Faissner A (1996) Tenascin-C contains distinct adhesive, anti-adhesive, and neurite outgrowth promoting sites for neurons. J Cell Biol 132:681–699
Götz M, Bolz J, Joester A, Faissner A (1997) Tenascin-C synthesis and influence on axonal growth during rat cortical development. Eur J Neurosci 9:496–506
Gratchev A, Kzhyshkowska J, Utikal J, Goerdt S (2005) Interleukin-4 and dexamethasone counterregulate extracellular matrix remodelling and phagocytosis in type-2 macrophages. Scand J Immunol 61:10–17
Grumet M, Hoffman S, Crossin KL, Edelman GM (1985) Cytotactin, an extracellular matrix protein of neural and non-neural tissues that mediates glia-neuron interaction. Proc Natl Acad Sci USA 82:8075–8079
Gueders MM, Hirst SJ, Quesada-Calvo F, Paulissen G, Hacha J, Gilles C, Gosset P, Louis R, Foidart JM, Lopez-Otin C, Noël A, Cataldo DD (2010) Matrix metalloproteinase-19 deficiency promotes tenascin-C accumulation and allergen-induced airway inflammation. Am J Respir Cell Mol Biol 43:286–295
Guntinas-Lichius O, Angelov DN, Morellini F, Lenzen M, Skouras E, Schachner M, Irintchev A (2005) Opposite impacts of tenascin-C and tenascin-R deficiency in mice on the functional outcome of facial nerve repair. Eur J Neurosci 22:2171–2179
Gurevicius K, Kuang F, Stoenica L, Irintchev A, Gureviciene I, Dityatev A, Schachner M, Tanila H (2009) Genetic ablation of tenascin-C expression leads to abnormal hippocampal CA1 structure and electrical activity in vivo. Hippocampus 19:1232–1246
Gutowski NJ, Newcombe J, Cuzner ML (1999) Tenascin-R and C in multiple sclerosis lesions: relevance to extracellular matrix remodelling. Neuropathol Appl Neurobiol 25:207–214
Hagihara K, Miura R, Kosaki R, Berglund E, Ranscht B, Yamaguchi Y (1999) Immunohistochemical evidence for the brevican-tenascin-R interaction: colocalization in perineuronal nets suggests a physiological role for the interaction in the adult rat brain. J Comp Neurol 410:256–264
Hagios C, Koch M, Spring J, Chiquet M, Chiquet-Ehrismann R (1996) Tenascin-Y: a protein of novel domain structure is secreted by differentiated fibroblasts of muscle connective tissue. J Cell Biol 134:1499–1512
Härkönen E, Virtanen I, Linnala A, Laitinen LL, Kinnula VL (1995) Modulation of fibronectin and tenascin production in human bronchial epithelial cells by inflammatory cytokines in vitro. Am J Respir Cell Mol Biol 13:109–115
Hasegawa M, Nakoshi Y, Muraki M, Sudo A, Kinoshita N, Yoshida T, Uchida A (2007) Expression of large tenascin-C splice variants in synovial fluid of patients with rheumatoid arthritis. J Orthop Res 25:563–568
Haunso A, Ibrahim M, Bartsch U, Letiembre M, Celio MR, Menoud P (2000) Morphology of perineuronal nets in tenascin-R and parvalbumin single and double knockout mice. Brain Res 864:142–145
Hauzenberger D, Olivier P, Gundersen D, Rüegg C (1999) Tenascin-C inhibits beta1 integrin-dependent T lymphocyte adhesion to fibronectin through the binding of its fnIII 1–5 repeats to fibronectin. Eur J Immunol 29:1435–1447
Hisatomi K, Sakamoto N, Mukae H, Hayashi T, Amenomori M, Ishimoto H, Fujita H, Ishii H, Nakayama S, Ishimatsu Y, Kohno S (2009) Elevated levels of tenascin-C in patients with cryptogenic organizing pneumonia. Intern Med 48:1501–1507
Hofstetter HH, Ibrahim SM, Koczan D, Kruse N, Weishaupt A, Toyka KV, Gold R (2005) Therapeutic efficacy of IL-17 neutralization in murine experimental autoimmune encephalomyelitis. Cell Immunol 237:123–130
Holley JE, Gveric D, Whatmore JL, Gutowski NJ (2005) Tenascin C induces a quiescent phenotype in cultured adult human astrocytes. Glia 52:53–58
Huang JY, Cheng YJ, Lin YP, Lin HC, Su CC, Juliano R, Yang BC (2010) Extracellular matrix of glioblastoma inhibits polarization and transmigration of T cells: the role of tenascin-C in immune suppression. J Immunol 185:1450–1459
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
Ikeshima-Kataoka H, Saito S, Yuasa S (2007) Tenascin-C is required for proliferation of astrocytes in primary culture. In Vivo 21:629–633
Ikeshima-Kataoka H, Shen JS, Eto Y, Saito S, Yuasa S (2008) Alteration of inflammatory cytokine production in the injured central nervous system of tenascin-deficient mice. In Vivo 22:409–413
Imanaka-Yoshida K, Hiroe M, Yasutomi Y, Toyozaki T, Tsuchiya T, Noda N, Maki T, Nishikawa T, Sakakura T, Yoshida T (2002) Tenascin-C is a useful marker for disease activity in myocarditis. J Pathol 197:388–394
Imanaka-Yoshida K, Hiroe M, Yoshida T (2004) Interaction between cell and extracellular matrix in heart disease: multiple roles of tenascin-C in tissue remodeling. Histol Histopathol 19:517–525
Irintchev A, Salvini TF, Faissner A, Wernig A (1993) Differential expression of tenascin after denervation, damage or paralysis of mouse soleus muscle. J Neurocytol 22:955–965
Jadidi-Niaragh F, Mirshafiey A (2011) Th17 cell, the new player of neuroinflammatory process in multiple sclerosis. Scand J Immunol 74:1–13
Jakovcevski I, Wu J, Karl N, Leshchyns’ka I, Sytnyk V, Chen J, Irintchev A, Schachner M (2007) Glial scar expression of CHL1, the close homolog of the adhesion molecule L1, limits recovery after spinal cord injury. J Neurosci 27:7222–7233
Jankovski A, Sotelo C (1996) Subventricular zone-olfactory bulb migratory pathway in the adult mouse: cellular composition and specificity as determined by heterochronic and heterotopic transplantation. J Comp Neurol 371:376–396
Joester A, Faissner A (1999) Evidence for combinatorial variability of tenascin-C isoforms and developmental regulation in the mouse central nervous system. J Biol Chem 274:17144–17151
Joester A, Faissner A (2001) The structure and function of tenascins in the nervous system. Matrix Biol 20:13–22
Jones FS, Jones PL (2000) The tenascin family of ECM glycoproteins: structure, function, and regulation during embryonic development and tissue remodeling. Dev Dyn 218:235–259
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 and segments of fibronectin and fibrinogen. Proc Natl Acad Sci USA 85:2186–2190
Kaarteenaho-Wiik R, Lakari E, Soini Y, Pöllänen R, Kinnula VL, Pääkkö P (2000) Tenascin expression and distribution in pleural inflammatory and fibrotic diseases. J Histochem Cytochem 48:1257–1268
Kanayama M, Morimoto J, Matsui Y, Ikesue M, Danzaki K, Kurotaki D, Ito K, Yoshida T, Uede T (2011) α9β1 integrin-mediated signaling serves as an intrinsic regulator of pathogenic Th17 cell generation. J Immunol 187:5851–5864
Knaggs HE, Layton AM, Morris C, Wood EJ, Holland DB, Cunliffe WJ (1994) Investigation of the expression of the extracellular matrix glycoproteins tenascin and fibronectin during acne vulgaris. Br J Dermatol 130:576–582
Koukoulis GK, Koso-Thomas AK, Zardi L, Gabbiani G, Gould VE (1999) Enhanced tenascin expression correlates with inflammation in primary sclerosing cholangitis. Pathol Res Pract 195:727–731
Koyama Y, Kusubata M, Yoshiki A, Hiraiwa N, Ohashi T, Irie S, Kusakabe M (1998) Effect of tenascin-C deficiency on chemically induced dermatitis in the mouse. J Invest Dermatol 111:930–935
Krishnamoorthy G, Wekerle H (2009) EAE: an immunologist’s magic eye. Eur J Immunol 39:2031–2035
Laitinen LA, Laitinen A, Altraja A, Virtanen I, Kämpe M, Simonsson BG, Karlsson SE, Håkansson L, Venge P, Sillastu H (1996) Bronchial biopsy findings in intermittent or “early” asthma. J Allergy Clin Immunol 98(5 Pt 2):S3-6; discussion S33-40
Laywell ED, Dörries 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
Lee HJ, Jakovcevski I, Radonjic N, Hoelters L, Schachner M, Irintchev A (2009) Better functional outcome of compression spinal cord injury in mice is associated with enhanced H-reflex responses. Exp Neurol 216:365–374
Lee HJ, Bian S, Jakovcevski I, Wu B, Irintchev A, Schachner M (2012) Delayed applications of L1 and chondroitinase ABC promote recovery after spinal cord injury. J Neurotrauma 29:1850–1863
Li X, Yuan FL, Lu WG, Zhao YQ, Li CW, Li JP, Xu RS (2010) The role of interleukin-17 in mediating joint destruction in rheumatoid arthritis. Biochem Biophys Res Commun 397:131–135
Liao H, Bu WY, Wang TH, Ahmed S, Xiao ZC (2005) Tenascin-R plays a role in neuroprotection via its distinct domains that coordinate to modulate the microglia function. J Biol Chem 280:8316–8323
Liao H, Huang W, Niu R, Sun L, Zhang L (2008) Cross-talk between the epidermal growth factor-like repeats/fibronectin 6–8 repeats domains of tenascin-R and microglia modulates neural stem/progenitor cell proliferation and differentiation. J Neurosci Res 86:27–34
Lochter A, Schachner M (1993) Tenascin and extracellular matrix glycoproteins: from promotion to polarization of neurite growth in vitro. J Neurosci 13:3986–4000
Lochter A, Taylor J, Braunewell KH, Holm J, Schachner M (1995) Control of neuronal morphology in vitro: interplay between adhesive substrate forces and molecular instruction. J Neurosci Res 42:145–158
Martini R (1994) Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerves. J Neurocytol 23:1–28
Maseruka H, Bonshek RE, Tullo AB (1997) Tenascin-C expression in normal, inflamed, and scarred human corneas. Br J Ophthalmol 81:677–682
Meiners S, Nur-e-Kamal MS, Mercado ML (2001) Identification of a neurite outgrowth-promoting motif within the alternatively spliced region of human tenascin-C. J Neurosci 21:7215–7225
Metzger M, Bartsch S, Bartsch U, Bock J, Schachner M, Braun K (2006) Regional and cellular distribution of the extracellular matrix protein tenascin-C in the chick forebrain and its role in neonatal learning. Neuroscience 141:1709–1719
Meuronen A, Karisola P, Leino M, Savinko T, Sirola K, Majuri ML, Piirilä P, Virtanen I, Mäkelä M, Laitinen A, Laitinen LA, Alenius H (2011) Attenuated expression of tenascin-C in ovalbumin-challenged STAT4−/− mice. Respir Res 12:2
Midwood K, Sacre S, Piccinini AM, Inglis J, Trebaul A, Chan E, Drexler S, Sofat N, Kashiwagi M, Orend G, Brennan F, Foxwell B (2009) Tenascin-C is an endogenous activator of Toll-like receptor 4 that is essential for maintaining inflammation in arthritic joint disease. Nat Med 15:774–780
Milev P, Fischer D, Haring M, Schulthess T, Margolis RK, Chiquet-Ehrismann R, Margolis RU (1997) The fibrinogen-like globe of tenascin-C mediates its interactions with neurocan and phosphacan/protein-tyrosine phosphatase-zeta/beta. J Biol Chem 272:15501–15509
Miljkovic D, Stosic-Grujicic S, Markovic M, Momcilovic M, Ramic Z, Maksimovic-Ivanic D, Mijatovic S, Popadic D, Cvetkovic I, Mostarica-Stojkovic M (2006) Strain difference in susceptibility to experimental autoimmune encephalomyelitis between Albino Oxford and Dark Agouti rats correlates with disparity in production of IL-17, but not nitric oxide. J Neurosci Res 84:379–388
Miljković D, Timotijević G, Mostarica Stojković M (2011) Astrocytes in the tempest of multiple sclerosis. FEBS Lett 585:3781–3788
Miller E (2012) Multiple sclerosis. Adv Exp Med Biol 724:222–238
Mitrovic N, Doerries U, Schachner M (1994) Expression of the extracellular matrix glycoprotein tenascin in the somatosensory cortex of the mouse during postnatal development: an immunocytochemical and in situ hybridization analysis. J Neurocytol 23:364–378
Moore CS, Abdullah SL, Brown A, Arulpragasam A, Crocker SJ (2011) How factors secreted from astrocytes impact myelin repair. J Neurosci Res 89:13–21
Morellini F, Sivukhina E, Stoenica L, Oulianova E, Bukalo O, Jakovcevski I, Dityatev A, Irintchev A, Schachner M (2010) Improved reversal learning and working memory and enhanced reactivity to novelty in mice with enhanced GABAergic innervation in the dentate gyrus. Cereb Cortex 20:2712–2727
Morganti MC, Taylor J, Pesheva P, Schachner M (1990) Oligodendrocyte-derived J1–160/180 extracellular matrix glycoproteins are adhesive or repulsive depending on the partner cell type and time of interaction. Exp Neurol 109:98–110
Nakic M, Mitrovic N, Sperk G, Schachner M (1996) Kainic acid activates transient expression of tenascin-C in the adult rat hippocampus. J Neurosci Res 44:355–362
Nash B, Thomson CE, Linington C, Arthur AT, McClure JD, McBride MW, Barnett SC (2011) Functional duality of astrocytes in myelination. J Neurosci 31:13028–13038
Neidhardt J, Fehr S, Kutsche M, Lohler J, Schachner M (2003) Tenascin-N: characterization of a novel member of the tenascin family that mediates neurite repulsion from hippocampal explants. Mol Cell Neurosci 23:193–209
Nies DE, Hemesath TJ, Kim JH, Gulcher JR, Stefansson K (1991) The complete cDNA sequence of human hexabrachion (Tenascin). A multidomain protein containing unique epidermal growth factor repeats. J Biol Chem 266:2818–2823
Paron I, Berchtold S, Vörös J, Shamarla M, Erkan M, Höfler H, Esposito I (2011) Tenascin-C enhances pancreatic cancer cell growth and motility and affects cell adhesion through activation of the integrin pathway. PLoS ONE 6:e21684
Patel L, Sun W, Glasson SS, Morris EA, Flannery CR, Chockalingam PS (2011) Tenascin-C induces inflammatory mediators and matrix degradation in osteoarthritic cartilage. BMC Musculoskelet Disord 12:164
Pesheva P, Probstmeier R (2000) The yin and yang of tenascin-R in CNS development and pathology. Prog Neurobiol 61:465–493
Pesheva P, Spiess E, Schachner M (1989) J1–160 and J1–180 are oligodendrocyte secreted nonpermissive substrates for cell adhesion. J Cell Biol 109:1765–1778
Pesheva P, Gennarini G, Goridis C, Schachner M (1993) The F3/11 cell adhesion molecule mediates the repulsion of neurons by the extracellular matrix glycoprotein J1–160/180. Neuron 10:69–82
Pesheva P, Probstmeier R, Skubitz AP, McCarthy JB, Furcht LT, Schachner M (1994) Tenascin-R (J1 160/180 inhibits fibronectin-mediated cell adhesion—functional relatedness to tenascin-C. J Cell Sci 107:2323–2333
Pesheva P, Gloor S, Schachner M, Probstmeier R (1997) Tenascin-R is an intrinsic autocrine factor for oligodendrocyte differentiation and promotes cell adhesion by a sulfatide-mediated mechanism. J Neurosci 17:4642–4651
Peter NR, Shah RT, Chen J, Irintchev A, Schachner M (2012) Adhesion molecules close homolog of L1 and tenascin-C affect blood-spinal cord barrier repair. NeuroReport 23:479–482
Prieto AL, Jones FS, Cunningham BA, Crossin KL, Edelman GM (1990) Localization during development of alternatively spliced forms of cytotactin mRNA by in situ hybridization. J Cell Biol 111:685–698
Ransohoff RM, Brown MA (2012) Innate immunity in the central nervous system. J Clin Invest 122:1164–1171
Rathjen FG, Wolff JM, Chiquet-Ehrismann R (1991) Restrictin: a chick neural extracellular matrix protein involved in cell attachment co-purifies with the cell recognition molecule F11. Development 113:151–164
Rhodes KE, Fawcett JW (2004) Chondroitin sulphate proteoglycans: preventing plasticity or protecting the CNS? J Anat 204:33–48
Riedl S, Tandara A, Reinshagen M, Hinz U, Faissner A, Bodenmüller H, Buhr HJ, Herfarth C, Möller P (2011) Serum tenascin-C is an indicator of inflammatory bowel disease activity. Int J Colorectal Dis 16:285–291
Rolls A, Shechter R, Schwartz M (2009) The bright side of the glial scar in CNS repair. Nat Rev Neurosci 10:235–241
Rüegg CR, Chiquet-Ehrismann R, Alkan SS (1989) Tenascin, an extracellular matrix protein, exerts immunomodulatory activities. Proc Natl Acad Sci U S A 86:7437–7441
Ruhmann M, Piccinini AM, Kong PL, Midwood KS (2012) Endogenous activation of adaptive immunity: tenascin-C drives interleukin-17 synthesis in murine arthritic joint disease. Arthritis Rheum 64:2179–2190
Saghatelyan AK, Gorissen S, Albert M, Hertlein B, Schachner M, Dityatev A (2000) The extracellular matrix molecule tenascin-R and its HNK-1 carbohydrate modulate perisomatic inhibition and long-term potentiation in the CA1 region of the hippocampus. Eur J Neurosci 12:3331–3342
Saghatelyan AK, Dityatev A, Schmidt S, Schuster T, Bartsch U, Schachner M (2001) Reduced perisomatic inhibition, increased excitatory transmission, and impaired long-term potentiation in mice deficient for the extracellular matrix glycoprotein tenascin-R. Mol Cell Neurosci 17:226–240
Salas A, Fernández-Bañares F, Casalots J, González C, Tarroch X, Forcada P, González G (2003) Subepithelial myofibroblasts and tenascin expression in microscopic colitis. Histopathology 43:48–54
Sandvig A, Berry M, Barrett LB, Butt A, Logan A (2004) Myelin-, reactive glia-, and scar-derived CNS axon growth inhibitors: expression, receptor signaling, and correlation with axon regeneration. Glia 46:225–251
Satta J, Soini Y, Pöllänen R, Pääkkö P, Juvonen T (1997) Tenascin expression is associated with a chronic inflammatory process in abdominal aortic aneurysms. J Vasc Surg 26:670–675
Schachner M (1994) Neural recognition molecules in disease and regeneration. Curr Opin Neurobiol 4:726–734
Schachner M, Taylor J, Bartsch U, Pesheva P (1994) The perplexing multifunctionality of janusin, a tenascin-related molecule. Perspect Dev Neurobiol 2:33–41
Schenk S, Muser J, Vollmer G, Chiquet-Ehrismann R (1995) Tenascin-C in serum: a questionable tumor marker. Int J Cancer 61:443–449
Šekeljić V, Andjus PR (2012) Tenascin-C and its functions in neuronal plasticity. Int J Biochem Cell Biol 44:825–829
Siri A, Carnemolla B, Saginati M, Leprini A, Casari G, Baralle F, Zardi L (1991) Human tenascin: primary structure, pre-mRNA splicing patterns and localization of the epitopes recognized by two monoclonal antibodies. Nucleic Acids Res 19:525–531
Smith GM, Hale JH (1997) Macrophage/Microglia regulation of astrocytic tenascin: synergistic action of transforming growth factor-beta and basic fibroblast growth factor. J Neurosci 17:9624–9633
Soini Y, Pöllänen R, Autio-Harmainen H, Lehto VP (1997) Tenascin expression in lichen sclerosus. Int J Gynecol Pathol 16:313–318
Sorokin L (2010) The impact of the extracellular matrix on inflammation. Nat Rev Immunol 10:712–723
Spring J, Beck K, Chiquet-Erishmann R (1989) Two contrary functions of tenascin: dissection of the active sites by recombinant tenascin fragments. Cell 59:325–334
Srinivasan J, Schachner M, Catterall WA (1998) Interaction of voltage-gated sodium channels with the extracellular matrix molecules tenascin-C and tenascin-R. Proc Natl Acad Sci U S A 95:15753–15757
Taylor HC, Lightner VA, Beyer WF Jr, McCaslin D, Briscoe G, Erickson HP (1989) Biochemical and structural studies of tenascin/hexabrachion proteins. J Cell Biochem 41:71–90
Taylor J, Pesheva P, Schachner M (1993) Influence of janusin and tenascin on growth cone behavior in vitro. J Neurosci Res 35:347–362
Tiitta O, Sipponen P, Gould V, Virtanen I (1994) Tenascin expression in inflammatory, dysplastic and neoplastic lesions of the human stomach. Virchows Arch 425:369–374
Tiitta O, Luomanen M, Hietanen J, Virtanen I (1995) Tenascin expression in mucocutaneous diseases and related lesions of human oral mucosa. Arch Oral Biol 40:1039–1045
Tojyo I, Yamaguchi A, Nitta T, Yoshida H, Fujita S, Yoshida T (2008) Effect of hypoxia and interleukin-1beta on expression of tenascin-C in temporomandibular joint. Oral Dis 14:45–50
Tongiorgi E, Bernhardt RR, Zinn K, Schachner M (1995) Tenascin-C mRNA is expressed in cranial neural crest cells, in some placodal derivatives, and in discrete domains of the embryonic zebrafish brain. J Neurobiol 28:391–407
Trebaul A, Chan EK, Midwood KS (2007) Regulation of fibroblast migration by tenascin-C. Biochem Soc Trans 35:695–697
Treloar HB, Ray A, Dinglasan LA, Schachner M, Greer CA (2009) Tenascin-C is an inhibitory boundary molecule in the developing olfactory bulb. J Neurosci 29:9405–9416
Truong LD, Foster SV, Barrios R, D’Agati V, Verani RR, Gonzalez JM, Suki WN (1996) Tenascin is an ubiquitous extracellular matrix protein of human renal interstitium in normal and pathologic conditions. Nephron 72:579–586
Tucker RP, Brunso-Bechtold JK, Jenrath DA, Khan NA, Poss PM, Sweatt AJ, Xu Y (1994) Cellular origins of tenascin in the developing nervous system. Perspect Dev Neurobiol 2:89–99
Uede T (2011) Osteopontin, intrinsic tissue regulator of intractable inflammatory diseases. Pathol Int 61:265–280
Vaughan L, Huber S, Chiquet M, Winterhalter KH (1987) A major, six-armed glycoprotein from embryonic cartilage. EMBO J 6:349–353
Veje K, Hyllested-Winge JL, Ostergaard K (2003) Topographic and zonal distribution of tenascin in human articular cartilage from femoral heads: normal versus mild and severe osteoarthritis. Osteoarthritis Cartilage 11:217–227
Wallner K, Li C, Shah PK, Fishbein MC, Forrester JS, Kaul S, Sharifi BG (1999) Tenascin-C is expressed in macrophage-rich human coronary atherosclerotic plaque. Circulation 99:1284–1289
Weber P, Montag D, Schachner M, Bernhardt RR (1998) Zebrafish tenascin-W, a new member of the tenascin family. J Neurobiol 35:1–16
Weber P, Bartsch U, Rasband MN, Czaniera R, Lang Y, Bluethmann H, Margolis RU, Levinson SR, Shrager P, Montag D, Schachner M (1999) Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J Neurosci 19:4245–4262
Wiese S, Karus M, Faissner A (2012) Astrocytes as a source for extracellular matrix molecules and cytokines. Front Pharmacol 3:120
Wintergerst ES, Fuss B, Bartsch U (1993) Localization of janusin mRNA in the central nervous system of the developing and adult mouse. Eur J Neurosci 5:299–310
Wu B, Matic D, Djogo N, Szpotowicz E, Schachner M, Jakovcevski I (2012) Improved regeneration after spinal cord injury in mice lacking functional T- and B-lymphocytes. Exp Neurol 237:274–285
Xiao ZC, Ragsdale DS, Malhotra JD, Mattei LN, Braun PE, Schachner M, Isom LL (1999) Tenascin-R is a functional modulator of sodium channel beta subunits. J Biol Chem 274:26511–26517
Yoshida H, Yoshida T, Iizuka T, Sakakura T, Fujita S (1996) An immunohistochemical and in situ hybridization study of the expression of tenascin in synovial membranes from human temporomandibular joints with internal derangement. Arch Oral Biol 41:1081–1085
Yuasa S (1996) Bergmann glial development in the mouse cerebellum as revealed by tenascin expression. Anat Embryol (Berl) 194:223–230
Zhang Y, Winterbottom JK, Schachner M, Lieberman AR, Anderson PN (1997) Tenascin-C expression and axonal sprouting following injury to the spinal dorsal columns in the adult rat. J Neurosci Res 49:433–450
Zhao Y, Young SL, McIntosh JC (1998) Induction of tenascin in rat lungs undergoing bleomycin-induced tenascin inflammation - pulmonary fibrosis. Am J Physiol 274:L1049–L1057
Zhao C, Fancy SP, Franklin RJ, ffrench-Constant C (2009) Up-regulation of oligodendrocyte precursor cell alphaV integrin and its extracellular ligands during central nervous system remyelination. J Neurosci Res 87:3447-345
Acknowledgments
The authors are indebted to COST Action BM1001, funding from MESRS grants III41005, ON 173035 and ON 173013, and to the Southeast-Europe-Cooperation Hamburg. Melitta Schachner is supported by grants from the German Research Foundation, New Jersey Commission for Spinal Cord Research and Li Ka-Shing Foundation.
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Jakovcevski, I., Miljkovic, D., Schachner, M. et al. Tenascins and inflammation in disorders of the nervous system. Amino Acids 44, 1115–1127 (2013). https://doi.org/10.1007/s00726-012-1446-0
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DOI: https://doi.org/10.1007/s00726-012-1446-0