Tenascin-C stimulates contactin-dependent neurite outgrowth via activation of phospholipase C

Molecular and Cellular Neuroscience

Volumn 41, Issue 4, 2009, Pages 397-408

  Michele, Melanie ^a   Faissner, Andreas ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

1 integrin; Calmodulin kinase; Cell adhesion molecules; Fibronectin type III domains; Growth cone; Hippocampal neurons; Ig superfamily; IP3; Neurite outgrowth; Protein kinase C; Ryanodine receptor; SERCA; Tenascin glycoprotein

Indexed keywords

ANTIBODY; BETA1 INTEGRIN; CALCIUM CHANNEL; CHELATING AGENT; CONTACTIN; EGTAZIC ACID; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; PHOSPHOLIPASE C; PROTEIN KINASE C; SCLEROPROTEIN; TENASCIN;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CALCIUM TRANSPORT; CELL ISOLATION; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; FEMALE; HIPPOCAMPUS; NERVE CELL CULTURE; NERVE FIBER; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; RAT;

ANIMALS; ANIMALS, NEWBORN; ANTIBODIES; ANTIGENS, CD19; CALCIUM; CALMODULIN; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME INHIBITORS; FEMALE; HIPPOCAMPUS; MICE; NEURAL INHIBITION; NEURITES; NEURONS; PREGNANCY; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ANTIGEN; TENASCIN; TIME FACTORS; TYPE C PHOSPHOLIPASES;

RATTUS;

EID: 67149113775     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2009.04.004     Document Type: Article

References (56)

1. Berglund E.O., Murai K.K., Fredette B., Sekerkova G., Marturano B., Weber L., Mugnaini E., and Ranscht B. Ataxia and abnormal cerebellar microorganization in mice with ablated contactin gene expression. Neuron 24 (1999) 739-750
2. Berridge M.J. Inositol trisphosphate and calcium signalling. Nature 361 (1993) 315-325
3. Bleasdale J.E., Thakur N.R., Gremban R.S., Bundy G.L., Fitzpatrick F.A., Smith R.J., and Bunting S. Selective inhibition of receptor-coupled phospholipase C-dependent processes in human platelets and polymorphonuclear neutrophils. J. Pharmacol. Exp. Ther. 255 (1990) 756-768
4. Bonnon C., Goutebroze L., Denisenko-Nehrbass N., Girault J.A., and Faivre-Sarrailh C. The paranodal complex of F3/contactin and caspr/paranodin traffics to the cell surface via a non-conventional pathway. J. Biol. Chem. 278 (2003) 48339-48347
5. Bootman M.D., Berridge M.J., and Roderick H.L. Calcium signalling: more messengers, more channels, more complexity. Curr. Biol. 12 (2002) R563-565
6. Campos L.S., Leone D.P., Relvas J.B., Brakebusch C., Fassler R., Suter U., and ffrench-Constant C. Beta1 integrins activate a MAPK signalling pathway in neural stem cells that contributes to their maintenance. Development 131 (2004) 3433-3444
7. Denisenko-Nehrbass N., Goutebroze L., Galvez T., Bonnon C., Stankoff B., Ezan P., Giovannini M., Faivre-Sarrailh C., and Girault J.A. Association of Caspr/paranodin with tumour suppressor schwannomin/merlin and beta1 integrin in the central nervous system. J. Neurochem. 84 (2003) 209-221
8. Erickson H.P. Tenascin-C, tenascin-R and tenascin-X: a family of talented proteins in search of functions. Curr. Opin. Cell Biol. 5 (1993) 869-876
9. Faissner A. The tenascin gene family in axon growth and guidance. Cell Tissue Res. 290 (1997) 331-341
10. Faissner A., and Kruse J. J1/tenascin is a repulsive substrate for central nervous system neurons. Neuron 5 (1990) 627-637
11. Faissner A., and Steindler D. Boundaries and inhibitory molecules in developing neural tissues. Glia 13 (1995) 233-254
12. Faissner A., Kruse J., Chiquet-Ehrismann R., and Mackie E. The high-molecular-weight J1 glycoproteins are immunochemically related to tenascin. Differentiation 37 (1988) 104-114
13. Falk J., Bonnon C., Girault J.A., and Faivre-Sarrailh C. F3/contactin, a neuronal cell adhesion molecule implicated in axogenesis and myelination. Biol. Cell 94 (2002) 327-334
14. Fukamauchi F., Mataga N., Wang Y.J., Sato S., Youshiki A., and Kusakabe M. Abnormal behavior and neurotransmissions of tenascin gene knockout mouse. Biochem. Biophys. Res. Commun. 221 (1996) 151-156
15. Fukamauchi F., Mataga N., Wang Y.J., Sato S., Yoshiki A., and Kusakabe M. Tyrosine hydroxylase activity and its mRNA level in dopaminergic neurons of tenascin gene knockout mouse. Biochem. Biophys. Res. Commun. 231 (1997) 356-359
16. Fukamauchi F., Aihara O., and Kusakabe M. The effects of central administration of neuropeptide Y on behavior of tenascin-gene knockout mice. Neuropeptides 32 (1998) 461-464
17. Gomez T.M., and Zheng J.Q. The molecular basis for calcium-dependent axon pathfinding. Nat. Rev. Neurosci. 7 (2006) 115-125
18. Goslin K., and Banker G. Experimental observations on the development of polarity by hippocampal neurons in culture. J. Cell. Biol. 108 (1989) 1507-1516
19. Götz B., Scholze A., Clement A., Joester A., Schutte K., Wigger F., Frank R., Spiess E., Ekblom P., and Faissner A. Tenascin-C contains distinct adhesive, anti-adhesive, and neurite outgrowth promoting sites for neurons. J. Cell. Biol. 132 (1996) 681-699
20. Hong K., Nishiyama M., Henley J., Tessier-Lavigne M., and Poo M. Calcium signalling in the guidance of nerve growth by netrin-1. Nature 403 (2000) 93-98
21. Irintchev A., Rollenhagen A., Troncoso E., Kiss J.Z., and Schachner M. Structural and functional aberrations in the cerebral cortex of tenascin-C deficient mice. Cereb. Cortex 15 (2005) 950-962
22. Joester A., and Faissner A. Evidence for combinatorial variability of tenascin-C isoforms and developmental regulation in the mouse central nervous system. J. Biol. Chem. 274 (1999) 17144-17151
23. Joester A., and Faissner A. The structure and function of tenascins in the nervous system. Matrix Biol. 20 (2001) 13-22
24. Jones F.S., and Jones P.L. The tenascin family of ECM glycoproteins: structure, function, and regulation during embryonic development and tissue remodeling. Dev. Dyn. 218 (2000) 235-259
25. Jones N.P., Peak J., Brader S., Eccles S.A., and Katan M. PLCgamma1 is essential for early events in integrin signalling required for cell motility. J. Cell. Sci. 118 (2005) 2695-2706
26. Juttner R., More M.I., Das D., Babich A., Meier J., Henning M., Erdmann B., Mu Ller E.C., Otto A., Grantyn R., and Rathjen F.G. Impaired synapse function during postnatal development in the absence of CALEB, an EGF-like protein processed by neuronal activity. Neuron 46 (2005) 233-245
27. Lee S.B., and Rhee S.G. Significance of PIP2 hydrolysis and regulation of phospholipase C isozymes. Curr. Opin. Cell Biol. 7 (1995) 183-189
28. Lipscombe D., Madison D.V., Poenie M., Reuter H., Tsien R.Y., and Tsien R.W. Spatial distribution of calcium channels and cytosolic calcium transients in growth cones and cell bodies of sympathetic neurons. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 2398-2402
29. Lochter A., and Schachner M. Tenascin and extracellular matrix glycoproteins: from promotion to polarization of neurite growth in vitro. J. Neurosci. 13 (1993) 3986-4000
30. Lochter A., Vaughan L., Kaplony A., Prochiantz A., Schachner M., and Faissner A. J1/tenascin in substrate-bound and soluble form displays contrary effects on neurite outgrowth. J. Cell. Biol. 113 (1991) 1159-1171
31. Maness P.F., and Schachner M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat. Neurosci. 10 (2007) 19-26
32. Mattson M.P. Calcium and neurodegeneration. Aging Cell 6 (2007) 337-350
33. Meiners S., and Geller H.M. Long and short splice variants of human tenascin differentially regulate neurite outgrowth. Mol. Cell. Neurosci. 10 (1997) 100-116
34. Meiners S., Mercado M.L., Nur-e-Kamal M.S., and Geller H.M. Tenascin-C contains domains that independently regulate neurite outgrowth and neurite guidance. J. Neurosci. 19 (1999) 8443-8453
35. Meiners S., Nur-e-Kamal M.S., and Mercado M.L. Identification of a neurite outgrowth-promoting motif within the alternatively spliced region of human tenascin-C. J. Neurosci. 21 (2001) 7215-7225
36. Mercado M.L., Nur-e-Kamal A., Liu H.Y., Gross S.R., Movahed R., and Meiners S. Neurite outgrowth by the alternatively spliced region of human tenascin-C is mediated by neuronal alpha7beta1 integrin. J. Neurosci. 24 (2004) 238-247
37. Muller-Decker K. Interruption of TPA-induced signals by an antiviral and antitumoral xanthate compound: inhibition of a phospholipase C-type reaction. Biochem. Biophys. Res. Commun. 162 (1989) 198-205
38. Norenberg U., Wille H., Wolff J.M., Frank R., and Rathjen F.G. The chicken neural extracellular matrix molecule restrictin: similarity with EGF-, fibronectin type III-, and fibrinogen-like motifs. Neuron 8 (1992) 849-863
39. Powell E.M., and Geller H.M. Dissection of astrocyte-mediated cues in neuronal guidance and process extension. Glia 26 (1999) 73-83
40. Revest J.M., Faivre-Sarrailh C., Maeda N., Noda M., Schachner M., and Rougon G. The interaction between F3 immunoglobulin domains and protein tyrosine phosphatases zeta/beta triggers bidirectional signalling between neurons and glial cells. Eur. J. Neurosci. 11 (1999) 1134-1147
41. Rigato F., Garwood J., Calco V., Heck N., Faivre-Sarrailh C., and Faissner A. 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. J. Neurosci. 22 (2002) 6596-6609
42. Rios J.C., Melendez-Vasquez C.V., Einheber S., Lustig M., Grumet M., Hemperly J., Peles E., and Salzer J.L. Contactin-associated protein (Caspr) and contactin form a complex that is targeted to the paranodal junctions during myelination. J. Neurosci. 20 (2000) 8354-8364
43. Staniszewska I., Sariyer I.K., Lecht S., Brown M.C., Walsh E.M., Tuszynski G.P., Safak M., Lazarovici P., and Marcinkiewicz C. Integrin alpha9 beta1 is a receptor for nerve growth factor and other neurotrophins. J. Cell Sci. 121 (2008) 504-513
44. Steindler D.A. Glial boundaries in the developing nervous system. Annu. Rev. Neurosci. 16 (1993) 445-470
45. Strekalova T., Sun M., Sibbe M., Evers M., Dityatev A., Gass P., and Schachner M. Fibronectin domains of extracellular matrix molecule tenascin-C modulate hippocampal learning and synaptic plasticity. Mol. Cell. Neurosci. 21 (2002) 173-187
46. Thomas D., and Hanley M.R. Pharmacological tools for perturbing intracellular calcium storage. Methods Cell Biol. 40 (1994) 65-89
47. Treubert U., and Brummendorf T. Functional cooperation of beta1-integrins and members of the Ig superfamily in neurite outgrowth induction. J. Neurosci. 18 (1998) 1795-1805
48. Tsien R.Y. New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry 19 (1980) 2396-2404
49. Tucker R.P. Guest editor of the special issue: the function of tenascin: hypotheses and current knowledge. Perspect. Dev. Neurobiol. 2 (1994) 1-132
50. Webb S.E., Moreau M., Leclerc C., and Miller A.L. Calcium transients and neural induction in vertebrates. Cell. Calcium 37 (2005) 375-385
51. Weissman T.A., Riquelme P.A., Ivic L., Flint A.C., and Kriegstein A.R. Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43 (2004) 647-661
52. Weller A., Beck S., and Ekblom P. Amino acid sequence of mouse tenascin and differential expression of two tenascin isoforms during embryogenesis. J. Cell Biol. 112 (1991) 355-362
53. Wen Z., and Zheng J.Q. Directional guidance of nerve growth cones. Curr. Opin. Neurobiol. 16 (2006) 52-58
54. Wigger F. Signal Transduction of Tenascin-C in Neurite Outgrowth of Hippocampal Neurons. Institute of Anatomy and Cellbiology III/Department of Neuroanatomy (2000), Ruprecht-Karls University, Heidelberg 128
55. Xiao Z.C., Revest J.M., Laeng P., Rougon G., Schachner M., and Montag D. Defasciculation of neurites is mediated by tenascin-R and its neuronal receptor F3/11. J Neurosci. Res. 52 (1998) 390-404
56. Zheng J.Q., and Poo M.M. Calcium signaling in neuronal motility. Annu. Rev. Cell Dev. Biol. 23 (2007) 375-404