Tenascin-C inhibits oligodendrocyte precursor cell migration by both adhesion-dependent and adhesion-independent mechanisms

Molecular and Cellular Neurosciences

Volumn 7, Issue 4, 1996, Pages 322-335

  Kiernan, B W ^a,b   Götz, Bernhard ^c   Faissner, Andreas ^c   Ffrench Constant, Charles ^a,b  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; TENASCIN;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; BRAIN CELL; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; MYELINATION; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; OLIGODENDROGLIA; OPTIC NERVE; PRIORITY JOURNAL; PROTEIN DOMAIN; RAT; STEM CELL;

EID: 0342748386     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1006/mcne.1996.0024     Document Type: Article

References (77)

1. Aukhil, I., Joshi, P., Yan, Y., and Erickson, H. P. (1993). Cell- and heparin-binding domains of the hexabrachion arm identified by tenascin expression proteins. J. Biol. Chem. 268: 2542-2553.
2. Barnea, G., Grumet, M., Milev, P., Silvennoinen, O., Levy, J. B., Sap, J., and Schlessinger, J. (1994). Receptor tyrosine phosphatase β is expressed in the form of proteoglycan and binds to the extracellular matrix protein tenascin. J. Biol. Chem. 269: 14349-14352.
3. Barres, B. A., Koroshetz, W. J., Swartz, K. J., Chun, L. L. Y., and Corey, D. P. (1990). Ion channel expression by white matter glia: The O-2A glial progenitor cell. Neuron 4: 507-524.
4. Bartsch, S., Bartsch, U., Dörries, U., Faissner, A., Weller, A., Ekblom, P., and Schachner, M. (1992a). Expression of tenascin in the developing and adult cerebellar cortex. J. Neurosci. 12: 736-749.
5. Bartsch, U., Bartsch, S., Dörries, U., and Schachner, M. (1992b). Immunohistological localization of tenascin in the developing and lesioned adult mouse optic nerve. Eur. J. Neurosci. 4: 338-352.
6. Bartsch, U., Faissner, A., Trotter, J., Dörries, U., Bartsch, S., Mohajeri, H., and Schachner, M. (1994). Tenascin demarcates the boundary between the myelinated and non-myelinated part of retinal ganglion cell axons in the developing and adult mouse. J. Neurosci. 14: 4756-4768.
7. Bottenstein, J. E., and Sato, G. H. (1979). Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc. Natl. Acad. Sci. USA 76: 515-517.
8. Bourdon, M. A., and Ruoslahti, E. (1989). Tenascin mediates cell attachment through an RGD-dependent receptor. J. Cell Biol. 108: 1149-1155.
9. Bristow, J., Tee, M. K., Gitelman, S. E., Mellon, S. H., and Miller, W. L. (1993). Tenascin-X: A novel extracellular matrix protein encoded by the human XB gene overlapping P450c21B. J. Cell Biol. 122: 265-278.
10. Cameron-Curry, P., and Le Douarin, N. M. (1995). Oligodendrocyte precursors originate from both the dorsal and the ventral parts of the spinal cord. Neuron 15: 1299-1310.
11. Chiquet-Ehrismann, R. (1991). Anti-adhesive molecules of the extracellular matrix. Curr. Op. Cell Biol. 3: 800-804.
12. Chung, C. Y., and Erickson, H. P. (1994). Cell surface annexin II is a high affinity receptor for the alternatively spliced segment of tenascin-C. J. Cell Biol. 126: 539-548.
13. Chuong, C-M., Crossin, K. L., and Edelman, G. M. (1987). Sequential expression and differential function of multiple adhesion molecules during the formation of the cerebellar cortical layers. J. Cell Biol. 104: 331-342.
14. Crossin, K. L. (1991). Cytotactin binding: inhibition of stimulated proliferation and intracellular alkalinization in fibroblasts. Proc. Natl. Acad. Sci. USA 88: 11403-11407.
15. Crossin, K. L., Hoffman, S., Tan, S.-S., and Edelman, G. M. (1989). Cytotactin and its proteoglycan ligand mark structural and functional boundaries in somatosensory cortex of the early postnatal mouse. Dev. Biol. 136: 381-392.
16. Davies, J. A., Cook, G. M. W., Stern, D. C., and Keynes, R. J. (1990). Isolation from chick somites of a glycoprotein fraction that causes collapse of dorsal root ganglion growth cones. Neuron 4: 11-20.
17. DiMilla, P. A., Stone, J. A., Quinn, J. A., Albelda, S. M., and Lauffenburger, D. A. (1993). Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength. J. Cell Biol. 122: 729-737.
18. Dodd, J., and Schuchardt, A. (1995). Axon guidance: A compelling case for repelling growth cones. Cell 81: 471-474.
19. Duncan, I. D., Hammang, J. P., Jackson, K. F., Wood, P. M., Bunge, R. P., and Langford, L. (1988). Transplantation of oligodendrocytes and schwann cells into the spinal cord of the myelin-deficient rat. J. Neurocytol. 17: 351-360.
20. Eisenbarth, G. S., Walsh, F. S., and Nirenberg, M. (1979). A monoclonal antibody to a plasma membrane antigen of neurones. Proc. Natl. Acad. Sci. USA 76: 4913-4917.
21. Erickson, H. P. (1993a). Gene knockouts of c-src, transforming growth factor B1, and tenascin suggest superfluous, nonfunctional expression of proteins. J. Cell Biol. 120: 1079-1081.
22. Erickson, H. P. (1993b). Tenascin-C, tenascin-R and tenascin-X: A family of talented proteins in search of functions. Curr. Op. Cell Biol. 5: 869-876.
23. Faissner, A., Gotz, B., Joester, A., and Scholze, A. (1995). The tenascin gene family - Versatile glycoproteins implicated in neural pattern formation and regeneration. Semin. Dev. Biol. 6: 139-148.
24. Faissner, A., and Kruse, J. (1990). J1/Tenascin is a repulsive substrate for central nervous system neurons. Neuron 5: 627-637.
25. Fan, J., and Raper, J. A. (1995). Localized collapsing cues can steer growth cones without inducing their full collapse. Neuron 14: 263-274.
26. ffrench-Constant, C., Miller, R. H., Burne, J. F., and Raff, M. C. (1988). Evidence that migratory oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells are kept out of the rat retina by a barrier at the eye-end of the optic nerve. J. Neurocytol. 17: 13-25.
27. Gansmuller, A., Clerin, E., Kruger, F., Gumpel, M., and Lachapelle, F. (1991). Tracing transplanted oligodendrocytes during migration and maturation in the shiverer mouse brain. Glia 4: 580-590.
28. Gonzalez, M. d. L., Malemud, C. J., and Silver, J. (1993). Role of astroglial extracellular matrix in the formation of rat olfactory bulb glomeruli. Exp. Neurol. 123: 91-105.
29. Götz, B., Scholze, A., Clement, A., Joester, A., Schütte, K., Wigger, F., Frank, R., Spiess, E., Ekblom, P., and Faissner, A. (1996). Tenascin-C contains distinct adhesive, anti-adhesive and neurite outgrowth promoting sites for neurons. J. Cell Biol. 132: 681-699.
30. Grumet, M., Milev, P., Sakurai, T., Karthikeyan, L., Bourdon, M., Margolis, R. K., and Margolis, R. U. (1994). Interactions with tenascin and differential effects on cell adhesion of neurocan and phosphacan, two major chondroitin sulfate proteoglycans of nervous tissue. J. Biol. Chem. 269: 12142-12146.
31. Gumpel, M., Gout, O., Gansmuller, A., and Baumann, N. (1989). Myelination and remyelination in the central nervous system by transplanted oligodendrocytes using the shiverer model. Dev. Neurosci. 11: 132-139.
32. Hoffman, S., and Edelman, G. M. (1987). A proteoglycan with HNK-1 antigenic determinants is a neuron-associated ligand for cytotactin. Proc. Natl. Acad. Sci. USA 84: 2523-2527.
33. Husmann, K., Faissner, A., and 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.
34. Johnson, G. D., Davidson, R. S., McNamee, K. C., Russell, G., Goodwin, D., and Holborow, E. J. (1982). Fading of immunofluorescence during microscopy: A study of the phenomenon and its remedy. J. Immunol. Methods 55: 231-242.
35. Kiernan, B. W., Faissner, A., and ffrench-Constant, C. (1993). The effect of tenascin on the adhesion and migration of O-2A progenitor cells. Soc. Neurosci. Abstr. 19: 874.
36. Kiernan, B. W., and ffrench-Constant, C. (1993). Oligodendrocyte precursor (O-2A progenitor cell) migration; a model system for the study of cell migration in the developing central nervous system. Development 1993 Supplement: 219-225.
37. Kolodkin, A. L., Matthes, D. J., O'Connor, T. P., Patel, N. H., Admon, A., Bentley, D., and Goodman, C. S. (1992). Fasciclin IV: Sequence, expression and function during growth cone guidance in the grasshopper embryo. Neuron 9: 831-845.
38. Kolodkin, A. L., Matthes, D. J., and Goodman, C. S. (1993). The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75: 1389-1399.
39. Krull, C. E., Morton, D. B., Faissner, A., Schachner, M., and Tolbert, L. P. (1994). Spatiotemporal pattern of expression of tenascin-like molecules in a developing insect olfactory system. J. Neurobiol. 25: 515-534.
40. Letourneau, P. C., Condic, M. L., and Snow, D. M. (1994). Interactions of developing neurons with the extracellular matrix. J. Neurosci. 14: 915-928.
41. Levison, S. W., Chuang, C., Abramson, B. J., and Goldman, J. E. (1993). The migrational patterns and developmental fates of glial precursors in the rat subventricular zone are temporally regulated. Development 119: 611-622.
42. 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. J. Cell Biol. 113: 1159-1171.
43. Louis, J.-C., Magal, E., Muir, D., Manthorpe, M., and Varon, S. (1992). CG-4, a new bipotential glial cell line from rat brain, is capable of differentiating in vitro into either mature oligodendrocytes or type-2 astrocytes. J. Neurosci. Res. 31: 193-204.
44. Luo, Y., Raible, D., and Raper, J. A. (1993). Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75: 217-227.
45. Luo, Y., and Raper, J. A. (1994). Inhibitory factors controlling growth cone motility and guidance. Curr. Op. Neurobiol. 4: 648-654.
46. Matsumoto, K., Arai, M., Ishihara, N., Ando, A., Inoko, H., and Ikemura, T. (1992). Cluster of fibronectin type III repeats found in the major histocompatibility complex class III region shows the highest homology with the repeats in an extracellular matrix protein, tenascin. Genomics 12: 485-491.
47. Matsumoto, K., Saga, Y., Ikemura, T., Sakakura, T., and Chiquet-Ehrismann, R. (1994). The distribution of tenascin-X is distinct and often reciprocal to that of tenascin-C. J. Cell Biol. 125: 483-493.
48. Maurel, P., Rauch, U., Flad, M., Margolis, R. K., and Margolis, R. U. (1994). Phosphacan, a chondroitin sulfate proteoglycan of brain that interacts with neurons and neural cell-adhesion molecules, is an extracellular variant of a receptor-type protein tyrosine phosphatase. Proc. Natl. Acad. Sci. USA 91: 2512-2516.
49. McCarthy, K. D., and de Vellis, J. (1980). Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85: 890-902.
50. Milner, R., and ffrench-Constant, C. (1994) A developmental analysis of oligodendroglial integrins in primary cells: changes β subunits during differentiation. Development 120: 3497-3506.
51. Mitrovic, N., and Schachner, M. (1995). Detection of tenascin-C in the nervous system of the tenascin-C mutant mouse. J. Neurosci. Res. 42: 710-717.
52. Murphy-Ullrich, J. E., Lightner, V. A., Aukhil, I., Yan, Y. Z., Erickson, H. P., and Hook, M. (1991). Focal adhesion integrity is downregulated by the alternatively spliced domain of human tenascin. J. Cell Biol. 115: 1127-1136.
53. Noble, M., Murray, K., Stroobant, P., Waterfield, M. D., and Riddle, P. (1988). Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature 333: 560-562.
54. Nörenberg, U., Wille, H., Wolff, J. M., Frank, R., and Rathjen, F. G. (1992). The chicken neural extracellular matrix molecule restrictin: similarity with EGF-, fibronectin Type III-, and fibrinogen-like motifs. Neuron 8: 849-863.
55. 3H-thymidine injection into the lateral ventricle of the brain of young rats. J. Comp. Neurol. 149: 83-102.
56. Perry, V. H., and Lund, R. D. (1990). Evidence that the lamina cribrosa prevents intraretinal myelination of retinal ganglion cell axons. J. Neurocytol. 19: 265-272.
57. Pesheva, P., Gennarini, G., Goridis, C., and 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.
58. Pesheva, P., Probstmeier, R., Skubitz, A. P. N., McCarthy, J. B., Furcht, L. T., and Schachner, M. (1994). Tenascin-R (J1 160/180) inhibits fibronectin-mediated cell adhesion-functional relatedness to tenascin-C. J. Cell Sci. 107: 2323-2333.
59. Pesheva, P., Spiess, E., and Schachner, M. (1989). J1-160 and J1-180 are oligodendrocyte-secreted nonpermissive substrates for cell adhesion. J. Cell Biol. 109: 1765-1778.
60. Prieto, A. L., Andersson-Fisone, C., and Crossin, K. L. (1992). Characterization of multiple adhesive and counteradhesive domains in the extracellular matrix protein cytotactin. J. Cell Biol. 119: 663-678.
61. Prieto, A. L., Edelman, G. M., and Crossin, K. L. (1993). Multiple integrins mediate cell attachment to cytotactin/tenascin. Proc. Natl. Acad. Sci. USA 90: 10154-10158.
62. Pringle, N. P., and Richardson, W. D. (1993). A singularity of PDGF alpha-receptor expression in the dorsoventral axis of the neural tube may define the origin of the oligodendroglial lineage. Development 117: 525-533.
63. Ranscht, B., Clapshaw, P. A., Price, J., Noble, M., and Seifert, W. (1982). Development of oligodendrocytes and Schwann cells studied with a monoclonal antibody against galactocerebroside. Proc. Natl. Acad. Sci. USA 79: 2709-2713.
64. Raper, J. A., and Kapfhammer, J. P. (1990). The enrichment of a neuronal growth cone collapsing activity from embryonic chick brain. Neuron 4: 21-29.
65. Riou, J.-F., Shi, D.-L., Chiquet, M., and Boucaut, J.-C. (1990). Exogenous tenascin inhibits mesodermal cell migration during amphibian gastrulation. Dev. Biol. 137: 305-317.
66. Saga, Y., Yagi, T., Ikawa, Y., Sakakura, T., and Aizawa, S. (1992). Mice develop normally without tenascin. Genes Dev. 6: 1821-1831.
67. Sheppard, A. M., Hamilton, S. K., and Pearlman, A. L. (1991). Changes in the distribution of extracellular matrix components accompany early morphogenetic events of mammalian cortical development. J. Neurosci. 11: 3928-3942.
68. Spring, J., Beck, K., and Chiquet-Ehrismann, R. (1989). Two contrary functions of tenascin: Dissection of the active sites by recombinant tenascin fragments. Cell 59: 325-334.
69. 3 integrins. J. Cell Sci. 105: 1001-1012.
70. Steindler, D. A., Cooper, N. G. F., Faissner, A., and 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.
71. Steindler, D. A., Settles, D., Erickson, H. P., Laywell, E. D., Yoshiki, A., Faissner, A., and Kusakabe, M. (1995). Tenascin knockout mice: Barrels, boundary molecules, and glial scars. J. Neurosci. 15: 1971-1983.
72. Tan, S.-S., Crossin, K. L., Hoffman, S., and Edelman, G. M. (1987). Asymmetric expression in somites of cytotactin and its proteoglycan ligand is correlated with neural crest cell distribution. Proc. Natl. Acad. Sci. USA 84: 7977-7981.
73. Taylor, J., Pesheva, P., and Schachner, M. (1993). Influence of janusin and tenascin on growth cone behavior in vitro. J. Neurosci. Res. 35: 347-362.
74. Varnum-Finney, B., Venstrom, K., Muller, M., Kypta, R., Backus, C., Chiquet, M., and Reichardt, L. F. (1995). The integrin receptor α8β1 mediates interactions of embryonic chick motor and sensory neurons with tenascin-C. Neuron 14: 1213-1222.
75. Wehrle, B., and Chiquet, M. (1990). Tenascin is accumulated along developing peripheral nerves and allows neurite outgrowth in vitro. Development 110: 401-415.
76. 1 mediates cell attachment to a non-RGD site in the third fibronectin type III repeat of tenascin. J. Biol. Chem. 269: 26691-26696.
77. Zisch, A. H., D'Alessandri, L., Ranscht, B., Falchetto, R., Winterhalter, K. H., and Vaughan, L. (1992). Neuronal cell adhesion molecule contactin/F11 binds to tenascin via its immunoglobulin-like domains. J. Cell Biol. 119: 203-213.