Chick sensory neuronal growth cones distinguish fibronectin from laminin by making substratum contacts that resemble focal contacts

Journal of Neurobiology

Volumn 29, Issue 1, 1996, Pages 18-34

  Gomez, Timothy M ^a   Roche, Florence K ^a   Letourneau, Paul C ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

fibronectin; focal contact; growth cone; integrin; phosphotyrosine

Indexed keywords

FIBRONECTIN; INTEGRIN; LAMININ; PHOSPHOTYROSINE;

ANIMAL CELL; ARTICLE; CHICKEN; GROWTH REGULATION; NERVE FIBER GROWTH; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 0030061703     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199601)29:1<18::AID-NEU2>3.0.CO;2-A     Document Type: Article

References (68)

1. ARREGUI, C. O., CARBONETTO, S., and MCKERRACHER, L. (1994). Characterization of neural cell adhesion sites: point contacts are the sites of interaction between integrins and the cytoskeleton. J. Neurosci. 14:6967-6977.
2. BIXBY, J. L. and JHABVALA, P. (1992). Inhibition of tyrosine phosphorylation potentiates substrate-induced neurite growth. J. Neurobiol. 23:468-480.
3. BIXBY, J. L. and JHABVALA, P. (1993). Tyrosine phosphorylation in early embryonic growth cones. J Neurosci. 13:3421-3432.
4. BRELJE, T. C., WESSENDORF, M. W., and SORENSON, R. L. (1993). Multicolor laser scanning confocal immunofluorescence microscopy: practical application and limitations. In: Methods in Cell Biology B. Matsumoto, Ed. Academic Press, New York, pp. 97-181.
5. BURRIDGE, K., TURNER, C. E., and ROMER, L. H. (1992). Tyrosine phosphorylation of paxillin and pp125FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol. 119:893-903.
6. CALOF, A. L. and LANDER, A. D. (1991). Relationship between neuronal migration and cell-substratum adhesion: laminin and merosin promote olfactory neuronal migration but are anti-adhesive. J. Cell Biol. 115:779-794.
7. CALOF, A. L., CAMPANERO, M. R., O'REAR, J. J., YURCHENKO, P. D., and LANDER, A. D. (1994). Domain-specific activation of neuronal migration and neurite outgrowth-promoting activities of laminin. Neuron 13:117-130.
8. CRAWFORD, A. W. and BECKERLE, M. C. (1991). Purification and characterization of zyxin, an 82,000-dalton component of adherens junctions. J. Biol. Chem. 266:5847-5853.
9. CRAWFORD, A. W., MICHELSEN, J. W., and BECKERLE, M. C. (1992). An interaction between zyxin and α-actinin. J. Cell Biol. 116:1381-1393.
10. CYPHER, C. and LETOURNEAU, P. C. (1991). Identification of cytoskeletal, focal adhesion, and cell adhesion proteins in growth cone particles isolated from developing chick brain. J. Neurosci. Res. 30:259-265.
11. DEPASQUALE, J. A. and IZZARD, C. S. (1987). Evidence for an actin-containing cytoplasmic precursor of the focal contact and the timing of incorporation of vinculin at the focal contact. J. Cell Biol. 105:2803-2809.
12. DOHERTY, P. and WALSH, F. S. (1994). Signal transduction events underlying neurite outgrowth stimulated by cell adhesion molecules. Curr. Opin. Neurobiol. 4:49-55.
13. DOHERTY, P., FURNESS, J., WILLIAMS, E. J., and WALSH, F. S. (1994). Neurite outgrowth stimulated by the tyrosine kinase inhibitor herbimycin A requires activation of tyrosine kinases and protein kinase C. J. Neurochem. 62:2124-2131.
14. FUKAZAWA, H., LI, P.-M., YAMAMOTO, C., MURAKAMI, Y., MIZUNO, S., and UEHARA, Y. (1991). Specific inhibition of cytoplasmic tyrosine kinases by herbimycin A in vitro. Biochem. Pharmacol. 42:1661-1671.
15. GOMEZ, T. M. and LETOURNEAU, P. C. (1994). Filopodia initiate choices made by sensory neuron growth cones at laminin/fibronectin borders in vitro. J. Neurosci. 14:5959-5972.
16. GUNDERSEN, R. W. (1987). Response of sensory neurites and growth cones to patterned substrata of laminin and fibronectin in vitro. Dev. Biol. 121:423-431.
17. GUNDERSEN, R. W. (1988). Interference reflection microscopic study of dorsal root growth cones on different substrates: assessment of growth cone-substrate contacts. J. Neurosci. Res. 21:298-306.
18. HANISSIAN, S. H., CHATILA, T. and SAHYOUN, N. E. (1992). Association of neuronal pp60c-src with growth cone glycoproteins of rat brain. J. Neurobiol. 23:803-813.
19. HEATH, J. P. and DUNN, G. A. (1978). Cell to substratum contacts of chick fibroblasts and their relation to the microfilament system. A correlated interference-reflexion and high voltage electron-microscope study. J. Cell Sci. 29:197-212.
20. HEIDEMANN, S. R., LAMOUREUX, P., and BUXBAUM, R. E. (1991). On the cytomechanics and fluid dynamics of growth cone motility. J. Cell Sci. 15(suppl.):35-44.
21. HELMKE, S. and PFENNINGER, K. H. (1995). Growth cone enrichment and cytoskeletal association of nonreceptor tyrosine kinases. Cell Motil. Cytoskel. 30:194-207.
22. HUMPHRIES, M. J., AKIYAMA, S. K., KOMIRIYA, A., OLDEN, K., and YAMADA, K. M. (1988). Neurite extension of chicken peripheral nervous system neurons on fibronectin. Relative importance of specific adhesion sites in the central cell-binding domain and the alternatively spliced type III connecting segment. J. Cell Biol. 106:1289-1298.
23. HYNES, R. O. (1992). Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69:11-25.
24. HYNES, R. O. and LANDER, A. D. (1992). Contact and adhesive specificities in the associations, migrations, and targeting of cells and axons. Cell 68:303-322.
25. IGNELZI, M. A., JR., MILLER, D. R., SORIANO, P., and MANESS, P. F. (1994). Impaired neurite outgrowth of src-minus cerebellar neurons on the cell adhesion molecule L1. Neuron 12:873-884.
26. IZZARD, C. S. and LOCHNER, L. R. (1976). Cell-to-substrate contacts in living fibroblasts: an interference reflexion study with an evaluation of the technique. J. Cell Sci. 21:129-159.
27. IZZARD, C. S. and LOCHNER, L. R. (1980). Formation of cell-to-substrate contacts during fibroblast motility: an interference-reflexion study. J. Cell Sci. 42:81-116.
28. JULIANO, R. L. and HASKILL, S. (1993). Signal transduction from extracellular matrix. J. Cell Biol. 120: 577-585.
29. KATER, S. B. and MILLS, L. R. (1991). Regulation of growth cone behavior by calcium. J. Neurosci. 11:891-899.
30. KORNBERG, L. J., EARP, H. S., TURNER, C. E., PROCKOP, C. and JULIANO, R. L. (1991). Signal transduction by integrins: increased protein tyrosine phosphorylation caused by clustering β1 integrins. Proc. Natl. Acad. Sci. USA 88:8392-8396.
31. KUHN, T. B., SCHMIDT, M. F., and KATER, S. B. (1995). Laminin and fibronectin guideposts signal sustained but opposite effects to passing growth cones. Neuron 14:275-285.
32. LANKFORD, K. L. and LETOURNEAU, P. C. (1989). Evidence that calcium may control neurite outgrowth by regulating the stability of actin filaments. J. Cell Biol. 109:1229-43.
33. LANKFORD, K. L. and LETOURNEAU, P. C. (1991). Roles of actin filaments and three second-messenger systems in short-term regulation of chick dorsal root ganglion neurite outgrowth. Cell Motil. Cytoskel. 20:7-29.
34. LETOURNEAU, P. C. (1975). Possible roles for cell-to-substratum adhesion in neuronal morphogenesis. Dev. Biol. 44:77-91.
35. LETOURNEAU, P. C. (1979). Cell-substratum adhesion of neurite growth cones, and its role in neurite elongation. Exp. Cell Res. 124:127-138.
36. LETOURNEAU, P. C. (1989). Nerve cell shape. In: Cell Shape, Determinants, Regulation and Regulatory Roles F. Bronner and W. D. Stein, Eds. Academic Press, New York, pp. 247-289.
37. LETOURNEAU, P. C. (1996). The cytoskeleton in nerve growth cone motility and axonal pathfinding. Perspect Dev. Neurobiol. (in press).
38. LETOURNEAU, P. C. and CYPHER, C. (1991). Regulation of growth cone motility. Cell Motil. Cytoskel. 20:267-271.
39. LETOURNEAU, P. C. and SHATTUCK, T. A. (1989). Distribution and possible interactions of actin-associated proteins and cell adhesion molecules of nerve growth cones. Development 105:505-519.
40. LETOURNEAU, P. C., PECH, I. V., ROGERS, S. L., PALM, S. L., MCCARTHY, J. B., and FURCHT, L. T. (1988). Growth cone migration across extracellular matrix components depends on integrin, but migration across glioma cells does not. J. Neurosci. Res. 21:286-297.
41. LETOURNEAU, P. C., SHATTUCK, T. A., ROCHE, F. K., TAKEICHI, M., and LEMMON, V. (1990). Nerve growth cone migration onto Schwann cells involves the calcium-dependent adhesion molecule, N-cadherin. Dev. Biol. 138:430-442.
42. ++-regulated proteins. Prog. Brain Res. 102:35-48.
43. LETOURNEAU, P. C., CONDIC, M. L., and SNOW, D. M. (1994b). Interactions of developing neurons with the extracellular matrix. J. Neurosci. 14:915-928.
44. FAK in platelets. J. Cell Biol. 119:905-912.
45. MAHER, P. A., PASQUALE, E. B., WANG, J. Y. J., and SINGER, S. J. (1985). Phosphotyrosine-containing proteins are concentrated in focal adhesions and intercellular junctions in normal cells. Proc. Natl. Acad. Sci. USA 82:6576-6580.
46. MANESS, P. F., AUBRY, M., SHORES, C. G., FRAME, L., and PFENNINGER, K. H. (1988). c-src gene product in developing rat brain is enriched in nerve growth cone membranes. Proc. Natl. Acad. Sci. USA 85:5001-5005.
47. MEYERSON, G., PFENNINGER, K. H., and PAHLMAN, N. E. (1992). A complex consisting of pp60c-src/ pp60c-srcN and a 38 kDa protein is highly enriched in growth cones from differentiated SH-SY5Y neurobtastoma cells. J. Cell Sci. 103:233-243.
48. PASQUALINI, R. and HEMLER, M. E. (1994). Contrasting roles for integrin β1 and β5 cytoplasmic domains in subcellular localization, cell proliferation and cell migration. J. Cell Biol. 125:447-460.
49. ROGERS, S. L., EDSON, K. J., LETOURNEAU, P. C., and MCLOON, S. C. (1986). Distribution of laminin in the developing nervous system of the chick. Dev. Biol. 113:429-435.
50. ROGERS, S. L., LETOURNEAU, P. C., and PECH, I. V. (1989). The role of fibronectin in neural development. Dev. Neurosci. 11:248-265.
51. ROMER, L. H., BURRIDGE, K., and TURNER, C. E. (1992). Signaling between the extracellular matrix and the cytoskeleton: tyrosine phosphorylation and focal adhesion assembly. Cold Spring Harbor Symp. Quant. Biol. 57:193-202.
52. SADLER, I., CRAWFORD, A. W., MICHELSEN, J. W., and BECKERLE, M. C. (1992). Zyxin and cCRP: two interactive LIM domain proteins associated with the cytoskeleton. J. Cell Biol. 119:1573-1588.
53. SASTRY, S. K. and HORWITZ, A. F. (1993). Integrin cytoplasmic domains: mediators of cytoskeletal linkages and extra- and intracellular initiated transmembrane signaling. Curr. Opin. Cell Biol. 5:819-831.
54. SCHALLER, M. D. and PARSONS, J. T. (1994). Focal adhesion kinase and associated proteins. Curr. Opin. Cell Biol. 5:705-709.
55. SCHALLER, M. D., BORGMAN, C. A., COBB, B. S., VINES, R. R., REYNOLDS, A. B., and PARSONS, J. T. (1992). pp125FAK, a structurally unique protein tyrosine kinase associated with focal adhesions. Proc. Natl. Acad. Sci. USA 89:5192-5196.
56. SOBUE, K. and KANDA, K. (1988). Localization of pp60c-src in growth cones of PC12 cells. Biochem. Biophys. Res Commun. 157:1383-1389.
57. STOSSEL, T. P. (1993). On the crawling of animal cells. Science 260:1086-1094.
58. TAWIL, N., WILSON, P., and CARBONETTO, S. (1993). Integrins in point contacts mediated cell spreading: factors that regulate integrin accumulation in point contacts vs. focal contacts. J. Cell Biol. 120:261-271.
59. TODD, I., MELLOR, J. S., GINGELL, D. (1988). Mapping cell-glass contacts of Dictyostelium amoebae by total internal reflection aqueous fluorescence overcomes a basic ambiguity of interference reflection microscopy. J. Cell Sci. 89:107-114.
60. TOMASELLI, K. J., DOHERTY, P., EMMETT, C. J., DAMSKY, C. H., WALSH, F. S., and REICHARDT, L. F. (1993). Expression of β1 integrins in sensory neurons of the dorsal root ganglion and their functions in neurite outgrowth on two laminin isoforms. J. Neurosci. 13:4880-4888.
61. TOWBIN, H., STAEHELIN, T., and GORDON, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
62. TURNER, C. E. (1991). Paxillin is a major phosphotyrosine-containing protein during embryonic development. J. Cell Biol. 115:201-207.
63. TURNER, C. E. (1994). Paxillin: a cytoskeletal target for tyrosine kinases. Bioessays 16:47-52.
64. TURNER, C. E., GLENNEY, J. R., and BURRIDGE, K. (1990). Paxillin: a new vinculin-binding protein in focal adhesions. J. Cell Biol. 111:1059-1068.
65. WILLIAMS, E. J., WALSH, F. S., and DOHERTY, P. (1994). Tyrosine kinase inhibitors can differentially inhibit integrin dependent and CAM-stimulated neurite outgrowth. J. Cell Biol. 124:1029-1038.
66. WU, D.-Y. and GOLDBERG, D. J. (1993). Regulated tyrosine phosphorylation at the tips of growth cone filopodia. J. Cell Biol. 123:653-644.
67. WU, D.-Y., WANG, L.-C., GOLDBERG, D. J., and MASON, C. A. (1994). Tyrosine phosphorylation at filopodial tips of vertebrate growth cones. Soc. Neurosci. Abstr. 20:1081.
68. ZHENG, J., BUXBAUM, R. E., and HEIDEMANN, S. R. (1994). Measurements of growth cone adhesion to culture surfaces by micromanipulation. J. Cell Biol. 127:2049-2060.