Transmission of growth cone traction force through apcam-cytoskeletal linkages is regulated by src family tyrosine kinase activity

Journal of Cell Biology

Volumn 155, Issue 3, 2001, Pages 427-438

  Suter, Daniel M ^a   Forscher, Paul ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

ApCAM; Growth cone steering; Receptor cytoskeletal coupling; Src family tyrosine kinase; Tyrosine phosphorylation

Indexed keywords

EID: 0035851919     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.200107063     Document Type: Article

References (62)

1. Akiyama, T., J. Ishida, S. Nakagawa, H. Ogawara, S. Watanabe, N. Itoh, M. Shibuya, and Y. Fukami. 1987. Genistein, a specific inhibitor of tyrosine specific protein kinases. J. Biol. Chem. 262:5592-5595.
2. Atashi, J.R., S.G. Klinz, CA. Ingraham, W.T. Matten, M. Schachner, and P.F. Maness. 1992. Neural cell adhesion molecules modulate tyrosine phosphorylation of tubulin in nerve growth cone membranes. Neuron. 8:831-842.
3. Beggs, H.E., P. Soriano, and P.F. Maness. 1994. NCAM-dependent neurite outgrowth is inhibited in neurons from Fyn-minus mice. J. Cell Biol. 127:825-833.
4. Beggs, H.E., S.C. Baragona, J.J. Hemperly, and P.F. Maness. 1997. NCAM140 interacts with the focal adhesion kinase p125(fak) and the SRC-related tyrosine kinase p59(fyn). J. Biol. Chem. 272:8310-8319.
5. Bray, D. 1984. Axonal growth in response to experimentally applied mechanical tension. Dev. Biol. 102:379-389.
6. Burden-Gulley, S.M., and V. Lemmon. 1996. L1, N-cadherin, and laminin induce distinct distribution patterns of cytoskeletal elements in growth cones. Cell Motil. Cytoskeleton. 35:1-23.
7. Burridge, K., and M. Chrzanowska-Wodnicka. 1996. Focal adhesions, contractility, and signaling. Annu. Rev. Cell. Dev. Biol. 12:463-518.
8. Cavallaro, U., J. Niedermeyer, M. Fuxa, and G. Christofori. 2001. N-CAM modulates tumour-cell adhesion to matrix by inducing FGF-receptor signalling. Nat. Cell Biol. 3:650-657.
9. Choquet, D., D.P. Felsenfeld, and M.P. Sheetz. 1997. Extracellular matrix rigidity causes strengthening of integrincytoskeleton linkages. Cell. 88:39-48.
10. Chrzanowska-Wodnicka, M., and K. Burridge. 1996. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133: 1403-1415.
11. Desai, C.J., Q. Sun, and K. Zinn. 1997. Tyrosine phosphorylation and axon guidance: of mice and flies. Curr. Opin. Neurobiol. 7:70-74.
12. Doherty, P., and F.S. Walsh. 1996. CAM-FGF receptor interactions: a model for axonal growth. Mol. Cell. Neurosci. 8:99-111.
13. Faivre-Sarrailh, C., J. Falk, E. Pollerberg, M. Schachner, and G. Rougon. 1999. NrCAM, cerebellar granule cell receptor for the neuronal adhesion molecule F3, displays an actin-dependent mobility in growth cones. J. Cell Sci. 112: 3015-3027.
14. Felsenfeld, D.P., P.L. Schwartzberg, A. Venegas, R. Tse, and M.P. Sheetz. 1999. Selective regulation of integrin-cytoskeleton interactions by the tyrosine kinase Src. Nat. Cell Biol. 1:200-206.
15. Forscher, P., and S.J. Smith. 1988. Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J. Cell Biol. 107:1505-1516.
16. Forscher, P., C.H. Lin, and C. Thompson. 1992. Novel form of growth cone motility involving site-directed actin filament assembly. Nature. 357:515-518.
17. Glogauer, M., P. Arora, G. Yao, I. Sokholov, J. Ferrier, and C.A. McCulloch. 1997. Calcium ions and tyrosine phosphorylation interact coordinately with actin to regulate cytoprotective responses to stretching. J. Cell Sci. 110:11-21.
18. Goldberg, D.J., and D.Y. Wu. 1996. Tyrosine phosphorylation and protrusive structures of the growth cone. Perspect. Dev. Neurobiol. 4:183-192.
19. Goodman, C.S. 1996. Mechanisms and molecules that control growth cone guidance. Annu. Rev. Neurosci. 19:341-377.
20. Hanke, J.H., J.P. Gardner, R.L. Dow, P.S. Changelian, W.H. Brissette, E.J. Weringer, B.A. Pollok, and PA. Connelly. 1996. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and Fyn T-dependent T cell activation. J. Biol. Chem. 271:695-701.
21. Helmke, S., and K.H. Pfenninger. 1995. Growth cone enrichment and cytoskeletal association of non-receptor tyrosine kinases. Cell. Motil. Cytoskeleton. 30: 194-207.
22. Ignelzi, M.A., Jr., D.R. Miller, P. Soriano, and P.F. Maness. 1994. Impaired neurite outgrowth of src-minus cerebellar neurons on the cell adhesion molecule L1. Neuron. 12:873-884.
23. Katz, B.Z., E. Zamir, A. Bershadsky, Z. Kam, K.M. Yamada, and B. Geiger. 2000. Physical state of the extracellular matrix regulates the structure and molecular composition of cell-matrix adhesions. Mol. Biol. Cell. 11:1047-1060.
24. Keller, F., and S. Schacher. 1990. Neuron-specific membrane glycoproteins promoting neurite fasciculation in Aplysia californica. J. Cell Biol. 111:2637-2650.
25. Kunz, S., U. Ziegler, B. Kunz, and P. Sonderegger. 1996. Intracellular signaling is changed after clustering of the neural cell adhesion molecules axonin-1 and NgCAM during neurite fasciculation. J. Cell Biol. 135:253-267.
26. Lamoureux, P., R.E. Buxbaum, and S.R. Heidemann. 1989. Direct evidence that growth cones pull. Nature. 340:159-162.
27. Lin, C.H., and P. Forscher. 1993. Cytoskeletal remodeling during growth cone target interactions. J. Cell Biol. 121:1369-1383.
28. Lin, C.H., C.A. Thompson, and P. Forscher. 1994. Cytoskeletal reorganization underlying growth cone motility. Curr. Opin. Neurobiol. 4:640-647.
29. Lin, C.H., and P. Forscher. 1995. Growth cone advance is inversely proportional to retrograde F-actin flow. Neuron. 14:763-771.
30. Lin, C.H., E.M. Espreafico, M.S. Mooseker, and P. Forscher. 1996. Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron. 16:769-782.
31. Mallavarapu, A., and T. Mitchison. 1999. Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction. J. Cell Biol. 146: 1097-1106.
32. Maness, P.F., M. Aubry, C.G. Shores, L. Frame, and K.H. Pfenninger. 1988. c-src gene product in developing rat brain is enriched in nerve growth cone membranes. Proc. Natl. Acad. Sci. USA. 85:5001-5005.
33. Maness, P.F., H.E. Beggs, S.G. Klinz, and W.R. Morse. 1996. Selective neural cell adhesion molecule signaling by Src family tyrosine kinases and tyrosine phosphatases. Perspect. Dev. Neurobiol. 4:169-181.
34. Matten, W.T., M. Aubry, J. West, and P.F. Maness. 1990. Tubulin is phosphorylated at tyrosine by pp60c-src in nerve growth cone membranes. J. Cell Biol. 111:1959-1970.
35. Mayford, M., A. Barzilai, F. Keller, S. Schacher, and E.R. Kandel. 1992. Modulation of an NCAM-related adhesion molecule with long-term synaptic plasticity in Aplysia. Science. 256:638-644.
36. Menon, K.P., and K. Zinn. 1998. Tyrosine kinase inhibition produces specific alterations in axon guidance in the grasshopper embryo. Development. 125: 4121-4131.
37. Mitchison, T., and M. Kirschner. 1988. Cytoskeletal dynamics and nerve growth. Neuron. 1:761-772.
38. Mohamed, A.S., K.A. Rivas-Plata, J.R. Kraas, S.M. Saleh, and S.L. Swope. 2001. Src-class kinases act within the agrin/MuSK pathway to regulate acetylcholine receptor phosphorylation, cytoskeletal anchoring, and clustering. J. Neurosci. 21:3806-3818.
39. Morse, W.R., J.G. Whitesides, A.S. LaMantia, and P.F. Maness. 1998. p59fyn and pp60c-src modulate axonal guidance in the developing mouse olfactory pathway. J. Neurobiol. 36:53-63.
40. Orioli, D., M. Henkemeyer, G. Lemke, R. Klein, and T. Pawson. 1996. Sek4 and Nuk receptors cooperate in guidance of commissural axons and in palate formation. EMBO J. 15:6035-6049.
41. Pelham, R.J., Jr., and Y. Wang. 1997. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. USA. 94:13661-13665.
42. Riveline, D., E. Zamir, N.Q. Balaban, U.S. Schwarz, T. Ishizaki, S. Narumiya, Z. Kam, B. Geiger, and A.D. Bershadsky. 2001. Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J. Cell Biol. 153:1175-1186.
43. Rochlin, M.W., M.E. Dailey, and P.C. Bridgman. 1999. Polymerizing microtubules activate site-directed F-actin assembly in nerve growth cones. Mol. Biol. Cell. 10:2309-2327.
44. Saffell, J.L., E.J. Williams, I.J. Mason, F.S. Walsh, and P. Doherty. 1997. Expression of a dominant negative FGF receptor inhibits axonal growth and FGF receptor phosphorylation stimulated by CAMs. Neuron. 18:231-242.
45. Sanna, P.P., F. Berton, M. Cammalleri, M.K. Tallent, G.R. Siggins, F.E. Bloom, and W. Francesconi. 2000. A role for Src kinase in spontaneous epileptiform activity in the CA3 region of the hippocampus. Proc. Natl. Acad. Sci. USA. 97:8653-8657.
46. Schaefer, A.W., H. Kamiguchi, E.V. Wong, C.M. Beach, G. Landreth, and V. Lemmon. 1999. Activation of the MAPK signal cascade by the neural cell adhesion molecule L1 requires L1 internalization. J. Biol. Chem. 274: 37965-37973.
47. Schmid, R.S., W.M. Pruitt, and P.F. Maness. 2000. A MAP kinase-signaling pathway mediates neurite outgrowth on L1 and requires Src-dependent endocytosis. J. Neurosci. 20:4177-4188.
48. Schmidt, C., H. Pommerenke, F. Durr, B. Nebe, and J. Rychly. 1998. Mechanical stressing of integrin receptors induces enhanced tyrosine phosphorylation of cytoskeletally anchored proteins. J. Biol. Chem. 273:5081-5085.
49. Schoenwaelder, S.M., and K. Burridge. 1999. Bidirectional signaling between the cytoskeleton and integrins. Curr. Opin. Cell Biol. 11:274-286.
50. Sicheri, F., and J. Kuriyan. 1997. Structures of Src-family tyrosine kinases. Curr. Opin. Struct. Biol. 7:777-785.
51. Suter, D.M., L.D. Errante, V. Belotserkovsky, and P. Forscher. 1998. The Ig superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substrate-cytoskeletal coupling. J. Cell Biol. 141:227-240.
52. Suter, D.M., and P. Forscher. 1998. An emerging link between cytoskeletal dynamics and cell adhesion molecules in growth cone guidance. Curr. Opin. Neurobiol. 8:106-116.
53. Tanaka, E., and J. Sabry. 1995. Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell. 83:171-176.
54. Tessier-Lavigne, M., and C.S. Goodman. 1996. The molecular biology of axon guidance. Science. 274:1123-1133.
55. Thomas, S.M., and J.S. Brugge. 1997. Cellular functions regulated by Src family kinases. Annu. Rev. Cell. Dev. Biol. 13:513-609.
56. Thompson, C., C.H. Lin, and P. Forscher. 1996. An Aplysia cell adhesion molecule associated with site-directed actin filament assembly in neuronal growth cones. J. Cell Sci. 109:2843-2854.
57. Walsh, F.S., and P. Doherty. 1997. Neural cell adhesion molecules of the immunoglobulin superfamily: role in axon growth and guidance. Annu. Rev. Cell. Dev. Biol. 13:425-456.
58. Wang, N., J.P. Butler, and D.E. Ingber. 1993. Mechanotransduction across the cell surface and through the cytoskeleton. Science. 260:1124-1127.
59. Williams, E.J., F.S. Walsh, and P. Doherty. 1994. Tyrosine kinase inhibitors can differentially inhibit integrin-dependent and CAM-stimulated neurite outgrowth. J. Cell Biol. 124:1029-1037.
60. Wills, Z., J. Bateman, C.A. Korey, A. Comer, and D. Van Vactor. 1999. The tyrosine kinase Abl and its substrate enabled collaborate with the receptor phosphatase Dlar to control motor axon guidance. Neuron. 22:301-312.
61. Worley, T., and C. Holt. 1996. Inhibition of protein tyrosine kinases impairs axon extension in the embryonic optic tract. J. Neurosci. 16:2294-2306.
62. Wu, D.Y., and D.J. Goldberg. 1993. Regulated tyrosine phosphorylation at the tips of growth cone filopodia. J. Cell Biol. 123:653-664.