Filopodial calcium transients regulate growth cone motility and guidance through local activation of calpain

Neuron

Volumn 38, Issue 4, 2003, Pages 597-609

  Robles, Estuardo ^a   Huttenlocher, Anna ^a   Gomez, Timothy M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALPAIN; PHOSPHOTYROSINE;

ADHESION; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL MOTILITY; ENZYME ACTIVATION; ENZYME ACTIVITY; FILOPODIUM; GROWTH CONE; LAMELLIPODIUM; NERVE FIBER GROWTH; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

EID: 0038689057     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(03)00260-5     Document Type: Article

References (65)

1. Al-Mohanna F.A., Bolsover S., Archer F.R. CAMs and FGF cause a local submembrane calcium signal promoting axon outgrowth without a rise in bulk calcium concentration. Brain Res. Dev. Brain Res. 92:1996;101-110.
2. Alderton J.M., Steinhardt R.A. Calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. J. Biol. Chem. 275:2000;9452-9460.
3. Bailly M., Ichetovkin I., Grant W., Zebda N., Machesky L.M., Segall J.E., Condeelis J. The F-actin side binding activity of the Arp2/3 complex is essential for actin nucleation and lamellipod extension. Curr. Biol. 11:2001;620-625.
4. Bandtlow C.E., Schmidt M.F., Hassinger T.D., Schwab M.E., Kater S.B. Role of intracellular calcium in NI-35-evoked collapse of neuronal growth cones. Science. 259:1993;80-83.
5. Behar O., Mizuno K., Badminton M., Woolf C.J. Semaphorin 3A growth cone collapse requires a sequence homologous to tarantula hanatoxin. Proc. Natl. Acad. Sci. USA. 96:1999;13501-13505.
6. Bentley D. Disoriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment. Dev. Biol. 119:1987;454-465.
7. 2+ influx and neurite growth in response to purified N-cadherin and laminin. J. Cell Biol. 127:1994;1461-1475.
8. Bray D., Chapman K. Analysis of microspike movements on the neuronal growth cone. J. Neurosci. 5:1985;3204-3213.
9. Campbell D.S., Holt C.E. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron. 32:2001;1013-1026.
10. Cheng S., Geddis M.S., Rehder V. Local calcium changes regulate the length of growth cone filopodia. J. Neurobiol. 50:2002;263-275.
11. Chien C.B., Rosenthal D.E., Harris W.A., Holt C.E. Navigational errors made by growth cones without filopodia in the embryonic Xenopus brain. Neuron. 11:1993;237-251.
12. Cooray P., Yuan Y., Schoenwaelder S.M., Mitchell C.A., Salem H.H., Jackson S.P. Focal adhesion kinase (pp125FAK) cleavage and regulation by calpain. Biochem. J. 318:1996;41-47.
13. Davenport R.W., Dou P., Rehder V., Kater S.B. A sensory role for neuronal growth cone filopodia. Nature. 361:1993;721-724.
14. DeMali K.A., Barlow C.A., Burridge K. Recruitment of the Arp2/3 complex to vinculin. coupling membrane protrusion to matrix adhesion J. Cell Biol. 159:2002;881-891.
15. Fan J., Raper J.A. Localized collapsing cues can steer growth cones without inducing their full collapse. Neuron. 14:1995;263-274.
16. Frangioni J.V., Oda A., Smith M., Salzman E.W., Neel B.G. Calpain-catalyzed cleavage and subcellular relocation of protein phosphotyrosine phosphatase 1B (PTP-1B) in human platelets. EMBO J. 12:1993;4843-4856.
17. Galbraith C.G., Yamada K.M., Sheetz M.P. The relationship between force and focal complex development. J. Cell Biol. 159:2002;695-705.
18. Geiger B., Bershadsky A. Assembly and mechanosensory function of focal contacts. Curr. Opin. Cell Biol. 13:2001;584-592.
19. Gitler D., Spira M.E. Real time imaging of calcium-induced localized proteolytic activity after axotomy and its relation to growth cone formation. Neuron. 20:1998;1123-1135.
20. Glading A., Lauffenburger D.A., Wells A. Cutting to the chase. calpain proteases in cell motility Trends Cell Biol. 12:2002;46-54.
21. Gomez T.M., Spitzer N.C. In vivo regulation of axon extension and pathfinding by growth-cone calcium transients. Nature. 397:1999;350-355.
22. Gomez T.M., Spitzer N.C. Regulation of growth cone behavior by calcium. new dynamics to earlier perspectives J. Neurobiol. 44:2000;174-183.
23. Gomez T.M., Snow D.M., Letourneau P.C. Characterization of spontaneous calcium transients in nerve growth cones and their effect on growth cone migration. Neuron. 14:1995;1233-1246.
24. Gomez T.M., Roche F.K., Letourneau P.C. Chick sensory neuronal growth cones distinguish fibronectin from laminin by making substratum contacts that resemble focal contacts. J. Neurobiol. 29:1996;18-34.
25. Gomez T.M., Robles E., Poo M., Spitzer N.C. Filopodial calcium transients promote substrate-dependent growth cone turning. Science. 291:2001;1983-1987.
26. Gomez T.M., Harrigan D., Henley J., Robles E. Working with Xenopus spinal neurons in live cell culture. Methods Cell Biol. in press:2003.
27. Gu X., Olson E.C., Spitzer N.C. Spontaneous neuronal calcium spikes and waves during early differentiation. J. Neurosci. 14:1994;6325-6335.
28. Hong K., Nishiyama M., Henley J., Tessier-Lavigne M., Poo M. Calcium signalling in the guidance of nerve growth by netrin-1. Nature. 403:2000;93-98.
29. Huttenlocher A., Palecek S.P., Lu Q., Zhang W., Mellgren R.L., Lauffenburger D.A., Ginsberg M.H., Horwitz A.F. Regulation of cell migration by the calcium-dependent protease calpain. J. Biol. Chem. 272:1997;32719-32722.
30. Ilic D., Furuta Y., Kanazawa S., Takeda N., Sobue K., Nakatsuji N., Nomura S., Fujimoto J., Okada M., Yamamoto T. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature. 377:1995;539-544.
31. Janmey P.A. Phosphoinositides and calcium as regulators of cellular actin assembly and disassembly. Annu. Rev. Physiol. 56:1994;169-191.
32. Jay D.G. The clutch hypothesis revisited. ascribing the roles of actin-associated proteins in filopodial protrusion in the nerve growth cone J. Neurobiol. 44:2000;114-125.
33. Kater S.B., Rehder V. The sensory-motor role of growth cone filopodia. Curr. Opin. Neurobiol. 5:1995;68-74.
34. Kornberg L.J., Earp H.S., Turner C.E., Prockop C., Juliano R.L. Signal transduction by integrins. increased protein tyrosine phosphorylation caused by clustering of beta 1 integrins Proc. Natl. Acad. Sci. USA. 88:1991;8392-8396.
35. Krotoski D., Bronner-Fraser M. Distribution of integrins and their ligands in the trunk of Xenopus laevis during neural crest cell migration. J. Exp. Zool. 253:1991;139-150.
36. Kuhn T.B., Williams C.V., Dou P., Kater S.B. Laminin directs growth cone navigation via two temporally and functionally distinct calcium signals. J. Neurosci. 18:1998;184-194.
37. Lokuta M.A., Nuzzi P.A., Huttenlocher A. Calpain regulates neutrophil chemotaxis. Proc. Natl. Acad. Sci. USA. 100:2003;4006-4011.
38. Menon K.P., Zinn K. Tyrosine kinase inhibition produces specific alterations in axon guidance in the grasshopper embryo. Development. 125:1998;4121-4131.
39. Mitchison T., Kirschner M. Cytoskeletal dynamics and nerve growth. Neuron. 1:1988;761-772.
40. Oda A., Smith M., Salzman E.W., Neel B.G. pp60src is an endogenous substrate for calpain in human blood platelets. EMBO J. 12:1993;4843-4856.
41. Pain S., Monstero-Lastres A., Falet H., Brohard-Bohn B., Fraiz N., Bachelot-Loza C., Cano E., Rendu F. Calpain controls the balance between protein tyrosine kinase and tyrosine phosphatase activities during platelet activation. FEBS Lett. 453:1999;119-123.
42. Pellicena P., Miller W.T. Coupling kinase activation to substrate recognition in SRC-family tyrosine kinases. Front. Biosci. 7:2002;d256-d267.
43. Renaudin A., Lehmann M., Girault J., McKerracher L. Organization of point contacts in neuronal growth cones. J. Neurosci. Res. 55:1999;458-471.
44. Sato K., Kawashima S. Calpain function in the modulation of signal transduction molecules. Biol. Chem. 382:2001;743-751.
45. Shea T.B., Cressman C.M., Spencer M.J., Beermann M.L., Nixon R.A. Enhancement of neurite outgrowth following calpain inhibition is mediated by protein kinase C. J. Neurochem. 65:1995;517-527.
46. Snow D.M., Atkinson P.B., Hassinger T.D., Letourneau P.C., Kater S.B. Chondroitin sulfate proteoglycan elevates cytoplasmic calcium in DRG neurons. Dev. Biol. 166:1994;87-100.
47. Somasekhar T., Nordlander R.H. Differential distributions of HNK-1 and tenascin immunoreactivity during innervation of myotomal muscle in Xenopus. Brain Res. Dev. Brain Res. 88:1995;53-67.
48. Song D.K., Malmstrom T., Kater S.B., Mykles D.L. Calpain inhibitors block Ca(2+)-induced suppression of neurite outgrowth in isolated hippocampal pyramidal neurons. J. Neurosci. Res. 39:1994;474-481.
49. Spitzer N.C., Lautermilch N.J., Smith R.D., Gomez T.M., Rohrbough J. Coding of neuronal differentiation by calcium transients. Bioessays. 22:2000;811-817.
50. Steketee M.B., Tosney K.W. Contact with isolated sclerotome cells steers sensory growth cones by altering distinct elements of extension. J. Neurosci. 19:1999;3495-3506.
51. Streit M., Kaiser R., Herzberg F., Schirner M., Schramm K., Kaufmann C., Henneken M., Schafer-Korting M., Thiel E., Kreuser E.D.et al. Mechanical stressing of integrin receptors induces enhanced tyrosine phosphorylation of cytoskeletally anchored proteins. Int. J. Cancer. 76:1998;91-98.
52. Suter D.M., Forscher P. Transmission of growth cone traction force through apCAM-cytoskeletal linkages is regulated by Src family tyrosine kinase activity. J. Cell Biol. 155:2001;327-330.
53. Tessier-Lavigne M., Goodman C.S. The molecular biology of axon guidance. Science. 274:1996;1123-1133.
54. Volberg T., Romer L., Zamir E., Geiger B. pp60(c-src) and related tyrosine kinases. a role in the assembly and reorganization of matrix adhesions J. Cell Sci. 114:2001;2279-2289.
55. Wang Q., Zheng J.Q. cAMP-mediated regulation of neurotrophin-induced collapse of nerve growth cones. J. Neurosci. 18:1998;4973-4984.
56. Welch M.D., DePace A.H., Verma S., Iwamatsu A., Mitchison T.J. The human Arp2/3 complex is composed of evolutionarily conserved subunits and is localized to cellular regions of dynamic actin filament assembly. J. Cell Biol. 138:1997;375-384.
57. Worley T., Holt C. Inhibition of protein tyrosine kinases impairs axon extension in the embryonic optic tract. J. Neurosci. 16:1996;2294-2306.
58. Wu D.Y., Goldberg D.J. Regulated tyrosine phosphorylation at the tips of growth cone filopodia. J. Cell Biol. 123:1993;653-664.
59. Wu D.Y., Wang L.C., Mason C.A., Goldberg D.J. Association of beta 1 integrin with phosphotyrosine in growth cone filopodia. J. Neurosci. 16:1996;1470-1478.
60. Zamir E., Bershadsky A., Kam Z., Yamada K.M., Geiger B. Molecular diversity of cell-matrix adhesions. Mol. Biol. Cell. 11:2000;1047-1060.
61. Zheng J.Q. Turning of nerve growth cones induced by localized increases in intracellular calcium ions. Nature. 403:2000;89-93.
62. Zheng J.Q., Felder M., Connor J.A., Poo M. Turning of nerve growth cones induced by neurotransmitters. Nature. 368:1994;140-144.
63. Zheng J.Q., Wan J.J., Poo M. Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J. Neurosci. 16:1996;1140-1149.
64. Zhou F.Q., Cohan C.S. Growth cone collapse through coincident loss of actin bundles and leading edge actin without actin depolymerization. J. Cell Biol. 153:2001;1071-1084.
65. Zucker R.S., Regehr W.G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64:2002;355-405.