Focal adhesion kinase promotes integrin adhesion dynamics necessary for chemotropic turning of nerve growth cones

Journal of Neuroscience

Volumn 31, Issue 38, 2011, Pages 13585-13595

  Myers, Jonathan P ^a   Gomez, Timothy M ^b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; FOCAL ADHESION KINASE; INTEGRIN; ISOENZYME; LAMININ; PAXILLIN; PHOSPHOTYROSINE; PROTEIN FRNK; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME SPECIFICITY; FILOPODIUM; GROWTH CONE; GROWTH REGULATION; LAMELLIPODIUM; MOLECULAR DYNAMICS; NERVE GROWTH; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; CHEMOTAXIS; EMBRYO, NONMAMMALIAN; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; GENE KNOCKDOWN TECHNIQUES; GROWTH CONES; MUTATION; OLIGONUCLEOTIDES, ANTISENSE; PAXILLIN; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTEIN-TYROSINE KINASES; PSEUDOPODIA; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; XENOPUS LAEVIS;

EID: 80053070162     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2381-11.2011     Document Type: Article

References (52)

1. Bechara A, Nawabi H, Moret F, Yaron A, Weaver E, Bozon M, Abouzid K, Guan JL, Tessier-Lavigne M, Lemmon V, Castellani V (2008) FAKMAPK- dependent adhesion disassembly downstream of L1 contributes to semaphorin3A-induced collapse. EMBO J 27:1549-1562.
2. Bouton AH, Riggins RB, Bruce-Staskal PJ (2001) Functions of the adapter protein Cas: signal convergence and the determination of cellular responses. Oncogene 20:6448-6458.
3. Brunton VG, Avizienyte E, Fincham VJ, Serrels B, Metcalf CA 3rd, Sawyer TK, Frame MC (2005) Identification of Src-specific phosphorylation site on focal adhesion kinase: dissection of the role of Src SH2 and catalytic functions and their consequences for tumor cell behavior. Cancer Res 65:1335-1342.
4. Cary LA, Chang JF, Guan JL (1996) Stimulation of cell migration by overexpression of focal adhesion kinase and its association with Src and Fyn. J Cell Sci 109:1787-1794.
5. Cho SY, Klemke RL (2002) Purification of pseudopodia from polarized cells reveals redistribution and activation of Rac through assembly of a CAS/ Crk scaffold. J Cell Biol 156:725-736.
6. Dent EW, Meiri KF (1992) GAP-43 phosphorylation is dynamically regulated in individual growth cones. J Neurobiol 23:1037-1053.
7. Dickson BJ (2001) Rho GTPases in growth cone guidance. Curr Opin Neurobiol 11:103-110.
8. Endo M, Yamashita T (2009) Inactivation of Ras by p120GAP via focal ad- hesion kinase dephosphorylation mediates RGMa-induced growth cone collapse. J Neurosci 29:6649-6662.
9. Etienne-Manneville S, Hall A (2002) Rho GTPases in cell biology. Nature 420:629-635.
10. Gehler S, Gallo G, Veien E, Letourneau PC (2004) p75 neurotrophin receptor signaling regulates growth cone filopodial dynamics through modulating RhoA activity. J Neurosci 24:4363-4372.
11. Goh EL, Young JK, Kuwako K, Tessier-Lavigne M, He Z, Griffin JW, Ming GL (2008) Beta1-integrin mediates myelin-associated glycoprotein signaling in neuronal growth cones. Mol Brain 1:10.
12. Gomez TM, Roche FK, Letourneau PC (1996) Chick sensory neuronal growth cones distinguish fibronectin from laminin by making substratum contacts that resemble focal contacts. J Neurobiol 29:18-34.
13. Gomez TM, Harrigan D, Henley J, Robles E (2003) Working with Xenopus spinal neurons in live cell culture. Methods Cell Biol 71:129-156.
14. Hamadi A, Bouali M, Dontenwill M, Stoeckel H, Takeda K, Rondé P (2005) Regulation of focal adhesion dynamics and disassembly by phosphorylation of FAK at tyrosine 397. J Cell Sci 118:4415-4425.
15. Hines JH, Abu-Rub M, Henley JR (2010) Asymmetric endocytosis and remodeling of beta1-integrin adhesions during growth cone chemorepulsion by MAG. Nat Neurosci 13:829-837.
16. Huber AB, Kolodkin AL, Ginty DD, Cloutier JF (2003) Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu Rev Neurosci 26:509-563.
17. Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110:673-687.
18. Ilić D, Furuta Y, Kanazawa S, Takeda N, Sobue K, Nakatsuji N, Nomura S, Fujimoto J, Okada M, Yamamoto T (1995) Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377:539-544.
19. Kirchner J, Kam Z, Tzur G, Bershadsky AD, Geiger B (2003) Live-cell monitoring of tyrosine phosphorylation in focal adhesions following microtubule disruption. J Cell Sci 116:975-986.
20. Letourneau PC, Condic ML, Snow DM (1994) Interactions of developing neurons with the extracellular matrix. J Neurosci 14:915-928.
21. Li W, Lee J, Vikis HG, Lee SH, Liu G, Aurandt J, Shen TL, Fearon ER, Guan JL, Han M, Rao Y, Hong K, Guan KL (2004) Activation of FAK and Src are receptor-proximal events required for netrin signaling. Nat Neurosci 7:1213-1221.
22. Lim Y, Han I, Jeon J, Park H, Bahk YY, Oh ES (2004) Phosphorylation of focal adhesion kinase at tyrosine 861 is crucial for Ras transformation of fibroblasts. J Biol Chem 279:29060-29065.
23. Lim Y, Lim ST, Tomar A, Gardel M, Bernard-Trifilo JA, Chen XL, Uryu SA, Canete-Soler R, Zhai J, Lin H, Schlaepfer WW, Nalbant P, Bokoch G, Ilic D, Waterman-Storer C, Schlaepfer DD (2008) PyK2 and FAK connections to p190Rho guanine nucleotide exchange factor regulate RhoA activity, focal adhesion formation, and cell motility. J Cell Biol 180:187-203.
24. Liu G, Beggs H, Jürgensen C, Park HT, Tang H, Gorski J, Jones KR, Reichardt LF, Wu J, Rao Y (2004) Netrin requires focal adhesion kinase and Src family kinases for axon outgrowth and attraction. Nat Neurosci 7:1222-1232.
25. Liu G, Li W, Gao X, Li X, Jürgensen C, Park HT, Shin NY, Yu J, He ML, Hanks SK, Wu JY, Guan KL, Rao Y (2007) p130CAS is required for netrin signaling and commissural axon guidance. J Neurosci 27:957-968.
26. Lowery LA, Van Vactor D (2009) The trip of the tip: understanding the growth cone machinery. Nat Rev Mol Cell Biol 10:332-343.
27. Ming G, Lohof AM, Zheng JQ (1997a) Acute morphogenic and chemotropic effects of neurotrophins on cultured embryonic Xenopus spinal neurons. J Neurosci 17:7860-7871.
28. Ming GL, Song HJ, Berninger B, Holt CE, Tessier-Lavigne M, Poo MM (1997b) cAMP-dependent growth cone guidance by netrin-1. Neuron 19:1225-1235.
29. Mitra SK, Hanson DA, Schlaepfer DD (2005) Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 6:56-68.
30. Nieuwkoop PD, Faber J (1994) Normal table of Xenopus laevis (Daudin). New York: Garland.
31. Okada M, Nakagawa H (1989) A protein tyrosine kinase involved in regulation of pp60c-src function. J Biol Chem 264:20886-20893.
32. Parri M, Buricchi F, Giannoni E, Grimaldi G, Mello T, Raugei G, Ramponi G, Chiarugi P (2007) EphrinA1 activates a Src/focal adhesion kinasemediated motility response leading to rho-dependent actino/myosin contractility. J Biol Chem 282:19619-19628.
33. Renaudin A, Lehmann M, Girault J, McKerracher L (1999) Organization of point contacts in neuronal growth cones. J Neurosci Res 55:458-471.
34. Ren XR, Ming GL, Xie Y, Hong Y, Sun DM, Zhao ZQ, Feng Z, Wang Q, Shim S, Chen ZF, Song HJ, Mei L, Xiong WC (2004) Focal adhesion kinase in netrin-1 signaling. Nat Neurosci 7:1204-1212.
35. Robles E, Gomez TM (2006) Focal adhesion kinase signaling at sites of integrin-mediated adhesion controls axon pathfinding. Nat Neurosci 9:1274-1283.
36. Robles E, Woo S, Gomez TM (2005) Src-dependent tyrosine phosphorylation at the tips of growth cone filopodia promotes extension. J Neurosci 25:7669-7681.
37. Santiago-Medina M, Myers JP, Gomez TM (2011) Imaging adhesion and signaling dynamics in Xenopus laevis growth cones. Dev Neurobiol. Advance online publication. doi:10.1002/dneu.20886.
38. Schaller MD (2010) Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions. J Cell Sci 123:1007-1013.
39. Schaller MD, Borgman CA, Parsons JT (1993) Autonomous expression of a noncatalytic domain of the focal adhesion-associated protein tyrosine kinase pp125FAK. Mol Cell Biol 13:785-791.
40. Schaller MD, Hildebrand JD, Shannon JD, Fox JW, Vines RR, Parsons JT (1994) Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src. Mol Cell Biol 14:1680-1688.
41. Scheswohl DM, Harrell JR, Rajfur Z, Gao G, Campbell SL, Schaller MD (2008) Multiple paxillin binding sites regulate FAK function. J Mol Signal 3:1.
42. Shi Y, Pontrello CG, DeFea KA, Reichardt LF, Ethell IM (2009) Focal adhesion kinase acts downstream of EphB receptors to maintain mature dendritic spines by regulating cofilin activity. J Neurosci 29:8129-8142.
43. Tan CL, Kwok JC, Patani R, Ffrench-Constant C, Chandran S, Fawcett JW (2011) Integrin activation promotes axon growth on inhibitory chondroitin sulfate proteoglycans by enhancing integrin signaling. J Neurosci 31:6289-6295.
44. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123-1133.
45. Thomas SM, Brugge JS (1997) Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 13:513-609.
46. Tomar A, Schlaepfer DD (2009) Focal adhesion kinase: switching between GAPs and GEFs in the regulation of cell motility. Curr Opin Cell Biol 21:676-683.
47. Tomar A, Lim ST, Lim Y, Schlaepfer DD (2009) A FAK-p120RasGAPp190RhoGAP complex regulates polarity in migrating cells. J Cell Sci 122:1852-1862.
48. Turner CE (2000) Paxillin and focal adhesion signalling. Nat Cell Biol 2:E231-E236.
49. Woo S, Gomez TM (2006) Rac1 and RhoA promote neurite outgrowth through formation and stabilization of growth cone point contacts. J Neurosci 26:1418-1428.
50. Woo S, Rowan DJ, Gomez TM (2009) Retinotopic mapping requires focal adhesion kinase-mediated regulation of growth cone adhesion. J Neurosci 29:13981-13991.
51. Yaron A, Zheng B (2007) Navigating their way to the clinic: emerging roles for axon guidance molecules in neurological disorders and injury. Dev Neurobiol 67:1216-1231.
52. Yu TW, Bargmann CI (2001) Dynamic regulation of axon guidance. Nat Neurosci 4 [Suppl]:1169-1176.