Netrin-1 Attracts axons through FAK-dependent mechanotransduction

Journal of Neuroscience

Volumn 32, Issue 34, 2012, Pages 11574-11585

  Moore Dr , Simon W ^a   Zhang, Xian ^a   Lynch, Christopher D ^a   Sheetz, Michael P ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRK ASSOCIATED SUBSTRATE PROTEIN; FOCAL ADHESION KINASE; MYOSIN II; NETRIN 1;

ADHESION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GROWTH CONE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; MALE; MECHANOTRANSDUCTION; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

ACTINS; ANIMALS; AXONS; CELL LINE, TRANSFORMED; CRK-ASSOCIATED SUBSTRATE PROTEIN; ELECTROPORATION; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GROWTH CONES; HEPARIN; HUMANS; LUMINESCENT PROTEINS; MALE; MECHANOTRANSDUCTION, CELLULAR; MICE; MYOSIN TYPE II; NERVE GROWTH FACTORS; NEURONS; ORGAN CULTURE TECHNIQUES; PHOSPHOPROTEINS; PHYSICAL STIMULATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; QUINOLONES; SPINAL CORD; SULFONES; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS; TYROSINE;

EID: 84865228361     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0999-12.2012     Document Type: Article

References (84)

1. Bashaw GJ, Klein R (2010) Signaling from axon guidance receptors. Cold Spring Harb Perspect Biol 2:a001941.
2. Brankatschk M, Dickson BJ (2006) Netrins guide Drosophila commissural axons at short range. Nat Neurosci 9:188-194.
3. Brown J, Bridgman PC (2003) Role of myosin II in axon outgrowth. J Histochem Cytochem 51:421-428.
4. Cai X, Lietha D, Ceccarelli DF, Karginov AV, Rajfur Z, Jacobson K, Hahn KM, Eck MJ, Schaller MD (2008) Spatial and temporal regulation of focal adhesion kinase activity in living cells. Mol Cell Biol 28:201-214.
5. Calalb MB, Polte TR, Hanks SK (1995) Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol Cell Biol 15:954-963.
6. Carter N, Nakamoto T, Hirai H, Hunter T (2002) EphrinA1-induced cytoskeletal re-organization requires FAK and p130(cas). Nat Cell Biol 4:565-573.
7. Choquet D, Felsenfeld DP, Sheetz MP (1997) Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell 88:39-48.
8. Cooper LA, Shen TL, Guan JL (2003) Regulation of focal adhesion kinase by its amino-terminal domain through an autoinhibitory interaction. Mol Cell Biol 23:8030-8041.
9. Dai J, Sheetz MP (1998) Chapter 09: Cell membrane mechanics. Methods Cell Biol 55:157-171.
10. Davenport RW, Dou P, Rehder V, Kater SB (1993) A sensory role for neuronal growth cone filopodia. Nature 361:721-724.
11. Deiner MS, Kennedy TE, Fazeli A, Serafini T, Tessier-Lavigne M, Sretavan DW (1997) Netrin-1 and DCC mediate axon guidance locally at the optic disc: loss of function leads to optic nerve hypoplasia. Neuron 19:575-589.
12. de la Torre JR, Höpker VH, Ming GL, Poo MM, Tessier-Lavigne M, Hemmati-Brivanlou A, Holt CE (1997) Turning of retinal growth cones in a netrin-1 gradient mediated by the netrin receptor DCC. Neuron 19:1211-1224.
13. de Wit J, Verhaagen J (2007) Proteoglycans as modulators of axon guidance cue function. Adv Exp Med Biol 600:73-89.
14. De Wit J, De Winter F, Klooster J, Verhaagen J (2005) Semaphorin 3A displays a punctate distribution on the surface of neuronal cells and interacts with proteoglycans in the extracellular matrix. Mol Cell Neurosci 29:40-55.
15. Dumbauld DW, Shin H, Gallant ND, Michael KE, Radhakrishna H, García AJ (2010) Contractility modulates cell adhesion strengthening through focal adhesion kinase and assembly of vinculin-containing focal adhesions. J Cell Physiol 223:746-756.
16. Falk J, Julien F, Bechara A, Fiore R, Nawabi H, Zhou H, Hoyo-Becerra C, Bozon M, Rougon G, Grumet M, Püschel AW, Sanes JR, Castellani V (2005) Dual functional activity of semaphorin 3B is required for positioning the anterior commissure. Neuron 48:63-75.
17. Fazeli A, Dickinson SL, Hermiston ML, Tighe RV, Steen RG, Small CG, Stoeckli ET, Keino-Masu K, Masu M, Rayburn H, Simons J, Bronson RT, Gordon JI, Tessier-Lavigne M, Weinberg RA (1997) Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 386:796-804.
18. Geisbrecht BV, Dowd KA, Barfield RW, Longo PA, Leahy DJ (2003) Netrin binds discrete subdomains of DCC and UNC5 and mediates interactions between DCC and heparin. J Biol Chem 278:32561-32568.
19. Harte MT, Hildebrand JD, Burnham MR, Bouton AH, Parsons JT (1996) p130Cas, a substrate associated with v-Src and v-Crk, localizes to focal adhesions and binds to focal adhesion kinase. J Biol Chem 271:13649-13655.
20. Hedgecock EM, Culotti JG, Hall DH (1990) The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4:61-85.
21. Hoffman BD, Grashoff C, Schwartz MA (2011) Dynamic molecular processes mediate cellular mechanotransduction. Nature 475:316-323.
22. Honda H, Nakamoto T, Sakai R, Hirai H (1999) p130(Cas), an assembling molecule of actin filaments, promotes cell movement, cell migration, and cell spreading in fibroblasts. Biochem Biophys Res Commun 262:25-30.
23. Hu H (2001) Cell-surface heparan sulfate is involved in the repulsive guidance activities of Slit2 protein. Nat Neurosci 4:695-701.
24. Huang J, Sakai R, Furuichi T (2006) The docking protein Cas links tyrosine phosphorylation signaling to elongation of cerebellar granule cell axons. Mol Biol Cell 17:3187-3196.
25. 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.
26. 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.
27. Inatani M, Yamaguchi Y (2003) Gene expression of EXT1 and EXT2 during mouse brain development. Brain Res Dev Brain Res 141:129-136.
28. Kappler J, Franken S, Junghans U, Hoffmann R, Linke T, Müller HW, Koch KW (2000) Glycosaminoglycan-binding properties and secondary structure of the C-terminus of netrin-1. Biochem Biophys Res Commun 271:287-291.
29. Keino-Masu K, Masu M, Hinck L, Leonardo ED, Chan SS, Culotti JG, Tessier- Lavigne M (1996) Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell 87:175-185.
30. Kennedy TE, Serafini T, de la Torre JR, Tessier-Lavigne M (1994) Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78:425-435.
31. Kennedy TE, Wang H, Marshall W, Tessier-Lavigne M (2006) Axon guidance by diffusible chemoattractants: a gradient of netrin protein in the developing spinal cord. J Neurosci 26:8866-8874.
32. Koshida R, Rocic P, Saito S, Kiyooka T, Zhang C, Chilian WM (2005) Role of focal adhesion kinase in flow-induced dilation of coronary arterioles. Arterioscler Thromb Vasc Biol 25:2548-2553.
33. Kovács M, Tóth J, Hetényi C, Málnási-Csizmadia A, Sellers JR (2004) Mechanism of blebbistatin inhibition of myosin II. J Biol Chem 279:35557-35563.
34. Lai Wing Sun K, Correia JP, Kennedy TE (2011) Netrins: versatile extracellular cues with diverse functions. Development 138:2153-2169.
35. Lamoureux P, Buxbaum RE, Heidemann SR (1989) Direct evidence that growth cones pull. Nature 340:159-162.
36. Leonardo ED, Hinck L, Masu M, Keino-Masu K, Ackerman SL, Tessier-Lavigne M (1997) Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 386:833-838.
37. Liang W, Han Q, Jin W, Xiao Z, Huang J, Ni H, Chen B, Kong J, Wu J, Dai J (2010) The promotion of neurological recovery in the rat spinal cord crushed injury model by collagen-binding BDNF. Biomaterials 31:8634-8641.
38. 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.
39. Lietha D, Cai X, Ceccarelli DFJ, Li Y, Schaller MD, Eck MJ (2007) Structural basis for the autoinhibition of focal adhesion kinase. Cell 129:1177-1187.
40. Lin TH, Aplin AE, Shen Y, Chen Q, Schaller M, Romer L, Aukhil I, Juliano RL (1997) Integrin-mediated activation of MAP kinase is independent of FAK: evidence for dual integrin signaling pathways in fibroblasts. J Cell Biol 136:1385-1395.
41. 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.
42. 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.
43. Ly A, Nikolaev A, Suresh G, Zheng Y, Tessier-Lavigne M, Stein E (2008) DSCAM is a netrin receptor that collaborates with DCC in mediating turning responses to netrin-1. Cell 133:1241-1254.
44. Mai J, Fok L, Gao H, Zhang X, Poo MM (2009) Axon initiation and growth cone turning on bound protein gradients. J Neurosci 29:7450-7458.
45. Manitt C, Kennedy TE (2002) Where the rubber meets the road: netrin expression and function in developing and adult nervous systems. Prog Brain Res 137:425-442.
46. Martino MM, Hubbell JA (2010) The 12th-14th type III repeats of fibronectin function as a highly promiscuous growth factor-binding domain. FASEB J 24:4711-4721.
47. Matsumoto Y, Irie F, Inatani M, Tessier-Lavigne M, Yamaguchi Y (2007) Netrin-1/DCC signaling in commissural axon guidance requires cellautonomous expression of heparan sulfate. J Neurosci 27:4342-4350.
48. McGee-Russell S, Allen R (1971) Reversible stabilization of labile microtubules in the reticulopodial network of allogromia. Adv Cell Mol Biol 1:153-184.
49. Michael KE, Dumbauld DW, Burns KL, Hanks SK, García AJ (2009) Focal adhesion kinase modulates cell adhesion strengthening via integrin activation. Mol Biol Cell 20:2508-2519.
50. Ming GL, Song HJ, Berninger B, Holt CE, Tessier-Lavigne M, Poo MM (1997) cAMP-dependent growth cone guidance by netrin-1. Neuron 19:1225-1235.
51. Mirzayan C (1997) Molecular mechanisms underlying the response of commissural axons to netrin-1 (UMI: 9818659) (Tessier-Lavigne M, ed). University of California, San Francisco.
52. Moore SW, Kennedy TE (2008) Dissection and culture of embryonic spinal commissural neurons. Curr Protoc Neurosci Chapter 3:Unit3.20.
53. Moore SW, Sheetz MP (2011) Biophysics of substrate interaction: influence on neural motility, differentiation, and repair. Dev Neurobiol 71:1090-1101.
54. Moore SW, Tessier-Lavigne M, Kennedy TE (2007) Netrins and their receptors. Adv Exp Med Biol 621:17-31.
55. Moore SW, Biais N, Sheetz MP (2009) Traction on immobilized netrin-1 is sufficient to reorient axons. Science 325:166.
56. Moore SW, Roca-Cusachs P, Sheetz MP (2010) Stretchy proteins on stretchy substrates: the important elements of integrin-mediated rigidity sensing. Dev Cell 19:194-206.
57. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20:87-90.
58. Nojima Y, Morino N, Mimura T, Hamasaki K, Furuya H, Sakai R, Sato T, Tachibana K, Morimoto C, Yazaki Y (1995) Integrin-mediated cell adhesion promotes tyrosine phosphorylation of p130Cas, a Src homology 3-containing molecule having multiple Src homology 2-binding motifs. J Biol Chem 270:15398-15402.
59. Ojaniemi M, Vuori K (1997) Epidermal growth factor modulates tyrosine phosphorylation of p130Cas. Involvement of phosphatidylinositol 3′- kinase and actin cytoskeleton. J Biol Chem 272:25993-25998.
60. Papusheva E, Mello de Queiroz F, Dalous J, Han Y, Esposito A, Jares-Erijmanxa EA, Jovin TM, Bunt G (2009) Dynamic conformational changes in the FERM domain of FAK are involved in focal-adhesion behavior during cell spreading and motility. J Cell Sci 122:656-666.
61. Pasapera AM, Schneider IC, Rericha E, Schlaepfer DD, Waterman CM (2010) Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation. J Cell Biol 188:877-890.
62. Poullet P, Gautreau A, Kadaré G, Girault JA, Louvard D, Arpin M (2001) Ezrin interacts with focal adhesion kinase and induces its activation independently of cell-matrix adhesion. J Biol Chem 276:37686-37691.
63. Raper J, Mason C (2010) Cellular strategies of axonal pathfinding. Cold Spring Harb Perspect Biol 2:a001933.
64. 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.
65. Rider CC (2006) Heparin/heparan sulphate binding in the TGF-beta cytokine superfamily. Biochem Soc Trans 34:458-460.
66. Robles E, Gomez TM (2006) Focal adhesion kinase signaling at sites of integrin-mediated adhesion controls axon pathfinding. Nat Neurosci 9:1274-1283.
67. Sanders MA, Basson MD (2005) p130cas but not paxillin is essential for Caco-2 intestinal epithelial cell spreading and migration on collagen IV. J Biol Chem 280:23516-23522.
68. Sawada Y, Tamada M, Dubin-Thaler BJ, Cherniavskaya O, Sakai R, Tanaka S, SheetzMP (2006) Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127:1015-1026.
69. 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.
70. Serafini T, Kennedy TE, Galko MJ, Mirzayan C, Jessell TM, Tessier-Lavigne M (1994) The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78:409-424.
71. Serafini T, Colamarino SA, Leonardo ED, Wang H, Beddington R, Skarnes WC, Tessier-Lavigne M (1996) Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87:1001-1014.
72. Serrels B, Serrels A, Brunton VG, Holt M, McLean GW, Gray CH, Jones GE, Frame MC (2007) Focal adhesion kinase controls actin assembly via a FERM-mediated interaction with the Arp2/3 complex. Nat Cell Biol 9:1046-1056.
73. Shekarabi M, Moore SW, Tritsch NX, Morris SJ, Bouchard JF, Kennedy TE (2005) Deleted in colorectal cancer binding netrin-1 mediates cell substrate adhesion and recruits Cdc42, Rac1, Pak1, and N-WASP into an intracellular signaling complex that promotes growth cone expansion. J Neurosci 25:3132-3141.
74. Singh MK, Dadke D, Nicolas E, Serebriiskii IG, Apostolou S, Canutescu A, Egleston BL, Golemis EA (2008) A novel Cas family member, HEPL, regulates FAK and cell spreading. Mol Biol Cell 19:1627-1636.
75. Slack-Davis JK, Martin KH, Tilghman RW, Iwanicki M, Ung EJ, Autry C, Luzzio MJ, Cooper B, Kath JC, Roberts WG, Parsons JT (2007) Cellular characterization of a novel focal adhesion kinase inhibitor. J Biol Chem 282:14845-14852.
76. Suter DM, Forscher P (2000) Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. J Neurobiol 44:97-113.
77. Tang D, Mehta D, Gunst SJ (1999) Mechanosensitive tyrosine phosphorylation of paxillin and focal adhesion kinase in tracheal smooth muscle. Am J Physiol 276:C250-C258.
78. Tazaki T, Miyazaki K, Hiyama E, Nakamoto T, Sakai R, Yamasaki N, Honda Z, Noda M, Miyasaka N, Sueda T, Honda H (2008) Functional analysis of Src homology 3-encoding exon (exon 2) of p130Cas in primary fibroblasts derived from exon 2-specific knockout mice. Genes Cells 13:145-157.
79. Vuori K, Ruoslahti E (1995) Tyrosine phosphorylation of p130Cas and cortactin accompanies integrin-mediated cell adhesion to extracellular matrix. J Biol Chem 270:22259-22262.
80. Wang HB, Dembo M, Hanks SK, Wang Y (2001) Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proc Natl Acad Sci U S A 98:11295-11300.
81. 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.
82. Yano Y, Geibel J, Sumpio BE (1996) Tyrosine phosphorylation of pp125FAK and paxillin in aortic endothelial cells induced by mechanical strain. Am J Physiol 271:C635-C649.
83. Yebra M, Montgomery AMP, Diaferia GR, Kaido T, Silletti S, Perez B, Just ML, Hildbrand S, Hurford R, Florkiewicz E, Tessier-Lavigne M, Cirulli V (2003) Recognition of the neural chemoattractant Netrin-1 by integrins alpha6beta4 and alpha3beta1 regulates epithelial cell adhesion and migration. Dev Cell 5:695-707.
84. Zhang X, Jiang G, Cai Y, Monkley SJ, Critchley DR, Sheetz MP (2008) Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nat Cell Biol 10:1062-1068.