Integrin signaling switches the cytoskeletal and exocytic machinery that drives neuritogenesis

Developmental Cell

Volumn 18, Issue 5, 2010, Pages 725-736

  Gupton, Stephanie L ^a   Gertler, Frank B ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Cellbio; Molneuro

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; FOCAL ADHESION KINASE; INTEGRIN; LAMIN; PROTEIN TYROSINE KINASE; PROTEIN VAMP7; SYNAPTOBREVIN; SYNAPTOBREVIN 2; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MOTILITY; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; EXOCYTOSIS; MORPHOGENESIS; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

ACTINS; ANIMALS; CELL ADHESION MOLECULES; CELL CULTURE TECHNIQUES; CEREBRAL CORTEX; CYTOSKELETON; EXOCYTOSIS; FOCAL ADHESION KINASE 1; HOMEOSTASIS; INTEGRINS; LAMININ; MICE; MICROFILAMENT PROTEINS; NEURITES; NEURONS; PHOSPHOPROTEINS; R-SNARE PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 77952928699     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2010.02.017     Document Type: Article

References (89)

1. Ahuja R., Pinyol R., Reichenbach N., Custer L., Klingensmith J., Kessels M.M., Qualmann B. Cordon-bleu is an actin nucleation factor and controls neuronal morphology. Cell 2007, 131:337-350.
2. Aizawa H., Wakatsuki S., Ishii A., Moriyama K., Sasaki Y., Ohashi K., Sekine-Aizawa Y., Sehara-Fujisawa A., Mizuno K., Goshima Y., et al. Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse. Nat. Neurosci. 2001, 4:367-373.
3. Alberts P., Rudge R., Irinopoulou T., Danglot L., Gauthier-Rouviere C., Galli T. Cdc42 and actin control polarized expression of TI-VAMP vesicles to neuronal growth cones and their fusion with the plasma membrane. Mol. Biol. Cell 2006, 17:1194-1203.
4. Applewhite D.A., Barzik M., Kojima S.I., Svitkina T.M., Gertler F.B., Borisy G.G. Ena/VASP proteins have an anti-capping independent function in filopodia formation. Mol. Biol. Cell 2007, 18:2579-2591.
5. Axelrod D., Thompson N.L., Burghardt T.P. Total internal inflection fluorescent microscopy. J. Microsc. 1983, 129:19-28.
6. Bachmann C., Fischer L., Walter U., Reinhard M. The EVH2 domain of the vasodilator-stimulated phosphoprotein mediates tetramerization, F-actin binding, and actin bundle formation. J. Biol. Chem. 1999, 274:23549-23557.
7. Barzik M., Kotova T.I., Higgs H.N., Hazelwood L., Hanein D., Gertler F.B., Schafer D.A. Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins. J. Biol. Chem. 2005, 280:28653-28662.
8. Bear J.E., Loureiro J.J., Libova I., Fassler R., Wehland J., Gertler F.B. Negative regulation of fibroblast motility by Ena/VASP proteins. Cell 2000, 101:717-728.
9. Bear J.E., Svitkina T.M., Krause M., Schafer D.A., Loureiro J.J., Strasser G.A., Maly I.V., Chaga O.Y., Cooper J.A., Borisy G.G., et al. Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 2002, 109:509-521.
10. Becker K.A., Hart N.H. Reorganization of filamentous actin and myosin-II in zebrafish eggs correlates temporally and spatially with cortical granule exocytosis. J. Cell Sci. 1999, 112:97-110.
11. Breitsprecher D., Kiesewetter A.K., Linkner J., Urbanke C., Resch G.P., Small J.V., Faix J. Clustering of VASP actively drives processive, WH2 domain-mediated actin filament elongation. EMBO J. 2008, 27:2943-2954.
12. Brouns M.R., Matheson S.F., Settleman J. p190 RhoGAP is the principal Src substrate in brain and regulates axon outgrowth, guidance and fasciculation. Nat. Cell Biol. 2001, 3:361-367.
13. Brown M.C., Cary L.A., Jamieson J.S., Cooper J.A., Turner C.E. Src and FAK kinases cooperate to phosphorylate paxillin kinase linker, stimulate its focal adhesion localization, and regulate cell spreading and protrusiveness. Mol. Biol. Cell 2005, 16:4316-4328.
14. Brunton V.G., MacPherson I.R., Frame M.C. Cell adhesion receptors, tyrosine kinases and actin modulators: a complex three-way circuitry. Biochim. Biophys. Acta 2004, 1692:121-144.
15. Buck C.A., Horwitz A.F. Integrin, a transmembrane glycoprotein complex mediating cell-substratum adhesion. J. Cell Sci. Suppl. 1987, 8:231-250.
16. Chen T.J., Gehler S., Shaw A.E., Bamburg J.R., Letourneau P.C. Cdc42 participates in the regulation of ADF/cofilin and retinal growth cone filopodia by brain derived neurotrophic factor. J. Neurobiol. 2006, 66:103-114.
17. Copeland J.W., Copeland S.J., Treisman R. Homo-oligomerization is essential for F-actin assembly by the formin family FH2 domain. J. Biol. Chem. 2004, 279:50250-50256.
18. Dehmelt L., Smart F.M., Ozer R.S., Halpain S. The role of microtubule-associated protein 2c in the reorganization of microtubules and lamellipodia during neurite initiation. J. Neurosci. 2003, 23:9479-9490.
19. Dent E.W., Kalil K. Axon branching requires interactions between dynamic microtubules and actin filaments. J. Neurosci. 2001, 21:9757-9769.
20. Dent E.W., Kwiatkowski A.V., Mebane L.M., Philippar U., Barzik M., Rubinson D.A., Gupton S., Van Veen J.E., Furman C., Zhang J., et al. Filopodia are required for cortical neurite initiation. Nat. Cell Biol. 2007, 9:1347-1359.
21. Dotti C.G., Sullivan C.A., Banker G.A. The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 1988, 8:1454-1468.
22. EauClaire S., Guo W. Conservation and specialization. The role of the exocyst in neuronal exocytosis. Neuron 2003, 37:369-370.
23. Flanagan L.A., Rebaza L.M., Derzic S., Schwartz P.H., Monuki E.S. Regulation of human neural precursor cells by laminin and integrins. J. Neurosci. Res. 2006, 83:845-856.
24. Furman C., Sieminski A.L., Kwiatkowski A.V., Rubinson D.A., Vasile E., Bronson R.T., Fassler R., Gertler F.B. Ena/VASP is required for endothelial barrier function in vivo. J. Cell Biol. 2007, 179:761-775.
25. Futerman A.H., Banker G.A. The economics of neurite outgrowth-the addition of new membrane to growing axons. Trends Neurosci. 1996, 19:144-149.
26. Galli T., Zahraoui A., Vaidyanathan V.V., Raposo G., Tian J.M., Karin M., Niemann H., Louvard D. A novel tetanus neurotoxin-insensitive vesicle-associated membrane protein in SNARE complexes of the apical plasma membrane of epithelial cells. Mol. Biol. Cell 1998, 9:1437-1448.
27. Gallo G., Yee H.F., Letourneau P.C. Actin turnover is required to prevent axon retraction driven by endogenous actomyosin contractility. J. Cell Biol. 2002, 158:1219-1228.
28. Gao Y., Dickerson J.B., Guo F., Zheng J., Zheng Y. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc. Natl. Acad. Sci. USA 2004, 101:7618-7623.
29. Gates J., Mahaffey J.P., Rogers S.L., Emerson M., Rogers E.M., Sottile S.L., Van Vactor D., Gertler F.B., Peifer M. Enabled plays key roles in embryonic epithelial morphogenesis in Drosophila. Development 2007, 134:2027-2039.
30. Geiger B., Bershadsky A., Pankov R., Yamada K.M. Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat. Rev. Mol. Cell Biol. 2001, 2:793-805.
31. Gorecki D.C., Derry J.M., Barnard E.A. Dystroglycan: brain localisation and chromosome mapping in the mouse. Hum. Mol. Genet. 1994, 3:1589-1597.
32. Gotoh T., Cai D., Tian X., Feig L.A., Lerner A. p130Cas regulates the activity of AND-34, a novel Ral, Rap1, and R-Ras guanine nucleotide exchange factor. J. Biol. Chem. 2000, 275:30118-30123.
33. Gupton S.L., Gertler F.B. Filopodia: the fingers that do the walking. Sci. STKE 2007, 2007:re5.
34. Han J., Han L., Tiwari P., Wen Z., Zheng J.Q. Spatial targeting of type II protein kinase A to filopodia mediates the regulation of growth cone guidance by cAMP. J. Cell Biol. 2007, 176:101-111.
35. Harris E.S., Rouiller I., Hanein D., Higgs H.N. Mechanistic differences in actin bundling activity of two mammalian formins, FRL1 and mDia2. J. Biol. Chem. 2006, 281:14383-14392.
36. Hong W. SNAREs and traffic. Biochim. Biophys. Acta 2005, 1744:493-517.
37. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell 2002, 110:673-687.
38. Ivins J.K., Colognato H., Kreidberg J.A., Yurchenco P.D., Lander A.D. Neuronal receptors mediating responses to antibodyactivated laminin-1. J. Neurosci. 1998, 18:9703-9715.
39. Korobova F., Svitkina T. Arp2/3 complex is important for filopodia formation, growth cone motility, and neuritogenesis in neuronal cells. Mol. Biol. Cell 2008, 19:1561-1574.
40. Kwiatkowski A.V., Rubinson D.A., Dent E.W., Edward van Veen J., Leslie J.D., Zhang J., Mebane L.M., Philippar U., Pinheiro E.M., Burds A.A., et al. Ena/VASP is required for neuritogenesis in the developing cortex. Neuron 2007, 56:441-455.
41. Lanzetti L. Actin in membrane trafficking. Curr. Opin. Cell Biol. 2007, 19:453-458.
42. Lebrand C., Dent E.W., Strasser G.A., Lanier L.M., Krause M., Svitkina T.M., Borisy G.G., Gertler F.B. Critical role of Ena/VASP proteins for filopodia formation in neurons and in function downstream of netrin-1. Neuron 2004, 42:37-49.
43. Liu J., Yue P., Artym V.V., Mueller S.C., Guo W. The role of the exocyst in matrix metalloproteinase secretion secretion and actin dynamics during tumor cell invadopodia formation. Mol. Biol. Cell 2009, 20:3763-3771.
44. Malsam J., Kreye S., Sollner T.H. Membrane fusion: SNAREs and regulation. Cell. Mol. Life Sci. 2008, 65:2814-2832.
45. Martinez-Arca S., Alberts P., Zahraoui A., Louvard D., Galli T. Role of tetanus neurotoxin insensitive vesicle-associated membrane protein (TI-VAMP) in vesicular transport mediating neurite outgrowth. J. Cell Biol. 2000, 149:889-900.
46. Matusek T., Gombos R., Szecsenyi A., Sanchez-Soriano N., Czibula A., Pataki C., Gedai A., Prokop A., Rasko I., Mihaly J. Formin proteins of the DAAM subfamily play a role during axon growth. J. Neurosci. 2008, 28:13310-13319.
47. May R.C., Hall M.E., Higgs H.N., Pollard T.D., Chakraborty T., Wehland J., Machesky L.M., Sechi A.S. The Arp2/3 complex is essential for the actin-based motility of Listeria monocytogenes. Curr. Biol. 1999, 9:759-762.
48. May R.C., Caron E., Hall A., Machesky L.M. Involvement of the Arp2/3 complex in phagocytosis mediated by FcgammaR or CR3. Nat. Cell Biol. 2000, 2:246-248.
49. Miesenbock G., De Angelis D.A., Rothman J.E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 1998, 394:192-195.
50. Miyashita M., Ohnishi H., Okazawa H., Tomonaga H., Hayashi A., Fujimoto T.T., Furuya N., Matozaki T. Promotion of neurite and filopodium formation by CD47: roles of integrins, Rac, and Cdc42. Mol. Biol. Cell 2004, 15:3950-3963.
51. Murthy M., Garza D., Scheller R.H., Schwarz T.L. Mutations in the exocyst component Sec5 disrupt neuronal membrane traffic, but neurotransmitter release persists. Neuron 2003, 37:433-447.
52. Nobes C.D., Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 1995, 81:53-62.
53. Ohnishi H., Yamamori S., Ono K., Aoyagi K., Kondo S., Takahashi M. A src family tyrosine kinase inhibits neurotransmitter release from neuronal cells. Proc. Natl. Acad. Sci. USA 2001, 98:10930-10935.
54. Osen-Sand A., Staple J.K., Naldi E., Schiavo G., Rossetto O., Petitpierre S., Malgaroli A., Montecucco C., Catsicas S. Common and distinct fusion proteins in axonal growth and transmitter release. J. Comp. Neurol. 1996, 367:222-234.
55. Pfenninger K.H. Plasma membrane expansion: a neuron's Herculean task. Nat. Rev. Neurosci. 2009, 10:251-261.
56. Pinyol R., Haeckel A., Ritter A., Qualmann B., Kessels M. Regulation of N-WASP and the Arp2/3 complex by Abp1 controls neuronal morphology. PLoS ONE 2007, 2:e400.
57. Plantman S., Patarroyo M., Fried K., Domogatskaya A., Tryggvason K., Hammarberg H., Cullheim S. Integrin-laminin interactions controlling neurite outgrowth from adult DRG neurons in vitro. Mol. Cell. Neurosci. 2008, 39:50-62.
58. Pommereit D., Wouters F.S. An NGF-induced Exo70-TC10 complex locally antagonises Cdc42-mediated activation of N-WASP to modulate neurite outgrowth. J. Cell Sci. 2007, 120:2694-2705.
59. Ridley A.J., Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 1992, 70:389-399.
60. Ridley A.J., Paterson H.F., Johnston C.L., Diekmann D., Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 1992, 70:401-410.
61. Rohatgi R., Ma L., Miki H., Lopez M., Kirchhausen T., Takenawa T., Kirschner M.W. The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 1999, 97:221-231.
62. Rohatgi R., Nollau P., Ho H.Y., Kirschner M.W., Mayer B.J. Nck and phosphatidylinositol 4,5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway. J. Biol. Chem. 2001, 276:26448-26452.
63. Sablina A.A., Chen W., Arroyo J.D., Corral L., Hector M., Bulmer S.E., DeCaprio J.A., Hahn W.C. The tumor suppressor PP2A Abeta regulates the RalA GTPase. Cell 2007, 129:969-982.
64. Schaefer A.W., Schoonderwoert V.T., Ji L., Mederios N., Danuser G., Forscher P. Coordination of actin filament and microtubule dynamics during neurite outgrowth. Dev. Cell 2008, 15:146-162.
65. Schaller M.D., Borgman C.A., Parsons J.T. Autonomous expression of a noncatalytic domain of the focal adhesion-associated protein tyrosine kinase pp125FAK. Mol. Cell. Biol. 1993, 13:785-791.
66. Schirenbeck A., Arasada R., Bretschneider T., Stradal T.E., Schleicher M., Faix J. The bundling activity of vasodilator-stimulated phosphoprotein is required for filopodium formation. Proc. Natl. Acad. Sci. USA 2006, 103:7694-7699.
67. Schoch S., Deak F., Konigstorfer A., Mozhayeva M., Sara Y., Sudhof T.C., Kavalali E.T. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 2001, 294:1117-1122.
68. Schroer T.A. Motors for fast axonal transport. Curr. Opin. Neurobiol. 1992, 2:618-621.
69. Shen Y., Mani S., Donovan S.L., Schwob J.E., Meiri K.F. Growth-associated protein-43 is required for commissural axon guidance in the developing vertebrate nervous system. J. Neurosci. 2002, 22:239-247.
70. Sikorra S., Henke T., Galli T., Binz T. Substrate recognition mechanism of VAMP/synaptobrevin-cleaving clostridial neurotoxins. J. Biol. Chem. 2008, 283:21145-21152.
71. Sokac A.M., Bement W.M. Kiss-and-coat and compartment mixing: coupling exocytosis to signal generation and local actin assembly. Mol. Biol. Cell 2006, 17:1495-1502.
72. Strasser G.A., Rahim N.A., VanderWaal K.E., Gertler F.B., Lanier L.M. Arp2/3 is a negative regulator of growth cone translocation. Neuron 2004, 43:81-94.
73. Sugihara K., Asano S., Tanaka K., Iwamatsu A., Okawa K., Ohta Y. The exocyst complex binds the small GTPase RalA to mediate filopodia formation. Nat. Cell Biol. 2002, 4:73-78.
74. Tang B.L. Protein trafficking mechanisms associated with neurite outgrowth and polarized sorting in neurons. J. Neurochem. 2001, 79:923-930.
75. Tehrani S., Tomasevic N., Weed S., Sakowicz R., Cooper J.A. Src phosphorylation of cortactin enhances actin assembly. Proc. Natl. Acad. Sci. USA 2007, 104:11933-11938.
76. TerBush D.R., Maurice T., Roth D., Novick P. The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 1996, 15:6483-6494.
77. Tian X., Rusanescu G., Hou W., Schaffhausen B., Feig L.A. PDK1 mediates growth factor-induced Ral-GEF activation by a kinase-independent mechanism. EMBO J. 2002, 21:1327-1338.
78. Tojima T., Akiyama H., Itofusa R., Li Y., Katayama H., Miyawaki A., Kamiguchi H. Attractive axon guidance involves asymmetric membrane transport and exocytosis in the growth cone. Nat. Neurosci. 2007, 10:58-66.
79. Tsaneva-Atanasova K., Burgo A., Galli T., Holcman D. Quantifying neurite growth mediated by interactions among secretory vesicles, microtubules, and actin networks. Biophys. J. 2009, 96:840-857.
80. Valentijn J.A., Valentijn K., Pastore L.M., Jamieson J.D. Actin coating of secretory granules during regulated exocytosis correlates with the release of rab3D. Proc. Natl. Acad. Sci. USA 2000, 97:1091-1095.
81. Vega I.E., Hsu S.C. The exocyst complex associates with microtubules to mediate vesicle targeting and neurite outgrowth. J. Neurosci. 2001, 21:3839-3848.
82. Verderio C., Coco S., Bacci A., Rossetto O., De Camilli P., Montecucco C., Matteoli M. Tetanus toxin blocks the exocytosis of synaptic vesicles clustered at synapses but not of synaptic vesicles in isolated axons. J. Neurosci. 1999, 19:6723-6732.
83. Vuori K., Ruoslahti E. Tyrosine phosphorylation of p130Cas and cortactin accompanies integrin-mediated cell adhesion to extracellular matrix. J. Biol. Chem. 1995, 270:22259-22262.
84. Wang Y., Tang B.L. SNAREs in neurons-beyond synaptic vesicle exocytosis. Mol. Membr. Biol. 2006, 23:377-384.
85. Wiederkehr A., De Craene J.O., Ferro-Novick S., Novick P. Functional specialization within a vesicle tethering complex: bypass of a subset of exocyst deletion mutants by Sec1p or Sec4p. J. Cell Biol. 2004, 167:875-887.
86. Withee J., Galligan B., Hawkins N., Garriga G. Caenorhabditis elegans WASP and Ena/VASP proteins play compensatory roles in morphogenesis and neuronal cell migration. Genetics 2004, 167:1165-1176.
87. Wolf A.M., Lyuksyutova A.I., Fenstermaker A.G., Shafer B., Lo C.G., Zou Y. Phosphatidylinositol-3-kinase-atypical protein kinase C signaling is required for Wnt attraction and anterior-posterior axon guidance. J. Neurosci. 2008, 28:3456-3467.
88. Yoon M.S., Yon C., Park S.Y., Oh D.Y., Han A.H., Kim D.S., Han J.S. Role of phospholipase D1 in neurite outgrowth of neural stem cells. Biochem. Biophys. Res. Commun. 2005, 329:804-811.
89. Zuo X., Zhang J., Zhang Y., Hsu S.C., Zhou D., Guo W. Exo70 interacts with the Arp2/3 complex and regulates cell migration. Nat. Cell Biol. 2006, 8:1383-1388.