The WASP-WAVE protein network: Connecting the membrane to the cytoskeleton

Nature Reviews Molecular Cell Biology

Volumn 8, Issue 1, 2007, Pages 37-48

  Takenawa, Tadaomi ^a   Suetsugu, Shiro ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; ADAPTOR PROTEIN; CARRIER PROTEINS AND BINDING PROTEINS; GUANOSINE TRIPHOSPHATASE; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; UNCLASSIFIED DRUG; WISKOTT ALDRICH SYNDROME PROTEIN; WISKOTT ALDRICH SYNDROME PROTEIN FAMILY VERPROLIN HOMOLOGOUS PROTEIN;

ACTIN POLYMERIZATION; CELL MEMBRANE; CELL SHAPE; CYTOPLASM; CYTOSKELETON; FILOPODIUM; INVADOPODIUM; LAMELLIPODIUM; NONHUMAN; PODOSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; ANIMALS; CELL MEMBRANE; CYTOSKELETON; HUMANS; PHYLOGENY; PSEUDOPODIA; WISKOTT-ALDRICH SYNDROME PROTEIN FAMILY;

EID: 33845729059     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm2069     Document Type: Review

References (150)

1. Wiskott, A. Familiarer, angeborener Morbus Welhofii? Monatsschr. Kinderheilkd. 68, 212-216 (1937).
2. Aldrich, R. A., Steinberg, A. G. & Campbell, D. C. Pedigree demonstrating a sex-linked recessive condition characterized by draining ears, eczematoid dermatitis and bloody diarrhea. Pediatrics 13, 133-139 (1954).
3. Thrasher, A. J. WASp in immune-system organization and function. Nature Rev. Immunol. 2, 635-646 (2002).
4. Ochs, H. D. & Notarangelo, L. D. Structure and function of the Wiskott-Aldrich syndrome protein. Curr. Opin. Hematol. 12, 284-291 (2005).
5. Derry, J. M., Ochs, H. D. & Francke, U. Isolation of a novel gene mutated in Wiskott-Aldrich syndrome. Cell 78, 635-644 (1994). Discovery of WASP.
6. Miki, H., Miura, K. & Takenawa, T. N-WASP, a novel actin-depolymerizing protein, regulates the cortical cytoskeletal rearrangement in a PIP2-dependent manner downstream of tyrosine kinases. EMBO J. 15, 5326-5335 (1996). Discovery of N-WASP.
7. Pollard, T. D. & Borisy, G. G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465 (2003).
8. Takenawa, T. & Miki, H. WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J. Cell Sci. 114, 1801-1809 (2001).
9. Miki, H., Suetsugu, S. & Takenawa, T. WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. EMBO J. 17, 6932-6941 (1998). Discovery of WAVE1.
10. Bear, J. E., Rawls, J. F. & Saxe III, C. L. SCAR, a WASP-related protein, isolated as a suppressor of receptor defects in late Dictyostelium development. J. Cell Biol. 142, 1325-1335 (1998).
11. Suetsugu, S., Miki, H. & Takenawa, T. Identification of two human WAVE/SCAR homologues as general actin regulatory molecules which associate with Arp2/3 complex. Biochem. Biophys. Res. Commun. 260, 296-302 (1999). Discovery of WAVE2 and WAVE3.
12. Li, R. Bee1, a yeast protein with homology to Wiscott-Aldrich syndrome protein, is critical for the assembly of cortical actin cytoskeleton. J. Cell Biol. 136, 649-658 (1997).
13. Panchal, S. C., Kaiser, D. A., Torres, E., Pollard, T. D. & Rosen, M. K. A conserved amphipathic helix in WASP/Scar proteins is essential for activation of Arp2/3 complex. Nature Struct. Biol. 10, 591-598 (2003).
14. Miki, H. & Takenawa, T. Direct binding of the verprolin-homology domain in N-WASP to actin is essential for cytoskeletal reorganization. Biochem. Biophys. Res. Commun. 243, 73-78 (1998).
15. Symons, M. et al. Wiskott-Aldrich syndrome protein, a novel effector for the GTPase CDC42Hs, is implicated in actin polymerization. Cell 84, 723-734 (1996).
16. Rohatgi, R. et al. The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97, 221-231 (1999). Demonstration of N-WASP autoinhibition.
17. Machesky, L. M. & Insall, R. H. Scar1 and the related Wiskott-Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr. Biol. 8, 1347-1356 (1998).
18. Machesky, L. M. et al. Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc. Natl Acad. Sci. USA 96, 3739-3744 (1999). References 17 and 18 reported the identification of the ARP2/3 complex as a WASP/WAVE binding partner and showed that ARP2/3 is activated by WAVE.
19. Pantaloni, D., Boujemaa, R., Didry, D., Gounon, P. & Carlier, M.-F. The Arp2/3 complex branches filament barbed ends: functional antagonism with capping proteins. Nature Cell. Biol. 2, 385-391 (2000).
20. Blanchoin, L. et al. Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins. Nature 404, 1007-1011 (2000).
21. Fujiwara, I., Suetsugu, S., Uemura, S., Takenawa, T. & Ishiwata, S. Visualization and force measurement of branching by Arp2/3 complex and N-WASP in actin filament. Biochem. Biophys. Res. Commun. 293, 1550-1555 (2002).
22. Yarar, D., D'Alessio, J. A., Jeng, R. L. & Welch, M. D. Motility determinants in WASP family proteins. Mol. Biol. Cell 13, 4045-4059 (2002).
23. Suetsugu, S., Miki, H. & Takenawa, T. Identification of another Actin-related protein (Arp) 2/3 complex binding site in neural Wiskott-Aldrich syndrome protein (N-WASP), that complements actin polymerization induced by the Arp2/3 complex activating (VCA) domain of N-WASP. J. Biol. Chem. 276, 33175-33180 (2001).
24. Suetsugu, S., Miki, H., Yamaguchi, H. & Takenawa, T. Requirement of the basic region of N-WASP/WAVE2 for actin-based motility. Biochem. Biophys. Res. Commun. 282, 739-744 (2001).
25. Rodal, A. A., Manning, A. L., Goode, B. L. & Drubin, D. G. Negative regulation of yeast WASp by two SH3 domain-containing proteins. Curr. Biol. 13, 1000-1008 (2003).
26. Aspenstrom, P., Lindberg, U. & Hall, A. Two GTPases, Cdc42 and Rac, bind directly to a protein implicated in the immunodeficiency disorder Wiskott-Aldrich syndrome. Curr. Biol. 6, 70-75 (1996).
27. Volkman, B. F., Prehoda, K. E., Scott, J. A., Peterson, F. C. & Lim, W. A. Structure of the N-WASP EVH1 domain-WIP complex: insight into the molecular basis of Wiskott-Aldrich syndrome. Cell 111, 565-576 (2002).
28. Ramesh, N., Anton, I. M., Hartwig, J. H. & Geha, R. S. WIP, a protein associated with Wiskott-Aldrich syndrome protein, induces actin polymerization and redistribution in lymphoid cells. Proc. Natl Acad. Sci. USA 94, 14671-14676 (1997). Identification of WIP.
29. Aspenstrom, P. The WASP-binding protein WIRE has a role in the regulation of the actin filament system downstream of the platelet-derived growth factor receptor. Exp. Cell Res. 279, 21-33 (2002).
30. Kato, M. et al. WICH, a novel verprolin homology domain-containing protein that functions cooperatively with N-WASP in actin-microspike formation. Biochem. Biophys. Res. Commun. 291, 41-47 (2002).
31. Ho, H. Y., Rohatgi, R., Ma, L. & Kirschner, M. W. CR16 forms a complex with N-WASP in brain and is a novel member of a conserved proline-rich actin-binding protein family. Proc. Natl Acad. Sci. USA 98, 11306-11311 (2001).
32. Aspenstrom, P. The mammalian verprolin homologue WIRE participates in receptor-mediated endocytosis and regulation of the actin filament system by distinct mechanisms. Exp. Cell Res. 298, 485-498 (2004).
33. Krzewski, K., Chen, X., Orange, J. S. & Strominger, J. L. Formation of a WIP-, WASp-, actin-, and myosin IIA-containing multiprotein complex in activated NK cells and its alteration by KIR inhibitory signaling. J. Cell Biol. 173, 121-132 (2006).
34. Sawa, M. & Takenawa, T. Caenorhabditis elegans WASP-interacting protein homologue WIP-1 is involved in morphogenesis through maintenance of WSP-1 protein levels. Biochem. Biophys. Res. Commun. 340, 709-717 (2006).
35. Martinez-Quiles, N. et al. WIP regulates N-WASP-mediated actin polymerization and filopodium formation. Nature Cell Biol. 3, 484-491 (2001).
36. Ho, H. Y. et al. Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex. Cell 118, 203-216 (2004).
37. Hertzog, M. et al. The β-thymosin/WH2 domain; structural basis for the switch from inhibition to promotion of actin assembly. Cell 117, 611-623 (2004).
38. Sasahara, Y. et al. Mechanism of recruitment of WASP to the immunological synapse and of its activation following TCR ligation. Mol. Cell 10, 1269-1281 (2002).
39. Moreau, V. et al. A complex of N-WASP and WIP integrates signalling cascades that lead to actin polymerization. Nature Cell Biol. 2, 441-448 (2000).
40. Frischknecht, F. et al. Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401, 926-929 (1999).
41. Anton, I. M. et al. WIP deficiency reveals a differential role for WIP and the actin cytoskeleton in T and B cell activation. Immunity 16, 193-204 (2002).
42. Snapper, S. B. et al. Wiskott-Aldrich syndrome protein-deficient mice reveal a role for WASP in T but not B cell activation. Immunity 9, 81-91 (1998).
43. Rohatgi, R., Ho, H. Y. & Kirschner, M. W. Mechanism of N-WASP activation by CDC42 and phosphatidylinositol 4,5-bisphosphate. J. Cell Biol. 150, 1299-1310 (2000).
44. Higgs, H. N. & Pollard, T. D. Activation by Cdc42 and PIP(2) of Wiskott-Aldrich syndrome protein (WASp) stimulates actin nucleation by Arp2/3 complex. J. Cell Biol. 150, 1311-1320 (2000).
45. Miki, H., Sasaki, T., Takai, Y. & Takenawa, T. Induction of filopodium formation by WASP-related actin-depolymerizing protein N-WASP. Nature 391, 93-96 (1998).
46. Hall, A. Rho GTPase and the actin cytoskeleton. Science 279, 509-514 (1998).
47. Abe, T., Kato, M., Miki, H., Takenawa, T. & Endo, T. Small GTPase Tc10 and its homologue RhoT induce N-WASP-mediated long process formation and neurite outgrowth. J. Cell Sci. 116, 155-168 (2003).
48. Hemsath, L., Dvorsky, R., Fiegen, D., Carlier, M. F. & Ahmadian, M. R. An electrostatic steering mechanism of Cdc42 recognition by Wiskott-Aldrich syndrome proteins. Mol. Cell 20, 313-324 (2005).
49. Aronheim, A. et al. Chp, a homologue of the GTPase Cdc42Hs, activates the JNK pathway and is implicated in reorganizing the actin cytoskeleton. Curr. Biol. 8, 1125-1128 (1998).
50. Kim, A. S., Kakalis, L. T., Abdul-Manan, N., Liu, G. A. & Rosen, M. K. Autoinhibition and activation mechanisms of the Wiskott-Aldrich syndrome protein. Nature 404, 151-158 (2000).
51. Prehoda, K. E., Scott, J. A., Mullins, D. R. & Lim, W. A. Integration of multiple signals through cooperative regulation of the N-WASP-Arp2/3 complex. Science 290, 801-806 (2000).
52. Suetsugu, S. et al. Regulation of actin cytoskeleton by mDab1 through N-WASP and ubiquitination of mDab1. Biochem. J. 384, 1-8 (2004).
53. Fukuoka, M. et al. A novel neural Wiskott-Aldrich syndrome protein (N-WASP) binding protein, WISH, induces Arp2/3 complex activation independent of Cdc42. J. Cell Biol. 152, 471-482 (2001).
54. Carlier, M.-F. et al. Grb2 links signaling to actin assembly by enhancing interaction of neural Wiskott-Aldrich syndrome protein (N-WASP) with actin-related protein (Arp2/3) complex. J. Biol. Chem. 275, 21946-21952 (2000).
55. 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. 276, 26448-26452 (2001).
56. Tsujita, K. et al. Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis. J. Cell Biol. 172, 269-279 (2006).
57. Cory, G. O., Garg, R., Cramer, R. & Ridley, A. J. Phosphorylation of tyrosine 291 enhances the ability of WASp to stimulate actin polymerization and filopodium formation. Wiskott-Aldrich syndrome protein. J. Biol. Chem. 277, 45115-45121 (2002).
58. Suetsugu, S. et al. Sustained activation of N-WASP through phosphorylation is essential for neurite extension. Dev. Cell 3, 645-658 (2002). The first report that WASP and WAVE proteins are degraded by proteasomes.
59. Torres, E. & Rosen, M. K. Contingent phosphorylation/ dephosphorylation provides a mechanism of molecular memory in WASP. Mol. Cell 11, 1215-1227 (2003).
60. Park, S. J., Suetsugu, S. & Takenawa, T. Interaction of HSP90 to N-WASP leads to activation and protection from proteasome-dependent degradation. EMBO J. 24, 1557-1570 (2005).
61. Schulte, R. J. & Sefton, B. M. Inhibition of the activity of SRC and Abl tyrosine protein kinases by the binding of the Wiskott-Aldrich syndrome protein. Biochemistry 42, 9424-9430 (2003).
62. Habermann, B. The BAR-domain family of proteins: a case of bending and binding? EMBO Rep. 5, 250-255 (2004).
63. Itoh, T. et al. Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev. Cell 9, 791-804 (2005). References 56 and 63 report the identification of the EFC domain as a membrane-deforming domain. The role of PCH family proteins in linking membrane deformation with the cytoskeleton was proposed in this paper.
64. Gundelfinger, E. D., Kessels, M. M. & Qualmann, B. Temporal and spatial coordination of exocytosis and endocytosis. Nature Rev. Mol. Cell Biol. 4, 127-139 (2003).
65. Peter, B. J. et al. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495-499 (2004). The structure of BAR domain indicates that the shape of the protein dictates the shape of the membrane.
66. Naqvi, S. N., Zahn, R., Mitchell, D. A., Stevenson, B. J. & Munn, A. L. The WASp homologue Las17p functions with the WIP homologue End5p/verprolin and is essential for endocytosis in yeast. Curr. Biol. 8, 959-962 (1998). Proposes a role for WASP family proteins in association with WIP in endocytosis.
67. Qualmann, B. & Kelly, R. B. Syndapin isoforms participate in receptor-mediated endocytosis and actin organization. J. Cell Biol. 148, 1047-1062 (2000). N-WASP is shown to be involved in endocytosis through binding to an EFC-domain-containing protein.
68. Kaksonen, M., Toret, C. P. & Drubin, D. G. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123, 305-320 (2005).
69. Otsuki, M., Itoh, T. & Takenawa, T. T. N-WASP is recruited to rafts and associates with endophilin A in response to EGF. J. Biol. Chem. 278, 6461-6469 (2002).
70. Madania, A. et al. The Saccharomyces cerevisiae homologue of human Wiskott-Aldrich syndrome protein Las17p interacts with the Arp2/3 complex. Mol. Biol. Cell 10, 3521-3538 (1999).
71. Kamioka, Y. et al. A novel dynamin-associating molecule, formin-binding protein 17, induces tubular membrane invaginations and participates in endocytosis. J. Biol. Chem. 279, 40091-40099 (2004).
72. Soulard, A. et al. Saccharomyces cerevisiae Bzz1p is implicated with type I myosins in actin patch polarization and is able to recruit actin-polymerizing machinery in vitro. Mol. Cell. Biol. 22, 7889-7906 (2002).
73. Merrifield, C. J., Perrais, D. & Zenisek, D. Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 121, 593-606 (2005).
74. Svitkina, T. M. & Borisy, G. G. Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J. Cell Biol. 145, 1009-1026 (1999).
75. Kaksonen, M., Toret, C. P. & Drubin, D. G. Harnessing actin dynamics for clathrin-mediated endocytosis. Nature Rev. Mol. Cell Biol. 7, 404-414 (2006).
76. Rozelle, A. L. et al. Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr. Biol. 10, 311-320 (2000).
77. Taunton, J. et al. Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J. Cell Biol. 148, 519-530 (2000).
78. Nakagawa, H. et al. N-WASP, WAVE and Mena play different roles in the organization of actin cytoskeleton in lamellipodia. J. Cell Sci. 114, 1555-1565 (2001).
79. Lommel, S. et al. Actin pedestal formation by enteropathogenic Escherichia coli and intracellular motility of Shigella flexneri are abolished in N-WASP-defective cells. EMBO Rep. 2, 850-857 (2001).
80. Snapper, S. B. et al. N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nature Cell Biol. 3, 897-904 (2001).
81. Suetsugu, S., Miki, H., Yamaguchi, H., Obinata, T. & Takenawa, T. Enhancement of branching efficiency by the actin filament-binding activity of N-WASP/WAVE2. J. Cell Sci. 114, 4533-4542 (2001).
82. Steffen, A. et al. Filopodia formation in the absence of functional WAVE and Arp2/3 complexes. Mol. Biol. Cell 17, 2581-2591 (2006).
83. Schirenbeck, A., Bretschneider, T., Arasada, R., Schleicher, M. & Faix, J. The Diaphanous-related formin dDia2 is required for the formation and maintenance of filopodia. Nature Cell Biol. 7, 619-625 (2005).
84. Buccione, R., Orth, J. D. & McNiven, M. A. Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nature Rev. Mol. Cell Biol. 5, 647-657 (2004).
85. Linder, S. & Aepfelbacher, M. Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol. 13, 376-385 (2003).
86. Mizutani, K., Miki, H., He, H., Maruta, H. & Takenawa, T. Essential role of neural Wiskott-Aldrich syndrome protein in podosome formation and degradation of extracellular matrix in src-transformed fibroblasts. Cancer Res. 62, 669-674 (2002).
87. Weaver, A. et al. Interaction of cortactin and N-WASP with Arp2/3 complex. Curr. Biol. 12, 1270 (2002).
88. Yamaguchi, H. et al. Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J. Cell Biol. 168, 441-452 (2005).
89. Weaver, A. M. et al. Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr. Biol. 11, 370-374 (2001).
90. Uruno, T. et al. Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nature Cell Biol. 3, 259-266 (2001).
91. Krueger, E. W., Orth, J. D., Cao, H. & McNiven, M. A. A dynamin-cortactin-Arp2/3 complex mediates Actin reorganization in growth factor-stimulated cells. Mol. Biol. Cell 14, 1085-1096 (2003).
92. Schafer, D. A. et al. Dynamin2 and cortactin regulate actin assembly and filament organization. Curr. Biol. 12, 1852-1857 (2002).
93. Wu, X., Suetsugu, S., Cooper, L. A., Takenawa, T. & Guan, J. L. Focal adhesion kinase regulation of NWASP subcellular localization and function. J. Biol. Chem. 279, 9565-9576 (2004).
94. Jones, N. et al. Nck adaptor proteins link nephrin to the actin cytoskeleton of kidney podocytes. Nature 440, 818-823 (2006).
95. Gruenheid, S. et al. Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells. Nature Cell Biol. 3, 856-859 (2001).
96. Rivera, G. M., Briceno, C. A., Takeshima, F., Snapper, S. B. & Mayer, B. J. Inducible clustering of membrane-targeted SH3 domains of the adaptor protein Nck triggers localized actin polymerization. Curr. Biol. 14, 11-22 (2004).
97. Oikawa, T. et al. PtdIns(3,4,5)P3 binding is necessary for WAVE2-induced formation of lamellipodia. Nature Cell Biol. 6, 420-426 (2004).
98. Eden, S., Rohatgi, R., Podtelejnikov, A. V., Mann, M. & Kirschner, M. W. Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418, 790-793 (2002). Identification of the WAVE complex that consists of WAVE1, ABI1/2, NAP1/p125NAP1, SRA1/PIR121 and HSPC300. Proposes trans-inhibition of WAVE. The presence of the Rac-binding molecule, SRA1/PIR121, in the WAVE complex was also described.
99. Innocenti, M. et al. Abi1 is essential for the formation and activation of a WAVE2 signalling complex. Nature Cell Biol. 6, 319-327 (2004). Demonstration of constitutive formation of the WAVE2 complex.
100. Gautreau, A. et al. Purification and architecture of the ubiquitous Wave complex. Proc. Natl Acad. Sci. USA 101, 4379-4383 (2004).
101. Suetsugu, S. et al. Optimization of WAVE2-complex-induced actin polymerization by membrane-bound IRSp53, PIP3, and Rac. J. Cell Biol. 173, 571-585 (2006). The WAVE2 complex was purified from cells and its activity in the ARP2/3 activation was examined. Reconcilement of two proposals, through SRA1/PIR121 and IRSp53, for Rac association with WAVE2.
102. Stovold, C. F., Millard, T. H. & Machesky, L. M. Inclusion of Scar/WAVE3 in a similar complex to Scar/WAVE1 and 2. BMC Cell Biol. 6, 11 (2005).
103. Leng, Y. et al. Abelson-interactor-1 promotes WAVE2 membrane translocation and Abelson-mediated tyrosine phosphorylation required for WAVE2 activation. Proc. Natl Acad. Sci. USA 102,1098-1103 (2005).
104. Soto, M. C. et al. The GEX-2 and GEX-3 proteins are required for tissue morphogenesis and cell migrations in C. elegans. Genes Dev. 16, 620-632 (2002).
105. Sawa, M. et al. Essential role of the C. elegans Arp2/3 complex in cell migration during ventral enclosure. J. Cell Sci. 116, 1505-1518 (2003).
106. Kitamura, T. et al. Molecular cloning of p125Nap1, a protein that associates with an SH3 domain of Nck. Biochem. Biophys. Res. Commun. 219, 509-514 (1996).
107. Kobayashi, K. et al. p140Sra-1 (specifically Rac1-associated protein) is a novel specific target for Rac1 small GTPase. J. Biol. Chem. 273, 291-295 (1998).
108. Steffen, A. et al. Sra-1 and Nap1 link Rac to actin assembly driving lamellipodia formation. EMBO J. 23, 749-759 (2004).
109. Kunda, P., Craig, G., Dominguez, V. & Baum, B. Abi, Sra1, and Kette control the stability and localization of SCAR/WAVE to regulate the formation of actin-based protrusions. Curr. Biol. 13, 1867-1875 (2003).
110. Rogers, S. L., Wiedemann, U., Stuurman, N. & Vale, R. D. Molecular requirements for actin-based lamella formation in Drosophila S2 cells. J. Cell Biol. 162, 1079-1088 (2003).
111. Nozumi, M., Nakagawa, H., Miki, H., Takenawa, T. & Miyamoto, S. Differential localization of WAVE isoforms in filopodia and lamellipodia of the neuronal growth cone. J. Cell Sci. 116, 239-246 (2003).
112. Suetsugu, S., Yamazaki, D., Kurisu, S. & Takenawa, T. Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration. Dev. Cell 5, 595-609 (2003). Description of differential roles for WAVE1 and WAVE2. The requirement of WAVE2 in lamellipodia formation is established in this paper and in reference 113.
113. Yamazaki, D., Fujiwara, T., Suetsugu, S. & Takenawa, T. A novel function of WAVE in lamellipodia: WAVE1 is required for stabilization of lamellipodial protrusions during cell spreading. Genes Cells 10, 381-392 (2005).
114. Kim, Y. et al. Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology. Nature 442, 814-817 (2006). Involvement of WAVE1 in spine formation. CDK5-mediated phosphorylation of WAVE1 is reported to inhibit WAVE1-induced ARP2/3 activation in spine formation.
115. Yan, C. et al. WAVE2 deficiency reveals distinct roles in embryogenesis and Rac-mediated actin-based motility. EMBO J. 22, 3602-3612 (2003).
116. Yamazaki, D. et al. WAVE2 is required for directed cell migration and cardiovascular development. Nature 424, 452-456 (2003).
117. Yeh, T. C., Ogawa, W., Danielsen, A. G. & Roth, R. A. Characterization and cloning of a 58/53-kDa substrate of the insulin receptor tyrosine kinase. J. Biol. Chem. 271, 2921-2928 (1996).
118. Miki, H., Yamaguchi, H., Suetsugu, S. & Takenawa, T. IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 408, 732-735 (2000). Identification of IRSp53 as a linker molecule between Rac and WAVE2.
119. Oda, A. et al. WAVE/Scars in platelets. Blood 105, 3141-3148 (2005).
120. Choi, J. et al. Regulation of dendritic spine morphogenesis by insulin receptor substrate 53, a downstream effector of Rac1 and Cdc42 small GTPases. J. Neurosci. 25, 869-879 (2005).
121. Nakagawa, H. et al. IRSp53 is colocalised with WAVE2 at the tips of protruding lamellipodia and filopodia independently of Mena. J. Cell Sci. 116, 2577-2583 (2003).
122. Krugmann, S. et al. Cdc42 induces filopodia by promoting the formation of an IRSp53:Mena complex. Curr. Biol. 11, 1645-1655 (2001).
123. Yamagishi, A., Masuda, M., Ohki, T., Onishi, H. & Mochizuki, N. A novel actin bundling/filopodiumforming domain conserved in insulin receptor tyrosine kinase substrate p53 and missing in metastasis protein. J. Biol. Chem. 279, 14929-14936 (2004).
124. Millard, T. H. et al. Structural basis of filopodia formation induced by the IRSp53/MIM homology domain of human IRSp53. EMBO J. 24, 240-250 (2005). First report of the structure of the RCB/IMD domain of IRSp53.
125. Suetsugu, S. et al. The RAC-binding domain/IRSP53-MIM homology domain of IRSP53 induces RAC-dependent membrane deformation. J. Biol. Chem. 281, 35347-35358 (2006). Reports Rac-dependent membrane deformation by the RCB/IMD domain.
126. Govind, S., Kozma, R., Monfries, C., Lim, L. & Ahmed, S. Cdc42Hs facilitates cytoskeletal reorganization and neurite outgrowth by localizing the 58-kD insulin receptor substrate to filamentous actin. J. Cell Biol. 152, 579-594 (2001).
127. Soderling, S. H. et al. The WRP component of the WAVE-1 complex attenuates Rac-mediated signalling. Nature Cell Biol. 4, 970-975 (2002).
128. Wu, R. F., Gu, Y., Xu, Y. C., Nwariaku, F. E. & Terada, L. S. Vascular endothelial growth factor causes translocation of p47phox to membrane ruffles through WAVE1. J. Biol. Chem. 278, 36830-36840 (2003).
129. Westphal, R. S., Soderling, S. H., Alto, N. M., Langeberg, L. K. & Scott, J. D. Scar/WAVE-1, a Wiskott-Aldrich syndrome protein, assembles an actin-associated multi-kinase scaffold. EMBO J. 19, 4589-4600 (2000).
130. Miki, H., Fukuda, M., Nishida, E. & Takenawa, T. Phosphorylation of WAVE downstream of mitogen-activated protein kinase signaling. J. Biol. Chem. 274, 27605-27609 (1999).
131. Theriot, J. A. & Mitchison, T. J. Actin microfilament dynamics in locomoting cells. Nature 352, 126-131 (1991).
132. Pantoloni, D. & Carlier, M.-F. How profilin promotes actin filament assembly in the presence of thymosin β4. Cell 75, 1007-1014 (1993).
133. Yang, C. et al. Profilin enhances Cdc42-induced nucleation of actin polymerization. J. Cell Biol. 150, 1001-1012 (2000).
134. Suetsugu, S., Miki, H. & Takenawa, T. The essential role of profilin in the assembly of actin for microspike formation. EMBO J. 17, 6516-6526 (1998). Demonstrates that profilin is important for actin reorganization induced by WASP and WAVE family proteins.
135. Mimuro, H. et al. Profilin is required for sustaining efficient intra- and intercellular spreading of Shigella flexneri. J. Biol. Chem. 275, 28893-28901 (2000).
136. Loisel, T. P., Boujemaa, R., Pantaloni, D. & Carlier, M. F. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401, 613-616 (1999). Reconstitution of actin-based motility from purified proteins without any live organisms.
137. Welch, M. D., Iwamatsu, A. & Mitchison, T. J. Actin polymerization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes. Nature 385, 265-269 (1997).
138. Suzuki, T., Miki, H., Takenawa, T. & Sasakawa, C. Neural Wiskott-Aldrich syndrome protein is implicated in the actin-based motility of Shigella flexneri. EMBO J. 17, 2767-2776 (1998).
139. Egile, C. et al. Activation of the CDC42 effector N-WASP by the Shigella flexneri IcsA protein promotes actin nucleation by Arp2/3 complex and bacterial actin-based motility. J. Cell Biol. 146, 1319-1332 (1999).
140. Cameron, L. A., Svitkina, T. M., Vignjevic, D., Theriot, J. A. & Borisy, G. G. Dendritic organization of actin comet tails. Curr. Biol. 11, 130-135 (2001).
141. Kalman, D. et al. Enteropathogenic E. coli acts through WASP and Arp2/3 complex to form actin pedestals. Nature Cell Biol. 1, 389-391 (1999).
142. Shi, J., Scita, G. & Casanova, J. E. WAVE2 signaling mediates invasion of polarized epithelial cells by Salmonella typhimurium. J. Biol. Chem. 280, 29849-29855 (2005).
143. Banzai, Y., Miki, H., Yamaguchi, H. & Takenawa, T. Essential role of neural Wiskott-Aldrich syndrome protein in neurite extension in PC12 cells and rat hippocampal primary culture cells. J. Biol. Chem. 275, 11987-11992 (2000).
144. 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 43, 81-94 (2004).
145. Kakimoto, T., Katoh, H. & Negishi, M. Regulation of neuronal morphology by Toca-1, an F-BAR/EFC protein that induces plasma membrane invagination. J. Biol. Chem. 281, 29042-29053 (2006).
146. Wong, K. et al. Signal transduction in neuronal migration: roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell 107, 209-221 (2001).
147. Fujita, H., Katoh, H., Ishikawa, Y., Mori, K. & Negishi, M. Rapostlin is a novel effector of Rnd2 GTPase inducing neurite branching. J. Biol. Chem. 277, 45428-45434 (2002).
148. Kawano, Y. et al. CRMP-2 is involved in kinesin-1-dependent transport of the Sra-1/WAVE1 complex and axon formation. Mol. Cell. Biol. 25, 9920-9935 (2005).
149. Irie, F. & Yamaguchi, Y. EphB receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP. Nature Neurosci. 5, 1117-1118 (2002).
150. Udo, H. et al. Serotonin-induced regulation of the actin network for learning-related synaptic growth requires Cdc42, N-WASP, and PAK in Aplysia sensory neurons. Neuron 45, 887-901 (2005).