Motility determinants in WASP family proteins

Molecular Biology of the Cell

Volumn 13, Issue 11, 2002, Pages 4045-4059

  Yarar, Defne ^a   D'Alessio, Joseph A ^a   Jeng, Robert L ^a   Welch, Matthew D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CELL PROTEIN; PROFILIN; PROLINE; PROTEIN ARP2/3 COMPLEX; PROTEIN EVH1; PROTEIN SCAR1; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN; WISKOTT ALDRICH SYNDROME PROTEIN; ACTIN BINDING PROTEIN; ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; ACTR2 PROTEIN, HUMAN; ACTR3 PROTEIN, HUMAN; CELL ADHESION MOLECULE; CONTRACTILE PROTEIN; CYTOSKELETON PROTEIN; HYBRID PROTEIN; PFN1 PROTEIN, HUMAN; PHOSPHOPROTEIN; PROTEIN; VASODILATOR-STIMULATED PHOSPHOPROTEIN; WAS PROTEIN, HUMAN;

ARTICLE; CELL MOTILITY; CELL NUCLEUS; CONTROLLED STUDY; GENE MUTATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FAMILY; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; WILD TYPE; WISKOTT ALDRICH SYNDROME; ANIMAL; BIOLOGICAL MODEL; CELL MOTION; GENETICS; METABOLISM; OOCYTE; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; XENOPUS LAEVIS;

ACTIN-RELATED PROTEIN 2; ACTIN-RELATED PROTEIN 3; ACTINS; ANIMALS; CELL ADHESION MOLECULES; CELL MOVEMENT; CONTRACTILE PROTEINS; CYTOSKELETAL PROTEINS; HUMANS; MICROFILAMENT PROTEINS; MODELS, BIOLOGICAL; OOCYTES; PHOSPHOPROTEINS; PROFILINS; PROTEIN STRUCTURE, TERTIARY; PROTEINS; RECOMBINANT FUSION PROTEINS; WISKOTT-ALDRICH SYNDROME; WISKOTT-ALDRICH SYNDROME PROTEIN; WISKOTT-ALDRICH SYNDROME PROTEIN FAMILY; XENOPUS LAEVIS;

EID: 0036854337     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-05-0294     Document Type: Article

References (63)

1. Anton, I.M., Lu, W., Mayer, B.J., Ramesh, N., and Geha, R.S. (1998). The Wiskott-Aldrich syndrome protein-interacting protein (WIP) binds to the adaptor protein Nck. J. Biol. Chem. 273, 20992-20995.
2. Bachmann, C., Fischer, L., Walter, U., and Reinhard, M. (1999). The EVH2 domain of the vasodilator-stimulated phosphoprotein mediates tetramerization, F-actin binding, and actin bundle formation. J. Biol. Chem. 274, 23549-23557.
3. Bear, J.E., Krause, M., and Gertler, F.B. (2001). Regulating cellular actin assembly. Curr. Opin. Cell Biol. 13, 158-166.
4. Bear, J.E., Svitkina, T.M., Krause, M., Schafer, D.A., Loureiro, J.J., Strasser, G.A., Maly, I.M., Chaga, O.Y., Cooper, J.A., Borisy, G.G., and Gertler, F.B. (2002). Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109, 509-524.
5. Bernheim-Groswasser, A., Wiesner, S., Golsteyn, R.M., Carlier, M.F., and Sykes, C. (2002). The dynamics of actin-based motility depend on surface parameters. Nature 417, 308-311.
6. Bjorkegren-Sjogren, C., Korenbaum, E., Nordberg, P., Lindberg, U., and Karlsson, R. (1997). Isolation and characterization of two mutants of human profilin I that do not bind poly-L-proline. FEBS Lett. 418, 258-264.
7. Blanchoin, L., Amann, K.J., Higgs, H.N., Marchand, J.B., Kaiser, D.A., and Pollard, T.D. (2000). Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins. Nature 404, 1007-1011.
8. Cameron, L.A., Footer, M.J., van Oudenaarden, A., and Theriot, J.A. (1999). Motility of Acta protein-coated microspheres driven by actin polymerization. Proc. Natl. Acad. Sci. USA 94, 1408-1413.
9. Carlier, M.F., Nioche, P., Broutin-L'Hermite, I., Boujemaa, R., Le Clainche, C., Egile, C., Garbay, C., Ducruix, A., Sansonetti, P., and Pantaloni, D. (2000). 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.
10. Castellano, F., Le Clainche, C., Patin, D., Carlier, M.F., and Chavrier, P. (2001). A WASp-VASP complex regulates actin polymerization at the plasma membrane. EMBO J. 20, 5603-5614.
11. Cooper, J.A., Walker, S.B., and Pollard, T.D. (1983). Pyrene actin: Documentation of the validity of a sensitive assay for actin polymerization. J. Muscle Res. Cell Motil. 4, 253-262.
12. Egile, C., Loisel, T.P., Laurent, V., Li, R., Pantaloni, D., Sansonetti, P.J., and Carlier, M.F. (1999). 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.
13. Fukuoka, M., Suetsugu, S., Miki, H., Fukami, K., Endo, T., and Takenawa, T. (2001). 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.
14. Geese, M., Loureiro, J.J., Bear, J.E., Wehland, J., Gertler, F.B., and Sechi, A.S. (2002). The contribution of Ena/VASP proteins to the intracellular motility of Listeria requires phosphorylation and the proline-rich core but not F-actin binding or multimerization. Mol. Biol. Cell 13, 2383-2396.
15. Janmey, P.A. (1991). Polyproline affinity method for purification of platelet profilin and modification with pyrene-maleimide. Methods Enzymol. 196, 92-99.
16. Harlow, E., and Lane, D, (1999). Using Antibodies; A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
17. Higgs, H.N., Blanchoin, L., and Pollard, T.D. (1999). Influence of the C terminus of Wiskott-Aldrich syndrome protein (WASp) and the Arp2/3 complex on actin polymerization. Biochemistry 38, 15212-15222.
18. Higgs, H.N., and Pollard, T.D. (2000). 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.
19. Kellogg, D.R., Mitchison, T.J., and Alberts, B.M. (1988). Behavior of microtubules and actin filaments in living Drosophila embryos. Development 103, 675-686.
20. Kim, A.S., Kakalis, L.T., Abdul-Manan, N., Liu, G.A., and Rosen, M.K. (2000). Autoinhibition and activation mechanisms of the Wiskott-Aldrich syndrome protein. Nature 404, 151-158.
21. Korenbaum, E., Nordberg, P., Bjorkegren-Sjogren, C., Schutt, C.E., Lindberg, U., Karlsson, R. (1998). The role of profilin in actin polymerization and nucleotide exchange. Biochemistry 37, 9274-9283.
22. Kouyama, T., and Mihashi, K. (1981). Fluorimetry study of N-(1-pyrenyl)iodoacetamide-labeled F-actin. Local structural change of actin protomer both on polymerization and on binding of heavy meromyosin. Eur. J. Biochem. 114, 33-38.
23. Lasa, I., David, V., Gouin, E., Marchand, J.B., and Cossart, P. (1995). The amino-terminal part of Acta is critical for the actin-based motility of Listeria monocytogenes; the central proline-rich region acts as a stimulator. Mol. Microbiol. 18, 425-436.
24. Laurent, V., Loisel, T.P., Harbeck, B., Wehman, A., Grobe, L., Jockusch, B.M., Wehland, J., Gertler, F.B., and Carlier, M.F. (1999). Role of proteins of the Ena/VASP family in actin-based motility of Listeria monocytogenes. J. Cell Biol. 144, 1245-1258.
25. Loisel, T.P., Boujemaa, R., Pantaloni, D., and Carlier, M.F. (1999). Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401, 613-616.
26. Ma, L., Cantley, L.C., Janmey, P.A., and Kirschner, M.W. (1998). Corequirement of specific phosphoinositides and small GTP-binding protein Cdc42 in inducing actin assembly in Xenopus egg extracts. J. Cell Biol. 140, 1125-1136.
27. Machesky, L.M., and Insall, R.H. (1998). Scarl and the related Wiskott-Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr. Biol. 8, 1347-1356.
28. Machesky, L.M., Mullins, R.D., Higgs, H.N., Kaiser, D.A., Blanchoin, L., May, R.C., Hall, M.E., and Pollard, T.D. (1999). Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc. Natl. Acad. Sci. USA 96, 3739-3744.
29. Marchand, J.B., Kaiser, D.A., Pollard, T.D., and Higgs, H.N. (2001). Interaction of WASP/Scar proteins with actin and vertebrate Arp2/3 complex. Nat. Cell Biol. 3, 76-82.
30. Marchand, J.B., Moreau, P., Paoletti, A., Cossart, P., Carlier, M.F., and Pantaloni, D. (1995). Actin-based movement of Listeria monocytogenes: Actin assembly results from the local maintenance of uncapped filament barbed ends at the bacterium surface. J. Cell Biol. 130, 331-343.
31. Martinez-Quiles, N., Rohatgi, R., Anton, I.M., Medina, M., Saville, S.P., Miki, H., Yamaguchi, H., Takenawa, T., Hartwig, J.H., Geha, R.S., and Ramesh, N. (2001). WIP regulates N-WASP-mediated actin polymerization and filopodium formation. Nat. Cell Biol. 3, 484-491.
32. May, R.C., Hall, M.E., Higgs, H.N., Pollard, T.D., Chakraborty, T., Wehland, J., Machesky, L.M., and Sechi, A.S. (1999). The Arp2/3 complex is essential for the actin-based motility of Listeria monocytogenes. Curr. Biol. 9, 759-762.
33. 2-dependent manner downstream of tyrosine kinases. EMBO J. 15, 5326-5335.
34. Miki, H., Sasaki, T., Takai, Y., and Takenawa, T. (1998a). Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASP. Nature 391, 93-96.
35. Miki, H., Suetsugu, S., and Takenawa, T. (1998b). WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. EMBO J. 17, 6932-6941.
36. Miki, H., Yamaguchi, H., Suetsugu, S., and Takenawa, T. (2000). IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 408, 732-735.
37. Mimuro, H., Suzuki, T., Suetsugu, S., Miki, H., Takenawa, T., and Sasakawa, C. (2000). Profilin is required for sustaining efficient intra- and intercellular spreading of Shigella flexneri. J. Biol. Chem. 275, 28893-28901.
38. Pantaloni, D., and Carlier, M.F. (1993). How profilin promotes actin filament assembly in the presence of thymosin β4. Cell 75, 1007-1014.
39. Prehoda, K.E., Scott, J.A., Dyche Mullins, R., and Lim, W.A. (2000). Integration of multiple signals through cooperative regulation of the N-WASP-Arp2/3 complex. Science 290, 801-806.
40. Ramesh, N., Anton, I.M., Hartwig, J.H., and Geha, R.S. (1997). 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.
41. Reinhard, M., Giehl, K., Abel, K., Haffner, C., Jarchau, T., Hoppe, V., Jockusch, B.M., and Walter, U. (1995). The proline-rich focal adhesion and microfilament protein VASP is a ligand for profilins. EMBO J. 14, 1583-1589.
42. Rohatgi, R., Ho, H.Y., and Kirschner, M.W. (2000). Mechanism of N-WASP activation by CDC42 and phosphatidylinositol 4,5-bisphosphate. J. Cell Biol. 150, 1299-1310.
43. Rohatgi, R., Ma, L., Miki, H., Lopez, M., Kirchhausen, T., Takenawa, T., and Kirschner, M.W. (1999). The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97, 221-231.
44. Rohatgi, R., Nollau, P., Ho, H.Y., Kirschner, M.W., and Mayer, B.J. (2001). Nck and phosphatidylinositol 4,5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway. J. Biol. Chem. 276, 26448-26452.
45. Schindelhauer, D., Weiss, M., Hellebrand, H., Golla, A., Hergersberg, M., Seger, R., Belohradsky, B.H., and Meindl, A. (1996). Wiskott-Aldrich syndrome: No strict genotype-phenotype correlations but clustering of missense mutations in the amino-terminal part of the WASP gene product. Hum. Genet. 98, 68-76.
46. Skoble, J., Auerbuch, V., Goley, E.D., Welch, M.D., and Portnoy, D.A. (2001). Pivotal role of VASP in Arp2/3 complex-mediated actin nucleation, actin branch-formation, and Listeria monocytogenes motility. J. Cell Biol. 155, 89-100.
47. Skoble, J., Portnoy, D.A., and Welch, M.D. (2000). Three regions within Acta promote Arp2/3 complex-mediated actin nucleation and Listeria monocytogenes motility. J. Cell Biol. 150, 527-538.
48. Spudich, J.A., and Watt, S. (1971). The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J. Biol. Chem. 246, 4866-4871.
49. Suetsugu, S., Miki, H., and Takenawa, T. (1998). The essential role of profilin in the assembly of actin for microspike formation. EMBO J. 17, 6516-6526.
50. Suetsugu, S., Miki, H., and Takenawa, T. (2001a). 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.
51. Suetsugu, S., Miki, H., Yamaguchi, H., and Takenawa, T. (2001b). Requirement of the basic region of N-WASP/WAVE2 for actin-based motility. Biochem. Biophys. Res. Commun. 282, 739-744.
52. Sun, H.Q., Kwiatkowska, K., and Yin, H.L. (1995). Actin monomer binding proteins. Curr. Opin. Cell Biol. 7, 102-110.
53. Suzuki, T., Miki, H., Takenawa, T., and Sasakawa, C. (1998). Neural Wiskott-Aldrich syndrome protein is implicated in the actin-based motility of Shigella flexneri. EMBO J. 17, 2767-2776.
54. Symons, M., Derry, J.M., Karlak, B., Jiang, S., Lemahieu, V., McCormick, F., Francke, U., and Abo, A. (1996). Wiskott-Aldrich syndrome protein, a novel effector for the GTPase CDC42Hs, is implicated in actin polymerization. Cell 84, 723-734.
55. Takenawa, T., and Miki, H. (2001). WASP and WAVE family proteins: Key molecules for rapid rearrangement of cortical actin filaments and cell movement. J. Cell Sci. 114, 1801-1809.
56. Theriot, J.A., Mitchison, T.J., Tilney, L.G., and Portnoy, D.A. (1992). The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization. Nature 357, 257-260.
57. Theriot, J.A., Rosenblatt, J., Portnoy, D.A., Goldschmidt-Clermont, P.J., and Mitchison, T.J. (1994). Involvement of profilin in the actin-based motility of L. monocytogenes in cells and in cell-free extracts. Cell 76, 505-517.
58. Welch, M.D., and Mitchison, T.J. (1998). Purification and assay of the platelet Arp2/3 complex. Methods Enzymol. 298, 52-61.
59. Winter, D., Lechler, T., and Li, R. (1999). Activation of the yeast Arp2/3 complex by Beelp, a WASP-family protein. Curr. Biol. 9, 501-504.
60. Yamaguchi, H., Miki, H., Suetsugu, S., Ma, L., Kirschner, M.W., and Takenawa, T. (2000). Two tandem verprolin homology domains are necessary for a strong activation of Arp2/3 complex-induced actin polymerization and induction of microspike formation by N-WASP. Proc. Natl. Acad. Sci. USA 97, 12631-12636.
61. Yang, C., Huang, M., DeBiasio, J., Pring, M., Joyce, M., Miki, H., Takenawa, T., and Zigmond, S.H. (2000). Profilin enhances Cdc42-induced nucleation of actin polymerization. J. Cell Biol. 150, 1001-1012.
62. Yarar, D., To, W., Abo, A., and Welch, M.D. (1999). The Wiskott-Aldrich syndrome protein directs actin-based motility by stimulating actin nucleation with the Arp2/3 complex. Curr. Biol. 9, 555-558.
63. Zalevsky, J., Lempert, L., Kranitz, H., and Mullins, R.D. (2001). Different WASP family proteins stimulate different Arp2/3 complex-dependent actin-nucleating activities. Curr. Biol. 11, 1903-1913.