How VASP enhances actin-based motility

Journal of Cell Biology

Volumn 163, Issue 1, 2003, Pages 131-142

  Samarin, Stanislav ^a   Romero, Stéphane ^a   Kocks, Christine ^b   Didry, Dominique ^a   Pantaloni, Dominique ^a   Carlier, Marie France ^a  

^a CNRS   (France)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

ActA; Arp2 3; Filament branching; Site directed polymerization; VASP

Indexed keywords

ACTIN; MICROSPHERE; PROTEIN ACTA; PROTEIN ARP2 3 COMPLEX; REGULATOR PROTEIN; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; BINDING SITE; BIOMIMETIC MOTILITY ASSAY; CATALYSIS; CELL ADHESION; CELL BRANCHING; CELL DETACHMENT; CELL GROWTH; CELL JUNCTION; CELL KINETICS; CELL MOTILITY; LAMELLIPODIUM; LISTERIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN IMMOBILIZATION; REGULATORY MECHANISM; VELOCITY;

ACTIN DEPOLYMERIZING FACTORS; ACTINS; ANIMALS; CELL ADHESION MOLECULES; CELL MOVEMENT; DESTRIN; HUMANS; MICROFILAMENT PROTEINS; MICROSPHERES; MUSCLES; PHOSPHOPROTEINS; RABBITS;

LISTERIA;

EID: 0142123248     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200303191     Document Type: Article

References (47)

1. Bachmann, C., L. Fischer, U. Walter, and M. Reinhard. 1999. The EVH2 domain of the vasodilator-stimulated phosphoprotein mediates tetramerization, F-actin binding, and actin bundle formation. J. Biol. Chem. 274:23549-23557.
2. Ball, L.J., T. Jarchau, H. Oschkinat, and U. Walter. 2002. EVH1 domains: structure, function and interactions. FEBS Lett. 513:45-52.
3. Bear, J.E., J.J. Loureiro, I. Libova, R. Fassler, J. Wehland, and F.B. Gertler. 2000. Negative regulation of fibroblast motility by Ena/VASP proteins. Cell. 101:717-728.
4. Bear, J.E., M. Krause, and F.B. Gertler. 2001. Regulating cellular actin assembly. Curr. Opin. Cell Biol. 13:158-166.
5. Bear, J.E., T.M. Svitkina, M. Krause, D.A. Schafer, J.J. Loureiro, G.A. Strasser, I.V. Maly, O.Y. Chaga, J.A. Cooper, G.G. Borisy, and F.B. Gertler. 2002. Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell. 109:509-521.
6. Bearer, E.L., J.M. Prakash, R.D. Manchester, and P.G. Allen. 2000. VASP protects actin filaments from gelsolin: an in vitro study with implications for platelet actin reorganizations. Cell Motil. Cytoskeleton. 47:351-364.
7. Bernheim-Grosswasser, A., S. Wiesner, R. M. Golsteyn, M.-F. Carlier, and C. Sykes. 2002. The dynamics of actin-based motility depends on surface parameters. Nature. 417:308-311.
8. Boujemaa-Paterski, R., E. Gouin, G. Hansen, S. Samarin, C. Le Clainche, D. Didry, P. Dehoux, P. Cossart, C. Kocks, M.F. Carlier, and D. Pantaloni. 2001. Listeria protein ActA mimics WASp family proteins: it activates filament barbed end branching by Arp2/3 complex. Biochemistry. 40:11390-11404.
9. Brindle, N.P., M.R. Holt, J.E. Davies, C.J. Price, and D.R. Critchley. 1996. The focal-adhesion vasodilator-stimulated phosphoprotein (VASP) binds to the proline-rich domain in vinculin. Biochem. J. 318:753-757.
10. 2+ at the high-affinity and low-affinity sites on the polymerization of actin and associated ATP hydrolysis. J. Biol. Chem. 261:10785-10792.
11. Carlsson, A.E. 2001. Growth of branched actin networks against obstacles. Biophys. J. 81:1907-1923.
12. Carlsson, A.E. 2003. Growth velocities of branched actin networks. Biophys. J. 84:2907-2918.
13. Castellano, F., C. Le Clainche, D. Patin, M.F. Carlier, and P. Chavrier. 2001. A WASp-VASP complex regulates actin polymerization at the plasma membrane. EMBO J. 20:5603-5614.
14. Chakraborty, T., F. Ebel, E. Domann, K. Niebuhr, B. Gerstel, S. Pistor, C.J. Temm-Grove, B.M. Jockusch, M. Reinhard, U. Walter, et al. 1995. A focal adhesion factor directly linking intracellularly motile Listeria monocytogenes and Listeria ivanovii to the actin-based cytoskeleton of mammalian cells. EMBO J. 14:1314-1321.
15. Cicchetti, G., P. Maurer, P. Wagener, and C. Kocks. 1999. Actin and phosphoinositide binding by the ActA protein of the bacterial pathogen Listeria monocytogenes. J. Biol. Chem. 274:33616-33626.
16. Drees, B., E. Friederich, J. Fradelizi, D. Louvard, M.C. Beckerle, and R.M. Golsteyn. 2000. Characterization of the interaction between zyxin and members of the Ena/vasodilator-stimulated phosphoprotein family of proteins. J. Biol. Chem. 275:22503-22511.
17. Egile, C., T.P. Loisel, V. Laurent, R. Li, D. Pantaloni, P.J. Sansonetti, and M.F. Carlier. 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.
18. Falet, H., K.M. Hoffmeister, R. Neujahr, J.E. Italiano, T.P. Stossel, F.S. Southwick, and J.H. Hartwig. 2002. Importance of free actin filament barbed ends for Arp2/3 complex function in platelets and fibroblasts. Proc. Natl. Acad. Sci. USA. 99:16782-16787.
19. Garcia Arguinzonis, M.I., A.B. Galler, U. Walter, M. Reinhard, and A. Simm. 2002. Increased spreading, Rac/p21-activated kinase (PAK) activity, and compromised cell motility in cells deficient in vasodilator-stimulated phosphoprotein (VASP). J. Biol. Chem. 277:45604-45610.
20. Geese, M., J.J. Loureiro, J.E. Bear, J. Wehland, F.B. Gertler, and A.S. Sechi. 2002. Contribution of Ena/VASP proteins to intracellular motility of Listeria requires phosphorylation and proline-rich core but not F-actin binding or multimerization. Mol. Biol. Cell. 13:2383-2396.
21. Gertler, F.B., K. Niebuhr, M, Reinhard, J. Wehland, and P. Soriano. 1996. Mena, a relative of VASP and Drosophila Enabled, is implicated in the control of microfilament dynamics. Cell. 87:227-239.
22. Han, Y.H., C.Y. Chung, D. Wessels, S. Stephens, M.A. Titus, D.R. Soll, and R.A. Firtel. 2002. Requirement of a vasodilator-stimulated phosphoprotein family member for cell adhesion, the formation of filopodia, and chemotaxis in dictyostelium. J. Biol. Chem. 277:49877-49887.
23. Holt, M.R., D.R. Critchley, and N.P. Brindle. 1998. The focal adhesion phosphoprotein, VAS P. Int. J. Biochem. Cell Biol. 30:307-311.
24. Huttelmaier, S., B. Harbeck, O. Steffens, T. Messerschmidt, S. Illenberger, and B.M. Jockusch. 1999. Characterization of the actin binding properties of the vasodilator-stimulated phosphoprotein VASP. FEBS Lett. 451:68-74.
25. Kocks, C., R. Hellio, P. Gounon, H. Ohayon, and P. Cossart. 1993. Polarized distribution of Listeria monocytogenes surface protein ActA at the site of directional actin assembly. J. Cell Sci. 105:699-710.
26. Kwiatkowski, A.V., F.B. Gertler, and J.J. Loureiro. 2003. Function and regulation of Ena/VASP proteins. Trends Cell Biol. 13:386-392.
27. Lambrechts, A., A.V. Kwiatkowski, L.M. Lanier, J.E. Bear, J. Vandekerckhove, C. Ampe, and F.B. Gertler. 2000. cAMP-dependent protein kinase phosphorylation of EVL, a Mena/VASP relative, regulates its interaction with actin and SH3 domains. J. Biol. Chem. 275:36143-36151.
28. Lanier, L.M., M.A. Gates, W. Witke, A.S. Menzies, A.M. Wehman, J.D. Macklis, D. Kwiatkowski, P. Soriano, and F.B. Gertler. 1999. Mena is required for neurulation and commissure formation. Neuron. 22:313-325.
29. Lasa, I., E. Gouin, M. Goethals, K. Vancompernolle, V. David, J. Vandekerckhove, and P. Cossart. 1997. Identification of two regions in the N-terminal domain of ActA involved in the actin comet tail formation by Listeria monocytogenes. EMBO J. 16:1531-1540.
30. Lauer, P., J.A. Theriot, J. Skoble, M.D. Welch, and D.A. Portnoy. 2001. Systematic mutational analysis of the amino-terminal domain of the Listeria monocytogenes ActA protein reveals novel functions in actin-based motility. Mol. Microbiol. 42:1163-1177.
31. Laurent, V., T.P. Loisel, B. Harbeck, A. Wehman, L. Grobe, B.M. Jockusch, J. Wehland, F.B. Gertler, and M.F. Carlier. 1999. Role of proteins of the Ena/ VASP family in actin-based motility of Listeria monocytogenes. J. Cell Biol. 144:1245-1258.
32. Loisel, T.P., R. Boujemaa, D. Pantaloni, and M.F. Carlier. 1999. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature. 401:613-616.
33. Loureiro, J.J., D.A. Rubinson, J.E. Bear, G.A. Balrus, A.V. Kwiatkowski, and F.B. Gertler. 2002. Critical roles of phosphorylation and actin binding motifs, but not the central proline-rich region, for Ena/vasodilator-stimulated phosphoprotein (VASP) function during cell migration. Mol. Biol. Cell. 13:2533-2546.
34. Mogilner, A., and G. Oster. 2003. Force generation by actin polymerization II: the elastic ratcher and tethered filaments. Biophys. J. 84:1591-1605.
35. Niebuhr, K., F. Ebel, R. Frank, M. Reinhard, E. Domann, U.D. Carl, U. Walter, F.B. Gertler, J. Wehland, and T. Chakraborty. 1997. A novel proline-rich motif present in ActA of Listeria monocytogenes and cytoskeletal proteins is the ligand for the EVH1 domain, a protein module present in the Ena/ VASP family. EMBO J. 16:5433-5444.
36. Pantaloni, D., R. Boujemaa, D. Didty, P. Gounon, and M.F. Carlier. 2000. The Arp2/3 complex branches filament barbed ends: functional antagonism with capping proteins. Nat. Cell Biol. 2:385-391.
37. Pantaloni, D., C. Le Clainche, and M.F. Carlier. 2001. Mechanism of actin-based motility. Science. 292:1502-1506.
38. Reinhard, M., T. Jarchau, and U. Walter. 2001. Actin-based motility: stop and go with Ena/VASP proteins. Trends Biochem. Sci. 26:243-249.
39. Renfranz, P.J., and M.C. Beckerle. 2002. Doing (F/L)PPPPs: EVH1 domains and their proline-rich partners in cell polarity and migration. Curr. Opin. Cell Biol. 14:88-103.
40. Rottner, K., B. Behrendt, J.V. Small, and J. Wehland. 1999. VASP dynamics during lamellipodia protrusion. Nat. Cell Biol. 1:321-322.
41. Skoble, J., V. Auerbuch, E.D. Goley, M.D. Welch, and D.A. Portnoy. 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.
42. Smith, G.A., J.A. Theriot, and D.A. Pormoy. 1996. The tandem repeat domain in the Listeria monocytogenes ActA protein controls the rate of actin-based motility, the percentage of moving bacteria, and the localization of vasodilator-stimulated phosphoprotein and profilin. J. Cell Biol. 135:647-660.
43. Svitkina, T.M., E.A. Bulanova, O.Y. Chaga, D.M. Vignjevic, S. Kojima, J.M. Vasiliev, and G.G. Borisy. 2003. Mechanism of filopodia initiation by reorganization of a dendritic network. J. Cell Biol. 160:409-421.
44. Walders-Harbeck, B., S.Y. Khaitlina, H. Hinssen, B.M. Jockusch, and S. Illenberger. 2002. The vasodilator-stimulated phosphoprotein promotes actin polymerisation through direct binding to monomeric actin. FEBS Lett. 529:275-280.
45. Waldmann, R., M. Nieberding, and U. Walter. 1987. Vasodilator-stimulated protein phosphotylation in platelets is mediated by cAMP- and cGMP-dependent protein kinases. Eur. J. Biochem. 167:441-448.
46. Wiesner, S., E. Helfer, D. Didty, G. Ducouret, F. Lafuma, M.F. Carlier, and D. Pantaloni. 2003. A biomimetic motility assay provides insight into the mechanism of actin-based motility. J. Cell Biol. 160:387-398.
47. Zimmerle, C.T., and C. Frieden. 1988. Effect of pH on the mechanism of actin polymerization. Biochemistry. 27:7766-7772.