Clustering of VASP actively drives processive, WH2 domain-mediated actin filament elongation

EMBO Journal

Volumn 27, Issue 22, 2008, Pages 2943-2954

  Breitsprecher, Dennis ^a   Kiesewetter, Antje K ^a   Linkner, Joern ^a   Urbanke, Claus ^a   Resch, Guenter P ^b,c   Small, J Victor ^b   Faix, Jan ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^c RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

Author keywords

Actin assembly; Capping protein; Ena VASP proteins; Processivity; TIRF microscopy

Indexed keywords

ACTIN; ACTIN CAPPING PROTEIN; PROFILIN; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; CONTROLLED STUDY; DICTYOSTELIUM; FLUORESCENCE MICROSCOPY; GENE CLUSTER; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN STRUCTURE;

ACTIN CAPPING PROTEINS; ACTINS; ANIMALS; CELL ADHESION MOLECULES; DICTYOSTELIUM; HUMANS; MICROFILAMENT PROTEINS; MICROFILAMENTS; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MUTATION; PHOSPHOPROTEINS; PROFILINS; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS;

DICTYOSTELIUM;

EID: 56549108193     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2008.211     Document Type: Article

References (51)

1. Aebi U, Baschong W (2006) Glycerol spraying/low-angle rotary metal shadowing. In Cell Biology - A Laboratory Handbook, J Celis (ed), 3rd ed, pp 241-246. London: Elsevier
2. Applewhite DA, Barzik M, Kojima S, Svitkina TM, Gertler FB, Borisy GG (2007) Ena/VASP proteins have an anti-capping independent function in filopodia formation. Mol Biol Cell 18: 2579-2591
3. Bachmann C, Fischer L, Walter U, 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
4. Ball LJ, Kuhne R, Hoffmann B, Hafner A, Schmieder P, Volkmer-Engert R, Hof M, Wahl M, Schneider-Mergener J, Walter U, Oschkinat H, Jarchau T (2000) Dual epitope recognition by the VASP EVH1 domain modulates polyproline ligand specificity and binding affinity. EMBO J 19: 4903-4914
5. Barzik M, Kotova TI, Higgs HN, Hazelwood L, Hanein D, Gertler FB, Schafer DA (2005) Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins. J Biol Chem 280: 28653-28662
6. Bear JE, Svitkina TM, Krause M, Schafer DA, Loureiro JJ, Strasser GA, Maly IV, Chaga OY, Cooper JA, Borisy GG, Gertler FB (2002) Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109: 509-521
7. Bosch M, Le KH, Bugyi B, Correia JJ, Renault L, Carlier MF (2007) Analysis of the function of Spire in actin assembly and its synergy with formin and profilin. Mol Cell 28: 555-568
8. Brindle NP, Holt MR, Davies JE, Price CJ, Critchley DR (1996) The focal-adhesion vasodilator-stimulated phosphoprotein (VASP) binds to the proline-rich domain in vinculin. Biochem J 318: 753-757
9. Carlier MF, Le Clainche C, Wiesner S, Pantaloni D (2003) Actin-based motility: from molecules to movement. Bioessays 25: 336-345
10. Carlier MF, Pantaloni D (2007) Control of actin assembly dynamics in cell motility. J Biol Chem 282: 23005-23009
11. Chereau D, Dominguez R (2006) Understanding the role of the G-actin-binding domain of Ena/VASP in actin assembly. J Struct Biol 155: 195-201
12. Co C, Wong DT, Gierke S, Chang V, Taunton J (2007) Mechanism of actin network attachment to moving membranes: barbed end capture by N-WASP WH2 domains. Cell 128: 901-913
13. Dent EW, Kwiatkowski AV, Mebane LM, Philippar U, Barzik M, Rubinson DA, Gupton S, Van Veen JE, Furman C, Zhang J, Alberts AS, Mori S, Gertler FB (2007) Filopodia are required for cortical neurite initiation. Nat Cell Biol 9: 1347-1359
14. Dickinson RB, Purich DL (2002) Clamped-filament elongation model for actin-based motors. Biophys J 2: 605-617
15. Dominguez R (2007) The beta-thymosin/WH2 fold: multifunctionality and structure. Ann N Y Acad Sci 1112: 86-94
16. Ferron F, Rebowski G, Lee SH, Dominguez R (2007) Structural basis for the recruitment of profilin-actin complexes during filament elongation by Ena/VASP. EMBO J 26: 4597-4606
17. Geese M, Loureiro JJ, Bear JE, Wehland J, Gertler FB, Sechi AS (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
18. Gertler FB, Niebuhr K, Reinhard M, Wehland J, Soriano P (1996) Mena, a relative of VASP and Drosophila enabled, is implicated in the control of microfilament dynamics. Cell 87: 227-239
19. Han YH, Chung CY, Wessels D, Stephens S, Titus MA, Soll DR, Firtel RA (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
20. Hertzog M, van Heijenoort C, Didry D, Gaudier M, Coutant J, Gigant B, Didelot G, Préat T, Knossow M, Guittet E, Carlier MF (2004) The beta-thymosin/WH2 domain; structural basis for the switch from inhibition to promotion of actin assembly. Cell 117: 611-623
21. Jenzora A, Behrendt B, Small JV, Wehland J, Stradal TE (2005) PREL1 provides a link from Ras signalling to the actin cytoskeleton via Ena/VASP proteins. FEBS Lett 580: 455-463
22. Koestler SA, Auinger S, Vinzenz M, Rottner K, Small JV (2008) Differentially oriented populations of actin filaments generated in lamellipodia collaborate in pushing and pausing at the cell front. Nat Cell Biol 10: 306-313
23. Kovar DR, Harris ES, Mahaffy R, Higgs HN, Pollard TD (2006) Control of the assembly of ATP- and ADP-actin by formins and profilin. Cell 124: 423-435
24. Kovar DR, Pollard TD (2004) Insertional assembly of actin filament barbed ends in association with formins produces piconewton forces. Proc Natl Acad Sci USA 101: 14725-14730
25. Krause M, Leslie JD, Stewart M, Lafuente EM, Valderrama F, Jagannathan R, Strasser GA, Rubinson DA, Liu H, Way M, Yaffe MB, Boussiotis VA, Gertler FB (2004) Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics. Dev Cell 7: 571-583
26. Kuhn JR, Pollard TD (2005) Real-time measurements of actin filament polymerization by total internal reflection fluorescence microscopy. Biophys J 88: 1387-1402
27. Kursula P, Kursula I, Massimi M, Song YH, Downer J, Stanley WA, Witke W, Wilmanns M (2008) High-resolution structural analysis of mammalian profilin 2a complex formation with two physiological ligands: the formin homology 1 domain of mDia1 and the proline-rich domain of VASP. J Mol Biol 375: 270-290
28. Kwiatkowski AV, Rubinson DA, Dent EW, Edward van Veen J, Leslie JD, Zhang J, Mebane LM, Philippar U, Pinheiro EM, Burds AA, Bronson RT, Mori S, Fässler R, Gertler FB (2007) Ena/VASP is required for neuritogenesis in the developing cortex. Neuron 56: 441-455
29. Lafuente EM, van Puijenbroek AA, Krause M, Carman CV, Freeman GJ, Berezovskaya A, Constantine E, Springer TA, Gertler FB, Boussiotis VA (2004) RIAM, an Ena/VASP and Profilin ligand, interacts with Rap1-GTP and mediates Rap1-induced adhesion. Dev Cell 7: 585-595
30. Lai APL, Szczodrak M, Block J, Faix J, Breitsprecher D, Mannherz HG, Stradal TE, Dunn GA, Small JV, Rottner K (2008) Arp2/3-complex interactions and actin network turnover in lamellipodia. EMBO J 27: 982-992
31. Lambrechts A, Kwiatkowski AV, Lanier LM, Bear JE, Vandekerckhove J, Ampe C, Gertler FB (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
32. Laurent V, Loisel TP, Harbeck B, Wehman A, Grobe L, Jockusch BM, Wehland J, Gertler FB, Carlier MF (1999) Role of proteins of the Ena/VASP family in actin-based motility of Listeria monocytogenes. J Cell Biol 144: 1245-1258
33. Loisel TP, Boujemaa R, Pantaloni D, Carlier MF (1999) Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401: 613-616
34. Loureiro JJ, Rubinson DA, Bear JE, Baltus GA, Kwiatkowski AV, Gertler FB (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
35. Mogilner A, Oster G (2003) Force generation by actin polymerization II: the elastic ratchet and tethered filaments. Biophys J 84: 1591-1605
36. Niebuhr K, Ebel F, Frank R, Reinhard M, Domann E, Carl UD, Walter U, Gertler FB, Wehland J, Chakraborty T (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
37. Pasic L, Kotova TI, Schafer DA (2008) Ena/VASP proteins capture actin filament barbed ends. J Biol Chem 283: 9814-9819
38. Paunola E, Mattila PK, Lappalainen P (2002) WH2 domain: a small, versatile adapter for actin monomers. FEBS Lett 513: 92-97
39. Pollard TD (2007) Regulation of actin filament assembly by Arp2/3 complex and formins. Annu Rev Biophys Biomol Struct 36: 451-477
40. Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112: 453-465
41. Reinhard M, Giehl K, Abel K, Haffner C, Jarchau T, Hoppe V, Jockusch BM, Walter U (1995a) The proline-rich focal adhesion and microfilament protein VASP is a ligand for profilins. EMBO J 14: 1583-1589
42. Reinhard M, Halbrugge M, Scheer U, Wiegand C, Jockusch BM, Walter U (1992) The 46/50 kDa phosphoprotein VASP purified from human platelets is a novel protein associated with actin filaments and focal contacts. EMBO J 11: 2063-2070
43. Reinhard M, Jouvenal K, Tripier D, Walter U (1995b) Identification, purification, and characterization of a zyxin-related protein that binds the focal adhesion and microfilament protein VASP (vasodilator-stimulated phosphoprotein). Proc Natl Acad Sci USA 92: 7956-7960
44. Romero S, Le Clainche C, Didry D, Egile C, Pantaloni D, Carlier MF (2004) Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 119: 419-429
45. Rottner K, Behrendt B, Small JV, Wehland J (1999) VASP dynamics during lamellipodia protrusion. Nat Cell Biol 1: 321-322
46. Rottner K, Stradal TE, Wehland J (2005) Bacteria-host-cell interactions at the plasma membrane: stories on actin cytoskeleton subversion. Dev Cell 9: 3-17
47. Samarin S, Romero S, Kocks C, Didry D, Pantaloni D, Carlier MF (2003) How VASP enhances actin-based motility. J Cell Biol 163: 131-142
48. Schirenbeck A, Arasada R, Bretschneider T, Stradal TE, Schleicher M, Faix J (2006) The bundling activity of vasodilator-stimulated phosphoprotein is required for filopodium formation. Proc Natl Acad Sci USA 103: 7694-7699
49. Svitkina TM, Bulanova EA, Chaga OY, Vignjevic DM, Kojima S, Vasiliev JM, Borisy GG (2003) Mechanism of filopodia initiation by reorganization of a dendritic network. J Cell Biol 160: 409-421
50. Trichet L, Sykes C, Plastino J (2008) Relaxing the actin cytoskeleton for adhesion and movement with Ena/VASP. J Cell Biol 181: 19-25
51. Watanabe N, Madaule P, Reid T, Ishizaki T, Watanabe G, Kakizuka A, Saito Y, Nakao K, Jockusch BM, Narumiya S (1997) p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J 16: 3044-3056