Ena/VASP: Towards resolving a pointed controversy at the barbed end

Journal of Cell Science

Volumn 122, Issue 12, 2009, Pages 1947-1953

  Bear, James E ^a   Gertler, Frank B ^b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Actin; Capping; Ena VASP; Filopodia; Lamellipodia; Mena; VASP

Indexed keywords

ACTIN; ACTIN CAPPING PROTEIN; ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; G ACTIN; METHENAMINE; PROFILIN; VASODILATOR STIMULATED PHOSPHOPROTEIN; DNA BINDING PROTEIN; ENA/VASP PROTEINS;

ACTIN POLYMERIZATION; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; BIOLOGICAL ACTIVITY; BRANCHING MORPHOGENESIS; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CYTOSKELETON; FILOPODIUM; LAMELLIPODIUM; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; CONFLICT; DRUG ANTAGONISM; HUMAN; METABOLISM; MICROFILAMENT; PHYSIOLOGY; PROTEIN MULTIMERIZATION; REVIEW;

ACTIN CAPPING PROTEINS; ANIMALS; CYTOSKELETON; DISSENT AND DISPUTES; DNA-BINDING PROTEINS; HUMANS; MICROFILAMENTS; MODELS, BIOLOGICAL; PROTEIN MULTIMERIZATION;

EID: 68949183227     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.038125     Document Type: Article

References (58)

1. Akin, O. and Mullins, R. D. (2008). Capping protein increases the rate of actin-based motility by promoting filament nucleation by the Arp2/3 complex. Cell 133, 841-851.
2. Applewhite, D. A., Barzik, M., Kojima, S., Svitkina, T. M., Gertler, F. B. and Borisy, G. G. (2007). Ena/VASP proteins have an anti-capping independent function in filopodia formation. Mol. Biol. Cell 18, 2579-2591.
3. Aszodi, A., Pfeifer, A., Ahmad, M., Glauner, M., Zhou, X. H., Ny, L., Andersson, K. E., Kehrel, B., Offermanns, S. and Fassler, R. (1999). The vasodilator-stimulated phosphoprotein (VASP) is involved in cGMP- and cAMP-mediated inhibition of agonist-induced platelet aggregation, but is dispensable for smooth muscle function. EMBO J. 18, 37-48.
4. 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.
5. Bailly, M., Macaluso, F., Cammer, M., Chan, A., Segall, J. E. and Condeelis, J. S. (1999). Relationship between Arp2/3 complex and the barbed ends of actin filaments at the leading edge of carcinoma cells after epidermal growth factor stimulation. J. Cell Biol. 145, 331-345.
6. Barzik, M., Kotova, T. I., Higgs, H. N., Hazelwood, L., Hanein, D., Gertler, F. B. and Schafer, D. A. (2005). Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins. J. Biol. Chem. 280, 28653-28662.
7. Bear, J. E., Loureiro, J. J., Libova, I., Fassler, R., Wehland, J. and Gertler, F. B. (2000). Negative regulation of fibroblast motility by Ena/VASP proteins. Cell 101, 717-728.
8. 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. (2002). Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109, 509-521.
9. 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, 100-1011.
10. Boujemaa-Paterski, R., Gouin, E., Hansen, G., Samarin, S., Le Clainche, C., Didry, D., Dehoux, P., Cossart, P., Kocks, C., Carlier, M. F. et al. (2001). Listeria protein ActA mimics WASp family proteins: it activates filament barbed end branching by Arp2/3 complex. Biochemistry 40, 11390-11404.
11. Breitsprecher, D., Kiesewetter, A. K., Linkner, J., Urbanke, C., Resch, G. P., Small, J. V. and Faix, J. (2008). Clustering of VASP actively drives processive, WH2 domain-mediated actin filament elongation. EMBO J. 27, 2943-2954.
12. Chereau, D. and Dominguez, R. (2006). Understanding the role of the G-actin-binding domain of Ena/VASP in actin assembly. J. Struct. Biol. 155, 195-201.
13. Chhabra, E. S. and Higgs, H. N. (2007). The many faces of actin: matching assembly factors with cellular structures. Nat. Cell Biol. 9, 1110-1121.
14. 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. (2007). Filopodia are required for cortical neurite initiation. Nat. Cell Biol. 9, 1347-1359.
15. DiNubile, M. J., Cassimeris, L., Joyce, M. and Zigmond, S. H. (1995). Actin filament barbed-end capping activity in neutrophil lysates: the role of capping protein-beta 2. Mol. Biol. Cell 6, 1659-1671.
16. Ferron, F., Rebowski, G., Lee, S. H. and Dominguez, R. (2007). Structural basis for the recruitment of profilin-actin complexes during filament elongation by Ena/VASP. EMBO J. 26, 4597-4606.
17. Furman, C., Sieminski, A. L., Kwiatkowski, A. V., Rubinson, D. A., Vasile, E., Bronson, R. T., Fassler, R. and Gertler, F. B. (2007). Ena/VASP is required for endothelial barrier function in vivo. J. Cell Biol. 179, 761-775.
18. Gates, J., Mahaffey, J. P., Rogers, S. L., Emerson, M., Rogers, E. M., Sottile, S. L., Van Vactor, D., Gertler, F. B. and Peifer, M. (2007). Enabled plays key roles in embryonic epithelial morphogenesis in Drosophila. Development 134, 2027-2039.
19. Gertler, F. B., Niebuhr, K., Reinhard, M., Wehland, J. and Soriano, P. (1996). Mena, a relative of VASP and Drosophila Enabled, is implicated in the control of microfilament dynamics. Cell 87, 227-239.
20. Gupton, S. L. and Gertler, F. B. (2007). Filopodia: the fingers that do the walking. Sci STKE 2007, re5.
21. Harbeck, B., Huttelmaier, S., Schluter, K., Jockusch, B. M. and Illenberger, S. (2000). Phosphorylation of the vasodilator-stimulated phosphoprotein regulates its interaction with actin. J. Biol. Chem. 275, 30817-30825.
22. Hauser, W., Knobeloch, K. P., Eigenthaler, M., Gambaryan, S., Krenn, V., Geiger, J., Glazova, M., Rohde, E., Horak, I., Walter, U. et al. (1999). Megakaryocyte hyperplasia and enhanced agonist-induced platelet activation in vasodilator-stimulated phosphoprotein knockout mice. Proc. Natl. Acad. Sci. USA 96, 8120-8125.
23. Huttelmaier, S., Harbeck, B., Steffens, O., Messerschmidt, T., Illenberger, S. and Jockusch, B. M. (1999). Characterization of the actin binding properties of the vasodilator-stimulated phosphoprotein VASP. FEBS Lett. 451, 68-74.
24. Ichetovkin, I., Grant, W. and Condeelis, J. (2002). Cofilin produces newly polymerized actin filaments that are preferred for dendritic nucleation by the Arp2/3 complex. Curr. Biol. 12, 79-84.
25. Krause, M., Dent, E. W., Bear, J. E., Loureiro, J. J. and Gertler, F. B. (2003). Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu. Rev. Cell Dev. Biol. 19, 541-564.
26. Krause, M., Leslie, J. D., Stewart, M., Lafuente, E. M., Valderrama, F., Jagannathan, R., Strasser, G. A., Rubinson, D. A., Liu, H., Way, M. et al. (2004). Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics. Dev. Cell 7, 571-583.
27. Kuhnel, K., Jarchau, T., Wolf, E., Schlichting, I., Walter, U., Wittinghofer, A. and Strelkov, S. V. (2004). The VASP tetramerization domain is a right-handed coiled coil based on a 15-residue repeat. Proc. Natl. Acad. Sci. USA 101, 17027-17032.
28. 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. (2007). Ena/VASP Is Required for neuritogenesis in the developing cortex. Neuron 56, 441-455.
29. Lacayo, C. I., Pincus, Z., VanDuijn, M. M., Wilson, C. A., Fletcher, D. A., Gertler, F. B., Mogilner, A. and Theriot, J. A. (2007). Emergence of large-scale cell morphology and movement from local actin filament growth dynamics. PLoS Biol. 5, e233.
30. Lambrechts, A., Kwiatkowski, A. V., Lanier, L. M., Bear, J. E., Vandekerckhove, J., Ampe, C. and Gertler, F. B. (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.
31. Lambrechts, A., Gevaert, K., Cossart, P., Vandekerckhove, J. and Van Troys, M. (2008). Listeria comet tails: the actin-based motility machinery at work. Trends Cell Biol. 18, 220-227.
32. Lanier, L. M., Gates, M. A., Witke, W., Menzies, A. S., Wehman, A. M., Macklis, J. D., Kwiatkowski, D., Soriano, P. and Gertler, F. B. (1999). Mena is required for neurulation and commissure formation. Neuron 22, 313-325.
33. 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.
34. 2+ switch. Am. J. Physiol. Cell Physiol. 282, C1235-C1245.
35. Lebrand, C., Dent, E. W., Strasser, G. A., Lanier, L. M., Krause, M., Svitkina, T. M., Borisy, G. G. and Gertler, F. B. (2004). Critical role of Ena/VASP proteins for filopodia formation in neurons and in function downstream of netrin-1. Neuron 42, 37-49.
36. Lindsay, S. L., Ramsey, S., Aitchison, M., Renne, T. and Evans, T. J. (2007). Modulation of lamellipodial structure and dynamics by NO-dependent phosphorylation of VASP Ser239. J. Cell Sci. 120, 3011-3021.
37. Massberg, S., Gruner, S., Konrad, I., Garcia Arguinzonis, M. I., Eigenthaler, M., Hemler, K., Kersting, J., Schulz, C., Muller, I., Besta, F. et al. (2004). Enhanced in vivo platelet adhesion in vasodilator-stimulated phosphoprotein (VASP)-deficient mice. Blood 103, 136-142.
38. Matusek, T., Gombos, R., Szecsenyi, A., Sanchez-Soriano, N., Czibula, A., Pataki, C., Gedai, A., Prokop, A., Rasko, I. and Mihaly, J. (2008). Formin proteins of the DAAM subfamily play a role during axon growth. J. Neurosci. 28, 13310-13319.
39. 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.
40. Menzies, A. S., Aszodi, A., Williams, S. E., Pfeifer, A., Wehman, A. M., Goh, K. L., Mason, C. A., Fassler, R. and Gertler, F. B. (2004). Mena and vasodilator-stimulated phosphoprotein are required for multiple actin-dependent processes that shape the vertebrate nervous system. J. Neurosci. 24, 8029-8038.
41. Mogilner, A. (2006). On the edge: modeling protrusion. Curr. Opin. Cell Biol. 18, 32-39.
42. Mogilner, A. and Oster, G. (2003). Force generation by actin polymerization II: the elastic ratchet and tethered filaments. Biophys. J. 84, 1591-1605.
43. Mullins, R. D., Heuser, J. A. and Pollard, T. D. (1998). The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc. Natl. Acad. Sci. USA 95, 6181-6186.
44. Pasic, L., Kotova, T. and Schafer, D. A. (2008). Ena/VASP proteins capture actin filament barbed ends. J. Biol. Chem. 283, 9814-9819.
45. Pistor, S., Grobe, L., Sechi, A. S., Domann, E., Gerstel, B., Machesky, L. M., Chakraborty, T. and Wehland, J. (2000). Mutations of arginine residues within the 146-KKRRK-150 motif of the ActA protein of Listeria monocytogenes abolish intracellular motility by interfering with the recruitment of the Arp2/3 complex. J. Cell Sci. 113, 3277-3287.
46. Plastino, J., Olivier, S. and Sykes, C. (2004). Actin filaments align into hollow comets for rapid VASP-mediated propulsion. Curr. Biol. 14, 1766-1771.
47. Pollard, T. D. and Borisy, G. G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
48. Purich, D. L. and Southwick, F. S. (1997). ABM-1 and ABM-2 homology sequences: consensus docking sites for actin-based motility defined by oligoproline regions in Listeria ActA surface protein and human VASP. Biochem. Biophys. Res. Commun. 231, 686-691.
49. Reinhard, M., Halbrugge, M., Scheer, U., Wiegand, C., Jockusch, B. M. and 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.
50. Samarin, S., Romero, S., Kocks, C., Didry, D., Pantaloni, D. and Carlier, M. F. (2003). How VASP enhances actin-based motility. J. Cell Biol. 163, 131-142.
51. Schirenbeck, A., Arasada, R., Bretschneider, T., Stradal, T. E., Schleicher, M. and Faix, J. (2006). The bundling activity of vasodilator-stimulated phosphoprotein is required for filopodium formation. Proc. Natl. Acad. Sci. USA 103, 7694-7699.
52. Scott, J. A., Shewan, A. M., den Elzen, N. R., Loureiro, J. J., Gertler, F. B. and Yap, A. S. (2006). Ena/VASP proteins can regulate distinct modes of actin organization at cadherin-adhesive contacts. Mol. Biol. Cell 17, 1085-1095.
53. 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.
54. Smith, G. A., Theriot, J. A. and Portnoy, D. A. (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.
55. Svitkina, T. M. and Borisy, G. G. (1999). 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.
56. Svitkina, T. M., Bulanova, E. A., Chaga, O. Y., Vignjevic, D. M., Kojima, S., Vasiliev, J. M. and Borisy, G. G. (2003). Mechanism of filopodia initiation by reorganization of a dendritic network. J. Cell Biol. 160, 409-421.
57. Vasioukhin, V., Bauer, C., Yin, M. and Fuchs, E. (2000). Directed actin polymerization is the driving force for epithelial cell- cell adhesion. Cell 100, 209-219.
58. Vignjevic, D., Yarar, D., Welch, M. D., Peloquin, J., Svitkina, T. and Borisy, G. G. (2003). Formation of filopodia-like bundles in vitro from a dendritic network. J. Cell Biol. 160, 951-962.