The mechanical role of VASP in an Arp2/3-complex-based motility assay

Journal of Molecular Biology

Volumn 413, Issue 3, 2011, Pages 573-583

  Suei, Sandy ^a   Seyan, Rajveer ^a   Noguera, Philippe ^b   Manzi, John ^b   Plastino, Julie ^b   Kreplak, Laurent ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b CNRS   (France)

Author keywords

actin comets; atomic force microscopy; elastic modulus; mechanical properties; nanoindentation

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ANIMAL CELL; ATOMIC FORCE MICROSCOPY; COMET ASSAY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; YOUNG MODULUS;

LISTERIA;

EID: 80054705187     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.08.054     Document Type: Article

References (41)

1. Cameron L., Footer M., Van Oudenaarden A., and Theriot J. Motility of ActA protein-coated microspheres driven by actin polymerization Proc. Natl Acad. Sci. USA 96 1999 4908
2. Pollard T. Actin cytoskeleton: missing link for intracellular bacterial motility? Curr. Biol. 5 1995 837 840
3. Theriot J. The cell biology of infection by intracellular bacterial pathogens Annu. Rev. Cell Dev. Biol. 11 1995 213 239
4. Trichet L., Sykes C., and Plastino J. Relaxing the actin cytoskeleton for adhesion and movement with Ena/VASP J. Cell Biol. 181 2008 19
5. Loisel T., Boujemaa R., Pantaloni D., and Carlier M. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins Nature 401 1999 613 616
6. Plastino J., Olivier S., and Sykes C. Actin filaments align into hollow comets for rapid VASP-mediated propulsion Curr. Biol. 14 2004 1766 1771 (Pubitemid 39301167)
7. Trichet L., Campàs O., Sykes C., and Plastino J. VASP governs actin dynamics by modulating filament anchoring Biophys. J. 92 2007 1081 1089 (Pubitemid 46203237)
8. Plastino J., and Sykes C. The actin slingshot Curr. Opin. Cell Biol. 17 2005 62 66 (Pubitemid 40138089)
9. Boukellal H., Campás O., Joanny J., Prost J., and Sykes C. Soft Listeria: actin-based propulsion of liquid drops Phys. Rev. E 69 2004 61906
10. Giardini P., Fletcher D., and Theriot J. Compression forces generated by actin comet tails on lipid vesicles Proc. Natl Acad. Sci. USA 100 2003 6493
11. Taunton J., Rowning B., Coughlin M., Wu M., Moon R., Mitchison T., and Larabell C. Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-Wasp J. Cell Biol. 148 2000 519
12. Upadhyaya A., Chabot J., Andreeva A., Samadani A., and Van Oudenaarden A. Probing polymerization forces by using actin-propelled lipid vesicles Proc. Natl Acad. Sci. USA 100 2003 4521
13. Marcy Y., Prost J., Carlier M., and Sykes C. Forces generated during actin-based propulsion: a direct measurement by micromanipulation Proc. Natl Acad. Sci. 101 2004 5992
14. Gerbal F., Chaikin P., Rabin Y., and Prost J. An elastic analysis of Listeria monocytogenes propulsion Biophys. J. 79 2000 2259 2275
15. Barzik M., Kotova T., Higgs H., Hazelwood L., Hanein D., Gertler F., and Schafer D. Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins J. Biol. Chem. 280 2005 28653
16. Bear J., Svitkina T., Krause M., Schafer D., Loureiro J., and Strasser G. Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility Cell 109 2002 509 521 (Pubitemid 34564477)
17. Han Y., Chung C., Wessels D., Stephens S., Titus M., Soll D., and Firtel R. Requirement of a vasodilator-stimulated phosphoprotein family member for cell adhesion, the formation of filopodia, and chemotaxis in dictyostelium J. Biol. Chem. 277 2002 49877
18. Laurent V., Loisel T., Harbeck B., Wehman A., Gröbe L., and Jockusch B. Role of proteins of the Ena/VASP family in actin-based motility of Listeria monocytogenes J. Cell Biol. 144 1999 1245
19. Zhang Y., Tu Y., Gkretsi V., and Wu C. Migfilin interacts with vasodilator-stimulated phosphoprotein (VASP) and regulates VASP localization to cell-matrix adhesions and migration J. Biol. Chem. 281 2006 12397
20. Wiesner S., Helfer E., Didry D., Ducouret G., Lafuma F., Carlier M., and Pantaloni D. A biomimetic motility assay provides insight into the mechanism of actin-based motility J. Cell Biol. 160 2003 387
21. Samarin S., Romero S., Kocks C., Didry D., Pantaloni D., and Carlier M. How VASP enhances actin-based motility J. Cell Biol. 163 2003 131
22. Sampath P., and Pollard T. Effects of cytochalasin, phalloidin and pH on the elongation of actin filaments Biochemistry 30 1991 1973 1980
23. Isambert H., Venier P., Maggs A.C., Fattoum A., Kassab R., Pantaloni D., and Carlier M.F. Flexibility of actin filaments derived from thermal fluctuations. Effect of bound nucleotide, phalloidin, and muscle regulatory proteins J. Biol. Chem. 270 1995 11437
24. Ichetovkin I., Grant W., and Condeelis J. Cofilin produces newly polymerized actin filaments that are preferred for dendritic nucleation by the Arp2/3 complex Curr. Biol. 12 2002 79 84 (Pubitemid 34063358)
25. Pfaendtner J., Branduardi D., Parrinello M., Pollard T.D., and Voth G.A. Nucleotide-dependent conformational states of actin Proc. Natl Acad. Sci. 106 2009 12723
26. Nakamura F., Osborn E., Janmey P.A., and Stossel T.P. Comparison of filamin A-induced cross-linking and Arp2/3 complex-mediated branching on the mechanics of actin filaments J. Biol. Chem. 277 2002 9148 9154 (Pubitemid 34952992)
27. Paluch E., van der Gucht J., Joanny J., and Sykes C. Deformations in actin comets from rocketing beads Biophys. J. 91 2006 3113 3122 (Pubitemid 44526500)
28. Abraham V.C., Krishnamurthi V., Taylor D.L., and Lanni F. The actin-based nanomachine at the leading edge of migrating cells Biophys. J. 77 1999 1721 1732 (Pubitemid 29407343)
29. MacKintosh F.C., Kas J., and Janmey P.A. Elasticity of semiflexible biopolymer networks Phys. Rev. Lett. 75 1995 4425 4428
30. Skoble J., Auerbuch V., Goley E.D., Welch M.D., and Portnoy D.A. Pivotal role of VASP in Arp2/3 complex-mediated actin nucleation, actin branch-formation, and Listeria monocytogenes motility J. Cell Biol. 155 2001 89 100 (Pubitemid 34286210)
31. Tseng Y., and Wirtz D. Dendritic branching and homogenization of actin networks mediated by Arp2/3 complex Phys. Rev. Lett. 93 2004 258104
32. Breitsprecher D., Kiesewetter A.K., Linkner J., Vinzenz M., Stradal T.E.B., and Small J.V. Molecular mechanism of Ena/VASP-mediated actin-filament elongation EMBO J. 30 2011 456 467
33. Hansen S.D., and Mullins R.D. VASP is a processive actin polymerase that requires monomeric actin for barbed end association J. Cell Biol. 191 2010 571 584
34. Huttelmaier S., Harbeck B., Steffens O., Messerschmidt T., Illenberger S., and Jockusch B.M. Characterization of the actin binding properties of the vasodilator-stimulated phosphoprotein VASP FEBS Lett. 451 1999 68 74 (Pubitemid 29236174)
35. Schirenbeck A., Arasada R., Bretschneider T., Stradal T.E.B., Schleicher M., and Faix J. The bundling activity of vasodilator-stimulated phosphoprotein is required for filopodium formation Proc. Natl Acad. Sci. USA 103 2006 7694 7699
36. Rottner K., Behrendt B., Small J.V., and Wehland J. VASP dynamics during lamellipodia protrusion Nat. Cell Biol. 1 1999 321 322 (Pubitemid 129495784)
37. Golsteyn R., Beckerle M., Koay T., and Friederich E. Structural and functional similarities between the human cytoskeletal protein zyxin and the ActA protein of Listeria monocytogenes J. Cell Sci. 110 1997 1893
38. Schafer D., Jennings P., and Cooper J. Dynamics of capping protein and actin assembly in vitro: uncapping barbed ends by polyphosphoinositides J. Cell Biol. 135 1996 169
39. Sneddon I. The relation between load and penetration in the axisymmetric Boussinesq problem for a punch of arbitrary profile Int. J. Eng. Sci. 3 1965 47 57
40. Bueckle H. The Science of Hardness Testing and Its Research Applications 1973 American Society for Metals Materials Park, OH
41. Persch G., Born C., and Utesch B. Nano-hardness investigations of thin films by an atomic force microscope Microelectron. Eng. 24 1994 113 121