Arp2/3 complex-mediated actin polymerisation occurs on specific pre-existing networks in cells and requires spatial restriction to sustain functional lamellipod extension

Cell Motility and the Cytoskeleton

Volumn 63, Issue 7, 2006, Pages 395-414

  Shao, D ^a,c   Forge, A ^b   Munro, P M G ^a   Bailly, M ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Actin; Arp2 3 complex; Cytoskeleton ultrastructure; Lamellipod

Indexed keywords

ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MOTILITY; CELL ULTRASTRUCTURE; CHEMICAL COMPOSITION; CONTROLLED STUDY; CYTOSKELETON; LAMELLIPODIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; ACTINS; ANIMALS; BLOOD PLATELETS; CELL LINE, TUMOR; CYTOSKELETON; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT ANTIBODY TECHNIQUE; FLUORESCENT DYES; GLUTATHIONE TRANSFERASE; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICROINJECTIONS; MUSCLE, SKELETAL; POLYMERS; PROTEIN STRUCTURE, TERTIARY; PSEUDOPODIA; RABBITS; RATS; RECOMBINANT FUSION PROTEINS; RHODAMINES; WISKOTT-ALDRICH SYNDROME PROTEIN;

EID: 33745336497     PISSN: 08861544     EISSN: 10970169     Source Type: Journal    
DOI: 10.1002/cm.20131     Document Type: Article

References (39)

1. Anderson SI, Behrendt B, Machesky LM, Insall RH, Nash GB. 2003. Linked regulation of motility and integrin function in activated migrating neutrophils revealed by interference in remodelling of the cytoskeleton. Cell Motil Cytoskeleton 54:135-146.
2. Atilgan E, Wirtz D, Sun S. 2005. Morphology of the lamellipodium and organization of actin filaments at the leading edge of crawling cells. Biophys J 89:3589-3602.
3. Bailly M, Yan L, Whitesides GM, Condeelis JS, Segall JE. 1998. Regulation of protrusion shape and adhesion to the substratum during chemotactic responses of mammalian carcinoma cells. Exp Cell Res 241:285-299.
4. Bailly M, Macaluso F, Cammer M, Chan A, Segall JE, Condeelis JS. 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.
5. Bailly M, Wyckoff J, Bouzahzah B, Hammerman R, Sylvestre V, Cammer M, Pestell R, Segall JE. 2000. Epidermal growth factor receptor distribution during chemotactic responses. Mol Biol Cell 11:3873-3883.
6. Bailly M, Ichetovkin I, Grant W, Zebda N, Machesky LM, Segall JE, Condeelis J. 2001. The F-actin side binding activity of the Arp2/3 complex is essential for actin nucleation and lamellipod extension. Curr Biol 11:620-625.
7. 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.
8. Bernheim-Groswasser A, Wiesner S, Golsteyn RM, Carlier MF, Sykes C. 2002. The dynamics of actin-based motility depend on surface parameters. Nature 417:308-311.
9. Blanchoin L, Pollard TD, Mullins RD. 2000. Interactions of ADF/cofilin, Arp2/3 complex, capping protein and profilin in remodeling of branched actin filament networks. Curr Biol 10:1273-1282.
10. Chan AY, Raft S, Bailly M, Wyckoff JB, Segall JE, Condeelis JS. 1998. EGF stimulates an increase in actin nucleation and filament number at the leading edge of the lamellipod in mammary adenocarcinoma cells. J Cell Sci 111 (Part 2):199-211.
11. Chan AY, Bailly M, Zebda N, Segall JE, Condeelis JS. 2000. Role of cofilin in epidermal growth factor-stimulated actin polymerization and lamellipod protrusion. J Cell Biol 148:531-542.
12. Cramer LP. 1999. Role of actin-filament disassembly in lamellipodium protrusion in motile cells revealed using the drug jasplakinolide. Curr Biol 9:1095-1105.
13. Cramer LP, Briggs LJ, Dawe HR. 2002. Use of fluorescently labelled deoxyribonuclease I to spatially measure G-actin levels in migrating and non-migrating cells. Cell Motil Cytoskeleton 51:27-38.
14. DesMarais V, Ichetovkin I, Condeelis J, Hitchcock-DeGregori SE. 2002. Spatial regulation of actin dynamics: A tropomyosin-free, actin-rich compartment at the leading edge. J Cell Sci 115:4649-4660.
15. DesMarais V, Macaluso F, Condeelis J, Bailly M. 2004. Synergistic interaction between the Arp2/3 complex and cofilin drives stimulated lamellipod extension. J Cell Sci 117:3499-3510.
16. Falet H, Hoffmeister KM, Neujahr R, Italiano JE, Jr, Stossel TP, Southwick FS, Hartwig JH. 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.
17. Ghosh M, Song X, Mouneimne G, Sidani M, Lawrence DS, Condeelis JS. 2004. Cofilin promotes actin polymerization and defines the direction of cell motility. Science 304:743-746.
18. Gupton SL, Anderson KL, Kole TP, Fischer RS, Ponti A, Hitchcock-DeGregori SE, Danuser G, Fowler VM, Wirtz D, Hanein D, Waterman-Storer CM. 2005. Cell migration without a lamellipodium: Translation of actin dynamics into cell movement mediated by tropomyosin. J Cell Biol 168:619-631.
19. Hufner K, Higgs HN, Pollard TD, Jacobi C, Aepfelbacher M, Linder S. 2001. The verprolin-like central (vc) region of Wiskott-Aldrich syndrome protein induces Arp2/3 complex-dependent actin nucleation. J Biol Chem 276:35761-35767.
20. Ichetovkin I, Grant W, 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.
21. Le Clainche C, Pantaloni D, Carlier MF. 2003. ATP hydrolysis on actin-related protein 2/3 complex causes debranching of dendritic actin arrays. Proc Natl Acad Sci USA 100:6337-6342.
22. Linder S, Nelson D, Weiss M, Aepfelbacher M. 1999. Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc Natl Acad Sci USA 96:9648-9653.
23. Linder S, Higgs H, Hufner K, Schwarz K, Pannicke U, Aepfelbacher M. 2000. The polarization defect of Wiskott-Aldrich syndrome macrophages is linked to dislocalization of the Arp2/3 complex. J Immunol 165:221-225.
24. Lorenz M, Yamaguchi H, Wang Y, Singer RH, Condeelis J. 2004. Imaging sites of N-wasp activity in lamellipodia and invadopodia of carcinoma cells. Curr Biol 14:697-703.
25. Machesky LM, Insall RH. 1998. Scarl and the related Wiskott-Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr Biol 8:1347-1356.
26. Machesky LM, Mullins RD, Higgs HN, Kaiser DA, Blanchoin L, May RC, Hall ME, Pollard TD. 1999. Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc Natl Acad Sci USA 96:3739-3744.
27. Maly IV, Borisy GG. 2001. Self-organization of a propulsive actin network as an evolutionary process. Proc Natl Acad Sci USA 98:11324-11329.
28. Mejillano MR, Kojima S, Applewhite DA, Gertler FB, Svitkina TM, Borisy GG. 2004. Lamellipodial versus filopodial mode of the actin nanomachinery: Pivotal role of the filament barbed end. Cell 118:363-373.
29. Millard TH, Sharp SJ, Machesky LM. 2004. Signalling to actin assembly via the WASP (Wiskott-Aldrich syndrome protein)-family proteins and the Arp2/3 complex. Biochem J 380:1-17.
30. Pantaloni D, Boujemaa R, Didry D, Gounon P, Carlier MF. 2000. The Arp2/3 complex branches filament barbed ends: Functional antagonism with capping proteins. Nat Cell Biol 2:385-391.
31. Plastino J, Olivier S, Sykes C. 2004. Actin filaments align into hollow comets for rapid VASP-mediated propulsion. Curr Biol 14:1766-1771.
32. Pollard TD, Borisy GG. 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453-465.
33. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR. 2003. Cell migration: Integrating signals from front to back. Science 302:1704-1709.
34. Servant G, Weiner OD, Herzmark P, Balla T, Sedat JW, Bourne HR. 2000. Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 287:1037-1040.
35. Svitkina TM, Borisy GG. 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.
36. Vignjevic D, Yarar D, Welch MD, Peloquin J, Svitkina T, Borisy GG. 2003. Formation of filopodia-like bundles in vitro from a dendritic network. J Cell Biol 160:951-962.
37. Welch MD, Mullins RD. 2002. Cellular control of actin nucleation. Annu Rev Cell Dev Biol 18:247-288.
38. Wiesner S, Helfer E, Didry D, Ducouret G, Lafuma F, Carlier MF, Pantaloni D. 2003. A biomimetic motility assay provides insight into the mechanism of actin-based motility. J Cell Biol 160:387-398.
39. Zebda N, Bernard O, Bailly M, Welti S, Lawrence DS, Condeelis JS. 2000. Phosphorylation of ADF/cofilin abolishes EGF-induced actin nucleation at the leading edge and subsequent lamellipod extension. J Cell Biol 151:1119-1128.