Structure and function of the Arp2/3 complex

Current Opinion in Structural Biology

Volumn 12, Issue 6, 2002, Pages 768-774

  Pollard, Thomas D ^a   Beltzner, Christopher C ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; MYOSIN I; PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; BIOCHEMISTRY; CELL MOTILITY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; MACROMOLECULE; MOLECULAR WEIGHT; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SEQUENCE HOMOLOGY;

EID: 0036909561     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(02)00396-2     Document Type: Review

References (70)

1. Machesky L.M., Atkinson S.J., Ampe C., Vandekerckhove J., Pollard T.D. Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin agarose. J Cell Biol. 127:1994;107-115.
2. Balasubramanian M.K., Feoktistova A., McCollum D., Gould K.L. Fission yeast Sop2p: a novel and evolutionarily conserved protein that interacts with Arp3p and modulates profilin function. EMBO J. 15:1996;6426-6437.
3. Welch M.D., Iwamatsu A., Mitchison T.J. Actin polymerization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes. Nature. 385:1997;265-269.
4. Winter D., Podtelejnikov A.V., Mann M., Li R. The complex containing actin-related proteins Arp2 and Arp3 is required for the motility and integrity of yeast actin patches. Curr Biol. 7:1997;519-529.
5. Ma L., Rohatgi R., Kirschner M.W. The Arp2/3 complex mediates actin polymerization induced by the small GTP-binding protein Cdc42. Proc Natl Acad Sci USA. 95:1998;15362-15367.
6. Machesky L.M., Reeves E., Wientjes F., Mattheyse F.J., Grogan A., Totty N.F., Burlingame A.L., Hsuan J.J., Segal A.W. Mammalian actin-related protein 2/3 complex localizes to regions of lamellipodial protrusion and is composed of evolutionarily conserved proteins. Biochem J. 328:1997;105-112.
7. Kelleher J.F., Atkinson S.J., Pollard T.D. Sequences, structural models, and cellular localization of the actin-related proteins Arp2 and Arp3 from Acanthamoeba. J Cell Biol. 131:1995;385-397.
8. Welch M.D., DePace A.H., Verma S., Iwamatsu A., Mitchison T.J. The human Arp2/3 complex is composed of evolutionarily conserved subunits and is localized to cellular regions of dynamic actin filament assembly. J Cell Biol. 138:1997;375-384.
9. Mullins R.D., Heuser J.A., Pollard T.D. 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. 95:1998;6181-6186.
10. Blanchoin L., Amann K.J., Higgs H.N., Marchand J.B., Kaiser D.A., Pollard T.D. Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASp/Scar proteins. Nature. 404:2000;1007-1011.
11. Svitkina T.M., Verkhovsky A.B., McQuade K.M., Borisy G.G. Analysis of the actin-myosin II system in fish epidermal keratocytes: mechanism of cell body translocation. J Cell Biol. 139:1997;397-415.
12. Svitkina T.M., Borisy G.G. Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J Cell Biol. 145:1999;1009-1026.
13. Welch M.D., Rosenblatt J., Skoble J., Portnoy D.A., Mitchison T.J. Interaction of human Arp2/3 complex and the Listeria monocytogenes ActA protein in actin filament nucleation. Science. 281:1998;105-108.
14. Machesky L.M., Insall R.H. Scar1 and the related Wiskott-Aldrich syndrome protein WASP regulate the actin cytoskeleton through the Arp2/3 complex. Curr Biol. 8:1998;1347-1356.
15. Machesky L.M., Mullins D.M., Higgs H.N., Kaiser D.A., Blanchoin L., May R.C., Hall M.E., Pollard T.D. Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc Natl Acad Sci USA. 96:1999;3739-3744.
16. Rohatgi R., Ma L., Miki H., Lopez M., Kirchhausen T., Takenawa T., Kirschner M.W. The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell. 97:1999;221-231.
17. Yarar D., To W., Abo A., Welch M.D. The Wiskott-Aldrich syndrome protein directs actin-based motility by stimulating actin nucleation with the Arp2/3 complex. Curr Biol. 9:1999;555-558.
18. Winter D., Lechler T., Li R. Activation of the yeast Arp2/3 complex by Bee1p, a WASP-family protein. Curr Biol. 9:1999;501-504.
19. Egile C., Loisel T.P., Laurent V., Li R., Pantaloni D., Sansonetti P.J., Carlier M.F. 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. 146:1999;1319-1332.
20. Weaver A.M., Karginov A.V., Weed S.A., Li Y., Parsons J.T., Cooper J.A. Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr Biol. 11:2001;370-374. Cortactin is the first example of a new class of activity, the stabilization of branches by a protein that interacts with both actin filaments and the Arp2/3 complex.
21. Evangelista M., Klebl B.M., Tong A.H., Webb B.A., Leeuw T., Leberer E., Whiteway M., Thomas D.Y., Boone C. A role for myosin-I in actin assembly through interactions with Vrp1p, Bee1p, and the Arp2/3 complex. J Cell Biol. 148:2000;353-362.
22. Lechler T., Shevchenko A., Li R. Direct involvement of yeast type I myosins in Cdc42-dependent actin polymerization. J Cell Biol. 148:2000;363-373.
23. Lee W.L., Bezanilla M., Pollard T.D. Fission yeast myosin-I, Myo1p, stimulates actin assembly by Arp2/3 complex and shares functions with WASp. J Cell Biol. 151:2000;789-800.
24. Goode B.L., Rodal A.A., Barnes G., Drubin D.G. Activation of the Arp2/3 complex by the actin filament binding protein Abp1p. J Cell Biol. 153:2001;627-634.
25. Duncan M.C., Cope M.J., Goode B.L., Wendland B., Drubin D.G. Yeast Eps15-like endocytic protein, Pan1p, activates the Arp2/3 complex. Nat Cell Biol. 3:2001;687-690.
26. Higgs N.H., Pollard T.D. Regulation of actin filament network formation through Arp2/3 complex: activation by a diverse array of proteins. Annu Rev Biochem. 70:2001;649-676.
27. Higgs H.N., Blanchoin L., Pollard T.D. Influence of the Wiskott-Aldrich syndrome protein (WASp) C terminus and Arp2/3 complex on actin polymerization. Biochemistry. 38:1999;15212-15222.
28. Pantaloni D., Boujemaa R., Didry D., Gounon P., Carlier M.-F. The Arp2/3 complex branches filament barbed ends: functional antagonism with capping proteins. Nat Cell Biol. 2:2000;385-391.
29. Amann K.J., Pollard T.D. Direct real-time observation of actin filament branching mediated by Arp2/3 complex using total internal reflection microscopy. Proc Natl Acad Sci USA. 98:2001;15009-15013. Actin filament branching is observed directly for the first time, confirming a strong preference for the Arp2/3 complex to form branches on the sides of mother filaments.
30. Ichetovkin I., Grant W., 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. This paper presents evidence that branching mediated by the Arp2/3 complex is favored on the sides of recently polymerized actin filaments.
31. Fujiwara I., Suetsugu S., Uemura S., Takenawa T., Ishiwata S. Visualization and force measurement of branching by Arp2/3 complex and N-WASP in actin filament. Biochem Biophys Res Commun. 293:2002;1550-1555. A second evanescent wave study showing branching on the sides of mother actin filaments, as well as the first direct observation of actin filament treadmilling.
32. Marchand J.B., Kaiser D.A., Pollard T.D., Higgs H.N. Interaction of WASp/Scar proteins with actin and vertebrate Arp2/3 complex. Nat Cell Biol. 3:2001;76-82.
33. Higgs H.N., Pollard T.P. Wiskott-Aldrich Syndrome protein (WASp) activation of Arp2/3 complex: effects of phosphatidylinositol-4,5-bisphosphate and Cdc42. J Cell Biol. 150:2000;1311-1320.
34. Rohatgi R., Ho H.H., Kirschner M.W. Mechanism of N-WASP activation by CDC42 and phosphatidylinositol 4,5-bisphosphate. J Cell Biol. 150:2000;1299-1310.
35. Rohatgi R., Nollau P., Ho H.Y., Kirschner M.W., Mayer B.J. Nck and phosphatidylinositol 4,5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway. J Biol Chem. 276:2001;26448-26452.
36. Carlier M.F., Nioche P., Broutin-L'Hermite I., Boujemaa R., Le Clainche C., Egile C., Garbay C., Ducruix A., Sansonetti P.J., Pantaloni D. Grb2 links signalling to actin assembly by enhancing interaction of neural Wiskott-Aldrich Syndrome protein (N-WASP) with actin-related-protein (Arp2/3) complex. J Biol Chem. 275:2000;21946-21952.
37. Abdul-Manan N., Aghazadeh B., Liu G.A., Majumdar A., Ouerfelli O., Siminovitch K.A., Rosen M.K. Structure of Cdc42 in complex with the GTPase-binding domain of the 'Wiskott-Aldrich Syndrome' protein. Nature. 399:1999;379-383.
38. Kim A.S., Kakalis L.T., Abdul-Manan N., Liu G.A., Rosen M.K. Autoinhibition and activation mechanisms of the Wiskott-Aldrich Syndrome protein. Nature. 404:2000;151-158.
39. Svitkina T.M., Borisy G.G. Progress in protrusion: the tell-tale scar. Trends Biochem Sci. 24:1999;432-436.
40. Pollard T.D., Blanchoin L., Mullins R.D. Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys. 29:2000;545-576.
41. Loisel T.P., Boujemaa R., Pantaloni D., Carlier M.F. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature. 401:1999;613-616.
42. Maly I.V., Borisy G.G. Self-organization of a propulsive actin network as an evolutionary process. Proc Natl Acad Sci USA. 98:2001;11324-11329.
43. Carlsson A.E. Growth of branched actin networks against obstacles. Biophys J. 81:2002;1907-1923.
44. Mogilner A., Edelstein-Keshet L. Regulation of actin dynamics in rapidly moving cells: a quantitative analysis. Biophys J. 83:2002;1237-1258.
45. Hartwig J.H., Bokoch G.M., Carpenter C.L., Janmey P.A., Taylor L.A., Toker A., Stossel T.P. Thrombin receptor ligation and activated Rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets. Cell. 82:1995;643-653.
46. Chan A.Y., Bailly M., Zebda N., Segall J.E., Condeelis J.S. Role of cofilin in epidermal growth factor-stimulated actin polymerization and lamellipod protrusion. J Cell Biol. 148:2000;531-542.
47. McGrath J.L., Osborn E.A., Tardy Y.S., Dewey C.F., Hartwig J.H. Regulation of the actin cycle in vivo by actin filament severing. Proc Natl Acad Sci USA. 97:2000;6532-6537.
48. Flanagan L.A., Chou J., Falet H., Neujahr R., Hartwig J.H., Stossel T.P. Filamin A, the Arp2/3 complex, and the morphology and function of cortical actin filaments in human melanoma cells. J Cell Biol. 155:2001;511-517.
49. Mullins R.D., Stafford W.F., Pollard T.D. Structure, subunit topology, and actin-binding activity of the Arp2/3 complex from Acanthamoeba. J Cell Biol. 136:1997;331-343.
50. Mullins R.D., Kelleher J.F., Xu J., Pollard T.D. Arp2/3 complex from Acanthamoeba binds profilin and crosslinks actin filaments. Mol Biol Cell. 9:1998;841-852.
51. Zhao X., Yang Z., Qian M., Zhu X. Interactions among subunits of human Arp2/3 complex: p20-Arc as the hub. Biochem Biophys Res Com. 280:2001;513-517.
52. Morrell J.L., Morphew M., Gould K.L. A mutant of Arp2p causes partial disassembly of the Arp2/3 complex and loss of cortical actin function in fission yeast. Mol Biol Cell. 10:1999;4201-4215.
53. Winter D.C., Choe E.Y., Li R. Genetic dissection of the budding yeast Arp2/3 complex: a comparison of the in vivo and structural roles of individual subunits. Proc Natl Acad Sci USA. 96:1999;7288-7293.
54. Borths E.L., Welch M.D. Turning on the Arp2/3 complex at atomic resolution. Structure (Camb). 10:2002;131-135.
55. Volkmann N., Amann K.J., Stoilova-McPhie S., Egile C., Winter D.C., Hazelwood L., Heuser J.E., Li R., Pollard T.D., Hanein D. Structure of Arp2/3 complex in its activated state and in actin filament branch junctions. Science. 293:2001;2456-2459. Cryoelectronmicroscopy and image processing are used to reconstruct activated Arp2/3 complex in three dimensions and actin filament branches in two dimensions.
56. Robinson R.C., Turbedsky K., Kaiser D., Higgs H., Marchand J.B., Choe S., Pollard T.D. Crystal structure of Arp2/3 complex. Science. 294:2001;1679-1684. The crystal structure of the Arp2/3 complex at 2.0 Å resolution suggests a mechanism for activation.
57. Gournier H., Goley E.D., Niederstrasser H., Trinh T., Welch M.D. Reconstitution of human Arp2/3 complex reveals critical roles of individual subunits in complex structure and activity. Mol Cell. 8:2001;1041-1052. Expression, purification and characterization of combinations of Arp2/3 complex subunits revealed which subcomplexes are stable and active.
58. Schutt C., Myslik J.C., Rozychi M.D., Goonesekere N.C.W., Lindberg U. The structure of crystalline profilin-β-actin. Nature. 365:1993;810-816.
59. McLaughin P.J., Gooch J.T., Mannherz H.G., Weeds A.G. Structure of gelsolin segment 1-actin complex and the mechanism of filament severing. Nature. 364:1993;685-692.
60. Mullins R.D., Pollard T.D. Structure and function of the Arp2/3 complex. Curr Opin Struct Biol. 9:1999;244-249.
61. Zalevsky J., Grigorova I., Mullins R.D. Activation of the Arp2/3 complex by the Listeria ActA protein: ActA binds two actin monomers and three subunits of the Arp2/3 complex. J Biol Chem. 276:2001;3468-3475.
62. Zalevsky J., Lempert L., Kranitz H., Mullins R.D. Different WASP family proteins stimulate different ARP2/3 complex-dependent actin-nucleating activities. Curr Biol. 11:2001;1903-1913.
63. Le Clainche C., Didry D., Carlier M.-F., Pantaloni C. Activation of Arp2/3 complex by Wiskott-Aldrich syndrome protein is linked to enhanced binding of ATP to Arp2. J Biol Chem. 276:2001;46689-46692. Two initial studies (see also [64••]) of nucleotide binding to the Arp2/3 complex differ in some details, but agree that ATP hydrolysis is an important factor in actin filament nucleation by the Arp2/3 complex.
64. Dayel M.J., Holleran R.D., Mullins D.M. Arp2/3 complex requires hydrolyzable ATP for nucleation of new actin filaments. Proc Natl Acad Sci USA. 98:2001;14871-14876. See annotation to [63••].
65. Sept D., McCammon J.A. Thermodynamics and kinetics of actin filament nucleation. Biophys J. 81:2001;667-674.
66. Blanchoin L., Pollard T.D., Mullins R.D. Interaction of ADF/cofilin, Arp2/3 complex, capping protein and profilin in remodeling of branched actin filament networks. Curr Biol. 10:2000;1273-1282.
67. Bailly M., Ichetovkin I., Grant W., Zebda N., Machesky L.M., Segall J.E., Condeelis J. The F-actin side binding activity of the Arp2/3 complex is essential for actin nucleation and lamellipod extension. Curr Biol. 11:2001;620-625.
68. Miki H., Takenawa T. Direct binding of the verprolin-homology domain in N-WASP to actin is essential for cytoskeletal reorganization. Biochem Biophys Res Commun. 243:1998;73-78.
69. Lechler T., Jonsdottir G.A., Klee S.K., Pellman D., Li R. A two-tiered mechanism by which Cdc42 controls the localization and activation of an Arp2/3-activating motor complex in yeast. J Cell Biol. 155:2001;261-270.
70. Weaver A.M., Heuser J.E., Karginov A.V., Lee W.L., Parsons J.T., Cooper J.A. Interaction of cortactin and N-WASp with Arp2/3 complex. Curr Biol. 12:2002;1270-1278.