Three-dimensional reconstructions of Arp2/3 complex with bound nucleation promoting factors

EMBO Journal

Volumn 31, Issue 1, 2012, Pages 236-247

  Xu, Xiao Ping ^a   Rouiller, Isabelle ^a,d   Slaughter, Brian D ^b   Egile, Coumaran ^b,e   Kim, Eldar ^a,f   Unruh, Jay R ^b   Fan, Xiaoxue ^b   Pollard, Thomas D ^c   Li, Rong ^b   Hanein, Dorit ^a   Volkmann, Niels ^a  

^a BURNHAM INSTITUTE   (United States)

^b STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c YALE UNIVERSITY   (United States)

^d MCGILL UNIVERSITY   (Canada)

^e Experimental Therapeutics and Translational Research Oncology   (France)

^f MSM Protein Technologies   (United States)

Author keywords

actin cytoskeleton; cell motility; docking; electron microscopy; image analysis

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN; ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 2-3 COMPLEX; CORTACTIN; NUCLEATION PROMOTING FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE;

ACANTHAMOEBA; ACTIN-RELATED PROTEIN 2; ACTIN-RELATED PROTEIN 3; BINDING SITES; FUNGAL PROTEINS; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTOZOAN PROTEINS; SACCHAROMYCETALES; WISKOTT-ALDRICH SYNDROME PROTEIN FAMILY;

EID: 84855359693     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.343     Document Type: Article

References (49)

1. Achard V, Martiel JL, Michelot A, Guerin C, Reymann AC, Blanchoin L, Boujemaa-Paterski R (2010) A 'primer'-based mechanism underlies branched actin filament network formation and moti-lity. Curr Biol 20: 423-428
2. Aguda AH, Burtnick LD, Robinson RC (2005) The state of the filament. EMBO Rep 6: 220-226 (Pubitemid 40485616)
3. Bacia K, Schwille P (2007) Practical guidelines for dual-color fluorescence cross-correlation spectroscopy. Nat Protoc 2: 2842-2856
4. Beltzner CC, Pollard TD (2004) Identification of functionally important residues of Arp2/3 complex by analysis of homology models from diverse species. J Mol Biol 336: 551-565 (Pubitemid 38147646)
5. Blanchoin L, Amann KJ, Higgs HN, Marchand JB, Kaiser DA, Pollard TD (2000) Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins. Nature 404: 1007-1011 (Pubitemid 30243596)
6. Boczkowska M, Rebowski G, Petoukhov MV, Hayes DB, Svergun DI, Dominguez R (2008) X-ray scattering study of activated Arp2/3 complex with bound actin-WCA. Structure 16: 695-704 (Pubitemid 351626898)
7. Chereau D, Kerff F, Graceffa P, Grabarek Z, Langsetmo K, Dominguez R (2005) Actin-bound structures of Wiskott-Aldrich syndrome protein (WASP)-homology domain 2 and the implications for filament assembly. Proc Natl Acad Sci USA 102: 16644-16649 (Pubitemid 41688830)
8. Ducka AM, Joel P, Popowicz GM, Trybus KM, Schleicher M, Noegel AA, Huber R, Holak TA, Sitar T (2010) Structures of actin-bound Wiskott-Aldrich syndrome protein homology 2 (WH2) domains of Spire and the implication for filament nucleation. Proc Natl Acad Sci USA 107 : 11757-11762
9. Egile C, Loisel TP, Laurent V, Li R, Pantaloni D, Sansonetti PJ, Carlier MF (1999) 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: 1319-1332 (Pubitemid 29477698)
10. Egile C, Rouiller I, Xu XP, Volkmann N, Li R, Hanein D (2005) Mechanism of filament nucleation and branch stability revealed by the structure of the Arp2/3 complex at actin branch junctions. PLoS Biol 3: e383
11. Goley ED, Rodenbusch SE, Martin AC, Welch MD (2004) Critical conformational changes in the Arp2/3 complex are induced by nucleotide and nucleation promoting factor. Mol Cell 16: 269-279 (Pubitemid 39388841)
12. Henderson R (1995) The potential and limitations of neutrons, electrons and X-ray for atomic resolution microscopy of unstained biological molecules. Q Rev Biophys 28: 171-194
13. Hohn M, Tang G, Goodyear G, Baldwin PR, Huang Z, Penczek PA, Yang C, Glaeser RM, Adams PD, Ludtke SJ (2007) SPARX, a new environment for Cryo-EM image processing. J Struct Biol 157: 47-55 (Pubitemid 44880795)
14. Janssen ME, Kim E, Liu H, Fujimoto LM, Bobkov A, Volkmann N, Hanein D (2006) Three-dimensional structure of vinculin bound to actin filaments. Mol Cell 21: 271-281 (Pubitemid 43099942)
15. Kelleher JF, Atkinson SJ, Pollard TD (1995) Sequences, structural models, and cellular localization of the actin-related proteins Arp2 and Arp3 from Acanthamoeba. J Cell Biol 131: 385-397
16. Kelly AE, Kranitz H, Dotsch V, Mullins RD (2006) Actin binding to the central domain of WASP/Scar proteins plays a critical role in the activation of the Arp2/3 complex. J Biol Chem 281: 10589-10597 (Pubitemid 43864601)
17. Kreishman-Deitrick M, Goley ED, Burdine L, Denison C, Egile C, Li R, Murali N, Kodadek TJ, Welch MD, Rosen MK (2005) NMR analyses of the activation of the Arp2/3 complex by neuronal Wiskott-Aldrich syndrome protein. Biochemistry 44: 15247-15256 (Pubitemid 41681459)
18. Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82-97 (Pubitemid 30013436)
19. 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 (Pubitemid 29168980)
20. Marchand JB, Kaiser DA, Pollard TD, Higgs HN (2001) Interaction of WASP/Scar proteins with actin and vertebrate Arp2/3 complex. Nat Cell Biol 3: 76-82 (Pubitemid 32114835)
21. Martin AC, Xu XP, Rouiller I, Kaksonen M, Sun Y, Belmont L, Volkmann N, Hanein D, Welch M, Drubin DG (2005) Effects of Arp2 and Arp3 nucleotide-binding pocket mutations on Arp2/3 complex function. J Cell Biol 168: 315-328 (Pubitemid 40248228)
22. Muller JD (2004) Cumulant analysis in fluorescence fluctuation spectroscopy. Biophys J 86: 3981-3992 (Pubitemid 38780274)
23. Mullins RD, Heuser JA, Pollard TD (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 (Pubitemid 28248985)
24. Nolen BJ, Littlefield RS, Pollard TD (2004) Crystal structures of actin-related protein 2/3 complex with bound ATP or ADP. Proc Natl Acad Sci USA 101 : 15627-15632 (Pubitemid 39473538)
25. Nolen BJ, Pollard TD (2007) Insights into the influence of nucleo-tides on actin family proteins from seven structures of Arp2/3 complex. Mol Cell 26: 449-457 (Pubitemid 46687105)
26. Nolen BJ, Pollard TD (2008) Structure and biochemical properties of fission yeast Arp2/3 complex lacking the Arp2 subunit. J Biol Chem 283: 26490-26498
27. Ohi M, Li Y, Cheng Y, Walz T (2004) Negative staining and image classification-powerful tools in modern electron microscopy. Biol Proced Online 6: 23-34 (Pubitemid 38597695)
28. Padrick SB, Doolittle LK, Brautigam CA, King DS, Rosen MK (2011) Arp2/3 complex is bound and activated by two WASP proteins. Proc Natl Acad Sci USA 108: E472-E479
29. Pan F, Egile C, Lipkin T, Li R (2004) ARPC1/Arc40 mediates the interaction of the actin-related protein 2 and 3 complex with Wiskott-Aldrich syndrome protein family activators. J Biol Chem 279: 54629-54636 (Pubitemid 40053206)
30. Pant K, Chereau D, Hatch V, Dominguez R, Lehman W (2006) Cortactin binding to F-actin revealed by electron microscopy and 3D reconstruction. J Mol Biol 359: 840-847 (Pubitemid 43831917)
31. Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112: 453-465 (Pubitemid 36263079)
32. Robinson RC, Turbedsky K, Kaiser DA, Marchand JB, Higgs HN, Choe S, Pollard TD (2001) Crystal structure of Arp2/3 complex. Science 294: 1679-1684 (Pubitemid 33104831)
33. Rodal AA, Sokolova O, Robins DB, Daugherty KM, Hippenmeyer S, Riezman H, Grigorieff N, Goode BL (2005) Conformational changes in the Arp2/3 complex leading to actin nucleation. Nat Struct Mol Biol 12: 26-31 (Pubitemid 40082913)
34. Rouiller I, Xu XP, Amann KJ, Egile C, Nickell S, Nicastro D, Li R, Pollard TD, Volkmann N, Hanein D (2008) The structural basis of actin filament branching by Arp2/3 complex. J Cell Biol 180: 887-895 (Pubitemid 351398416)
35. Spahn CM, Penczek PA (2009) Exploring conformational modes of macromolecular assemblies by multiparticle cryo-EM. Curr Opin Struct Biol 19: 623-631
36. Sweeney HL, Houdusse A (2004) The motor mechanism of myosin V: insights for muscle contraction. Philos Trans R Soc Lond B Biol Sci 359: 1829-1841 (Pubitemid 40199230)
37. Ti SC, Jurgenson C, Nolen BJ, Pollard TD (2011) Structural and biochemical characterization of two binding sites for nucleation promoting factor WASp-VCA on Arp2/3 complex. Proc Natl Acad Sci USA 108: E463-E471
38. Volkmann N (2002) A novel three-dimensional variant of the watershed transform for segmentation of electron density maps. J Struct Biol 138: 123
39. Volkmann N (2009) Confidence intervals for fitting of atomic models into low-resolution densities. Acta Crystallogr D Biol Crystallogr 65: 679-689
40. Volkmann N, Amann KJ, Stoilova-McPhie S, Egile C, Winter DC, Hazelwood L, Heuser JE, Li R, Pollard TD, Hanein D (2001) Structure of Arp2/3 complex in its activated state and in actin filament branch junctions. Science 293: 2456-2459 (Pubitemid 32917327)
41. Volkmann N, Hanein D (1999) Quantitative fitting of atomic models into observed densities derived by electron microscopy. J Struct Biol 125: 176-184 (Pubitemid 29402602)
42. Volkmann N, Hanein D (2003) Docking of atomic models into reconstructions from electron microscopy. Methods Enzymol 374: 204-225 (Pubitemid 37547910)
43. Volkmann N, Hanein D, Ouyang G, Trybus KM, DeRosier DJ, Lowey S (2000) Evidence for cleft closure in actomyosin upon ADP release. Nat Struct Biol 7: 1147-1155
44. Volkmann N, Liu H, Hazelwood L, Krementsova EB, Lowey S, Trybus KM, Hanein D (2005) The structural basis of myosin V processive movement as revealed by electron cryomicroscopy. Mol Cell 19: 595-605 (Pubitemid 41219436)
45. Weaver AM, Karginov AV, Kinley AW, Weed SA, Li Y, Parsons JT, Cooper JA (2001) Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr Biol 11 : 370-374 (Pubitemid 32200742)
46. Weed SA, Karginov AV, Schafer DA, Weaver AM, Kinley AW, Cooper JA, Parsons JT (2000) Cortactin localization to sites of actin assembly in lamellipodia requires interactions with F-actin and the Arp2/3 complex. J Cell Biol 151: 29-40
47. Winter D, Lechler T, Li R (1999) Activation of the yeast Arp2/3 complex by Bee1p, a WASP-family protein. Curr Biol 9: 501-504 (Pubitemid 29228625)
48. Zalevsky J, Lempert L, Kranitz H, Mullins RD (2001) Different WASP family proteins stimulate different Arp2/3 complex-dependent actin-nucleating activities. Curr Biol 11 : 1903-1913 (Pubitemid 33146416)
49. Zencheck WD, Xiao H, Nolen BJ, Angeletti RH, Pollard TD, Almo SC (2009) Nucleotide-and activator-dependent structural and dynamic changes of arp2/3 complex monitored by hydrogen/deuterium exchange and mass spectrometry. J Mol Biol 390: 414-427