Key structural features of the actin filament Arp2/3 complex branch junction revealed by molecular simulation

Journal of Molecular Biology

Volumn 416, Issue 1, 2012, Pages 148-161

  Pfaendtner, Jim ^a   Volkmann, Niels ^b   Hanein, Dorit ^b   Dalhaimer, Paul ^c,d   Pollard, Thomas D ^c   Voth, Gregory A ^e  

^a University of Washington   (United States)

^b BURNHAM INSTITUTE   (United States)

^c YALE UNIVERSITY   (United States)

^d University of Tennessee   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

Author keywords

actin; Arp2 3 complex; cytoskeleton; molecular dynamics

Indexed keywords

ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 2-3 COMPLEX; ACTIN RELATED PROTEIN 3; BRIDGED COMPOUND; DEOXYRIBONUCLEASE; SODIUM CHLORIDE;

ACTIN FILAMENT; ARTICLE; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; ENZYME BINDING; HYDROPHOBICITY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN SUBUNIT;

EID: 84856498983     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.12.025     Document Type: Article

References (43)

1. Pollard T.D. Regulation of actin filament assembly by Arp2/3 complex and formins Annu. Rev. Biophys. Biomol. Struct. 36 2007 451 477 (Pubitemid 47007562)
2. Dayel M.J., Holleran E.A., and Mullins R.D. Arp2/3 complex requires hydrolyzable ATP for nucleation of new actin filaments Proc. Natl Acad. Sci. USA 98 2001 14871 14876 (Pubitemid 34013937)
3. Nolen B.J., and Pollard T.D. Insights into the influence of nucleotides on actin family proteins from seven structures of Arp2/3 complex Mol. Cell 26 2007 449 457 (Pubitemid 46687105)
4. Kiselar J.G., Mahaffy R., Pollard T.D., and Almo S.C. Visualizing Arp2/3 complex activation mediated by binding of ATP and WASp using structural mass spectrometry Proc. Natl Acad. Sci. USA 104 2007 1552 1557 (Pubitemid 46214628)
5. Robinson R.C., Turbedsky K., Kaiser D.A., Marchand J.B., Higgs H.N., Choe S., and Pollard T.D. Crystal structure of Arp2/3 complex Science 294 2001 1679 1684 (Pubitemid 33104831)
6. Nolen B.J., Littlefield R.S., and Pollard T.D. Crystal structures of actin-related protein 2/3 complex with bound ATP or ADP Proc. Natl Acad. Sci. USA 101 2004 15627 15632 (Pubitemid 39473538)
7. Nolen B.J., and Pollard T.D. Structure and biochemical properties of fission yeast Arp2/3 complex lacking the Arp2 subunit J. Biol. Chem. 283 2008 26490 26498
8. Nolen B.J., Tomasevic N., Russell A., Pierce D.W., Jia Z., and McCormick C.D. Characterization of two classes of small molecule inhibitors of Arp2/3 complex Nature 460 2009 1031 1034
9. Volkmann N., Amann K.J., Stoilova-McPhie S., Egile C., Winter D.C., and Hazelwood L. Structure of Arp2/3 complex in its activated state and in actin filament branch junctions Science 293 2001 2456 2459 (Pubitemid 32917327)
10. Egile C., Rouiller I., Xu X.P., Volkmann N., Li R., and Hanein D. Mechanism of filament nucleation and branch stability revealed by the structure of the Arp2/3 complex at actin branch junctions PLoS Biol. 3 2005 1902 1909 (Pubitemid 41652442)
11. Rouiller I., Xu X., Amann K.J., Egile C., Nickell S., and Nicastro D. The structural basis of actin filament branching by the Arp2/3 complex J. Cell Biol. 180 2008 887 895 (Pubitemid 351398416)
12. Goley E.D., Rammohan A., Znameroski E.A., Firat-Karalar E.N., Sept D., and Welch M.D. An actin-filament-binding interface on the Arp2/3 complex is critical for nucleation and branch stability Proc. Natl Acad. Sci. USA 107 2010 8159 8164
13. Chu J.W., and Voth G.A. Allostery of actin filaments: molecular dynamics simulations and coarse-grained analysis Proc. Natl Acad. Sci. USA 102 2005 13111 13116 (Pubitemid 41324987)
14. Zheng X., Diraviyam K., and Sept D. Nucleotide effects on the structure and dynamics of actin Biophys. J. 93 2007 1277 1283 (Pubitemid 47330907)
15. Dalhaimer P., Pollard T.D., and Nolen B.J. Nucleotide-mediated conformational changes of monomeric actin and Arp3 studied by molecular dynamics simulations J. Mol. Biol. 376 2008 166 183
16. Pfaendtner J., and Voth G.A. Molecular dynamics simulation and coarse-grained analysis of the Arp2/3 complex Biophys. J. 95 2008 5324 5333
17. Pfaendtner J., Branduardi D., Parrinello M., Pollard T.D., and Voth G.A. Nucleotide-dependent conformational states of actin Proc. Natl Acad. Sci. USA 106 2009 12723 12728
18. Splettstoesser T., Noe F., Oda T., and Smith J.C. Nucleotide-dependence of G-actin conformation from multiple molecular dynamics simulations and observation of a putatively polymerization-competent superclosed state Proteins 76 2009 353 364
19. Chu J.W., and Voth G.A. Coarse-grained modeling of the actin filament derived from atomistic-scale simulations Biophys. J. 90 2006 1572 1582
20. Oztug Durer Z.A., Diraviyam K., Sept D., Kudryashov D.S., and Reisler E. F-actin structure destabilization and DNase I binding loop fluctuations: mutational cross-linking and electron microscopy analysis of loop states and effects on F-actin J. Mol. Biol. 395 2010 544 557
21. Pfaendtner J., Lyman E., Pollard T.D., and Voth G.A. Structure and dynamics of the actin filament J. Mol. Biol. 396 2010 252 263
22. Dalhaimer P., and Pollard T.D. Molecular dynamics simulations of Arp2/3 complex activation Biophys. J. 99 2010 2568 2576
23. Fujii T., Iwane A.H., Yanagida T., and Namba K. Direct visualization of secondary structures of F-actin by electron cryomicroscopy Nature 467 2010 724 728
24. Blanchoin L., Amann K.J., Higgs H.N., Marchand J.B., Kaiser D.A., and Pollard T.D. Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins Nature 404 2000 1007 1011 (Pubitemid 30243596)
25. Humphrey W., Dalke A., and Schulten K. VMD: visual molecular dynamics J. Mol. Graphics 14 1996 33 38 (Pubitemid 26152973)
26. Gournier H., Goley E.D., Niederstrasser H., Trinh T., and 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 (Pubitemid 34031806)
27. Volkmann N., and Hanein D. Quantitative fitting of atomic models into observed densities derived by electron microscopy J. Struct. Biol. 125 1999 176 184 (Pubitemid 29402602)
28. Volkmann N., and Hanein D. Docking of atomic models into reconstructions from electron microscopy Methods Enzymol. 374 2003 204 225 (Pubitemid 37547910)
29. Volkmann N. Confidence intervals for fitting of atomic models into low-resolution densities Acta Crystallogr., Sect. D: Biol. Crystallogr. 65 2009 679 689
30. Pfaendtner J., De La Cruz E., and Voth G.A. Actin filament remodeling by cofilin Proc. Natl Acad. Sci. USA 107 2010 7299 7304
31. Narita A., Oda T., and Maeda Y. Structural basis for the slow dynamics of the actin filament pointed end EMBO J. 30 2011 1230 1237
32. Volkmann N., Liu H., Hazelwood L., Krementsova E.B., Lowey S., Trybus K.M., and Hanein D. The structural basis of myosin V processive movement as revealed by electron cryomicroscopy Mol. Cell 19 2005 595 605 (Pubitemid 41219436)
33. Holmes K.C., Popp D., Gebhard W., and Kabsch W. Atomic model of the actin filament Nature 347 1990 44 49
34. Oda T., Iwasa M., Aihara T., Maeda Y., and Narita A. The nature of the globular- to fibrous-actin transition Nature 457 2009 441 445
35. Phillips J.C., Braun R., Wang W., and Gumbart J. Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802 (Pubitemid 43078511)
36. MacKerell A.D., Bashford D., Bellott M., Dunbrack R.L., Evanseck J.D., and Field M.J. All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102 1998 3586 3616 (Pubitemid 128576688)
37. Mackerell A.D. Jr., Feig M., and Brooks C.L. 3rd Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations J. Comput. Chem. 25 2004 1400 1415
38. Otterbein L.R., Graceffa P., and Dominguez R. The crystal structure of uncomplexed actin in the ADP state Science 293 2001 708 711 (Pubitemid 32728675)
39. Jorgensen W.L., Chandrasekhar J., Madura J.D., Impey R.W., and Klein M.L. Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79 1983 926 935
40. Darden T., York D., and Pedersen L. Particle mesh Ewald: an Nlog(N) method for ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
41. Ryckaert J.P., Ciccotti G., and Berendsen H.J.C. Numerical integration of cartesian equations of motion of a system with constraints: molecular-dynamics of n-alkanes J. Comput. Phys. 23 1977 327 341
42. Feller S.E., Zhang Y.H., Pastor R.W., and Brooks B.R. Constant-pressure molecular-dynamics simulation: the Langevin piston method J. Chem. Phys. 103 1995 4613 4621
43. Martyna G.J., Tobias D.J., and Klein M.L. Constant-pressure molecular-dynamics algorithms J. Chem. Phys. 101 1994 4177 4189