Small molecules CK-666 and CK-869 inhibit actin-related protein 2/3 complex by blocking an activating conformational change

Chemistry and Biology

Volumn 20, Issue 5, 2013, Pages 701-712

  Hetrick, Byron ^a   Han, Min Suk ^a   Helgeson, Luke A ^a   Nolen, Brad J ^a  

^a UNIVERSITY OF OREGON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; CK 666; CK 869; PROTEIN INHIBITOR; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; DRUG MECHANISM; DRUG PROTEIN BINDING; DRUG STRUCTURE; PRIORITY JOURNAL;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; ACTINS; ADENOSINE TRIPHOSPHATE; ANIMALS; BINDING SITES; CATTLE; CRYSTALLOGRAPHY, X-RAY; INDOLES; MODELS, MOLECULAR; ORGANOSELENIUM COMPOUNDS; ORGANOSILICON COMPOUNDS; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPS;

EID: 84878261069     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2013.03.019     Document Type: Article

References (51)

1. V. Achard, J.L. Martiel, A. Michelot, C. Guérin, A.C. Reymann, L. Blanchoin, and R. Boujemaa-Paterski A "primer"-based mechanism underlies branched actin filament network formation and motility Curr. Biol. 20 2010 423 428
2. C. B-Rao, J. Subramanian, and S.D. Sharma Managing protein flexibility in docking and its applications Drug Discov. Today 14 2009 394 400
3. A.W. Baggett, Z. Cournia, M.S. Han, G. Patargias, A.C. Glass, S.Y. Liu, and B.J. Nolen Structural characterization and computer-aided optimization of a small-molecule inhibitor of the Arp2/3 complex, a key regulator of the actin cytoskeleton ChemMedChem 7 2012 1286 1294
4. C.C. Beltzner, and T.D. Pollard Pathway of actin filament branch formation by Arp2/3 complex J. Biol. Chem. 283 2008 7135 7144
5. M. Boczkowska, G. Rebowski, M.V. Petoukhov, D.B. Hayes, D.I. Svergun, and R. Dominguez X-ray scattering study of activated Arp2/3 complex with bound actin-WCA Structure 16 2008 695 704
6. A.T. Brünger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszewski, M. Nilges, and N.S. Pannu Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54 1998 905 921
7. D. Chereau, F. Kerff, P. Graceffa, Z. Grabarek, K. Langsetmo, and R. Dominguez Actin-bound structures of Wiskott-Aldrich syndrome protein (WASP)-homology domain 2 and the implications for filament assembly Proc. Natl. Acad. Sci. USA 102 2005 16644 16649
8. J.A. Cooper, E.L. Buhle Jr., S.B. Walker, T.Y. Tsong, and T.D. Pollard Kinetic evidence for a monomer activation step in actin polymerization Biochemistry 22 1983 2193 2202
9. M.J. Dayel, and R.D. Mullins Activation of Arp2/3 complex: addition of the first subunit of the new filament by a WASP protein triggers rapid ATP hydrolysis on Arp2 PLoS Biol. 2 2004 E91
10. M.J. Dayel, E.A. Holleran, and R.D. Mullins Arp2/3 complex requires hydrolyzable ATP for nucleation of new actin filaments Proc. Natl. Acad. Sci. USA 98 2001 14871 14876
11. C. Egile, I. Rouiller, X.P. Xu, N. Volkmann, R. Li, and D. Hanein Mechanism of filament nucleation and branch stability revealed by the structure of the Arp2/3 complex at actin branch junctions PLoS Biol. 3 2005 e383
12. E.N. Firat-Karalar, and M.D. Welch New mechanisms and functions of actin nucleation Curr. Opin. Cell Biol. 23 2011 4 13
13. J.F. Gaucher, C. Maugé, D. Didry, B. Guichard, L. Renault, and M.F. Carlier Interactions of isolated C-terminal fragments of neural Wiskott-Aldrich syndrome protein (N-WASP) with actin and Arp2/3 complex J. Biol. Chem. 287 2012 34646 34659
14. E.D. Goley, and M.D. Welch The ARP2/3 complex: an actin nucleator comes of age Nat. Rev. Mol. Cell Biol. 7 2006 713 726
15. E.D. Goley, S.E. Rodenbusch, A.C. Martin, and M.D. Welch Critical conformational changes in the Arp2/3 complex are induced by nucleotide and nucleation promoting factor Mol. Cell 16 2004 269 279
16. E.D. Goley, A. Rammohan, E.A. Znameroski, E.N. Firat-Karalar, D. Sept, and M.D. Welch 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
17. H. Gournier, E.D. Goley, H. Niederstrasser, T. Trinh, and M.D. Welch Reconstitution of human Arp2/3 complex reveals critical roles of individual subunits in complex structure and activity Mol. Cell 8 2001 1041 1052
18. J.A. Hardy, and J.A. Wells Searching for new allosteric sites in enzymes Curr. Opin. Struct. Biol. 14 2004 706 715
19. H.N. Higgs, L. Blanchoin, and T.D. Pollard Influence of the C terminus of Wiskott-Aldrich syndrome protein (WASp) and the Arp2/3 complex on actin polymerization Biochemistry 38 1999 15212 15222
20. E. Ingerman, J.Y. Hsiao, and R.D. Mullins Arp2/3 complex ATP hydrolysis promotes lamellipodial actin network disassembly but is dispensable for assembly J. Cell Biol. 200 2013 619 633
21. C. Le Clainche, D. Didry, M.F. Carlier, and D. Pantaloni 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
22. L.L. LeClaire 3rd, M. Baumgartner, J.H. Iwasa, R.D. Mullins, and D.L. Barber Phosphorylation of the Arp2/3 complex is necessary to nucleate actin filaments J. Cell Biol. 182 2008 647 654
23. G.M. Lee, and C.S. Craik Trapping moving targets with small molecules Science 324 2009 213 215
24. S.L. Liu, K.M. Needham, J.R. May, and B.J. Nolen Mechanism of a concentration-dependent switch between activation and inhibition of Arp2/3 complex by coronin J. Biol. Chem. 286 2011 17039 17046
25. L.M. Machesky, R.D. Mullins, H.N. Higgs, D.A. Kaiser, L. Blanchoin, R.C. May, M.E. Hall, and T.D. Pollard Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex Proc. Natl. Acad. Sci. USA 96 1999 3739 3744
26. J.B. Marchand, D.A. Kaiser, T.D. Pollard, and H.N. Higgs Interaction of WASP/Scar proteins with actin and vertebrate Arp2/3 complex Nat. Cell Biol. 3 2001 76 82
27. A.C. Martin, X.P. Xu, I. Rouiller, M. Kaksonen, Y. Sun, L. Belmont, N. Volkmann, D. Hanein, M. Welch, and D.G. Drubin Effects of Arp2 and Arp3 nucleotide-binding pocket mutations on Arp2/3 complex function J. Cell Biol. 168 2005 315 328
28. A.C. Martin, M.D. Welch, and D.G. Drubin Arp2/3 ATP hydrolysis-catalysed branch dissociation is critical for endocytic force generation Nat. Cell Biol. 8 2006 826 833
29. H. Miki, and T. Takenawa 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
30. K. Murakami, T. Yasunaga, T.Q. Noguchi, Y. Gomibuchi, K.X. Ngo, T.Q. Uyeda, and T. Wakabayashi Structural basis for actin assembly, activation of ATP hydrolysis, and delayed phosphate release Cell 143 2010 275 287
31. A. Narita, T. Oda, and Y. Maéda Structural basis for the slow dynamics of the actin filament pointed end EMBO J. 30 2011 1230 1237
32. B.J. Nolen, and T.D. Pollard Insights into the influence of nucleotides on actin family proteins from seven structures of Arp2/3 complex Mol. Cell 26 2007 449 457
33. B.J. Nolen, R.S. Littlefield, and T.D. Pollard Crystal structures of actin-related protein 2/3 complex with bound ATP or ADP Proc. Natl. Acad. Sci. USA 101 2004 15627 15632
34. B.J. Nolen, N. Tomasevic, A. Russell, D.W. Pierce, Z. Jia, C.D. McCormick, J. Hartman, R. Sakowicz, and T.D. Pollard Characterization of two classes of small molecule inhibitors of Arp2/3 complex Nature 460 2009 1031 1034
35. L.R. Otterbein, P. Graceffa, and R. Dominguez The crystal structure of uncomplexed actin in the ADP state Science 293 2001 708 711
36. S.B. Padrick, L.K. Doolittle, C.A. Brautigam, D.S. King, and M.K. Rosen Arp2/3 complex is bound and activated by two WASP proteins Proc. Natl. Acad. Sci. USA 108 2011 E472 E479
37. T.D. Pollard Regulation of actin filament assembly by Arp2/3 complex and formins Annu. Rev. Biophys. Biomol. Struct. 36 2007 451 477
38. Y. Pommier, and C. Marchand Interfacial inhibitors: targeting macromolecular complexes Nat. Rev. Drug Discov. 11 2012 25 36
39. S.A. Rizvi, E.M. Neidt, J. Cui, Z. Feiger, C.T. Skau, M.L. Gardel, S.A. Kozmin, and D.R. Kovar Identification and characterization of a small molecule inhibitor of formin-mediated actin assembly Chem. Biol. 16 2009 1158 1168
40. R.C. Robinson, K. Turbedsky, D.A. Kaiser, J.B. Marchand, H.N. Higgs, S. Choe, and T.D. Pollard Crystal structure of Arp2/3 complex Science 294 2001 1679 1684
41. A.A. Rodal, O. Sokolova, D.B. Robins, K.M. Daugherty, S. Hippenmeyer, H. Riezman, N. Grigorieff, and B.L. Goode Conformational changes in the Arp2/3 complex leading to actin nucleation Nat. Struct. Mol. Biol. 12 2005 26 31
42. I. Rouiller, X.P. Xu, K.J. Amann, C. Egile, S. Nickell, D. Nicastro, R. Li, T.D. Pollard, N. Volkmann, and D. Hanein The structural basis of actin filament branching by the Arp2/3 complex J. Cell Biol. 180 2008 887 895
43. P. Schuck Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling Biophys. J. 78 2000 1606 1619
44. A.W. Schüttelkopf, and D.M. van Aalten PRODRG: a tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr. D Biol. Crystallogr. 60 2004 1355 1363
45. D. Sept, and J.A. McCammon Thermodynamics and kinetics of actin filament nucleation Biophys. J. 81 2001 667 674
46. S.C. Ti, C.T. Jurgenson, B.J. Nolen, and T.D. Pollard Structural and biochemical characterization of two binding sites for nucleation-promoting factor WASp-VCA on Arp2/3 complex Proc. Natl. Acad. Sci. USA 108 2011 E463 E471
47. A.M. Weaver, J.E. Heuser, A.V. Karginov, W.L. Lee, J.T. Parsons, and J.A. Cooper Interaction of cortactin and N-WASp with Arp2/3 complex Curr. Biol. 12 2002 1270 1278
48. J.A. Wells, and C.L. McClendon Reaching for high-hanging fruit in drug discovery at protein-protein interfaces Nature 450 2007 1001 1009
49. K.K. Wen, and P.A. Rubenstein Acceleration of yeast actin polymerization by yeast Arp2/3 complex does not require an Arp2/3-activating protein J. Biol. Chem. 280 2005 24168 24174
50. A.J. Wilson Inhibition of protein-protein interactions using designed molecules Chem. Soc. Rev. 38 2009 3289 3300
51. X.P. Xu, I. Rouiller, B.D. Slaughter, C. Egile, E. Kim, J.R. Unruh, X. Fan, T.D. Pollard, R. Li, and D. Hanein Three-dimensional reconstructions of Arp2/3 complex with bound nucleation promoting factors EMBO J. 31 2011 236 247