Mechanism of synergistic activation of Arp2/3 complex by cortactin and N-WASP

eLife

Volumn 2013, Issue 2, 2013, Pages

  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; GROWTH FACTOR; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; NUCLEATION PROMOTING FACTOR; UNCLASSIFIED DRUG; CORTACTIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; BINDING COMPETITION; FLUORESCENCE MICROSCOPY; MATHEMATICAL MODEL; OLIGOMERIZATION; PROTEIN PURIFICATION; METABOLISM; POLYMERIZATION;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; CORTACTIN; POLYMERIZATION; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EID: 84884676960     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.00884     Document Type: Article

References (63)

1. Achard V, Jean-louis M, Michelot A, Guérin C, Reymann A-C, Blanchoin L, et al. 2010. A 'Primer'-based mechanism underlies branched actin filament network formation and motility. Curr Biol 20:423-8. doi: 10.1016/j.cub.2009.12.056.
2. Akin O, Mullins RD. 2008. Capping protein increases the rate of actin-based motility by promoting filament nucleation by the Arp2/3 complex. Cell 133:841-51. doi: 10.1016/j.cell.2008.04.011.
3. Ayala I, Baldassarre M, Giacchetti G, Caldieri G, Tetè S, Luini A, et al. 2008. Multiple regulatory inputs converge on cortactin to control invadopodia biogenesis and extracellular matrix degradation. J Cell Sci 121:369-78. doi: 10.1242/jcs.008037.
4. Beltzner CC, Pollard TD. 2008. Pathway of actin filament branch formation by Arp2/3 complex. J Biol Chem 283:7135-44. doi: 10.1074/jbc.M705894200.
5. 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 10:1273-82. doi: 10.1016/S0960-9822(00)00749-1.
6. Bryce NS, Clark ES, Leysath JL, Currie JD, Webb DJ, Weaver AM. 2005. Cortactin promotes cell motility by enhancing lamellipodial persistence. Curr Biol 15:1276-85. doi: 10.1016/j.cub.2005.06.043.
7. Cai L, Makhov AM, Schafer DA, Bear JE. 2008. Coronin 1B antagonizes cortactin and remodels Arp2/3-containing actin branches in lamellipodia. Cell 134:828-42. doi: 10.1016/j.cell.2008.06.054.
8. Chereau D, Kerff F, Graceffa P, Grabarek Z, Knut L, 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 102:16644-9. doi: 10.1073/pnas.0507021102.
9. Chhabra ES, Higgs HN. 2007. The many faces of actin: matching assembly factors with cellular structures. Nat Cell Biol 9:1110-21. doi: 10.1038/ncb1007-1110.
10. Co C, Wong DT, Gierke S, Chang V, Taunton J. 2007. Mechanism of actin network attachment to moving membranes: barbed end capture by N-WASP WH2 domains. Cell 128:901-13. doi: 10.1016/j.cell.2006.12.049.
11. Cordes T, Vogelsang J, Tinnefeld P. 2009. On the mechanism of Trolox as antiblinking and antibleaching reagent. J Am Chem Soc 131:5018-9. doi: 10.1021/ja809117z.
12. De La Cruz EM, Wells AL, Rosenfeld SS, Ostap EM, Sweeney HL. 1999. The kinetic mechanism of myosin V. Proc Natl Acad Sci USA 96:13726-31. doi: 10.1073/pnas.96.24.13726.
13. DesMarais V, Yamaguchi H, Oser M, Soon L, Mouneimne G, Sarmiento C, et al. 2009. N-WASP and cortactin are involved in invadopodium-dependent chemotaxis to EGF in breast tumor cells. Cell Motil Cytoskel 66:303-16. doi: 10.1002/cm.20361.
14. Didry D, Cantrelle F-X, Husson C, Roblin P, Moorthy AME, Perez J, et al. 2011. How a single residue in individual β-thymosin/WH2 domains controls their functions in actin assembly. EMBO J 31:1000-3013. doi: 10.1038/emboj.2011.461.
15. Edelstein A, Amodaj N, Hoover K, Vale R, Stuurman N. 2010. Computer control of microscopes using μManager. Curr Protoc Mol Biol Chapter 14: Unit14.20. doi: 10.1002/0471142727.mb1420s92.
16. Egile C, Rouiller I, Xu X-P, 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. doi: 10.1371/journal.pbio.0030383.
17. Footer MJ, John KL, Theriot JA. 2008. Close packing of Listeria monocytogenes ActA, a natively unfolded protein, enhances F-actin assembly without dimerization. J Biol Chem 283:23852-62. doi: 10.1074/jbc.M803448200.
18. Galletta BJ, Chuang DY, Cooper JA. 2008. Distinct roles for Arp2/3 regulators in actin assembly and endocytosis. PLOS Biol 6:e1. doi: 10.1371/journal.pbio.0060001.
19. Gandhi M, Smith BA, Bovellan M, Paavilainen V, Daugherty-Clarke K, Gelles J, et al. 2010. GMF is a cofilin homolog that binds Arp2/3 complex to stimulate filament debranching and inhibit actin nucleation. Curr Biol 20:861-7. doi: 10.1016/j.cub.2010.03.026.
20. Gaucher JF, Mauge C, Didry D, Guichard B, Renault L, Carlier M-F. 2012. Interactions of isolated C-terminal fragments of neural Wiskott-Aldrich syndrome protein (N-WASP) with actin and Arp2/3 complex. J Biol Chem doi: 10.1074/jbc.M112.394361.
21. Gohl C, Banovic D, Grevelhörster A, Bogdan S. 2010. WAVE forms hetero-and homo-oligomeric complexes at integrin junctions in Drosophila visualized by bimolecular fluorescence complementation. J Biol Chem 285:40171-9. doi: 10.1074/jbc.M110.139337.
22. Goley ED, Welch MD. 2006. The ARP2/3 complex: an actin nucleator comes of age. Nat Rev Mol Cell Biol 7:713-26. doi: 10.1038/nrm2026.
23. Grassart A, Meas-Yedid V, Dufour A, Olivo-Marin J-C, Dautry-Varsat A, Sauvonnet N. 2010. Pak1 phosphorylation enhances cortactin-N-WASP interaction in clathrin-caveolin-independent endocytosis. Traffic 11:1079-91. doi: 10.1111/j.1600-0854.2010.01075.x.
24. Hansen SD, Mullins RD. 2010. VASP is a processive actin polymerase that requires monomeric actin for barbed end association. J Cell Biol 191:571-84. doi: 10.1083/jcb.201003014.
25. Hetrick B, Han MS, Helgeson LA, Nolen BJ. 2013. Small molecules CK-666 and CK-869 inhibit actin-related protein 2/3 complex by blocking an activating conformational change. Chem Biol 20:1-12. doi: 10.1016/j.chembiol.2013.03.019.
26. Higgs HN, Pollard TD. 2000. Activation by Cdc42 and PIP2 of Wiskott-Aldrich syndrome protein (WASp) stimulates actin nucleation by Arp2/3 complex. J Cell Biol 150:1311-20. doi: 10.1083/jcb.150.6.1311.
27. Hoops S, Sahle S, Gauges R, Lee C, Pahle J, Simus N, et al. 2006. COPASI-a COmplex PAthway SImulator. Bioinformatics 22:3067-74. doi: 10.1093/bioinformatics/btl485.
28. Kelly AE, Kranitz H, Dötsch 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 281:10589-97. doi: 10.1074/jbc.M507470200.
29. Kinley AW, Weed SA, Weaver AM, Karginov AV, Bissonette E, Cooper JA, et al. 2003. Cortactin interacts with WIP in regulating Arp2/3 activation and membrane protrusion. Curr Biol 13:384-93. doi: 10.1016/S0960-9822(03)00107-6.
30. Kirkbride KC, Sung BH, Sinha S, Weaver AM. 2011. Cortactin: a multifunctional regulator of cellular invasiveness. Cell Adh Migr 5:187-98. doi: 10.4161/cam.5.2.14773.
31. Kovács M, Tóth J, Hetényi C, Málnási-Csizmadia A, Sellers JR. 2004. Mechanism of Blebbistatin inhibition of myosin ii. J Biol Chem 279:35557-63. doi: 10.1074/jbc.M405319200.
32. Kowalski JR, Egile C, Gil S, Snapper SB, Li R, Thomas SM. 2005. Cortactin regulates cell migration through activation of n-WASP. J Cell Sci 118:79-87. doi: 10.1242/jcs.01586.
33. Kuhn JR, Pollard TD. 2005. Real-time measurements of actin filament polymerization by total internal reflection fluorescence microscopy. Biophys J 88:1387-402. doi: 10.1529/biophysj.104.047399.
34. Lai FPL, Szczodrak M, Block J, Faix J, Breitsprecher D, Mannherz HG, et al. 2008. Arp2/3 complex interactions and actin network turnover in lamellipodia. EMBO J 27:982-92. doi: 10.1038/emboj.2008.34.
35. Li P, Banjade S, Cheng H-C, Kim S, Chen B, Guo L, et al. 2012. Phase transitions in the assembly of multivalent signalling proteins. Nature 483:336-40. doi: 10.1038/nature10879.
36. Liu SL, Needham KM, May JR, Nolen BJ. 2011. Mechanism of a concentration-dependent Switch between activation and Inhibition of Arp2/3 complex by coronin. J Biol Chem 286:17039-46. doi: 10.1074/jbc.M111.219964.
37. Mahaffy RE, Pollard TD. 2006. Kinetics of the formation and dissociation of actin filament branches mediated by Arp2/3 complex. Biophys J 91:3519-28. doi: 10.1529/biophysj.106.080937.
38. Marchand J-B, 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. doi: 10.1038/35050590.
39. Martin AC, Welch MD, Drubin DG. 2006. Arp2/3 ATP hydrolysis-catalysed branch dissociation is critical for endocytic force generation. Nat Cell Biol 8:826-33. doi: 10.1038/ncb1443.
40. Martinez-Quiles N, Ho HY, Kirschner MW, Ramesh N, Geha RS. 2004. Erk/Src phosphorylation of cortactin acts as a switch on-switch off mechanism that controls its ability to activate N-WASP. Mol Cell Biol 24:5269-80. doi: 10.1128/MCB.24.12.5269-5280.2004.
41. Padrick SB, Cheng HC, Ismail AM, Panchal SC, Doolittle LK, Soyeon K, et al. 2008. Hierarchical regulation of WASP/WAVE proteins. Mol Cell 32:426-38. doi: 10.1016/j.molcel.2008.10.012.
42. 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:E472-79. doi: 10.1073/pnas.1100236108.
43. 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 359:840-7. doi: 10.1016/j.jmb.2006.03.065.
44. Pollard TD. 1986. Rate constants for the reactions of ATP-and ADP-actin with the ends of actin filaments. J Cell Biol 103:2747-54. doi: 10.1083/jcb.103.6.2747.
45. Pollard TD. 2007. Regulation of actin filament assembly by Arp2/3 complex and formins. Annu Rev Biophys Biomol Struct 36:451-77. doi: 10.1146/annurev.biophys.35.040405.101936.
46. Pollard TD, Cooper JA. 2009. Actin, a central player in cell shape and movement. Science 326:1208-12. doi: 10.1126/science.1175862.
47. Rebowski G, Namgoong S, Boczkowska M, Leavis PC, Navaza J, Dominguez R. 2010. Structure of a longitudinal actin dimer assembled by tandem W domains-implications for actin filament nucleation. J Mol Biol 403:11-23. doi: 10.1016/j.jmb.2010.08.040.
48. Rotty JD, Wu C, Bear JE. 2013. New insights into the regulation and cellular functions of the ARP2/3 complex. Nat Rev Mol Cell Biol 14:7-12. doi: 10.1038/nrm3492.
49. Shvetsov A, Berkane E, Chereau D, Dominguez R, Reisler E. 2009. The actin-binding domain of cortactin is dynamic and unstructured and affects lateral and longitudinal contacts in F-actin. Cell Motil Cytoskeleton 66:90-8. doi: 10.1002/cm.20328.
50. Siton O, Ideses Y, Albeck S, Unger T, Bershadsky AD, Gov NS, et al. 2011. Cortactin releases the brakes in actin-based motility by enhancing WASP-VCA detachment from Arp2/3 branches. Curr Biol 21:2092-97. doi: 10.1016/j.cub.2011.11.010.
51. Smith BA, Daugherty-Clarke K, Goode BL, Gelles J. 2013. Pathway of actin filament branch formation by Arp2/3 complex revealed by single-molecule imaging. Proc Natl Acad Sci USA 110:1285-90. doi: 10.1073/pnas.1211164110.
52. Suetsugu S. 2013. Activation of nucleation promoting factors for directional actin filament elongation: allosteric regulation and multimerization on the membrane. Semin Cell Dev Biol 24:267-71. doi: 10.1016/j.semcdb.2013.01.006.
53. Ti SC, Jurgenson CT, 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:E472-9. doi: 10.1073/pnas.1100125108.
54. Uruno T, Liu J, Li Y, Smith N, Zhan X. 2003. Sequential interaction of actin-related proteins 2 and 3 (Arp2/3) complex with neural Wiscott-Aldrich syndrome protein (N-WASP) and cortactin during branched actin filament network formation. J Biol Chem 278:26086-93. doi: 10.1074/jbc.M301997200.
55. Uruno T, Liu J, Zhang P, Fan YX, Egile C, Li R, et al. 2001. Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nat Cell Biol 3:259-66. doi: 10.1038/35060051.
56. Van Oijen AM. 2011. Single-molecule approaches to characterizing kinetics of biomolecular interactions. Curr Opin Biotechnol 22:75-80. doi: 10.1016/j.copbio.2010.10.002.
57. Wang ZX. 1995. An exact mathematical expression for describing competitive binding of two different ligands to a protein molecule. FEBS Lett 360:111-4. doi: 10.1016/0014-5793(95)00062-E.
58. Weaver AM, Heuser JE, Karginov AV, Lee WL, Parsons JT, Cooper JA. 2002. Interaction of cortactin and N-WASp with Arp2/3 complex. Curr Biol 12:1270-8. doi: 10.1016/S0960-9822(02)01035-7.
59. Weaver AM, Karginov AV, Kinley AW, Weed SA, Li Y, Parsons JT, et al. 2001. Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr Biol 11:370-4. doi: 10.1016/S0960-9822(01)00098-7.
60. Weed SA, Karginov AV, Schafer DA, Weaver AM, Kinley AW, Cooper JA, et al. 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. doi: 10.1083/jcb.151.1.29.
61. Wegner A, Ruhnau K. 1988. Rate of binding of tropomyosin to actin filaments. Biochemistry 27:6994-7000. doi: 10.1021/bi00418a049.
62. Wu H, Parsons JT. 1993. Cortactin, an 80/85-kilodalton Pp60src substrate, is a filamentous actin-binding protein enriched in the cell cortex. J Cell Biol 120:1417-26. doi: 10.1083/jcb.120.6.1417.
63. Yamaguchi H, Lorenz M, Kempiak S, Sarmiento C, Coniglio S, Symons M, et al. 2005. Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J Cell Biol 168:441-52. doi: 10.1083/jcb.200407076.