Actin Filament Elongation in Arp2/3-Derived Networks Is Controlled by Three Distinct Mechanisms

Developmental Cell

Volumn 24, Issue 2, 2013, Pages 182-195

  Michelot, Alphée ^a,c   Grassart, Alexandre ^a   Okreglak, Voytek ^a   Costanzo, Michael ^b   Boone, Charles ^b   Drubin, David G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c CEA GRENOBLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ABP1 PROTEIN; ACTIN CAPPING PROTEIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; AIM3 PROTEIN; COFILIN; PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; BIOCHEMISTRY; CELL MEMBRANE; CYTOLOGY; ENDOCYTOSIS; GENE INTERACTION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ACTIN CAPPING PROTEINS; ACTIN CYTOSKELETON; ACTIN DEPOLYMERIZING FACTORS; ACTIN-RELATED PROTEIN 2-3 COMPLEX; ANIMALS; CELL LINE; MICROFILAMENT PROTEINS; POTOROIDAE; RAS GTPASE-ACTIVATING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84873096363     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.12.008     Document Type: Article

References (42)

1. Aghamohammadzadeh S., Ayscough K.R. Differential requirements for actin during yeast and mammalian endocytosis. Nat. Cell Biol. 2009, 11:1039-1042.
2. Balcer H.I., Goodman A.L., Rodal A.A., Smith E., Kugler J., Heuser J.E., Goode B.L. Coordinated regulation of actin filament turnover by a high-molecular-weight Srv2/CAP complex, cofilin, profilin, and Aip1. Curr. Biol. 2003, 13:2159-2169.
3. Blanchoin L., Pollard T.D. Mechanism of interaction of Acanthamoeba actophorin (ADF/Cofilin) with actin filaments. J. Biol. Chem. 1999, 274:15538-15546.
4. Blanchoin L., Pollard T.D., Mullins R.D. Interactions of ADF/cofilin, Arp2/3 complex, capping protein and profilin in remodeling of branched actin filament networks. Curr. Biol. 2000, 10:1273-1282.
5. 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 2000, 404:1007-1011.
6. Campellone K.G., Welch M.D. A nucleator arms race: cellular control of actin assembly. Nat. Rev. Mol. Cell Biol. 2010, 11:237-251.
7. Costanzo M., Baryshnikova A., Bellay J., Kim Y., Spear E.D., Sevier C.S., Ding H., Koh J.L., Toufighi K., Mostafavi S., et al. The genetic landscape of a cell. Science 2010, 327:425-431.
8. Drubin D.G., Miller K.G., Botstein D. Yeast actin-binding proteins: evidence for a role in morphogenesis. J. Cell Biol. 1988, 107:2551-2561.
9. Goode B.L. Purification of yeast actin and actin-associated proteins. Methods Enzymol. 2002, 351:433-441.
10. 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. 2001, 153:627-634.
11. Helfer E., Nevalainen E.M., Naumanen P., Romero S., Didry D., Pantaloni D., Lappalainen P., Carlier M.F. Mammalian twinfilin sequesters ADP-G-actin and caps filament barbed ends: implications in motility. EMBO J. 2006, 25:1184-1195.
12. Huang S., Blanchoin L., Kovar D.R., Staiger C.J. Arabidopsis capping protein (AtCP) is a heterodimer that regulates assembly at the barbed ends of actin filaments. J. Biol. Chem. 2003, 278:44832-44842.
13. Iwasa J.H., Mullins R.D. Spatial and temporal relationships between actin-filament nucleation, capping, and disassembly. Curr. Biol. 2007, 17:395-406.
14. Kaksonen M., Sun Y., Drubin D.G. A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 2003, 115:475-487.
15. Kaksonen M., Toret C.P., Drubin D.G. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 2005, 123:305-320.
16. Kouyama T., Mihashi K. Fluorimetry study of N-(1-pyrenyl)iodoacetamide-labelled F-actin. Local structural change of actin protomer both on polymerization and on binding of heavy meromyosin. Eur. J. Biochem. 1981, 114:33-38.
17. Lai F.P., Szczodrak M., Block J., Faix J., Breitsprecher D., Mannherz H.G., Stradal T.E., Dunn G.A., Small J.V., Rottner K. Arp2/3 complex interactions and actin network turnover in lamellipodia. EMBO J. 2008, 27:982-992.
18. Lappalainen P., Kessels M.M., Cope M.J., Drubin D.G. The ADF homology (ADF-H) domain: a highly exploited actin-binding module. Mol. Biol. Cell 1998, 9:1951-1959.
19. Loisel T.P., Boujemaa R., Pantaloni D., Carlier M.F. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 1999, 401:613-616.
20. Michelot A., Drubin D.G. Building distinct actin filament networks in a common cytoplasm. Curr. Biol. 2011, 21:R560-R569.
21. Michelot A., Berro J., Guérin C., Boujemaa-Paterski R., Staiger C.J., Martiel J.L., Blanchoin L. Actin-filament stochastic dynamics mediated by ADF/cofilin. Curr. Biol. 2007, 17:825-833.
22. Michelot A., Costanzo M., Sarkeshik A., Boone C., Yates J.R., Drubin D.G. Reconstitution and protein composition analysis of endocytic actin patches. Curr. Biol. 2010, 20:1890-1899.
23. Miyoshi T., Tsuji T., Higashida C., Hertzog M., Fujita A., Narumiya S., Scita G., Watanabe N. Actin turnover-dependent fast dissociation of capping protein in the dendritic nucleation actin network: evidence of frequent filament severing. J. Cell Biol. 2006, 175:947-955.
24. Moseley J.B., Goode B.L. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol. Mol. Biol. Rev. 2006, 70:605-645.
25. Okada K., Blanchoin L., Abe H., Chen H., Pollard T.D., Bamburg J.R. Xenopus actin-interacting protein 1 (XAip1) enhances cofilin fragmentation of filaments by capping filament ends. J. Biol. Chem. 2002, 277:43011-43016.
26. Okreglak V., Drubin D.G. Cofilin recruitment and function during actin-mediated endocytosis dictated by actin nucleotide state. J. Cell Biol. 2007, 178:1251-1264.
27. Okreglak V., Drubin D.G. Loss of Aip1 reveals a role in maintaining the actin monomer pool and an in vivo oligomer assembly pathway. J. Cell Biol. 2010, 188:769-777.
28. Paavilainen V.O., Hellman M., Helfer E., Bovellan M., Annila A., Carlier M.F., Permi P., Lappalainen P. Structural basis and evolutionary origin of actin filament capping by twinfilin. Proc. Natl. Acad. Sci. USA 2007, 104:3113-3118.
29. Palmgren S., Ojala P.J., Wear M.A., Cooper J.A., Lappalainen P. Interactions with PIP2, ADP-actin monomers, and capping protein regulate the activity and localization of yeast twinfilin. J. Cell Biol. 2001, 155:251-260.
30. Pantaloni D., Le Clainche C., Carlier M.F. Mechanism of actin-based motility. Science 2001, 292:1502-1506.
31. Pollard T.D., Borisy G.G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003, 112:453-465.
32. Pollard T.D., Blanchoin L., Mullins R.D. Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu. Rev. Biophys. Biomol. Struct. 2000, 29:545-576.
33. Rodal A.A., Tetreault J.W., Lappalainen P., Drubin D.G., Amberg D.C. Aip1p interacts with cofilin to disassemble actin filaments. J. Cell Biol. 1999, 145:1251-1264.
34. Rodal A.A., Manning A.L., Goode B.L., Drubin D.G. Negative regulation of yeast WASp by two SH3 domain-containing proteins. Curr. Biol. 2003, 13:1000-1008.
35. Schafer D.A., Welch M.D., Machesky L.M., Bridgman P.C., Meyer S.M., Cooper J.A. Visualization and molecular analysis of actin assembly in living cells. J. Cell Biol. 1998, 143:1919-1930.
36. Spudich J.A., Watt S. The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J. Biol. Chem. 1971, 246:4866-4871.
37. St-Pierre J., Douziech M., Bazile F., Pascariu M., Bonneil E., Sauvé V., Ratsima H., D'Amours D. Polo kinase regulates mitotic chromosome condensation by hyperactivation of condensin DNA supercoiling activity. Mol. Cell 2009, 34:416-426.
38. 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. 1997, 139:397-415.
39. Tonikian R., Xin X., Toret C.P., Gfeller D., Landgraf C., Panni S., Paoluzi S., Castagnoli L., Currell B., Seshagiri S., et al. Bayesian modeling of the yeast SH3 domain interactome predicts spatiotemporal dynamics of endocytosis proteins. PLoS Biol. 2009, 7:e1000218.
40. Wear M.A., Cooper J.A. Capping protein: new insights into mechanism and regulation. Trends Biochem. Sci. 2004, 29:418-428.
41. Wear M.A., Yamashita A., Kim K., Maéda Y., Cooper J.A. How capping protein binds the barbed end of the actin filament. Curr. Biol. 2003, 13:1531-1537.
42. Wiesner S., Helfer E., Didry D., Ducouret G., Lafuma F., Carlier M.F., Pantaloni D. A biomimetic motility assay provides insight into the mechanism of actin-based motility. J. Cell Biol. 2003, 160:387-398.