Coordination of the filament stabilizing versus destabilizing activities of cofilin through its secondary binding site on actin

Cytoskeleton

Volumn 71, Issue 6, 2014, Pages 361-379

  Aggeli, Dimitra ^a   Kish Trier, Erik ^b   Lin, Meng Chi ^c   Haarer, Brian ^a   Cingolani, Gino ^d   Cooper, John A ^e   Wilkens, Stephan ^a   Amberg, David C ^a  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c RIKEN   (Japan)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Actin cytoskeleton; Cofilin; Endocytosis; S. cerevisiae; Severing

Indexed keywords

ACTIN; ACTIN DEPOLYMERIZING FACTOR;

ACTIN FILAMENT; ANIMAL; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; X RAY CRYSTALLOGRAPHY; YEAST;

ACTIN CYTOSKELETON; ACTIN DEPOLYMERIZING FACTORS; ACTINS; ANIMALS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; YEASTS;

EID: 84904426660     PISSN: 19493584     EISSN: 19493592     Source Type: Journal    
DOI: 10.1002/cm.21178     Document Type: Article

References (80)

1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66:213-221.
2. Amberg DC, Basart E, Botstein D. 1995. Defining protein interactions with yeast actin in vivo. Nat Struct Biol 2:28-35.
3. Andrianantoandro E, Pollard TD. 2006. Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol Cell 24:13-23.
4. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, and Struhl K, editors. 1989. Current Protocols in Molecular Biology. New York: Wiley.
5. Balcer HI, Goodman AL, Rodal AA, Smith E, Kugler J, Heuser JE, Goode BL. 2003. Coordinated regulation of actin filament turnover by a high-molecular-weight Srv2/CAP complex, cofilin, profilin, and Aip1. Curr Biol 13:2159-2169.
6. Blanchoin L, Pollard TD. 1999. Mechanism of interaction of Acanthamoeba actophorin (ADF/Cofilin) with actin filaments. J Biol Chem 274:15538-15546.
7. Bobkov AA, Muhlrad A, Kokabi K, Vorobiev S, Almo SC, Reisler E. 2002. Structural effects of cofilin on longitudinal contacts in F-actin. J Mol Biol 323:739-750.
8. Bobkov AA, Muhlrad A, Pavlov DA, Kokabi K, Yilmaz A, Reisler E. 2006. Cooperative effects of cofilin (ADF) on actin structure suggest allosteric mechanism of cofilin function. J Mol Biol 356:325-334.
9. Bobkov AA, Muhlrad A, Shvetsov A, Benchaar S, Scoville D, Almo SC, Reisler E. 2004. Cofilin (ADF) affects lateral contacts in F-actin. J Mol Biol 337:93-104.
10. Cao W, Goodarzi JP, De La Cruz EM. 2006. Energetics and kinetics of cooperative cofilin-actin filament interactions. J Mol Biol 361:257-267.
11. Carlier MF, Laurent V, Santolini J, Melki R, Didry D, Xia GX, Hong Y, Chua NH, Pantaloni D. 1997. Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J Cell Biol 136:1307-1322.
12. Carlsson AE, Shah AD, Elking D, Karpova TS, Cooper JA. 2002. Quantitative analysis of actin patch movement in yeast. Biophys J 82:2333-2343.
13. Chaudhry F, Breitsprecher D, Little K, Sharov G, Sokolova O, Goode BL. 2013. Srv2/cyclase-associated protein forms hexameric shurikens that directly catalyze actin filament severing by cofilin. Mol Biol Cell 24:31-41.
14. Chen H, Bernstein BW, Sneider JM, Boyle JA, Minamide LS, Bamburg JR. 2004. In vitro activity differences between proteins of the ADF/cofilin family define two distinct subgroups. Biochemistry 43:7127-7142.
15. Chen Q, Pollard TD. 2013. Actin filament severing by cofilin dismantles actin patches and produces mother filaments for new patches. Curr Biol 23:1154-1162.
16. Chen VB, Arendall WB, III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, and Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66:12-21.
17. Clark MG, Amberg DC. 2007. Biochemical and genetic analyses provide insight into the structural and mechanistic properties of actin filament disassembly by the Aip1p cofilin complex in Saccharomyces cerevisiae. Genetics 176:1527-1539.
18. Clark MG, Teply J, Haarer BK, Viggiano SC, Sept D, Amberg DC. 2006. A genetic dissection of Aip1p's interactions leads to a model for Aip1p-Cofilin cooperative Activities. Mol Biol Cell 17:1971-1984.
19. Cooper JA, Walker SB, Pollard TD. 1983. Pyrene actin: documentation of the validity of a sensitive assay for actin polymerization. J Muscle Res Cell Motil 4:253-262.
20. De La Cruz EM. 2005. Cofilin binding to muscle and non-muscle actin filaments: isoform-dependent cooperative interactions. J Mol Biol 346:557-564.
21. De La Cruz EM. 2009. How cofilin severs an actin filament. Biophys Rev 1:51-59.
22. De La Cruz EM, Sept D. 2010. The kinetics of cooperative cofilin binding reveals two states of the cofilin-actin filament. Biophys J 98:1893-1901.
23. Dedova IV, Dedov VN, Nosworthy NJ, Hambly BD, dos Remedios CG. 2002. Cofilin and DNase I affect the conformation of the small domain of actin. Biophys J 82:3134-3143.
24. Du J, Frieden C. 1998. Kinetic studies on the effect of yeast cofilin on yeast actin polymerization. Biochemistry 37:13276-13284.
25. Dube P, Tavares P, Lurz R, van Heel M. 1993. The portal protein of bacteriophage SPP1: a DNA pump with 13-fold symmetry. EMBO J 12:1303-1309.
26. Egelman EH. 2000. A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy 85:225-234.
27. Elam WA, Kang H, De la Cruz EM. 2013. Biophysics of actin filament severing by cofilin. FEBS Lett 587:1215-1219.
28. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66:486-501.
29. Fan J, Saunders MG, Haddadian EJ, Freed KF, De La Cruz EM, Voth GA. 2013. Molecular origins of cofilin-linked changes in actin filament mechanics. J Mol Biol 425:1225-1240.
30. Federov AA, Lappalainen P, Federov EV, Drubin DG, Almo SC. 1997. Structure determination of yeast cofilin. Nat Struct Biol 4:366-369.
31. Galkin VE, Orlova A, Kudryashov DS, Solodukhin A, Reisler E, Schroder GF, Egelman EH. 2011. Remodeling of actin filaments by ADF/cofilin proteins. Proc Natl Acad Sci USA 108:20568-20572.
32. Galkin VE, Orlova A, Schroder GF, Egelman EH. 2010. Structural polymorphism in F-actin. Nat Struct Mol Biol 17:1318-1323.
33. Galkin VE, Orlova A, VanLoock MS, Shvetsov A, Reisler E, Egelman EH. 2003. ADF/cofilin use an intrinsic mode of F-actin instability to disrupt actin filaments. J Cell Biol 163:1057-1066.
34. Galkin VE, VanLoock MS, Orlova A, Egelman EH. 2002. A new internal mode in F-actin helps explain the remarkable evolutionary conservation of actin's sequence and structure. Curr Biol 12:570-575.
35. Galletta BJ, Chuang DY, Cooper JA. 2008. Distinct roles for Arp2/3 regulators in actin assembly and endocytosis. PLoS Biol 6:e1.
36. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK, Weissman JS. 2003. Global analysis of protein expression in yeast. Nature 425:737-741.
37. Goode BL. 2002. Purification of yeast actin and actin-associated proteins. In: Guthrie C, Fink GR, editors. Methods in Enzymology; Guide to Yeast Genetics and Molecular Biology, Part C. London: Academin Press. pp 433-441.
38. Hawkins M, Pope B, Maciver SK, Weeds AG. 1993. Human actin depolymerizing factor mediates a pH-sensitive destruction of actin filaments. Biochemistry 32:9985-9993.
39. Hayden SM, Miller PS, Brauweiler A, Bamburg JR. 1993. Analysis of the interactions of actin depolymerizing factor with G- and F-actin. Biochemistry 32:9994-10004.
40. Higgs HN, Blanchoin L, Pollard TD. 1999. Influence of the C terminus of Wiskott-Aldrich syndrome protein (WASp) and the Arp2/3 complex on actin polymerization. Biochemistry 38:15212-15222.
41. Iida K, Moriyama K, Matsumoto S, Kawasaki H, Nishida E, Yahara I. 1993. Isolation of a yeast essential gene, COF1, that encodes a homologue of mammalian cofilin, a low-Mr actin-binding and depolymerizing protein. Gene 124:115-120.
42. Kaksonen M, Sun Y, Drubin DG. 2003. A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 115:475-487.
43. Kaksonen M, Toret CP, Drubin DG. 2005. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123:305-320.
44. Karpovich DS, Blanchard GJ. 1995. Relating the polarity-dependent fluorescence response of pyrene to vibronic coupling. Achieving a fundamental understanding of the py polarity scale. J Phys Chem 99:3951-3958.
45. Kim K, Galletta BJ, Schmidt KO, Chang FS, Blumer KJ, Cooper JA. 2006. Actin-based motility during endocytosis in budding yeast. Mol Biol Cell 17:1354-1363.
46. Kouyama T, Mihashi K. 1981. 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 114:33-38.
47. Kudryashov DS, Galkin VE, Orlova A, Phan M, Egelman EH, Reisler E. 2006. Cofilin cross-bridges adjacent actin protomers and replaces part of the longitudinal F-actin interface. J Mol Biol 358:785-797.
48. Kuhn JR, Pollard TD. 2005. Real-time measurements of actin filament polymerization by total internal reflection fluorescence microscopy. Biophys J 88:1387-1402.
49. Lappalainen P, Federov EV, Federov AA, Almo SC, Drubin DG. 1997. Essential functions and actin-binding surfaces of yeast cofilin revealed by systematic mutagenesis. EMBO J 16:5520-5530.
50. Lin MC, Galletta BJ, Sept D, Cooper JA. 2010. Overlapping and distinct functions for cofilin, coronin and Aip1 in actin dynamics in vivo. J Cell Sci 123:1329-1342.
51. Ludtke SJ, Baldwin PR, Chiu W. 1999. EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128:82-97.
52. Maciver SK, Zot HG, Pollard TD. 1991. Characterization of actin filament severing by actophorin from Acanthamoeba castellanii. J Cell Biol 115:1611-1620.
53. 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.
54. McCullough BR, Blanchoin L, Martiel JL, De la Cruz EM. 2008. Cofilin increases the bending flexibility of actin filaments: implications for severing and cell mechanics. J Mol Biol 381:550-558.
55. McGhee JD, von Hippel PH. 1974. Theoretical aspects of DNA-protein interactions: co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice. J Mol Biol 86:469-489.
56. McGough A, Chiu W. 1999. ADF/cofilin weakens lateral contacts in the actin filament. J Mol Biol 291:513-519.
57. McGough A, Pope B, Chiu W, Weeds A. 1997. Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J Cell Biol 138:771-781.
58. Moon AL, Janmey PA, Louie KA, Drubin DG. 1993. Cofilin is an essential component of the yeast cortical cytoskeleton. J Cell Biol 120:421-435.
59. Mooren OL, Galletta BJ, Cooper JA. 2012. Roles for actin assembly in endocytosis. Annu Rev Biochem 81:661-686.
60. Okada K, Ravi H, Smith EM, Goode BL. 2006. Aip1 and cofilin promote rapid turnover of yeast actin patches and cables: a coordinated mechanism for severing and capping filaments. Mol Biol Cell 17:2855-2868.
61. Okreglak V, Drubin DG. 2007. Cofilin recruitment and function during actin-mediated endocytosis dictated by actin nucleotide state. J Cell Biol 178:1251-1264.
62. Okreglak V, Drubin DG. 2010. Loss of Aip1 reveals a role in maintaining the actin monomer pool and an in vivo oligomer assembly pathway. J Cell Biol 188:769-777.
63. Ono S, Mohri K, Ono K. 2004. Microscopic evidence that actin-interacting protein 1 actively disassembles actin depolymerizing factor/cofilin-bound actin filaments. J Biol Chem 279:14207-14212.
64. Orlova A, Shvetsov A, Galkin VE, Kudryashov DS, Rubenstein PA, Egelman EH, Reisler E. 2004. Actin-destabilizing factors disrupt filaments by means of a time reversal of polymerization. Proc Natl Acad Sci USA 101:17664-17668.
65. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326.
66. Pavlov D, Muhlrad A, Cooper J, Wear M, Reisler E. 2007. Actin filament severing by cofilin. J Mol Biol 365:1350-1358.
67. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25:1605-1612.
68. Pollard TD. 1986. Rate Constants for the reactions of ATP- and ADP-actin with the ends of actin filaments. J Cell Biol 103:2747-2754.
69. Pollard TD. 2010. A guide to simple and informative binding assays. Mol Biol Cell 21, 4061-4067.
70. Pollard TD, Blanchoin L, and Mullins RD. 2000. Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 29, 545-576.
71. Poukkula M, Kremneva E, Serlachius M, and Lappalainen P. 2011. Actin-depolymerizing factor homology domain: a conserved fold performing diverse roles in cytoskeletal dynamics. Cytoskeleton (Hoboken) 68:471-490.
72. Pring M, Evangelista M, Boone C, Yang C, Zigmond SH. 2003. Mechanism of formin-induced nucleation of actin filaments. Biochemistry 42:486-496.
73. Prochniewicz E, Janson N, Thomas DD, De la Cruz EM. 2005. Cofilin increases the torsional flexibility and dynamics of actin filaments. J Mol Biol 353:990-1000.
74. Ressad F, Didry D, Xia GX, Hong Y, Chua NH, Pantaloni D, Carlier MF. 1998. Kinetic analysis of the interaction of actin-depolymerizing factor (ADF)/cofilin with G- and F-actins. Comparison of plant and human ADFs and effect of phosphorylation. J Biol Chem 273:20894-20902.
75. Rodal AA, Tetreault JW, Lappalainen P, Drubin DG, Amberg DC. 1999. Aip1p interacts with cofilin to disassemble actin filaments. J Cell Biol 145:1251-1264.
76. Suarez C, Roland J, Boujemaa-Paterski R, Kang H, McCullough BR, Reymann AC, Guerin C, Martiel JL, De la Cruz EM, Blanchoin L. 2011. Cofilin tunes the nucleotide state of actin filaments and severs at bare and decorated segment boundaries. Curr Biol 21:862-868.
77. van Heel M, Harauz G, Orlova EV, Schmidt R, Schatz M. 1996. A new generation of the IMAGIC image processing system. J Struct Biol 116:17-24.
78. Vartiainen MK, Mustonen T, Mattila PK, Ojala PJ, Thesleff I, Partanen J, Lappalainen P. 2002. The three mouse actin-depolymerizing factor/cofilins evolved to fulfill cell-type-specific requirements for actin dynamics. Mol Biol Cell 13:183-194.
79. Wong DY, Sept D. 2011. The interaction of cofilin with the actin filament. J Mol Biol 413:97-105.
80. Yeoh S, Pope B, Mannherz HG, Weeds A. 2002. Determining the differences in actin binding by human ADF and cofilin. J Mol Biol 315:911-925.