Molecular origins of cofilin-linked changes in actin filament mechanics

Journal of Molecular Biology

Volumn 425, Issue 7, 2013, Pages 1225-1240

  Fan, Jun ^a,b   Saunders, Marissa G ^a,b   Haddadian, Esmael J ^c   Freed, Karl F ^a   De La Cruz, Enrique M ^d   Voth, Gregory A ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d YALE UNIVERSITY   (United States)

Author keywords

actin filament; coarse graining; cofilin; molecular dynamics; persistence length

Indexed keywords

ACTIN; COFILIN;

ACTIN FILAMENT; ARTICLE; CRYOELECTRON MICROSCOPY; ENVIRONMENTAL TEMPERATURE; MECHANICAL TORSION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION;

EID: 84875213105     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.01.020     Document Type: Article

References (64)

1. G. Drewes, and H. Faulstich Cooperative effects on filament stability in actin modified at the C-terminus by substitution or truncation Eur. J. Biochem. 212 1993 247 253
2. E. Prochniewicz, E. Katayama, T. Yanagida, and D.D. Thomas Cooperativity in F-actin - chemical modifications of actin monomers affect the functional interactions of myosin with unmodified monomers in the same actin filament Biophys. J. 65 1993 113 123
3. T. Oda, and Y. Maeda Multiple conformations of F-actin Structure 18 2010 761 767
4. G. Hild, B. Bugyi, and M. Nyitrai Conformational dynamics of actin: effectors and implications for biological function Cytoskeleton 67 2010 609 629
5. R. Dominguez, and K.C. Holmes Actin structure and function Annu. Rev. Biophys. 40 2011 169 186
6. A. McGough, B. Pope, W. Chiu, and A. Weeds Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function J. Cell Biol. 138 1997 771 781
7. S.K. Maciver How ADF/cofilin depolymerizes actin filaments - commentary Curr. Opin. Cell Biol. 10 1998 140 144
8. A. McGough, and W. Chiu ADF/cofilin weakens lateral contacts in the actin filament J. Mol. Biol. 291 1999 513 519
9. V.E. Galkin, A. Orlova, N. Lukoyanova, W. Wriggers, and E.H. Egelman Actin depolymerizing factor stabilizes an existing state of F-actin and can change the tilt of F-actin subunits J. Cell Biol. 153 2001 75 86
10. I.V. Dedova, V.N. Dedov, N.J. Nosworthy, B.D. Hambly, and C.G. dos Remedios Cofilin and DNase I affect the conformation of the small domain of actin Biophys. J. 82 2002 3134 3143
11. A.A. Bobkov, A. Muhlrad, K. Kokabi, S. Vorobiev, S.C. Almo, and E. Reisler Structural effects of cofilin on longitudinal contacts in F-actin J. Mol. Biol. 323 2002 739 750
12. V.E. Galkin, A. Orlova, M.S. VanLoock, A. Shvetsov, E. Reisler, and E.H. Egelman ADF/cofilin use an intrinsic mode of F-actin instability to disrupt actin filaments J. Cell Biol. 163 2003 1057 1066
13. I.V. Dedova, O.P. Nikolaeva, V.V. Mikhailova, C.G. dos Remedios, and D.I. Levitsky Two opposite effects of cofilin on the thermal unfolding of F-actin: a differential scanning calorimetric study Biophys. Chem. 110 2004 119 128
14. A.A. Bobkov, A. Muhlrad, A. Shvetsov, S. Benchaar, D. Scoville, S.C. Almo, and E. Reisler Cofilin (ADF) affects lateral contacts in F-actin J. Mol. Biol. 337 2004 93 104
15. A. Muhlrad, D. Kudryashov, Y. Michael Peyser, A.A. Bobkov, S.C. Almo, and E. Reisler Cofilin induced conformational changes in F-actin expose subdomain 2 to proteolysis J. Mol. Biol. 342 2004 1559 1567
16. E. Prochniewicz, N. Janson, D.D. Thomas, and E.M. De la Cruz Cofilin increases the torsional flexibility and dynamics of actin filaments J. Mol. Biol. 353 2005 990 1000
17. E.M. De La Cruz Cofilin binding to muscle and non-muscle actin filaments: isoform-dependent cooperative interactions J. Mol. Biol. 346 2005 557 564
18. E. Andrianantoandro, and T.D. Pollard Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilins Mol. Cell 24 2005 13 23
19. A.A. Bobkov, A. Muhlrad, D.A. Pavlov, K. Kokabi, A. Yilmaz, and E. Reisler Cooperative effects of cofilin (ADF) on actin structure suggest allosteric mechanism of cofilin function J. Mol. Biol. 356 2006 325 334
20. A. Muhlrad, D. Pavlov, Y.M. Peyser, and E. Reisler Inorganic phosphate regulates the binding of cofilin to actin filaments FEBS J. 273 2006 1488 1496
21. D.S. Kudryashov, V.E. Galkin, A. Orlova, M. Phan, E.H. Egelman, and E. Reisler Cofilin cross-bridges adjacent actin protomers and replaces part of the longitudinal F-actin interface J. Mol. Biol. 358 2006 785 797
22. A. Muhlrad, I. Ringel, D. Pavlov, Y.M. Peyser, and E. Reisler Antagonistic effects of cofilin, beryllium fluoride complex, and phalloidin on subdomain 2 and nucleotide-binding cleft in F-actin Biophys. J. 91 2006 4490 4499
23. D. Pavlov, A. Muhlrad, J. Cooper, M. Wear, and E. Reisler Actin filament severing by cofilin J. Mol. Biol. 365 2007 1350 1358
24. B.R. McCullough, L. Blanchoin, J.L. Martiel, and E.M. De La Cruz Cofilin increases the bending flexibility of actin filaments: implications for severing and cell mechanics J. Mol. Biol. 381 2008 550 558
25. D. Scoville, J.D. Stamm, C. Altenbach, A. Shvetsov, K. Kokabi, and P.A. Rubenstein Effects of binding factors on structural elements in F-actin Biochemistry 48 2009 370 378
26. E.M. De La Cruz How cofilin severs an actin filament Biophys. Rev. 1 2009 51 59
27. J. Pfaendtner, E.M. De La Cruz, and G.A. Voth Actin filament remodeling by actin depolymerization factor/cofilin Proc. Natl Acad. Sci. USA 107 2010 7299 7304
28. B.R. McCullough, E.E. Grintsevich, C.K. Chen, H.R. Kang, A.L. Hutchison, and A. Henn Cofilin-linked changes in actin filament flexibility promote severing Biophys. J. 101 2011 151 159
29. V.E. Galkin, A. Orlova, D.S. Kudryashov, A. Solodukhin, E. Reisler, G.F. Schroder, and E.H. Egelman Remodeling of actin filaments by ADF/cofilin proteins Proc. Natl Acad. Sci. USA 108 2011 20568 20572
30. C. Suarez, J. Roland, R. Boujemaa-Paterski, H. Kang, B.R. McCullough, and A.C. Reymann Cofilin tunes the nucleotide state of actin filaments and severs at bare and decorated segment boundaries Curr. Biol. 21 2011 862 868
31. D.Y. Wong, and D. Sept The interaction of cofilin with the actin filament J. Mol. Biol. 413 2011 97 105
32. J.W. Chu, and G.A. Voth Allostery of actin filaments: molecular dynamics simulations and coarse-grained analysis Proc. Natl Acad. Sci. USA 102 2005 13111 13116
33. J. Pfaendtner, E. Lyman, T.D. Pollard, and G.A. Voth Structure and dynamics of the actin filament J. Mol. Biol. 396 2010 252 263
34. S. Matsushita, T. Adachi, Y. Inoue, M. Hojo, and M. Sokabe Evaluation of extensional and torsional stiffness of single actin filaments by molecular dynamics analysis J. Biomech. 43 2010 3162 3167
35. M.A. Deriu, T.C. Bidone, F. Mastrangelo, G. Di Benedetto, M. Soncini, F.M. Montevecchi, and U. Morbiducci Biomechanics of actin filaments: a computational multi-level study J. Biomech. 44 2011 630 636
36. T. Oda, M. Iwasa, T. Aihara, Y. Maéda, and A. Narita The nature of the globular- to fibrous-actin transition Nature 457 2009 441 445
37. M.G. Saunders, and G.A. Voth Comparison between actin filament models: coarse-graining reveals essential differences Structure 20 2012 641 653
38. E.H. Egelman, N. Francis, and D.J. DeRosier F-actin: A helix with a random variable twist Nature 298 1982 131 135
39. J. Fan, M.G. Saunders, and G.A. Voth Coarse-graining provides insights on the essential nature of heterogeneity in actin filaments Biophys. J. 103 2012 1334 1342
40. E.H. Egelman, and D.J. Derosier Image-analysis shows that variations in actin crossover spacings are random, not compensatory Biophys. J. 63 1992 1299 1305
41. J.N. Forkey, M.E. Quinlan, and Y.E. Goldman Measurement of single macromolecule orientation by total internal reflection fluorescence polarization microscopy Biophys. J. 89 2005 1261 1271
42. A. Orlova, and E.H. Egelman F-actin retains a memory of angular order Biophys. J. 78 2000 2180 2185
43. J.W. Chu, and G.A. Voth Coarse-grained modeling of the actin filament derived from atomistic-scale simulations Biophys. J. 90 2006 1572 1582
44. E.M. De La Cruz, J. Roland, B.R. McCullough, L. Blanchoin, and J.L. Martiel Origin of twist-bend coupling in actin filaments Biophys. J. 99 2010 1852 1860
45. L. Blondin, V. Sapountzi, S.K. Maciver, C. Renoult, Y. Benyamin, and C. Roustan The second ADF/cofilin actin-binding site exists in F-actin, the cofilin-G-actin complex, but not in G-actin Eur. J. Biochem. 268 2001 6426 6434
46. F. Ressad, D. Didry, G.X. Xia, Y. Hong, N.H. Chua, D. Pantaloni, and M.F. Carlier 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 1998 20894 20902
47. A. Shvetsov, V.E. Galkin, A. Orlova, M. Phillips, S.E. Bergeron, and P.A. Rubenstein Actin hydrophobic loop 262-274 and filament nucleation and elongation J. Mol. Biol. 375 2008 793 801
48. V.E. Galkin, A. Orlova, G.F. Schroder, and E.H. Egelman Structural polymorphism in F-actin Nat. Struct. Mol. Biol. 17 2010 1318 1323
49. E.M. De La Cruz, and D. Sept The kinetics of cooperative cofilin binding reveals two states of the cofilin-actin filament Biophys. J. 98 2010 1893 1901
50. E.J. Haddadian, H.P. Gong, A.K. Jha, X.J. Yang, J. DeBartolo, and J.R. Hinshaw Automated real-space refinement of protein structures using a realistic backbone move set Biophys. J. 101 2011 899 909
51. L.G. Trabuco, E. Villa, K. Mitra, J. Frank, and K. Schulten Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics Structure 16 2008 673 683
52. W.X. Cao, J.P. Goodarzi, and E.M. De la Cruz Energetics and kinetics of cooperative cofilin-actin filament interactions J. Mol. Biol. 361 2006 257 267
53. T. Splettstoesser, K.C. Holmes, F. Noe, and J.C. Smith Structural modeling and molecular dynamics simulation of the actin filament Proteins: Struct. Funct. Bioinformat. 79 2011 2033 2043
54. P. Lappalainen, E.V. Fedorov, A.A. Fedorov, S.C. Almo, and D.G. Drubin Essential functions and actin-binding surfaces of yeast cofilin revealed by systematic mutagenesis EMBO J. 16 1997 5520 5530
55. R.A. Grassucci, D.J. Taylor, and J. Frank Preparation of macromolecular complexes for cryo-electron microscopy Nat. Protoc. 2 2007 3239 3246
56. M.G. Saunders, and G.A. Voth Water molecules in the nucleotide binding cleft of actin: effects on subunit conformation and implications for ATP hydrolysis J. Mol. Biol. 413 2011 279 291
57. W.L. Jorgensen, J. Chandrasekhar, J.D. Madura, R.W. Impey, and M.L. Klein Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79 1983 926 935
58. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graphics 14 1996 33 38
59. J.C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, and E. Villa Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802
60. A.D. Mackerell, M. Feig, and C.L. Brooks 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
61. T. Darden, D. York, and L. Pedersen Particle mesh Ewald - an N.Log(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
62. J.P. Ryckaert, G. Ciccotti, and H.J.C. Berendsen Numerical integration of Cartesian equations of motion of a system with constraints - molecular dynamics of n-alkanes J. Comput. Phys. 23 1977 327 341
63. E. Lyman, J. Pfaendtner, and G.A. Voth Systematic multiscale parameterization of heterogeneous elastic network models of proteins Biophys. J. 95 2008 4183 4192
64. B.R. Brooks, R.E. Bruccoleri, B.D. Olafson, D.J. States, S. Swaminathan, and M. Karplus CHARMM - a program for macromolecular energy, minimization, and dynamics calculations J. Comput. Chem. 4 1983 187 217