Understanding the cooperative interaction between myosin II and actin cross-linkers mediated by actin filaments during mechanosensation

Biophysical Journal

Volumn 102, Issue 2, 2012, Pages 238-247

  Luo, Tianzhi ^a   Mohan, Krithika ^b   Srivastava, Vasudha ^a,b   Ren, Yixin ^a   Iglesias, Pablo A ^b   Robinson, Douglas N ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; CROSS LINKING REAGENT; CTXA PROTEIN, DICTYOSTELIUM DISCOIDEUM; MYOSIN II; PROTOZOAL PROTEIN;

ACTIN FILAMENT; ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; CYTOLOGY; DICTYOSTELIUM; KINETICS; MECHANICAL STRESS; MECHANOTRANSDUCTION; METABOLISM; MONTE CARLO METHOD; PROTEIN BINDING;

ACTIN CYTOSKELETON; ACTINS; CROSS-LINKING REAGENTS; DICTYOSTELIUM; KINETICS; MECHANOTRANSDUCTION, CELLULAR; MICROFILAMENT PROTEINS; MODELS, BIOLOGICAL; MONTE CARLO METHOD; MYOSIN TYPE II; PROTEIN BINDING; PROTOZOAN PROTEINS; STRESS, MECHANICAL;

EID: 84856019168     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.12.020     Document Type: Article

References (40)

1. J.A. Spudich The myosin swinging cross-bridge model Nat. Rev. Mol. Cell Biol. 2 2001 387 392 (Pubitemid 33674051)
2. J.C. Effler, and Y.-S. Kee D.N. Robinson Mitosis-specific mechanosensing and contractile protein redistribution control cell shape Curr. Biol. 16 2006 1962 1967 (Pubitemid 44486758)
3. Y. Ren, and J.C. Effler D.N. Robinson Mechanosensing through cooperative interactions between myosin II and the actin crosslinker cortexillin I Curr. Biol. 19 2009 1421 1428
4. M.A. Wozniak, and C.S. Chen Mechanotransduction in development: a growing role for contractility Nat. Rev. Mol. Cell Biol. 10 2009 34 43
5. L.E. Greene, and E. Eisenberg Cooperative binding of myosin subfragment-1 to the actin-troponin-tropomyosin complex Proc. Natl. Acad. Sci. USA 77 1980 2616 2620
6. K.M. Trybus, and E.W. Taylor Kinetic studies of the cooperative binding of subfragment 1 to regulated actin Proc. Natl. Acad. Sci. USA 77 1980 7209 7213 (Pubitemid 11189442)
7. A. Orlova, and E.H. Egelman Cooperative rigor binding of myosin to actin is a function of F-actin structure J. Mol. Biol. 265 1997 469 474 (Pubitemid 27113033)
8. C. Veigel, and J.E. Molloy J. Kendrick-Jones Load-dependent kinetics of force production by smooth muscle myosin measured with optical tweezers Nat. Cell Biol. 5 2003 980 986 (Pubitemid 37406911)
9. T.Q. Uyeda, P.D. Abramson, and J.A. Spudich The neck region of the myosin motor domain acts as a lever arm to generate movement Proc. Natl. Acad. Sci. USA 93 1996 4459 4464 (Pubitemid 26144308)
10. A.A. Bobkov, and A. Muhlrad E. Reisler Cooperative effects of cofilin (ADF) on actin structure suggest allosteric mechanism of cofilin function J. Mol. Biol. 356 2006 325 334 (Pubitemid 43099974)
11. 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
12. H. Shin, and K.R. Purdy Drew G.M. Grason Cooperativity and frustration in protein-mediated parallel actin bundles Phys. Rev. Lett. 103 2009 238102
13. V.E. Galkin, A. Orlova, and E.H. Egelman Actin filaments as tension sensors Curr. Biol. 2011 In press
14. M.S.P. Siddique, and G. Mogami M. Suzuki Cooperative structural change of actin filaments interacting with activated myosin motor domain, detected with copolymers of pyrene-labeled actin and acto-S1 chimera protein Biochem. Biophys. Res. Commun. 337 2005 1185 1191 (Pubitemid 41505249)
15. R.K. Mahajan, and K.T. Vaughan J.D. Pardee Actin filaments mediate Dictyostelium myosin assembly in vitro Proc. Natl. Acad. Sci. USA 86 1989 6161 6165
16. F.C. MacKintosh Active gels: motors keep dynamics steady Nat. Mater. 10 2011 414 415
17. A. Surcel, and Y.-S. Kee D.N. Robinson Cytokinesis through biochemical-mechanical feedback loops Semin. Cell Dev. Biol. 21 2010 866 873
18. G. Bao, and S. Suresh Cell and molecular mechanics of biological materials Nat. Mater. 2 2003 715 725
19. S. Yumura, and M. Yoshida T.T. Egelhoff Multiple myosin II heavy chain kinases: roles in filament assembly control and proper cytokinesis in Dictyostelium Mol. Biol. Cell 16 2005 4256 4266 (Pubitemid 41262894)
20. J.D. Schmit, E. Kamber, and J. Kondev Lattice model of diffusion-limited bimolecular chemical reactions in confined environments Phys. Rev. Lett. 102 2009 218302
21. L.D. Landau, and E.M. Lifshitz Theory of Elasticity 1986 Elsevier Oxford, UK
22. 2+-actin filaments in the presence of low concentrations of ATP J. Mol. Biol. 386 2009 149 162
23. C.T. Murphy, and J.A. Spudich Dictyostelium myosin 25-50K loop substitutions specifically affect ADP release rates Biochemistry 37 1998 6738 6744 (Pubitemid 28228107)
24. R. Uehara, and G. Goshima E.R. Griffis Determinants of myosin II cortical localization during cytokinesis Curr. Biol. 20 2010 1080 1085
25. 2+, and actin filaments Biochemistry 35 1996 15504 15514 (Pubitemid 26408888)
26. J.H. Sinard, W.F. Stafford, and T.D. Pollard The mechanism of assembly of Acanthamoeba myosin-II minifilaments: minifilaments assemble by three successive dimerization steps J. Cell Biol. 109 1989 1537 1547
27. S.L. Moores, and J.A. Spudich Conditional loss-of-myosin-II-function mutants reveal a position in the tail that is critical for filament nucleation Mol. Cell 1 1998 1043 1050 (Pubitemid 128379265)
28. E.M. Reichl, and Y. Ren D.N. Robinson Interactions between myosin and actin crosslinkers control cytokinesis contractility dynamics and mechanics Curr. Biol. 18 2008 471 480
29. C.H. Berlot, P.N. Devreotes, and J.A. Spudich Chemoattractant-elicited increases in Dictyostelium myosin phosphorylation are due to changes in myosin localization and increases in kinase activity J. Biol. Chem. 262 1987 3918 3926
30. B. Takács, and E. O'Neall-Hennessey M. Kovács Myosin cleft closure determines the energetics of the actomyosin interaction FASEB J. 25 2011 111 121
31. M. Kovacs, and K. Thirumurugan J.R. Sellers Load-dependent mechanism of nonmuscle myosin 2 Proc. Natl. Acad. Sci. USA 104 2007 9994 9999 (Pubitemid 47175251)
32. A. Ben-Naim Cooperativity and Regulation in Biochemical Processes 2001 Kluwer Academic/Plenum Publishers New York
33. W. 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 (Pubitemid 44092784)
34. Q. Zhou, and Y.-S. Kee D.N. Robinson 14-3-3 coordinates microtubules, rac, and myosin II to control cell mechanics and cytokinesis Curr. Biol. 20 2010 1881 1889
35. D.E. Discher, D.H. Boal, and S.K. Boey Simulations of the erythrocyte cytoskeleton at large deformation. II. Micropipette aspiration Biophys. J. 75 1998 1584 1597 (Pubitemid 28397627)
36. I. Derényi, F. Jülicher, and J. Prost Formation and interaction of membrane tubes Phys. Rev. Lett. 88 2002 238101
37. S.L. Moores, J.H. Sabry, and J.A. Spudich Myosin dynamics in live Dictyostelium cells Proc. Natl. Acad. Sci. USA 93 1996 443 446 (Pubitemid 26038173)
38. Y. Xiong, and C. Kabacoff P. Iglesias Automated characterization of cell shape changes during amoeboid motility by skeletonization BMC Syst. Biol. 4 2010 33
39. T.Q.P. Uyeda, and Y. Iwadate S. Yumura Stretching actin filaments within cells enhances their affinity for the myosin II motor domain PLoS ONE 6 2011 e26200
40. J.-C. Kuo, and X. Han C.M. Waterman Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for β-Pix in negative regulation of focal adhesion maturation Nat. Cell Biol. 13 2011 383 393