Mechanochemical coupling in the myosin motor domain. II. Analysis of critical residues

PLoS Computational Biology

Volumn 3, Issue 2, 2007, Pages 0214-0230

  Yu, Haibo ^a   Ma, Liang ^a   Yang, Yang ^a   Cui, Qiang ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ANALYSIS; COMPUTATIONAL CHEMISTRY; MOLECULAR DYNAMICS;

ACTIVE SITE; CHEMICAL SITES; COMPUTATIONAL TECHNIQUE; MECHANOCHEMICAL COUPLINGS; MOLECULAR MOTORS; MOTOR DOMAIN; MYOSIN MOTORS; STRUCTURAL REARRANGEMENT; TARGETED MOLECULAR DYNAMICS; TIGHT COUPLING;

REGRESSION ANALYSIS;

MOLECULAR MOTOR; MYOSIN; AMINO ACID;

ARTICLE; BAY REGION BINDING SITE; COMPUTER SIMULATION; FLUORESCENCE ANALYSIS; MECHANOTRANSDUCTION; MOLECULAR DYNAMICS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; STRUCTURAL PROTEOMICS; BIOLOGICAL MODEL; CHEMICAL MODEL; CHEMISTRY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION;

AMINO ACIDS; COMPUTER SIMULATION; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; MODELS, CHEMICAL; MOLECULAR MOTOR PROTEINS; MYOSINS; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 33847270136     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.0030023     Document Type: Article

References (88)

1. Alberts B, Bray D, Lewis J, Raff M, Roberts K, et al. (1994) Molecular biology of the cell. Garland Publishing. 1616 p.
2. Monod J, Wyman J, Changeux JP (1965) On the nature of allosteric transitions: A plausible model. J Mol Biol 12: 88-118.
3. Koshland DEJ, Nemethy G, Filmer D (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochem 5: 365-385.
4. Changeux JP, Edelstein SJ (2005) Allosteric mechanisms of signal transduction. Science 308: 1424-1428.
5. Kern D, Zuiderweg ERP (2003) The role of dynamics in allosteric regulation. Protein Science 11: 184-197.
6. Swain JF, Gierasch LM (2006) The changing landscape of protein allostery. Curr Opin Struct Biol 16: 102-108.
7. Vale RD, Milligan RA (2000) The way things move: Looking under the hood of molecular motor proteins. Science 288: 88-95.
8. Howard J (2001) Mechanics of motor proteins and the cytoskeleton. Sunderland (Massachusetts): Sinauer Associates. 384 p.
9. Schliwa Meditor (2002) Molecular motors. Wenheim, Germany: Wiley-VCH. 604 p.
10. Bustamante C, Keller D, Oster G (2001) The physics of molecular motors. Acc Chem Res 34: 412-420.
11. 1-ATPase paradigm. Curr Opin Struct Biol 14: 250-259.
12. Ito K, Uyeda QP, Suzuki Y, Sutoh K, Yamamoto K (2003) Requirement of domain-domain interaction for conformational change and functional ATP hydrolysis in myosin. J Biol Chem 278: 31049-31057.
13. Sasaki N, Ohkura R, Sutoh K (2003) Dictyostelium myosin II mutations that uncouple the converter swing and ATP hydrolysis cycle. Biochem 42: 90-95.
14. Lockless SW, Ranganathan R (1999) Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286: 295-299.
15. Zheng WJ, Brooks B (2005) Identification of dynamical correlations within the myosin motor domain by the normal mode analysis of an elastic network model. J Mol Biol 346: 745-759.
16. Zheng WJ, Brooks BR, Thirumalai D (2006) Low-frequency normal modes that describe allosteric transitions in biological nanomachines are robust to sequence variations. Proc Acad Natl Sci U S A 103: 7664-7669.
17. Keike MC, Titus MA (2002) The myosi superfamily: An overview. In: Molecular motors. Muchen, Germany: Wiley-VCH. pp. 3-44.
18. Lymn RW, Taylor EW (1971) Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochem 10: 4617-4624.
19. Trentham DR, Eccleston JF, Bagshaw CR (1976) Kinetic-analysis of ATPase mechanisms. Q Rev Biophys 9: 217-281.
20. Rayment I (1996) The structural basis of the myosin ATPase activity. J Biol Chem 271: 15850-15853.
21. Geeves MA, Holmes KC (1999) Structural mechanism of muscle contraction. Annu Rev Biochem 68: 687-728.
22. Holmes KC (2004) Introduction. In: Proceedings of a discussion meeting held at the Royal Society on 17 and 18 May 2004. Phil Trans R Soc Lond B Biol Sci 359: 1813-1818.
23. Geeves MA, Holmes KC (2005) The molecular mechanism of muscle contraction. Adv Prot Chem 71: 161-193.
24. Yu H, Ma L, Yang Y, Cui Q (2006) Mechanochemical coupling in the myosin motor domain. I. Insights from equilibrium active-site simulations. PLoS 3 (2): e21.
25. 2+-ATPase. Biophys J 86: 743-763.
26. Li GH, Cui Q (2004) Mechanochemical coupling in myosin: A theoretical analysis with molecular dynamics and combined QM/MM reaction path calculations. J Phys Chem B 108: 3342-3357.
27. Schlitter J, Engels M, Krüger P, Jacoby E, Wollmer A (1993) Targeted molecular dynamics simuation of conformational change: Application to the T ↔ R transition in insulin. Mol Simu 10: 291-308.
28. Schlitter J, Engels M, Krüger P (1994) Targeted molecular-dynamics: A new approach for searching pathways of conformational transitions. J Mol Graph 12: 84-89.
29. Bauer CB, Holden HM, Thoden JB, Smith R, Rayment I (2000) X-ray structures of the Apo and MgATP-bound states of Dictyostelium discoideum myosin motor domain. J Biol Chem 275: 38494-38499.
30. Smith CA, Rayment I (1996) X-ray structure of the Magnesium(II)- ADP·Vanadate complex of the Dictyostelium discoideum myosin motor domain to 1.9 Å resolution. Biochemistry 35: 5404-5417.
31. Fischer S, Windshugel B, Horak D, Holmes KC, Smith JC (2005) Structural mechanism of the recovery stroke in the myosin molecular motor. Proc Natl Acad Sci U S A 102: 6873-6878.
32. Case DA (1994) Normal-mode analysis of protein dynamics. Curr Opin Struct Biol 4: 285-290.
33. Cui Q, Bahar I, editors (2005) Normal mode analysis: Theory and applications to biological and chemical systems. Mathematical and Computational Biology Series. New York: Chapman and Hall/CRC. 432 p.
34. Suel GM, Lockless SW, Wall MA, Ranganathan R (2003) Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nat Struct Biol 10: 59-69.
35. Conibear PB, Málnási-Csizmadia A, Bagshaw CR (2004) The effect of F-actin on the relay helix position of myosin II, as revealed by tryptophan fluorescence, and its implications for mechanochemical coupling. Biochem 43: 15404-15417.
36. Coureux PD, Sweeney HL, Houdusse A (2004) Three myosin V structures delineate essential features of chemo-mechanical transduction. EMBO J 23: 4527-4537.
37. Reubold TF, Eschenburg S, Becker A, Kull FJ, Manstein DJ (2003) A structural model for actin-induced nucleotide release in myosin. Nat Struct Biol 10: 826-830.
38. Málnási-Csizmadia A, Woolley RJ, Bagshaw CR (2000) Resolution of conformational states of Dictyostelium myosin II motor domain using tryptophan (W501) mutants: Implications for the open-closed transition identified by crystallography. Biochem 39: 16135-16146.
39. Málnási-Csizmadia A, Pearson DS, Kovács M, Woolley RJ, Geeves MA, et al. (2001) Kinetic resolution of a conformational transition and the ATP hydrolysis step using relaxation methods with a Dictyostelium myosin II mutant containing a single tryptophan residue. Biochemistry 40: 12727-12737.
40. Málnási-Csizmadia A, Kovács M, Woolley RJ, Botchway SW, Bagshaw CR (2001) The dynamics of the relay loop tryptophan residue in the Dictyostelium myosin motor domain and the origin of spectroscopic signals. J Biol Chem 276: 19483-19490.
41. Tama F, Gadea FX, Marques O, Sanejouand YH (2000) Building-block approach for determining low-frequency normal modes of macromolecules. Proteins 41: 1-7.
42. 2+-ATPase. Biophys J 83: 2457-2474.
43. Navizet I, Lavery R, Jernigan RL (2004) Myosin flexibility: Structural domains and collective vibrations. Proteins: Structure, Function, and Bioinformatics 54: 384-393.
44. Sasaki N, Shimada T, Sutoh K (1998) Mutational analysis of the switch II loop of Dictyostelium myosin II. J Biol Chem 273: 20334-20340.
45. Murphy CT, Spudich JA (1999) The sequence of the myosin 50-20-K loop affects myosin's affinity for actin throughout the actin-myosin ATPase cycle and its maximum ATPase activity. Biochem 38: 3785-3792.
46. Volkmann N, Hanein D, Ouyang G, Trybus KM, DeRosier DJ, et al. (2000) Evidence for cleft closure in actomyosin upon ADP release. Nat Struct Biol 7: 1147-1155.
47. Joel PB, Trybus KM, Sweeney HL (2001) Two conserved lysines at the 50/20 kDa junction of myosin are necessary for triggering actin activation. J Biol Chem 276: 2998-3003.
48. Joel PB, Sweeney HL, Trybus KM (2003) Addition of lysines to the 50/20 kDa junction of myosin strengthens weak binding to actin without affecting the maximum ATPase activity. Biochem 42: 9160-9166.
49. Volkmann N, Ouyang G, Trybus KM, DeRosier DJ, Lowey S, et al. (2003) Myosin isoforms show unique conformations in the actin-bound state. Proc Acad Natl Sci U S A 100: 3227-3232.
50. Shih WM, Gryczynski Z, Lakowicz JR, Spudich JA (2000) A FRET-based sensor reveals large ATP hydrolysis-induced conformational changes and three distinct states of the molecular motor myosin. Cell 102: 683-694.
51. Burgess SA, Walker ML, White HD, Trinick J (1997) Flexibility within myosin heads revealed by negative stain and single-particle analysis. J Cell Biol 139: 675-681.
52. Volkman BF, Lipson D, Wemmer DE, Kern D (2001) Two-state allosteric behavior in a single-domain signaling protein. Science 291: 2429-2433.
53. Jardetzky O (1996) Protein dynamics and conformational transitions in allosteric proteins. Prog Biophys Mol Biol 65: 171-219.
54. Formaneck MS, Ma L, Cui Q (2006) Reconciling the "old" and "new" views of protein allostery. A molecular simulation study of chemotaxis Y protein (CheY). Proteins 83: 846-867.
55. Hall BE, Bar-Sagi D, Nassar N (2002) The structural basis for the transition from ras-GTP to ras-GDP. Proc Acad Natl Sci U S A 99: 12138-12142.
56. Dyner CM, Dahlquist FW (2006) Switched or not? The structure of unphosphorylated CheY bound to the N terminus of FliM. J Bacter 188: 7354-7363.
57. Stock AM, Guhaniyogi J (2006) A new perspective on response regulator activation. J Bacter 188: 7328-7330.
58. Shih WM, Spudich JA (2001) The myosin relay helix to converter interface remains intact throughout the actomyosin ATPase cycle. J Biol Chem 276: 19491-19494.
59. Daily MD, Gray JJ (2006) Local motions in a benchmark of allosteric proteins. Proteins: Structure, function, and bioinformatics. In press.
60. Tsiavaliaris G, Fujita-Becker S, Batra R, Levitsky DI, Kull FJ, et al. (2002) Mutations in the relay loop region result in dominant-negative inhibition of myosin II function in Dictyostelium. EMBO Reports 3: 1099-1105.
61. Coureux PD, Wells AL, Menetry J, Yengo CM, Morris CA, et al. (2003) A structural state of the myosin V motor without bound nucleotide. Nature 425: 419-423.
62. Holmes KC, Angert I, Kull FJ, Jahn W, Schroder RR (2003) Electron cryomicroscopy shows how strong binding of myosin to actin releases nucleotide. Nature 425: 423-427.
63. Murphy CT, Spudich JA (1998) Dictyostelium myosin 25-50-K loop substitutions specifically affect ADP release rates. Biochem 37: 6738-6744.
64. Kurzawa-Goertz SE, Perreault-Micale CL, Trybus KM, Szent-Györgyi AG, Geeves MA (1998) Loop I can modulate ADP affinity, ATPase activity, and motility of different scallop myosins. Transient kinetic analysis of S1 isoforms. Biochem 37: 7517-7525.
65. Sweeney HL, Rosenfeld SS, Brown F, Faust L, Smith J, et al. (1998) Kinetic tuning of myosin via a flexible loop adjacent to the nucleotide binding pocket. J Biol Chem 273: 6262-6270.
66. Murphy CT, Rock RS, Spudich JA (2001) A myosin II mutation uncouples ATPase activity from motility and shortens step size. Nat Cell Biol 3: 311-315.
67. Ruppel KM, Spudich JA (1996) Structure-function studies of the myosin motor domain: Importance of the 50-kDa cleft. Mol Biol Cell 7: 1123-1136.
68. Suzuki Y, Ohkura R, Sugiura S, Yasuda R, Kinoshita K, et al. (1997) Modulation of actin filament sliding by mutations of the SH2 cysteine in dictyostelium myosin II. Biochem Biophys Res Commun 234: 701-706.
69. 1-ATPase. J Mol Biol 340: 345-372.
70. MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102: 3586-3616.
71. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79: 926-935.
72. Im W, Lee M, Brooks CL III (2003) Generalized born model with a simple smoothing function. J Comput Chem 24: 1691-1702.
73. Ryckaert JP, Ciccotti G, Berendsen HJC (1977) Numerical integration of Cartesian equations of motion of a system with constraints - Molecular dynamics of n-alkanes. J Comput Phys 23: 327-341.
74. Nina M, Beglov D, Roux B (1997) Atomic radii for continuum electrostatics calculations based on molecular dynamics free energy simulations. J Phys Chem B 101: 5239-5248.
75. Nina M, Im W, Roux B (1999) Optimized atomic radii for protein continuum electrostatics solvation forces. Biophys Chem 78: 89-96.
76. Berendsen HJC, Postma JPM, van Gunsteren WF, Di Nola A, Haak JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81: 3684-3690.
77. Lee B, Richards FM (1971) Interpretation of protein structures: Estimation of static accessibility. J Mol Biol 55: 379-380.
78. Lazaridis T, Karplus M (1999) Effective energy function for proteins in solution. Proteins 35: 133-152.
79. Neria E, Fischer S, Karplus M (1996) Simulation of activation free energies in molecular systems. J Chem Phys 105: 1902-1921.
80. Brooks B, Karplus M (1985) Normal-modes for specific motions of macromolecules: Application to the hinge-bending mode of lysozyme. Proc Natl Acad Sci U S A 82: 4995-4999.
81. Tama F, Sanejouand YH (2001) Conformational change of proteins arising from normal mode calculations. Prot Eng 14: 1-6.
82. Brooks CL III, Karplus M, Pettitt BM (1988) Proteins: A theoretical perspective of dynamics, structure, and thermodynamics. New York: Wiley and Sons.
83. Van Wynsberghe AW, Cui Q (2006) Interpretating correlated motions using normal mode analysis. Structure 14: 1647-1653.
84. Hayward S, Kitao A, Berendsen HJC (1997) Model-free methods of analyzing domain motions in proteins from simulation: A comparison of normal mode analysis and molecular dynamics simulation of lysozyme. Proteins 27: 425-437.
85. Hayward S, Berendsen HJC (1998) Systematic analysis of domain motions in proteins from conformational change: New results on citrate synthase and T4 lysozyme. Proteins 30: 144-154.
86. Pruitt KD, Tatusova T, Maglott DR (2005) NCBI Reference Sequence (RefSeq): A curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 33: D501-D504.
87. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
88. Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.