The Structural Coupling between ATPase Activation and Recovery Stroke in the Myosin II Motor

Structure

Volumn 15, Issue 7, 2007, Pages 825-837

  Koppole, Sampath ^a   Smith, Jeremy C ^a,b   Fischer, Stefan ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; MOLECULAR MOTOR; MYOSIN II;

ARTICLE; CELL MOTILITY; DICTYOSTELIUM DISCOIDEUM; ENZYME ACTIVATION; MOLECULAR MECHANICS; MUSCLE CONTRACTILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION;

ADENOSINE TRIPHOSPHATASES; ANIMALS; DICTYOSTELIUM; ENZYME ACTIVATION; MODELS, MOLECULAR; MOTION; MYOSIN TYPE II; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

DICTYOSTELIUM DISCOIDEUM;

EID: 34447276474     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2007.06.008     Document Type: Article

References (57)

1. Bashford D., and Case D.A. Generalized Born models of macromolecular solvation effects. Annu. Rev. Phys. Chem. 51 (2000) 129-152
2. Batra R., Geeves M.A., and Manstein D.J. Kinectic analysis of Dictyostelium discoideum myosin motor domains with glycine-to-alanine mutations in the reactive thiol region. Biochemistry 38 (1999) 6126-6134
3. Bondar A.N., Elstner M., Suhai S., Smith J.C., and Fischer S. Mechanism of primary proton transfer in bacteriorhodopsin. Structure 12 (2004) 1281-1288
4. Brooks B.R., Bruccoleri R.E., Olafson B.D., States D.J., Swaminathan S., and Karplus M. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4 (1983) 87-217
5. Cope M.J.T.V., Whisstock J., Rayment I., and Jones J.K. Conservation within the myosin motor domain: implications for structure and function. Structure 4 (1996) 969-987
6. Coureux P.D., Sweeney H.L., and Houdusse A. Three myosin V structures delineate essential features of chemo-mechanical transduction. EMBO J. 23 (2004) 4527-4537
7. Dutzler R., Schirmer T., Karplus M., and Fischer S. Translocation mechanism of long sugar chains across the maltoporin membrane channel. Structure 10 (2002) 1273-1284
8. Fischer S., and Karplus M. Conjugate Peak Refinement: an algorithm for finding reaction paths and accurate transition states in systems with many degrees of freedom. Chem. Phys. Lett. 194 (1992) 252-261
9. Fischer S., Dunbrack Jr. R.L., and Karplus M. Cis-trans imide isomerization of the proline dipeptide. J. Am. Chem. Soc. 116 (1994) 11931-11937
10. Fischer S., Windshügel B., Horak D., Holmes K.C., and Smith J.C. Structural mechanism of the recovery stroke in the myosin molecular motor. Proc. Natl. Acad. Sci. USA 102 (2005) 6873-6878
11. 4. Biochemistry 34 (1995) 8960-8972
12. Geeves M.A., and Holmes K.C. Structural mechanism of muscle contraction. Annu. Rev. Biochem. 68 (1999) 687-728
13. Geeves M.A., and Holmes K.C. The molecular mechanism of muscle contraction. Adv. Protein Chem. 71 (2005) 161-193
14. Gulick A.M., Bauer C.B., Thoden J.B., and Rayment I. X-ray structures of the Mg·ADP, Mg·ATP·γS, and Mg·AMP·PNP complexes of the Dictyostelium discoideum myosin motor domain. Biochemistry 36 (1997) 11618-11619
15. Hayward S., and Berendsen H.J.C. Systematic analysis of domain motions in proteins from conformational change: new results on citrate synthase and T4 lysozyme. Proteins 30 (1998) 144-154
16. Hodge T., and Cope M.J.T.V. Myosin motor domain sequence alignment (2000), MRC Laboratory of Molecular Biology, Cambridge, UK. http://www.mrc-lmb.cam.ac.uk/myosin/trees/colour.html
17. Holmes K.C., and Geeves M.A. The structural basis of muscle contraction. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355 (2000) 419-431
18. Holmes K.C., Schröder R.R., Eschenburg S., Sweeney H.L., and Houdusse A. The structure of the rigor complex and its implications for the power-stroke. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359 (2004) 1819-1828
19. Hoover W.G. Canonical dynamics: equilibrium phase-space distributions. Phys. Rev. A. 31 (1985) 1695-1697
20. Humphrey W., Dalke A., and Schulten K. VMD: visual molecular dynamics. J. Mol. Graph. Model. 14 (1996) 33-38
21. Im W., Beglov D., and Roux B. Continuum solvation model: electrostatic forces from numerical solutions to the Poisson-Bolztmann equation. Comput. Phys. Commun. 111 (1998) 59-75
22. Itakura S., Yamakawa H., Toyoshima Y.Y., Ishijima A., Kojima T., Harada Y., Yanagida T., Wakabayashi T., and Sutoh K. Force-generating domain of myosin motor. Biochem. Biophys. Res. Commun. 196 (1993) 1504-1510
23. Karamanou S., Vrontou E., Sianidis G., Baud C., Roos T., Kuhn A., Politou A.S., and Economou A. A molecular switch in SecA protein couples ATP hydrolysis to protein translocation. Mol. Microbiol. 34 (1999) 1133-1145
24. Kirkpatrick S., Gelatt C.D., and Vecchi M.P. Optimization by simulated annealing. Science 220 (1983) 671-680
25. Koppole S., Smith J.C., and Fischer S. Simulations of the myosin II motor reveal a nucleotide-state sensing element that controls the recovery stroke. J. Mol. Biol. 361 (2006) 604-616
26. Kuriyan J., Brunger A.T., Karplus M., and Hendrickson W.A. X-ray refinement of protein structures by simulated annealing: test of the method on myohemerythrin. Acta Crystallogr. A 45 (1989) 396-409
27. Li G., and Cui Q. Mechanochemical coupling in myosin: a theoretical analysis with molecular dynamics and combined QM/MM reaction path calculations. J. Phys. Chem. B 108 (2004) 3342-3357
28. Lymn R.W., and Taylor E.W. Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10 (1971) 4617-4624
29. Malnasi-Csizmadia A., Pearson D.S., Kovacs M., Woolley R.J., Geeves M.A., and Bagshaw C.R. 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 (2001) 12727-12737
30. Malnasi-Csizmadia A., Woolley R.J., and Bagshaw C.R. Resolution of conformational states of Dictyostelium myosin II motor domain using tryptophan (W501) mutants: implications for the open-closed transition identified by crystallography. Biochemistry 39 (2000) 16135-16146
31. Mesentean S., Koppole S., Smith J.C., and Fischer S. The principal motions involved in the coupling mechanism of the recovery stroke of the myosin motor. J. Mol. Biol. 367 (2007) 591-602
32. Murphy T., Rock R.S., and Spudich J.A. A myosin II mutation uncouples ATPase activity from motility and shortens step size. Nat. Cell Biol. 33 (2001) 311-315
33. Neria E., Fischer S., and Karplus M. Simulation of activation free energies in molecular systems. J. Chem. Phys. 105 (1996) 1902-1921
34. Noé F., Ille F., Smith J.C., and Fischer S. Automated computation of low-energy pathways for complex rearrangements in proteins: application to the conformational switch of Ras p21. Proteins 59 (2004) 534-544
35. Noé F., Krachtus D., Smith J.C., and Fischer S. Transition networks for the comprehensive characterization of complex conformational change in proteins. J. Chem. Theory Comput. 2 (2006) 840-857
36. Norberg J., and Nilsson L. On the truncation of long-range electrostatic interactions in DNA. Biophys. J. 79 (2000) 1537-1553
37. Nosé S. A unified formulation of the constant temperature molecular dynamics methods. J. Chem. Phys. 81 (1984) 511-519
38. Patterson B., Ruppel K.M., Wu Y., and Spudich J.A. Cold-sensitive mutants G680V and G691C of Dictyostelium myosin II confer dramatically different biochemical defects. J. Biol. Chem. 272 (1997) 27612-27617
39. Rayment I., Rypniewski W.R., Schmidt-Bäse K., Smith R., Tomchick D.R., Benning M.M., Winkelmann D.A., Wesenberg G., and Holden H.M. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261 (1993) 50-58
40. Reubold T.F., Eschenburg S., Becker A., Kull F.J., and Manstein D.J. A structural model for actin-induced nucleotide release in myosin. Nat. Struct. Biol. 10 (2003) 826-830
41. Sasaki N., and Sutoh K. Structure-mutation analysis of the ATPase site of Dictyostelium discoideum myosin II. Adv. Biophys. 35 (1998) 1-24
42. Sasaki N., Shimada T., and Sutoh K. Mutational analysis of the switch II loop of Dictyostelium myosin II. J. Biol. Chem. 273 (1998) 20334-20340
43. Schaefer M., and Karplus M. A comprehensive analytical treatment of continuum electrostatics. J. Phys. Chem. B 100 (1996) 1578-1599
44. Schaefer M., Bartels C., and Karplus M. Solution conformations and thermodynamics of structured peptides: molecular dynamics simulation with an implicit solvation model. J. Mol. Biol. 284 (1998) 835-847
45. Schlitter J., Engels M., and Kruger P. Targeted molecular dynamics: a new approach for searching pathways of conformational transitions. J. Mol. Graph. 12 (1994) 84-89
46. Schwarzl S.M., Smith J.C., and Fischer S. Insights into the chemomechanical coupling of the myosin motor from simulation of its ATP hydrolysis mechanism. Biochemistry 45 (2006) 5830-5847
47. Sellers J.R. Myosins: a diverse superfamily. Biochim. Biophys. Acta 1496 (2000) 3-22
48. Smith A., and Rayment I. X-ray structure of the magnesium(II)·ADP·vanadate complex of the Dictyostelium discoideum myosin motor domain to 1.9 Å resolution. Biochemistry 35 (1996) 5404-5417
49. Sopkova-De Oliveira Santos J., Fischer S., Guilbert C., Lewit-Bentley A., and Smith J.C. Pathway for large-scale conformational change in annexin V. Biochemistry 39 (2000) 14065-14074
50. Spudich J.A. The myosin swinging cross-bridge model. Nat. Rev. Mol. Cell Biol. 2 (2001) 387-392
51. Still W.C., Tempczyk A., Hawley R.C., and Hendrickson T. Semi-analytical treatment of solvation for molecular mechanics and dynamics. J. Am. Chem. Soc. 112 (1990) 6127-6129
52. Tsiavaliaris G., Fujita-Becker S., Batra R., Levitsky D.I., Kull J.F., Geeves M.A., and Manstein D.J. Mutations in the relay loop region result in dominant-negative inhibition of myosin II function in Dictyostelium. EMBO Rep. 3 (2002) 1099-1105
53. Urbanke A., and Wray J. A fluorescence temperature-jump study of conformational transitions in myosin subfragment 1. Biochem. J. 358 (2001) 165-173
54. Warrick H.M., and Spudich J.A. Myosin structure and function in cell motility. Annu. Rev. Cell Biol. 3 (1987) 379-421
55. Weber J., and Senior A.E. ATP synthase: what we know about ATP hydrolysis and what we do not know about ATP synthesis. Biochim. Biophys. Acta 1458 (2000) 300-309
56. Yu H., Ma L., Yang Y., and Cui Q. Mechanochemical coupling in the myosin motor domain. I: insights from equilibrium active-site simulations. PLoS-Computational Biology 3 (2007) 199-213
57. Yu H., Ma L., Yang Y., and Cui Q. Mechanochemical coupling in the myosin motor domain. II: analysis of critical residues. PLoS Comput. Biol. 3 (2007) 214-230