Insights into the importance of hydrogen bonding in the γ-phosphate binding pocket of myosin: Structural and functional studies of serine 236

Biochemistry

Volumn 49, Issue 23, 2010, Pages 4897-4907

  Frye, Jeremiah J ^a   Klenchin, Vadim A ^a   Bagshaw, Clive R ^b   Rayment, Ivan ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; AMINO ACID RESIDUES; ATP HYDROLYSIS; CRITICAL FUNCTIONS; DICTYOSTELIUM DISCOIDEUM; ENERGY TRANSDUCTION; HYDROGEN BONDINGS; HYDROGEN TRANSFER; HYDROLYTIC ACTIVITIES; KINETIC ANALYSIS; KINETIC STUDY; KINETIC VALUES; MOTOR DOMAIN; MUTANT PROTEINS; MYOSIN II; NUCLEOTIDE HYDROLYSIS; PHOSPHATE BINDING; STRUCTURAL MECHANISMS; WATER MOLECULE; WILD TYPES;

AMINO ACIDS; ENERGY CONSERVATION; HYDROGEN BONDS; HYDROLYSIS; MAGNESIUM; NUCLEOTIDES; ORGANIC ACIDS; PHOSPHATASES;

PROTEINS;

MAGNESIUM PYROPHOSPHATE; MUTANT PROTEIN; MYOSIN; PYROPHOSPHATE; SERINE 236; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; BINDING SITE; CRYSTAL STRUCTURE; DICTYOSTELIUM DISCOIDEUM; HYDROGEN BOND; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN HYDROLYSIS; PROTEIN STRUCTURE, FUNCTION AND VARIABILITY; STRUCTURE ANALYSIS;

ACTINS; ADENOSINE TRIPHOSPHATE; ADENYLYL IMIDODIPHOSPHATE; ANIMALS; BINDING SITES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DICTYOSTELIUM; HYDROGEN BONDING; MYOSIN TYPE II; MYOSINS; SERINE; STRUCTURE-ACTIVITY RELATIONSHIP;

DICTYOSTELIUM DISCOIDEUM;

EID: 77953255485     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1001344     Document Type: Article

References (43)

1. Geeves, M. A. and Holmes, K. C. (1999) Structural mechanism of muscle contraction Annu. Rev. Biochem. 68, 687-728
2. Howard, J. (2001) Mechanics of motor proteins and the cytoskeleton, Sinauer Associates, Sunderland, MA.
3. Wakelin, S., Conibear, P. B., Woolley, R. J., Floyd, D. N., Bagshaw, C. R., Kovacs, M., and Malnasi-Csizmadia, A. (2002) Engineering Dictyostelium discoideum myosin II for the introduction of site-specific fluorescence probes J. Muscle Res. Cell Motil. 23, 673-683
4. De La Cruz, E. M. and Ostap, E. M. (2004) Relating biochemistry and function in the myosin superfamily Curr. Opin. Cell Biol. 16, 61-67
5. Zeng, W., Conibear, P. B., Dickens, J. L., Cowie, R. A., Wakelin, S., Malnasi-Csizmadia, A., and Bagshaw, C. R. (2004) Dynamics of actomyosin interactions in relation to the cross-bridge cycle Philos. Trans. R. Soc. London, Ser. B 359, 1843-1855
6. El-Mezgueldi, M. and Bagshaw, C. R. (2008) The myosin family: biochemical and kinetic properties, in Myosins: a superfamily of molecular motors (Coluccio, L. M., Ed.) pp 55-93, Springer, Berlin.
7. Malnasi-Csizmadia, A., Woolley, R. J., and Bagshaw, C. R. (2000) 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, 16135-16146
8. Kovacs, M., Malnasi-Csizmadia, A., Woolley, R. J., and Bagshaw, C. R. (2002) Analysis of nucleotide binding to Dictyostelium myosin II motor domains containing a single tryptophan near the active site J. Biol. Chem. 277, 28459-28467
9. Bagshaw, C. R., Eccleston, J. F., Eckstein, F., Goody, R. S., Gutfreund, H., and Trentham, D. R. (1974) The magnesium ion-dependent adenosine triphosphatase of myosin. Two-step processes of adenosine triphosphate association and adenosine diphosphate dissociation Biochem. J. 141, 351-364
10. Johnson, K. A. and Taylor, E. W. (1978) Intermediate states of subfragment 1 and actosubfragment 1 ATPase: reevaluation of the mechanism Biochemistry 17, 3432-3442
11. Millar, N. C. and Geeves, M. A. (1988) Protein fluorescence changes associated with ATP and adenosine 5′-[gamma-thio]triphosphate binding to skeletal muscle myosin subfragment 1 and actomyosin subfragment 1 Biochem. J. 249, 735-743
12. Kurzawa, S. E., Manstein, D. J., and Geeves, M. A. (1997) Dictyostelium discoideum myosin II: characterization of functional myosin motor fragments Biochemistry 36, 317-323
13. Kuhlman, P. A. and Bagshaw, C. R. (1998) ATPase kinetics of the Dictyostelium discoideum myosin II motor domain J. Muscle Res. Cell Motil. 19, 491-504
14. Malnasi-Csizmadia, A., Pearson, D. S., Kovacs, M., Woolley, R. J., Geeves, M. A., and Bagshaw, C. R. (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
15. Batra, R. and Manstein, D. J. (1999) Functional characterisation of Dictyostelium myosin II with conserved tryptophanyl residue 501 mutated to tyrosine Biol. Chem. 380, 1017-1023
16. 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. (1993) Three-dimensional structure of myosin subfragment-1: a molecular motor Science 261, 50-58 (Pubitemid 23265379)
17. Dominguez, R., Freyzon, Y., Trybus, K. M., and Cohen, C. (1998) Crystal structure of a vertebrate smooth muscle myosin motor domain and its complex with the essential light chain: visualization of the pre-power stroke state Cell 94, 559-571
18. Fisher, A. J., Smith, C. A., Thoden, J. B., Smith, R., Sutoh, K., Holden, H. M., and Rayment, I. (1995) X-ray structures of the myosin motor domain of Dictyostelium discoideum complexed with MgADPBeFx and MgADPAlF4 Biochemistry 34, 8960-8972
19. Coureux, P. D., Wells, A. L., Menetrey, J., Yengo, C. M., Morris, C. A., Sweeney, H. L., and Houdusse, A. (2003) A structural state of the myosin V motor without bound nucleotide Nature 425, 419-423
20. Coureux, P. D., Sweeney, H. L., and Houdusse, A. (2004) Three myosin V structures delineate essential features of chemo-mechanical transduction EMBO J. 23, 4527-4537
21. Menetrey, J., Bahloul, A., Wells, A. L., Yengo, C. M., Morris, C. A., Sweeney, H. L., and Houdusse, A. (2005) The structure of the myosin VI motor reveals the mechanism of directionality reversal Nature 435, 779-785
22. Yang, Y., Gourinath, S., Kovacs, M., Nyitray, L., Reutzel, R., Himmel, D. M., ONeall-Hennessey, E., Reshetnikova, L., Szent-Gyorgyi, A. G., Brown, J. H., and Cohen, C. (2007) Rigor-like structures from muscle myosins reveal key mechanical elements in the transduction pathways of this allosteric motor Structure 15, 553-564
23. Smith, C. A. and Rayment, I. (1996) X-ray structure of the magnesium(II)ADPvanadate complex of the Dictyostelium discoideum myosin motor domain to 1.9 Å resolution Biochemistry 35, 5404-5417
24. Holmes, K. C., Schroder, R. R., Sweeney, H. L., and Houdusse, A. (2004) The structure of the rigor complex and its implications for the power stroke Philos. Trans. R. Soc. London, Ser. B 359, 1819-1828
25. Smith, C. A. and Rayment, I. (1995) X-ray structure of the magnesium(II)-pyrophosphate complex of the truncated head of Dictyostelium discoideum myosin to 2.7 Å resolution Biochemistry 34, 8973-8981
26. Gulick, A. M., Bauer, C. B., Thoden, J. B., and Rayment, I. (1997) X-ray structures of the MgADP, MgATPgammaS, and MgAMPPNP complexes of the Dictyostelium discoideum myosin motor domain Biochemistry 36, 11619-11628
27. Li, X. D., Rhodes, T. E., Ikebe, R., Kambara, T., White, H. D., and Ikebe, M. (1998) Effects of mutations in the gamma-phosphate binding site of myosin on its motor function J. Biol. Chem. 273, 27404-27411
28. Shimada, T., Sasaki, N., Ohkura, R., and Sutoh, K. (1997) Alanine scanning mutagenesis of the switch I region in the ATPase site of Dictyostelium discoideum myosin II Biochemistry 36, 14037-14043
29. Li, G. H. and 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
30. Kovacs, M., Toth, J., Hetenyi, C., Malnasi-Csizmadia, A., and Sellers, J. R. (2004) Mechanism of blebbistatin inhibition of myosin II J. Biol. Chem. 279, 35557-35563
31. Xu, S., White, H. D., Offer, G. W., and Yu, L. C. (2009) Stabilization of helical order in the thick filaments by blebbistatin: further evidence of coexisting multiple conformations of myosin Biophys. J. 96, 3673-3681
32. Manstein, D. J., Schuster, H. P., Morandini, P., and Hunt, D. M. (1995) Cloning vectors for the production of proteins in Dictyostelium discoideum Gene 162, 129-134
33. Manstein, D. J. and Hunt, D. M. (1995) Overexpression of myosin motor domains in Dictyostelium: screening of transformants and purification of the affinity tagged protein J. Muscle Res. Cell Motil. 16, 325-332
34. Allingham, J. S., Smith, R., and Rayment, I. (2005) The structural basis of blebbistatin inhibition and specificity for myosin II Nat. Struct. Mol. Biol. 12, 378-379
35. Blommel, P. G. and Fox, B. G. (2007) A combined approach to improving large-scale production of tobacco etch virus protease Protein Expression Purif. 55, 53-68
36. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326
37. Vagin, A. and Teplyakov, A. (2000) An approach to multi-copy search in molecular replacement Acta Crystallogr., Sect. D: Biol. Crystallogr. 56, 1622-1624
38. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D: Biol. Crystallogr. 53, 240-255
39. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132
40. Walmsley, A. R. and Bagshaw, C. R. (1989) Logarithmic timebase for stopped-flow data acquisition and analysis Anal. Biochem. 176, 313-318
41. Bauer, C. B., Holden, H. M., Thoden, J. B., Smith, R., and 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 (Pubitemid 32009176)
42. DeLano, W. L. (2002) The PyMOL Molecular Graphics System.
43. Cohen, G. H. (1997) ALIGN: a program to superimpose protein coordinates, accounting for insertions and deletions J. Appl. Crystallogr. 30, 1160-1161