Predicting Allosteric Communication in Myosin via a Pathway of Conserved Residues

Journal of Molecular Biology

Volumn 373, Issue 5, 2007, Pages 1361-1373

  Tang, Susan ^a   Liao, Jung Chi ^a   Dunn, Alexander R ^b   Altman, Russ B ^a   Spudich, James A ^b   Schmidt, Jeanette P ^a  

^a Stanford University   (United States)

^b STANFORD UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

allostery; computation; conservation; myosin; pathway

Indexed keywords

ADENOSINE TRIPHOSPHATE; MYOSIN; MYOSIN I; MYOSIN II;

ALLOSTERISM; ANALYTIC METHOD; ARTICLE; CHICKEN; CONFORMATIONAL TRANSITION; DICTYOSTELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; RESIDUE ANALYSIS; SCALLOP; SEQUENCE ALIGNMENT;

DICTYOSTELIUM;

EID: 35148894521     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.08.059     Document Type: Article

References (50)

1. Dang Q.D., and Di Cera E. Residue 225 determines the Na(+)-induced allosteric regulation of catalytic activity in serine proteases. Proc. Natl Acad. Sci. USA 93 (1996) 10653-10656
2. Gether U. Uncovering molecular mechanisms involved in activation of G protein-coupled receptors. Endocr. Rev. 21 (2000) 90-113
3. Perutz M.F. Stereochemistry of cooperative effects in haemoglobin. Nature 228 (1970) 726-739
4. Koshland Jr. D.E., Nemethy G., and Filmer D. Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5 (1966) 365-385
5. Keskin O., Bahar I., Flatow D., Covell D.G., and Jernigan R.L. Molecular mechanisms of chaperonin GroEL-GroES function. Biochemistry 41 (2002) 491-501
6. Houdusse A., Szent-Gyorgyi A.G., and Cohen C. Three conformational states of scallop myosin S1. Proc. Natl Acad. Sci. USA 97 (2000) 11238-11243
7. Cheney R.E., and Mooseker M.S. Unconventional myosins. Curr. Opin. Cell Biol. 4 (1992) 27-35
8. Suel G.M., Lockless S.W., Wall M.A., and Ranganathan R. Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nature Struct. Biol. 10 (2003) 59-69
9. Cope M.J., Whisstock J., Rayment I., and Kendrick-Jones J. Conservation within the myosin motor domain: implications for structure and function. Structure 4 (1996) 969-987
10. Smith C.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
11. Zheng W., and Brooks B. Identification of dynamical correlations within the myosin motor domain by the normal mode analysis of an elastic network model. J. Mol. Biol. 346 (2005) 745-759
12. Guex N., and Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18 (1997) 2714-2723
13. Shatsky M., Nussinov R., and Wolfson H.J. A method for simultaneous alignment of multiple protein structures. Proteins: Struct. Funct. Genet. 56 (2004) 143-156
14. Gourinath S., Himmel D.M., Brown J.H., Reshetnikova L., Szent-Gyorgyi A.G., and Cohen C. Crystal structure of scallop myosin S1 in the pre-power stroke state to 2.6 Å resolution: flexibility and function in the head. Structure 11 (2003) 1621-1627
15. Kollmar M., Durrwang U., Kliche W., Manstein D.J., and Kull F.J. Crystal structure of the motor domain of a class-I myosin. EMBO J. 21 (2002) 2517-2525
16. Dominguez R., Freyzon Y., Trybus K.M., and Cohen C. 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 (1998) 559-571
17. Allingham J.S., Smith R., and Rayment I. The structural basis of blebbistatin inhibition and specificity for myosin II. Nature Struct. Mol. Biol. 12 (2005) 378-379
18. Himmel D.M., Gourinath S., Reshetnikova L., Shen Y., Szent-Gyorgyi A.G., and Cohen C. Crystallographic findings on the internally uncoupled and near-rigor states of myosin: further insights into the mechanics of the motor. Proc. Natl Acad. Sci. USA 99 (2002) 12645-12650
19. 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
20. Fisher A.J., Smith C.A., Thoden J.B., Smith R., Sutoh K., Holden H.M., and Rayment I. X-ray structures of the myosin motor domain of Dictyostelium discoideum complexed with MgADP.BeFx and MgADP.AlF4. Biochemistry 34 (1995) 8960-8972
21. Bauer C.B., Holden H.M., Thoden J.B., Smith R., and Rayment I. X-ray structures of the apo and MgATP-bound states of Dictyostelium discoideum myosin motor domain. J. Biol. Chem. 275 (2000) 38494-38499
22. Gulick A.M., Bauer C.B., Thoden J.B., and Rayment I. X-ray structures of the MgADP, MgATPgammaS, and MgAMPPNP complexes of the Dictyostelium discoideum myosin motor domain. Biochemistry 36 (1997) 11619-11628
23. Reubold T.F., Eschenburg S., Becker A., Leonard M., Schmid S.L., Vallee R.B., et al. Crystal structure of the GTPase domain of rat dynamin 1. Proc. Natl Acad. Sci. USA 102 (2005) 13093-13098
24. Coureux P.D., Wells A.L., Menetrey J., Yengo C.M., Morris C.A., Sweeney H.L., and Houdusse A. A structural state of the myosin V motor without bound nucleotide. Nature 425 (2003) 419-423
25. Zheng W., Brooks B.R., and Thirumalai D. Low-frequency normal modes that describe allosteric transitions in biological nanomachines are robust to sequence variations. Proc. Natl Acad. Sci. USA 103 (2006) 7664-7669
26. Zheng W., and Doniach S. A comparative study of motor-protein motions by using a simple elastic-network model. Proc. Natl Acad. Sci. USA 100 (2003) 13253-13258
27. Fischer S., Windshugel 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
28. 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
29. Lockless S.W., and Ranganathan R. Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286 (1999) 295-299
30. Yu H., Ma L., Yang Y., and Cui Q. Mechanochemical coupling in the myosin motor domain. I. Insights from equilibrium active-site simulations. PLoS Comput. Biol. 3 (2007) e21
31. 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) e23
32. Spudich J.A. The myosin swinging cross-bridge model. Nature Rev. Mol. Cell. Biol. 2 (2001) 387-392
33. Houdusse A., Kalabokis V.N., Himmel D., Szent-Gyorgyi A.G., and Cohen C. Atomic structure of scallop myosin subfragment S1 complexed with MgADP: a novel conformation of the myosin head. Cell 97 (1999) 459-470
34. Reubold T.F., Eschenburg S., Becker A., Kull F.J., and Manstein D.J. A structural model for actin-induced nucleotide release in myosin. Nature Struct. Biol. 10 (2003) 826-830
35. Lawson J.D., Pate E., Rayment I., and Yount R.G. Molecular dynamics analysis of structural factors influencing back door Pi release in myosin. Biophys. J. 86 (2004) 3794-3803
36. Murphy C.T., Rock R.S., and Spudich J.A. A myosin II mutation uncouples ATPase activity from motility and shortens step size. Nature Cell Biol. 3 (2001) 311-315
37. Smith C.A., and Rayment I. Active site comparisons highlight structural similarities between myosin and other P-loop proteins. Biophys. J. 70 (1996) 1590-1602
38. Kull F.J., Vale R.D., and Fletterick R.J. The case for a common ancestor: kinesin and myosin motor proteins and G proteins. J. Muscle Res. Cell Motil. 19 (1998) 877-886
39. Goody R.S., and Hofmann-Goody W. Exchange factors, effectors, GAPs and motor proteins: common thermodynamic and kinetic principles for different functions. Eur. Biophys. J. 31 (2002) 268-274
40. 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
41. Ito K., Uyeda T.Q., Suzuki Y., Sutoh K., and Yamamoto K. Requirement of domain-domain interaction for conformational change and functional ATP hydrolysis in myosin. J. Biol. Chem. 278 (2003) 31049-31057
42. Tsiavaliaris G., Fujita-Becker S., Batra R., Levitsky D.I., Kull F.J., 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
43. Sasaki N., Ohkura R., and Sutoh K. Dictyostelium myosin II mutations that uncouple the converter swing and ATP hydrolysis cycle. Biochemistry 42 (2003) 90-95
44. Batra R., Geeves M.A., and Manstein D.J. Kinetic analysis of Dictyostelium discoideum myosin motor domains with glycine-to-alanine mutations in the reactive thiol region. Biochemistry 38 (1999) 6126-6134
45. Uyeda T.Q., Tokuraku K., Kaseda K., Webb M.R., and Patterson B. Evidence for a novel, strongly bound acto-S1 complex carrying ADP and phosphate stabilized in the G680V mutant of Dictyostelium myosin II. Biochemistry 41 (2002) 9525-9534
46. Shih W.M., and Spudich J.A. The myosin relay helix to converter interface remains intact throughout the actomyosin ATPase cycle. J. Biol. Chem. 276 (2001) 19491-19494
47. Richards T.A., and Cavalier-Smith T. Myosin domain evolution and the primary divergence of eukaryotes. Nature 436 (2005) 1113-1118
48. Miyata T., Miyazawa S., and Yasunaga T. Two types of amino acid substitutions in protein evolution. J. Mol. Evol. 12 (1979) 219-236
49. Wei L., Altman R.B., and Chang J.T. Using the radial distributions of physical features to compare amino acid environments and align amino acid sequences. Pac. Symp. Biocomput. (1997) 465-476
50. Dijkstra E.W. A note on two problems in connexion with graphs. Numerische Mathematik V1 (1959) 269-271