Multiple conformations of the nucleotide site of kinesin family motors in the triphosphate state

Journal of Molecular Biology

Volumn 408, Issue 4, 2011, Pages 628-642

  Naber, Nariman ^a   Larson, Adam ^b   Rice, Sarah ^b   Cooke, Roger ^a,c   Pate, Edward ^d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Washington State University   (United States)

Author keywords

electron paramagnetic resonance spectroscopy; kinesin; ncd; spin probes; Switch 1

Indexed keywords

ADENINE NUCLEOTIDE DERIVATIVE; ADENOSINE TRIPHOSPHATE; KINESIN; KINESIN 1; MOLECULAR MOTOR; NUCLEOTIDE;

ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTRON SPIN RESONANCE; GENE MUTATION; MICROTUBULE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; SPECTROSCOPY; X RAY CRYSTALLOGRAPHY;

EID: 79955020377     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.01.001     Document Type: Article

References (64)

1. Kull F.J., Sablin E.P., Lau R., Fletterick R.J., and Vale R.D. Crystal structure of the kinesin motor domain reveals a structural similarity to myosin Nature 380 1996 550 555 (Pubitemid 26110647)
2. Sablin E.P., Kull F.J., Cooke R., Vale R.D., and Fletterick R.J. Crystal structure of the motor domain of the kinesin-related motor ncd Nature 380 1996 555 559 (Pubitemid 26111333)
3. 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 (Pubitemid 29054483)
4. Endres N.F., Yoshioka C., Milligan R.A., and Vale R.D. A lever-arm rotation drives motility of the minus-end-directed kinesin Ncd Nature 439 2006 875 878 (Pubitemid 43255708)
5. Rice S., Lin A.W., Safer D., Hart C.L., Naber N., and Carragher B.O. A structural change in the kinesin motor protein that drives motility Nature 402 1999 778 784
6. Sablin E.P., Case R.B., Dai S.C., Hart C.L., Ruby A., Vale R.D., and Fletterick R.J. Direction determination in the minus-end-directed kinesin motor ncd Nature 395 1998 813 816 (Pubitemid 28485450)
7. Gulick A.M., Song H., Endow S.A., and Rayment I. X-ray crystal structure of the yeast Kar3 motor domain complexed with Mg•ADP to 2.3 Å resolution Biochemistry 37 1998 1769 1776 (Pubitemid 28099799)
8. Song Y.H., Marx A., Muller J., Woehlke G., Schliwa M., and Krebs A. Structure of a fast kinesin: implications for ATPase mechanism and interactions with microtubules EMBO J. 20 2001 6213 6225 (Pubitemid 33078695)
9. Turner J., Anderson R., Guo J., Beraud C., Fletterick R., and Sakowicz R. Crystal structure of the mitotic spindle kinesin Eg5 reveals a novel conformation of the neck-linker J. Biol. Chem. 276 2001 25496 25502
10. Kikkawa M., Sablin E.P., Okada Y., Yajima H., Fletterick R.J., and Hirokawa N. Switch-based mechanism of kinesin motors Nature 411 2001 439 445 (Pubitemid 32494382)
11. Cochran J.C., Sindelar C.V., Mulko N.K., Collins K.A., Kong S.E., Hawley R.S., and Kull F.J. ATPase cycle of the nonmotile kinesin NOD allows microtubule end tracking and drives chromosome movement Cell 136 2009 110 122
12. Marx A., Muller J., Mandelkow E.M., Woehlke G., Bouchet-Marquis C., Hoenger A., and Mandelkow E. X-ray structure and microtubule interaction of the motor domain of Neurospora crassa NcKin3, a kinesin with unusual processivity Biochemistry 47 2008 1848 1861 (Pubitemid 351287111)
13. Hoeng J.C., Dawson S.C., House S.A., Sagolla M.S., Pham J.K., and Mancuso J.J. High-resolution crystal structure and in vivo function of a kinesin-2 homologue in Giardia intestinalis Mol. Biol. Cell 19 2008 3124 3137
14. Nitta R., Kikkawa M., Okada Y., and Hirokawa N. KIF1A alternately uses two loops to bind microtubules Science 305 2004 678 683 (Pubitemid 39006759)
15. Yount R.G., Lawson D., and Rayment I. Is myosin a "back door" enzyme? Biophys. J. 68 1995 44S 47S discussion, 47S-49S
16. 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 (Pubitemid 32009176)
17. 4 Biochemistry 34 1995 8960 8972
18. 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
19. Minehardt T.J., Cooke R., Pate E., and Kollman P.A. Molecular dynamics study of the energetic, mechanistic, and structural implications of a closed phosphate tube in ncd Biophys. J. 80 2001 1151 1168
20. Naber N., Minehardt T.J., Rice S., Chen X., Grammer J., and Matuska M. Closing of the nucleotide pocket of kinesin-family motors upon binding to microtubules Science 300 2003 798 801 (Pubitemid 36532115)
21. Larson A.G., Naber N., Cooke R., Pate E., and Rice S.E. The conserved L5 loop establishes the pre-powerstroke conformation of the kinesin-5 motor, eg5 Biophys. J. 98 2010 2619 2627
22. Naber N., Rice S., Matuska M., Vale R.D., Cooke R., and Pate E. EPR spectroscopy shows a microtubule-dependent conformational change in the kinesin switch 1 domain Biophys. J. 84 2003 3190 3196 (Pubitemid 36531766)
23. Sindelar C.V., and Downing K.H. An atomic-level mechanism for activation of the kinesin molecular motors Proc. Natl Acad. Sci. USA 107 2010 4111 4116
24. Kozielski F., Sack S., Marx A., Thormahlen M., Schonbrunn E., and Biou V. The crystal structure of dimeric kinesin and implications for microtubule-dependent motility Cell 91 1997 985 994 (Pubitemid 28027831)
25. Yun M., Bronner C.E., Park C.G., Cha S.S., Park H.W., and Endow S.A. Rotation of the stalk/neck and one head in a new crystal structure of the kinesin motor protein, Ncd EMBO J. 22 2003 5382 5389 (Pubitemid 37279948)
26. Sindelar C.V., Budny M.J., Rice S., Naber N., Fletterick R., and Cooke R. Two conformations in the human kinesin power stroke defined by X-ray crystallography and EPR spectroscopy Nat. Struct. Biol. 9 2002 844 848 (Pubitemid 35257785)
27. Parke C.L., Wojcik E.J., Kim S., and Worthylake D.K. ATP hydrolysis in Eg5 kinesin involves a catalytic two-water mechanism J. Biol. Chem. 285 2009 5859 5867
28. Nordio P.L. General magnetic resonance theory L.J. Berliner, Spin Labeling Theory and Applications 1976 Academic Press New York, NY 5 52
29. Griffith O.H., and Jost P.C. Lipid spin labels in biological membranes L.J. Berliner, Spin Labeling Theory and Applications 1976 Academic Press New York, NY 454 523
30. Alessi D.R., Corrie J.E., Fajer P.G., Ferenczi M.A., Thomas D.D., Trayer I.P., and Trentham D.R. Synthesis and properties of a conformationally restricted spin-labeled analog of ATP and its interaction with myosin and skeletal muscle Biochemistry 31 1992 8043 8054
31. Suzuki Y., Shimizu T., Morii H., and Tanokura M. Hydrolysis of AMPPNP by the motor domain of ncd, a kinesin-related protein FEBS Lett. 409 1997 29 32 (Pubitemid 27248560)
32. Foster K.A., Correia J.J., and Gilbert S.P. Equilibrium binding studies of non-claret disjunctional protein (Ncd) reveal cooperative interactions between the motor domains J. Biol. Chem. 273 1998 35307 35318 (Pubitemid 29028239)
33. Vale R.D. Switches, latches, and amplifiers: common themes of G proteins and molecular motors J. Cell Biol. 135 1996 291 302
34. Marx A., Hoenger A., and Mandelkow E. Structures of kinesin motor proteins Cell Motil. Cytoskeleton 66 2009 958 966
35. Vale R.D., and Milligan R.A. The way things move: looking under the hood of molecular motor proteins Science 288 2000 88 95
36. Larsen M., Willett R., and Yount R.G. Imidodiphosphate and pyrophosphate: possible biological significance of similar structures Science 166 1969 1510 1511
37. Ogawa T., Nitta R., Okada Y., and Hirokawa N. A common mechanism for microtubule destabilizers-M type kinesins stabilize curling of the protofilament using the class-specific neck and loops Cell 116 2004 591 602 (Pubitemid 38268103)
38. Kast D., Espinoza-Fonseca L.M., Yi C., and Thomas D.D. Phosphorylation-induced structural changes in smooth muscle myosin regulatory light chain Proc. Natl Acad. Sci. USA 107 2010 8207 8212
39. 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 (Pubitemid 39657853)
40. Sweeney H.L., and Houdusse A. Structural and functional insights into the myosin motor mechanism Annu. Rev. Biophys. 39 2010 539 557
41. Holmes K.C., Angert I., Kull F.J., Jahn W., and Schroder R.R. Electron cryo-microscopy shows how strong binding of myosin to actin releases nucleotide Nature 425 2003 423 427 (Pubitemid 37187274)
42. Kintses B., Gyimesi M., Pearson D.S., Geeves M.A., Zeng W., Bagshaw C.R., and Malnasi-Csizmadia A. Reversible movement of switch 1 loop of myosin determines actin interaction EMBO J. 26 2007 265 274 (Pubitemid 46094717)
43. Naber N., Malnasi-Csizmadia A., Purcell T.J., Cooke R., and Pate E. Combining EPR with fluorescence spectroscopy to monitor conformational changes at the myosin nucleotide pocket J. Mol. Biol. 396 2010 937 948
44. Naber N., Purcell T.J., Pate E., and Cooke R. Dynamics of the nucleotide pocket of myosin measured by spin-labeled nucleotides Biophys. J. 92 2007 172 184 (Pubitemid 46055204)
45. Robertson C.I., Gaffney D.P. II, Chrin L.R., and Berger C.L. Structural rearrangements in the active site of smooth-muscle myosin Biophys. J. 89 2005 1882 1892 (Pubitemid 41233543)
46. Sun M., Oakes J.L., Ananthanarayanan S.K., Hawley K.H., Tsien R.Y., Adams S.R., and Yengo C.M. Dynamics of the upper 50-kDa domain of myosin V examined with fluorescence resonance energy transfer J. Biol. Chem. 281 2006 5711 5717 (Pubitemid 43847669)
47. Cooke R. Actomyosin interaction in striated muscle Physiol. Rev. 77 1997 671 697 (Pubitemid 27328737)
48. Taylor E.W. Mechanism of actomyosin ATPase and the problem of muscle contraction CRC Crit. Rev. Biochem. 6 1979 103 164
49. Cross R.A. The kinetic mechanism of kinesin Trends Biochem. Sci. 29 2004 301 309 (Pubitemid 38968762)
50. Williams R.C. Jr., and Lee J.C. Preparation of tubulin from brain Methods Enzymol. 85 1982 376 385
51. Peloquin J., Komarova Y., and Borisy G. Conjugation of fluorophores to tubulin Nat. Methods 2 2005 299 303 (Pubitemid 41131012)
52. Crowder M.S., and Cooke R. Orientation of spin-labeled nucleotides bound to myosin in glycerinated muscle fibers Biophys. J. 51 1987 323 333 (Pubitemid 17008708)
53. Case D.A., Darden T.A., Cheatham T.E.I., Simmerling C.L., Wang J., and Duke R.E. AMBER10 2008 University of California San Francisco, CA
54. Frisch M.J., Trucks G.W., Schlegel H.B., Scuseria G.E., Robb M.A., and Cheeseman J.R. Gaussian03 Revision C.02 2004 Gaussian, Inc. Wallingford, CT
55. Bayly C.I., Ciepak W.D., Cornell W.D., and Kollman P.A. A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: the RESP model J. Phys. Chem. 97 1993 10269 10280
56. Turley W., and Boer F.P. The crystal structure of the free radical 2,2,5,5-tetramethyl-3-carbamidopyrroline-1-oxyl Acta Crystallogr. Sect. B 28 1972 1641 1644
57. Dickman M.H., and Doedens R.J. Preparation and crystal structure of aqua(3-cyano-2,2,5,5-tetramethylpyrrolinyl-1-oxy)bis(hexafluoroacetylacetonato) copper(II), a metal complex of a nitroxide radical having a hydrogen-bonded one-dimensional chain structure Inorg. Chem. 22 1983 1591 1594
58. Aqvist J. Modelling of ion-ligand interactions in solutions and biomolecules J. Mol. Struct. (Theochem.) 256 1992 135 152
59. Bashford D., and Case D.A. Generalized Born models of macromolecular solvation effects Annu. Rev. Phys. Chem. 51 2000 129 152
60. Baker N.A. Improving implicit solvent simulations: a Poisson-centric view Curr. Opin. Struct. Biol. 15 2005 137 143
61. Feig M., Chocholousova J., and Tanizaki S. Extending the horizon: towards the efficient modeling of large biomolecular complexes in atomic detail Theor. Chem. Acc. 116 2006 194 205 (Pubitemid 44318424)
62. Berendsen H.J.C., Postma J.P.M., Gunsteren W.F. V., DiNola A., and Ghaak J.R. Molecular dynamics with coupling to an external bath J. Chem. Phys. 113 1984 3684 3690
63. Ryckaert A.J., Ciccotti G., and Berendsen H.J.C. Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes J. Comput. Phys. 23 1977 327 341
64. LaConte L.E., Voelz V., Nelson W., Enz M., and Thomas D.D. Molecular dynamics simulation of site-directed spin labeling: experimental validation in muscle fibers Biophys. J. 83 2002 1854 1866