Structure-based Molecular Simulations Reveal the Enhancement of Biased Brownian Motions in Single-headed Kinesin

PLoS Computational Biology

Volumn 9, Issue 2, 2013, Pages

  Kanada, Ryo ^a   Kuwata, Takeshi ^b   Kenzaki, Hiroo ^a   Takada, Shoji ^a,c  

^a KYOTO UNIVERSITY   (Japan)

^b KOBE UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FREE ENERGY; HYDROLYSIS; MOLECULAR STRUCTURE; STOCHASTIC SYSTEMS;

ATP HYDROLYSIS; COORDINATED MOTION; HAND OVER; IN-VITRO; KINESINS; MICROTUBULES; MOLECULAR MOTORS; MOLECULAR SIMULATIONS; SINGLE MOLECULE EXPERIMENTS; STRUCTURE-BASED;

BROWNIAN MOVEMENT;

ADENOSINE TRIPHOSPHATE; KINESIN; PROTEIN KIF1A; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; MICROTUBULE; MOLECULAR MECHANICS; MOLECULAR MODEL; PROTEIN ANALYSIS; PROTEIN HYDROLYSIS; PROTEIN STRUCTURE; PROTEIN TRANSPORT;

EID: 84874768085     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002907     Document Type: Article

References (47)

1. Klepeis JL, Lindorff-Larsen K, Dror RO, Shaw DE, (2009) Long-timescale molecular dynamics simulations of protein structure and function. Current Opinion in Structural Biology 19: 120-127.
2. Hyeon C, Thirumalai D, (2011) Capturing the essence of folding and functions of biomolecules using coarse-grained models. Nature Communications 2: 487.
3. Takada S, (2012) Coarse-grained molecular simulations of large biomolecules. Curr Opin Struct Biol 22: 130-7.
4. Koga N, Takada S, (2006) Folding-based molecular simulations reveal mechanisms of the rotary motor F1-ATPase. Proc Natl Acad Sci U S A 103: 5367-5372.
5. Koga N, Kameda T, Okazaki K, Takada S, (2009) Paddling mechanism for the substrate translocation by AAA+ motor revealed by multiscale molecular simulations. Proc Natl Acad Sci U S A 106: 18237-18242.
6. Hackney DD, (1994) Evidence for alternating head catalysis by kinesin during microtubule-stimulated ATP hydrolysis. Proc Natl Acad Sci U S A 91: 6865-6869.
7. Hyeon C, Onuchic JN, (2007) Mechanical control of the directional stepping dynamics of the kinesin motor. Proc Natl Acad Sci U S A 104: 17382-17387.
8. Hyeon C, Onuchic JN, (2007) Internal strain regulates the nucleotide binding site of the kinesin leading head. Proc Natl Acad Sci U S A 104: 2175-2180.
9. Yildiz A, Tomishige M, Gennerich A, Vale RD, (2008) Intramolecular strain coordinates kinesin stepping behavior along microtubules. Cell 134: 1030-1041.
10. Hirokawa N, (1998) Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279: 519-526.
11. Svoboda K, Schmidt CF, Schnapp BJ, Block SM, (1993) Direct observation of kinesin stepping by optical trapping interferometry. Nature 365: 721-727.
12. Vale RD, Funatsu T, Pierce DW, Romberg L, Harada Y, et al. (1996) Direct observation of single kinesin molecules moving along microtubules. Nature 380: 451-453.
13. Inoue Y, Toyoshima YY, Iwane AH, Morimoto S, Higuchi H, et al. (1997) Movements of truncated kinesin fragments with a short or an artificial flexible neck. Proc Natl Acad Sci U S A 94: 7275-7280.
14. Hancock WO, Howard J, (1998) Processivity of the motor protein kinesin requires two heads. J Cell Biol 140: 1395-1405.
15. Higuchi H, Muto E, Inoue Y, Yanagida T, (1997) Kinetics of force generation by single kinesin molecules activated by laser photolysis of caged ATP. Proc Natl Acad Sci U S A 94: 4395-4400.
16. Kojima H, Muto E, Higuchi H, Yanagida T, (1997) Mechanics of single kinesin molecules measured by optical trapping nanometry. Biophys J 73: 2012-2022.
17. Asenjo AB, Krohn N, Sosa H, (2003) Configuration of the two kinesin motor domains during ATP hydrolysis. Nat Struct Biol 10: 836-842.
18. Yildiz A, Tomishige M, Vale RD, Selvin PR, (2004) Kinesin walks hand-over-hand. Science 303: 676-678.
19. Okada Y, Hirokawa N, (2000) Mechanism of the single-headed processivity: diffusional anchoring between the K-loop of kinesin and the C terminus of tubulin. Proc Natl Acad Sci U S A 97: 640-645.
20. Okada Y, Hirokawa N, (1999) A processive single-headed motor: kinesin superfamily protein KIF1A. Science 283: 1152-1157.
21. Okada Y, Higuchi H, Hirokawa N, (2003) Processivity of the single-headed kinesin KIF1A through biased binding to tubulin. Nature 424: 574-577.
22. Grant BJ, Gheorghe D, Zheng W, Alonso M, Huber G, et al. (2011) Electrostatically biased binding of kinesin to microtubules. PLoS Biol 9: e1001207.
23. Li MH, Zheng WJ, (2011) Probing the Structural and Energetic Basis of Kinesin-Microtubule Binding Using Computational Alanine-Scanning Mutagenesis. Biochemistry 50: 8645-8655.
24. Yang Y, Cui Q, (2009) The Hydrolysis Activity of Adenosine Triphosphate in Myosin: A Theoretical Analysis of Anomeric Effects and the Nature of the Transition State. Journal of Physical Chemistry A 113: 12439-12446.
25. Kikkawa M, Sablin EP, Okada Y, Yajima H, Fletterick RJ, et al. (2001) Switch-based mechanism of kinesin motors. Nature 411: 439-445.
26. Nitta R, Kikkawa M, Okada Y, Hirokawa N, (2004) KIF1A alternately uses two loops to bind microtubules. Science 305: 678-683.
27. Nitta R, Okada Y, Hirokawa N, (2008) Structural model for strain-dependent microtubule activation of Mg-ADP release from kinesin. Nat Struct Mol Biol 15: 1067-1075.
28. Rice S, Lin AW, Safer D, Hart CL, Naber N, et al. (1999) A structural change in the kinesin motor protein that drives motility. Nature 402: 778-784.
29. Hwang W, Lang MJ, Karplus M, (2008) Force generation in kinesin hinges on cover-neck bundle formation. Structure 16: 62-71.
30. Kikkawa M, Okada Y, Hirokawa N, (2000) 15 A resolution model of the monomeric kinesin motor, KIF1A. Cell 100: 241-252.
31. Kikkawa M, Hirokawa N, (2006) High-resolution cryo-EM maps show the nucleotide binding pocket of KIF1A in open and closed conformations. EMBO J 25: 4187-4194.
32. Bryngelson JD, Onuchic JN, Socci ND, Wolynes PG, (1995) Funnels, Pathways, and the Energy Landscape of Protein-Folding- a Synthesis. Proteins-Structure Function and Genetics 21: 167-195.
33. Frauenfelder H, Sligar SG, Wolynes PG, (1991) The Energy Landscapes and Motions of Proteins. Science 254: 1598-1603.
34. Clementi C, Nymeyer H, Onuchic JN, (2000) Topological and energetic factors: what determines the structural details of the transition state ensemble and "en-route" intermediates for protein folding? An investigation for small globular proteins. J Mol Biol 298: 937-953.
35. Okazaki K, Koga N, Takada S, Onuchic JN, Wolynes PG, (2006) Multiple-basin energy landscapes for large-amplitude conformational motions of proteins: Structure-based molecular dynamics simulations. Proc Natl Acad Sci U S A 103: 11844-11849.
36. Hyeon C, Lorimer GH, Thirumalai D, (2006) Dynamics of allosteric transitions in GroEL. Proc Natl Acad Sci U S A 103: 18939-18944.
37. Go N, (1983) Theoretical studies of protein folding. Annu Rev Biophys Bioeng 12: 183-210.
38. Iwaki M, Iwane AH, Ikebe M, Yanagida T, (2008) Biased Brownian motion mechanism for processivity and directionality of single-headed myosin-VI. Biosystems 93: 39-47.
39. Inoue Y, Iwane AH, Miyai T, Muto E, Yanagida T, (2001) Motility of single one-headed kinesin molecules along microtubules. Biophys J 81: 2838-2850.
40. Hammond JW, Cai DW, Blasius TL, Li Z, Jiang YY, et al. (2009) Mammalian Kinesin-3 Motors Are Dimeric In Vivo and Move by Processive Motility upon Release of Autoinhibition. PLoS Biology 7: 650-663.
41. Tomishige M, Klopfenstein DR, Vale RD, (2002) Conversion of Unc104/KIF1A kinesin into a processive motor after dimerization. Science 297: 2263-2267.
42. Zhang ZC, Thirumalai D, (2012) Dissecting the Kinematics of the Kinesin Step. Structure 20: 628-640.
43. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, et al. (2007) Comparative protein structure modeling using MODELLER. Curr Protoc Protein Sci Chapter 2: Unit 2-9.
44. Sindelar CV, Downing KH, (2010) An atomic-level mechanism for activation of the kinesin molecular motors. Proc Natl Acad Sci U S A 107: 4111-4116.
45. Skiniotis G, Surrey T, Altmann S, Gross H, Song YH, et al. (2003) Nucleotide-induced conformations in the neck region of dimeric kinesin. EMBO J 22: 1518-1528.
46. Asenjo AB, Weinberg Y, Sosa H, (2006) Nucleotide binding and hydrolysis induces a disorder-order transition in the kinesin neck-linker region. Nat Struct Mol Biol 13: 648-654.
47. Kenzaki H, Koga N, Hori N, Kanada R, Li W, et al. (2011) CafeMol: A Coarse-Grained Biomolecular Simulator for Simulating Proteins at Work. Journal of Chemical Theory and Computation 7: 1979-1989.