Are coiled-coils of dimeric kinesins unwound during their walking on microtubule?

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Duan, Zhao Wen ^a   Xie, Ping ^a   Li, Wei ^a   Wang, Peng Ye ^a  

^a INSTITUTE OF PHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; KINESIN; MOLECULAR MOTOR; PROTEIN KAR3; PROTEIN NCD; UNCLASSIFIED DRUG; VIK1 PROTEIN; AMINO ACID; HETERODUPLEX;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; CELL INTERACTION; CELL MIGRATION; DNA DENATURATION; MICROTUBULE; MICROTUBULE ASSEMBLY; MOLECULAR DYNAMICS; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN UNFOLDING; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TRANSPORT; THERMODYNAMICS;

AMINO ACID SEQUENCE; AMINO ACIDS; KINESIN; MICROTUBULES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID HETERODUPLEXES; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; PROTEIN UNFOLDING; THERMODYNAMICS;

EID: 84860467720     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036071     Document Type: Article

References (60)

1. Scholey JM, (1996) Kinesin-II, a membrane traffic motor in axons, axonemes, and spindles. J Cell Biol 133: 1-4.
2. Hirokawa N, (1998) Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279: 519-526.
3. Yang JT, Laymon RA, Goldstein LS, (1989) A three-domain structure of kinesin heavy chain revealed by DNA sequence and microtubule binding analyses. Cell 56: 879-889.
4. Vale RD, (2003) The molecular motor toolbox for intracellular transport. Cell 112: 467-480.
5. Hua W, Chung J, Gelles J, (2002) Distinguishing inchworm and hand-over-hand processive kinesin movement by neck rotation measurements. Science 295: 844-848.
6. Asbury CL, Fehr AN, Block SM, (2003) Kinesin moves by an asymmetric hand-over-hand mechanism. Science 302: 2130-2134.
7. Kaseda K, Higuchi H, Hirose K, (2003) Alternate fast and slow stepping of a heterodimeric kinesin molecule. Nat Cell Biol 5: 1079-1082.
8. Yildiz A, Tomishige M, Vale RD, Selvin PR, (2004) Kinesin walks hand-over-hand. Science 303: 676-678.
9. 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.
10. Wade RH, Kozielski F, (2000) Structural links to kinesin directionality and movement. Nat Struct Biol 7: 456-460.
11. Miyazono Y, Hayashi M, Karagiannis P, Harada Y, Tadakuma H, (2010) Strain through the neck linker ensures processive runs: a DNA-kinesin hybrid nanomachine study. EMBO J 29: 93-106.
12. Shastry S, Hancock WO, (2010) Neck linker length determines the degree of processivity in kinesin-1 and kinesin-2 motors. Curr Biol 20: 939-943.
13. Hwang W, Lang MJ, Karplus M, (2008) Force generation in kinesin hinges on cover-neck bundle formation. Structure 16: 62-71.
14. Vale RD, Milligan RA, (2000) The way things move: looking under the hood of molecular motor proteins. Science 288: 88-95.
15. Xie P, (2010) Mechanism of processive movement of monomeric and dimeric kinesin molecules. Int J Biol Sci 6: 665-674.
16. Kutys ML, Fricks J, Hancock WO, (2010) Monte Carlo analysis of neck linker extension in kinesin molecular motors. PLoS Comput Biol 6: e1000980.
17. Howard J, (1996) The movement of kinesin along microtubules. Annu Rev Physiol 58: 703-729.
18. Walker RA, Salmon ED, Endow SA, (1990) The Drosophila claret segregation protein is a minus-end directed motor molecule. Nature 347: 780-782.
19. Endow SA, Kang SJ, Satterwhite LL, Rose MD, Skeen VP, et al. (1994) Yeast Kar3 is a minus-end microtubule motor protein that destabilizes microtubules preferentially at the minus ends. EMBO J 13: 2708-2713.
20. Sablin EP, Kull FJ, Cooke R, Vale RD, Fletterick RJ, (1996) Crystal structure of the motor domain of the kinesin-related motor ncd. Nature 380: 555-559.
21. Sablin EP, Case RB, Dai SC, Hart CL, Ruby A, et al. (1998) Direction determination in the minus-end-directed kinesin motor ncd. Nature 395: 813-816.
22. Sosa H, Dias DP, Hoenger A, Whittaker M, Wilson-Kubalek E, et al. (1997) A model for the microtubule-Ncd motor protein complex obtained by cryo-electron microscopy and image analysis. Cell 90: 217-224.
23. Hirose K, Cross RA, Amos LA, (1998) Nucleotide-dependent structural changes in dimeric NCD molecules complexed to microtubules. J Mol Biol 278: 389-400.
24. Wendt TG, Volkmann N, Skiniotis G, Goldie KN, Muller J, et al. (2002) Microscopic evidence for a minus-end-directed power stroke in the kinesin motor ncd. EMBO Journal 21: 5969-5978.
25. Endres NF, Yoshioka C, Milligan RA, Vale RD, (2006) A lever-arm rotation drives motility of the minus-end-directed kinesin Ncd. Nature 439: 875-878.
26. Kozielski F, De Bonis S, Burmeister WP, Cohen-Addad C, Wade RH, (1999) The crystal structure of the minus-end-directed microtubule motor protein ncd reveals variable dimer conformations. Structure 7: 1407-1416.
27. Yun M, Bronner CE, Park CG, Cha SS, Park HW, et al. (2003) Rotation of the stalk/neck and one head in a new crystal structure of the kinesin motor protein, Ncd. EMBO J 22: 5382-5389.
28. Cross RA, (2010) Kinesin-14: the roots of reversal. BMC Biol 8: 107.
29. Heuston E, Bronner CE, Kull FJ, Endow SA, (2010) A kinesin motor in a force-producing conformation. BMC Struct Biol 10: 19.
30. Page BD, Satterwhite LL, Rose MD, Snyder M, (1994) Localization of the Kar3 kinesin heavy chain-related protein requires the Cik1 interacting protein. J Cell Biol 124: 507-519.
31. Manning BD, Barrett JG, Wallace JA, Granok H, Snyder M, (1999) Differential regulation of the Kar3p kinesin-related protein by two associated proteins, Cik1p and Vik1p. J Cell Biol 144: 1219-1233.
32. Barrett JG, Manning BD, Snyder M, (2000) The Kar3p kinesin-related protein forms a novel heterodimeric structure with its associated protein Cik1p. Mol Biol Cell 11: 2373-2385.
33. Manning BD, Snyder M, (2000) Drivers and passengers wanted! the role of kinesin-associated proteins. Trends Cell Biol 10: 281-289.
34. Chu HM, Yun M, Anderson DE, Sage H, Park HW, et al. (2005) Kar3 interaction with Cik1 alters motor structure and function. EMBO J 24: 3214-3223.
35. Sproul LR, Anderson DJ, Mackey AT, Saunders WS, Gilbert SP, (2005) Cik1 targets the minus-end kinesin depolymerase kar3 to microtubule plus ends. Curr Biol 15: 1420-1427.
36. Allingham J, Sproul L, Rayment I, Gilbert S, (2007) Vik1 Modulates Microtubule-Kar3 Interactions through a Motor Domain that Lacks an Active Site. Cell 128: 1161-1172.
37. Gulick AM, Song H, Endow SA, Rayment I, (1998) X-ray crystal structure of the yeast Kar3 motor domain complexed with Mg.ADP to 2.3 A resolution. Biochemistry 37: 1769-1776.
38. Woehlke G, Schliwa M, (2007) Kinesin Kar3 and Vik1 Go Head to Head. Cell 128: 1033-1034.
39. Xie P, Dou SX, Wang PY, (2007) Limping of homodimeric kinesin motors. J Mol Biol 366: 976-985.
40. Hou R, Wang Z, (2010) A coordinated molecular 'fishing' mechanism in heterodimeric kinesin. Physical Biology 7: 036003.
41. Cai D, Hoppe AD, Swanson JA, Verhey KJ, (2007) Kinesin-1 structural organization and conformational changes revealed by FRET stoichiometry in live cells. J Cell Biol 176: 51-63.
42. Evans E, Ritchie K, (1997) Dynamic strength of molecular adhesion bonds. Biophys J 72: 1541-1555.
43. Rief M, Pascual J, Saraste M, Gaub HE, (1999) Single molecule force spectroscopy of spectrin repeats: low unfolding forces in helix bundles. J Mol Biol 286: 553-561.
44. Paci E, Karplus M, (2000) Unfolding proteins by external forces and temperature: the importance of topology and energetics. Proc Natl Acad Sci U S A 97: 6521-6526.
45. Essevaz-Roulet B, Bockelmann U, Heslot F, (1997) Mechanical separation of the complementary strands of DNA. Proc Natl Acad Sci U S A 94: 11935-11940.
46. Uemura S, Kawaguchi K, Yajima J, Edamatsu M, Toyoshima YY, et al. (2002) Kinesin-microtubule binding depends on both nucleotide state and loading direction. Proc Natl Acad Sci U S A 99: 5977-5981.
47. Bornschlogl T, Woehlke G, Rief M, (2009) Single molecule mechanics of the kinesin neck. Proc Natl Acad Sci U S A 106: 6992-6997.
48. Tomishige M, Vale RD, (2000) Controlling kinesin by reversible disulfide cross-linking. Identifying the motility-producing conformational change. J Cell Biol 151: 1081-1092.
49. Mason JM, Arndt KM, (2004) Coiled coil domains: stability, specificity, and biological implications. Chembiochem 5: 170-176.
50. Thormahlen M, Marx A, Sack S, Mandelkow E, (1998) The coiled-coil helix in the neck of kinesin. J Struct Biol 122: 30-41.
51. Tripet B, Hodges RS, (2002) Helix capping interactions stabilize the N-terminus of the kinesin neck coiled-coil. J Struct Biol 137: 220-235.
52. Ito M, Morii H, Shimizu T, Tanokura M, (2006) Coiled coil in the stalk region of ncd motor protein is nonlocally sustained. Biochemistry 45: 3315-3324.
53. 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.
54. Alonso MC, Drummond DR, Kain S, Hoeng J, Amos L, et al. (2007) An ATP gate controls tubulin binding by the tethered head of kinesin-1. Science 316: 120-123.
55. Xie P, (2008) Stepping behavior of two-headed kinesin motors. Biochim Biophys Acta 1777: 1195-1202.
56. Altman D, Sweeney HL, Spudich JA, (2004) The mechanism of myosin VI translocation and its load-induced anchoring. Cell 116: 737-749.
57. Xie P, Dou SX, Wang PY, (2006) A hand-over-hand diffusing model for myosin-VI molecular motors. Biophys Chem 122: 90-100.
58. Kozielski F, (1997) The Crystal Structure of Dimeric Kinesin and Implications for Microtubule-Dependent Motility. Cell 91.
59. Kumar S, Bouzida D, Swendsen RH, Kollman PA, Rosenberg JM, (1992) The Weighted Histogram Analysis Method for Free-Energy Calculations on Biomolecules. 1. The Method. Journal of Computational Chemistry 13: 1011-1021.
60. Bartels C, (2000) Analyzing biased Monte Carlo and molecular dynamics simulations. Chemical Physics Letters 331: 446-454.