Strain through the neck linker ensures processive runs: A DNA-kinesin hybrid nanomachine study

EMBO Journal

Volumn 29, Issue 1, 2010, Pages 93-106

  Miyazono, Yuya ^a   Hayashi, Masahito ^b   Karagiannis, Peter ^c   Harada, Yoshie ^b,d   Tadakuma, Hisashi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

DNA; FRET; Kinesin; Nanomachine; Single molecule

Indexed keywords

DNA; KINESIN; ADENOSINE TRIPHOSPHATE; CYSTEINE; FLUORESCENT DYE; NANOMATERIAL; RECOMBINANT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DNA STRUCTURE; MICROTUBULE; PRIORITY JOURNAL; PROTEIN STRUCTURE; WILD TYPE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; ENERGY METABOLISM; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; HUMAN; IN VITRO STUDY; METABOLISM; NANOTECHNOLOGY; SITE DIRECTED MUTAGENESIS;

ADENOSINE TRIPHOSPHATE; BINDING SITES; CYSTEINE; DNA; ENERGY METABOLISM; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; HUMANS; KINESIN; MICROTUBULES; MODELS, MOLECULAR; MOLECULAR STRUCTURE; MUTAGENESIS, SITE-DIRECTED; NANOSTRUCTURES; NANOTECHNOLOGY; RECOMBINANT PROTEINS;

EID: 75649106490     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.319     Document Type: Article

References (57)

1. Alonso MC, Drummond DR, Kain S, Hoeng J, Amos L, Cross RA (2007) An ATP gate controls tubulin binding by the tethered head of kinesin-1. Science 316: 120-123
2. Asbury CL, Fehr AN, Block SM (2003) Kinesin moves by an asymmetric hand-overhand mechanism. Science 302: 2130-2134
3. Asenjo AB, Krohn N, Sosa H (2003) Configuration of the two kinesin motor domains during ATP hydrolysis. Nat Struct Biol 10: 836-842
4. Asenjo AB, Sosa H (2009) A mobile kinesin-head intermediate during the ATP-waiting state. Proc Natl Acad Sci USA 106: 5657-5662
5. Block SM (2007) Kinesin motor mechanics: binding, stepping, tracking, gating, and limping. Biophys J 92: 2986-2995
6. Bustamante C, Marko JF, Siggia ED, Smith S (1994) Entropic elasticity of lambda-phage DNA. Science 265: 1599-1600
7. Carter NJ, Cross RA (2005) Mechanics of the kinesin step. Nature 435: 308-312
8. Case RB, Rice S, Hart CL, Ly B, Vale RD (2000) Role of the kinesin neck linker and catalytic core in microtubule-based motility. Curr Biol 10: 157-160
9. Dunn AR, Spudich JA (2007) Dynamics of the unbound head during myosin V processive translocation. Nat Struct Mol Biol 14: 246-248
10. Funatsu T, Harada Y, Tokunaga M, Saito K, Yanagida T (1995) Imaging of single fluorescent molecules and individual ATP turnovers by single myosin molecules in aqueous solution. Nature 374: 555-559
11. Guydosh NR, Block SM (2009) Direct observation of the binding sate of the kinesin head to the microtubule. Nature 461: 125-128
12. Hackney DD (1994) Evidence for alternating head catalysis by kinesin during microtubule-stimulated ATP hydrolysis. Proc Natl Acad Sci USA 91: 6865-6869
13. Hackney DD (2007) Biochemistry. Processive motor movement. Science 316: 58-59
14. Hackney DD, Stock MF, Moore J, Patterson RA (2003) Modulation of kinesin half-site ADP release and kinetic processivity by a spacer between the head groups. Biochemistry 42: 12011-12018
15. Hahlen K, Ebbing B, Reinders J, Mergler J, Sickmann A, Woehlke G (2006) Feedback of the kinesin-1 neck-linker position on the catalytic site. J Biol Chem 281: 18868-18877
16. Hancock WO, Howard J (1999) Kinesin's processivity results from mechanical and chemical coordination between the ATP hydrolysis cycles of the two motor domains. Proc Natl Acad Sci USA 96: 13147-13152
17. Hirokawa N, Takemura R (2005) Molecular motors and mechanisms of directional transport in neurons. Nat Rev Neurosci 6: 201-214
18. Huxley AF, Simmons RM (1971) Proposed mechanism of force generation in striated muscle. Nature 233: 533-538
19. Huxley HE (1969) The mechanism of muscular contraction. Science 164: 1356-1365
20. Hwang W, Lang MJ, Karplus M (2008) Force generation in kinesin hinges on cover-neck bundle formation. Structure 16: 62-71
21. Jiang W, Stock MF, Li X, Hackney DD (1997) Influence of the kinesin neck domain on dimerization and ATPase kinetics. J Biol Chem 272: 7626-7632
22. Kaseda K, Higuchi H, Hirose K (2003) Alternate fast and slow stepping of a heterodimeric kinesin molecule. Nat Cell Biol 5: 1079-1082
23. Klumpp LM, Hoenger A, Gilbert SP (2004) Kinesin's second step. Proc Natl Acad Sci USA 101: 3444-3449
24. Mathew-Fenn RS, Das R, Harbury PA (2008) Remeasuring the double helix. Science 322: 446-449
25. Mori T, Vale RD, Tomishige M (2007) How kinesin waits between steps. Nature 450: 750-754
26. Nishiyama M, Higuchi H, Yanagida T (2002) Chemomechanical coupling of the forward and backward steps of single kinesin molecules. Nat Cell Biol 4: 790-797
27. Nishiyama M, Muto E, Inoue Y, Yanagida T, Higuchi H (2001) Substeps within the 8-nm step of the ATPase cycle of single kinesin molecules. Nat Cell Biol 3: 425-428
28. Okada Y, Hirokawa N (1999) A processive single-headed motor: kinesin superfamily protein KIF1A. Science 283: 1152-1157
29. Okada Y, Higuchi H, Hirokawa N (2003) Processivity of the singleheaded kinesin KIF1A through biased binding to tubulin. Nature 424: 574-577
30. Press W, Teukolsky SA, Vetterling WV, Flannery BP (1992) Numerical Recipes in C. San Diego: Cambridge University Press
31. Purcell TJ, Morris C, Spudich JA, Sweeney HL (2002) Role of the lever arm in the processive stepping of myosin V. Proc Natl Acad Sci USA 99: 14159-14164
32. Rice S, Lin AW, Safer D, Hart CL, Naber N, Carragher BO, Cain SM, Pechatnikova E, Wilson-Kubalek EM, Whittaker M, Pate E, Cooke R, Taylor EW, Milligan RA, Vale RD (1999) A structural change in the kinesin motor protein that drives motility. Nature 402: 778-784
33. Rosenfeld SS, Fordyce PM, Jefferson GM, King PH, Block SM (2003) How kinesin uses internal strain to walk processively. J Biol Chem 278: 18550-18556
34. Rothemund PW (2006) Folding DNA to create nanoscale shapes and patterns. Nature 440: 297-302
35. Sahoo H, Roccatano D, Zacharias M, Nau WM (2006) Distance distributions of short polypeptides recovered by fluorescence resonance energy transfer in the 10 A domain. J Am Chem Soc 128: 8118-8119
36. Sakamoto T, Wang F, Schmitz S, Xu Y, Xu Q, Molloy JE, Veigel C, Sellers JR (2003) Neck length and processivity of myosin V. J Biol Chem 278: 29201-29207
37. Sakamoto T, Yildez A, Selvin PR, Sellers JR (2005) Step-size is determined by neck length in myosin V. Biochemistry 44: 16203-16210
38. Schief WR, Howard J (2001) Conformational changes during kinesin motility. Curr Opin Cell Biol 13: 19-28
39. Schuler B, Lipman EA, Steinbach PJ, Kumke M, Eaton WA (2005) Polyproline and the 'spectroscopic ruler' revisited with single-molecule fluorescence. Proc Natl Acad Sci USA 102: 2754-2759
40. Seeman NC (2003) DNA in a material world. Nature 421: 427-431
41. Shiroguchi K, Kinosita Jr K (2007) Myosin V walks by lever action and Brownian motion. Science 316: 1208-1212
42. Spudich JA (1994) How molecular motors work. Nature 372: 515-518
43. Spudich JA (2001) The myosin swinging cross-bridge model. Nat Rev Mol Cell Biol 2: 387-392
44. Svoboda K, Schmidt CF, Schnapp BJ, Block SM (1993) Direct observation of kinesin stepping by optical trapping interferometry. Nature 365: 721-727
45. Tadakuma H, Ishihama Y, Shibuya T, Tani T, Funatsu T (2006) Imaging of single mRNA molecules moving within a living cell nucleus. Biochem Biophys Res Commun 344: 772-779
46. Taguchi H, Ueno T, Tadakuma H, Yoshida M, Funatsu T (2001) Single-molecule observation of protein-protein interactions in the chaperonin system. Nat Biotechnol 19: 861-865
47. Thorn KS, Ubersax JA, Vale RD (2000) Engineering the processive run length of the kinesin motor. J Cell Biol 151: 1093-1100
48. Tomishige M, Klopfenstein DR, Vale RD (2002) Conversion of Unc104/KIF1A kinesin into a processive motor after dimerization. Science 297: 2263-2267
49. Tomishige M, Stuurman N, Vale RD (2006) Single-molecule observations of neck linker conformational changes in the kinesin motor protein. Nat Struct Mol Biol 13: 887-894
50. Tomishige M, Vale RD (2000) Controlling kinesin by reversible disulfide cross-linking: identifying the motility-producing conformational change. J Cell Biol 151: 1081-1092
51. Uemura S, Ishiwata S (2003) Loading direction regulates the affinity of ADP for kinesin. Nat Struct Biol 10: 308-311
52. Uemura S, Kawaguchi K, Yajima J, Edamatsu M, Toyoshima YY, Ishiwata S (2002) Kinesin-microtubule binding depends on both nucleotide state and loading direction. Proc Natl Acad Sci USA 99: 5977-5981
53. Vale RD, Funatsu T, Pierce DW, Romberg L, Harada Y, Yanagida T (1996) Direct observation of single kinesin molecules moving along microtubules. Nature 380: 451-453
54. Vale RD, Milligan RA (2000) The way things move: looking under the hood of molecular motor proteins. Science 288: 88-95
55. Wang MD, Yin H, Landick R, Gelles J, Block SM (1997) Stretching DNA with optical tweezers. Biophys J 72: 1335-1346
56. Yildiz A, Tomishige M, Gennerich A, Vale RD (2008) Intramolecular strain coordinates kinesin stepping behavior along microtubules. Cell 134: 1030-1041
57. Yildiz A, Tomishige M, Vale RD, Selvin PR (2004) Kinesin walks hand-over-hand. Science 303: 676-678