Structural Change in the Dynein Stalk Region Associated with Two Different Affinities for the Microtubule

Journal of Molecular Biology

Volumn 428, Issue 9, 2016, Pages 1886-1896

  Nishikawa, Yosuke ^a   Inatomi, Momoko ^a   Iwasaki, Haruka ^a   Kurisu, Genji ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

cytoskeletal motor protein; dynein; stalk coiled coil; X ray crystallography

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOPLASMIC DYNEIN; DYNEIN ADENOSINE TRIPHOSPHATASE; MOLECULAR MOTOR; PROTEIN BINDING;

ARTICLE; BINDING SITE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DISULFIDE BOND; ENZYME STRUCTURE; GEL MOBILITY SHIFT ASSAY; HEAVY CHAIN; HYDROLYSIS; INTRACELLULAR TRANSPORT; MICROTUBULE; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; METABOLISM; MOLECULAR MODEL; MOUSE; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

ADENOSINE TRIPHOSPHATE; ANIMALS; CRYSTALLOGRAPHY, X-RAY; DYNEINS; HYDROLYSIS; MICE; MICROTUBULES; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR MOTOR PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84949656634     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.11.008     Document Type: Article

References (41)

1. R.D. Vale The molecular motor toolbox for intracellular transport Cell 112 2003 467 480
2. L.M. DiBella, and S.M. King Dynein motors of the Chlamydomonas flagellum Int. Rev. Cytol. 210 2001 227 268
3. N. Hirokawa Kinesin and dynein superfamily proteins and the mechanism of organelle transport Science 279 1998 519 526
4. R.D. Vale, and R.A. Milligan The way things move: Looking under the hood of molecular motor proteins Science 288 2000 88 95
5. M. Schliwa, and G. Woehlke Molecular motors Nature 422 2003 759 765
6. P.D. Coureux, A.L. Wells, J. Ménétrey, C.M. Yengo, C.A. Morris, H.L. Sweeney, and A. Houdusse A structural state of the myosin V motor without bound nucleotide Nature 425 2003 419 423
7. F. Kozielski, S. Sack, A. Marx, M. Thormählen, E. Schönbrunn, V. Biou, A. Thompson, E.M. Mandelkow, and E. Mandelkow The crystal structure of dimeric kinesin and implications for microtubule-dependent motility Cell 91 1997 985 994
8. D.J. Asai, and M.F. Koonce The dynein heavy chain: Structure, mechanics and evolution Trends Cell Biol. 11 2001 196 202
9. N. Mizuno, A. Narita, T. Kon, K. Sutoh, and M. Kikkawa Three-dimensional structure of cytoplasmic dynein bound to microtubules Proc. Natl. Acad. Sci. USA 104 2007 20832 20837
10. M.P. Koonce, P.M. Grissom, M. Lyon, T. Pope, and J.R. McIntosh Molecular characterization of a cytoplasmic dynein from Dictyostelium J. Eukaryot. Microbiol. 41 1994 645 651
11. N. Pollock, M.P. Koonce, E.L. de Hostos, and R.D. Vale In vitro microtubule-based organelle transport in wild-type Dictyostelium and cells overexpressing a truncated dynein heavy chain Cell Motil. Cytoskeleton 40 1998 304 314
12. M. Samsó, M. Radermacher, J. Frank, and M.P. Koonce Structural characterization of a dynein motor domain J. Mol. Biol. 276 1998 927 937
13. P. Höök, A. Mikami, B. Shafer, B.T. Chait, S.S. Rosenfeld, and R.B. Vallee Long range allosteric control of cytoplasmic dynein ATPase activity by the stalk and C-terminal domains J. Biol. Chem. 280 2005 33045 33054
14. T. Kon, T. Mogami, R. Ohkura, M. Nishiura, and K. Sutoh ATP hydrolysis cycle-dependent tail motions in cytoplasmic dynein Nat. Struct. Mol. Biol. 12 2005 513 519
15. T. Shima, T. Kon, K. Imamula, R. Ohkura, and K. Sutoh Two modes of microtubule sliding driven by cytoplasmic dynein Proc. Natl. Acad. Sci. USA 103 2006 17736 17740
16. A.J. Roberts, N. Numata, M.L. Walker, Y.S. Kato, B. Malkova, T. Kon, R. Ohkura, F. Arisaka, P.J. Knight, K. Sutoh, and S.A. Burgess AAA + Ring and linker swing mechanism in the dynein motor Cell 136 2009 485 495
17. S.A. Burgess, S.D. Dover, and D.M. Woolley Architecture of the outer arm dynein ATPase in an avian sperm flagellum, with further evidence for the B-link J. Cell Sci. 98 1991 17 26
18. I.R. Gibbons, J.E. Garbarino, C.E. Tan, S.L. Reck-Peterson, R.D. Vale, and A.P. Carter The affinity of the dynein microtubule-binding domain is modulated by the conformation of its coiled-coil stalk J. Biol. Chem. 280 2005 23960 23965
19. T. Kon, K. Imamula, A.J. Roberts, R. Ohkura, P.J. Knight, I.R. Gibbons, S.A. Burgess, and K. Sutoh Helix sliding in the stalk coiled coil of dynein couples ATPase and microtubule binding Nat. Struct. Mol. Biol. 16 2009 325 333
20. H. Sakakibara, H. Kojima, Y. Sakai, E. Katayama, and K. Oiwa Inner-arm dynein c of Chlamydomonas flagella is a single-headed processive motor Nature 400 1999 586 590
21. S.A. Burgess, M.L. Walker, H. Sakakibara, P.J. Knight, and K. Oiwa Dynein structure and power stroke Nature 421 2003 715 718
22. A.P. Carter, C. Cho, L. Jin, and R.D. Vale Crystal structure of the dynein motor domain Science 331 2011 1159 1165
23. T. Kon, K. Sutoh, and G. Kurisu X-ray structure of a functional full-length dynein motor domain Nat. Struct. Mol. Biol. 18 2011 638 642
24. T. Kon, T. Oyama, R. Shimo-Kon, K. Imamula, T. Shima, K. Sutoh, and G. Kurisu The 2.8 Å crystal structure of the dynein motor domain Nature 484 2012 345 350
25. G. Bhabha, H.C. Cheng, N. Zhang, A. Moeller, M.F. Liao, J.A. Speir, Y.F. Cheng, and R.D. Vale Allosteric communication in the dynein motor domain Cell 159 2014 857 868
26. H. Schmidt, E.S. Gleave, and A.P. Carter Insights into dynein motor domain function from a 3.3-Å crystal structure Nat. Struct. Mol. Biol. 19 2012 492 497
27. H. Schmidt, R. Zalyte, L. Urnavicius, and A.P. Carter Structure of human cytoplasmic dynein-2 primed for its power stroke Nature 518 2015 435 438
28. A.P. Carter, J.E. Garbarino, E.M. Wilson-Kubalek, W.E. Shipley, C. Cho, R.A. Milligan, R.D. Vale, and I.R. Gibbons Structure and functional role of dynein's microtubule-binding domain Science 322 2008 1691 1695
29. Y. Nishikawa, T. Oyama, N. Kamiya, T. Kon, Y.Y. Toyoshima, H. Nakamura, and G. Kurisu Structure of the entire stalk region of the Dynein motor domain J. Mol. Biol. 426 2014 3232 3245
30. Y. Shimizu, Y. Kato, H. Morii, M. Edamatsu, Y.Y. Toyoshima, and M. Tanokura The dynein stalk head, the microtubule binding-domain of dynein: NMR assignment and ligand binding J. Biomol. NMR 41 2008 89 96
31. Y.S. Kato, T. Yagi, S.A. Harris, S.Y. Ohki, K. Yura, Y. Shimizu, S. Honda, R. Kamiya, S.A. Burgess, and M. Tanokura Structure of the microtubule-binding domain of flagellar dynein Structure 22 2014 1628 1638
32. W.B. Redwine, R. Hernández-López, S. Zou, J. Huang, S.L. Reck-Peterson, and A.E. Leschziner Structural basis for microtubule binding and release by dynein Science 337 2012 1532 1536
33. S. Uchimura, T. Fujii, H. Takazaki, R. Ayukawa, Y. Nishikawa, I. Minoura, Y. Hachikubo, G. Kurisu, K. Sutoh, T. Kon, K. Namba, and E. Muto A flipped ion pair at the dynein-microtubule interface is critical for dynein motility and ATPase activation J. Cell Biol. 208 2015 211 222
34. W.L. DeLano The PyMOL Molecular Graphics System, Version 1.6.0.0 2013 Schrodinger, LLC New York, NY
35. H. Imai, T. Shima, K. Sutoh, M.L. Walker, P.J. Knight, T. Kon, and S.A. Burgess Direct observation shows superposition and large scale flexibility within cytoplasmic dynein motors moving along microtubules Nat. Commun. 6 2015 8179
36. J. Walshaw, and D.N. Woolfson SOCKET: A program for identifying and analysing coiled-coil motifs within protein structures J. Mol. Biol. 307 2001 1427 1450
37. S.V. Strelkov, and P. Burkhard Analysis of alpha-helical coiled coils with the program TWISTER reveals a structural mechanism for stutter compensation J. Struct. Biol. 137 2002 54 64
38. A.P. Carter, and R.D. Vale Communication between the AAA + ring and microtubule-binding domain of dynein Biochem. Cell Biol. 88 2010 15 21
39. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
40. P.D. Adams, R.W. Grosse-Kunstleve, L.W. Hung, T.R. Ioerger, A.J. McCoy, N.W. Moriarty, R.J. Read, J.C. Sacchettini, N.K. Sauter, and T.C. Terwilliger PHENIX: Building new software for automated crystallographic structure determination Acta Crystallogr. D Biol. Crystallogr. 58 2002 1948 1954
41. S.C. Lovell, I.W. Davis, W.B. Arendall, P.I. de Bakker, J.M. Word, M.G. Prisant, J.S. Richardson, and D.C. Richardson Structure validation by Calpha geometry: phi, psi and Cbeta Deviation Proteins 50 2003 437 450