Mechanistic origin of microtubule dynamic instability and its modulation by EB proteins

Cell

Volumn 162, Issue 4, 2015, Pages 849-859

  Zhang, Rui ^a   Alushin, Gregory M ^b,d   Brown, Alan ^c   Nogales, Eva ^a,b  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; BINDING PROTEIN; END BINDING PROTEIN; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE DERIVATIVE; KINESIN; NUCLEOTIDE; UNCLASSIFIED DRUG; MICROTUBULE ASSOCIATED PROTEIN;

ARTICLE; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; HYDROLYSIS; MICROTUBULE ASSEMBLY; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; METABOLISM; MICROTUBULE; MOLECULAR GENETICS; MOLECULAR MODEL; PIG; SEQUENCE ALIGNMENT; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANIMALS; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SUS SCROFA;

EID: 84939265872     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.07.012     Document Type: Article

References (42)

1. A. Akhmanova, and M.O. Steinmetz Tracking the ends: a dynamic protein network controls the fate of microtubule tips Nat. Rev. Mol. Cell Biol. 9 2008 309 322
2. M. Allegretti, D.J. Mills, G. McMullan, W. Kühlbrandt, and J. Vonck Atomic model of the F420-reducing [NiFe] hydrogenase by electron cryo-microscopy using a direct electron detector eLife 3 2014 e01963
3. G.M. Alushin, V.H. Ramey, S. Pasqualato, D.A. Ball, N. Grigorieff, A. Musacchio, and E. Nogales The Ndc80 kinetochore complex forms oligomeric arrays along microtubules Nature 467 2010 805 810
4. G.M. Alushin, G.C. Lander, E.H. Kellogg, R. Zhang, D. Baker, and E. Nogales High-resolution microtubule structures reveal the structural transitions in αβ-tubulin upon GTP hydrolysis Cell 157 2014 1117 1129
5. A. Amunts, A. Brown, X.C. Bai, J.L. Llácer, T. Hussain, P. Emsley, F. Long, G. Murshudov, S.H. Scheres, and V. Ramakrishnan Structure of the yeast mitochondrial large ribosomal subunit Science 343 2014 1485 1489
6. K.R. Anders, and D. Botstein Dominant-lethal alpha-tubulin mutants defective in microtubule depolymerization in yeast Mol. Biol. Cell 12 2001 3973 3986
7. A. Brown, F. Long, R.A. Nicholls, J. Toots, P. Emsley, and G. Murshudov Tools for macromolecular model building and refinement into electron cryo-microscopy reconstructions Acta Crystallogr. D Biol. Crystallogr. 71 2015 136 153
8. M.G. Campbell, A. Cheng, A.F. Brilot, A. Moeller, D. Lyumkis, D. Veesler, J. Pan, S.C. Harrison, C.S. Potter, B. Carragher, and N. Grigorieff Movies of ice-embedded particles enhance resolution in electron cryo-microscopy Structure 20 2012 1823 1828
9. M. Caplow, R.L. Ruhlen, and J. Shanks The free energy for hydrolysis of a microtubule-bound nucleotide triphosphate is near zero: all of the free energy for hydrolysis is stored in the microtubule lattice J. Cell Biol. 127 1994 779 788
10. A. des Georges, M. Katsuki, D.R. Drummond, M. Osei, R.A. Cross, and L.A. Amos Mal3, the Schizosaccharomyces pombe homolog of EB1, changes the microtubule lattice Nat. Struct. Mol. Biol. 15 2008 1102 1108
11. A. Desai, and T.J. Mitchison Microtubule polymerization dynamics Annu. Rev. Cell Dev. Biol. 13 1997 83 117
12. C. Dumontet, and M.A. Jordan Microtubule-binding agents: a dynamic field of cancer therapeutics Nat. Rev. Drug Discov. 9 2010 790 803
13. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
14. N. Galjart Plus-end-tracking proteins and their interactions at microtubule ends Curr. Biol. 20 2010 R528 R537
15. V.E. Galkin, A. Orlova, O. Cherepanova, M.C. Lebart, and E.H. Egelman High-resolution cryo-EM structure of the F-actin-fimbrin/plastin ABD2 complex Proc. Natl. Acad. Sci. USA 105 2008 1494 1498
16. E. Hamel, and C.M. Lin Guanosine 5′-O-(3-thiotriphosphate), a potent nucleotide inhibitor of microtubule assembly J. Biol. Chem. 259 1984 11060 11069
17. I. Hayashi, and M. Ikura Crystal structure of the amino-terminal microtubule-binding domain of end-binding protein 1 (EB1) J. Biol. Chem. 278 2003 36430 36434
18. S. Honnappa, S.M. Gouveia, A. Weisbrich, F.F. Damberger, N.S. Bhavesh, H. Jawhari, I. Grigoriev, F.J. van Rijssel, R.M. Buey, A. Lawera, and et al. An EB1-binding motif acts as a microtubule tip localization signal Cell 138 2009 366 376
19. J. Howard, and A.A. Hyman Dynamics and mechanics of the microtubule plus end Nature 422 2003 753 758
20. A.A. Hyman, S. Salser, D.N. Drechsel, N. Unwin, and T.J. Mitchison Role of GTP hydrolysis in microtubule dynamics: information from a slowly hydrolyzable analogue, GMPCPP Mol. Biol. Cell 3 1992 1155 1167
21. Y. Komarova, C.O. De Groot, I. Grigoriev, S.M. Gouveia, E.L. Munteanu, J.M. Schober, S. Honnappa, R.M. Buey, C.C. Hoogenraad, M. Dogterom, and et al. Mammalian end binding proteins control persistent microtubule growth J. Cell Biol. 184 2009 691 706
22. H.Y. Kueh, and T.J. Mitchison Structural plasticity in actin and tubulin polymer dynamics Science 325 2009 960 963
23. X. Li, P. Mooney, S. Zheng, C.R. Booth, M.B. Braunfeld, S. Gubbens, D.A. Agard, and Y. Cheng Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM Nat. Methods 10 2013 584 590
24. E.M. Mandelkow, R. Schultheiss, R. Rapp, M. Müller, and E. Mandelkow On the surface lattice of microtubules: helix starts, protofilament number, seam and handedness J. Cell Biol. 102 1986 1067 1073
25. S.P. Maurer, P. Bieling, J. Cope, A. Hoenger, and T. Surrey GTPgammaS microtubules mimic the growing microtubule end structure recognized by end-binding proteins (EBs) Proc. Natl. Acad. Sci. USA 108 2011 3988 3993
26. S.P. Maurer, F.J. Fourniol, G. Bohner, C.A. Moores, and T. Surrey EBs recognize a nucleotide-dependent structural cap at growing microtubule ends Cell 149 2012 371 382
27. S.P. Maurer, N.I. Cade, G. Bohner, N. Gustafsson, E. Boutant, and T. Surrey EB1 accelerates two conformational transitions important for microtubule maturation and dynamics Curr. Biol. 24 2014 372 384
28. M. Menéndez, G. Rivas, J.F. Díaz, and J.M. Andreu Control of the structural stability of the tubulin dimer by one high affinity bound magnesium ion at nucleotide N-site J. Biol. Chem. 273 1998 167 176
29. T. Mitchison, and M. Kirschner Dynamic instability of microtubule growth Nature 312 1984 237 242
30. A. Nawrotek, M. Knossow, and B. Gigant The determinants that govern microtubule assembly from the atomic structure of GTP-tubulin J. Mol. Biol. 412 2011 35 42
31. E. Nogales, K.H. Downing, L.A. Amos, and J. Löwe Tubulin and FtsZ form a distinct family of GTPases Nat. Struct. Biol. 5 1998 451 458
32. E. Nogales, S.G. Wolf, and K.H. Downing Structure of the alpha beta tubulin dimer by electron crystallography Nature 391 1998 199 203
33. E. Nogales, M. Whittaker, R.A. Milligan, and K.H. Downing High-resolution model of the microtubule Cell 96 1999 79 88
34. M.A. Oliva, S.C. Cordell, and J. Löwe Structural insights into FtsZ protofilament formation Nat. Struct. Mol. Biol. 11 2004 1243 1250
35. A.E. Prota, K. Bargsten, D. Zurwerra, J.J. Field, J.F. Díaz, K.H. Altmann, and M.O. Steinmetz Molecular mechanism of action of microtubule-stabilizing anticancer agents Science 339 2013 587 590
36. L.M. Rice, E.A. Montabana, and D.A. Agard The lattice as allosteric effector: structural studies of alphabeta- and gamma-tubulin clarify the role of GTP in microtubule assembly Proc. Natl. Acad. Sci. USA 105 2008 5378 5383
37. K.C. Slep, and R.D. Vale Structural basis of microtubule plus end tracking by XMAP215, CLIP-170 and EB1 Mol. Cell 27 2007 976 991
38. Y. Song, F. DiMaio, R.Y. Wang, D. Kim, C. Miles, T. Brunette, J. Thompson, and D. Baker High-resolution comparative modeling with RosettaCM Structure 21 2013 1735 1742
39. H. Sui, and K.H. Downing Structural basis of interprotofilament interaction and lateral deformation of microtubules Structure 18 2010 1022 1031
40. C. Suloway, J. Pulokas, D. Fellmann, A. Cheng, F. Guerra, J. Quispe, S. Stagg, C.S. Potter, and B. Carragher Automated molecular microscopy: the new Leginon system J. Struct. Biol. 151 2005 41 60
41. B. Vitre, F.M. Coquelle, C. Heichette, C. Garnier, D. Chrétien, and I. Arnal EB1 regulates microtubule dynamics and tubulin sheet closure in vitro Nat. Cell Biol. 10 2008 415 421
42. Z.C. Zhu, K.K. Gupta, A.R. Slabbekoorn, B.A. Paulson, E.S. Folker, and H.V. Goodson Interactions between EB1 and microtubules: dramatic effect of affinity tags and evidence for cooperative behavior J. Biol. Chem. 284 2009 32651 32661