Molecular basis for age-dependent microtubule acetylation by tubulin acetyltransferase

Cell

Volumn 157, Issue 6, 2014, Pages 1405-1415

  Szyk, Agnieszka ^a   Deaconescu, Alexandra M ^b   Spector, Jeffrey ^a   Goodman, Benjamin ^a   Valenstein, Max L ^a   Ziolkowska, Natasza E ^a   Kormendi, Vasilisa ^a   Grigorieff, Nikolaus ^b   Roll Mecak, Antonina ^a,c  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; LYSINE; POLYMER; TUBULIN;

ACETYLATION; ARTICLE; CATALYSIS; ENZYME ACTIVE SITE; MICROTUBULE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; SURFACE PROPERTY;

ACETYLATION; ACETYLTRANSFERASES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HUMANS; LYSINE; MICROSCOPY, ELECTRON, TRANSMISSION; MICROTUBULES; MODELS, MOLECULAR; TUBULIN;

EID: 84902106884     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.03.061     Document Type: Article

References (74)

1. J.S. Akella, D. Wloga, J. Kim, N.G. Starostina, S. Lyons-Abbott, N.S. Morrissette, S.T. Dougan, E.T. Kipreos, and J. Gaertig MEC-17 is an alpha-tubulin acetyltransferase Nature 467 2010 218 222
2. S. Bechstedt, and G.J. Brouhard Doublecortin recognizes the 13-protofilament microtubule cooperatively and tracks microtubule ends Dev. Cell 23 2012 181 192
3. M.M. Black, P.W. Baas, and S. Humphries Dynamics of alpha-tubulin deacetylation in intact neurons J. Neurosci. 9 1989 358 368
4. P.M. Bungay, and H. Brenner The motion of a closely-fitting sphere in a fluid-filled tube Int. J. Multiph. Flow 1 1973 25 56
5. P.R. Burton Luminal material in microtubules of frog olfactory axons: structure and distribution J. Cell Biol. 99 1984 520 528
6. D. Cai, D.P. McEwen, J.R. Martens, E. Meyhofer, and K.J. Verhey Single molecule imaging reveals differences in microtubule track selection between Kinesin motors PLoS Biol. 7 2009 e1000216
7. D. Chrétien, F. Metoz, F. Verde, E. Karsenti, and R.H. Wade Lattice defects in microtubules: protofilament numbers vary within individual microtubules J. Cell Biol. 117 1992 1031 1040
8. J.R. Cooper, and L. Wordeman The diffusive interaction of microtubule binding proteins Curr. Opin. Cell Biol. 21 2009 68 73
9. J.G. Cueva, J. Hsin, K.C. Huang, and M.B. Goodman Posttranslational acetylation of α-tubulin constrains protofilament number in native microtubules Curr. Biol. 22 2012 1066 1074
10. J.P. Dompierre, J.D. Godin, B.C. Charrin, F.P. Cordelières, S.J. King, S. Humbert, and F. Saudou Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation J. Neurosci. 27 2007 3571 3583
11. F.J. Fourniol, C.V. Sindelar, B. Amigues, D.K. Clare, G. Thomas, M. Perderiset, F. Francis, A. Houdusse, and C.A. Moores Template-free 13-protofilament microtubule-MAP assembly visualized at 8 A resolution J. Cell Biol. 191 2010 463 470
12. D.R. Friedmann, A. Aguilar, J. Fan, M.V. Nachury, and R. Marmorstein Structure of the α-tubulin acetyltransferase, αTAT1, and implications for tubulin-specific acetylation Proc. Natl. Acad. Sci. USA 109 2012 19655 19660
13. C.P. Garnham, and A. Roll-Mecak The chemical complexity of cellular microtubules: tubulin post-translational modification enzymes and their roles in tuning microtubule functions Cytoskeleton (Hoboken) 69 2012 442 463
14. B.K. Garvalov, B. Zuber, C. Bouchet-Marquis, M. Kudryashev, M. Gruska, M. Beck, A. Leis, F. Frischknecht, F. Bradke, and W. Baumeister et al. Luminal particles within cellular microtubules J. Cell Biol. 174 2006 759 765
15. B. Gigant, C. Wang, R.B. Ravelli, F. Roussi, M.O. Steinmetz, P.A. Curmi, A. Sobel, and M. Knossow Structural basis for the regulation of tubulin by vinblastine Nature 435 2005 519 522
16. K. Greer, H. Maruta, S.W. L'Hernault, and J.L. Rosenbaum Alpha-tubulin acetylase activity in isolated Chlamydomonas flagella J. Cell Biol. 101 1985 2081 2084
17. J.W. Hammond, C.F. Huang, S. Kaech, C. Jacobson, G. Banker, and K.J. Verhey Posttranslational modifications of tubulin and the polarized transport of kinesin-1 in neurons Mol. Biol. Cell 21 2010 572 583
18. J. Helenius, G. Brouhard, Y. Kalaidzidis, S. Diez, and J. Howard The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends Nature 441 2006 115 119
19. M.H. Hinrichs, A. Jalal, B. Brenner, E. Mandelkow, S. Kumar, and T. Scholz Tau protein diffuses along the microtubule lattice J. Biol. Chem. 287 2012 38559 38568
20. S.C. Howes, G.M. Alushin, T. Shida, M.V. Nachury, and E. Nogales Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure Mol. Biol. Cell 25 2014 257 266
21. C. Hubbert, A. Guardiola, R. Shao, Y. Kawaguchi, A. Ito, A. Nixon, M. Yoshida, X.F. Wang, and T.P. Yao HDAC6 is a microtubule-associated deacetylase Nature 417 2002 455 458
22. N. Kalebic, C. Martinez, E. Perlas, P. Hublitz, D. Bilbao-Cortes, K. Fiedorczuk, A. Andolfo, and P.A. Heppenstall Tubulin acetyltransferase αTAT1 destabilizes microtubules independently of its acetylation activity Mol. Cell. Biol. 33 2013 1114 1123
23. G.W. Kim, L. Li, M. Gorbani, L. You, and X.J. Yang Mice lacking α-tubulin acetyltransferase 1 are viable but display α-tubulin acetylation deficiency and dentate gyrus distortion J. Biol. Chem. 288 2013 20334 20350
24. V. Kormendi, A. Szyk, G. Piszczek, and A. Roll-Mecak Crystal structures of tubulin acetyltransferase reveal a conserved catalytic core and the plasticity of the essential N terminus J. Biol. Chem. 287 2012 41569 41575
25. S.W. L'Hernault, and J.L. Rosenbaum Chlamydomonas alpha-tubulin is posttranslationally modified by acetylation on the epsilon-amino group of a lysine Biochemistry 24 1985 473 478
26. M. LeDizet, and G. Piperno Identification of an acetylation site of Chlamydomonas alpha-tubulin Proc. Natl. Acad. Sci. USA 84 1987 5720 5724
27. L. Li, D. Wei, Q. Wang, J. Pan, R. Liu, X. Zhang, and L. Bao MEC-17 deficiency leads to reduced α-tubulin acetylation and impaired migration of cortical neurons J. Neurosci. 32 2012 12673 12683
28. X. Liu, L. Wang, K. Zhao, P.R. Thompson, Y. Hwang, R. Marmorstein, and P.A. Cole The structural basis of protein acetylation by the p300/CBP transcriptional coactivator Nature 451 2008 846 850
29. H. Maruta, K. Greer, and J.L. Rosenbaum The acetylation of alpha-tubulin and its relationship to the assembly and disassembly of microtubules J. Cell Biol. 103 1986 571 579
30. 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
31. E. Meijering, O. Dzyubachyk, and I. Smal Methods for cell and particle tracking Methods Enzymol. 504 2012 183 200
32. A.M. Mulder, A. Glavis-Bloom, C.A. Moores, M. Wagenbach, B. Carragher, L. Wordeman, and R.A. Milligan A new model for binding of kinesin 13 to curved microtubule protofilaments J. Cell Biol. 185 2009 51 57
33. B. Neumann, and M.A. Hilliard Loss of MEC-17 leads to microtubule instability and axonal degeneration Cell Rep. 6 2014 93 103
34. D. Nicastro, C. Schwartz, J. Pierson, R. Gaudette, M.E. Porter, and J.R. McIntosh The molecular architecture of axonemes revealed by cryoelectron tomography Science 313 2006 944 948
35. E. Nogales, S.G. Wolf, and K.H. Downing Structure of the alpha beta tubulin dimer by electron crystallography Nature 391 1998 199 203
36. E. Nogales, M. Whittaker, R.A. Milligan, and K.H. Downing High-resolution model of the microtubule Cell 96 1999 79 88
37. B.J. North, B.L. Marshall, M.T. Borra, J.M. Denu, and E. Verdin The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase Mol. Cell 11 2003 437 444
38. D. Odde Diffusion inside microtubules Eur. Biophys. J. 27 1998 514 520
39. G. Piperno, and M.T. Fuller Monoclonal antibodies specific for an acetylated form of alpha-tubulin recognize the antigen in cilia and flagella from a variety of organisms J. Cell Biol. 101 1985 2085 2094
40. G. Piperno, M. LeDizet, and X.J. Chang Microtubules containing acetylated alpha-tubulin in mammalian cells in culture J. Cell Biol. 104 1987 289 302
41. A.N. Poux, M. Cebrat, C.M. Kim, P.A. Cole, and R. Marmorstein Structure of the GCN5 histone acetyltransferase bound to a bisubstrate inhibitor Proc. Natl. Acad. Sci. USA 99 2002 14065 14070
42. N.A. Reed, D. Cai, T.L. Blasius, G.T. Jih, E. Meyhofer, J. Gaertig, and K.J. Verhey Microtubule acetylation promotes kinesin-1 binding and transport Curr. Biol. 16 2006 2166 2172
43. A. Roll-Mecak, and R.D. Vale Structural basis of microtubule severing by the hereditary spastic paraplegia protein spastin Nature 451 2008 363 367
44. E. Schulze, and M. Kirschner Dynamic and stable populations of microtubules in cells J. Cell Biol. 104 1987 277 288
45. E. Schulze, D.J. Asai, J.C. Bulinski, and M. Kirschner Posttranslational modification and microtubule stability J. Cell Biol. 105 1987 2167 2177
46. T. Shida, J.G. Cueva, Z. Xu, M.B. Goodman, and M.V. Nachury The major alpha-tubulin K40 acetyltransferase alphaTAT1 promotes rapid ciliogenesis and efficient mechanosensation Proc. Natl. Acad. Sci. USA 107 2010 21517 21522
47. V. Soppina, J.F. Herbstman, G. Skiniotis, and K.J. Verhey Luminal localization of α-tubulin K40 acetylation by cryo-EM analysis of fab-labeled microtubules PLoS ONE 7 2012 e48204
48. R. Subramanian, S.C. Ti, L. Tan, S.A. Darst, and T.M. Kapoor Marking and measuring single microtubules by PRC1 and kinesin-4 Cell 154 2013 377 390
49. H. Sui, and K.H. Downing Molecular architecture of axonemal microtubule doublets revealed by cryo-electron tomography Nature 442 2006 475 478
50. S. Tahirovic, and F. Bradke Neuronal polarity Cold Spring Harb. Perspect. Biol. 1 2009 a001644
51. R. Takemura, S. Okabe, T. Umeyama, Y. Kanai, N.J. Cowan, and N. Hirokawa Increased microtubule stability and alpha tubulin acetylation in cells transfected with microtubule-associated proteins MAP1B, MAP2 or tau J. Cell Sci. 103 1992 953 964
52. M. Taschner, M. Vetter, and E. Lorentzen Atomic resolution structure of human α-tubulin acetyltransferase bound to acetyl-CoA Proc. Natl. Acad. Sci. USA 109 2012 19649 19654
53. I. Topalidou, C. Keller, N. Kalebic, K.C. Nguyen, H. Somhegyi, K.A. Politi, P. Heppenstall, D.H. Hall, and M. Chalfie Genetically separable functions of the MEC-17 tubulin acetyltransferase affect microtubule organization Curr. Biol. 22 2012 1057 1065
54. V. Varga, C. Leduc, V. Bormuth, S. Diez, and J. Howard Kinesin-8 motors act cooperatively to mediate length-dependent microtubule depolymerization Cell 138 2009 1174 1183
55. P.H. von Hippel, and O.G. Berg Facilitated target location in biological systems J. Biol. Chem. 264 1989 675 678
56. D.R. Webster, and G.G. Borisy Microtubules are acetylated in domains that turn over slowly J. Cell Sci. 92 1989 57 65
57. D. Wloga, and J. Gaertig Post-translational modifications of microtubules J. Cell Sci. 123 2010 3447 3455
58. H. Xiao, P. Verdier-Pinard, N. Fernandez-Fuentes, B. Burd, R. Angeletti, A. Fiser, S.B. Horwitz, and G.A. Orr Insights into the mechanism of microtubule stabilization by Taxol Proc. Natl. Acad. Sci. USA 103 2006 10166 10173
59. H. Yajima, T. Ogura, R. Nitta, Y. Okada, C. Sato, and N. Hirokawa Conformational changes in tubulin in GMPCPP and GDP-taxol microtubules observed by cryoelectron microscopy J. Cell Biol. 198 2012 315 322
60. Y. Zhang, C. Ma, T. Delohery, B. Nasipak, B.C. Foat, A. Bounoutas, H.J. Bussemaker, S.K. Kim, and M. Chalfie Identification of genes expressed in C. elegans touch receptor neurons Nature 418 2002 331 335
61. N.E. Ziółkowska, and A. Roll-Mecak In vitro microtubule severing assays Methods Mol. Biol. 1046 2013 323 334
62. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
63. D. Beckett, E. Kovaleva, and P.J. Schatz A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation Protein Sci. 8 1999 921 929
64. J. Crank The Mathematics of Diffusion Second Edition 1975 Oxford University Press London, UK
65. A.O. Demchouk, M.K. Gardner, and D.J. Odde Microtubule tip tracking and tip structures at the nanometer scale using digital fluorescence microscopy Cell Mol. Bioeng. 4 2011 192 204
66. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
67. J.R. Kremer, D.N. Mastronarde, and J.R. McIntosh Computer visualization of three-dimensional image data using IMOD J. Struct. Biol. 116 1996 71 76
68. T. Manna, S. Honnappa, M.O. Steinmetz, and L. Wilson Suppression of microtubule dynamic instability by the +TIP protein EB1 and its modulation by the CAP-Gly domain of p150glued Biochemistry 47 2008 779 786
69. D.N. Mastronarde Automated electron microscope tomography using robust prediction of specimen movements J. Struct. Biol. 152 2005 36 51
70. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Cryst. 40 2007 658 674
71. A.W. Murray Cell cycle extracts Methods Cell Biol. 36 1991 581 605
72. G.N. Murshudov, P. Skubák, A.A. Lebedev, N.S. Pannu, R.A. Steiner, R.A. Nicholls, M.D. Winn, F. Long, and A.A. Vagin REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr. D Biol. Crystallogr. 67 2011 355 367
73. T.F. Outeiro, E. Kontopoulos, S.M. Altmann, I. Kufareva, K.E. Strathearn, A.M. Amore, C.B. Volk, M.M. Maxwell, J.C. Rochet, and P.J. McLean et al. Sirtuin 2 inhibitors rescue alpha-synuclein-mediated toxicity in models of Parkinson's disease Science 317 2007 516 519
74. P.O. Widlund, M. Podolski, S. Reber, J. Alper, M. Storch, A.A. Hyman, J. Howard, and D.N. Drechsel One-step purification of assembly-competent tubulin from diverse eukaryotic sources Mol. Biol. Cell 23 2012 4393 4401