Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure

Howes, Stuart C.; Alushin, Gregory M.; Shida, Toshinobu; Nachury, Maxence V.; Nogales, Eva

doi:10.1091/mbc.e13-07-0387

Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure

Journal Article · Wed Nov 13 04:00:00 EST 2013 · Molecular Biology of the Cell

DOI:https://doi.org/10.1091/mbc.e13-07-0387· OSTI ID:1625232

Howes, Stuart C. ^[1]; Alushin, Gregory M. ^[2]; Shida, Toshinobu ^[3]; Nachury, Maxence V. ^[3]; Nogales, Eva ^[4]

Univ. of California, Berkeley, CA (United States). Biophysics Graduate Group; DOE/OSTI
Univ. of California, Berkeley, CA (United States).Howard Hughes Medical Inst. Dept. of Molecular and Cell Biology
Stanford Univ., CA (United States). School of Medicine. Dept. of Molecular and Cellular Physiology
Univ. of California, Berkeley, CA (United States).Howard Hughes Medical Inst. Dept. of Molecular and Cell Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division

Tubulin undergoes posttranslational modifications proposed to specify microtubule subpopulations for particular functions. Most of these modifications occur on the C-termini of tubulin and may directly affect the binding of microtubule-associated proteins (MAPs) or motors. Acetylation of Lys-40 on α-tubulin is unique in that it is located on the luminal surface of microtubules, away from the interaction sites of most MAPs and motors. We investigate whether acetylation alters the architecture of microtubules or the conformation of tubulin, using cryo–electron microscopy (cryo-EM). No significant changes are observed based on protofilament distributions or microtubule helical lattice parameters. Furthermore, no clear differences in tubulin structure are detected between cryo-EM reconstructions of maximally deacetylated or acetylated microtubules. Our results indicate that the effect of acetylation must be highly localized and affect interaction with proteins that bind directly to the lumen of the microtubule. We also investigate the interaction of the tubulin acetyltransferase, αTAT1, with microtubules and find that αTAT1 is able to interact with the outside of the microtubule, at least partly through the tubulin C-termini. Binding to the outside surface of the microtubule could facilitate access of αTAT1 to its luminal site of action if microtubules undergo lateral opening between protofilaments.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1625232

Journal Information:: Molecular Biology of the Cell, Journal Name: Molecular Biology of the Cell Journal Issue: 2 Vol. 25; ISSN 1059-1524

Publisher:: American Society for Cell BiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (71)

Requirement for Microtubules in New Membrane Formation during Cytokinesis ofXenopusEmbryos Danilchik, M. V.; Funk, W. C.; Brown, E. E. Developmental Biology, Vol. 194, Issue 1 https://doi.org/10.1006/dbio.1997.8815	journal	February 1998
Relationship between the Golgi complex and microtubules enriched in detyrosinated or acetylated ?-tubulin: studies on cells recovering from nocodazole and cells in the terminal phase of cytokinesis Thyberg, Johan; Moskalewski, Stanislaw Cell & Tissue Research, Vol. 273, Issue 3 https://doi.org/10.1007/bf00333700	journal	September 1993
Diffusion inside microtubules Odde, David European Biophysics Journal, Vol. 27, Issue 5 https://doi.org/10.1007/s002490050161	journal	August 1998
Microtubule Modification: Acetylation Speeds Anterograde Traffic Flow Bulinski, J. Chloë Current Biology, Vol. 17, Issue 1 https://doi.org/10.1016/j.cub.2006.11.036	journal	January 2007
Posttranslational Acetylation of α-Tubulin Constrains Protofilament Number in Native Microtubules Cueva, Juan G.; Hsin, Jen; Huang, Kerwyn Casey Current Biology, Vol. 22, Issue 12 https://doi.org/10.1016/j.cub.2012.05.012	journal	June 2012
The bromodomain interaction module Filippakopoulos, Panagis; Knapp, Stefan FEBS Letters, Vol. 586, Issue 17 https://doi.org/10.1016/j.febslet.2012.04.045	journal	May 2012
Automated molecular microscopy: The new Leginon system Suloway, Christian; Pulokas, James; Fellmann, Denis Journal of Structural Biology, Vol. 151, Issue 1 https://doi.org/10.1016/j.jsb.2005.03.010	journal	July 2005
EMAN2: An extensible image processing suite for electron microscopy Tang, Guang; Peng, Liwei; Baldwin, Philip R. Journal of Structural Biology, Vol. 157, Issue 1 https://doi.org/10.1016/j.jsb.2006.05.009	journal	January 2007
The iterative helical real space reconstruction method: Surmounting the problems posed by real polymers Egelman, Edward H. Journal of Structural Biology, Vol. 157, Issue 1 https://doi.org/10.1016/j.jsb.2006.05.015	journal	January 2007
Appion: An integrated, database-driven pipeline to facilitate EM image processing Lander, Gabriel C.; Stagg, Scott M.; Voss, Neil R. Journal of Structural Biology, Vol. 166, Issue 1 https://doi.org/10.1016/j.jsb.2009.01.002	journal	April 2009
Structural Basis of Interprotofilament Interaction and Lateral Deformation of Microtubules Sui, Haixin; Downing, Kenneth H. Structure, Vol. 18, Issue 8 https://doi.org/10.1016/j.str.2010.05.010	journal	August 2010
+TIPs: SxIPping along microtubule ends Kumar, Praveen; Wittmann, Torsten Trends in Cell Biology, Vol. 22, Issue 8 https://doi.org/10.1016/j.tcb.2012.05.005	journal	August 2012
CLIP-170 Highlights Growing Microtubule Ends In Vivo Perez, Franck; Diamantopoulos, Georgios S.; Stalder, Romaine Cell, Vol. 96, Issue 4 https://doi.org/10.1016/s0092-8674(00)80656-x	journal	February 1999
High-Resolution Model of the Microtubule Nogales, Eva; Whittaker, Michael; Milligan, Ronald A. Cell, Vol. 96, Issue 1 https://doi.org/10.1016/s0092-8674(00)80961-7	journal	January 1999
How does taxol stabilize microtubules? Arnal, Isabelle; Wade, Richard H. Current Biology, Vol. 5, Issue 8 https://doi.org/10.1016/s0960-9822(95)00180-1	journal	August 1995
The Human Sir2 Ortholog, SIRT2, Is an NAD+-Dependent Tubulin Deacetylase North, Brian J.; Marshall, Brett L.; Borra, Margie T. Molecular Cell, Vol. 11, Issue 2 https://doi.org/10.1016/s1097-2765(03)00038-8	journal	February 2003
Chlamydomonas .alpha.-tubulin is posttranslationally modified by acetylation on the .epsilon.-amino group of a lysine L'Hernault, Steven W.; Rosenbaum, Joel L. Biochemistry, Vol. 24, Issue 2 https://doi.org/10.1021/bi00323a034	journal	January 1985
Microtubule Structure at Improved Resolution ^† Meurer-Grob, Patricia; Kasparian, Jérôme; Wade, Richard H. Biochemistry, Vol. 40, Issue 27 https://doi.org/10.1021/bi010343p	journal	July 2001
A structural change in the kinesin motor protein that drives motility Rice, Sarah; Lin, Abel W.; Safer, Daniel Nature, Vol. 402, Issue 6763 https://doi.org/10.1038/45483	journal	December 1999
Molecular basis of the acetyltransferase activity of MEC-17 towards α-tubulin Li, Wenjing; Zhong, Chen; Li, Lei Cell Research, Vol. 22, Issue 12 https://doi.org/10.1038/cr.2012.154	journal	November 2012
Structural basis for the regulation of tubulin by vinblastine Gigant, Benoît; Wang, Chunguang; Ravelli, Raimond B. G. Nature, Vol. 435, Issue 7041 https://doi.org/10.1038/nature03566	journal	May 2005
Tubulin tyrosination navigates the kinesin-1 motor domain to axons Konishi, Yoshiyuki; Setou, Mitsutoshi Nature Neuroscience, Vol. 12, Issue 5 https://doi.org/10.1038/nn.2314	journal	April 2009
Tubulin acetyltransferase discovered: Ciliary role in the ancestral eukaryote expanded to neurons in metazoans Leroux, Michel R. Proceedings of the National Academy of Sciences, Vol. 107, Issue 50 https://doi.org/10.1073/pnas.1016396108	journal	December 2010
Structure of the -tubulin acetyltransferase, TAT1, and implications for tubulin-specific acetylation Friedmann, D. R.; Aguilar, A.; Fan, J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 48 https://doi.org/10.1073/pnas.1209357109	journal	October 2012
α-Tubulin acetylation from the inside out Al-Bassam, Jawdat; Corbett, Kevin D. Proceedings of the National Academy of Sciences, Vol. 109, Issue 48 https://doi.org/10.1073/pnas.1217594109	journal	November 2012
Identification of an acetylation site of Chlamydomonas alpha-tubulin. LeDizet, M.; Piperno, G. Proceedings of the National Academy of Sciences, Vol. 84, Issue 16 https://doi.org/10.1073/pnas.84.16.5720	journal	August 1987
Crystal Structures of Tubulin Acetyltransferase Reveal a Conserved Catalytic Core and the Plasticity of the Essential N Terminus* Kormendi, Vasilisa; Szyk, Agnieszka; Piszczek, Grzegorz Journal of Biological Chemistry, Vol. 287, Issue 50 https://doi.org/10.1074/jbc.c112.421222	journal	December 2012
Cytoplasmic microtubules containing acetylated alpha-tubulin in Chlamydomonas reinhardtii: spatial arrangement and properties LeDizet, M. The Journal of Cell Biology, Vol. 103, Issue 1 https://doi.org/10.1083/jcb.103.1.13	journal	July 1986
The acetylation of alpha-tubulin and its relationship to the assembly and disassembly of microtubules Maruta, H. The Journal of Cell Biology, Vol. 103, Issue 2 https://doi.org/10.1083/jcb.103.2.571	journal	August 1986
Microtubules containing acetylated alpha-tubulin in mammalian cells in culture. Piperno, G.; LeDizet, M.; Chang, X. J. The Journal of Cell Biology, Vol. 104, Issue 2 https://doi.org/10.1083/jcb.104.2.289	journal	February 1987
Motor-dependent microtubule disassembly driven by tubulin tyrosination Peris, Leticia; Wagenbach, Michael; Lafanechère, Laurence Journal of Cell Biology, Vol. 185, Issue 7 https://doi.org/10.1083/jcb.200902142	journal	June 2009
ER sliding dynamics and ER–mitochondrial contacts occur on acetylated microtubules Friedman, Jonathan R.; Webster, Brant M.; Mastronarde, David N. Journal of Cell Biology, Vol. 190, Issue 3 https://doi.org/10.1083/jcb.200911024	journal	August 2010
Chlamydomonas alpha-tubulin is posttranslationally modified in the flagella during flagellar assembly. L'Hernault, S. W.; Rosenbaum, J. L. Journal of Cell Biology, Vol. 97, Issue 1 https://doi.org/10.1083/jcb.97.1.258	journal	July 1983
Luminal material in microtubules of frog olfactory axons: structure and distribution. Burton, P. R. Journal of Cell Biology, Vol. 99, Issue 2 https://doi.org/10.1083/jcb.99.2.520	journal	August 1984
A novel acetylation of β-tubulin by San modulates microtubule polymerization via down-regulating tubulin incorporation Chu, Chih-Wen; Hou, Fajian; Zhang, Junmei Molecular Biology of the Cell, Vol. 22, Issue 4 https://doi.org/10.1091/mbc.e10-03-0203	journal	February 2011
The posttranslational modification of tubulin undergoes a switch from detyrosination to acetylation as epithelial cells become polarized Quinones, Geraldine B.; Danowski, Barbara A.; Devaraj, Anjan Molecular Biology of the Cell, Vol. 22, Issue 7 https://doi.org/10.1091/mbc.e10-06-0519	journal	April 2011
Lysine Acetylation Targets Protein Complexes and Co-Regulates Major Cellular Functions Choudhary, C.; Kumar, C.; Gnad, F. Science, Vol. 325, Issue 5942 https://doi.org/10.1126/science.1175371	journal	July 2009
Posttranslational glutamylation of alpha-tubulin Edde, B.; Rossier, J.; Le Caer, J. Science, Vol. 247, Issue 4938 https://doi.org/10.1126/science.1967194	journal	January 1990
Tubulin Acetyltransferase αTAT1 Destabilizes Microtubules Independently of Its Acetylation Activity Kalebic, Nereo; Martinez, Concepcion; Perlas, Emerald Molecular and Cellular Biology, Vol. 33, Issue 6 https://doi.org/10.1128/mcb.01044-12	journal	December 2012
Tubulin in sea urchin embryonic cilia: post-translational modifications during regeneration Stephens, R. E. Journal of Cell Science, Vol. 101, Issue 4 https://doi.org/10.1242/jcs.101.4.837	journal	April 1992
Single Molecule Imaging Reveals Differences in Microtubule Track Selection Between Kinesin Motors Cai, Dawen; McEwen, Dyke P.; Martens, Jeffery R. PLoS Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pbio.1000216	journal	October 2009
Acetylation of Microtubules Influences Their Sensitivity to Severing by Katanin in Neurons and Fibroblasts Sudo, H.; Baas, P. W. Journal of Neuroscience, Vol. 30, Issue 21 https://doi.org/10.1523/jneurosci.0048-10.2010	journal	May 2010
Luminal particles within cellular microtubules. Bradke, Frank; Frischknecht, Friedrich; Dubochet, Jacques Rockefeller Institute Press https://doi.org/10.7892/boris.74797	text	January 2006
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
The Effect of Temperature on the Structure of Vinblastine-induced Polymers of Purified Tubulin: Detection of a Reversible Conformational Change Nogales, Eva; Medrano, Francisco J.; Diakun, Greg P. Journal of Molecular Biology, Vol. 254, Issue 3 https://doi.org/10.1006/jmbi.1995.0628	journal	December 1995
Relationship between the Golgi complex and microtubules enriched in detyrosinated or acetylated ?-tubulin: studies on cells recovering from nocodazole and cells in the terminal phase of cytokinesis Thyberg, Johan; Moskalewski, Stanislaw Cell & Tissue Research, Vol. 273, Issue 3 https://doi.org/10.1007/BF00333700	journal	September 1993
Low resolution structure of microtubules in solution Andreu, J. M.; Bordas, J.; Diaz, J. F. Journal of Molecular Biology, Vol. 226, Issue 1 https://doi.org/10.1016/0022-2836(92)90132-4	journal	July 1992
CLIP-170 Highlights Growing Microtubule Ends In Vivo Perez, Franck; Diamantopoulos, Georgios S.; Stalder, Romaine Cell, Vol. 96, Issue 4 https://doi.org/10.1016/S0092-8674(00)80656-X	journal	February 1999
High-Resolution Model of the Microtubule Nogales, Eva; Whittaker, Michael; Milligan, Ronald A. Cell, Vol. 96, Issue 1 https://doi.org/10.1016/S0092-8674(00)80961-7	journal	January 1999
The dynamic behavior of the APC-binding protein EB1 on the distal ends of microtubules Mimori-Kiyosue, Yuko; Shiina, Nobuyuki; Tsukita, Shoichiro Current Biology, Vol. 10, Issue 14 https://doi.org/10.1016/S0960-9822(00)00600-X	journal	July 2000
How does taxol stabilize microtubules? Arnal, Isabelle; Wade, Richard H. Current Biology, Vol. 5, Issue 8 https://doi.org/10.1016/S0960-9822(95)00180-1	journal	August 1995
Microtubule Structure at 8 Å Resolution Li, Huilin; DeRosier, David J.; Nicholson, William V. Structure, Vol. 10, Issue 10 https://doi.org/10.1016/S0969-2126(02)00827-4	journal	October 2002
HDAC6 Deacetylase Activity Links the Tubulin Cytoskeleton with Immune Synapse Organization Serrador, Juan M.; Cabrero, Jose Román; Sancho, David Immunity, Vol. 20, Issue 4 https://doi.org/10.1016/S1074-7613(04)00078-0	journal	April 2004
The Human Sir2 Ortholog, SIRT2, Is an NAD+-Dependent Tubulin Deacetylase North, Brian J.; Marshall, Brett L.; Borra, Margie T. Molecular Cell, Vol. 11, Issue 2 https://doi.org/10.1016/S1097-2765(03)00038-8	journal	February 2003
Elongator Controls the Migration and Differentiation of Cortical Neurons through Acetylation of α-Tubulin Creppe, Catherine; Malinouskaya, Lina; Volvert, Marie-Laure Cell, Vol. 136, Issue 3 https://doi.org/10.1016/j.cell.2008.11.043	journal	February 2009
Microtubule Acetylation Promotes Kinesin-1 Binding and Transport Reed, Nathan A.; Cai, Dawen; Blasius, T. Lynne Current Biology, Vol. 16, Issue 21 https://doi.org/10.1016/j.cub.2006.09.014	journal	November 2006
HDAC6 is a microtubule-associated deacetylase Hubbert, Charlotte; Guardiola, Amaris; Shao, Rong Nature, Vol. 417, Issue 6887 https://doi.org/10.1038/417455a	journal	May 2002
MEC-17 is an α-tubulin acetyltransferase Akella, Jyothi S.; Wloga, Dorota; Kim, Jihyun Nature, Vol. 467, Issue 7312 https://doi.org/10.1038/nature09324	journal	September 2010
Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions Janke, Carsten; Chloë Bulinski, Jeannette Nature Reviews Molecular Cell Biology, Vol. 12, Issue 12 https://doi.org/10.1038/nrm3227	journal	November 2011
Visualization of cell microtubules in their native state Bouchet-Marquis, Cédric; Zuber, Benoît; Glynn, Anne-Marie Biology of the Cell, Vol. 99, Issue 1 https://doi.org/10.1042/BC20060081	journal	January 2007
The major -tubulin K40 acetyltransferase TAT1 promotes rapid ciliogenesis and efficient mechanosensation Shida, T.; Cueva, J. G.; Xu, Z. Proceedings of the National Academy of Sciences, Vol. 107, Issue 50 https://doi.org/10.1073/pnas.1013728107	journal	November 2010
Atomic resolution structure of human -tubulin acetyltransferase bound to acetyl-CoA Taschner, M.; Vetter, M.; Lorentzen, E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 48 https://doi.org/10.1073/pnas.1209343109	journal	October 2012
Crystal Structures of Tubulin Acetyltransferase Reveal a Conserved Catalytic Core and the Plasticity of the Essential N Terminus* Kormendi, Vasilisa; Szyk, Agnieszka; Piszczek, Grzegorz Journal of Biological Chemistry, Vol. 287, Issue 50 https://doi.org/10.1074/jbc.C112.421222	journal	December 2012
Fast Kinetics of Taxol Binding to Microtubules Dı́az, José Fernando; Barasoain, Isabel; Andreu, José Manuel Journal of Biological Chemistry, Vol. 278, Issue 10 https://doi.org/10.1074/jbc.M211163200	journal	March 2003
Monoclonal antibodies specific for an acetylated form of alpha-tubulin recognize the antigen in cilia and flagella from a variety of organisms. Piperno, G.; Fuller, M. T. The Journal of Cell Biology, Vol. 101, Issue 6 https://doi.org/10.1083/jcb.101.6.2085	journal	December 1985
Posttranslational modifications of alpha tubulin: detyrosination and acetylation differentiate populations of interphase microtubules in cultured cells. Bulinski, J. C.; Richards, J. E.; Piperno, G. Journal of Cell Biology, Vol. 106, Issue 4 https://doi.org/10.1083/jcb.106.4.1213	journal	April 1988
Kinesin-13s form rings around microtubules Tan, Dongyan; Asenjo, Ana B.; Mennella, Vito Journal of Cell Biology, Vol. 175, Issue 1 https://doi.org/10.1083/jcb.200605194	journal	October 2006
Luminal particles within cellular microtubules Garvalov, Boyan K.; Zuber, Benoît; Bouchet-Marquis, Cédric The Journal of Cell Biology, Vol. 174, Issue 6 https://doi.org/10.1083/jcb.200606074	journal	September 2006
Differential trafficking of Kif5c on tyrosinated and detyrosinated microtubules in live cells Dunn, Sarah; Morrison, Ewan E.; Liverpool, Tanniemola B. Journal of Cell Science, Vol. 121, Issue 7 https://doi.org/10.1242/jcs.026492	journal	April 2008
Dysferlin Interacts with Histone Deacetylase 6 and Increases alpha-Tubulin Acetylation Di Fulvio, Sabrina; Azakir, Bilal A.; Therrien, Christian PLoS ONE, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pone.0028563	journal	December 2011
Acetylation of Microtubules Influences Their Sensitivity to Severing by Katanin in Neurons and Fibroblasts Sudo, H.; Baas, P. W. Journal of Neuroscience, Vol. 30, Issue 21 https://doi.org/10.1523/JNEUROSCI.0048-10.2010	journal	May 2010

Cited By (53)

Back to the tubule: microtubule dynamics in Parkinson’s disease Pellegrini, Laura; Wetzel, Andrea; Grannó, Simone Cellular and Molecular Life Sciences, Vol. 74, Issue 3 https://doi.org/10.1007/s00018-016-2351-6	journal	September 2016
The world of protein acetylation Drazic, Adrian; Myklebust, Line M.; Ree, Rasmus Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1864, Issue 10 https://doi.org/10.1016/j.bbapap.2016.06.007	journal	October 2016
Effects of α-Tubulin K40 Acetylation and Detyrosination on Kinesin-1 Motility in a Purified System Kaul, Neha; Soppina, Virupakshi; Verhey, Kristen J. Biophysical Journal, Vol. 106, Issue 12 https://doi.org/10.1016/j.bpj.2014.05.008	journal	June 2014
The Motility of Axonemal Dynein Is Regulated by the Tubulin Code Alper, Joshua D.; Decker, Franziska; Agana, Bernice Biophysical Journal, Vol. 107, Issue 12 https://doi.org/10.1016/j.bpj.2014.10.061	journal	December 2014
Causes and Consequences of Microtubule Acetylation Janke, Carsten; Montagnac, Guillaume Current Biology, Vol. 27, Issue 23 https://doi.org/10.1016/j.cub.2017.10.044	journal	December 2017
Exome-wide Rare Variant Analysis Identifies TUBA4A Mutations Associated with Familial ALS Smith, Bradley N.; Ticozzi, Nicola; Fallini, Claudia Neuron, Vol. 84, Issue 2 https://doi.org/10.1016/j.neuron.2014.09.027	journal	October 2014
Long intergenic non-coding RNA APOC1P1-3 inhibits apoptosis by decreasing α-tubulin acetylation in breast cancer Liao, X-H; Wang, J-G; Li, L-Y Cell Death & Disease, Vol. 7, Issue 5 https://doi.org/10.1038/cddis.2016.142	journal	May 2016
Oncogenic microtubule hyperacetylation through BEX4-mediated sirtuin 2 inhibition Lee, Jin-Kwan; Lee, Janet; Go, Heounjeong Cell Death & Disease, Vol. 7, Issue 8 https://doi.org/10.1038/cddis.2016.240	journal	August 2016
αTAT1 downregulation induces mitotic catastrophe in HeLa and A549 cells Chien, J-Y; Tsen, S-D; Chien, C-C Cell Death Discovery, Vol. 2, Issue 1 https://doi.org/10.1038/cddiscovery.2016.6	journal	February 2016
MicroRNA-92a is a circadian modulator of neuronal excitability in Drosophila Chen, Xiao; Rosbash, Michael Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14707	journal	March 2017
Nucleotide– and Mal3-dependent changes in fission yeast microtubules suggest a structural plasticity view of dynamics von Loeffelholz, Ottilie; Venables, Neil A.; Drummond, Douglas Robert Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-02241-5	journal	December 2017
The Elongator subunit Elp3 is a non-canonical tRNA acetyltransferase Lin, Ting-Yu; Abbassi, Nour El Hana; Zakrzewski, Karol Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08579-2	journal	February 2019
Human histone deacetylase 6 shows strong preference for tubulin dimers over assembled microtubules Skultetyova, Lubica; Ustinova, Kseniya; Kutil, Zsofia Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-11739-3	journal	September 2017
αTAT1 controls longitudinal spreading of acetylation marks from open microtubules extremities Ly, Nathalie; Elkhatib, Nadia; Bresteau, Enzo Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep35624	journal	October 2016
Regulation of microtubule disassembly by spatially heterogeneous patterns of acetylation J. S., Aparna; Padinhateeri, Ranjith; Das, Dibyendu Soft Matter, Vol. 16, Issue 12 https://doi.org/10.1039/c9sm02198a	journal	January 2020
Cilium structure, assembly, and disassembly regulated by the cytoskeleton Mirvis, Mary; Stearns, Tim; James Nelson, W. Biochemical Journal, Vol. 475, Issue 14 https://doi.org/10.1042/bcj20170453	journal	July 2018
Histone deacetylase 3 indirectly modulates tubulin acetylation Bacon, Travis; Seiler, Caroline; Wolny, Marcin Biochemical Journal, Vol. 472, Issue 3 https://doi.org/10.1042/bj20150660	journal	November 2015
Effects of α-tubulin acetylation on microtubule structure and stability Eshun-Wilson, Lisa; Zhang, Rui; Portran, Didier Proceedings of the National Academy of Sciences, Vol. 116, Issue 21 https://doi.org/10.1073/pnas.1900441116	journal	May 2019
Structural and functional differences between porcine brain and budding yeast microtubules Howes, Stuart C.; Geyer, Elisabeth A.; LaFrance, Benjamin Cell Cycle, Vol. 17, Issue 3 https://doi.org/10.1080/15384101.2017.1415680	journal	January 2018
The tubulin code: Molecular components, readout mechanisms, and functions Janke, Carsten Journal of Cell Biology, Vol. 206, Issue 4 https://doi.org/10.1083/jcb.201406055	journal	August 2014
A conceptual view at microtubule plus end dynamics in neuronal axons Voelzmann, Andre; Hahn, Ines; Pearce, Simon P. Brain Research Bulletin https://doi.org/10.1101/062711	journal	August 2016
TgATAT-Mediated α-Tubulin Acetylation Is Required for Division of the Protozoan Parasite Toxoplasma gondii Varberg, Joseph M.; Padgett, Leah R.; Arrizabalaga, Gustavo mSphere, Vol. 1, Issue 1 https://doi.org/10.1128/msphere.00088-15	journal	February 2016
The primary cilium is a self-adaptable, integrating nexus for mechanical stimuli and cellular signaling Nguyen, An M.; Young, Y. -N.; Jacobs, Christopher R. Biology Open, Vol. 4, Issue 12 https://doi.org/10.1242/bio.014787	journal	November 2015
The tubulin code at a glance Gadadhar, Sudarshan; Bodakuntla, Satish; Natarajan, Kathiresan Journal of Cell Science, Vol. 130, Issue 8 https://doi.org/10.1242/jcs.199471	journal	March 2017
A Case for Microtubule Vulnerability in Amyotrophic Lateral Sclerosis: Altered Dynamics During Disease Clark, Jayden A.; Yeaman, Elise J.; Blizzard, Catherine A. Frontiers in Cellular Neuroscience, Vol. 10 https://doi.org/10.3389/fncel.2016.00204	journal	September 2016
A Systematic Review of Suggested Molecular Strata, Biomarkers and Their Tissue Sources in ALS Vijayakumar, Udaya Geetha; Milla, Vanessa; Cynthia Stafford, Mei Yu Frontiers in Neurology, Vol. 10 https://doi.org/10.3389/fneur.2019.00400	journal	May 2019
The HDAC6 Inhibitor Trichostatin A Acetylates Microtubules and Protects Axons From Excitotoxin-Induced Degeneration in a Compartmented Culture Model Hanson, Kelsey; Tian, Nan; Vickers, James C. Frontiers in Neuroscience, Vol. 12 https://doi.org/10.3389/fnins.2018.00872	journal	November 2018
The Altered Hepatic Tubulin Code in Alcoholic Liver Disease Groebner, Jennifer; Tuma, Pamela Biomolecules, Vol. 5, Issue 3 https://doi.org/10.3390/biom5032140	journal	September 2015
Tubulin Acetylation Mediates Bisphenol A Effects on the Microtubule Arrays of Allium cepa and Triticum turgidum Adamakis, Ioannis-Dimosthenis S.; Panteris, Emmanuel; Eleftheriou, Eleftherios P. Biomolecules, Vol. 9, Issue 5 https://doi.org/10.3390/biom9050185	journal	May 2019
Differences in Functional Expression of Connexin43 and NaV1.5 by Pan- and Class-Selective Histone Deacetylase Inhibition in Heart Zhang, Xian; Patel, Dakshesh; Xu, Qin International Journal of Molecular Sciences, Vol. 19, Issue 8 https://doi.org/10.3390/ijms19082288	journal	August 2018
High-resolution Time-lapse Imaging and Automated Analysis of Microtubule Dynamics in Living Human Umbilical Vein Endothelial Cells Braun, Alexander; Caesar, Nicole M.; Dang, Kyvan Journal of Visualized Experiments, Issue 114 https://doi.org/10.3791/54265	journal	August 2016
Expression of acetylated tubulin in the postnatal developing mouse cochlea Liu, Wenjing; Wang, Chuanxi; Yu, Hao European Journal of Histochemistry https://doi.org/10.4081/ejh.2018.2942	journal	August 2018
Histamine and histidine decarboxylase in the olfactory system and brain of the common cuttlefish Sepia officinalis (Linnaeus, 1758) Scaros, Alexia T.; Andouche, Aude; Baratte, Sébastien Journal of Comparative Neurology, Vol. 528, Issue 7 https://doi.org/10.1002/cne.24809	journal	November 2019
ATAT1 regulates forebrain development and stress-induced tubulin hyperacetylation Li, Lin; Jayabal, Sriram; Ghorbani, Mohammad Cellular and Molecular Life Sciences, Vol. 76, Issue 18 https://doi.org/10.1007/s00018-019-03088-3	journal	April 2019
Role of LPS-elicited signaling in triggering gastric mucosal inflammatory responses to H. pylori: modulatory effect of ghrelin Slomiany, B. L.; Slomiany, A. Inflammopharmacology, Vol. 25, Issue 4 https://doi.org/10.1007/s10787-017-0360-1	journal	May 2017
G protein-coupled receptor kinase 5 modifies cancer cell resistance to paclitaxel Lagman, Joann; Sayegh, Paula; Lee, Christina S. Molecular and Cellular Biochemistry, Vol. 461, Issue 1-2 https://doi.org/10.1007/s11010-019-03594-9	journal	July 2019
The Inner Junction Complex of the Cilia is an Interaction Hub that Involves Tubulin Post-translational Modifications Khalifa, Ahmad; Ichikawa, Muneyoshi; Dai, Daniel Biophysical Journal, Vol. 118, Issue 3 https://doi.org/10.1016/j.bpj.2019.11.349	journal	February 2020
Tubulin acetylation protects long-lived microtubules against mechanical ageing Portran, Didier; Schaedel, Laura; Xu, Zhenjie Nature Cell Biology, Vol. 19, Issue 4 https://doi.org/10.1038/ncb3481	journal	February 2017
The methyltransferase Ezh2 controls cell adhesion and migration through direct methylation of the extranuclear regulatory protein talin Gunawan, Merry; Venkatesan, Nandini; Loh, Jia Tong Nature Immunology, Vol. 16, Issue 5 https://doi.org/10.1038/ni.3125	journal	March 2015
The therapeutic hope for HDAC6 inhibitors in malignancy and chronic disease Batchu, Sri N.; Brijmohan, Angela S.; Advani, Andrew Clinical Science, Vol. 130, Issue 12 https://doi.org/10.1042/cs20160084	journal	May 2016
The actin-MRTF-SRF transcriptional circuit controls tubulin acetylation via α-TAT1 gene expression Fernández-Barrera, Jaime; Bernabé-Rubio, Miguel; Casares-Arias, Javier The Journal of Cell Biology, Vol. 217, Issue 3 https://doi.org/10.1083/jcb.201702157	journal	January 2018
α-Tubulin K40 acetylation is required for contact inhibition of proliferation and cell–substrate adhesion Aguilar, Andrea; Becker, Lars; Tedeschi, Thomas Molecular Biology of the Cell, Vol. 25, Issue 12 https://doi.org/10.1091/mbc.e13-10-0609	journal	June 2014
Insights of the tubulin code in gametes and embryos: from basic research to potential clinical applications in humans† Amargant, Farners; Barragan, Montserrat; Vassena, Rita Biology of Reproduction, Vol. 100, Issue 3 https://doi.org/10.1093/biolre/ioy203	journal	September 2018
Effects of mutating α-tubulin lysine 40 on sensory dendrite development Jenkins, Brian V.; Saunders, Harriet A. J.; Record, Helena L. Journal of Cell Science https://doi.org/10.1101/212373	posted_content	November 2017
Regulation of Microtubule Disassembly by Spatially Heterogeneous Patterns of Acetylation Aparna, J. S.; Padinhateeri, Ranjith; Das, Dibyendu Soft Matter https://doi.org/10.1101/725895	posted_content	August 2019
Posttranslational Modifications of Tubulin and Cilia Wloga, Dorota; Joachimiak, Ewa; Louka, Panagiota Cold Spring Harbor Perspectives in Biology, Vol. 9, Issue 6 https://doi.org/10.1101/cshperspect.a028159	journal	December 2016
ATAT1-enriched vesicles promote microtubule acetylation via axonal transport Even, Aviel; Morelli, Giovanni; Broix, Loïc Science Advances, Vol. 5, Issue 12 https://doi.org/10.1126/sciadv.aax2705	journal	December 2019
Cardiac microtubules in health and heart disease Caporizzo, Matthew A.; Chen, Christina Yingxian; Prosser, Benjamin L. Experimental Biology and Medicine, Vol. 244, Issue 15 https://doi.org/10.1177/1535370219868960	journal	August 2019
The model of local axon homeostasis - explaining the role and regulation of microtubule bundles in axon maintenance and pathology Hahn, Ines; Voelzmann, André; Liew, Yu-Ting Neural Development, Vol. 14, Issue 1 https://doi.org/10.1186/s13064-019-0134-0	journal	November 2019
Effects of mutating α-tubulin lysine 40 on sensory dendrite development Jenkins, Brian V.; Saunders, Harriet A. J.; Record, Helena L. Journal of Cell Science https://doi.org/10.1242/jcs.210203	journal	January 2017
The Elongator subunit Elp3 is a non-canonical tRNA acetyltransferase Lin, Ting-Yu; Abbassi, Nour El Hana; Zakrzewski, Karol Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2019-01203	text	January 2019
Tubulin Post-Translational Modifications and Microtubule Dynamics Wloga, Dorota; Joachimiak, Ewa; Fabczak, Hanna International Journal of Molecular Sciences, Vol. 18, Issue 10 https://doi.org/10.3390/ijms18102207	journal	October 2017
The inner junction complex of the cilia is an interaction hub that involves tubulin post-translational modifications Khalifa, Ahmad Abdelzaher Zaki; Ichikawa, Muneyoshi; Dai, Daniel eLife, Vol. 9 https://doi.org/10.7554/elife.52760	journal	January 2020

Similar Records

Effects of α-tubulin acetylation on microtubule structure and stability

Journal Article · Thu May 09 00:00:00 EDT 2019 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1559217

Structural and functional features of lysine acetylation of plant and animal tubulins

Journal Article · Tue Nov 14 23:00:00 EST 2017 · Cell Biology International · OSTI ID:1409472

Prion protein inhibits microtubule assembly by inducing tubulin oligomerization

Journal Article · Fri Oct 13 00:00:00 EDT 2006 · Biochemical and Biophysical Research Communications · OSTI ID:20854517

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Cell Biology

Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure

Citation Formats

References (71)

Cited By (53)

Similar Records

Related Subjects