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Title: Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure

Abstract

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.

Authors:
 [1];  [2];  [3];  [3];  [4]
+ Show Author Affiliations
  1. Univ. of California, Berkeley, CA (United States). Biophysics Graduate Group
  2. Univ. of California, Berkeley, CA (United States).Howard Hughes Medical Inst. Dept. of Molecular and Cell Biology
  3. Stanford Univ., CA (United States). School of Medicine. Dept. of Molecular and Cellular Physiology
  4. 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
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
OSTI Identifier:
1625232
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Molecular Biology of the Cell
Additional Journal Information:
Journal Volume: 25; Journal Issue: 2; Journal ID: ISSN 1059-1524
Publisher:
American Society for Cell Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Cell Biology

Citation Formats

Howes, Stuart C., Alushin, Gregory M., Shida, Toshinobu, Nachury, Maxence V., and Nogales, Eva. Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure. United States: N. p., 2013. Web. doi:10.1091/mbc.e13-07-0387.
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Howes, Stuart C., Alushin, Gregory M., Shida, Toshinobu, Nachury, Maxence V., & Nogales, Eva. Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure. United States. https://doi.org/10.1091/mbc.e13-07-0387
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Howes, Stuart C., Alushin, Gregory M., Shida, Toshinobu, Nachury, Maxence V., and Nogales, Eva. Wed . "Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure". United States. https://doi.org/10.1091/mbc.e13-07-0387. https://www.osti.gov/servlets/purl/1625232.
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@article{osti_1625232,
title = {Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure},
author = {Howes, Stuart C. and Alushin, Gregory M. and Shida, Toshinobu and Nachury, Maxence V. and Nogales, Eva},
abstractNote = {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.},
doi = {10.1091/mbc.e13-07-0387},
journal = {Molecular Biology of the Cell},
number = 2,
volume = 25,
place = {United States},
year = {Wed Nov 13 00:00:00 EST 2013},
month = {Wed Nov 13 00:00:00 EST 2013}
}
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https://doi.org/10.1091/mbc.e13-07-0387
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  • Peris, Leticia; Wagenbach, Michael; Lafanechère, Laurence
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ER sliding dynamics and ER–mitochondrial contacts occur on acetylated microtubules
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The posttranslational modification of tubulin undergoes a switch from detyrosination to acetylation as epithelial cells become polarized
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Lysine Acetylation Targets Protein Complexes and Co-Regulates Major Cellular Functions
journal, July 2009

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journal, January 1990

Tubulin in sea urchin embryonic cilia: post-translational modifications during regeneration
journal, April 1992

Single Molecule Imaging Reveals Differences in Microtubule Track Selection Between Kinesin Motors
journal, October 2009

Acetylation of Microtubules Influences Their Sensitivity to Severing by Katanin in Neurons and Fibroblasts
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Luminal particles within cellular microtubules.
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    • Scaros, Alexia T.; Andouche, Aude; Baratte, Sébastien
    • Journal of Comparative Neurology, Vol. 528, Issue 7
    • DOI: 10.1002/cne.24809

    The tubulin code at a glance
    journal, March 2017

    • Gadadhar, Sudarshan; Bodakuntla, Satish; Natarajan, Kathiresan
    • Journal of Cell Science, Vol. 130, Issue 8
    • DOI: 10.1242/jcs.199471

    The tubulin code: Molecular components, readout mechanisms, and functions
    journal, August 2014

    MicroRNA-92a is a circadian modulator of neuronal excitability in Drosophila
    journal, March 2017

    The therapeutic hope for HDAC6 inhibitors in malignancy and chronic disease
    journal, May 2016

    • Batchu, Sri N.; Brijmohan, Angela S.; Advani, Andrew
    • Clinical Science, Vol. 130, Issue 12
    • DOI: 10.1042/cs20160084

    The model of local axon homeostasis - explaining the role and regulation of microtubule bundles in axon maintenance and pathology
    journal, November 2019

    Tubulin Acetylation Mediates Bisphenol A Effects on the Microtubule Arrays of Allium cepa and Triticum turgidum
    journal, May 2019

    • Adamakis, Ioannis-Dimosthenis S.; Panteris, Emmanuel; Eleftheriou, Eleftherios P.
    • Biomolecules, Vol. 9, Issue 5
    • DOI: 10.3390/biom9050185

    Effects of α-tubulin acetylation on microtubule structure and stability
    journal, May 2019

    • Eshun-Wilson, Lisa; Zhang, Rui; Portran, Didier
    • Proceedings of the National Academy of Sciences, Vol. 116, Issue 21
    • DOI: 10.1073/pnas.1900441116

    Tubulin acetylation protects long-lived microtubules against mechanical ageing
    journal, February 2017

    • Portran, Didier; Schaedel, Laura; Xu, Zhenjie
    • Nature Cell Biology, Vol. 19, Issue 4
    • DOI: 10.1038/ncb3481

    A Case for Microtubule Vulnerability in Amyotrophic Lateral Sclerosis: Altered Dynamics During Disease
    journal, September 2016

    • Clark, Jayden A.; Yeaman, Elise J.; Blizzard, Catherine A.
    • Frontiers in Cellular Neuroscience, Vol. 10
    • DOI: 10.3389/fncel.2016.00204

    The Elongator subunit Elp3 is a non-canonical tRNA acetyltransferase
    text, January 2019

    • Lin, Ting-Yu; Abbassi, Nour El Hana; Zakrzewski, Karol
    • Deutsches Elektronen-Synchrotron, DESY, Hamburg
    • DOI: 10.3204/pubdb-2019-01203

    The Elongator subunit Elp3 is a non-canonical tRNA acetyltransferase
    journal, February 2019

    G protein-coupled receptor kinase 5 modifies cancer cell resistance to paclitaxel
    journal, July 2019

    • Lagman, Joann; Sayegh, Paula; Lee, Christina S.
    • Molecular and Cellular Biochemistry, Vol. 461, Issue 1-2
    • DOI: 10.1007/s11010-019-03594-9

    Cardiac microtubules in health and heart disease
    journal, August 2019

    • Caporizzo, Matthew A.; Chen, Christina Yingxian; Prosser, Benjamin L.
    • Experimental Biology and Medicine, Vol. 244, Issue 15
    • DOI: 10.1177/1535370219868960

    Insights of the tubulin code in gametes and embryos: from basic research to potential clinical applications in humans†
    journal, September 2018

    • Amargant, Farners; Barragan, Montserrat; Vassena, Rita
    • Biology of Reproduction, Vol. 100, Issue 3
    • DOI: 10.1093/biolre/ioy203

    Back to the tubule: microtubule dynamics in Parkinson’s disease
    journal, September 2016

    • Pellegrini, Laura; Wetzel, Andrea; Grannó, Simone
    • Cellular and Molecular Life Sciences, Vol. 74, Issue 3
    • DOI: 10.1007/s00018-016-2351-6

    The world of protein acetylation
    journal, October 2016

    • Drazic, Adrian; Myklebust, Line M.; Ree, Rasmus
    • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1864, Issue 10
    • DOI: 10.1016/j.bbapap.2016.06.007

    Effects of α-Tubulin K40 Acetylation and Detyrosination on Kinesin-1 Motility in a Purified System
    journal, June 2014

    • Kaul, Neha; Soppina, Virupakshi; Verhey, Kristen J.
    • Biophysical Journal, Vol. 106, Issue 12
    • DOI: 10.1016/j.bpj.2014.05.008

    The Motility of Axonemal Dynein Is Regulated by the Tubulin Code
    journal, December 2014

    • Alper, Joshua D.; Decker, Franziska; Agana, Bernice
    • Biophysical Journal, Vol. 107, Issue 12
    • DOI: 10.1016/j.bpj.2014.10.061

    Causes and Consequences of Microtubule Acetylation
    journal, December 2017

    Exome-wide Rare Variant Analysis Identifies TUBA4A Mutations Associated with Familial ALS
    journal, October 2014

    Long intergenic non-coding RNA APOC1P1-3 inhibits apoptosis by decreasing α-tubulin acetylation in breast cancer
    journal, May 2016

    Oncogenic microtubule hyperacetylation through BEX4-mediated sirtuin 2 inhibition
    journal, August 2016

    αTAT1 downregulation induces mitotic catastrophe in HeLa and A549 cells
    journal, February 2016

    MicroRNA-92a is a circadian modulator of neuronal excitability in Drosophila
    journal, March 2017

    Nucleotide– and Mal3-dependent changes in fission yeast microtubules suggest a structural plasticity view of dynamics
    journal, December 2017

    • von Loeffelholz, Ottilie; Venables, Neil A.; Drummond, Douglas Robert
    • Nature Communications, Vol. 8, Issue 1
    • DOI: 10.1038/s41467-017-02241-5

    The Elongator subunit Elp3 is a non-canonical tRNA acetyltransferase
    journal, February 2019

    Human histone deacetylase 6 shows strong preference for tubulin dimers over assembled microtubules
    journal, September 2017

    αTAT1 controls longitudinal spreading of acetylation marks from open microtubules extremities
    journal, October 2016

    • Ly, Nathalie; Elkhatib, Nadia; Bresteau, Enzo
    • Scientific Reports, Vol. 6, Issue 1
    • DOI: 10.1038/srep35624

    Regulation of microtubule disassembly by spatially heterogeneous patterns of acetylation
    journal, January 2020

    • J. S., Aparna; Padinhateeri, Ranjith; Das, Dibyendu
    • Soft Matter, Vol. 16, Issue 12
    • DOI: 10.1039/c9sm02198a

    Cilium structure, assembly, and disassembly regulated by the cytoskeleton
    journal, July 2018

    • Mirvis, Mary; Stearns, Tim; James Nelson, W.
    • Biochemical Journal, Vol. 475, Issue 14
    • DOI: 10.1042/bcj20170453

    Histone deacetylase 3 indirectly modulates tubulin acetylation
    journal, November 2015

    • Bacon, Travis; Seiler, Caroline; Wolny, Marcin
    • Biochemical Journal, Vol. 472, Issue 3
    • DOI: 10.1042/bj20150660

    Effects of α-tubulin acetylation on microtubule structure and stability
    journal, May 2019

    • Eshun-Wilson, Lisa; Zhang, Rui; Portran, Didier
    • Proceedings of the National Academy of Sciences, Vol. 116, Issue 21
    • DOI: 10.1073/pnas.1900441116

    Structural and functional differences between porcine brain and budding yeast microtubules
    journal, January 2018

    The tubulin code: Molecular components, readout mechanisms, and functions
    journal, August 2014

    A conceptual view at microtubule plus end dynamics in neuronal axons
    journal, August 2016

    • Voelzmann, Andre; Hahn, Ines; Pearce, Simon P.
    • Brain Research Bulletin
    • DOI: 10.1101/062711

    TgATAT-Mediated α-Tubulin Acetylation Is Required for Division of the Protozoan Parasite Toxoplasma gondii
    journal, February 2016

    The primary cilium is a self-adaptable, integrating nexus for mechanical stimuli and cellular signaling
    journal, November 2015

    • Nguyen, An M.; Young, Y. -N.; Jacobs, Christopher R.
    • Biology Open, Vol. 4, Issue 12
    • DOI: 10.1242/bio.014787

    The tubulin code at a glance
    journal, March 2017

    • Gadadhar, Sudarshan; Bodakuntla, Satish; Natarajan, Kathiresan
    • Journal of Cell Science, Vol. 130, Issue 8
    • DOI: 10.1242/jcs.199471

    A Case for Microtubule Vulnerability in Amyotrophic Lateral Sclerosis: Altered Dynamics During Disease
    journal, September 2016

    • Clark, Jayden A.; Yeaman, Elise J.; Blizzard, Catherine A.
    • Frontiers in Cellular Neuroscience, Vol. 10
    • DOI: 10.3389/fncel.2016.00204

    A Systematic Review of Suggested Molecular Strata, Biomarkers and Their Tissue Sources in ALS
    journal, May 2019

    • Vijayakumar, Udaya Geetha; Milla, Vanessa; Cynthia Stafford, Mei Yu
    • Frontiers in Neurology, Vol. 10
    • DOI: 10.3389/fneur.2019.00400

    The Altered Hepatic Tubulin Code in Alcoholic Liver Disease
    journal, September 2015

    Tubulin Acetylation Mediates Bisphenol A Effects on the Microtubule Arrays of Allium cepa and Triticum turgidum
    journal, May 2019

    • Adamakis, Ioannis-Dimosthenis S.; Panteris, Emmanuel; Eleftheriou, Eleftherios P.
    • Biomolecules, Vol. 9, Issue 5
    • DOI: 10.3390/biom9050185

    Differences in Functional Expression of Connexin43 and NaV1.5 by Pan- and Class-Selective Histone Deacetylase Inhibition in Heart
    journal, August 2018

    • Zhang, Xian; Patel, Dakshesh; Xu, Qin
    • International Journal of Molecular Sciences, Vol. 19, Issue 8
    • DOI: 10.3390/ijms19082288

    High-resolution Time-lapse Imaging and Automated Analysis of Microtubule Dynamics in Living Human Umbilical Vein Endothelial Cells
    journal, August 2016

    • Braun, Alexander; Caesar, Nicole M.; Dang, Kyvan
    • Journal of Visualized Experiments, Issue 114
    • DOI: 10.3791/54265

    Expression of acetylated tubulin in the postnatal developing mouse cochlea
    journal, August 2018

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