Effects of α-tubulin acetylation on microtubule structure and stability
Abstract
Acetylation of K40 in α-tubulin is the sole posttranslational modification to mark the luminal surface of microtubules. It is still controversial whether its relationship with microtubule stabilization is correlative or causative. We have obtained high-resolution cryo-electron microscopy (cryo-EM) reconstructions of pure samples of αTAT1-acetylated and SIRT2-deacetylated microtubules to visualize the structural consequences of this modification and reveal its potential for influencing the larger assembly properties of microtubules. We modeled the conformational ensembles of the unmodified and acetylated states by using the experimental cryo-EM density as a structural restraint in molecular dynamics simulations. We found that acetylation alters the conformational landscape of the flexible loop that contains αK40. Modification of αK40 reduces the disorder of the loop and restricts the states that it samples. We propose that the change in conformational sampling that we describe, at a location very close to the lateral contacts site, is likely to affect microtubule stability and function.
- Authors:
-
- Univ. of California, Berkeley, CA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Washington Univ., St. Louis, MO (United States)
- Univ. of California, San Francisco, CA (United States); Univ. Montpellier, Montpellier (France)
- Univ. of California, San Francisco, CA (United States)
- Univ. of Cambridge, Cambridge (United Kingdom)
- Univ. of Cambridge, Cambridge (United Kingdom); Inst. Pasteur, Paris (France)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, San Francisco, CA (United States)
- Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Science Foundation (NSF); National Institute of General Medical Sciences (NIGMS); National Academy of Sciences National Research Council Ford Foundation
- OSTI Identifier:
- 1559217
- Grant/Contract Number:
- AC02-05CH11231; 2016222703; R01-GM123159; R35-GM127018; P01-GM063210
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 116; Journal Issue: 21; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences, Washington, DC (United States)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; cryo-EM; MD; tubulin modifications; microtubule; acetylation
Citation Formats
Eshun-Wilson, Lisa, Zhang, Rui, Portran, Didier, Nachury, Maxence V., Toso, Daniel B., Löhr, Thomas, Vendruscolo, Michele, Bonomi, Massimiliano, Fraser, James S., and Nogales, Eva. Effects of α-tubulin acetylation on microtubule structure and stability. United States: N. p., 2019.
Web. doi:10.1073/pnas.1900441116.
Eshun-Wilson, Lisa, Zhang, Rui, Portran, Didier, Nachury, Maxence V., Toso, Daniel B., Löhr, Thomas, Vendruscolo, Michele, Bonomi, Massimiliano, Fraser, James S., & Nogales, Eva. Effects of α-tubulin acetylation on microtubule structure and stability. United States. https://doi.org/10.1073/pnas.1900441116
Eshun-Wilson, Lisa, Zhang, Rui, Portran, Didier, Nachury, Maxence V., Toso, Daniel B., Löhr, Thomas, Vendruscolo, Michele, Bonomi, Massimiliano, Fraser, James S., and Nogales, Eva. Thu .
"Effects of α-tubulin acetylation on microtubule structure and stability". United States. https://doi.org/10.1073/pnas.1900441116. https://www.osti.gov/servlets/purl/1559217.
@article{osti_1559217,
title = {Effects of α-tubulin acetylation on microtubule structure and stability},
author = {Eshun-Wilson, Lisa and Zhang, Rui and Portran, Didier and Nachury, Maxence V. and Toso, Daniel B. and Löhr, Thomas and Vendruscolo, Michele and Bonomi, Massimiliano and Fraser, James S. and Nogales, Eva},
abstractNote = {Acetylation of K40 in α-tubulin is the sole posttranslational modification to mark the luminal surface of microtubules. It is still controversial whether its relationship with microtubule stabilization is correlative or causative. We have obtained high-resolution cryo-electron microscopy (cryo-EM) reconstructions of pure samples of αTAT1-acetylated and SIRT2-deacetylated microtubules to visualize the structural consequences of this modification and reveal its potential for influencing the larger assembly properties of microtubules. We modeled the conformational ensembles of the unmodified and acetylated states by using the experimental cryo-EM density as a structural restraint in molecular dynamics simulations. We found that acetylation alters the conformational landscape of the flexible loop that contains αK40. Modification of αK40 reduces the disorder of the loop and restricts the states that it samples. We propose that the change in conformational sampling that we describe, at a location very close to the lateral contacts site, is likely to affect microtubule stability and function.},
doi = {10.1073/pnas.1900441116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 21,
volume = 116,
place = {United States},
year = {Thu May 09 00:00:00 EDT 2019},
month = {Thu May 09 00:00:00 EDT 2019}
}
Web of Science
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- Luo, Yanzhang; Xiang, ShengQi; Hooikaas, Peter Jan
- Nature Communications, Vol. 11, Issue 1
The speed of GTP hydrolysis determines GTP cap size and controls microtubule stability.
text, January 2020
- Roostalu, Johanna; Thomas, Claire; Cade, Nicholas Ian
- The Francis Crick Institute
Suppressing migration and invasion of H1299 lung cancer cells by honokiol through disrupting expression of an HDAC6‐mediated matrix metalloproteinase 9
journal, February 2020
- Pai, Jih‐Tung; Hsu, Chia‐Yun; Hsieh, Yei‐San
- Food Science & Nutrition, Vol. 8, Issue 3
What Will Computational Modeling Approaches Have to Say in the Era of Atomistic Cryo-EM Data?
journal, February 2020
- Fraser, James S.; Lindorff-Larsen, Kresten; Bonomi, Massimiliano
- Journal of Chemical Information and Modeling, Vol. 60, Issue 5
Direct observation of dynamic protein interactions involving human microtubules using solid-state NMR spectroscopy
journal, January 2020
- Luo, Yanzhang; Xiang, ShengQi; Hooikaas, Peter Jan
- Nature Communications, Vol. 11, Issue 1
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
Lysine Acetylation, Cancer Hallmarks and Emerging Onco-Therapeutic Opportunities
journal, January 2022
- Hu, Meilan; He, Fule; Thompson, Erik W.
- Cancers, Vol. 14, Issue 2
PAK1 Regulates MEC-17 Acetyltransferase Activity and Microtubule Acetylation during Proplatelet Extension
journal, October 2020
- van Dijk, Juliette; Bompard, Guillaume; Rabeharivelo, Gabriel
- International Journal of Molecular Sciences, Vol. 21, Issue 20
Molecular Evolution of Tubulins in Diatoms
journal, January 2022
- Khabudaev, Kirill V.; Petrova, Darya P.; Bedoshvili, Yekaterina D.
- International Journal of Molecular Sciences, Vol. 23, Issue 2
Microtubules in Influenza Virus Entry and Egress
journal, January 2020
- Simpson, Caitlin; Yamauchi, Yohei
- Viruses, Vol. 12, Issue 1