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Title: Separating the effects of nucleotide and EB binding on microtubule structure

Abstract

Microtubules (MTs) are polymers assembled from αβ-tubulin heterodimers that display the hallmark behavior of dynamic instability. MT dynamics are driven by GTP hydrolysis within the MT lattice, and are highly regulated by a number of MT-associated proteins (MAPs). How MAPs affect MTs is still not fully understood, partly due to a lack of high-resolution structural data on undecorated MTs, which need to serve as a baseline for further comparisons. Here we report three structures of MTs in different nucleotide states (GMPCPP, GDP, and GTPγS) at near-atomic resolution and in the absence of any binding proteins. These structures allowed us to differentiate the effects of nucleotide state versus MAP binding on MT structure. Kinesin binding has a small effect on the extended, GMPCPP-bound lattice, but hardly affects the compacted GDP-MT lattice, while binding of end-binding (EB) proteins can induce lattice compaction (together with lattice twist) in MTs that were initially in an extended and more stable state. We propose a MT lattice-centric model in which the MT lattice serves as a platform that integrates internal tubulin signals, such as nucleotide state, with outside signals, such as binding of MAPs or mechanical forces, resulting in global lattice rearrangements that in turn affectmore » the affinity of other MT partners and result in the exquisite regulation of MT dynamics.« less

Authors:
 [1];  [2]; ORCiD logo [3]
+ Show Author Affiliations
  1. Lawrence Berkeley National Laboratory, Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division; University of California, Berkeley, CA (United States). Department of Molecular and Cell Biology
  2. University of California, Berkeley, CA (United States). Molecular and Cell Biology Graduate Program
  3. Lawrence Berkeley National Laboratory, Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division; University of California, Berkeley, CA (United States). Department of Molecular and Cell Biology; University of California, Berkeley, CA (United States). Howard Hughes Medical Institute
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1625018
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 115; Journal Issue: 27; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
Science & Technology - Other Topics

Citation Formats

Zhang, Rui, LaFrance, Benjamin, and Nogales, Eva. Separating the effects of nucleotide and EB binding on microtubule structure. United States: N. p., 2018. Web. doi:10.1073/pnas.1802637115.
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Zhang, Rui, LaFrance, Benjamin, & Nogales, Eva. Separating the effects of nucleotide and EB binding on microtubule structure. United States. https://doi.org/10.1073/pnas.1802637115
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Zhang, Rui, LaFrance, Benjamin, and Nogales, Eva. Mon . "Separating the effects of nucleotide and EB binding on microtubule structure". United States. https://doi.org/10.1073/pnas.1802637115. https://www.osti.gov/servlets/purl/1625018.
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@article{osti_1625018,
title = {Separating the effects of nucleotide and EB binding on microtubule structure},
author = {Zhang, Rui and LaFrance, Benjamin and Nogales, Eva},
abstractNote = {Microtubules (MTs) are polymers assembled from αβ-tubulin heterodimers that display the hallmark behavior of dynamic instability. MT dynamics are driven by GTP hydrolysis within the MT lattice, and are highly regulated by a number of MT-associated proteins (MAPs). How MAPs affect MTs is still not fully understood, partly due to a lack of high-resolution structural data on undecorated MTs, which need to serve as a baseline for further comparisons. Here we report three structures of MTs in different nucleotide states (GMPCPP, GDP, and GTPγS) at near-atomic resolution and in the absence of any binding proteins. These structures allowed us to differentiate the effects of nucleotide state versus MAP binding on MT structure. Kinesin binding has a small effect on the extended, GMPCPP-bound lattice, but hardly affects the compacted GDP-MT lattice, while binding of end-binding (EB) proteins can induce lattice compaction (together with lattice twist) in MTs that were initially in an extended and more stable state. We propose a MT lattice-centric model in which the MT lattice serves as a platform that integrates internal tubulin signals, such as nucleotide state, with outside signals, such as binding of MAPs or mechanical forces, resulting in global lattice rearrangements that in turn affect the affinity of other MT partners and result in the exquisite regulation of MT dynamics.},
doi = {10.1073/pnas.1802637115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 27,
volume = 115,
place = {United States},
year = {Mon Jun 18 00:00:00 EDT 2018},
month = {Mon Jun 18 00:00:00 EDT 2018}
}
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    Structural state recognition facilitates tip tracking of EB1 at growing microtubule ends
    journal, September 2019

    Axonal transport: Driving synaptic function
    journal, October 2019

    Polyglutamylation of tubulin's C-terminal tail controls pausing and motility of kinesin-3 family member KIF1A
    journal, February 2019

    • Lessard, Dominique V.; Zinder, Oraya J.; Hotta, Takashi
    • Journal of Biological Chemistry, Vol. 294, Issue 16
    • DOI: 10.1074/jbc.ra118.005765

    Microtubules Gate Tau Condensation to Spatially Regulate Microtubule Functions
    journal, February 2020

    Mechanical properties of tubulin intra- and inter-dimer interfaces and their implications for microtubule dynamic instability
    journal, August 2019

    • Fedorov, Vladimir A.; Orekhov, Philipp S.; Kholina, Ekaterina G.
    • PLOS Computational Biology, Vol. 15, Issue 8
    • DOI: 10.1371/journal.pcbi.1007327

    The structure of a 15-stranded actin-like filament from Clostridium botulinum
    journal, June 2019

    Oligomer Formation of Tau Protein Hyperphosphorylated in Cells
    journal, December 2014

    • Tepper, Katharina; Biernat, Jacek; Kumar, Satish
    • Journal of Biological Chemistry, Vol. 289, Issue 49
    • DOI: 10.1074/jbc.M114.611368

    Automated cryo-EM Structure Refinement using Correlation-Driven Molecular Dynamics
    journal, February 2020

    A microtubule RELION-based pipeline for cryo-EM image processing
    journal, January 2020

    • Cook, Alexander D.; Manka, Szymon W.; Wang, Su
    • Journal of Structural Biology, Vol. 209, Issue 1
    • DOI: 10.1016/j.jsb.2019.10.004

    Tubulin lattice in cilia is in a stressed form regulated by microtubule inner proteins
    journal, September 2019

    • Ichikawa, Muneyoshi; Khalifa, Ahmad Abdelzaher Zaki; Kubo, Shintaroh
    • Proceedings of the National Academy of Sciences, Vol. 116, Issue 40
    • DOI: 10.1073/pnas.1911119116

    Structural determinants of microtubule minus end preference in CAMSAP CKK domains
    journal, November 2019

    Mitotic phosphorylation by NEK6 and NEK7 reduces the microtubule affinity of EML4 to promote chromosome congression
    journal, August 2019

    • Adib, Rozita; Montgomery, Jessica M.; Atherton, Joseph
    • Science Signaling, Vol. 12, Issue 594
    • DOI: 10.1126/scisignal.aaw2939

    Spatial positioning of EB family proteins at microtubule tips involves distinct nucleotide-dependent binding properties
    journal, September 2018

    • Roth, Daniel; Fitton, Benjamin P.; Chmel, Nikola P.
    • Journal of Cell Science, Vol. 132, Issue 4
    • DOI: 10.1242/jcs.219550

    TAPping into the treasures of tubulin using novel protein production methods
    journal, November 2018

    An estimate to the first approximation of microtubule rupture force
    journal, May 2019

    Microtubule minus-end stability is dictated by the tubulin off-rate
    journal, August 2019

    • Strothman, Claire; Farmer, Veronica; Arpağ, Göker
    • Journal of Cell Biology, Vol. 218, Issue 9
    • DOI: 10.1083/jcb.201905019

    Microtubules gate tau condensation to spatially regulate microtubule functions
    journal, September 2019

    A microtubule RELION-based pipeline for cryo-EM image processing
    journal, January 2020

    • Cook, Alexander D.; Manka, Szymon W.; Wang, Su
    • Journal of Structural Biology, Vol. 209, Issue 1
    • DOI: 10.1016/j.jsb.2019.10.004

    Selection and Characterization of Artificial Proteins Targeting the Tubulin α Subunit
    journal, March 2019

    The structure of a 15-stranded actin-like filament from Clostridium botulinum
    journal, June 2019

    Microtubule structure by cryo-EM: snapshots of dynamic instability
    journal, October 2018

    • Manka, Szymon W.; Moores, Carolyn A.
    • Essays in Biochemistry, Vol. 62, Issue 6
    • DOI: 10.1042/ebc20180031

    TAPping into the treasures of tubulin using novel protein production methods
    journal, November 2018

    GTP-tubulin loves microtubule plus ends but marries the minus ends
    journal, August 2019

    The speed of GTP hydrolysis determines GTP cap size and controls microtubule stability.
    text, January 2020

    Structural model for differential cap maturation at growing microtubule ends
    journal, March 2020

    • Estévez-Gallego, Juan; Josa-Prado, Fernando; Ku, Siou
    • eLife, Vol. 9
    • DOI: 10.7554/elife.50155
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