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Title: Structural differences between yeast and mammalian microtubules revealed by cryo-EM

Abstract

Microtubules are polymers of αβ-tubulin heterodimers essential for all eukaryotes. Despite sequence conservation, there are significant structural differences between microtubules assembled in vitro from mammalian or budding yeast tubulin. Yeast MTs were not observed to undergo compaction at the interdimer interface as seen for mammalian microtubules upon GTP hydrolysis. Lack of compaction might reflect slower GTP hydrolysis or a different degree of allosteric coupling in the lattice. The microtubule plus end–tracking protein Bim1 binds yeast microtubules both between αβ-tubulin heterodimers, as seen for other organisms, and within tubulin dimers, but binds mammalian tubulin only at interdimer contacts. At the concentrations used in cryo-electron microscopy, Bim1 causes the compaction of yeast microtubules and induces their rapid disassembly. In conclusion, our studies demonstrate structural differences between yeast and mammalian microtubules that likely underlie their differing polymerization dynamics. These differences may reflect adaptations to the demands of different cell size or range of physiological growth temperatures.

Authors:
ORCiD logo [1];  [2];  [3];  [4];  [4]; ORCiD logo [5];  [2]; ORCiD logo [6]
  1. Univ. of California, Berkeley, CA (United States). Biophysics Graduate Group
  2. Univ. of Texas Southwestern Medical Center, Dallas, TX (United States). Dept. of Biophysics; Univ. of Texas Southwestern Medical Center, Dallas, TX (United States). Dept. of Biochemistry
  3. Univ. of California, Berkeley, CA (United States). Molecular and Cell Biology Graduate Program
  4. Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst.; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division
  5. Univ. of Duisburg-Essen, Essen (Germany). Dept. of Molecular Genetics, Center for Medical Biotechnology
  6. Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst.; Univ. of California, Berkeley, CA (United States). Dept. of Molecular Biology and California Inst. for Quantitative Biosciences; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
National Institutes of Health (NIH); USDOE; National Science Foundation (NSF)
OSTI Identifier:
1393251
DOE Contract Number:  
AC02-05CH11231; 1106400; MCB 1054947; 1615938; P01-GM051487; T32 GM008297; 2014177758
Resource Type:
Journal Article
Journal Name:
Journal of Cell Biology
Additional Journal Information:
Journal Volume: 216; Journal Issue: 9; Journal ID: ISSN 0021-9525
Publisher:
Rockefeller University Press
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Howes, Stuart C., Geyer, Elisabeth A., LaFrance, Benjamin, Zhang, Rui, Kellogg, Elizabeth H., Westermann, Stefan, Rice, Luke M., and Nogales, Eva. Structural differences between yeast and mammalian microtubules revealed by cryo-EM. United States: N. p., 2017. Web. doi:10.1083/jcb.201612195.
Howes, Stuart C., Geyer, Elisabeth A., LaFrance, Benjamin, Zhang, Rui, Kellogg, Elizabeth H., Westermann, Stefan, Rice, Luke M., & Nogales, Eva. Structural differences between yeast and mammalian microtubules revealed by cryo-EM. United States. doi:10.1083/jcb.201612195.
Howes, Stuart C., Geyer, Elisabeth A., LaFrance, Benjamin, Zhang, Rui, Kellogg, Elizabeth H., Westermann, Stefan, Rice, Luke M., and Nogales, Eva. Mon . "Structural differences between yeast and mammalian microtubules revealed by cryo-EM". United States. doi:10.1083/jcb.201612195.
@article{osti_1393251,
title = {Structural differences between yeast and mammalian microtubules revealed by cryo-EM},
author = {Howes, Stuart C. and Geyer, Elisabeth A. and LaFrance, Benjamin and Zhang, Rui and Kellogg, Elizabeth H. and Westermann, Stefan and Rice, Luke M. and Nogales, Eva},
abstractNote = {Microtubules are polymers of αβ-tubulin heterodimers essential for all eukaryotes. Despite sequence conservation, there are significant structural differences between microtubules assembled in vitro from mammalian or budding yeast tubulin. Yeast MTs were not observed to undergo compaction at the interdimer interface as seen for mammalian microtubules upon GTP hydrolysis. Lack of compaction might reflect slower GTP hydrolysis or a different degree of allosteric coupling in the lattice. The microtubule plus end–tracking protein Bim1 binds yeast microtubules both between αβ-tubulin heterodimers, as seen for other organisms, and within tubulin dimers, but binds mammalian tubulin only at interdimer contacts. At the concentrations used in cryo-electron microscopy, Bim1 causes the compaction of yeast microtubules and induces their rapid disassembly. In conclusion, our studies demonstrate structural differences between yeast and mammalian microtubules that likely underlie their differing polymerization dynamics. These differences may reflect adaptations to the demands of different cell size or range of physiological growth temperatures.},
doi = {10.1083/jcb.201612195},
journal = {Journal of Cell Biology},
issn = {0021-9525},
number = 9,
volume = 216,
place = {United States},
year = {2017},
month = {6}
}

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