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

Howes, Stuart C.; Geyer, Elisabeth A.; LaFrance, Benjamin; Zhang, Rui; Kellogg, Elizabeth H.; Westermann, Stefan; Rice, Luke M.; Nogales, Eva

doi:10.1083/jcb.201612195

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

Journal Article · Mon Jun 26 00:00:00 EDT 2017 · Journal of Cell Biology

DOI:https://doi.org/10.1083/jcb.201612195· OSTI ID:1393251

^[1]; Geyer, Elisabeth A. ^[2]; LaFrance, Benjamin ^[3]; Zhang, Rui ^[4]; Kellogg, Elizabeth H. ^[4]; ^[5]; Rice, Luke M. ^[2]; ^[6]

Univ. of California, Berkeley, CA (United States). Biophysics Graduate Group; DOE/OSTI
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
Univ. of California, Berkeley, CA (United States). Molecular and Cell Biology Graduate Program
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
Univ. of Duisburg-Essen, Essen (Germany). Dept. of Molecular Genetics, Center for Medical Biotechnology
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

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.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); National Science Foundation (NSF); USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1393251

Journal Information:: Journal of Cell Biology, Journal Name: Journal of Cell Biology Journal Issue: 9 Vol. 216; ISSN 0021-9525

Publisher:: Rockefeller University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (67)

Loss-of-Function Plays a Major Role in Early Neurogenesis of Tubulin α-1 A (TUBA1A) Mutation-Related Brain Malformations Xie, Liangqun; Huang, Jingrui; Dai, Lei Molecular Neurobiology, Vol. 58, Issue 4 https://doi.org/10.1007/s12035-020-02193-w	journal	November 2020
Asymmetric Friction of Non-Motor Maps can lead to their Directional Motion in Active Microtubule Networks Forth, Scott; Hsia, Kuo-Chiang; Shimamoto, Yuta Biophysical Journal, Vol. 108, Issue 2 https://doi.org/10.1016/j.bpj.2014.11.2456	journal	January 2015
EBs Recognize a Nucleotide-Dependent Structural Cap at Growing Microtubule Ends Maurer, Sebastian P.; Fourniol, Franck J.; Bohner, Gergő Cell, Vol. 149, Issue 2 https://doi.org/10.1016/j.cell.2012.02.049	journal	April 2012
High-Resolution Microtubule Structures Reveal the Structural Transitions in αβ-Tubulin upon GTP Hydrolysis Alushin, Gregory M.; Lander, Gabriel C.; Kellogg, Elizabeth H. Cell, Vol. 157, Issue 5 https://doi.org/10.1016/j.cell.2014.03.053	journal	May 2014
Graded Control of Microtubule Severing by Tubulin Glutamylation Valenstein, Max L.; Roll-Mecak, Antonina Cell, Vol. 164, Issue 5 https://doi.org/10.1016/j.cell.2016.01.019	journal	February 2016
A Force-Induced Directional Switch of a Molecular Motor Enables Parallel Microtubule Bundle Formation Molodtsov, Maxim I.; Mieck, Christine; Dobbelaere, Jeroen Cell, Vol. 167, Issue 2 https://doi.org/10.1016/j.cell.2016.09.029	journal	October 2016
EB1 Accelerates Two Conformational Transitions Important for Microtubule Maturation and Dynamics Maurer, Sebastian P.; Cade, Nicholas I.; Bohner, Gergő Current Biology, Vol. 24, Issue 4 https://doi.org/10.1016/j.cub.2013.12.042	journal	February 2014
Mutations in Human Tubulin Proximal to the Kinesin-Binding Site Alter Dynamic Instability at Microtubule Plus- and Minus-Ends Ti, Shih-Chieh; Pamula, Melissa C.; Howes, Stuart C. Developmental Cell, Vol. 37, Issue 1 https://doi.org/10.1016/j.devcel.2016.03.003	journal	April 2016
Overexpression, purification, and functional analysis of recombinant human tubulin dimer Minoura, Itsushi; Hachikubo, You; Yamakita, Yoshihiko FEBS Letters, Vol. 587, Issue 21 https://doi.org/10.1016/j.febslet.2013.08.032	journal	September 2013
Insights into the Distinct Mechanisms of Action of Taxane and Non-Taxane Microtubule Stabilizers from Cryo-EM Structures Kellogg, Elizabeth H.; Hejab, Nisreen M. A.; Howes, Stuart Journal of Molecular Biology, Vol. 429, Issue 5 https://doi.org/10.1016/j.jmb.2017.01.001	journal	March 2017
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
Likelihood-based classification of cryo-EM images using FREALIGN Lyumkis, Dmitry; Brilot, Axel F.; Theobald, Douglas L. Journal of Structural Biology, Vol. 183, Issue 3 https://doi.org/10.1016/j.jsb.2013.07.005	journal	September 2013
CTFFIND4: Fast and accurate defocus estimation from electron micrographs Rohou, Alexis; Grigorieff, Nikolaus Journal of Structural Biology, Vol. 192, Issue 2 https://doi.org/10.1016/j.jsb.2015.08.008	journal	November 2015
Purification and Characterization of Assembly-Competent Tubulin from Aspergillus nidulans Yoon, Yisang; Oakley, Berl R. Biochemistry, Vol. 34, Issue 19 https://doi.org/10.1021/bi00019a016	journal	May 1995
Design, Overexpression, and Purification of Polymerization-Blocked Yeast αβ-Tubulin Mutants Johnson, Vinu; Ayaz, Pelin; Huddleston, Patrick Biochemistry, Vol. 50, Issue 40 https://doi.org/10.1021/bi2005174	journal	October 2011
Detection of GTP and P _i in Wild-Type and Mutated Yeast Microtubules: Implications for the Role of the GTP/GDP−P _i Cap in Microtubule Dynamics ^† Dougherty, Cynthia A.; Himes, Richard H.; Wilson, Leslie Biochemistry, Vol. 37, Issue 31 https://doi.org/10.1021/bi980677n	journal	August 1998
Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM Li, Xueming; Mooney, Paul; Zheng, Shawn Nature Methods, Vol. 10, Issue 6 https://doi.org/10.1038/nmeth.2472	journal	May 2013
Atomic-accuracy models from 4.5-Å cryo-electron microscopy data with density-guided iterative local refinement DiMaio, Frank; Song, Yifan; Li, Xueming Nature Methods, Vol. 12, Issue 4 https://doi.org/10.1038/nmeth.3286	journal	February 2015
Tracking the ends: a dynamic protein network controls the fate of microtubule tips Akhmanova, Anna; Steinmetz, Michel O. Nature Reviews Molecular Cell Biology, Vol. 9, Issue 4 https://doi.org/10.1038/nrm2369	journal	April 2008
Mal3, the Schizosaccharomyces pombe homolog of EB1, changes the microtubule lattice des Georges, Amédée; Katsuki, Miho; Drummond, Douglas R. Nature Structural & Molecular Biology, Vol. 15, Issue 10 https://doi.org/10.1038/nsmb.1482	journal	September 2008
De novo mutations of TUBB2A cause infantile-onset epilepsy and developmental delay Cai, Shuying; Li, Jinliang; Wu, Ye Journal of Human Genetics, Vol. 65, Issue 7 https://doi.org/10.1038/s10038-020-0739-5	journal	March 2020
GTP S microtubules mimic the growing microtubule end structure recognized by end-binding proteins (EBs) Maurer, S. P.; Bieling, P.; Cope, J. Proceedings of the National Academy of Sciences, Vol. 108, Issue 10 https://doi.org/10.1073/pnas.1014758108	journal	February 2011
Understanding tubulin-Taxol interactions: Mutations that impart Taxol binding to yeast tubulin Gupta, M. L.; Bode, C. J.; Georg, G. I. Proceedings of the National Academy of Sciences, Vol. 100, Issue 11 https://doi.org/10.1073/pnas.1131967100	journal	May 2003
Structural changes accompanying GTP hydrolysis in microtubules: information from a slowly hydrolyzable analogue guanylyl-(alpha,beta)- methylene-diphosphonate Hyman, A. A. The Journal of Cell Biology, Vol. 128, Issue 1 https://doi.org/10.1083/jcb.128.1.117	journal	January 1995
Phosphoregulation of the budding yeast EB1 homologue Bim1p by Aurora/Ipl1p Zimniak, Tomasz; Stengl, Katharina; Mechtler, Karl The Journal of Cell Biology, Vol. 186, Issue 3 https://doi.org/10.1083/jcb.200901036	journal	August 2009
Thirty years of search and capture: The complex simplicity of mitotic spindle assembly Heald, Rebecca; Khodjakov, Alexey Journal of Cell Biology, Vol. 211, Issue 6 https://doi.org/10.1083/jcb.201510015	journal	December 2015
Structure–Function Relationships in Yeast Tubulins Richards, Kristy L.; Anders, Kirk R.; Nogales, Eva Molecular Biology of the Cell, Vol. 11, Issue 5 https://doi.org/10.1091/mbc.11.5.1887	journal	May 2000
Systematic mutational analysis of the yeast beta-tubulin gene. Reijo, R. A.; Cooper, E. M.; Beagle, G. J. Molecular Biology of the Cell, Vol. 5, Issue 1 https://doi.org/10.1091/mbc.5.1.29	journal	January 1994
Microtubule stability in budding yeast: characterization and dosage suppression of a benomyl-dependent tubulin mutant. Machin, N. A.; Lee, J. M.; Barnes, G. Molecular Biology of the Cell, Vol. 6, Issue 9 https://doi.org/10.1091/mbc.6.9.1241	journal	September 1995
ISOLATION AND CHARACTERIZATION OF MUTATIONS IN THE β-TUBULIN GENE OF SACCHAROMYCES CEREVISIAE Thomas, James H.; Neff, Norma F.; Botstein, David Genetics, Vol. 111, Issue 4 https://doi.org/10.1093/genetics/111.4.715	journal	December 1985
Structural analysis of mutations in the Drosophila beta 2-tubulin isoform reveals regions in the beta-tubulin molecular required for general and for tissue-specific microtubule functions. Fackenthal, J. D.; Hutchens, J. A.; Turner, F. R. Genetics, Vol. 139, Issue 1 https://doi.org/10.1093/genetics/139.1.267	journal	January 1995
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/s0907444910007493	journal	March 2010
Detection of GTP-Tubulin Conformation in Vivo Reveals a Role for GTP Remnants in Microtubule Rescues Dimitrov, A.; Quesnoit, M.; Moutel, S. Science, Vol. 322, Issue 5906 https://doi.org/10.1126/science.1165401	journal	November 2008
A TOG: -tubulin Complex Structure Reveals Conformation-Based Mechanisms for a Microtubule Polymerase Ayaz, P.; Ye, X.; Huddleston, P. Science, Vol. 337, Issue 6096 https://doi.org/10.1126/science.1221698	journal	August 2012
Microtubule Polymerization Dynamics Desai, Arshad; Mitchison, Timothy J. Annual Review of Cell and Developmental Biology, Vol. 13, Issue 1 https://doi.org/10.1146/annurev.cellbio.13.1.83	journal	November 1997
Computed Origami Tomography Kittenberger, Axel; Mindrinos, Leonidas; Scherzer, Otmar arXiv https://doi.org/10.48550/arxiv.2006.03446	preprint	January 2020
Purification of Tubulin from the Fission Yeast Schizosaccharomyces pombe Drummond, Douglas R.; Kain, Susan; Newcombe, Anthony Methods in Molecular Biology https://doi.org/10.1007/978-1-61779-252-6_3	book	January 2011
Radioimmunoassay for tubulin: a quantitative comparison of the tubulin content of different established tissue culture cells and tissues Hiller, Gerhard; Weber, Klaus Cell, Vol. 14, Issue 4 https://doi.org/10.1016/0092-8674(78)90335-5	journal	August 1978
Asymmetric Friction of Nonmotor MAPs Can Lead to Their Directional Motion in Active Microtubule Networks Forth, Scott; Hsia, Kuo-Chiang; Shimamoto, Yuta Cell, Vol. 157, Issue 2 https://doi.org/10.1016/j.cell.2014.02.018	journal	April 2014
Mechanistic Origin of Microtubule Dynamic Instability and Its Modulation by EB Proteins Zhang, Rui; Alushin, Gregory M.; Brown, Alan Cell, Vol. 162, Issue 4 https://doi.org/10.1016/j.cell.2015.07.012	journal	August 2015
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
Bsoft: Image processing and molecular modeling for electron microscopy Heymann, J. Bernard; Belnap, David M. Journal of Structural Biology, Vol. 157, Issue 1 https://doi.org/10.1016/j.jsb.2006.06.006	journal	January 2007
A new protocol to accurately determine microtubule lattice seam location Zhang, Rui; Nogales, Eva Journal of Structural Biology, Vol. 192, Issue 2 https://doi.org/10.1016/j.jsb.2015.09.015	journal	November 2015
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
The Phenix software for automated determination of macromolecular structures Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Methods, Vol. 55, Issue 1 https://doi.org/10.1016/j.ymeth.2011.07.005	journal	September 2011
Purification and biochemical characterization of tubulin from the budding yeast Saccharomyces cerevisiae Davis, Ashley; Sage, Carleton R.; Wilson, Leslie Biochemistry, Vol. 32, Issue 34 https://doi.org/10.1021/bi00085a013	journal	August 1993
Dynamic instability of microtubule growth Mitchison, Tim; Kirschner, Marc Nature, Vol. 312, Issue 5991 https://doi.org/10.1038/312237a0	journal	November 1984
Structure of the αβ tubulin dimer by electron crystallography Nogales, Eva; Wolf, Sharon G.; Downing, Kenneth H. Nature, Vol. 391, Issue 6663 https://doi.org/10.1038/34465	journal	January 1998
The Ndc80 kinetochore complex forms oligomeric arrays along microtubules Alushin, Gregory M.; Ramey, Vincent H.; Pasqualato, Sebastiano Nature, Vol. 467, Issue 7317 https://doi.org/10.1038/nature09423	journal	October 2010
Microtubule assembly, organization and dynamics in axons and dendrites Conde, Cecilia; Cáceres, Alfredo Nature Reviews Neuroscience, Vol. 10, Issue 5 https://doi.org/10.1038/nrn2631	journal	May 2009
Ring closure activates yeast γTuRC for species-specific microtubule nucleation Kollman, Justin M.; Greenberg, Charles H.; Li, Sam Nature Structural & Molecular Biology, Vol. 22, Issue 2 https://doi.org/10.1038/nsmb.2953	journal	January 2015
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
Preclinical Development of a Fusion Peptide Conjugate as an HIV Vaccine Immunogen Ou, Li; Kong, Wing-Pui; Chuang, Gwo-Yu Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-59711-y	journal	February 2020
Stu2, the Budding Yeast XMAP215/Dis1 Homolog, Promotes Assembly of Yeast Microtubules by Increasing Growth Rate and Decreasing Catastrophe Frequency Podolski, Marija; Mahamdeh, Mohammed; Howard, Jonathon Journal of Biological Chemistry, Vol. 289, Issue 41 https://doi.org/10.1074/jbc.M114.584300	journal	August 2014
Role of GTP hydrolysis in microtubule dynamics: information from a slowly hydrolyzable analogue, GMPCPP. Hyman, A. A.; Salser, S.; Drechsel, D. N. Molecular Biology of the Cell, Vol. 3, Issue 10 https://doi.org/10.1091/mbc.3.10.1155	journal	October 1992
One-step purification of assembly-competent tubulin from diverse eukaryotic sources Widlund, Per O.; Podolski, Marija; Reber, Simone Molecular Biology of the Cell, Vol. 23, Issue 22 https://doi.org/10.1091/mbc.E12-06-0444	journal	November 2012
Structural comparison of the Caenorhabditis elegans and human Ndc80 complexes bound to microtubules reveals distinct binding behavior Wilson-Kubalek, Elizabeth M.; Cheeseman, Iain M.; Milligan, Ronald A. Molecular Biology of the Cell, Vol. 27, Issue 8 https://doi.org/10.1091/mbc.E15-12-0858	journal	April 2016
Isolation and characterization of conditional-lethal mutations in the TUB1 alpha-tubulin gene of the yeast Saccharomyces cerevisiae. Schatz, P. J.; Solomon, F.; Botstein, D. Genetics, Vol. 120, Issue 3 https://doi.org/10.1093/genetics/120.3.681	journal	November 1988
geopandas/geopandas: v0.8.1 Jordahl, Kelsey; Van den Bossche, Joris; Fleischmann, Martin https://doi.org/10.1101/020917	posted_content	July 2020
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Tools for macromolecular model building and refinement into electron cryo-microscopy reconstructions Brown, Alan; Long, Fei; Nicholls, Robert A. Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 1 https://doi.org/10.1107/S1399004714021683	journal	January 2015
Mechanical design principles of a mitotic spindle. Ward, Jonathan J.; Roque, Hélio; Antony, Claude Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.55647	text	January 2014
Mechanical design principles of a mitotic spindle Ward, Jonathan J.; Roque, Hélio; Antony, Claude eLife, Vol. 3 https://doi.org/10.7554/eLife.03398	journal	December 2014
A mutation uncouples the tubulin conformational and GTPase cycles, revealing allosteric control of microtubule dynamics Geyer, Elisabeth A.; Burns, Alexander; Lalonde, Beth A. eLife, Vol. 4 https://doi.org/10.7554/eLife.10113	journal	October 2015

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