An isolated CLASP TOG domain suppresses microtubule catastrophe and promotes rescue

Majumdar, Shreoshi; Kim, Tae; Chen, Zhe; Munyoki, Sarah; Tso, Shih-Chia; Brautigam, Chad A.; Rice, Luke M.; Surrey, Thomas

doi:10.1091/mbc.E17-12-0748

An isolated CLASP TOG domain suppresses microtubule catastrophe and promotes rescue

Journal Article · Fri Jun 01 04:00:00 EDT 2018 · Molecular Biology of the Cell

DOI:https://doi.org/10.1091/mbc.E17-12-0748· OSTI ID:1510247

Majumdar, Shreoshi ^[1]; Kim, Tae ^[1]; Chen, Zhe ^[2]; Munyoki, Sarah ^[1]; Tso, Shih-Chia ^[2]; Brautigam, Chad A. ^[3]; Rice, Luke M. ^[1]; Surrey, Thomas

Department of Biophysics, UT Southwestern Medical Center, Dallas, TX 75390; Department of Biochemistry, UT Southwestern Medical Center, Dallas, TX 75390
Department of Biophysics, UT Southwestern Medical Center, Dallas, TX 75390
Department of Biophysics, UT Southwestern Medical Center, Dallas, TX 75390; Department of Microbiology, UT Southwestern Medical Center, Dallas, TX 75390

Microtubules are heavily regulated dynamic polymers of αβ-tubulin that are required for proper chromosome segregation and organization of the cytoplasm. Polymerases in the XMAP215 family use arrayed TOG domains to promote faster microtubule elongation. Regulatory factors in the cytoplasmic linker associated protein (CLASP) family that reduce catastrophe and/or increase rescue also contain arrayed TOGs, but how CLASP TOGs contribute to activity is poorly understood. Here, using Saccharomyces cerevisiae Stu1 as a model CLASP, we report structural, biochemical, and reconstitution studies that clarify functional properties of CLASP TOGs. The two TOGs in Stu1 have very different tubulin-binding properties: TOG2 binds to both unpolymerized and polymerized tubulin, and TOG1 binds very weakly to either. The structure of Stu1-TOG2 reveals a CLASP-specific residue that likely confers distinctive tubulin-binding properties. The isolated TOG2 domain strongly suppresses microtubule catastrophe and increases microtubule rescue in vitro, contradicting the expectation that regulatory activity requires an array of TOGs. Single point mutations on the tubulin-binding surface of TOG2 ablate its anti-catastrophe and rescue activity in vitro, and Stu1 function in cells. Revealing that an isolated CLASP TOG can regulate polymerization dynamics without being part of an array provides insight into the mechanism of CLASPs and diversifies the understanding of TOG function.

Research Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Sponsoring Organization:: NIH

OSTI ID:: 1510247

Journal Information:: Molecular Biology of the Cell, Journal Name: Molecular Biology of the Cell Journal Issue: 11 Vol. 29; ISSN 1059-1524

Publisher:: American Society for Cell Biology

Country of Publication:: United States

Language:: ENGLISH

References (58)

Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae Longtine, Mark S.; Mckenzie III, Amos; Demarini, Douglas J. Yeast, Vol. 14, Issue 10 https://doi.org/10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U	journal	July 1998
Multiple domains of human CLASP contribute to microtubule dynamics and organization in vitro and in Xenopus egg extracts Patel, Kieren; Nogales, Eva; Heald, Rebecca Cytoskeleton, Vol. 69, Issue 3 https://doi.org/10.1002/cm.21005	journal	February 2012
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
T-coffee: a novel method for fast and accurate multiple sequence alignment 1 1Edited by J. Thornton Notredame, Cédric; Higgins, Desmond G.; Heringa, Jaap Journal of Molecular Biology, Vol. 302, Issue 1 https://doi.org/10.1006/jmbi.2000.4042	journal	September 2000
Size-Distribution Analysis of Macromolecules by Sedimentation Velocity Ultracentrifugation and Lamm Equation Modeling Schuck, Peter Biophysical Journal, Vol. 78, Issue 3 https://doi.org/10.1016/S0006-3495(00)76713-0	journal	March 2000
Restoring Low Resolution Structure of Biological Macromolecules from Solution Scattering Using Simulated Annealing Svergun, D. I. Biophysical Journal, Vol. 76, Issue 6, p. 2879-2886 https://doi.org/10.1016/S0006-3495(99)77443-6	journal	June 1999
Fluorescent labeling of recombinant proteins in living cells with FlAsH Albert, B. Albert; Adams, Stephen R.; Jones, Jay Methods in Enzymology, Vol. 327, p. 565-578 https://doi.org/10.1016/S0076-6879(00)27302-3	book	January 2000
CLASPs Are CLIP-115 and -170 Associating Proteins Involved in the Regional Regulation of Microtubule Dynamics in Motile Fibroblasts Akhmanova, Anna; Hoogenraad, Casper C.; Drabek, Ksenija Cell, Vol. 104, Issue 6 https://doi.org/10.1016/S0092-8674(01)00288-4	journal	March 2001
Human CLASP1 Is an Outer Kinetochore Component that Regulates Spindle Microtubule Dynamics Maiato, Helder; Fairley, Elizabeth A. L.; Rieder, Conly L. Cell, Vol. 113, Issue 7 https://doi.org/10.1016/S0092-8674(03)00465-3	journal	June 2003
Calculations and Publication-Quality Illustrations for Analytical Ultracentrifugation Data Brautigam, Chad A. Methods in Enzymology https://doi.org/10.1016/bs.mie.2015.05.001	book	January 2015
On the acquisition and analysis of microscale thermophoresis data Scheuermann, Thomas H.; Padrick, Shae B.; Gardner, Kevin H. Analytical Biochemistry, Vol. 496 https://doi.org/10.1016/j.ab.2015.12.013	journal	March 2016
Sedimentation Patterns of Rapidly Reversible Protein Interactions Schuck, Peter Biophysical Journal, Vol. 98, Issue 9 https://doi.org/10.1016/j.bpj.2009.12.4336	journal	May 2010
An EB1-Binding Motif Acts as a Microtubule Tip Localization Signal Honnappa, Srinivas; Gouveia, Susana Montenegro; Weisbrich, Anke Cell, Vol. 138, Issue 2 https://doi.org/10.1016/j.cell.2009.04.065	journal	July 2009
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
A TOG Protein Confers Tension Sensitivity to Kinetochore-Microtubule Attachments Miller, Matthew P.; Asbury, Charles L.; Biggins, Sue Cell, Vol. 165, Issue 6 https://doi.org/10.1016/j.cell.2016.04.030	journal	June 2016
Role of CLASP2 in Microtubule Stabilization and the Regulation of Persistent Motility Drabek, Ksenija; van Ham, Marco; Stepanova, Tatiana Current Biology, Vol. 16, Issue 22 https://doi.org/10.1016/j.cub.2006.09.065	journal	November 2006
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
Stabilization of Overlapping Microtubules by Fission Yeast CLASP Bratman, Scott V.; Chang, Fred Developmental Cell, Vol. 13, Issue 6 https://doi.org/10.1016/j.devcel.2007.10.015	journal	December 2007
CLASP Promotes Microtubule Rescue by Recruiting Tubulin Dimers to the Microtubule Al-Bassam, Jawdat; Kim, Hwajin; Brouhard, Gary Developmental Cell, Vol. 19, Issue 2 https://doi.org/10.1016/j.devcel.2010.07.016	journal	August 2010
CLASP2 Has Two Distinct TOG Domains That Contribute Differently to Microtubule Dynamics Maki, Takahisa; Grimaldi, Ashley D.; Fuchigami, Sotaro Journal of Molecular Biology, Vol. 427, Issue 14 https://doi.org/10.1016/j.jmb.2015.05.012	journal	July 2015
Structural Basis of Microtubule Plus End Tracking by XMAP215, CLIP-170, and EB1 Slep, Kevin C.; Vale, Ronald D. Molecular Cell, Vol. 27, Issue 6 https://doi.org/10.1016/j.molcel.2007.07.023	journal	September 2007
Crystal Structure of a TOG Domain: Conserved Features of XMAP215/Dis1-Family TOG Domains and Implications for Tubulin Binding Al-Bassam, Jawdat; Larsen, Nicholas A.; Hyman, Anthony A. Structure, Vol. 15, Issue 3 https://doi.org/10.1016/j.str.2007.01.012	journal	March 2007
A Cryptic TOG Domain with a Distinct Architecture Underlies CLASP-Dependent Bipolar Spindle Formation Leano, Jonathan B.; Rogers, Stephen L.; Slep, Kevin C. Structure, Vol. 21, Issue 6 https://doi.org/10.1016/j.str.2013.04.018	journal	June 2013
Regulation of microtubule dynamics by TOG-domain proteins XMAP215/Dis1 and CLASP Al-Bassam, Jawdat; Chang, Fred Trends in Cell Biology, Vol. 21, Issue 10 https://doi.org/10.1016/j.tcb.2011.06.007	journal	October 2011
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
Reconstitution of a microtubule plus-end tracking system in vitro Bieling, Peter; Laan, Liedewij; Schek, Henry Nature, Vol. 450, Issue 7172 https://doi.org/10.1038/nature06386	journal	December 2007
Drosophila CLASP is required for the incorporation of microtubule subunits into fluxing kinetochore fibres Maiato, Helder; Khodjakov, Alexey; Rieder, Conly L. Nature Cell Biology, Vol. 7, Issue 1 https://doi.org/10.1038/ncb1207	journal	December 2004
An auxin-based degron system for the rapid depletion of proteins in nonplant cells Nishimura, Kohei; Fukagawa, Tatsuo; Takisawa, Haruhiko Nature Methods, Vol. 6, Issue 12 https://doi.org/10.1038/nmeth.1401	journal	November 2009
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
Control of microtubule organization and dynamics: two ends in the limelight Akhmanova, Anna; Steinmetz, Michel O. Nature Reviews Molecular Cell Biology, Vol. 16, Issue 12 https://doi.org/10.1038/nrm4084	journal	November 2015
The role of TOG domains in microtubule plus end dynamics Slep, Kevin C. Biochemical Society Transactions, Vol. 37, Issue 5 https://doi.org/10.1042/BST0371002	journal	September 2009
XMAP215 polymerase activity is built by combining multiple tubulin-binding TOG domains and a basic lattice-binding region Widlund, P. O.; Stear, J. H.; Pozniakovsky, A. Proceedings of the National Academy of Sciences, Vol. 108, Issue 7 https://doi.org/10.1073/pnas.1016498108	journal	January 2011
Drosophila melanogaster Mini Spindles TOG3 Utilizes Unique Structural Elements to Promote Domain Stability and Maintain a TOG1- and TOG2-like Tubulin-binding Surface Howard, Amy E.; Fox, Jaime C.; Slep, Kevin C. Journal of Biological Chemistry, Vol. 290, Issue 16 https://doi.org/10.1074/jbc.M114.633826	journal	February 2015
Biophysical and Structural Characterization of the Centriolar Protein Cep104 Interaction Network Rezabkova, Lenka; Kraatz, Sebastian H. W.; Akhmanova, Anna Journal of Biological Chemistry, Vol. 291, Issue 35 https://doi.org/10.1074/jbc.M116.739771	journal	July 2016
STU1, a suppressor of a beta-tubulin mutation, encodes a novel and essential component of the yeast mitotic spindle Pasqualone, D. The Journal of Cell Biology, Vol. 127, Issue 6 https://doi.org/10.1083/jcb.127.6.1973	journal	December 1994
Mutations in orbit/mast reveal that the central spindle is comprised of two microtubule populations, those that initiate cleavage and those that propagate furrow ingression Inoue, Yoshihiro H.; Savoian, Matthew S.; Suzuki, Takao The Journal of Cell Biology, Vol. 166, Issue 1 https://doi.org/10.1083/jcb.200402052	journal	July 2004
CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex Mimori-Kiyosue, Yuko; Grigoriev, Ilya; Lansbergen, Gideon The Journal of Cell Biology, Vol. 168, Issue 1 https://doi.org/10.1083/jcb.200405094	journal	January 2005
A TOGL domain specifically targets yeast CLASP to kinetochores to stabilize kinetochore microtubules Funk, Caroline; Schmeiser, Verena; Ortiz, Jennifer The Journal of Cell Biology, Vol. 205, Issue 4 https://doi.org/10.1083/jcb.201310018	journal	May 2014
Five factors can reconstitute all three phases of microtubule polymerization dynamics Moriwaki, Takashi; Goshima, Gohta The Journal of Cell Biology, Vol. 215, Issue 3 https://doi.org/10.1083/jcb.201604118	journal	October 2016
TOG–tubulin binding specificity promotes microtubule dynamics and mitotic spindle formation Byrnes, Amy E.; Slep, Kevin C. The Journal of Cell Biology, Vol. 216, Issue 6 https://doi.org/10.1083/jcb.201610090	journal	May 2017
BIM1 Encodes a Microtubule-binding Protein in Yeast Schwartz, Katja; Richards, Kristy; Botstein, David Molecular Biology of the Cell, Vol. 8, Issue 12 https://doi.org/10.1091/mbc.8.12.2677	journal	December 1997
Mammalian CLASP1 and CLASP2 Cooperate to Ensure Mitotic Fidelity by Regulating Spindle and Kinetochore Function Pereira, Ana L.; Pereira, António J.; Maia, Ana R. R. Molecular Biology of the Cell, Vol. 17, Issue 10 https://doi.org/10.1091/mbc.e06-07-0579	journal	October 2006
The XMAP215 family drives microtubule polymerization using a structurally diverse TOG array Fox, Jaime C.; Howard, Amy E.; Currie, Joshua D. Molecular Biology of the Cell, Vol. 25, Issue 16 https://doi.org/10.1091/mbc.e13-08-0501	journal	August 2014
Crescerin uses a TOG domain array to regulate microtubules in the primary cilium Das, Alakananda; Dickinson, Daniel J.; Wood, Cameron C. Molecular Biology of the Cell, Vol. 26, Issue 23 https://doi.org/10.1091/mbc.e15-08-0603	journal	November 2015
GDP-to-GTP exchange on the microtubule end can contribute to the frequency of catastrophe Piedra, Felipe-Andrés; Kim, Tae; Garza, Emily S. Molecular Biology of the Cell, Vol. 27, Issue 22 https://doi.org/10.1091/mbc.e16-03-0199	journal	November 2016
Stu1 inversely regulates kinetochore capture and spindle stability Ortiz, J.; Funk, C.; Schafer, A. Genes & Development, Vol. 23, Issue 23 https://doi.org/10.1101/gad.541309	journal	December 2009
Uniqueness of ab initio shape determination in small-angle scattering Volkov, Vladimir V.; Svergun, Dmitri I. Journal of Applied Crystallography, Vol. 36, Issue 3, p. 860-864 https://doi.org/10.1107/S0021889803000268	journal	April 2003
DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering Franke, Daniel; Svergun, Dmitri I. Journal of Applied Crystallography, Vol. 42, Issue 2, p. 342-346 https://doi.org/10.1107/S0021889809000338	journal	January 2009
Determination of the regularization parameter in indirect-transform methods using perceptual criteria Svergun, D. I. Journal of Applied Crystallography, Vol. 25, Issue 4, p. 495-503 https://doi.org/10.1107/S0021889892001663	journal	August 1992
HKL -3000: the integration of data reduction and structure solution – from diffraction images to an initial model in minutes Minor, Wladek; Cymborowski, Marcin; Otwinowski, Zbyszek Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 8 https://doi.org/10.1107/S0907444906019949	journal	July 2006
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
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
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
EB1 Recognizes the Nucleotide State of Tubulin in the Microtubule Lattice Zanic, Marija; Stear, Jeffrey H.; Hyman, Anthony A. PLoS ONE, Vol. 4, Issue 10 https://doi.org/10.1371/journal.pone.0007585	journal	October 2009
A tethered delivery mechanism explains the catalytic action of a microtubule polymerase Ayaz, Pelin; Munyoki, Sarah; Geyer, Elisabeth A. eLife, Vol. 3 https://doi.org/10.7554/eLife.03069	journal	August 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
The size of the EB cap determines instantaneous microtubule stability Duellberg, Christian; Cade, Nicholas I.; Holmes, David eLife, Vol. 5 https://doi.org/10.7554/eLife.13470	journal	April 2016

Similar Records

Structures of TOG1 and TOG2 from the human microtubule dynamics regulator CLASP1

Journal Article · Thu Jul 18 20:00:00 EDT 2019 · PLoS ONE · OSTI ID:1834802

TOG–Tubulin Binding Specificity Promotes Microtubule Dynamics and Mitotic Spindle Formation

Journal Article · Tue May 16 00:00:00 EDT 2017 · Journal of Cell Biology · OSTI ID:1497194

Multiple domains of human CLASP contribute to microtubule dynamics and organization in vitro and in Xenopus egg extracts

Journal Article · Tue Jan 24 19:00:00 EST 2012 · Cytoskeleton · OSTI ID:1623516

An isolated CLASP TOG domain suppresses microtubule catastrophe and promotes rescue

Citation Formats

References (58)

Similar Records

Related Subjects