Structures of TOG1 and TOG2 from the human microtubule dynamics regulator CLASP1
Abstract
Tubulin-binding TOG domains are found arrayed in a number of proteins that regulate microtubule dynamics. While much is known about the structure and function of TOG domains from the XMAP215 microtubule polymerase family, less in known about the TOG domain array found in animal CLASP family members. The animal CLASP TOG array promotes microtubule pause, potentiates rescue, and limits catastrophe. How structurally distinct the TOG domains of animal CLASP are from one another, from XMAP215 family TOG domains, and whether a specific order of structurally distinct TOG domains in the TOG array is conserved across animal CLASP family members is poorly understood. We present the x-ray crystal structures of Homo sapiens (H.s.) CLASP1 TOG1 and TOG2. The structures of H.s. CLASP1 TOG1 and TOG2 are distinct from each other and from the previously determined structure of Mus musculus (M.m.) CLASP2 TOG3. Comparative analyses of CLASP family TOG domain structures determined to date across species and paralogs supports a conserved CLASP TOG array paradigm in which structurally distinct TOG domains are arrayed in a specific order. H.s. CLASP1 TOG1 bears structural similarity to the free-tubulin binding TOG domains of the XMAP215 family but lacks many of the key tubulin-binding determinants foundmore »
- Authors:
-
[2]
- Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Biochemistry & Biophysics. Program in Molecular and Cellular Biophysics
- Univ. of North Carolina, Chapel Hill, NC (United States). Program in Molecular and Cellular Biophysics. Dept. of Biology
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1834802
- Grant/Contract Number:
- AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 14; Journal Issue: 7; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Tubulins; Microtubules; Crystal structure; Microtubule dynamics; Sequence alignment; Built structures; Electron density; Polymerases
Citation Formats
Leano, Jonathan B., and Slep, Kevin C. Structures of TOG1 and TOG2 from the human microtubule dynamics regulator CLASP1. United States: N. p., 2019.
Web. doi:10.1371/journal.pone.0219823.
Leano, Jonathan B., & Slep, Kevin C. Structures of TOG1 and TOG2 from the human microtubule dynamics regulator CLASP1. United States. https://doi.org/10.1371/journal.pone.0219823
Leano, Jonathan B., and Slep, Kevin C. Fri .
"Structures of TOG1 and TOG2 from the human microtubule dynamics regulator CLASP1". United States. https://doi.org/10.1371/journal.pone.0219823. https://www.osti.gov/servlets/purl/1834802.
@article{osti_1834802,
title = {Structures of TOG1 and TOG2 from the human microtubule dynamics regulator CLASP1},
author = {Leano, Jonathan B. and Slep, Kevin C.},
abstractNote = {Tubulin-binding TOG domains are found arrayed in a number of proteins that regulate microtubule dynamics. While much is known about the structure and function of TOG domains from the XMAP215 microtubule polymerase family, less in known about the TOG domain array found in animal CLASP family members. The animal CLASP TOG array promotes microtubule pause, potentiates rescue, and limits catastrophe. How structurally distinct the TOG domains of animal CLASP are from one another, from XMAP215 family TOG domains, and whether a specific order of structurally distinct TOG domains in the TOG array is conserved across animal CLASP family members is poorly understood. We present the x-ray crystal structures of Homo sapiens (H.s.) CLASP1 TOG1 and TOG2. The structures of H.s. CLASP1 TOG1 and TOG2 are distinct from each other and from the previously determined structure of Mus musculus (M.m.) CLASP2 TOG3. Comparative analyses of CLASP family TOG domain structures determined to date across species and paralogs supports a conserved CLASP TOG array paradigm in which structurally distinct TOG domains are arrayed in a specific order. H.s. CLASP1 TOG1 bears structural similarity to the free-tubulin binding TOG domains of the XMAP215 family but lacks many of the key tubulin-binding determinants found in XMAP215 family TOG domains. This aligns with studies that report that animal CLASP family TOG1 domains cannot bind free tubulin or microtubules. In contrast, animal CLASP family TOG2 and TOG3 domains have reported microtubule-binding activity but are structurally distinct from the free-tubulin binding TOG domains of the XMAP215 family. H.s. CLASP1 TOG2 has a convex architecture, predicted to engage a hyper-curved tubulin state that may underlie its ability to limit microtubule catastrophe and promote rescue. M.m. CLASP2 TOG3 has unique structural elements in the C-terminal half of its α-solenoid domain that our modeling studies implicate in binding to laterally-associated tubulin subunits in the microtubule lattice in a mode similar to, yet distinct from those predicted for the XMAP215 family TOG4 domain. The potential ability of the animal CLASP family TOG3 domain to engage lateral tubulin subunits may underlie the microtubule rescue activity ascribed to the domain. These findings highlight the structural diversity of TOG domains within the CLASP family TOG array and provide a molecular foundation for understanding CLASP-dependent effects on microtubule dynamics.},
doi = {10.1371/journal.pone.0219823},
journal = {PLoS ONE},
number = 7,
volume = 14,
place = {United States},
year = {Fri Jul 19 00:00:00 EDT 2019},
month = {Fri Jul 19 00:00:00 EDT 2019}
}
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The Arabidopsis CLASP Gene Encodes a Microtubule-Associated Protein Involved in Cell Expansion and Division
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A TOG: -tubulin Complex Structure Reveals Conformation-Based Mechanisms for a Microtubule Polymerase
journal, August 2012
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The Conserved Proteins CHE-12 and DYF-11 Are Required for Sensory Cilium Function in Caenorhabditis elegans
journal, February 2008
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- Genetics, Vol. 178, Issue 2
Drosophila melanogaster Mini Spindles TOG3 Utilizes Unique Structural Elements to Promote Domain Stability and Maintain a TOG1- and TOG2-like Tubulin-binding Surface
text, January 2015
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- The University of North Carolina at Chapel Hill University Libraries
A Cryptic TOG Domain with a Distinct Architecture Underlies CLASP-Dependent Bipolar Spindle Formation
text, January 2013
- L., Rogers, Stephen; C., Slep, Kevin; B., Leano, Jonathan
- The University of North Carolina at Chapel Hill University Libraries
TOG–tubulin binding specificity promotes microtubule dynamics and mitotic spindle formation
text, January 2017
- C., Slep, Kevin; E., Byrnes, Amy
- The University of North Carolina at Chapel Hill University Libraries
Crescerin uses a TOG domain array to regulate microtubules in the primary cilium
text, January 2015
- C., Wood, Cameron; C., Slep, Kevin; J., Dickinson, Daniel
- The University of North Carolina at Chapel Hill University Libraries
PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Apollo - University of Cambridge Repository
An EB1-binding motif acts as a microtubule tip localization signal
text, January 2009
- Honnappa, S.; Gouveia, S. M.; Weisbrich, A.
- Elsevier
A tethered delivery mechanism explains the catalytic action of a microtubule polymerase
journal, August 2014
- Ayaz, Pelin; Munyoki, Sarah; Geyer, Elisabeth A.
- eLife, Vol. 3
Structural basis of tubulin recruitment and assembly by microtubule polymerases with tumor overexpressed gene (TOG) domain arrays
journal, November 2018
- Nithianantham, Stanley; Cook, Brian D.; Beans, Madeleine
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Works referencing / citing this record:
The Inner Junction Complex of the Cilia is an Interaction Hub that Involves Tubulin Post-translational Modifications
journal, February 2020
- Khalifa, Ahmad; Ichikawa, Muneyoshi; Dai, Daniel
- Biophysical Journal, Vol. 118, Issue 3
CLASP2 binding to curved microtubule tips promotes flux and stabilizes kinetochore attachments
journal, November 2019
- Girão, Hugo; Okada, Naoyuki; Rodrigues, Tony A.
- The Journal of Cell Biology
CLASP2 binding to curved microtubule tips promotes flux and stabilizes kinetochore attachments
journal, November 2019
- Girão, Hugo; Okada, Naoyuki; Rodrigues, Tony A.
- The Journal of Cell Biology