An unconventional interaction between Dis1/TOG and Mal3/EB1 in fission yeast promotes the fidelity of chromosome segregation

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• dc.contributor.author Matsuo, Yuzyca
• dc.contributor.author Maurer, Sebastianca
• dc.contributor.author Yukawa, Masashica
• dc.contributor.author Zakian, Silvaca
• dc.contributor.author Singleton, Martin R.ca
• dc.contributor.author Surrey, Thomasca
• dc.contributor.author Toda, Takashica
• dc.date.accessioned 2017-04-24T10:29:42Z
• dc.date.available 2017-04-24T10:29:42Z
• dc.date.issued 2016
• dc.description.abstract Dynamic microtubule plus-ends interact with various intracellular target regions such as the cell cortex and the kinetochore. Two conserved families of microtubule plus-end-tracking proteins, the XMAP215, ch-TOG or CKAP5 family and the end-binding 1 (EB1, also known as MAPRE1) family, play pivotal roles in regulating microtubule dynamics. Here, we study the functional interplay between fission yeast Dis1, a member of the XMAP215/TOG family, and Mal3, an EB1 protein. Using an in vitro microscopy assay, we find that purified Dis1 autonomously tracks growing microtubule ends and is a bona fide microtubule polymerase. Mal3 recruits additional Dis1 to microtubule ends, explaining the synergistic enhancement of microtubule dynamicity by these proteins. A non-canonical binding motif in Dis1 mediates the interaction with Mal3. X-ray crystallography shows that this new motif interacts in an unconventional configuration with the conserved hydrophobic cavity formed within the Mal3 C-terminal region that typically interacts with the canonical SXIP motif. Selectively perturbing the Mal3–Dis1 interaction in living cells demonstrates that it is important for accurate chromosome segregation. Whereas, in some metazoans, the interaction between EB1 and the XMAP215/TOG family members requires an additional binding partner, fission yeast relies on a direct interaction, indicating evolutionary plasticity of this critical interaction module.
• dc.description.sponsorship This work was supported by Cancer Research UK and the Francis Crick Institute which receives its core funding from Cancer Research UK (FC001155, FC001163, FC001184), the UK Medical Research Council (FC001155, FC001163, FC001184), and the Wellcome Trust (FC001155, FC001163, FC001184), the Japan Society for the Promotion of Science (JSPS) [KAKENHI Scientific Research (A) (16H02503 to T.T.), a Challenging Exploratory Research grant (16K14672 to T.T.), Scientific Research (C) (16K07694 to M.Y.)], the Naito Foundation (T.T.) and a Marie Curie fellowship from the European Commission (PIEF-GA-2009-253043 to S.P.M.). Deposited in PMC for immediate release.
• dc.format.mimetype application/pdfca
• dc.identifier.citation Matsuo Y, Maurer S, Yukawa M, Zakian S, Singleton MR, Surrey T, Toda T. An unconventional interaction between Dis1/TOG and Mal3/EB1 in fission yeast promotes the fidelity of chromosome segregation. Journal of Cell Science. 2016;129:4592-606. DOI: 10.1242/jcs.197533
• dc.identifier.doi http://dx.doi.org/10.1242/jcs.197533
• dc.identifier.issn 0021-9533
• dc.identifier.uri http://hdl.handle.net/10230/30882
• dc.language.iso eng
• dc.publisher Company of Biologistsca
• dc.relation.ispartof Journal of Cell Science. 2016;129:4592-606
• dc.rights © 2016. Published by The Company of Biologists Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
• dc.rights.accessRights info:eu-repo/semantics/openAccess
• dc.rights.uri https://creativecommons.org/licenses/by/3.0/
• dc.subject.keyword Crystallography
• dc.subject.keyword EB1
• dc.subject.keyword Microtubule polymerase
• dc.subject.keyword TIRF microscopy
• dc.subject.keyword XMAP215
• dc.subject.keyword TOG
• dc.title An unconventional interaction between Dis1/TOG and Mal3/EB1 in fission yeast promotes the fidelity of chromosome segregationca
• dc.type info:eu-repo/semantics/article
• dc.type.version info:eu-repo/semantics/publishedVersion