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Mitotic exit kinase Dbf2 directly phosphorylates chitin synthase Chs2 to regulate cytokinesis in budding yeast

Oh, Younghoon and Chang, Kuang-Jung and Orlean, Peter and Wloka, Carsten and Deshaies, Raymond and Bi, Erfei (2012) Mitotic exit kinase Dbf2 directly phosphorylates chitin synthase Chs2 to regulate cytokinesis in budding yeast. Molecular Biology of the Cell, 23 (13). pp. 2445-2456. ISSN 1059-1524. PMCID PMC3386209. https://resolver.caltech.edu/CaltechAUTHORS:20120807-123207702

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Abstract

How cell cycle machinery regulates extracellular matrix (ECM) remodeling during cytokinesis remains poorly understood. In the budding yeast Saccharomyces cerevisiae, the primary septum (PS), a functional equivalent of animal ECM, is synthesized during cytokinesis by the chitin synthase Chs2. Here, we report that Dbf2, a conserved mitotic exit kinase, localizes to the division site after Chs2 and directly phosphorylates Chs2 on several residues, including Ser-217. Both phosphodeficient (chs2‑S217A) and phosphomimic (chs2‑S217D) mutations cause defects in cytokinesis, suggesting that dynamic phosphorylation–dephosphorylation of Ser-217 is critical for Chs2 function. It is striking that Chs2‑S217A constricts asymmetrically with the actomyosin ring (AMR), whereas Chs2-S217D displays little or no constriction and remains highly mobile at the division site. These data suggest that Chs2 phosphorylation by Dbf2 triggers its dissociation from the AMR during the late stage of cytokinesis. Of interest, both chs2‑S217A and chs2‑S217D mutants are robustly suppressed by increased dosage of Cyk3, a cytokinesis protein that displays Dbf2‑dependent localization and also stimulates Chs2‑mediated chitin synthesis. Thus Dbf2 regulates PS formation through at least two independent pathways: direct phosphorylation and Cyk3‑mediated activation of Chs2. Our study establishes a mechanism for direct cell cycle control of ECM remodeling during cytokinesis.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1091/mbc.E12-01-0033DOIArticle
http://www.molbiolcell.org/content/23/13/2445PublisherArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3386209/PubMed CentralArticle
ORCID:
AuthorORCID
Deshaies, Raymond0000-0002-3671-9354
Additional Information:© 2012 Oh et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). Received: Jan 17, 2012; Revised: Apr 20, 2012; Accepted: May 3, 2012. Published online before print May 9, 2012. We thank Aaron Gitler and Gislene Pereira for providing plasmids and the members of the Bi, Deshaies, and Orlean laboratories for discussions. This work was supported by National Institutes of Health Grants GM59216 and GM87365 (to E.B.), a fellowship from the Boehringer Ingelheim Fonds (to C.W.), and Taiwan Merit Scholarship TMS-094-1-A-026 (to K.J.C.). R.D. is an Investigator of the Howard Hughes Medical Institute.
Funders:
Funding AgencyGrant Number
NIHGM59216
NIHGM87365
Boehringer Ingelheim FondsUNSPECIFIED
Taiwan Merit ScholarshipTMS-094-1-A-026
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Issue or Number:13
PubMed Central ID:PMC3386209
Record Number:CaltechAUTHORS:20120807-123207702
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20120807-123207702
Official Citation:Younghoon Oh, Kuang-Jung Chang, Peter Orlean, Carsten Wloka, Raymond Deshaies, and Erfei Bi Mitotic exit kinase Dbf2 directly phosphorylates chitin synthase Chs2 to regulate cytokinesis in budding yeast Mol. Biol. Cell 2012 23:13 2445-2456; First Published on May 9, 2012; doi:10.1091/mbc.E12-01-0033
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:32984
Collection:CaltechAUTHORS
Deposited By: Aucoeur Ngo
Deposited On:07 Aug 2012 20:40
Last Modified:03 Oct 2019 04:05

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