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The chromosome passenger complex is required for fidelity of chromosome transmission and cytokinesis in meiosis of mouse oocytes

Sharif, Bedra and Na, Jie and Lykke-Hartmann, Karin and McLaughlin, Stephen H. and Laue, Ernest and Glover, David M. and Zernicka-Goetz, Magdalena (2010) The chromosome passenger complex is required for fidelity of chromosome transmission and cytokinesis in meiosis of mouse oocytes. Journal of Cell Science, 123 (24). pp. 4292-4300. ISSN 0021-9533. PMCID PMC2995614. doi:10.1242/jcs.067447. https://resolver.caltech.edu/CaltechAUTHORS:20190417-163114460

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[img] PDF (Table S1. siRNA sequences used in this study) - Supplemental Material
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[img] PDF (Table S2. Effects of exogenous Aurora kinases B and C on polar body extrusion (PBE)) - Supplemental Material
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[img] Image (JPEG) (Fig. S1. Expression of Aurora B in the mouse oocyte) - Supplemental Material
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[img] Image (JPEG) (Fig. S2. Depletion of INCENP disrupts localization of Aurora kinases) - Supplemental Material
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[img] Image (JPEG) (Fig. S3. RNAi does not effectively deplete Aurora C) - Supplemental Material
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[img] Image (JPEG) (Fig. S4. Treatment of oocytes with very high concentrations of siRNAs leads to MI arrest) - Supplemental Material
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Abstract

The existence of two forms of the chromosome passenger complex (CPC) in the mammalian oocyte has meant that its role in female meiosis has remained unclear. Here we use loss- and gain-of function approaches to assess the meiotic functions of one of the shared components of these complexes, INCENP, and of the variable kinase subunits, Aurora B or Aurora C. We show that either the depletion of INCENP or the combined inhibition of Aurora kinases B and C activates the anaphase-promoting complex or cyclosome (APC/C) before chromosomes have properly congressed in meiosis I and also prevents cytokinesis and hence extrusion of the first polar body. Overexpression of Aurora C also advances APC/C activation and results in cytokinesis failure in a high proportion of oocytes, indicative of a dominant effect on CPC function. Together, this points to roles for the meiotic CPC in functions similar to the mitotic roles of the complex: correcting chromosome attachment to microtubules, facilitating the spindle-assembly checkpoint (SAC) function and enabling cytokinesis. Surprisingly, overexpression of Aurora B leads to a failure of APC/C activation, stabilization of securin and consequently a failure of chiasmate chromosomes to resolve – a dominant phenotype that is completely suppressed by depletion of INCENP. Taken together with the differential distribution of Aurora proteins B and C on chiasmate chromosomes, this points to differential functions of the two forms of CPC in regulating the separation of homologous chromosomes in meiosis I.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1242/jcs.067447DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2995614/PubMed CentralArticle
http://jcs.biologists.org/lookup/suppl/doi:10.1242/jcs.067447/-/DC1PublisherSupporting Information
ORCID:
AuthorORCID
Glover, David M.0000-0003-0956-0103
Zernicka-Goetz, Magdalena0000-0002-7004-2471
Additional Information:© 2010 The Company of Biologists. Accepted 2 September 2010. We thank Anna Ajduk for help in assaying Aurora B function in the second meiosis, Bernhard Strauss for help in establishing conditions for monitoring Securin degradation and Jonathan Pines for the gift of the Securin–GFP construct; we also thank Helen Bolton for examining the role of Aurora C in embryos and John Crang for help in compiling figures. This work was supported by a Wellcome Trust grant to M.Z.-G. and an MRC Programme Grant to D.M.G. B.S. held a Gates Foundation Studentship of the University of Cambridge. J.N. is supported by a MRC Career Development Fellowship. K.L.-H. was supported by the Alfred Benzon Stipend, Denmark (current address: Institute of Medical Biochemistry, Aarhus University, Denmark). Part of the image acquisition was carried out in the Wellcome-Trust-supported light microscopy facility in the University of Sheffield, UK (grant: GR077544AIA). Confocal microscope facilities in the D.M.G. laboratory were supported by grants from CR-UK and BBSRC. Deposited in PMC for release after 6 months. Supplementary material available online at http://jcs.biologists.org/lookup/suppl/doi:10.1242/jcs.067447/-/DC1
Funders:
Funding AgencyGrant Number
Wellcome TrustGR077544AIA
Medical Research Council (UK)UNSPECIFIED
Bill and Melinda Gates FoundationUNSPECIFIED
Alfred Benzon Stipend, DenmarkUNSPECIFIED
Cancer Research UKUNSPECIFIED
Biotechnology and Biological Sciences Research Council (BBSRC)UNSPECIFIED
Subject Keywords:Aurora B, Aurora C, Chromosome passenger complex, INCENP, Meiosis, Mouse oocyte
Issue or Number:24
PubMed Central ID:PMC2995614
DOI:10.1242/jcs.067447
Record Number:CaltechAUTHORS:20190417-163114460
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190417-163114460
Official Citation:The chromosome passenger complex is required for fidelity of chromosome transmission and cytokinesis in meiosis of mouse oocytes Bedra Sharif, Jie Na, Karin Lykke-Hartmann, Stephen H. McLaughlin, Ernest Laue, David M. Glover, Magdalena Zernicka-Goetz J Cell Sci 2010 123: 4292-4300; doi: 10.1242/jcs.067447
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:94768
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:18 Apr 2019 22:43
Last Modified:16 Nov 2021 17:07

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