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The Chromosomal Passenger Complex Activates Polo Kinase at Centromeres

Carmena, Mar and Pinson, Xavier and Platani, Melpi and Salloum, Zeina and Xu, Zhenjie and Clark, Anthony and MacIsaac, Fiona and Ogawa, Hiromi and Eggert, Ulrike and Glover, David M. and Archambault, Vincent and Earnshaw, William C. (2012) The Chromosomal Passenger Complex Activates Polo Kinase at Centromeres. PLoS Biology, 10 (1). Art. No. e1001250. ISSN 1545-7885. PMCID PMC3265468. https://resolver.caltech.edu/CaltechAUTHORS:20200807-170352108

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[img] Image (TIFF) (Figure S1. Localization of Polo, INCENP, and tubulin during mitosis in Drosophila cultured cells) - Supplemental Material
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[img] Image (TIFF) (Figure S2. Relative localizations of Polo and Aurora kinases during mitosis in Drosophila cultured cells) - Supplemental Material
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[img] Image (TIFF) (Figure S3. Characterization of the anti-Polo^(T182Ph) antibody by immunofluorescence) - Supplemental Material
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[img] Image (TIFF) (Figure S4. Colocalization of INCENP/Polo/Polo^(T182Ph) changes through mitosis) - Supplemental Material
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[img] Image (TIFF) (Figure S5. CPC localization is similar in Binucleine-2 treated cells and incenp mutants in prometaphase) - Supplemental Material
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[img] Image (TIFF) (Figure S6. RNAi depletion of Aurora B or INCENP does not reduce Polo^(T182Ph) levels at centrosomes) - Supplemental Material
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[img] Image (TIFF) (Figure S7. A decrease in INCENP activity partially rescues the lethality induced by a gain of Polo function) - Supplemental Material
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[img] Image (TIFF) (Figure S8. Aurora B activity is required for activation of Plk1 at centromere/kinetochores in human cells) - Supplemental Material
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Abstract

The coordinated activities at centromeres of two key cell cycle kinases, Polo and Aurora B, are critical for ensuring that the two sister kinetochores of each chromosome are attached to microtubules from opposite spindle poles prior to chromosome segregation at anaphase. Initial attachments of chromosomes to the spindle involve random interactions between kinetochores and dynamic microtubules, and errors occur frequently during early stages of the process. The balance between microtubule binding and error correction (e.g., release of bound microtubules) requires the activities of Polo and Aurora B kinases, with Polo promoting stable attachments and Aurora B promoting detachment. Our study concerns the coordination of the activities of these two kinases in vivo. We show that INCENP, a key scaffolding subunit of the chromosomal passenger complex (CPC), which consists of Aurora B kinase, INCENP, Survivin, and Borealin/Dasra B, also interacts with Polo kinase in Drosophila cells. It was known that Aurora A/Bora activates Polo at centrosomes during late G2. However, the kinase that activates Polo on chromosomes for its critical functions at kinetochores was not known. We show here that Aurora B kinase phosphorylates Polo on its activation loop at the centromere in early mitosis. This phosphorylation requires both INCENP and Aurora B activity (but not Aurora A activity) and is critical for Polo function at kinetochores. Our results demonstrate clearly that Polo kinase is regulated differently at centrosomes and centromeres and suggest that INCENP acts as a platform for kinase crosstalk at the centromere. This crosstalk may enable Polo and Aurora B to achieve a balance wherein microtubule mis-attachments are corrected, but proper attachments are stabilized allowing proper chromosome segregation.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1371/journal.pbio.1001250DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3265468/PubMed CentralArticle
https://doi.org/10.1371/annotation/7832f573-e0d9-465f-b5d4-0ac1014b6112.s005.cnDOICorrection
https://doi.org/10.1371/annotation/7832f573-e0d9-465f-b5d4-0ac1014b6112 DOICorrection
ORCID:
AuthorORCID
Carmena, Mar0000-0002-2352-1066
Platani, Melpi0000-0001-6408-4774
Salloum, Zeina0000-0003-4658-5000
Ogawa, Hiromi0000-0002-1972-1225
Eggert, Ulrike0000-0003-0932-5525
Glover, David M.0000-0003-0956-0103
Archambault, Vincent0000-0002-2857-7667
Earnshaw, William C.0000-0002-7191-0621
Additional Information:© 2012 Carmena et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received: June 10, 2011; Accepted: December 8, 2011; Published: January 24, 2012. The WCE Lab is supported by Wellcome Trust Principal Research Fellowship to WCE 073915/Z/03/Z (The Wellcome Trust: http://www.wellcome.ac.uk/). The Wellcome Trust Centre for Cell Biology is funded by core grants number 077707 and 092076. VA Holds a Career Development Award from the Human Frontier Science Program Organization - CDA00036/2009 (www.hfspo.org)and a fellowship from the Fonds de recherche en santé du Québec. Work in VA's lab was funded by the Canadian Institutes of Health Research (www.cihr-irsc.gc.ca). U.S.E. was supported by NIH grant R01 GM082834. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We would like to thank Sonia Lain for advising the use of the PLA technique; Jose de las Heras and Diana Papini for advice with data analysis; Sasha Kaganski and Laura Wood for help with the manuscript; P.P. D'Avino for generous sharing of cell lines; K. McKim for his generous gift of antibodies; and Karine Normandin for technical assistance. Author Contributions. The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: MC XP VA. Performed the experiments: MC XP MP ZS AC ZX FM VA. Analyzed the data: MC XP MP ZS WCE VA. Contributed reagents/materials/analysis tools: MC XF MP UE DMG VA. Wrote the paper: MC VA WCE. Provided technical assistance: HO. The authors have declared that no competing interests exist.
Errata:Carmena M, Pinson X, Platani M, Salloum Z, Xu Z, Clark A, et al. (2012) Correction: The Chromosomal Passenger Complex Activates Polo Kinase at Centromeres. PLoS Biol 10(1): 10.1371/annotation/7832f573-e0d9-465f-b5d4-0ac1014b6112. https://doi.org/10.1371/annotation/7832f573-e0d9-465f-b5d4-0ac1014b6112
Funders:
Funding AgencyGrant Number
Wellcome Trust073915/Z/03/Z
Wellcome Trust077707
Wellcome Trust092076
Human Frontier Science ProgramCDA00036/2009
Fonds de recherche en santé du QuébecUNSPECIFIED
Canadian Institutes of Health Research (CIHR)UNSPECIFIED
NIHR01 GM082834
Issue or Number:1
PubMed Central ID:PMC3265468
Record Number:CaltechAUTHORS:20200807-170352108
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200807-170352108
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:104853
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:12 Aug 2020 22:37
Last Modified:12 Aug 2020 22:37

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