Plk1/Polo Phosphorylates Sas-4 at the Onset of Mitosis for an Efficient Recruitment of Pericentriolar Material to Centrosomes

Summary: Centrosomes are the major microtubule-organizing centers, consisting of centrioles surrounded by a pericentriolar material (PCM). Centrosomal PCM is spatiotemporally regulated to be minimal during interphase and expands as cells enter mitosis. It is unclear how PCM expansion is initiated at...

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Main Authors: Anand Ramani, Aruljothi Mariappan, Marco Gottardo, Sunit Mandad, Henning Urlaub, Tomer Avidor-Reiss, Maria Riparbelli, Giuliano Callaini, Alain Debec, Regina Feederle, Jay Gopalakrishnan
Format: Article
Language:English
Published: Elsevier 2018-12-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124718319089
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language English
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author Anand Ramani
Aruljothi Mariappan
Marco Gottardo
Sunit Mandad
Henning Urlaub
Tomer Avidor-Reiss
Maria Riparbelli
Giuliano Callaini
Alain Debec
Regina Feederle
Jay Gopalakrishnan
spellingShingle Anand Ramani
Aruljothi Mariappan
Marco Gottardo
Sunit Mandad
Henning Urlaub
Tomer Avidor-Reiss
Maria Riparbelli
Giuliano Callaini
Alain Debec
Regina Feederle
Jay Gopalakrishnan
Plk1/Polo Phosphorylates Sas-4 at the Onset of Mitosis for an Efficient Recruitment of Pericentriolar Material to Centrosomes
Cell Reports
author_facet Anand Ramani
Aruljothi Mariappan
Marco Gottardo
Sunit Mandad
Henning Urlaub
Tomer Avidor-Reiss
Maria Riparbelli
Giuliano Callaini
Alain Debec
Regina Feederle
Jay Gopalakrishnan
author_sort Anand Ramani
title Plk1/Polo Phosphorylates Sas-4 at the Onset of Mitosis for an Efficient Recruitment of Pericentriolar Material to Centrosomes
title_short Plk1/Polo Phosphorylates Sas-4 at the Onset of Mitosis for an Efficient Recruitment of Pericentriolar Material to Centrosomes
title_full Plk1/Polo Phosphorylates Sas-4 at the Onset of Mitosis for an Efficient Recruitment of Pericentriolar Material to Centrosomes
title_fullStr Plk1/Polo Phosphorylates Sas-4 at the Onset of Mitosis for an Efficient Recruitment of Pericentriolar Material to Centrosomes
title_full_unstemmed Plk1/Polo Phosphorylates Sas-4 at the Onset of Mitosis for an Efficient Recruitment of Pericentriolar Material to Centrosomes
title_sort plk1/polo phosphorylates sas-4 at the onset of mitosis for an efficient recruitment of pericentriolar material to centrosomes
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2018-12-01
description Summary: Centrosomes are the major microtubule-organizing centers, consisting of centrioles surrounded by a pericentriolar material (PCM). Centrosomal PCM is spatiotemporally regulated to be minimal during interphase and expands as cells enter mitosis. It is unclear how PCM expansion is initiated at the onset of mitosis. Here, we identify that, in Drosophila, Plk1/Polo kinase phosphorylates the conserved centrosomal protein Sas-4 in vitro. This phosphorylation appears to occur at the onset of mitosis, enabling Sas-4’s localization to expand outward from meiotic and mitotic centrosomes. The Plk1/Polo kinase site of Sas-4 is then required for an efficient recruitment of Cnn and γ-tubulin, bona fide PCM proteins that are essential for PCM expansion and centrosome maturation. Point mutations at Plk1/Polo sites of Sas-4 affect neither centrosome structure nor centriole duplication but specifically reduce the affinity to bind Cnn and γ-tubulin. These observations identify Plk1/Polo kinase regulation of Sas-4 as essential for efficient PCM expansion. : Ramani et al. show that Plk1/Polo phosphorylates Drosophila Sas-4 at the onset of mitosis. Cell-cycle-specific modification of Sas-4 determines the spatiotemporal localization of Sas-4 in centrosomes, which is required for an efficient recruitment of PCM proteins in mitosis. Keywords: pericentriolar material, centrosomes, Sas-4, Drosophila melanogaster, Plk1, centrosome maturation
url http://www.sciencedirect.com/science/article/pii/S2211124718319089
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spelling doaj-0b85e528dc404c1fb4a97258f852b5682020-11-25T02:21:27ZengElsevierCell Reports2211-12472018-12-01251336183630.e6Plk1/Polo Phosphorylates Sas-4 at the Onset of Mitosis for an Efficient Recruitment of Pericentriolar Material to CentrosomesAnand Ramani0Aruljothi Mariappan1Marco Gottardo2Sunit Mandad3Henning Urlaub4Tomer Avidor-Reiss5Maria Riparbelli6Giuliano Callaini7Alain Debec8Regina Feederle9Jay Gopalakrishnan10Institute of Human Genetics, Universitätsklinikum Heinrich-Heine-Universität Düsseldorf, Universität Str. 1, 40225 Düsseldorf, Germany; Center for Molecular Medicine Cologne, University of Cologne, Robert-Koch-Str. 21, 50931 Cologne, Germany; IUF–Leibniz-Institut für umweltmedizinische Forschung gGmbH, Auf’m Hennekamp 50, 40225 Düsseldorf, GermanyInstitute of Human Genetics, Universitätsklinikum Heinrich-Heine-Universität Düsseldorf, Universität Str. 1, 40225 Düsseldorf, Germany; Center for Molecular Medicine Cologne, University of Cologne, Robert-Koch-Str. 21, 50931 Cologne, GermanyInstitute of Human Genetics, Universitätsklinikum Heinrich-Heine-Universität Düsseldorf, Universität Str. 1, 40225 Düsseldorf, Germany; Center for Molecular Medicine Cologne, University of Cologne, Robert-Koch-Str. 21, 50931 Cologne, GermanyBioanalytical Mass Spectrometry Group, Max Planck Institute for Biophysical Chemistry, Am Fassberg 11, 37077 Göttingen, Germany; Bioanalytics, University Medical Center Goettingen, Robert-Koch-Strasse 40, 37075 Goettingen, Germany; Department of Neuro- and Sensory Physiology, University Medical Center Göttingen, Göttingen, GermanyBioanalytical Mass Spectrometry Group, Max Planck Institute for Biophysical Chemistry, Am Fassberg 11, 37077 Göttingen, Germany; Bioanalytics, University Medical Center Goettingen, Robert-Koch-Strasse 40, 37075 Goettingen, GermanyDepartment of Biological Sciences, College of Natural Sciences and Mathematics, University of Toledo, Toledo, OH 43606Department of Life Sciences, University of Siena, 53100 Siena, ItalyDepartment of Life Sciences, University of Siena, 53100 Siena, ItalyPolarity and Morphogenesis Group, Institut Jacques Monod, Centre National de la Recherche Scientifique, University Paris Diderot, 75013 Paris, FranceHelmholtz Zentrum München, German Research Center for Environmental Health, Institute for Diabetes and Obesity, Core Facility, 81377 Munich, GermanyInstitute of Human Genetics, Universitätsklinikum Heinrich-Heine-Universität Düsseldorf, Universität Str. 1, 40225 Düsseldorf, Germany; Center for Molecular Medicine Cologne, University of Cologne, Robert-Koch-Str. 21, 50931 Cologne, Germany; IUF–Leibniz-Institut für umweltmedizinische Forschung gGmbH, Auf’m Hennekamp 50, 40225 Düsseldorf, Germany; Corresponding authorSummary: Centrosomes are the major microtubule-organizing centers, consisting of centrioles surrounded by a pericentriolar material (PCM). Centrosomal PCM is spatiotemporally regulated to be minimal during interphase and expands as cells enter mitosis. It is unclear how PCM expansion is initiated at the onset of mitosis. Here, we identify that, in Drosophila, Plk1/Polo kinase phosphorylates the conserved centrosomal protein Sas-4 in vitro. This phosphorylation appears to occur at the onset of mitosis, enabling Sas-4’s localization to expand outward from meiotic and mitotic centrosomes. The Plk1/Polo kinase site of Sas-4 is then required for an efficient recruitment of Cnn and γ-tubulin, bona fide PCM proteins that are essential for PCM expansion and centrosome maturation. Point mutations at Plk1/Polo sites of Sas-4 affect neither centrosome structure nor centriole duplication but specifically reduce the affinity to bind Cnn and γ-tubulin. These observations identify Plk1/Polo kinase regulation of Sas-4 as essential for efficient PCM expansion. : Ramani et al. show that Plk1/Polo phosphorylates Drosophila Sas-4 at the onset of mitosis. Cell-cycle-specific modification of Sas-4 determines the spatiotemporal localization of Sas-4 in centrosomes, which is required for an efficient recruitment of PCM proteins in mitosis. Keywords: pericentriolar material, centrosomes, Sas-4, Drosophila melanogaster, Plk1, centrosome maturationhttp://www.sciencedirect.com/science/article/pii/S2211124718319089