A SUMO-Dependent Protein Network Regulates Chromosome Congression During Oocyte Meiosis

Federico Pelisch; Triin Tammsalu; Bin Wang; Ellis G. Jaffray; Anton Gartner; Ronald T. Hay

doi:10.1016/j.molcel.2016.11.001

A SUMO-Dependent Protein Network Regulates Chromosome Congression During Oocyte Meiosis

Federico Pelisch, Triin Tammsalu, Bin Wang, Ellis G. Jaffray, Anton Gartner, Ronald T. Hay (Lead / Corresponding author)

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Abstract

During Caenorhabditis elegans oocyte meiosis, a multi-protein ring complex (RC) localised between homologous chromosomes, promotes chromosome congression through the action of the chromokinesin KLP-19. While some RC components are known, the mechanism of RC assembly has remained obscure. We show that SUMO E3 ligase GEI-17/PIAS is required for KLP-19 recruitment to the RC and proteomic analysis identified KLP-19 as a SUMO substrate in vivo. In vitro analysis revealed that KLP-19 is efficiently sumoylated in a GEI-17-dependent manner, while GEI-17 undergoes extensive auto-sumoylation. GEI-17 and another RC component, the kinase BUB-1, contain functional SUMO Interaction Motifs (SIMs) allowing them to recruit SUMO modified proteins, including KLP-19, into the RC. Thus dynamic SUMO modification and the presence of SIMs in RC components generate a SUMO-SIM network that facilitates assembly of the RC. Our results highlight the importance of SUMO-SIM networks in regulating the assembly of dynamic protein complexes.

Original language	English
Pages (from-to)	66-77
Number of pages	12
Journal	Molecular Cell
Volume	65
Issue number	1
Early online date	8 Dec 2016
DOIs	https://doi.org/10.1016/j.molcel.2016.11.001
Publication status	Published - 5 Jan 2017

Keywords

SUMO
PIAS
meiosis
C. elegans
SUMO-interaction motif
kinesin
spindle
chromosomes

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10.1016/j.molcel.2016.11.001Licence: CC BY

Final Published Version
©2017 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/)
Final published version, 4.58 MBLicence: CC BY

Determining the Role and Mechanism of Action of SUMO Targeted Ubiquitin Ligase RNF4 in Maintaining Genome Integrity (Senior Investigator Award)
Hay, R. (Investigator)
1/10/12 → 31/01/20
Project: Research
CeleSUMOMS: SUMO Proteomics in C. Elegans: Focus on Meiosis and the DNA Damage Response (Fellow: Federico Pelisch)
Hay, R. (Investigator)
COMMISSION OF THE EUROPEAN COMMUNITIES
17/09/12 → 16/09/14
Project: Research

Global identification of SUMO modification sites
Tammsalu, T. (Author), Hay, R. (Supervisor), 2016
Student thesis: Doctoral Thesis › Doctor of Philosophy

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Hay, Ronald
- Molecular Cell and Developmental Biology - Professor
Person: Academic

Cite this

@article{650f8f7540e7463c91d3f88bb4eb1952,

title = "A SUMO-Dependent Protein Network Regulates Chromosome Congression During Oocyte Meiosis",

abstract = "During Caenorhabditis elegans oocyte meiosis, a multi-protein ring complex (RC) localised between homologous chromosomes, promotes chromosome congression through the action of the chromokinesin KLP-19. While some RC components are known, the mechanism of RC assembly has remained obscure. We show that SUMO E3 ligase GEI-17/PIAS is required for KLP-19 recruitment to the RC and proteomic analysis identified KLP-19 as a SUMO substrate in vivo. In vitro analysis revealed that KLP-19 is efficiently sumoylated in a GEI-17-dependent manner, while GEI-17 undergoes extensive auto-sumoylation. GEI-17 and another RC component, the kinase BUB-1, contain functional SUMO Interaction Motifs (SIMs) allowing them to recruit SUMO modified proteins, including KLP-19, into the RC. Thus dynamic SUMO modification and the presence of SIMs in RC components generate a SUMO-SIM network that facilitates assembly of the RC. Our results highlight the importance of SUMO-SIM networks in regulating the assembly of dynamic protein complexes.",

keywords = "SUMO, PIAS, meiosis, C. elegans, SUMO-interaction motif, kinesin, spindle, chromosomes",

author = "Federico Pelisch and Triin Tammsalu and Bin Wang and Jaffray, {Ellis G.} and Anton Gartner and Hay, {Ronald T.}",

note = "Wellcome Trust Investigator Award (098391/Z/12/7), Cancer Research UK (C434/A13067), BBSRC (BB/J015199/1)",

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AU - Pelisch, Federico

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AU - Wang, Bin

AU - Jaffray, Ellis G.

AU - Gartner, Anton

AU - Hay, Ronald T.

N1 - Wellcome Trust Investigator Award (098391/Z/12/7), Cancer Research UK (C434/A13067), BBSRC (BB/J015199/1)

PY - 2017/1/5

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N2 - During Caenorhabditis elegans oocyte meiosis, a multi-protein ring complex (RC) localised between homologous chromosomes, promotes chromosome congression through the action of the chromokinesin KLP-19. While some RC components are known, the mechanism of RC assembly has remained obscure. We show that SUMO E3 ligase GEI-17/PIAS is required for KLP-19 recruitment to the RC and proteomic analysis identified KLP-19 as a SUMO substrate in vivo. In vitro analysis revealed that KLP-19 is efficiently sumoylated in a GEI-17-dependent manner, while GEI-17 undergoes extensive auto-sumoylation. GEI-17 and another RC component, the kinase BUB-1, contain functional SUMO Interaction Motifs (SIMs) allowing them to recruit SUMO modified proteins, including KLP-19, into the RC. Thus dynamic SUMO modification and the presence of SIMs in RC components generate a SUMO-SIM network that facilitates assembly of the RC. Our results highlight the importance of SUMO-SIM networks in regulating the assembly of dynamic protein complexes.

AB - During Caenorhabditis elegans oocyte meiosis, a multi-protein ring complex (RC) localised between homologous chromosomes, promotes chromosome congression through the action of the chromokinesin KLP-19. While some RC components are known, the mechanism of RC assembly has remained obscure. We show that SUMO E3 ligase GEI-17/PIAS is required for KLP-19 recruitment to the RC and proteomic analysis identified KLP-19 as a SUMO substrate in vivo. In vitro analysis revealed that KLP-19 is efficiently sumoylated in a GEI-17-dependent manner, while GEI-17 undergoes extensive auto-sumoylation. GEI-17 and another RC component, the kinase BUB-1, contain functional SUMO Interaction Motifs (SIMs) allowing them to recruit SUMO modified proteins, including KLP-19, into the RC. Thus dynamic SUMO modification and the presence of SIMs in RC components generate a SUMO-SIM network that facilitates assembly of the RC. Our results highlight the importance of SUMO-SIM networks in regulating the assembly of dynamic protein complexes.

KW - SUMO

KW - PIAS

KW - meiosis

KW - C. elegans

KW - SUMO-interaction motif

KW - kinesin

KW - spindle

KW - chromosomes

U2 - 10.1016/j.molcel.2016.11.001

DO - 10.1016/j.molcel.2016.11.001

M3 - Article

C2 - 27939944

SN - 1097-2765

VL - 65

SP - 66

EP - 77

JO - Molecular Cell

JF - Molecular Cell

IS - 1

ER -

A SUMO-Dependent Protein Network Regulates Chromosome Congression During Oocyte Meiosis

Abstract

Keywords

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Projects

Determining the Role and Mechanism of Action of SUMO Targeted Ubiquitin Ligase RNF4 in Maintaining Genome Integrity (Senior Investigator Award)

CeleSUMOMS: SUMO Proteomics in C. Elegans: Focus on Meiosis and the DNA Damage Response (Fellow: Federico Pelisch)

Student theses

Global identification of SUMO modification sites

Profiles

Hay, Ronald

Cite this