SUMO fosters assembly and functionality of the MutSγ complex to facilitate meiotic crossing over.

Cell Nucleus / genetics Chromosome Segregation Crossing Over, Genetic DNA / genetics DNA Damage DNA Repair DNA-Binding Proteins / genetics Meiosis Saccharomyces cerevisiae / genetics Saccharomyces cerevisiae Proteins / genetics Small Ubiquitin-Related Modifier Proteins / genetics Sumoylation Ubiquitin-Conjugating Enzymes / genetics
DNA repair MutS SUMO aneuploidy chromosome segregation crossing over double-strand break homologous recombination meiosis protein modification

Journal

Developmental cell
ISSN: 1878-1551
Titre abrégé: Dev Cell
Pays: United States
ID NLM: 101120028

Informations de publication

Date de publication:
26 07 2021
Historique:
received: 07 10 2020
revised: 31 03 2021
accepted: 10 06 2021
pubmed: 3 7 2021
medline: 10 11 2021
entrez: 2 7 2021
Statut: ppublish

Résumé

Crossing over is essential for chromosome segregation during meiosis. Protein modification by SUMO is implicated in crossover control, but pertinent targets have remained elusive. Here we identify Msh4 as a target of SUMO-mediated crossover regulation. Msh4 and Msh5 constitute the MutSγ complex, which stabilizes joint-molecule (JM) recombination intermediates and facilitates their resolution into crossovers. Msh4 SUMOylation enhances these processes to ensure that each chromosome pair acquires at least one crossover. Msh4 is directly targeted by E2 conjugase Ubc9, initially becoming mono-SUMOylated in response to DNA double-strand breaks, then multi/poly-SUMOylated forms arise as homologs fully engage. Mechanistically, SUMOylation fosters interaction between Msh4 and Msh5. We infer that initial SUMOylation of Msh4 enhances assembly of MutSγ in anticipation of JM formation, while secondary SUMOylation may promote downstream functions. Regulation of Msh4 by SUMO is distinct and independent of its previously described stabilization by phosphorylation, defining MutSγ as a hub for crossover control.

Identifiants

DOI: 10.1016/j.devcel.2021.06.012 PMID: 34214491 PMC: PMC8319151
pubmed: 34214491
pii: S1534-5807(21)00519-0
doi: 10.1016/j.devcel.2021.06.012
pmc: PMC8319151
mid: NIHMS1717573
pii:
doi:

Substances chimiques

DNA-Binding Proteins 0
MSH4 protein, S cerevisiae 0
MSH5 protein, S cerevisiae 0
Saccharomyces cerevisiae Proteins 0
Small Ubiquitin-Related Modifier Proteins 0
DNA 9007-49-2
Ubiquitin-Conjugating Enzymes EC 2.3.2.23
ubiquitin-conjugating enzyme UBC9 EC 6.3.2.-

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2073-2088.e3

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM074223
Pays : United States
Organisme : NIGMS NIH HHS
ID : R15 GM135904
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States

Informations de copyright

Copyright © 2021 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

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Auteurs

Wei He (W)

Howard Hughes Medical Institute, University of California, Davis, Davis, CA, USA; Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, CA, USA.

Gerrik F Verhees (GF)

Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, CA, USA.

Nikhil Bhagwat (N)

Howard Hughes Medical Institute, University of California, Davis, Davis, CA, USA; Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, CA, USA.

Ye Yang (Y)

Howard Hughes Medical Institute, University of California, Davis, Davis, CA, USA; Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, CA, USA.

Dhananjaya S Kulkarni (DS)

Howard Hughes Medical Institute, University of California, Davis, Davis, CA, USA; Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, CA, USA.

Zane Lombardo (Z)

Department of Molecular Biology and Biochemistry, Molecular Biophysics Program, Wesleyan University, Middletown, CT, USA.

Sudipta Lahiri (S)

Department of Molecular Biology and Biochemistry, Molecular Biophysics Program, Wesleyan University, Middletown, CT, USA.

Pritha Roy (P)

Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, CA, USA.

Jiaming Zhuo (J)

Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, CA, USA.

Brian Dang (B)

Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, CA, USA.

Andriana Snyder (A)

Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, CA, USA.

Shashank Shastry (S)

Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, CA, USA.

Michael Moezpoor (M)

Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, CA, USA.

Lilly Alocozy (L)

Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, CA, USA.

Kathy Gyehyun Lee (KG)

Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, CA, USA.

Daniel Painter (D)

Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, CA, USA.

Ishita Mukerji (I)

Department of Molecular Biology and Biochemistry, Molecular Biophysics Program, Wesleyan University, Middletown, CT, USA.

Neil Hunter (N)

Howard Hughes Medical Institute, University of California, Davis, Davis, CA, USA; Department of Microbiology & Molecular Genetics, University of California, Davis, Davis, CA, USA. Electronic address: nhunter@ucdavis.edu.

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Classifications MeSH

Recherchemedicale.com › Cellules › Structures cellulaires › Espace intracellulaire › Cytoplasme › Structures cytoplasmiques › Organites › Noyau de la cellule › SUMO fosters assembly and functionality of the...
Recherchemedicale.com › Phénomènes génétiques › Division du noyau cellulaire › Ségrégation des chromosomes › SUMO fosters assembly and functionality of the...
Recherchemedicale.com › Phénomènes génétiques › Recombinaison génétique › Recombinaison homologue › Crossing-over › SUMO fosters assembly and functionality of the...
Recherchemedicale.com › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ADN › SUMO fosters assembly and functionality of the...
Recherchemedicale.com › Phénomènes génétiques › Altération de l'ADN › SUMO fosters assembly and functionality of the...
Recherchemedicale.com › Phénomènes génétiques › Réparation de l'ADN › SUMO fosters assembly and functionality of the...
Recherchemedicale.com › Acides aminés, peptides et protéines › Protéines › Protéines de liaison à l'ADN › SUMO fosters assembly and functionality of the...
Recherchemedicale.com › Phénomènes génétiques › Division du noyau cellulaire › Méiose › SUMO fosters assembly and functionality of the...
Recherchemedicale.com › Eucaryotes › Champignons › Levures › Saccharomyces › Saccharomyces cerevisiae › SUMO fosters assembly and functionality of the...
Recherchemedicale.com › Acides aminés, peptides et protéines › Protéines › Protéines fongiques › Protéines de Saccharomyces cerevisiae › SUMO fosters assembly and functionality of the...
Recherchemedicale.com › Acides aminés, peptides et protéines › Protéines › Ubiquitines › Petites protéines modificatrices apparentées à l'ubiquitine › SUMO fosters assembly and functionality of the...
Recherchemedicale.com › Phénomènes génétiques › Régulation de l'expression des gènes › Modification traductionnelle des protéines › Maturation post-traductionnelle des protéines › Ubiquitination › Sumoylation › SUMO fosters assembly and functionality of the...
Recherchemedicale.com › Enzymes et coenzymes › Enzymes › Ligases › Ubiquitin-protein ligase complexes › Ubiquitin-conjugating enzymes › SUMO fosters assembly and functionality of the...