Structural maturation of SYCP1-mediated meiotic chromosome synapsis by SYCE3.


Journal

Nature structural & molecular biology
ISSN: 1545-9985
Titre abrégé: Nat Struct Mol Biol
Pays: United States
ID NLM: 101186374

Informations de publication

Date de publication:
02 2023
Historique:
received: 09 10 2018
accepted: 06 12 2022
pubmed: 13 1 2023
medline: 22 2 2023
entrez: 12 1 2023
Statut: ppublish

Résumé

In meiosis, a supramolecular protein structure, the synaptonemal complex (SC), assembles between homologous chromosomes to facilitate their recombination. Mammalian SC formation is thought to involve hierarchical zipper-like assembly of an SYCP1 protein lattice that recruits stabilizing central element (CE) proteins as it extends. Here we combine biochemical approaches with separation-of-function mutagenesis in mice to show that, rather than stabilizing the SYCP1 lattice, the CE protein SYCE3 actively remodels this structure during synapsis. We find that SYCP1 tetramers undergo conformational change into 2:1 heterotrimers on SYCE3 binding, removing their assembly interfaces and disrupting the SYCP1 lattice. SYCE3 then establishes a new lattice by its self-assembly mimicking the role of the disrupted interface in tethering together SYCP1 dimers. SYCE3 also interacts with CE complexes SYCE1-SIX6OS1 and SYCE2-TEX12, providing a mechanism for their recruitment. Thus, SYCE3 remodels the SYCP1 lattice into a CE-binding integrated SYCP1-SYCE3 lattice to achieve long-range synapsis by a mature SC.

Identifiants

pubmed: 36635604
doi: 10.1038/s41594-022-00909-1
pii: 10.1038/s41594-022-00909-1
pmc: PMC7614228
mid: EMS159613
doi:

Substances chimiques

Chromosomal Proteins, Non-Histone 0
DNA-Binding Proteins 0
Nuclear Proteins 0
SYCE2 protein, mouse 0
Sycp1 protein, mouse 0
Syce3 protein, mouse 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

188-199

Subventions

Organisme : Wellcome Trust
ID : 219413
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_00007/6
Pays : United Kingdom

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature America, Inc.

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Auteurs

James H Crichton (JH)

MRC Human Genetics Unit, MRC Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, UK.

James M Dunce (JM)

Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Newcastle upon Tyne, UK.
Department of Biochemistry, University of Cambridge, Cambridge, UK.

Orla M Dunne (OM)

Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Newcastle upon Tyne, UK.
Vienna BioCenter Core Facilities GmbH, Vienna, Austria.

Lucy J Salmon (LJ)

Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Newcastle upon Tyne, UK.

Paul S Devenney (PS)

MRC Human Genetics Unit, MRC Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, UK.

Jennifer Lawson (J)

MRC Human Genetics Unit, MRC Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, UK.

Ian R Adams (IR)

MRC Human Genetics Unit, MRC Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, UK. Ian.Adams@ed.ac.uk.

Owen R Davies (OR)

Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Newcastle upon Tyne, UK. Owen.Davies@ed.ac.uk.
Wellcome Centre for Cell Biology, Institute of Cell Biology, University of Edinburgh, Edinburgh, UK. Owen.Davies@ed.ac.uk.

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