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Mouse ANKRD31 Regulates Spatiotemporal Patterning of Meiotic Recombination Initiation and Ensures Recombination between X and Y Sex Chromosomes

F. Papanikos, JAJ. Clément, E. Testa, R. Ravindranathan, C. Grey, I. Dereli, A. Bondarieva, S. Valerio-Cabrera, M. Stanzione, A. Schleiffer, P. Jansa, D. Lustyk, JF. Fei, IR. Adams, J. Forejt, M. Barchi, B. de Massy, A. Toth,

. 2019 ; 74 (5) : 1069-1085.e11. [pub] 20190415

Jazyk angličtina Země Spojené státy americké

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/bmc19044872

Orderly segregation of chromosomes during meiosis requires that crossovers form between homologous chromosomes by recombination. Programmed DNA double-strand breaks (DSBs) initiate meiotic recombination. We identify ANKRD31 as a key component of complexes of DSB-promoting proteins that assemble on meiotic chromosome axes. Genome-wide, ANKRD31 deficiency causes delayed recombination initiation. In addition, loss of ANKRD31 alters DSB distribution because of reduced selectivity for sites that normally attract DSBs. Strikingly, ANKRD31 deficiency also abolishes uniquely high rates of recombination that normally characterize pseudoautosomal regions (PARs) of X and Y chromosomes. Consequently, sex chromosomes do not form crossovers, leading to chromosome segregation failure in ANKRD31-deficient spermatocytes. These defects co-occur with a genome-wide delay in assembling DSB-promoting proteins on autosome axes and loss of a specialized PAR-axis domain that is highly enriched for DSB-promoting proteins in wild type. Thus, we propose a model for spatiotemporal patterning of recombination by ANKRD31-dependent control of axis-associated DSB-promoting proteins.

Citace poskytuje Crossref.org

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$a Orderly segregation of chromosomes during meiosis requires that crossovers form between homologous chromosomes by recombination. Programmed DNA double-strand breaks (DSBs) initiate meiotic recombination. We identify ANKRD31 as a key component of complexes of DSB-promoting proteins that assemble on meiotic chromosome axes. Genome-wide, ANKRD31 deficiency causes delayed recombination initiation. In addition, loss of ANKRD31 alters DSB distribution because of reduced selectivity for sites that normally attract DSBs. Strikingly, ANKRD31 deficiency also abolishes uniquely high rates of recombination that normally characterize pseudoautosomal regions (PARs) of X and Y chromosomes. Consequently, sex chromosomes do not form crossovers, leading to chromosome segregation failure in ANKRD31-deficient spermatocytes. These defects co-occur with a genome-wide delay in assembling DSB-promoting proteins on autosome axes and loss of a specialized PAR-axis domain that is highly enriched for DSB-promoting proteins in wild type. Thus, we propose a model for spatiotemporal patterning of recombination by ANKRD31-dependent control of axis-associated DSB-promoting proteins.
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$a Schleiffer, Alexander $u Research Institute of Molecular Pathology (IMP), Campus Vienna BioCenter 1, Vienna BioCenter (VBC), 1030 Vienna, Austria; Institute of Molecular Biotechnology (IMBA), Dr. Bohr-Gasse 3, Vienna BioCenter (VBC), 1030 Vienna, Austria.
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$a Jansa, Petr $u Institute of Molecular Genetics, Division BIOCEV, Prumyslova 595, 25250 Vestec, Czech Republic.
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$a Fei, Ji-Feng $u Institute for Brain Research and Rehabilitation, South China Normal University, 510631 Guangzhou, China.
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$a Forejt, Jiri $u Institute of Molecular Genetics, Division BIOCEV, Prumyslova 595, 25250 Vestec, Czech Republic.
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$a Barchi, Marco $u Department of Biomedicine and Prevention, Faculty of Medicine, University of Rome Tor Vergata, Via Montpellier n.1, 00133 Rome, Italy.
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$a de Massy, Bernard $u Institute of Human Genetics, UMR 9002, CNRS, Université de Montpellier, 34396 Montpellier Cedex 5, France. Electronic address: bernard.de-massy@igh.cnrs.fr.
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$a Toth, Attila $u Institute of Physiological Chemistry, Faculty of Medicine, Technische Universität Dresden, Fetscherstraße 74, 01307 Dresden, Germany. Electronic address: attila.toth@mailbox.tu-dresden.de.
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