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Three-Dimensional Genomic Structure and Cohesin Occupancy Correlate with Transcriptional Activity during Spermatogenesis

Mammalian gametogenesis involves dramatic and tightly regulated chromatin remodeling, whose regulatory pathways remain largely unexplored. Here, we generate a comprehensive high-resolution structural and functional atlas of mouse spermatogenesis by combining in situ chromosome conformation capture s...

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Autores principales: Vara, Covadonga, Paytuví-Gallart, Andreu, Cuartero, Yasmina, Le Dily, François, Garcia, Francisca, Salvà-Castro, Judit, Gómez-H, Laura, Julià, Eva, Moutinho, Catia, Aiese Cigliano, Riccardo, Sanseverino, Walter, Fornas, Oscar, Pendás, Alberto M., Heyn, Holger, Waters, Paul D., Marti-Renom, Marc A., Ruiz-Herrera, Aurora
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6635386/
https://www.ncbi.nlm.nih.gov/pubmed/31291573
http://dx.doi.org/10.1016/j.celrep.2019.06.037
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author Vara, Covadonga
Paytuví-Gallart, Andreu
Cuartero, Yasmina
Le Dily, François
Garcia, Francisca
Salvà-Castro, Judit
Gómez-H, Laura
Julià, Eva
Moutinho, Catia
Aiese Cigliano, Riccardo
Sanseverino, Walter
Fornas, Oscar
Pendás, Alberto M.
Heyn, Holger
Waters, Paul D.
Marti-Renom, Marc A.
Ruiz-Herrera, Aurora
author_facet Vara, Covadonga
Paytuví-Gallart, Andreu
Cuartero, Yasmina
Le Dily, François
Garcia, Francisca
Salvà-Castro, Judit
Gómez-H, Laura
Julià, Eva
Moutinho, Catia
Aiese Cigliano, Riccardo
Sanseverino, Walter
Fornas, Oscar
Pendás, Alberto M.
Heyn, Holger
Waters, Paul D.
Marti-Renom, Marc A.
Ruiz-Herrera, Aurora
author_sort Vara, Covadonga
collection PubMed
description Mammalian gametogenesis involves dramatic and tightly regulated chromatin remodeling, whose regulatory pathways remain largely unexplored. Here, we generate a comprehensive high-resolution structural and functional atlas of mouse spermatogenesis by combining in situ chromosome conformation capture sequencing (Hi-C), RNA sequencing (RNA-seq), and chromatin immunoprecipitation sequencing (ChIP-seq) of CCCTC-binding factor (CTCF) and meiotic cohesins, coupled with confocal and super-resolution microscopy. Spermatogonia presents well-defined compartment patterns and topological domains. However, chromosome occupancy and compartmentalization are highly re-arranged during prophase I, with cohesins bound to active promoters in DNA loops out of the chromosomal axes. Compartment patterns re-emerge in round spermatids, where cohesin occupancy correlates with transcriptional activity of key developmental genes. The compact sperm genome contains compartments with actively transcribed genes but no fine-scale topological domains, concomitant with the presence of protamines. Overall, we demonstrate how genome-wide cohesin occupancy and transcriptional activity is associated with three-dimensional (3D) remodeling during spermatogenesis, ultimately reprogramming the genome for the next generation.
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spelling pubmed-66353862019-07-25 Three-Dimensional Genomic Structure and Cohesin Occupancy Correlate with Transcriptional Activity during Spermatogenesis Vara, Covadonga Paytuví-Gallart, Andreu Cuartero, Yasmina Le Dily, François Garcia, Francisca Salvà-Castro, Judit Gómez-H, Laura Julià, Eva Moutinho, Catia Aiese Cigliano, Riccardo Sanseverino, Walter Fornas, Oscar Pendás, Alberto M. Heyn, Holger Waters, Paul D. Marti-Renom, Marc A. Ruiz-Herrera, Aurora Cell Rep Article Mammalian gametogenesis involves dramatic and tightly regulated chromatin remodeling, whose regulatory pathways remain largely unexplored. Here, we generate a comprehensive high-resolution structural and functional atlas of mouse spermatogenesis by combining in situ chromosome conformation capture sequencing (Hi-C), RNA sequencing (RNA-seq), and chromatin immunoprecipitation sequencing (ChIP-seq) of CCCTC-binding factor (CTCF) and meiotic cohesins, coupled with confocal and super-resolution microscopy. Spermatogonia presents well-defined compartment patterns and topological domains. However, chromosome occupancy and compartmentalization are highly re-arranged during prophase I, with cohesins bound to active promoters in DNA loops out of the chromosomal axes. Compartment patterns re-emerge in round spermatids, where cohesin occupancy correlates with transcriptional activity of key developmental genes. The compact sperm genome contains compartments with actively transcribed genes but no fine-scale topological domains, concomitant with the presence of protamines. Overall, we demonstrate how genome-wide cohesin occupancy and transcriptional activity is associated with three-dimensional (3D) remodeling during spermatogenesis, ultimately reprogramming the genome for the next generation. Cell Press 2019-07-09 /pmc/articles/PMC6635386/ /pubmed/31291573 http://dx.doi.org/10.1016/j.celrep.2019.06.037 Text en © 2019 The Author(s) http://creativecommons.org/licenses/by/4.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Vara, Covadonga
Paytuví-Gallart, Andreu
Cuartero, Yasmina
Le Dily, François
Garcia, Francisca
Salvà-Castro, Judit
Gómez-H, Laura
Julià, Eva
Moutinho, Catia
Aiese Cigliano, Riccardo
Sanseverino, Walter
Fornas, Oscar
Pendás, Alberto M.
Heyn, Holger
Waters, Paul D.
Marti-Renom, Marc A.
Ruiz-Herrera, Aurora
Three-Dimensional Genomic Structure and Cohesin Occupancy Correlate with Transcriptional Activity during Spermatogenesis
title Three-Dimensional Genomic Structure and Cohesin Occupancy Correlate with Transcriptional Activity during Spermatogenesis
title_full Three-Dimensional Genomic Structure and Cohesin Occupancy Correlate with Transcriptional Activity during Spermatogenesis
title_fullStr Three-Dimensional Genomic Structure and Cohesin Occupancy Correlate with Transcriptional Activity during Spermatogenesis
title_full_unstemmed Three-Dimensional Genomic Structure and Cohesin Occupancy Correlate with Transcriptional Activity during Spermatogenesis
title_short Three-Dimensional Genomic Structure and Cohesin Occupancy Correlate with Transcriptional Activity during Spermatogenesis
title_sort three-dimensional genomic structure and cohesin occupancy correlate with transcriptional activity during spermatogenesis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6635386/
https://www.ncbi.nlm.nih.gov/pubmed/31291573
http://dx.doi.org/10.1016/j.celrep.2019.06.037
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