Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes

Autores
Bisig, Carlos Gaston; Guiraldelli, Michel F.; Kouznetsova, Anna; Scherthan, Harry; Höög, Christer; Dawson, Dean S.; Pezza, Roberto J.
Año de publicación
2012
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Recent studies in simple model organisms have shown that centromere pairing is important for ensuring high-fidelity meiotic chromosome segregation. However, this process and the mechanisms regulating it in higher eukaryotes are unknown. Here we present the first detailed study of meiotic centromere pairing in mouse spermatogenesis and link it with key events of the G2/metaphase I transition. In mouse we observed no evidence of the persistent coupling of centromeres that has been observed in several model organisms. We do however find that telomeres associate in non-homologous pairs or small groups in B type spermatogonia and pre-leptotene spermatocytes, and this association is disrupted by deletion of the synaptonemal complex component SYCP3. Intriguingly, we found that, in mid prophase, chromosome synapsis is not initiated at centromeres, and centromeric regions are the last to pair in the zygotene-pachytene transition. In late prophase, we first identified the proteins that reside at paired centromeres. We found that components of the central and lateral element and transverse filaments of the synaptonemal complex are retained at paired centromeres after disassembly of the synaptonemal complex along diplotene chromosome arms. The absence of SYCP1 prevents centromere pairing in knockout mouse spermatocytes. The localization dynamics of SYCP1 and SYCP3 suggest that they play different roles in promoting homologous centromere pairing. SYCP1 remains only at paired centromeres coincident with the time at which some kinetochore proteins begin loading at centromeres, consistent with a role in assembly of meiosis-specific kinetochores. After removal of SYCP1 from centromeres, SYCP3 then accumulates at paired centromeres where it may promote bi-orientation of homologous centromeres. We propose that, in addition to their roles as synaptonemal complex components, SYCP1 and SYCP3 act at the centromeres to promote the establishment and/or maintenance of centromere pairing and, by doing so, improve the segregation fidelity of mammalian meiotic chromosomes.
Fil: Bisig, Carlos Gaston. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Centro de Investigaciones en Química Biológica de Córdoba. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Centro de Investigaciones en Química Biológica de Córdoba; Argentina
Fil: Guiraldelli, Michel F.. Oklahoma Medical Research Foundation; Estados Unidos
Fil: Kouznetsova, Anna. Karolinska Institute; Suecia
Fil: Scherthan, Harry. Universitat Ulm; Alemania
Fil: Höög, Christer. Karolinska Institutet. Department of Cell and Molecular Biology; Suecia
Fil: Dawson, Dean S.. Oklahoma Medical Research Foundation; Estados Unidos. Oklahoma State University; Estados Unidos
Fil: Pezza, Roberto J.. Oklahoma Medical Research Foundation; Estados Unidos. Oklahoma State University; Estados Unidos
Materia
Synaptonemal Complex
Homologous Centromere Pairing
Spermatocytes
Tubulin
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/229572

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oai_identifier_str oai:ri.conicet.gov.ar:11336/229572
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytesBisig, Carlos GastonGuiraldelli, Michel F.Kouznetsova, AnnaScherthan, HarryHöög, ChristerDawson, Dean S.Pezza, Roberto J.Synaptonemal ComplexHomologous Centromere PairingSpermatocytesTubulinhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Recent studies in simple model organisms have shown that centromere pairing is important for ensuring high-fidelity meiotic chromosome segregation. However, this process and the mechanisms regulating it in higher eukaryotes are unknown. Here we present the first detailed study of meiotic centromere pairing in mouse spermatogenesis and link it with key events of the G2/metaphase I transition. In mouse we observed no evidence of the persistent coupling of centromeres that has been observed in several model organisms. We do however find that telomeres associate in non-homologous pairs or small groups in B type spermatogonia and pre-leptotene spermatocytes, and this association is disrupted by deletion of the synaptonemal complex component SYCP3. Intriguingly, we found that, in mid prophase, chromosome synapsis is not initiated at centromeres, and centromeric regions are the last to pair in the zygotene-pachytene transition. In late prophase, we first identified the proteins that reside at paired centromeres. We found that components of the central and lateral element and transverse filaments of the synaptonemal complex are retained at paired centromeres after disassembly of the synaptonemal complex along diplotene chromosome arms. The absence of SYCP1 prevents centromere pairing in knockout mouse spermatocytes. The localization dynamics of SYCP1 and SYCP3 suggest that they play different roles in promoting homologous centromere pairing. SYCP1 remains only at paired centromeres coincident with the time at which some kinetochore proteins begin loading at centromeres, consistent with a role in assembly of meiosis-specific kinetochores. After removal of SYCP1 from centromeres, SYCP3 then accumulates at paired centromeres where it may promote bi-orientation of homologous centromeres. We propose that, in addition to their roles as synaptonemal complex components, SYCP1 and SYCP3 act at the centromeres to promote the establishment and/or maintenance of centromere pairing and, by doing so, improve the segregation fidelity of mammalian meiotic chromosomes.Fil: Bisig, Carlos Gaston. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Centro de Investigaciones en Química Biológica de Córdoba. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Centro de Investigaciones en Química Biológica de Córdoba; ArgentinaFil: Guiraldelli, Michel F.. Oklahoma Medical Research Foundation; Estados UnidosFil: Kouznetsova, Anna. Karolinska Institute; SueciaFil: Scherthan, Harry. Universitat Ulm; AlemaniaFil: Höög, Christer. Karolinska Institutet. Department of Cell and Molecular Biology; SueciaFil: Dawson, Dean S.. Oklahoma Medical Research Foundation; Estados Unidos. Oklahoma State University; Estados UnidosFil: Pezza, Roberto J.. Oklahoma Medical Research Foundation; Estados Unidos. Oklahoma State University; Estados UnidosPublic Library of Science2012-06-28info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/229572Bisig, Carlos Gaston; Guiraldelli, Michel F.; Kouznetsova, Anna; Scherthan, Harry; Höög, Christer; et al.; Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes; Public Library of Science; Plos Genetics; 8; 6; 28-6-2012; 1-131553-73901553-7404CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1002701info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pgen.1002701info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:36:11Zoai:ri.conicet.gov.ar:11336/229572instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:36:12.14CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes
title Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes
spellingShingle Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes
Bisig, Carlos Gaston
Synaptonemal Complex
Homologous Centromere Pairing
Spermatocytes
Tubulin
title_short Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes
title_full Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes
title_fullStr Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes
title_full_unstemmed Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes
title_sort Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes
dc.creator.none.fl_str_mv Bisig, Carlos Gaston
Guiraldelli, Michel F.
Kouznetsova, Anna
Scherthan, Harry
Höög, Christer
Dawson, Dean S.
Pezza, Roberto J.
author Bisig, Carlos Gaston
author_facet Bisig, Carlos Gaston
Guiraldelli, Michel F.
Kouznetsova, Anna
Scherthan, Harry
Höög, Christer
Dawson, Dean S.
Pezza, Roberto J.
author_role author
author2 Guiraldelli, Michel F.
Kouznetsova, Anna
Scherthan, Harry
Höög, Christer
Dawson, Dean S.
Pezza, Roberto J.
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv Synaptonemal Complex
Homologous Centromere Pairing
Spermatocytes
Tubulin
topic Synaptonemal Complex
Homologous Centromere Pairing
Spermatocytes
Tubulin
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Recent studies in simple model organisms have shown that centromere pairing is important for ensuring high-fidelity meiotic chromosome segregation. However, this process and the mechanisms regulating it in higher eukaryotes are unknown. Here we present the first detailed study of meiotic centromere pairing in mouse spermatogenesis and link it with key events of the G2/metaphase I transition. In mouse we observed no evidence of the persistent coupling of centromeres that has been observed in several model organisms. We do however find that telomeres associate in non-homologous pairs or small groups in B type spermatogonia and pre-leptotene spermatocytes, and this association is disrupted by deletion of the synaptonemal complex component SYCP3. Intriguingly, we found that, in mid prophase, chromosome synapsis is not initiated at centromeres, and centromeric regions are the last to pair in the zygotene-pachytene transition. In late prophase, we first identified the proteins that reside at paired centromeres. We found that components of the central and lateral element and transverse filaments of the synaptonemal complex are retained at paired centromeres after disassembly of the synaptonemal complex along diplotene chromosome arms. The absence of SYCP1 prevents centromere pairing in knockout mouse spermatocytes. The localization dynamics of SYCP1 and SYCP3 suggest that they play different roles in promoting homologous centromere pairing. SYCP1 remains only at paired centromeres coincident with the time at which some kinetochore proteins begin loading at centromeres, consistent with a role in assembly of meiosis-specific kinetochores. After removal of SYCP1 from centromeres, SYCP3 then accumulates at paired centromeres where it may promote bi-orientation of homologous centromeres. We propose that, in addition to their roles as synaptonemal complex components, SYCP1 and SYCP3 act at the centromeres to promote the establishment and/or maintenance of centromere pairing and, by doing so, improve the segregation fidelity of mammalian meiotic chromosomes.
Fil: Bisig, Carlos Gaston. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Centro de Investigaciones en Química Biológica de Córdoba. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Centro de Investigaciones en Química Biológica de Córdoba; Argentina
Fil: Guiraldelli, Michel F.. Oklahoma Medical Research Foundation; Estados Unidos
Fil: Kouznetsova, Anna. Karolinska Institute; Suecia
Fil: Scherthan, Harry. Universitat Ulm; Alemania
Fil: Höög, Christer. Karolinska Institutet. Department of Cell and Molecular Biology; Suecia
Fil: Dawson, Dean S.. Oklahoma Medical Research Foundation; Estados Unidos. Oklahoma State University; Estados Unidos
Fil: Pezza, Roberto J.. Oklahoma Medical Research Foundation; Estados Unidos. Oklahoma State University; Estados Unidos
description Recent studies in simple model organisms have shown that centromere pairing is important for ensuring high-fidelity meiotic chromosome segregation. However, this process and the mechanisms regulating it in higher eukaryotes are unknown. Here we present the first detailed study of meiotic centromere pairing in mouse spermatogenesis and link it with key events of the G2/metaphase I transition. In mouse we observed no evidence of the persistent coupling of centromeres that has been observed in several model organisms. We do however find that telomeres associate in non-homologous pairs or small groups in B type spermatogonia and pre-leptotene spermatocytes, and this association is disrupted by deletion of the synaptonemal complex component SYCP3. Intriguingly, we found that, in mid prophase, chromosome synapsis is not initiated at centromeres, and centromeric regions are the last to pair in the zygotene-pachytene transition. In late prophase, we first identified the proteins that reside at paired centromeres. We found that components of the central and lateral element and transverse filaments of the synaptonemal complex are retained at paired centromeres after disassembly of the synaptonemal complex along diplotene chromosome arms. The absence of SYCP1 prevents centromere pairing in knockout mouse spermatocytes. The localization dynamics of SYCP1 and SYCP3 suggest that they play different roles in promoting homologous centromere pairing. SYCP1 remains only at paired centromeres coincident with the time at which some kinetochore proteins begin loading at centromeres, consistent with a role in assembly of meiosis-specific kinetochores. After removal of SYCP1 from centromeres, SYCP3 then accumulates at paired centromeres where it may promote bi-orientation of homologous centromeres. We propose that, in addition to their roles as synaptonemal complex components, SYCP1 and SYCP3 act at the centromeres to promote the establishment and/or maintenance of centromere pairing and, by doing so, improve the segregation fidelity of mammalian meiotic chromosomes.
publishDate 2012
dc.date.none.fl_str_mv 2012-06-28
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/229572
Bisig, Carlos Gaston; Guiraldelli, Michel F.; Kouznetsova, Anna; Scherthan, Harry; Höög, Christer; et al.; Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes; Public Library of Science; Plos Genetics; 8; 6; 28-6-2012; 1-13
1553-7390
1553-7404
CONICET Digital
CONICET
url http://hdl.handle.net/11336/229572
identifier_str_mv Bisig, Carlos Gaston; Guiraldelli, Michel F.; Kouznetsova, Anna; Scherthan, Harry; Höög, Christer; et al.; Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes; Public Library of Science; Plos Genetics; 8; 6; 28-6-2012; 1-13
1553-7390
1553-7404
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1002701
info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pgen.1002701
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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