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
- Institución
- Consejo Nacional de Investigaciones Científicas y Técnicas
- OAI Identificador
- oai:ri.conicet.gov.ar:11336/229572
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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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1844613132895387648 |
score |
13.070432 |