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Distinct dynein complexes defined by DYNLRB1 and DYNLRB2 regulate mitotic and male meiotic spindle bipolarity

Spindle formation in male meiosis relies on the canonical centrosome system, which is distinct from acentrosomal oocyte meiosis, but its specific regulatory mechanisms remain unknown. Herein, we report that DYNLRB2 (Dynein light chain roadblock-type-2) is a male meiosis-upregulated dynein light chai...

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Autores principales: He, Shuwen, Gillies, John P., Zang, Juliana L., Córdoba-Beldad, Carmen M., Yamamoto, Io, Fujiwara, Yasuhiro, Grantham, Julie, DeSantis, Morgan E., Shibuya, Hiroki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10042829/
https://www.ncbi.nlm.nih.gov/pubmed/36973253
http://dx.doi.org/10.1038/s41467-023-37370-7
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author He, Shuwen
Gillies, John P.
Zang, Juliana L.
Córdoba-Beldad, Carmen M.
Yamamoto, Io
Fujiwara, Yasuhiro
Grantham, Julie
DeSantis, Morgan E.
Shibuya, Hiroki
author_facet He, Shuwen
Gillies, John P.
Zang, Juliana L.
Córdoba-Beldad, Carmen M.
Yamamoto, Io
Fujiwara, Yasuhiro
Grantham, Julie
DeSantis, Morgan E.
Shibuya, Hiroki
author_sort He, Shuwen
collection PubMed
description Spindle formation in male meiosis relies on the canonical centrosome system, which is distinct from acentrosomal oocyte meiosis, but its specific regulatory mechanisms remain unknown. Herein, we report that DYNLRB2 (Dynein light chain roadblock-type-2) is a male meiosis-upregulated dynein light chain that is indispensable for spindle formation in meiosis I. In Dynlrb2 KO mouse testes, meiosis progression is arrested in metaphase I due to the formation of multipolar spindles with fragmented pericentriolar material (PCM). DYNLRB2 inhibits PCM fragmentation through two distinct pathways; suppressing premature centriole disengagement and targeting NuMA (nuclear mitotic apparatus) to spindle poles. The ubiquitously expressed mitotic counterpart, DYNLRB1, has similar roles in mitotic cells and maintains spindle bipolarity by targeting NuMA and suppressing centriole overduplication. Our work demonstrates that two distinct dynein complexes containing DYNLRB1 or DYNLRB2 are separately used in mitotic and meiotic spindle formations, respectively, and that both have NuMA as a common target.
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spelling pubmed-100428292023-03-29 Distinct dynein complexes defined by DYNLRB1 and DYNLRB2 regulate mitotic and male meiotic spindle bipolarity He, Shuwen Gillies, John P. Zang, Juliana L. Córdoba-Beldad, Carmen M. Yamamoto, Io Fujiwara, Yasuhiro Grantham, Julie DeSantis, Morgan E. Shibuya, Hiroki Nat Commun Article Spindle formation in male meiosis relies on the canonical centrosome system, which is distinct from acentrosomal oocyte meiosis, but its specific regulatory mechanisms remain unknown. Herein, we report that DYNLRB2 (Dynein light chain roadblock-type-2) is a male meiosis-upregulated dynein light chain that is indispensable for spindle formation in meiosis I. In Dynlrb2 KO mouse testes, meiosis progression is arrested in metaphase I due to the formation of multipolar spindles with fragmented pericentriolar material (PCM). DYNLRB2 inhibits PCM fragmentation through two distinct pathways; suppressing premature centriole disengagement and targeting NuMA (nuclear mitotic apparatus) to spindle poles. The ubiquitously expressed mitotic counterpart, DYNLRB1, has similar roles in mitotic cells and maintains spindle bipolarity by targeting NuMA and suppressing centriole overduplication. Our work demonstrates that two distinct dynein complexes containing DYNLRB1 or DYNLRB2 are separately used in mitotic and meiotic spindle formations, respectively, and that both have NuMA as a common target. Nature Publishing Group UK 2023-03-27 /pmc/articles/PMC10042829/ /pubmed/36973253 http://dx.doi.org/10.1038/s41467-023-37370-7 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
He, Shuwen
Gillies, John P.
Zang, Juliana L.
Córdoba-Beldad, Carmen M.
Yamamoto, Io
Fujiwara, Yasuhiro
Grantham, Julie
DeSantis, Morgan E.
Shibuya, Hiroki
Distinct dynein complexes defined by DYNLRB1 and DYNLRB2 regulate mitotic and male meiotic spindle bipolarity
title Distinct dynein complexes defined by DYNLRB1 and DYNLRB2 regulate mitotic and male meiotic spindle bipolarity
title_full Distinct dynein complexes defined by DYNLRB1 and DYNLRB2 regulate mitotic and male meiotic spindle bipolarity
title_fullStr Distinct dynein complexes defined by DYNLRB1 and DYNLRB2 regulate mitotic and male meiotic spindle bipolarity
title_full_unstemmed Distinct dynein complexes defined by DYNLRB1 and DYNLRB2 regulate mitotic and male meiotic spindle bipolarity
title_short Distinct dynein complexes defined by DYNLRB1 and DYNLRB2 regulate mitotic and male meiotic spindle bipolarity
title_sort distinct dynein complexes defined by dynlrb1 and dynlrb2 regulate mitotic and male meiotic spindle bipolarity
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10042829/
https://www.ncbi.nlm.nih.gov/pubmed/36973253
http://dx.doi.org/10.1038/s41467-023-37370-7
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