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Orbit/CLASP determines centriole length by antagonising Klp10A in Drosophila spermatocytes

After centrosome duplication, centrioles elongate before M phase. To identify genes required for this process and to understand the regulatory mechanism, we investigated the centrioles in Drosophila premeiotic spermatocytes expressing fluorescently tagged centriolar proteins. We demonstrated that an...

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Autores principales: Shoda, Tsuyoshi, Yamazoe, Kanta, Tanaka, Yuri, Asano, Yuki, Inoue, Yoshihiro H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8015252/
https://www.ncbi.nlm.nih.gov/pubmed/33674447
http://dx.doi.org/10.1242/jcs.251231
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author Shoda, Tsuyoshi
Yamazoe, Kanta
Tanaka, Yuri
Asano, Yuki
Inoue, Yoshihiro H.
author_facet Shoda, Tsuyoshi
Yamazoe, Kanta
Tanaka, Yuri
Asano, Yuki
Inoue, Yoshihiro H.
author_sort Shoda, Tsuyoshi
collection PubMed
description After centrosome duplication, centrioles elongate before M phase. To identify genes required for this process and to understand the regulatory mechanism, we investigated the centrioles in Drosophila premeiotic spermatocytes expressing fluorescently tagged centriolar proteins. We demonstrated that an essential microtubule polymerisation factor, Orbit (the Drosophila CLASP orthologue, encoded by chb), accumulated at the distal end of centrioles and was required for the elongation. Conversely, a microtubule-severing factor, Klp10A, shortened the centrioles. Genetic analyses revealed that these two proteins functioned antagonistically to determine centriole length. Furthermore, Cp110 in the distal tip complex was closely associated with the factors involved in centriolar dynamics at the distal end. We observed loss of centriole integrity, including fragmentation of centrioles and earlier separation of the centriole pairs, in Cp110-null mutant cells either overexpressing Orbit or depleted of Klp10A. Excess centriole elongation in the absence of the distal tip complex resulted in the loss of centriole integrity, leading to the formation of multipolar spindle microtubules emanating from centriole fragments, even when they were unpaired. Our findings contribute to understanding the mechanism of centriole integrity, disruption of which leads to chromosome instability in cancer cells.
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spelling pubmed-80152522021-04-07 Orbit/CLASP determines centriole length by antagonising Klp10A in Drosophila spermatocytes Shoda, Tsuyoshi Yamazoe, Kanta Tanaka, Yuri Asano, Yuki Inoue, Yoshihiro H. J Cell Sci Research Article After centrosome duplication, centrioles elongate before M phase. To identify genes required for this process and to understand the regulatory mechanism, we investigated the centrioles in Drosophila premeiotic spermatocytes expressing fluorescently tagged centriolar proteins. We demonstrated that an essential microtubule polymerisation factor, Orbit (the Drosophila CLASP orthologue, encoded by chb), accumulated at the distal end of centrioles and was required for the elongation. Conversely, a microtubule-severing factor, Klp10A, shortened the centrioles. Genetic analyses revealed that these two proteins functioned antagonistically to determine centriole length. Furthermore, Cp110 in the distal tip complex was closely associated with the factors involved in centriolar dynamics at the distal end. We observed loss of centriole integrity, including fragmentation of centrioles and earlier separation of the centriole pairs, in Cp110-null mutant cells either overexpressing Orbit or depleted of Klp10A. Excess centriole elongation in the absence of the distal tip complex resulted in the loss of centriole integrity, leading to the formation of multipolar spindle microtubules emanating from centriole fragments, even when they were unpaired. Our findings contribute to understanding the mechanism of centriole integrity, disruption of which leads to chromosome instability in cancer cells. The Company of Biologists Ltd 2021-03-26 /pmc/articles/PMC8015252/ /pubmed/33674447 http://dx.doi.org/10.1242/jcs.251231 Text en © 2021. Published by The Company of Biologists Ltd http://creativecommons.org/licenses/by/4.0This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Shoda, Tsuyoshi
Yamazoe, Kanta
Tanaka, Yuri
Asano, Yuki
Inoue, Yoshihiro H.
Orbit/CLASP determines centriole length by antagonising Klp10A in Drosophila spermatocytes
title Orbit/CLASP determines centriole length by antagonising Klp10A in Drosophila spermatocytes
title_full Orbit/CLASP determines centriole length by antagonising Klp10A in Drosophila spermatocytes
title_fullStr Orbit/CLASP determines centriole length by antagonising Klp10A in Drosophila spermatocytes
title_full_unstemmed Orbit/CLASP determines centriole length by antagonising Klp10A in Drosophila spermatocytes
title_short Orbit/CLASP determines centriole length by antagonising Klp10A in Drosophila spermatocytes
title_sort orbit/clasp determines centriole length by antagonising klp10a in drosophila spermatocytes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8015252/
https://www.ncbi.nlm.nih.gov/pubmed/33674447
http://dx.doi.org/10.1242/jcs.251231
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