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Unique properties of Drosophila spermatocyte primary cilia

The primary cilium is an essential organelle required for animal development and adult homeostasis that is found on most animal cells. The primary cilium contains a microtubule-based axoneme cytoskeleton that typically grows from the mother centriole in G0/G1 phase of the cell cycle as a membrane-bo...

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Autores principales: Riparbelli, Maria Giovanna, Cabrera, Oscar A., Callaini, Giuliano, Megraw, Timothy L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3828760/
https://www.ncbi.nlm.nih.gov/pubmed/24244850
http://dx.doi.org/10.1242/bio.20135355
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author Riparbelli, Maria Giovanna
Cabrera, Oscar A.
Callaini, Giuliano
Megraw, Timothy L.
author_facet Riparbelli, Maria Giovanna
Cabrera, Oscar A.
Callaini, Giuliano
Megraw, Timothy L.
author_sort Riparbelli, Maria Giovanna
collection PubMed
description The primary cilium is an essential organelle required for animal development and adult homeostasis that is found on most animal cells. The primary cilium contains a microtubule-based axoneme cytoskeleton that typically grows from the mother centriole in G0/G1 phase of the cell cycle as a membrane-bound compartment that protrudes from the cell surface. A unique system of bidirectional transport, intraflagellar transport (IFT), maintains the structure and function of cilia. While the axoneme is dynamic, growing and shrinking at its tip, at the same time it is very stable to the effects of microtubule-targeting drugs. The primary cilia found on Drosophila spermatocytes diverge from the general rules of primary cilium biology in several respects. Among these unique attributes, spermatocyte cilia assemble from all four centrioles in an IFT-independent manner in G2 phase, and persist continuously through two cell divisions. Here, we show that Drosophila spermatocyte primary cilia are extremely sensitive to microtubule-targeting drugs, unlike their mammalian counterparts. Spermatocyte cilia and their axonemes fail to assemble or be maintained upon nocodazole treatment, while centriole replication appears unperturbed. On the other hand, paclitaxel (Taxol), a microtubule-stabilizing drug, disrupted transition zone assembly and anchoring to the plasma membrane while causing spermatocyte primary cilia to grow extensively long during the assembly/elongation phase, but did not overtly affect the centrioles. However, once assembled to their mature length, spermatocyte cilia appeared unaffected by Taxol. The effects of these drugs on axoneme dynamics further demonstrate that spermatocyte primary cilia are endowed with unique assembly properties.
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spelling pubmed-38287602013-11-15 Unique properties of Drosophila spermatocyte primary cilia Riparbelli, Maria Giovanna Cabrera, Oscar A. Callaini, Giuliano Megraw, Timothy L. Biol Open Research Article The primary cilium is an essential organelle required for animal development and adult homeostasis that is found on most animal cells. The primary cilium contains a microtubule-based axoneme cytoskeleton that typically grows from the mother centriole in G0/G1 phase of the cell cycle as a membrane-bound compartment that protrudes from the cell surface. A unique system of bidirectional transport, intraflagellar transport (IFT), maintains the structure and function of cilia. While the axoneme is dynamic, growing and shrinking at its tip, at the same time it is very stable to the effects of microtubule-targeting drugs. The primary cilia found on Drosophila spermatocytes diverge from the general rules of primary cilium biology in several respects. Among these unique attributes, spermatocyte cilia assemble from all four centrioles in an IFT-independent manner in G2 phase, and persist continuously through two cell divisions. Here, we show that Drosophila spermatocyte primary cilia are extremely sensitive to microtubule-targeting drugs, unlike their mammalian counterparts. Spermatocyte cilia and their axonemes fail to assemble or be maintained upon nocodazole treatment, while centriole replication appears unperturbed. On the other hand, paclitaxel (Taxol), a microtubule-stabilizing drug, disrupted transition zone assembly and anchoring to the plasma membrane while causing spermatocyte primary cilia to grow extensively long during the assembly/elongation phase, but did not overtly affect the centrioles. However, once assembled to their mature length, spermatocyte cilia appeared unaffected by Taxol. The effects of these drugs on axoneme dynamics further demonstrate that spermatocyte primary cilia are endowed with unique assembly properties. The Company of Biologists 2013-09-11 /pmc/articles/PMC3828760/ /pubmed/24244850 http://dx.doi.org/10.1242/bio.20135355 Text en © 2013. Published by The Company of Biologists Ltd http://creativecommons.org/licenses/by/3.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Riparbelli, Maria Giovanna
Cabrera, Oscar A.
Callaini, Giuliano
Megraw, Timothy L.
Unique properties of Drosophila spermatocyte primary cilia
title Unique properties of Drosophila spermatocyte primary cilia
title_full Unique properties of Drosophila spermatocyte primary cilia
title_fullStr Unique properties of Drosophila spermatocyte primary cilia
title_full_unstemmed Unique properties of Drosophila spermatocyte primary cilia
title_short Unique properties of Drosophila spermatocyte primary cilia
title_sort unique properties of drosophila spermatocyte primary cilia
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3828760/
https://www.ncbi.nlm.nih.gov/pubmed/24244850
http://dx.doi.org/10.1242/bio.20135355
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