Orbit/CLASP is required for germline cyst formation through its developmental control of fusomes and ring canals in Drosophila males.

Orbit, a Drosophila ortholog of microtubule plus-end enriched protein CLASP, plays an important role in many developmental processes involved in microtubule dynamics. Previous studies have shown that Orbit is required for asymmetric stem cell division and cystocyte divisions in germline cysts and fo...

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Autores principales:	Chie Miyauchi, Daishi Kitazawa, Itaru Ando, Daisuke Hayashi, Yoshihiro H Inoue
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2013
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/9afda57da25e4fa7bf2f625708493660
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spelling	oai:doaj.org-article:9afda57da25e4fa7bf2f6257084936602021-11-18T07:54:11ZOrbit/CLASP is required for germline cyst formation through its developmental control of fusomes and ring canals in Drosophila males.1932-620310.1371/journal.pone.0058220https://doaj.org/article/9afda57da25e4fa7bf2f6257084936602013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23520495/?tool=EBIhttps://doaj.org/toc/1932-6203Orbit, a Drosophila ortholog of microtubule plus-end enriched protein CLASP, plays an important role in many developmental processes involved in microtubule dynamics. Previous studies have shown that Orbit is required for asymmetric stem cell division and cystocyte divisions in germline cysts and for the development of microtubule networks that interconnect oocyte and nurse cells during oogenesis. Here, we examined the cellular localization of Orbit and its role in cyst formation during spermatogenesis. In male germline stem cells, distinct localization of Orbit was first observed on the spectrosome, which is a spherical precursor of the germline-specific cytoskeleton known as the fusome. In dividing stem cells and spermatogonia, Orbit was localized around centrosomes and on kinetochores and spindle microtubules. After cytokinesis, Orbit remained localized on ring canals, which are cytoplasmic bridges between the cells. Thereafter, it was found along fusomes, extending through the ring canal toward all spermatogonia in a cyst. Fusome localization of Orbit was not affected by microtubule depolymerization. Instead, our fluorescence resonance energy transfer experiments suggested that Orbit is closely associated with F-actin, which is abundantly found in fusomes. Surprisingly, F-actin depolymerization influenced neither fusome organization nor Orbit localization on the germline-specific cytoskeleton. We revealed that two conserved regions of Orbit are required for fusome localization. Using orbit hypomorphic mutants, we showed that the protein is required for ring canal formation and for fusome elongation mediated by the interaction of newly generated fusome plugs with the pre-existing fusome. The orbit mutation also disrupted ring canal clustering, which is essential for folding of the spermatogonia after cytokinesis. Orbit accumulates around centrosomes at the onset of spermatogonial mitosis and is required for the capture of one of the duplicated centrosomes onto the fusome. Moreover, Orbit is involved in the proper orientation of spindles towards fusomes during synchronous mitosis of spermatogonial cysts.Chie MiyauchiDaishi KitazawaItaru AndoDaisuke HayashiYoshihiro H InouePublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 8, Iss 3, p e58220 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Chie Miyauchi Daishi Kitazawa Itaru Ando Daisuke Hayashi Yoshihiro H Inoue Orbit/CLASP is required for germline cyst formation through its developmental control of fusomes and ring canals in Drosophila males.
description	Orbit, a Drosophila ortholog of microtubule plus-end enriched protein CLASP, plays an important role in many developmental processes involved in microtubule dynamics. Previous studies have shown that Orbit is required for asymmetric stem cell division and cystocyte divisions in germline cysts and for the development of microtubule networks that interconnect oocyte and nurse cells during oogenesis. Here, we examined the cellular localization of Orbit and its role in cyst formation during spermatogenesis. In male germline stem cells, distinct localization of Orbit was first observed on the spectrosome, which is a spherical precursor of the germline-specific cytoskeleton known as the fusome. In dividing stem cells and spermatogonia, Orbit was localized around centrosomes and on kinetochores and spindle microtubules. After cytokinesis, Orbit remained localized on ring canals, which are cytoplasmic bridges between the cells. Thereafter, it was found along fusomes, extending through the ring canal toward all spermatogonia in a cyst. Fusome localization of Orbit was not affected by microtubule depolymerization. Instead, our fluorescence resonance energy transfer experiments suggested that Orbit is closely associated with F-actin, which is abundantly found in fusomes. Surprisingly, F-actin depolymerization influenced neither fusome organization nor Orbit localization on the germline-specific cytoskeleton. We revealed that two conserved regions of Orbit are required for fusome localization. Using orbit hypomorphic mutants, we showed that the protein is required for ring canal formation and for fusome elongation mediated by the interaction of newly generated fusome plugs with the pre-existing fusome. The orbit mutation also disrupted ring canal clustering, which is essential for folding of the spermatogonia after cytokinesis. Orbit accumulates around centrosomes at the onset of spermatogonial mitosis and is required for the capture of one of the duplicated centrosomes onto the fusome. Moreover, Orbit is involved in the proper orientation of spindles towards fusomes during synchronous mitosis of spermatogonial cysts.
format	article
author	Chie Miyauchi Daishi Kitazawa Itaru Ando Daisuke Hayashi Yoshihiro H Inoue
author_facet	Chie Miyauchi Daishi Kitazawa Itaru Ando Daisuke Hayashi Yoshihiro H Inoue
author_sort	Chie Miyauchi
title	Orbit/CLASP is required for germline cyst formation through its developmental control of fusomes and ring canals in Drosophila males.
title_short	Orbit/CLASP is required for germline cyst formation through its developmental control of fusomes and ring canals in Drosophila males.
title_full	Orbit/CLASP is required for germline cyst formation through its developmental control of fusomes and ring canals in Drosophila males.
title_fullStr	Orbit/CLASP is required for germline cyst formation through its developmental control of fusomes and ring canals in Drosophila males.
title_full_unstemmed	Orbit/CLASP is required for germline cyst formation through its developmental control of fusomes and ring canals in Drosophila males.
title_sort	orbit/clasp is required for germline cyst formation through its developmental control of fusomes and ring canals in drosophila males.
publisher	Public Library of Science (PLoS)
publishDate	2013
url	https://doaj.org/article/9afda57da25e4fa7bf2f625708493660
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Orbit/CLASP is required for germline cyst formation through its developmental control of fusomes and ring canals in Drosophila males.

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