Rbp4-Gal4, a germline driver that activates in meiosis, reveals functions for VCP in spermatid development
Valosin-containing protein (VCP) is a versatile and ubiquitously expressed AAA+ ATPase that regulates multiple stages of Drosophila spermatogenesis. While VCP has documented roles in mitotic spermatogonia and meiotic spermatocytes, it is also highly expressed in post-meiotic spermatids, suggesting p...
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Format: | Article |
Language: | English |
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Taylor & Francis Group
2023-12-01
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Series: | Fly |
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Online Access: | http://dx.doi.org/10.1080/19336934.2023.2234795 |
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author | Tyler J. Butsch Alyssa E. Johnson K. Adam Bohnert |
author_facet | Tyler J. Butsch Alyssa E. Johnson K. Adam Bohnert |
author_sort | Tyler J. Butsch |
collection | DOAJ |
description | Valosin-containing protein (VCP) is a versatile and ubiquitously expressed AAA+ ATPase that regulates multiple stages of Drosophila spermatogenesis. While VCP has documented roles in mitotic spermatogonia and meiotic spermatocytes, it is also highly expressed in post-meiotic spermatids, suggesting potential late-stage developmental functions as well. However, tools to assess late-stage activities of pleiotropic spermatogenesis genes such as VCP are lacking. Available germline-specific Gal4 drivers activate in stem cells or spermatogonia; consequently, knocking down VCP using one of these drivers disrupts or blocks early germ-cell development, precluding analysis of VCP in later stages. A Gal4 driver that activates later in development, such as at the meiotic spermatocyte stage, may permit functional analyses of VCP and other factors in post-meiotic stages. Here, we describe a germline-specific Gal4 driver, Rbp4-Gal4, which drives transgene expression beginning in the early spermatocyte stage. We find that Rbp4-Gal4-driven knockdown of VCP causes defects in spermatid chromatin condensation and individualization without affecting earlier developmental stages. Interestingly, the defect in chromatin condensation appears linked to errors in the histone-to-protamine transition, a key event in spermatid development. Overall, our study reveals roles for VCP in spermatid development and establishes a powerful tool to dissect the functions of pleiotropic spermatogenesis genes. |
first_indexed | 2024-03-11T22:58:30Z |
format | Article |
id | doaj.art-50f9272c03964b54956385b1d57f5899 |
institution | Directory Open Access Journal |
issn | 1933-6934 1933-6942 |
language | English |
last_indexed | 2024-03-11T22:58:30Z |
publishDate | 2023-12-01 |
publisher | Taylor & Francis Group |
record_format | Article |
series | Fly |
spelling | doaj.art-50f9272c03964b54956385b1d57f58992023-09-21T15:17:01ZengTaylor & Francis GroupFly1933-69341933-69422023-12-0117110.1080/19336934.2023.22347952234795Rbp4-Gal4, a germline driver that activates in meiosis, reveals functions for VCP in spermatid developmentTyler J. Butsch0Alyssa E. Johnson1K. Adam Bohnert2Louisiana State University 202 Life Sciences BuildingLouisiana State University 202 Life Sciences BuildingLouisiana State University 202 Life Sciences BuildingValosin-containing protein (VCP) is a versatile and ubiquitously expressed AAA+ ATPase that regulates multiple stages of Drosophila spermatogenesis. While VCP has documented roles in mitotic spermatogonia and meiotic spermatocytes, it is also highly expressed in post-meiotic spermatids, suggesting potential late-stage developmental functions as well. However, tools to assess late-stage activities of pleiotropic spermatogenesis genes such as VCP are lacking. Available germline-specific Gal4 drivers activate in stem cells or spermatogonia; consequently, knocking down VCP using one of these drivers disrupts or blocks early germ-cell development, precluding analysis of VCP in later stages. A Gal4 driver that activates later in development, such as at the meiotic spermatocyte stage, may permit functional analyses of VCP and other factors in post-meiotic stages. Here, we describe a germline-specific Gal4 driver, Rbp4-Gal4, which drives transgene expression beginning in the early spermatocyte stage. We find that Rbp4-Gal4-driven knockdown of VCP causes defects in spermatid chromatin condensation and individualization without affecting earlier developmental stages. Interestingly, the defect in chromatin condensation appears linked to errors in the histone-to-protamine transition, a key event in spermatid development. Overall, our study reveals roles for VCP in spermatid development and establishes a powerful tool to dissect the functions of pleiotropic spermatogenesis genes.http://dx.doi.org/10.1080/19336934.2023.2234795germlinemale fertilityspermatogenesisspermatocytespermatidvcpindividualizationgal4/uas |
spellingShingle | Tyler J. Butsch Alyssa E. Johnson K. Adam Bohnert Rbp4-Gal4, a germline driver that activates in meiosis, reveals functions for VCP in spermatid development Fly germline male fertility spermatogenesis spermatocyte spermatid vcp individualization gal4/uas |
title | Rbp4-Gal4, a germline driver that activates in meiosis, reveals functions for VCP in spermatid development |
title_full | Rbp4-Gal4, a germline driver that activates in meiosis, reveals functions for VCP in spermatid development |
title_fullStr | Rbp4-Gal4, a germline driver that activates in meiosis, reveals functions for VCP in spermatid development |
title_full_unstemmed | Rbp4-Gal4, a germline driver that activates in meiosis, reveals functions for VCP in spermatid development |
title_short | Rbp4-Gal4, a germline driver that activates in meiosis, reveals functions for VCP in spermatid development |
title_sort | rbp4 gal4 a germline driver that activates in meiosis reveals functions for vcp in spermatid development |
topic | germline male fertility spermatogenesis spermatocyte spermatid vcp individualization gal4/uas |
url | http://dx.doi.org/10.1080/19336934.2023.2234795 |
work_keys_str_mv | AT tylerjbutsch rbp4gal4agermlinedriverthatactivatesinmeiosisrevealsfunctionsforvcpinspermatiddevelopment AT alyssaejohnson rbp4gal4agermlinedriverthatactivatesinmeiosisrevealsfunctionsforvcpinspermatiddevelopment AT kadambohnert rbp4gal4agermlinedriverthatactivatesinmeiosisrevealsfunctionsforvcpinspermatiddevelopment |