Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster

Detalhes bibliográficos
Autor(a) principal: Saari, Sina
Data de Publicação: 2017
Outros Autores: Andjelkovic, Ana, Garcia, Geovana S. [UNESP], Jacobs, Howard T., Oliveira, Marcos T. [UNESP]
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1186/s12861-017-0151-3
http://hdl.handle.net/11449/162992
Resumo: Background: Mitochondrial alternative respiratory-chain enzymes are phylogenetically widespread, and buffer stresses affecting oxidative phosphorylation in species that possess them. However, they have been lost in the evolutionary lineages leading to vertebrates and arthropods, raising the question as to what survival or reproductive disadvantages they confer. Recent interest in using them in therapy lends a biomedical dimension to this question. Methods: Here, we examined the impact of the expression of Ciona intestinalis alternative oxidase, AOX, on the reproductive success of Drosophila melanogaster males. Sperm-competition assays were performed between flies carrying three copies of a ubiquitously expressed AOX construct, driven by the a-tubulin promoter, and wild-type males of the same genetic background. Results: In sperm-competition assays, AOX conferred a substantial disadvantage, associated with decreased production of mature sperm. Sperm differentiation appeared to proceed until the last stages, but was spatially deranged, with spermatozoids retained in the testis instead of being released to the seminal vesicle. High AOX expression was detected in the outermost cell-layer of the testis sheath, which we hypothesize may disrupt a signal required for sperm maturation. Conclusions: AOX expression in Drosophila thus has effects that are deleterious to male reproductive function. Our results imply that AOX therapy must be developed with caution.
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spelling Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogasterMitochondriaRespiratory chainSpermatogenesisSperm competitionBackground: Mitochondrial alternative respiratory-chain enzymes are phylogenetically widespread, and buffer stresses affecting oxidative phosphorylation in species that possess them. However, they have been lost in the evolutionary lineages leading to vertebrates and arthropods, raising the question as to what survival or reproductive disadvantages they confer. Recent interest in using them in therapy lends a biomedical dimension to this question. Methods: Here, we examined the impact of the expression of Ciona intestinalis alternative oxidase, AOX, on the reproductive success of Drosophila melanogaster males. Sperm-competition assays were performed between flies carrying three copies of a ubiquitously expressed AOX construct, driven by the a-tubulin promoter, and wild-type males of the same genetic background. Results: In sperm-competition assays, AOX conferred a substantial disadvantage, associated with decreased production of mature sperm. Sperm differentiation appeared to proceed until the last stages, but was spatially deranged, with spermatozoids retained in the testis instead of being released to the seminal vesicle. High AOX expression was detected in the outermost cell-layer of the testis sheath, which we hypothesize may disrupt a signal required for sperm maturation. Conclusions: AOX expression in Drosophila thus has effects that are deleterious to male reproductive function. Our results imply that AOX therapy must be developed with caution.European Union (Marie Curie International Incoming Fellowship)European Research Council Advanced GrantFundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Finnish Cultural FoundationAcademy of FinlandTampere University Medical Research FundSigrid Juselius FoundationUniv Tampere, Tampere Univ Hosp, Inst Biosci & Med Technol, FI-33014 Tampere, FinlandUniv Estadual Paulista, Dept Tecnol, Fac Ciencias Agr & Vet, BR-14884900 Jaboticabal, SP, BrazilUniv Helsinki, Inst Biotechnol, FI-00014 Helsinki, FinlandUniv Estadual Paulista, Dept Tecnol, Fac Ciencias Agr & Vet, BR-14884900 Jaboticabal, SP, BrazilEuropean Union (Marie Curie International Incoming Fellowship): GA328988European Research Council Advanced Grant: 232,738FAPESP: 2014/02253-6Academy of Finland: 256,615Academy of Finland: 272,376Biomed Central LtdUniv TampereUniversidade Estadual Paulista (Unesp)Univ HelsinkiSaari, SinaAndjelkovic, AnaGarcia, Geovana S. [UNESP]Jacobs, Howard T.Oliveira, Marcos T. [UNESP]2018-11-26T17:39:40Z2018-11-26T17:39:40Z2017-07-03info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/article11application/pdfhttp://dx.doi.org/10.1186/s12861-017-0151-3Bmc Developmental Biology. London: Biomed Central Ltd, v. 17, 11 p., 2017.1471-213Xhttp://hdl.handle.net/11449/16299210.1186/s12861-017-0151-3WOS:000405439300001WOS000405439300001.pdfWeb of Sciencereponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengBmc Developmental Biologyinfo:eu-repo/semantics/openAccess2024-06-07T15:31:35Zoai:repositorio.unesp.br:11449/162992Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-06-07T15:31:35Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster
title Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster
spellingShingle Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster
Saari, Sina
Mitochondria
Respiratory chain
Spermatogenesis
Sperm competition
title_short Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster
title_full Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster
title_fullStr Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster
title_full_unstemmed Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster
title_sort Expression of Ciona intestinalis AOX causes male reproductive defects in Drosophila melanogaster
author Saari, Sina
author_facet Saari, Sina
Andjelkovic, Ana
Garcia, Geovana S. [UNESP]
Jacobs, Howard T.
Oliveira, Marcos T. [UNESP]
author_role author
author2 Andjelkovic, Ana
Garcia, Geovana S. [UNESP]
Jacobs, Howard T.
Oliveira, Marcos T. [UNESP]
author2_role author
author
author
author
dc.contributor.none.fl_str_mv Univ Tampere
Universidade Estadual Paulista (Unesp)
Univ Helsinki
dc.contributor.author.fl_str_mv Saari, Sina
Andjelkovic, Ana
Garcia, Geovana S. [UNESP]
Jacobs, Howard T.
Oliveira, Marcos T. [UNESP]
dc.subject.por.fl_str_mv Mitochondria
Respiratory chain
Spermatogenesis
Sperm competition
topic Mitochondria
Respiratory chain
Spermatogenesis
Sperm competition
description Background: Mitochondrial alternative respiratory-chain enzymes are phylogenetically widespread, and buffer stresses affecting oxidative phosphorylation in species that possess them. However, they have been lost in the evolutionary lineages leading to vertebrates and arthropods, raising the question as to what survival or reproductive disadvantages they confer. Recent interest in using them in therapy lends a biomedical dimension to this question. Methods: Here, we examined the impact of the expression of Ciona intestinalis alternative oxidase, AOX, on the reproductive success of Drosophila melanogaster males. Sperm-competition assays were performed between flies carrying three copies of a ubiquitously expressed AOX construct, driven by the a-tubulin promoter, and wild-type males of the same genetic background. Results: In sperm-competition assays, AOX conferred a substantial disadvantage, associated with decreased production of mature sperm. Sperm differentiation appeared to proceed until the last stages, but was spatially deranged, with spermatozoids retained in the testis instead of being released to the seminal vesicle. High AOX expression was detected in the outermost cell-layer of the testis sheath, which we hypothesize may disrupt a signal required for sperm maturation. Conclusions: AOX expression in Drosophila thus has effects that are deleterious to male reproductive function. Our results imply that AOX therapy must be developed with caution.
publishDate 2017
dc.date.none.fl_str_mv 2017-07-03
2018-11-26T17:39:40Z
2018-11-26T17:39:40Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1186/s12861-017-0151-3
Bmc Developmental Biology. London: Biomed Central Ltd, v. 17, 11 p., 2017.
1471-213X
http://hdl.handle.net/11449/162992
10.1186/s12861-017-0151-3
WOS:000405439300001
WOS000405439300001.pdf
url http://dx.doi.org/10.1186/s12861-017-0151-3
http://hdl.handle.net/11449/162992
identifier_str_mv Bmc Developmental Biology. London: Biomed Central Ltd, v. 17, 11 p., 2017.
1471-213X
10.1186/s12861-017-0151-3
WOS:000405439300001
WOS000405439300001.pdf
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Bmc Developmental Biology
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 11
application/pdf
dc.publisher.none.fl_str_mv Biomed Central Ltd
publisher.none.fl_str_mv Biomed Central Ltd
dc.source.none.fl_str_mv Web of Science
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
repository.mail.fl_str_mv
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