Cargando…

BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior

Male reproductive glands secrete signals into seminal fluid to facilitate reproductive success. In Drosophila melanogaster, these signals are generated by a variety of seminal peptides, many produced by the accessory glands (AGs). One epithelial cell type in the adult male AGs, the secondary cell (S...

Descripción completa

Detalles Bibliográficos
Autores principales: Corrigan, Laura, Redhai, Siamak, Leiblich, Aaron, Fan, Shih-Jung, Perera, Sumeth M.W., Patel, Rachel, Gandy, Carina, Wainwright, S. Mark, Morris, John F., Hamdy, Freddie, Goberdhan, Deborah C.I., Wilson, Clive
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Rockefeller University Press 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4151142/
https://www.ncbi.nlm.nih.gov/pubmed/25154396
http://dx.doi.org/10.1083/jcb.201401072
_version_ 1782333002056990720
author Corrigan, Laura
Redhai, Siamak
Leiblich, Aaron
Fan, Shih-Jung
Perera, Sumeth M.W.
Patel, Rachel
Gandy, Carina
Wainwright, S. Mark
Morris, John F.
Hamdy, Freddie
Goberdhan, Deborah C.I.
Wilson, Clive
author_facet Corrigan, Laura
Redhai, Siamak
Leiblich, Aaron
Fan, Shih-Jung
Perera, Sumeth M.W.
Patel, Rachel
Gandy, Carina
Wainwright, S. Mark
Morris, John F.
Hamdy, Freddie
Goberdhan, Deborah C.I.
Wilson, Clive
author_sort Corrigan, Laura
collection PubMed
description Male reproductive glands secrete signals into seminal fluid to facilitate reproductive success. In Drosophila melanogaster, these signals are generated by a variety of seminal peptides, many produced by the accessory glands (AGs). One epithelial cell type in the adult male AGs, the secondary cell (SC), grows selectively in response to bone morphogenetic protein (BMP) signaling. This signaling is involved in blocking the rapid remating of mated females, which contributes to the reproductive advantage of the first male to mate. In this paper, we show that SCs secrete exosomes, membrane-bound vesicles generated inside late endosomal multivesicular bodies (MVBs). After mating, exosomes fuse with sperm (as also seen in vitro for human prostate-derived exosomes and sperm) and interact with female reproductive tract epithelia. Exosome release was required to inhibit female remating behavior, suggesting that exosomes are downstream effectors of BMP signaling. Indeed, when BMP signaling was reduced in SCs, vesicles were still formed in MVBs but not secreted as exosomes. These results demonstrate a new function for the MVB–exosome pathway in the reproductive tract that appears to be conserved across evolution.
format Online
Article
Text
id pubmed-4151142
institution National Center for Biotechnology Information
language English
publishDate 2014
publisher The Rockefeller University Press
record_format MEDLINE/PubMed
spelling pubmed-41511422015-03-01 BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior Corrigan, Laura Redhai, Siamak Leiblich, Aaron Fan, Shih-Jung Perera, Sumeth M.W. Patel, Rachel Gandy, Carina Wainwright, S. Mark Morris, John F. Hamdy, Freddie Goberdhan, Deborah C.I. Wilson, Clive J Cell Biol Research Articles Male reproductive glands secrete signals into seminal fluid to facilitate reproductive success. In Drosophila melanogaster, these signals are generated by a variety of seminal peptides, many produced by the accessory glands (AGs). One epithelial cell type in the adult male AGs, the secondary cell (SC), grows selectively in response to bone morphogenetic protein (BMP) signaling. This signaling is involved in blocking the rapid remating of mated females, which contributes to the reproductive advantage of the first male to mate. In this paper, we show that SCs secrete exosomes, membrane-bound vesicles generated inside late endosomal multivesicular bodies (MVBs). After mating, exosomes fuse with sperm (as also seen in vitro for human prostate-derived exosomes and sperm) and interact with female reproductive tract epithelia. Exosome release was required to inhibit female remating behavior, suggesting that exosomes are downstream effectors of BMP signaling. Indeed, when BMP signaling was reduced in SCs, vesicles were still formed in MVBs but not secreted as exosomes. These results demonstrate a new function for the MVB–exosome pathway in the reproductive tract that appears to be conserved across evolution. The Rockefeller University Press 2014-09-01 /pmc/articles/PMC4151142/ /pubmed/25154396 http://dx.doi.org/10.1083/jcb.201401072 Text en © 2014 Corrigan et al. This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/).
spellingShingle Research Articles
Corrigan, Laura
Redhai, Siamak
Leiblich, Aaron
Fan, Shih-Jung
Perera, Sumeth M.W.
Patel, Rachel
Gandy, Carina
Wainwright, S. Mark
Morris, John F.
Hamdy, Freddie
Goberdhan, Deborah C.I.
Wilson, Clive
BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior
title BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior
title_full BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior
title_fullStr BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior
title_full_unstemmed BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior
title_short BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior
title_sort bmp-regulated exosomes from drosophila male reproductive glands reprogram female behavior
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4151142/
https://www.ncbi.nlm.nih.gov/pubmed/25154396
http://dx.doi.org/10.1083/jcb.201401072
work_keys_str_mv AT corriganlaura bmpregulatedexosomesfromdrosophilamalereproductiveglandsreprogramfemalebehavior
AT redhaisiamak bmpregulatedexosomesfromdrosophilamalereproductiveglandsreprogramfemalebehavior
AT leiblichaaron bmpregulatedexosomesfromdrosophilamalereproductiveglandsreprogramfemalebehavior
AT fanshihjung bmpregulatedexosomesfromdrosophilamalereproductiveglandsreprogramfemalebehavior
AT pererasumethmw bmpregulatedexosomesfromdrosophilamalereproductiveglandsreprogramfemalebehavior
AT patelrachel bmpregulatedexosomesfromdrosophilamalereproductiveglandsreprogramfemalebehavior
AT gandycarina bmpregulatedexosomesfromdrosophilamalereproductiveglandsreprogramfemalebehavior
AT wainwrightsmark bmpregulatedexosomesfromdrosophilamalereproductiveglandsreprogramfemalebehavior
AT morrisjohnf bmpregulatedexosomesfromdrosophilamalereproductiveglandsreprogramfemalebehavior
AT hamdyfreddie bmpregulatedexosomesfromdrosophilamalereproductiveglandsreprogramfemalebehavior
AT goberdhandeborahci bmpregulatedexosomesfromdrosophilamalereproductiveglandsreprogramfemalebehavior
AT wilsonclive bmpregulatedexosomesfromdrosophilamalereproductiveglandsreprogramfemalebehavior