Mating-regulated atrial proteases control reinsemination rates in Anopheles gambiae females

Abstract Anopheles gambiae mosquitoes are the most important vectors of human malaria. The reproductive success of these mosquitoes relies on a single copulation event after which the majority of females become permanently refractory to further mating. This refractory behavior is at least partially...

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Main Authors: Priscila Bascuñán, Paolo Gabrieli, Enzo Mameli, Flaminia Catteruccia
Format: Article
Language:English
Published: Nature Publishing Group 2020-12-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-020-78967-y
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spelling doaj-fdc3e364bf0746819a7ba70ba5f299b92020-12-20T12:28:26ZengNature Publishing GroupScientific Reports2045-23222020-12-0110111010.1038/s41598-020-78967-yMating-regulated atrial proteases control reinsemination rates in Anopheles gambiae femalesPriscila Bascuñán0Paolo Gabrieli1Enzo Mameli2Flaminia Catteruccia3Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public HealthDepartment of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public HealthDepartment of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public HealthDepartment of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public HealthAbstract Anopheles gambiae mosquitoes are the most important vectors of human malaria. The reproductive success of these mosquitoes relies on a single copulation event after which the majority of females become permanently refractory to further mating. This refractory behavior is at least partially mediated by the male-synthetized steroid hormone 20-hydroxyecdysone (20E), which is packaged together with other seminal secretions into a gelatinous mating plug and transferred to the female atrium during mating. In this study, we show that two 20E-regulated chymotrypsin-like serine proteases specifically expressed in the reproductive tract of An. gambiae females play an important role in modulating the female susceptibility to mating. Silencing these proteases by RNA interference impairs correct plug processing and slows down the release of the steroid hormone 20E from the mating plug. In turn, depleting one of these proteases, the Mating Regulated Atrial Protease 1 (MatRAP1), reduces female refractoriness to further copulation, so that a significant proportion of females mate again. Microscopy analysis reveals that MatRAP1 is localized on a previously undetected peritrophic matrix-like structure surrounding the mating plug. These data provide novel insight into the molecular mechanisms shaping the post-mating biology of these important malaria vectors.https://doi.org/10.1038/s41598-020-78967-y
collection DOAJ
language English
format Article
sources DOAJ
author Priscila Bascuñán
Paolo Gabrieli
Enzo Mameli
Flaminia Catteruccia
spellingShingle Priscila Bascuñán
Paolo Gabrieli
Enzo Mameli
Flaminia Catteruccia
Mating-regulated atrial proteases control reinsemination rates in Anopheles gambiae females
Scientific Reports
author_facet Priscila Bascuñán
Paolo Gabrieli
Enzo Mameli
Flaminia Catteruccia
author_sort Priscila Bascuñán
title Mating-regulated atrial proteases control reinsemination rates in Anopheles gambiae females
title_short Mating-regulated atrial proteases control reinsemination rates in Anopheles gambiae females
title_full Mating-regulated atrial proteases control reinsemination rates in Anopheles gambiae females
title_fullStr Mating-regulated atrial proteases control reinsemination rates in Anopheles gambiae females
title_full_unstemmed Mating-regulated atrial proteases control reinsemination rates in Anopheles gambiae females
title_sort mating-regulated atrial proteases control reinsemination rates in anopheles gambiae females
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2020-12-01
description Abstract Anopheles gambiae mosquitoes are the most important vectors of human malaria. The reproductive success of these mosquitoes relies on a single copulation event after which the majority of females become permanently refractory to further mating. This refractory behavior is at least partially mediated by the male-synthetized steroid hormone 20-hydroxyecdysone (20E), which is packaged together with other seminal secretions into a gelatinous mating plug and transferred to the female atrium during mating. In this study, we show that two 20E-regulated chymotrypsin-like serine proteases specifically expressed in the reproductive tract of An. gambiae females play an important role in modulating the female susceptibility to mating. Silencing these proteases by RNA interference impairs correct plug processing and slows down the release of the steroid hormone 20E from the mating plug. In turn, depleting one of these proteases, the Mating Regulated Atrial Protease 1 (MatRAP1), reduces female refractoriness to further copulation, so that a significant proportion of females mate again. Microscopy analysis reveals that MatRAP1 is localized on a previously undetected peritrophic matrix-like structure surrounding the mating plug. These data provide novel insight into the molecular mechanisms shaping the post-mating biology of these important malaria vectors.
url https://doi.org/10.1038/s41598-020-78967-y
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