BMP-regulated exosomes from <i>Drosophila</i> male reproductive glands reprogram female behavior

Corrigan, Laura; Redhai, Siamak; Leiblich, Aaron; Fan, Shih‐Jung; Perera, Sumeth; Patel, Raf; Gandy, Carina; Wainwright, S. Mark; Morris, John F.; Hamdy, Freddie C.; Goberdhan, Deborah C. I.; Wilson, Clive

doi:10.1083/jcb.201401072

Cited by 143 publications

(290 citation statements)

References 89 publications

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“…After eggs have begun to move through the RT (12) and to be laid (3,5, and 8 h ASM), the lumen of the uterus contracts back to resemble the uterine lumen of a virgin female (except when it contains an egg; Fig. 4 and Fig.…”

Section: Mating and Seminal Proteins Cause Coordinated Looping Andmentioning

confidence: 99%

Integrated 3D view of postmating responses by the Drosophila melanogaster female reproductive tract, obtained by micro-computed tomography scanning

Mattei

Riccio

Avila

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

140

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Physiological changes in females during and after mating are triggered by seminal fluid components in conjunction with female-derived molecules. In insects, these changes include increased egg production, storage of sperm, and changes in muscle contraction within the reproductive tract (RT). Such postmating changes have been studied in dissected RT tissues, but understanding their coordination in vivo requires a holistic view of the tissues and their interrelationships. Here, we used high-resolution, multiscale micro-computed tomography (CT) scans to visualize and measure postmating changes in situ in the Drosophila female RT before, during, and after mating. These studies reveal previously unidentified dynamic changes in the conformation of the female RT that occur after mating. Our results also reveal how the reproductive organs temporally shift in concert within the confines of the abdomen. For example, we observed chiral loops in the uterus and in the upper common oviduct that relax and constrict throughout sperm storage and egg movement. We found that specific seminal fluid proteins or female secretions mediate some of the postmating changes in morphology. The morphological movements, in turn, can cause further changes due to the connections among organs. In addition, we observed apparent copulatory damage to the female intima, suggesting a mechanism for entry of seminal proteins, or other exogenous components, into the female’s circulatory system. The 3D reconstructions provided by high-resolution micro-CT scans reveal how male and female molecules and anatomy interface to carry out and coordinate mating-dependent changes in the female’s reproductive physiology.

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Section: Mating and Seminal Proteins Cause Coordinated Looping Andmentioning

confidence: 99%

Integrated 3D view of postmating responses by the Drosophila melanogaster female reproductive tract, obtained by micro-computed tomography scanning

Mattei

Riccio

Avila

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

140

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“…protein or RNA) have been the focus of investigation46. A similar process has also been characterized in Drosophila , where exosomes produced in the secondary cells of the accessory gland bind and fuse with sperm61. Although it is not possible to make firm conclusions based on our data alone, our analysis is consistent with the continued maturation of sperm during transit, and points to the presence of secreted vesicles that could sustain the final stages of maturation in a manner analogous to those described in other systems.…”

Section: Discussionmentioning

confidence: 99%

The Seminal fluid proteome of the polyandrous Red junglefowl offers insights into the molecular basis of fertility, reproductive ageing and domestication

Borziak

Alvarez-Fernandez

Karr

et al. 2016

Sci Rep

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Seminal fluid proteins (SFPs) are emerging as fundamental contributors to sexual selection given their role in post-mating reproductive events, particularly in polyandrous species where the ejaculates of different males compete for fertilisation. SFP identification however remains taxonomically limited and little is known about avian SFPs, despite extensive work on sexual selection in birds. We characterize the SF proteome of the polyandrous Red junglefowl, Gallus gallus, the wild species that gave rise to the domestic chicken. We identify 1,141 SFPs, including proteins involved in immunity and antimicrobial defences, sperm maturation, and fertilisation, revealing a functionally complex SF proteome. This includes a predominant contribution of blood plasma proteins that is conserved with human SF. By comparing the proteome of young and old males with fast or slow sperm velocity in a balanced design, we identify proteins associated with ageing and sperm velocity, and show that old males that retain high sperm velocity have distinct proteome characteristics. SFP comparisons with domestic chickens revealed both qualitative and quantitative differences likely associated with domestication and artificial selection. Collectively, these results shed light onto the functional complexity of avian SF, and provide a platform for molecular studies of fertility, reproductive ageing, and domestication.

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“…EV uptake by recipient cells can reprogram signalling pathways to modulate the phenotype and function of the target cell [31,[44][45][46][47][48]. For example, mechanisms include transmembrane protein transfer to the plasma membrane to trigger signalling, oncoprotein transfer, transcriptional regulators transferred into the nucleus to regulate promoter activity, translational regulation mediated by mRNA/miRNA transfer, and DNA transfer for integration into the recipient cell genome [49].…”

Section: Extracellular Vesicles: Exosomes and Microvesiclesmentioning

confidence: 99%

Emerging roles of exosomes during epithelial–mesenchymal transition and cancer progression

Greening

Gopal

Mathias

et al. 2015

Seminars in Cell & Developmental Biology

197

145

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

Abstract: Male Drosophila reproductive glands secrete exosomes in a BMP-dependent manner that fuse with sperm after mating and suppress female remating.

Cited by 143 publications

References 89 publications

Integrated 3D view of postmating responses by the Drosophila melanogaster female reproductive tract, obtained by micro-computed tomography scanning

Integrated 3D view of postmating responses by the Drosophila melanogaster female reproductive tract, obtained by micro-computed tomography scanning

The Seminal fluid proteome of the polyandrous Red junglefowl offers insights into the molecular basis of fertility, reproductive ageing and domestication

Emerging roles of exosomes during epithelial–mesenchymal transition and cancer progression

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