BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior
Open accessAbstract
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.
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Six-day-old adult virgin males were used throughout this study to ensure that age- and mating-dependent effects on SC biology were mitigated.
“Six-day-old adult virgin males were used throughout this study to ensure that age- and mating-dependent effects on SC biology were mitigated44,45.”
From GAPDH controls extracellular vesicle biogenesis and enhances the therapeutic potential of EV mediated siRNA delivery to the brain (2021) · cites this paper as [45]
Figure 5 describes analysis of SCs from 6-day-old virgin males. The Results section on exosome transfer also reports that older, multiply mated males can transfer SCs and says this paper used 4-day-old males for its mating experiments to avoid that complication. These passages support controlling age and mating history, but do not establish that using 6-day-old virgins throughout the citing study mitigates age- and mating-dependent effects on SC biology generally. (LLM, conf=0.83)
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Extracellular Vesicles Isolated from the Leaf Apoplast Carry Stress-Response Proteins
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Cortactin promotes exosome secretion by controlling branched actin dynamics
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The Drosophila seminal proteome and its role in postcopulatory sexual selection
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Self-citationPost‐ejaculatory modifications to sperm (PEMS)
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Soma-to-germline RNA communication
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Myristoylated CIL-7 regulates ciliary extracellular vesicle biogenesis
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The Small GTPase Ral orchestrates MVB biogenesis and exosome secretion
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The Drosophila Accessory Gland as a Model for Prostate Cancer and Other Pathologies
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Self-citationAn early endosome–derived retrograde trafficking pathway promotes secretory granule maturation
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Microguards and micromessengers of the genome
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Extracellular Vesicles in Joint Disease and Therapy
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An Emerging Frontier in Intercellular Communication: Extracellular Vesicles in Regeneration
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A phosphate-sensing organelle regulates phosphate and tissue homeostasis
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Self-citationNew and Prospective Roles for lncRNAs in Organelle Formation and Function
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Going live with tumor exosomes and microvesicles
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Divergence in Transcriptional and Regulatory Responses to Mating in Male and Female Fruitflies
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Drosophila Sex Peptide controls the assembly of lipid microcarriers in seminal fluid
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Zebrafish as a preclinical model for Extracellular Vesicle-based therapeutic development
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Nature and Functions of Glands and Ducts in the Drosophila Reproductive Tract
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A surfactant lipid layer of endosomal membranes facilitates airway gas filling in Drosophila
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Females translate male mRNA transferred during mating
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On the Role of Seminal Fluid Protein and Nucleic Acid Content in Paternal Epigenetic Inheritance
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Drosophila Accessory Gland: A Complementary In Vivo Model to Bring New Insight to Prostate Cancer
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Exosomes: Ultrastructural evidence in epithelial cells of Malpighian tubules
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Vacuolar protein sorting 4 is required for silkworm metamorphosis
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Villa-Arias, S., la Ossa, J. A. M.-D., Avila, F. W., Dorus, S., & Alfonso‐Parra, C. (2025) · Journal of Proteomics · doi:10.1016/j.jprot.2025.105410 · Cited by 8 · see citing works
- Authors
- Corrigan, L., Redhai, S., Leiblich, A., Fan, S.-J., Perera, S. M. W., Patel, R., Gandy, C., Wainwright, S. M., Morris, J. F., Hamdy, F., Goberdhan, D. C. I., & Wilson, C.
- Affiliations
- University of Oxford (GB)
- Corresponding author
- Wilson, Clive
- ORCID
- Venue
- Journal of Cell Biology
- Publisher
- Rockefeller University Press
- Published
- 2014-08-25
- Volume
- 206
- Issue
- 5
- Pages
- 671-688
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC4151142
- OpenAlex
- W2057486059
- Cited by
- 155
- References
- 92
- Citations by year
- 2026: 12 · 2025: 15 · 2024: 16 · 2023: 15 · 2022: 15 · 2021: 16 · 2020: 10 · 2019: 14 · 2018: 8 · 2017: 8 · 2016: 16 · 2015: 8 · 2014: 2
- FWCI
- 4.64
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Cell Biology (publishedVersion)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust (092927/Z/10/Z)
- Cancer Research UK (C38302/A12278)
- National Institute for Health and Care Research (NF-SI-0509-10242)
- Biotechnology and Biological Sciences Research Council (BB/K017462/1)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Keywords
- exosomes, BMP signaling, Drosophila melanogaster, male accessory glands, secondary cells, seminal plasma, multivesicular bodies, female reproductive tract, sperm competition, mating behavior
- MeSH terms
- Animals, Drosophila melanogaster, Epithelial Cells, Female, Genitalia, Female, Genitalia, Male, Lysosomes, Male, Membrane Fusion, Sexual Behavior, Animal, Spermatozoa, Vacuoles, Signal Transduction, Bone Morphogenetic Proteins, Protein Transport, Membrane Microdomains, Secretory Vesicles, Drosophila Proteins, Exosomes, Multivesicular Bodies, Tetraspanin 30
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