scholarly journals Mating Induces Switch From Hormone-Dependent to – Independent Steroid Receptor-Mediated Growth in Drosophila Prostate-Like Cells

2019 ◽  
Author(s):  
Aaron Leiblich ◽  
Josephine E. E. U. Hellberg ◽  
Aashika Sekar ◽  
Carina Gandy ◽  
Siamak Redhai ◽  
...  
Keyword(s):  
Cancer Progression ◽  
Seminal Fluid ◽  
Sexual Experience ◽  
Adult Life ◽  
Accessory Gland ◽  
Accessory Glands ◽  
Morphogenetic Protein ◽  
A Cell ◽  
Cell Type Specific ◽  
Bmp Signalling

AbstractMale reproductive glands like the mammalian prostate and the paired Drosophila melanogaster accessory glands secrete seminal fluid components that enhance fecundity. In humans, the prostate grows throughout adult life, stimulated by environmentally regulated endocrine and local androgens. We previously showed that in each fly accessory gland, secondary cells (SCs) and their nuclei also grow in adults, a process enhanced by mating and controlled by bone morphogenetic protein (BMP) signalling. Here we demonstrate that BMP-mediated SC growth is dependent on the receptor for the developmental steroid, ecdysone, whose concentration reflects socio-sexual experience in adults. BMP signalling regulates ecdysone receptor (EcR) levels post-transcriptionally, partly via EcR’s N-terminus. Nuclear growth in virgin males is ecdysone-dependent. However, mating activates genome endoreplication to drive additional BMP-mediated nuclear growth via a cell type-specific form of hormone-independent EcR signalling. In virgin males with low ecdysone levels, this mechanism ensures resources are conserved. However, by switching to hormone-independence after mating, this control is overridden to hyper-activate growth of secretory secondary cells. Our data suggest parallels between this physiological, behaviour-induced switch and altered pathological signalling associated with prostate cancer progression.

scholarly journals Rab-mediated trafficking in the secondary cells of Drosophila male accessory glands and its role in fecundity

2018 ◽  
Author(s):  
E. Prince ◽  
M. Brankatschk ◽  
B. Kroeger ◽  
D. Gligorov ◽  
C. Wilson ◽  
...  
Keyword(s):  
Mating Behavior ◽  
Seminal Fluid ◽  
Cell Types ◽  
Accessory Gland ◽  
Molecular Organization ◽  
Secretory Cells ◽  
Rab Proteins ◽  
Intracellular Membrane ◽  
Accessory Glands ◽  
Intracellular Membrane Transport

AbstractIt is known that the male seminal fluid contains factors that affect female post-mating behavior and physiology. In Drosophila, most of these factors are secreted by the two epithelial cell types that make up the male accessory gland: the main and secondary cells. Although secondary cells represent only 4% of the cells of the accessory gland, their contribution to the male seminal fluid is essential for sustaining the female post-mating response. To better understand the function of the secondary cells, here we investigate their molecular organization, particularly with respect to the intracellular membrane transport machinery. We determined that large vacuole-like structures found in the secondary cells are trafficking hubs labeled by Rab6, 7, 11 and 19. Furthermore, these cell-specific organelles are essential for the long-term post-mating behavior of females and that their formation is directly dependent upon Rab6. Our discovery adds to our understanding of Rab proteins function in secretory cells. We have created an online, open-access imaging resource as a valuable tool for the intracellular membrane and protein traffic community.

Reproductive behaviour and physiology of Tenebrio molitor (Coleoptera: Tenebrionidae). III. Histogenetic changes in the internal genitalia, mesenteron, and cuticle during sexual maturation

1976 ◽  
Vol 54 (6) ◽  
pp. 990-1002 ◽  
Author(s):  
G. H. Gerber
Keyword(s):  
Sexual Maturation ◽  
Adult Life ◽  
Tenebrio Molitor ◽  
Reproductive Behaviour ◽  
Accessory Gland ◽  
Peritrophic Membrane ◽  
Secretory Cells ◽  
Accessory Glands ◽  
Internal Genitalia ◽  
Day By Day

The histogenic changes in the internal genitalia and mesenteron and the hardening and darkening of the cuticle during the first days of adult life in Tenebrio molitor L. are described. At emergence, the testes contain mature spermatozoa and the ovaries possess small oocytes. During the first 3 days, the shape, size, appearance, and staining characteristics of the secretory cells of the lateral oviducts, female accessory gland, tube accessory glands, bean-shaped accessory glands, and glandular region of the vasa deferentia change. Similar changes were not seen in the seminal vesicles and spermatheca. All of the secondary sex glands are filled with secretion by day 4. In the midgut, changes occur in the size, shape, and appearance of the epithelial cells by the 3rd day, and a peritrophic membrane is secreted during days 2 and 3. Most adults do not begin to feed until after the 3rd day. By day 3, the hardening and darkening of the cuticle are completed. All of these changes clearly are associated with adult maturation, especially sexual maturation, and most or all of the them must take place before the adults are able to copulate and oviposit.

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

2014 ◽  
Vol 206 (5) ◽  
pp. 671-688 ◽  
Author(s):  
Laura Corrigan ◽  
Siamak Redhai ◽  
Aaron Leiblich ◽  
Shih-Jung Fan ◽  
Sumeth M.W. Perera ◽  
...  
Keyword(s):  
Reproductive Tract ◽  
Seminal Fluid ◽  
Bmp Signaling ◽  
Female Reproductive Tract ◽  
Female Behavior ◽  
Accessory Glands ◽  
Morphogenetic Protein ◽  
Downstream Effectors ◽  
Membrane Bound

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.

scholarly journals Multi-level analysis of reproduction in the Antarctic midge, Belgica antarctica, identifies female and male accessory gland products that are altered by larval stress and impact progeny viability

2019 ◽  
Author(s):  
Geoffrey Finch ◽  
Sonya Nandyal ◽  
Carlie Perrieta ◽  
Benjamin Davies ◽  
Andrew J. Rosendale ◽  
...  
Keyword(s):  
Molecular Mechanisms ◽  
Storage Proteins ◽  
Adult Life ◽  
Accessory Gland ◽  
Specific Gene ◽  
Functional Studies ◽  
Accessory Glands ◽  
Belgica Antarctica ◽  
The Antarctic ◽  
The Impact

AbstractThe Antarctic midge, Belgica antarctica, is a wingless, non-biting midge endemic to Antarctica. Larval development requires at least two years, but adult life lasts only two weeks. The nonfeeding adults mate in swarms and females die shortly after oviposition. Eggs are suspended in a gel of unknown composition that is expressed from the female accessory gland. This project characterizes molecular mechanisms underlying reproduction in this midge by examining differential gene expression in whole males, females, and larvae, as well as in male and female accessory glands. Functional studies were used to assess the role of the gel encasing the eggs, as well as the impact of stress on reproductive biology. RNA-seq analyses revealed sex- and development-specific gene sets along with those associated with the accessory glands. Proteomic analyses were used to define the composition of the egg-containing gel, which is generated during multiple developmental stages and derived from both the accessory gland and other female organs. Functional studies indicate the gel provides a larval food source and thermal and dehydration buffer, all of which are critical for viability. Larval dehydration stress directly reduces production of storage proteins and key accessory gland components, a feature that impacts adult reproductive success. Modeling reveals that bouts of dehydration may significantly impact population growth. This work lays a foundation for further examination of reproduction in midges and provides new information related to general reproduction in dipterans. A key aspect is that reproduction and stress dynamics, currently understudied in polar organisms, are likely to prove critical for determining how climate change will alter survivability.

scholarly journals GATA- and Smad1-Dependent Enhancers in the Smad7 Gene Differentially Interpret Bone Morphogenetic Protein Concentrations

2003 ◽  
Vol 23 (18) ◽  
pp. 6646-6661 ◽  
Author(s):  
Hassina Benchabane ◽  
Jeffrey L. Wrana
Keyword(s):  
Bone Morphogenetic Protein ◽  
Transforming Growth Factor Beta ◽  
Binding Sites ◽  
Transforming Growth Factor ◽  
Physical Interaction ◽  
Gata Factor ◽  
Morphogenetic Protein ◽  
Inhibitory Feedback ◽  
A Cell ◽  
Cell Type Specific

ABSTRACT Smad7, an inhibitor of transforming growth factor beta superfamily signaling, is induced by bone morphogenetic protein (BMP) in an inhibitory feedback loop. Here, we identify multiple BMP response elements (BREs) in the Smad7 gene and demonstrate that they function differentially to interpret BMP signals in a cell type-specific manner. Two BREs (BRE-1 and -2) reside in the promoter region. One of these contains several conserved Smad1 and Smad4 binding sites that cooperate to mediate BMP-dependent induction, most likely in the absence of DNA binding partners. The third BRE (I-BRE) resides in the first intron and contains GATA factor binding sites. GATA-1, -5, or -6 is required for strong activation of I-BRE, and we show that they assemble with Smad1 on the I-BRE in living cells. Activation of the I-BRE is mediated by a specific region in GATA-5 and -6 but does not require direct physical interaction with Smad1. Comparison of I-BRE to BRE-1 showed that I-BRE is more responsive to low BMP concentrations. Moreover, analysis by chromatin immunoprecipitation experiments demonstrates that the endogenous I-BRE is occupied more robustly by endogenous Smad1 than is BRE-1. This correlates with regulation of the Smad7 gene, which is induced at lower BMP concentrations in GATA-expressing cell lines compared to non-GATA-expressing lines. These data thus define how cooperative and noncooperative Smad-dependent transcriptional regulation can function to interpret different BMP concentrations.

Male sexual maturation of the tsetse fliesglossina morsitanswestwood andg. austeniNewstead (Dipt., Glossinidae) in relation to blood feeding

1976 ◽  
Vol 66 (3) ◽  
pp. 389-399 ◽  
Author(s):  
Woodbridge A. Foster
Keyword(s):  
Sexual Maturation ◽  
Adult Life ◽  
Blood Feeding ◽  
Accessory Gland ◽  
Copulation Duration ◽  
Tsetse Flies ◽  
Sexual Performance ◽  
Glossina Morsitans ◽  
Accessory Glands ◽  
Gland Development

AbstractThe effect of blood feeding on male sexual maturation in the tsetse fliesGlossina morsitansWestwood andG. austeniNewstead was studied by comparing copulation and insemination performance of unfed and fed males during the first five days of adult life. These species differed conspicuously, both in the course of maturation and in the influence of blood feeding on it.G. morsitansmales copulated before they could inseminate, and even fed flies did not all inseminate until day 3; unfed flies showed retarded insemination performance by day 2, before copulation performance declined.G. austenimales were less sexually responsive at first, but they nearly always inseminated when they did copulate, even on day 1. Unfed flies showed less increase in copulation performance by day 4, but no decline. Accessory glands were larger inG. austenithanG. morsitansat emergence, and in unfed flies of both species they ceased to grow after day 3. Both accessory gland size and copulation duration (beyond a minimum duration) were related to insemination success in a general way, though copulation duration was quite variable. Vertebrate blood apparently provides male tsetse with specific nutrients or stimuli which promote sexual performance, in addition to basic energy and water requirements. Feeding probably affects insemination inG. morsitansthrough accessory gland development, allowing more complete spermatophore formation and sperm transfer, but its mode of action onG. austenisexual responsiveness is not evident.

scholarly journals Morphological and Developmental Traits of the Binucleation of Male Accessory Gland Cells in the Benthic Water Bug, Aphelocheirus vittatus (Hemiptera: Aphelochiridae)

2020 ◽  
Vol 20 (4) ◽  
Author(s):  
Koji Takeda ◽  
Jun Yamauchi ◽  
Takashi Adachi-Yamada
Keyword(s):  
Epithelial Cells ◽  
Cell Fusion ◽  
Seminal Fluid ◽  
Physiological Role ◽  
Reproductive Organs ◽  
Accessory Gland ◽  
Male Reproductive Success ◽  
Reproductive Behaviors ◽  
Accessory Glands ◽  
Close Relationship

Abstract The male accessory glands (MAGs) in insects are pair(s) of internal reproductive organs that produce and secrete the plasma component of seminal fluid. In various insects, MAG size is important for male reproductive success because the fluid provides physiologically active substances and/or nutrients to females to control sperm as well as female reproductive behaviors. Although the MAG epithelial cells in most insect species are standard mononucleate cells, those in some insect taxa are binucleate due to incomplete cytokinesis (e.g., Drosophila [Fallén] [Diptera: Drosophilidae]) or cell fusion (e.g., Cimex [Linnaeus] [Hemiptera: Cimicidae]). In the case of Drosophila, the apicobasal position of the two nuclei relative to the epithelial plane changes from vertical to horizontal after nutrient intake, which allows the volume of the MAG cavity to expand effectively. On the other hand, in the case of Cimex, the positions of the two nuclei do not change apicobasally in response to feeding, but their position relative to the proximodistal axis varies depending on the tubular/spherical organ morphology. Here, we report that the MAG of the benthic water bug Aphelocheirus vittatus (Matsumura) (Hemiptera: Aphelochiridae) shows binucleation in all epithelial cells. Despite the phylogenetically close relationship between Aphelocheirus and Cimex, the MAG cells in Aphelocheirus showed a Drosophila-like apicobasal change in the position of the two nuclei in response to feeding. Furthermore, the cytological processes during binucleation are more similar to those in Drosophila (incomplete cytokinesis) than to those in Cimex (cell fusion). These results indicate that the physiological role and mechanism of binucleation in MAG cells changed during the evolution of Hemiptera.

scholarly journals BMP signaling inhibition in Drosophila secondary cells remodels the seminal proteome and self and rival ejaculate functions

2019 ◽  
Vol 116 (49) ◽  
pp. 24719-24728 ◽  
Author(s):  
Ben R. Hopkins ◽  
Irem Sepil ◽  
Sarah Bonham ◽  
Thomas Miller ◽  
Philip D. Charles ◽  
...  
Keyword(s):  
Seminal Fluid ◽  
Cell Types ◽  
Bmp Signaling ◽  
Secretory Cells ◽  
Normal Female ◽  
Seminal Fluid Proteins ◽  
Accessory Glands ◽  
Offspring Production ◽  
Morphogenetic Protein ◽  
And Function

Seminal fluid proteins (SFPs) exert potent effects on male and female fitness. Rapidly evolving and molecularly diverse, they derive from multiple male secretory cells and tissues. In Drosophila melanogaster, most SFPs are produced in the accessory glands, which are composed of ∼1,000 fertility-enhancing “main cells” and ∼40 more functionally cryptic “secondary cells.” Inhibition of bone morphogenetic protein (BMP) signaling in secondary cells suppresses secretion, leading to a unique uncoupling of normal female postmating responses to the ejaculate: refractoriness stimulation is impaired, but offspring production is not. Secondary-cell secretions might therefore make highly specific contributions to the seminal proteome and ejaculate function; alternatively, they might regulate more global—but hitherto undiscovered—SFP functions and proteome composition. Here, we present data that support the latter model. We show that in addition to previously reported phenotypes, secondary-cell-specific BMP signaling inhibition compromises sperm storage and increases female sperm use efficiency. It also impacts second male sperm, tending to slow entry into storage and delay ejection. First male paternity is enhanced, which suggests a constraint on ejaculate evolution whereby high female refractoriness and sperm competitiveness are mutually exclusive. Using quantitative proteomics, we reveal changes to the seminal proteome that surprisingly encompass alterations to main-cell–derived proteins, indicating important cross-talk between classes of SFP-secreting cells. Our results demonstrate that ejaculate composition and function emerge from the integrated action of multiple secretory cell types, suggesting that modification to the cellular make-up of seminal-fluid-producing tissues is an important factor in ejaculate evolution.

scholarly journals BMP-signalling inhibition in Drosophila secondary cells remodels the seminal proteome, and self and rival ejaculate functions

2019 ◽  
Author(s):  
Ben R. Hopkins ◽  
Irem Sepil ◽  
Sarah Bonham ◽  
Thomas Miller ◽  
Philip D. Charles ◽  
...  
Keyword(s):  
Seminal Fluid ◽  
Cell Types ◽  
Secretory Cells ◽  
Normal Female ◽  
Seminal Fluid Proteins ◽  
Accessory Glands ◽  
Offspring Production ◽  
Use Efficiency ◽  
Bmp Signalling ◽  
And Function

ABSTRACTSeminal fluid proteins (SFPs) exert potent effects on male and female fitness. Rapidly evolving and molecularly diverse, they derive from multiple male secretory cells and tissues. In Drosophila melanogaster, most SFPs are produced in the accessory glands, which are composed of ∼1000 fertility-enhancing ‘main cells’ and ∼40, more functionally cryptic, ‘secondary cells’. Inhibition of BMP-signalling in secondary cells suppresses secretion, leading to a unique uncoupling of normal female post-mating responses to the ejaculate: refractoriness stimulation is impaired, but offspring production is not. Secondary cell secretions might therefore make a highly specific contribution to the seminal proteome and ejaculate function; alternatively, they might regulate more global – but hitherto-undiscovered – SFP functions and proteome composition. Here, we present data that supports the latter model. We show that in addition to previously reported phenotypes, secondary cell-specific BMP-signalling inhibition compromises sperm storage and increases female sperm use efficiency. It also impacts second male sperm, tending to slow entry into storage and delay ejection. First male paternity is enhanced, which suggests a novel constraint on ejaculate evolution whereby high female refractoriness and sperm competitiveness are mutually exclusive. Using quantitative proteomics, we reveal a mix of specific and widespread changes to the seminal proteome that surprisingly encompass alterations to main cell-derived proteins, indicating important cross-talk between classes of SFP-secreting cells. Our results demonstrate that ejaculate composition and function emerge from the integrated action of multiple secretory cell-types suggesting that modification to the cellular make-up of seminal fluid-producing tissues is an important factor in ejaculate evolution.

scholarly journals FACS-based isolation and RNA extraction of Secondary Cells from the Drosophila male Accessory Gland

2019 ◽  
Author(s):  
Clément Immarigeon ◽  
François Karch ◽  
Robert K. Maeda
Keyword(s):  
Cell Population ◽  
Seminal Fluid ◽  
Rna Extraction ◽  
Cell Types ◽  
Accessory Gland ◽  
Specific Cell ◽  
Male Accessory Gland ◽  
Accessory Gland Proteins ◽  
Accessory Glands ◽  
Study Gene Expression

ABSTRACTTo appreciate the function of an organ, it is often critical to understand the role of rare cell populations. Unfortunately, this rarity often makes it difficult to obtain material for study. This is the case for the Drosophila male accessory gland, the functional homolog of mammalian prostate and seminal vesicle. In Drosophila, this gland is made up of two morphologically distinct cell types: the polygonally-shaped main cells, which compose 96% of the organ, and the larger, vacuole-containing secondary cells (SCs), which represent the remaining 4% of cells (~40 cells per lobe). Both cell types are known to produce accessory gland proteins (Acps), which are important components of the seminal fluid and are responsible for triggering multiple physiological and behavioral processes in females, collectively called the post-mating response (PMR). While a few genes are known to be specific to the SCs, the relative rarity of SCs has hindered the study of their whole transcriptome. Here, a method allowing for the isolation of SCs is presented, enabling the extraction and sequencing of RNAs from this rare cell population. The protocol consists of dissection, protease digestion and mechanical dissociation of the glands to obtain individual cells. Then, the cells are sorted by FACS, and living GFP-expressing SC singulets are isolated for RNA extraction. This procedure is able to provide SC-specific RNAs from ~40 males per condition in the course of one day. Given the speed and low number of flies required, this method enables the use of downstream RT-qPCR and/or RNA sequencing to the study gene expression in the SCs from different genetic backgrounds, ages, mating statuses or environmental conditions.SUMMARYHere, we describe the dissociation and sorting of a specific cell population from the Drosophila male accessory glands (Secondary cells), followed by RNA extraction for sequencing and RT-qPCR. The dissociation consists of dissection, proteases digestion and mechanical dispersion, followed by FACS purification of GFP-expressing cells.

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