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 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 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.

scholarly journals Molecular Diversification of the Seminal Fluid Proteome in a Recently Diverged Passerine Species Pair

2019 ◽  
Vol 37 (2) ◽  
pp. 488-506 ◽  
Author(s):  
Melissah Rowe ◽  
Emma Whittington ◽  
Kirill Borziak ◽  
Mark Ravinet ◽  
Fabrice Eroukhmanoff ◽  
...  
Keyword(s):  
Seminal Fluid ◽  
Passer Domesticus ◽  
Species Pair ◽  
Seminal Fluid Proteins ◽  
Passerine Species ◽  
Immunity Genes ◽  
Evolutionary Genomic ◽  
Whole Genome Resequencing ◽  
And Function ◽  
Reproductive Processes

Abstract Seminal fluid proteins (SFPs) mediate an array of postmating reproductive processes that influence fertilization and fertility. As such, it is widely held that SFPs may contribute to postmating, prezygotic reproductive barriers between closely related taxa. We investigated seminal fluid (SF) diversification in a recently diverged passerine species pair (Passer domesticus and Passer hispaniolensis) using a combination of proteomic and comparative evolutionary genomic approaches. First, we characterized and compared the SF proteome of the two species, revealing consistencies with known aspects of SFP biology and function in other taxa, including the presence and diversification of proteins involved in immunity and sperm maturation. Second, using whole-genome resequencing data, we assessed patterns of genomic differentiation between house and Spanish sparrows. These analyses detected divergent selection on immunity-related SF genes and positive selective sweeps in regions containing a number of SF genes that also exhibited protein abundance diversification between species. Finally, we analyzed the molecular evolution of SFPs across 11 passerine species and found a significantly higher rate of positive selection in SFPs compared with the rest of the genome, as well as significant enrichments for functional pathways related to immunity in the set of positively selected SF genes. Our results suggest that selection on immunity pathways is an important determinant of passerine SF composition and evolution. Assessing the role of immunity genes in speciation in other recently diverged taxa should be prioritized given the potential role for immunity-related proteins in reproductive incompatibilities in Passer sparrows.

scholarly journals Endocycles support tissue growth and regeneration of the adult Drosophila accessory gland

2019 ◽  
Author(s):  
Allison M. Box ◽  
Samuel Jaimian Church ◽  
David Hayes ◽  
Shyama Nandakumar ◽  
Russell S. Taichman ◽  
...  
Keyword(s):  
Cell Size ◽  
Seminal Fluid ◽  
Cell Types ◽  
Accessory Gland ◽  
Tissue Growth ◽  
Critical Function ◽  
Seminal Fluid Proteins ◽  
Functional Analog ◽  
Secretory Epithelial Cell ◽  
Adult Drosophila

AbstractThe Drosophila melanogaster accessory gland is a functional analog of the mammalian prostate made up of two secretory epithelial cell types, termed main and secondary cells. This tissue is responsible for making and secreting seminal fluid proteins and other molecules that contribute to successful reproduction. Here we show that similar to the mammalian prostate, this tissue grows with age. We find that the adult accessory gland grows in part via endocycles to increase DNA content and cell size, independent of mating status. The differentiated, bi-nucleated main cells remain poised to endocycle in the adult gland and upregulation of signals that promote endocycling and tissue growth are sufficient to trigger dramatic endocycling leading to increases in cell size and ploidy. The main cells of this tissue remain poised to enter the cell cycle and endocycling of main cells increases during recovery from severe tissue damage. Our data establish that the adult accessory gland is not quiescent, but instead uses endocycles to maintain the accessory gland’s critical function throughout the fruit fly’s lifespan.

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.

Formation of spermatophore in ejaculatory duct of yellow mealworm beetle, Tenebrio molitor: SEM study

1992 ◽  
Vol 50 (1) ◽  
pp. 674-675
Author(s):  
Frantíšek Weyda ◽  
George M. Happ
Keyword(s):  
Seminal Fluid ◽  
Ejaculatory Duct ◽  
Tenebrio Molitor ◽  
High Viscosity ◽  
Secretory Cells ◽  
Main Role ◽  
Whole Process ◽  
Accessory Glands ◽  
Low Viscosity ◽  
Mealworm Beetle

Main role of the accessory glands of Tenebrio molitor male is to facilitate transfer of sperm to the females. They produce heterogeneous secretions. Two anatomically distinct glands are present. While the tubular accessory glands (TAG) are composed of the secretory cells of one type only, the bean-shaped accessory glands (BAG) consist of eight cellular types. Low viscosity secretion of the TAG mix with sperms forming seminal fluid while high viscosity secretions (spermatophorins) of the BAG are largely transformed into the insoluble wall and core of the spermatophore. The prespermatophoric mass is transferred to the ejaculatory duct (EJD) where solidify and forms the complex spermatophore. Immunocytochemical experiments with monoclonal antibodies based on the colloidal gold technique were used in order to understand exact composition of individual layers of the spermatophore. In the recent study we have used SEM to observe the whole process of the formation of spermatophore in the ejaculatory duct.

Single-nucleus transcriptomes reveal evolutionary and functional properties of cell types in the Drosophila accessory gland

Genetics ◽  
2021 ◽  
Author(s):  
Alex C Majane ◽  
Julie M Cridland ◽  
David J Begun
Keyword(s):  
Seminal Fluid ◽  
Ejaculatory Duct ◽  
Evolutionary Process ◽  
Cell Types ◽  
Accessory Gland ◽  
Male Reproduction ◽  
Seminal Fluid Proteins ◽  
Cell Diversity ◽  
Single Nucleus ◽  
First Time

Abstract Many traits responsible for male reproduction evolve quickly, including gene expression phenotypes in germline and somatic male reproductive tissues. Rapid male evolution in polyandrous species is thought to be driven by competition among males for fertilizations and conflicts between male and female fitness interests that manifest in post-copulatory phenotypes. In Drosophila, seminal fluid proteins secreted by three major cell types of the male accessory gland and ejaculatory duct are required for female sperm storage and use, and influence female post-copulatory traits. Recent work has shown that these cell types have overlapping but distinct effects on female post-copulatory biology, yet relatively little is known about their evolutionary properties. Here we use single-nucleus RNA-Seq of the accessory gland and ejaculatory duct from Drosophila melanogaster and two closely related species to comprehensively describe the cell diversity of these tissues and their transcriptome evolution for the first time. We find that seminal fluid transcripts are strongly partitioned across the major cell types, and expression of many other genes additionally define each cell type. We also report previously undocumented diversity in main cells. Transcriptome divergence was found to be heterogeneous across cell types and lineages, revealing a complex evolutionary process. Furthermore, protein adaptation varied across cell types, with potential consequences for our understanding of selection on male post-copulatory traits.

scholarly journals Sperm wars and the evolution of male fertility

Reproduction ◽  
2012 ◽  
Vol 144 (5) ◽  
pp. 519-534 ◽  
Author(s):  
Leigh W Simmons ◽  
John L Fitzpatrick
Keyword(s):  
Sperm Competition ◽  
Swimming Speed ◽  
Male Fertility ◽  
Seminal Fluid ◽  
Future Research ◽  
Sperm Length ◽  
Seminal Fluid Proteins ◽  
Control Male ◽  
Form And Function ◽  
And Function

Females frequently mate with several males, whose sperm then compete to fertilize available ova. Sperm competition represents a potent selective force that is expected to shape male expenditure on the ejaculate. Here, we review empirical data that illustrate the evolutionary consequences of sperm competition. Sperm competition favors the evolution of increased testes size and sperm production. In some species, males appear capable of adjusting the number of sperm ejaculated, depending on the perceived levels of sperm competition. Selection is also expected to act on sperm form and function, although the evidence for this remains equivocal. Comparative studies suggest that sperm length and swimming speed may increase in response to selection from sperm competition. However, the mechanisms driving this pattern remain unclear. Evidence that sperm length influences sperm swimming speed is mixed and fertilization trials performed across a broad range of species demonstrate inconsistent relationships between sperm form and function. This ambiguity may in part reflect the important role that seminal fluid proteins (sfps) play in affecting sperm function. There is good evidence that sfps are subject to selection from sperm competition, and recent work is pointing to an ability of males to adjust their seminal fluid chemistry in response to sperm competition from rival males. We argue that future research must consider sperm and seminal fluid components of the ejaculate as a functional unity. Research at the genomic level will identify the genes that ultimately control male fertility.

scholarly journals A General Role for Rab27a in Secretory Cells

2004 ◽  
Vol 15 (1) ◽  
pp. 332-344 ◽  
Author(s):  
Tanya Tolmachova ◽  
Ross Anders ◽  
Jane Stinchcombe ◽  
Giovanna Bossi ◽  
Gillian M. Griffiths ◽  
...  
Keyword(s):  
Fusion Protein ◽  
Knockout Mouse ◽  
Cell Types ◽  
Secretory Cells ◽  
Rab Gtpases ◽  
Specific Expression ◽  
General Role ◽  
Multistep Process ◽  
And Function ◽  
First Time

Vesicular transport is a complex multistep process regulated by distinct Rab GTPases. Here, we show for the first time that an EGFP-Rab fusion protein is fully functional in a mammalian organism. We constructed a PAC-based transgenic mouse, which expresses EGFP-Rab27a under the control of endogenous Rab27a promoter. The EGFP-Rab27a transgene was fully functional and rescued the two major defects of the ashen Rab27a knockout mouse. We achieved cell-specific expression of EGFP-Rab27a, which faithfully followed the pattern of expression of endogenous Rab27a. We found that Rab27a is expressed in an exceptionally broad range of specialized secretory cells, including exocrine (particularly in mucin- and zymogen-secreting cells), endocrine, ovarian, and hematopoietic cells, most of which undergo regulated exocytosis. We suggest that Rab27a acts in concert with Rab3 proteins in most regulated secretory events. The present strategy represents one way in which the complex pattern of expression and function of proteins involved in specialized cell types may be unraveled.

scholarly journals Experimental modification of rat pituitary growth hormone cell function during and after spaceflight

1996 ◽  
Vol 80 (3) ◽  
pp. 955-970 ◽  
Author(s):  
W. C. Hymer ◽  
R. E. Grindeland ◽  
T. Salada ◽  
P. Nye ◽  
E. J. Grossman ◽  
...  
Keyword(s):  
Growth Hormone ◽  
Cell Function ◽  
Cell Types ◽  
Secretory Cells ◽  
Mixed Cell ◽  
Pituitary Growth Hormone ◽  
Gh Cells ◽  
Growth Hormone Cell ◽  
And Function

Space-flown rats show a number of flight-induced changes in the structure and function of pituitary growth hormone (GH) cells after in vitro postflight testing (W. C. Hymen, R. E. Grindeland, I. Krasnov, I, Victorov, K. Motter, P. Mukherjee, K. Shellenberger, and M. Vasques. J. Appl. Physiol. 73, Suppl.: 151S-157S, 1992). To evaluate the possible effects of microgravity on growth hormone (GH) cells themselves, freshly dispersed rat anterior pituitary gland cells were seeded into vials containing serum +/- microM hydrocortisone (HC) before flight. Five different cell preparations were used: the entire mixed-cell population of various hormone-producing cell types, cells of density < 1.071 g/cm3 (band 1), cells of density > 1.071 g/cm3 (band 2), and cells prepared from either the dorsal or ventral part of the gland. Relative to ground control samples, bioactive GH released from dense cells during flight was reduced in HC-free medium but was increased in HC-containing medium. Band 1 and mixed cells usually showed opposite HC-dependent responses. Release of bioactive GH from ventral flight cells was lower; postflight responses to GH-releasing hormone challenge were reduced, and the cytoplasmic area occupied by GH in the dense cells was greater. Collectively, the data show that the chemistry and cellular makeup of the culture system modifies the response of GH cells to microgravity. As such, these cells offer a system to identify gravisensing mechanisms in secretory cells in future microgravity research.

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