Synthesis, depletion and cell-type expression of a protein from the male accessory glands of the dengue vector mosquito Aedes aegypti

Alfonso-Parra, Catalina; Avila, Frank W.; Deewatthanawong, Prasit; Sirot, Laura K.; Wolfner, Mariana F.; Harrington, Laura C.

doi:10.1016/j.jinsphys.2014.07.004

Cited by 31 publications

(34 citation statements)

References 38 publications

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“…Because the UPR is so well conserved, our approach can be extended to impair accessory gland function in other insects, if an AG-specific promoter (e.g. in Aedes aegypti [ 37 ]) is available to drive expression of the misfolded protein. Thus, this may provide a general method applicable to the control of fertility of insect vectors of human disease.…”

Section: Discussionmentioning

confidence: 99%

Induction of Excessive Endoplasmic Reticulum Stress in the Drosophila Male Accessory Gland Results in Infertility

et al. 2015

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Endoplasmic reticulum (ER) stress occurs when misfolded proteins accumulate in the lumen of the ER. A cell responds to ER stress with the unfolded protein response (UPR), a complex program of transcriptional and translational changes aimed at clearing misfolded proteins. Secretory tissues and cells are particularly well adapted to respond to ER stress because their function requires high protein production and secretory load. The insect male accessory gland (AG) is a secretory tissue involved in male fertility. The AG secretes many seminal fluid proteins (SFPs) essential for male reproduction. Among adult Drosophila tissues, we find that genes upregulated by ER stress are most highly expressed in the AG, suggesting that the AG is already undergoing high levels of ER stress due to its normal secretory functions. We hypothesized that induction of excessive ER stress in the AG above basal levels, would perturb normal function and provide a genetic tool for studying AG and SFP biology. To test this, we genetically induced excessive ER stress in the AG by conditional 1) expression of a misfolded protein or 2) knockdown of the UPR regulatory protein, BiP. Both genetic manipulations induced excessive ER stress in the AG, as indicated by the increase in Xbp1 splicing, a marker of ER stress. Both models resulted in a large decrease in or loss of SFP production and male infertility. Sperm production, motility, and transfer appeared unaffected. The induction of strong ER stress in the insect male AG may provide a simple way for studying or manipulating male fertility, as it eliminates AG function while preserving sperm production.

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Section: Discussionmentioning

confidence: 99%

Induction of Excessive Endoplasmic Reticulum Stress in the Drosophila Male Accessory Gland Results in Infertility

et al. 2015

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“…Previous work has demonstrated that Ae. 203 aegypti males become depleted after mating with three to five females in succession, and 204 seminal fluid is slowly regenerated over 48 h [46]. In our study, we provided males with 205 four virgin females for a period of 8 h to allow for male seminal fluid depletion.…”

Section: /30mentioning

confidence: 94%

“…Interestingly these vesicles, which may carry 715 RNA cargo including miRNAs, fuse with sperm and have the capacity to interact with 716 the female reproductive tract. Some male-derived transcripts are detectable in the 717 female for up to 24 h post-mating [46], and it has been postulated that they could be 718 used by females in some capacity [104]. In Ae.…”

Section: /30mentioning

confidence: 99%

“…Because males regenerate seminal fluid over the course of 48 h after depleting their 424 reserves by repeated insemination [46], we reasoned that MAG transcriptional 425 regulation after mating might inform our understanding of pathways required to restore 426 depleted SFPs. Differential expression analysis of virgin and mated MAGs' 427 transcriptomes revealed a significant bias towards gene upregulation in mated males, 428 with 320 transcripts that are upregulated and 126 that are downregulated after mating 429 (binomial test; p < 0.001; Figure 3A).…”

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confidence: 99%

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Reproductive functions and genetic architecture of the seminal fluid and sperm proteomes of the mosquitoAedes aegypti

Degner

Ahmed-Braimah

Borziak

et al. 2018

Preprint

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The yellow fever mosquito, Aedes aegypti, transmits several viruses, including dengue, Zika, and chikungunya. Some proposed efforts to control this vector involve manipulating reproduction to suppress wild populations or replacing them with disease-resistant mosquitoes. The design of such strategies requires an intimate knowledge of reproductive processes, yet our basic understanding of reproductive genetics in this vector remains largely incomplete. To accelerate future investigations, we have comprehensively catalogued sperm and seminal fluid proteins (SFPs) transferred to females in the ejaculate using tandem mass spectrometry. By excluding female-derived proteins using an isotopic labelling approach, we identified 870 sperm proteins and 280 seminal fluid proteins. Functional composition analysis revealed parallels with known aspects of sperm biology and SFP function in other insects. To corroborate our proteome characterization, we also generated transcriptomes for testes and the male accessory glands-the primary contributors to Ae. aegypti sperm and seminal fluid, respectively. Differential gene expression of accessory glands from virgin and mated males suggests that protein translation is upregulated post-mating. Several SFP transcripts were also modulated after mating, but >90% remained unchanged. Finally, a significant enrichment of SFPs was observed on chromosome 1, which harbors the male sex determining locus in this species. Our study provides a comprehensive proteomic and transcriptomic characterization of ejaculate production and composition and thus provides a foundation for future investigations of Ae. aegypti reproductive biology, from functional analysis of individual proteins to broader examination of reproductive processes.

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“…During copulation, males are thought to transfer a cocktail of sperm and SFPs, but 533 recent work has shown that males can also transfer mRNAs that can be detected in 534 the female's post-mating transcriptome [35,91]. In both of the reported cases in 535 insects, the mRNAs appear to originate from the male accessory glands as the mRNAs 536 are derived from known SFP genes or show strong expression bias in the accessory 537 glands.…”

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Differences in post-mating transcriptional responses between conspecific and heterospecific matings inDrosophila

Ahmed-Braimah

Wolfner

Clark

2020

Preprint

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In many animal species, females undergo physiological and behavioral changes after mating. Some of these changes are driven by male-derived seminal fluid proteins, and are critical for fertilization success. Unfortunately, our understanding of the molecular interplay between female and male reproductive proteins remains superficial. Here we analyze the post-mating response in a Drosophila species that has evolved strong gametic incompatibility with its sister species; D. novamexicana females produce only 1% fertilized eggs in crosses with D. americana males, compared to ~98% produced in within-species crosses. This incompatibility is likely caused by mismatched male and female reproductive molecules. In this study we use short-read RNA sequencing to examine the evolutionary dynamics of female reproductive genes and the post-mating transcriptome response in crosses within and between species. First, we found that most female reproductive tract genes are slow-evolving compared to the genome average. Second, post-mating responses in con- and heterospecific matings are largely congruent, but heterospecific mating induces expression of additional stress-response genes. Some of those are immunity genes that are activated by the Imd pathway. We also identify several genes in the JAK/STAT signaling pathway that are induced in heterospecific, but not conspecific mating. While this immune response was most pronounced in the female reproductive tract, we also detect it in the female head and ovaries. Our results show that the female’s post-mating transcriptome-level response is determined in part by the genotype of the male, and that divergence in male reproductive genes and/or traits can have immunogenic effects on females.

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Synthesis, depletion and cell-type expression of a protein from the male accessory glands of the dengue vector mosquito Aedes aegypti

Cited by 31 publications

References 38 publications

Induction of Excessive Endoplasmic Reticulum Stress in the Drosophila Male Accessory Gland Results in Infertility

Induction of Excessive Endoplasmic Reticulum Stress in the Drosophila Male Accessory Gland Results in Infertility

Reproductive functions and genetic architecture of the seminal fluid and sperm proteomes of the mosquitoAedes aegypti

Differences in post-mating transcriptional responses between conspecific and heterospecific matings inDrosophila

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