An evolutionary conserved interaction between the Gcm transcription factor and the SF1 nuclear receptor in the female reproductive system

Cattenoz, Pierre B.; Delaporte, Claude; Bazzi, Wael; Giangrande, Angela

doi:10.1038/srep37792

Cited by 8 publications

(6 citation statements)

References 85 publications

(153 reference statements)

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“…Multiple factors have been linked to sperm longevity, including ions, sugars, pH, antioxidants, and enzymes for energy metabolism [13][14][15][16][17][18]. However, the current understanding of biochemical and physiological processes within the spermathecae is incomplete.…”

Section: Introductionmentioning

confidence: 99%

Transcriptional profiling and physiological roles of Aedes aegypti spermathecal-related genes

et al. 2020

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Background: Successful mating of female mosquitoes typically occurs once, with the male sperm being stored in the female spermatheca for every subsequent oviposition event. The female spermatheca is responsible for the maintenance, nourishment, and protection of the male sperm against damage during storage. Aedes aegypti is a major vector of arboviruses, including Yellow Fever, Dengue, Chikungunya, and Zika. Vector control is difficult due to this mosquito high reproductive capacity. Results: Following comparative RNA-seq analyses of spermathecae obtained from virgin and inseminated females, eight transcripts were selected based on their putative roles in sperm maintenance and survival, including energy metabolism, chitin components, transcriptional regulation, hormonal signaling, enzymatic activity, antimicrobial activity, and ionic homeostasis. In situ RNA hybridization confirmed tissue-specific expression of the eight transcripts. Following RNA interference (RNAi), observed outcomes varied between targeted transcripts, affecting mosquito survival, egg morphology, fecundity, and sperm motility within the spermathecae. Conclusions: This study identified spermatheca-specific transcripts associated with sperm storage in Ae. aegypti. Using RNAi we characterized the role of eight spermathecal transcripts on various aspects of female fecundity and offspring survival. RNAi-induced knockdown of transcript AeSigP-66,427, coding for a Na + /Ca 2+ protein exchanger, specifically interfered with egg production and reduced sperm motility. Our results bring new insights into the molecular basis of sperm storage and identify potential targets for Ae. aegypti control.

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Section: Introductionmentioning

confidence: 99%

Transcriptional profiling and physiological roles of Aedes aegypti spermathecal-related genes

et al. 2020

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“…We have shown that dynamic Notch signaling regulates binary fate determination in Drosophila spermathecal lineage (Shen and Sun, 2017). Drosophila spermatheca is a class-III insect gland containing ∼80 secretory units that produce essential secretions for sperm storage and ovulation (Filosi and Perotti, 1975;Schnakenberg et al, 2011;Sun and Spradling, 2013;Cattenoz et al, 2016). Lineage-tracing experiments show that spermathecal gland precursors (P0) in the genital imaginal disc proliferate to give rise to one secretory unit precursor (SUP) and one lumen epithelial precursor (LEP) around 26 hours (h) after puparium formation (APF; Sun and Spradling, 2012;Fig.…”

Section: Introductionmentioning

confidence: 99%

Different modes of Notch activation and strength regulation in the spermathecal secretory lineage

Shen

Sun

2020

Development

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The strength of Notch signaling contributes to pleiotropic actions of Notch; however, we do not yet have a full understanding of the molecular regulation of Notch-signaling strength. We have investigated the mode of Notch activation in binary fate specification in the Drosophila spermathecal linage, where Notch is asymmetrically activated across three divisions to specify different cell fates. Using clonal analysis, we show that Delta (Dl) serves as the ligand for Notch in the first and second divisions. Dl and Serrate (Ser) function redundantly in the third division. Compared with the third division, cell-fate decision in the second division requires a lower level of Suppressor of Hairless protein, and, consequently, a lower level of Notch signaling. Several Notch endosomal trafficking regulators differentially regulate Notch signaling between the second and third divisions. Here, we demonstrate that cell differentiation in spermathecae involves different Notch-activation modes, Notchsignaling strengths and Notch-trafficking regulations. Thus, the Drosophila spermathecal lineage is an exciting model for probing the molecular mechanisms that modulate the Notch signaling pathway.

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“…This is likely true in other insect species ( Shaw et al 2014 ). In addition, glandular secretions from spermathecae and parovaria regulate ovulation and egg laying ( Schnakenberg et al 2011 ; Sun and Spradling 2013 ; Cattenoz et al 2016 ). Although the exact identities of the secreted products regulating sperm and ovulation are unknown, it is clear that secretions through the canonical protein secretory pathway are required for sperm storage but not ovulation ( Sun and Spradling 2013 ).…”

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confidence: 99%

“…The sex determination cascade activates the runt-domain transcription factor Lozenge (Lz) in these primordial cells, which is essential for gland formation ( Anderson 1945 ; Chatterjee et al 2011 ; Sun and Spradling 2012 ). NR5A-family nuclear receptor Hr39 regulates the proliferation, survival, and protrusion of these primordial cells during early pupae development; Hr39 expression is likely regulated by the transcription factor Glial cell missing ( Allen and Spradling 2008 ; Sun and Spradling 2012 ; Cattenoz et al 2016 ). Precursor cells except those at the middle region of the spermathecal head continue to express Lz and differentiate into epithelia cells (ECs) to form adult spermathecal lumen and duct.…”

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confidence: 99%

Dynamic Notch Signaling Specifies Each Cell Fate inDrosophilaSpermathecal Lineage

Shen

Sun

2017

G3 Genes|Genomes|Genetics

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Spermathecae are glandular organs in the insect female reproductive tract that play essential roles in insect reproduction; however, the molecular mechanism involved in their development is largely unknown. Drosophila spermathecae consist of class-III secretory units, in which each secretory cell (SC) discharges its products to the central lumen through an end-apparatus and a canal. Secretory unit formation in Drosophila spermathecae utilizes a fixed cell lineage, in which each secretory unit precursor (SUP) divides to produce one pIIb cell and one pIIa cell. The former differentiates into an apical cell (AC), whereas the latter divides again to produce an SC and a basal cell (BC). It is unclear how each cell acquires its identity and contributes to secretory unit formation. Here, we demonstrate that Notch signaling is required and sufficient for the specification of lumen epithelial precursors (LEPs; vs. SUPs), pIIb (vs. pIIa), and SCs (vs. BCs) sequentially. To our surprise, Notch activation in LEPs and SCs apparently utilizes different ligand mechanisms. In addition, Notch signaling both suppresses and activates transcription factors Hindsight (Hnt) and Cut during spermathecal lineage specification, supporting the notion that Notch signaling can have opposite biological outcomes in different cellular environments. Furthermore, LEP-derived epithelial cells (ECs) and ACs show distinct cellular morphology and are essential for securing secretory units to the epithelial lumen. Our work demonstrates, for the first time, the dynamic role of Notch signaling in binary cell fate determination in Drosophila spermathecae and the role of ECs and ACs in secretory unit formation. KEYWORDSclass-III secretory gland spermathecae Notch signaling binary cell fate determination Cut Spermathecae are sperm-storage organs found in the female reproductive tract of many insect species, and they are important for reproduction and cryptic female choice (Eberhard 1996;Pitnick et al. 1999;Manier et al. 2010). Studies in Drosophila have shown that glandular secretions from spermathecae and parovaria act to attract, nourish, and protect sperm by creating an appropriate environment (Filosi and Perotti 1975;Allen and Spradling 2008;Prokupek et al. 2008Prokupek et al. , 2009Schnakenberg et al. 2011;Sun and Spradling 2013). This is likely true in other insect species (Shaw et al. 2014). In addition, glandular secretions from spermathecae and parovaria regulate ovulation and egg laying (Schnakenberg et al. 2011;Sun and Spradling 2013;Cattenoz et al. 2016). Although the exact identities of the secreted products regulating sperm and ovulation are unknown, it is clear that secretions through the canonical protein secretory pathway are required for sperm storage but not ovulation (Sun and Spradling 2013). Despite recent progress on the physiology of spermatheca secretion, the molecular mechanisms involved in spermathecal gland formation are largely unknown.Spermathecae in Drosophila melanogaster are a pair of mushroomshaped organs with a h...

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An evolutionary conserved interaction between the Gcm transcription factor and the SF1 nuclear receptor in the female reproductive system

Cited by 8 publications

References 85 publications

Transcriptional profiling and physiological roles of Aedes aegypti spermathecal-related genes

Transcriptional profiling and physiological roles of Aedes aegypti spermathecal-related genes

Different modes of Notch activation and strength regulation in the spermathecal secretory lineage

Dynamic Notch Signaling Specifies Each Cell Fate inDrosophilaSpermathecal Lineage

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