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Structure of the gilthead seabream spermatic duct. Photographs (A, B) and histological sections stained with H&E (C, D) of the spermatic duct from males at the resting and spermiating stage. Scale bars: 5 lm. C, cilia (extended microvilli); Ec, epithelial cell; Ic, interstitial cell; SD, spermatic duct; Smf, smooth muscle fiber; Sz, spermatozoa; TMD, testicular main duct.
Source publication
Aquaporin‐mediated fluid transport in the mammalian efferent duct and epididymis is believed to play a role in sperm maturation and concentration. In fish, such as the marine teleost gilthead seabream (Sparus aurata), the control of fluid homeostasis in the spermatic duct seems also to be crucial for male fertility, but no information exists on the...
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... cilia of the epithelial cells of the spermatic duct elongate during the spermiation period Anatomical analysis confims that in the gilthead seabream the spermatic duct originates from the testicular main duct and ends in the gonopore ( Fig. 2A,B). At the resting stage, the spermatic duct appears as a thin and translucent conduct with the lumen free of spermatozoa ( Fig. 2A). During spermiation, coinciding with the strong increase in the size of the testis and the gonadosomatic index ( Boj et al. 2015b), the spermatic duct becomes larger and longer and appears filled with sperm ...
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... cells of the spermatic duct elongate during the spermiation period Anatomical analysis confims that in the gilthead seabream the spermatic duct originates from the testicular main duct and ends in the gonopore ( Fig. 2A,B). At the resting stage, the spermatic duct appears as a thin and translucent conduct with the lumen free of spermatozoa ( Fig. 2A). During spermiation, coinciding with the strong increase in the size of the testis and the gonadosomatic index ( Boj et al. 2015b), the spermatic duct becomes larger and longer and appears filled with sperm (Fig. 2B). Histological analyses on transversal sections of the spermatic duct reveal that at the resting stage the spermatic duct ...
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... Fig. 2A,B). At the resting stage, the spermatic duct appears as a thin and translucent conduct with the lumen free of spermatozoa ( Fig. 2A). During spermiation, coinciding with the strong increase in the size of the testis and the gonadosomatic index ( Boj et al. 2015b), the spermatic duct becomes larger and longer and appears filled with sperm (Fig. 2B). Histological analyses on transversal sections of the spermatic duct reveal that at the resting stage the spermatic duct is composed by a monolayered unfolded epithelium external to a smooth muscle fiber array, where some dispersed interstitial/laminal cells are observed ( Fig. 2C). At this stage, the epithelial cells show scarce ...
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... duct becomes larger and longer and appears filled with sperm (Fig. 2B). Histological analyses on transversal sections of the spermatic duct reveal that at the resting stage the spermatic duct is composed by a monolayered unfolded epithelium external to a smooth muscle fiber array, where some dispersed interstitial/laminal cells are observed ( Fig. 2C). At this stage, the epithelial cells show scarce sterocilia (microvilli; Fig. 2C). In contrast, at the spermiating stage the height of the epithelium increases and folds, as the epithelial cells elongated and exhibit cilia and vacuoles, probably reflecting the apocrine secretive stage of the cells (Fig. 2D). Trapped spermatozoa in the ...
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... analyses on transversal sections of the spermatic duct reveal that at the resting stage the spermatic duct is composed by a monolayered unfolded epithelium external to a smooth muscle fiber array, where some dispersed interstitial/laminal cells are observed ( Fig. 2C). At this stage, the epithelial cells show scarce sterocilia (microvilli; Fig. 2C). In contrast, at the spermiating stage the height of the epithelium increases and folds, as the epithelial cells elongated and exhibit cilia and vacuoles, probably reflecting the apocrine secretive stage of the cells (Fig. 2D). Trapped spermatozoa in the cilia can be observed in the vicinity of the epithelium (Fig. ...
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... cells are observed ( Fig. 2C). At this stage, the epithelial cells show scarce sterocilia (microvilli; Fig. 2C). In contrast, at the spermiating stage the height of the epithelium increases and folds, as the epithelial cells elongated and exhibit cilia and vacuoles, probably reflecting the apocrine secretive stage of the cells (Fig. 2D). Trapped spermatozoa in the cilia can be observed in the vicinity of the epithelium (Fig. ...
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... sterocilia (microvilli; Fig. 2C). In contrast, at the spermiating stage the height of the epithelium increases and folds, as the epithelial cells elongated and exhibit cilia and vacuoles, probably reflecting the apocrine secretive stage of the cells (Fig. 2D). Trapped spermatozoa in the cilia can be observed in the vicinity of the epithelium (Fig. ...
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... cilia of the epithelial cells of the spermatic duct elongate during the spermiation period Anatomical analysis confims that in the gilthead seabream the spermatic duct originates from the testicular main duct and ends in the gonopore ( Fig. 2A,B). At the resting stage, the spermatic duct appears as a thin and translucent conduct with the lumen free of spermatozoa ( Fig. 2A). During spermiation, coinciding with the strong increase in the size of the testis and the gonadosomatic index ( Boj et al. 2015b), the spermatic duct becomes larger and longer and appears filled with sperm ...
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... cells of the spermatic duct elongate during the spermiation period Anatomical analysis confims that in the gilthead seabream the spermatic duct originates from the testicular main duct and ends in the gonopore ( Fig. 2A,B). At the resting stage, the spermatic duct appears as a thin and translucent conduct with the lumen free of spermatozoa ( Fig. 2A). During spermiation, coinciding with the strong increase in the size of the testis and the gonadosomatic index ( Boj et al. 2015b), the spermatic duct becomes larger and longer and appears filled with sperm (Fig. 2B). Histological analyses on transversal sections of the spermatic duct reveal that at the resting stage the spermatic duct ...
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... Fig. 2A,B). At the resting stage, the spermatic duct appears as a thin and translucent conduct with the lumen free of spermatozoa ( Fig. 2A). During spermiation, coinciding with the strong increase in the size of the testis and the gonadosomatic index ( Boj et al. 2015b), the spermatic duct becomes larger and longer and appears filled with sperm (Fig. 2B). Histological analyses on transversal sections of the spermatic duct reveal that at the resting stage the spermatic duct is composed by a monolayered unfolded epithelium external to a smooth muscle fiber array, where some dispersed interstitial/laminal cells are observed ( Fig. 2C). At this stage, the epithelial cells show scarce ...
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... duct becomes larger and longer and appears filled with sperm (Fig. 2B). Histological analyses on transversal sections of the spermatic duct reveal that at the resting stage the spermatic duct is composed by a monolayered unfolded epithelium external to a smooth muscle fiber array, where some dispersed interstitial/laminal cells are observed ( Fig. 2C). At this stage, the epithelial cells show scarce sterocilia (microvilli; Fig. 2C). In contrast, at the spermiating stage the height of the epithelium increases and folds, as the epithelial cells elongated and exhibit cilia and vacuoles, probably reflecting the apocrine secretive stage of the cells (Fig. 2D). Trapped spermatozoa in the ...
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... analyses on transversal sections of the spermatic duct reveal that at the resting stage the spermatic duct is composed by a monolayered unfolded epithelium external to a smooth muscle fiber array, where some dispersed interstitial/laminal cells are observed ( Fig. 2C). At this stage, the epithelial cells show scarce sterocilia (microvilli; Fig. 2C). In contrast, at the spermiating stage the height of the epithelium increases and folds, as the epithelial cells elongated and exhibit cilia and vacuoles, probably reflecting the apocrine secretive stage of the cells (Fig. 2D). Trapped spermatozoa in the cilia can be observed in the vicinity of the epithelium (Fig. ...
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... cells are observed ( Fig. 2C). At this stage, the epithelial cells show scarce sterocilia (microvilli; Fig. 2C). In contrast, at the spermiating stage the height of the epithelium increases and folds, as the epithelial cells elongated and exhibit cilia and vacuoles, probably reflecting the apocrine secretive stage of the cells (Fig. 2D). Trapped spermatozoa in the cilia can be observed in the vicinity of the epithelium (Fig. ...
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... sterocilia (microvilli; Fig. 2C). In contrast, at the spermiating stage the height of the epithelium increases and folds, as the epithelial cells elongated and exhibit cilia and vacuoles, probably reflecting the apocrine secretive stage of the cells (Fig. 2D). Trapped spermatozoa in the cilia can be observed in the vicinity of the epithelium (Fig. ...
Citations
... Samples were processed and immunostained as previously described (Chauvigné et al. 2018). Control sections were incubated without primary antibodies (when using commercial antibodies) or with antibodies preincubated with the corresponding peptides used for immunization (for custom-made antibodies). ...
Aquaporin-mediated oocyte hydration is considered important for the evolution of pelagic eggs and the radiative success of marine teleosts. However, the molecular regulatory mechanisms controlling this vital process are not fully understood. Here, we analyzed >400 piscine genomes to uncover a previously unknown teleost-specific aquaporin-1 cluster (TSA1C) comprised of tandemly arranged aqp1aa-aqp1ab2-aqp1ab1 genes. Functional evolutionary analysis of the TSA1C reveals a ∼300-million-year history of downstream aqp1ab-type gene loss, neofunctionalization and subfunctionalization, but with marine species that spawn highly hydrated pelagic eggs almost exclusively retaining at least one of the downstream paralogs. Unexpectedly, one third of the modern marine euacanthomorph teleosts selectively retain both aqp1ab-type channels, and co-evolved protein kinase-mediated phosphorylation sites in the intracellular subdomains together with teleost-specific Ywhaz-like (14-3-3ζ-like) binding proteins for co-operative membrane trafficking regulation. To understand the selective evolutionary advantages of these mechanisms, we show that a two-step regulated channel shunt avoids competitive occupancy of the same plasma membrane space in the oocyte and accelerates hydration. These data suggest that the evolution of the adaptive molecular regulatory features of the TSA1C facilitated the rise of pelagic eggs and their subsequent geodispersal in the oceanic currents.
... In teleosts, AQPs support spermatogenesis, spermiation, sperm motility, and participate in controlling the composition of seminal fluid in the spermatic duct Chauvign e et al., 2018;Chauvign e et al., 2011;Zilli et al., 2009). In sea bream testis, hormonal control of AQP/aqp expression varies depending upon the developmental stage of the tissue (Boj, Chauvign e, Zapater, & Cerdà, 2015). ...
... Collectively, these patterns demonstrate that tight temporal regulation of multiple AQPs underlies fluid transport necessary for sperm production. It was recently revealed that nine AQPs are expressed in the spermatic duct of sea bream where they presumably support the further maturation and nourishment of sperm (Chauvign e et al., 2018). Whether hormones regulate AQPs in the spermatic duct is unknown; estrogens and progestins are candidates given their activities in mammalian spermatic duct (Chauvign e et al., 2018). ...
Comparative studies over the last two decades have revealed that fishes leverage aquaporins (AQPs) to facilitate the movements of water, small non-ionic solutes, and gases across cell membranes. Accordingly, AQPs are expressed in tissues responsible for maintaining hydromineral balance of the whole organism. In teleost fishes, threats to hydromineral balance imposed by fluctuations in environmental salinity are met with the activation of multiple endocrine axes. This chapter first discusses recent advances in our understanding of how hormones control the expression of AQPs in tissues that support hydromineral balance, namely the gastrointestinal tract, kidney, and gill. The second objective of this chapter is to review how hormones regulate teleost AQPs in support of fluid transport processes underlying the production of gametes specialized for release into aquatic environments.
... Various AQP isoforms have been studied in gills, kidneys and intestinal epithelium for their expression with reference to changes in environmental salinity (Giffard-Mena et al., 2007) and suggested to have a critical role of AQPs in osmoregulation. However, presence of AQPs in testis, spermatic duct and spermatozoa (Watanabe et al., 2009;Zilli et al., 2009;Cerdà and Finn, 2010;Chaube et al., 2011;Boj et al., 2015 andChauvigne et al., 2018) imply its role in reproduction in general, specifically hydration of the seminal fluid and in sperm physiology. Similar role of AQP in oocyte hydration was reported in sea bream (Fabra et al., 2005). ...
... In teleost, few studies reported AQP3 from teleost gill, intestine, oesophagus, eye, kidney, intestine and rectum (Cutler and Cramb, 2002;Watanabe et al., 2005;Cutler et al., 2007;Kim et al., 2014: Salati et al., 2014 and for the first time AQP3a was reported from zebrafish testis (Tingaud-Sequeira et al., 2010). In a recent study, AQP3a has been localized in different interstitial/lamina cells of spermatic ducts in gilthead sea bream (Chauvigne et al., 2018). Very limited information is available with respect to the presence of AQP3a in gonads and its expression during reproduction. ...
... The group of aquaglyceroporins which includes AQP3, AQP7, AQP9, and AQP10, are non-selective water channels which are permeable to glycerol, urea and other small non-electrolytes as well as to water (Borgnia et al., 1999;Agre et al., 2002;Ishibashi et al., 2002). Aquaglyceroporins (AQP3a,-7,-9b, and -10b) are reported from the spermatic duct of gilt head sea bream along with water selective AQPs (Chauvigne et al., 2018). The present study aimed at identifying AQP3a gene in C. carpio and its expression in gonadal tissues during reproduction. ...
Aquaporins are suggested to be involved in hydration, activation and final release of gametes. Aquaporin3a (AQP3a) was cloned and sequenced from Cyprinus carpio to investigate its role in reproduction. AQP3a was amplified with primers based on conserved regions of other related species. 5′ and 3′ end were amplified using RACE PCR. The predicted protein showed the typical six transmembrane domains and two Asn-Pro-Ala (NPA) motifs conserved among the members of the AQP superfamily. The phylogenetic analysis based on AQP3a complete sequence showed the similarity between C. carpio and Carassius auratus. During differential tissue expression study of AQP3a using real-time PCR, highest expression was seen in testis followed by gill, skin, eye, liver, muscle, and kidney. The seasonal expression in both testis and ovary showed highest in spawning phase (June–July) than that of preparatory phase (March–April) and resting phase (September–October). The expression was higher in testis as compared to the ovary in the entire phases studied, even though the trend was similar. On induced breeding, AQP3a transcripts were found more after 5 h post ovatide injection in male and 24 h post ovatide injection in female as compared to the control testis and ovary respectively. Sharp decline after the spermiation/ovulation suggests its role in controlling water and other solute movements across the membrane during spawning.
The dual aquaporin (Aqp1ab1/Aqp1ab2)-mediated hydration of marine teleost eggs, which occurs during oocyte meiosis resumption (maturation), is considered a key adaptation underpinning their evolutionary success in the oceans. However, the endocrine signals controlling this mechanism are almost unknown. Here, we investigated whether the nonapeptides arginine vasopressin (Avp, formerly vasotocin) and oxytocin (Oxt, formerly isotocin) are involved in marine teleost oocyte hydration using the gilthead seabream ( Sparus aurata ) as a model. We show that concomitant with an increased systemic production of Avp and Oxt, the nonapeptides are also produced and accumulated locally in the ovarian follicles during oocyte maturation and hydration. Functional characterization of representative Avp and Oxt receptor subtypes indicates that Avpr1aa and Oxtrb, expressed in the postvitellogenic oocyte, activate phospholipase C and protein kinase C pathways, while Avpr2aa, which is highly expressed in the oocyte and in the follicular theca and granulosa cells, activates the cAMP-protein kinase A (PKA) cascade. Using ex vivo, in vitro and mutagenesis approaches, we determined that Avpr2aa plays a major role in the PKA-mediated phosphorylation of the aquaporin subdomains driving membrane insertion of Aqp1ab2 in the theca and granulosa cells, and of Aqp1ab1 and Aqp1ab2 in the distal and proximal regions of the oocyte microvilli, respectively. The data further indicate that luteinizing hormone, which surges during oocyte maturation, induces the synthesis of Avp in the granulosa cells via progestin production and the nuclear progestin receptor. Collectively, our data suggest that both the neurohypophysial and paracrine vasopressinergic systems integrate to differentially regulate the trafficking of the Aqp1ab-type paralogs via a common Avp-Avpr2aa-PKA pathway to avoid competitive occupancy of the same plasma membrane space and maximize water influx during oocyte hydration.
Comparative studies over the last two decades have revealed that fishes leverage aquaporins (AQPs) to facilitate the movements of water, small non-ionic solutes, and gases across cell membranes. Accordingly, AQPs are expressed in tissues responsible for maintaining hydromineral balance of the whole organism. In teleost fishes, threats to hydromineral balance imposed by fluctuations in environmental salinity are met with the activation of multiple endocrine axes. This chapter first discusses recent advances in our understanding of how hormones control the expression of AQPs in tissues that support hydromineral balance, namely the gastrointestinal tract, kidney, and gill. The second objective of this chapter is to review how hormones regulate teleost AQPs in support of fluid transport processes underlying the production of gametes specialized for release into aquatic environments.
