Neurohypophysial and paracrine vasopressinergic signaling regulates aquaporin trafficking to hydrate marine teleost oocytes
Author
Ferré, Alba
Chauvigné, François
Gozdowska, Magdalena
Kulczykowska, Ewa
Publication date
2023-08-11ISSN
1664-2392
Abstract
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.
Document Type
Article
Document version
Published version
Language
English
Subject (CDU)
637 - Produce of domestic (farmyard) animals and game
Pages
19
Publisher
Frontiers
Is part of
Frontiers in Endocrinology
Citation
Ferré, Alba, François Chauvigné, Magdalena Gozdowska, Ewa Kulczykowska, Roderick Nigel Finn, and Joan Cerdà. 2023. “Neurohypophysial and paracrine vasopressinergic signaling regulates aquaporin trafficking to hydrate marine teleost oocytes”. Frontiers in Endocrinology 14: 1222724. doi: 10.3389/fendo.2023.1222724
Grant agreement number
MINECO/Programa Estatal de I+D+I orientada a los retos de la sociedad/AGL2016-76802-R/ES/Canales de agua e ionicos como nuevos marcadores de estrés oxidativo y cinemáticos de la calidad del esperma en teleosteos marinos/SPERMIOPORIN
FEDER/ / /EU/ /
Program
Aqüicultura
This item appears in the following Collection(s)
- ARTICLES CIENTÍFICS [2555]
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Except where otherwise noted, this item's license is described as http://creativecommons.org/licenses/by/4.0/