Institute of Agrifood Research and Technology (IRTA)-Institute of Biotechnology and Biomedicine (IBB), Universitat Autònoma de Barcelona, Barcelona, Spain.
Institute of Marine Sciences, Spanish National Research Council (CSIC), Barcelona, Spain.
Front Endocrinol (Lausanne). 2023 Aug 11;14:1222724. doi: 10.3389/fendo.2023.1222724. eCollection 2023.
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 () 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 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 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 a common Avp-Avpr2aa-PKA pathway to avoid competitive occupancy of the same plasma membrane space and maximize water influx during oocyte hydration.
海洋硬骨鱼类卵母细胞在减数分裂恢复（成熟）过程中发生的双水通道蛋白 (Aqp1ab1/Aqp1ab2) 介导的水合作用，被认为是它们在海洋中成功进化的关键适应。然而，控制这种机制的内分泌信号几乎未知。在这里，我们使用金头鲷 () 作为模型，研究了非肽类血管加压素 (Avp，以前称为血管升压素) 和催产素 (Oxt，以前称为缩宫素) 是否参与海洋硬骨鱼类卵母细胞的水合作用。我们表明，随着 Avp 和 Oxt 系统产生增加，非肽类物质也在卵母细胞成熟和水合过程中在卵巢滤泡中局部产生和积累。代表性 Avp 和 Oxt 受体亚型的功能表征表明，在卵黄后期卵母细胞中表达的 Avpr1aa 和 Oxtrb 激活磷脂酶 C 和蛋白激酶 C 途径，而在卵母细胞中和滤泡的内膜和颗粒细胞中高度表达的 Avpr2aa 则激活 cAMP-蛋白激酶 A (PKA) 级联反应。使用 和诱变方法，我们确定 Avpr2aa 在 PKA 介导的 Aqp1ab2 亚域磷酸化中起主要作用，该磷酸化驱动 Aqp1ab2 在膜插入内膜和颗粒细胞中，以及 Aqp1ab1 和 Aqp1ab2 在卵母细胞微绒毛的远端和近端区域。数据还表明，促黄体激素在卵母细胞成熟过程中激增，诱导颗粒细胞中 Avp 的合成 孕激素的产生和核孕激素受体。总的来说，我们的数据表明，神经垂体和旁分泌血管加压素系统整合，以差异调节 Aqp1ab 型同源物的运输 - 共同的 Avp-Avpr2aa-PKA 途径，以避免同一质膜空间的竞争占据并在卵母细胞水合过程中最大限度地增加水流入。
