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The roles of cyclic guanosine monophosphate (cGMP) signaling in oocyte maturation attracts much attention in mammals, but its roles in fish are still largely unknown. Using zebrafish as a model, we demonstrated for the first time in fish that cGMP is involved in oocyte maturation, and its functional model in oocyte maturation is different from that of mammals. The intracellular cGMP could be regulated by nitric oxide (NO), we found that all three NO synthase enzymes and four soluble guanylyl cyclases (sGC) are expressed in the zebrafish ovary. Intriguingly, either the activation or inhibition of the NO/sGC/cGMP pathway in fully grown follicles could lead to oocyte maturation. During oocyte maturation, cGMP levels increased in the follicular cell layer but decreased in oocytes, while NO levels increased in follicular cells but remained constant in oocytes. Based on these findings in zebrafish, we propose a hypothetical model on the dual role of cGMP in oocyte maturation: in follicular cells the LH signal could increase the level of NO and cGMP which induces oocyte maturation, while in the oocyte the decreased cGMP level can also induce oocyte maturation. These findings help us to understand the molecular mechanism of fish oocyte maturation., (Copyright © 2018 The Authors. Published by Elsevier Inc. All rights reserved.)

Abstract Recently the importance of cyclic guanosine monophosphate (cGMP) signaling pathway in oocyte maturation has been well demonstrated in several species. However, as the primary downstream effector of the cGMP signaling pathway, little is known on the role of cGMP-dependent protein kinase (PKG) in oocyte maturation. In the present study, the expression, regulation and function of PKG in oocyte maturation was investigated in zebrafish. We identified four distinct PKG coding genes (named Prkg1a, Prkg1b, Prkg2, and Prkg3) in zebrafish. All prkgs are expressed in the ovary, and both prkg1a and prkg1b could be regulated by human chronic gonadotropin in follicular cells during oocyte maturation. We found that a cGMP analogue, 8-Br-cGMP, could stimulate oocyte maturation in a dose- and time-dependent manner. Such stimulatory effects of cGMP could be totally blocked by a PKG specific inhibitor, KT-5823. Intriguingly, we further found KT5823 could significantly attenuate spontaneous oocyte maturation in intact follicles but not in the denuded oocytes, suggesting that the activity of PKG in follicular cells is important for oocyte maturation. All of these results clearly demonstrate that PKG is involved in oocyte maturation in zebrafish. Highlights • Four PKG coding genes (Prkg1a, Prkg1b, Prkg2, and Prkg3) were identified in zebrafish. • Both prkg1a and prkg1b could be regulated by LH during oocyte maturation. • PKG activity is required for both cGMP-regulated and spontaneous oocyte maturation. • PKG activity in follicular cells is essential for oocyte maturation. [ABSTRACT FROM AUTHOR]