Role of Arachidonic Acid and Protein Kinase C During Maturation-Inducing Hormone-Dependent Meiotic Resumption and Ovulation in Ovarian Follicles of Atlantic Croaker1

Abstract

The roles of arachidonic acid (AA) and protein kinase C (PKC) during in vitro maturation-inducing hormone (MIH)-dependent meiotic resumption (maturation) and ovulation were studied in ovarian follicles of Atlantic croaker (Micropogonias undulatus). The requirement for cyclooxygenase (COX) metabolites of AA was examined using a nonspecific COX inhibitor, indomethacin (IM), as well as two COX products, prostaglandin (PG) F(2alpha) and PGE(2), whereas the role of lipoxygenase (LOX) was investigated using a specific LOX inhibitor, nordihydroguaiaretic acid (NDGA). The involvement of PKC was examined using phorbol 12-myristate 13-acetate (PMA), a PKC activator, as well as GF109203X (GF), a specific inhibitor of PKC and 1-(5-isoquinolinesulfonyl)-2-methylpiperazine (H7), nonspecific inhibitor of protein kinases. Genomic mechanisms were examined with the transcription-inhibitor actinomycin D (ActD) and the functionality of heterologous (oocyte-granulosa) gap junctions (GJ) with a dye transfer assay. The AA (100 microM) and PGF(2alpha) (5 microM) did not induce maturation, and NDGA (10 microM) did not affect MIH-dependent maturation. However, IM (100 microM) partially inhibited MIH-dependent maturation. Conversely, AA and both PGs induced, and IM and NDGA inhibited, MIH-dependent ovulation in matured follicles. The PMA (1 microg/ml) did not induce maturation but caused ovulation in matured follicles, whereas PKC inhibitors (GF, 5 microM; H7, 50 microM) did not affect MIH-dependent maturation but inhibited MIH- and PMA-dependent ovulation. The PMA-dependent ovulation was inhibited by IM but not by NDGA. In addition, ActD (5 microM) blocked MIH-dependent, but not PMA-dependent, ovulation, and PGF(2alpha) restored MIH-dependent ovulation in ActD-blocked follicles. The AA and PGs did not induce, and GF did not inhibit, MIH-dependent heterologous GJ uncoupling. In conclusion, AA and PKC mediate MIH-dependent ovulation but not meiotic resumption or heterologous GJ uncoupling in croaker follicles, but a permissive role of COX products of AA during maturation is possible. A novel model of MIH-dependent ovulation is proposed in which 1). LOX and COX metabolites of AA are both required for ovulation, but at upstream and downstream sites of the pathway, respectively, relative to PKC, and 2). PKC is downstream of genomic activation.

New evidence for the involvement of prostaglandin receptor EP4b in ovulation of the medaka, Oryzias latipes

“…The involvement of PGs in the ovulatory process has also been reported for some teleosts and amphibians (Cetta and Goetz, 1982;Patino et al, 2003;Van Der Kraak, 2008, 2009;Schuetz, 1986;Chang et al, 1995Chang et al, , 1997Ramos et al, 2008;Sena and Liu, 2008;Liu et al, 2010;Fujimori et al, 2011). These studies strongly suggest that PGs have a conserved role in ovulation in vertebrates, including teleost fish.…”

Effects of Dietary Arachidonic Acid on the Reproductive Physiology of Female Atlantic Cod (Gadus morhua L.).

“…Bruce et al, 1999;Furuita et al, 2003;Lund et al, 2008;Mazorra et al, 2003;Pickova et al, 2007Pickova et al, , 1997Røjbek et al, 2014;Salze et al, 2005). Furthermore, a number of studies have documented in vitro effects of ARA and other fatty acids on steroidogenesis and follicular maturation in fish (Knight and Van der Kraak, 2015;Van der Kraak, 2008, 2009;Van Der Kraak, 1995, 1996;Patino et al, 2003;Sorbera et al, 2001;Van Der Kraak and Chang, 1990;Wade et al, 1994). In contrast, few studies address the influence in vivo of dietary ARA on reproductive physiology and endocrinology (Norambuena et al, 2013a,b).…”

“…It is well documented that ARA-derived eicosanoids are involved in regulation of final maturation and ovulation, in both fish and mammals (Abayasekara and Wathes, 1999;Goetz and Garczynski, 1997 Kraak, 2015). A surge of MIS just before ovulation stimulates synthesis of eicosanoids, which in turn activate the mechanisms involved in ovulation (Goetz and Garczynski, 1997;Patino et al, 2003).…”

Effect of Prostaglandins on in vitro Oocyte Final Maturation (GVBD) and Ovulation in the Longchin Goby Chasmichthys dolichognathus

“…, (Sales and Jabbour, 2003), , , (Wade and Van Der Kraak, 1993;Patino et al, 2003;Lister and Van Der Kraak, 점망둑(Chasmichthys dolichognathus)의 최종성숙(GVBD)과 배란 유도에 미치는 Prostaglandins의 영향 2008;Chourasia and Joy, 2012;Joy and Singh, 2013).…”

“…PGF 2 PGE 2 GVBD (Sorbera et al, 2001), (Patino et al, 2003). Zebrafish (Pang and Ge, 2002 Goetz and Theofan (1979) yellow perch (Perca flavescens) PGE 2 PGF 2 PGE 2 , (Dicentrarchus labrax) PGE 2 PGF 2 GVBD PGE 2 (Sorbera et al, 2001).…”