Shift in Steroidogenesis in the Ovarian Follicles of the Goldfish (Carassius auratus) during Gonadotropin‐Induced Oocyte Maturation

Abstract

Both partially purified chum salmon gonadotropin and 17a-hydroxyprogesterone stimulated in vitro production of testosterone by postvitellogenic follicles of goldfish (Carassius aurafus). Chum salmon gonadotropin further enhanced the conversion of exogenously supplied 17a-hydroxyprogesterone to 17a, 2OP-dihydroxy-4-pregnen-3-one. The increased medium concentrations of 17a, 20&dihydroxy-4-pregnen-3-one were associated with the induction of final oocyte maturation.The capacity of postvitellogenic follicles to produce steroids in response to exogenous 17a-hydroxyprogesterone was examined in females at various stages of final oocyte maturation following the administration of human chorionic gonadotropin in vivo combined with elevation of holding temperature. The maximum production of testosterone in response to 17a-hydroxyprogesterone was obtained in follicles from initial controls. In contrast, 17n, 20P-diOHprog production was very low in initial controls and markedly increased during oocyte maturation (3-6 hr following injection), followed by a significant dxrease in follicles collected at 15 hr. Estradiol-17P production by the follicles was very lo# at any stages of gonadotropin-induced oocyte maturation. These results suggest that gonadotropin-induced shift in the biosynthetic pathway in the follicle from the secretion of predominantly testosterone to 17a, 2OP-dihydroxy-4-pregnen-3-one secretion is a prerequisite step for the induction of oocyte maturation in goldfish.In most vertebrates, full-grown follicle-enclosed oocytes resume meiotic maturation after the preovulatory gonadotropin surge (1). In lower vertebrates, such as amphibians and teleosts, gonadotropin action is mediated by ovarian follicle layers through the production of steroidal mediators, maturation-inducing steroid (MIS) (1, 2, 3). Recently, 17a, 20/3-dihydroxy-4-pregnen-3-one (17cl, 20P-diQHprog) has been identified as the naturally occurring MIS of amago salmon, Oncorhynchus rhodurus (4). 17a, 20P-DiOHprog has also been considered to be a major MIS in several other species of salmonids (3, 5, 6).In goldfish, high plasma levels of 17a, 20B-diQHprog have been reported in females undergoing oocyte maturation and ovulation (7, 8). Previous in vitro studies revealed that 17a, 20P-diQHprog is the most potent steroid for the induction of oocyte maturation in goldfish (5, 9). These results suggest that 17a, 20P-diOHprog is a major MIS responsible for oocyte 555

Diurnal rhythm of serum steroid hormone levels in the Japanese whiting, Sillago japonica, a daily-spawning teleost

“…The difference in the time of increase of 17a,203-diOHprog levels between the Japanese whiting and the other fishes is probably due to the rhythm of oocyte development and oocyte composition in the ovary. The changeover in the pathways of follicular steroidogenesis is associated with a decrease in aromatase activity in post-vitellogenic follicles Kagawa et al 1984;Sakai et al 1987;Kanamori et al 1988) and a change in capacity of the follicles to produce 17a-hydroxyprogesterone (precursor of 17ot,203-diOHprog) rather than testosterone in response to GtH stimulation (Scott et al 1983;Nagahama et al 1986;Sakai et al 1988;Kanamori et al 1988). In the Japanese whiting, as described earlier, when the largest oocytes undergo oocyte final maturation, the second-largest oocytes enter the active vitellogenic phase.…”

Comparative study of reproductive biology in single and multiple‐spawner cyprinid fish. II. Sex steroid and plasma protein phosphorus concentrations

“…This steroid represents a substrate for oestradiol-17 production (Kagawa et al, 1982) and may play a role in maintaining the oocytes once vitellogenesis is completed (Kime, 1993). Once the oocytes are fully grown, final oocyte maturation occurs and is mediated by the maturation inducing hormone (particularly C 21 -steroids) produced by the ovarian follicle just prior to ovulation (Goetz, 1983;Nagahama et al, 1986Nagahama et al, , 1993Kime, 1993). In single spawners, the regulation of oocyte development is clear since the two major events, vitellogenesis and maturation, are consecutive.…”

Cloning and expression of P450c17-I (17α-hydroxylase/17,20-lyase) in brain and ovary during gonad development in Cynoglossus semilaevis

“…However, both steroidogenic pathways commence with progesterone and then branch off into two after the production of 17a-hydroxyprogesterone. An obvious change of steroidogenic pathways from E 2 to 17a, 20b-DHP has been reported during the ovarian development (Kagawa et al 1983;Kanamori et al 1988;Nagahama et al 1986;Nagahama et al 1995;Nagahama 1997;Joy et al 1998;Planas et al 2000, Shoonen et al 1989Suzuki et al 1991;Sreenivasulu and Senthilkumaran 2009) implicating the role of P450c17 in this steroidogenic pathway switch. Moreover, previous study has shown that P450c17 expression appears to ovary developmental stage-dependence in some species of teleost fish (Kazeto et al 2000;Sakai et al 1992;Kumar et al 2000).…”