Dynamics of insulin and insulin-like growth factor-I (IGF-I) ovarian receptors during maturation in the brown trout (Salmo trutta)

Abstract

In salmonid fishes, the role of insulin and insulin-like growth factor-I (IGF-I) in the regulation of ovarian function is not well understood. Recently, we reported that isolated follicular layers of the preovulatory ovarian follicle of coho salmon (Oncorhynchus kisutch) have specific receptors for insulin and IGF-I and that IGF-I modulates steroid production in the follicular layers. In the present study we have investigated the structural and functional characteristics of insulin and IGF-I receptors in the ovary of brown trout (Salmo trutta) and the changes in insulin and IGF-I binding throughout the reproductive cycle of this species. The specific binding for IGF-I was 8- to 15-fold higher than the specific binding for insulin. IGF-I receptors were also more specific than insulin receptors because unlabeled insulin displaced bound radiolabeled insulin at concentrations 40- to 80-fold lower than unlabeled IGF-I; whereas, unlabeled IGF-I displaced bound radiolabeled IGF-I at concentrations 4000- to 8000-fold lower than unlabeled insulin. Insulin and IGF-I receptors from the brown trout ovary were composed of 120 kDa α-subunits and 90 kDa β-subunits, which underwent autophosphorylation in a concentration-dependent manner. Receptor tyrosine kinase activity was also stimulated in a concentration-dependent manner by insulin and IGF-I. When ovarian insulin and IGF-I binding was determined from mid-vitellogenesis (March) until ovulation (November), maximal binding for both peptides was detected in mid-vitellogenesis and gradually decreased until the end of vitellogenesis (August). In the preovulatory period (October), a small increase of insulin and IGF-I binding was observed. After ovulation, insulin binding was no longer detectable and IGF-I binding was very low. These results suggest that insulin and IGF-I receptors in the salmonid ovary follow the structural pattern described in other vertebrate species and that insulin and IGF-I could be involved in the regulation of ovarian function during reproductive stages other than the preovulatory period.