In Vitro Actions of Insulin-like Growth Factor-I on Ovarian Follicle Maturation in White Perch (Morone americana)

Authors: Weber, Gregory - Greg; MOORE, ALICIA - DEPT OF ZOOLOGY, NC STATE; SULLIVAN, CRAIG - DEPT OF ZOOLOGY, NS STATE

Submitted to: General and Comparative Endocrinology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/16/2007
Publication Date: 1/20/2007
Citation: Weber, G.M., Moore, A.B., Sullivan, C.V. 2007. In Vitro Actions of Insulin-like Growth Factor-I on Ovarian Follicle Maturation in White Perch (Morone americana). General and Comparative Endocrinology 151, 180-187.

Interpretive Summary: Fully grown ovarian follicles must undergo maturation before the oocyte can be fertilized. Follicle maturation is regulated by hormones including gonadotropin and the steroid maturation inducing hormone (MIH). Follicle maturation consists of two phases. The first phase is oocyte maturational competence (OMC) in which the follicle acquires the ability to respond to the MIH. Gonadotropin (GtH) induces OMC and production of the MIH. The second phase is meiotic resumption, in which the oocyte resumes nuclear division to reduce chromosome number. Meiotic resumption is induced by the MIH. We previously discovered that insulin-like growth factor-I (IGF-I) can also induce meiotic resumption but not OMC in striped bass, and induce OMC but not meiotic resumption in follicles of the congeneric white bass. Striped bass spawn once a year whereas white bass and white perch spawn several times during the spawning season. In the present study, we found that IGFs induced OMC and not meiotic resumption in white perch. We also found that as with the other Morone species, chemicals that inhibit the intracellular signaling molecule phosphatidylinositiol 3-kinase, or inhibit the follicles ability to make proteins from mRNA, attenuated the hormone induced resumption of meiosis. The results of our study show that the IGFs have shared and disparate actions on ovarian follicle maturation among Morone species that appear to be linked to reproductive strategy and exhibit similarities in mechanisms of action. These differences in actions suggest the use of IGF-I in reproductive technologies must be exploited in species specific ways, depending on the fish’s reproductive strategy.

Technical Abstract: Previous studies of follicle maturation in temperate basses showed that insulin-like growth factor (IGF)-I and -II can induce meiotic resumption, indicated by germinal vesicle breakdown (GVBD), and oocyte maturational competence (OMC), the ability to respond to the maturation-inducing hormone (MIH, 17,20 beta-21-trihydroxy-4-pregnen-3-one, 20 beta-S). The IGFs induced GVBD but not OMC in striped bass follicles in vitro, but OMC and not GVBD in white bass follicles. Striped bass are group-synchronous single-clutch spawners whereas white bass and white perch are group-synchronous multiple-clutch spawners. In the present study, we found that IGFs induced OMC in white perch. Although IGF-I weakly stimulated GVBD in follicles from some late stage fish, it is likely that IGF-I did not directly induce GVBD but instead induced OMC, enabling endogenous MIH to act. Bovine insulin was less potent than IGFs at inducing OMC, suggesting that the IGFs were acting through an IGF-I receptor. IGF-I increased testosterone and estradiol-17 beta production by ovarian fragments but decreased production of 17,20 beta-dihydroxy-4-pregnen-3-one, a precursor to the MIH, which was below detection levels. As with the other Morone species, phosphatidylinositiol 3-kinase inhibitors, wortmannin and LY 294002, and the translation inhibitor cyclohexamide, attenuated GVBD induced by human chorionic gonadotropin (hCG), 20 beta-S, and a combination of IGF-I and 20 beta-S. Only hCG-induced GVBD was attenuated by the transcription inhibitor actinomycin D. The IGFs have shared and disparate actions on ovarian follicle maturation among Morone species that appear to be linked to reproductive strategy and exhibit similarities in mechanisms of action.