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Cloning, Regulation of Messenger Ribonucleic Acid Expression, and Function of a New Isoform of Pituitary Adenylate Cyclase-Activating Polypeptide in the Zebrafish Ovary

Department of Biology (Y.W., W.G.), The Chinese University of Hong Kong, Hong Kong, China; and Department of Zoology (A.O.L.W.), The University of Hong Kong, Hong Kong, China

Address all correspondence and requests for reprints to: Wei Ge, Department of Biology, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, China. E-mail: weige{at}cuhk.edu.hk.

Increasing evidence suggests that pituitary adenylate cyclase-activating polypeptide (PACAP) acts as a local factor in the ovary of mammals. In nonmammalian vertebrates, although the expression of PACAP has also been demonstrated in the ovary, the information on its functions and regulation is limited. In the present study, we identified a new type of PACAP, zebrafish (zf)PACAP₃₈-2, from the zebrafish ovary. The precursor of GHRH-zfPACAP₃₈-2 consists of 175 amino acids with only 64% homology with another type of zebrafish PACAP, zfPACAP₃₈-1. RT-PCR analysis detected two messengers of zfPACAP₃₈-2 in the zebrafish ovary. The short product was more abundant, and it encodes zfPACAP₃₈-2 only, whereas the long form codes for both zfPACAP₃₈-2 and GHRH. Using a primary culture of zebrafish follicle cells, we demonstrated that gonadotropin (human chorionic gonadotropin and goldfish pituitary extract) significantly stimulated zfPACAP₃₈-2 expression within 2 h; however, the effect decreased to the control level after 8 h of treatment. The stimulation of zfPACAP₃₈-2 expression by gonadotropin could be mimicked by cAMP analogs and forskolin but suppressed by H89 (10 µM), suggesting the involvement of the cAMP-protein kinase A signaling pathway. We also examined the expression of PACAP receptor VPAC₂-R in the zebrafish ovary. Unlike zfPACAP₃₈-2, which showed a trend of increase during follicle development, the expression of VPAC₂-R mRNA in the follicles showed no significant stage-dependent variation, and its expression in the follicle cells did not respond to gonadotropin treatment. Our studies further demonstrated that synthetic zfPACAP₃₈-2 stimulated oocyte maturation and increased the expression of follistatin in zebrafish ovarian follicle cells. These results suggest that zfPACAP₃₈-2 is a potential ovarian factor that mediates gonadotropin actions in paracrine/autocrine manners, and its functional roles are likely, to some extent, related to the ovarian activin/follistatin system.

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