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Progestin Signaling through an Olfactory G Protein and Membrane Progestin Receptor- in Atlantic Croaker Sperm: Potential Role in Induction of Sperm Hypermotility

Marine Science Institute, The University of Texas at Austin, Port Aransas, Texas 78373

Address all correspondence and requests for reprints to: Christopher Tubbs, San Diego Zoo Conservation Research, 15600 San Pasqual Valley Road, Escondido, California 92027. E-mail: ctubbs{at}sandiegozoo.org.

Progestin stimulation of sperm hypermotility remains poorly understood despite having been described in numerous vertebrate species. We show here that progestin stimulation of sperm hypermotility in a teleost, the Atlantic croaker (Micropogonias undulatus) is associated with activation of an olfactory G protein (G_olf). Furthermore, we provide evidence that this progestin action is mediated by membrane progestin receptor- (mPR). G_olf was identified in croaker sperm membranes and was specifically activated after treatment with the progestin 17,20β,21-trihydroxy-4-pregnen-3-one (20β-S). Treatment of sperm membranes with 20β-S caused an increase in cAMP production, which was blocked by pretreatment with cholera toxin and two membrane adenylyl cyclase inhibitors: 2',5'-dideoxyadenosine and SQ22536. Moreover, preincubation of croaker sperm with 2',5'-dideoxyadenosine and SQ22536 resulted in a significant inhibition of 20β-S-stimulated hypermotility. Binding of [³H]20β-S to sperm membranes was decreased after pretreatment with GTPS but not pertussis toxin, suggesting the receptor is coupled to a pertussis toxin-insensitive G protein. G_olf and mPR were coexpressed on the sperm midpiece and flagella and were coimmunoprecipitated from sperm membranes. Finally, expression of mPR protein on sperm increased after in vivo treatment with LHRH and was associated with increased induction of sperm motility by 20β-S. These results suggest that 20β-S activates mPR in croaker sperm, which in turn activates G_olf and membrane adenylyl cyclase to stimulate sperm hypermotility. Taken together these findings provide a plausible mechanism by which progestins stimulate sperm hypermotility in croaker and provide the first evidence of hormonal activation of G_olf in any species.