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Intracellular cAMP and Calcium Signaling by Serotonin in Mouse Cumulus-Oocyte Complexes

Département d'Obstétrique-Gynécologie, Université de Montréal, and Centre de Recherche, Centre Hospitalier de l'Université de Montréal-Hôpital Saint-Luc, Montréal, Québec, Canada

cAMP and intracellular Ca²⁺ are important second messengers involved in mammalian follicular growth and oocyte meiotic maturation. We investigated the capacity of the neurohormone serotonin (5-hydroxytryptamine, 5-HT) to regulate intracellular cAMP and Ca²⁺ in mouse oocytes and surrounding cumulus cells. On the basis of a reverse transcription-polymerase chain reaction study, 5-HT₇ receptor mRNA is expressed in cumulus cells, oocytes, and embryos up to the four-cell stage, and 5-HT_2A and 5-HT_2B receptor mRNAs are expressed in cumulus cells only, whereas 5-HT_2C, 5-HT₄, and 5-HT₆ receptors are expressed in neither oocytes nor cumulus cells. The addition of 5-HT (10 nM to 10 µM) to isolated metaphase II oocytes had no effect on their internal cAMP or Ca²⁺ levels, whereas it caused dose-dependent cAMP and Ca²⁺ increases in cumulus cells. This cAMP increase in cumulus cells could be mimicked by 5-HT agonists with the following order of potency: 5-HT > 8-hydroxy-2-(di-n-propylamino) tetralin = -methyl-5-HT = 5-carboxamidotryptamine maleate > 2-[1-(4-piperonyl)piperazinyl]benzo-triazole, thereby supporting a preferential involvement of 5-HT₇ receptors. As measured with cumulus cells preloaded with fura-2/acetoxymethyl ester (AM), the addition of 5-HT also caused dose-dependent Ca²⁺ increases, which were probably linked to detected 5-HT_2A and 5-HT_2B receptors. Adding the Ca²⁺ ionophore ionomycin to cumulus cells resulted in both Ca²⁺ and cAMP elevations, whereas preincubation of cells with the Ca²⁺ chelator 1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid (BAPTA)-AM abolished the 5-HT-induced Ca²⁺ increase and reduced the cAMP increase, indicating cross-talk between the 5-HT-sensitive Ca²⁺ and cAMP pathways. Our results show that 5-HT may be a local regulator in mouse cumulus-oocyte complexes through its actions on cAMP and Ca²⁺ signaling, as mediated by 5-HT_2A, 5-HT_2B, and 5-HT₇ receptors.

Address correspondence to: Dr. François Dubé, Centre de recherche du Centre Hospitalier de l'Universitié de Montréal, Hôpital Saint-Luc 264, René-Lévesque Est, Montréal, Québec, Canada H2X 1P1. E-mail: francois.dube{at}umontreal.ca

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