ATP Suppresses the K+ Current Responses to FSH and Adenosine in the Follicular Cells of Xenopus Oocyte.

Abstract

The follicular cells of Xenopus laevis are known to have various types of receptors such as ␤-adrenergic-[1], muscarinic [2,3], , , adenosine- [8][9][10], and purinergic receptors [3,[11][12][13] in their cytoplasmic membranes. Among the agonists (transmitters or hormones) for these receptors, noradrenaline and ATP are released from sympathetic nerve endings [14], and acetylcholine is released from parasympathetic nerve endings. FSH and LH are released from the hypophysis and delivered via circulating blood. The blood is also known to contain several M of adenosine and ATP [15]. When these agonists stimulate their receptors, they trigger the activation of various intracellular enzyme systems, which subsequently synthesize intracellular second messengers such as cyclic adenosine 3Ј,5Ј-monophosphate (cAMP), diacylglycerol (DAG), and inositol 1,4,5-triphosphate (IP 3 ). These second messengers initiate or modulate various kinds of intracellular signaling of the cells, which are considered necessary for oocyte maturation.Xenopus follicles consist of a single large oocyte surrounded by a monolayer of small follicle cells attached to the oocyte by gap junctions. The gap junctions have connexin channels, which can permeate various molecules and ions smaller than a molecular weight of 1,000, including second messengers such as cAMP, IP 3 , and Ca

Electrophysiological and Pharmacological Characterization of the KATP Channel Involved in the K+-Current Responses to FSH and Adenosine in the Follicular Cells of Xenopus Oocyte

“…This response is mediated by an activation of phospholipase C (PLC) and subsequent PI-turnover followed by an increase in [Ca 2+ ] i [12]. It is interesting that prior stimulation of the P2Y receptor markedly suppresses both the FSH-and Ade-induced K + -current responses, as already reported [1]. This effect is considered to be due to the phosphorylation of a signaling molecule by PKC activated after the P2Y receptor stimulation, since the direct activation of PKC by PDBu also shows a similar suppressing effect on the receptor-induced K + -current responses [1].…”

“…Thus neuronal, hormonal, and humoral controls of the follicular cells might largely affect the maturation and maintenance of the oocyte. We previously reported that the application of either a follicle-stimulating hormone (FSH) or adenosine (Ade) induces a K + -current response in the follicular cells surrounding Xenopus oocyte under voltage clamp [1]. This K + -current response is mimicked by either an intracellular application of cAMP or an extracellular application of cAMP analogue resistant to phosphodiesterase [1,2].…”

“…We previously reported that the application of either a follicle-stimulating hormone (FSH) or adenosine (Ade) induces a K + -current response in the follicular cells surrounding Xenopus oocyte under voltage clamp [1]. This K + -current response is mimicked by either an intracellular application of cAMP or an extracellular application of cAMP analogue resistant to phosphodiesterase [1,2]. Since the receptor-and cAMP-induced K + -current responses are not observed with defolliculated oocyte [3], these types of receptor-induced responses are thought to be produced in the follicular cells after the activation of adenylate cyclase and subsequent cAMP production.…”

Ion Currents Induced by ATP and Angiotensin II in Cultured Follicular Cells of Xenopus laevis

“…Our observations suggest the existence of cell type-dependent roles for ATP. The balance of ions across the membrane is important throughout oogenesis, and hyperpolarization of the oocyte plasma membrane by activation of ATP receptors may contribute to restarting meiosis (Fujita et al, 2001;Wibrand et al, 1992). In addition, the activation of ATP receptors can depress the facilitating action of cAMP, a second messenger produced in the FCs by several stimuli (e.g.…”

Functional interaction between native G protein-coupled purinergic receptors in Xenopus follicles

“…Three main subtypes have been described: (i) A2 receptors responsive to Adenosine (Ado), coupled to cAMP synthesis and opening of K ϩ channels (cAMP-dependent K ϩ current, I K,cAMP ), that are sensitive to glibenclamide (3-7); (ii) P2Y receptors responsive to ATP and UTP that operate Cl Ϫ channels generating fast and slow Ca 2ϩ -independent currents (F Cl and S Cl ) (2,8,9); and (iii) a purinergic receptor, referred to as a P3 or novel P1 receptor, that is sensitive to both Ado and ATP and coupled to I K,cAMP generation (10,11). Also, there is a P2Y receptor that inhibits I K,cAMP and is probably the same as the receptor involved in F Cl and S Cl activation (2,12,13).…”