Hormonal activation of ionic currents in follicle-enclosed Xenopus oocytes.

Woodward, Richard M.; Miledi, Ricardo

doi:10.1073/pnas.84.12.4135

Cited by 39 publications

(40 citation statements)

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“…The first (1 in Fig. 1 A ) was an outward current (FSH-K+), associated with an increase in K ÷ conductance caused by an intraceUular rise in cAMP (Woodward and Miledi, 1987a). This first component was frequently cut short by the development of a second component (2 in Fig.…”

Section: Components Of the Membrane Currents Elicited By Fsh And Ach mentioning

confidence: 99%

“…Activation of these receptors stimulates the synthesis of adenosine 3':5'-cyclic monophosphate (cAMP) and activates a K + current via intermediate steps still not well characterized. Previous studies have strongly suggested that all the elements involved in this type of follicle response are in the follicular cell compartment and not in the oocyte (Woodward and Miledi, 1987a;Miledi and Woodward, 1989a).…”

Section: Introductionmentioning

confidence: 99%

“…A great variety of transmitters and hormones elicit slow membrane current responses due to activation of native receptors and channels in the follicle-enclosed oocytes Stinnakre, 1977, 1982;Woodward and Miledi, 1987a, b; Miledi and Woodward, 1989a, b). Moreover, several exogenous receptors and channels can be expressed in the membrane of the oocyte by microinjection of messenger RNAs from different sources (e.g., Miledi, Parker, and Sumikawa, 1989a).…”

Section: Introductionmentioning

confidence: 99%

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Novel Cl- currents elicited by follicle stimulating hormone and acetylcholine in follicle-enclosed Xenopus oocytes.

Arellano

Miledi

1993

The Journal of General Physiology

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Voltage-clamp techniques were used to study the membrane currents elicited by follicle stimulating hormone (FSH) and acetylcholine (ACh) in follicleenclosed oocytes of Xenopus laevis (follides). Both agonists caused complex responses that were more evident when the follicles were in hypotonic Ringer solution (HR; 190.4 mosM). In this medium, currents activated by FSH regularly showed three phases whereas currents activated by ACh displayed three to six phases. At a holding potential of -60 mV, FSH, and ACh responses involved combinations of inward and outward currents. Both FSH and ACh responses included a slow smooth inward component that was associated with an increase in membrane conductance, mainly to C1-(Sin)-This current was strongly dependent on the osmolarity of the external solution: an increase in osmolarity of the HR solution of 18-20 mosM caused a 50% decrease in Sin. In contrast, a fast and transient C1-current (Fin) specifically elicited by ACh was not dependent on osmolarity. Both, Fin and Sin currents required the presence of follicular cells, since defolliculation using three different methods abolished all the response to FSH and at least four components of the ACh responses, The membrane channels carrying Fin and oscillatory CIcurrents elicited by stimulation of ACh or serum receptors, were much more permeable to I-and Br-than CI-, whereas Sm channels were equally permeable to these anions. Unlike the oscillatory CI-currents generated in the oocyte itself, Sin and Fin currents in follicle-enclosed oocytes were not abolished by chelation of intracellular Ca 2+, either with EGTA or BAPTA, which suggests that intracellular Ca 2+ does not play a critical role in the activation of these currents. Our experiments show that Si, and Fin currents are quite distinct from the previously characterized oscillatory C1-responses of oocytes. Moreover, the results strongly suggest that the FSH and ACh receptors, the CI-channels mediating the Fin and Sin currents, together with the necessary elements for their activation, are all located in the follicular cells and not in the oocyte.Many aspects of follicular cell physiology in Xenopus laevis, and other species, are regulated by hormones and neurotransmitters, including FSH and ACh. The follicular CI-currents described in this paper may play an important role in the follicular cell-oocyte development.

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Section: Components Of the Membrane Currents Elicited By Fsh And Ach mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Novel Cl- currents elicited by follicle stimulating hormone and acetylcholine in follicle-enclosed Xenopus oocytes.

Arellano

Miledi

1993

The Journal of General Physiology

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“…follicles that showed residual responses to ␤,␥-meATP were also tested with ATP alone (1-100 M) or coapplied with a threshold concentration of forskolin (FSK), a drug that directly activates adenylyl cyclase; thereby, increasing the synthesis of cAMP. In the Xenopus follicle, FSK strongly potentiates I K,cAMP responses to specific stimulation of different receptors coupled to cAMP synthesis (1,20), including responses to Ado and ATP in w.f. (4,10,13).…”

Section: Relationship Of Current Responses Elicited By Purinergic Agomentioning

confidence: 99%

“…UTP is a specific agonist of F Cl , and shows a weak or null capacity to generate I K,cAMP (8). In this series of experiments, I K,cAMP was elicited by Ado (10 M) or by follicle-stimulating hormone (0.5 g/mL) (20), and the amplitude of I K,cAMP was compared with that obtained in the presence of UTP (100 M), using a 40-s preincubation with UTP alone to ensure maximal effect (Fig. 3A).…”

Section: Relationship Of Current Responses Elicited By Purinergic Agomentioning

confidence: 99%

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

Arellano

Garay

Vázquez‐Cuevas

2009

Proc. Natl. Acad. Sci. U.S.A.

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Purinergic receptors are expressed in the membrane of the follicular cell layer that communicates with the Xenopus oocyte. Adenosine (Ado) generates a cAMP-dependent K ؉ current (IK,cAMP), whereas ATP activates a Cl ؊ current (FCl) and has a dual effect on I K,cAMP, provoking both its activation and inhibition. Here, purinergic responses were studied electrophysiologically, first in the whole follicle (w.f.), and then in the same follicle after removal of its epithelium/theca layers (e.t.r. follicle). Responses were analyzed as the ratio of the current amplitudes (ietr/iwf) in the two preparations. For ATP activation of IK,cAMP and FCl, the ratios ietr/iwf were 0.053 and 22, respectively, whereas that for Ado was 0.75. Thus, epithelium/theca removal drastically altered the ATP response, suggesting a change in the signaling pathway that correlated with changes in the pharmacological characteristics: the half-maximal effective concentration for activation of the main current in w.f. (I K,cAMP) was 14 ؎ 3.8 M [Hill coefficient (nH) ‫؍‬ 2.7 ؎ 0.61], and that in e.t.r. follicles (FCl) was 1.8 ؎ 0.68 M (nH ‫؍‬ 0.76 ؎ 0.09), whereas Ado-response parameters did not change. Responses to UTP and ␤,␥-methylene-ATP, specific agonists for IK,cAMP inhibition and activation, respectively, indicated that in e.t.r. follicles inhibition increased and activation decreased drastically. Thus, purinergic responses were not independent; instead, they were functionally linked. We hypothesize that this property was due to direct interactions between receptors for Ado (A2 subtype) and ATP (P2Y subtype) in the Xenopus follicle.Xenopus oocyte ͉ P2Y receptor ͉ A2 receptor ͉ G protein-coupled receptor oligomerization F ollicle-enclosed Xenopus oocytes are endowed with purinergic receptors located in the follicular cell membrane (1, 2). 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).Removal of epithelium and theca layers from the follicle (e.t.r. follicle) has been shown to eliminate the ability of ATP to generate I K,cAMP (13), an effect that was explained by upregulation of the ATP inhibitory action on these channels mediated by the P2Y receptor. Although this explanation accounted for most of the effects observed in e.t.r. follicles, additional observations indicated further effects on the purinergic system that suggested functional interactions between the receptors expressed in the follicle. For example, responses t...

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Epithelium and/or theca are required for ATP‐elicited K⁺ current in follicle‐enclosed Xenopus oocytes

Saldaña

Vázquez‐Cuevas

Garay

et al. 2004

Journal Cellular Physiology

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The Xenopus follicular cell membrane is endowed with ATP-sensitive K+ channels, which are operated by various transmitters. These generate the ionic response named IK,cAMP via a mechanism that involves intracellular cAMP synthesis. It is known that opening these K+ channels favors oocyte maturation. Follicle stimulation by adenosine (Ado) or ATP consistently generates a strong IK,cAMP via activation of P1 and P3 purinergic receptors; however, ATP can also inhibit IK,cAMP, apparently acting on a third receptor type. Here, we show that IK,cAMP might be elicited by ATP released within the follicle, and that current activation by ATP was entirely dependent on the presence of epithelial and/or theca layers. Morphological studies confirmed that removal of epithelium/theca in these follicles (e.t.r.) was complete, and activation of fast Cl- (Fin) currents by ATP in e.t.r. follicles confirmed that communication between oocyte and follicular cells remained unchanged. Thus, dependence on epithelium/theca was specific for ATP-elicited K+ current. Using UTP and betagamma-MeATP as specific purinergic agents for IK,cAMP inhibition and activation, respectively, it was found that inhibition of IK,cAMP elicited by ATP or UTP was robustly present in e.t.r. follicles but was absent or strongly decreased in whole follicles (w.f.). Accordingly, this indicated that in w.f., epithelium and/or theca downregulated the IK,cAMP inhibition evoked by ATP, and that this control mechanism was absent in e.t.r. follicles. We suggest that this notable action on follicular cells involves one or both of two mechanisms, a paracrine transmitter released from epithelial and/or theca layers and action of ecto-ATPases.

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Hormonal activation of ionic currents in follicle-enclosed Xenopus oocytes.

Cited by 39 publications

References 29 publications

Novel Cl- currents elicited by follicle stimulating hormone and acetylcholine in follicle-enclosed Xenopus oocytes.

Novel Cl- currents elicited by follicle stimulating hormone and acetylcholine in follicle-enclosed Xenopus oocytes.

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

Epithelium and/or theca are required for ATP‐elicited K⁺ current in follicle‐enclosed Xenopus oocytes

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Hormonal activation of ionic currents in follicle-enclosed Xenopus oocytes.

Cited by 39 publications

References 29 publications

Novel Cl- currents elicited by follicle stimulating hormone and acetylcholine in follicle-enclosed Xenopus oocytes.

Novel Cl- currents elicited by follicle stimulating hormone and acetylcholine in follicle-enclosed Xenopus oocytes.

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

Epithelium and/or theca are required for ATP‐elicited K+ current in follicle‐enclosed Xenopus oocytes

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Epithelium and/or theca are required for ATP‐elicited K⁺ current in follicle‐enclosed Xenopus oocytes