ION Channels and Membrane Receptors in Follicle-Enclosed Xenopus Oocytes

Arellano, Rogelio O.; Woodward, Richard M.; Miledi, Ricardo

doi:10.1007/978-1-4899-1775-1_6

Cited by 22 publications

(69 citation statements)

References 128 publications

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“…1B, ATP induced inward currents in oocytes with characteristics similar to those described above for FCs. This current reached 125 nA and decayed in the presence of ATP, returning to base line after ∼70 s. These inward currents were similar to those found in a few oocytes that responded to ATP (Arellano et al, 1996), probably due to FCs that remained attached to the oocytes.…”

Section: Atp Responses In Follicular Cellssupporting

confidence: 78%

“…1C). This current is similar to that activated by ATP in epitheliumremoved follicles, and it is assumed to originate in the FCs (Arellano et al, 1996). However, as shown in Fig.…”

Section: Atp Responses In Follicular Cellssupporting

confidence: 60%

“…Further investigations showed that after defolliculation (the process of removing FCs from the oocyte membrane, see ref. Miledi and Woodward, 1989), the Ang II responses still prevailed (Arellano et al, 1996). These results suggested the presence of Ang II receptors in the oocyte membrane.…”

Section: Introductionmentioning

confidence: 79%

“…The electrophysiological responses generated by follicular cells (FCs) are scarce and poorly understood, given that most of the relevant information has been obtained indirectly from follicles (individual oocytes each surrounded by a monolayer of FCs). For example, diverse substances such as acetylcholine, adenosine, noradrenaline, serotonin, and gonadotrophic hormones have been tested for their effect on follicles, primarily to understand their roles in oocyte maturation and their metabolism as second messengers (Arellano et al, 1996;Miledi, 1982).…”

Section: Introductionmentioning

confidence: 99%

“…On the other hand, ATP induces at least two types of chloride inward currents in follicles, a fast desensitizing current (F in ) and a slow current (S in ), both induced by the intracellular calcium metabolism (Arellano et al, 1996). However, the ATP responses observed in follicles are absent after defolliculation (Arellano et al, 1996;King et al, 1996;Miledi and Woodward, 1989). This finding suggested that ATP receptors were expressed specifically in the FC membranes, but the response of individual FCs to ATP has not yet been directly investigated.…”

Section: Introductionmentioning

confidence: 99%

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

Montiel‐Herrera

Zaske

Garcı́a-Colunga

et al. 2011

Molecules and Cells

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Xenopus laevis oocytes are commonly used to study the biophysical and pharmacological properties of foreign ion channels and receptors, but little is known about those endogenously expressed in their enveloping layer of follicular cells (FCs). Whole-cell recordings and the perforated patch-clamp technique in cultured FCs held at -60 mV revealed that ATP (20-250 μM) generates inward currents of 465 ± 93 pA (mean ± standard error) in ∼60% of the FCs studied, whereas outward currents of 317 ± 100 pA were found in ∼5% of the cells. The net effect of ATP on the FCs was to activate both mono-and biphasic inward currents, with an associated increase in membrane chloride conductance. Two-microelectrode voltage-clamp recordings of nude oocytes held at -60 mV disclosed that ATP elicited biphasic inward currents, corresponding to the well-known F in and S in -like currents. ATP receptor antagonists like suramin, TNP-ATP, and RB2 did not inhibit any of these responses. On the other hand, when using wholecell recordings, 1 μM Ang II yielded smooth inward currents of 157 ± 45 pA in ∼16% of the FC held at -60 mV. The net Ang II response, mediated by the activation of the AT 1 receptor, was a chloride current inhibited by 10 nM ZD7155. This study will help to better understand the roles of ATP and Ang II receptors in the physiology of X. laevis oocytes.

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Section: Atp Responses In Follicular Cellssupporting

confidence: 78%

“…1C). This current is similar to that activated by ATP in epitheliumremoved follicles, and it is assumed to originate in the FCs (Arellano et al, 1996). However, as shown in Fig.…”

Section: Atp Responses In Follicular Cellssupporting

confidence: 60%

Section: Introductionmentioning

confidence: 79%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

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

Montiel‐Herrera

Zaske

Garcı́a-Colunga

et al. 2011

Molecules and Cells

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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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Native ion current coupled to purinergic activation via basal and mechanically induced ATP release in xenopus follicles

Saldaña

Garay

Rangel

et al. 2008

Journal Cellular Physiology

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Xenopus follicle-enclosed oocytes are endowed with purinergic receptors located in the follicular cell membrane; their stimulation by ATP elicits an electrical response that includes generation of a fast inward current (F(Cl)) carried by Cl(-). Here, it was found that mechanical stimulation of the follicle provoked a native electrical response named I(mec). This was dependent on coupling between oocyte and follicular cells, because I(mec) was eliminated by enzymatic defolliculation or application of uncoupling drugs, such as heptanol or carbenoxolone. Moreover, the characteristics of I(mec) suggested that it corresponded with opening of the Cl(-) channel involved in F(Cl). For example, I(mec) showed cross-talk with the membrane mechanism that activates the F(Cl) response and anionic selectivity similar to that displayed by F(Cl). Also like F(Cl), I(mec) was independent of extracellular or intracellular Ca(2+). Furthermore, I(mec) was inhibited by superfusion with a purinergic antagonist, suramin, or by an enzyme that rapidly hydrolyzes ATP, apyrase. The response to mechanical stimulation was reconstituted in defolliculated oocytes expressing P2X channels as an ATP sensor. Recently, it has been shown that ATP release from the Xenopus oocyte is triggered by mechanical stimulation. Together, these observations seemed to indicate that I(mec) is activated through a mechanism that involves oocyte release of ATP that diffuses and activates purinergic receptors in follicular cells, with subsequent opening of F(Cl) channels. Thus, I(mec) generation disclosed a paracrine communication system via ATP between the oocyte and its companion follicular cells that might be of physiological importance during the growth and development of the gamete.

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ION Channels and Membrane Receptors in Follicle-Enclosed Xenopus Oocytes

Cited by 22 publications

References 128 publications

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

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

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

Native ion current coupled to purinergic activation via basal and mechanically induced ATP release in xenopus follicles

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ION Channels and Membrane Receptors in Follicle-Enclosed Xenopus Oocytes

Cited by 22 publications

References 128 publications

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

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

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

Native ion current coupled to purinergic activation via basal and mechanically induced ATP release in xenopus follicles

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