Atrial natriuretic factor potentiates glibenclamide-sensitive K+ currents via the activation of receptor guanylate cyclase in follicle-enclosed Xenopus oocytes

ejp ELSEVIER

European Journal of Pharmacology Molecular PharmacologySection 267 (1994) 281-287

molecular

pharmacology

Atrial natriuretic factor potentiates glibenclamide-sensitive K + currents via the activation of receptor guanylate cyclase in follicle-enclosed Xenopus oocytes Hidenari Sakuta *, Koichi Okamoto, Megumi Tandai

a

Department of Pharmacology and "Departmentof Physiology, National DefenseMedical College, 3-2 Namiki, Tokorozawa, Saitama 359, Japan (Received 6 August 1993; revised MS received 10 November 1993; accepted 4 January 1994)

Abstract

The effect of the atrial natriuretic factor (ANF) on K + channel opener-induced glibenclamide-sensitive K ÷ currents was studied using follicle-enclosed Xenopus oocytes. K ÷ currents induced by the K ÷ channel opener Y-26763 were potentiated by ANF (0.5-50 nM) in a concentration-dependent manner. 50 nM ANF increased the peak amplitude of the current by 59.4 + 9.9% (mean + S.E., n = 8). ANF (1-1000 nM) increased the cGMP contents of follicle-enclosed oocytes; about 13-fold increase was achieved by 100 nM ANF, showing a peak at 5 min. The ANF-stimulated accumulation of cGMP was suppressed by HS-142-1 (a non-peptide antagonist of the ANF receptor), at concentrations of 3-300 p~g/ml. The K ÷ current-potentiating effect of ANF was mimicked by membrane-permeable cGMP (1 mM 8-bromo cGMP). These results .suggest that ANF potentiates glibenclamide-sensitive K + currents via the activation of receptor guanylate cyclase and consequent accumulation of cGMP in follicle-enclosed Xenopus oocytes. Key words: Atrial natriuretic factor; cGMP; HS-142-1; K + channel; Glibenclamide; Y-26763; Cromakalim; Xenopus oocyte

I. Introduction

The ATP-sensitive K + channel is activated by a decrease in intracellular ATP (Noma, 1983) and by various K + channel openers (Escande et al., 1988). Antidiabetic sulfonylureas including glibenclamide (Sturgess et al., 1985) and tolbutamide selectively inhibit this type of K + channel. The ATP-sensitive K + channel is suggested to play an important role in several biological events, such as the sulfonylurea-induced insulin release from pancreatic/3 cells (Sturgess et al., 1988), the vasodilation induced by endotheliumderived hyperpolarizing factor (Brayden et al., 1991), the regulation of growth hormone release from pituitary gland (Bernardi et al., 1993) and the gonadotropin-triggered oocyte maturation (Wibrand et al., 1992). The atrial natriuretic factor (ANF) has been shown to potentiate various types of K + currents, such as the

* Corresponding author. 0922-4106/94/$07.00 © 1994 Elsevier Science B.V. All rights reserved SSDI 0922-4106(93)00009-N

delayed rectifier K + current in the rabbit aortic smooth muscle (Bkaily, 1990), the Ca2+-activated K + currents in the bovine aortic smooth muscle (Williams et al., 1988) and the transient outward K + current in the guinea-pig inferior mesenteric ganglion (Cheung, 1988). In the rat pituitary, A N F inhibits hormone secretion by increasing membrane conductance to K + (Antoni and Dayanithi, 1990). So far, little is known, however, as to the effect of A N F on the ATP-sensitive K + currents. Follicle-enclosed oocytes of Xenopus laeeis have the endogenous K + channels which are activated by K + channel openers such as cromakalim and Y-26763, and inactivated by glibenclamide (Honor6 and Lazdunski, 1991a,b; Sakuta et al., 1992a,b, 1993a,b; Sakuta and Okamoto, 1993). Recently, Honor6 and Lazdunski (1993) have demonstrated the A T P sensitivity of K + currents induced by P1060 (a K ÷ channel opener which is structurally related to pinacidil) in follicular cells at a single channel level. In the present study, we have examined the effect of A N F on the K + channel opener-induced/glibenclamide-sensitive K + currents in follicle-enclosed oocytes. As a result, we have found

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that ANF potentiates the K ÷ currents by stimulating intrafollicular accumulation of cGMP.

was subjected to the radioimmunoassay of cGMP using the cGMP 1251 assay system (Amersham). The cGMP content was expressed by fmol cGMP per follicle-enclosed oocyte.

2. Materials and methods 2.3. Agents used 2.1. Electrophysiological recording

The methods used were similar to those described previously (Sakuta et al., 1993a). Briefly, female frogs (Xenopus laevis) were anesthetized in ice, and oocytes at stages V-VI (Dumont, 1972) were collected and incubated in modified Barth's medium for 1-4 days at 19°C. An incubated follicle-enclosed oocyte was placed in a recording well (about 200 txM in capacity) and superfused at a constant rate of 3 ml/min with frog Ringer solution consisting of (in mM) 120 NaC1, 2 KC1, 1.8 CaC12 and 5 Hepes (pH 7.4). The membrane potential of the oocyte was voltage-clamped routinely at - 2 0 mV, which is close to the C1- equilibrium potential of oocytes (Sakuta et al., 1992a,b), using two glass microelectrodes, each filled with 3 M KC1 (1-2 M) and the amplifier, CEZ-1200 (Nihon Kohden, Tokyo, Japan). All current responses were directly recorded using the Thermalarray recorder, RTA-1100 (Nihon Kohden). All experiments were carried out at 19-23°C. Cromakalim or Y-26763 was dissolved in frog Ringer solution and repetitively applied at 6 min intervals to a voltage-clamped oocyte for 20 s by constant flow superfusion (3 ml/min) to evoke an outward current response. Rat ANF and 8-bromo cGMP were dissolved in frog Ringer solution to the desired concentrations and applied to a voltage-clamped oocyte by superfusion (3 ml/min) for 2 min immediately before the application of a K ÷ channel opener. To test the effect of KT5823 on the current modulating effect of ANF or 8-bromo cGMP, KT5823 (1 /zM) was dissolved in frog Ringer solution, preperfused for 2 min alone and then coperfused with ANF (50 nM) or 8-bromo cGMP (1 mM) for 2 min before the application of K ÷ channel openers. Application of KT5823 (1 /zM) alone for 4 min (control) did not affect the peak amplitude of Y-26763- or cromakalim-induced K ÷ currents (n = 5, respectively). 2.2. c G M P assay

Follicle-enclosed oocytes (stages V-VI), ten oocytes as a group, were incubated with varied concentrations of ANF (0-50 nM) in frog Ringer solution for 0-600 s. Then the incubation was terminated by transferring the oocytes into the ice-cold acetate buffer (50 mM, pH 5.8) containing 4 mM EDTA. The oocytes were then homogenized using a Teflon/glass homogenizer, centrifuged (10000 x g for 15 min) and the supernatant

Rat ANF and 8-bromo cGMP were purchased from Sigma Chemical Co. (St. Louis, MO, USA). Cromakalim was kindly offered by Kirin Brewery Co. (Takasaki, Japan). Y-26763 ((+)-(3S,4R)-4-N-acetylN-benzyloxy-amino)-6-cyano-3,4-dihydro-2,2-dimethyl2H-l-benzopyran-3-ol) was generously donated by Yoshitomi Pharmaceutical Industry (Osaka, Japan). HS-142-1 (a mixture of polysaccharides consisting of /3-1,6, bonding glucoses and caproic acids, Morishita et al., 1991; Imura et al., 1992; Hirata et al., 1993) was donated by Dr. Matsuda of the Tokyo Research Laboratory of Kyowa Hakko Co. (Machida, Japan). Glibenclamide was obtained from Funakoshi Co. (Tokyo, Japan). KT5823 ([9S-(9a,10a,12a)]-2,3,9,10,11,12-hexahydro-10-methoxy-2,9-dimethyl-l-oxo-9,12-epoxy-1Hdiindolo[1,2,3-fg : 3',2',l'-kl ]pyrrolo[3,4-i ][1,6]benzodiazocine-10-carboxylic acid methylester) was obtained from Kyowa Hakko Medical Co. (Tokyo, Japan). All other chemicals used were purchased from Wako Pure Chemicals Industry (Osaka, Japan). Xenopus laevis frogs were obtained from Hamamatsu Biological Research Service (Hamamatsu, Japan). 2.4. Statistics

For statistical comparison of two data groups, the homo- and hetero-schedasticities between the two data groups in the population distribution were first examined by the F-test, then the t-test for small samples was applied based on the results of the F-test.

3. Results 3.1. Potentiation by A N F o f glibenclamide-sensitive K + currents

Cromakalim (100 /~M) and Y-26763 (50 IzM) induced outward K + currents in follicle-enclosed oocytes. These K + currents were completely and reversibly blocked by 5 ~M glibenclamide as previously reported (Honor6 and Lazdunski, 1991a; Sakuta et al., 1992b, 1993a) (data not shown). Fig. 1A and B show the effect of 50 nM ANF applied for 2 min on the K ÷ current induced by Y-26763 (50 tzM for 20 s in A) and by cromakalim (CK, 100 g M for 20 s in B). Although ANF (50 nM) alone showed no current response (Fig. 1A, B), it enhanced

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Molecular Pharmacology Section 267 (1994) 281-287

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3.2. Potentiation of glibenclamide-sensitiL~e K + currents by 8-bromo cGMP

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Fig. 1. Potentiation by A N F of the glibenclamide-sensitive K + currents induced by Y-26763 and cromakalim in follicle-enclosed oocytes. Y-26763 (50/zM; A) and cromakalim (CK, 100/xM; B) were applied for 20 s (short bars) at 6 min intervals, and A N F (50 nM) was applied for 2 min (long bars; A and B), all by superfusion. The upward deflection shows an outward current. Records A and B were from different oocytes. In C, m e a n increases (+_S.E.)in the K ÷ currents induced by Y-26763 (50 /zM, open circles, n = 8) and cromakalim (100/xM, closed circles, n = 5)were obtained from recordings similar to those in A and were plotted as the function of trial numbers. The time of application of A N F (50 nM) is indicated with an arrow. CT1 and CT2 are controls before A N F application, and peak amplitudes of test responses were normalized to CT2. CTI, CT2, and the following trials 1-5 on the abscissa were at intervals of 6 min.

ANF activates guanylate cyclase-containing receptors and stimulates the accumulation of intracellular cGMP in various tissues. As shown in Fig. 3A, the K + currents induced by Y-26763 (50 /xM) were enhanced by 1 mM 8-bromo cGMP. The effects reached a peak at 6-12 min and persisted for longer than 24 min with a gradual decline (Fig. 3B). In confirmation of our previous report (Sakuta et al., 1993b), 8-bromo cGMP (1 mM), a membrane permeable analogue of cGMP, also enhanced cromakalim-induced K + currents by about 50% in follicle-enclosed oocytes (data not shown). 8-Bromo cGMP (1 mM) alone did not induce current response in follicle-enclosed oocytes. KT5823 (1 /~M) did not affect the potentiating effects of 8bromo GMP (1 raM) on Y-26763 (50 ~M)- or cromakalim (100 gM)-induced K + currents (data not shown). The K + current potentiating effects of ANF and 8-bromo cGMP were additive. Namely the current amplitude caused by 2 nM ANF alone, 0.1 mM 8-bromo cGMP alone and 2 nM ANF plus 0.1 mM 8-bromo cGMP were 116.7 _+ 2.4 %, 122.0 + 2.2% and 134.6 _+ 2.2% of control respectively (mean + S.E., n = 5).

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the K + current induced by Y-26763 or cromakalim immediately after its application by about 60%, and this enhancement was maintained for 6 rain and gradually declined in 12-24 min (Fig. 1A-C). No significant difference was observed between Y-26763- and cromakalim-induced K + currents as to the sensitivity to ANF (Fig. 1C). The enhancing effect of ANF on K + channel opener-induced K + currents showed concentration dependency in the range from 0.05 nM to 50 nM (Fig. 2). KT5823 (1 /xM), an inhibitor of cGMP-dependent protein kinase (White et al., 1993), did not affect the potentiating effects of ANF (50 nM) on Y-26763 (50 ~M)- or cromakalim (100 /zM)-induced K + currents (Fig. 2, rightmost columns).

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Fig. 2. Concentration dependence of the potentiating effect of A N F on the K ÷ currents induced by Y-26763 (50 /zM) and cromakalim (CK, 100/zM), and no effect of KT5823 thereon. The data illustrated were obtained from experiments similar to those shown in Fig. 1A and B for each A N F concentration and each K + channel opener. The ordinate is the m e a n peak amplitude of K + currents ( ± S . E . , n = 5) expressed as the percentage to the p r e - A N F control. Left four column groups indicate the concentration-dependent increase in the potentiating effect of A N F (0.05-50 nM) on the K ÷ currents. The rightmost column group was in the presence of 50 nM KT5823 and indicates no effect of this inhibitor of c G M P - d e p e n d e n t protein kinase on the current potentiating effect of A N F (50 nM).

H. Sakuta et aL / European Journal of Pharmacology MolecularPharmacology Section 267 (1994) 281-287

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Trial number Fig. 3. Potentiating effect of 8-bromo c G M P on Y-26763-induced K + currents. In A, Y-26763 was applied for 20 s (short bars) at 6 min intervals and 8-bromo c G M P (cGMP, 1 mM) was applied for 2 min (long bar), both by superfusion. In B, m e a n increases (_+ S.E., n = 8) in Y-26763 (50 /zM)-induced K ÷ currents by 8-bromo c G M P were obtained by experiments similar to those in A, normalized to CT2 and plotted as the function of trial numbers. The time of application of 8-bromo c G M P (1 mM) is indicated with an arrow. CT1 and CT2 on the abscissa were controls before 8-bromo cGMP application. CT1, CT2 and the following trials 1-5 were at intervals of 6 rain.

3.3. Effects of A N F and HS-142-1 on the cGMP level in follicle-enclosed Xenopus oocytes As shown in Fig. 4A, the cGMP level in follicle-enclosed oocytes concentration dependently increased in response to ANF (5 min exposure). It increased from the basal level of 27 fmol/oocyte up to 450 fmol/oocyte as the ANF concentration in the incubation medium was raised from 0.1 nM to 1 /zM. Fig. 4B shows the

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Fig. 5. Effects of HS-142-1 on the A N F - e n h a n c e d cGMP levels in follicle-enclosed oocyte. Six oocyte groups, each consisting of ten oocytes were incubated for 5 min in the presence or absence of A N F (50 nM) and HS-142-1 (HS) as indicated, and the c G M P level in each oocyte group was assayed. The ordinate is the m e a n (+_ S.E., n = 3) cGMP level. Significance of difference: * P < 0.025 and ** P < 0.005 vs. oocyte group incubated with A N F (50 nM) alone.

incubation time dependence of the effect of ANF on cGMP production. In response to ANF (100 nM), the cGMP level time dependently increased and reached a peak at 5 min incubation. The selective antagonist of the ANF receptor, HS142-1 (Morishita et al., 1991; Imura et al., 1992; Hirata et al., 1993) concentration dependently antagonized the enhancing effect of ANF on the cGMP level when the oocytes were coincubated with 3-300 /zg/ml HS142-1 (Fig. 5). HS-142-1 alone (300 /zg/ml) did not affect the basal level of cGMP (Fig. 5). These results suggest that the ANF-stimulated increase in cGMP is mediated by the activation of ANF receptor guanylate cyclase in follicle-enclosed oocytes. In addition, HS-142-1 inhibited the current potentiating effect of ANF (Fig. 6). HS-142-1 (100 /zg/ml) a

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Fig. 4. Concentration and time dependence of ANF-stimulated c G M P accumulation in follicle-enclosed oocytes. In A, six oocyte groups, each consisting of ten oocytes, were incubated with 0.1, 1, 10, 100, 300 and 1000 nM A N F for 5 min in frog Ringer solution, and the cGMP level in each oocyte group was assayed. The cGMP level for each oocyte was plotted against the A N F concentration. In B, six oocyte groups, each consisting of ten oocytes, were incubated with 100 n M A N F for 0, 30, 60, 180, 300 and 600 s in frog Ringer solution, and the assayed cGMP level for each oocyte group was plotted against the time of incubation. In A and B, values plotted are the m e a n (_+ S.E., n = 3) cGMP level.

H. Sakuta et aL / European Journal of Pharmacology - Molecular Pharmacology Section 267 (1994) 281-287

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decreased the current potentiating effect of ANF (5 nM) from 135.5 + 5.8 of control to 102.9 + 4.0% of control (mean + S.E., n = 4). Application of HS-142-1 (100 /zg/ml) alone for 5 min (control) did not affect the peak amplitude of Y-26763-induced K ÷ currents (n = 5).

be the mechanism of ANF-induced potentiation of glibenclamide-sensitive K ÷ currents in oocytes, because inhibitors of cyclic nucleotide phosphodiesterase, which inhibits the breakdown of cAMP, potentiate cromakalim-induced K ÷ currents in follicle-enclosed Xenopus oocytes (Honor6 and Lazdunski, 1991a; Sakuta et al., 1992b). Furthermore 8-bromo cGMP, which does not alter cyclic nucleotide phosphodiesterase activity in other tissues (Fischmeister and Hartzell, 1987; Doerner and Alger, 1988), increased glibenclamidesensitive K ÷ currents as effectively as ANF (Fig. 3). It has been shown that the ANF receptor exists in the follicle cell but not in the oocyte itself in different species (Pandey et al., 1987; T6rnel et al., 1990). Thus, it seems likely that the ANF receptors of follicle-enclosed Xenopus oocytes (Miledi and Woodward, 1989b) localize in follicle cells and modulate ATP/glibenclamide-sensitive K + channels which also exist in follicle cells (Honor6 and Lazdunski, 1991a, 1993). However, the possibility remains that the ANF receptor might exist in the plasma membrane of oocyte. In this case, cGMP may be produced in oocyte, transfer from oocyte to follicle cell through gap junctions and there modulate ATP/glibenclamide-sensitive K + channels.

4. Discussion

4.2. Implications of ANF-induced potentiation of glibenclamide-sensitive K + currents

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F'ig. 6. The inhibition by HS-142-1 of the current potentiating effect of ANF. In A and B, Y-26763 (50 /zM) was applied for 20 s (short bars) at 6 min intervals, and ANF (5 nM) was applied for 2 min (long bars) with (A) or without (B) HS-142-1 (100/zg/ml, the longest bar), all by superfusion. The upward deflection shows an outward current. Records A and B are from different oocytes.

4.1. Mechanism of ANF-induced enhancement of glibenclamide-sensitive K + currents The present study has first shown that ANF potentiates the glibenclamide-sensitive K + currents. ANF was also found to increase cGMP contents in follicle-enclosed oocytes. Since the K + current-enhancing effect of ANF was mimicked by 8-bromo cGMP and inhibited by HS-142-1, the K + current potentiating effect of ANF seems to be mediated by the activation of ANF receptor guanylate cyclase and the consequent accumulation of cGMP. ANF potentiates the voltage- and calcium-dependent K + current (BK current) via the formation of cGMP in pituitary adenoma cells (White et al., 1993). This effect is shown to be mediated by the activation of cGMP-dependent protein kinase (PKG). Unlike the BK current, however, the potentiating effect of ANF on glibenclamide-sensitive K + currents seems not to be associated with the activation of PKG, since the glibenclamide-sensitive K + current potentiating effect of ANF or 8-bromo cGMP was not affected by KT5823, a relatively selective inhibitor of PKG (cf. Fig. 2). ANF-induced increase in cGMP may activate the cGMP-activated cAMP phosphodiesterase and promote cAMP breakdown (Fischmeister and Hartzell, 1987; Doerner and Alger, 1988) in oocytes. The decrease in cAMP, however, even if it occurred, may not

ANF induces K + currents in follicle-enclosed Xenopus oocytes in the presence (but not in the absence) of 3-isobutyl-l-methylxanthine (IBMX), an inhibitor of cyclic nucleotide phosphodiesterase (Miledi and Woodward, 1989b). Microinjection of cGMP also induces K + currents in follicle-enclosed Xenopus oocytes (Miledi and Woodward, 1989a). In the present study, we have shown that ANF facilitates the accumulation of cGMP in follicle-enclosed Xenopus oocytes. Thus, the reported induction of K + currents by ANF in the presence of IBMX appears to be caused by the suprathreshold accumulation of cGMP. ANF in combination with cicletanine (an inhibitor of cGMP-dependent phosphodiesterase, Silver et al., 1990, 1991) relaxes glomeruli in low-sodium rats (Szczepanska-Konkel et al., 1991). The relaxing effect of ANF on glomeruli is blocked by glibenclamide. From these findings, Szczepanska-Konkel et al. (1991) have postulated that cGMP might modulate the glibenclamide-sensitive K + channels in glomeruli. The present result, which shows the potentiation by ANF or cGMP of glibenclamide-sensitive K ÷ currents in follicle-enclosed oocytes, is in consistent with the hypothesis of Szczepanska-Konkel et al. (1991). A K + channel opener, diazoxide, inhibits the growth hormone (GH) release from adenohypophysis by activating the ATP/glibenclamide-sensitive K ÷ channels (Bernardi et al., 1993). Also ANF inhibits the release

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of GH in pituitary cells (Shibasaki et al., 1986). Thus the inhibition of GH release by ANF might be mediated by the potentiating effect of ANF on the ATP/glibenclamide-sensitive K ÷ channels. Does the potentiating effect of ANF on glibenclamide-sensitive K ÷ channels have any physiological meaning in follicle-enclosed Xenopus oocytes? The gonadotropin-induced maturation of follicle-enclosed Xenopus oocytes is largely inhibited by glibenclamide (Honor6 and Lazdunski, 1991a; Wibrand et al., 1992), suggesting that the glibenclamide-sensitive K ÷ channels are, at least partly, responsible for the gonadotropin-triggered maturation. Therefore, ANF or cGMP might act as to facilitate the gonadotropin-initiated maturation by potentiating glibenclamide-sensitive K ÷ channels in Xenopus oocytes. In this connection, cGMP is reported to facilitate the gonadotropin-induced maturation of follicle-enclosed oocyte in guinea pig (Hubbard, 1986). In conclusion, ANF potentiates the glibenclamidesensitive K ÷ currents via the stimulation of ANF receptor guanylate cyclase and consequent accumulation of cGMP in follicle-enclosed Xenopus oocytes.

Acknowledgments We express our sincere thanks to Yoshitomi Pharmaceutical Industry, Ltd., Osaka, Japan, for the kind offer of Y-26763 and Tokyo Research Laboratory, Kyowa Hakko Kogyo Co. Ltd., Tokyo, Japan, for the generous gift of HS-142-1.

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