Two Types of Pharmacologically Distinct Ca 2+ Currents with Voltage-dependent Similarities in Zona Fasciculata Cells Isolated from Bovine Adrenal Gland

Guyot, Annick; Dupré-Aucouturier, Sylvie; Ojeda, Carlos; Rougier, O; Bilbaut, André

doi:10.1007/s002320001016

Cited by 7 publications

(7 citation statements)

References 36 publications

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“…From studies performed by Yanagibashi et al (32) and confirmed subsequently by Enyeart et al (8), ACTH-induced cortisol secretion in bovine ZF cells was inhibited in the presence of Ca 2ϩ channel blockers. In agreement with the conclusions of Enyeart et al, we proposed that the membrane depolarization induced by ACTH would be a sufficient condition to activate voltage-dependent Ca 2ϩ channels identified in this cell type (13), even though this depolarization failed to trigger action potentials in control solution. Indeed, the activation threshold of T-and L-type Ca 2ϩ currents described by Guyot et al (13) in bovine adrenal ZF cells was about Ϫ50 mV in control physiological saline (2.5 mM Ca 2ϩ ), a potential 15-20 mV more negative than that reached during the ACTH-induced membrane depolarization.…”

Section: Physiological Role Of the CLsupporting

confidence: 92%

“…This type of membrane activity, previously described after inhibition of the transient K ϩ current (2), started when ACTH-induced membrane depolarization was close to Ϫ50 mV. This value corresponds to the activation potential of voltage-sensitive Ca 2ϩ channels identified in this preparation (13). With Cs ϩ in the pipette solution, the maximum value of the depolarizing plateau potential evoked by ACTH stimulation was Ϫ36.5 Ϯ 1.5 mV (n ϭ 19), and membrane conductance, which was 0.38 Ϯ 0.05 nS (n ϭ 19) at rest, rose to 2.9 Ϯ 0.7 nS (n ϭ 19) during the ACTH-induced membrane response.…”

Section: Acth-induced Membrane Depolarizationsupporting

confidence: 69%

“…Consequently, although no experiment was performed on freshly isolated cells, the hypothesis according to which the expression of the ACTH-induced Cl Ϫ current in adrenal ZF cells would be dependent on time in culture cannot be excluded. Development of ionic currents in relation to time in culture have been reported in bovine ZF cells (13) as in other cell types (25,31).…”

Section: Acth-induced CLmentioning

confidence: 88%

“…The increase of the ionic current in the inward or outward direction was associated with an increase in membrane conductance, which was determined by applying every 10 s short test pulses 30 mV more negative than the holding potential of Ϫ60 or Ϫ10 mV. When the holding potential was Ϫ10 mV, a potential where voltage-dependent Ca 2ϩ (13) and K ϩ currents (2) were both fully inactivated, voltage steps of 75-ms duration ranging from Ϫ100 to ϩ40 mV were delivered by increments of 20 mV to the cell membrane in control conditions and during the maximum activation of the ACTH-induced current. In the presence of ACTH, membrane currents recorded during these voltage steps did not display time dependence and were much larger than those obtained in the control solution over the entire voltage range studied (Fig.…”

Section: Effect Of Holding Potential Changes On Acthinduced Membrane mentioning

confidence: 99%

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ACTH-induced Cl⁻current in bovine adrenocortical cells: correlation with cortisol secretion

Dupré-Aucouturier

Penhoat

Rougier

et al. 2002

American Journal of Physiology-Endocrinology and Metabolism

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ACTH has been shown to depolarize bovine adrenal zona fasciculata cells by inhibiting a K+ current. The effects of this hormone on such cells have been reexamined using perforated and standard patch recording methods. In current clamp experiments, ACTH (10 nM) induced a membrane depolarization to −36 ± 1 mV ( n = 56), which was mimicked by forskolin (10 μM) or by 8-(4-chlorophenylthio)-cAMP (8 mM). ACTH-induced membrane depolarizations were associated in the majority of cells with an increase in membrane conductance. In the other cells, these membrane responses could occur without change or could be correlated with a transient or with a continuous Cs+-sensitive decrease in membrane conductance. The depolarizations associated with an increase in membrane conductance were depressed by Cl− current inhibitors diphenylamine-2-carboxylic acid (DPC; 1 mM), anthracene-9-carboxylic acid (9-AC; 1 mM), DIDS (400 μM), verapamil (100 μM), and glibenclamide (20 μM). In voltage-clamped Cs+-loaded cells, ACTH activated a time-independent current that displayed an outward rectification and reversed at −21.5 mV ± 2 ( n = 6). This current, observed in the presence of internal EGTA (5 mM), was depressed in low Cl− external solution and was inhibited by DPC, 9-AC, DIDS, 5-nitro-2-(3-phenylpropylamino)benzoic acid, verapamil, and glibenclamide. ACTH-stimulated cortisol secretion was blocked by Cl− channel inhibitors DIDS (400 μM) and DPC (1 mM). The present results reveal that, in addition to inhibiting a K+current, ACTH activates in bovine zona fasciculata cells a Ca2+-insensitive, cAMP-dependent Cl− current. This Cl− current is involved in the ACTH-induced membrane depolarization, which seems to be a crucial step in stimulating steroidogenesis.

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Section: Physiological Role Of the CLsupporting

confidence: 92%

Section: Acth-induced Membrane Depolarizationsupporting

confidence: 69%

Section: Acth-induced CLmentioning

confidence: 88%

Section: Effect Of Holding Potential Changes On Acthinduced Membrane mentioning

confidence: 99%

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ACTH-induced Cl⁻current in bovine adrenocortical cells: correlation with cortisol secretion

Dupré-Aucouturier

Penhoat

Rougier

et al. 2002

American Journal of Physiology-Endocrinology and Metabolism

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“…Accordingly, in a large fraction of cells, only a T-type current later identified as Ca v 3.2 was detected. Later, in perforated patch-clamp recordings of bovine AZF cells, a small, noninactivating L-type current was detected in ϳ40% of tested cells (22).…”

mentioning

confidence: 99%

Adrenal fasciculata cells express T-type and rapidly and slowly activating L-type Ca²⁺ channels that regulate cortisol secretion

Enyeart

2015

American Journal of Physiology-Cell Physiology

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Enyeart JJ, Enyeart JA. Adrenal fasciculata cells express T-type and rapidly and slowly activating L-type Ca 2ϩ channels that regulate cortisol secretion. Am J Physiol Cell Physiol 308: C899 -C918, 2015. First published March 18, 2015; doi:10.1152/ajpcell.00002.2015.-In whole cell patch-clamp recordings, we characterized the L-type Ca 2ϩ currents in bovine adrenal zona fasciculata (AZF) cells and explored their role, along with the role of T-type channels, in ACTH-and angiotensin II (ANG II)-stimulated cortisol secretion. Two distinct dihydropyridine-sensitive L-type currents were identified, both of which were activated at relatively hyperpolarized potentials. One activated with rapid kinetics and, in conjunction with Northern blotting and PCR, was determined to be Cav1.3. The other, expressed in approximately one-half of AZF cells, activated with extremely slow voltage-dependent kinetics and combined properties not previously reported for an L-type Ca 2ϩ channel. The T-type Ca 2ϩ channel antagonist 3,5-dichloro-N-[1-(2,2-dimethyl-tetrahydro-pyran-4-ylmethyl)-4-fluoro-piperidin-4-ylmethyl]-benzamide (TTA-P2) inhibited Cav3.2 current in these cells, as well as ACTH-and ANG II-stimulated cortisol secretion, at concentrations that did not affect L-type currents. In contrast, nifedipine specifically inhibited L-type currents and cortisol secretion, but less effectively than TTA-P2. Diphenylbutylpiperidine Ca 2ϩ antagonists, including pimozide, penfluridol, and fluspirilene, and the dihydropyridine niguldipine blocked Cav3.2 and L-type currents and inhibited ACTH-stimulated cortisol secretion with similar potency. This study shows that bovine AZF cells express three Ca 2ϩ channels, the voltage-dependent gating and kinetics of which could orchestrate complex mechanisms linking peptide hormone receptors to cortisol secretion through action potentials or sustained depolarization. The function of the novel, slowly activating L-type channel is of particular interest in this respect. Regardless, the well-correlated selective inhibition of T-and L-type currents and ACTH-and ANG II-stimulated cortisol secretion by TTA-P2 and nifedipine establish the critical importance of these channels in AZF cell physiology. adrenal fasciculata; cortisol; ACTH; ANG II; TTA-P2; L-type Ca 2ϩ channel; Cav3.2; Cav1.3 IN MAMMALS, ZONA FASCICULATA cells of the adrenal cortex secrete glucocorticoids in a diurnal rhythm under the control of the pituitary peptide adrenocorticotropic hormone (ACTH) (57). Physical and psychological stress triggers additional bursts of corticosteroid secretion in response to activation of the hypothalamic-pituitary-adrenal axis (57). In some species, including bovine and human, angiotensin II (ANG II) also stimulates glucocorticoid production (10,30,43).Glucocorticoids, including cortisol and corticosterone, regulate a variety of physiological processes, ranging from energy metabolism to long-term memory formation and emotional behavior (8,10,25,32). Chronic excessive cortisol secretion, which occurs in prolonged str...

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Volume-sensitive Cl− Current in Bovine Adrenocortical Cells: Comparison with the ACTH-induced Cl− Current

Dupré-Aucouturier

Penhoat²,

Rougier³

et al. 2004

J Membrane Biol

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In a previous study performed on zona fasciculata (ZF) cells isolated from calf adrenal glands, we identified an ACTH-induced Cl- current involved in cell membrane depolarization. In the present work, we describe a volume-sensitive Cl- current and compare it with the ACTH-activated Cl- current. Experiments were performed using the whole-cell patch-clamp recording method, video microscopy and cortisol-secretion measurements. In current-clamp experiments, hypotonic solutions induced a membrane depolarization to -22 mV. This depolarization, correlated with an increase in the membrane conductance, was sensitive to different Cl- channel inhibitors. In voltage-clamp experiments, hypotonic solution induced a membrane current that slowly decayed and reversed at -21 mV. This ionic current displayed no time dependence and showed a slight outward rectification. It was blocked to variable extent by different conventional Cl- channel inhibitors. Under hypotonic conditions, membrane depolarizations were preceded by an increase in cell volume that was not detected under ACTH stimulation. It was concluded that hypotonic solution induced cell swelling, which activated a Cl- current involved in membrane depolarization. Although cell volume change was not observed in the presence of ACTH, biophysical properties and pharmacological profile of the volume-sensitive Cl- current present obvious similarities with the ACTH-activated Cl- current. As compared to ACTH, hypotonic solutions failed to trigger cortisol production that was weakly stimulated in the presence of high-K+ solution. This shows that in ZF cells, membrane depolarization is not a sufficient condition to fully activate secretory activities.

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Two Types of Pharmacologically Distinct Ca 2+ Currents with Voltage-dependent Similarities in Zona Fasciculata Cells Isolated from Bovine Adrenal Gland

Cited by 7 publications

References 36 publications

ACTH-induced Cl⁻current in bovine adrenocortical cells: correlation with cortisol secretion

ACTH-induced Cl⁻current in bovine adrenocortical cells: correlation with cortisol secretion

Adrenal fasciculata cells express T-type and rapidly and slowly activating L-type Ca²⁺ channels that regulate cortisol secretion

Volume-sensitive Cl− Current in Bovine Adrenocortical Cells: Comparison with the ACTH-induced Cl− Current

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Two Types of Pharmacologically Distinct Ca 2+ Currents with Voltage-dependent Similarities in Zona Fasciculata Cells Isolated from Bovine Adrenal Gland

Cited by 7 publications

References 36 publications

ACTH-induced Cl−current in bovine adrenocortical cells: correlation with cortisol secretion

ACTH-induced Cl−current in bovine adrenocortical cells: correlation with cortisol secretion

Adrenal fasciculata cells express T-type and rapidly and slowly activating L-type Ca2+ channels that regulate cortisol secretion

Volume-sensitive Cl− Current in Bovine Adrenocortical Cells: Comparison with the ACTH-induced Cl− Current

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ACTH-induced Cl⁻current in bovine adrenocortical cells: correlation with cortisol secretion

ACTH-induced Cl⁻current in bovine adrenocortical cells: correlation with cortisol secretion

Adrenal fasciculata cells express T-type and rapidly and slowly activating L-type Ca²⁺ channels that regulate cortisol secretion