Endocrinology, Vol 135, 751-758, Copyright © 1994 by Endocrine Society

ARTICLES

Role of the capacitative calcium influx in the activation of steroidogenesis by angiotensin-II in adrenal glomerulosa cells

MM Burnay, CP Python, MB Vallotton, AM Capponi and MF Rossier
Division of Endocrinology, University Hospital, Geneva, Switzerland.

Angiotensin-II (AngII)-induced Ca2+ influx in adrenal glomerulosa cells, a signal necessary for the stimulation of steroidogenesis by the hormone, is believed to involve two distinct mechanisms: 1) opening of voltage-operated Ca2+ channels, and 2) activation of a capacitative Ca2+ entry pathway that is dependent on calcium release from intracellular stores. Nicardipine, a dihydropyridine calcium antagonist, has been used to investigate the role of these Ca2+ entry mechanisms in the steroidogenic response to AngII. As demonstrated with the patch-clamp technique, micromolar concentrations of nicardipine completely blocked voltage-operated Ca2+ channel activity of both T- and L-types. This agent similarly inhibited the rise of cytosolic free calcium concentration induced by potassium, but did not significantly affect the response to thapsigargin, an activator of the capacitative pathway. Nicardipine reduced by only 22% the calcium influx stimulated by AngII, and the nicardipine-insensitive part of this response was abolished after exhausting the intracellular Ca2+ stores with thapsigargin. Similarly, aldosterone secretion induced by AngII was only partially inhibited (40%) by nicardipine at concentrations that completely abolished the steroidogenic response to potassium. Thapsigargin by itself was able to stimulate aldosterone production, an action highly potentiated by physiological concentrations of extracellular potassium. These data strongly suggest that the major part of the calcium influx response to AngII, leading to aldosterone formation, involves a capacitative calcium entry pathway activated by the release of calcium from intracellular stores. This mechanism of calcium influx could be responsible for some features of aldosterone response to the hormone, such as its poor sensitivity to dihydropyridines or its potentiation by potassium.

This article has been cited by other articles:

				A. Sen, A. Bettegowda, F. Jimenez-Krassel, J. J. Ireland, and G. W. Smith Cocaine- and Amphetamine-Regulated Transcript Regulation of Follicle-Stimulating Hormone Signal Transduction in Bovine Granulosa Cells Endocrinology, September 1, 2007; 148(9): 4400 - 4410. [Abstract] [Full Text] [PDF]

				S. Gambaryan, E. Butt, P. Tas, A. Smolenski, B. Allolio, and U. Walter Regulation of aldosterone production from zona glomerulosa cells by ANG II and cAMP: evidence for PKA-independent activation of CaMK by cAMP Am J Physiol Endocrinol Metab, March 1, 2006; 290(3): E423 - E433. [Abstract] [Full Text] [PDF]

				J. J. Enyeart, S. J. Danthi, H. Liu, and J. A. Enyeart Angiotensin II Inhibits bTREK-1 K+ Channels in Adrenocortical Cells by Separate Ca2+- and ATP Hydrolysis-dependent Mechanisms J. Biol. Chem., September 2, 2005; 280(35): 30814 - 30828. [Abstract] [Full Text] [PDF]

				A. SPAT and L. HUNYADY Control of Aldosterone Secretion: A Model for Convergence in Cellular Signaling Pathways Physiol Rev, April 1, 2004; 84(2): 489 - 539. [Abstract] [Full Text] [PDF]

				J. Li, R. E. Feltzer, K. L. Dawson, E. A. Hudson, and B. J. Clark Janus Kinase 2 and Calcium Are Required for Angiotensin II-dependent Activation of Steroidogenic Acute Regulatory Protein Transcription in H295R Human Adrenocortical Cells J. Biol. Chem., December 26, 2003; 278(52): 52355 - 52362. [Abstract] [Full Text] [PDF]

				N. Cherradi, B. Pardo, A. S. Greenberg, F. B. Kraemer, and A. M. Capponi Angiotensin II Activates Cholesterol Ester Hydrolase in Bovine Adrenal Glomerulosa Cells through Phosphorylation Mediated by p42/p44 Mitogen-Activated Protein Kinase Endocrinology, November 1, 2003; 144(11): 4905 - 4915. [Abstract] [Full Text] [PDF]

				N. Lalevee, V. Resin, S. Arnaudeau, N. Demaurex, and M. F. Rossier Intracellular Transport of Calcium from Plasma Membrane to Mitochondria in Adrenal H295R Cells: Implication for Steroidogenesis Endocrinology, October 1, 2003; 144(10): 4575 - 4585. [Abstract] [Full Text] [PDF]

				O. Lesouhaitier, A. Chiappe, and M. F. Rossier Aldosterone Increases T-Type Calcium Currents in Human Adrenocarcinoma (H295R) Cells by Inducing Channel Expression Endocrinology, October 1, 2001; 142(10): 4320 - 4330. [Abstract] [Full Text] [PDF]

				D. R. Yingst, J. Davis, and R. Schiebinger Effects of extracellular calcium and potassium on the sodium pump of rat adrenal glomerulosa cells Am J Physiol Cell Physiol, January 1, 2001; 280(1): C119 - C125. [Abstract] [Full Text] [PDF]

				G. Czirják, T. Fischer, A. Spät, F. Lesage, and P. Enyedi TASK (TWIK-Related Acid-Sensitive K+ Channel) Is Expressed in Glomerulosa Cells of Rat Adrenal Cortex and Inhibited by Angiotensin II Mol. Endocrinol., June 1, 2000; 14(6): 863 - 874. [Abstract] [Full Text]

				C. Aguirre, F. C. L. Jayes, and J. D. Veldhuis Luteinizing Hormone (LH) Drives Diverse Intracellular Calcium Second Messenger Signals in Isolated Porcine Ovarian Thecal Cells: Preferential Recruitment of Intracellular Ca2+ Oscillatory Cells by Higher Concentrations of LH Endocrinology, June 1, 2000; 141(6): 2220 - 2228. [Abstract] [Full Text] [PDF]

				B. J. Clark and R. Combs Angiotensin II and Cyclic Adenosine 3',5'-Monophosphate Induce Human Steroidogenic Acute Regulatory Protein Transcription through a Common Steroidogenic Factor-1 Element Endocrinology, October 1, 1999; 140(10): 4390 - 4398. [Abstract] [Full Text]

				A. D. Maturana, A. J. Casal, N. Demaurex, M. B. Vallotton, A. M. Capponi, and M. F. Rossier Angiotensin II Negatively Modulates L-type Calcium Channels through a Pertussis Toxin-sensitive G Protein in Adrenal Glomerulosa Cells J. Biol. Chem., July 9, 1999; 274(28): 19943 - 19948. [Abstract] [Full Text] [PDF]

				X.-L. Chen, D. A. Bayliss, R. J. Fern, and P. Q. Barrett A role for T-type Ca2+ channels in the synergistic control of aldosterone production by ANG II and K+ Am J Physiol Renal Physiol, May 1, 1999; 276(5): F674 - F683. [Abstract] [Full Text] [PDF]

				P. R. Manna, P. Pakarinen, T. El-Hefnawy, and I. T. Huhtaniemi Functional Assessment of the Calcium Messenger System in Cultured Mouse Leydig Tumor Cells: Regulation of Human Chorionic Gonadotropin-Induced Expression of the Steroidogenic Acute Regulatory Protein Endocrinology, April 1, 1999; 140(4): 1739 - 1751. [Abstract] [Full Text]

				M. F. Rossier, E. A. Ertel, M. B. Vallotton, and A. M. Capponi Inhibitory Action of Mibefradil on Calcium Signaling and Aldosterone Synthesis in Bovine Adrenal Glomerulosa Cells J. Pharmacol. Exp. Ther., December 1, 1998; 287(3): 824 - 831. [Abstract] [Full Text]

				T. Yamazaki, T. Kimoto, K. Higuchi, Y. Ohta, S. Kawato, and S. Kominami Calcium Ion as a Second Messenger for o-Nitrophenylsulfenyl-Adrenocorticotropin (NPS-ACTH) and ACTH in Bovine Adrenal Steroidogenesis Endocrinology, December 1, 1998; 139(12): 4765 - 4771. [Abstract] [Full Text] [PDF]

				G. Boulay, X. Zhu, M. Peyton, M. Jiang, R. Hurst, E. Stefani, and L. Birnbaumer Cloning and Expression of a Novel Mammalian Homolog of Drosophila Transient Receptor Potential (Trp) Involved in Calcium Entry Secondary to Activation of Receptors Coupled by the Gq Class of G Protein J. Biol. Chem., November 21, 1997; 272(47): 29672 - 29680. [Abstract] [Full Text] [PDF]

				N. Cherradi, M. F. Rossier, M. B. Vallotton, and A. M. Capponi Calcium Stimulates Intramitochondrial Cholesterol Transfer in Bovine Adrenal Glomerulosa Cells J. Biol. Chem., October 18, 1996; 271(42): 25971 - 25975. [Abstract] [Full Text] [PDF]

				F. W. Hopf, P. Reddy, J. Hong, and R. A. Steinhardt A Capacitative Calcium Current in Cultured Skeletal Muscle Cells Is Mediated by the Calcium-specific Leak Channel and Inhibited by Dihydropyridine Compounds J. Biol. Chem., September 13, 1996; 271(37): 22358 - 22367. [Abstract] [Full Text] [PDF]

				L. Rossig, A. Zolyomi, K. J. Catt, and T. Balla Regulation of Angiotensin II-stimulated Ca2+ Oscillations by Ca2+ Influx Mechanisms in Adrenal Glomerulosa Cells J. Biol. Chem., September 6, 1996; 271(36): 22063 - 22069. [Abstract] [Full Text] [PDF]

				M. F. Rossier, H. B. C. Aptel, C. P. Python, M. M. Burnay, M. B. Vallotton, and A. M. Capponi Inhibition of Low Threshold Calcium Channels by Angiotensin II in Adrenal Glomerulosa Cells through Activation of Protein Kinase C J. Biol. Chem., June 23, 1995; 270(25): 15137 - 15142. [Abstract] [Full Text] [PDF]