Modulation of agonist-induced inositol phosphate metabolism by cyclic adenosine 3′,5′-monophosphate in adrenal glomerulosa cells

Albert J. Baukal, László Hunyady, Tamás Balla, Julie A. Ely, Kevin J. Catt

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

Activation of the cAMP messenger system was found to cause specific changes in angiotensin-II (AII)-induced inositol phosphate production and metabolism in bovine adrenal glomerulosa cells. Pretreatment of [3H]inositol-labeled glomerulosa cells with 8-bromo-cAMP (8Br-cAMP) caused both short and long term changes in the inositol phosphate response to stimulation by All. Exposure to 8Br-cAMP initially caused dose-dependent enhancement (ED50 = 0.7 μM) of the stimulatory action of All (50 nM; 10 min) on the formation of D-myo-inositol 1,4,5-trisphosphate [lns(1,4,5)P3] and its immediate metabolites. This effect of 8Br-cAMP was also observed in permeabilized [3H]inositol-labeled glomerulosa cells in which degradation of lns(1,4,5)P3 was inhibited, consistent with increased activity of phospholipase-C. Continued exposure to 8Br-cAMP for 5-16 h caused selective enhancement of the All-induced increases in D-myo-inositol 1,3,4,6-tetrakisphosphate [lns(1,3,4,6)P4] and myo-inositol 1,4,5,6-tetrakisphosphate. The long term effect of 8Br-cAMP on the 6-phosphorylated lnsP4 isomers, but not the initial enhancement of lns(1,4,5)P3 formation, was inhibited by cycloheximide. The characteristic biphasic kinetics of All-induced lns(1,4,5)P3 formation were also changed by prolonged treatment with 8Br-cAMP to a monophasic response in which lns(1,4,5)P3 increased rapidly and remained elevated during All stimulation. In permeabilized glomerulosa cells treated with 8Br-cAMP for 16 h, the conversion of D-myo-inositol 1,3,4-trisphosphate [lns(1,3,4)P3] to lns(1,3,4,6)P4 was consistently increased, whereas dephosphorylation of lns(1,4,5)P3 to D-myo-inositol 1,4-bisphosphate and of D-myo-inositol 1,3,4,5-tetrakisphosphate to lns(1,3,4)P3, was reduced. Thus, the increased production of higher inositol phosphates during All stimulation of 8Br-cAMP-treated cells results in part from increased phosphorylation of lns(1,3,4)P3 to lns(1,3,4,6)P4, as well as decreased lns(1,4,5)P3-5-phosphatase activity. These findings demonstrate that interactions between the cAMP and inositol phosphate signal generation pathways in the glomerulosa cell lead to enhanced production of higher inositol phosphates that could mediate long term changes in the function of agonist-stimulated adrenal cells.

Original languageEnglish
Pages (from-to)1712-1719
Number of pages8
JournalMolecular Endocrinology
Volume4
Issue number11
Publication statusPublished - 1990

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Zona Glomerulosa
8-Bromo Cyclic Adenosine Monophosphate
Adenosine
Inositol Phosphates
Inositol
Inositol 1,4,5-Trisphosphate
inositol cyclic phosphate
Type C Phospholipases
Cycloheximide
Phosphoric Monoester Hydrolases
Angiotensin II
Signal Transduction
Phosphorylation

ASJC Scopus subject areas

  • Molecular Biology
  • Endocrinology, Diabetes and Metabolism

Cite this

Modulation of agonist-induced inositol phosphate metabolism by cyclic adenosine 3′,5′-monophosphate in adrenal glomerulosa cells. / Baukal, Albert J.; Hunyady, László; Balla, Tamás; Ely, Julie A.; Catt, Kevin J.

In: Molecular Endocrinology, Vol. 4, No. 11, 1990, p. 1712-1719.

Research output: Contribution to journalArticle

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abstract = "Activation of the cAMP messenger system was found to cause specific changes in angiotensin-II (AII)-induced inositol phosphate production and metabolism in bovine adrenal glomerulosa cells. Pretreatment of [3H]inositol-labeled glomerulosa cells with 8-bromo-cAMP (8Br-cAMP) caused both short and long term changes in the inositol phosphate response to stimulation by All. Exposure to 8Br-cAMP initially caused dose-dependent enhancement (ED50 = 0.7 μM) of the stimulatory action of All (50 nM; 10 min) on the formation of D-myo-inositol 1,4,5-trisphosphate [lns(1,4,5)P3] and its immediate metabolites. This effect of 8Br-cAMP was also observed in permeabilized [3H]inositol-labeled glomerulosa cells in which degradation of lns(1,4,5)P3 was inhibited, consistent with increased activity of phospholipase-C. Continued exposure to 8Br-cAMP for 5-16 h caused selective enhancement of the All-induced increases in D-myo-inositol 1,3,4,6-tetrakisphosphate [lns(1,3,4,6)P4] and myo-inositol 1,4,5,6-tetrakisphosphate. The long term effect of 8Br-cAMP on the 6-phosphorylated lnsP4 isomers, but not the initial enhancement of lns(1,4,5)P3 formation, was inhibited by cycloheximide. The characteristic biphasic kinetics of All-induced lns(1,4,5)P3 formation were also changed by prolonged treatment with 8Br-cAMP to a monophasic response in which lns(1,4,5)P3 increased rapidly and remained elevated during All stimulation. In permeabilized glomerulosa cells treated with 8Br-cAMP for 16 h, the conversion of D-myo-inositol 1,3,4-trisphosphate [lns(1,3,4)P3] to lns(1,3,4,6)P4 was consistently increased, whereas dephosphorylation of lns(1,4,5)P3 to D-myo-inositol 1,4-bisphosphate and of D-myo-inositol 1,3,4,5-tetrakisphosphate to lns(1,3,4)P3, was reduced. Thus, the increased production of higher inositol phosphates during All stimulation of 8Br-cAMP-treated cells results in part from increased phosphorylation of lns(1,3,4)P3 to lns(1,3,4,6)P4, as well as decreased lns(1,4,5)P3-5-phosphatase activity. These findings demonstrate that interactions between the cAMP and inositol phosphate signal generation pathways in the glomerulosa cell lead to enhanced production of higher inositol phosphates that could mediate long term changes in the function of agonist-stimulated adrenal cells.",
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N2 - Activation of the cAMP messenger system was found to cause specific changes in angiotensin-II (AII)-induced inositol phosphate production and metabolism in bovine adrenal glomerulosa cells. Pretreatment of [3H]inositol-labeled glomerulosa cells with 8-bromo-cAMP (8Br-cAMP) caused both short and long term changes in the inositol phosphate response to stimulation by All. Exposure to 8Br-cAMP initially caused dose-dependent enhancement (ED50 = 0.7 μM) of the stimulatory action of All (50 nM; 10 min) on the formation of D-myo-inositol 1,4,5-trisphosphate [lns(1,4,5)P3] and its immediate metabolites. This effect of 8Br-cAMP was also observed in permeabilized [3H]inositol-labeled glomerulosa cells in which degradation of lns(1,4,5)P3 was inhibited, consistent with increased activity of phospholipase-C. Continued exposure to 8Br-cAMP for 5-16 h caused selective enhancement of the All-induced increases in D-myo-inositol 1,3,4,6-tetrakisphosphate [lns(1,3,4,6)P4] and myo-inositol 1,4,5,6-tetrakisphosphate. The long term effect of 8Br-cAMP on the 6-phosphorylated lnsP4 isomers, but not the initial enhancement of lns(1,4,5)P3 formation, was inhibited by cycloheximide. The characteristic biphasic kinetics of All-induced lns(1,4,5)P3 formation were also changed by prolonged treatment with 8Br-cAMP to a monophasic response in which lns(1,4,5)P3 increased rapidly and remained elevated during All stimulation. In permeabilized glomerulosa cells treated with 8Br-cAMP for 16 h, the conversion of D-myo-inositol 1,3,4-trisphosphate [lns(1,3,4)P3] to lns(1,3,4,6)P4 was consistently increased, whereas dephosphorylation of lns(1,4,5)P3 to D-myo-inositol 1,4-bisphosphate and of D-myo-inositol 1,3,4,5-tetrakisphosphate to lns(1,3,4)P3, was reduced. Thus, the increased production of higher inositol phosphates during All stimulation of 8Br-cAMP-treated cells results in part from increased phosphorylation of lns(1,3,4)P3 to lns(1,3,4,6)P4, as well as decreased lns(1,4,5)P3-5-phosphatase activity. These findings demonstrate that interactions between the cAMP and inositol phosphate signal generation pathways in the glomerulosa cell lead to enhanced production of higher inositol phosphates that could mediate long term changes in the function of agonist-stimulated adrenal cells.

AB - Activation of the cAMP messenger system was found to cause specific changes in angiotensin-II (AII)-induced inositol phosphate production and metabolism in bovine adrenal glomerulosa cells. Pretreatment of [3H]inositol-labeled glomerulosa cells with 8-bromo-cAMP (8Br-cAMP) caused both short and long term changes in the inositol phosphate response to stimulation by All. Exposure to 8Br-cAMP initially caused dose-dependent enhancement (ED50 = 0.7 μM) of the stimulatory action of All (50 nM; 10 min) on the formation of D-myo-inositol 1,4,5-trisphosphate [lns(1,4,5)P3] and its immediate metabolites. This effect of 8Br-cAMP was also observed in permeabilized [3H]inositol-labeled glomerulosa cells in which degradation of lns(1,4,5)P3 was inhibited, consistent with increased activity of phospholipase-C. Continued exposure to 8Br-cAMP for 5-16 h caused selective enhancement of the All-induced increases in D-myo-inositol 1,3,4,6-tetrakisphosphate [lns(1,3,4,6)P4] and myo-inositol 1,4,5,6-tetrakisphosphate. The long term effect of 8Br-cAMP on the 6-phosphorylated lnsP4 isomers, but not the initial enhancement of lns(1,4,5)P3 formation, was inhibited by cycloheximide. The characteristic biphasic kinetics of All-induced lns(1,4,5)P3 formation were also changed by prolonged treatment with 8Br-cAMP to a monophasic response in which lns(1,4,5)P3 increased rapidly and remained elevated during All stimulation. In permeabilized glomerulosa cells treated with 8Br-cAMP for 16 h, the conversion of D-myo-inositol 1,3,4-trisphosphate [lns(1,3,4)P3] to lns(1,3,4,6)P4 was consistently increased, whereas dephosphorylation of lns(1,4,5)P3 to D-myo-inositol 1,4-bisphosphate and of D-myo-inositol 1,3,4,5-tetrakisphosphate to lns(1,3,4)P3, was reduced. Thus, the increased production of higher inositol phosphates during All stimulation of 8Br-cAMP-treated cells results in part from increased phosphorylation of lns(1,3,4)P3 to lns(1,3,4,6)P4, as well as decreased lns(1,4,5)P3-5-phosphatase activity. These findings demonstrate that interactions between the cAMP and inositol phosphate signal generation pathways in the glomerulosa cell lead to enhanced production of higher inositol phosphates that could mediate long term changes in the function of agonist-stimulated adrenal cells.

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