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Calcium Signaling Systems

Stanko S. Stojilkovic

10.1002/cphy.cp070109

Source: Supplement 20: Handbook of Physiology, The Endocrine System, Cellular Endocrinology

Originally published: 1998

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Voltage‐Dependent Calcium‐Signaling System
1.1 Voltage‐Gated Calcium Channels
1.2 Basal Pacemaker Activity
1.3 Agonist‐Induced Modulation of Pacemaker Activity
2 Calcium Mobilization–Dependent Signaling System
2.1 Inositol (1,4,5)‐Triphosphate (IP3) and IP3 Receptor (IP3R) Channels
2.2 cADP Ribose and RyR Channels
2.3 Calcium Pumps
2.4 Intracellular Calcium Buffers
3 Calcium Entry Controlled by Calcium Mobilization
3.1 Capacitative Calcium Entry
3.2 Voltage‐Gated Calcium Entry
4 Temporal and Spatial Organization of Calcium Signals
4.1 Local and Global Calcium Spikes
4.2 Cell Specificity of Calcium Signaling
4.3 Receptor Specificity of Calcium Signaling
4.4 Concentration‐Dependent Regulation
4.5 Intraorganelle Calcium Signaling
5 Amplification and Synchronization of Calcium Signals
5.1 Purinergic Receptor Channels
5.2 Gap Junction Channels
6 Cellular Functions of Calcium Signals
6.1 Calcium‐Controlled Enzymes
6.2 Calcium‐Controlled Channels
6.3 Calcium Signaling and Exocytosis
6.4 Mitochondrial Functions and Calcium Signals
6.5 Nuclear Functions and Calcium Signals
7 Summary
Figure 1. Figure 1.

Spontaneous plasma membrane oscillator activity in rat pituitary gonadotrophs. A: Simultaneous recording of membrane potential Vm and [Ca2+]i during spontaneous firing of action potentials. B: Sensitivity of firing frequency to current injection. [From Li et al. 234 with permission.]
Figure 2. Figure 2.

Comparison of effects of gonadotropin‐releasing hormone (GnRH) (left panels) and inositol(1,4,5)‐triphosphate [Ins(1,4,5)P3] (right panels) on pattern of Ca2+ spiking in rat gonadotrophs: GnRH‐induced [Ca2+]i oscillations were measured in intact cells loaded with Indo 1‐AM; IP3‐induced [Ca2+]i oscillations were measured indirectly, by a calcium‐controlled potassium current, and IP3 was injected through the pipette. [From Stojilkovic et al. 429 with permission.]
Figure 3. Figure 3.

Schematic representation of the endoplasmic reticulum (ER) oscillator. CMR, seven‐membrane‐domain calcium‐mobilizing receptor; PM, plasma membrane; PLC, phospholipase C; DAG, diacyglycerol; PKC, protein kinase C; InsP3, inositol1,4,5‐trisphosphate.
Figure 4. Figure 4.

Components of the agonist‐induced calcium signal in an excitable cell. A: Spike and plateau phases of the [Ca2+]i response to agonist stimulation can be resolved into a largely extracellular calcium–independent component and an influx‐dependent component (dashed area). B: Extracellular calcium–dependent component in agonist‐induced [Ca2+]i response can be analyzed further by utilizing specific inhibitors of plasma membrane calcium channels.
Figure 5. Figure 5.

Kinetics of depletion and repletion of agonist‐sensitive calcium pool. A: Typical pattern of [Ca2+]i oscillations in a single rat gonadotroph. B: Store calcium content is expressed as a percentage of prestimulus level. Open circles, endoplasmic reticulum calcium content during gonadotropin‐releasing hormone (GnRH) stimulation. Closed circles, endoplasmic reticulum calcium content after withdrawal of GnRH. Estimation of intraluminal Ca2+ was done by ionomycin applied at different times after GnRH stimulation.
Figure 6. Figure 6.

Patterns of synchronization of [Ca2+]i and membrane potentials in cells operated by calcium‐mobilizing receptors. Schematic representation of thyroid‐releasing hormone (TRH)‐induced [Ca2+]i and membrane potential (Vm) responses in lactotrophs (A) and gonadotropin‐releasing hormone (GnRH)‐induced [Ca2+]i and Vm responses in gonadotrophs (B).

[From S. S. Stojilkovic and K. J. Catt. Calcium oscillations in anterior pituitary cells. Endocr. Rev. 13: 256–280, 1992, with permission. © The Endocrine Society.]
Figure 7. Figure 7.

Concentration‐dependent voltage‐response profiles in agonist (experimental records)‐ and inositol1,4,5‐triphosphate (InsP3) (model simulations) stimulated gonadotrophs. In experiments, increasing concentrations of gonadotropin‐releasing hormone (GnRH) were applied at the arrow. In model simulations, increasing concentrations of InsP3 were used.

[From Li et al. 235 with permission.]
Figure 8. Figure 8.

Dependence of spiking frequency on agonist concentration and calcium influx. A: Modulation of Ca2+ spiking frequency by depolarization (left panel) and by increase in gonadotropin‐releasing hormone (GnRH) concentration (right panel). B: Membrane potential (Vm) dependence of depolarization on sustained GnRH‐induced Ca2+ oscillations. Dashed horizontal line indicates maximum frequency response reached 150 s after initiation of oscillations at the holding potential of −50 mV. In a step‐depolarization protocol, calcium‐activated potassium current was employed as an indicator of cytosolic calcium concentration.

[From Kukuljan et al. 211 with permission.]
Figure 9. Figure 9.

Nonoscillatory calcium responses in single parathyroid cells, GT1‐7 neurons, and Leydig cells. No obvious modulations of the amplitude of [Ca2+]i response to increasing endothelin‐1(ET‐1) concentrations were observed in parathyroid and Leydig cells. In GT1‐7 cells, a consistent increase in the amplitude of [Ca2+]i response to increasing concentrations of endothelin‐1 was observed. GnRH, gonadotropin‐releasing hormone; GnRH‐Ant., GnRh antagonist; BQ‐123, ETA receptor antagonist.

[From M. Tomic, M. L. Dufau, K. K. Catt, and S. S. Stojilkovic. Calcium signaling in single rat Leydig cells. Endocrinology 136: 3422–3429, 1995. © The Endocrine Society.]
Figure 10. Figure 10.

Comparison of the patterns of gonadotropin‐releasing hormone (GnRH)‐induced [Ca2+]i responses in rat gonadotrophs and Leydig cells. A: Time dependence of the [Ca2+]i response in the two cell types. Two upper tracings are from gonadotrophs and bottom tracing from a Leydig cell. B: Concentration‐dependent effects of GnRH on the number of cells showing biphasic responses in gonadotrophs and Leydig cells. Dotted lines illustrate EC50 values.
Figure 11. Figure 11.

Dependence of the frequency of Ca2+ spiking on agonist concentrations in rat gonadotrophs. Data for concentration responses for gonadotropin‐releasing hormone (GnRH) and endothelin‐1 (ET‐1) were derived from Stojilkovic et al. 422 and those for pituitary adenylate cyclase–activating polypeptide (PACAP) from unpublished results.
Figure 12. Figure 12.

Comparison of concentration dependence and [Ca2+]i signaling patterns in Leydig cells, GT1‐7 neurons, and pituitary gonadotrophs stimulated with gonadotropin‐releasing hormone (GnRH). Left panels: Data for concentration responses were derived from Iida et al. 169, Krsmanovic et al. 208, and Tomic et al. 453. Right panels: Schematic representation of the pattern of Ca2+ signals.

[From M. Tomic, M. L. Dufau, K. J. Catt, and S. S. Stojikovic 454. Calcium signaling in single rat Leydig cells. Endocrinology 136: 3422–3429, 1995. © The Endocrine Society.]
Figure 13. Figure 13.

Schematic representation of intracellular calcium releasable pools. PM, plasma membrane, ER, endoplasmic reticulum; IP3R, inositol‐1,4,5‐triphosphate receptor; m., membrane.
Figure 14. Figure 14.

Schematic representation of purinergic system for self‐amplification of Ca2+ signals and secretion, as well as cell‐to‐cell spreading of Ca2+ signals. Co‐secretion of ATP with hormone is essential for initiation of this signaling system. CMR, calcium‐mobilizing receptors; DAG, diacylglycerol; PKC, protein kinase C; IP3, inositol‐1,4,5‐triphosphate.
Figure 15. Figure 15.

Effects of ATP on the plasma membrane oscillator in identified rat gonadotrophs. A: Initiation of [Ca2+]i spiking in silent cells by ATP (left panel) and modulation of spiking frequency in spontaneously active cells by increasing concentrations of ATP (right panel). B: Effects of Mg2+ on ATP‐induced spiking (left panel) and lack of effects of Mg2+ on spontaneously driven Ca2+ (right panel). C: Addition of high (100 μM) ATP abolishes spontaneous and ATP‐induced Ca2+ transients. D: In cells stimulated with high ATP, addition of P2 receptor blocker suramin and Mg2+ reestablished the oscillatory pattern of [Ca2+]i spiking.

[From Tomic et al. 455 with permission.]
Figure 16. Figure 16.

Effects of extracellular ATP on gonadotropin‐releasing hormone (GnRH)‐induced [Ca2+]i and secretory response. A: Effects of ATP on frequency of spiking during sustained GnRH stimulation. B: Effects of ATP on sustained GnRH‐induced luteinizing hormone (LH) release in perifused pituitary cells.

[From Tomic et al. 455 with permission.]
Figure 17. Figure 17.

Transcriptional regulation of c‐fos by multiple intracellular messengers. DAG, diacylglycerol; PKC, protein kinase C; CaMK, calmodulin kinase; PKA, protein kinase A; CREB, cAMP‐responsive element‐binding protein; SRF, serum response factor.

[From S. S. Stojilkovic, J. Reinhart, and K. J. Catt 431. GnRH receptors: structure and signal transduction pathways. Endocr. Rev. 15: 462–499, 1994, with permission. © The Endocrine Society.]


Figure 1.

Spontaneous plasma membrane oscillator activity in rat pituitary gonadotrophs. A: Simultaneous recording of membrane potential Vm and [Ca2+]i during spontaneous firing of action potentials. B: Sensitivity of firing frequency to current injection. [From Li et al. 234 with permission.]



Figure 2.

Comparison of effects of gonadotropin‐releasing hormone (GnRH) (left panels) and inositol(1,4,5)‐triphosphate [Ins(1,4,5)P3] (right panels) on pattern of Ca2+ spiking in rat gonadotrophs: GnRH‐induced [Ca2+]i oscillations were measured in intact cells loaded with Indo 1‐AM; IP3‐induced [Ca2+]i oscillations were measured indirectly, by a calcium‐controlled potassium current, and IP3 was injected through the pipette. [From Stojilkovic et al. 429 with permission.]



Figure 3.

Schematic representation of the endoplasmic reticulum (ER) oscillator. CMR, seven‐membrane‐domain calcium‐mobilizing receptor; PM, plasma membrane; PLC, phospholipase C; DAG, diacyglycerol; PKC, protein kinase C; InsP3, inositol1,4,5‐trisphosphate.



Figure 4.

Components of the agonist‐induced calcium signal in an excitable cell. A: Spike and plateau phases of the [Ca2+]i response to agonist stimulation can be resolved into a largely extracellular calcium–independent component and an influx‐dependent component (dashed area). B: Extracellular calcium–dependent component in agonist‐induced [Ca2+]i response can be analyzed further by utilizing specific inhibitors of plasma membrane calcium channels.



Figure 5.

Kinetics of depletion and repletion of agonist‐sensitive calcium pool. A: Typical pattern of [Ca2+]i oscillations in a single rat gonadotroph. B: Store calcium content is expressed as a percentage of prestimulus level. Open circles, endoplasmic reticulum calcium content during gonadotropin‐releasing hormone (GnRH) stimulation. Closed circles, endoplasmic reticulum calcium content after withdrawal of GnRH. Estimation of intraluminal Ca2+ was done by ionomycin applied at different times after GnRH stimulation.



Figure 6.

Patterns of synchronization of [Ca2+]i and membrane potentials in cells operated by calcium‐mobilizing receptors. Schematic representation of thyroid‐releasing hormone (TRH)‐induced [Ca2+]i and membrane potential (Vm) responses in lactotrophs (A) and gonadotropin‐releasing hormone (GnRH)‐induced [Ca2+]i and Vm responses in gonadotrophs (B).

[From S. S. Stojilkovic and K. J. Catt. Calcium oscillations in anterior pituitary cells. Endocr. Rev. 13: 256–280, 1992, with permission. © The Endocrine Society.]


Figure 7.

Concentration‐dependent voltage‐response profiles in agonist (experimental records)‐ and inositol1,4,5‐triphosphate (InsP3) (model simulations) stimulated gonadotrophs. In experiments, increasing concentrations of gonadotropin‐releasing hormone (GnRH) were applied at the arrow. In model simulations, increasing concentrations of InsP3 were used.

[From Li et al. 235 with permission.]


Figure 8.

Dependence of spiking frequency on agonist concentration and calcium influx. A: Modulation of Ca2+ spiking frequency by depolarization (left panel) and by increase in gonadotropin‐releasing hormone (GnRH) concentration (right panel). B: Membrane potential (Vm) dependence of depolarization on sustained GnRH‐induced Ca2+ oscillations. Dashed horizontal line indicates maximum frequency response reached 150 s after initiation of oscillations at the holding potential of −50 mV. In a step‐depolarization protocol, calcium‐activated potassium current was employed as an indicator of cytosolic calcium concentration.

[From Kukuljan et al. 211 with permission.]


Figure 9.

Nonoscillatory calcium responses in single parathyroid cells, GT1‐7 neurons, and Leydig cells. No obvious modulations of the amplitude of [Ca2+]i response to increasing endothelin‐1(ET‐1) concentrations were observed in parathyroid and Leydig cells. In GT1‐7 cells, a consistent increase in the amplitude of [Ca2+]i response to increasing concentrations of endothelin‐1 was observed. GnRH, gonadotropin‐releasing hormone; GnRH‐Ant., GnRh antagonist; BQ‐123, ETA receptor antagonist.

[From M. Tomic, M. L. Dufau, K. K. Catt, and S. S. Stojilkovic. Calcium signaling in single rat Leydig cells. Endocrinology 136: 3422–3429, 1995. © The Endocrine Society.]


Figure 10.

Comparison of the patterns of gonadotropin‐releasing hormone (GnRH)‐induced [Ca2+]i responses in rat gonadotrophs and Leydig cells. A: Time dependence of the [Ca2+]i response in the two cell types. Two upper tracings are from gonadotrophs and bottom tracing from a Leydig cell. B: Concentration‐dependent effects of GnRH on the number of cells showing biphasic responses in gonadotrophs and Leydig cells. Dotted lines illustrate EC50 values.



Figure 11.

Dependence of the frequency of Ca2+ spiking on agonist concentrations in rat gonadotrophs. Data for concentration responses for gonadotropin‐releasing hormone (GnRH) and endothelin‐1 (ET‐1) were derived from Stojilkovic et al. 422 and those for pituitary adenylate cyclase–activating polypeptide (PACAP) from unpublished results.



Figure 12.

Comparison of concentration dependence and [Ca2+]i signaling patterns in Leydig cells, GT1‐7 neurons, and pituitary gonadotrophs stimulated with gonadotropin‐releasing hormone (GnRH). Left panels: Data for concentration responses were derived from Iida et al. 169, Krsmanovic et al. 208, and Tomic et al. 453. Right panels: Schematic representation of the pattern of Ca2+ signals.

[From M. Tomic, M. L. Dufau, K. J. Catt, and S. S. Stojikovic 454. Calcium signaling in single rat Leydig cells. Endocrinology 136: 3422–3429, 1995. © The Endocrine Society.]


Figure 13.

Schematic representation of intracellular calcium releasable pools. PM, plasma membrane, ER, endoplasmic reticulum; IP3R, inositol‐1,4,5‐triphosphate receptor; m., membrane.



Figure 14.

Schematic representation of purinergic system for self‐amplification of Ca2+ signals and secretion, as well as cell‐to‐cell spreading of Ca2+ signals. Co‐secretion of ATP with hormone is essential for initiation of this signaling system. CMR, calcium‐mobilizing receptors; DAG, diacylglycerol; PKC, protein kinase C; IP3, inositol‐1,4,5‐triphosphate.



Figure 15.

Effects of ATP on the plasma membrane oscillator in identified rat gonadotrophs. A: Initiation of [Ca2+]i spiking in silent cells by ATP (left panel) and modulation of spiking frequency in spontaneously active cells by increasing concentrations of ATP (right panel). B: Effects of Mg2+ on ATP‐induced spiking (left panel) and lack of effects of Mg2+ on spontaneously driven Ca2+ (right panel). C: Addition of high (100 μM) ATP abolishes spontaneous and ATP‐induced Ca2+ transients. D: In cells stimulated with high ATP, addition of P2 receptor blocker suramin and Mg2+ reestablished the oscillatory pattern of [Ca2+]i spiking.

[From Tomic et al. 455 with permission.]


Figure 16.

Effects of extracellular ATP on gonadotropin‐releasing hormone (GnRH)‐induced [Ca2+]i and secretory response. A: Effects of ATP on frequency of spiking during sustained GnRH stimulation. B: Effects of ATP on sustained GnRH‐induced luteinizing hormone (LH) release in perifused pituitary cells.

[From Tomic et al. 455 with permission.]


Figure 17.

Transcriptional regulation of c‐fos by multiple intracellular messengers. DAG, diacylglycerol; PKC, protein kinase C; CaMK, calmodulin kinase; PKA, protein kinase A; CREB, cAMP‐responsive element‐binding protein; SRF, serum response factor.

[From S. S. Stojilkovic, J. Reinhart, and K. J. Catt 431. GnRH receptors: structure and signal transduction pathways. Endocr. Rev. 15: 462–499, 1994, with permission. © The Endocrine Society.]
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Article Title: Calcium Signaling Systems
 

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Stanko S. Stojilkovic. Calcium Signaling Systems. Compr Physiol 2011, Supplement 20: Handbook of Physiology, The Endocrine System, Cellular Endocrinology: 177-224. First published in print 1998. doi: 10.1002/cphy.cp070109