Activation of a cGMP-sensitive calcium-dependent chloride channel may cause transition from calcium waves to whole cell oscillations in smooth muscle cells.

Jens Christian Brings Jacobsen; Christian Aalkjær; Holger Nilsson; Vladimir V Matchkov; Jacob Freiberg; N.-H. Holstein-Rathlou

doi:10.1152/ajpheart.00726.2006

Activation of a cGMP-sensitive calcium-dependent chloride channel may cause transition from calcium waves to whole cell oscillations in smooth muscle cells.

Jens Christian Brings Jacobsen, Christian Aalkjær, Holger Nilsson, Vladimir V Matchkov, Jacob Freiberg, N.-H. Holstein-Rathlou

36 Citations (Scopus)

Abstract

In vitro, alpha-adrenoreceptor stimulation of rat mesenteric small arteries often leads to a rhythmic change in wall tension, i.e., vasomotion. Within the individual smooth muscle cells of the vascular wall, vasomotion is often preceded by a period of asynchronous calcium waves. Abruptly, these low-frequency waves may transform into high-frequency whole cell calcium oscillations. Simultaneously, multiple cells synchronize, leading to rhythmic generation of tension. We present a mathematical model of vascular smooth muscle cells that aims at characterizing this sudden transition. Simulations show calcium waves sweeping through the cytoplasm when the sarcoplasmic reticulum (SR) is stimulated to release calcium. A rise in cGMP leads to the experimentally observed transition from waves to whole cell calcium oscillations. At the same time, membrane potential starts to oscillate and the frequency approximately doubles. In this transition, the simulated results point to a key role for a recently discovered cGMP-sensitive calcium-dependent chloride channel. This channel depolarizes the membrane in response to calcium released from the SR. In turn, depolarization causes a uniform opening of L-type calcium channels on the cell surface, stimulating a synchronized release of SR calcium and inducing the shift from waves to whole cell oscillations. The effect of the channel is therefore to couple the processes of the SR with those of the membrane. We hypothesize that the shift in oscillatory mode and the associated onset of oscillations in membrane potential within the individual cell may underlie sudden intercellular synchronization and the appearance of vasomotion.

Original language	English
Journal	American Journal of Physiology: Heart and Circulatory Physiology
Volume	293
Issue number	1
Pages (from-to)	H215-28
ISSN	0363-6135
DOIs	https://doi.org/10.1152/ajpheart.00726.2006
Publication status	Published - 2007

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Jacobsen, J. C. B., Aalkjær, C., Nilsson, H., Matchkov, V. V., Freiberg, J., & Holstein-Rathlou, N-H. (2007). Activation of a cGMP-sensitive calcium-dependent chloride channel may cause transition from calcium waves to whole cell oscillations in smooth muscle cells. American Journal of Physiology: Heart and Circulatory Physiology, 293(1), H215-28. https://doi.org/10.1152/ajpheart.00726.2006

Activation of a cGMP-sensitive calcium-dependent chloride channel may cause transition from calcium waves to whole cell oscillations in smooth muscle cells. / Jacobsen, Jens Christian Brings ; Aalkjær, Christian; Nilsson, Holger et al.

In: American Journal of Physiology: Heart and Circulatory Physiology, Vol. 293, No. 1, 2007, p. H215-28.

Research output: Contribution to journal › Journal article › Research › peer-review

Jacobsen, JCB , Aalkjær, C, Nilsson, H, Matchkov, VV, Freiberg, J & Holstein-Rathlou, N-H 2007, 'Activation of a cGMP-sensitive calcium-dependent chloride channel may cause transition from calcium waves to whole cell oscillations in smooth muscle cells.', American Journal of Physiology: Heart and Circulatory Physiology, vol. 293, no. 1, pp. H215-28. https://doi.org/10.1152/ajpheart.00726.2006

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title = "Activation of a cGMP-sensitive calcium-dependent chloride channel may cause transition from calcium waves to whole cell oscillations in smooth muscle cells.",

abstract = "In vitro, alpha-adrenoreceptor stimulation of rat mesenteric small arteries often leads to a rhythmic change in wall tension, i.e., vasomotion. Within the individual smooth muscle cells of the vascular wall, vasomotion is often preceded by a period of asynchronous calcium waves. Abruptly, these low-frequency waves may transform into high-frequency whole cell calcium oscillations. Simultaneously, multiple cells synchronize, leading to rhythmic generation of tension. We present a mathematical model of vascular smooth muscle cells that aims at characterizing this sudden transition. Simulations show calcium waves sweeping through the cytoplasm when the sarcoplasmic reticulum (SR) is stimulated to release calcium. A rise in cGMP leads to the experimentally observed transition from waves to whole cell calcium oscillations. At the same time, membrane potential starts to oscillate and the frequency approximately doubles. In this transition, the simulated results point to a key role for a recently discovered cGMP-sensitive calcium-dependent chloride channel. This channel depolarizes the membrane in response to calcium released from the SR. In turn, depolarization causes a uniform opening of L-type calcium channels on the cell surface, stimulating a synchronized release of SR calcium and inducing the shift from waves to whole cell oscillations. The effect of the channel is therefore to couple the processes of the SR with those of the membrane. We hypothesize that the shift in oscillatory mode and the associated onset of oscillations in membrane potential within the individual cell may underlie sudden intercellular synchronization and the appearance of vasomotion.",

author = "Jacobsen, {Jens Christian Brings} and Christian Aalkj{\ae}r and Holger Nilsson and Matchkov, {Vladimir V} and Jacob Freiberg and N.-H. Holstein-Rathlou",

note = "Keywords: Adaptation, Physiological; Animals; Biological Clocks; Calcium; Calcium Signaling; Cells, Cultured; Chloride Channels; Computer Simulation; Cyclic GMP; Humans; Ion Channel Gating; Models, Cardiovascular; Muscle, Smooth, Vascular; Myocytes, Smooth Muscle",

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AU - Jacobsen, Jens Christian Brings

AU - Aalkjær, Christian

AU - Nilsson, Holger

AU - Matchkov, Vladimir V

AU - Freiberg, Jacob

AU - Holstein-Rathlou, N.-H.

N1 - Keywords: Adaptation, Physiological; Animals; Biological Clocks; Calcium; Calcium Signaling; Cells, Cultured; Chloride Channels; Computer Simulation; Cyclic GMP; Humans; Ion Channel Gating; Models, Cardiovascular; Muscle, Smooth, Vascular; Myocytes, Smooth Muscle

PY - 2007

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N2 - In vitro, alpha-adrenoreceptor stimulation of rat mesenteric small arteries often leads to a rhythmic change in wall tension, i.e., vasomotion. Within the individual smooth muscle cells of the vascular wall, vasomotion is often preceded by a period of asynchronous calcium waves. Abruptly, these low-frequency waves may transform into high-frequency whole cell calcium oscillations. Simultaneously, multiple cells synchronize, leading to rhythmic generation of tension. We present a mathematical model of vascular smooth muscle cells that aims at characterizing this sudden transition. Simulations show calcium waves sweeping through the cytoplasm when the sarcoplasmic reticulum (SR) is stimulated to release calcium. A rise in cGMP leads to the experimentally observed transition from waves to whole cell calcium oscillations. At the same time, membrane potential starts to oscillate and the frequency approximately doubles. In this transition, the simulated results point to a key role for a recently discovered cGMP-sensitive calcium-dependent chloride channel. This channel depolarizes the membrane in response to calcium released from the SR. In turn, depolarization causes a uniform opening of L-type calcium channels on the cell surface, stimulating a synchronized release of SR calcium and inducing the shift from waves to whole cell oscillations. The effect of the channel is therefore to couple the processes of the SR with those of the membrane. We hypothesize that the shift in oscillatory mode and the associated onset of oscillations in membrane potential within the individual cell may underlie sudden intercellular synchronization and the appearance of vasomotion.

AB - In vitro, alpha-adrenoreceptor stimulation of rat mesenteric small arteries often leads to a rhythmic change in wall tension, i.e., vasomotion. Within the individual smooth muscle cells of the vascular wall, vasomotion is often preceded by a period of asynchronous calcium waves. Abruptly, these low-frequency waves may transform into high-frequency whole cell calcium oscillations. Simultaneously, multiple cells synchronize, leading to rhythmic generation of tension. We present a mathematical model of vascular smooth muscle cells that aims at characterizing this sudden transition. Simulations show calcium waves sweeping through the cytoplasm when the sarcoplasmic reticulum (SR) is stimulated to release calcium. A rise in cGMP leads to the experimentally observed transition from waves to whole cell calcium oscillations. At the same time, membrane potential starts to oscillate and the frequency approximately doubles. In this transition, the simulated results point to a key role for a recently discovered cGMP-sensitive calcium-dependent chloride channel. This channel depolarizes the membrane in response to calcium released from the SR. In turn, depolarization causes a uniform opening of L-type calcium channels on the cell surface, stimulating a synchronized release of SR calcium and inducing the shift from waves to whole cell oscillations. The effect of the channel is therefore to couple the processes of the SR with those of the membrane. We hypothesize that the shift in oscillatory mode and the associated onset of oscillations in membrane potential within the individual cell may underlie sudden intercellular synchronization and the appearance of vasomotion.

U2 - 10.1152/ajpheart.00726.2006

DO - 10.1152/ajpheart.00726.2006

M3 - Journal article

C2 - 17369468

SN - 0363-6135

VL - 293

SP - H215-28

JO - American Journal of Physiology - Heart and Circulatory Physiology

JF - American Journal of Physiology - Heart and Circulatory Physiology

IS - 1

ER -

Activation of a cGMP-sensitive calcium-dependent chloride channel may cause transition from calcium waves to whole cell oscillations in smooth muscle cells.

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