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© The Rockefeller University Press, 0022-1295/1999//229/ $5.00
Journal of General Physiology, Volume 113, Number 2, 1999

Article

Functional Coupling of Ryanodine Receptors to KCa Channels in Smooth Muscle Cells from Rat Cerebral Arteries

Guillermo J. Pérez*, Adrian D. Bonev*, Joseph B. Patlak{ddagger}, and Mark T. Nelson*

From the * Department of Pharmacology and {ddagger} Department of Molecular Physiology and Biophysics, The University of Vermont, Burlington, Vermont 05405

The relationship between Ca2+ release ("Ca2+ sparks") through ryanodine-sensitive Ca2+ release channels in the sarcoplasmic reticulum and KCa channels was examined in smooth muscle cells from rat cerebral arteries. Whole cell potassium currents at physiological membrane potentials (–40 mV) and intracellular Ca2+ were measured simultaneously, using the perforated patch clamp technique and a laser two-dimensional (x–y) scanning confocal microscope and the fluorescent Ca2+ indicator, fluo-3. Virtually all (96%) detectable Ca2+ sparks were associated with the activation of a spontaneous transient outward current (STOC) through KCa channels. A small number of sparks (5 of 128) were associated with currents smaller than 6 pA (mean amplitude, 4.7 pA, at –40 mV). Approximately 41% of STOCs occurred without a detectable Ca2+ spark. The amplitudes of the Ca2+ sparks correlated with the amplitudes of the STOCs (regression coefficient 0.8; P < 0.05). The half time of decay of Ca2+ sparks (56 ms) was longer than the associated STOCs (9 ms). The mean amplitude of the STOCs, which were associated with Ca2+ sparks, was 33 pA at –40 mV. The mean amplitude of the "sparkless" STOCs was smaller, 16 pA. The very significant increase in KCa channel open probability (>104-fold) during a Ca2+ spark is consistent with local Ca2+ during a spark being in the order of 1–100 µM. Therefore, the increase in fractional fluorescence (F/Fo) measured during a Ca2+ spark (mean 2.04 F/Fo or ~310 nM Ca2+) appears to significantly underestimate the local Ca2+ that activates KCa channels. These results indicate that the majority of ryanodine receptors that cause Ca2+ sparks are functionally coupled to KCa channels in the surface membrane, providing direct support for the idea that Ca2+ sparks cause STOCs.

Key Words: Ca2+ sparks • ryanodine receptor • sarcoplasmic reticulum • potassium currents • smooth muscle

Address correspondence to Dr. M.T. Nelson, Department of Pharmacology, Given Building, The University of Vermont, Burlington, VT 05405. Fax: 802-656-4523; E-mail: nelson{at}salus.med.uvm.edu

Abbreviations: ES, enzyme solution; Fo, baseline fluorescence; RyR, ryanodine receptors; SR, sarcoplasmic reticulum; STOC, spontaneous transient outward current


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 Am. J. Physiol. Cell Physiol.Home page
O. Bayguinov, B. Hagen, J. L. Kenyon, and K. M. Sanders
Coupling strength between localized Ca2+ transients and K+ channels is regulated by protein kinase C
Am J Physiol Cell Physiol, November 1, 2001; 281(5): C1512 - C1523.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
T. Szado, M. McLarnon, X. Wang, and C. van Breemen
Role of sarcoplasmic reticulum in regulation of tonic contraction of rabbit basilar artery
Am J Physiol Heart Circ Physiol, October 1, 2001; 281(4): H1481 - H1489.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
M. Lohn, B. Lauterbach, H. Haller, O. Pongs, F. C. Luft, and M. Gollasch
{beta}1-subunit of BK channels regulates arterial wall [Ca2+] and diameter in mouse cerebral arteries
J Appl Physiol, September 1, 2001; 91(3): 1350 - 1354.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
K. M. Sanders
Signal Transduction in Smooth Muscle: Invited Review: Mechanisms of calcium handling in smooth muscles
J Appl Physiol, September 1, 2001; 91(3): 1438 - 1449.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
G. C. Wellman, L. F. Santana, A. D. Bonev, and M. T. Nelson
Role of phospholamban in the modulation of arterial Ca2+ sparks and Ca2+-activated K+ channels by cAMP
Am J Physiol Cell Physiol, September 1, 2001; 281(3): C1029 - C1037.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
M. A. Hill, H. Zou, S. J. Potocnik, G. A. Meininger, and M. J. Davis
Signal Transduction in Smooth Muscle: Invited Review: Arteriolar smooth muscle mechanotransduction: Ca2+ signaling pathways underlying myogenic reactivity
J Appl Physiol, August 1, 2001; 91(2): 973 - 983.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
J. H. Jaggar
Intravascular pressure regulates local and global Ca2+ signaling in cerebral artery smooth muscle cells
Am J Physiol Cell Physiol, August 1, 2001; 281(2): C439 - C448.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
Y. Ohi, H. Yamamura, N. Nagano, S. Ohya, K. Muraki, M. Watanabe, and Y. Imaizumi
Local Ca2+ transients and distribution of BK channels and ryanodine receptors in smooth muscle cells of guinea-pig vas deferens and urinary bladder
J. Physiol., July 15, 2001; 534(2): 313 - 326.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
C. M. Pabelick, G. C. Sieck, and Y. S. Prakash
Signal Transduction in Smooth Muscle: Invited Review: Significance of spatial and temporal heterogeneity of calcium transients in smooth muscle
J Appl Physiol, July 1, 2001; 91(1): 488 - 496.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
J. Arima, N. Matsumoto, K. Kishimoto, and N. Akaike
Spontaneous miniature outward currents in mechanically dissociated rat Meynert neurons
J. Physiol., July 1, 2001; 534(1): 99 - 107.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
G. M. Herrera, T. J. Heppner, and M. T. Nelson
Voltage dependence of the coupling of Ca2+ sparks to BKCa channels in urinary bladder smooth muscle
Am J Physiol Cell Physiol, March 1, 2001; 280(3): C481 - C490.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
O. Bayguinov, B. Hagen, and K. M. Sanders
Muscarinic stimulation increases basal Ca2+ and inhibits spontaneous Ca2+ transients in murine colonic myocytes
Am J Physiol Cell Physiol, March 1, 2001; 280(3): C689 - C700.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
M. T Kirber, E. F Etter, K. A Bellve, L. M Lifshitz, R. A Tuft, F. S Fay, J. V Walsh Jr, and K. E Fogarty
Relationship of Ca2+ sparks to STOCs studied with 2D and 3D imaging in feline oesophageal smooth muscle cells
J. Physiol., March 1, 2001; 531(2): 315 - 327.
[Abstract] [Full Text] [PDF]

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 J. Neurophysiol.Home page
F. S. Scornik, L. A. Merriam, and R. L. Parsons
Number of KCa Channels Underlying Spontaneous Miniature Outward Currents (SMOCs) in Mudpuppy Cardiac Neurons
J Neurophysiol, January 1, 2001; 85(1): 54 - 60.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
R. Janiak, S. M. Wilson, S. Montague, and J. R. Hume
Heterogeneity of calcium stores and elementary release events in canine pulmonary arterial smooth muscle cells
Am J Physiol Cell Physiol, January 1, 2001; 280(1): C22 - C33.
[Abstract] [Full Text] [PDF]

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 JGPHome page
R. ZhuGe, K. E. Fogarty, R. A. Tuft, L. M. Lifshitz, K. Sayar, and J. V. Walsh Jr.
Dynamics of Signaling between Ca2+ Sparks and Ca2+- Activated K+ Channels Studied with a Novel Image-Based Method for Direct Intracellular Measurement of Ryanodine Receptor Ca2+ Current
J. Gen. Physiol., December 1, 2000; 116(6): 845 - 864.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
M. Lohn, M. Furstenau, V. Sagach, M. Elger, W. Schulze, F. C. Luft, H. Haller, and M. Gollasch
Ignition of Calcium Sparks in Arterial and Cardiac Muscle Through Caveolae
Circ. Res., November 24, 2000; 87(11): 1034 - 1039.
[Abstract] [Full Text] [PDF]

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 JGPHome page
T. Akita and K. Kuba
Functional Triads Consisting of Ryanodine Receptors, Ca2+ Channels, and Ca2+-Activated K+ Channels in Bullfrog Sympathetic Neurons: Plastic Modulation of Action Potential
J. Gen. Physiol., November 1, 2000; 116(5): 697 - 720.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
J. H. Jaggar and M. T. Nelson
Differential regulation of Ca2+ sparks and Ca2+ waves by UTP in rat cerebral artery smooth muscle cells
Am J Physiol Cell Physiol, November 1, 2000; 279(5): C1528 - C1539.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
V. A. Porter, H. L. Reeve, and D. N. Cornfield
Fetal rabbit pulmonary artery smooth muscle cell response to ryanodine is developmentally regulated
Am J Physiol Lung Cell Mol Physiol, October 1, 2000; 279(4): L751 - L757.
[Abstract] [Full Text] [PDF]

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 JGPHome page
D.H. Cox and R.W. Aldrich
Role of the {beta}1 Subunit in Large-Conductance Ca2+-Activated K+ Channel Gating Energetics: Mechanisms of Enhanced Ca2+ Sensitivity
J. Gen. Physiol., September 1, 2000; 116(3): 411 - 432.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
Y.-X. WANG, P. K. DHULIPALA, and M. I. KOTLIKOFF
Hypoxia inhibits the Na+/Ca2+ exchanger in pulmonary artery smooth muscle cells
FASEB J, September 1, 2000; 14(12): 1731 - 1740.
[Abstract] [Full Text]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
W. Long, L. Zhang, and L. D. Longo
Cerebral artery sarcoplasmic reticulum Ca2+ stores and contractility: changes with development
Am J Physiol Regulatory Integrative Comp Physiol, September 1, 2000; 279(3): R860 - R873.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
G. M. Herrera, T. J. Heppner, and M. T. Nelson
Regulation of urinary bladder smooth muscle contractions by ryanodine receptors and BK and SK channels
Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2000; 279(1): R60 - R68.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
O. Bayguinov, B. Hagen, A. D. Bonev, M. T. Nelson, and K. M. Sanders
Intracellular calcium events activated by ATP in murine colonic myocytes
Am J Physiol Cell Physiol, July 1, 2000; 279(1): C126 - C135.
[Abstract] [Full Text] [PDF]

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 JGPHome page
M.L. Collier, G. Ji, Y.-X. Wang, and M.I. Kotlikoff
Calcium-Induced Calcium Release in Smooth Muscle: Loose Coupling between the Action Potential and Calcium Release
J. Gen. Physiol., May 1, 2000; 115(5): 653 - 662.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
J. H. Jaggar, V. A. Porter, W. J. Lederer, and M. T. Nelson
Calcium sparks in smooth muscle
Am J Physiol Cell Physiol, February 1, 2000; 278(2): C235 - C256.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
I. D. Kong, S. D. Koh, and K. M. Sanders
Purinergic activation of spontaneous transient outward currents in guinea pig taenia colonic myocytes
Am J Physiol Cell Physiol, February 1, 2000; 278(2): C352 - C362.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Gastrointest. Liver Physiol.Home page
M. J. Pozo, G. J. Perez, M. T. Nelson, and G. M. Mawe
Ca2+ sparks and BK currents in gallbladder myocytes: role in CCK-induced response
Am J Physiol Gastrointest Liver Physiol, January 1, 2002; 282(1): G165 - G174.
[Abstract] [Full Text] [PDF]

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 JGPHome page
P. Mitra and M. M. Slaughter
Mechanism of Generation of Spontaneous Miniature Outward Currents (SMOCs) in Retinal Amacrine Cells
J. Gen. Physiol., April 1, 2002; 119(4): 355 - 372.
[Abstract] [Full Text] [PDF]

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 JGPHome page
P. Mitra and M. M. Slaughter
Calcium-induced Transitions between the Spontaneous Miniature Outward and the Transient Outward Currents in Retinal Amacrine Cells
J. Gen. Physiol., April 1, 2002; 119(4): 373 - 388.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
M. Lohn, W. Jessner, M. Furstenau, M. Wellner, V. Sorrentino, H. Haller, F. C. Luft, and M. Gollasch
Regulation of Calcium Sparks and Spontaneous Transient Outward Currents by RyR3 in Arterial Vascular Smooth Muscle Cells
Circ. Res., November 23, 2001; 89(11): 1051 - 1057.
[Abstract] [Full Text] [PDF]


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