Circulation Research. 2001
Published online before print May 24, 2001, doi: 10.1161/hh1101.091268
Published online before print May 24, 2001, doi: 10.1161/hh1101.091268
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
© 2001 American Heart Association, Inc.
Article |
Coupled Gating Between Cardiac Calcium Release Channels (Ryanodine Receptors)
From the Center for Molecular Cardiology, Department of Medicine, and Department of Pharmacology, Columbia University College of Physicians and Surgeons, New York, NY, and the Institute of Molecular Physiology and Genetics (K.O.), Slovak Academy of Sciences, Bratislava, Slovak Republic.
Correspondence to Andrew R. Marks, MD, Center for Molecular Cardiology, Box 65, Columbia University College of Physicians and Surgeons, Room 9-401, 630 W 168th St, New York, NY 10032. E-mail arm42{at}columbia.edu
Abstract
Abstract— Excitation-contraction coupling in heart muscle requires the activation of Ca2+-release channels/type 2 ryanodine receptors (RyR2s) by Ca2+ influx. RyR2s are arranged on the sarcoplasmic reticular membrane in closely packed arrays such that their large cytoplasmic domains contact one another. We now show that multiple RyR2s can be isolated under conditions such that they remain physically coupled to one another. When these coupled channels are examined in planar lipid bilayers, multiple channels exhibit simultaneous gating, termed "coupled gating." Removal of the regulatory subunit, the FK506 binding protein (FKBP12.6), functionally but not physically uncouples multiple RyR2 channels. Coupled gating between RyR2 channels may be an important regulatory mechanism in excitation-contraction coupling as well as in other signaling pathways involving intracellular Ca2+ release.
Key Words: ryanodine receptors • Ca2+ channels • coupled gating • FKBP12.6 • excitation-contraction coupling
This article has been cited by other articles:
 |
|
 |
|
  W. Chen, J. A. Wasserstrom, and Y. Shiferaw Role of coupled gating between cardiac ryanodine receptors in the genesis of triggered arrhythmias Am J Physiol Heart Circ Physiol, July 1, 2009; 297(1): H171 - H180. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Hayashi, M. E. Martone, Z. Yu, A. Thor, M. Doi, M. J. Holst, M. H. Ellisman, and M. Hoshijima Three-dimensional electron microscopy reveals new details of membrane systems for Ca2+ signaling in the heart J. Cell Sci., April 1, 2009; 122(7): 1005 - 1013. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Cheng and W. J. Lederer Calcium Sparks Physiol Rev, October 1, 2008; 88(4): 1491 - 1545. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Bao, L. M. Lifshitz, R. A. Tuft, K. Bellve, K. E. Fogarty, and R. ZhuGe A Close Association of RyRs with Highly Dense Clusters of Ca2+-activated Cl- Channels Underlies the Activation of STICs by Ca2+ Sparks in Mouse Airway Smooth Muscle J. Gen. Physiol., July 1, 2008; 132(1): 145 - 160. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Seidler, C. M. Loughrey, D. Zibrova, S. Kettlewell, N. Teucher, H. Kogler, G. Hasenfuss, and G. L. Smith Overexpression of FK-506 Binding Protein 12.0 Modulates Excitation Contraction Coupling in Adult Rabbit Ventricular Cardiomyocytes Circ. Res., November 9, 2007; 101(10): 1020 - 1029. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Seidler, G. Hasenfuss, and L. S. Maier Targeting Altered Calcium Physiology in the Heart: Translational Approaches to Excitation, Contraction, and Transcription Physiology, October 1, 2007; 22(5): 328 - 334. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y.-a. Zhang, R. A. Tuft, L. M. Lifshitz, K. E. Fogarty, J. J. Singer, and H. Zou Caffeine-activated large-conductance plasma membrane cation channels in cardiac myocytes: characteristics and significance Am J Physiol Heart Circ Physiol, October 1, 2007; 293(4): H2448 - H2461. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 V. Lukyanenko, A. Ziman, A. Lukyanenko, V. Salnikov, and W. J. Lederer Functional groups of ryanodine receptors in rat ventricular cells J. Physiol., August 15, 2007; 583(1): 251 - 269. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Hotta, K. Morimura, S. Ohya, K. Muraki, H. Takeshima, and Y. Imaizumi Ryanodine receptor type 2 deficiency changes excitation-contraction coupling and membrane potential in urinary bladder smooth muscle J. Physiol., July 15, 2007; 582(2): 489 - 506. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. A. Copello, A. V. Zima, P. L. Diaz-Sylvester, M. Fill, and L. A. Blatter Ca2+ entry-independent effects of L-type Ca2+ channel modulators on Ca2+ sparks in ventricular myocytes Am J Physiol Cell Physiol, June 1, 2007; 292(6): C2129 - C2140. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. P. Katra, T. Oya, G. S. Hoeker, and K. R. Laurita Ryanodine receptor dysfunction and triggered activity in the heart Am J Physiol Heart Circ Physiol, May 1, 2007; 292(5): H2144 - H2151. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Zissimopoulos, N. Docrat, and F. A. Lai Redox Sensitivity of the Ryanodine Receptor Interaction with FK506-binding Protein J. Biol. Chem., March 9, 2007; 282(10): 6976 - 6983. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. A. Armoundas, J. Rose, R. Aggarwal, B. D. Stuyvers, B. O'Rourke, D. A. Kass, E. Marban, S. R. Shorofsky, G. F. Tomaselli, and C. William Balke Cellular and molecular determinants of altered Ca2+ handling in the failing rabbit heart: primary defects in SR Ca2+ uptake and release mechanisms Am J Physiol Heart Circ Physiol, March 1, 2007; 292(3): H1607 - H1618. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. Iyer, R. J. Hajjar, and A. A. Armoundas Mechanisms of Abnormal Calcium Homeostasis in Mutations Responsible for Catecholaminergic Polymorphic Ventricular Tachycardia Circ. Res., February 2, 2007; 100(2): e22 - e31. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Lucats, L. Vinet, A. Bize, X. Monnet, D. Morin, J. B. Su, P. Rouet-Benzineb, O. Cazorla, J.-J. Mercadier, L. Hittinger, et al. The inotropic adaptation during late preconditioning against myocardial stunning is associated with an increase in FKBP12.6 Cardiovasc Res, February 1, 2007; 73(3): 560 - 567. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. E. Louch, H. K. Mork, J. Sexton, T. A. Stromme, P. Laake, I. Sjaastad, and O. M. Sejersted T-tubule disorganization and reduced synchrony of Ca2+ release in murine cardiomyocytes following myocardial infarction J. Physiol., July 15, 2006; 574(2): 519 - 533. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. L. Molina, F. N. Barrera, A. M. Fernandez, J. A. Poveda, M. L. Renart, J. A. Encinar, G. Riquelme, and J. M. Gonzalez-Ros Clustering and Coupled Gating Modulate the Activity in KcsA, a Potassium Channel Model J. Biol. Chem., July 7, 2006; 281(27): 18837 - 18848. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Carter, J. Colyer, and R. Sitsapesan Maximum Phosphorylation of the Cardiac Ryanodine Receptor at Serine-2809 by Protein Kinase A Produces Unique Modifications to Channel Gating and Conductance Not Observed at Lower Levels of Phosphorylation Circ. Res., June 23, 2006; 98(12): 1506 - 1513. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Ji, M. Feldman, R. Doran, W. Zipfel, and M. I. Kotlikoff Ca2+-Induced Ca2+ Release through Localized Ca2+ Uncaging in Smooth Muscle J. Gen. Physiol., February 27, 2006; 127(3): 225 - 235. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 W. Creighton, R. Virmani, R. Kutys, and A. Burke Identification of Novel Missense Mutations of Cardiac Ryanodine Receptor Gene in Exercise-Induced Sudden Death at Autopsy J. Mol. Diagn., February 1, 2006; 8(1): 62 - 67. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. A. Goonasekera, S. R. W. Chen, and R. T. Dirksen Reconstitution of local Ca2+ signaling between cardiac L-type Ca2+ channels and ryanodine receptors: insights into regulation by FKBP12.6 Am J Physiol Cell Physiol, December 1, 2005; 289(6): C1476 - C1484. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. Yaras, M. Ugur, S. Ozdemir, H. Gurdal, N. Purali, A. Lacampagne, G. Vassort, and B. Turan Effects of Diabetes on Ryanodine Receptor Ca Release Channel (RyR2) and Ca2+ Homeostasis in Rat Heart Diabetes, November 1, 2005; 54(11): 3082 - 3088. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-L. Jones, D. F. Reynolds, F. A. Lai, and L. M. Blayney Ryanodine receptor binding to FKBP12 is modulated by channel activation state J. Cell Sci., October 15, 2005; 118(20): 4613 - 4619. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Balasubramaniam, S. Chawla, A. A. Grace, and C. L.-H. Huang Caffeine-induced arrhythmias in murine hearts parallel changes in cellular Ca2+ homeostasis Am J Physiol Heart Circ Physiol, October 1, 2005; 289(4): H1584 - H1593. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Lindegger and E. Niggli Paradoxical SR Ca2+ release in guinea-pig cardiac myocytes after {beta}-adrenergic stimulation revealed by two-photon photolysis of caged Ca2+ J. Physiol., June 15, 2005; 565(3): 801 - 813. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Zissimopoulos and F. A. Lai Interaction of FKBP12.6 with the Cardiac Ryanodine Receptor C-terminal Domain J. Biol. Chem., February 18, 2005; 280(7): 5475 - 5485. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Z. Yang and D. S. Steele Characteristics of Prolonged Ca2+ Release Events Associated With the Nuclei in Adult Cardiac Myocytes Circ. Res., January 7, 2005; 96(1): 82 - 90. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Laporte, A. Hui, and I. Laher Pharmacological Modulation of Sarcoplasmic Reticulum Function in Smooth Muscle Pharmacol. Rev., December 1, 2004; 56(4): 439 - 513. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. D. Belke, E. A. Swanson, and W. H. Dillmann Decreased Sarcoplasmic Reticulum Activity and Contractility in Diabetic db/db Mouse Heart Diabetes, December 1, 2004; 53(12): 3201 - 3208. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. R. Laver, E. R. O'Neill, and G. D. Lamb Luminal Ca2+-regulated Mg2+ Inhibition of Skeletal RyRs Reconstituted as Isolated Channels or Coupled Clusters J. Gen. Physiol., November 29, 2004; 124(6): 741 - 758. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. M. Gomez, I. Schuster, J. Fauconnier, J. Prestle, G. Hasenfuss, and S. Richard FKBP12.6 overexpression decreases Ca2+ spark amplitude but enhances [Ca2+]i transient in rat cardiac myocytes Am J Physiol Heart Circ Physiol, November 1, 2004; 287(5): H1987 - H1993. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
U. Kirchhefer, H. A. Baba, G. Hanske, L. R. Jones, P. Kirchhof, W. Schmitz, and J. Neumann Age-dependent biochemical and contractile properties in atrium of transgenic mice overexpressing junctin Am J Physiol Heart Circ Physiol, November 1, 2004; 287(5): H2216 - H2225. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. M. Loughrey, T. Seidler, S. L. W. Miller, J. Prestle, K. E. MacEachern, D. F. Reynolds, G. Hasenfuss, and G. L. Smith Over-expression of FK506-binding protein FKBP12.6 alters excitation-contraction coupling in adult rabbit cardiomyocytes J. Physiol., May 1, 2004; 556(3): 919 - 934. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S.-Q. Wang, C. Wei, G. Zhao, D. X.P. Brochet, J. Shen, L.-S. Song, W. Wang, D. Yang, and H. Cheng Imaging Microdomain Ca2+ in Muscle Cells Circ. Res., April 30, 2004; 94(8): 1011 - 1022. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. S. Ginsburg and D. M. Bers Modulation of excitation-contraction coupling by isoproterenol in cardiomyocytes with controlled SR Ca2+ load and Ca2+ current trigger J. Physiol., April 15, 2004; 556(2): 463 - 480. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. M. Blayney, S. Zissimopoulos, E. Ralph, E. Abbot, L. Matthews, and F. A. Lai Ryanodine Receptor Oligomeric Interaction: IDENTIFICATION OF A PUTATIVE BINDING REGION J. Biol. Chem., April 9, 2004; 279(15): 14639 - 14648. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. M. Gallant, J. Hart, K. Eager, S. Curtis, and A. F. Dulhunty Caffeine sensitivity of native RyR channels from normal and malignant hyperthermic pigs: effects of a DHPR II-III loop peptide Am J Physiol Cell Physiol, April 1, 2004; 286(4): C821 - C830. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
U. Kirchhefer, L. R Jones, F. Begrow, P. Boknik, L. Hein, M. J Lohse, B. Riemann, W. Schmitz, J. Stypmann, and J. Neumann Transgenic triadin 1 overexpression alters SR Ca2+ handling and leads to a blunted contractile response to {beta}-adrenergic agonists Cardiovasc Res, April 1, 2004; 62(1): 122 - 134. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Ji, M. E. Feldman, K. S. Greene, V. Sorrentino, H.-B. Xin, and M. I. Kotlikoff RYR2 Proteins Contribute to the Formation of Ca2+ Sparks in Smooth Muscle J. Gen. Physiol., March 29, 2004; 123(4): 377 - 386. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Q. Wang, M. D. Stern, E. Rios, and H. Cheng The quantal nature of Ca2+ sparks and in situ operation of the ryanodine receptor array in cardiac cells PNAS, March 16, 2004; 101(11): 3979 - 3984. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Van Acker, G. Bultynck, D. Rossi, V. Sorrentino, N. Boens, L. Missiaen, H. De Smedt, J. B. Parys, and G. Callewaert The 12 kDa FK506-binding protein, FKBP12, modulates the Ca2+-flux properties of the type-3 ryanodine receptor J. Cell Sci., March 1, 2004; 117(7): 1129 - 1137. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Stange, L. Xu, D. Balshaw, N. Yamaguchi, and G. Meissner Characterization of Recombinant Skeletal Muscle (Ser-2843) and Cardiac Muscle (Ser-2809) Ryanodine Receptor Phosphorylation Mutants J. Biol. Chem., December 19, 2003; 278(51): 51693 - 51702. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Rodriguez, M. S. Bhogal, and J. Colyer Stoichiometric Phosphorylation of Cardiac Ryanodine Receptor on Serine 2809 by Calmodulin-dependent Kinase II and Protein Kinase A J. Biol. Chem., October 3, 2003; 278(40): 38593 - 38600. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. R. Shannon, T. Guo, and D. M. Bers Ca2+ Scraps: Local Depletions of Free [Ca2+] in Cardiac Sarcoplasmic Reticulum During Contractions Leave Substantial Ca2+ Reserve Circ. Res., July 11, 2003; 93(1): 40 - 45. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Bull, J. J. Marengo, J. P. Finkelstein, M. I. Behrens, and O. Alvarez SH oxidation coordinates subunits of rat brain ryanodine receptor channels activated by calcium and ATP Am J Physiol Cell Physiol, July 1, 2003; 285(1): C119 - C128. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Reiken, X. H.T. Wehrens, J. A. Vest, A. Barbone, S. Klotz, D. Mancini, D. Burkhoff, and A. R. Marks {beta}-Blockers Restore Calcium Release Channel Function and Improve Cardiac Muscle Performance in Human Heart Failure Circulation, May 20, 2003; 107(19): 2459 - 2466. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M Scoote, P A Poole-Wilson, and A J Williams The therapeutic potential of new insights into myocardial excitation-contraction coupling Heart, April 1, 2003; 89(4): 371 - 376. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Hasenfuss and T. Seidler Treatment of Heart Failure Through Stabilization of the Cardiac Ryanodine Receptor Circulation, January 28, 2003; 107(3): 378 - 380. [Full Text] [PDF]
|
|
|
|
|
|
M. Yano, S. Kobayashi, M. Kohno, M. Doi, T. Tokuhisa, S. Okuda, M. Suetsugu, T. Hisaoka, M. Obayashi, T. Ohkusa, et al. FKBP12.6-Mediated Stabilization of Calcium-Release Channel (Ryanodine Receptor) as a Novel Therapeutic Strategy Against Heart Failure Circulation, January 28, 2003; 107(3): 477 - 484. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Reiken, M. Gaburjakova, S. Guatimosim, A. M. Gomez, J. D'Armiento, D. Burkhoff, J. Wang, G. Vassort, W. J. Lederer, and A. R. Marks Protein Kinase A Phosphorylation of the Cardiac Calcium Release Channel (Ryanodine Receptor) in Normal and Failing Hearts. ROLE OF PHOSPHATASES AND RESPONSE TO ISOPROTERENOL J. Biol. Chem., January 3, 2003; 278(1): 444 - 453. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Scoote and A. J Williams The cardiac ryanodine receptor (calcium release channel): Emerging role in heart failure and arrhythmia pathogenesis Cardiovasc Res, December 1, 2002; 56(3): 359 - 372. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D.A. Eisner and A.W. Trafford Heart Failure and the Ryanodine Receptor: Does Occam's Razor Rule? Circ. Res., November 29, 2002; 91(11): 979 - 981. [Full Text] [PDF]
|
|
|
|
|
|
M.E. Diaz, D.A. Eisner, and S.C. O'Neill Depressed Ryanodine Receptor Activity Increases Variability and Duration of the Systolic Ca2+ Transient in Rat Ventricular Myocytes Circ. Res., October 4, 2002; 91(7): 585 - 593. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Terentyev, S. Viatchenko-Karpinski, H. H. Valdivia, A. L. Escobar, and S. Gyorke Luminal Ca2+ Controls Termination and Refractory Behavior of Ca2+-Induced Ca2+ Release in Cardiac Myocytes Circ. Res., September 6, 2002; 91(5): 414 - 420. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Lipp, M. Egger, and E. Niggli Spatial characteristics of sarcoplasmic reticulum Ca2+ release events triggered by L-type Ca2+ current and Na+ current in guinea-pig cardiac myocytes J. Physiol., July 15, 2002; 542(2): 383 - 393. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Ji, R. J. Barsotti, M. E. Feldman, and M. I. Kotlikoff Stretch-induced Calcium Release in Smooth Muscle J. Gen. Physiol., June 1, 2002; 119(6): 533 - 543. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Doi, M. Yano, S. Kobayashi, M. Kohno, T. Tokuhisa, S. Okuda, M. Suetsugu, Y. Hisamatsu, T. Ohkusa, M. Kohno, et al. Propranolol Prevents the Development of Heart Failure by Restoring FKBP12.6-Mediated Stabilization of Ryanodine Receptor Circulation, March 19, 2002; 105(11): 1374 - 1379. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. R. Marks, S. Reiken, and S. O. Marx Progression of Heart Failure: Is Protein Kinase A Hyperphosphorylation of the Ryanodine Receptor a Contributing Factor? Circulation, January 22, 2002; 105(3): 272 - 275. [Full Text] [PDF]
|
|
|
|
 |
|
 X.H.T. WEHRENS and A.R. MARKS Myocardial Disease in Failing Hearts: Defective Excitation-Contraction Coupling Cold Spring Harb Symp Quant Biol, January 1, 2002; 67(0): 533 - 542. [Abstract] [PDF]
|
|
|
|
|
|
G. Bultynck, D. Rossi, G. Callewaert, L. Missiaen, V. Sorrentino, J. B. Parys, and H. De Smedt The Conserved Sites for the FK506-binding Proteins in Ryanodine Receptors and Inositol 1,4,5-Trisphosphate Receptors Are Structurally and Functionally Different J. Biol. Chem., December 7, 2001; 276(50): 47715 - 47724. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Reiken, M. Gaburjakova, J. Gaburjakova, K.-l. He, A. Prieto, E. Becker, G.-h. Yi, J. Wang, D. Burkhoff, and A. R. Marks {beta}-Adrenergic Receptor Blockers Restore Cardiac Calcium Release Channel (Ryanodine Receptor) Structure and Function in Heart Failure Circulation, December 4, 2001; 104(23): 2843 - 2848. [Abstract] [Full Text] [PDF]
|
|