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Physiol. Rev. 76: 1027-1071, 1996;
0031-9333/96 $15.00
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Physiological Reviews, Vol 76, 1027-1071, Copyright © 1996 by American Physiological Society

JOURNAL ARTICLE

Ryanodine receptor Ca2+ release channels: does diversity in form equal diversity in function?

J. L. Sutko and J. A. Airey
Department of Pharmacology, University of Nevada School of Medicine, Reno, USA.

Complexities in calcium signaling in eukaryotic cells require diversity in the proteins involved in generating these signals. In this review, we consider the ryanodine receptor (RyR) family of intracellular calcium release channels. This includes species, tissue, and cellular distributions of the RyRs and mechanisms of activation, deactivation, and inactivation of RyR calcium release events. In addition, as first observed in nonmammalian vertebrate skeletal muscles, it is now clear that more than one RyR isoform is frequently coexpressed within many cell types. How multiple ryanodine receptor release channels are used to generate intracellular calcium transients is unknown. Therefore, a primary focus of this review is why more than one RyR is required for this purpose, particularly in a tissue, such as vertebrate fast-twitch skeletal muscles, where a relatively simple and straightforward change in calcium would appear to be required to elicit contraction. Finally, the roles of the RyR isoforms and the calcium release events they mediate in the development of embryonic skeletal muscle are considered.


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M. R. Pelletier, J. S. Wadia, L. R. Mills, and P. L. Carlen
Seizure-Induced Cell Death Produced by Repeated Tetanic Stimulation In Vitro: Possible Role of Endoplasmic Reticulum Calcium Stores
J Neurophysiol, June 1, 1999; 81(6): 3054 - 3064.
[Abstract] [Full Text] [PDF]

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 Cardiovasc ResHome page
D. M Bers and E. Perez-Reyes
Ca channels in cardiac myocytes: structure and function in Ca influx and intracellular Ca release
Cardiovasc Res, May 1, 1999; 42(2): 339 - 360.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
D. Balshaw, L. Gao, and G. Meissner
Luminal loop of the ryanodine receptor: A pore-forming segment?
PNAS, March 30, 1999; 96(7): 3345 - 3347.
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 Am. J. Physiol. Cell Physiol.Home page
A. Yamada, S. Ohya, M. Hirano, M. Watanabe, M. P. Walsh, and Y. Imaizumi
Ca2+ sensitization of smooth muscle contractility induced by ruthenium red
Am J Physiol Cell Physiol, March 1, 1999; 276(3): C566 - C575.
[Abstract] [Full Text] [PDF]

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 JCBHome page
M. T. Alonso, M. J. Barrero, P. Michelena, E. Carnicero, I. Cuchillo, A. G. Garcia, J. Garcia-Sancho, M. Montero, and J. Alvarez
Ca2+-induced Ca2+ Release in Chromaffin Cells Seen from inside the ER with Targeted Aequorin
J. Cell Biol., January 25, 1999; 144(2): 241 - 254.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
E. M. Balog and E. M. Gallant
Modulation of the sarcolemmal L-type current by alteration in SR Ca2+ release
Am J Physiol Cell Physiol, January 1, 1999; 276(1): C128 - C135.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
B Dietze, F Bertocchini, V Barone, A Struk, V Sorrentino, and W Melzer
Voltage-controlled Ca2+ release in normal and ryanodine receptor type 3 (RyR3)-deficient mouse myotubes
J. Physiol., November 15, 1998; 513(1): 3 - 9.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
N. Shirokova, J. Garcia, and E. Rios
Local calcium release in mammalian skeletal muscle
J. Physiol., October 15, 1998; 512(2): 377 - 384.
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 Am. J. Physiol. Cell Physiol.Home page
J. P. C. Franck, J. Morrissette, J. E. Keen, R. L. Londraville, M. Beamsley, and B. A. Block
Cloning and characterization of fiber type-specific ryanodine receptor isoforms in skeletal muscles of fish
Am J Physiol Cell Physiol, August 1, 1998; 275(2): C401 - C415.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. R. Sharma, P. Penczek, R. Grassucci, H.-B. Xin, S. Fleischer, and T. Wagenknecht
Cryoelectron Microscopy and Image Analysis of the Cardiac Ryanodine Receptor
J. Biol. Chem., July 17, 1998; 273(29): 18429 - 18434.
[Abstract] [Full Text] [PDF]

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 JGPHome page
B. Tanna, W. Welch, L. Ruest, J. L. Sutko, and A. J. Williams
Interactions of a Reversible Ryanoid (21-Amino-9{alpha}-Hydroxy-Ryanodine) with Single Sheep Cardiac Ryanodine Receptor Channels
J. Gen. Physiol., July 1, 1998; 112(1): 55 - 69.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
L. H. Jeyakumar, J. A. Copello, A. M. O'Malley, G.-M. Wu, R. Grassucci, T. Wagenknecht, and S. Fleischer
Purification and Characterization of Ryanodine Receptor 3 from Mammalian Tissue
J. Biol. Chem., June 26, 1998; 273(26): 16011 - 16020.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. R. W. Chen, K. Ebisawa, X. Li, and L. Zhang
Molecular Identification of the Ryanodine Receptor Ca2+ Sensor
J. Biol. Chem., June 12, 1998; 273(24): 14675 - 14678.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
A. P. Somlyo
How many messengers to send calcium? Focus on "IP3 receptor blockade fails to prevent intracellular Ca2+ release by ET-1 and alpha -thrombin"
Am J Physiol Cell Physiol, June 1, 1998; 274(6): C1453 - C1455.
[Full Text] [PDF]

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 JGPHome page
A. Tripathy, W. Resch, Le Xu, H. H. Valdivia, and G. Meissner
Imperatoxin A Induces Subconductance States in Ca2+ Release Channels (Ryanodine Receptors) of Cardiac and Skeletal Muscle
J. Gen. Physiol., May 1, 1998; 111(5): 679 - 690.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
H. Tanaka, T. Sekine, T. Kawanishi, R. Nakamura, and K. Shigenobu
Intrasarcomere [Ca2+] gradients and their spatio-temporal relation to Ca2+ sparks in rat cardiomyocytes
J. Physiol., April 1, 1998; 508(1): 145 - 152.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
F. Pfeiffer, L. Sternfeld, A. Schmid, and I. Schulz
Control of Ca2+ wave propagation in mouse pancreatic acinar cells
Am J Physiol Cell Physiol, March 1, 1998; 274(3): C663 - C672.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
R. E. Lesh, G. F. Nixon, S. Fleischer, J. A. Airey, A. P. Somlyo, and A. V. Somlyo
Localization of Ryanodine Receptors in Smooth Muscle
Circ. Res., February 9, 1998; 82(2): 175 - 185.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
E. Maryon, B Saari, and P Anderson
Muscle-specific functions of ryanodine receptor channels in Caenorhabditis elegans
J. Cell Sci., January 10, 1998; 111(19): 2885 - 2895.
[Abstract] [PDF]

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 J. Biol. Chem.Home page
T. Wagenknecht, M. Radermacher, R. Grassucci, J. Berkowitz, H.-B. Xin, and S. Fleischer
Locations of Calmodulin and FK506-binding Protein on the Three-dimensional Architecture of the Skeletal Muscle Ryanodine Receptor
J. Biol. Chem., December 19, 1997; 272(51): 32463 - 32471.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
A.-S. Jobert, C. Leroy, D. Butlen, and C. Silve
Parathyroid Hormone-Induced Calcium Release from Intracellular Stores in a Human Kidney Cell Line in the Absence of Stimulation of Cyclic Adenosine 3',5'-Monophosphate Production
Endocrinology, December 1, 1997; 138(12): 5282 - 5292.
[Abstract] [Full Text] [PDF]

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 JGPHome page
M. B. Bhat, J. Zhao, W. Zang, C. W. Balke, H. Takeshima, W. G. Wier, and J. Ma
Caffeine-induced Release of Intracellular Ca2+ from Chinese Hamster Ovary Cells Expressing Skeletal Muscle Ryanodine Receptor: Effects on Full-Length and Carboxyl-Terminal Portion of Ca2+Release Channels
J. Gen. Physiol., December 1, 1997; 110(6): 749 - 762.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
T. Oba
Niflumic acid differentially modulates two types of skeletal ryanodine-sensitive Ca2+-release channels
Am J Physiol Cell Physiol, November 1, 1997; 273(5): C1588 - C1595.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
B. R. Fruen, J. R. Mickelson, and C. F. Louis
Dantrolene Inhibition of Sarcoplasmic Reticulum Ca2+ Release by Direct and Specific Action at Skeletal Muscle Ryanodine Receptors
J. Biol. Chem., October 24, 1997; 272(43): 26965 - 26971.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. J. Lokuta, M. B. Meyers, P. R. Sander, G. I. Fishman, and H. H. Valdivia
Modulation of Cardiac Ryanodine Receptors by Sorcin
J. Biol. Chem., October 3, 1997; 272(40): 25333 - 25338.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
Y. M. Usachev and S. A. Thayer
All-or-None Ca2+ Release from Intracellular Stores Triggered by Ca2+ Influx through Voltage-Gated Ca2+ Channels in Rat Sensory Neurons
J. Neurosci., October 1, 1997; 17(19): 7404 - 7414.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. R. W. Chen, X. Li, K. Ebisawa, and L. Zhang
Functional Characterization of the Recombinant Type 3 Ca2+ Release Channel (Ryanodine Receptor) Expressed in HEK293 Cells
J. Biol. Chem., September 26, 1997; 272(39): 24234 - 24246.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
T. Murayama and Y. Ogawa
Characterization of Type 3 Ryanodine Receptor (RyR3) of Sarcoplasmic Reticulum from Rabbit Skeletal Muscles
J. Biol. Chem., September 19, 1997; 272(38): 24030 - 24037.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
P. Tarroni, D. Rossi, A. Conti, and V. Sorrentino
Expression of the Ryanodine Receptor Type 3 Calcium Release Channel during Development and Differentiation of Mammalian Skeletal Muscle Cells
J. Biol. Chem., August 8, 1997; 272(32): 19808 - 19813.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
T. Yamazawa, H. Takeshima, M. Shimuta, and M. Iino
A Region of the Ryanodine Receptor Critical for Excitation-Contraction Coupling in Skeletal Muscle
J. Biol. Chem., March 28, 1997; 272(13): 8161 - 8164.
[Abstract] [Full Text] [PDF]

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 Pharmacol. Rev.Home page
R. Zucchi and S. Ronca-Testoni
The Sarcoplasmic Reticulum Ca2+ Channel/Ryanodine Receptor: Modulation by Endogenous Effectors, Drugs and Disease States
Pharmacol. Rev., March 1, 1997; 49(1): 1 - 52.
[Abstract] [Full Text] [PDF]

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 Pharmacol. Rev.Home page
J. L. Sutko, J. A. Airey, W. Welch, and L. Ruest
The Pharmacology of Ryanodine and Related Compounds
Pharmacol. Rev., March 1, 1997; 49(1): 53 - 98.
[Abstract] [Full Text] [PDF]


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