Chicken skeletal muscle ryanodine receptor isoforms: ion channel properties

• Published in: Biophysical journal Vol. 67; no. 5; pp. 1834 - 1850
• Main Authors: Percival, A.L., Williams, A.J., Kenyon, J.L., Grinsell, M.M., Airey, J.A., Sutko, J.L.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01-11-1994
• Subjects: Adenosine Triphosphate - pharmacology; Animals; Biophysical Phenomena; Biophysics; Calcium - pharmacology; Calcium Channels - drug effects; Calcium Channels - metabolism; Chickens; Electric Conductivity; In Vitro Techniques; Ion Channel Gating; Ion Channels - drug effects; Ion Channels - metabolism; Lipid Bilayers; Membrane Potentials; Microsomes - metabolism; Muscle Contraction - physiology; Muscle Proteins - drug effects; Muscle Proteins - metabolism; Muscle, Skeletal - metabolism; Ryanodine Receptor Calcium Release Channel
• ISSN: 0006-3495; 1542-0086
• DOI: 10.1016/S0006-3495(94)80665-4

To define the roles of the alpha- and beta-ryanodine receptor (RyR) (sarcoplasmic reticulum Ca2+ release channel) isoforms expressed in chicken skeletal muscles, we investigated the ion channel properties of these proteins in lipid bilayers. alpha- and beta RyRs embody Ca2+ channels with similar conductances (792, 453, and 118 pS for K+, Cs+ and Ca2+) and selectivities (PCa2+/PK+ = 7.4), but the two channels have different gating properties. alpha RyR channels switch between two gating modes, which differ in the extent they are activated by Ca2+ and ATP, and inactivated by Ca2+. Either mode can be assumed in a spontaneous and stable manner. In a low activity mode, alpha RyR channels exhibit brief openings (tau o = 0.14 ms) and are minimally activated by Ca2+ in the absence of ATP. In a high activity mode, openings are longer (tau o1–3 = 0.17, 0.51, and 1.27 ms), and the channels are activated by Ca2+ in the absence of ATP and are in general less sensitive to the inactivating effects of Ca2+. beta RyR channel openings are longer (tau 01–3 = 0.34, 1.56, and 3.31 ms) than those of alpha RyR channels in either mode. beta RyR channels are activated to a greater relative extent by Ca2+ than ATP and are inactivated by millimolar Ca2+ in the absence, but not the presence, of ATP. Both alpha- and beta RyR channels are activated by caffeine, inhibited by Mg2+ and ruthenium red, inactivated by voltage (cytoplasmic side positive), and modified to a long-lived substate by ryanodine, but only alpha RyR channels are activated by perchlorate anions. The differences in gating and responses to channel modifiers may give the alpha- and beta RyRs distinct roles in muscle activation.