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A Possible Role for Allosteric Interactions between Ryanodine Receptors
Division of Pulmonary and Critical Care Medicine, Johns Hopkins Medical Institutes, Baltimore, Maryland 21224; and Molecular Biophysics and Physiology, Rush University School of Medicine, Chicago, Illinois 60612
In cardiac muscle, release of activator calcium from the sarcoplasmic reticulum occurs by calcium- induced calcium release through ryanodine receptors (RyRs), which are clustered in a dense, regular, two-dimensional lattice array at the diad junction. We simulated numerically the stochastic dynamics of RyRs and L-type sarcolemmal calcium channels interacting via calcium nano-domains in the junctional cleft. Four putative RyR gating schemes based on single-channel measurements in lipid bilayers all failed to give stable excitation–contraction coupling, due either to insufficiently strong inactivation to terminate locally regenerative calcium-induced calcium release or insufficient cooperativity to discriminate against RyR activation by background calcium. If the ryanodine receptor was represented, instead, by a phenomenological four-state gating scheme, with channel opening resulting from simultaneous binding of two Ca2+ ions, and either calcium-dependent or activation-linked inactivation, the simulations gave a good semiquantitative accounting for the macroscopic features of excitation–contraction coupling. It was possible to restore stability to a model based on a bilayer-derived gating scheme, by introducing allosteric interactions between nearest-neighbor RyRs so as to stabilize the inactivated state and produce cooperativity among calcium binding sites on different RyRs. Such allosteric coupling between RyRs may be a function of the foot process and lattice array, explaining their conservation during evolution.
Key Words: sarcoplasmic reticulum • Monte Carlo • calcium-induced calcium release • dihydropyridine receptor • diad junction
Abbreviations: CICR, calcium-induced calcium release; DHPR, dihydropyridine receptor; EC, excitation–contraction; RyR, ryanodine receptor; SR, sarcoplasmic reticulum
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