Role of Ryanodine Receptors in the Assembly of Calcium Release Units in Skeletal Muscle

doi:10.1083/jcb.140.4.831

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J. Cell Biol., Volume 140, Number 4, February 23, 1998 831-842

Role of Ryanodine Receptors in the Assembly of Calcium Release Units in Skeletal Muscle

Feliciano Protasi,^*^§ Clara Franzini-Armstrong,^* and Paul D. Allen^§

^* Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6058; Department of Cardiology, Laboratory of Molecular Cardiology, Children's Hospital, Boston, Massachusetts 02115; and ^§ Department of Anesthesiology, Brigham and Women's Hospital, Boston, Massachusetts 02115

Abstract. In muscle cells, excitation-contraction (e-c) coupling is mediated by "calcium release units," junctions betweenthe sarcoplasmic reticulum (SR) and exterior membranes. Two proteins,which face each other, are known to functionally interact in thosestructures: the ryanodine receptors (RyRs), or SR calcium releasechannels, and the dihydropyridine receptors (DHPRs), or L-typecalcium channels of exterior membranes. In skeletal muscle, DHPRsform tetrads, groups of four receptors, and tetrads are organizedin arrays that face arrays of feet (or RyRs). Triadin is a proteinof the SR located at the SR-exterior membrane junctions, whoserole is not known. We have structurally characterized calciumrelease units in a skeletal muscle cell line (1B5) lacking Ry₁R.Using immunohistochemistry and freeze-fracture electron microscopy,we find that DHPR and triadin are clustered in foci in differentiating1B5 cells. Thin section electron microscopy reveals numerous SR-exteriormembrane junctions lacking foot structures (dyspedic). These resultssuggest that components other than Ry₁Rs are responsible for targetingDHPRs and triadin to junctional regions. However, DHPRs in 1B5cells are not grouped into tetrads as in normal skeletal musclecells suggesting that anchoring to Ry₁Rs is necessary for positioningDHPRs into ordered arrays of tetrads. This hypothesis is confirmedby finding a "restoration of tetrads" in junctional domains ofsurface membranes after transfection of 1B5 cells with cDNA encodingfor Ry₁R.

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