Abstract
Peripheral couplings are junctions between the sarcoplasmic reticulum
(SR) and the surface membrane (SM). Feet occupy the SR/SM junctional
gap and are identified as the SR calcium release channels, or ryanodine
receptors (RyRs). In cardiac muscle, the activation of RyRs during
excitation-contraction (e-c) coupling is initiated by surface membrane
depolarization, followed by the opening of surface membrane calcium
channels, the dihydropyridine receptors (DHPRs). We have studied
the disposition of DHPRs and RyRs, and the structure of peripheral
couplings in chick myocardium, a muscle that has no transverse tubules.
Immunolabeling shows colocalization of RyRs and DHPRs in clusters
at the fiber's periphery. The positions of DHPR and RyR clusters
change coincidentally during development. Freeze-fracture of the
surface membrane reveals the presence of domains (junctional domains)
occupied by clusters of large particles. Junctional domains in the
surface membrane and arrays of feet in the junctional gap have similar
sizes and corresponding positions during development, suggesting
that both are components of peripheral couplings. As opposed to skeletal
muscle, membrane particles in junctional domains of cardiac muscle
do not form tetrads. Thus, despite their proximity to the feet, they
do not appear to be specifically associated with them. Two observations
establish the identify of the structurally identified feet arrays/junctional
domain complexes with the immunocytochemically defined RyRs/DHPRs
coclusters: the concomitant changes during development and the identification
of feet as the cytoplasmic domains of RyRs. We suggest that the large
particles in junctional domains of the surface membrane represent
DHPRs. These observations have two important functional consequences.
First, the apposition of DHPRs and RyRs indicates that most of the
inward calcium current flows into the restricted space where feet
are located. Secondly, contrary to skeletal muscle, presumptive DHPRs
do not show a specific association with the feet, which is consistent
with a less direct role of charge movement in cardiac than in skeletal
e-c coupling.
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