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Biophys J, November 2000, p. 2494-2508, Vol. 79, No. 5
*Department of Anesthesia Research, Brigham and Women's Hospital,
Boston, Massachusetts 02115 USA; Department of Cell and
Developmental Biology, University of Pennsylvania, Philadelphia,
Pennsylvania 19104 USA; Department of Biochemistry and
Molecular Biology, University of Calgary, Calgary, Alberta, Canada; and
§Department of Biochemistry and Biophysics, University of
North Carolina, Chapel Hill, North Carolina 27599 USA
Calcium release units (CRUs) are junctions between the
sarcoplasmic reticulum (SR) and exterior membranes that mediates
excitation contraction (e-c) coupling in muscle cells. In skeletal
muscle CRUs contain two isoforms of the sarcoplasmic reticulum
Ca2+release channel: ryanodine receptors type 1 and type 3 (RyR1 and RyR3). 1B5s are a mouse skeletal muscle cell line that
carries a null mutation for RyR1 and does not express either RyR1 or
RyR3. These cells develop dyspedic SR/exterior membrane junctions
(i.e., dyspedic calcium release units, dCRUs) that contain
dihydropyridine receptors (DHPRs) and triadin, two essential components
of CRUs, but no RyRs (or feet). Lack of RyRs in turn affects the
disposition of DHPRs, which is normally dictated by a linkage to RyR
subunits. In the dCRUs of 1B5 cells, DHPRs are neither grouped into
tetrads nor aligned in two orthogonal directions. We have explored the structural role of RyR3 in the assembly of CRUs in 1B5 cells
independently expressing either RyR1 or RyR3. Either isoform
colocalizes with DHPRs and triadin at the cell periphery. Electron
microscopy shows that expression of either isoform results in CRUs
containing arrays of feet, indicating the ability of both isoforms to
be targeted to dCRUs and to assemble in ordered arrays in the absence
of the other. However, a significant difference between RyR1- and
RyR3-rescued junctions is revealed by freeze fracture. While cells
transfected with RyR1 show restoration of DHPR tetrads and DHPR
orthogonal alignment indicative of a link to RyRs, those transfected
with RyR3 do not. This indicates that RyR3 fails to link to DHPRs in a
specific manner. This morphological evidence supports the hypothesis that activation of RyR3 in skeletal muscle cells must be indirect and
provides the basis for failure of e-c coupling in muscle cells containing RyR3 but lacking RyR1 (see the accompanying report, Fessenden et al., 2000).
Biophys J, November 2000, p. 2494-2508, Vol. 79, No. 5
© 2000 by the Biophysical Society 0006-3495/00/11/2494/15 $2.00
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