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First published online March 18, 2009
doi: 10.1242/10.1242/jcs.028175

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Three-dimensional electron microscopy reveals new details of membrane systems for Ca²⁺ signaling in the heart

¹ The Center for Research in Biological Systems, University of California San Diego, La Jolla, CA 92093, USA
² The National Center for Microscopy and Imaging Research, University of California San Diego, La Jolla, CA 92093, USA
³ Department of Medicine, University of California San Diego, La Jolla, CA 92093, USA
⁴ Department of Mathematics, University of California San Diego, La Jolla, CA 92093, USA

^* Author for correspondence (e-mail: mhoshijima{at}ucsd.edu)

Accepted 1 December 2008

In the current study, the three-dimensional (3D) topologies of dyadic clefts and associated membrane organelles were mapped in mouse ventricular myocardium using electron tomography. The morphological details and the distribution of membrane systems, including transverse tubules (T-tubules), junctional sarcoplasmic reticulum (SR) and vicinal mitochondria, were determined and presumed to be crucial for controlling cardiac Ca²⁺ dynamics. The geometric complexity of T-tubules that varied in diameter with frequent branching was clarified. Dyadic clefts were intricately shaped and remarkably small (average 4.39x10⁵ nm³, median 2.81x10⁵ nm³). Although a dyadic cleft of average size could hold maximum 43 ryanodine receptor (RyR) tetramers, more than one-third of clefts were smaller than the size that is able to package as many as 15 RyR tetramers. The dyadic clefts were also adjacent to one another (average end-to-end distance to the nearest dyadic cleft, 19.9 nm) and were distributed irregularly along T-tubule branches. Electron-dense structures that linked membrane organelles were frequently observed between mitochondrial outer membranes and SR or T-tubules. We, thus, propose that the topology of dyadic clefts and the neighboring cellular micro-architecture are the major determinants of the local control of Ca²⁺ in the heart, including the establishment of the quantal nature of SR Ca²⁺ releases (e.g. Ca²⁺ sparks).

Key words: Ca²⁺ channel, Cardiac muscle, Electron microscopy, Excitation-contraction coupling, Membrane-bound organelle, Mitochondria

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