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Published online 18 September 2006. doi:10.1083/jcb.200604016
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 174, Number 7, 915-921
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 Structural and functional features and significance of the physical linkage between ER and mitochondria

György Csordás1, Christian Renken2, Péter Várnai3, Ludivine Walter1, David Weaver1, Karolyn F. Buttle2, Tamás Balla3, Carmen A. Mannella2, and György Hajnóczky1

1 Department of Pathology, Anatomy and Cell Biology, Thomas Jefferson University, Philadelphia, PA 19107
2 Resource for Visualization of Biological Complexity, Wadsworth Center, Albany, NY 12201
3 Endocrinology and Reproduction Research Branch, National Institutes of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892

Correspondence to György Hajnóczky: gyorgy.hajnoczky{at}jefferson.edu

The role of mitochondria in cell metabolism and survival is controlled by calcium signals that are commonly transmitted at the close associations between mitochondria and endoplasmic reticulum (ER). However, the physical linkage of the ER–mitochondria interface and its relevance for cell function remains elusive. We show by electron tomography that ER and mitochondria are adjoined by tethers that are ~10 nm at the smooth ER and ~25 nm at the rough ER. Limited proteolysis separates ER from mitochondria, whereas expression of a short "synthetic linker" (<5 nm) leads to tightening of the associations. Although normal connections are necessary and sufficient for proper propagation of ER-derived calcium signals to the mitochondria, tightened connections, synthetic or naturally observed under apoptosis-inducing conditions, make mitochondria prone to Ca2+ overloading and ensuing permeability transition. These results reveal an unexpected dependence of cell function and survival on the maintenance of proper spacing between the ER and mitochondria.

Abbreviations used in this paper: [Ca2+]c, cytoplasmic [Ca2+]; [Ca2+]m, mitochondrial matrix [Ca2+]; ET, electron tomography; IP3R, IP3 receptor; mRFP, monomeric red fluorescent protein; OMM, outer mitochondrial membrane; SBI, soybean trypsin inhibitor; TEM, transmission EM; Tg, thapsigargin.


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