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The Journal of Neuroscience, December 19, 2007, 27(51):14089-14098; doi:10.1523/JNEUROSCI.4179-07.2007

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Cellular/Molecular
Nanoscale Organization of the MEC-4 DEG/ENaC Sensory Mechanotransduction Channel in Caenorhabditis elegans Touch Receptor Neurons

Juan G. Cueva, Atticus Mulholland, and Miriam B. Goodman

Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, California 94305

Correspondence should be addressed to Dr. Miriam B. Goodman, B-111 Beckman Center, 279 Campus Drive, Stanford, CA 94305. Email: mbgoodman{at}stanford.edu

Hearing, touch and proprioception are thought to involve direct activation of mechano-electrical transduction (MeT) channels. In Caenorhabditis elegans touch receptor neurons (TRNs), such channels contain two pore-forming subunits (MEC-4 and MEC-10) and two auxiliary subunits (MEC-2 and MEC-6). MEC-4 and MEC-10 belong to a large superfamily of ion channel proteins (DEG/ENaCs) that form nonvoltage-gated, amiloride-sensitive Na⁺ channels. In TRNs, unique 15-protofilament microtubules and an electron-dense extracellular matrix have been proposed to serve as gating tethers critical for MeT channel activation. We combined high-pressure freezing and serial-section immunoelectron microscopy to determine the position of MeT channels relative to putative gating tethers. MeT channels were visualized using antibodies against MEC-4 and MEC-2. This nanometer-resolution view of a sensory MeT channel establishes structural constraints on the mechanics of channel gating. We show here that MEC-2 and MEC-5 collagen, a putative extracellular tether, occupy overlapping but distinct domains in TRN neurites. Although channels decorate all sides of TRN neurites; they are not associated with the distal endpoints of 15-protofilament microtubules hypothesized to be gating tethers. These specialized microtubules, which are unique to TRNs, assemble into a cross-linked bundle connected by a network of kinked filaments to the neurite membrane. We speculate that the microtubule bundle converts external point loads into membrane stretch which, in turn, facilitates MeT channel activation.

Key words: somatosensory; mechanosensory; cytoskeleton; ENaC (epithelial sodium channels); transduction; C. elegans

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Received Sept. 12, 2007; revised Oct. 31, 2007; accepted Nov. 1, 2007.

Correspondence should be addressed to Dr. Miriam B. Goodman, B-111 Beckman Center, 279 Campus Drive, Stanford, CA 94305. Email: mbgoodman{at}stanford.edu

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