Abstract
Mechanoelectrical transduction (MeT) channels embedded in neuronal cell membranes are essential for touch and proprioception. Little is understood about the interplay between native MeT channels and membrane phospholipids, in part because few techniques are available for altering plasma membrane composition invivo. Here, we leverage genetic dissection, chemical complementation, and optogenetics to establish that arachidonic acid (AA), an omega-6 polyunsaturated fatty acid, enhances touch sensation and mechanoelectrical transduction activity while incorporated into membrane phospholipids in C.elegans touch receptor neurons (TRNs). Because dynamic force spectroscopy reveals that AA modulates the mechanical properties of TRN plasma membranes, we propose that this polyunsaturated fatty acid (PUFA) is needed for MeT channel activity. These findings establish that polyunsaturated phospholipids are crucial determinants of both the biochemistry and mechanics of mechanoreceptor neurons and reinforce the idea that sensory mechanotransduction in animals relies on a cellular machine composed of both proteins and membrane lipids.
Highlights
The sensory neurons embedded in our skin use mechano-electrical transduction (MeT) channels to detect mechanical stimuli delivered by a feather’s brush, a pin’s prick, or a mobile phone’s buzz
Additional MeT channel subunits have been identified in fruit flies and mice: NOMPC is thought to be a pore-forming subunit in fly mechanoreceptor neurons (Gong et al, 2013; Yan et al, 2013; Zhang et al, 2013); Piezo proteins are thought to function as MeT channels in body mechanoreceptor neurons and in red blood cells (Bae et al, 2013; Coste et al, 2010; Kim et al, 2013); TMHS and TMC proteins are required for mechanotransduction by inner ear hair cells in mice (Pan et al, 2013; Xiong et al, 2012)
Arachidonic acid is likely synthesized within touch receptor neurons (TRNs) in vivo, since we show that enzymes needed for its synthesis are expressed in TRNs
Summary
The sensory neurons embedded in our skin use mechano-electrical transduction (MeT) channels to detect mechanical stimuli delivered by a feather’s brush, a pin’s prick, or a mobile phone’s buzz. If not all MeT channels belong to macromolecular complexes whose protein constituents have been identified only for a few mechanoreceptor cells. While many of the proteins needed to form MeT channels in mechanoreceptor cells have been identified, very little is known about how the composition of the membrane modulates MeT channel function
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