C. elegans PEZO-1 is a mechanosensitive ion channel involved in food sensation

PIEZO channels are force sensors essential for physiological processes, including baroreception and proprioception. The Caenorhabditis elegans genome encodes an orthologue gene of the Piezo family, pezo-1, which is expressed in several tissues, including the pharynx. This myogenic pump is an essenti...

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Bibliographic Details
Published in:The Journal of general physiology 2022-01, Vol.154 (1)
Main Authors: Millet, Jonathan R M, Romero, Luis O, Lee, Jungsoo, Bell, Briar, Vásquez, Valeria
Format: Article
Language:English
Subjects:
Animals
Biophysics
Caenorhabditis elegans - genetics
Caenorhabditis elegans Proteins - genetics
Caenorhabditis elegans Proteins - metabolism
Cellular physiology
Food
Gastrointestinal tract
Genome editing
Genomes
Ion Channels - genetics
Isoforms
Mechanical properties
Mechanical stimuli
Mechanotransduction by Membrane Proteins
Microfluidics
Neurons - metabolism
Osmolarity
Pharynx
Proprioception
Sensation
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Summary:PIEZO channels are force sensors essential for physiological processes, including baroreception and proprioception. The Caenorhabditis elegans genome encodes an orthologue gene of the Piezo family, pezo-1, which is expressed in several tissues, including the pharynx. This myogenic pump is an essential component of the C. elegans alimentary canal, whose contraction and relaxation are modulated by mechanical stimulation elicited by food content. Whether pezo-1 encodes a mechanosensitive ion channel and contributes to pharyngeal function remains unknown. Here, we leverage genome editing, genetics, microfluidics, and electropharyngeogram recording to establish that pezo-1 is expressed in the pharynx, including in a proprioceptive-like neuron, and regulates pharyngeal function. Knockout (KO) and gain-of-function (GOF) mutants reveal that pezo-1 is involved in fine-tuning pharyngeal pumping frequency, as well as sensing osmolarity and food mechanical properties. Using pressure-clamp experiments in primary C. elegans embryo cultures, we determine that pezo-1 KO cells do not display mechanosensitive currents, whereas cells expressing wild-type or GOF PEZO-1 exhibit mechanosensitivity. Moreover, infecting the Spodoptera frugiperda cell line with a baculovirus containing the G-isoform of pezo-1 (among the longest isoforms) demonstrates that pezo-1 encodes a mechanosensitive channel. Our findings reveal that pezo-1 is a mechanosensitive ion channel that regulates food sensation in worms.
ISSN:0022-1295
1540-7748
DOI:10.1085/jgp.202112960