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

• Published in: The Journal of general physiology Vol. 154; no. 1
• Main Authors: Millet, Jonathan R M, Romero, Luis O, Lee, Jungsoo, Bell, Briar, Vásquez, Valeria
• Format: Journal Article
• Language: English
• Published: United States Rockefeller University Press 03.01.2022
• Series: Mechanotransduction by Membrane Proteins
• 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
• ISSN: 0022-1295; 1540-7748
• DOI: 10.1085/jgp.202112960

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.