skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Distinct mechanoreceptor pezo-1 isoforms modulate food intake in the nematode Caenorhabditis elegans
Two PIEZO mechanosensitive cation channels, PIEZO1 and PIEZO2, have been identified in mammals, where they are involved in numerous sensory processes. While structurally similar, PIEZO channels are expressed in distinct tissues and exhibit unique properties. How different PIEZOs transduce force, how their transduction mechanism varies, and how their unique properties match the functional needs of the distinct tissues where they are expressed remain all-important unanswered questions. The nematode Caenorhabditis elegans has a single PIEZO ortholog (pezo-1) predicted to have twelve isoforms. These isoforms share many transmembrane domains, but differ in those that distinguish PIEZO1 and PIEZO2 in mammals. Here we use translational and transcriptional reporters to show that long pezo-1 isoforms are selectively expressed in mesodermally derived tissues (such as muscle and glands). In contrast, shorter pezo-1 isoforms are primarily expressed in neurons. In the digestive system, different pezo-1 isoforms appear to be expressed in different cells of the same organ. We show that pharyngeal muscles, glands, and valve rely on long pezo-1 isoforms to respond appropriately to the presence of food. The unique pattern of complementary expression of pezo-1 isoforms suggest that different isoforms possess distinct functions. The number of pezo-1 isoforms in C. elegans, their differential pattern of expression, and their roles in experimentally tractable processes make this an attractive system to investigate the molecular basis for functional differences between members of the PIEZO family of mechanoreceptors.  more » « less
Award ID(s):
1818140
PAR ID:
10274105
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ; ; ;
Date Published:
Journal Name:
bioRxiv
ISSN:
2692-8205
Page Range / eLocation ID:
doi: https://doi.org/10.1101/2021.05.24.445504
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Zetka, M (Ed.)
    Abstract Two PIEZO mechanosensitive cation channels, PIEZO1 and PIEZO2, have been identified in mammals, where they are involved in numerous sensory processes. While structurally similar, PIEZO channels are expressed in distinct tissues and exhibit unique properties. How different PIEZOs transduce force, how their transduction mechanism varies, and how their unique properties match the functional needs of the tissues they are expressed in remain all-important unanswered questions. The nematode Caenorhabditis elegans has a single PIEZO ortholog (pezo-1) predicted to have 12 isoforms. These isoforms share many transmembrane domains but differ in those that distinguish PIEZO1 and PIEZO2 in mammals. We used transcriptional and translational reporters to show that putative promoter sequences immediately upstream of the start codon of long pezo-1 isoforms predominantly drive green fluorescent protein (GFP) expression in mesodermally derived tissues (such as muscle and glands). In contrast, sequences upstream of shorter pezo-1 isoforms resulted in GFP expression primarily in neurons. Putative promoters upstream of different isoforms drove GFP expression in different cells of the same organs of the digestive system. The observed unique pattern of complementary expression suggests that different isoforms could possess distinct functions within these organs. We used mutant analysis to show that pharyngeal muscles and glands require long pezo-1 isoforms to respond appropriately to the presence of food. The number of pezo-1 isoforms in C. elegans, their putative differential pattern of expression, and roles in experimentally tractable processes make this an attractive system to investigate the molecular basis for functional differences between members of the PIEZO family of mechanoreceptors. 
    more » « less
  2. In animals, PIEZOs are plasma membrane–localized cation channels involved in diverse mechanosensory processes. We investigated PIEZO function in tip-growing cells in the mossPhyscomitrium patensand the flowering plantArabidopsis thaliana.PpPIEZO1 andPpPIEZO2 redundantly contribute to the normal growth, size, and cytoplasmic calcium oscillations of caulonemal cells. BothPpPIEZO1 andPpPIEZO2 localized to vacuolar membranes. Loss-of-function, gain-of-function, and overexpression mutants revealed that moss PIEZO homologs promote increased complexity of vacuolar membranes through tubulation, internalization, and/or fission.ArabidopsisPIEZO1 also localized to the tonoplast and is required for vacuole tubulation in the tips of pollen tubes. We propose that in plant cells the tonoplast has more freedom of movement than the plasma membrane, making it a more effective location for mechanosensory proteins. 
    more » « less
  3. The discovery in 2010 of the PIEZO family of mechanoreceptors revolutionized our understanding of the role of proprioceptive feedback in mammalian physiology. Much remains to be elucidated. This study looks at the role this receptor plays in normal locomotion. Like humans, the nematode C. elegans expresses PIEZO-type channels (encoded by the pezo-1 gene) throughout its somatic musculature. Here we use the unbiased automated behavioral software Tierpsy to characterize the effects that mutations removing PEZO-1 from body wall musculature have on C. elegans crawling. We find that loss of PEZO-1 results in disrupted locomotion and posture, consistent with phenotypes associated with loss of PIEZO2 in human musculature. C. elegans is thus an amenable system to study the role of mechanoreception on muscle physiology and function. 
    more » « less
  4. FOXO transcription factors regulate development, longevity, and stress-resistance across species. The C. elegans FOXO ortholog, daf-16, has three major isoforms with distinct promoters and N-termini. Different combinations of isoforms regulate different processes. Adverse environments can induce dauer diapause after the second larval molt. During dauer, daf-16 blocks specification of vulval precursor cells, including EGFR/Ras-mediated 1˚ fate specification and LIN-12/Notch-mediated 2˚ fate specification. Using isoform-specific mutants, we find that daf-16a and daf-16f are functionally redundant for the block to the expression of 1˚ fate markers. In contrast, all three isoforms contribute to blocking the expression of 2˚ fate markers. 
    more » « less
  5. Mechanosensitive PIEZO ion channels are evolutionarily conserved proteins that are widely expressed in neuronal and muscular tissues. This study explores the role of the mechanoreceptor PEZO-1 in the body wall muscles of Caenorhabditis elegans, focusing on its influence on two locomotor behaviors, swimming and crawling. Using confocal imaging, we reveal that PEZO-1 localizes to the sarcolemma and plays a crucial role in modulating calcium dynamics that are important for muscle contraction. When we knocked down pezo-1 expression in striated muscles with RNA interference, calcium levels in head and tail muscles increased. While heightened, the overall trajectory of the calcium signal during the crawl cycle remained the same. While downregulation of pezo-1 led to an increase in crawling speed, it caused a reduction in swimming speed. Reduction in pezo-1 expression also resulted in the increased activation of the ventral tail muscles, and a disruption of dorsoventral movement asymmetry, a critical feature that enables propulsion in water. These alterations were correlated with impaired swimming posture and path curvature, suggesting that PEZO-1 has different functions during swimming and crawling. 
    more » « less