Piezo proteins: incidence and abundance in the enteric nervous system. Is there a link with mechanosensitivity?

Piezo channels play fundamental roles in many physiological processes. Their presence and functional role in the enteric nervous system is still not known. We hypothesize that they play a role in mechanotransduction in enteric neurons. Our aims are to quantify the presence of both Piezo1 and 2 in en...

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Bibliographic Details
Published in:Cell and tissue research 2019-03, Vol.375 (3), p.605-618
Main Authors: Mazzuoli-Weber, Gemma, Kugler, Eva Maria, Bühler, Carina Ines, Kreutz, Florian, Demir, Ihsan Ekin, Ceyhan, Onur Güralp, Zeller, Florian, Schemann, Michael
Format: Article
Language:English
Subjects:
Acetyltransferase
Animal experimentation
Axons
Biomedical and Life Sciences
Biomedicine
Choline
Choline O-acetyltransferase
Comparative analysis
Comparative literature
Enteric nervous system
Experiments
Gastrointestinal system
Gastrointestinal tract
Human Genetics
Immunohistochemistry
Intestine
Mechanotransduction
Mediation
Molecular Medicine
Myenteric plexus
Nervous system
Neuroimaging
Neurons
Nitric oxide
Nitric-oxide synthase
Nitrogen oxides
Peptides
Physiological aspects
Proteomics
Regular Article
Rodents
Statistical analysis
Stomach
Submucosal plexus
Vasoactive agents
Vasoactive intestinal peptide
Vasoactive intestinal peptides
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Summary:Piezo channels play fundamental roles in many physiological processes. Their presence and functional role in the enteric nervous system is still not known. We hypothesize that they play a role in mechanotransduction in enteric neurons. Our aims are to quantify the presence of both Piezo1 and 2 in enteric neurons throughout the gastrointestinal tract using immunohistochemistry and analyze their function(s) using neuroimaging techniques and pharmacological investigations. In order to perform a systematic and comparative study, we performed our experiments in gastrointestinal tissue from guinea pigs, mice and humans. Piezo1 (20–70%) is expressed by both enteric neuronal cell bodies and fibers in the myenteric and submucosal plexi of all the species investigated. Generally, Piezo1 expressing somata are more numerous in the submucosal plexus (50–80%) than in the myenteric plexus (15–35%) apart from the stomach where Piezo1 is expressed in up to 60% of cell bodies. Myenteric Piezo1 neurons mainly (60–100%) but not exclusively, also express nitric oxide synthase, a minority express choline acetyltransferase. In the submucosal plexus, Piezo1 neurons co-express vasoactive intestinal peptide (40–90%). Conversely, expression of Piezo2 is extremely rare in the somata of enteric neurons and is present in few neurites. In functional experiments, 38–76% of the mechanosensitive neurons expressed Piezo1 channels. Statistical analysis showed a positive significant correlation between mechanosensitive and Piezo1 positive neurons. However, pharmacological experiments using an activator and an inhibitor of Piezo channels did not demonstrate changes in mechanotransduction. A major role of Piezo1 in the mechanosensitivity of enteric neurons can be excluded.
ISSN:0302-766X
1432-0878
DOI:10.1007/s00441-018-2926-7