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

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A Correction to this article was published on 07 May 2019

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Abstract

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.

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  • 07 May 2019

    The Authors regret forgetting in the original version of this article to mention that this work was also supported by the US National Institute of Health (NIH) (1OT2OD024899-01).

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Acknowledgments

We gratefully thank Birgit Kuch for her technical assistance, the hours she spent performing immunohistochemical studies and the beautiful pictures she produced.

Funding

This work was supported by the German Research Foundation DFG (MA-5202/1-1 and 1-2).

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Authors and Affiliations

  1. Human Biology, Technische Universitaet Muenchen, Freising, Germany

    Gemma Mazzuoli-Weber, Eva Maria Kugler, Carina Ines Bühler, Florian Kreutz & Michael Schemann

  2. Institute for Physiology, University of Veterinary Medicine Hannover, Foundation, Bischofsholer Damm 15, 30173, Hannover, Germany

    Gemma Mazzuoli-Weber

  3. Department of Surgery, Klinikum Rechts der Isar, Technische Universitaet Muenchen, Munich, Germany

    Ihsan Ekin Demir & Onur Güralp Ceyhan

  4. Department of Surgery, Klinikum Freising, Freising, Germany

    Florian Zeller

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  1. Gemma Mazzuoli-Weber
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Correspondence to Gemma Mazzuoli-Weber.

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Mazzuoli-Weber, G., Kugler, E.M., Bühler, C.I. et al. Piezo proteins: incidence and abundance in the enteric nervous system. Is there a link with mechanosensitivity?. Cell Tissue Res 375, 605–618 (2019). https://doi.org/10.1007/s00441-018-2926-7

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