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Piezo Is Essential for Amiloride-Sensitive Stretch-Activated Mechanotransduction in Larval Drosophila Dorsal Bipolar Dendritic Sensory Neurons

Lookup NU author(s): Fiona Shenton

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This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0).


Abstract

Stretch-activated afferent neurons, such as those of mammalian muscle spindles, are essential for proprioception and motor co-ordination, but the underlying mechanisms of mechanotransduction are poorly understood. The dorsal bipolar dendritic (dbd) sensory neurons are putative stretch receptors in the Drosophila larval body wall. We have developed an in vivo protocol to obtain receptor potential recordings from intact dbd neurons in response to stretch. Receptor potential changes in dbd neurons in response to stretch showed a complex, dynamic profile with similar characteristics to those previously observed for mammalian muscle spindles. These profiles were reproduced by a general in silico model of stretch-activated neurons. This in silico model predicts an essential role for a mechanosensory cation channel (MSC) in all aspects of receptor potential generation. Using pharmacological and genetic techniques, we identified the mechanosensory channel, DmPiezo, in this functional role in dbd neurons, with TRPA1 playing a subsidiary role. We also show that rat muscle spindles exhibit a ruthenium red-sensitive current, but found no expression evidence to suggest that this corresponds to Piezo activity. In summary, we show that the dbd neuron is a stretch receptor and demonstrate that this neuron is a tractable model for investigating mechanisms of mechanotransduction.


Publication metadata

Author(s): Suslak TJ, Watson S, Thompson KJ, Shenton FC, Bewick GS, Armstrong JD, Jarman AP

Publication type: Article

Publication status: Published

Journal: PLoS One

Year: 2015

Volume: 10

Issue: 7

Online publication date: 17/07/2015

Acceptance date: 27/05/2015

Date deposited: 20/04/2016

ISSN (electronic): 1932-6203

Publisher: Public Library of Science

URL: http://dx.doi.org/10.1371/journal.pone.0130969

DOI: 10.1371/journal.pone.0130969


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Funding

Funder referenceFunder name
Scottish Universities Life Sciences Alliance (SULSA) BioSkape grant
UK Biotechnology and Biological Sciences Research Council (BBSRC)
UK Medical Research Council (MRC)
Eli Lilly
BB/F529254/1UK Engineering and Physical Sciences Research Council (EPSRC)
EP/F500385/1UK Engineering and Physical Sciences Research Council (EPSRC)
G13/08Tenovus Scotland Moulton-Barrett Research Scholarship
OL-532Tenovus Scotland Moulton-Barrett Research Scholarship

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