Piezo is essential for amiloride-sensitive stretch-activated mechanotransduction in larval Drosophila dorsal bipolar dendritic sensory neurons

Suslak, T. J., Watson, S., Thompson, K. J., Shenton, F. C., Bewick, G. S., Armstrong, J. D. and Jarman, A. P. (2015) Piezo is essential for amiloride-sensitive stretch-activated mechanotransduction in larval Drosophila dorsal bipolar dendritic sensory neurons. PLoS ONE, 10(7), e0130969. (doi: 10.1371/journal.pone.0130969) (PMID:26186008) (PMCID:PMC4506125)

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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.

Item Type:Articles
Additional Information:TJS supported in part by grants EP/F500385/1 and BB/F529254/1 for the University of Edinburgh School of Informatics Doctoral Training Centre in Neuroinformatics and Computational Neuroscience (http://www.anc.ed.ac.uk/dtc/) from the UK Engineering and Physical Sciences Research Council (EPSRC), UK Biotechnology and Biological Sciences Research Council (BBSRC), and the UK Medical Research Council (MRC). KJT is supported by a Tenovus Scotland Moulton-Barrett Research Scholarship (OL-532) and Research Grant (G13/08). SW is supported by a Scottish Universities Life Sciences Alliance (SULSA) BioSkape grant in collaboration with Eli Lilly.
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Thompson, Ms Karen
Authors: Suslak, T. J., Watson, S., Thompson, K. J., Shenton, F. C., Bewick, G. S., Armstrong, J. D., and Jarman, A. P.
Subjects:Q Science > QP Physiology
College/School:College of Medical Veterinary and Life Sciences > School of Molecular Biosciences
Journal Name:PLoS ONE
Publisher:Public Library of Science
ISSN:1932-6203
ISSN (Online):1932-6203
Copyright Holders:Copyright © 2015 Suslak et al.
First Published:First published in PLoS ONE 10(7): e0130969
Publisher Policy:Reproduced under a Creative Commons License

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