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

Thomas J Suslak, Sonia Watson, Karen J. Thompson, Fiona C. Shenton, Guy S Bewick, J. Douglas Armstrong, Andrew P. Jarman

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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.
Original languageEnglish
Article number0130969
Number of pages16
JournalPloS ONE
Volume10
Issue number7
DOIs
Publication statusPublished - 17 Jul 2015

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Amiloride
sensory neurons
Sensory Receptor Cells
Drosophila
Neurons
neurons
Muscle Spindles
receptors
Mechanoreceptors
Muscle
Computer Simulation
muscles
proprioception
Genetic Techniques
Ruthenium Red
Afferent Neurons
Proprioception
integument
mechanotransduction
Cations

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Piezo is essential for amiloride-sensitive stretch-activated mechanotransduction in larval Drosophila dorsal bipolar dendritic sensory neurons. / J Suslak, Thomas; Watson, Sonia; Thompson, Karen J.; Shenton, Fiona C.; Bewick, Guy S; Armstrong, J. Douglas; Jarman, Andrew P.

In: PloS ONE, Vol. 10, No. 7, 0130969 , 17.07.2015.

Research output: Contribution to journalArticle

J Suslak, Thomas ; Watson, Sonia ; Thompson, Karen J. ; Shenton, Fiona C. ; Bewick, Guy S ; Armstrong, J. Douglas ; Jarman, Andrew P. / Piezo is essential for amiloride-sensitive stretch-activated mechanotransduction in larval Drosophila dorsal bipolar dendritic sensory neurons. In: PloS ONE. 2015 ; Vol. 10, No. 7.
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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.",
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