TRPV channel-mediated calcium transients in nociceptor neurons are dispensable for avoidance behaviour

Amanda S. Lindy, Puja K. Parekh, Richard Zhu, Patrick Kanju, Sree V. Chintapalli, Volodymyr Tsvilovskyy, Randen L. Patterson, Andriy Anishkin, Damian B. Van Rossum, Wolfgang B. Liedtke

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Animals need to sense and react to potentially dangerous environments. TRP ion channels participate in nociception, presumably via Ca2+ influx, in most animal species. However, the relationship between ion permeation and animals' nocifensive behaviour is unknown. Here we use an invertebrate animal model with relevance for mammalian pain. We analyse the putative selectivity filter of OSM-9, a TRPV channel, in osmotic avoidance behaviour of Caenorhabditis elegans. Using mutagenized OSM-9 expressed in the head nociceptor neuron, ASH, we study nocifensive behaviour and Ca2+ influx. Within the selectivity filter, M601-F609, Y604G strongly reduces avoidance behaviour and eliminates Ca2+ transients. Y604F also abolishes Ca2+ transients in ASH, while sustaining avoidance behaviour, yet it disrupts behavioral plasticity. Homology modelling of the OSM-9 pore suggests that Y604 may assume a scaffolding role. Thus, aromatic residues in the OSM-9 selectivity filter are critical for pain behaviour and ion permeation. These findings have relevance for understanding evolutionary roots of mammalian nociception.

Original languageEnglish (US)
Article number4734
JournalNature Communications
Volume5
DOIs
StatePublished - Sep 2 2014

Fingerprint

Avoidance Learning
Nociceptors
avoidance
Calcium Channels
neurons
Neurons
calcium
Animals
Nociception
Calcium
Permeation
Ions
animals
Pain
Animal Behavior
pain
selectivity
Caenorhabditis elegans
Invertebrates
Ion Channels

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Chemistry(all)
  • Physics and Astronomy(all)

Cite this

Lindy, A. S., Parekh, P. K., Zhu, R., Kanju, P., Chintapalli, S. V., Tsvilovskyy, V., ... Liedtke, W. B. (2014). TRPV channel-mediated calcium transients in nociceptor neurons are dispensable for avoidance behaviour. Nature Communications, 5, [4734]. https://doi.org/10.1038/ncomms5734

TRPV channel-mediated calcium transients in nociceptor neurons are dispensable for avoidance behaviour. / Lindy, Amanda S.; Parekh, Puja K.; Zhu, Richard; Kanju, Patrick; Chintapalli, Sree V.; Tsvilovskyy, Volodymyr; Patterson, Randen L.; Anishkin, Andriy; Van Rossum, Damian B.; Liedtke, Wolfgang B.

In: Nature Communications, Vol. 5, 4734, 02.09.2014.

Research output: Contribution to journalArticle

Lindy, AS, Parekh, PK, Zhu, R, Kanju, P, Chintapalli, SV, Tsvilovskyy, V, Patterson, RL, Anishkin, A, Van Rossum, DB & Liedtke, WB 2014, 'TRPV channel-mediated calcium transients in nociceptor neurons are dispensable for avoidance behaviour', Nature Communications, vol. 5, 4734. https://doi.org/10.1038/ncomms5734
Lindy, Amanda S. ; Parekh, Puja K. ; Zhu, Richard ; Kanju, Patrick ; Chintapalli, Sree V. ; Tsvilovskyy, Volodymyr ; Patterson, Randen L. ; Anishkin, Andriy ; Van Rossum, Damian B. ; Liedtke, Wolfgang B. / TRPV channel-mediated calcium transients in nociceptor neurons are dispensable for avoidance behaviour. In: Nature Communications. 2014 ; Vol. 5.
@article{b2a57d68698d4f25912dd9ff21f14508,
title = "TRPV channel-mediated calcium transients in nociceptor neurons are dispensable for avoidance behaviour",
abstract = "Animals need to sense and react to potentially dangerous environments. TRP ion channels participate in nociception, presumably via Ca2+ influx, in most animal species. However, the relationship between ion permeation and animals' nocifensive behaviour is unknown. Here we use an invertebrate animal model with relevance for mammalian pain. We analyse the putative selectivity filter of OSM-9, a TRPV channel, in osmotic avoidance behaviour of Caenorhabditis elegans. Using mutagenized OSM-9 expressed in the head nociceptor neuron, ASH, we study nocifensive behaviour and Ca2+ influx. Within the selectivity filter, M601-F609, Y604G strongly reduces avoidance behaviour and eliminates Ca2+ transients. Y604F also abolishes Ca2+ transients in ASH, while sustaining avoidance behaviour, yet it disrupts behavioral plasticity. Homology modelling of the OSM-9 pore suggests that Y604 may assume a scaffolding role. Thus, aromatic residues in the OSM-9 selectivity filter are critical for pain behaviour and ion permeation. These findings have relevance for understanding evolutionary roots of mammalian nociception.",
author = "Lindy, {Amanda S.} and Parekh, {Puja K.} and Richard Zhu and Patrick Kanju and Chintapalli, {Sree V.} and Volodymyr Tsvilovskyy and Patterson, {Randen L.} and Andriy Anishkin and {Van Rossum}, {Damian B.} and Liedtke, {Wolfgang B.}",
year = "2014",
month = "9",
day = "2",
doi = "10.1038/ncomms5734",
language = "English (US)",
volume = "5",
journal = "Nature Communications",
issn = "2041-1723",
publisher = "Nature Publishing Group",

}

TY - JOUR

T1 - TRPV channel-mediated calcium transients in nociceptor neurons are dispensable for avoidance behaviour

AU - Lindy, Amanda S.

AU - Parekh, Puja K.

AU - Zhu, Richard

AU - Kanju, Patrick

AU - Chintapalli, Sree V.

AU - Tsvilovskyy, Volodymyr

AU - Patterson, Randen L.

AU - Anishkin, Andriy

AU - Van Rossum, Damian B.

AU - Liedtke, Wolfgang B.

PY - 2014/9/2

Y1 - 2014/9/2

N2 - Animals need to sense and react to potentially dangerous environments. TRP ion channels participate in nociception, presumably via Ca2+ influx, in most animal species. However, the relationship between ion permeation and animals' nocifensive behaviour is unknown. Here we use an invertebrate animal model with relevance for mammalian pain. We analyse the putative selectivity filter of OSM-9, a TRPV channel, in osmotic avoidance behaviour of Caenorhabditis elegans. Using mutagenized OSM-9 expressed in the head nociceptor neuron, ASH, we study nocifensive behaviour and Ca2+ influx. Within the selectivity filter, M601-F609, Y604G strongly reduces avoidance behaviour and eliminates Ca2+ transients. Y604F also abolishes Ca2+ transients in ASH, while sustaining avoidance behaviour, yet it disrupts behavioral plasticity. Homology modelling of the OSM-9 pore suggests that Y604 may assume a scaffolding role. Thus, aromatic residues in the OSM-9 selectivity filter are critical for pain behaviour and ion permeation. These findings have relevance for understanding evolutionary roots of mammalian nociception.

AB - Animals need to sense and react to potentially dangerous environments. TRP ion channels participate in nociception, presumably via Ca2+ influx, in most animal species. However, the relationship between ion permeation and animals' nocifensive behaviour is unknown. Here we use an invertebrate animal model with relevance for mammalian pain. We analyse the putative selectivity filter of OSM-9, a TRPV channel, in osmotic avoidance behaviour of Caenorhabditis elegans. Using mutagenized OSM-9 expressed in the head nociceptor neuron, ASH, we study nocifensive behaviour and Ca2+ influx. Within the selectivity filter, M601-F609, Y604G strongly reduces avoidance behaviour and eliminates Ca2+ transients. Y604F also abolishes Ca2+ transients in ASH, while sustaining avoidance behaviour, yet it disrupts behavioral plasticity. Homology modelling of the OSM-9 pore suggests that Y604 may assume a scaffolding role. Thus, aromatic residues in the OSM-9 selectivity filter are critical for pain behaviour and ion permeation. These findings have relevance for understanding evolutionary roots of mammalian nociception.

UR - http://www.scopus.com/inward/record.url?scp=84907339245&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84907339245&partnerID=8YFLogxK

U2 - 10.1038/ncomms5734

DO - 10.1038/ncomms5734

M3 - Article

VL - 5

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

M1 - 4734

ER -