Activation of planarian TRPA1 by reactive oxygen species reveals a conserved mechanism for animal nociception

Oscar M. Arenas, Emanuela E. Zaharieva, Alessia Para, Constanza Vásquez-Doorman, Christian Paul Petersen, Marco Gallio*

*Corresponding author for this work

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

All animals must detect noxious stimuli to initiate protective behavior, but the evolutionary origin of nociceptive systems is not well understood. Here we show that noxious heat and irritant chemicals elicit robust escape behaviors in the planarian Schmidtea mediterranea and that the conserved ion channel TRPA1 is required for these responses. TRPA1-mutant Drosophila flies are also defective in noxious-heat responses. We find that either planarian or human TRPA1 can restore noxious-heat avoidance to TRPA1-mutant Drosophila, although neither is directly activated by heat. Instead, our data suggest that TRPA1 activation is mediated by H2O2 and reactive oxygen species, early markers of tissue damage rapidly produced as a result of heat exposure. Together, our data reveal a core function for TRPA1 in noxious heat transduction, demonstrate its conservation from planarians to humans, and imply that animal nociceptive systems may share a common ancestry, tracing back to a progenitor that lived more than 500 million years ago.

Original languageEnglish (US)
Pages (from-to)1686-1693
Number of pages8
JournalNature Neuroscience
Volume20
Issue number12
DOIs
StatePublished - Dec 1 2017

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Planarians
Nociception
Reactive Oxygen Species
Hot Temperature
Drosophila
Irritants
Ion Channels
Diptera

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

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abstract = "All animals must detect noxious stimuli to initiate protective behavior, but the evolutionary origin of nociceptive systems is not well understood. Here we show that noxious heat and irritant chemicals elicit robust escape behaviors in the planarian Schmidtea mediterranea and that the conserved ion channel TRPA1 is required for these responses. TRPA1-mutant Drosophila flies are also defective in noxious-heat responses. We find that either planarian or human TRPA1 can restore noxious-heat avoidance to TRPA1-mutant Drosophila, although neither is directly activated by heat. Instead, our data suggest that TRPA1 activation is mediated by H2O2 and reactive oxygen species, early markers of tissue damage rapidly produced as a result of heat exposure. Together, our data reveal a core function for TRPA1 in noxious heat transduction, demonstrate its conservation from planarians to humans, and imply that animal nociceptive systems may share a common ancestry, tracing back to a progenitor that lived more than 500 million years ago.",
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Activation of planarian TRPA1 by reactive oxygen species reveals a conserved mechanism for animal nociception. / Arenas, Oscar M.; Zaharieva, Emanuela E.; Para, Alessia; Vásquez-Doorman, Constanza; Petersen, Christian Paul; Gallio, Marco.

In: Nature Neuroscience, Vol. 20, No. 12, 01.12.2017, p. 1686-1693.

Research output: Contribution to journalArticle

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