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A core signaling mechanism at the origin of animal nociception

Oscar M. Arenas, Emanuela E. Zaharieva, Alessia Para, Constanza Vásquez-Doorman, Christian P. Petersen, View ORCID ProfileMarco Gallio
doi: https://doi.org/10.1101/185405
Oscar M. Arenas
1Department of Neurobiology, Northwestern University, Evanston, Illinois, USA
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Emanuela E. Zaharieva
1Department of Neurobiology, Northwestern University, Evanston, Illinois, USA
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Alessia Para
1Department of Neurobiology, Northwestern University, Evanston, Illinois, USA
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Constanza Vásquez-Doorman
2Department of Molecular Biosciences, Northwestern University, Evanston, Illinois, USA.
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Christian P. Petersen
2Department of Molecular Biosciences, Northwestern University, Evanston, Illinois, USA.
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Marco Gallio
1Department of Neurobiology, Northwestern University, Evanston, Illinois, USA
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  • ORCID record for Marco Gallio
  • For correspondence: marco.gallio@northwestern.edu
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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 a remarkably conserved signaling mechanism mediates the detection of noxious stimuli in animals as diverse as flatworms and humans. Planarian flatworms are amongst the simplest bilateral animals with a centralized nervous system, and capable of directed behavior. We demonstrate 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 fruit flies (Drosophila) are also defective in the avoidance of noxious heat 1-3. Unexpectedly, we find that either the planarian or the human TRPA1 can restore noxious heat avoidance to TRPA1 mutant Drosophila, even though neither is directly activated by heat. Instead, our data suggest that TRPA1 activation is mediated by H2O2/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 human nociceptive systems may share a common ancestry with those of most extant animals, tracing back their origin to a progenitor that lived more than 500 million years ago.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 12, 2017.
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A core signaling mechanism at the origin of animal nociception
Oscar M. Arenas, Emanuela E. Zaharieva, Alessia Para, Constanza Vásquez-Doorman, Christian P. Petersen, Marco Gallio
bioRxiv 185405; doi: https://doi.org/10.1101/185405
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A core signaling mechanism at the origin of animal nociception
Oscar M. Arenas, Emanuela E. Zaharieva, Alessia Para, Constanza Vásquez-Doorman, Christian P. Petersen, Marco Gallio
bioRxiv 185405; doi: https://doi.org/10.1101/185405

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