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Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception

Research output: Contribution to journalArticlepeer-review

DOI

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Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception. / Kang, Kyeongjin; Pulver, Stefan R; Panzano, Vincent C; Chang, Elaine C; Griffith, Leslie C; Theobald, Douglas L; Garrity, Paul A.

In: Nature, Vol. 464, No. 7288, 25.03.2010, p. 597-600.

Research output: Contribution to journalArticlepeer-review

Harvard

Kang, K, Pulver, SR, Panzano, VC, Chang, EC, Griffith, LC, Theobald, DL & Garrity, PA 2010, 'Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception', Nature, vol. 464, no. 7288, pp. 597-600. https://doi.org/10.1038/nature08848

APA

Kang, K., Pulver, S. R., Panzano, V. C., Chang, E. C., Griffith, L. C., Theobald, D. L., & Garrity, P. A. (2010). Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception. Nature, 464(7288), 597-600. https://doi.org/10.1038/nature08848

Vancouver

Kang K, Pulver SR, Panzano VC, Chang EC, Griffith LC, Theobald DL et al. Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception. Nature. 2010 Mar 25;464(7288):597-600. https://doi.org/10.1038/nature08848

Author

Kang, Kyeongjin ; Pulver, Stefan R ; Panzano, Vincent C ; Chang, Elaine C ; Griffith, Leslie C ; Theobald, Douglas L ; Garrity, Paul A. / Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception. In: Nature. 2010 ; Vol. 464, No. 7288. pp. 597-600.

Bibtex - Download

@article{108371f70f874fabb808c4831455f76c,
title = "Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception",
abstract = "Chemical nociception, the detection of tissue-damaging chemicals, is important for animal survival and causes human pain and inflammation, but its evolutionary origins are largely unknown. Reactive electrophiles are a class of noxious compounds humans find pungent and irritating, such as allyl isothiocyanate (in wasabi) and acrolein (in cigarette smoke). Diverse animals, from insects to humans, find reactive electrophiles aversive, but whether this reflects conservation of an ancient sensory modality has been unclear. Here we identify the molecular basis of reactive electrophile detection in flies. We demonstrate that Drosophila TRPA1 (Transient receptor potential A1), the Drosophila melanogaster orthologue of the human irritant sensor, acts in gustatory chemosensors to inhibit reactive electrophile ingestion. We show that fly and mosquito TRPA1 orthologues are molecular sensors of electrophiles, using a mechanism conserved with vertebrate TRPA1s. Phylogenetic analyses indicate that invertebrate and vertebrate TRPA1s share a common ancestor that possessed critical characteristics required for electrophile detection. These findings support emergence of TRPA1-based electrophile detection in a common bilaterian ancestor, with widespread conservation throughout vertebrate and invertebrate evolution. Such conservation contrasts with the evolutionary divergence of canonical olfactory and gustatory receptors and may relate to electrophile toxicity. We propose that human pain perception relies on an ancient chemical sensor conserved across approximately 500 million years of animal evolution.",
keywords = "Amino Acid Sequence, Animals, Conserved Sequence, Drosophila Proteins, Drosophila melanogaster, Evolution, Molecular, Gene Expression Profiling, Gene Expression Regulation, Humans, Molecular Sequence Data, Mutation, Phylogeny, Sensory Receptor Cells, TRPC Cation Channels, Taste Perception",
author = "Kyeongjin Kang and Pulver, {Stefan R} and Panzano, {Vincent C} and Chang, {Elaine C} and Griffith, {Leslie C} and Theobald, {Douglas L} and Garrity, {Paul A}",
year = "2010",
month = mar,
day = "25",
doi = "10.1038/nature08848",
language = "English",
volume = "464",
pages = "597--600",
journal = "Nature",
issn = "0028-0836",
publisher = "Nature publishing group",
number = "7288",

}

RIS (suitable for import to EndNote) - Download

TY - JOUR

T1 - Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception

AU - Kang, Kyeongjin

AU - Pulver, Stefan R

AU - Panzano, Vincent C

AU - Chang, Elaine C

AU - Griffith, Leslie C

AU - Theobald, Douglas L

AU - Garrity, Paul A

PY - 2010/3/25

Y1 - 2010/3/25

N2 - Chemical nociception, the detection of tissue-damaging chemicals, is important for animal survival and causes human pain and inflammation, but its evolutionary origins are largely unknown. Reactive electrophiles are a class of noxious compounds humans find pungent and irritating, such as allyl isothiocyanate (in wasabi) and acrolein (in cigarette smoke). Diverse animals, from insects to humans, find reactive electrophiles aversive, but whether this reflects conservation of an ancient sensory modality has been unclear. Here we identify the molecular basis of reactive electrophile detection in flies. We demonstrate that Drosophila TRPA1 (Transient receptor potential A1), the Drosophila melanogaster orthologue of the human irritant sensor, acts in gustatory chemosensors to inhibit reactive electrophile ingestion. We show that fly and mosquito TRPA1 orthologues are molecular sensors of electrophiles, using a mechanism conserved with vertebrate TRPA1s. Phylogenetic analyses indicate that invertebrate and vertebrate TRPA1s share a common ancestor that possessed critical characteristics required for electrophile detection. These findings support emergence of TRPA1-based electrophile detection in a common bilaterian ancestor, with widespread conservation throughout vertebrate and invertebrate evolution. Such conservation contrasts with the evolutionary divergence of canonical olfactory and gustatory receptors and may relate to electrophile toxicity. We propose that human pain perception relies on an ancient chemical sensor conserved across approximately 500 million years of animal evolution.

AB - Chemical nociception, the detection of tissue-damaging chemicals, is important for animal survival and causes human pain and inflammation, but its evolutionary origins are largely unknown. Reactive electrophiles are a class of noxious compounds humans find pungent and irritating, such as allyl isothiocyanate (in wasabi) and acrolein (in cigarette smoke). Diverse animals, from insects to humans, find reactive electrophiles aversive, but whether this reflects conservation of an ancient sensory modality has been unclear. Here we identify the molecular basis of reactive electrophile detection in flies. We demonstrate that Drosophila TRPA1 (Transient receptor potential A1), the Drosophila melanogaster orthologue of the human irritant sensor, acts in gustatory chemosensors to inhibit reactive electrophile ingestion. We show that fly and mosquito TRPA1 orthologues are molecular sensors of electrophiles, using a mechanism conserved with vertebrate TRPA1s. Phylogenetic analyses indicate that invertebrate and vertebrate TRPA1s share a common ancestor that possessed critical characteristics required for electrophile detection. These findings support emergence of TRPA1-based electrophile detection in a common bilaterian ancestor, with widespread conservation throughout vertebrate and invertebrate evolution. Such conservation contrasts with the evolutionary divergence of canonical olfactory and gustatory receptors and may relate to electrophile toxicity. We propose that human pain perception relies on an ancient chemical sensor conserved across approximately 500 million years of animal evolution.

KW - Amino Acid Sequence

KW - Animals

KW - Conserved Sequence

KW - Drosophila Proteins

KW - Drosophila melanogaster

KW - Evolution, Molecular

KW - Gene Expression Profiling

KW - Gene Expression Regulation

KW - Humans

KW - Molecular Sequence Data

KW - Mutation

KW - Phylogeny

KW - Sensory Receptor Cells

KW - TRPC Cation Channels

KW - Taste Perception

U2 - 10.1038/nature08848

DO - 10.1038/nature08848

M3 - Article

C2 - 20237474

VL - 464

SP - 597

EP - 600

JO - Nature

JF - Nature

SN - 0028-0836

IS - 7288

ER -

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