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Nucleophile sensitivity of Drosophila TRPA1 underlies light-induced feeding deterrence

  1. Eun Jo Du
  2. Tae Jung Ahn
  3. Xianlan Wen
  4. Dae-Won Seo
  5. Duk L Na
  6. Jae Young Kwon
  7. Myunghwan Choi
  8. Hyung-Wook Kim
  9. Hana Cho
  10. KyeongJin Kang  Is a corresponding author
  1. Sungkyunkwan University School of Medicine, Republic of Korea
  2. Sungkyunkwan University, Republic of Korea
  3. Sejong University, Republic of Korea
Research Article
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Cite this article as: eLife 2016;5:e18425 doi: 10.7554/eLife.18425

Abstract

Solar irradiation including ultraviolet (UV) light causes tissue damage by generating reactive free radicals that can be electrophilic or nucleophilic due to unpaired electrons. Little is known about how free radicals induced by natural sunlight are rapidly detected and avoided by animals. We discover that Drosophila Transient Receptor Potential Ankyrin 1 (TRPA1), previously known only as an electrophile receptor, sensitively detects photochemically active sunlight through nucleophile sensitivity. Rapid light-dependent feeding deterrence in Drosophila was mediated only by the TRPA1(A) isoform, despite the TRPA1(A) and TRPA1(B) isoforms having similar electrophile sensitivities. Such isoform dependentce re-emerges in the detection of structurally varied nucleophilic compounds and nucleophilicity-accompanying hydrogen peroxide (H2O2). Furthermore, these isoform-dependent mechanisms require a common set of TRPA1(A)-specific residues dispensable for electrophile detection. Collectively, TRPA1(A) rapidly responds to natural sunlight intensities through its nucleophile sensitivity as a receptor of photochemically generated radicals, leading to an acute light-induced behavioral shift in Drosophila.

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Author details

  1. Eun Jo Du

    Department of Anatomy and Cell Biology, Sungkyunkwan University School of Medicine, Suwon, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  2. Tae Jung Ahn

    Department of Anatomy and Cell Biology, Sungkyunkwan University School of Medicine, Suwon, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  3. Xianlan Wen

    Department of Physiology, Sungkyunkwan University School of Medicine, Suwon, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  4. Dae-Won Seo

    Department of Neurology, Sungkyunkwan University School of Medicine, Suwon, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  5. Duk L Na

    Department of Neurology, Sungkyunkwan University School of Medicine, Suwon, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  6. Jae Young Kwon

    Department of Biological Sciences, Sungkyunkwan University, Suwon, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  7. Myunghwan Choi

    Department of Biomedical Engineering, Sungkyunkwan University, Suwon, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  8. Hyung-Wook Kim

    College of Life Sciences, Sejong University, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  9. Hana Cho

    Department of Physiology, Sungkyunkwan University School of Medicine, Suwon, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9394-8671
  10. KyeongJin Kang

    Department of Anatomy and Cell Biology, Sungkyunkwan University School of Medicine, Suwon, Republic of Korea
    For correspondence
    kangk@skku.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0446-469X

Funding

Ministry of Education (NRF-2015R1D1A1A01057288)

  • KyeongJin Kang

Ministry of Education (2015H-1A2A-1034723)

  • Tae Jung Ahn

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Leslie C Griffith, Brandeis University, United States

Publication history

  1. Received: June 2, 2016
  2. Accepted: September 21, 2016
  3. Accepted Manuscript published: September 22, 2016 (version 1)
  4. Version of Record published: October 18, 2016 (version 2)

Copyright

© 2016, Du et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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