Drosophila TRPA1 isoforms detect UV light via photochemical production of H2O2

Ananya R. Guntur, Pengyu Gu, Kendra Takle, Jingyi Chen, Yang Xiang, and Chung-Hui Yang
PNAS October 20, 2015 112 (42) E5753-E5761; published ahead of print October 6, 2015 https://doi.org/10.1073/pnas.1514862112

  1. Edited by Yuh Nung Jan, Howard Hughes Medical Institute, University of California, San Francisco, CA, and approved September 16, 2015 (received for review July 27, 2015)

Significance

Discovering new light-sensing mechanisms and cell types are of considerable interest to researchers across disciplines. Understanding how cells sense light is one of the most fundamental problems in biology. In addition, optogenetics has become a critical research tool and discovery of new light-sensing mechanisms may expand the existing toolbox. In this work, we described our discovery of a dTRPA1-dependent photochemical pathway that is sufficient to confer UV sensitivity to light-insensitive cells. We also discovered a group of neuroendocrine cells that express these isoforms endogenously and can sense UV. These findings demonstrate a new cell type that can sense strong UV and the potential of exploiting dTRPA1 channel as an optogenetic tool.

Abstract

The transient receptor potential A1 (TRPA1) channel is an evolutionarily conserved detector of temperature and irritant chemicals. Here, we show that two specific isoforms of TRPA1 in Drosophila are H2O2 sensitive and that they can detect strong UV light via sensing light-induced production of H2O2. We found that ectopic expression of these H2O2-sensitive Drosophila TRPA1 (dTRPA1) isoforms conferred UV sensitivity to light-insensitive HEK293 cells and Drosophila neurons, whereas expressing the H2O2-insensitive isoform did not. Curiously, when expressed in one specific group of motor neurons in adult flies, the H2O2-sensitive dTRPA1 isoforms were as competent as the blue light-gated channelrhodopsin-2 in triggering motor output in response to light. We found that the corpus cardiacum (CC) cells, a group of neuroendocrine cells that produce the adipokinetic hormone (AKH) in the larval ring gland endogenously express these H2O2-sensitive dTRPA1 isoforms and that they are UV sensitive. Sensitivity of CC cells required dTRPA1 and H2O2 production but not conventional phototransduction molecules. Our results suggest that specific isoforms of dTRPA1 can sense UV light via photochemical production of H2O2. We speculate that UV sensitivity conferred by these isoforms in CC cells may allow young larvae to activate stress response—a function of CC cells—when they encounter strong UV, an aversive stimulus for young larvae.

Footnotes

  • ↵1To whom correspondence may be addressed. Email: yang{at}neuro.duke.edu or Yang.Xiang{at}umassmed.edu.

  • Author contributions: A.R.G., P.G., K.T., Y.X., and C.-H.Y. designed research; A.R.G., P.G., K.T., and J.C. performed research; A.R.G., P.G., K.T., Y.X., and C.-H.Y. analyzed data; and A.R.G., Y.X., and C.-H.Y. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1514862112/-/DCSupplemental.

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Photochemical sensation by dTRPA1 channels
Ananya R. Guntur, Pengyu Gu, Kendra Takle, Jingyi Chen, Yang Xiang, Chung-Hui Yang
Proceedings of the National Academy of Sciences Oct 2015, 112 (42) E5753-E5761; DOI: 10.1073/pnas.1514862112
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