Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors

Marios Chatzigeorgiou; Sungjae Yoo; Joseph D. Watson; Wei Hsiang Lee; W. Clay Spencer; Katie S. Kindt; Sun Wook Hwang; David M. Miller; Millet Treinin; Monica Driscoll; William R. Schafer

doi:10.1038/nn.2581

Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors

Marios Chatzigeorgiou, Sungjae Yoo, Joseph D. Watson, Wei Hsiang Lee, W. Clay Spencer, Katie S. Kindt, Sun Wook Hwang, David M. Miller, Millet Treinin, Monica Driscoll, William R. Schafer

Research output: Contribution to journal › Article › peer-review

194 Citations (Scopus)

Abstract

Polymodal nociceptors detect noxious stimuli, including harsh touch, toxic chemicals and extremes of heat and cold. The molecular mechanisms by which nociceptors are able to sense multiple qualitatively distinct stimuli are not well understood. We found that the C. elegans PVD neurons are mulitidendritic nociceptors that respond to harsh touch and cold temperatures. The harsh touch modality specifically required the DEG/ENaC proteins MEC-10 and DEGT-1, which represent putative components of a harsh touch mechanotransduction complex. In contrast, responses to cold required the TRPA-1 channel and were MEC-10 and DEGT-1 independent. Heterologous expression of C. elegans TRPA-1 conferred cold responsiveness to other C. elegans neurons and to mammalian cells, indicating that TRPA-1 is a cold sensor. Our results suggest that C. elegans nociceptors respond to thermal and mechanical stimuli using distinct sets of molecules and identify DEG/ENaC channels as potential receptors for mechanical pain.

Original language	English
Pages (from-to)	861-868
Number of pages	8
Journal	Nature Neuroscience
Volume	13
Issue number	7
DOIs	https://doi.org/10.1038/nn.2581
Publication status	Published - 2010 Jul

Bibliographical note

Funding Information:
We thank the Caenorhabditis Genetics Center, the National Bioresource Project and the Mitani laboratory for worm strains, N. Barry for help with microscopy, I. Rabinowitz for writing software to analyze averaged ratio traces, D. Cattermole and P. Heard in the LMB technical workshop for designing and building thermal controllers, the Vanderbilt Functional Genomics Shared Resource for help with microarray experiments and R. Branicky for comments on the manuscript. This research was supported by the Medical Research Council and grants from the National Institute on Drug Abuse (W.R.S.) and the National Institute of Neurological Disorders and Stroke (M.D. and D.M.M.), from the Brain Research Center of the 21st Century Frontier Research Program funded by the Ministry of Education, Science and Technology of Korea (code M103KV010015-06K2201-01510) and National Research Foundation of Korea (codes KRF-2008-331-E00457 and 2009-0076543) to S.W.H., and from the US-Israel Binational Science Foundation (grant 2005036 to M.T. and D.M.M.).

ASJC Scopus subject areas

General Neuroscience

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10.1038/nn.2581

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@article{50a949c185004458bec9705f5921d15f,

title = "Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors",

abstract = "Polymodal nociceptors detect noxious stimuli, including harsh touch, toxic chemicals and extremes of heat and cold. The molecular mechanisms by which nociceptors are able to sense multiple qualitatively distinct stimuli are not well understood. We found that the C. elegans PVD neurons are mulitidendritic nociceptors that respond to harsh touch and cold temperatures. The harsh touch modality specifically required the DEG/ENaC proteins MEC-10 and DEGT-1, which represent putative components of a harsh touch mechanotransduction complex. In contrast, responses to cold required the TRPA-1 channel and were MEC-10 and DEGT-1 independent. Heterologous expression of C. elegans TRPA-1 conferred cold responsiveness to other C. elegans neurons and to mammalian cells, indicating that TRPA-1 is a cold sensor. Our results suggest that C. elegans nociceptors respond to thermal and mechanical stimuli using distinct sets of molecules and identify DEG/ENaC channels as potential receptors for mechanical pain.",

author = "Marios Chatzigeorgiou and Sungjae Yoo and Watson, {Joseph D.} and Lee, {Wei Hsiang} and Spencer, {W. Clay} and Kindt, {Katie S.} and Hwang, {Sun Wook} and Miller, {David M.} and Millet Treinin and Monica Driscoll and Schafer, {William R.}",

note = "Funding Information: We thank the Caenorhabditis Genetics Center, the National Bioresource Project and the Mitani laboratory for worm strains, N. Barry for help with microscopy, I. Rabinowitz for writing software to analyze averaged ratio traces, D. Cattermole and P. Heard in the LMB technical workshop for designing and building thermal controllers, the Vanderbilt Functional Genomics Shared Resource for help with microarray experiments and R. Branicky for comments on the manuscript. This research was supported by the Medical Research Council and grants from the National Institute on Drug Abuse (W.R.S.) and the National Institute of Neurological Disorders and Stroke (M.D. and D.M.M.), from the Brain Research Center of the 21st Century Frontier Research Program funded by the Ministry of Education, Science and Technology of Korea (code M103KV010015-06K2201-01510) and National Research Foundation of Korea (codes KRF-2008-331-E00457 and 2009-0076543) to S.W.H., and from the US-Israel Binational Science Foundation (grant 2005036 to M.T. and D.M.M.).",

year = "2010",

month = jul,

doi = "10.1038/nn.2581",

language = "English",

volume = "13",

pages = "861--868",

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T1 - Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors

AU - Chatzigeorgiou, Marios

AU - Yoo, Sungjae

AU - Watson, Joseph D.

AU - Lee, Wei Hsiang

AU - Spencer, W. Clay

AU - Kindt, Katie S.

AU - Hwang, Sun Wook

AU - Miller, David M.

AU - Treinin, Millet

AU - Driscoll, Monica

AU - Schafer, William R.

N1 - Funding Information: We thank the Caenorhabditis Genetics Center, the National Bioresource Project and the Mitani laboratory for worm strains, N. Barry for help with microscopy, I. Rabinowitz for writing software to analyze averaged ratio traces, D. Cattermole and P. Heard in the LMB technical workshop for designing and building thermal controllers, the Vanderbilt Functional Genomics Shared Resource for help with microarray experiments and R. Branicky for comments on the manuscript. This research was supported by the Medical Research Council and grants from the National Institute on Drug Abuse (W.R.S.) and the National Institute of Neurological Disorders and Stroke (M.D. and D.M.M.), from the Brain Research Center of the 21st Century Frontier Research Program funded by the Ministry of Education, Science and Technology of Korea (code M103KV010015-06K2201-01510) and National Research Foundation of Korea (codes KRF-2008-331-E00457 and 2009-0076543) to S.W.H., and from the US-Israel Binational Science Foundation (grant 2005036 to M.T. and D.M.M.).

PY - 2010/7

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N2 - Polymodal nociceptors detect noxious stimuli, including harsh touch, toxic chemicals and extremes of heat and cold. The molecular mechanisms by which nociceptors are able to sense multiple qualitatively distinct stimuli are not well understood. We found that the C. elegans PVD neurons are mulitidendritic nociceptors that respond to harsh touch and cold temperatures. The harsh touch modality specifically required the DEG/ENaC proteins MEC-10 and DEGT-1, which represent putative components of a harsh touch mechanotransduction complex. In contrast, responses to cold required the TRPA-1 channel and were MEC-10 and DEGT-1 independent. Heterologous expression of C. elegans TRPA-1 conferred cold responsiveness to other C. elegans neurons and to mammalian cells, indicating that TRPA-1 is a cold sensor. Our results suggest that C. elegans nociceptors respond to thermal and mechanical stimuli using distinct sets of molecules and identify DEG/ENaC channels as potential receptors for mechanical pain.

AB - Polymodal nociceptors detect noxious stimuli, including harsh touch, toxic chemicals and extremes of heat and cold. The molecular mechanisms by which nociceptors are able to sense multiple qualitatively distinct stimuli are not well understood. We found that the C. elegans PVD neurons are mulitidendritic nociceptors that respond to harsh touch and cold temperatures. The harsh touch modality specifically required the DEG/ENaC proteins MEC-10 and DEGT-1, which represent putative components of a harsh touch mechanotransduction complex. In contrast, responses to cold required the TRPA-1 channel and were MEC-10 and DEGT-1 independent. Heterologous expression of C. elegans TRPA-1 conferred cold responsiveness to other C. elegans neurons and to mammalian cells, indicating that TRPA-1 is a cold sensor. Our results suggest that C. elegans nociceptors respond to thermal and mechanical stimuli using distinct sets of molecules and identify DEG/ENaC channels as potential receptors for mechanical pain.

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EP - 868

JO - Nature Neuroscience

JF - Nature Neuroscience

IS - 7

ER -

Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors

Abstract

Bibliographical note

ASJC Scopus subject areas

UN SDGs

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