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LITE-1 mediates behavioral responses to X-rays in Caenorhabditis elegans

Rapid sensory detection of X-ray stimulation has been documented across a wide variety of species, but few studies have explored the underlying molecular mechanisms. Here we report the discovery of an acute behavioral avoidance response in wild type Caenorhabditis elegans to X-ray stimulation. The e...

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Autores principales: Cannon, Kelli E., Ranasinghe, Meenakshi, Millhouse, Paul W., Roychowdhury, Ayona, Dobrunz, Lynn E., Foulger, Stephen H., Gauntt, David M., Anker, Jeffrey N., Bolding, Mark
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10450342/
https://www.ncbi.nlm.nih.gov/pubmed/37638310
http://dx.doi.org/10.3389/fnins.2023.1210138
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author Cannon, Kelli E.
Ranasinghe, Meenakshi
Millhouse, Paul W.
Roychowdhury, Ayona
Dobrunz, Lynn E.
Foulger, Stephen H.
Gauntt, David M.
Anker, Jeffrey N.
Bolding, Mark
author_facet Cannon, Kelli E.
Ranasinghe, Meenakshi
Millhouse, Paul W.
Roychowdhury, Ayona
Dobrunz, Lynn E.
Foulger, Stephen H.
Gauntt, David M.
Anker, Jeffrey N.
Bolding, Mark
author_sort Cannon, Kelli E.
collection PubMed
description Rapid sensory detection of X-ray stimulation has been documented across a wide variety of species, but few studies have explored the underlying molecular mechanisms. Here we report the discovery of an acute behavioral avoidance response in wild type Caenorhabditis elegans to X-ray stimulation. The endogenous C. elegans UV-photoreceptor protein LITE-1 was found to mediate the locomotory avoidance response. Transgenic expression of LITE-1 in C. elegans muscle cells resulted in paralysis and egg ejection responses to X-ray stimulation, demonstrating that ectopic expression of LITE-1 can confer X-ray sensitivity to otherwise X-ray insensitive cells. This work represents the first demonstration of rapid X-ray based genetically targeted (X-genetic) manipulation of cellular electrical activity in intact behaving animals. Our findings suggest that LITE-1 has strong potential for use in this minimally invasive form of neuromodulation to transduce transcranial X-ray signals for precise manipulation of neural activity in mammals, bypassing the need for invasive surgical implants to deliver stimulation.
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spelling pubmed-104503422023-08-26 LITE-1 mediates behavioral responses to X-rays in Caenorhabditis elegans Cannon, Kelli E. Ranasinghe, Meenakshi Millhouse, Paul W. Roychowdhury, Ayona Dobrunz, Lynn E. Foulger, Stephen H. Gauntt, David M. Anker, Jeffrey N. Bolding, Mark Front Neurosci Neuroscience Rapid sensory detection of X-ray stimulation has been documented across a wide variety of species, but few studies have explored the underlying molecular mechanisms. Here we report the discovery of an acute behavioral avoidance response in wild type Caenorhabditis elegans to X-ray stimulation. The endogenous C. elegans UV-photoreceptor protein LITE-1 was found to mediate the locomotory avoidance response. Transgenic expression of LITE-1 in C. elegans muscle cells resulted in paralysis and egg ejection responses to X-ray stimulation, demonstrating that ectopic expression of LITE-1 can confer X-ray sensitivity to otherwise X-ray insensitive cells. This work represents the first demonstration of rapid X-ray based genetically targeted (X-genetic) manipulation of cellular electrical activity in intact behaving animals. Our findings suggest that LITE-1 has strong potential for use in this minimally invasive form of neuromodulation to transduce transcranial X-ray signals for precise manipulation of neural activity in mammals, bypassing the need for invasive surgical implants to deliver stimulation. Frontiers Media S.A. 2023-08-10 /pmc/articles/PMC10450342/ /pubmed/37638310 http://dx.doi.org/10.3389/fnins.2023.1210138 Text en Copyright © 2023 Cannon, Ranasinghe, Millhouse, Roychowdhury, Dobrunz, Foulger, Gauntt, Anker and Bolding. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Cannon, Kelli E.
Ranasinghe, Meenakshi
Millhouse, Paul W.
Roychowdhury, Ayona
Dobrunz, Lynn E.
Foulger, Stephen H.
Gauntt, David M.
Anker, Jeffrey N.
Bolding, Mark
LITE-1 mediates behavioral responses to X-rays in Caenorhabditis elegans
title LITE-1 mediates behavioral responses to X-rays in Caenorhabditis elegans
title_full LITE-1 mediates behavioral responses to X-rays in Caenorhabditis elegans
title_fullStr LITE-1 mediates behavioral responses to X-rays in Caenorhabditis elegans
title_full_unstemmed LITE-1 mediates behavioral responses to X-rays in Caenorhabditis elegans
title_short LITE-1 mediates behavioral responses to X-rays in Caenorhabditis elegans
title_sort lite-1 mediates behavioral responses to x-rays in caenorhabditis elegans
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10450342/
https://www.ncbi.nlm.nih.gov/pubmed/37638310
http://dx.doi.org/10.3389/fnins.2023.1210138
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