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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Main Authors: Kelli E. Cannon, Meenakshi Ranasinghe, Paul W. Millhouse, Ayona Roychowdhury, Lynn E. Dobrunz, Stephen H. Foulger, David M. Gauntt, Jeffrey N. Anker, Mark Bolding
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-08-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2023.1210138/full
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author Kelli E. Cannon
Kelli E. Cannon
Kelli E. Cannon
Meenakshi Ranasinghe
Paul W. Millhouse
Ayona Roychowdhury
Lynn E. Dobrunz
Stephen H. Foulger
David M. Gauntt
Jeffrey N. Anker
Mark Bolding
author_facet Kelli E. Cannon
Kelli E. Cannon
Kelli E. Cannon
Meenakshi Ranasinghe
Paul W. Millhouse
Ayona Roychowdhury
Lynn E. Dobrunz
Stephen H. Foulger
David M. Gauntt
Jeffrey N. Anker
Mark Bolding
author_sort Kelli E. Cannon
collection DOAJ
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 doaj.art-0f7cd475191145e393c4e0c076928f8d2023-08-11T08:50:32ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-08-011710.3389/fnins.2023.12101381210138LITE-1 mediates behavioral responses to X-rays in Caenorhabditis elegansKelli E. Cannon0Kelli E. Cannon1Kelli E. Cannon2Meenakshi Ranasinghe3Paul W. Millhouse4Ayona Roychowdhury5Lynn E. Dobrunz6Stephen H. Foulger7David M. Gauntt8Jeffrey N. Anker9Mark Bolding10Department of Vision Sciences, School of Optometry, University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Neurobiology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Radiology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Chemistry, Clemson University, Clemson, SC, United StatesDepartment of Chemistry, Clemson University, Clemson, SC, United StatesDepartment of Radiology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Neurobiology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Materials Science and Engineering, College of Engineering, Computing and Applied Sciences, Clemson University, Clemson, SC, United StatesDepartment of Radiology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Chemistry, Clemson University, Clemson, SC, United StatesDepartment of Radiology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, United StatesRapid 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.https://www.frontiersin.org/articles/10.3389/fnins.2023.1210138/fullnoninvasive neuromodulationX-raysX-geneticsoptogeneticslite-1X-ray optogenetics
spellingShingle Kelli E. Cannon
Kelli E. Cannon
Kelli E. Cannon
Meenakshi Ranasinghe
Paul W. Millhouse
Ayona Roychowdhury
Lynn E. Dobrunz
Stephen H. Foulger
David M. Gauntt
Jeffrey N. Anker
Mark Bolding
LITE-1 mediates behavioral responses to X-rays in Caenorhabditis elegans
Frontiers in Neuroscience
noninvasive neuromodulation
X-rays
X-genetics
optogenetics
lite-1
X-ray optogenetics
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 noninvasive neuromodulation
X-rays
X-genetics
optogenetics
lite-1
X-ray optogenetics
url https://www.frontiersin.org/articles/10.3389/fnins.2023.1210138/full
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