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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Frontiers Media S.A.
2023-08-01
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Series: | Frontiers in Neuroscience |
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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. |
first_indexed | 2024-03-12T15:18:32Z |
format | Article |
id | doaj.art-0f7cd475191145e393c4e0c076928f8d |
institution | Directory Open Access Journal |
issn | 1662-453X |
language | English |
last_indexed | 2024-03-12T15:18:32Z |
publishDate | 2023-08-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Neuroscience |
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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