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

Kelli E Cannon; Meenakshi Ranasinghe; Paul W Millhouse; Ayona Roychowdhury; Lynn E Dobrunz; Stephen H Foulger; David M Gauntt; Jeffrey N Anker; Mark Bolding

doi:10.3389/fnins.2023.1210138

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

Front Neurosci. 2023 Aug 10:17:1210138. doi: 10.3389/fnins.2023.1210138. eCollection 2023.

Authors

Affiliations

¹ Department of Vision Sciences, School of Optometry, University of Alabama at Birmingham, Birmingham, AL, United States.
² Department of Neurobiology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, United States.
³ Department of Radiology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, United States.
⁴ Department of Chemistry, Clemson University, Clemson, SC, United States.
⁵ Department of Materials Science and Engineering, College of Engineering, Computing and Applied Sciences, Clemson University, Clemson, SC, United States.

Abstract

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.

Keywords: X-genetics; X-ray optogenetics; X-rays; lite-1; noninvasive neuromodulation; optogenetics.