Polymodal Functionality of C. elegans OLL Neurons in Mechanosensation and Thermosensation

Yuedan Fan; Wenjuan Zou; Jia Liu; Umar Al-Sheikh; Hankui Cheng; Duo Duan; Du Chen; Siyan Liu; Luyi Chen; Jilei Xu; Firdosh Ruhomutally; Lijun Kang

doi:10.1007/s12264-021-00629-4

Polymodal Functionality of C. elegans OLL Neurons in Mechanosensation and Thermosensation

Neurosci Bull. 2021 May;37(5):611-622. doi: 10.1007/s12264-021-00629-4. Epub 2021 Feb 8.

Authors

Yuedan Fan^#^{1

2}, Wenjuan Zou^#^{1

2}, Jia Liu^#^{1

2}, Umar Al-Sheikh^#^{1

2}, Hankui Cheng^{1

2}, Duo Duan^{1

2}, Du Chen^{1

2}, Siyan Liu^{1

2}, Luyi Chen³, Jilei Xu³, Firdosh Ruhomutally⁴, Lijun Kang^{5

6}

Affiliations

¹ Department of Neurobiology and Department of Neurosurgery of the First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, 310053, China.
² NHC and CAMS Key Laboratory of Medical Neurobiology, MOE Frontier Science Center for Brain Research and Brain-Machine Integration, School of Brain Science and Brain Medicine, Zhejiang University, Hangzhou, 310053, China.
³ Department of Gastroenterology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, 310016, China.
⁴ Department of Human Sciences and Psychology, University of South Africa (UNISA), Pretoria, 0003, South Africa.
⁵ Department of Neurobiology and Department of Neurosurgery of the First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, 310053, China. [email protected].
⁶ NHC and CAMS Key Laboratory of Medical Neurobiology, MOE Frontier Science Center for Brain Research and Brain-Machine Integration, School of Brain Science and Brain Medicine, Zhejiang University, Hangzhou, 310053, China. [email protected].

^# Contributed equally.

Abstract

Sensory modalities are important for survival but the molecular mechanisms remain challenging due to the polymodal functionality of sensory neurons. Here, we report the C. elegans outer labial lateral (OLL) sensilla sensory neurons respond to touch and cold. Mechanosensation of OLL neurons resulted in cell-autonomous mechanically-evoked Ca²⁺ transients and rapidly-adapting mechanoreceptor currents with a very short latency. Mechanotransduction of OLL neurons might be carried by a novel Na⁺ conductance channel, which is insensitive to amiloride. The bona fide mechano-gated Na⁺-selective degenerin/epithelial Na⁺ channels, TRP-4, TMC, and Piezo proteins are not involved in this mechanosensation. Interestingly, OLL neurons also mediated cold but not warm responses in a cell-autonomous manner. We further showed that the cold response of OLL neurons is not mediated by the cold receptor TRPA-1 or the temperature-sensitive glutamate receptor GLR-3. Thus, we propose the polymodal functionality of OLL neurons in mechanosensation and cold sensation.

Keywords: Cold receptor; Mechanosensation; OLL neurons; Polymodal sensory neuron; Sodium channel; Thermosensation.

MeSH terms

Animals
Caenorhabditis elegans Proteins* / genetics
Caenorhabditis elegans*
Mechanotransduction, Cellular
Sensory Receptor Cells
Touch

Substances

Caenorhabditis elegans Proteins