OSM-9 and an amiloride-sensitive channel, but not PKD-2, are involved in mechanosensation in C. elegans male ray neurons

Hu Zhang; Xiaomin Yue; Hankui Cheng; Xiaoyan Zhang; Yang Cai; Wenjuan Zou; Guifang Huang; Lufeng Cheng; Fang Ye; Lijun Kang

doi:10.1038/s41598-018-25542-1

OSM-9 and an amiloride-sensitive channel, but not PKD-2, are involved in mechanosensation in C. elegans male ray neurons

Sci Rep. 2018 May 8;8(1):7192. doi: 10.1038/s41598-018-25542-1.

Authors

Hu Zhang¹, Xiaomin Yue¹, Hankui Cheng¹, Xiaoyan Zhang¹, Yang Cai^{1

2}, Wenjuan Zou¹, Guifang Huang¹, Lufeng Cheng², Fang Ye³, Lijun Kang⁴

Affiliations

¹ Department of Neurobiology, Institute of Neuroscience, Key Laboratory of Medical Neurobiology of the Ministry of Health of China, Zhejiang University School of Medicine, Hangzhou, China.
² Department of Pharmacology, Basic Medical College, Xinjiang Medical University, Urumqi, China.
³ Department of Immunology, School of Preclinical Medicine, Guangxi Medical University, Nanning, China. [email protected].
⁴ Department of Neurobiology, Institute of Neuroscience, Key Laboratory of Medical Neurobiology of the Ministry of Health of China, Zhejiang University School of Medicine, Hangzhou, China. [email protected].

Abstract

Mechanotransduction is crucial for touch sensation, hearing, proprioception, and pain sensing. In C. elegans, male ray neurons have been implicated to be involved in the mechanosensation required for mating behavior. However, whether ray neurons directly sense mechanical stimulation is not yet known, and the underlying molecular mechanisms have not been identified. Using in vivo calcium imaging, we recorded the touch-induced calcium responses in male ray neurons. Our data demonstrated that ray neurons are sensitive to mechanical stimulation in a neurotransmitter-independent manner. PKD-2, a putative sensor component for both mechanosensation and chemosensation in male-specific neurons, was not required for the touch-induced calcium responses in RnB neurons, whereas the TRPV channel OSM-9 shaped the kinetics of the responses. We further showed that RnB-neuron mechanosensation is likely mediated by an amiloride-sensitive DEG/ENaC channel. These observations lay a foundation for better understanding the molecular mechanisms of mechanosensation.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Amiloride / pharmacology
Animals
Caenorhabditis elegans / drug effects
Caenorhabditis elegans / genetics*
Caenorhabditis elegans / metabolism
Caenorhabditis elegans Proteins / antagonists & inhibitors
Caenorhabditis elegans Proteins / genetics*
Caenorhabditis elegans Proteins / metabolism
Calcium / metabolism*
Epithelial Sodium Channel Blockers / pharmacology
Gene Expression Regulation
Male
Mechanotransduction, Cellular*
Membrane Proteins / antagonists & inhibitors
Membrane Proteins / genetics*
Membrane Proteins / metabolism
Molecular Imaging / methods
Nerve Tissue Proteins / antagonists & inhibitors
Nerve Tissue Proteins / genetics*
Nerve Tissue Proteins / metabolism
Neurons / cytology
Neurons / drug effects
Neurons / metabolism*
Sexual Behavior, Animal / physiology
TRPP Cation Channels / antagonists & inhibitors
TRPP Cation Channels / genetics
TRPP Cation Channels / metabolism
TRPV Cation Channels / antagonists & inhibitors
TRPV Cation Channels / genetics*
TRPV Cation Channels / metabolism
Touch / drug effects
Touch / physiology

Substances

Caenorhabditis elegans Proteins
Deg-1 protein, C elegans
Epithelial Sodium Channel Blockers
Membrane Proteins
Nerve Tissue Proteins
OSM-9 protein, C elegans
PKD-2 protein, C elegans
TRPP Cation Channels
TRPV Cation Channels
Amiloride
Calcium

Grants and funding

P40 OD010440/OD/NIH HHS/United States