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Evidence for the involvement of ASIC3 in sensory mechanotransduction in proprioceptors

Author

Listed:
  • Shing-Hong Lin

    (Institute of Biomedical Sciences)

  • Yuan-Ren Cheng

    (Institute of Biomedical Sciences
    National Taiwan University)

  • Robert W. Banks

    (School of Biological and Biomedical Sciences, University of Durham)

  • Ming-Yuan Min

    (National Taiwan University)

  • Guy S. Bewick

    (School of Medicine, Medical Sciences and Nutrition, University of Aberdeen)

  • Chih-Cheng Chen

    (Institute of Biomedical Sciences
    National Taiwan University
    Taiwan Mouse Clinic-National Comprehensive Mouse Phenotyping and Drug Testing Center)

Abstract

Acid-sensing ion channel 3 (ASIC3) is involved in acid nociception, but its possible role in neurosensory mechanotransduction is disputed. We report here the generation of Asic3-knockout/eGFPf-knockin mice and subsequent characterization of heterogeneous expression of ASIC3 in the dorsal root ganglion (DRG). ASIC3 is expressed in parvalbumin (Pv+) proprioceptor axons innervating muscle spindles. We further generate a floxed allele of Asic3 (Asic3f/f) and probe the role of ASIC3 in mechanotransduction in neurite-bearing Pv+ DRG neurons through localized elastic matrix movements and electrophysiology. Targeted knockout of Asic3 disrupts spindle afferent sensitivity to dynamic stimuli and impairs mechanotransduction in Pv+ DRG neurons because of substrate deformation-induced neurite stretching, but not to direct neurite indentation. In behavioural tasks, global knockout (Asic3−/−) and Pv-Cre::Asic3f/f mice produce similar deficits in grid and balance beam walking tasks. We conclude that, at least in mouse, ASIC3 is a molecular determinant contributing to dynamic mechanosensitivity in proprioceptors.

Suggested Citation

  • Shing-Hong Lin & Yuan-Ren Cheng & Robert W. Banks & Ming-Yuan Min & Guy S. Bewick & Chih-Cheng Chen, 2016. "Evidence for the involvement of ASIC3 in sensory mechanotransduction in proprioceptors," Nature Communications, Nature, vol. 7(1), pages 1-15, September.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms11460
    DOI: 10.1038/ncomms11460
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    Cited by:

    1. Rangjuan Cao & Peng Chen & Hongsheng Wang & Hongyang Jing & Hongsheng Zhang & Guanglin Xing & Bin Luo & Jinxiu Pan & Zheng Yu & Wen-Cheng Xiong & Lin Mei, 2023. "Intrafusal-fiber LRP4 for muscle spindle formation and maintenance in adult and aged animals," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Martina Nicoletti & Letizia Chiodo & Alessandro Loppini, 2021. "Biophysics and Modeling of Mechanotransduction in Neurons: A Review," Mathematics, MDPI, vol. 9(4), pages 1-32, February.
    3. Chen Huang & Pei-Yi Sun & Yiming Jiang & Yuandong Liu & Zhichao Liu & Shao-Ling Han & Bao-Shan Wang & Yong-Xin Huang & An-Ran Ren & Jian-Fei Lu & Qin Jiang & Ying Li & Michael X. Zhu & Zhirong Yao & Y, 2024. "Sensory ASIC3 channel exacerbates psoriatic inflammation via a neurogenic pathway in female mice," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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