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Supersulphides provide airway protection in viral and chronic lung diseases

Author

Listed:
  • Tetsuro Matsunaga

    (Tohoku University Graduate School of Medicine)

  • Hirohito Sano

    (Tohoku University Graduate School of Medicine)

  • Katsuya Takita

    (Tohoku University Graduate School of Medicine)

  • Masanobu Morita

    (Tohoku University Graduate School of Medicine)

  • Shun Yamanaka

    (Tohoku University Graduate School of Medicine)

  • Tomohiro Ichikawa

    (Tohoku University Graduate School of Medicine)

  • Tadahisa Numakura

    (Tohoku University Graduate School of Medicine)

  • Tomoaki Ida

    (Tohoku University Graduate School of Medicine)

  • Minkyung Jung

    (Tohoku University Graduate School of Medicine)

  • Seiryo Ogata

    (Tohoku University Graduate School of Medicine)

  • Sunghyeon Yoon

    (Tohoku University Graduate School of Medicine)

  • Naoya Fujino

    (Tohoku University Graduate School of Medicine)

  • Yorihiko Kyogoku

    (Tohoku University Graduate School of Medicine)

  • Yusaku Sasaki

    (Tohoku University Graduate School of Medicine)

  • Akira Koarai

    (Tohoku University Graduate School of Medicine)

  • Tsutomu Tamada

    (Tohoku University Graduate School of Medicine)

  • Atsuhiko Toyama

    (Shimadzu Corporation)

  • Takakazu Nakabayashi

    (Tohoku University)

  • Lisa Kageyama

    (Tohoku University)

  • Shigeru Kyuwa

    (The University of Tokyo)

  • Kenji Inaba

    (Tohoku University)

  • Satoshi Watanabe

    (Tohoku University)

  • Péter Nagy

    (National Institute of Oncology)

  • Tomohiro Sawa

    (Kumamoto University)

  • Hiroyuki Oshiumi

    (Kumamoto University)

  • Masakazu Ichinose

    (Tohoku University Graduate School of Medicine)

  • Mitsuhiro Yamada

    (Tohoku University Graduate School of Medicine)

  • Hisatoshi Sugiura

    (Tohoku University Graduate School of Medicine)

  • Fan-Yan Wei

    (Tohoku University)

  • Hozumi Motohashi

    (Tohoku University)

  • Takaaki Akaike

    (Tohoku University Graduate School of Medicine)

Abstract

Supersulphides are inorganic and organic sulphides with sulphur catenation with diverse physiological functions. Their synthesis is mainly mediated by mitochondrial cysteinyl-tRNA synthetase (CARS2) that functions as a principal cysteine persulphide synthase (CPERS). Here, we identify protective functions of supersulphides in viral airway infections (influenza and COVID-19), in aged lungs and in chronic lung diseases, including chronic obstructive pulmonary disease (COPD), idiopathic pulmonary fibrosis (IPF). We develop a method for breath supersulphur-omics and demonstrate that levels of exhaled supersulphides increase in people with COVID-19 infection and in a hamster model of SARS-CoV-2 infection. Lung damage and subsequent lethality that result from oxidative stress and inflammation in mouse models of COPD, IPF, and ageing were mitigated by endogenous supersulphides production by CARS2/CPERS or exogenous administration of the supersulphide donor glutathione trisulphide. We revealed a protective role of supersulphides in airways with various viral or chronic insults and demonstrated the potential of targeting supersulphides in lung disease.

Suggested Citation

  • Tetsuro Matsunaga & Hirohito Sano & Katsuya Takita & Masanobu Morita & Shun Yamanaka & Tomohiro Ichikawa & Tadahisa Numakura & Tomoaki Ida & Minkyung Jung & Seiryo Ogata & Sunghyeon Yoon & Naoya Fujin, 2023. "Supersulphides provide airway protection in viral and chronic lung diseases," Nature Communications, Nature, vol. 14(1), pages 1-25, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40182-4
    DOI: 10.1038/s41467-023-40182-4
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    References listed on IDEAS

    as
    1. Takaaki Akaike & Tomoaki Ida & Fan-Yan Wei & Motohiro Nishida & Yoshito Kumagai & Md. Morshedul Alam & Hideshi Ihara & Tomohiro Sawa & Tetsuro Matsunaga & Shingo Kasamatsu & Akiyuki Nishimura & Masano, 2017. "Cysteinyl-tRNA synthetase governs cysteine polysulfidation and mitochondrial bioenergetics," Nature Communications, Nature, vol. 8(1), pages 1-15, December.
    2. Mirjam Eberhardt & Maria Dux & Barbara Namer & Jan Miljkovic & Nada Cordasic & Christine Will & Tatjana I. Kichko & Jeanne de la Roche & Michael Fischer & Sebastián A. Suárez & Damian Bikiel & Karola , 2014. "H2S and NO cooperatively regulate vascular tone by activating a neuroendocrine HNO–TRPA1–CGRP signalling pathway," Nature Communications, Nature, vol. 5(1), pages 1-17, September.
    3. Zhenming Jin & Xiaoyu Du & Yechun Xu & Yongqiang Deng & Meiqin Liu & Yao Zhao & Bing Zhang & Xiaofeng Li & Leike Zhang & Chao Peng & Yinkai Duan & Jing Yu & Lin Wang & Kailin Yang & Fengjiang Liu & Re, 2020. "Structure of Mpro from SARS-CoV-2 and discovery of its inhibitors," Nature, Nature, vol. 582(7811), pages 289-293, June.
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    Cited by:

    1. Qi Cui & Meg Shieh & Tony W. Pan & Akiyuki Nishimura & Tetsuro Matsunaga & Shane S. Kelly & Shi Xu & Minkyung Jung & Seiryo Ogata & Masanobu Morita & Jun Yoshitake & Xiaoyan Chen & Jerome R. Robinson , 2024. "2H-Thiopyran-2-thione sulfine, a compound for converting H2S to HSOH/H2S2 and increasing intracellular sulfane sulfur levels," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

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