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GSNOR negatively regulates the NLRP3 inflammasome via S-nitrosation of MAPK14

Cellular & Molecular Immunology (2024)Cite this article

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Abstract

Hyperactivation of the NLRP3 inflammasome has been implicated in the pathogenesis of numerous diseases. However, the precise molecular mechanisms that modulate the transcriptional regulation of NLRP3 remain largely unknown. In this study, we demonstrated that S-nitrosoglutathione reductase (GSNOR) deficiency in macrophages leads to significant increases in the Nlrp3 and Il-1β expression levels and interleukin-1β (IL-1β) secretion in response to NLRP3 inflammasome stimulation. Furthermore, in vivo experiments utilizing Gsnor−/− mice revealed increased disease severity in both lipopolysaccharide (LPS)-induced septic shock and dextran sodium sulfate (DSS)-induced colitis models. Additionally, we showed that both LPS-induced septic shock and DSS-induced colitis were ameliorated in Gsnor−/− Nlrp3−/− double-knockout (DKO) mice. Mechanistically, GSNOR deficiency increases the S-nitrosation of mitogen-activated protein kinase 14 (MAPK14) at the Cys211 residue and augments MAPK14 kinase activity, thereby promoting Nlrp3 and Il-1β transcription and stimulating NLRP3 inflammasome activity. Our findings suggested that GSNOR is a regulator of the NLRP3 inflammasome and that reducing the level of S-nitrosylated MAPK14 may constitute an effective strategy for alleviating diseases associated with NLRP3-mediated inflammation.

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Acknowledgements

The authors thank Prof. Rongbin Zhou for sharing the Nlrp3−/− mice. We are grateful to Dr. Ian Logan for the helpful comments and language editing of this manuscript. This study was supported by Yunnan Fundamental Research Project (202305AH340006), the National Natural Science Foundation of China (32201018), the Basic Research Program and Key Project of Yunnan Province (202301AW070013 and 202003AD150009), and the Youth Innovation Promotion Association (2023403).

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Authors and Affiliations

  1. Key Laboratory of Genetic Evolution & Animal Models, and Key Laboratory of Animal Models & Human Disease Mechanisms of Yunnan Province, Kunming Institute of Zoology, Chinese Academy of Sciences, 650201, Kunming, Yunnan, China

    Qianjin Liu, Lijin Jiao, Mao-Sen Ye, Zhiyu Ma, Jinsong Yu, Ling-Yan Su, Wei-Yin Zou, Lu-Xiu Yang & Yong-Gang Yao

  2. Kunming College of Life Science, University of Chinese Academy of Sciences, 650204, Kunming, Yunnan, China

    Zhiyu Ma, Wei-Yin Zou & Yong-Gang Yao

  3. Key Laboratory of Biomacromolecules (CAS), National Laboratory of Biomacromolecules, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, 100101, Beijing, China

    Chang Chen

  4. KIZ/CUHK Joint Laboratory of Bioresources and Molecular Research in Common Diseases, Kunming Institute of Zoology, Chinese Academy of Sciences, 650201, Kunming, Yunnan, China

    Yong-Gang Yao

  5. National Research Facility for Phenotypic & Genetic Analysis of Model Animals (Primate Facility), National Resource Center for Non-Human Primates, Kunming Institute of Zoology, Chinese Academy of Sciences, 650201, Kunming, China

    Yong-Gang Yao

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  1. Qianjin Liu
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Contributions

Yong-Gang Yao and Qianjin Liu conceived and designed the experiments. Qianjin Liu, Lijin Jiao, Zhiyu Ma, Jinsong Yu, Ling-Yan Su, Wei-Yin Zou and Lu-Xiu Yang performed the cellular and mouse experiments. Mao-Sen Ye performed the RNA-seq data analysis. Chang Chen provided mouse lines and provided constructive suggestions. Yong-Gang Yao and Qianjin Liu wrote the manuscript. All authors reviewed the content and approved the final version for publication.

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Correspondence to Qianjin Liu or Yong-Gang Yao.

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Liu, Q., Jiao, L., Ye, MS. et al. GSNOR negatively regulates the NLRP3 inflammasome via S-nitrosation of MAPK14. Cell Mol Immunol (2024). https://doi.org/10.1038/s41423-024-01155-9

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