A non-canonical cGAS–STING–PERK pathway facilitates the translational program critical for senescence and organ fibrosis
Innate DNA sensing via the cyclic GMP-AMP synthase–stimulator of interferon genes (cGAS–STING) mechanism surveys microbial invasion and cellular damage and thus participates in various human infectious diseases, autoimmune diseases and cancers. However, how DNA sensing rapidly and adaptively shapes...
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| Published in | Nature cell biology Vol. 24; no. 5; pp. 766 - 782 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.05.2022
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Innate DNA sensing via the cyclic GMP-AMP synthase–stimulator of interferon genes (cGAS–STING) mechanism surveys microbial invasion and cellular damage and thus participates in various human infectious diseases, autoimmune diseases and cancers. However, how DNA sensing rapidly and adaptively shapes cellular physiology is incompletely known. Here we identify the STING–PKR-like endoplasmic reticulum kinase (PERK)–eIF2α pathway, a previously unknown cGAS–STING mechanism, enabling an innate immunity control of cap-dependent messenger RNA translation. Upon cGAMP binding, STING at the ER binds and directly activates the ER-located kinase PERK via their intracellular domains, which precedes TBK1–IRF3 activation and is irrelevant to the unfolded protein response. The activated PERK phosphorylates eIF2α, forming an inflammatory- and survival-preferred translation program. Notably, this STING–PERK–eIF2α pathway is evolutionarily primitive and physiologically critical to cellular senescence and organ fibrosis. Pharmacologically or genetically targeting this non-canonical cGAS–STING pathway attenuated lung and kidney fibrosis. Collectively, the findings identify an alternative innate immune pathway and its critical role in organ fibrosis, report an innate immunity-directed translation program and suggest the therapeutic potential for targeting the STING–PERK pathway in treating fibrotic diseases.
Zhang et al. report that a non-canonical cGAS–STING pathway activates PERK–eIF2α to elaborate cap-dependent mRNA translation and contributes to senescence and fibrosis. |
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| AbstractList | Innate DNA sensing via the cyclic GMP-AMP synthase-stimulator of interferon genes (cGAS-STING) mechanism surveys microbial invasion and cellular damage and thus participates in various human infectious diseases, autoimmune diseases and cancers. However, how DNA sensing rapidly and adaptively shapes cellular physiology is incompletely known. Here we identify the STING-PKR-like endoplasmic reticulum kinase (PERK)-eIF2α pathway, a previously unknown cGAS-STING mechanism, enabling an innate immunity control of cap-dependent messenger RNA translation. Upon cGAMP binding, STING at the ER binds and directly activates the ER-located kinase PERK via their intracellular domains, which precedes TBK1-IRF3 activation and is irrelevant to the unfolded protein response. The activated PERK phosphorylates eIF2α, forming an inflammatory- and survival-preferred translation program. Notably, this STING-PERK-eIF2α pathway is evolutionarily primitive and physiologically critical to cellular senescence and organ fibrosis. Pharmacologically or genetically targeting this non-canonical cGAS-STING pathway attenuated lung and kidney fibrosis. Collectively, the findings identify an alternative innate immune pathway and its critical role in organ fibrosis, report an innate immunity-directed translation program and suggest the therapeutic potential for targeting the STING-PERK pathway in treating fibrotic diseases. Innate DNA sensing via the cyclic GMP-AMP synthase–stimulator of interferon genes (cGAS–STING) mechanism surveys microbial invasion and cellular damage and thus participates in various human infectious diseases, autoimmune diseases and cancers. However, how DNA sensing rapidly and adaptively shapes cellular physiology is incompletely known. Here we identify the STING–PKR-like endoplasmic reticulum kinase (PERK)–eIF2α pathway, a previously unknown cGAS–STING mechanism, enabling an innate immunity control of cap-dependent messenger RNA translation. Upon cGAMP binding, STING at the ER binds and directly activates the ER-located kinase PERK via their intracellular domains, which precedes TBK1–IRF3 activation and is irrelevant to the unfolded protein response. The activated PERK phosphorylates eIF2α, forming an inflammatory- and survival-preferred translation program. Notably, this STING–PERK–eIF2α pathway is evolutionarily primitive and physiologically critical to cellular senescence and organ fibrosis. Pharmacologically or genetically targeting this non-canonical cGAS–STING pathway attenuated lung and kidney fibrosis. Collectively, the findings identify an alternative innate immune pathway and its critical role in organ fibrosis, report an innate immunity-directed translation program and suggest the therapeutic potential for targeting the STING–PERK pathway in treating fibrotic diseases.Zhang et al. report that a non-canonical cGAS–STING pathway activates PERK–eIF2α to elaborate cap-dependent mRNA translation and contributes to senescence and fibrosis. Innate DNA sensing via the cyclic GMP-AMP synthase–stimulator of interferon genes (cGAS–STING) mechanism surveys microbial invasion and cellular damage and thus participates in various human infectious diseases, autoimmune diseases and cancers. However, how DNA sensing rapidly and adaptively shapes cellular physiology is incompletely known. Here we identify the STING–PKR-like endoplasmic reticulum kinase (PERK)–eIF2α pathway, a previously unknown cGAS–STING mechanism, enabling an innate immunity control of cap-dependent messenger RNA translation. Upon cGAMP binding, STING at the ER binds and directly activates the ER-located kinase PERK via their intracellular domains, which precedes TBK1–IRF3 activation and is irrelevant to the unfolded protein response. The activated PERK phosphorylates eIF2α, forming an inflammatory- and survival-preferred translation program. Notably, this STING–PERK–eIF2α pathway is evolutionarily primitive and physiologically critical to cellular senescence and organ fibrosis. Pharmacologically or genetically targeting this non-canonical cGAS–STING pathway attenuated lung and kidney fibrosis. Collectively, the findings identify an alternative innate immune pathway and its critical role in organ fibrosis, report an innate immunity-directed translation program and suggest the therapeutic potential for targeting the STING–PERK pathway in treating fibrotic diseases. Zhang et al. report that a non-canonical cGAS–STING pathway activates PERK–eIF2α to elaborate cap-dependent mRNA translation and contributes to senescence and fibrosis. Innate DNA sensing via the cyclic GMP-AMP synthase-stimulator of interferon genes (cGAS-STING) mechanism surveys microbial invasion and cellular damage and thus participates in various human infectious diseases, autoimmune diseases and cancers. However, how DNA sensing rapidly and adaptively shapes cellular physiology is incompletely known. Here we identify the STING-PKR-like endoplasmic reticulum kinase (PERK)-eIF2α pathway, a previously unknown cGAS-STING mechanism, enabling an innate immunity control of cap-dependent messenger RNA translation. Upon cGAMP binding, STING at the ER binds and directly activates the ER-located kinase PERK via their intracellular domains, which precedes TBK1-IRF3 activation and is irrelevant to the unfolded protein response. The activated PERK phosphorylates eIF2α, forming an inflammatory- and survival-preferred translation program. Notably, this STING-PERK-eIF2α pathway is evolutionarily primitive and physiologically critical to cellular senescence and organ fibrosis. Pharmacologically or genetically targeting this non-canonical cGAS-STING pathway attenuated lung and kidney fibrosis. Collectively, the findings identify an alternative innate immune pathway and its critical role in organ fibrosis, report an innate immunity-directed translation program and suggest the therapeutic potential for targeting the STING-PERK pathway in treating fibrotic diseases.Innate DNA sensing via the cyclic GMP-AMP synthase-stimulator of interferon genes (cGAS-STING) mechanism surveys microbial invasion and cellular damage and thus participates in various human infectious diseases, autoimmune diseases and cancers. However, how DNA sensing rapidly and adaptively shapes cellular physiology is incompletely known. Here we identify the STING-PKR-like endoplasmic reticulum kinase (PERK)-eIF2α pathway, a previously unknown cGAS-STING mechanism, enabling an innate immunity control of cap-dependent messenger RNA translation. Upon cGAMP binding, STING at the ER binds and directly activates the ER-located kinase PERK via their intracellular domains, which precedes TBK1-IRF3 activation and is irrelevant to the unfolded protein response. The activated PERK phosphorylates eIF2α, forming an inflammatory- and survival-preferred translation program. Notably, this STING-PERK-eIF2α pathway is evolutionarily primitive and physiologically critical to cellular senescence and organ fibrosis. Pharmacologically or genetically targeting this non-canonical cGAS-STING pathway attenuated lung and kidney fibrosis. Collectively, the findings identify an alternative innate immune pathway and its critical role in organ fibrosis, report an innate immunity-directed translation program and suggest the therapeutic potential for targeting the STING-PERK pathway in treating fibrotic diseases. |
| Author | Ouyang, Songying Feng, Xin-Hua Mei, Chen Liang, Tingbo Zhu, Yezhang Zhang, Qian Shen, Li Zhang, Dan Chen, Shasha Liu, Yutong Chen, Chen Liu, Shengduo Xi, Ying Xu, Pinglong Guan, Hongxing Liao, Zhiyong |
| Author_xml | – sequence: 1 givenname: Dan orcidid: 0000-0002-9594-4818 surname: Zhang fullname: Zhang, Dan organization: The MOE Key Laboratory of Biosystems Homeostasis & Protection and Zhejiang Provincial Key Laboratory of Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University, Department of Hepatobiliary and Pancreatic Surgery and Zhejiang Provincial Key Laboratory of Pancreatic Disease, The First Affiliated Hospital, Zhejiang University School of Medicine – sequence: 2 givenname: Yutong surname: Liu fullname: Liu, Yutong organization: The MOE Key Laboratory of Biosystems Homeostasis & Protection and Zhejiang Provincial Key Laboratory of Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University – sequence: 3 givenname: Yezhang surname: Zhu fullname: Zhu, Yezhang organization: The MOE Key Laboratory of Biosystems Homeostasis & Protection and Zhejiang Provincial Key Laboratory of Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University – sequence: 4 givenname: Qian surname: Zhang fullname: Zhang, Qian organization: The MOE Key Laboratory of Biosystems Homeostasis & Protection and Zhejiang Provincial Key Laboratory of Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University, Department of Hepatobiliary and Pancreatic Surgery and Zhejiang Provincial Key Laboratory of Pancreatic Disease, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou Global Scientific and Technological Innovation Center, Zhejiang University (HIC-ZJU), Cancer Center, Zhejiang University – sequence: 5 givenname: Hongxing surname: Guan fullname: Guan, Hongxing organization: The Key Laboratory of Innate Immune Biology of Fujian Province, Biomedical Research Center of South China, College of Life Sciences, Fujian Normal University – sequence: 6 givenname: Shengduo surname: Liu fullname: Liu, Shengduo organization: The MOE Key Laboratory of Biosystems Homeostasis & Protection and Zhejiang Provincial Key Laboratory of Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University, Hangzhou Global Scientific and Technological Innovation Center, Zhejiang University (HIC-ZJU), Cancer Center, Zhejiang University – sequence: 7 givenname: Shasha surname: Chen fullname: Chen, Shasha organization: The MOE Key Laboratory of Biosystems Homeostasis & Protection and Zhejiang Provincial Key Laboratory of Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University, Zhejiang Provincial Key Laboratory for Water Environment and Marine Biological Resources Protection, College of Life and Environmental Science, Wenzhou University – sequence: 8 givenname: Chen surname: Mei fullname: Mei, Chen organization: The MOE Key Laboratory of Biosystems Homeostasis & Protection and Zhejiang Provincial Key Laboratory of Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University – sequence: 9 givenname: Chen surname: Chen fullname: Chen, Chen organization: The MOE Key Laboratory of Biosystems Homeostasis & Protection and Zhejiang Provincial Key Laboratory of Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University – sequence: 10 givenname: Zhiyong surname: Liao fullname: Liao, Zhiyong organization: Zhejiang Provincial Key Laboratory for Water Environment and Marine Biological Resources Protection, College of Life and Environmental Science, Wenzhou University – sequence: 11 givenname: Ying surname: Xi fullname: Xi, Ying organization: School of Life Science and Technology, ShanghaiTech University – sequence: 12 givenname: Songying orcidid: 0000-0002-1120-1524 surname: Ouyang fullname: Ouyang, Songying organization: The Key Laboratory of Innate Immune Biology of Fujian Province, Biomedical Research Center of South China, College of Life Sciences, Fujian Normal University – sequence: 13 givenname: Xin-Hua surname: Feng fullname: Feng, Xin-Hua organization: The MOE Key Laboratory of Biosystems Homeostasis & Protection and Zhejiang Provincial Key Laboratory of Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University, Cancer Center, Zhejiang University – sequence: 14 givenname: Tingbo orcidid: 0000-0003-0143-3353 surname: Liang fullname: Liang, Tingbo email: liangtingbo@zju.edu.cn organization: Department of Hepatobiliary and Pancreatic Surgery and Zhejiang Provincial Key Laboratory of Pancreatic Disease, The First Affiliated Hospital, Zhejiang University School of Medicine, Cancer Center, Zhejiang University – sequence: 15 givenname: Li orcidid: 0000-0002-5696-2191 surname: Shen fullname: Shen, Li email: li_shen@zju.edu.cn organization: The MOE Key Laboratory of Biosystems Homeostasis & Protection and Zhejiang Provincial Key Laboratory of Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University – sequence: 16 givenname: Pinglong orcidid: 0000-0001-7726-5443 surname: Xu fullname: Xu, Pinglong email: xupl@zju.edu.cn organization: The MOE Key Laboratory of Biosystems Homeostasis & Protection and Zhejiang Provincial Key Laboratory of Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University, Department of Hepatobiliary and Pancreatic Surgery and Zhejiang Provincial Key Laboratory of Pancreatic Disease, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou Global Scientific and Technological Innovation Center, Zhejiang University (HIC-ZJU), Cancer Center, Zhejiang University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35501370$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | The Author(s), under exclusive licence to Springer Nature Limited 2022 2022. The Author(s), under exclusive licence to Springer Nature Limited. The Author(s), under exclusive licence to Springer Nature Limited 2022. |
| Copyright_xml | – notice: The Author(s), under exclusive licence to Springer Nature Limited 2022 – notice: 2022. The Author(s), under exclusive licence to Springer Nature Limited. – notice: The Author(s), under exclusive licence to Springer Nature Limited 2022. |
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| DOI | 10.1038/s41556-022-00894-z |
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| Title | A non-canonical cGAS–STING–PERK pathway facilitates the translational program critical for senescence and organ fibrosis |
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