Cited by 261interferon and immune responsesDNA and Nucleic Acid ChemistryImmune Response and Inflammation

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The molecular basis of tight nuclear tethering and inactivation of cGAS

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Zhao, Baoyu, Xu, Pengbiao, Rowlett, Chesley M., Jing, Tao, Shinde, Omkar, Lei, Yuanjiu, West, A. Phillip, Liu, Wenshe Ray, Li, Pingwei·2020·Nature

DOI 10.1038/s41586-020-2749-zPMC PMC7704945

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Abstract

Nucleic acids derived from pathogens induce potent innate immune responses1–6. Cyclic GMP–AMP synthase (cGAS) is a double-stranded DNA sensor that catalyses the synthesis of the cyclic dinucleotide cyclic GMP–AMP, which mediates the induction of type I interferons through the STING–TBK1–IRF3 signalling axis7–11. cGAS was previously thought to not react with self DNA owing to its cytosolic localization2,12,13; however, recent studies have shown that cGAS is localized mostly in the nucleus and has low activity as a result of tight nuclear tethering14–18. Here we show that cGAS binds to nucleosomes with nanomolar affinity and that nucleosome binding potently inhibits its catalytic activity. To elucidate the molecular basis of cGAS inactivation by nuclear tethering, we determined the structure of mouse cGAS bound to human nucleosome by cryo-electron microscopy. The structure shows that cGAS binds to a negatively charged acidic patch formed by histones H2A and H2B via its second DNA-binding site19. High-affinity nucleosome binding blocks double-stranded DNA binding and maintains cGAS in an inactive conformation. Mutations of cGAS that disrupt nucleosome binding alter cGAS-mediated signalling in cells. Structural studies show that cyclic GMP–AMP synthase binds to nucleosomes through its DNA-binding site, which maintains it in an inactive conformation and prevents self-DNA binding.

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Self-citation
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Self-citation
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“Strikingly, independent of its enzymatic activity, nuclear cGAS physically impedes the recruitment of homologous recombination (Liu et al., 2018; Zhao et al., 2020).”
Self-citation
The cGAS/STING pathway in cancer: translating innate DNA sensing into therapeutic potential
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Authors: Zhao, B., Xu, P., Rowlett, C. M., Jing, T., Shinde, O., Lei, Y., West, A. P., Liu, W. R., & Li, P.
Affiliations: Texas A&M University (US)
Texas A&M Health Science Center (US)
Corresponding author: Liu, Wenshe Ray
Li, Pingwei
ORCID: Xu, Pengbiao
Rowlett, Chesley M.
Jing, Tao
Shinde, Omkar
Lei, Yuanjiu
West, A. Phillip
Liu, Wenshe Ray
Li, Pingwei
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2020-09-10
Volume: 587
Issue: 7835
Pages: 673-677
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/s41586-020-2749-z
PMC: PMC7704945
OpenAlex: W3083971280
Semantic Scholar: e3ee6a242101a668250c6be62a691a28b1ea9829
Cited by: 261
References: 23
Citations by year: 2026: 37 · 2025: 38 · 2024: 51 · 2023: 31 · 2022: 39 · 2021: 56 · 2020: 8
FWCI: 11.82
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: National Heart, Lung, and Blood Institute (R01HL148153)
National Institute of General Medical Sciences (R01GM121584, R01GM127575)
National Institute of Allergy and Infectious Diseases (R01AI145287)
Topics: Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords: cGAS, nucleosome binding, nucleic acid sensing, type I interferon, double-stranded DNA binding, protein-DNA complex structure, innate immunity
MeSH terms: Cyclic Guanosine Monophosphate-Adenosine Monophosphate Synthase, Animals, Cell Line, DNA, Humans, Models, Molecular, Mutation, Nucleosomes, Nucleotidyltransferases, Protein Binding, Signal Transduction, Catalytic Domain, Cryoelectron Microscopy, Mice, Biocatalysis

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The molecular basis of tight nuclear tethering and inactivation of cGAS

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