A conserved PLPLRT/SD motif of STING mediates the recruitment and activation of TBK1

Nucleic acids from bacteria or viruses induce potent immune responses in infected cells 1 – 4 . The detection of pathogen-derived nucleic acids is a central strategy by which the host senses infection and initiates protective immune responses 5 , 6 . Cyclic GMP-AMP synthase (cGAS) is a double-strand...

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Published inNature (London) Vol. 569; no. 7758; pp. 718 - 722
Main Authors Zhao, Baoyu, Du, Fenglei, Xu, Pengbiao, Shu, Chang, Sankaran, Banumathi, Bell, Samantha L., Liu, Mengmeng, Lei, Yuanjiu, Gao, Xinsheng, Fu, Xiaofeng, Zhu, Fanxiu, Liu, Yang, Laganowsky, Arthur, Zheng, Xueyun, Ji, Jun-Yuan, West, A. Phillip, Watson, Robert O., Li, Pingwei
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.05.2019
Nature Publishing Group
Subjects
14/19
631/250/262
631/535/1258
631/535/1266
82/1
82/103
82/16
82/29
82/58
82/80
82/83
Amino Acid Motifs
Analysis
Antagonists
Autoimmune diseases
BASIC BIOLOGICAL SCIENCES
Chemical synthesis
Conserved Sequence
Crystallography, X-Ray
Cyclic GMP
EF hand proteins
Enzyme Activation
HEK293 Cells
Humanities and Social Sciences
Humans
Hydrogen bonds
Immune response
Influence
Interferon
Interferon regulatory factor 3
Interferon-beta - metabolism
Letter
Membrane Proteins - chemistry
Membrane Proteins - genetics
Membrane Proteins - metabolism
Models, Molecular
multidisciplinary
Mutation
Nucleic acids
Nucleotides, Cyclic - metabolism
Oligomerization
Peptides
Phosphorylation
Protein Binding
Protein kinases
Protein Serine-Threonine Kinases - metabolism
Science
Science (multidisciplinary)
Signal Transduction
β-Interferon
Online AccessGet full text

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Abstract Nucleic acids from bacteria or viruses induce potent immune responses in infected cells 1 – 4 . The detection of pathogen-derived nucleic acids is a central strategy by which the host senses infection and initiates protective immune responses 5 , 6 . Cyclic GMP-AMP synthase (cGAS) is a double-stranded DNA sensor 7 , 8 . It catalyses the synthesis of cyclic GMP-AMP (cGAMP) 9 – 12 , which stimulates the induction of type I interferons through the STING–TBK1–IRF-3 signalling axis 13 – 15 . STING oligomerizes after binding of cGAMP, leading to the recruitment and activation of the TBK1 kinase 8 , 16 . The IRF-3 transcription factor is then recruited to the signalling complex and activated by TBK1 8 , 17 – 20 . Phosphorylated IRF-3 translocates to the nucleus and initiates the expression of type I interferons 21 . However, the precise mechanisms that govern activation of STING by cGAMP and subsequent activation of TBK1 by STING remain unclear. Here we show that a conserved PLPLRT/SD motif within the C-terminal tail of STING mediates the recruitment and activation of TBK1. Crystal structures of TBK1 bound to STING reveal that the PLPLRT/SD motif binds to the dimer interface of TBK1. Cell-based studies confirm that the direct interaction between TBK1 and STING is essential for induction of IFNβ after cGAMP stimulation. Moreover, we show that full-length STING oligomerizes after it binds cGAMP, and highlight this as an essential step in the activation of STING-mediated signalling. These findings provide a structural basis for the development of STING agonists and antagonists for the treatment of cancer and autoimmune disorders. A molecular model of STING-mediated signalling is proposed, as structural analysis identifies a crucial motif for the binding of TBK1 to STING, and a separate model involved in IRF-3 binding.
AbstractList Nucleic acids from bacteria or viruses induce potent immune responses in infected cells.sup.1-4. The detection of pathogen-derived nucleic acids is a central strategy by which the host senses infection and initiates protective immune responses.sup.5,6. Cyclic GMP-AMP synthase (cGAS) is a double-stranded DNA sensor.sup.7,8. It catalyses the synthesis of cyclic GMP-AMP (cGAMP).sup.9-12, which stimulates the induction of type I interferons through the STING-TBK1-IRF-3 signalling axis.sup.13-15. STING oligomerizes after binding of cGAMP, leading to the recruitment and activation of the TBK1 kinase.sup.8,16. The IRF-3 transcription factor is then recruited to the signalling complex and activated by TBK1.sup.8,17-20. Phosphorylated IRF-3 translocates to the nucleus and initiates the expression of type I interferons.sup.21. However, the precise mechanisms that govern activation of STING by cGAMP and subsequent activation of TBK1 by STING remain unclear. Here we show that a conserved PLPLRT/SD motif within the C-terminal tail of STING mediates the recruitment and activation of TBK1. Crystal structures of TBK1 bound to STING reveal that the PLPLRT/SD motif binds to the dimer interface of TBK1. Cell-based studies confirm that the direct interaction between TBK1 and STING is essential for induction of IFN[beta] after cGAMP stimulation. Moreover, we show that full-length STING oligomerizes after it binds cGAMP, and highlight this as an essential step in the activation of STING-mediated signalling. These findings provide a structural basis for the development of STING agonists and antagonists for the treatment of cancer and autoimmune disorders. A molecular model of STING-mediated signalling is proposed, as structural analysis identifies a crucial motif for the binding of TBK1 to STING, and a separate model involved in IRF-3 binding.
Nucleic acids from bacteria or viruses induce potent immune responses in infected cells.sup.1-4. The detection of pathogen-derived nucleic acids is a central strategy by which the host senses infection and initiates protective immune responses.sup.5,6. Cyclic GMP-AMP synthase (cGAS) is a double-stranded DNA sensor.sup.7,8. It catalyses the synthesis of cyclic GMP-AMP (cGAMP).sup.9-12, which stimulates the induction of type I interferons through the STING-TBK1-IRF-3 signalling axis.sup.13-15. STING oligomerizes after binding of cGAMP, leading to the recruitment and activation of the TBK1 kinase.sup.8,16. The IRF-3 transcription factor is then recruited to the signalling complex and activated by TBK1.sup.8,17-20. Phosphorylated IRF-3 translocates to the nucleus and initiates the expression of type I interferons.sup.21. However, the precise mechanisms that govern activation of STING by cGAMP and subsequent activation of TBK1 by STING remain unclear. Here we show that a conserved PLPLRT/SD motif within the C-terminal tail of STING mediates the recruitment and activation of TBK1. Crystal structures of TBK1 bound to STING reveal that the PLPLRT/SD motif binds to the dimer interface of TBK1. Cell-based studies confirm that the direct interaction between TBK1 and STING is essential for induction of IFN[beta] after cGAMP stimulation. Moreover, we show that full-length STING oligomerizes after it binds cGAMP, and highlight this as an essential step in the activation of STING-mediated signalling. These findings provide a structural basis for the development of STING agonists and antagonists for the treatment of cancer and autoimmune disorders.
Nucleic acids from bacteria or viruses induce potent immune responses in infected cells . The detection of pathogen-derived nucleic acids is a central strategy by which the host senses infection and initiates protective immune responses . Cyclic GMP-AMP synthase (cGAS) is a double-stranded DNA sensor . It catalyses the synthesis of cyclic GMP-AMP (cGAMP) , which stimulates the induction of type I interferons through the STING-TBK1-IRF-3 signalling axis . STING oligomerizes after binding of cGAMP, leading to the recruitment and activation of the TBK1 kinase . The IRF-3 transcription factor is then recruited to the signalling complex and activated by TBK1 . Phosphorylated IRF-3 translocates to the nucleus and initiates the expression of type I interferons . However, the precise mechanisms that govern activation of STING by cGAMP and subsequent activation of TBK1 by STING remain unclear. Here we show that a conserved PLPLRT/SD motif within the C-terminal tail of STING mediates the recruitment and activation of TBK1. Crystal structures of TBK1 bound to STING reveal that the PLPLRT/SD motif binds to the dimer interface of TBK1. Cell-based studies confirm that the direct interaction between TBK1 and STING is essential for induction of IFNβ after cGAMP stimulation. Moreover, we show that full-length STING oligomerizes after it binds cGAMP, and highlight this as an essential step in the activation of STING-mediated signalling. These findings provide a structural basis for the development of STING agonists and antagonists for the treatment of cancer and autoimmune disorders.
Nucleic acids from bacteria or viruses induce potent immune responses in infected cells1-4. The detection of pathogen-derived nucleic acids is a central strategy by which the host senses infection and initiates protective immune responses5,6. Cyclic GMP-AMP synthase (cGAS) is a double-stranded DNA sensor7,8. It catalyses the synthesis of cyclic GMP-AMP (cGAMP)9-12, which stimulates the induction of type I interferons through the STING-TBK1-IRF-3 signalling axis13-15. STING oligomerizes after binding of cGAMP, leading to the recruitment and activation of the TBK1 kinase8,16. The IRF-3 transcription factor is then recruited to the signalling complex and activated by TBK18,17-20. Phosphorylated IRF-3 translocates to the nucleus and initiates the expression of type I interferons21. However, the precise mechanisms that govern activation of STING by cGAMP and subsequent activation of TBK1 by STING remain unclear. Here we show that a conserved PLPLRT/SD motif within the C-terminal tail of STING mediates the recruitment and activation of TBK1. Crystal structures of TBK1 bound to STING reveal that the PLPLRT/SD motif binds to the dimer interface of TBK1. Cell-based studies confirm that the direct interaction between TBK1 and STING is essential for induction of IFNβ after cGAMP stimulation. Moreover, we show that full-length STING oligomerizes after it binds cGAMP, and highlight this as an essential step in the activation of STING-mediated signalling. These findings provide a structural basis for the development of STING agonists and antagonists for the treatment of cancer and autoimmune disorders.Nucleic acids from bacteria or viruses induce potent immune responses in infected cells1-4. The detection of pathogen-derived nucleic acids is a central strategy by which the host senses infection and initiates protective immune responses5,6. Cyclic GMP-AMP synthase (cGAS) is a double-stranded DNA sensor7,8. It catalyses the synthesis of cyclic GMP-AMP (cGAMP)9-12, which stimulates the induction of type I interferons through the STING-TBK1-IRF-3 signalling axis13-15. STING oligomerizes after binding of cGAMP, leading to the recruitment and activation of the TBK1 kinase8,16. The IRF-3 transcription factor is then recruited to the signalling complex and activated by TBK18,17-20. Phosphorylated IRF-3 translocates to the nucleus and initiates the expression of type I interferons21. However, the precise mechanisms that govern activation of STING by cGAMP and subsequent activation of TBK1 by STING remain unclear. Here we show that a conserved PLPLRT/SD motif within the C-terminal tail of STING mediates the recruitment and activation of TBK1. Crystal structures of TBK1 bound to STING reveal that the PLPLRT/SD motif binds to the dimer interface of TBK1. Cell-based studies confirm that the direct interaction between TBK1 and STING is essential for induction of IFNβ after cGAMP stimulation. Moreover, we show that full-length STING oligomerizes after it binds cGAMP, and highlight this as an essential step in the activation of STING-mediated signalling. These findings provide a structural basis for the development of STING agonists and antagonists for the treatment of cancer and autoimmune disorders.
Nucleic acids from bacteria or viruses induce potent immune responses in infected cells1-4. The detection of pathogen-derived nucleic acids is a central strategy by which the host senses infection and initiates protective immune responses5,6. Cyclic GMP-AMP synthase (cGAS) is a double-stranded DNA sensor7,8. It catalyses the synthesis of cyclic GMP-AMP (cGAMP)9-12, which stimulates the induction of type I interferons through the STING-TBK1-IRF-3 signalling axis13-15. STING oligomerizes after binding of cGAMP, leading to the recruitment and activation of the TBK1 kinase8,16. The IRF-3 transcription factor is then recruited to the signalling complex and activated by TBK18,17-20. Phosphorylated IRF-3 translocates to the nucleus and initiates the expression of type I interferons21. However, the precise mechanisms that govern activation of STING by cGAMP and subsequent activation of TBK1 by STING remain unclear. Here we show that a conserved PLPLRT/SD motif within the C-terminal tail of STING mediates the recruitment and activation of TBK1. Crystal structures of TBK1 bound to STING reveal that the PLPLRT/SD motif binds to the dimer interface of TBK1. Cell-based studies confirm that the direct interaction between TBK1 and STING is essential for induction of IFNß after cGAMP stimulation. Moreover, we show that full-length STING oligomerizes after it binds cGAMP, and highlight this as an essential step in the activation of STING-mediated signalling. These findings provide a structural basis for the development of STING agonists and antagonists for the treatment of cancer and autoimmune disorders.
Nucleic acids from bacteria or viruses induce potent immune responses in infected cells 1 – 4 . The detection of pathogen-derived nucleic acids is a central strategy by which the host senses infection and initiates protective immune responses 5 , 6 . Cyclic GMP-AMP synthase (cGAS) is a double-stranded DNA sensor 7 , 8 . It catalyses the synthesis of cyclic GMP-AMP (cGAMP) 9 – 12 , which stimulates the induction of type I interferons through the STING–TBK1–IRF-3 signalling axis 13 – 15 . STING oligomerizes after binding of cGAMP, leading to the recruitment and activation of the TBK1 kinase 8 , 16 . The IRF-3 transcription factor is then recruited to the signalling complex and activated by TBK1 8 , 17 – 20 . Phosphorylated IRF-3 translocates to the nucleus and initiates the expression of type I interferons 21 . However, the precise mechanisms that govern activation of STING by cGAMP and subsequent activation of TBK1 by STING remain unclear. Here we show that a conserved PLPLRT/SD motif within the C-terminal tail of STING mediates the recruitment and activation of TBK1. Crystal structures of TBK1 bound to STING reveal that the PLPLRT/SD motif binds to the dimer interface of TBK1. Cell-based studies confirm that the direct interaction between TBK1 and STING is essential for induction of IFNβ after cGAMP stimulation. Moreover, we show that full-length STING oligomerizes after it binds cGAMP, and highlight this as an essential step in the activation of STING-mediated signalling. These findings provide a structural basis for the development of STING agonists and antagonists for the treatment of cancer and autoimmune disorders. A molecular model of STING-mediated signalling is proposed, as structural analysis identifies a crucial motif for the binding of TBK1 to STING, and a separate model involved in IRF-3 binding.
Nucleic acids from bacteria or viruses induce potent immune responses in infected cells 1 – 4 . The detection of pathogen-derived nucleic acids is a central strategy by which the host senses infection and initiates protective immune responses 5 , 6 . Cyclic GMP-AMP synthase (cGAS) is a double-stranded DNA sensor 7 , 8 . It catalyzes the synthesis of cyclic GMP-AMP (cGAMP) 9 – 12 , which stimulates the induction of type I interferons (IFN-Is) through the STING-TBK1-IRF-3 signaling axis 13 – 15 . Stimulator of interferon genes (STING) oligomerizes upon cGAMP binding, leading to the recruitment and activation of tank-binding kinase 1 (TBK1) 8 , 16 . Interferon regulatory factor 3 (IRF-3) is then recruited to the signaling complex and activated by TBK1 8 , 17 – 20 . Phosphorylated IRF-3 translocates to the nucleus and initiates the expression of IFN-Is 21 . However, the precise mechanisms governing STING activation by cGAMP and subsequent TBK1 activation by STING remained poorly understood. Here we show that a conserved PLPLRT/SD motif within the C-terminal tail of STING mediates the recruitment and activation of TBK1. Crystal structures of TBK1 bound to STING reveal that the PLPLRT/SD motif binds to the dimer interface of TBK1. Cell-based studies confirm that the direct interaction between TBK1 and STING is essential for IFN-β induction upon cGAMP stimulation. Moreover, we show that full-length STING oligomerizes upon cGAMP binding and highlight this as an essential step in the activation of STING-mediated signaling.
Nucleic acids from bacteria or viruses induce potent immune responses in infected cells. The detection of pathogen-derived nucleic acids is a central strategy by which the host senses infection and initiates protective immune responses. Cyclic GMP-AMP synthase (cGAS) is a double-stranded DNA sensor. It catalyses the synthesis of cyclic GMP-AMP (cGAMP), which stimulates the induction of type I interferons through the STING-TBK1-IRF-3 signalling axis. STING oligomerizes after binding of cGAMP, leading to the recruitment and activation of the TBK1 kinase. The IRF-3 transcription factor is then recruited to the signalling complex and activated by TBK1. Phosphorylated IRF-3 translocates to the nucleus and initiates the expression of type I interferons. However, the precise mechanisms that govern activation of STING by cGAMP and subsequent activation of TBK1 by STING remain unclear. Here we show that a conserved PLPLRT/SD motif within the C-terminal tail of STING mediates the recruitment and activation of TBK1. Crystal structures of TBK1 bound to STING reveal that the PLPLRT/SD motif binds to the dimer interface of TBK1. Cell-based studies confirm that the direct interaction between TBK1 and STING is essential for induction of IFNβ after cGAMP stimulation. Moreover, we show that full-length STING oligomerizes after it binds cGAMP, and highlight this as an essential step in the activation of STING-mediated signalling. Furthermore, these findings provide a structural basis for the development of STING agonists and antagonists for the treatment of cancer and autoimmune disorders.
Audience Academic
Author Bell, Samantha L.
Liu, Yang
Laganowsky, Arthur
Sankaran, Banumathi
Zhu, Fanxiu
Xu, Pengbiao
Lei, Yuanjiu
Li, Pingwei
Fu, Xiaofeng
Shu, Chang
Watson, Robert O.
Zhao, Baoyu
Du, Fenglei
West, A. Phillip
Liu, Mengmeng
Gao, Xinsheng
Ji, Jun-Yuan
Zheng, Xueyun
AuthorAffiliation 1 Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843, USA
4 Department of Molecular and Cellular Medicine, Texas A&M University Health Science Center, College Station, TX 77843, USA
6 Department of Chemistry, Texas A&M University, College Station, TX 77843, USA
3 Department of Microbial Pathogenesis and Immunology, Texas A&M University Health Science Center, TX, 77802, USA
5 Department of Biological Science, Florida State University, Tallahassee, FL 32306-4370, USA
2 Molecular Biophysics and Bioimaging, Berkeley Center for Structural Biology, Lawrence Berkeley Laboratory, 1 Cyclotron Road, Berkeley, CA 94720, USA
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– name: 2 Molecular Biophysics and Bioimaging, Berkeley Center for Structural Biology, Lawrence Berkeley Laboratory, 1 Cyclotron Road, Berkeley, CA 94720, USA
– name: 5 Department of Biological Science, Florida State University, Tallahassee, FL 32306-4370, USA
– name: 6 Department of Chemistry, Texas A&M University, College Station, TX 77843, USA
– name: 4 Department of Molecular and Cellular Medicine, Texas A&M University Health Science Center, College Station, TX 77843, USA
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  surname: Zhao
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  surname: Du
  fullname: Du, Fenglei
  organization: Department of Biochemistry and Biophysics, Texas A&M University
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  organization: Department of Biochemistry and Biophysics, Texas A&M University
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  fullname: Shu, Chang
  organization: Department of Biochemistry and Biophysics, Texas A&M University
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  surname: Sankaran
  fullname: Sankaran, Banumathi
  organization: Molecular Biophysics and Integrated Bioimaging, Berkeley Center for Structural Biology, Lawrence Berkeley National Laboratory
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  fullname: Bell, Samantha L.
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  givenname: Mengmeng
  surname: Liu
  fullname: Liu, Mengmeng
  organization: Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M University Health Science Center
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  givenname: Yuanjiu
  surname: Lei
  fullname: Lei, Yuanjiu
  organization: Department of Microbial Pathogenesis and Immunology, Texas A&M University Health Science Center
– sequence: 9
  givenname: Xinsheng
  surname: Gao
  fullname: Gao, Xinsheng
  organization: Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M University Health Science Center
– sequence: 10
  givenname: Xiaofeng
  surname: Fu
  fullname: Fu, Xiaofeng
  organization: Department of Biological Science, Florida State University
– sequence: 11
  givenname: Fanxiu
  surname: Zhu
  fullname: Zhu, Fanxiu
  organization: Department of Biological Science, Florida State University
– sequence: 12
  givenname: Yang
  surname: Liu
  fullname: Liu, Yang
  organization: Department of Chemistry, Texas A&M University
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  surname: Laganowsky
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  organization: Department of Chemistry, Texas A&M University
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  surname: Zheng
  fullname: Zheng, Xueyun
  organization: Department of Chemistry, Texas A&M University
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  surname: Ji
  fullname: Ji, Jun-Yuan
  organization: Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M University Health Science Center
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  surname: West
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  organization: Department of Microbial Pathogenesis and Immunology, Texas A&M University Health Science Center
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  givenname: Robert O.
  surname: Watson
  fullname: Watson, Robert O.
  organization: Department of Microbial Pathogenesis and Immunology, Texas A&M University Health Science Center
– sequence: 18
  givenname: Pingwei
  surname: Li
  fullname: Li, Pingwei
  email: pingwei@tamu.edu
  organization: Department of Biochemistry and Biophysics, Texas A&M University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31118511$$D View this record in MEDLINE/PubMed
https://www.osti.gov/servlets/purl/1577334$$D View this record in Osti.gov
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AC02-05CH11231
USDOE Office of Science (SC), Basic Energy Sciences (BES)
These authors made equal contributions to the work
P.L. conceived the study. B.Z. and F.D. expressed the proteins, conducted the binding studies and solved the structures. B.S. collected the data at ALS. B.Z., C.S., M.L., X. G., and Y.L. contributed to the cell-based studies. S.L.B. and R.O.W. generated the TBK1 KO cells. P.W. and J.J. supervised some of the cell-based studies. P.X. conducted the cryo-EM studies. F.Z., and X.F. helped with EM data collection. Y.L., X.Z. and A.L. conducted MS/MS analysis of phosphorylated STING. B.Z. and P.L. wrote the paper. P.W., R.O.W., and S.L.B helped with revising the manuscript.
Author contributions
OpenAccessLink https://pubmed.ncbi.nlm.nih.gov/PMC6596994
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Snippet Nucleic acids from bacteria or viruses induce potent immune responses in infected cells 1 – 4 . The detection of pathogen-derived nucleic acids is a central...
Nucleic acids from bacteria or viruses induce potent immune responses in infected cells . The detection of pathogen-derived nucleic acids is a central strategy...
Nucleic acids from bacteria or viruses induce potent immune responses in infected cells.sup.1-4. The detection of pathogen-derived nucleic acids is a central...
Nucleic acids from bacteria or viruses induce potent immune responses in infected cells1-4. The detection of pathogen-derived nucleic acids is a central...
Nucleic acids from bacteria or viruses induce potent immune responses in infected cells. The detection of pathogen-derived nucleic acids is a central strategy...
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SubjectTerms 14/19
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82/1
82/103
82/16
82/29
82/58
82/80
82/83
Amino Acid Motifs
Analysis
Antagonists
Autoimmune diseases
BASIC BIOLOGICAL SCIENCES
Chemical synthesis
Conserved Sequence
Crystallography, X-Ray
Cyclic GMP
EF hand proteins
Enzyme Activation
HEK293 Cells
Humanities and Social Sciences
Humans
Hydrogen bonds
Immune response
Influence
Interferon
Interferon regulatory factor 3
Interferon-beta - metabolism
Letter
Membrane Proteins - chemistry
Membrane Proteins - genetics
Membrane Proteins - metabolism
Models, Molecular
multidisciplinary
Mutation
Nucleic acids
Nucleotides, Cyclic - metabolism
Oligomerization
Peptides
Phosphorylation
Protein Binding
Protein kinases
Protein Serine-Threonine Kinases - metabolism
Science
Science (multidisciplinary)
Signal Transduction
β-Interferon
Title A conserved PLPLRT/SD motif of STING mediates the recruitment and activation of TBK1
URI https://link.springer.com/article/10.1038/s41586-019-1228-x
https://www.ncbi.nlm.nih.gov/pubmed/31118511
https://www.proquest.com/docview/2841415721
https://www.proquest.com/docview/2232109656
https://www.osti.gov/servlets/purl/1577334
https://pubmed.ncbi.nlm.nih.gov/PMC6596994
Volume 569
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