cGAS produces a 2′-5′-linked cyclic dinucleotide second messenger that activates STING
Cytosolic DNA induces type I interferon via activation of STING; the immediate STING activator is produced by the recently identified DNA sensor cGAS and is shown here to be an unorthodox cyclic dinucleotide harbouring a 2′-5′ linkage between guanosine and adenosine. DNA sensing by cGAS The mechanis...
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| Published in | Nature (London) Vol. 498; no. 7454; pp. 380 - 384 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
20.06.2013
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Cytosolic DNA induces type I interferon via activation of STING; the immediate STING activator is produced by the recently identified DNA sensor cGAS and is shown here to be an unorthodox cyclic dinucleotide harbouring a 2′-5′ linkage between guanosine and adenosine.
DNA sensing by cGAS
The mechanism of sensing and signalling of cytosolic DNA by the innate immune system is a topic of intense research interest as it is the means by which invading bacteria and viruses are detected. Cytosolic DNA is known to induce type I interferon through activation of the DNA sensor cyclic-GMP-AMP synthetase (cGAS), which catalyses the synthesis of a cyclic dinucleotide which in turn activates a protein known as STING (stimulator of interferon genes). Karl-Peter Hopfner and co-workers present the crystal structures of a C-terminal fragment of cGAS alone, in complex with UTP, and as a DNA–ATP–GTP complex. In a complementary paper [in this issue], Veit Hornung and coworkers show that the product of cGAS is distinct from previously characterized cyclic dinucleotides. Rather it is an unorthodox cyclic dinucleotide with a 2′–5′ linkage between guanosine and adenosine. This two-step synthesis of cGAMP(2′–5′) could be a focus for the development of specific inhibitors for the treatment of autoimmune diseases that engage the cGAS–STING axis.
Detection of cytoplasmic DNA represents one of the most fundamental mechanisms of the innate immune system to sense the presence of microbial pathogens
1
. Moreover, erroneous detection of endogenous DNA by the same sensing mechanisms has an important pathophysiological role in certain sterile inflammatory conditions
2
,
3
. The endoplasmic-reticulum-resident protein STING is critically required for the initiation of type I interferon signalling upon detection of cytosolic DNA of both exogenous and endogenous origin
4
,
5
,
6
,
7
,
8
. Next to its pivotal role in DNA sensing, STING also serves as a direct receptor for the detection of cyclic dinucleotides, which function as second messenger molecules in bacteria
9
,
10
,
11
,
12
,
13
. DNA recognition, however, is triggered in an indirect fashion that depends on a recently characterized cytoplasmic nucleotidyl transferase, termed cGAMP synthase (cGAS), which upon interaction with DNA synthesizes a dinucleotide molecule that in turn binds to and activates STING
14
,
15
. We here show
in vivo
and
in vitro
that the cGAS-catalysed reaction product is distinct from previously characterized cyclic dinucleotides. Using a combinatorial approach based on mass spectrometry, enzymatic digestion, NMR analysis and chemical synthesis we demonstrate that cGAS produces a cyclic GMP-AMP dinucleotide, which comprises a 2′-5′ and a 3′-5′ phosphodiester linkage >Gp(2′-5′)Ap(3′-5′)>. We found that the presence of this 2′-5′ linkage was required to exert potent activation of human STING. Moreover, we show that cGAS first catalyses the synthesis of a linear 2′-5′-linked dinucleotide, which is then subject to cGAS-dependent cyclization in a second step through a 3′-5′ phosphodiester linkage. This 13-membered ring structure defines a novel class of second messenger molecules, extending the family of 2′-5′-linked antiviral biomolecules. |
|---|---|
| AbstractList | Detection of cytoplasmic DNA represents one of the most fundamental mechanisms of the innate immune system to sense the presence of microbial pathogens^sup 1^. Moreover, erroneous detection of endogenous DNA by the same sensing mechanisms has an important pathophysiological role in certain sterile inflammatory conditions^sup 2,3^. The endoplasmic-reticulum-resident protein STING is critically required for the initiation of type I interferon signalling upon detection of cytosolic DNA of both exogenous and endogenous origin^sup 4-8^. Next to its pivotal role in DNA sensing, STING also serves as a direct receptor for the detection of cyclic dinucleotides, which function as second messenger molecules in bacteria^sup 9-13^. DNA recognition, however, is triggered in an indirect fashion that depends on a recently characterized cytoplasmic nucleotidyl transferase, termed cGAMP synthase (cGAS), which upon interaction withDNAsynthesizes a dinucleotide molecule that in turn binds to and activates STING^sup 14,15^. We here showin vivo and in vitro that the cGAS-catalysed reaction product is distinct from previously characterized cyclic dinucleotides.Using a combinatorial approach based on mass spectrometry, enzymatic digestion,NMRanalysis and chemical synthesis we demonstrate that cGAS produces a cyclic GMP-AMP dinucleotide, which comprises a 2'-5' and a 3'-5' phosphodiester linkage >Gp(2'-5')Ap(3'-5')>. We found that the presence of this 2'-5' linkage was required to exert potent activation of human STING. Moreover, we show that cGAS first catalyses the synthesis of a linear 2'-5'-linked dinucleotide, which is then subject to cGASdependent cyclization in a second step through a 3'-5' phosphodiester linkage. This 13-membered ring structure defines a novel class of second messengermolecules, extending the family of 2'-5'-linked antiviral biomolecules. [PUBLICATION ABSTRACT] Detection of cytoplasmic DNA represents one of the most fundamental mechanisms of the innate immune system to sense the presence of microbial pathogens. Moreover, erroneous detection of endogenous DNA by the same sensing mechanisms has an important pathophysiological role in certain sterile inflammatory conditions. The endoplasmic-reticulum-resident protein STING is critically required for the initiation of type I interferon signalling upon detection of cytosolic DNA of both exogenous and endogenous origin. Next to its pivotal role in DNA sensing, STING also serves as a direct receptor for the detection of cyclic dinucleotides, which function as second messenger molecules in bacteria. DNA recognition, however, is triggered in an indirect fashion that depends on a recently characterized cytoplasmic nucleotidyl transferase, termed cGAMP synthase (cGAS), which upon interaction with DNA synthesizes a dinucleotide molecule that in turn binds to and activates STING. We here show in vivo and in vitro that the cGAS-catalysed reaction product is distinct from previously characterized cyclic dinucleotides. Using a combinatorial approach based on mass spectrometry, enzymatic digestion, NMR analysis and chemical synthesis we demonstrate that cGAS produces a cyclic GMP-AMP dinucleotide, which comprises a 2'-5' and a 3'-5' phosphodiester linkage >Gp(2'-5')Ap(3'-5')>. We found that the presence of this 2'-5' linkage was required to exert potent activation of human STING. Moreover, we show that cGAS first catalyses the synthesis of a linear 2'-5'-linked dinucleotide, which is then subject to cGAS-dependent cyclization in a second step through a 3'-5' phosphodiester linkage. This 13-membered ring structure defines a novel class of second messenger molecules, extending the family of 2'-5'-linked antiviral biomolecules.Detection of cytoplasmic DNA represents one of the most fundamental mechanisms of the innate immune system to sense the presence of microbial pathogens. Moreover, erroneous detection of endogenous DNA by the same sensing mechanisms has an important pathophysiological role in certain sterile inflammatory conditions. The endoplasmic-reticulum-resident protein STING is critically required for the initiation of type I interferon signalling upon detection of cytosolic DNA of both exogenous and endogenous origin. Next to its pivotal role in DNA sensing, STING also serves as a direct receptor for the detection of cyclic dinucleotides, which function as second messenger molecules in bacteria. DNA recognition, however, is triggered in an indirect fashion that depends on a recently characterized cytoplasmic nucleotidyl transferase, termed cGAMP synthase (cGAS), which upon interaction with DNA synthesizes a dinucleotide molecule that in turn binds to and activates STING. We here show in vivo and in vitro that the cGAS-catalysed reaction product is distinct from previously characterized cyclic dinucleotides. Using a combinatorial approach based on mass spectrometry, enzymatic digestion, NMR analysis and chemical synthesis we demonstrate that cGAS produces a cyclic GMP-AMP dinucleotide, which comprises a 2'-5' and a 3'-5' phosphodiester linkage >Gp(2'-5')Ap(3'-5')>. We found that the presence of this 2'-5' linkage was required to exert potent activation of human STING. Moreover, we show that cGAS first catalyses the synthesis of a linear 2'-5'-linked dinucleotide, which is then subject to cGAS-dependent cyclization in a second step through a 3'-5' phosphodiester linkage. This 13-membered ring structure defines a novel class of second messenger molecules, extending the family of 2'-5'-linked antiviral biomolecules. Detection of cytoplasmic DNA represents one of the most fundamental mechanisms of the innate immune system to sense the presence of microbial pathogens 1 . Moreover, erroneous detection of endogenous DNA by the same sensing mechanisms has an important pathophysiological role in certain sterile inflammatory conditions 2 , 3 . The endoplasmic-reticulum-resident protein STING is critically required for the initiation of type I interferon signalling upon detection of cytosolic DNA of both exogenous and endogenous origin 4 , 5 , 6 , 7 , 8 . Next to its pivotal role in DNA sensing, STING also serves as a direct receptor for the detection of cyclic dinucleotides, which function as second messenger molecules in bacteria 9 , 10 , 11 , 12 , 13 . DNA recognition, however, is triggered in an indirect fashion that depends on a recently characterized cytoplasmic nucleotidyl transferase, termed cGAMP synthase (cGAS), which upon interaction with DNA synthesizes a dinucleotide molecule that in turn binds to and activates STING 14 , 15 . We here show in vivo and in vitro that the cGAS-catalysed reaction product is distinct from previously characterized cyclic dinucleotides. Using a combinatorial approach based on mass spectrometry, enzymatic digestion, NMR analysis and chemical synthesis we demonstrate that cGAS produces a cyclic GMP-AMP dinucleotide, which comprises a 2′-5′ and a 3′-5′ phosphodiester linkage >Gp(2′-5′)Ap(3′-5′)>. We found that the presence of this 2′-5′ linkage was required to exert potent activation of human STING. Moreover, we show that cGAS first catalyses the synthesis of a linear 2′-5′-linked dinucleotide, which is then subject to cGAS-dependent cyclization in a second step through a 3′-5′ phosphodiester linkage. This 13-membered ring structure defines a novel class of second messenger molecules, extending the family of 2′-5′-linked antiviral biomolecules. Detection of cytoplasmic DNA represents one of the most fundamental mechanisms of the innate immune system to sense the presence of microbial pathogens. Moreover, erroneous detection of endogenous DNA by the same sensing mechanisms has an important pathophysiological role in certain sterile inflammatory conditions. The endoplasmic-reticulum-resident protein STING is critically required for the initiation of type I interferon signalling upon detection of cytosolic DNA of both exogenous and endogenous origin. Next to its pivotal role in DNA sensing, STING also serves as a direct receptor for the detection of cyclic dinucleotides, which function as second messenger molecules in bacteria. DNA recognition, however, is triggered in an indirect fashion that depends on a recently characterized cytoplasmic nucleotidyl transferase, termed cGAMP synthase (cGAS), which upon interaction with DNA synthesizes a dinucleotide molecule that in turn binds to and activates STING. We here show in vivo and in vitro that the cGAS-catalysed reaction product is distinct from previously characterized cyclic dinucleotides. Using a combinatorial approach based on mass spectrometry, enzymatic digestion, NMR analysis and chemical synthesis we demonstrate that cGAS produces a cyclic GMP-AMP dinucleotide, which comprises a 2'-5' and a 3'-5' phosphodiester linkage >Gp(2'-5')Ap(3'-5')>. We found that the presence of this 2'-5' linkage was required to exert potent activation of human STING. Moreover, we show that cGAS first catalyses the synthesis of a linear 2'-5'-linked dinucleotide, which is then subject to cGAS-dependent cyclization in a second step through a 3'-5' phosphodiester linkage. This 13-membered ring structure defines a novel class of second messenger molecules, extending the family of 2'-5'-linked antiviral biomolecules. Cytosolic DNA induces type I interferon via activation of STING; the immediate STING activator is produced by the recently identified DNA sensor cGAS and is shown here to be an unorthodox cyclic dinucleotide harbouring a 2′-5′ linkage between guanosine and adenosine. DNA sensing by cGAS The mechanism of sensing and signalling of cytosolic DNA by the innate immune system is a topic of intense research interest as it is the means by which invading bacteria and viruses are detected. Cytosolic DNA is known to induce type I interferon through activation of the DNA sensor cyclic-GMP-AMP synthetase (cGAS), which catalyses the synthesis of a cyclic dinucleotide which in turn activates a protein known as STING (stimulator of interferon genes). Karl-Peter Hopfner and co-workers present the crystal structures of a C-terminal fragment of cGAS alone, in complex with UTP, and as a DNA–ATP–GTP complex. In a complementary paper [in this issue], Veit Hornung and coworkers show that the product of cGAS is distinct from previously characterized cyclic dinucleotides. Rather it is an unorthodox cyclic dinucleotide with a 2′–5′ linkage between guanosine and adenosine. This two-step synthesis of cGAMP(2′–5′) could be a focus for the development of specific inhibitors for the treatment of autoimmune diseases that engage the cGAS–STING axis. Detection of cytoplasmic DNA represents one of the most fundamental mechanisms of the innate immune system to sense the presence of microbial pathogens 1 . Moreover, erroneous detection of endogenous DNA by the same sensing mechanisms has an important pathophysiological role in certain sterile inflammatory conditions 2 , 3 . The endoplasmic-reticulum-resident protein STING is critically required for the initiation of type I interferon signalling upon detection of cytosolic DNA of both exogenous and endogenous origin 4 , 5 , 6 , 7 , 8 . Next to its pivotal role in DNA sensing, STING also serves as a direct receptor for the detection of cyclic dinucleotides, which function as second messenger molecules in bacteria 9 , 10 , 11 , 12 , 13 . DNA recognition, however, is triggered in an indirect fashion that depends on a recently characterized cytoplasmic nucleotidyl transferase, termed cGAMP synthase (cGAS), which upon interaction with DNA synthesizes a dinucleotide molecule that in turn binds to and activates STING 14 , 15 . We here show in vivo and in vitro that the cGAS-catalysed reaction product is distinct from previously characterized cyclic dinucleotides. Using a combinatorial approach based on mass spectrometry, enzymatic digestion, NMR analysis and chemical synthesis we demonstrate that cGAS produces a cyclic GMP-AMP dinucleotide, which comprises a 2′-5′ and a 3′-5′ phosphodiester linkage >Gp(2′-5′)Ap(3′-5′)>. We found that the presence of this 2′-5′ linkage was required to exert potent activation of human STING. Moreover, we show that cGAS first catalyses the synthesis of a linear 2′-5′-linked dinucleotide, which is then subject to cGAS-dependent cyclization in a second step through a 3′-5′ phosphodiester linkage. This 13-membered ring structure defines a novel class of second messenger molecules, extending the family of 2′-5′-linked antiviral biomolecules. |
| Author | Ablasser, Andrea Witte, Gregor Goldeck, Marion Ludwig, Janos Röhl, Ingo Deimling, Tobias Hopfner, Karl-Peter Hornung, Veit Cavlar, Taner |
| AuthorAffiliation | 4 Center for Integrated Protein Sciences, Munich, Germany 2 Department of Biochemistry and Gene Center, Ludwig-Maximilians-University, Munich, Germany 3 Axolabs GmbH, Kulmbach, Germany 1 Institute for Clinical Chemistry and Clinical Pharmacology, University Hospital, University of Bonn, Germany |
| AuthorAffiliation_xml | – name: 4 Center for Integrated Protein Sciences, Munich, Germany – name: 3 Axolabs GmbH, Kulmbach, Germany – name: 1 Institute for Clinical Chemistry and Clinical Pharmacology, University Hospital, University of Bonn, Germany – name: 2 Department of Biochemistry and Gene Center, Ludwig-Maximilians-University, Munich, Germany |
| Author_xml | – sequence: 1 givenname: Andrea surname: Ablasser fullname: Ablasser, Andrea email: andrea.ablasser@uni-bonn.de organization: Institute for Clinical Chemistry and Clinical Pharmacology, University Hospital, University of Bonn, 53127 Bonn, Germany – sequence: 2 givenname: Marion surname: Goldeck fullname: Goldeck, Marion organization: Institute for Clinical Chemistry and Clinical Pharmacology, University Hospital, University of Bonn, 53127 Bonn, Germany – sequence: 3 givenname: Taner surname: Cavlar fullname: Cavlar, Taner organization: Institute for Clinical Chemistry and Clinical Pharmacology, University Hospital, University of Bonn, 53127 Bonn, Germany – sequence: 4 givenname: Tobias surname: Deimling fullname: Deimling, Tobias organization: Department of Biochemistry and Gene Center, Ludwig-Maximilians-University, 81377 Munich, Germany – sequence: 5 givenname: Gregor surname: Witte fullname: Witte, Gregor organization: Department of Biochemistry and Gene Center, Ludwig-Maximilians-University, 81377 Munich, Germany – sequence: 6 givenname: Ingo surname: Röhl fullname: Röhl, Ingo organization: Axolabs GmbH, 95326 Kulmbach, Germany – sequence: 7 givenname: Karl-Peter surname: Hopfner fullname: Hopfner, Karl-Peter organization: Department of Biochemistry and Gene Center, Ludwig-Maximilians-University, 81377 Munich, Germany, Center for Integrated Protein Sciences, 81377 Munich, Germany – sequence: 8 givenname: Janos surname: Ludwig fullname: Ludwig, Janos organization: Institute for Clinical Chemistry and Clinical Pharmacology, University Hospital, University of Bonn, 53127 Bonn, Germany – sequence: 9 givenname: Veit surname: Hornung fullname: Hornung, Veit email: veit.hornung@uni-bonn.de organization: Institute for Clinical Chemistry and Clinical Pharmacology, University Hospital, University of Bonn, 53127 Bonn, Germany |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23722158$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-2 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 Author Contributions: A.A., M.G., T.C., G.W., T.D., I.R., J.L., K.-P.H. and V.H. designed experiments and analysed the data. A.A., M.G., T.C., G.W., T.D. and I.R. performed experiments. A.A. and V.H. wrote the manuscript. V.H. supervised the project. |
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| Snippet | Cytosolic DNA induces type I interferon via activation of STING; the immediate STING activator is produced by the recently identified DNA sensor cGAS and is... Detection of cytoplasmic DNA represents one of the most fundamental mechanisms of the innate immune system to sense the presence of microbial pathogens.... Detection of cytoplasmic DNA represents one of the most fundamental mechanisms of the innate immune system to sense the presence of microbial pathogens^sup 1^.... Detection of cytoplasmic DNA represents one of the most fundamental mechanisms of the innate immune system to sense the presence of microbial pathogens 1 .... |
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| SubjectTerms | 631/250/256 631/250/262 631/250/516 Adenosine Monophosphate - chemistry Animals Autoimmune diseases Biocatalysis Cell Line Chromatography Crystal structure Cyclic GMP - chemistry Cyclization Deoxyribonucleic acid DNA Enzymes HEK293 Cells Humanities and Social Sciences Humans Immune system letter Magnetic Resonance Spectroscopy Mass spectrometry Membrane Proteins - metabolism Mice Models, Molecular Molecular Structure multidisciplinary Nucleotidyltransferases - genetics Nucleotidyltransferases - metabolism Oligoribonucleotides - biosynthesis Oligoribonucleotides - chemistry Oligoribonucleotides - metabolism Science Second Messenger Systems - physiology |
| Title | cGAS produces a 2′-5′-linked cyclic dinucleotide second messenger that activates STING |
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