Cyclic GMP-AMP Synthase Is Activated by Double-Stranded DNA-Induced Oligomerization

Cyclic GMP-AMP synthase (cGAS) is a cytosolic DNA sensor mediating innate antimicrobial immunity. It catalyzes the synthesis of a noncanonical cyclic dinucleotide, 2′,5′ cGAMP, that binds to STING and mediates the activation of TBK1 and IRF-3. Activated IRF-3 translocates to the nucleus and initiate...

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Published in	Immunity (Cambridge, Mass.) Vol. 39; no. 6; pp. 1019 - 1031
Main Authors	Li, Xin, Shu, Chang, Yi, Guanghui, Chaton, Catherine T., Shelton, Catherine L., Diao, Jiasheng, Zuo, Xiaobing, Kao, C. Cheng, Herr, Andrew B., Li, Pingwei
Format	Journal Article
Language	English
Published	United States Elsevier Inc 12.12.2013 Elsevier Limited
Subjects	Animals Binding Sites - genetics Catalytic Domain Chromatography Deoxyribonucleic acid DNA DNA - metabolism Enzymes Humans Kinases Ligands Mice Models, Molecular Nucleotides, Cyclic - metabolism Nucleotidyltransferases - chemistry Nucleotidyltransferases - genetics Nucleotidyltransferases - metabolism Protein Binding Protein Structure, Quaternary Proteins Sperm Studies Transcription factors
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Abstract	Cyclic GMP-AMP synthase (cGAS) is a cytosolic DNA sensor mediating innate antimicrobial immunity. It catalyzes the synthesis of a noncanonical cyclic dinucleotide, 2′,5′ cGAMP, that binds to STING and mediates the activation of TBK1 and IRF-3. Activated IRF-3 translocates to the nucleus and initiates the transcription of the IFN-β gene. The structure of mouse cGAS bound to an 18 bp dsDNA revealed that cGAS interacts with dsDNA through two binding sites, forming a 2:2 complex. Enzyme assays and IFN-β reporter assays of cGAS mutants demonstrated that interactions at both DNA binding sites are essential for cGAS activation. Mutagenesis and DNA binding studies showed that the two sites bind dsDNA cooperatively and that site B plays a critical role in DNA binding. The structure of mouse cGAS bound to dsDNA and 2′,5′ cGAMP provided insight into the catalytic mechanism of cGAS. These results demonstrated that cGAS is activated by dsDNA-induced oligomerization. •cGAS is activated by dsDNA and catalyzes the synthesis of 2′,5′ cGAMP•cGAS is activated by dsDNA-induced oligomerization•cGAS binds dsDNA cooperatively through two binding sites•Mutations at the DNA binding sites and the dimer interface affect cGAS activity
AbstractList	Cyclic GMP-AMP synthase (cGAS) is a cytosolic DNA sensor mediating innate antimicrobial immunity. It catalyzes the synthesis of a noncanonical cyclic dinucleotide, 2',5' cGAMP, that binds to STING and mediates the activation of TBK1 and IRF-3. Activated IRF-3 translocates to the nucleus and initiates the transcription of the IFN-β gene. The structure of mouse cGAS bound to an 18 bp dsDNA revealed that cGAS interacts with dsDNA through two binding sites, forming a 2:2 complex. Enzyme assays and IFN-β reporter assays of cGAS mutants demonstrated that interactions at both DNA binding sites are essential for cGAS activation. Mutagenesis and DNA binding studies showed that the two sites bind dsDNA cooperatively and that site B plays a critical role in DNA binding. The structure of mouse cGAS bound to dsDNA and 2',5' cGAMP provided insight into the catalytic mechanism of cGAS. These results demonstrated that cGAS is activated by dsDNA-induced oligomerization. Cyclic GMP-AMP synthase (cGAS) is a cytosolic DNA sensor mediating innate antimicrobial immunity. It catalyzes the synthesis of a noncanonical cyclic dinucleotide, 2',5' cGAMP, that binds to STING and mediates the activation of TBK1 and IRF-3. Activated IRF-3 translocates to the nucleus and initiates the transcription of the IFN-β gene. The structure of mouse cGAS bound to an 18 bp dsDNA revealed that cGAS interacts with dsDNA through two binding sites, forming a 2:2 complex. Enzyme assays and IFN-β reporter assays of cGAS mutants demonstrated that interactions at both DNA binding sites are essential for cGAS activation. Mutagenesis and DNA binding studies showed that the two sites bind dsDNA cooperatively and that site B plays a critical role in DNA binding. The structure of mouse cGAS bound to dsDNA and 2',5' cGAMP provided insight into the catalytic mechanism of cGAS. These results demonstrated that cGAS is activated by dsDNA-induced oligomerization.Cyclic GMP-AMP synthase (cGAS) is a cytosolic DNA sensor mediating innate antimicrobial immunity. It catalyzes the synthesis of a noncanonical cyclic dinucleotide, 2',5' cGAMP, that binds to STING and mediates the activation of TBK1 and IRF-3. Activated IRF-3 translocates to the nucleus and initiates the transcription of the IFN-β gene. The structure of mouse cGAS bound to an 18 bp dsDNA revealed that cGAS interacts with dsDNA through two binding sites, forming a 2:2 complex. Enzyme assays and IFN-β reporter assays of cGAS mutants demonstrated that interactions at both DNA binding sites are essential for cGAS activation. Mutagenesis and DNA binding studies showed that the two sites bind dsDNA cooperatively and that site B plays a critical role in DNA binding. The structure of mouse cGAS bound to dsDNA and 2',5' cGAMP provided insight into the catalytic mechanism of cGAS. These results demonstrated that cGAS is activated by dsDNA-induced oligomerization. Cyclic GMP-AMP synthase (cGAS) is a cytosolic DNA sensor mediating innate antimicrobial immunity. It catalyzes the synthesis of a noncanonical cyclic dinucleotide 2′,5′ cGAMP that binds to STING and mediates the activation of TBK1 and IRF-3. Activated IRF-3 translocates to the nucleus and initiates the transcription of the IFN-β gene. The structure of mouse cGAS bound to an 18 bp dsDNA revealed that cGAS interacts with dsDNA through two binding sites, forming a 2:2 complex. Enzyme assays and IFN-β reporter assays of cGAS mutants demonstrated that interactions at both DNA binding sites are essential for cGAS activation. Mutagenesis and DNA binding studies showed that the two sites bind dsDNA cooperatively and site B plays a critical role in DNA binding. The structure of mouse cGAS bound to dsDNA and 2′,5′ cGAMP provided insight into the catalytic mechanism of cGAS. These results demonstrated that cGAS is activated by dsDNA-induced oligomerization. Cyclic GMP-AMP synthase (cGAS) is a cytosolic DNA sensor mediating innate antimicrobial immunity. It catalyzes the synthesis of a noncanonical cyclic dinucleotide, 2\',5\' cGAMP, that binds to STING and mediates the activation of TBK1 and IRF-3. Activated IRF-3 translocates to the nucleus and initiates the transcription of the IFN- beta gene. The structure of mouse cGAS bound to an 18 bp dsDNA revealed that cGAS interacts with dsDNA through two binding sites, forming a 2:2 complex. Enzyme assays and IFN- beta reporter assays of cGAS mutants demonstrated that interactions at both DNA binding sites are essential for cGAS activation. Mutagenesis and DNA binding studies showed that the two sites bind dsDNA cooperatively and that site B plays a critical role in DNA binding. The structure of mouse cGAS bound to dsDNA and 2\',5\' cGAMP provided insight into the catalytic mechanism of cGAS. These results demonstrated that cGAS is activated by dsDNA-induced oligomerization. Cyclic GMP-AMP synthase (cGAS) is a cytosolic DNA sensor mediating innate antimicrobial immunity. It catalyzes the synthesis of a noncanonical cyclic dinucleotide, 2′,5′ cGAMP, that binds to STING and mediates the activation of TBK1 and IRF-3. Activated IRF-3 translocates to the nucleus and initiates the transcription of the IFN-β gene. The structure of mouse cGAS bound to an 18 bp dsDNA revealed that cGAS interacts with dsDNA through two binding sites, forming a 2:2 complex. Enzyme assays and IFN-β reporter assays of cGAS mutants demonstrated that interactions at both DNA binding sites are essential for cGAS activation. Mutagenesis and DNA binding studies showed that the two sites bind dsDNA cooperatively and that site B plays a critical role in DNA binding. The structure of mouse cGAS bound to dsDNA and 2′,5′ cGAMP provided insight into the catalytic mechanism of cGAS. These results demonstrated that cGAS is activated by dsDNA-induced oligomerization. •cGAS is activated by dsDNA and catalyzes the synthesis of 2′,5′ cGAMP•cGAS is activated by dsDNA-induced oligomerization•cGAS binds dsDNA cooperatively through two binding sites•Mutations at the DNA binding sites and the dimer interface affect cGAS activity
Author	Shelton, Catherine L. Diao, Jiasheng Li, Pingwei Shu, Chang Herr, Andrew B. Yi, Guanghui Zuo, Xiaobing Li, Xin Kao, C. Cheng Chaton, Catherine T.
AuthorAffiliation	4 X-Ray Science Division, Advanced Photon Source, Argonne National Laboratory, 9700 South Cass Avenue, Argonne, IL 60439, USA 2 Department of Molecular and Cellular Biochemistry, Indiana University, Bloomington, IN 47405, USA 1 Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843-2128, USA 3 Department of Molecular Genetics, Biochemistry & Microbiology, University of Cincinnati College of Medicine, Cincinnati, OH 45267, USA
AuthorAffiliation_xml	– name: 1 Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843-2128, USA – name: 4 X-Ray Science Division, Advanced Photon Source, Argonne National Laboratory, 9700 South Cass Avenue, Argonne, IL 60439, USA – name: 2 Department of Molecular and Cellular Biochemistry, Indiana University, Bloomington, IN 47405, USA – name: 3 Department of Molecular Genetics, Biochemistry & Microbiology, University of Cincinnati College of Medicine, Cincinnati, OH 45267, USA
Author_xml	– sequence: 1 givenname: Xin surname: Li fullname: Li, Xin organization: Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843-2128, USA – sequence: 2 givenname: Chang surname: Shu fullname: Shu, Chang organization: Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843-2128, USA – sequence: 3 givenname: Guanghui surname: Yi fullname: Yi, Guanghui organization: Department of Molecular and Cellular Biochemistry, Indiana University, Bloomington, IN 47405, USA – sequence: 4 givenname: Catherine T. surname: Chaton fullname: Chaton, Catherine T. organization: Department of Molecular Genetics, Biochemistry & Microbiology, University of Cincinnati College of Medicine, Cincinnati, OH 45267, USA – sequence: 5 givenname: Catherine L. surname: Shelton fullname: Shelton, Catherine L. organization: Department of Molecular Genetics, Biochemistry & Microbiology, University of Cincinnati College of Medicine, Cincinnati, OH 45267, USA – sequence: 6 givenname: Jiasheng surname: Diao fullname: Diao, Jiasheng organization: Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843-2128, USA – sequence: 7 givenname: Xiaobing surname: Zuo fullname: Zuo, Xiaobing organization: X-Ray Science Division, Advanced Photon Source, Argonne National Laboratory, 9700 South Cass Avenue, Argonne, IL 60439, USA – sequence: 8 givenname: C. Cheng surname: Kao fullname: Kao, C. Cheng organization: Department of Molecular and Cellular Biochemistry, Indiana University, Bloomington, IN 47405, USA – sequence: 9 givenname: Andrew B. surname: Herr fullname: Herr, Andrew B. organization: Department of Molecular Genetics, Biochemistry & Microbiology, University of Cincinnati College of Medicine, Cincinnati, OH 45267, USA – sequence: 10 givenname: Pingwei surname: Li fullname: Li, Pingwei email: pingwei@tamu.edu organization: Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843-2128, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/24332030$$D View this record in MEDLINE/PubMed
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Struct. Mol. Biol. doi: 10.1038/nsmb.2332 – reference: 24332024 - Immunity. 2013 Dec 12;39(6):992-4
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Snippet	Cyclic GMP-AMP synthase (cGAS) is a cytosolic DNA sensor mediating innate antimicrobial immunity. It catalyzes the synthesis of a noncanonical cyclic...
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SubjectTerms	Animals Binding Sites - genetics Catalytic Domain Chromatography Deoxyribonucleic acid DNA DNA - metabolism Enzymes Humans Kinases Ligands Mice Models, Molecular Nucleotides, Cyclic - metabolism Nucleotidyltransferases - chemistry Nucleotidyltransferases - genetics Nucleotidyltransferases - metabolism Protein Binding Protein Structure, Quaternary Proteins Sperm Studies Transcription factors
Title	Cyclic GMP-AMP Synthase Is Activated by Double-Stranded DNA-Induced Oligomerization
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