Structural basis for concerted recruitment and activation of IRF-3 by innate immune adaptor proteins
Type I IFNs are key cytokines mediating innate antiviral immunity. cGMP-AMP synthase, ritinoic acid-inducible protein 1 (RIG-I)–like receptors, and Toll-like receptors recognize microbial double-stranded (ds)DNA, dsRNA, and LPS to induce the expression of type I IFNs. These signaling pathways conver...
Saved in:
| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 113; no. 24; pp. E3403 - E3412 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
14.06.2016
National Academy of Sciences, Washington, DC (United States) |
| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
Cover
Loading…
| Abstract | Type I IFNs are key cytokines mediating innate antiviral immunity. cGMP-AMP synthase, ritinoic acid-inducible protein 1 (RIG-I)–like receptors, and Toll-like receptors recognize microbial double-stranded (ds)DNA, dsRNA, and LPS to induce the expression of type I IFNs. These signaling pathways converge at the recruitment and activation of the transcription factor IRF-3 (IFN regulatory factor 3). The adaptor proteins STING (stimulator of IFN genes), MAVS (mitochondrial antiviral signaling), and TRIF (TIR domain-containing adaptor inducing IFN-β) mediate the recruitment of IRF-3 through a conserved pLxIS motif. Here we show that the pLxIS motif of phosphorylated STING, MAVS, and TRIF binds to IRF-3 in a similar manner, whereas residues upstream of the motif confer specificity. The structure of the IRF-3 phosphomimetic mutant S386/396E bound to the cAMP response element binding protein (CREB)-binding protein reveals that the pLxIS motif also mediates IRF-3 dimerization and activation. Moreover, rotavirus NSP1 (nonstructural protein 1) employs a pLxIS motif to target IRF-3 for degradation, but phosphorylation of NSP1 is not required for its activity. These results suggest a concerted mechanism for the recruitment and activation of IRF-3 that can be subverted by viral proteins to evade innate immune responses. |
|---|---|
| AbstractList | Type I IFNs are key cytokines involved in antiviral immunity. A number of innate sensing pathways regulate the induction of type I IFNs. These pathways converge at the activation of the transcription factor IRF-3 (IFN regulatory factor 3). Three different adaptors mediate the recruitment of IRF-3 using a conserved structural motif. In this study, we determined the molecular mechanisms by which these adaptors recruit IRF-3 upon phosphorylation, the mechanism of IRF-3 activation, and how rotavirus subverts these signaling mechanisms to evade innate immune surveillance. These results provide critical insights into the molecular basis of innate immunity against microbial and viral infections.
Type I IFNs are key cytokines mediating innate antiviral immunity. cGMP-AMP synthase, ritinoic acid-inducible protein 1 (RIG-I)–like receptors, and Toll-like receptors recognize microbial double-stranded (ds)DNA, dsRNA, and LPS to induce the expression of type I IFNs. These signaling pathways converge at the recruitment and activation of the transcription factor IRF-3 (IFN regulatory factor 3). The adaptor proteins STING (stimulator of IFN genes), MAVS (mitochondrial antiviral signaling), and TRIF (TIR domain-containing adaptor inducing IFN-β) mediate the recruitment of IRF-3 through a conserved
p
L
x
IS motif. Here we show that the
p
L
x
IS motif of phosphorylated STING, MAVS, and TRIF binds to IRF-3 in a similar manner, whereas residues upstream of the motif confer specificity. The structure of the IRF-3 phosphomimetic mutant S386/396E bound to the cAMP response element binding protein (CREB)-binding protein reveals that the
p
L
x
IS motif also mediates IRF-3 dimerization and activation. Moreover, rotavirus NSP1 (nonstructural protein 1) employs a
p
L
x
IS motif to target IRF-3 for degradation, but phosphorylation of NSP1 is not required for its activity. These results suggest a concerted mechanism for the recruitment and activation of IRF-3 that can be subverted by viral proteins to evade innate immune responses. Type I IFNs are key cytokines mediating innate antiviral immunity. cGMP-AMP synthase, ritinoic acid-inducible protein 1 (RIG-I)-like receptors, and Toll-like receptors recognize microbial double-stranded (ds)DNA, dsRNA, and LPS to induce the expression of type I IFNs. These signaling pathways converge at the recruitment and activation of the transcription factor IRF-3 (IFN regulatory factor 3). The adaptor proteins STING (stimulator of IFN genes), MAVS (mitochondrial antiviral signaling), and TRIF (TIR domain-containing adaptor inducing IFN-β) mediate the recruitment of IRF-3 through a conserved pLxIS motif. Here we show that the pLxIS motif of phosphorylated STING, MAVS, and TRIF binds to IRF-3 in a similar manner, whereas residues upstream of the motif confer specificity. The structure of the IRF-3 phosphomimetic mutant S386/396E bound to the cAMP response element binding protein (CREB)-binding protein reveals that the pLxIS motif also mediates IRF-3 dimerization and activation. Moreover, rotavirus NSP1 (nonstructural protein 1) employs a pLxIS motif to target IRF-3 for degradation, but phosphorylation of NSP1 is not required for its activity. These results suggest a concerted mechanism for the recruitment and activation of IRF-3 that can be subverted by viral proteins to evade innate immune responses.Type I IFNs are key cytokines mediating innate antiviral immunity. cGMP-AMP synthase, ritinoic acid-inducible protein 1 (RIG-I)-like receptors, and Toll-like receptors recognize microbial double-stranded (ds)DNA, dsRNA, and LPS to induce the expression of type I IFNs. These signaling pathways converge at the recruitment and activation of the transcription factor IRF-3 (IFN regulatory factor 3). The adaptor proteins STING (stimulator of IFN genes), MAVS (mitochondrial antiviral signaling), and TRIF (TIR domain-containing adaptor inducing IFN-β) mediate the recruitment of IRF-3 through a conserved pLxIS motif. Here we show that the pLxIS motif of phosphorylated STING, MAVS, and TRIF binds to IRF-3 in a similar manner, whereas residues upstream of the motif confer specificity. The structure of the IRF-3 phosphomimetic mutant S386/396E bound to the cAMP response element binding protein (CREB)-binding protein reveals that the pLxIS motif also mediates IRF-3 dimerization and activation. Moreover, rotavirus NSP1 (nonstructural protein 1) employs a pLxIS motif to target IRF-3 for degradation, but phosphorylation of NSP1 is not required for its activity. These results suggest a concerted mechanism for the recruitment and activation of IRF-3 that can be subverted by viral proteins to evade innate immune responses. Type I IFNs are key cytokines mediating innate antiviral immunity. cGMP-AMP synthase, ritinoic acid-inducible protein 1 (RIG-I)-like receptors, and Toll-like receptors recognize microbial double-stranded (ds)DNA, dsRNA, and LPS to induce the expression of type I IFNs. These signaling pathways converge at the recruitment and activation of the transcription factor IRF-3 (IFN regulatory factor 3). The adaptor proteins STING (stimulator of IFN genes), MAVS (mitochondrial antiviral signaling), and TRIF (TIR domain-containing adaptor inducing IFN- beta ) mediate the recruitment of IRF-3 through a conserved pLxIS motif. Here we show that the pLxIS motif of phosphorylated STING, MAVS, and TRIF binds to IRF-3 in a similar manner, whereas residues upstream of the motif confer specificity. The structure of the IRF-3 phosphomimetic mutant S386/396E bound to the cAMP response element binding protein (CREB)-binding protein reveals that the pLxIS motif also mediates IRF-3 dimerization and activation. Moreover, rotavirus NSP1 (nonstructural protein 1) employs a pLxIS motif to target IRF-3 for degradation, but phosphorylation of NSP1 is not required for its activity. These results suggest a concerted mechanism for the recruitment and activation of IRF-3 that can be subverted by viral proteins to evade innate immune responses. Type I IFNs are key cytokines mediating innate antiviral immunity. cGMP-AMP synthase, ritinoic acid-inducible protein 1 (RIG-I)–like receptors, and Toll-like receptors recognize microbial double-stranded (ds)DNA, dsRNA, and LPS to induce the expression of type I IFNs. These signaling pathways converge at the recruitment and activation of the transcription factor IRF-3 (IFN regulatory factor 3). The adaptor proteins STING (stimulator of IFN genes), MAVS (mitochondrial antiviral signaling), and TRIF (TIR domain-containing adaptor inducing IFN-β) mediate the recruitment of IRF-3 through a conserved pLxIS motif. Here we show that the pLxIS motif of phosphorylated STING, MAVS, and TRIF binds to IRF-3 in a similar manner, whereas residues upstream of the motif confer specificity. The structure of the IRF-3 phosphomimetic mutant S386/396E bound to the cAMP response element binding protein (CREB)-binding protein reveals that the pLxIS motif also mediates IRF-3 dimerization and activation. Moreover, rotavirus NSP1 (nonstructural protein 1) employs a pLxIS motif to target IRF-3 for degradation, but phosphorylation of NSP1 is not required for its activity. These results suggest a concerted mechanism for the recruitment and activation of IRF-3 that can be subverted by viral proteins to evade innate immune responses. Type I IFNs are key cytokines mediating innate antiviral immunity. cGMP-AMP synthase, ritinoic acid-inducible protein 1 (RIG-I)–like receptors, and Toll-like receptors recognize microbial double-stranded (ds)DNA, dsRNA, and LPS to induce the expression of type I IFNs. These signaling pathways converge at the recruitment and activation of the transcription factor IRF-3 (IFN regulatory factor 3). The adaptor proteins STING (stimulator of IFN genes), MAVS (mitochondrial antiviral signaling), and TRIF (TIR domain-containing adaptor inducing IFN-β) mediate the recruitment of IRF-3 through a conserved pLxIS motif. Here in this paper, we show that the pLxIS motif of phosphorylated STING, MAVS, and TRIF binds to IRF-3 in a similar manner, whereas residues upstream of the motif confer specificity. The structure of the IRF-3 phosphomimetic mutant S386/396E bound to the cAMP response element binding protein (CREB)-binding protein reveals that the pLxIS motif also mediates IRF-3 dimerization and activation. Moreover, rotavirus NSP1 (nonstructural protein 1) employs a pLxIS motif to target IRF-3 for degradation, but phosphorylation of NSP1 is not required for its activity. These results suggest a concerted mechanism for the recruitment and activation of IRF-3 that can be subverted by viral proteins to evade innate immune responses. |
| Author | Li, Pingwei Shu, Chang Zhao, Baoyu Du, Fenglei Shelton, Catherine L. Gao, Xinsheng Herr, Andrew B. Ji, Jun-Yuan Sankaran, Banumathi |
| Author_xml | – sequence: 1 givenname: Baoyu surname: Zhao fullname: Zhao, Baoyu organization: Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843 – sequence: 2 givenname: Chang surname: Shu fullname: Shu, Chang organization: Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843 – sequence: 3 givenname: Xinsheng surname: Gao fullname: Gao, Xinsheng organization: Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M University Health Science Center, College Station, TX 77843 – sequence: 4 givenname: Banumathi surname: Sankaran fullname: Sankaran, Banumathi organization: Berkeley Center for Structural Biology, Physical Biosciences Division, Lawrence Berkeley Laboratory, Berkeley, CA 94720 – sequence: 5 givenname: Fenglei surname: Du fullname: Du, Fenglei organization: Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843 – sequence: 6 givenname: Catherine L. surname: Shelton fullname: Shelton, Catherine L. organization: Division of Infectious Diseases, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229 – sequence: 7 givenname: Andrew B. surname: Herr fullname: Herr, Andrew B. organization: Division of Infectious Diseases, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229 – sequence: 8 givenname: Jun-Yuan surname: Ji fullname: Ji, Jun-Yuan organization: Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M University Health Science Center, College Station, TX 77843 – sequence: 9 givenname: Pingwei surname: Li fullname: Li, Pingwei organization: Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843 |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27302953$$D View this record in MEDLINE/PubMed https://www.osti.gov/servlets/purl/1379399$$D View this record in Osti.gov |
| BookMark | eNqFks1rFTEUxYNU7OvTtSsl2I2bafM1yWQjSGm1UBD8WIdM5o7NYyZ5JplC_3vzfK3VgrjKIr9zknPPPUIHIQZA6CUlJ5QofroNNp9QSTiTmlL-BK0o0bSRQpMDtCKEqaYTTByio5w3hBDdduQZOmSKE6ZbvkLDl5IWV5ZkJ9zb7DMeY8IuBgepwIATuLT4MkMo2IYBW1f8jS0-BhxHfPn5ouG4v8U-BFsA-3leAmA72G2pNtsUC_iQn6Ono50yvLg71-jbxfnXs4_N1acPl2fvrxrXSl0aKykRzhEnQMpBDCNrZUdb0KSXvQMxwKDUqPu-lRL0yCzvOiXHXlM5KMJ6vkbv9r7bpZ9hcPXTNZfZJj_bdGui9ebvm-Cvzfd4Y4SmgkpdDd7sDWIu3mTnC7jrOowArhjKleZ6B729eyXFHwvkYmafHUyTDRCXbGjHGROtkuL_qNKqFYxzVtHjR-gmLinUce0oXR27Wtgavf4z4e9o94VWoN0DLsWcE4ymhvjVVw3sJ0OJ2S2O2S2OeVicqjt9pLu3_rfi1V6xybXrh59IoQgnHf8J5HHPtQ |
| CitedBy_id | crossref_primary_10_1002_eji_202350386 crossref_primary_10_1016_j_celrep_2023_112306 crossref_primary_10_4155_fmc_2017_0322 crossref_primary_10_1002_ajoc_202200597 crossref_primary_10_1038_s41420_023_01735_0 crossref_primary_10_1038_s41586_022_05354_0 crossref_primary_10_2147_JIR_S465978 crossref_primary_10_3389_fimmu_2022_808607 crossref_primary_10_1038_s41586_019_1000_2 crossref_primary_10_1111_febs_16137 crossref_primary_10_1128_mBio_01213_17 crossref_primary_10_1186_s13567_025_01474_3 crossref_primary_10_1146_annurev_biochem_040320_101629 crossref_primary_10_1093_jmcb_mjac042 crossref_primary_10_1002_med_22016 crossref_primary_10_1128_mbio_01308_22 crossref_primary_10_1016_j_bcp_2020_113831 crossref_primary_10_3389_fimmu_2020_624597 crossref_primary_10_4049_jimmunol_2000026 crossref_primary_10_1073_pnas_2100383118 crossref_primary_10_1038_s41594_023_00933_9 crossref_primary_10_3390_biom13091344 crossref_primary_10_3390_antiox11122485 crossref_primary_10_1021_acschembio_9b00307 crossref_primary_10_15252_embj_2022112907 crossref_primary_10_1016_j_apsb_2025_03_011 crossref_primary_10_1038_s41423_022_00967_x crossref_primary_10_1016_j_immuni_2024_12_002 crossref_primary_10_1016_j_it_2022_04_011 crossref_primary_10_1038_s41586_019_1228_x crossref_primary_10_1038_s41586_018_0135_x crossref_primary_10_1002_bies_202300042 crossref_primary_10_1038_s41586_022_05452_z crossref_primary_10_1016_j_jad_2024_10_126 crossref_primary_10_1038_s41392_022_01224_3 crossref_primary_10_3389_fimmu_2022_812774 crossref_primary_10_1016_j_tcb_2022_11_001 crossref_primary_10_1016_j_apsb_2021_05_011 crossref_primary_10_3389_fphar_2024_1383000 crossref_primary_10_1073_pnas_1718426115 crossref_primary_10_3389_fimmu_2023_1231057 crossref_primary_10_3390_biomedicines13030571 crossref_primary_10_1038_s41586_020_2282_0 crossref_primary_10_1093_nar_gkaa873 crossref_primary_10_1093_nar_gkab689 crossref_primary_10_1073_pnas_2305420120 crossref_primary_10_1073_pnas_1618424114 crossref_primary_10_1016_j_coi_2020_04_002 crossref_primary_10_1126_scisignal_aaw4673 crossref_primary_10_1371_journal_pntd_0011001 crossref_primary_10_3390_v12070733 crossref_primary_10_1016_j_cbi_2020_109031 crossref_primary_10_1111_cns_14671 crossref_primary_10_1016_j_bcp_2022_115026 crossref_primary_10_1016_j_celrep_2019_03_098 crossref_primary_10_1371_journal_ppat_1012609 crossref_primary_10_1021_acschembio_1c00912 crossref_primary_10_1021_acs_jcim_2c00595 crossref_primary_10_1016_j_celrep_2024_114678 crossref_primary_10_1002_wcms_1397 crossref_primary_10_1016_j_molcel_2017_10_032 crossref_primary_10_1016_j_ejmech_2020_113113 crossref_primary_10_1002_iub_1566 crossref_primary_10_1038_s41556_021_00659_0 crossref_primary_10_3390_v13040589 crossref_primary_10_1080_15592294_2023_2276371 crossref_primary_10_1080_17568919_2024_2383164 crossref_primary_10_1073_pnas_2105465118 crossref_primary_10_1093_nar_gkx1077 crossref_primary_10_1016_j_celrep_2023_112185 crossref_primary_10_1016_j_molimm_2017_12_007 crossref_primary_10_1073_pnas_2200285119 crossref_primary_10_1097_QAD_0000000000003111 crossref_primary_10_3390_v13122369 crossref_primary_10_1016_j_ejmech_2023_115941 crossref_primary_10_1111_febs_70023 crossref_primary_10_1080_08820139_2024_2392587 crossref_primary_10_1073_pnas_2200230119 crossref_primary_10_1128_spectrum_01883_21 crossref_primary_10_1371_journal_ppat_1011742 crossref_primary_10_1111_ejn_15967 crossref_primary_10_1016_j_drudis_2023_103694 crossref_primary_10_1038_s41392_022_01252_z crossref_primary_10_1007_s11684_023_1026_6 crossref_primary_10_3390_ani13162573 crossref_primary_10_1074_jbc_RA120_015283 crossref_primary_10_3389_fcvm_2022_965726 crossref_primary_10_1016_j_bcp_2022_115246 crossref_primary_10_1038_s41580_020_0244_x crossref_primary_10_1016_j_bbrc_2024_149945 crossref_primary_10_1016_j_bbrc_2024_150326 crossref_primary_10_3389_fimmu_2020_02064 crossref_primary_10_1096_fj_202000600RR crossref_primary_10_2147_OTT_S298958 crossref_primary_10_1093_nar_gkab550 crossref_primary_10_1002_1873_3468_12762 crossref_primary_10_3389_fimmu_2023_1200245 crossref_primary_10_1016_j_molcel_2024_05_030 crossref_primary_10_1016_j_smim_2021_101580 crossref_primary_10_1038_s41467_023_39410_8 crossref_primary_10_12677_hjbm_2024_143056 crossref_primary_10_1016_j_heliyon_2024_e33093 crossref_primary_10_1016_j_jmb_2021_167320 crossref_primary_10_1038_s41594_023_00988_8 crossref_primary_10_1631_jzus_B2000808 crossref_primary_10_1186_s12985_021_01548_6 crossref_primary_10_1021_acs_jcim_2c00026 crossref_primary_10_1038_s41586_018_0621_1 crossref_primary_10_1080_22221751_2020_1870414 crossref_primary_10_1038_s41421_022_00481_4 crossref_primary_10_3389_fimmu_2017_01431 crossref_primary_10_1016_j_xjidi_2022_100176 crossref_primary_10_1146_annurev_biochem_061516_044813 crossref_primary_10_1111_liv_70063 crossref_primary_10_1016_S1875_5364_23_60381_4 crossref_primary_10_1016_j_heliyon_2024_e29338 crossref_primary_10_1016_j_tcb_2020_01_010 crossref_primary_10_3390_vaccines8030369 crossref_primary_10_2222_jsv_67_99 crossref_primary_10_1038_s12276_023_00965_7 crossref_primary_10_1002_mco2_511 crossref_primary_10_1016_j_bbcan_2021_188661 crossref_primary_10_3390_vetsci7010014 |
| Cites_doi | 10.1016/j.cell.2010.01.022 10.1128/JVI.01146-13 10.1038/nri2079 10.1126/scisignal.2002521 10.1016/j.coi.2014.12.012 10.3390/v1031035 10.1111/j.1365-2443.2010.01427.x 10.1126/science.1087262 10.1016/j.immuni.2007.08.012 10.1038/nsb1002 10.1016/j.str.2013.04.025 10.1016/S0076-6879(97)76066-X 10.1016/j.immuni.2013.10.019 10.1126/science.1229963 10.4049/jimmunol.169.12.6668 10.1126/science.1232458 10.1016/j.immuni.2006.08.007 10.1016/j.cytogfr.2014.06.006 10.1074/jbc.M703019200 10.1016/j.cell.2007.05.019 10.1107/S0907444910007493 10.1016/j.jmb.2008.03.050 10.1107/S0907444910045749 10.1146/annurev-immunol-032713-120231 10.1038/nsmb.1496 10.1016/j.molcel.2013.05.022 10.1073/pnas.0408376102 10.1038/nature12306 10.1084/jem.20142274 10.1111/j.1600-065X.2011.01052.x 10.1126/science.aaa2630 10.1016/j.immuni.2006.08.009 10.1038/nature10429 10.1016/j.cell.2005.08.012 10.1107/S0907444909052925 10.1016/j.cell.2013.04.046 10.1016/j.cell.2013.07.023 10.1016/j.it.2013.10.010 10.1146/annurev-immunol-032713-120156 10.1016/j.molcel.2007.04.022 10.1016/j.str.2005.06.011 |
| ContentType | Journal Article |
| Copyright | Volumes 1–89 and 106–113, copyright as a collective work only; author(s) retains copyright to individual articles Copyright National Academy of Sciences Jun 14, 2016 |
| Copyright_xml | – notice: Volumes 1–89 and 106–113, copyright as a collective work only; author(s) retains copyright to individual articles – notice: Copyright National Academy of Sciences Jun 14, 2016 |
| CorporateAuthor | Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States) |
| CorporateAuthor_xml | – name: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States) |
| DBID | AAYXX CITATION CGR CUY CVF ECM EIF NPM 7QG 7QL 7QP 7QR 7SN 7SS 7T5 7TK 7TM 7TO 7U9 8FD C1K FR3 H94 M7N P64 RC3 7X8 OIOZB OTOTI 5PM |
| DOI | 10.1073/pnas.1603269113 |
| DatabaseName | CrossRef Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed Animal Behavior Abstracts Bacteriology Abstracts (Microbiology B) Calcium & Calcified Tissue Abstracts Chemoreception Abstracts Ecology Abstracts Entomology Abstracts (Full archive) Immunology Abstracts Neurosciences Abstracts Nucleic Acids Abstracts Oncogenes and Growth Factors Abstracts Virology and AIDS Abstracts Technology Research Database Environmental Sciences and Pollution Management Engineering Research Database AIDS and Cancer Research Abstracts Algology Mycology and Protozoology Abstracts (Microbiology C) Biotechnology and BioEngineering Abstracts Genetics Abstracts MEDLINE - Academic OSTI.GOV - Hybrid OSTI.GOV PubMed Central (Full Participant titles) |
| DatabaseTitle | CrossRef MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) Virology and AIDS Abstracts Oncogenes and Growth Factors Abstracts Technology Research Database Nucleic Acids Abstracts Ecology Abstracts Neurosciences Abstracts Biotechnology and BioEngineering Abstracts Environmental Sciences and Pollution Management Entomology Abstracts Genetics Abstracts Animal Behavior Abstracts Bacteriology Abstracts (Microbiology B) Algology Mycology and Protozoology Abstracts (Microbiology C) AIDS and Cancer Research Abstracts Chemoreception Abstracts Immunology Abstracts Engineering Research Database Calcium & Calcified Tissue Abstracts MEDLINE - Academic |
| DatabaseTitleList | MEDLINE - Academic AIDS and Cancer Research Abstracts MEDLINE CrossRef Virology and AIDS Abstracts |
| Database_xml | – sequence: 1 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: EIF name: MEDLINE url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search sourceTypes: Index Database |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Sciences (General) |
| DocumentTitleAlternate | Structural basis of IRF-3 recruitment |
| EISSN | 1091-6490 |
| EndPage | E3412 |
| ExternalDocumentID | PMC4914169 1379399 4099154961 27302953 10_1073_pnas_1603269113 26470308 |
| Genre | Research Support, U.S. Gov't, Non-P.H.S Research Support, Non-U.S. Gov't Journal Article Research Support, N.I.H., Extramural Feature |
| GrantInformation_xml | – fundername: NIAID NIH HHS grantid: R01 AI087741 – fundername: NIDDK NIH HHS grantid: R01 DK095013 – fundername: Cancer Prevention and Research Institute of Texas (CPRIT) grantid: RP150454 – fundername: HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) grantid: AI087741 – fundername: Welch Foundation grantid: A-1816 |
| GroupedDBID | --- -DZ -~X .55 0R~ 123 29P 2AX 2FS 2WC 4.4 53G 5RE 5VS 85S AACGO AAFWJ AANCE ABBHK ABOCM ABPLY ABPPZ ABTLG ABXSQ ABZEH ACGOD ACHIC ACIWK ACNCT ACPRK ADQXQ ADULT AENEX AEUPB AEXZC AFFNX AFRAH ALMA_UNASSIGNED_HOLDINGS AQVQM BKOMP CS3 D0L DCCCD DIK DU5 E3Z EBS EJD F5P FRP GX1 H13 HH5 HYE IPSME JAAYA JBMMH JENOY JHFFW JKQEH JLS JLXEF JPM JSG JST KQ8 L7B LU7 N9A N~3 O9- OK1 PNE PQQKQ R.V RHI RNA RNS RPM RXW SA0 SJN TAE TN5 UKR W8F WH7 WOQ WOW X7M XSW Y6R YBH YKV YSK ZCA ~02 ~KM AAYXX AFOSN CITATION CGR CUY CVF ECM EIF NPM 7QG 7QL 7QP 7QR 7SN 7SS 7T5 7TK 7TM 7TO 7U9 8FD C1K FR3 H94 M7N P64 RC3 7X8 79B AAPBV ABPTK ADZLD ASUFR DNJUQ DOOOF DWIUU JSODD OIOZB OTOTI PQEST RHF VQA ZA5 5PM |
| ID | FETCH-LOGICAL-c569t-a6104cc0c4e66d4df256815e90b6bce4ded77f9bb566e9f2a38876fb916d702b3 |
| ISSN | 0027-8424 1091-6490 |
| IngestDate | Thu Aug 21 18:02:16 EDT 2025 Mon Jul 03 03:56:41 EDT 2023 Thu Jul 10 17:28:54 EDT 2025 Fri Jul 11 16:06:31 EDT 2025 Mon Jun 30 07:50:50 EDT 2025 Thu Apr 03 07:00:33 EDT 2025 Tue Jul 01 03:19:15 EDT 2025 Thu Apr 24 22:57:06 EDT 2025 Sun Aug 24 12:10:37 EDT 2025 |
| IsDoiOpenAccess | true |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 24 |
| Keywords | type I interferon crystal structure transcription factor signaling innate immunity |
| Language | English |
| LinkModel | OpenURL |
| MergedId | FETCHMERGED-LOGICAL-c569t-a6104cc0c4e66d4df256815e90b6bce4ded77f9bb566e9f2a38876fb916d702b3 |
| Notes | SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 AC02-05CH11231 USDOE Office of Science (SC), Basic Energy Sciences (BES) 1B.Z. and C.S. contributed equally to this work. Edited by Pamela J. Bjorkman, California Institute of Technology, Pasadena, CA, and approved April 27, 2016 (received for review February 29, 2016) Author contributions: B.Z., C.S, and P.L. designed research; B.Z., C.S., X.G., B.S., F.D., C.L.S., A.B.H., and P.L. performed research; B.Z., C.S., A.B.H., and P.L. analyzed data; and B.Z., C.S., X.G., F.D., A.B.H., J.-Y.J., and P.L. wrote the paper. |
| OpenAccessLink | https://www.osti.gov/servlets/purl/1379399 |
| PMID | 27302953 |
| PQID | 1799224895 |
| PQPubID | 42026 |
| ParticipantIDs | pubmedcentral_primary_oai_pubmedcentral_nih_gov_4914169 osti_scitechconnect_1379399 proquest_miscellaneous_1832245764 proquest_miscellaneous_1797542332 proquest_journals_1799224895 pubmed_primary_27302953 crossref_citationtrail_10_1073_pnas_1603269113 crossref_primary_10_1073_pnas_1603269113 jstor_primary_26470308 |
| ProviderPackageCode | CITATION AAYXX |
| PublicationCentury | 2000 |
| PublicationDate | 2016-06-14 |
| PublicationDateYYYYMMDD | 2016-06-14 |
| PublicationDate_xml | – month: 06 year: 2016 text: 2016-06-14 day: 14 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States – name: Washington |
| PublicationSeriesTitle | PNAS Plus |
| PublicationTitle | Proceedings of the National Academy of Sciences - PNAS |
| PublicationTitleAlternate | Proc Natl Acad Sci U S A |
| PublicationYear | 2016 |
| Publisher | National Academy of Sciences National Academy of Sciences, Washington, DC (United States) |
| Publisher_xml | – name: National Academy of Sciences – name: National Academy of Sciences, Washington, DC (United States) |
| References | Sun L (e_1_3_4_12_2) 2013; 339 Takeuchi O (e_1_3_4_1_2) 2010; 140 Panne D (e_1_3_4_30_2) 2007; 282 Qin BY (e_1_3_4_41_2) 2005; 13 Chen W (e_1_3_4_29_2) 2008; 379 Wu J (e_1_3_4_15_2) 2013; 339 Escalante CR (e_1_3_4_36_2) 2007; 26 Takahasi K (e_1_3_4_33_2) 2010; 15 Ablasser A (e_1_3_4_9_2) 2013; 498 Tanaka Y (e_1_3_4_16_2) 2012; 5 Qin BY (e_1_3_4_27_2) 2003; 10 Burdette DL (e_1_3_4_28_2) 2011; 478 Pichlmair A (e_1_3_4_4_2) 2007; 27 Barber GN (e_1_3_4_7_2) 2014; 35 Yoneyama M (e_1_3_4_19_2) 2015; 32 Liu S (e_1_3_4_23_2) 2015; 347 Andersen LL (e_1_3_4_31_2) 2015; 212 Arnold MM (e_1_3_4_25_2) 2009; 1 Barro M (e_1_3_4_24_2) 2005; 102 Shu C (e_1_3_4_34_2) 2013; 21 Shu C (e_1_3_4_8_2) 2014; 25 Yamamoto M (e_1_3_4_21_2) 2003; 301 Seth RB (e_1_3_4_18_2) 2005; 122 O’Neill LA (e_1_3_4_22_2) 2007; 7 Emsley P (e_1_3_4_40_2) 2010; 66 Honda K (e_1_3_4_17_2) 2006; 25 Chen W (e_1_3_4_32_2) 2008; 15 Gao P (e_1_3_4_10_2) 2013; 153 Yamamoto M (e_1_3_4_20_2) 2002; 169 Arnold MM (e_1_3_4_26_2) 2013; 87 Adams PD (e_1_3_4_39_2) 2010; 66 Stetson DB (e_1_3_4_5_2) 2006; 25 Panne D (e_1_3_4_35_2) 2007; 129 Winn MD (e_1_3_4_38_2) 2011; 67 Zhang X (e_1_3_4_11_2) 2013; 51 Gao P (e_1_3_4_14_2) 2013; 154 e_1_3_4_37_2 Schneider WM (e_1_3_4_6_2) 2014; 32 Li X (e_1_3_4_13_2) 2013; 39 Wu J (e_1_3_4_2_2) 2014; 32 Kato H (e_1_3_4_3_2) 2011; 243 |
| References_xml | – volume: 140 start-page: 805 year: 2010 ident: e_1_3_4_1_2 article-title: Pattern recognition receptors and inflammation publication-title: Cell doi: 10.1016/j.cell.2010.01.022 – volume: 87 start-page: 9813 year: 2013 ident: e_1_3_4_26_2 article-title: Rotavirus NSP1 mediates degradation of interferon regulatory factors through targeting of the dimerization domain publication-title: J Virol doi: 10.1128/JVI.01146-13 – volume: 7 start-page: 353 year: 2007 ident: e_1_3_4_22_2 article-title: The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling publication-title: Nat Rev Immunol doi: 10.1038/nri2079 – volume: 5 start-page: ra20 year: 2012 ident: e_1_3_4_16_2 article-title: STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway publication-title: Sci Signal doi: 10.1126/scisignal.2002521 – volume: 32 start-page: 48 year: 2015 ident: e_1_3_4_19_2 article-title: Viral RNA detection by RIG-I-like receptors publication-title: Curr Opin Immunol doi: 10.1016/j.coi.2014.12.012 – volume: 1 start-page: 1035 year: 2009 ident: e_1_3_4_25_2 article-title: Rotavirus antagonism of the innate immune response publication-title: Viruses doi: 10.3390/v1031035 – volume: 15 start-page: 901 year: 2010 ident: e_1_3_4_33_2 article-title: Ser386 phosphorylation of transcription factor IRF-3 induces dimerization and association with CBP/p300 without overall conformational change publication-title: Genes Cells doi: 10.1111/j.1365-2443.2010.01427.x – volume: 301 start-page: 640 year: 2003 ident: e_1_3_4_21_2 article-title: Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway publication-title: Science doi: 10.1126/science.1087262 – volume: 27 start-page: 370 year: 2007 ident: e_1_3_4_4_2 article-title: Innate recognition of viruses publication-title: Immunity doi: 10.1016/j.immuni.2007.08.012 – volume: 10 start-page: 913 year: 2003 ident: e_1_3_4_27_2 article-title: Crystal structure of IRF-3 reveals mechanism of autoinhibition and virus-induced phosphoactivation publication-title: Nat Struct Biol doi: 10.1038/nsb1002 – volume: 21 start-page: 1137 year: 2013 ident: e_1_3_4_34_2 article-title: Structural insights into the functions of TBK1 in innate antimicrobial immunity publication-title: Structure doi: 10.1016/j.str.2013.04.025 – ident: e_1_3_4_37_2 doi: 10.1016/S0076-6879(97)76066-X – volume: 39 start-page: 1019 year: 2013 ident: e_1_3_4_13_2 article-title: Cyclic GMP-AMP synthase is activated by double-stranded DNA-induced oligomerization publication-title: Immunity doi: 10.1016/j.immuni.2013.10.019 – volume: 339 start-page: 826 year: 2013 ident: e_1_3_4_15_2 article-title: Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA publication-title: Science doi: 10.1126/science.1229963 – volume: 169 start-page: 6668 year: 2002 ident: e_1_3_4_20_2 article-title: Cutting edge: A novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling publication-title: J Immunol doi: 10.4049/jimmunol.169.12.6668 – volume: 339 start-page: 786 year: 2013 ident: e_1_3_4_12_2 article-title: Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway publication-title: Science doi: 10.1126/science.1232458 – volume: 25 start-page: 373 year: 2006 ident: e_1_3_4_5_2 article-title: Type I interferons in host defense publication-title: Immunity doi: 10.1016/j.immuni.2006.08.007 – volume: 25 start-page: 641 year: 2014 ident: e_1_3_4_8_2 article-title: The mechanism of double-stranded DNA sensing through the cGAS-STING pathway publication-title: Cytokine Growth Factor Rev doi: 10.1016/j.cytogfr.2014.06.006 – volume: 282 start-page: 22816 year: 2007 ident: e_1_3_4_30_2 article-title: Interferon regulatory factor 3 is regulated by a dual phosphorylation-dependent switch publication-title: J Biol Chem doi: 10.1074/jbc.M703019200 – volume: 129 start-page: 1111 year: 2007 ident: e_1_3_4_35_2 article-title: An atomic model of the interferon-beta enhanceosome publication-title: Cell doi: 10.1016/j.cell.2007.05.019 – volume: 66 start-page: 486 year: 2010 ident: e_1_3_4_40_2 article-title: Features and development of Coot publication-title: Acta Crystallogr D Biol Crystallogr doi: 10.1107/S0907444910007493 – volume: 379 start-page: 251 year: 2008 ident: e_1_3_4_29_2 article-title: Contribution of Ser386 and Ser396 to activation of interferon regulatory factor 3 publication-title: J Mol Biol doi: 10.1016/j.jmb.2008.03.050 – volume: 67 start-page: 235 year: 2011 ident: e_1_3_4_38_2 article-title: Overview of the CCP4 suite and current developments publication-title: Acta Crystallogr D Biol Crystallogr doi: 10.1107/S0907444910045749 – volume: 32 start-page: 513 year: 2014 ident: e_1_3_4_6_2 article-title: Interferon-stimulated genes: A complex web of host defenses publication-title: Annu Rev Immunol doi: 10.1146/annurev-immunol-032713-120231 – volume: 15 start-page: 1213 year: 2008 ident: e_1_3_4_32_2 article-title: Insights into interferon regulatory factor activation from the crystal structure of dimeric IRF5 publication-title: Nat Struct Mol Biol doi: 10.1038/nsmb.1496 – volume: 51 start-page: 226 year: 2013 ident: e_1_3_4_11_2 article-title: Cyclic GMP-AMP containing mixed phosphodiester linkages is an endogenous high-affinity ligand for STING publication-title: Mol Cell doi: 10.1016/j.molcel.2013.05.022 – volume: 102 start-page: 4114 year: 2005 ident: e_1_3_4_24_2 article-title: Rotavirus nonstructural protein 1 subverts innate immune response by inducing degradation of IFN regulatory factor 3 publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.0408376102 – volume: 498 start-page: 380 year: 2013 ident: e_1_3_4_9_2 article-title: cGAS produces a 2′-5′-linked cyclic dinucleotide second messenger that activates STING publication-title: Nature doi: 10.1038/nature12306 – volume: 212 start-page: 1371 year: 2015 ident: e_1_3_4_31_2 article-title: Functional IRF3 deficiency in a patient with herpes simplex encephalitis publication-title: J Exp Med doi: 10.1084/jem.20142274 – volume: 243 start-page: 91 year: 2011 ident: e_1_3_4_3_2 article-title: RIG-I-like receptors: Cytoplasmic sensors for non-self RNA publication-title: Immunol Rev doi: 10.1111/j.1600-065X.2011.01052.x – volume: 347 start-page: aaa2630 year: 2015 ident: e_1_3_4_23_2 article-title: Phosphorylation of innate immune adaptor proteins MAVS, STING, and TRIF induces IRF3 activation publication-title: Science doi: 10.1126/science.aaa2630 – volume: 25 start-page: 349 year: 2006 ident: e_1_3_4_17_2 article-title: Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors publication-title: Immunity doi: 10.1016/j.immuni.2006.08.009 – volume: 478 start-page: 515 year: 2011 ident: e_1_3_4_28_2 article-title: STING is a direct innate immune sensor of cyclic di-GMP publication-title: Nature doi: 10.1038/nature10429 – volume: 122 start-page: 669 year: 2005 ident: e_1_3_4_18_2 article-title: Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3 publication-title: Cell doi: 10.1016/j.cell.2005.08.012 – volume: 66 start-page: 213 year: 2010 ident: e_1_3_4_39_2 article-title: PHENIX: A comprehensive Python-based system for macromolecular structure solution publication-title: Acta Crystallogr D Biol Crystallogr doi: 10.1107/S0907444909052925 – volume: 153 start-page: 1094 year: 2013 ident: e_1_3_4_10_2 article-title: Cyclic [G(2′,5′)pA(3′,5′)p] is the metazoan second messenger produced by DNA-activated cyclic GMP-AMP synthase publication-title: Cell doi: 10.1016/j.cell.2013.04.046 – volume: 154 start-page: 748 year: 2013 ident: e_1_3_4_14_2 article-title: Structure-function analysis of STING activation by c[G(2′,5′)pA(3′,5′)p] and targeting by antiviral DMXAA publication-title: Cell doi: 10.1016/j.cell.2013.07.023 – volume: 35 start-page: 88 year: 2014 ident: e_1_3_4_7_2 article-title: STING-dependent cytosolic DNA sensing pathways publication-title: Trends Immunol doi: 10.1016/j.it.2013.10.010 – volume: 32 start-page: 461 year: 2014 ident: e_1_3_4_2_2 article-title: Innate immune sensing and signaling of cytosolic nucleic acids publication-title: Annu Rev Immunol doi: 10.1146/annurev-immunol-032713-120156 – volume: 26 start-page: 703 year: 2007 ident: e_1_3_4_36_2 article-title: Structure of IRF-3 bound to the PRDIII-I regulatory element of the human interferon-beta enhancer publication-title: Mol Cell doi: 10.1016/j.molcel.2007.04.022 – volume: 13 start-page: 1269 year: 2005 ident: e_1_3_4_41_2 article-title: Crystal structure of IRF-3 in complex with CBP publication-title: Structure doi: 10.1016/j.str.2005.06.011 |
| SSID | ssj0009580 |
| Score | 2.5503862 |
| Snippet | Type I IFNs are key cytokines mediating innate antiviral immunity. cGMP-AMP synthase, ritinoic acid-inducible protein 1 (RIG-I)–like receptors, and Toll-like... Type I IFNs are key cytokines involved in antiviral immunity. A number of innate sensing pathways regulate the induction of type I IFNs. These pathways... Type I IFNs are key cytokines mediating innate antiviral immunity. cGMP-AMP synthase, ritinoic acid-inducible protein 1 (RIG-I)-like receptors, and Toll-like... |
| SourceID | pubmedcentral osti proquest pubmed crossref jstor |
| SourceType | Open Access Repository Aggregation Database Index Database Enrichment Source Publisher |
| StartPage | E3403 |
| SubjectTerms | 60 APPLIED LIFE SCIENCES Adaptor Proteins, Signal Transducing - chemistry Adaptor Proteins, Signal Transducing - genetics Adaptor Proteins, Signal Transducing - immunology Adaptor Proteins, Vesicular Transport - chemistry Adaptor Proteins, Vesicular Transport - genetics Adaptor Proteins, Vesicular Transport - immunology Amino Acid Motifs BASIC BIOLOGICAL SCIENCES Binding sites Biological Sciences CREB-Binding Protein - chemistry CREB-Binding Protein - genetics CREB-Binding Protein - immunology crystal structure Cytokines Gene expression Humans Immune Evasion Immunity, Innate innate immunity Interferon Regulatory Factor-3 - chemistry Interferon Regulatory Factor-3 - genetics Interferon Regulatory Factor-3 - immunology Membrane Proteins - chemistry Membrane Proteins - genetics Membrane Proteins - immunology Phosphorylation PNAS Plus Protein Domains Proteins Reoviridae Rotavirus - chemistry Rotavirus - genetics Rotavirus - immunology Rotavirus Infections - genetics Rotavirus Infections - immunology Signal transduction signaling transcription factor type I interferon Viral Nonstructural Proteins - chemistry Viral Nonstructural Proteins - genetics Viral Nonstructural Proteins - immunology |
| Title | Structural basis for concerted recruitment and activation of IRF-3 by innate immune adaptor proteins |
| URI | https://www.jstor.org/stable/26470308 https://www.ncbi.nlm.nih.gov/pubmed/27302953 https://www.proquest.com/docview/1799224895 https://www.proquest.com/docview/1797542332 https://www.proquest.com/docview/1832245764 https://www.osti.gov/servlets/purl/1379399 https://pubmed.ncbi.nlm.nih.gov/PMC4914169 |
| Volume | 113 |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3Nb9MwFLfKuHBBDBiEDWQkDkNVSps4cXwciKlwmCa2SRWXyHYcNRokU9sgjb-DP5jnjzht2dDgElWJ47h5v7wP-72fEXqTZZrzLk7DaELKkPA0C3kRyzDLmEgypsalNAmyJ-n0gnyeJbPB4Nda1lK7EiP588a6kv-RKpwDueoq2X-QrO8UTsBvkC8cQcJwvJOMzwz5qyHOAGtUGWoFnUcu1UI7kqDMFm3Vp5HrGoYf3kX89OU4jLX3WdU1OJzDSleKqCEv-BXE4UND4FC5uTznvZ56a7fscgtOusnEo740xemL5TAcnp70Gx1_nfPGLnE0162f2Zm3btXfmVCdC2TbzeDpc9WfPuP1JV_YCdv3vG6_68TJ9VmLSaqzq2y1qK8iAOtIbP30SFnlC75LmBK7fajXzrZU1cHQtv9D7YOe0nsV13ypZ8vAI2XdbRsE21uGz6cjmoV4Gue6g7zv4B66H0HwYdJFp-tUzpktbHL_oCOMovG7rRFs-Do23RUsfwO6-6Z4Zjstd83POX-EHroABR9ZtO2igaofo91OpPjQ8ZS_fYKKHn7YwA8D_LCHH16DHwb44R5-uCmxgR8W19jCD1v4YQc_3MHvKbo4_nj-YRq6TTtCmaRsFXLwx4mUY0lUmhakKCNNcZcoNhapkIoUqqC0ZEJAHKFYGfEYzFxaCghTCjqORLyHduqmVs8RlpOYqkKVQnLokhYipqBxaJEUkcjGqgzQqHu9uXSM9npjlW_5LQIN0KG_4cqSudzedM_Iy7eDwEEbxyxA-1qAOTiommVZ6nQ0ucphqAx8_QAddHLNnaKAXqkmfyYZSwL02l8GNa7X5nitmta00XtRx3H0lzba-pKEpiRAzyxU-uGBpY5YAuOmGyDyDTSN_OaVupobOnnCJhCVsRd3fzn76EH_TR-gHUCbegm--Uq8Mp_Kb9Mk5lY |
| linkProvider | ABC ChemistRy |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Structural+basis+for+concerted+recruitment+and+activation+of+IRF-3+by+innate+immune+adaptor+proteins&rft.jtitle=Proceedings+of+the+National+Academy+of+Sciences+-+PNAS&rft.au=Zhao%2C+Baoyu&rft.au=Shu%2C+Chang&rft.au=Gao%2C+Xinsheng&rft.au=Sankaran%2C+Banumathi&rft.date=2016-06-14&rft.issn=0027-8424&rft.eissn=1091-6490&rft.volume=113&rft.issue=24&rft_id=info:doi/10.1073%2Fpnas.1603269113&rft.externalDBID=n%2Fa&rft.externalDocID=10_1073_pnas_1603269113 |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0027-8424&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0027-8424&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0027-8424&client=summon |