STAT1 N-terminal domain discriminatively controls type I and type II IFN signaling

Cytokine - Tập 144 - Trang 155552 - 2021
Anja Göder1, Torsten Ginter2, Thorsten Heinzel2, Svenja Stroh1, Jörg Fahrer1, Andreas Henke3, Oliver H. Krämer1
1Department of Toxicology, University Medical Center, Obere Zahlbacher Str. 67, 55131 Mainz, Germany
2Center for Molecular Biomedicine (CMB), Institute for Biochemistry, Friedrich-Schiller University Jena, Hans-Knöll Str. 2, 07745 Jena, Germany
3Section Experimental Virology, Institute of Medical Microbiology, Jena University Hospital, Friedrich Schiller University Jena, Hans-Knöll-Str. 2, 07745 Jena, Germany

Tài liệu tham khảo

Owen, 2019, JAK-STAT Signaling: A Double-Edged Sword of Immune Regulation and Cancer Progression, Cancers, 11, 10.3390/cancers11122002 Au-Yeung, 2018, Transcriptional and chromatin regulation in interferon and innate antiviral gene expression, Cytokine Growth Factor Rev., 44, 11, 10.1016/j.cytogfr.2018.10.003 Wieczorek, 2012, Acetylation modulates the STAT signaling code, Cytokine Growth Factor Rev., 23, 293, 10.1016/j.cytogfr.2012.06.005 Sehgal, 2008, Paradigm shifts in the cell biology of STAT signaling, Semin. Cell Dev. Biol., 19, 329, 10.1016/j.semcdb.2008.07.003 Chen, 1998, Crystal structure of a tyrosine phosphorylated STAT-1 dimer bound to DNA, Cell, 93, 827, 10.1016/S0092-8674(00)81443-9 Krämer, 2010, Phosphorylation-acetylation switch in the regulation of STAT1 signaling, Mol. Cell. Endocrinol., 315, 40, 10.1016/j.mce.2009.10.007 Chen, 2003, A reinterpretation of the dimerization interface of the N-terminal domains of STATs, Protein Sci., 12, 361, 10.1110/ps.0218903 Mertens, 2006, Dephosphorylation of phosphotyrosine on STAT1 dimers requires extensive spatial reorientation of the monomers facilitated by the N-terminal domain, Genes Dev., 20, 3372, 10.1101/gad.1485406 Staab, 2013, Clinically relevant dimer interface mutants of STAT1 transcription factor exhibit differential gene expression, PLoS ONE, 8, 10.1371/journal.pone.0069903 Meyer, 2004, A single residue modulates tyrosine dephosphorylation, oligomerization, and nuclear accumulation of stat transcription factors, J. Biol. Chem., 279, 18998, 10.1074/jbc.M400766200 Zhong, 2005, Implications of an antiparallel dimeric structure of nonphosphorylated STAT1 for the activation-inactivation cycle, Proc. Natl. Acad. Sci. U S A, 102, 3966, 10.1073/pnas.0501063102 Ho, 2016, STAT2 Is a Pervasive Cytokine Regulator due to Its Inhibition of STAT1 in Multiple Signaling Pathways, PLoS Biol., 14, 10.1371/journal.pbio.2000117 Vinkemeier, 1996, DNA binding of in vitro activated Stat1 alpha, Stat1 beta and truncated Stat1: interaction between NH2-terminal domains stabilizes binding of two dimers to tandem DNA sites, EMBO J., 15, 5616, 10.1002/j.1460-2075.1996.tb00946.x Mao, 2005, Structural bases of unphosphorylated STAT1 association and receptor binding, Mol. Cell, 17, 761, 10.1016/j.molcel.2005.02.021 Braunstein, 2003, STATs dimerize in the absence of phosphorylation, J. Biol. Chem., 278, 34133, 10.1074/jbc.M304531200 Ndubuisi, 1999, Cellular physiology of STAT3: Where's the cytoplasmic monomer?, J. Biol. Chem., 274, 25499, 10.1074/jbc.274.36.25499 Liu, 2005, STAT3 nuclear import is independent of tyrosine phosphorylation and mediated by importin-alpha3, Proc. Natl. Acad. Sci. U S A, 102, 8150, 10.1073/pnas.0501643102 Krämer, 2009, A phosphorylation-acetylation switch regulates STAT1 signaling, Genes Dev., 23, 223, 10.1101/gad.479209 Begitt, 2014, STAT1-cooperative DNA binding distinguishes type 1 from type 2 interferon signaling, Nat. Immunol., 15, 168, 10.1038/ni.2794 Wang, 2020, A virus-induced conformational switch of STAT1-STAT2 dimers boosts antiviral defenses, Cell Res Liu, 2020, USP12 translocation maintains interferon antiviral efficacy by inhibiting CBP acetyltransferase activity, PLoS Pathog., 16, 10.1371/journal.ppat.1008215 Krämer, 2006, Acetylation of Stat1 modulates NF-kappaB activity, Genes Dev., 20, 473, 10.1101/gad.364306 Ginter, 2012, Histone deacetylase inhibitors block IFNgamma-induced STAT1 phosphorylation, Cell. Signal, 24, 1453, 10.1016/j.cellsig.2012.02.018 Zhang, 2020, The HDAC3 inhibitor RGFP966 ameliorated ischemic brain damage by downregulating the AIM2 inflammasome, FASEB J., 34, 648, 10.1096/fj.201900394RRR Deng, 2018, HDAC is indispensable for IFN-gamma-induced B7–H1 expression in gastric cancer, Clin. Epigenetics, 10, 153, 10.1186/s13148-018-0589-6 Kaowinn, 2017, Increased EGFR expression induced by a novel oncogene, CUG2, confers resistance to doxorubicin through Stat1-HDAC4 signaling, Cell. Oncol. (Dordr.), 40, 549, 10.1007/s13402-017-0343-7 Kotla, 2015, Reactive Oxygen Species (ROS) Mediate p300-dependent STAT1 Protein Interaction with Peroxisome Proliferator-activated Receptor (PPAR)-gamma in CD36 Protein Expression and Foam Cell Formation, J. Biol. Chem., 290, 30306, 10.1074/jbc.M115.686865 Kotla, 2017, ROS via BTK-p300-STAT1-PPARgamma signaling activation mediates cholesterol crystals-induced CD36 expression and foam cell formation, Redox Biol., 11, 350, 10.1016/j.redox.2016.12.005 Park, 2018, Novel identification of STAT1 as a crucial mediator of ETV6-NTRK3-induced tumorigenesis, Oncogene, 37, 2270, 10.1038/s41388-017-0102-2 Noack, 2017, Analysis of the interplay between all-trans retinoic acid and histone deacetylase inhibitors in leukemic cells, Arch. Toxicol., 91, 2191, 10.1007/s00204-016-1878-5 Cudejko, 2011, p16INK4a deficiency promotes IL-4-induced polarization and inhibits proinflammatory signaling in macrophages, Blood, 118, 2556, 10.1182/blood-2010-10-313106 Stronach, 2011, HDAC4-regulated STAT1 activation mediates platinum resistance in ovarian cancer, Cancer Res., 71, 4412, 10.1158/0008-5472.CAN-10-4111 Weinert, 2018, Time-Resolved Analysis Reveals Rapid Dynamics and Broad Scope of the CBP/p300 Acetylome, Cell, 174, 231, 10.1016/j.cell.2018.04.033 Hansen, 2019, Analysis of human acetylation stoichiometry defines mechanistic constraints on protein regulation, Nat. Commun., 10, 1055, 10.1038/s41467-019-09024-0 Ginter, 2014, Arginine residues within the DNA binding domain of STAT3 promote intracellular shuttling and phosphorylation of STAT3, Cell. Signal, 26, 1698, 10.1016/j.cellsig.2014.03.033 Mahendrarajah, 2017, HSP90 is necessary for the ACK1-dependent phosphorylation of STAT1 and STAT3, Cell. Signal, 39, 9, 10.1016/j.cellsig.2017.07.014 Krämer, 2008, Histone deacetylase inhibitors and hydroxyurea modulate the cell cycle and cooperatively induce apoptosis, Oncogene, 27, 732, 10.1038/sj.onc.1210677 Göder, 2015, Lipoic acid inhibits the DNA repair protein O 6-methylguanine-DNA methyltransferase (MGMT) and triggers its depletion in colorectal cancer cells with concomitant autophagy induction, Carcinogenesis, 36, 817, 10.1093/carcin/bgv070 Nyman, 2000, Proteome analysis reveals ubiquitin-conjugating enzymes to be a new family of interferon-alpha-regulated genes, Eur. J. Biochem., 267, 4011, 10.1046/j.1432-1327.2000.01433.x Chang, 1991, Molecular and functional analysis of the virus- and interferon-inducible human MxA promoter, Arch. Virol., 117, 1, 10.1007/BF01310488 Brierley, 2006, Identification of GAS-dependent interferon-sensitive target genes whose transcription is STAT2-dependent but ISGF3-independent, FEBS J., 273, 1569, 10.1111/j.1742-4658.2006.05176.x Blaszczyk, 2015, STAT2/IRF9 directs a prolonged ISGF3-like transcriptional response and antiviral activity in the absence of STAT1, Biochem J., 466, 511, 10.1042/BJ20140644 Leung, 1995, Role of STAT2 in the alpha interferon signaling pathway, Mol. Cell. Biol., 15, 1312, 10.1128/MCB.15.3.1312 Licht, 2014, Caspase-3 and caspase-6 cleave STAT1 in leukemic cells, Oncotarget, 5, 2305, 10.18632/oncotarget.1911 Platanitis, 2019, A molecular switch from STAT2-IRF9 to ISGF3 underlies interferon-induced gene transcription, Nat. Commun., 10, 2921, 10.1038/s41467-019-10970-y Urin, 2019, CRISPR/Cas9-based Knockout Strategy Elucidates Components Essential for Type 1 Interferon Signaling in Human HeLa Cells, J. Mol. Biol., 431, 3324, 10.1016/j.jmb.2019.06.007 Friedrich, 2017, Steering of carcinoma progression by the YIN/YANG interaction of STAT1/STAT3, Biosci. Trends, 11, 1, 10.5582/bst.2016.01250 Göder, 2020, Impact of the STAT1 N-terminal domain for fibrosarcoma cell responses to ɣ-irradiation, Exp. Results, 1, 10.1017/exp.2020.25 Mo, 2008, Nuclear beta-arrestin1 functions as a scaffold for the dephosphorylation of STAT1 and moderates the antiviral activity of IFN-gamma, Mol. Cell, 31, 695, 10.1016/j.molcel.2008.06.017 Suryawanshi, 2021, Dysregulation of Cell Signaling by SARS-CoV-2, Trends Microbiol., 29, 224, 10.1016/j.tim.2020.12.007 Mu, 2020, SARS-CoV-2 N protein antagonizes type I interferon signaling by suppressing phosphorylation and nuclear translocation of STAT1 and STAT2, Cell Discov., 6, 65, 10.1038/s41421-020-00208-3 Xia, 2020, Evasion of Type I Interferon by SARS-CoV-2, Cell Rep., 33, 10.1016/j.celrep.2020.108234 Miorin, 2020, SARS-CoV-2 Orf6 hijacks Nup98 to block STAT nuclear import and antagonize interferon signaling, PNAS, 117, 28344, 10.1073/pnas.2016650117 Matsuyama, 2020, An aberrant STAT pathway is central to COVID-19, Cell Death Differ., 27, 3209, 10.1038/s41418-020-00633-7 Li, 2020, An integrative analysis identifying transcriptional features and key genes involved in COVID-19, Epigenomics, 12, 1969, 10.2217/epi-2020-0168 de Araujo, 2019, Structural Implications of STAT3 and STAT5 SH2 Domain Mutations, Cancers, 11, 10.3390/cancers11111757 Ahmed, 2020, A Network-Based Analysis Reveals the Mechanism Underlying Vitamin D in Suppressing Cytokine Storm and Virus in SARS-CoV-2 Infection, Front. Immunol., 11, 10.3389/fimmu.2020.590459 Karki, 2021, Synergism of TNF-alpha and IFN-gamma Triggers Inflammatory Cell Death, Tissue Damage, and Mortality in SARS-CoV-2 Infection and Cytokine Shock Syndromes, Cell, 184, 149, 10.1016/j.cell.2020.11.025 Boudewijns, 2020, STAT2 signaling restricts viral dissemination but drives severe pneumonia in SARS-CoV-2 infected hamsters, Nat. Commun., 11, 5838, 10.1038/s41467-020-19684-y