The IL-10 receptor inhibits cell extrinsic signals necessary for STAT1-dependent macrophage accumulation during colitis

Mucosal Immunology - Tập 16 - Trang 233-249 - 2023
Izabel Patik1, Naresh S. Redhu1,2, Alal Eran3, Bin Bao1, Anubhab Nandy1, Ying Tang1, Shorouk El Sayed1,4, Zeli Shen5, Jonathan Glickman6, James G. Fox5, Scott B. Snapper1, Bruce H. Horwitz1,7
1Division of Gastroenterology, Hepatology and Nutrition, Boston Children’s Hospital, Boston, Massachusetts, USA
2Morphic Therapeutic, Waltham, Massachusetts, USA
3Computational Health Informatics Program, Boston Children’s Hospital, Boston, Massachusetts, USA
4Faculty of Veterinary Medicine, Department of Microbiology, Zagazig University, Zagazig, Ash Sharkia, Egypt
5Division of Comparative Medicine, Massachusetts Institute of Technology, Massachusetts, USA
6Department of Pathology, Beth Israel Deaconess Medical Center, Boston, Massachusetts, USA
7Division of Emergency Medicine, Boston Children’s Hospital, Boston, Massachusetts, USA

Tài liệu tham khảo

Glocker, 2010, Infant colitis-it’s in the genes, Lancet, 376, 1272, 10.1016/S0140-6736(10)61008-2 Glocker, 2009, Inflammatory bowel disease and mutations affecting the interleukin-10 receptor, N. Engl. J. Med., 361, 2033, 10.1056/NEJMoa0907206 Glocker, 2011, IL-10 and IL-10 receptor defects in humans, Ann. N. Y. Acad. Sci., 1246, 102, 10.1111/j.1749-6632.2011.06339.x Na, 2019, Macrophages in intestinal inflammation and resolution: a potential therapeutic target in IBD, Nat. Rev. Gastroenterol. Hepatol., 16, 531, 10.1038/s41575-019-0172-4 Bain, 2014, Macrophages in intestinal homeostasis and inflammation, Immunol. Rev., 260, 102, 10.1111/imr.12192 Zigmond, 2012, Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells, Immunity, 37, 1076, 10.1016/j.immuni.2012.08.026 Redhu, 2017, Macrophage dysfunction initiates colitis during weaning of infant mice lacking the interleukin-10 receptor, eLife, 6, 1, 10.7554/eLife.27652 Caruso, 2020, Host-microbiota interactions in inflammatory bowel disease, Nat. Rev. Immunol., 20, 411, 10.1038/s41577-019-0268-7 Kang, 2020, Commensal microbiota drive the functional diversification of colon macrophages, Mucosal Immunol., 13, 216, 10.1038/s41385-019-0228-3 El Sayed, 2022, CCR2 promotes monocyte recruitment and intestinal inflammation in mice lacking the interleukin–10 receptor, Sci. Rep., 12, 452, 10.1038/s41598-021-04098-7 Kühn, 1993, Interleukin-10-deficient mice develop chronic enterocolitis, Cell, 75, 263, 10.1016/0092-8674(93)80068-P Sellon, 1998, Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice, Infect. Immun., 66, 5224, 10.1128/IAI.66.11.5224-5231.1998 Shouval, 2014, Interleukin-10 receptor signaling in innate immune cells regulates mucosal immune tolerance and anti-inflammatory macrophage function, Immunity, 40, 706, 10.1016/j.immuni.2014.03.011 Bain, 2018, Proinflammatory role of monocyte-derived CX3CR1int macrophages in Helicobacter hepaticus-induced colitis, Infect. Immun., 86, e00579, 10.1128/IAI.00579-17 Kullberg, 1998, Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12- and gamma interferon-dependent mechanism, Infect. Immun., 66, 5157, 10.1128/IAI.66.11.5157-5166.1998 Ryzhakov, 2018, Alpha kinase 1 controls intestinal inflammation by suppressing the IL-12/Th1 axis, Nat. Commun., 9, 3797, 10.1038/s41467-018-06085-5 Kang, 2017, Interferon-γ represses M2 gene expression in human macrophages by disassembling enhancers bound by the transcription factor MAF, Immunity, 47, 235, 10.1016/j.immuni.2017.07.017 Hu, 2009, Cross-regulation of signaling pathways by interferon-γ: implications for immune responses and autoimmune diseases, Immunity, 31, 539, 10.1016/j.immuni.2009.09.002 Begue, 2011, Defective IL10 signaling defining a subgroup of patients with inflammatory bowel disease, Am. J. Gastroenterol., 106, 1544, 10.1038/ajg.2011.112 Ramana, 2000, Complex roles of Stat1 in regulating gene expression, Oncogene, 19, 2619, 10.1038/sj.onc.1203525 Rauch, 2013, The regulation of inflammation by interferons and their STATs, JAKSTAT, 2, 1 Nakanishi, 2018, IFN-γ-dependent epigenetic regulation instructs colitogenic monocyte/macrophage lineage differentiation in vivo, Mucosal Immunol., 11, 871, 10.1038/mi.2017.104 Wu, 2007, Genome-wide gene expression differences in Crohn’s disease and ulcerative colitis from endoscopic pinch biopsies: insights into distinctive pathogenesis, Inflamm. Bowel Dis., 13, 807, 10.1002/ibd.20110 Mudter, 2005, Activation pattern of signal transducers and activators of transcription (STAT) factors in inflammatory bowel diseases, Am. J. Gastroenterol., 100, 64, 10.1111/j.1572-0241.2005.40615.x Schreiber, 2002, Activation of signal transducer and activator of transcription (STAT) 1 in human chronic inflammatory bowel disease, Gut, 51, 379, 10.1136/gut.51.3.379 Haberman, 2014, Pediatric Crohn disease patients exhibit specific ileal transcriptome and microbiome signature, J. Clin. Invest., 124, 3617, 10.1172/JCI75436 Ito, 1999, Interleukin-10 inhibits expression of both interferon α- and interferon γ-induced genes by suppressing tyrosine phosphorylation of STAT1, Blood, 93, 1456, 10.1182/blood.V93.5.1456 Rogler, 2020, Efficacy of JAK inhibitors in Crohn’s disease, J. Crohns Colitis, 14, S746, 10.1093/ecco-jcc/jjz186 Cordes, 2020, Differential regulation of JAK/STAT-signaling in patients with ulcerative colitis and Crohn’s disease, World J. Gastroenterol., 26, 4055, 10.3748/wjg.v26.i28.4055 Salas, 2020, JAK–STAT pathway targeting for the treatment of inflammatory bowel disease, Nat. Rev. Gastroenterol. Hepatol., 17, 323, 10.1038/s41575-020-0273-0 Ip, 2017, Anti-inflammatory effect of IL-10 mediated by metabolic reprogramming of macrophages, Science, 356, 513, 10.1126/science.aal3535 Conaway, 2017, Inhibition of inflammatory gene transcription by IL-10 is associated with rapid suppression of lipopolysaccharide-induced enhancer activation, J. Immunol., 198, 2906, 10.4049/jimmunol.1601781 Lang, 2002, Shaping gene expression in activated and resting primary macrophages by IL-10, J. Immunol., 169, 2253, 10.4049/jimmunol.169.5.2253 Hu, 2005, IFN-γ-primed macrophages exhibit increased CCR2-dependent migration and altered IFN-γ responses mediated by Stat1, J. Immunol., 175, 3637, 10.4049/jimmunol.175.6.3637 Cypowyj, 2012, Immunity to infection in IL-17-deficient mice and humans, Eur. J. Immunol., 42, 2246, 10.1002/eji.201242605 Bernshtein, 2019, IL-23 – producing IL-10Ra – deficient gut macrophages elicit an IL-22 – driven proinflammatory epithelial cell response, Sci. Immunol., 6571, 1 Liu, 2011, Gain-of-function human STAT1 mutations impair IL-17 immunity and underlie chronic mucocutaneous candidiasis, J. Exp. Med., 208, 1635, 10.1084/jem.20110958 Li, 2015, IL-10 engages macrophages to shift Th17 cytokine dependency and pathogenicity during T-cell-mediated colitis, Nat. Commun., 6, 6131, 10.1038/ncomms7131 Shouval, 2017, Enhanced TH17 responses in patients with IL10 receptor deficiency and infantile-onset IBD, Inflamm. Bowel Dis., 23, 1950, 10.1097/MIB.0000000000001270 Shouval, 2016, Interleukin 1β Mediates intestinal Inflammation in Mice and Patients with interleukin 10 Receptor Deficiency, Gastroenterology, 151, 1100, 10.1053/j.gastro.2016.08.055 Morrison, 2015, Differential requirements for IL-17A and IL-22 in cecal versus colonic inflammation induced by Helicobacter hepaticus, Am. J. Pathol., 185, 3290, 10.1016/j.ajpath.2015.08.015 Zhu, 2022, The deletion of IL-17A enhances Helicobacter hepaticus colonization and triggers colitis, J. Inflamm. Res., 15, 2761, 10.2147/JIR.S359100 Ho, 2006, Role of STAT3 in type I interferon responses. Negative regulation of STAT1-dependent inflammatory gene activation, J. Biol. Chem., 281, 14111, 10.1074/jbc.M511797200 Schridde, 2017, Tissue-specific differentiation of colonic macrophages requires TGFβ receptor-mediated signaling, Mucosal Immunol., 10, 1387, 10.1038/mi.2016.142 Girard-Madoux, 2016, IL-10 control of CD11c+ myeloid cells is essential to maintain immune homeostasis in the small and large intestine, Oncotarget, 7, 32015, 10.18632/oncotarget.8337 Bleich, 2010, Cdcsl a major colitis susceptibility locus in mice; subcongenic analysis reveals genetic complexity, Inflamm. Bowel Dis., 16, 765, 10.1002/ibd.21146 Dobin, 2013, STAR: ultrafast universal RNA-seq aligner, Bioinformatics, 29, 15, 10.1093/bioinformatics/bts635 Robinson, 2010, A scaling normalization method for differential expression analysis of RNA-seq data, Genome Biol., 11, R25, 10.1186/gb-2010-11-3-r25 Ritchie, 2015, Limma powers differential expression analyses for RNA-sequencing and microarray studies, Nucleic Acids Res., 43, e47, 10.1093/nar/gkv007 Lu, 2020, Investigating transcriptome-wide sex dimorphism by multi-level analysis of single-cell RNA sequencing data in ten mouse cell types, Biol. Sex Differ., 11, 61, 10.1186/s13293-020-00335-2 Szklarczyk, 2021, The STRING database in 2021: customizable protein-protein networks, and functional characterization of user-uploaded gene/measurement sets, Nucleic Acids Res., 49, D605, 10.1093/nar/gkaa1074 Subramanian, 2005, Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles, Proc. Natl Acad. Sci. U. S. A., 102, 15545, 10.1073/pnas.0506580102 Benjamini, 1995, Controlling the false discovery rate: a practical and powerful approach to multiple testing, J. R. Stat. Soc. B, 57, 289 Shannon, 2003, Cytoscape: A software environment for integrated models of biomolecular interaction networks, Genome Res., 13, 2498, 10.1101/gr.1239303 Liu, 2012, Systematic identification of type I and type II interferon-induced antiviral factors, Proc. Natl Acad. Sci. U. S. A., 109, 4239, 10.1073/pnas.1114981109