Neurotrophic tyrosine kinase receptor 1 is a direct transcriptional and epigenetic target of IL-13 involved in allergic inflammation

Mucosal Immunology - Tập 8 - Trang 785-798 - 2015
M Rochman1, A V Kartashov1, J M Caldwell1, M H Collins2, E M Stucke1, K KC1, J D Sherrill1, J Herren1, A Barski1, M E Rothenberg1
1Divisions of Allergy and Immunology, Cincinnati Children's Hospital Medical Center, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA
2Divisions of Pathology and Laboratory Medicine, Cincinnati Children's Hospital Medical Center, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA

Tài liệu tham khảo

Brightling, 2010, Interleukin-13: prospects for new treatments, Clin. Exp. Allergy, 40, 42 Abonia, 2012, Eosinophilic esophagitis: rapidly advancing insights, Annu. Rev. Med., 63, 421, 10.1146/annurev-med-041610-134138 Zheng, 2009, Transgenic expression of interleukin-13 in the skin induces a pruritic dermatitis and skin remodeling, J. Invest. Dermatol., 129, 742, 10.1038/jid.2008.295 Lee, 2001, Interleukin-13 induces dramatically different transcriptional programs in three human airway cell types, Am. J. Respir. Cell Mol. Biol., 25, 474, 10.1165/ajrcmb.25.4.4522 Kuperman, 1998, Signal transducer and activator of transcription factor 6 (Stat6)-deficient mice are protected from antigen-induced airway hyperresponsiveness and mucus production, J. Exp. Med., 187, 939, 10.1084/jem.187.6.939 Kuperman, 2002, Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma, Nat. Med., 8, 885, 10.1038/nm734 Mishra, 2003, Intratracheal IL-13 induces eosinophilic esophagitis by an IL-5, eotaxin-1, and STAT6-dependent mechanism, Gastroenterology, 125, 1419, 10.1016/j.gastro.2003.07.007 Blanchard, 2005, Eotaxin-3/CCL26 gene expression in intestinal epithelial cells is up-regulated by interleukin-4 and interleukin-13 via the signal transducer and activator of transcription 6, Int. J. Biochem. Cell Biol., 37, 2559, 10.1016/j.biocel.2005.06.010 Matsukura, 2001, Interleukin-13 upregulates eotaxin expression in airway epithelial cells by a STAT6-dependent mechanism, Am. J. Respir. Cell Mol. Biol., 24, 755, 10.1165/ajrcmb.24.6.4351 Blanchard, 2007, IL-13 involvement in eosinophilic esophagitis: transcriptome analysis and reversibility with glucocorticoids, J. Allergy Clin. Immunol., 120, 1292, 10.1016/j.jaci.2007.10.024 Levi-Montalcini, 1987, The nerve growth factor 35 years later, Science, 237, 1154, 10.1126/science.3306916 Bonini, 1996, Circulating nerve growth factor levels are increased in humans with allergic diseases and asthma, Proc. Natl. Acad. Sci. USA, 93, 10955, 10.1073/pnas.93.20.10955 Sin, 2001, Nerve growth factor or IL-3 induces more IL-13 production from basophils of allergic subjects than from basophils of nonallergic subjects, J. Allergy Clin. Immunol., 108, 387, 10.1067/mai.2001.117459 Hahn, 2006, Airway epithelial cells produce neurotrophins and promote the survival of eosinophils during allergic airway inflammation, J. Allergy Clin. Immunol., 117, 787, 10.1016/j.jaci.2005.12.1339 Milbrandt, 1987, A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor, Science, 238, 797, 10.1126/science.3672127 Cho, 2006, Role of early growth response-1 (Egr-1) in interleukin-13-induced inflammation and remodeling, J. Biol. Chem., 281, 8161, 10.1074/jbc.M506770200 Nishihira, 1993, Molecular and cellular features of esophageal cancer cells, J. Cancer Res. Clin. Oncol., 119, 441, 10.1007/BF01215923 Anders, 2010, Differential expression analysis for sequence count data, Genome Biol., 11, R106, 10.1186/gb-2010-11-10-r106 Blanchard, 2006, Eotaxin-3 and a uniquely conserved gene-expression profile in eosinophilic esophagitis, J. Clin. Invest., 116, 536, 10.1172/JCI26679 Trengove, 2013, SOCS proteins in development and disease, Am. J. Clin. Exp. Immunol., 2, 1 Spicer, 1997, Molecular cloning and characterization of a cDNA encoding the third putative mammalian hyaluronan synthase, J. Biol. Chem., 272, 8957, 10.1074/jbc.272.14.8957 HajMohammadi, 2003, Normal levels of anticoagulant heparan sulfate are not essential for normal hemostasis, J. Clin. Invest., 111, 989, 10.1172/JCI200315809 Stone, 2010, Characterization of mice with targeted deletion of the gene encoding core 2 beta1,6-N-acetylglucosaminyltransferase-2, Methods Enzymol., 479, 155, 10.1016/S0076-6879(10)79009-1 Hata, 2013, Arid5b facilitates chondrogenesis by recruiting the histone demethylase Phf2 to Sox9-regulated genes, Nat. Commun., 4, 2850, 10.1038/ncomms3850 Malinin, 1997, MAP3K-related kinase involved in NF-kappaB induction by TNF, CD95 and IL-1, Nature, 385, 540, 10.1038/385540a0 Kas, 2000, ESE-3, a novel member of an epithelium-specific ets transcription factor subfamily, demonstrates different target gene specificity from ESE-1, J. Biol. Chem., 275, 2986, 10.1074/jbc.275.4.2986 Albino, 2012, ESE3/EHF controls epithelial cell differentiation and its loss leads to prostate tumors with mesenchymal and stem-like features, Cancer Res., 72, 2889, 10.1158/0008-5472.CAN-12-0212 Wang, 2013, Inhibition of RUNX2 transcriptional activity blocks the proliferation, migration and invasion of epithelial ovarian carcinoma cells, PLoS One, 8, e74384, 10.1371/journal.pone.0074384 Golonzhka, 2009, Ctip2/Bcl11b controls ameloblast formation during mammalian odontogenesis, Proc. Natl. Acad. Sci. USA, 106, 4278, 10.1073/pnas.0900568106 Dillon, 2004, Interleukin 31, a cytokine produced by activated T cells, induces dermatitis in mice, Nat. Immunol., 5, 752, 10.1038/ni1084 Ip, 2007, Interleukin-31 induces cytokine and chemokine production from human bronchial epithelial cells through activation of mitogen-activated protein kinase signalling pathways: implications for the allergic response, Immunology, 122, 532, 10.1111/j.1365-2567.2007.02668.x Indo, 2001, Molecular basis of congenital insensitivity to pain with anhidrosis (CIPA): mutations and polymorphisms in TRKA (NTRK1) gene encoding the receptor tyrosine kinase for nerve growth factor, Hum Mutat., 18, 462, 10.1002/humu.1224 Freund-Michel, 2008, The nerve growth factor and its receptors in airway inflammatory diseases, Pharmacol. Ther., 117, 52, 10.1016/j.pharmthera.2007.07.003 Frossard, 2004, Nerve growth factor and its receptors in asthma and inflammation, Eur. J. Pharmacol., 500, 453, 10.1016/j.ejphar.2004.07.044 Raap, 2010, The role of neurotrophins in the pathophysiology of allergic rhinitis, Curr. Opin. Allergy Clin. Immunol., 10, 8, 10.1097/ACI.0b013e328334f5de Manning, 2002, The protein kinase complement of the human genome, Science, 298, 1912, 10.1126/science.1075762 Ernst, 2010, Discovery and characterization of chromatin states for systematic annotation of the human genome, Nat. Biotechnol., 28, 817, 10.1038/nbt.1662 Segal, 1996, Differential utilization of Trk autophosphorylation sites, J. Biol. Chem., 271, 20175, 10.1074/jbc.271.33.20175 Ginty, 1991, Induction of immediate early genes by Ca2+ influx requires cAMP-dependent protein kinase in PC12 cells, J. Biol. Chem., 266, 17454, 10.1016/S0021-9258(19)47394-8 Vaishnavi, 2013, Oncogenic and drug-sensitive NTRK1 rearrangements in lung cancer, Nat. Med., 19, 1469, 10.1038/nm.3352 Festuccia, 2007, Tyrosine kinase inhibitor CEP-701 blocks the NTRK1/NGF receptor and limits the invasive capability of prostate cancer cells in vitro, Int. J. Oncol., 30, 193 Vroling, 2008, Comparison of expression profiles induced by dust mite in airway epithelia reveals a common pathway, Allergy, 63, 461, 10.1111/j.1398-9995.2007.01621.x Cao, 1992, Regulation of the Egr-1 gene by tumor necrosis factor and interferons in primary human fibroblasts, J. Biol. Chem., 267, 1345, 10.1016/S0021-9258(18)48437-2 Hodge, 1998, Growth hormone stimulates phosphorylation and activation of elk-1 and expression of c-fos, egr-1, and junB through activation of extracellular signal-regulated kinases 1 and 2, J. Biol. Chem., 273, 31327, 10.1074/jbc.273.47.31327 Morawietz, 1999, Rapid induction and translocation of Egr-1 in response to mechanical strain in vascular smooth muscle cells, Circ. Res., 84, 678, 10.1161/01.RES.84.6.678 Yan, 2000, Egr-1, a master switch coordinating upregulation of divergent gene families underlying ischemic stress, Nat. Med., 6, 1355, 10.1038/82168 Ingram, 2006, Opposing actions of Stat1 and Stat6 on IL-13-induced up-regulation of early growth response-1 and platelet-derived growth factor ligands in pulmonary fibroblasts, J. Immunol., 177, 4141, 10.4049/jimmunol.177.6.4141 Lohoff, 2010, Early growth response protein-1 (Egr-1) is preferentially expressed in T helper type 2 (Th2) cells and is involved in acute transcription of the Th2 cytokine interleukin-4, J. Biol. Chem., 285, 1643, 10.1074/jbc.M109.011585 Shen, 1998, Interaction of stat6 and NF-kappaB: direct association and synergistic activation of interleukin-4-induced transcription, Mol. Cell. Biol., 18, 3395, 10.1128/MCB.18.6.3395 Inoue, 2009, Early growth response 1 loops the CYP2B6 promoter for synergistic activation by the distal and proximal nuclear receptors CAR and HNF4alpha, FEBS Lett., 583, 2126, 10.1016/j.febslet.2009.05.031 Lovinsky-Desir, 2012, Epigenetics, asthma, and allergic diseases: a review of the latest advancements, Curr. Allergy Asthma Rep., 12, 211, 10.1007/s11882-012-0257-4 Tezza, 2013, Epigenetics of allergy, Early Hum. Dev., 89, S20, 10.1016/S0378-3782(13)70007-0 Lim, 2011, Epigenetic regulation of the IL-13-induced human eotaxin-3 gene by CREB-binding protein-mediated histone 3 acetylation, J. Biol. Chem., 286, 13193, 10.1074/jbc.M110.210724 Lu, 2012, MiR-375 is downregulated in epithelial cells after IL-13 stimulation and regulates an IL-13-induced epithelial transcriptome, Mucosal Immunol., 5, 388, 10.1038/mi.2012.16 Lim, 2014, Demethylation of the human eotaxin-3 gene promoter leads to the elevated expression of eotaxin-3, J. Immunol., 192, 466, 10.4049/jimmunol.1302454 Barski, 2009, Chromatin poises miRNA- and protein-coding genes for expression, Genome Res., 19, 1742, 10.1101/gr.090951.109 Zediak, 2011, Cutting edge: persistently open chromatin at effector gene loci in resting memory CD8+ T cells independent of transcriptional status, J. Immunol., 186, 2705, 10.4049/jimmunol.1003741 Russ, 2013, T cell immunity as a tool for studying epigenetic regulation of cellular differentiation, Front. Genet., 4, 218, 10.3389/fgene.2013.00218 Guenther, 2007, A chromatin landmark and transcription initiation at most promoters in human cells, Cell, 130, 77, 10.1016/j.cell.2007.05.042 Creyghton, 2010, Histone H3K27ac separates active from poised enhancers and predicts developmental state, Proc. Natl. Acad. Sci. USA, 107, 21931, 10.1073/pnas.1016071107 Lei, 2007, Transcriptional regulation of Trk family neurotrophin receptors, Cell. Mol. Life Sci., 64, 522, 10.1007/s00018-006-6328-8 Dohrman, 1997, Ethanol reduces expression of the nerve growth factor receptor, but not nerve growth factor protein levels in the neonatal rat cerebellum, Alcohol. Clin. Exp. Res., 21, 882, 10.1111/j.1530-0277.1997.tb03853.x Dalal, 1997, Molecular characterization of neurotrophin expression and the corresponding tropomyosin receptor kinases (trks) in epithelial and stromal cells of the human prostate, Mol. Cell. Endocrinol., 134, 15, 10.1016/S0303-7207(97)00165-2 Descamps, 2001, Expression of nerve growth factor receptors and their prognostic value in human breast cancer, Cancer Res., 61, 4337 Brodeur, 1997, Expression of TrkA, TrkB and TrkC in human neuroblastomas, J. Neurooncol., 31, 49, 10.1023/A:1005729329526 Indo, 2012, Nerve growth factor and the physiology of pain: lessons from congenital insensitivity to pain with anhidrosis, Clin. Genet., 82, 341, 10.1111/j.1399-0004.2012.01943.x Indo, 1996, Mutations in the TRKA/NGF receptor gene in patients with congenital insensitivity to pain with anhidrosis, Nat. Genet., 13, 485, 10.1038/ng0896-485 Allosteric Small Molecule Inhibitors of the NGF/TrkA Pathway A New Approach to Treating Inflammatory Pain http://www.arraybiopharma.com/files/6313/9810/8021/PubAttachment587.pdf Accessed Date. Madhusudan, 2007, Tyrosine kinase inhibitors and cancer therapy, Recent Results Cancer Res., 172, 25, 10.1007/978-3-540-31209-3_3 Kariyawasam, 2009, Activin and transforming growth factor-beta signaling pathways are activated after allergen challenge in mild asthma, J. Allergy Clin. Immunol., 124, 454, 10.1016/j.jaci.2009.06.022 Trapnell, 2012, Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks, Nat. Protoc., 7, 562, 10.1038/nprot.2012.016 Meyer, 2013, The UCSC Genome Browser database: extensions and updates 2013, Nucleic Acids Res., 41, D64 Robinson, 2000, The protein tyrosine kinase family of the human genome, Oncogene, 19, 5548, 10.1038/sj.onc.1203957