Estrogen-regulated STAT1 activation promotes TLR8 expression to facilitate signaling via microRNA-21 in systemic lupus erythematosus

Kumar, 1987, Functional domains of the human estrogen receptor, Cell, 51, 941, 10.1016/0092-8674(87)90581-2 Welboren, 2007, Identifying estrogen receptor target genes, Mol. Oncol., 1, 138, 10.1016/j.molonc.2007.04.001 Svenson, 2008, Impact of estrogen receptor deficiency on disease expression in the NZM2410 lupus prone mouse, Clin. Immunol., 128, 259, 10.1016/j.clim.2008.03.508 Cunningham, 2012, Estrogen receptor alpha modulates Toll-like receptor signaling in murine lupus, Clin. Immunol., 144, 1, 10.1016/j.clim.2012.04.001 Feng, 2010, The induction of the lupus phenotype by estrogen is via an estrogen receptor-alpha-dependent pathway, Clin. Immunol., 134, 226, 10.1016/j.clim.2009.10.004 Young, 2014, Estrogen modulation of endosome-associated toll-like receptor 8: an IFNalpha-independent mechanism of sex-bias in systemic lupus erythematosus, Clin. Immunol., 151, 66, 10.1016/j.clim.2014.01.006 Zarember, 2002, Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines, J. Immunol., 168, 554, 10.4049/jimmunol.168.2.554 Aringer, 2013, Innate immune processes in lupus erythematosus, Clin. Immunol., 147, 216, 10.1016/j.clim.2012.11.012 Fabbri, 2012, MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response, Proc. Natl. Acad. Sci. U. S. A., 109, E2110, 10.1073/pnas.1209414109 Carlsen, 2013, Circulating microRNA expression profiles associated with systemic lupus erythematosus, Arthritis Rheum., 65, 1324, 10.1002/art.37890 Amarilyo, 2012, miRNA in systemic lupus erythematosus, Clin. Immunol., 144, 26, 10.1016/j.clim.2012.04.005 Hochberg, 1997, Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus, Arthritis Rheum., 40, 1725, 10.1002/art.1780400928 Jablonski, 2015, Novel markers to delineate murine M1 and M2 macrophages, PLoS One, 10, 10.1371/journal.pone.0145342 Young, 2013, Novel estrogen target gene ZAS3 is overexpressed in systemic lupus erythematosus, Mol. Immunol., 54, 23, 10.1016/j.molimm.2012.10.026 Burd, C.J., et al., Analysis of chromatin dynamics during glucocorticoid receptor activation. Mol. Cell. Biol. 32(10): p. 1805–17. Heinz, S., et al., Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell. 38(4): p. 576–89. Robinson, J.T., et al., Integrative genomics viewer. Nat. Biotechnol. 29(1): p. 24–6. Zannetti, 2010, C/EBP{delta} and STAT-1 are required for TLR8 transcriptional activity, J. Biol. Chem., 285, 34773, 10.1074/jbc.M110.133884 Kasperkovitz, 2004, Activation of the STAT1 pathway in rheumatoid arthritis, Ann. Rheum. Dis., 63, 233, 10.1136/ard.2003.013276 Gysemans, 2005, Disruption of the gamma-interferon signaling pathway at the level of signal transducer and activator of transcription-1 prevents immune destruction of beta-cells, Diabetes, 54, 2396, 10.2337/diabetes.54.8.2396 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 Dong, 2007, Activation of the STAT1 signalling pathway in lupus nephritis in MRL/lpr mice, Lupus, 16, 101, 10.1177/0961203306075383 Klinge, 2001, Estrogen receptor interaction with estrogen response elements, Nucleic Acids Res., 29, 2905, 10.1093/nar/29.14.2905 Bartlett, 2006, Insights into the kinetics of siRNA-mediated gene silencing from live-cell and live-animal bioluminescent imaging, Nucleic Acids Res., 34, 322, 10.1093/nar/gkj439 Chaussabel, 2008, A modular analysis framework for blood genomics studies: application to systemic lupus erythematosus, Immunity, 29, 150, 10.1016/j.immuni.2008.05.012 Dai, 2009, Estrogen regulates transcription factors STAT-1 and NF-kappaB to promote inducible nitric oxide synthase and inflammatory responses, J. Immunol., 183, 6998, 10.4049/jimmunol.0901737 Akira, 2004, Toll-like receptor signalling, Nat. Rev. Immunol., 4, 499, 10.1038/nri1391 Ghosh, 2006, Toll-like receptor (TLR) 2-9 agonists-induced cytokines and chemokines: I. Comparison with T cell receptor-induced responses, Cell. Immunol., 243, 48, 10.1016/j.cellimm.2006.12.002 Berger, 2009, TLR8-driven IL-12-dependent reciprocal and synergistic activation of NK cells and monocytes by immunostimulatory RNA, J. Immunother., 32, 262, 10.1097/CJI.0b013e318198bd2a Laxton, 2011, Selection, optimization, and pharmacokinetic properties of a novel, potent antiviral locked nucleic acid-based antisense oligomer targeting hepatitis C virus internal ribosome entry site, Antimicrob. Agents Chemother., 55, 3105, 10.1128/AAC.00222-11 Kuznik, 2011, Mechanism of endosomal TLR inhibition by antimalarial drugs and imidazoquinolines, J. Immunol., 186, 4794, 10.4049/jimmunol.1000702 Lockshin, 2006, Sex differences in autoimmune disease, Lupus, 15, 753, 10.1177/0961203306069353 Tedeschi, 2013, Sexual disparities in the incidence and course of SLE and RA, Clin. Immunol., 149, 211, 10.1016/j.clim.2013.03.003 Yoachim, 2015, Estrogen receptor alpha signaling promotes Sle1-induced loss of tolerance and immune cell activation and is responsible for sex bias in B6.Sle1 congenic mice, Clin. Immunol., 158, 153, 10.1016/j.clim.2015.03.026 Johnstone, 1987, Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes), J. Biol. Chem., 262, 9412, 10.1016/S0021-9258(18)48095-7 Valadi, 2007, Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells, Nat. Cell Biol., 9, 654, 10.1038/ncb1596 Mitchell, 2008, Circulating microRNAs as stable blood-based markers for cancer detection, Proc. Natl. Acad. Sci. U. S. A., 105, 10513, 10.1073/pnas.0804549105 Gallo, 2012, The majority of microRNAs detectable in serum and saliva is concentrated in exosomes, PLoS One, 7, 10.1371/journal.pone.0030679 Arroyo, 2011, Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma, Proc. Natl. Acad. Sci. U. S. A., 108, 5003, 10.1073/pnas.1019055108 Zhang, 2010, Secreted monocytic miR-150 enhances targeted endothelial cell migration, Mol. Cell, 39, 133, 10.1016/j.molcel.2010.06.010 El-Hefnawy, 2004, Characterization of amplifiable, circulating RNA in plasma and its potential as a tool for cancer diagnostics, Clin. Chem., 50, 564, 10.1373/clinchem.2003.028506 Guduric-Fuchs, 2012, Selective extracellular vesicle-mediated export of an overlapping set of microRNAs from multiple cell types, BMC Genomics, 13, 357, 10.1186/1471-2164-13-357 Nolte-’t Hoen, 2012, Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions, Nucleic Acids Res., 40, 9272, 10.1093/nar/gks658 Bhat-Nakshatri, 2009, Estradiol-regulated microRNAs control estradiol response in breast cancer cells, Nucleic Acids Res., 37, 4850, 10.1093/nar/gkp500 Di Leva, 2010, MicroRNA cluster 221-222 and estrogen receptor alpha interactions in breast cancer, J. Natl. Cancer Inst., 102, 706, 10.1093/jnci/djq102 Zhao, 2010, Hypomethylation of IL10 and IL13 promoters in CD4+ T cells of patients with systemic lupus erythematosus, J. Biomed. Biotechnol., 2010, 931018, 10.1155/2010/931018 Xu, 2005, Determination of serum interleukin-13 and nerve growth factor in patients with systemic lupus erythematosus and clinical significance, J. Huazhong Univ. Sci. Technolog. Med. Sci., 25, 360, 10.1007/BF02828168 Hagiwara, 1996, Disease severity in patients with systemic lupus erythematosus correlates with an increased ratio of interleukin-10:interferon-gamma-secreting cells in the peripheral blood, Arthritis Rheum., 39, 379, 10.1002/art.1780390305 Garchow, 2016, MicroRNA-21 deficiency protects from lupus-like autoimmunity in the chronic graft-versus-host disease model of systemic lupus erythematosus, Clin. Immunol., 162, 100, 10.1016/j.clim.2015.11.010 Rainsford, 2015, Therapy and pharmacological properties of hydroxychloroquine and chloroquine in treatment of systemic lupus erythematosus, rheumatoid arthritis and related diseases, Inflammopharmacology, 23, 231, 10.1007/s10787-015-0239-y Hacker, 1998, CpG-DNA-specific activation of antigen-presenting cells requires stress kinase activity and is preceded by non-specific endocytosis and endosomal maturation, EMBO J., 17, 6230, 10.1093/emboj/17.21.6230