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ORIGINAL RESEARCH

MBL Binding with AhR Controls Th17 Immunity in Silicosis-Associated Lung Inflammation and Fibrosis

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Pages 4315-4329 | Published online: 28 Jul 2022

References

  • Leung CC, Yu IT, Chen W. Silicosis. Lancet. 2012;379(9830):2008–2018. PubMed PMID: 22534002. doi:10.1016/S0140-6736(12)60235-9
  • Latoche JD, Ufelle AC, Fazzi F, Ganguly K, Leikauf GD, Fattman CL. Secreted phosphoprotein 1 and sex-specific differences in silica-induced pulmonary fibrosis in mice. Environ Health Perspect. 2016;124(8):1199–1207. PubMed PMID: 26955063; PubMed Central PMCID: PMCPMC4977050. doi:10.1289/ehp.1510335
  • The Lancet Respiratory M. The world is failing on silicosis. Lancet Respir Med. 2019;7(4):283. PubMed PMID: 30872128. doi:10.1016/S2213-2600(19)30078-5
  • Alcorn JF, Crowe CR, Kolls JK. TH17 cells in asthma and COPD. Annu Rev Physiol. 2010;72:495–516. PubMed PMID: 20148686. doi:10.1146/annurev-physiol-021909-135926
  • Simonian PL, Roark CL, Wehrmann F, et al. Th17-polarized immune response in a murine model of hypersensitivity pneumonitis and lung fibrosis. J Immunol. 2009;182(1):657–665. PubMed PMID: 19109199; PubMed Central PMCID: PMCPMC2766086. doi:10.4049/jimmunol.182.1.657
  • Ponce-Gallegos MA, Ramirez-Venegas A, Falfan-Valencia R. Th17 profile in COPD exacerbations. Int J Chron Obstruct Pulmon Dis. 2017;12:1857–1865. PubMed PMID: 28694696; PubMed Central PMCID: PMCPMC5491572. doi:10.2147/COPD.S136592
  • Tan HL, Regamey N, Brown S, Bush A, Lloyd CM, Davies JC. The Th17 pathway in cystic fibrosis lung disease. Am J Respir Crit Care Med. 2011;184(2):252–258. PubMed PMID: 21474644; PubMed Central PMCID: PMCPMC3381840. doi:10.1164/rccm.201102-0236OC
  • Song L, Weng D, Liu F, et al. Tregs promote the differentiation of Th17 cells in silica-induced lung fibrosis in mice. PLoS One. 2012;7(5):e37286. PubMed PMID: 22615967; PubMed Central PMCID: PMCPMC3352873. doi:10.1371/journal.pone.0037286
  • Chen Y, Li C, Weng D, et al. Neutralization of interleukin-17A delays progression of silica-induced lung inflammation and fibrosis in C57BL/6 mice. Toxicol Appl Pharmacol. 2014;275(1):62–72. PubMed PMID: 24291675. doi:10.1016/j.taap.2013.11.012
  • Veldhoen M, Hirota K, Westendorf AM, et al. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature. 2008;453(7191):106–109. PubMed PMID: 18362914. doi:10.1038/nature06881
  • Veldhoen M, Hirota K, Christensen J, O’Garra A, Stockinger B. Natural agonists for aryl hydrocarbon receptor in culture medium are essential for optimal differentiation of Th17 T cells. J Exp Med. 2009;206(1):43–49. PubMed PMID: 19114668; PubMed Central PMCID: PMCPMC2626686. doi:10.1084/jem.20081438
  • Nakahama T, Kimura A, Nguyen NT, et al. Aryl hydrocarbon receptor deficiency in T cells suppresses the development of collagen-induced arthritis. Proc Natl Acad Sci USA. 2011;108(34):14222–14227. PubMed PMID: 21825138; PubMed Central PMCID: PMCPMC3161527. doi:10.1073/pnas.1111786108
  • Sun L, Fu J, Lin SH, et al. Particulate matter of 2.5 μm or less in diameter disturbs the balance of TH17/regulatory T cells by targeting glutamate oxaloacetate transaminase 1 and hypoxia-inducible factor 1α in an asthma model. J Allergy Clin Immunol. 2020;145(1):402–414. PubMed PMID: 31647966. doi:10.1016/j.jaci.2019.10.008
  • Jaligama S, Patel VS, Wang P, et al. Radical containing combustion derived particulate matter enhance pulmonary Th17 inflammation via the aryl hydrocarbon receptor. Part Fibre Toxicol. 2018;15(1):20. PubMed PMID: 29724254; PubMed Central PMCID: PMCPMC5934866. doi:10.1186/s12989-018-0255-3
  • Garred P, Genster N, Pilely K, et al. A journey through the lectin pathway of complement-MBL and beyond. Immunol Rev. 2016;274(1):74–97. PubMed PMID: 27782323. doi:10.1111/imr.12468
  • Dean MM, Flower RL, Eisen DP, Minchinton RM, Hart DN, Vuckovic S. Mannose-binding lectin deficiency influences innate and antigen-presenting functions of blood myeloid dendritic cells. Immunology. 2011;132(2):296–305. PubMed PMID: 21091907; PubMed Central PMCID: PMCPMC3050452. doi:10.1111/j.1365-2567.2010.03365.x
  • Zhou J, Hu MY, Li J, et al. Mannan-binding lectin regulates inflammatory cytokine production, proliferation, and cytotoxicity of human peripheral natural killer cells. Mediat Inflamm. 2019;2019:1–12. PubMed PMID: WOS: 000504247100001. doi:10.1155/2019/6738286
  • Tang Y, Ma D, Ming S, et al. Mannan-binding lectin reduces CpG DNA-induced inflammatory cytokine production by human monocytes. Microbiol Immunol. 2015;59(4):231–237. PMID: 25664598. doi:10.1111/1348-0421.12245
  • Liu H, Zhou J, Ma D, et al. Mannan binding lectin attenuates double-stranded RNA-mediated TLR3 activation and innate immunity. FEBS Lett. 2014;588(6):866–872. PubMed PMID: 24530528. doi:10.1016/j.febslet.2014.01.064
  • Zhao N, Wu J, Xiong S, et al. Mannan-binding lectin, a serum collectin, suppresses T-cell proliferation via direct interaction with cell surface calreticulin and inhibition of proximal T-cell receptor signaling. FASEB J. 2017;31(6):2405–2417. PubMed PMID: 28209773. doi:10.1096/fj.201601200RR
  • Ashcroft T, Simpson JM, Timbrell V. Simple method of estimating severity of pulmonary fibrosis on a numerical scale. J Clin Pathol. 1988;41(4):467–470. PMID: 3366935; PubMed Central PMCID: PMCPMC1141479. doi:10.1136/jcp.41.4.467
  • Song L, Weng D, Dai W, et al. Th17 can regulate silica-induced lung inflammation through an IL-1beta-dependent mechanism. J Cell Mol Med. 2014;18(9):1773–1784. PubMed PMID: 25091058; PubMed Central PMCID: PMCPMC4196653. doi:10.1111/jcmm.12341
  • Lee S, Hayashi H, Mastuzaki H, Kumagai-Takei N, Otsuki T. Silicosis and autoimmunity. Curr Opin Allergy Clin Immunol. 2017;17(2):78–84. PubMed PMID: 28177948. doi:10.1097/ACI.0000000000000350
  • Liu X, Hu H, Fan H, et al. The role of STAT3 and AhR in the differentiation of CD4+ T cells into Th17 and Treg cells. Medicine. 2017;96(17):e6615. PubMed PMID: 28445259; PubMed Central PMCID: PMCPMC5413224. doi:10.1097/MD.0000000000006615
  • Yuan X, Dou Y, Wu X, Wei Z, Dai Y. Tetrandrine, an agonist of aryl hydrocarbon receptor, reciprocally modulates the activities of STAT3 and STAT5 to suppress Th17 cell differentiation. J Cell Mol Med. 2017;21(9):2172–2183. PubMed PMID: 28332288; PubMed Central PMCID: PMCPMC5571555. doi:10.1111/jcmm.13141
  • Nebert DW, Dalton TP, Okey AB, Gonzalez FJ. Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J Biol Chem. 2004;279(23):23847–23850. PubMed PMID: 15028720. doi:10.1074/jbc.R400004200
  • Li J, Li H, Yu Y, et al. Mannan-binding lectin suppresses growth of hepatocellular carcinoma by regulating hepatic stellate cell activation via the ERK/COX-2/PGE2 pathway. Oncoimmunology. 2019;8(2):e1527650. PubMed PMID: 30713782; PubMed Central PMCID: PMCPMC6343806. doi:10.1080/2162402X.2018.1527650
  • Thiel S, Frederiksen PD, Jensenius JC. Clinical manifestations of mannan-binding lectin deficiency. Mol Immunol. 2006;43(1–2):86–96. PubMed PMID: 16023210; PubMed Central PMCID: PMCPMC7132399. doi:10.1016/j.molimm.2005.06.018
  • Chalmers JD, Fleming GB, Hill AT, Kilpatrick DC. Impact of mannose-binding lectin insufficiency on the course of cystic fibrosis: a review and meta-analysis. Glycobiology. 2011;21(3):271–282. PMID: 21045008. doi:10.1093/glycob/cwq161
  • Eisen DP. Mannose-binding lectin deficiency and respiratory tract infection. J Innate Immun. 2010;2(2):114–122. PubMed PMID: 20375630; PubMed Central PMCID: PMCPMC7179718. doi:10.1159/000228159
  • Mandal J, Malla B, Steffensen R, et al. Mannose-binding lectin protein and its association to clinical outcomes in COPD: a longitudinal study. Respir Res. 2015;16:150. PubMed PMID: 26684757; PubMed Central PMCID: PMCPMC4750539. doi:10.1186/s12931-015-0306-3
  • Chang WC, White MR, Moyo P, et al. Lack of the pattern recognition molecule mannose-binding lectin increases susceptibility to influenza A virus infection. BMC Immunol. 2010;11:64. PubMed PMID: 21182784; PubMed Central PMCID: PMCPMC3022599. doi:10.1186/1471-2172-11-64
  • Hodge S, Matthews G, Dean MM, et al. Therapeutic role for mannose-binding lectin in cigarette smoke-induced lung inflammation? Evidence from a murine model. Am J Respir Cell Mol Biol. 2010;42(2):235–242. PubMed PMID: 19411612. doi:10.1165/rcmb.2008-0486OC
  • Garred P, Pressler T, Madsen HO, et al. Association of mannose-binding lectin gene heterogeneity with severity of lung disease and survival in cystic fibrosis. J Clin Invest. 1999;104(4):431–437. PubMed PMID: 10449435; PubMed Central PMCID: PMCPMC408526. doi:10.1172/JCI6861
  • Garred P, Pressler T, Lanng S, et al. Mannose-binding lectin (MBL) therapy in an MBL-deficient patient with severe cystic fibrosis lung disease. Pediatr Pulmonol. 2002;33(3):201–207. PubMed PMID: 11836800. doi:10.1002/ppul.10064
  • Videbaek K, Buchvald F, Holgersen MG, et al. The impact of mannose-binding lectin polymorphisms on lung function in primary ciliary dyskinesia. Pediatr Pulmonol. 2019;54(8):1182–1189. PubMed PMID: 31012247. doi:10.1002/ppul.24346
  • Zheng X, Zhang L, Chen J, Gu Y, Xu J, Ouyang Y. Dendritic cells and Th17/Treg ratio play critical roles in pathogenic process of chronic obstructive pulmonary disease. Biomed Pharmacother. 2018;108:1141–1151. PubMed PMID: 30372815. doi:10.1016/j.biopha.2018.09.113
  • Wang H, Ying H, Wang S, et al. Imbalance of peripheral blood Th17 and Treg responses in patients with chronic obstructive pulmonary disease. Clin Respir J. 2015;9(3):330–341. PubMed PMID: 24720797. doi:10.1111/crj.12147
  • Cervilha DA, Ito JT, Lourenco JD, et al. The Th17/Treg cytokine imbalance in chronic obstructive pulmonary disease exacerbation in an animal model of cigarette smoke exposure and lipopolysaccharide challenge association. Sci Rep. 2019;9(1):1921. doi:10.1038/s41598-019-38600-z
  • Liu FW, Liu J, Weng D, et al. CD4+CD25+Foxp3+Regulatory T cells depletion may attenuate the development of silica-induced lung fibrosis in mice. PLoS One. 2010;5(11):e15404. PubMed PMID: WOS: 000283780800027. doi:10.1371/journal.pone.0015404
  • Zhang W, Wang Y, Yang L, et al. Effects of mannan-binding lectin on differentiation of Th17 cells. Chin J Microbiol Immunol. 2017;15(12):666–673. PubMed PMID: 35300210; PubMed Central PMCID: PMCPMC8923702.
  • Wingelhofer B, Neubauer HA, Valent P, et al. Implications of STAT3 and STAT5 signaling on gene regulation and chromatin remodeling in hematopoietic cancer. Leukemia. 2018;32(8):1713–1726. PubMed PMID: 29728695; PubMed Central PMCID: PMCPMC6087715. doi:10.1038/s41375-018-0117-x
  • Qi QR, Yang ZM. Regulation and function of signal transducer and activator of transcription 3. World J Biol Chem. 2014;5(2):231–239. PubMed PMID: 24921012; PubMed Central PMCID: PMCPMC4050116. doi:10.4331/wjbc.v5.i2.231
  • Xiong J, Zhang X, Zhang Y, et al. Aryl hydrocarbon receptor mediates Jak2/STAT3 signaling for non-small cell lung cancer stem cell maintenance. Exp Cell Res. 2020;396(1):112288. PubMed PMID: 32941808. doi:10.1016/j.yexcr.2020.112288
  • Stobbe-Maicherski N, Wolff S, Wolff C, et al. The interleukin-6-type cytokine oncostatin M induces aryl hydrocarbon receptor expression in a STAT3-dependent manner in human HepG2 hepatoma cells. FEBS J. 2013;280(24):6681–6690. PubMed PMID: 24127753. doi:10.1111/febs.12571
  • Wincent E, Amini N, Luecke S, et al. The suggested physiologic aryl hydrocarbon receptor activator and cytochrome P4501 substrate 6-formylindolo[3,2-b]carbazole is present in humans. J Biol Chem. 2009;284(5):2690–2696. PubMed PMID: 19054769. doi:10.1074/jbc.M808321200
  • Hussain T, Al-Attas OS, Al-Daghri NM, et al. Induction of CYP1A1, CYP1A2, CYP1B1, increased oxidative stress and inflammation in the lung and liver tissues of rats exposed to incense smoke. Mol Cell Biochem. 2014;391(1–2):127–136. PubMed PMID: WOS: 000335570400014. doi:10.1007/s11010-014-1995-5
  • Chang TK, Chen J, Yang G, Yeung EY. Inhibition of procarcinogen-bioactivating human CYP1A1, CYP1A2 and CYP1B1 enzymes by melatonin. J Pineal Res. 2010;48(1):55–64. PubMed PMID: 19919601. doi:10.1111/j.1600-079X.2009.00724.x
  • Mescher M, Haarmann-Stemmann T. Modulation of CYP1A1 metabolism: from adverse health effects to chemoprevention and therapeutic options. Pharmacol Ther. 2018;187:71–87. PubMed PMID: 29458109. doi:10.1016/j.pharmthera.2018.02.012
  • Swierzko AS, Kilpatrick DC, Cedzynski M. Mannan-binding lectin in malignancy. Mol Immunol. 2013;55(1):16–21. PubMed PMID: 23062612. doi:10.1016/j.molimm.2012.09.005
  • Stockinger B, Di Meglio P, Gialitakis M, Duarte JH. The aryl hydrocarbon receptor: multitasking in the immune system. Annu Rev Immunol. 2014;32:403–432. PubMed PMID: 24655296. doi:10.1146/annurev-immunol-032713-120245