Xuanbai Chengqi Decoction Ameliorates Pulmonary Inflammation via Reshaping Gut Microbiota and Rectifying Th17/Treg Imbalance in a Murine Model of Chronic Obstructive Pulmonary Disease

References

• Guan WJ, Zheng XY, Chung KF, Zhong NS. Impact of air pollution on the burden of chronic respiratory diseases in China: time for urgent action. Lancet. 2016;388(10054):1939–1951. doi:10.1016/S0140-6736(16)31597-5
   PubMed Web of Science ®Google Scholar
• Collaborators GBDCoD. Global, regional, and national age-sex specific mortality for 264 causes of death, 1980–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet. 2017;390(10100):1151–1210. doi:10.1016/S0140-6736(17)32152-9
   PubMed Web of Science ®Google Scholar
• Barnes PJ. Targeting cytokines to treat asthma and chronic obstructive pulmonary disease. Nat Rev Immunol. 2018;18(7):454–466. doi:10.1038/s41577-018-0006-6
   PubMed Web of Science ®Google Scholar
• Bowerman KL, Rehman SF, Vaughan A, et al. Disease-associated gut microbiome and metabolome changes in patients with chronic obstructive pulmonary disease. Nat Commun. 2020;11(1):5886. doi:10.1038/s41467-020-19701-0
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1016/j.biopha.2018.09.113
   PubMed Web of Science ®Google Scholar
• Alcorn JF, Crowe CR, Kolls JK. TH17 cells in asthma and COPD. Annu Rev Physiol. 2010;72:495–516. doi:10.1146/annurev-physiol-021909-135926
   PubMed Web of Science ®Google Scholar
• Weaver CT, Hatton RD. Interplay between the TH17 and TReg cell lineages: a (co-) evolutionary perspective. Nat Rev Immunol. 2009;9(12):883–889. doi:10.1038/nri2660
   PubMed Web of Science ®Google Scholar
• Di Stefano A, Caramori G, Gnemmi I, et al. T helper type 17-related cytokine expression is increased in the bronchial mucosa of stable chronic obstructive pulmonary disease patients. Clin Exp Immunol. 2009;157(2):316–324. doi:10.1111/j.1365-2249.2009.03965.x
   PubMed Web of Science ®Google Scholar
• Brusselle GG, Joos GF, Bracke KR. New insights into the immunology of chronic obstructive pulmonary disease. Lancet. 2011;378(9795):1015–1026. doi:10.1016/S0140-6736(11)60988-4
   PubMed Web of Science ®Google Scholar
• Lee SH, Goswami S, Grudo A, et al. Antielastin autoimmunity in tobacco smoking-induced emphysema. Nat Med. 2007;13(5):567–569. doi:10.1038/nm1583
   PubMed Web of Science ®Google Scholar
• Hou J, Sun Y, Hao Y, et al. Imbalance between subpopulations of regulatory T cells in COPD. Thorax. 2013;68(12):1131–1139. doi:10.1136/thoraxjnl-2012-201956
   PubMed Web of Science ®Google Scholar
• Cervilha DAB, Ito JT, Lourenço 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
   PubMed Web of Science ®Google Scholar
• Donaldson GP, Lee SM, Mazmanian SK. Gut biogeography of the bacterial microbiota. Nat Rev Microbiol. 2016;14(1):20–32. doi:10.1038/nrmicro3552
   PubMed Web of Science ®Google Scholar
• Li N, Zuo B, Huang S, et al. Spatial heterogeneity of bacterial colonization across different gut segments following inter-species microbiota transplantation. Microbiome. 2020;8(1):161. doi:10.1186/s40168-020-00917-7
   PubMed Web of Science ®Google Scholar
• Mendez R, Banerjee S, Bhattacharya SK, Banerjee S. Lung inflammation and disease: a perspective on microbial homeostasis and metabolism. IUBMB Life. 2019;71(2):152–165. doi:10.1002/iub.1969
   PubMed Web of Science ®Google Scholar
• Caballero S, Pamer EG. Microbiota-mediated inflammation and antimicrobial defense in the intestine. Annu Rev Immunol. 2015;33:227–256. doi:10.1146/annurev-immunol-032713-120238
   PubMed Web of Science ®Google Scholar
• Mayhew D, Devos N, Lambert C, et al. Longitudinal profiling of the lung microbiome in the AERIS study demonstrates repeatability of bacterial and eosinophilic COPD exacerbations. Thorax. 2018;73(5):422–430. doi:10.1136/thoraxjnl-2017-210408
   PubMed Web of Science ®Google Scholar
• Pragman AA, Lyu T, Baller JA, et al. The lung tissue microbiota of mild and moderate chronic obstructive pulmonary disease. Microbiome. 2018;6(1):7. doi:10.1186/s40168-017-0381-4
   PubMedGoogle Scholar
• He Y, Wen Q, Yao F, Xu D, Huang Y, Wang J. Gut-lung axis: the microbial contributions and clinical implications. Crit Rev Microbiol. 2017;43(1):81–95. doi:10.1080/1040841X.2016.1176988
   PubMed Web of Science ®Google Scholar
• Allais L, Kerckhof FM, Verschuere S, et al. Chronic cigarette smoke exposure induces microbial and inflammatory shifts and mucin changes in the murine gut. Environ Microbiol. 2016;18(5):1352–1363. doi:10.1111/1462-2920.12934
   PubMed Web of Science ®Google Scholar
• Lai HC, Lin TL, Chen TW, et al. Gut microbiota modulates COPD pathogenesis: role of anti-inflammatory Parabacteroides goldsteinii lipopolysaccharide. Gut. 2021;gutjnl-2020-322599. doi:10.1136/gutjnl-2020-322599
   Web of Science ®Google Scholar
• Pandiyan P, Bhaskaran N, Zou M, Schneider E, Jayaraman S, Huehn J. Microbiome dependent regulation of Tregs and Th17 cells in mucosa. Front Immunol. 2019;10:426. doi:10.3389/fimmu.2019.00426
   PubMed Web of Science ®Google Scholar
• Omenetti S, Pizarro TT. The Treg/Th17 axis: a dynamic balance regulated by the gut microbiome. Front Immunol. 2015;6:639. doi:10.3389/fimmu.2015.00639
   PubMed Web of Science ®Google Scholar
• Jin J, Zhang H, Li D, et al. Effectiveness of Xin Jia Xuan Bai Cheng Qi Decoction in treating acute exacerbation of chronic obstructive pulmonary disease: study protocol for a multicentre, randomised, controlled trial. BMJ Open. 2019;9(11):e030249. doi:10.1136/bmjopen-2019-030249
   PubMed Web of Science ®Google Scholar
• Liu M, Zhong X, Li Y, et al. Xuan Bai Cheng Qi formula as an adjuvant treatment of acute exacerbation of chronic obstructive pulmonary disease of the syndrome type phlegm-heat obstructing the lungs: a multicenter, randomized, double-blind, placebo-controlled clinical trial. BMC Complement Altern Med. 2014;14(1):239. doi:10.1186/1472-6882-14-239
   PubMedGoogle Scholar
• Qin H, Wen HT, Gu KJ, et al. Total extract of Xin Jia Xuan Bai Cheng Qi decoction inhibits pulmonary fibrosis via the TGF-beta/Smad signaling pathways in vivo and in vitro. Drug Des Devel Ther. 2019;13:2873–2886. doi:10.2147/DDDT.S185418
   PubMed Web of Science ®Google Scholar
• Zhu H, Wang S, Shan C, et al. Mechanism of protective effect of xuan-bai-cheng-qi decoction on LPS-induced acute lung injury based on an integrated network pharmacology and RNA-sequencing approach. Respir Res. 2021;22(1):188. doi:10.1186/s12931-021-01781-1
   PubMed Web of Science ®Google Scholar
• Mao Z, Wang H. Effects of Xuanbai Chengqi decoction on lung compliance for patients with exogenous pulmonary acute respiratory distress syndrome. Drug Des Devel Ther. 2016;10:793–798. doi:10.2147/DDDT.S93165
   PubMed Web of Science ®Google Scholar
• Wang Z, Fang K, Wang G, et al. Protective effect of amygdalin on epithelial-mesenchymal transformation in experimental chronic obstructive pulmonary disease mice. Phytother Res. 2019;33(3):808–817. doi:10.1002/ptr.6274
   PubMed Web of Science ®Google Scholar
• D’Hulst AI, Vermaelen KY, Brusselle GG, Joos GF, Pauwels RA. Time course of cigarette smoke-induced pulmonary inflammation in mice. Eur Respir J. 2005;26(2):204–213. doi:10.1183/09031936.05.00095204
   PubMed Web of Science ®Google Scholar
• Yoshida T, Tuder RM. Pathobiology of cigarette smoke-induced chronic obstructive pulmonary disease. Physiol Rev. 2007;87(3):1047–1082. doi:10.1152/physrev.00048.2006
   PubMed Web of Science ®Google Scholar
• Shin NR, Ko JW, Park SH, et al. Protective effect of HwangRyunHaeDok-Tang water extract against chronic obstructive pulmonary disease induced by cigarette smoke and lipopolysaccharide in a mouse model. J Ethnopharmacol. 2017;200:60–65. doi:10.1016/j.jep.2017.02.027
   PubMed Web of Science ®Google Scholar
• Cheng Q, Fang L, Feng D, et al. Memantine ameliorates pulmonary inflammation in a mice model of COPD induced by cigarette smoke combined with LPS. Biomed Pharmacother. 2019;109:2005–2013. doi:10.1016/j.biopha.2018.11.002
   PubMed Web of Science ®Google Scholar
• Zhu K, Zhou S, Xu A, et al. Microbiota imbalance contributes to COPD deterioration by enhancing IL-17a production via miR-122 and miR-30a. Mol Ther Nucleic Acids. 2020;22:520–529. doi:10.1016/j.omtn.2020.09.017
   PubMedGoogle Scholar
• Su Y, Han W, Giraldo C, De li Y, Block ER. Effect of cigarette smoke extract on nitric oxide synthase in pulmonary artery endothelial cells. Am J Respir Cell Mol Biol. 1998;19(5):819–825. doi:10.1165/ajrcmb.19.5.3091
   PubMed Web of Science ®Google Scholar
• Amano H, Murata K, Matsunaga H, et al. p38 Mitogen-activated protein kinase accelerates emphysema in mouse model of chronic obstructive pulmonary disease. J Recept Signal Transduct Res. 2014;34(4):299–306. doi:10.3109/10799893.2014.896380
   PubMed Web of Science ®Google Scholar
• Nair AB, Jacob S. A simple practice guide for dose conversion between animals and human. J Basic Clin Pharm. 2016;7(2):27–31. doi:10.4103/0976-0105.177703
   PubMedGoogle Scholar
• Huang J, Huang X, Chen Z, Zheng Q, Sun R. Dose conversion among different animals and healthy volunteers in pharmacological study. Chin J Clin Pharmacol Ther. 2004;9(9):1069.
   Google Scholar
• Zhang W, Li Q, Li D, Li J, Aki D, Liu YC. The E3 ligase VHL controls alveolar macrophage function via metabolic-epigenetic regulation. J Exp Med. 2018;215(12):3180–3193. doi:10.1084/jem.20181211
   PubMed Web of Science ®Google Scholar
• Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol. 1995;57(1):289–300.
   Web of Science ®Google Scholar
• Knochelmann HM, Dwyer CJ, Bailey SR, et al. When worlds collide: th17 and Treg cells in cancer and autoimmunity. Cell Mol Immunol. 2018;15(5):458–469. doi:10.1038/s41423-018-0004-4
   PubMed Web of Science ®Google Scholar
• Luo AN, Leach ST, Barres R, Hesson LB, Grimm MC, Simar D. The microbiota and epigenetic regulation of T helper 17/regulatory T cells: in search of a balanced immune system. Front Immunol. 2017;8. doi:10.3389/fimmu.2017.00008
   PubMed Web of Science ®Google Scholar
• Vlahos R, Bozinovski S. Recent advances in pre-clinical mouse models of COPD. Clin Sci (Lond). 2014;126(4):253–265. doi:10.1042/CS20130182
   PubMed Web of Science ®Google Scholar
• Kwan HY, Maddocks M, Nolan CM, et al. The prognostic significance of weight loss in chronic obstructive pulmonary disease-related cachexia: a prospective cohort study. J Cachexia Sarcopenia Muscle. 2019;10(6):1330–1338. doi:10.1002/jcsm.12463
   PubMed Web of Science ®Google Scholar
• Dransfield MT, Kunisaki KM, Strand MJ, et al. Acute exacerbations and lung function loss in smokers with and without chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2017;195(3):324–330. doi:10.1164/rccm.201605-1014OC
   PubMed Web of Science ®Google Scholar
• Chu X, Wei M, Yang X, et al. Effects of an anthraquinone derivative from Rheum officinale Baill, emodin, on airway responses in a murine model of asthma. Food Chem Toxicol. 2012;50(7):2368–2375. doi:10.1016/j.fct.2012.03.076
   PubMed Web of Science ®Google Scholar
• Zhang K, Jiao XF, Li JX, Wang XW. Rhein inhibits lipopolysaccharide-induced intestinal injury during sepsis by blocking the toll-like receptor 4 nuclear factor-kappaB pathway. Mol Med Rep. 2015;12(3):4415–4421. doi:10.3892/mmr.2015.3925
   PubMed Web of Science ®Google Scholar
• Lee HS, Jeong GS. Chrysophanol attenuates manifestations of immune bowel diseases by regulation of colorectal cells and T cells activation in vivo. Molecules. 2021;26(6):1682. doi:10.3390/molecules26061682
   PubMed Web of Science ®Google Scholar
• Yang HY, Chang HK, Lee JW, et al. Amygdalin suppresses lipopolysaccharide-induced expressions of cyclooxygenase-2 and inducible nitric oxide synthase in mouse BV2 microglial cells. Neurol Res. 2007;29(Suppl 1):S59–64. doi:10.1179/016164107X172248
   PubMed Web of Science ®Google Scholar
• Lang GP, Li C, Han YY. Rutin pretreatment promotes microglial M1 to M2 phenotype polarization. Neural Regen Res. 2021;16(12):2499–2504. doi:10.4103/1673-5374.313050
   PubMed Web of Science ®Google Scholar
• Ma C, Jiang Y, Zhang X, Chen X, Liu Z, Tian X. Isoquercetin ameliorates myocardial infarction through anti-inflammation and anti-apoptosis factor and regulating TLR4-NF-κB signal pathway. Mol Med Rep. 2018;17(5):6675–6680. doi:10.3892/mmr.2018.8709
   PubMed Web of Science ®Google Scholar
• Kim KH, Song -H-H, Ahn K-S, Oh S-R, Sadikot RT, Joo M. Ethanol extract of the tuber of Alisma orientale reduces the pathologic features in a chronic obstructive pulmonary disease mouse model. J Ethnopharmacol. 2016;188:21–30. doi:10.1016/j.jep.2016.05.004
   PubMed Web of Science ®Google Scholar
• Ghebre MA, Pang PH, Diver S, et al. Biological exacerbation clusters demonstrate asthma and chronic obstructive pulmonary disease overlap with distinct mediator and microbiome profiles. J Allergy Clin Immun. 2018;141(6):2027–2036.e2012. doi:10.1016/j.jaci.2018.04.013
   PubMed Web of Science ®Google Scholar
• Chakrabarti S, Patel KD. Matrix metalloproteinase-2 (MMP-2) and MMP-9 in pulmonary pathology. Exp Lung Res. 2005;31(6):599–621. doi:10.1080/019021490944232
   PubMed Web of Science ®Google Scholar
• Greenlee KJ, Werb Z, Kheradmand F. Matrix metalloproteinases in lung: multiple, multifarious, and multifaceted. Physiol Rev. 2007;87(1):69–98. doi:10.1152/physrev.00022.2006
   PubMed Web of Science ®Google Scholar
• Kumar M, Bhadoria DP, Dutta K, et al. Combinatorial effect of TIMP-1 and alpha1AT gene polymorphisms on development of chronic obstructive pulmonary disease. Clin Biochem. 2011;44(13):1067–1073. doi:10.1016/j.clinbiochem.2011.06.986
   PubMed Web of Science ®Google Scholar
• Abd E-FM-F, Ghazy MA, Mostafa MS, El-Attar MM, Osman A. Identification of MMP-9 as a biomarker for detecting progression of chronic obstructive pulmonary disease. Biochem Cell Biol. 2015;93(6):541–547. doi:10.1139/bcb-2015-0073
   PubMedGoogle Scholar
• Budden KF, Gellatly SL, Wood DLA, et al. Emerging pathogenic links between microbiota and the gut-lung axis. Nat Rev Microbiol. 2017;15(1):55–63. doi:10.1038/nrmicro.2016.142
   PubMed Web of Science ®Google Scholar
• Man WH, de Steenhuijsen Piters WA, Bogaert D. The microbiota of the respiratory tract: gatekeeper to respiratory health. Nat Rev Microbiol. 2017;15(5):259–270. doi:10.1038/nrmicro.2017.14
   PubMed Web of Science ®Google Scholar
• Le Bourvellec C, Boas PBV, Lepercq P, et al. Procyanidin-cell wall interactions within apple matrices decrease the metabolization of procyanidins by the human gut microbiota and the anti-inflammatory effect of the resulting microbial metabolome in vitro. Nutrients. 2019;11(3):664. doi:10.3390/nu11030664
   PubMed Web of Science ®Google Scholar
• Hu L, Jin L, Xia D, et al. Nitrate ameliorates dextran sodium sulfate-induced colitis by regulating the homeostasis of the intestinal microbiota. Free Radic Biol Med. 2020;152:609–621. doi:10.1016/j.freeradbiomed.2019.12.002
   PubMed Web of Science ®Google Scholar
• Opstelten JL, Plassais J, van Mil SWC, et al. Gut microbial diversity is reduced in smokers with Crohn’s disease. Inflamm Bowel Dis. 2016;22(9):2070–2077. doi:10.1097/MIB.0000000000000875
   PubMed Web of Science ®Google Scholar
• Pujo J, Petitfils C, Le Faouder P, et al. Bacteria-derived long chain fatty acid exhibits anti-inflammatory properties in colitis. Gut. 2021;70(6):1088–1097. doi:10.1136/gutjnl-2020-321173
   PubMed Web of Science ®Google Scholar
• Ruocco C, Ragni M, Rossi F, et al. Manipulation of dietary amino acids prevents and reverses obesity in mice through multiple mechanisms that modulate energy homeostasis. Diabetes. 2020;69(11):2324–2339. doi:10.2337/db20-0489
   PubMed Web of Science ®Google Scholar
• Zhao JB, Liu P, Wu Y, et al. Dietary fiber increases butyrate-producing bacteria and improves the growth performance of weaned piglets. J Agr Food Chem. 2018;66(30):7995–8004. doi:10.1021/acs.jafc.8b02545
   PubMed Web of Science ®Google Scholar
• Zheng DP, Liwinski T, Elinav E. Interaction between microbiota and immunity in health and disease. Cell Res. 2020;30(6):492–506. doi:10.1038/s41422-020-0332-7
   PubMed Web of Science ®Google Scholar
• Ansaldo E, Farley TK, Belkaid Y. Control of immunity by the microbiota. Annu Rev Immunol. 2021;39:449–479. doi:10.1146/annurev-immunol-093019-112348
   PubMed Web of Science ®Google Scholar
• Michalovich D, Rodriguez-Perez N, Smolinska S, et al. Obesity and disease severity magnify disturbed microbiome-immune interactions in asthma patients. Nat Commun. 2019;10(1):5711. doi:10.1038/s41467-019-13751-9
   PubMed Web of Science ®Google Scholar
• Wang Z, Maschera B, Lea S, et al. Airway host-microbiome interactions in chronic obstructive pulmonary disease. Respir Res. 2019;20(1):113. doi:10.1186/s12931-019-1085-z
   PubMed Web of Science ®Google Scholar
• Wright JL, Churg A. Animal models of cigarette smoke-induced COPD. Chest. 2002;122(6 Suppl):301S–306S. doi:10.1378/chest.122.6_suppl.301S
   PubMed Web of Science ®Google Scholar
• Limjunyawong N, Craig JM, Lagasse HAD, Scott AL, Mitzner W. Experimental progressive emphysema in BALB/cJ mice as a model for chronic alveolar destruction in humans. Am J Physiol-Lung C. 2015;309(7):L662–L676. doi:10.1152/ajplung.00214.2015
   PubMed Web of Science ®Google Scholar