Gegen Qinlian Decoction Alleviates Experimental Colitis and Concurrent Lung Inflammation by Inhibiting the Recruitment of Inflammatory Myeloid Cells and Restoring Microbial Balance

References

• Rubin DT, Ananthakrishnan AN, Siegel CA, Sauer BG, Long MD. ACG clinical guideline: ulcerative colitis in adults. Am J Gastroenterol. 2019;114(3):384–413.
   PubMed Web of Science ®Google Scholar
• Zippi M, Corrado C, Pica R, et al. Extraintestinal manifestations in a large series of Italian inflammatory bowel disease patients. World J Gastroenterol. 2014;20(46):17463–17467.
   PubMed Web of Science ®Google Scholar
• Massart A, Hunt DP. Pulmonary manifestations of inflammatory bowel disease. Am J Med. 2020;133(1):39–43.
   PubMed Web of Science ®Google Scholar
• Turner-Warwick M. Fibrosing alveolitis and chronic liver disease. Q J Med. 1968;37(145):133–149.
   PubMedGoogle Scholar
• Camus P, Piard F, Ashcroft T, Gal AA, Colby TV. The lung in inflammatory bowel disease. Medicine (Baltimore). 1993;72(3):151–183.
   PubMed Web of Science ®Google Scholar
• Sato H, Okada F, Matsumoto S, et al. Chest high-resolution computed tomography findings in 601 patients with inflammatory bowel diseases. Acad Radiol. 2018;25(4):407–414.
   PubMed Web of Science ®Google Scholar
• Ates F, Karincaoglu M, Hacievliyagil SS, Yalniz M, Seckin Y. Alterations in the pulmonary function tests of inflammatory bowel diseases. Turk J Gastroenterol. 2011;22(3):293–299.
   PubMed Web of Science ®Google Scholar
• Kraft SC, Earle RH, Roesler M, Esterly JR. Unexplained bronchopulmonary disease with inflammatory bowel disease. Arch Intern Med. 1976;136(4):454–459.
   PubMedGoogle Scholar
• Dang AT, Marsland BJ. Microbes, metabolites, and the gut-lung axis. Mucosal Immunol. 2019;12(4):843–850.
   PubMed Web of Science ®Google Scholar
• Enaud R, Prevel R, Ciarlo E, et al. The gut-lung axis in health and respiratory diseases: a place for inter-organ and inter-Kingdom crosstalks. Front Cell Infect Microbiol. 2020;10:9.
   PubMed Web of Science ®Google Scholar
• Tulic MK, Piche T, Verhasselt V. Lung-gut cross-talk: evidence, mechanisms and implications for the mucosal inflammatory diseases. Clin Exp Allergy. 2016;46(4):519–528.
   PubMed Web of Science ®Google Scholar
• Tulic MK, Vivinus-Nebot M, Rekima A, et al. Presence of commensal house dust mite allergen in human gastrointestinal tract: a potential contributor to intestinal barrier dysfunction. Gut. 2016;65(5):757–766.
   PubMed Web of Science ®Google Scholar
• Eksteen B, Grant AJ, Miles A, et al. Hepatic endothelial CCL25 mediates the recruitment of CCR9+ gut-homing lymphocytes to the liver in primary sclerosing cholangitis. J Exp Med. 2004;200(11):1511–1517.
   PubMed Web of Science ®Google Scholar
• Leal MC, Dabritz J. Immunoregulatory role of myeloid-derived cells in inflammatory bowel disease. Inflamm Bowel Dis. 2015;21(12):2936–2947.
   PubMed Web of Science ®Google Scholar
• Glennon-Alty L, Hackett AP, Chapman EA, Wright HL. Neutrophils and redox stress in the pathogenesis of autoimmune disease. Free Radic Biol Med. 2018;125:25–35.
   PubMed Web of Science ®Google Scholar
• Zhang T, Jiang JH, Liu JT, et al. MK2 is required for neutrophil-derived ROS production and inflammatory bowel disease. Front Med. 2020;7:207.
   Web of Science ®Google Scholar
• Fournier BM, Parkos CA. The role of neutrophils during intestinal inflammation. Mucosal Immunol. 2012;5(4):354–366.
   PubMed Web of Science ®Google Scholar
• Li Q, Wang D, Hao S, et al. CD169 expressing macrophage, a key subset in mesenteric lymph nodes promotes mucosal inflammation in dextran sulfate sodium-induced colitis. Front Immunol. 2017;8:669.
   PubMed Web of Science ®Google Scholar
• Asano K, Takahashi N, Ushiki M, et al. Intestinal CD169(+) macrophages initiate mucosal inflammation by secreting CCL8 that recruits inflammatory monocytes. Nature Commun. 2015;6:1–4.
   Web of Science ®Google Scholar
• Jones GR, Bain CC, Fenton TM, et al. Dynamics of colon monocyte and macrophage activation during colitis. Front Immunol. 2018;9:2764.
   PubMed Web of Science ®Google Scholar
• Nishida A, Inoue R, Inatomi O, Bamba S, Naito Y, Andoh A. Gut microbiota in the pathogenesis of inflammatory bowel disease. Clin J Gastroenterol. 2018;11(1):1–10.
   PubMed Web of Science ®Google Scholar
• Huffnagle GB, Dickson RP, Lukacs NW. The respiratory tract microbiome and lung inflammation: a two-way street. Mucosal Immunol. 2017;10(2):299–306.
   PubMed Web of Science ®Google Scholar
• Scales BS, Dickson RP, Huffnagle GB. A tale of two sites: how inflammation can reshape the microbiomes of the gut and lungs. J Leukoc Biol. 2016;100(5):943–950.
   PubMed Web of Science ®Google Scholar
• Fan YL, Yi W, Huang H, Mei ZG, Feng ZT. Efficacy of herbal medicine (Gegen Qinlian Decoction) on ulcerative colitis: a systematic review of randomized controlled trials. Medicine. 2019;98:52.
   Web of Science ®Google Scholar
• Xu BL, Zhang GJ, Ji YB. Active components alignment of Gegenqinlian decoction protects ulcerative colitis by attenuating inflammatory and oxidative stress. J Ethnopharmacol. 2015;162:253–260.
   PubMed Web of Science ®Google Scholar
• Cui L, Feng L, Zhang ZH, Jia XB. The anti-inflammation effect of baicalin on experimental colitis through inhibiting TLR4/NF-κB pathway activation. Int Immunopharmacol. 2014;23(1):294–303.
   PubMed Web of Science ®Google Scholar
• Kwon HS, Oh SM, Kim JK. Glabridin, a functional compound of liquorice, attenuates colonic inflammation in mice with dextran sulphate sodium-induced colitis. Clin Exp Immunol. 2008;151(1):165–173.
   PubMed Web of Science ®Google Scholar
• Yan F, Wang L, Shi Y, et al. Berberine promotes recovery of colitis and inhibits inflammatory responses in colonic macrophages and epithelial cells in DSS-treated mice. Am J Physiol Gastrointest Liver Physiol. 2012;302(5):G504–514.
   PubMed Web of Science ®Google Scholar
• Liu X, Fan Y, Du L, Mei Z, Fu Y. In silico and in vivo studies on the mechanisms of Chinese medicine formula (Gegen Qinlian decoction) in the treatment of ulcerative colitis. Front Pharmacol. 2021;12:665102.
   PubMed Web of Science ®Google Scholar
• Ding Z, Zhong R, Yang Y, et al. Systems pharmacology reveals the mechanism of activity of Ge-Gen-Qin-Lian decoction against LPS-induced acute lung injury: a novel strategy for exploring active components and effective mechanism of TCM formulae. Pharmacol Res. 2020;156:104759.
   PubMed Web of Science ®Google Scholar
• Li Y, Liu J, Ma P, et al. Gegen Qinlian Tang regulates MMP-9/p38 MAPK pathway to repair intestinal mucosal barrier function in mice with ulcerative colitis. Chinese J Exp Tradit Med Formulae. 2021;27(4):8–15.
   Google Scholar
• Dutton JW 3rd, Artwohl JE, Huang X, Fortman JD. Assessment of pain associated with the injection of sodium pentobarbital in laboratory mice (mus musculus). J Am Assoc Lab Anim Sci. 2019;58(3):373–379.
   PubMed Web of Science ®Google Scholar
• Sun Z, Li J, Dai Y, et al. Indigo naturalis alleviates dextran sulfate sodium-induced colitis in rats via altering gut microbiota. Front Microbiol. 2020;11:731.
   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;71:322599.
   Web of Science ®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.
   PubMed Web of Science ®Google Scholar
• Singh UP, Singh NP, Murphy EA, et al. Chemokine and cytokine levels in inflammatory bowel disease patients. Cytokine. 2016;77:44–49.
   PubMed Web of Science ®Google Scholar
• Popivanova BK, Kostadinova FI, Furuichi K, et al. Blockade of a chemokine, CCL2, reduces chronic colitis-associated carcinogenesis in mice. Cancer Res. 2009;69(19):7884–7892.
   PubMed Web of Science ®Google Scholar
• Pei LY, Ke YS, Zhao HH, et al. Role of colonic microbiota in the pathogenesis of ulcerative colitis. BMC Gastroenterol. 2019;19(1):10.
   PubMed Web of Science ®Google Scholar
• Jin S, Zhao D, Cai CW, et al. Low-dose penicillin exposure in early life decreases Th17 and the susceptibility to DSS colitis in mice through gut microbiota modification. Sci Rep. 2017;7:43662.
   PubMed Web of Science ®Google Scholar
• Yao D, Dong M, Dai C, Wu S. Inflammation and inflammatory cytokine contribute to the initiation and development of ulcerative colitis and its associated cancer. Inflamm Bowel Dis. 2019;25(10):1595–1602.
   PubMed Web of Science ®Google Scholar
• Varol C, Vallon-Eberhard A, Elinav E, et al. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity. 2009;31(3):502–512.
   PubMed Web of Science ®Google Scholar
• Kratofil RM, Kubes P, Deniset JF. Monocyte conversion during inflammation and injury. Arterioscler Thromb Vasc Biol. 2017;37(1):35–42.
   PubMed Web of Science ®Google Scholar
• Raghu H, Lepus CM, Wang Q, et al. CCL2/CCR2, but not CCL5/CCR5, mediates monocyte recruitment, inflammation and cartilage destruction in osteoarthritis. Ann Rheum Dis. 2017;76(5):914–922.
   PubMed Web of Science ®Google Scholar
• Li QT, Wang D, Hao SY, et al. CD169 expressing macrophage, a key subset in mesenteric lymph nodes promotes mucosal inflammation in dextran sulfate sodium-induced colitis. Front Immunol. 2017;8:669.
   PubMed Web of Science ®Google Scholar
• Gupta SJ, Gupta VL, Kothari HG, Samarth AR, Gaikwad NR, Parmar SM. Assessment of occult pulmonary involvement in ulcerative colitis. Inflamm Intest Dis. 2020;5(3):144–150.
   PubMedGoogle Scholar
• Liu G, Mateer SW, Hsuz A, et al. Platelet activating factor receptor regulates colitis-induced pulmonary inflammation through the NLRP3 inflammasome. Mucosal Immunol. 2019;12(4):862–873.
   PubMed Web of Science ®Google Scholar
• Nay MA, Auvet A, Mankikian J, Herve V, Dequin PF, Guillon A. Evaluation of a flexible bronchoscope prototype designed for bronchoscopy during mechanical ventilation: a proof-of-concept study. Anaesthesia. 2017;72(6):719–728.
   PubMed Web of Science ®Google Scholar
• Lokwani R, Wark PAB, Baines KJ, Barker D, Simpson JL. Hypersegmented airway neutrophils and its association with reduced lung function in adults with obstructive airway disease: an exploratory study. BMJ Open. 2019;9(1):e024330.
   PubMed Web of Science ®Google Scholar
• Abraham E. Neutrophils and acute lung injury. Crit Care Med. 2003;31(4 Suppl):S195–199.
   PubMed Web of Science ®Google Scholar
• Yamasaki K, Eeden SFV. Lung macrophage phenotypes and functional responses: role in the pathogenesis of COPD. Int J Mol Sci. 2018;19:2.
   Web of Science ®Google Scholar
• Zhang WK, Dai HJ, Lin F, et al. Ly-6C(high) inflammatory-monocyte recruitment is regulated by p38 MAPK/MCP-1 activation and promotes ventilator-induced lung injury. Int Immunopharmacol. 2020;78:106015.
   PubMed Web of Science ®Google Scholar
• Yang JB, Agarwal M, Ling S, et al. Diverse injury pathways induce alveolar epithelial cell CCL2/12, which promotes lung fibrosis. Am J Respir Cell Mol Biol. 2020;62(5):622–632.
   PubMed Web of Science ®Google Scholar
• Guillamat-Prats R, Camprubi-Rimblas M, Tantinya N, Artigas A. Local depletion of the recruitment of macrophages reduces acute lung injury in rats. Eur Respir J. 2018;52:PA4296.
   Web of Science ®Google Scholar
• Mateer SW, Mathe A, Bruce J, et al. IL-6 drives neutrophil-mediated pulmonary inflammation associated with bacteremia in murine models of colitis. Am J Pathol. 2018;188(7):1625–1639.
   PubMed Web of Science ®Google Scholar
• Walujkar SA, Kumbhare SV, Marathe NP, et al. Molecular profiling of mucosal tissue associated microbiota in patients manifesting acute exacerbations and remission stage of ulcerative colitis. World J Microbiol Biotechnol. 2018;34(6):76.
   PubMed Web of Science ®Google Scholar
• El-Dallal M, Stein DJ, Raita Y, Feuerstein JD. The impact of obesity on hospitalized patients with ulcerative colitis. Ann Gastroenterol. 2021;34(2):196–201.
   PubMed Web of Science ®Google Scholar
• Song YJ, Shen HT, Liu TT, et al. Effects of three different mannans on obesity and gut microbiota in high-fat diet-fed C57BL/6J mice. Food Funct. 2021;12(10):4606–4620.
   PubMed Web of Science ®Google Scholar
• Vich Vila A, Imhann F, Collij V, et al. Gut microbiota composition and functional changes in inflammatory bowel disease and irritable bowel syndrome. Sci Transl Med. 2018;10:472.
   Web of Science ®Google Scholar
• Lo Presti A, Zorzi F, Del Chierico F, et al. Fecal and mucosal microbiota profiling in irritable bowel syndrome and inflammatory bowel disease. Front Microbiol. 2019;10:1655.
   PubMed Web of Science ®Google Scholar
• Yilmaz B, Juillerat P, Oyas O, et al. Microbial network disturbances in relapsing refractory Crohn’s disease. Nat Med. 2019;25(2):323–336.
   PubMed Web of Science ®Google Scholar
• Zhang T, Ji X, Lu G, Zhang F. The potential of Akkermansia muciniphila in inflammatory bowel disease. Appl Microbiol Biotechnol. 2021;105(14–15):5785–5794.
   PubMed Web of Science ®Google Scholar
• Lee Y, Sugihara K, Gillilland MG 3rd, Jon S, Kamada N, Moon JJ. Hyaluronic acid-bilirubin nanomedicine for targeted modulation of dysregulated intestinal barrier, microbiome and immune responses in colitis. Nat Mater. 2020;19(1):118–126.
   PubMed Web of Science ®Google Scholar
• Zhu W, Yan J, Zhi C, Zhou Q, Yuan X. 1,25(OH)2D3 deficiency-induced gut microbial dysbiosis degrades the colonic mucus barrier in Cyp27b1 knockout mouse model. Gut Pathog. 2019;11(1):1–11.
   PubMed Web of Science ®Google Scholar
• Van Treuren W, Dodd D. Microbial contribution to the human metabolome: implications for health and disease. Annu Rev Pathol. 2020;15:345–369.
   PubMed Web of Science ®Google Scholar
• Martinez-Fierro ML, Garza-Veloz I, Rocha-Pizana MR, et al. Serum cytokine, chemokine, and growth factor profiles and their modulation in inflammatory bowel disease. Medicine. 2019;98:38.
   Web of Science ®Google Scholar
• Dumas A, Bernard L, Poquet Y, Lugo-Villarino G, Neyrolles O. The role of the lung microbiota and the gut-lung axis in respiratory infectious diseases. Cell Microbiol. 2018;20(12):e12966.
   PubMed Web of Science ®Google Scholar
• Leiva-Juarez MM, Kolls JK, Evans SE. Lung epithelial cells: therapeutically inducible effectors of antimicrobial defense. Mucosal Immunol. 2018;11(1):21–34.
   PubMed Web of Science ®Google Scholar
• Zhang DP, Li S, Wang N, Tan HY, Zhang ZM, Feng YB. The cross-talk between gut microbiota and lungs in common lung diseases. Front Microbiol. 2020;11:301.
   PubMed Web of Science ®Google Scholar
• Zhao F, An R, Wang L, Shan J, Wang X. Specific gut microbiome and serum metabolome changes in lung cancer patients. Front Cell Infect Microbiol. 2021;11:725284.
   PubMed Web of Science ®Google Scholar
• Aguilera-Arreola MG, Ostria-Hernandez ML, Albarran-Fernandez E, et al. Correct identification of Ochrobactrum anthropi from blood culture using 16rRNA sequencing: a first case report in an immunocompromised patient in Mexico. Front Med. 2018;5:205.
   Web of Science ®Google Scholar
• Ryan MP, Pembroke JT. The genus Ochrobactrum as major opportunistic pathogens. Microorganisms. 2020;8(11):1797.
   PubMed Web of Science ®Google Scholar
• Comberiati P, Di Cicco M, Paravati F, et al. The role of gut and lung microbiota in susceptibility to tuberculosis. Int J Environ Res Public Health. 2021;18(22):12220.
   PubMed Web of Science ®Google Scholar
• Wu J, Liu W, He L, et al. Sputum microbiota associated with new, recurrent and treatment failure tuberculosis. PLoS One. 2013;8(12):e83445.
   PubMed Web of Science ®Google Scholar