题名

Dachengqi Decoction alleviates intestinal inflammation in ovalbumin-induced asthma by reducing group 2 innate lymphoid cells in a microbiota-dependent manner

DOI

10.1016/j.jtcme.2023.01.003

作者

Zirui Liu;Yalan Li;Na Li;Yongan Wang;Qiuyi Li;Dongyu Ge;Guiying Peng;Mengyu Zhou

关键词

Dachengqi Decoction ; Asthma ; Intestinal inflammation ; Gut microbiota ; ILC2

期刊名称

Journal of Traditional and Complementary Medicine

卷期/出版年月

13卷2期(2023 / 03 / 01)

页次

183 - 192

内容语文

英文

中文摘要

Background and aim: Dachengqi Decoction (DCQD) as a classic traditional Chinese medicine has been reported to be effective in treating asthma, but its mechanism remains unknown. This study aimed to reveal the mechanisms of DCQD on the intestinal complications of asthma mediated by group 2 innate lymphoid cells (ILC2) and intestinal microbiota. Experimental procedure: Ovalbumin (OVA) was used to construct asthmatic murine models. IgE, cytokines (e.g., IL-4, IL-5), fecal water content, colonic length, histopathologic appearance, and gut microbiota were evaluated in asthmatic mice treated with DCQD. Finally, we administered DCQD to antibiotic-treated asthmatic mice to measure the ILC2 in the small intestine and colon. Results and conclusion: DCQD decreased pulmonary IgE, IL-4, and IL-5 levels in asthmatic mice. The fecal water content, the colonic length weight loss, and the epithelial damage of jejunum, ileum, and colon of asthmatic mice were ameliorated by DCQD. Meanwhile, DCQD greatly improved intestinal dysbiosis by enriching Allobaculum, Romboutsia and Turicibacter in the whole intestine, and Lactobacillus gasseri only in the colon. However, DCQD caused less abundant Faecalibaculum and Lactobacillus vaginalis in the small intestine of asthmatic mice. A higher ILC2 proportion in different gut segments of asthmatic mice was reversed by DCQD. Finally, significant correlations appeared between DCQD-mediated specific bacteria and cytokines (e.g., IL-4, IL-5) or ILC2. These findings indicate that DCQD alleviated the concurrent intestinal inflammation in OVA-induced asthma by decreasing the excessive accumulation of intestinal ILC2 in a microbiota-dependent manner across different gut locations.

主题分类 醫藥衛生 > 中醫藥學
参考文献
  1. Alam, MA,Subhan, N,Rahman, MM,Uddin, SJ,Reza, HM,Sarker, SD(2014).Effect of citrus flavonoids, naringin and naringenin, on metabolic syndrome and their mechanisms of action.Adv Nutr,5(4),404-417.
  2. Athari, SS(2019).Targeting cell signaling in allergic asthma.Signal Transduct Targeted Ther,4,45.
  3. Barcik, W,Boutin, RCT,Sokolowska, M,Finlay, BB(2020).The role of lung and gut microbiota in the pathology of asthma.Immunity,52(2),241-255.
  4. Benjamini, Y,Hochberg, Y(1995).Controlling the false discovery rate: a practical and powerful approach to multiple testing.J R Stat Soc Series B Stat Methodol,57(1),289-300.
  5. Bowerman, KL,Rehman, SF,Vaughan, A(2020).Disease-associated gut microbiome and metabolome changes in patients with chronic obstructive pulmonary disease.Nat Commun,11(1),5886.
  6. Chen, M,Fan, HN,Chen, XY,Yi, YC,Zhang, J,Zhu, JS(2022).Alterations in the saliva microbiome in patients with gastritis and small bowel inflammation.Microb Pathog,165,105491.
  7. Colman, RJ,Rosario, NBS,Gutierrez Bonilla, A(2018).Prevalence of functional GI disorders among pediatric patients with persistent asthma.J Dig Dis.,19(9),522-528.
  8. Cristofori, F,Dargenio, VN,Dargenio, C,Miniello, VL,Barone, M,Francavilla, R(2021).Anti-inflammatory and immunomodulatory effects of probiotics in gut inflammation: a door to the body.Front Immunol,12,578386.
  9. Deshmukh, F,Vasudevan, A,Mengalie, E(2019).Association between irritable bowel syndrome and asthma: a meta-analysis and systematic review.Ann Gastroenterol,32(6),570-577.
  10. Fallon, PG,Schwartz, C(2020).The high and lows of type 2 asthma and mouse models.J Allergy Clin Immunol,145(2),496-498.
  11. Frati, F,Salvatori, C,Incorvaia, C(2018).The role of the microbiome in asthma: the gut-lung axis.Int J Mol Sci.,20(1),123.
  12. Freuer, D,Linseisen, J,Meisinger, C(2022).Asthma and the risk of gastrointestinal disorders: a Mendelian randomization study.BMC Med,20(1),82.
  13. Ganal-Vonarburg, SC,Duerr, CU(2020).The interaction of intestinal microbiota and innate lymphoid cells in health and disease throughout life.Immunology,159(1),39-51.
  14. Gurram, RK,Zhu, J(2019).Orchestration between ILC2s and Th2 cells in shaping type 2 immune responses.Cell Mol Immunol,16(3),225-235.
  15. Halim, TYF,Rana, BMJ,Walker, JA(2018).Tissue-restricted adaptive type 2 immunity is orchestrated by expression of the costimulatory molecule OX40L on group 2 innate lymphoid cells.Immunity,48(6),1195-1207.e6.
  16. Han, DH,Kim, WK,Lee, C(2022).Co-administration of Lactobacillus gasseri KBL697 and tumor necrosis factor-alpha inhibitor infliximab improves colitis in mice.Sci Rep,12(1),9640.
  17. Helfrich, S,Mindt, BC,Fritz, JH,Duerr, CU(2019).Group 2 innate lymphoid cells in respiratory allergic inflammation.Front Immunol,10,930.
  18. Hong, Y,Chu, Z,Kong, J(2022).IL-17A aggravates asthma-induced intestinal immune injury by promoting neutrophil trafficking.J Leukoc Biol,112(3),425-435.
  19. Hu, X,Liu, S,Zhu, J,Ni, H(2019).Dachengqi Decoction alleviates acute lung injury and inhibits inflammatory cytokines production through TLR4/NF-kB signaling pathway in vivo and in vitro.J Cell Biochem,120(6),8956-8964.
  20. Hu, Y,Huang, W,Luo, Y(2021).Assessment of the anti-inflammatory effects of three rhubarb anthraquinones in LPS-stimulated RAW264.7 macrophages using a pharmacodynamic model and evaluation of the structure-activity relationships.J Ethnopharmacol,273,114027.
  21. Huang, J,Zhang, J,Wang, X(2022).Effect of probiotics on respiratory tract allergic disease and gut microbiota.Front Nutr,9,821900.
  22. Huang, K,Yang, T,Xu, J(2019).Prevalence, risk factors, and management of asthma in China: a national cross-sectional study.Lancet,394(10196),407-418.
  23. Huang, Y,Mao, K,Chen, X(2018).S1P-dependent interorgan trafficking of group 2 innate lymphoid cells supports host defense.Science.,359(6371),114-119.
  24. Hufnagl, K,Pali-Schöll, I,Roth-Walter, F,Jensen-Jarolim, E(2020).Dysbiosis of the gut and lung microbiome has a role in asthma.Semin Immunopathol,42(1),75-93.
  25. Kato, A(2019).Group 2 innate lymphoid cells in airway diseases.Chest,156(1),141-149.
  26. Kaur, R,Chupp, G.(2019).Phenotypes and endotypes of adult asthma: moving toward precision medicine.J Allergy Clin Immunol,144(1),1-12.
  27. Kim, JY,Park, YJ,Lee, HJ,Park, MY,Kwon, O(2017).Effect of Lactobacillus gasseri BNR17 on irritable bowel syndrome: a randomized, double-blind, placebo-controlled, dose-finding trial.Food Sci Biotechnol,27(3),853-857.
  28. Kim, SJ,Kim, MC,Lee, BJ,Park, DH,Hong, SH,Um, JY(2010).Anti-inflammatory activity of chrysophanol through the suppression of NF-kappaB/caspase-1 activation in vitro and in vivo.Molecules,15(9),6436-6451.
  29. Kuenzig, ME,Bishay, K,Leigh, R,Kaplan, GG,Benchimol, EI,Crowdscreen SR Review Team(2018).Co-occurrence of asthma and the inflammatory bowel diseases: a systematic review and meta-analysis.Clin Transl Gastroenterol,9(9),188.
  30. Lee, J,Jung, E,Park, J(2005).Anti-inflammatory effects of magnolol and honokiol are mediated through inhibition of the downstream pathway of MEKK-1 in NF-kappaB activation signaling.Planta Med.,71(4),338-343.
  31. Li, Q,Li, D,Zhang, X(2018).E3 Ligase VHL Promotes group 2 innate lymphoid cell maturation and function via glycolysis inhibition and induction of interleukin33 receptor.Immunity,48(2),258-270. e5.
  32. Liu, ZR,Wang, YA,Zhong, DL,Dong, RJ,Ge, DY,Peng, GY(2019).Effect of Da Chengqitang on pulmonary inflammation and MAPK signal pathway in mice with allergic asthma.Chine J Experimen Tradition Med Formulae,25(9),1-5.
  33. Loo, EXL,Wang, Y,Siah, KTH(2020).Association between irritable bowel syndrome and allergic diseases: to make a case for aeroallergen.Int Arch Allergy Immunol,181(1),31-42.
  34. Mangifesta, M,Mancabelli, L,Milani, C(2018).Mucosal microbiota of intestinal polyps reveals putative biomarkers of colorectal cancer.Sci Rep,8(1),13974.
  35. Manosalva, C,Quiroga, J,Hidalgo, AI(2022).Role of lactate in inflammatory processes: friend or foe.Front Immunol,12,808799.
  36. Nair, AB,Jacob, S(2016).A simple practice guide for dose conversion between animals and human.J Basic Clin Pharm,7(2),27-31.
  37. Ning, QJ,Zhan, SY,Feng, XX(2020).Simultaneous determination of 10 active ingredients in Dachengqi Decoction by HPLC.J China Prescrip Drug,18(10),35-38.
  38. Niu, L,Hou, Y,Jiang, M,Bai, G(2021).The rich pharmacological activities of Magnolia officinalis and secondary effects based on significant intestinal contributions.J Ethnopharmacol,281,114524.
  39. Oliphant, CJ,Hwang, YY,Walker, JA(2014).MHCII-mediated dialog between group 2 innate lymphoid cells and CD4(+) T cells potentiates type 2 immunity and promotes parasitic helminth expulsion.Immunity,41(2),283-295.
  40. Papi, A,Brightling, C,Pedersen, SE,Reddel, HK(2018).Asthma.Lancet,391(10122),783-800.
  41. Peters, MC,Wenzel, SE(2020).Intersection of biology and therapeutics: type 2 targeted therapeutics for adult asthma.Lancet,395(10221),371-383.
  42. Pivniouk, V,Gimenes, Junior JA,Honeker, LK,Vercelli, D(2020).The role of innate immunity in asthma development and protection: lessons from the environment.Clin Exp Allergy,50(3),282-290.
  43. Pu, Q,Lin, P,Gao, P(2021).Gut microbiota regulate gut-lung axis inflammatory responses by mediating ILC2 compartmental migration.J Immunol,207(1),257-267.
  44. Reddy, AT,Lakshmi, SP,Reddy, RC(2012).Murine model of allergen induced asthma.JoVE,63,e3771.
  45. Serhan, CN,Chiang, N,Van Dyke, TE(2008).Resolving inflammation: dual antiinflammatory and pro-resolution lipid mediators.Nat Rev Immunol,8(5),349-361.
  46. Sun, W,Chen, Y,Li, H(2020).Material basis and molecular mechanisms of Dachengqi decoction in the treatment of acute pancreatitis based on network pharmacology.Biomed Pharmacother,121,109656.
  47. Tang, T,Wang, F,Liu, J,Ye, W,Zhao, T,Li, Z(2022).Rhubarb alleviates acute lung injury by modulating gut microbiota dysbiosis in mice.Curr Microbiol,79(4),116.
  48. Tang, X,Li, X,Wang, Y(2020).Butyric acid increases the therapeutic effect of EHLJ7 on ulcerative colitis by inhibiting JAK2/STAT3/SOCS1 signaling pathway.Front Pharmacol,10,1553.
  49. Wang, Z,Li, F,Liu, J(2022).Intestinal Microbiota - an unmissable bridge to severe acute pancreatitis-associated acute lung injury.Front Immunol,13,913178.
  50. Yin, FT,Zhou, XH,Kang, SY(2022).Prediction of the mechanism of Dachengqi Decoction treating colorectal cancer based on the analysis method of "into serum components-action target-key pathway".J Ethnopharmacol,293,115286.
  51. Zhang, D,Li, S,Wang, N,Tan, HY,Zhang, Z,Feng, Y(2020).The cross-talk between gut microbiota and lungs in common lung diseases.Front Microbiol,11,301.
  52. Zhao, X,Zhang, Y,Li, J(2015).Tissue Pharmacology of Da-Cheng-Qi Decoction in experimental acute pancreatitis in rats.Evid Based Complement Alternat Med,2015,283175.
  53. Zheng, H,Zhang, Y,Pan, J(2021).The role of type 2 innate lymphoid cells in allergic diseases.Front Immunol,12,586078.
  54. Zheng, HC,Liu, ZR,Li, YL(2021).Allium tuberosum alleviates pulmonary inflammation by inhibiting activation of innate lymphoid cells and modulating intestinal microbiota in asthmatic mice.J Integr Med,19(2),158-166.
  55. Zheng, HC,Wang, YA,Liu, ZR(2020).Consumption of lamb meat or basa fish shapes the gut microbiota and aggravates pulmonary inflammation in asthmatic mice.J Asthma Allergy,13,509-520.
  56. Zhou, P,Hao, X,Liu, Y(2021).Determination of the protective effects of Hua-Zhuo-Jie-Du in chronic atrophic gastritis by regulating intestinal microbiota and metabolites: combination of liquid chromatograph mass spectrometer metabolic profiling and 16S rRNA gene sequencing.Chin Med.,16(1),37.