Alpinetin exerts anti-colitis efficacy by activating AhR, regulating miR-302/DNMT-1/CREB signals, and therefore promoting Treg differentiation

Cell Death and Disease

Volumn 9, Issue 9, 2018, Pages

  Lv, Qi ^a   Shi, Can ^a   Qiao, Simiao ^a   Cao, Na ^a   Guan, Chunge ^a   Dai, Yue ^a   Wei, Zhifeng ^a  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPINETIN; AROMATIC HYDROCARBON RECEPTOR; BAICALEIN; BAICALIN; CH 223191; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYTOCHROME P450 1A1; DACTINOMYCIN; DNA (CYTOSINE 5) METHYLTRANSFERASE 1; EPIGALLOCATECHIN GALLATE; FLAVONOID; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; KAEMPFEROL; LUTEOLIN; MESALAZINE; MICRORNA; MICRORNA 148A; MICRORNA 155; MICRORNA 21; MICRORNA 302; MICRORNA 31; MICRORNA 490; MYELOPEROXIDASE; PROTEIN INHIBITOR; RETINOID RELATED ORPHAN RECEPTOR GAMMA; RETINOID RELATED ORPHAN RECEPTOR GAMMA T; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CREB1 PROTEIN, MOUSE; CYP1A1 PROTEIN, MOUSE; DEXTRAN SULFATE; DNMT1 PROTEIN, MOUSE; FLAVANONE DERIVATIVE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; HEAT SHOCK PROTEIN 90; MIRN302 MICRORNA, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTI COLITIS ACTIVITY; ARTICLE; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; CELL VIABILITY; COLONIC LAMINA PROPRIA; CONTROLLED STUDY; DEXTRAN SULFATE SODIUM-INDUCED COLITIS; DNA BINDING; DOWN REGULATION; DRUG ACTIVITY; DRUG EFFICACY; EL4 CELL LINE; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE TARGETING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; LYMPHOCYTE DIFFERENTIATION; MESENTERY LYMPH NODE; MOUSE; MTT ASSAY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY T LYMPHOCYTE; REPORTER GENE; RNA SYNTHESIS; TH17 CELL; UPREGULATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; COLON; CYTOLOGY; DNA METHYLATION; DRUG EFFECT; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; ULCERATIVE COLITIS;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; COLITIS, ULCERATIVE; COLON; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYTOCHROME P-450 CYP1A1; DEXTRAN SULFATE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; DNA METHYLATION; FEMALE; FLAVANONES; FORKHEAD TRANSCRIPTION FACTORS; HSP90 HEAT-SHOCK PROTEINS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICRORNAS; PROMOTER REGIONS, GENETIC; RECEPTORS, ARYL HYDROCARBON; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 85052696566     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/s41419-018-0814-4     Document Type: Article

References (49)

1. Ungaro, R., Mehandru, S., Allen, P. B., Peyrin-Biroulet, L. & Colombel, J. F. Ulcerative colitis. Lancet 389, 1756–1770 (2016)
2. de Souza, H. S. & Fiocchi, C. Immunopathogenesis of IBD: current state of the art. Nat. Rev. Gastroenterol. Hepatol. 13, 13–27 (2016)
3. Abraham, C., Dulai, P. S., Vermeire, S. & Sandborn, W. J. Lessons learned from trials targeting cytokine pathways in patients with inflammatory bowel diseases. Gastroenterology 152, 374–388.e4 (2017)
4. Hu, X. et al. Phosphatase Wip1 masters IL-17-producing neutrophil-mediated colitis in mice. Inflamm. Bowel Dis. 22, 1316–1325 (2016)
5. Ueno, A. et al. Increased prevalence of circulating novel IL-17 secreting Foxp3 expressing CD4 + T cells and defective suppressive function of circulating Foxp3 + regulatory cells support plasticity between Th17 and regulatory T cells in inflammatory bowel disease patients. Inflamm. Bowel Dis. 19, 2522–2534 (2013)
6. Reißig, S. et al. Elevated levels of Bcl-3 inhibits Treg development and function resulting in spontaneous colitis. Nat. Commun. 8, 15069 (2017)
7. Esser, C., Rannug, A. & Stockinger, B. The aryl hydrocarbon receptor in immunity. Trends Immunol. 30, 447–454 (2009)
8. Quintana, F. J. et al. Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature 453, 65–71 (2008)
9. Furumatsu, K. et al. A role of the aryl hydrocarbon receptor in attenuation of colitis. Dig. Dis. Sci. 56, 2532–2544 (2011)
10. Singh, N. P. et al. Activation of aryl hydrocarbon receptor (AhR) leads to reciprocal epigenetic regulation of FoxP3 and IL-17 expression and amelioration of experimental colitis. PLoS ONE 6, e23522 (2011)
11. Lanis, J. M. et al. Tryptophan metabolite activation of the aryl hydrocarbon receptor regulates IL-10 receptor expression on intestinal epithelia. Mucosal Immunol. 10, 1133–1144 (2017)
12. Hu, K., Yang, Y., Tu, Q., Luo, Y. & Ma, R. Alpinetin inhibits LPS-induced inflammatory mediator response by activating PPAR-γ in THP-1-derived macrophages. Eur. J. Pharmacol. 721, 96–102 (2013)
13. Guan, S., Fang, B., Song, B., Xiong, Y. & Lu, J. Immunosuppressive activity of alpinetin on activation and cytokines secretion of murine T lymphocytes. Immunopharmacol. Immunotoxicol. 36, 290–296 (2014)
14. He, X. et al. Alpinetin attenuates inflammatory responses by suppressing TLR4 and NLRP3 signaling pathways in DSS-induced acute colitis. Sci. Rep. 6, 28370 (2016)
15. Zou, Y. et al. Baicalin attenuates TNBS-induced colitis in rats by modulating the Th17/Treg paradigm. Arch. Pharm. Res. 38, 1873–1887 (2015)
16. Wu, D., Wang, J., Pae, M. & Meydani, S. N. Green tea EGCG, T cells, and T cell-mediated autoimmune diseases. Mol. Asp. Med. 33, 107–118 (2012)
17. Zhang, S., Qin, C. & Safe, S. H. Flavonoids as aryl hydrocarbon receptor agonists/antagonists: effects of structure and cell context. Environ. Health Perspect. 111, 1877–1882 (2003)
18. Baumjohann, D. & Ansel, K. M. MicroRNA-mediated regulation of T helper cell differentiation and plasticity. Nat. Rev. Immunol. 13, 666–678 (2013)
19. Kalla, R. et al. MicroRNAs: new players in IBD. Gut 64, 504–517 (2015)
20. Singh, N. P. et al. Dietary Indoles Suppress Delayed-Type Hypersensitivity by Inducing a Switch from Proinflammatory Th17 Cells to Anti-Inflammatory Regulatory T Cells through Regulation of MicroRNA. J. Immunol. 196, 1108–1122 (2016)
21. Jin, Y., Zou, X. & Feng, X. 3,3’-Diindolylmethane negatively regulates Cdc25A and induces a G2/M arrest by modulation of microRNA 21 in human breast cancer cells. Anticancer Drugs 21, 814–822 (2010)
22. Li, X., Ma, J., Fang, Q. & Li, Y. Transcription alterations of microRNAs, cytochrome P4501A1 and 3A65, and AhR and PXR in the liver of zebrafish exposed to crude microcystins. Toxicon 73, 17–22 (2013)
23. Ma, F. et al. Anti-inflammatory effects of curcumin are associated with downregulating microRNA-155 in LPS-treated macrophages and mice. Pharm. Biol. 55, 1263–1273 (2017)
24. Hu, W., Zhao, J. & Pei, G. Activation of aryl hydrocarbon receptor (ahr) by tranilast, an anti-allergy drug, promotes miR-302 expression and cell reprogramming. J. Biol. Chem. 288, 22972–22984 (2013)
25. Lin, S. L. Concise review: Deciphering the mechanism behind induced pluripotent stem cell generation. Stem Cells 29, 1645–1649 (2011)
26. Lu, C. H. et al. DNA Methyltransferase Inhibitor Promotes Human CD4 + CD25hFOXP3 + Regulatory T Lymphocyte Induction under Suboptimal TCR Stimulation. Front. Immunol. 7, 488 (2016)
27. Lal, G. et al. Epigenetic regulation of Foxp3 expression in regulatory T cells by DNA methylation. J. Immunol. 182, 259–273 (2009)
28. Ogawa, C. et al. TGF-β-mediated Foxp3 gene expression is cooperatively regulated by Stat5, Creb, and AP-1 through CNS2. J. Immunol. 192, 475–483 (2014)
29. Kim, H. P. & Leonard, W. J. CREB/ATF-dependent T cell receptor-induced FoxP3 gene expression: a role for DNA methylation. J. Exp. Med. 204, 1543–1551 (2007)
30. Blonski, W., Buchner, A. M. & Lichtenstein, G. R. Treatment of ulcerative colitis. Curr. Opin. Gastroenterol. 30, 84–96 (2014)
31. Zhang, M. et al. Edible ginger-derived nanoparticles: A novel therapeutic approach for the prevention and treatment of inflammatory bowel disease and colitis-associated cancer. Biomaterials 101, 321–340 (2016)
32. Thakur, B. K. et al. Live and heat-killed probiotic Lactobacillus casei Lbs2 protects from experimental colitis through Toll-like receptor 2-dependent induction of T-regulatory response. Int. Immunopharmacol. 36, 39–50 (2016)
33. Ding, S., Blue, R. E., Morgan, D. R. & Lund, P. K. Comparison of multiple enzyme activatable near-infrared fluorescent molecular probes for detection and quantification of inflammation in murine colitis models. Inflamm. Bowel Dis. 20, 363–377 (2014)
34. Tsun, A., Chen, Z. & Li, B. Romance of the three kingdoms: RORgammat allies with HIF1alpha against FoxP3 in regulating T cell metabolism and differentiation. Protein Cell 2, 778–781 (2011)
35. Wang, J. et al. Epigallocatechin-3-gallate ameliorates experimental autoimmune encephalomyelitis by altering balance among CD4 + T-cell subsets. Am. J. Pathol. 180, 221–234 (2012)
36. Lee, S. Y. et al. Epigallocatechin-3-gallate ameliorates autoimmune arthritis by reciprocal regulation of T helper-17 regulatory T cells and inhibition of osteoclastogenesis by inhibiting STAT3 signaling. J. Leukoc. Biol. 100, 559–568 (2016)
37. Huai, W. et al. Aryl hydrocarbon receptor negatively regulates NLRP3 inflammasome activity by inhibiting NLRP3 transcription. Nat. Commun. 5, 4738 (2014)
38. Pedersen, I. & David, M. MicroRNAs in the immune response. Cytokine 43, 391–394 (2008)
39. Nakahama, T. et al. Aryl hydrocarbon receptor-mediated induction of the microRNA-132/212 cluster promotes interleukin-17-producing T-helper cell differentiation. Proc. Natl Acad. Sci. USA 110, 11964–11969 (2013)
40. Fujii, S., Katake, Y. & Tanaka, H. Increased expression of DNA methyltransferase-1 in non-neoplastic epithelium helps predict colorectal neoplasia risk in ulcerative colitis. Digestion 82, 179–186 (2010)
41. Lal, G. & Bromberg, J. S. Epigenetic mechanisms of regulation of Foxp3 expression. Blood 114, 3727–3735 (2009)
42. Fransolet, G. et al. Azacytidine mitigates experimental sclerodermic chronic graft-versus-host disease. J. Hematol. Oncol. 9, 53 (2016)
43. Chan, M. W. et al. Low-dose 5-aza-2’-deoxycytidine pretreatment inhibits experimental autoimmune encephalomyelitis by induction of regulatory T cells. Mol. Med. 20, 248–256 (2014)
44. Zhang, G., Zhao, N., Hu, X. & Tian, J. Interaction of alpinetin with bovine serum albumin: Probing of the mechanism and binding site by spectroscopic methods. Spectrochim. Acta A. Mol. Biomol. Spectrosc. 76, 410–417 (2010)
45. Li, G., Liu, J., Xia, W. F., Zhou, C. L. & Lv, L. Q. Protective effects of ghrelin in ventilator-induced lung injury in rats. Int. Immunopharmacol. 52, 85–91 (2017)
46. Yuan, D. et al. The evaluation of antioxidant and anti-inflammatory effects of eucommia ulmoides flavones using diquat-challenged piglet models. Oxid. Med. Cell Longev. 2017, 8140962 (2017)
47. Rouse, M. et al. Indoles mitigate the development of experimental autoimmune encephalomyelitis by induction of reciprocal differentiation of regulatory T cells and Th17 cells. Br. J. Pharmacol. 169, 1305–1321 (2013)
48. Zhu., J. et al. The metastasis suppressor CD82/KAI1 regulates cell migration and invasion via inhibiting TGF-β 1/Smad signaling in renal cell carcinoma. Oncotarget 8, 51559–51568 (2017)
49. Yang, Y. et al. Chemoprevention of dietary digitoflavone on colitis-associated colon tumorigenesis through inducing Nrf2 signaling pathway and inhibition of inflammation. Mol. Cancer 13, 48 (2014)