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Published in: Inflammation 5/2020

01-10-2020 | Crohn's Disease | Original Article

MiR-124a Mediates the Impairment of Intestinal Epithelial Integrity by Targeting Aryl Hydrocarbon Receptor in Crohn’s Disease

Authors: Xiaojing Zhao, Jiajia Li, Jingjing Ma, Chunhua Jiao, Xinyun Qiu, Xiufang Cui, Di Wang, Hongjie Zhang

Published in: Inflammation | Issue 5/2020

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Abstract

Growing evidence suggested that microRNAs (miRNAs) contributed to the progression of Crohn’s disease (CD), but the exact physiological functions of many miRNAs in CD patients still remain illusive. In this study, we explore the potent pathogenicity of miRNAs in CD. Expressions of miRNAs and aryl hydrocarbon receptor (AHR) protein were determined in the colitic colon of 2,4,6-trinitrobenzenesulfonic acid (TNBS)-induced colitis mice and CD patients. Colitis was induced in wild-type (WT), miR-124a overexpression (miR-124a-Nju), and AHR knockout (AHR−/−) mice. Intestinal barrier function was evaluated in colitis mice and Caco2 monolayers. There was a negative relationship between miR-124a and AHR protein in inflamed colons from CD patients. MiR-124a-Nju and AHR−/− mice treated with TNBS had more severe intestinal inflammation than WT mice. Both miR-124a-Nju mice and AHR−/− mice underwent evident intestinal barrier destruction, and anti-miR-124a administration could reverse this dysfunction in miR-124a-Nju mice but not in AHR−/− mice. In vitro studies revealed that miR-124a mimics downregulated the expression of AHR and tight junction proteins and induced hyperpermeability by increasing miR-124a expression, which was abrogated by miR-124a inhibitor and AHR antagonist FICZ. This study suggests that miR-124a can induce intestinal inflammation and cause intestinal barrier dysfunction by supressing AHR.
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Literature
1.
go back to reference Baumgart, D.C., and S.R. Carding. 2007. Inflammatory bowel disease: cause and immunobiology. Lancet 369 (9573): 1627–1640.CrossRef Baumgart, D.C., and S.R. Carding. 2007. Inflammatory bowel disease: cause and immunobiology. Lancet 369 (9573): 1627–1640.CrossRef
2.
go back to reference Loftus, E.V., Jr. 2004. Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences. Gastroenterology 126 (6): 1504–1517.CrossRef Loftus, E.V., Jr. 2004. Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences. Gastroenterology 126 (6): 1504–1517.CrossRef
3.
go back to reference Hollander, D. 2013. Intestinal permeability barrier in Crohn's disease: the difficulty in shifting the paradigm. Digestive Diseases and Sciences 58 (7): 1827–1829.CrossRef Hollander, D. 2013. Intestinal permeability barrier in Crohn's disease: the difficulty in shifting the paradigm. Digestive Diseases and Sciences 58 (7): 1827–1829.CrossRef
4.
go back to reference Libertucci, J., U. Dutta, S. Kaur, J. Jury, L. Rossi, M.E. Fontes, M.S. Shajib, W.I. Khan, M.G. Surette, E.F. Verdu, and D. Armstrong. 2018. Inflammation-related differences in mucosa-associated microbiota and intestinal barrier function in colonic Crohn's disease. American Journal of Physiology. Gastrointestinal and Liver Physiology 315: G420–G431.CrossRef Libertucci, J., U. Dutta, S. Kaur, J. Jury, L. Rossi, M.E. Fontes, M.S. Shajib, W.I. Khan, M.G. Surette, E.F. Verdu, and D. Armstrong. 2018. Inflammation-related differences in mucosa-associated microbiota and intestinal barrier function in colonic Crohn's disease. American Journal of Physiology. Gastrointestinal and Liver Physiology 315: G420–G431.CrossRef
5.
go back to reference Franchimont, D., S. Vermeire, H. El Housni, M. Pierik, K. Van Steen, T. Gustot, E. Quertinmont, M. Abramowicz, A. Van Gossum, J. Deviere, and P. Rutgeerts. 2004. Deficient host-bacteria interactions in inflammatory bowel disease? The toll-like receptor (TLR)-4 Asp299gly polymorphism is associated with Crohn's disease and ulcerative colitis. Gut 53 (7): 987–992.CrossRef Franchimont, D., S. Vermeire, H. El Housni, M. Pierik, K. Van Steen, T. Gustot, E. Quertinmont, M. Abramowicz, A. Van Gossum, J. Deviere, and P. Rutgeerts. 2004. Deficient host-bacteria interactions in inflammatory bowel disease? The toll-like receptor (TLR)-4 Asp299gly polymorphism is associated with Crohn's disease and ulcerative colitis. Gut 53 (7): 987–992.CrossRef
6.
go back to reference Orholm, M., V. Binder, T.I. Sorensen, L.P. Rasmussen, and K.O. Kyvik. 2000. Concordance of inflammatory bowel disease among Danish twins. Results of a nationwide study. Scandinavian Journal of Gastroenterology 35 (10): 1075–1081.CrossRef Orholm, M., V. Binder, T.I. Sorensen, L.P. Rasmussen, and K.O. Kyvik. 2000. Concordance of inflammatory bowel disease among Danish twins. Results of a nationwide study. Scandinavian Journal of Gastroenterology 35 (10): 1075–1081.CrossRef
7.
go back to reference Zheng, J.J., X.S. Zhu, Z. Huangfu, Z.X. Gao, Z.R. Guo, and Z. Wang. 2005. Crohn's disease in mainland China: a systematic analysis of 50 years of research. Chinese Journal of Digestive Diseases 6 (4): 175–181.CrossRef Zheng, J.J., X.S. Zhu, Z. Huangfu, Z.X. Gao, Z.R. Guo, and Z. Wang. 2005. Crohn's disease in mainland China: a systematic analysis of 50 years of research. Chinese Journal of Digestive Diseases 6 (4): 175–181.CrossRef
8.
go back to reference Chen, G., X. Ran, B. Li, Y. Li, D. He, B. Huang, S. Fu, J. Liu, and W. Wang. 2018. Sodium butyrate inhibits inflammation and maintains epithelium barrier integrity in a TNBS-induced inflammatory bowel disease mice model. EBioMedicine 30: 317–325.CrossRef Chen, G., X. Ran, B. Li, Y. Li, D. He, B. Huang, S. Fu, J. Liu, and W. Wang. 2018. Sodium butyrate inhibits inflammation and maintains epithelium barrier integrity in a TNBS-induced inflammatory bowel disease mice model. EBioMedicine 30: 317–325.CrossRef
9.
go back to reference Chang, J., R.W. Leong, V.C. Wasinger, M. Ip, M. Yang, and T.G. Phan. 2017. Impaired intestinal permeability contributes to ongoing bowel symptoms in patients with inflammatory bowel disease and mucosal healing. Gastroenterology 153 (3): 723–731 e1.CrossRef Chang, J., R.W. Leong, V.C. Wasinger, M. Ip, M. Yang, and T.G. Phan. 2017. Impaired intestinal permeability contributes to ongoing bowel symptoms in patients with inflammatory bowel disease and mucosal healing. Gastroenterology 153 (3): 723–731 e1.CrossRef
10.
go back to reference Lamas, B., J.M. Natividad, and H. Sokol. 2018. Aryl hydrocarbon receptor and intestinal immunity. Mucosal Immunology 11: 1024–1038.CrossRef Lamas, B., J.M. Natividad, and H. Sokol. 2018. Aryl hydrocarbon receptor and intestinal immunity. Mucosal Immunology 11: 1024–1038.CrossRef
11.
go back to reference Kewley, R.J., M.L. Whitelaw, and A. Chapman-Smith. 2004. The mammalian basic helix-loop-helix/PAS family of transcriptional regulators. The International Journal of Biochemistry & Cell Biology 36 (2): 189–204.CrossRef Kewley, R.J., M.L. Whitelaw, and A. Chapman-Smith. 2004. The mammalian basic helix-loop-helix/PAS family of transcriptional regulators. The International Journal of Biochemistry & Cell Biology 36 (2): 189–204.CrossRef
12.
go back to reference Veldhoen, M., K. Hirota, A.M. Westendorf, J. Buer, L. Dumoutier, J.C. Renauld, and B. Stockinger. 2008. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 453 (7191): 106–109.CrossRef Veldhoen, M., K. Hirota, A.M. Westendorf, J. Buer, L. Dumoutier, J.C. Renauld, and B. Stockinger. 2008. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 453 (7191): 106–109.CrossRef
13.
go back to reference Arsenescu, R., V. Arsenescu, J. Zhong, M. Nasser, R. Melinte, R.W. Dingle, H. Swanson, and W.J. de Villiers. 2011. Role of the xenobiotic receptor in inflammatory bowel disease. Inflammatory Bowel Diseases 17 (5): 1149–1162.CrossRef Arsenescu, R., V. Arsenescu, J. Zhong, M. Nasser, R. Melinte, R.W. Dingle, H. Swanson, and W.J. de Villiers. 2011. Role of the xenobiotic receptor in inflammatory bowel disease. Inflammatory Bowel Diseases 17 (5): 1149–1162.CrossRef
14.
go back to reference Monteleone, I., A. Rizzo, M. Sarra, G. Sica, P. Sileri, L. Biancone, T.T. MacDonald, F. Pallone, and G. Monteleone. 2011. Aryl hydrocarbon receptor-induced signals up-regulate IL-22 production and inhibit inflammation in the gastrointestinal tract. Gastroenterology 141 (1): 237–248 48 e1.CrossRef Monteleone, I., A. Rizzo, M. Sarra, G. Sica, P. Sileri, L. Biancone, T.T. MacDonald, F. Pallone, and G. Monteleone. 2011. Aryl hydrocarbon receptor-induced signals up-regulate IL-22 production and inhibit inflammation in the gastrointestinal tract. Gastroenterology 141 (1): 237–248 48 e1.CrossRef
15.
go back to reference Li, Y., S. Innocentin, D.R. Withers, N.A. Roberts, A.R. Gallagher, E.F. Grigorieva, C. Wilhelm, and M. Veldhoen. 2011. Exogenous stimuli maintain intraepithelial lymphocytes via aryl hydrocarbon receptor activation. Cell 147 (3): 629–640.CrossRef Li, Y., S. Innocentin, D.R. Withers, N.A. Roberts, A.R. Gallagher, E.F. Grigorieva, C. Wilhelm, and M. Veldhoen. 2011. Exogenous stimuli maintain intraepithelial lymphocytes via aryl hydrocarbon receptor activation. Cell 147 (3): 629–640.CrossRef
16.
go back to reference Qiu, J., X. Guo, Z.M. Chen, L. He, G.F. Sonnenberg, D. Artis, Y.X. Fu, and L. Zhou. 2013. Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora. Immunity 39 (2): 386–399.CrossRef Qiu, J., X. Guo, Z.M. Chen, L. He, G.F. Sonnenberg, D. Artis, Y.X. Fu, and L. Zhou. 2013. Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora. Immunity 39 (2): 386–399.CrossRef
17.
go back to reference Yu, M., Q. Wang, Y. Ma, L. Li, K. Yu, Z. Zhang, G. Chen, X. Li, W. Xiao, P. Xu, and H. Yang. 2018. Aryl hydrocarbon receptor activation modulates intestinal epithelial barrier function by maintaining tight junction integrity. International Journal of Biological Sciences 14 (1): 69–77.CrossRef Yu, M., Q. Wang, Y. Ma, L. Li, K. Yu, Z. Zhang, G. Chen, X. Li, W. Xiao, P. Xu, and H. Yang. 2018. Aryl hydrocarbon receptor activation modulates intestinal epithelial barrier function by maintaining tight junction integrity. International Journal of Biological Sciences 14 (1): 69–77.CrossRef
18.
go back to reference Makeyev, E.V., and T. Maniatis. 2008. Multilevel regulation of gene expression by microRNAs. Science 319 (5871): 1789–1790.CrossRef Makeyev, E.V., and T. Maniatis. 2008. Multilevel regulation of gene expression by microRNAs. Science 319 (5871): 1789–1790.CrossRef
19.
go back to reference Momen-Heravi, F., and S. Bala. 2018. miRNA regulation of innate immunity. Journal of Leukocyte Biology 103: 1205–1217.CrossRef Momen-Heravi, F., and S. Bala. 2018. miRNA regulation of innate immunity. Journal of Leukocyte Biology 103: 1205–1217.CrossRef
20.
go back to reference Ceribelli, A., M. Satoh, and E.K. Chan. 2012. MicroRNAs and autoimmunity. Current Opinion in Immunology 24 (6): 686–691.CrossRef Ceribelli, A., M. Satoh, and E.K. Chan. 2012. MicroRNAs and autoimmunity. Current Opinion in Immunology 24 (6): 686–691.CrossRef
21.
go back to reference Zhao, Y., T. Ma, W. Chen, Y. Chen, M. Li, L. Ren, J. Chen, R. Cao, Y. Feng, H. Zhang, and R. Shi. 2016. MicroRNA-124 promotes intestinal inflammation by targeting aryl hydrocarbon receptor in Crohn's disease. Journal of Crohn's & Colitis 10 (6): 703–712.CrossRef Zhao, Y., T. Ma, W. Chen, Y. Chen, M. Li, L. Ren, J. Chen, R. Cao, Y. Feng, H. Zhang, and R. Shi. 2016. MicroRNA-124 promotes intestinal inflammation by targeting aryl hydrocarbon receptor in Crohn's disease. Journal of Crohn's & Colitis 10 (6): 703–712.CrossRef
22.
go back to reference Neurath, M.F., I. Fuss, B.L. Kelsall, E. Stuber, and W. Strober. 1995. Antibodies to interleukin 12 abrogate established experimental colitis in mice. The Journal of Experimental Medicine 182 (5): 1281–1290.CrossRef Neurath, M.F., I. Fuss, B.L. Kelsall, E. Stuber, and W. Strober. 1995. Antibodies to interleukin 12 abrogate established experimental colitis in mice. The Journal of Experimental Medicine 182 (5): 1281–1290.CrossRef
23.
go back to reference Huang, Z., T. Shi, Q. Zhou, S. Shi, R. Zhao, H. Shi, L. Dong, C. Zhang, K. Zeng, J. Chen, and J. Zhang. 2014. miR-141 regulates colonic leukocytic trafficking by targeting CXCL12beta during murine colitis and human Crohn's disease. Gut 63 (8): 1247–1257.CrossRef Huang, Z., T. Shi, Q. Zhou, S. Shi, R. Zhao, H. Shi, L. Dong, C. Zhang, K. Zeng, J. Chen, and J. Zhang. 2014. miR-141 regulates colonic leukocytic trafficking by targeting CXCL12beta during murine colitis and human Crohn's disease. Gut 63 (8): 1247–1257.CrossRef
24.
go back to reference Thorlacius-Ussing, G., B. Schnack Nielsen, V. Andersen, K. Holmstrom, and A.E. Pedersen. 2017. Expression and localization of miR-21 and miR-126 in mucosal tissue from patients with inflammatory bowel disease. Inflammatory Bowel Diseases 23 (5): 739–752.CrossRef Thorlacius-Ussing, G., B. Schnack Nielsen, V. Andersen, K. Holmstrom, and A.E. Pedersen. 2017. Expression and localization of miR-21 and miR-126 in mucosal tissue from patients with inflammatory bowel disease. Inflammatory Bowel Diseases 23 (5): 739–752.CrossRef
25.
go back to reference Kihara, N., S.G. de la Fuente, K. Fujino, T. Takahashi, T.N. Pappas, and C.R. Mantyh. 2003. Vanilloid receptor-1 containing primary sensory neurones mediate dextran sulphate sodium induced colitis in rats. Gut 52 (5): 713–719.CrossRef Kihara, N., S.G. de la Fuente, K. Fujino, T. Takahashi, T.N. Pappas, and C.R. Mantyh. 2003. Vanilloid receptor-1 containing primary sensory neurones mediate dextran sulphate sodium induced colitis in rats. Gut 52 (5): 713–719.CrossRef
26.
go back to reference Dawson, P.A., S. Huxley, B. Gardiner, T. Tran, J.L. McAuley, S. Grimmond, M.A. McGuckin, and D. Markovich. 2009. Reduced mucin sulfonation and impaired intestinal barrier function in the hyposulfataemic NaS1 null mouse. Gut 58 (7): 910–919.CrossRef Dawson, P.A., S. Huxley, B. Gardiner, T. Tran, J.L. McAuley, S. Grimmond, M.A. McGuckin, and D. Markovich. 2009. Reduced mucin sulfonation and impaired intestinal barrier function in the hyposulfataemic NaS1 null mouse. Gut 58 (7): 910–919.CrossRef
27.
go back to reference Ma, T.Y., N.T. Hoa, D.D. Tran, V. Bui, A. Pedram, S. Mills, and M. Merryfield. 2000. Cytochalasin B modulation of Caco-2 tight junction barrier: role of myosin light chain kinase. American Journal of Physiology. Gastrointestinal and Liver Physiology 279 (5): G875–G885.CrossRef Ma, T.Y., N.T. Hoa, D.D. Tran, V. Bui, A. Pedram, S. Mills, and M. Merryfield. 2000. Cytochalasin B modulation of Caco-2 tight junction barrier: role of myosin light chain kinase. American Journal of Physiology. Gastrointestinal and Liver Physiology 279 (5): G875–G885.CrossRef
28.
go back to reference Cario, E., G. Gerken, and D.K. Podolsky. 2004. Toll-like receptor 2 enhances ZO-1-associated intestinal epithelial barrier integrity via protein kinase C. Gastroenterology 127 (1): 224–238.CrossRef Cario, E., G. Gerken, and D.K. Podolsky. 2004. Toll-like receptor 2 enhances ZO-1-associated intestinal epithelial barrier integrity via protein kinase C. Gastroenterology 127 (1): 224–238.CrossRef
29.
go back to reference Tian, Y., J. Xu, Y. Li, R. Zhao, S. Du, C. Lv, W. Wu, R. Liu, X. Sheng, Y. Song, X. Bi, G. Li, M. Li, X. Wu, P. Lou, H. You, W. Cui, J. Sun, J. Shuai, F. Ren, B. Zhang, M. Guo, X. Hou, K. Wu, L. Xue, H. Zhang, M.V. Plikus, Y. Cong, C.J. Lengner, Z. Liu, and Z. Yu. 2019. MicroRNA-31 reduces inflammatory signaling and promotes regeneration in colon epithelium, and delivery of mimics in microspheres reduces colitis in mice. Gastroenterology 156 (8): 2281–2296 e6.CrossRef Tian, Y., J. Xu, Y. Li, R. Zhao, S. Du, C. Lv, W. Wu, R. Liu, X. Sheng, Y. Song, X. Bi, G. Li, M. Li, X. Wu, P. Lou, H. You, W. Cui, J. Sun, J. Shuai, F. Ren, B. Zhang, M. Guo, X. Hou, K. Wu, L. Xue, H. Zhang, M.V. Plikus, Y. Cong, C.J. Lengner, Z. Liu, and Z. Yu. 2019. MicroRNA-31 reduces inflammatory signaling and promotes regeneration in colon epithelium, and delivery of mimics in microspheres reduces colitis in mice. Gastroenterology 156 (8): 2281–2296 e6.CrossRef
30.
go back to reference He, C., T. Yu, Y. Shi, C. Ma, W. Yang, L. Fang, M. Sun, W. Wu, F. Xiao, F. Guo, M. Chen, H. Yang, J. Qian, Y. Cong, and Z. Liu. 2017. MicroRNA 301A promotes intestinal inflammation and colitis-associated cancer development by inhibiting BTG1. Gastroenterology 152 (6): 1434–1448 e15.CrossRef He, C., T. Yu, Y. Shi, C. Ma, W. Yang, L. Fang, M. Sun, W. Wu, F. Xiao, F. Guo, M. Chen, H. Yang, J. Qian, Y. Cong, and Z. Liu. 2017. MicroRNA 301A promotes intestinal inflammation and colitis-associated cancer development by inhibiting BTG1. Gastroenterology 152 (6): 1434–1448 e15.CrossRef
31.
go back to reference Makeyev, E.V., J. Zhang, M.A. Carrasco, and T. Maniatis. 2007. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Molecular Cell 27 (3): 435–448.CrossRef Makeyev, E.V., J. Zhang, M.A. Carrasco, and T. Maniatis. 2007. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Molecular Cell 27 (3): 435–448.CrossRef
32.
go back to reference Visvanathan, J., S. Lee, B. Lee, J.W. Lee, and S.K. Lee. 2007. The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes & Development 21 (7): 744–749.CrossRef Visvanathan, J., S. Lee, B. Lee, J.W. Lee, and S.K. Lee. 2007. The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes & Development 21 (7): 744–749.CrossRef
33.
go back to reference Ponomarev, E.D., T. Veremeyko, N. Barteneva, A.M. Krichevsky, and H.L. Weiner. 2011. MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-alpha-PU.1 pathway. Nature Medicine 17 (1): 64–70.CrossRef Ponomarev, E.D., T. Veremeyko, N. Barteneva, A.M. Krichevsky, and H.L. Weiner. 2011. MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-alpha-PU.1 pathway. Nature Medicine 17 (1): 64–70.CrossRef
34.
go back to reference Nakamachi, Y., S. Kawano, M. Takenokuchi, K. Nishimura, Y. Sakai, T. Chin, R. Saura, M. Kurosaka, and S. Kumagai. 2009. MicroRNA-124a is a key regulator of proliferation and monocyte chemoattractant protein 1 secretion in fibroblast-like synoviocytes from patients with rheumatoid arthritis. Arthritis and Rheumatism 60 (5): 1294–1304.CrossRef Nakamachi, Y., S. Kawano, M. Takenokuchi, K. Nishimura, Y. Sakai, T. Chin, R. Saura, M. Kurosaka, and S. Kumagai. 2009. MicroRNA-124a is a key regulator of proliferation and monocyte chemoattractant protein 1 secretion in fibroblast-like synoviocytes from patients with rheumatoid arthritis. Arthritis and Rheumatism 60 (5): 1294–1304.CrossRef
35.
go back to reference Koukos, G., C. Polytarchou, J.L. Kaplan, A. Morley-Fletcher, B. Gras-Miralles, E. Kokkotou, M. Baril-Dore, C. Pothoulakis, H.S. Winter, and D. Iliopoulos. 2013. MicroRNA-124 regulates STAT3 expression and is down-regulated in colon tissues of pediatric patients with ulcerative colitis. Gastroenterology 145 (4): 842–852 e2.CrossRef Koukos, G., C. Polytarchou, J.L. Kaplan, A. Morley-Fletcher, B. Gras-Miralles, E. Kokkotou, M. Baril-Dore, C. Pothoulakis, H.S. Winter, and D. Iliopoulos. 2013. MicroRNA-124 regulates STAT3 expression and is down-regulated in colon tissues of pediatric patients with ulcerative colitis. Gastroenterology 145 (4): 842–852 e2.CrossRef
36.
go back to reference Schmidt, J.V., and C.A. Bradfield. 1996. Ah receptor signaling pathways. Annual Review of Cell and Developmental Biology 12: 55–89.CrossRef Schmidt, J.V., and C.A. Bradfield. 1996. Ah receptor signaling pathways. Annual Review of Cell and Developmental Biology 12: 55–89.CrossRef
37.
go back to reference Denison, M.S., and S.R. Nagy. 2003. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annual Review of Pharmacology and Toxicology 43: 309–334.CrossRef Denison, M.S., and S.R. Nagy. 2003. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annual Review of Pharmacology and Toxicology 43: 309–334.CrossRef
38.
go back to reference Han, B., B. Sheng, Z. Zhang, A. Pu, J. Yin, Q. Wang, K. Yang, L. Sun, M. Yu, Y. Qiu, W. Xiao, and H. Yang. 2016. Aryl hydrocarbon receptor activation in intestinal obstruction ameliorates intestinal barrier dysfunction via suppression of MLCK-MLC phosphorylation pathway. Shock 46 (3): 319–328.CrossRef Han, B., B. Sheng, Z. Zhang, A. Pu, J. Yin, Q. Wang, K. Yang, L. Sun, M. Yu, Y. Qiu, W. Xiao, and H. Yang. 2016. Aryl hydrocarbon receptor activation in intestinal obstruction ameliorates intestinal barrier dysfunction via suppression of MLCK-MLC phosphorylation pathway. Shock 46 (3): 319–328.CrossRef
39.
go back to reference Liu, Z., L. Li, W. Chen, Q. Wang, W. Xiao, Y. Ma, B. Sheng, X. Li, L. Sun, M. Yu, and H. Yang. 2018. Aryl hydrocarbon receptor activation maintained the intestinal epithelial barrier function through Notch1 dependent signaling pathway. International Journal of Molecular Medicine 41 (3): 1560–1572.PubMed Liu, Z., L. Li, W. Chen, Q. Wang, W. Xiao, Y. Ma, B. Sheng, X. Li, L. Sun, M. Yu, and H. Yang. 2018. Aryl hydrocarbon receptor activation maintained the intestinal epithelial barrier function through Notch1 dependent signaling pathway. International Journal of Molecular Medicine 41 (3): 1560–1572.PubMed
Metadata
Title
MiR-124a Mediates the Impairment of Intestinal Epithelial Integrity by Targeting Aryl Hydrocarbon Receptor in Crohn’s Disease
Authors
Xiaojing Zhao
Jiajia Li
Jingjing Ma
Chunhua Jiao
Xinyun Qiu
Xiufang Cui
Di Wang
Hongjie Zhang
Publication date
01-10-2020
Publisher
Springer US
Keyword
Crohn's Disease
Published in
Inflammation / Issue 5/2020
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-020-01259-0

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