A dietary flavone confers communicable protection against colitis through NLRP6 signaling independently of inflammasome activation

Mucosal Immunology - Tập 11 - Trang 811-819 - 2018
K Radulovic1,2, S Normand1, A Rehman3, A Delanoye-Crespin1, J Chatagnon1, M Delacre1, N Waldschmitt1, L F Poulin1, J Iovanna4, B Ryffel5,6, P Rosenstiel3, M Chamaillard1
1Univ. Lille, CNRS, Inserm, CHRU Lille, Institut Pasteur de Lille, U1019–UMR 8204–CIIL–Centre d'Infection et d'Immunité de Lille, Lille, France
2Department of Biomedicine, University Hospital Basel and University of Basel, Basel, Switzerland
3Institute of Clinical Molecular Biology, Christian-Albrechts-University and University Hospital Schleswig-Holstein, Campus Kiel, Kiel, Germany
4Centre de Recherche en Cancérologie de Marseille, INSERM U1068, CNRS UMR 7258, Aix-Marseille Université and Institut Paoli-Calmettes, Parc Scientifique Et Technologique de Luminy, Marseille, France
5CNRS, UMR7355; Experimental and Molecular Immunology and Neurogenetics, University of Orleans, France and IDM University of Cape Town
6Experimental and Molecular Immunology and Neurogenetics, University of Orleans, France and IDM University of Cape Town, Orleans, France

Tài liệu tham khảo

Ley, 2008, Evolution of mammals and their gut microbes, Science, 320, 1647, 10.1126/science.1155725 Scanlan, 2006, Culture-independent analyses of temporal variation of the dominant fecal microbiota and targeted bacterial subgroups in Crohn's disease, J. Clin. Microbiol., 44, 3980, 10.1128/JCM.00312-06 Manichanh, 2006, Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach, Gut, 55, 205, 10.1136/gut.2005.073817 Lamas, 2016, CARD9 impacts colitis by altering gut microbiota metabolism of tryptophan into aryl hydrocarbon receptor ligands, Nat. Med., 22, 598, 10.1038/nm.4102 Gonzalez, 2011, Effects of flavonoids and other polyphenols on inflammation, Crit. Rev. Food Sci. Nutr., 51, 331, 10.1080/10408390903584094 Lopez-Posadas, 2010, Flavonoids exert distinct modulatory actions on cyclooxygenase 2 and NF-kappaB in an intestinal epithelial cell line (IEC18), Br. J. Pharmacol., 160, 1714, 10.1111/j.1476-5381.2010.00827.x Seo, 2015, Apigenin induces caspase-dependent apoptosis by inhibiting signal transducer and activator of transcription 3 signaling in HER2-overexpressing SKBR3 breast cancer cells, Mol. Med. Rep., 12, 2977, 10.3892/mmr.2015.3698 Xu, 2016, Apigenin attenuates oxidative injury in ARPE-19 cells thorough activation of Nrf2 pathway, Oxid. Med. Cell Longev., 2016, 4378461, 10.1155/2016/4378461 Hoensch, 2010, [Colorectal cancer prevention by flavonoids], Med. Klin., 105, 554, 10.1007/s00063-010-1094-7 Banerjee, 2015, Oxidative stress triggered by naturally occurring flavone apigenin results in senescence and chemotherapeutic effect in human colorectal cancer cells, Redox Biol., 5, 153, 10.1016/j.redox.2015.04.009 Mascaraque, 2015, Intestinal anti-inflammatory activity of apigenin K in two rat colitis models induced by trinitrobenzenesulfonic acid and dextran sulphate sodium, Br. J. Nutr., 113, 618, 10.1017/S0007114514004292 Marquez-Flores, 2016, Apigenin supplementation protects the development of dextran sulfate sodium-induced murine experimental colitis by inhibiting canonical and non-canonical inflammasome signaling pathways, J. Nutr. Biochem., 30, 143, 10.1016/j.jnutbio.2015.12.002 Ganjare, 2011, Use of apigenin from Cordia dichotoma in the treatment of colitis, Fitoterapia, 82, 1052, 10.1016/j.fitote.2011.06.008 Vezza, 2016, Flavonoids in inflammatory bowel disease: a review, Nutrients, 8, 211, 10.3390/nu8040211 Shin, 2009, Chrysin, a natural flavone, improves murine inflammatory bowel diseases, Biochem. Biophys. Res. Commun., 381, 502, 10.1016/j.bbrc.2009.02.071 Elinav, 2011, NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis, Cell, 145, 745, 10.1016/j.cell.2011.04.022 Normand, 2011, Nod-like receptor pyrin domain-containing protein 6 (NLRP6) controls epithelial self-renewal and colorectal carcinogenesis upon injury, Proc. Natl. Acad. Sci. USA, 108, 9601, 10.1073/pnas.1100981108 Chen, 2011, A functional role for Nlrp6 in intestinal inflammation and tumorigenesis, J. Immunol., 186, 7187, 10.4049/jimmunol.1100412 Zhang, 2014, Flavonoid apigenin inhibits lipopolysaccharide-induced inflammatory response through multiple mechanisms in macrophages, PLoS ONE, 9, e107072, 10.1371/journal.pone.0107072 Feng, 2016, Activation of PPARgamma by a natural flavonoid modulator, apigenin ameliorates obesity-related inflammation via regulation of macrophage polarization, EBioMedicine, 9, 61, 10.1016/j.ebiom.2016.06.017 Sun, 2013, Stress-induced corticotropin-releasing hormone-mediated NLRP6 inflammasome inhibition and transmissible enteritis in mice, Gastroenterology, 144, 1478, 10.1053/j.gastro.2013.02.038 Kempster, 2011, Developmental control of the Nlrp6 inflammasome and a substrate, IL-18, in mammalian intestine, Am. J. Physiol. Gastrointest. Liver Physiol., 300, G253, 10.1152/ajpgi.00397.2010 Ortiz-Masia, 2016, M1 macrophages activate notch signalling in epithelial cells: relevance in Crohn's disease, J. Crohns Colitis, 10, 582, 10.1093/ecco-jcc/jjw009 Fre, 2005, Notch signals control the fate of immature progenitor cells in the intestine, Nature, 435, 964, 10.1038/nature03589 Chang, 2014, The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition, Proc. Natl. Acad. Sci. USA, 111, 2247, 10.1073/pnas.1322269111 Kaiko, 2016, The colonic crypt protects stem cells from microbiota-derived metabolites, Cell, 165, 1708, 10.1016/j.cell.2016.05.018 Vital, 2014, Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data, mBio, 5, e00889, 10.1128/mBio.00889-14 Gironella, 2005, Anti-inflammatory effects of pancreatitis associated protein in inflammatory bowel disease, Gut, 54, 1244, 10.1136/gut.2004.056309 Simons, 2005, Human gut microbial degradation of flavonoids: structure-function relationships, J. Agric. Food Chem., 53, 4258, 10.1021/jf0500177 Seregin, 2017, NLRP6 protects Il10−/− mice from colitis by limiting colonization of Akkermansia muciniphila, Cell Rep., 19, 733, 10.1016/j.celrep.2017.03.080 Levy, 2015, Microbiota-modulated metabolites shape the intestinal microenvironment by regulating NLRP6 inflammasome signaling, Cell, 163, 1428, 10.1016/j.cell.2015.10.048 Wlodarska, 2014, NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion, Cell, 156, 1045, 10.1016/j.cell.2014.01.026 Adolph, 2013, Paneth cells as a site of origin for intestinal inflammation, Nature, 503, 272, 10.1038/nature12599 Ren, 2016, Apigenin and naringenin regulate glucose and lipid metabolism, and ameliorate vascular dysfunction in type 2 diabetic rats, Eur. J. Pharmacol., 773, 13, 10.1016/j.ejphar.2016.01.002 Jung, 2016, Apigenin ameliorates dyslipidemia, hepatic steatosis and insulin resistance by modulating metabolic and transcriptional profiles in the liver of high-fat diet-induced obese mice, Nutrients, 8, pii: E305, 10.3390/nu8050305 Thaiss, 2016, Persistent microbiome alterations modulate the rate of post-dieting weight regain, Nature, 540, 544, 10.1038/nature20796 Wang, 2016, Intestinal REG3 lectins protect against alcoholic steatohepatitis by reducing mucosa-associated microbiota and preventing bacterial translocation, Cell Host Microbe, 19, 227, 10.1016/j.chom.2016.01.003 Wirtz, 2007, Chemically induced mouse models of intestinal inflammation, Nat. Protoc., 2, 541, 10.1038/nprot.2007.41 Fadrosh, 2014, An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform, Microbiome, 2, 6, 10.1186/2049-2618-2-6 DeSantis, 2006, Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB, Appl. Environ. Microbiol., 72, 5069, 10.1128/AEM.03006-05 Segata, 2011, Metagenomic biomarker discovery and explanation, Genome Biol., 12, R60, 10.1186/gb-2011-12-6-r60