Dietary AhR Ligands Regulate AhRR Expression in Intestinal Immune Cells and Intestinal Microbiota Composition
Open accessAbstract
A diet rich in vegetables and fruit is generally considered healthy because of a high content of phytochemicals, vitamins, and fiber. The phytochemical indole-3-carbinol (I3C), a derivative of glucobrassicin, is sold as a dietary supplement promising diverse health benefits. I3C metabolites act as ligands of the aryl hydrocarbon receptor (AhR), an important sensor for environmental polyaromatic chemicals. Here, we investigated how dietary AhR ligand supplementation influences AhR target gene expression and intestinal microbiota composition. For this, we used AhR repressor (AhRR)-reporter mice as a tool to study AhR activation in the intestine following dietary I3C-supplementation in comparison with AhR ligand-deprived diets, including a high fat diet. AhRR expression in intestinal immune cells was mainly driven by dietary AhR ligands and was independent of microbial metabolites. A lack of dietary AhR ligands caused enhanced susceptibility to dextran sodium sulfate (DSS)-induced colitis and correlated with the expansion of Enterobacteriaceae, whereas Clostridiales, Muribaculaceae, and Rikenellaceae were strongly reduced. I3C supplementation largely reverted this effect. Comparison of I3C-induced changes in microbiota composition using wild-type (WT), AhRR-deficient, and AhR-deficient mice revealed both AhR-dependent and -independent alterations in the microbiome. Overall, our study demonstrates that dietary AhR ligand supplementation has a profound influence on Ahrr expression in intestinal immune cells as well as microbiota composition.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Environmental differences such as diet, ligand amount in diet, bedding, caging, or facility pathogens can influence observed phenotypes in Ahr null mice.
“Differences in the environment such as diet, amount of ligand in the diet, bedding, caging, or the presence of pathogens in the facility can influence observed phenotypes.”
From Rodent Genetic Models of Ah Receptor Signaling (2021) · cites this paper as Schanz et al., 2020
The Results (§2.4; page unavailable) show that diet and AhR-ligand supplementation change gut microbial composition, including some responses specific to AhR-null mice. The Discussion (§3; page unavailable) also warns that diet comparisons can confound observed AhR-signaling effects. The paper does not establish that bedding, caging, or facility pathogens influence those phenotypes; its discussion of a specific-pathogen-free facility concerns possible differences in commensal bacteria. (LLM, conf=0.88)
Experimental — accuracy not yet measuredDietary ligands can influence the microbiome and AHR signaling.
“These environmental considerations are particularly important as it is now known that ligands obtained through the diet can influence microbiome and AHR signaling, and it is also likely that differences in pathogens can affect immune output in laboratory mice (Brawner et al., 2019; Leavy, 2011; Schanz et al., 2020).”
From Rodent Genetic Models of Ah Receptor Signaling (2021) · cites this paper as Schanz et al., 2020
Differences in pathogens can affect immune output in laboratory mice.
“These environmental considerations are particularly important as it is now known that ligands obtained through the diet can influence microbiome and AHR signaling, and it is also likely that differences in pathogens can affect immune output in laboratory mice (Brawner et al., 2019; Leavy, 2011; Schanz et al., 2020).”
From Rodent Genetic Models of Ah Receptor Signaling (2021) · cites this paper as Schanz et al., 2020
The Discussion (page unavailable) considers whether commensal bacteria in the authors’ specific-pathogen-free facility affect AhR signaling, and the Results report immune differences associated with diet. Neither passage addresses whether differences in pathogens affect immune output in laboratory mice. Searches for pathogen differences and immune responses found no passage making that point. (LLM, conf=0.73)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Gut Microbiota Regulation of Tryptophan Metabolism in Health and Disease
Agus, A., Planchais, J., & Sokol, H. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2018.05.003 · Cited by 3,180 · cited 1× · see citing works
“Furthermore, tryptophan derivatives derived from the diet or bacterial metabolites have been shown to tune the intestinal immune system by signalling through the AhR [5,25].”
BackgroundZelante, T., Iannitti, R. G., Cunha, C., De Luca, A., Giovannini, G., Pieraccini, G., Zecchi, R., D’Angelo, C., Massi-Benedetti, C., Fallarino, F., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.08.003 · Cited by 2,614 · see citing works
Lee, J. S., Cella, M., McDonald, K. G., Garlanda, C., Kennedy, G. D., Nukaya, M., Mantovani, A., Kopan, R., Bradfield, C. A., Newberry, R. D., et al. (2012) · Nature Immunology · doi:10.1038/ni.2187 · Cited by 777 · see citing works
Depletion of dietary aryl hydrocarbon receptor ligands alters microbiota composition and function
Brawner, K. M., Yeramilli, V. A., Duck, L. W., Van Der Pol, W., Smythies, L. E., Morrow, C. D., Elson, C. O., & Martin, C. A. (2019) · Scientific Reports · doi:10.1038/s41598-019-51194-w · Cited by 64 · see citing works
Flagged first, then by citations
Research works printed but not linked: 50
- [1]Esser C. Rannug A. The aryl hydrocarbon receptor in barrier organ physiology, immunology, and toxicology Pharmacol. Rev. 2015 67 259 279 10.1124/pr.114.009001 25657351 · DOI · Paper page
- [2]Bernshausen T. Jux B. Esser C. Abel J. Fritsche E. Tissue distribution and function of the Aryl hydrocarbon receptor repressor (AhRR) in C57BL/6 and Aryl hydrocarbon receptor deficient mice Arch. Toxicol. 2006 80 206 211 10.1007/s00204-005-0025-5 16205913 · DOI
- [3]Qiu J. Guo X. Chen Z.-M.E. He L. Sonnenberg G.F. Artis D. Fu Y.-X. Zhou L. Group 3 Innate Lymphoid Cells Inhibit T-Cell-Mediated Intestinal Inflammation through Aryl Hydrocarbon Receptor Signaling and Regulation of Microflora Immunity 2013 39 386 399 10.1016/j.immuni.2013.08.002 23954130 PMC3884586 · DOI
- [4]Kiss E.A. Vonarbourg C. Kopfmann S. Hobeika E. Finke D. Esser C. Diefenbach A. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles Science 2011 334 1561 1565 10.1126/science.1214914 22033518 · DOI · Paper page
- [6]Li Y. Innocentin S. Withers D.R. Roberts N.A. Gallagher A.R. Grigorieva E.F. Wilhelm C. Veldhoen M. Exogenous Stimuli Maintain Intraepithelial Lymphocytes via Aryl Hydrocarbon Receptor Activation Cell 2011 147 629 640 10.1016/j.cell.2011.09.025 21999944 · DOI
- [8]Schiering C. Wincent E. Metidji A. Iseppon A. Li Y. Potocnik A.J. Omenetti S. Henderson C.J. Wolf C.R. Nebert D.W. Feedback control of AHR signalling regulates intestinal immunity Nature 2017 542 242 245 10.1038/nature21080 28146477 PMC5302159 · DOI
- [9]Singh N.P. Singh U.P. Rouse M. Zhang J. Chatterjee S. Nagarkatti P.S. Nagarkatti M. 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. 2016 196 1108 1122 10.4049/jimmunol.1501727 26712945 PMC4724476 · DOI
- [10]Chinen I. Nakahama T. Kimura A. Nguyen N.T. Takemori H. Kumagai A. Kayama H. Takeda K. Lee S. Hanieh H. The aryl hydrocarbon receptor/microRNA-212/132 axis in T cells regulates IL-10 production to maintain intestinal homeostasis Int. Immunol. 2015 27 405 415 10.1093/intimm/dxv015 25862525 · DOI
- [11]Lamas B. Natividad J.M. Sokol H. Aryl hydrocarbon receptor and intestinal immunity review-article Mucosal Immunol. 2018 11 1024 1038 10.1038/s41385-018-0019-2 29626198 · DOI
- [12]Monteleone I. Rizzo A. Sarra M. Sica G. Sileri P. Biancone L. MacDonald T.T. Pallone F. Monteleone G. Aryl Hydrocarbon Receptor-Induced Signals Up-regulate IL-22 Production and Inhibit Inflammation in the Gastrointestinal Tract Gastroenterology 2011 141 237 248.e1 10.1053/j.gastro.2011.04.007 21600206 · DOI · Paper page
- [13]Haarmann-Stemmann T. Bothe H. Kohli A. Sydlik U. Abel J. Fritsche E. Analysis of the transcriptional regulation and molecular function of the aryl hydrocarbon receptor repressor in human cell lines Drug Metab. Dispos. 2007 35 2262 2269 10.1124/dmd.107.016253 17890447 · DOI
- [14]Baba T. Mimura J. Gradin K. Kuroiwa A. Watanabe T. Matsuda Y. Inazawa J. Sogawa K. Fujii-Kuriyama Y. Structure and Expression of the Ah Receptor Repressor Gene J. Biol. Chem. 2001 276 33101 33110 10.1074/jbc.M011497200 11423533 · DOI
- [15]Cauchi S. Stücker I. Cénée S. Kremers P. Beaune P. Massaad-Massade L. Structure and Polymorphisms of Human Aryl Hydrocarbon Receptor Repressor (AhRR) Gene in a French Population: Relationship With CYP1A1 Inducibility and Lung Cancer Pharmacogenetics 2003 13 339 347 10.1097/00008571-200306000-00005 12777964 · DOI
- [16]Mimura J. Ema M. Sogawa K. Fujii-Kuriyama Y. Identification of a novel mechanism of regulation of Ah (dioxin) receptor function Genes Dev. 1999 13 20 25 10.1101/gad.13.1.20 9887096 PMC316371 · DOI
- [17]Vogel C.F.A. Ishihara Y. Campbell C.E. Kado S.Y. Nguyen-Chi A. Sweeney C. Pollet M. Stemmann T.H. Tuscano J.M. A protective role of aryl hydrocarbon receptor repressor in inflammation and tumor growth Cancers (Basel) 2019 11 589 10.3390/cancers11050589 PMC6563059 31035533 · DOI
- [18]Yamamoto J. Ihara K. Nakayama H. Hikino S. Satoh K. Kubo N. Iida T. Fujii Y. Hara T. Characteristic expression of aryl hydrocarbon receptor repressor gene in human tissues: Organ-specific distribution and variable induction patterns in mononuclear cells Life Sci. 2004 74 1039 1049 10.1016/j.lfs.2003.07.022 14672759 · DOI
- [19]Frericks M. Meissner M. Esser C. Microarray analysis of the AHR system: Tissue-specific flexibility in signal and target genes Toxicol. Appl. Pharmacol. 2007 220 320 332 10.1016/j.taap.2007.01.014 17350064 · DOI
- [20]Tigges J. Weighardt H. Wolff S. Götz C. Förster I. Kohne Z. Huebenthal U. Merk H.F. Abel J. Haarmann-Stemmann T. Aryl hydrocarbon receptor repressor (AhRR) function revisited: Repression of CYP1 activity in human skin fibroblasts is not related to AhRR expression J. Investig. Dermatol. 2013 133 87 96 10.1038/jid.2012.259 22951721 · DOI
- [21]Brandstätter O. Schanz O. Vorac J. König J. Mori T. Maruyama T. Korkowski M. Haarmann-Stemmann T. Von Smolinski D. Schultze J.L. Balancing intestinal and systemic inflammation through cell type-specific expression of the aryl hydrocarbon receptor repressor Sci. Rep. 2016 6 1 17 10.1038/srep26091 27184933 PMC4869119 · DOI
- [22]Busbee P.B. Menzel L. Alrafas H.R. Dopkins N. Becker W. Miranda K. Tang C. Chatterjee S. Singh U.P. Nagarkatti M. Indole-3-carbinol prevents colitis and associated microbial dysbiosis in an IL-22–dependent manner JCI Insight 2020 5 1 18 10.1172/jci.insight.127551 31941837 PMC7030851 · DOI
- [23]Hubbard T.D. Murray I.A. Nichols R.G. Cassel K. Podolsky M. Kuzu G. Tian Y. Smith P. Kennett M.J. Patterson A.D. Dietary broccoli impacts microbial community structure and attenuates chemically induced colitis in mice in an Ah receptor dependent manner J. Funct. Foods 2017 37 685 698 10.1016/j.jff.2017.08.038 29242716 PMC5726276 · DOI
- [24]Moura-Alves P. Faé K. Houthuys E. Dorhoi A. Kreuchwig A. Furkert J. Barison N. Diehl A. Munder A. Constant P. AhR sensing of bacterial pigments regulates antibacterial defence Nature 2014 512 387 392 10.1038/nature13684 25119038 · DOI
- [26]Takamura T. Harama D. Fukumoto S. Nakamura Y. Shimokawa N. Ishimaru K. Ikegami S. Makino S. Kitamura M. Nakao A. Lactobacillus bulgaricus OLL1181 activates the aryl hydrocarbon receptor pathway and inhibits colitis Immunol. Cell Biol. 2011 89 817 822 10.1038/icb.2010.165 21321579 PMC3257032 · DOI
- [27]Cervantes-Barragan L. Chai J.N. Tianero M.D. Di Luccia B. Ahern P.P. Merriman J. Cortez V.S. Caparon M.G. Donia M.S. Gilfillan S. Lactobacillus reuteri induces gut intraepithelial CD4+CD8αα+ T cells Science 2017 357 806 810 10.1126/science.aah5825 28775213 PMC5687812 · DOI · Paper page
- [28]Stallhofer J. Friedrich M. Konrad-Zerna A. Wetzke M. Lohse P. Glas J. Tillack-Schreiber C. Schnitzler F. Beigel F. Brand S. Lipocalin-2 Is a Disease Activity Marker in Inflammatory Bowel Disease Regulated by IL-17A, IL-22, and TNF-α and Modulated by IL23R Genotype Status Inflamm. Bowel Dis. 2015 21 2327 2340 10.1097/MIB.0000000000000515 26263469 · DOI
- [29]Alex P. Zachos N.C. Nguyen T. Gonzales L. Chen T.-E. Conklin L.S. Centola M. Li X. Distinct cytokine patterns identified from multiplex profiles of murine DSS and TNBS-induced colitis Inflamm. Bowel Dis. 2009 15 341 352 10.1002/ibd.20753 18942757 PMC2643312 · DOI
- [30]Qiu J. Heller J.J. Guo X. Chen Z.-M.E. Fish K. Fu Y.-X. Zhou L. The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells Immunity 2012 36 92 104 10.1016/j.immuni.2011.11.011 22177117 PMC3268875 · DOI
- [31]Reeves P.G. Nielsen F.H. Fahey G.C. AIN-93 purified diets for laboratory rodents: Final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet J. Nutr. 1993 123 1939 1951 10.1093/jn/123.11.1939 8229312 · DOI
- [32]Warden C.H. Fisler J.S. Comparisons of Diets Used in Animal Models of High-Fat Feeding Cell Metab. 2008 7 277 10.1016/j.cmet.2008.03.014 18396128 PMC2394560 · DOI
- [33]Segata N. Izard J. Waldron L. Gevers D. Miropolsky L. Garrett W.S. Huttenhower C. Metagenomic biomarker discovery and explanation Genome Biol. 2011 12 R60 10.1186/gb-2011-12-6-r60 21702898 PMC3218848 · DOI · Paper page
- [34]Lagkouvardos I. Lesker T.R. Hitch T.C.A. Gálvez E.J.C. Smit N. Neuhaus K. Wang J. Baines J.F. Abt B. Stecher B. Sequence and cultivation study of Muribaculaceae reveals novel species, host preference, and functional potential of this yet undescribed family Microbiome 2019 7 28 10.1186/s40168-019-0637-2 30782206 PMC6381624 · DOI
- [35]Kostic A.D. Xavier R.J. Gevers D. The microbiome in inflammatory bowel disease: Current status and the future ahead Gastroenterology 2014 146 1489 1499 10.1053/j.gastro.2014.02.009 24560869 PMC4034132 · DOI · Paper page
- [36]Korecka A. Dona A. Lahiri S. Tett A.J. Al-Asmakh M. Braniste V. D’Arienzo R. Abbaspour A. Reichardt N. Fujii-Kuriyama Y. Bidirectional communication between the Aryl hydrocarbon Receptor (AhR) and the microbiome tunes host metabolism NPJ Biofilms Microbiomes 2016 2 16014 10.1038/npjbiofilms.2016.14 28721249 PMC5515264 · DOI
- [38]Poland A. Knutson J.C. 2,3,7,8-Tetrachlorodibenzo- p -Dioxin and Related Halogenated Aromatic Hydrocarbons: Examination of the Mechanism of Toxicity Annu. Rev. Pharmacol. Toxicol. 1982 22 517 554 10.1146/annurev.pa.22.040182.002505 6282188 · DOI · Paper page
- [39]Landers J.P. Bunce N.J. The Ah receptor and the mechanism of dioxin toxicity Biochem. J. 1991 276 273 287 10.1042/bj2760273 1646595 PMC1151088 · DOI
- [40]Lin Y.H. Luck H. Khan S. Schneeberger P.H.H. Tsai S. Clemente-Casares X. Lei H. Leu Y.L. Chan Y.T. Chen H.Y. Aryl hydrocarbon receptor agonist indigo protects against obesity-related insulin resistance through modulation of intestinal and metabolic tissue immunity Int. J. Obes. 2019 43 2407 2421 10.1038/s41366-019-0340-1 PMC6892742 30944419 · DOI
- [41]Zhang L. Nichols R.G. Correll J. Murray I.A. Tanaka N. Smith P.B. Hubbard T.D. Sebastian A. Albert I. Hatzakis E. Persistent organic pollutants modify gut microbiota–host metabolic homeostasis in mice through aryl hydrocarbon receptor activation Environ. Health Perspect. 2015 123 679 688 10.1289/ehp.1409055 25768209 PMC4492271 · DOI
- [42]Bjeldanes L.F. Kim J.Y. Grose K.R. Bartholomew J.C. Bradfield C.A. Aromatic hydrocarbon responsiveness-receptor agonists generated from indole-3-carbinol in vitro and in vivo: Comparisons with 2,3,7,8-tetrachlorodibenzo-p-dioxin Proc. Natl. Acad. Sci. USA 1991 88 9543 9547 10.1073/pnas.88.21.9543 1658785 PMC52754 · DOI
- [43]Anderton M.J. Manson M.M. Verschoyle R.D. Gescher A. Lamb J.H. Farmer P.B. Steward W.P. Williams M.L. Pharmacokinetics and tissue disposition of indole-3-carbinol and its acid condensation products after oral administration to mice Clin. Cancer Res. 2004 10 5233 5241 10.1158/1078-0432.CCR-04-0163 15297427 · DOI
- [44]Natividad J.M. Agus A. Planchais J. Lamas B. Jarry A.C. Martin R. Michel M.L. Chong-Nguyen C. Roussel R. Straube M. Impaired Aryl Hydrocarbon Receptor Ligand Production by the Gut Microbiota Is a Key Factor in Metabolic Syndrome Cell Metab. 2018 28 737 749.e4 10.1016/j.cmet.2018.07.001 30057068 · DOI · Paper page
- [45]Lopetuso L.R. Scaldaferri F. Petito V. Gasbarrini A. Commensal Clostridia: Leading players in the maintenance of gut homeostasis Gut Pathog. 2013 5 1 8 10.1186/1757-4749-5-23 23941657 PMC3751348 · DOI · Paper page
- [46]Stefka A.T. Feehley T. Tripathi P. Qiu J. McCoy K. Mazmanian S.K. Tjota M.Y. Seo G.Y. Cao S. Theriault B.R. Commensal bacteria protect against food allergen sensitization Proc. Natl. Acad. Sci. USA 2014 111 13145 13150 10.1073/pnas.1412008111 25157157 PMC4246970 · DOI
- [47]Nagano Y. Itoh K. Honda K. The induction of Treg cells by gut-indigenous Clostridium Curr. Opin. Immunol. 2012 24 392 397 10.1016/j.coi.2012.05.007 22673877 · DOI
- [48]Julliard W. De Wolfe T.J. Fechner J.H. Safdar N. Agni R. Mezrich J.D. Amelioration of Clostridium difficile infection in mice by dietary supplementation with indole-3-carbinol Ann. Surg. 2017 265 1183 1191 10.1097/SLA.0000000000001830 27280500 PMC5743052 · DOI
- [49]Sung W.S. Lee D.G. In vitro antimicrobial activity and the mode of action of indole-3-carbinol against human pathogenic microorganisms Biol. Pharm. Bull. 2007 30 1865 1869 10.1248/bpb.30.1865 17917252 · DOI
- [50]Pillaiyar T. Köse M. Sylvester K. Weighardt H. Thimm D. Borges G. Förster I. Von Kügelgen I. Müller C.E. Diindolylmethane Derivatives: Potent Agonists of the Immunostimulatory Orphan G Protein-Coupled Receptor GPR84 J. Med. Chem. 2017 60 3636 3655 10.1021/acs.jmedchem.6b01593 28406627 · DOI
- [51]Recio C. Lucy D. Purvis G.S.D. Iveson P. Zeboudj L. Iqbal A.J. Lin D. O’Callaghan C. Davison L. Griesbach E. Activation of the immune-metabolic receptor GPR84 enhances inflammation and phagocytosis in macrophages Front. Immunol. 2018 9 1419 10.3389/fimmu.2018.01419 29973940 PMC6019444 · DOI
- [52]Gevers D. Kugathasan S. Denson L.A. Vázquez-Baeza Y. Van Treuren W. Ren B. Schwager E. Knights D. Song S.J. Yassour M. The treatment-naive microbiome in new-onset Crohn’s disease Cell Host Microbe 2014 15 382 392 10.1016/j.chom.2014.02.005 24629344 PMC4059512 · DOI · Paper page
- [53]Loh G. Blaut M. Role of commensal gut bacteria in inflammatory bowel diseases Gut Microbes 2012 3 544 555 10.4161/gmic.22156 23060017 PMC3495792 · DOI
- [54]Schmidt J.V. Su G.H.T. Reddy J.K. Simon M.C. Bradfield C.A. Characterization of a murine Ahr null allele: Involvement of the Ah receptor in hepatic growth and development Proc. Natl. Acad. Sci. USA 1996 93 6731 6736 10.1073/pnas.93.13.6731 8692887 PMC39095 · DOI
Cited by
Sorted by citations
Sun, J., Zhang, Y., Kong, Y., Ye, T., Yu, Q., Kumaran Satyanarayanan, S., Su, K.-P., & Liu, J. (2022) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2022.08.003 · Cited by 255 · see citing works
Kynurenine Pathway of Tryptophan Metabolism in Migraine and Functional Gastrointestinal Disorders
Fila, M., Chojnacki, J., Pawlowska, E., Szczepanska, J., Chojnacki, C., & Blasiak, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221810134 · Cited by 50 · see citing works
Rodent Genetic Models of Ah Receptor Signaling
Wilson, R. H., & Bradfield, C. A. (2021) · Drug Metabolism Reviews · doi:10.1080/03602532.2021.1955916 · Cited by 16 · see citing works
“…considerations are particularly important as it is now known that ligands obtained through the diet can influence microbiome and AHR signaling, and it is also likely that differences in pathogens can affect immune status in laboratory mice (Leavy 2011; Brawner et al. 2019; Schanz et al. 2020).”
Background
- Authors
- Schanz, O., Chijiiwa, R., Cengiz, S. C., Majlesain, Y., Weighardt, H., Takeyama, H., & Förster, I.
- Affiliations
- University of Bonn (DE)
- Waseda University (JP)
- Corresponding author
- Weighardt, Heike
- Takeyama, Haruko
- Förster, Irmgard
- Venue
- International Journal of Molecular Sciences
- Publisher
- MDPI AG
- Published
- 2020-04-30
- Volume
- 21
- Issue
- 9
- Pages
- 3189
- ISSN
- 1422-0067 (ISSN-L)
- PMC
- PMC7246938
- OpenAlex
- W3023164985
- Cited by
- 60
- References
- 4
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 9 · 2023: 10 · 2022: 11 · 2021: 11 · 2020: 4 · 2019: 1
- FWCI
- 2.92
- Type
- journal article
- Language
- en
- Open access
- gold
- dx.doi.org
- Licence
- Locations
- International Journal of Molecular Sciences (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Deutsche Forschungsgemeinschaft (EXC 2151-Project No. 390873048)
- Jürgen Manchot Foundation (MOI-P14, PhD stipend Majlesain)
- Ministry of Education, Culture, Sports, Science and Technology (Top Global University Project)
- Innovation Advancement Organization, Japan (H.T.)
- Deutscher Akademischer Austauschdienst (Short-Term Grants, 2019 (57440917))
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics, phytochemicals, and oxidative stress
- Keywords
- aryl hydrocarbon receptor, indole-3-carbinol, intestinal immune cells, gut microbiota, DSS-induced colitis, Enterobacteriaceae, high-fat diet, phytochemicals
- MeSH terms
- Gastrointestinal Microbiome, Animals, Colitis, Female, Flow Cytometry, Indoles, Male, RNA, Ribosomal, 16S, Dextran Sulfate, Receptors, Aryl Hydrocarbon, Mice, Real-Time Polymerase Chain Reaction
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review