Cited by 489Toxic Organic Pollutants ImpactPharmacogenetics and Drug MetabolismCarcinogens and Genotoxicity Assessment

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Ligand binding and activation of the Ah receptor

Denison, Michael S, Pandini, Alessandro, Nagy, Scott R, Baldwin, Enoch P, Bonati, Laura·2002·Chemico-Biological Interactions

DOI 10.1016/s0009-2797(02)00063-7

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Abstract

The Ah receptor (AhR) is a ligand-dependent transcription factor that can be activated by structurally diverse synthetic and naturally-occurring chemicals. Although a significant amount of information is available with respect to the planar aromatic hydrocarbon AhR ligands, the actual spectrum of chemicals that can bind to and activate the AhR is only now being elucidated. In addition, the lack of information regarding the actual three-dimensional structure of the AhR ligand binding domain (LBD) has hindered detailed analysis of the molecular mechanisms by which these ligands bind to and active AhR signal transduction. In this review we describe the current state of knowledge with respect to naturally occurring AhR ligands and present and discuss the first theoretical model of the AhR LBD based on crystal structures of homologous PAS family members.

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Aryl Hydrocarbon Receptor Activation Impairs the Priming but Not the Recall of Influenza Virus-Specific CD8+ T Cells in the Lung
Lawrence, B. P., Roberts, A. D., Neumiller, J. J., Cundiff, J. A., & Woodland, D. L. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.9.5819 · Cited by 82
Identification and expression of multiple CYP1-like and CYP3-like genes in the bivalve mollusk Mytilus edulis
Zanette, J., Jenny, M. J., Goldstone, J. V., Parente, T. E., Woodin, B. R., Bainy, A. C. D., & Stegeman, J. J. (2012) · Aquatic Toxicology · doi:10.1016/j.aquatox.2012.11.017 · Cited by 81
“The induction of vertebrate CYP1 genes occurs via the aryl-hydrocarbon receptor (AHR), activated by xenobiotic chemicals such as planar halogenated hydrocarbons and PAHs, and by dietary compounds such as flavonoids (Denison et al., 2002; Hahn, 2002).”
Background
New Aryl Hydrocarbon Receptor Homology Model Targeted To Improve Docking Reliability
Motto, I., Bordogna, A., Soshilov, A. A., Denison, M. S., & Bonati, L. (2011) · Journal of Chemical Information and Modeling · doi:10.1021/ci2001617 · Cited by 80
Self-citation
Regulation of an insect cytochrome P450 monooxygenase gene (CYP6B1) by aryl hydrocarbon and xanthotoxin response cascades
Brown, R. P., McDonnell, C. M., Berenbaum, M. R., & Schuler, M. A. (2005) · Gene · doi:10.1016/j.gene.2005.05.026 · Cited by 79
The Aryl Hydrocarbon Receptor Affects Mouse Ovarian Follicle Growth via Mechanisms Involving Estradiol Regulation and Responsiveness1
Barnett-Ringgold, K., Tomic, D., Gupta, R. K., Miller, K. P., Meachum, S., Paulose, T., & Flaws, J. A. (2007) · Biology of Reproduction · doi:10.1095/biolreprod.106.057687 · Cited by 77
“The aryl hydrocarbon receptor (AHR) is a basic helix-loophelix (bHLH) and Per-Arnt-Sim (PAS)-containing transcription factor that regulates the expression of genes in a liganddependent manner [1, 2].”
Background
Persistent Binding of Ligands to the Aryl Hydrocarbon Receptor
Bohonowych, J. E. S., & Denison, M. S. (2007) · Toxicological Sciences · doi:10.1093/toxsci/kfm085 · Cited by 81
“…cytosol was prepared in HEDG (25mM 4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid, pH 7.5, 1mM ethylenediaminetetraacetic acid, 1mM dithiotreitol, 10% [v/v] glycerol) buffer as previously described (Denison et al., 2002b) and protein concentrations determined by dye-binding (Bradford, 1976).”
MethodInfluentialSelf-citation
The crystal structure of the AhRR–ARNT heterodimer reveals the structural basis of the repression of AhR-mediated transcription
Sakurai, S., Shimizu, T., & Ohto, U. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.812974 · Cited by 80
The Intersection Between the Aryl Hydrocarbon Receptor (AhR)‐ and Retinoic Acid‐Signaling Pathways
Murphy, K. A., Quadro, L., & White, L. A. (2007) · Vitamins and hormones · doi:10.1016/s0083-6729(06)75002-6 · Cited by 74
The Aryl Hydrocarbon Receptor Directly Regulates Expression of the Potent Mitogen Epiregulin
Patel, R. D., Kim, D. J., Peters, J. M., & Perdew, G. H. (2005) · Toxicological Sciences · doi:10.1093/toxsci/kfi344 · Cited by 74
“A number of exogenous and endogenous ligands are capable of activating the AhR (Denison et al., 2002).”
Background
Knockdown of aberrantly upregulated aryl hydrocarbon receptor reduces tumor growth and metastasis of MDA-MB-231 human breast cancer cell line
Goode, G., Ballard, B., Manning, H., Freeman, M., Kang, Y.-B., & Eltom, S. E. (2013) · International Journal of Cancer · doi:10.1002/ijc.28297 · Cited by 66
“Binding to exogenous ligands such as PAH, leads to conformational changes that result in nuclear translocation of AhR, where it heterodimerizes with the AhR nuclear translocator protein (ARNT).(11,13) The heterodimer binds to a consensus DNA sequence xenobiotic responsive element (XRE), on the enhancer regions of targ…”
Background
Toxicology mechanism of the persistent organic pollutants (POPs) in fish through AhR pathway
Zhou, H., Wu, H., Liao, C., Diao, X., Jiping, Z., Chen, L., & Xue, Q. (2010) · Toxicology Mechanisms and Methods · doi:10.3109/15376516.2010.485227 · Cited by 71
“…step is ligand binding to the AhR ligand binding domain which results in conformational changes that expose the nuclear localization sequence through alterations of XAP2 binding (Denison et al. 2002), which makes it necessary to facilitate interaction of the NLS with nuclear import components.”
Background
The Long Winding Road toward Understanding the Molecular Mechanisms for B-Cell Suppression by 2,3,7,8-Tetrachlorodibenzo-p-dioxin
Sulentic, C. E. W., & Kaminski, N. E. (2010) · Toxicological Sciences · doi:10.1093/toxsci/kfq324 · Cited by 71
“…B cells exhibited slower kinetics and reduced magnitude of induction by TCDD when compared with mouse B cells, which was consistent with the generally observed 10-fold lower sensitivity of human AhR to TCDD binding and CYP1A1 induction (reviewed by Harper et al., 2002 and Denison et al., 2002).”
Background
The effect of aryl hydrocarbon receptor ligands on the expression of AhR, AhRR, ARNT, Hif1α, CYP1A1 and NQO1 genes in rat liver
Brauze, D., Widerak, M., Cwykiel, J. M., Szyfter, K., & Baer‐Dubowska, W. (2006) · Toxicology Letters · doi:10.1016/j.toxlet.2006.09.010 · Cited by 73
“AhR can bind several structurally diverse classes f xenobiotic ligands, but their binding affinity difers to great extent (Denison et al., 2002; Denison and agy, 2003).”
Background
Evaluation of Toxic Activities of Polycyclic Aromatic Hydrocarbon Derivatives Using In Vitro Bioassays
Bekki, K., Takigami, H., Suzuki, G., Tang, N., & Hayakawa, K. (2009) · Eisei kagaku · doi:10.1248/jhs.55.601 · Cited by 70
“Benzo[c]phenanthrene-[1, 4 ]-quinone was the most TTR-active compound (IC50 :2 .5µM).”
Molecular toxicology of polybrominated diphenyl ethers: nuclear hormone receptor mediated pathways
Ren, X., & Guo, L. (2013) · Environmental Science Processes & Impacts · doi:10.1039/c3em00023k · Cited by 68
Comparative Metabolomic and Genomic Analyses of TCDD-Elicited Metabolic Disruption in Mouse and Rat Liver
Karmaus, A. L., Kent, M. N., Makley, M. K., Mets, B. D., DelRaso, N. J., Jahns, G. L., Burgoon, L. D., Zacharewski, T. R., & Reo, N. V. (2011) · Toxicological Sciences · doi:10.1093/toxsci/kfr262 · Cited by 67
“This heterodimer binds to dioxin response elements (DREs) in the regulatory regions of target genes causing altered gene expression (Denison et al., 2002; Hankinson, 1995).”
Background
Xenobiotic-sensing nuclear receptors involved in drug metabolism: a structural perspective
Wallace, B. D., & Redinbo, M. R. (2012) · Drug Metabolism Reviews · doi:10.3109/03602532.2012.740049 · Cited by 69
“The AhR is known to bind include many synthetic xenobiotic compounds, such as halogenated and polycyclic aromatic hydrocarbons (Denison et al., 2002; Denison and Nagy, 2003), including dioxins (environmental toxins), Drug Metab Rev. Author manuscript; available in PMC 2016 May 24.”
Melatonin and Its Metabolites Can Serve as Agonists on the Aryl Hydrocarbon Receptor and Peroxisome Proliferator-Activated Receptor Gamma
Slominski, A. T., Kim, T., Slominski, R. M., Song, Y., Qayyum, S., Placha, W., Janjetović, Z., Kleszczyński, K., Atigadda, V. R., Song, Y., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242015496 · Cited by 67
Generalized Concentration Addition Predicts Joint Effects of Aryl Hydrocarbon Receptor Agonists with Partial Agonists and Competitive Antagonists
Howard, G. J., Schlezinger, J. J., Hahn, M. E., & Webster, T. F. (2009) · Environmental Health Perspectives · doi:10.1289/ehp.0901312 · Cited by 63
“Exogenous ligands induce AhR trans location to the nucleus, dimerization with the AhR nuclear translocator protein, binding to target genes at specific DNA binding sites (AhREs), and activation of gene transcription (Denison et al. 2002).”
Background
Aryl hydrocarbon receptor ligand activity of polycyclic aromatic ketones and polycyclic aromatic quinones
Misaki, K., Kawami, H., Tanaka, T., Handa, H., Nakamura, M., Matsui, S., & Matsuda, T. (2007) · Environmental Toxicology and Chemistry · doi:10.1897/06-465r.1 · Cited by 63
“Lower AhR potency of TCDD in yeast cells than mammalian cells also may be caused by the reduction of ligand-binding activity in the polymorphic form of human AhR [19,35].”
Background
The tryptophan photoproduct 6-formylindolo[3,2-b]carbazole (FICZ) binds multiple AHRs and induces multiple CYP1 genes via AHR2 in zebrafish
Jönsson, M. E., Franks, D. G., Woodin, B. R., Jenny, M. J., Garrick, R. A., Behrendt, L., Hahn, M. E., & Stegeman, J. J. (2009) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2009.07.003 · Cited by 63
Inhibition of osteoclast differentiation by polycyclic aryl hydrocarbons is dependent on cell density and RANKL concentration
Voronov, I., Heersche, J. N. M., Casper, R. F., Tenenbaum, H. C., & Manolson, M. F. (2005) · Biochemical Pharmacology · doi:10.1016/j.bcp.2005.04.028 · Cited by 64
Baltic salmon (Salmo salar) yolk-sac fry mortality is associated with disturbances in the function of hypoxia-inducible transcription factor (HIF-1$alpha;) and consecutive gene expression
Vuori, K. A. M., Soitamo, A. J., Vuorinen, P. J., & Nikinmaa, M. (2004) · Aquatic Toxicology · doi:10.1016/j.aquatox.2004.03.019 · Cited by 65
“In addition, the activation of AhR-dependent gene expression pathway may be of dietary origin (Denison et al., 2002).”
Background
Sulforaphane induces CYP1A1 mRNA, protein, and catalytic activity levels via an AhR-dependent pathway in murine hepatoma Hepa 1c1c7 and human HepG2 cells
Anwar‐Mohamed, A., & El‐Kadi, A. O. S. (2008) · Cancer Letters · doi:10.1016/j.canlet.2008.10.003 · Cited by 63
“To visualize the ability of SUL to induce the transformation and subsequent DNA binding of the AhR, a complementary pair of synthetic oligonucleotides containing the sequence 50-GAT CTG GCT CTT CTC ACG CAA CTC CG-30 and 50-GAT CCG GAG TTG CGT GAG AAG AGC CA-30, corresponding to the XRE binding site, were synthesized a…”
Method
Automated Dose-Response Analysis and Comparative Toxicogenomic Evaluation of the Hepatic Effects Elicited by TCDD, TCDF, and PCB126 in C57BL/6 Mice
Kopec, A. K., Burgoon, L. D., Aibo, D. I., Burg, A. R., Lee, A. W., Tashiro, C. H. M., Potter, D., Sharratt, B., Harkema, J. R., Rowlands, J. C., et al. (2010) · Toxicological Sciences · doi:10.1093/toxsci/kfq236 · Cited by 61
Role of Dioxin Response Element and Nuclear Factor-κB Motifs in 2,3,7,8-Tetrachlorodibenzo-p-dioxin-Mediated Regulation of Fas and Fas Ligand Expression
Singh, N. P., Nagarkatti, M., & Nagarkatti, P. S. (2006) · Molecular Pharmacology · doi:10.1124/mol.106.028365 · Cited by 60
“…by toxic compounds, including 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) (Hankinson, 1995; Fernandez-Salguero et al., 1996; Schmidt and Bradfield, 1996; Gonzalez and Fernandez-Salguero, 1998; Gu et al., 2000; Safe, 2001; Denison et al., 2002; Mimura and FujiiKuriyama, 2003; Camacho et al., 2005).”
Role of Aryl Hydrocarbon Receptor Activation in Inflammatory Chronic Skin Diseases
Napolitano, M., Fabbrocini, G., Martora, F., Picone, V., Morelli, P., & Patruno, C. (2021) · Cells · doi:10.3390/cells10123559 · Cited by 59
“The chaperon complex maintains AhR in an inactive and stable conformation with a high-binding affinity for ligand and retains the receptor in the cytoplasm [4].”
Background
Comparison of Gene Expression Patterns between 2,3,7,8-Tetrachlorodibenzo-p-dioxin and a Natural Arylhydrocarbon Receptor Ligand, Indirubin
Adachi, J. (2004) · Toxicological Sciences · doi:10.1093/toxsci/kfh129 · Cited by 59
“The majority of natural AhR ligands identified to date are dietary or related to dietary plant products (Denison et al., 2002).”
Background
Interaction between the aryl hydrocarbon receptor and its antagonists, flavonoids
Fukuda, I., Mukai, R., Kawase, M., Yoshida, K., & Ashida, H. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.05.199 · Cited by 58
“Following binding of ligands including dioxins to the AhR, the receptor translocates from cytosol to the nucleus, detaches partner proteins of the complex, heterodimerizes with AhR nuclear translocator (Arnt), and binds to an enhancer sequence called dioxin response element (DRE) of several drug metabolizing enzymes […”
Background
Polyphenols and Tryptophan Metabolites Activate the Aryl Hydrocarbon Receptor in an in vitro Model of Colonic Fermentation
Koper, J. E. B., Loonen, L. M. P., Wells, J. M., Troise, A. D., Capuano, E., & Fogliano, V. (2018) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201800722 · Cited by 59
Oncology Therapeutics Targeting the Metabolism of Amino Acids
Muhammad, N., Lee, H. M., & Kim, J. (2020) · Cells · doi:10.3390/cells9081904 · Cited by 59
“AhR is also a receptor to the exogenous ligand 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)[211], which showed an immunosuppressive effector of T cells and dendritic cells (DCs)[212].”
Background
Glutathione transferase pi class 2 (GSTp2) protects against the cardiac deformities caused by exposure to PAHs but not PCB-126 in zebrafish embryos
Garner, L. V. T., & Giulio, R. T. D. (2012) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/j.cbpc.2012.01.007 · Cited by 57
“…particularly CYP1A, are well-characterized phase I enzymes, and phase II enzymes known to be activated by the AHR include UDP-glucuronosyltransferases (UDPGTs), NAD(P)H:quinone oxidoreductase 1 (NQO1), and glutathione transferases (GSTs; EC 2.5.1.18) (Nebert et al., 2000; Denison et al., 2002).”
Influential
Benzo[a]pyrene inhibits osteoclastogenesis by affecting RANKL-induced activation of NF-κB
Voronov, I., Li, K., Tenenbaum, H. C., & Manolson, M. F. (2008) · Biochemical Pharmacology · doi:10.1016/j.bcp.2008.02.025 · Cited by 57
The toxicological profile of polychlorinated naphthalenes (PCNs)
Fernandes, A., Kilanowicz, A., Stragierowicz, J., Klimczak, M., & Falandysz, J. (2022) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2022.155764 · Cited by 59
AhR agonist and genotoxicant bioavailability in a PAH-contaminated soil undergoing biological treatment
Andersson, E., Rotander, A., von Kronhelm, T., Berggren, A., Ivarsson, P., Hollert, H., & Engwall, M. (2009) · Environmental Science and Pollution Research · doi:10.1007/s11356-009-0121-9 · Cited by 56
“... this study, the bio-TEQs calculated using the CALUX assay were higher than the TEQs calculated from chemical analysis in both the toluene and butanol extracts (Fig. 3 and Table 1). These results indicate that there are additional toxic PAHs or related AhR activating compounds in both extracts that are not included…”
Method
AhR expression is increased in hepatocellular carcinoma
Liu, Z., Wu, X., Zhang, F., Han, L., Bao, G., He, X., & Xu, Z. (2013) · Journal of Molecular Histology · doi:10.1007/s10735-013-9495-6 · Cited by 60
Epigenetic and MicroRNA-Dependent Control of Cytochrome P450 Expression: A Gap Between DNA and Protein
Gomez, A. V., & Ingelman‐Sundberg, M. (2009) · Pharmacogenomics · doi:10.2217/pgs.09.56 · Cited by 55

Authors: Denison, M. S., Pandini, A., Nagy, S. R., Baldwin, E. P., & Bonati, L.
Affiliations: University of California, Davis (US)
University of Milano-Bicocca (IT)
Corresponding author: Denison, Michael S
ORCID: Denison, Michael S
Pandini, Alessandro
Baldwin, Enoch P
Bonati, Laura
Venue: Chemico-Biological Interactions
Publisher: Elsevier BV
Published: 2002-09
Volume: 141
Issue: 1-2
Pages: 3-24
ISSN: 0009-2797 (ISSN-L)
DOI: 10.1016/s0009-2797(02)00063-7
OpenAlex: W1985754063
Cited by: 485
References: 153
Citations by year: 2026: 7 · 2025: 8 · 2024: 12 · 2023: 16 · 2022: 18 · 2021: 7 · 2020: 18 · 2019: 13 · 2018: 18 · 2017: 18 · 2016: 20 · 2015: 16 · 2014: 30 · 2013: 24 · 2012: 30
FWCI: 15.36
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Chemico-Biological Interactions (publishedVersion)
PubMed (publishedVersion)
BOA (University of Milano-Bicocca) (submittedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: National Institutes of Health (5r01es007072-04)
National Institute of Environmental Health Sciences (ES07059, ES 07685, R01ES007685, ES-07072, ES5707, T32ES007059)
Topics: Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Toxic Organic Pollutants Impact
Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmacology › Pharmacogenetics and Drug Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Carcinogens and Genotoxicity Assessment
Keywords: aryl hydrocarbon receptor, ligand binding, receptor activation, ligand-binding domain, aromatic hydrocarbons, crystal structure, signal transduction, transcription factors
MeSH terms: Animals, Binding Sites, Humans, Ligands, Protein Binding, Protein Conformation, Signal Transduction, Receptors, Aryl Hydrocarbon

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Ligand binding and activation of the Ah receptor

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