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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Background
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Background
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BackgroundMethodInfluential
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Background
The Aryl Hydrocarbon Receptor
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Background
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“To visualize the ability of As(III) to alter the transformation and subsequent DNA binding of the AhR, a complementary pair of synthetic oligonucleotides containing the sequence 5 -GAT CTG GCT CTT CTC ACG CAA CTC CG-3 and 5 -GAT CCG GAG TTG CGT GAG AAG AGC CA-3 , corresponding to the XRE binding site, were synthesized…”
Method
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Background
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Self-citation
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“In the past decades, the major concerns on Ah- Aryl hydrocarbon receptor agonists (Ah-agonists), which include structurally diverse synthetic and naturally-occurring chemicals, are ubiquitous in the environment (Denison et al., 2002).”
Background
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“As has been pointed out by this work and others [5, 6], planarity appears to be an important requirement for AhR ligands.”
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“Most notable of these genes in the fields of toxicology and pharmacology include phase I and II drug-metabolizing enzymes and transporters (Nebert et al., 2000; Denison et al., 2002; Hu et al., 2007; Kohle and Bock, 2007).”
Background
Isozyme- and gender-specific induction of glutathione S-transferases by flavonoids
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“High-aYnity ligands of the AhR receptor are characterized as being planar, aromatic and hydrophobic molecules.”
BackgroundInfluential
Mutational analysis of the mouse aryl hydrocarbon receptor tyrosine residues necessary for recognition of dioxin response elements
Minsavage, G. D., Vorojeikina, D. P., & Gasiewicz, T. A. (2003) · Archives of Biochemistry and Biophysics · doi:10.1016/s0003-9861(03)00033-x · Cited by 18
Predicting Chemical Immunotoxicity through Data-Driven QSAR Modeling of Aryl Hydrocarbon Receptor Agonism and Related Toxicity Mechanisms
Daood, N. J., Russo, D. P., Chung, E., Qin, X., & Zhu, H. (2024) · Environment & Health · doi:10.1021/envhealth.4c00026 · Cited by 16
Aromatic hydrocarbon receptors in mitochondrial biogenesis and function
Sahebnasagh, A., Hashemi, J., Khoshi, A., Saghafi, F., Avan, R., Faramarzi, F., Azimi, S., Habtemariam, S., Sureda, A., Khayatkashani, M., et al. (2021) · Mitochondrion · doi:10.1016/j.mito.2021.09.012 · Cited by 20
In Vitro Genotoxicity Evaluation of PAHs in Mixtures Using Experimental Design
Castel, R., Tassistro, V., Claeys‐Bruno, M., Malleret, L., & Orsière, T. G. (2023) · Toxics · doi:10.3390/toxics11050470 · Cited by 17
“PAHs bind to the Aryl hydrocarbon receptor (AhR), which in turn will induce the production of the phases I and II enzymes [18].”
Background
StemRegenin-1 Attenuates Endothelial Progenitor Cell Senescence by Regulating the AhR Pathway-Mediated CYP1A1 and ROS Generation
Lim, H. J., Jang, W. B., Rethineswaran, V. K., Choi, J., Lee, E. J., Park, S., Jeong, Y., Ha, J. S., Yun, J., Choi, Y. J., et al. (2023) · Cells · doi:10.3390/cells12152005 · Cited by 17
“AhR is a transcription factor that regulates gene expression in an exo/endogenous ligand-dependent manner [24].”
Background
Aryl hydrocarbon receptor role in chronic inflammatory skin diseases: a narrative review
Dec, M., & Arasiewicz, H. (2024) · Advances in Dermatology and Allergology · doi:10.5114/ada.2023.135617 · Cited by 22
“It is activated by a variety of low-molecular-weight ligands that can be obtained from endogenous, dietary, environmental, and microbial sources [3].”
Background
Predicting the Activity of Unidentified Chemicals in Complementary Bioassays from the HRMS Data to Pinpoint Potential Endocrine Disruptors
Rahu, I., Kull, M., & Kruve, A. (2024) · Journal of Chemical Information and Modeling · doi:10.1021/acs.jcim.3c02050 · Cited by 18
“44 Nevertheless, the informativeness of this feature is limited due to its broad chemical space coverage.”
Background
Fused mesoionic heterocyclic compounds are a new class of aryl hydrocarbon receptor (AhR) agonist of exceptional potency
Wall, R. J., Bell, D., Bazzi, R., Fernandes, A., Rose, M., Rowlands, J. C., & Mellor, I. R. (2012) · Toxicology · doi:10.1016/j.tox.2012.09.003 · Cited by 17
Novel 2-amino-isoflavones exhibit aryl hydrocarbon receptor agonist or antagonist activity in a species/cell-specific context
Wall, R. J., He, G., Denison, M. S., Congiu, C., Onnis, V., Fernandes, A., Bell, D., Rose, M., Rowlands, J. C., Balboni, G., et al. (2012) · Toxicology · doi:10.1016/j.tox.2012.03.011 · Cited by 17
“, 2000) and while this difference in potency is most likely due to sequence differences between the ligand binding domain of the rodent and human AhR, it may also be affected by other factors such as ligand pharmacokinetics, metabolism and AhR concentration (Denison et al., 2002).”
Self-citation
AHR gene-dioxin interactions and birthweight in the Seveso Second Generation Health Study
Ames, J., Warner, M. L., Mocarelli, P., Brambilla, P., Signorini, S. G., Siracusa, C., Huen, K., Holland, N., & Eskenazi, B. (2018) · International Journal of Epidemiology · doi:10.1093/ije/dyy165 · Cited by 18
Gene cloning and expression analysis of AhR and CYP4 from Pinctada martensii after exposed to pyrene
Du, J., Liao, C., Zhou, H., Diao, X., Li, Y., Zheng, P., & Wang, F. (2015) · Ecotoxicology · doi:10.1007/s10646-015-1424-x · Cited by 17
“…by a variety of chemicals (Denison and Heath-Pagliuso 1998), including a diverse array of anthropogenic compounds present in the environment, such as polycyclic aromatic hydrocarbons (PAHs), halogenated aromatic hydrocarbons (HAHs) and low affinity-binding natural compounds (Denison et al. 2002).”
Background
Gene–chemical interactions in the developing mammalian nervous system: Effects on proliferation, neurogenesis and differentiation
Fox, D. A., Opanashuk, L. A., Žarkovski, A., & Weiss, B. (2010) · NeuroToxicology · doi:10.1016/j.neuro.2010.03.007 · Cited by 17
“Nevertheless, most information regarding AhR function has been obtained from studies that involve the persistent environmental contaminant TCDD, which has the highest binding affinity among all of the reported ligands [46,47].”
Background
Influence of Toxic Chemicals on Female Reproduction: A Review
Bhardwaj, J. K. (2014) · Cell Biology Research & Therapy · doi:10.4172/2324-9293.1000110 · Cited by 17
“It leads to germ cell loss by acting as an unnatural ligand for orphan transcription factor referred to as aromatic hydro carbon receptor, member of PAS family of transcriptional regulators that modulate large physiological functions of body [123].”
Background
Antagonistic and synergistic interactions during the binding of binary mixtures of polycyclic aromatic hydrocarbons to the aryl hydrocarbon receptor
Pushparajah, D. S., & Ioannides, C. (2018) · Toxicology in Vitro · doi:10.1016/j.tiv.2018.02.011 · Cited by 17
Black Tea Theaflavins Suppress Dioxin-Induced Transformation of the Aryl Hydrocarbon Receptor
Fukuda, I., Sakane, I., Yabushita, Y., Sawamura, S., Kanazawa, K., & Ashida, H. (2005) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.69.883 · Cited by 17
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
“More detailed descriptions of AHR signaling and receptor subdomains, as well as the role of the ARNT protein, can be found in a number of excellent reviews (Whitlock 1990; Schmidt and Bradfield 1996; Denison et al. 2002; Nebert 2017; Larigot et al. 2018; Avilla et al. 2020).”
Background
Allergic responses and aryl hydrocarbon receptor novel pathway of mast cell activation
Sibilano, R., Pucillo, C. E. M., & Gri, G. (2014) · Molecular Immunology · doi:10.1016/j.molimm.2014.02.015 · Cited by 16
Ecology and animal health
Norrgren, L., & Levengood, J. M. (2012) · Cited by 16
Establishment of a primary human hepatocyte spheroid system for evaluating metabolic toxicity using dacarbazine under conditions of CYP1A2 induction
Mizoi, K., Hosono, M., Kojima, H., & Ogihara, T. (2019) · Drug Metabolism and Pharmacokinetics · doi:10.1016/j.dmpk.2019.11.002 · Cited by 16
Benzo[ghi]perylene induces cellular dormancy signaling and endoplasmic reticulum stress in NL-20 human bronchial epithelial cells
Zaragoza‐Ojeda, M., Torres-Flores, U., Rodríguez-Leviz, A., & Arenas‐Huertero, F. (2022) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2022.115925 · Cited by 16
Characteristic single glucosinolates from Moringa oleifera: Induction of detoxifying enzymes and lack of genotoxic activity in various model systems
Förster, N., Mewis, I., Glatt, H. R., Haack, M., Brigelius‐Flohé, R., Schreiner, M., & Ulrichs, C. (2016) · Food & Function · doi:10.1039/c6fo01231k · Cited by 16
Novel fluorescent and secreted transcriptional reporters for quantifying activity of the xenobiotic sensor aryl hydrocarbon receptor (AHR)
Degrelle, S. A., Ferecatu, I., & Fournier, T. (2022) · Environment International · doi:10.1016/j.envint.2022.107545 · Cited by 15
Rats fed soy protein isolate (SPI) have impaired hepatic CYP1A1 induction by polycyclic aromatic hydrocarbons as a result of interference with aryl hydrocarbon receptor signaling
Singhal, R., Badger, T. M., & Ronis, M. J. J. (2007) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2007.11.009 · Cited by 15
A Comprehensive Pan-Cancer Analysis of 33 Human Cancers Reveals the Immunotherapeutic Value of Aryl Hydrocarbon Receptor
Mo, Z., Li, P., Cao, Z., & Zhang, S. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.564948 · Cited by 15
A Critical Review: 2,3,7,8 –Tetrachlorodibenzo-p-dioxin (2,3,7,8-TCDD) Effects on Gonad Development in Bivalve Mollusks
Cooper, K. R., & Wintermyer, M. L. (2009) · Journal of Environmental Science and Health Part C · doi:10.1080/10590500903310112 · Cited by 15
“Tryptophan and related indole containing compounds are present in bivalve gonad tissue and may be the endogenous ligand for the AhR (14).”
BackgroundInfluential
Tristetraprolin suppresses AHRR expression through mRNA destabilization
Lee, H. H., Kim, W., Kim, D. H., Park, J. W., Kang, T., Chung, J. W., & Leem, S. (2013) · FEBS Letters · doi:10.1016/j.febslet.2013.03.031 · Cited by 15
“The AHR is a ligand-activated transcription factor that mediates a pleiotropic response to various environmental toxins [4], such as benzo[a]pyrene, and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) [5].”
Background
Direct Assessment of Cumulative Aryl Hydrocarbon Receptor Agonist Activity in Sera from Experimentally Exposed Mice and Environmentally Exposed Humans
Schlezinger, J. J., Bernard, P. L., Haas, A., Grandjean, P., Weihe, P., & Sherr, D. H. (2009) · Environmental Health Perspectives · doi:10.1289/ehp.0901113 · Cited by 15
“The AhR activates transcription of multiple genes, such as those responsible for metabolism of PAHs and HAHs [e.g., cytochrome P450 (CYP) genes], and suppresses the transcription of others (e.g., immunoglobulin) (Denison et al. 2002; Sulentic et al. 1998).”
Candidate cytochrome P450 genes for ethoxyresorufin O-deethylase activity in oyster Crassostrea gigas
Siebert, M. N., Mattos, J. J., Toledo‐Silva, G., Razzera, G., & Bainy, A. C. D. (2017) · Aquatic Toxicology · doi:10.1016/j.aquatox.2017.06.004 · Cited by 15
Role of Flavonoids in the Prevention of AhR-Dependent Resistance During Treatment with BRAF Inhibitors
Leclair, H. M., Tardif, N., Paris, A., Galibert, M., & Corre, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21145025 · Cited by 16
Environmental Toxins as Modulators of Antiviral Immune Responses
Lawrence, B. P. (2007) · Viral Immunology · doi:10.1089/vim.2007.0013 · Cited by 15
Health Risks from Dioxin and Related Compounds
Board on Environmental Studies and Toxicology, & Studies, D. O. E. A. L. (2006) · National Academies Press eBooks · doi:10.17226/11688 · Cited by 15
Fractionation and Determination of Ah Receptor (AhR) Agonists in Organic Waste After Anaerobic Biodegradation and in Batch Experiments with PCB and decaBDE (8 pp)
Olsman, H., Schnürer, A., Björnfoth, H., van Bavel, B., & Engwall, M. (2007) · Environmental Science and Pollution Research · doi:10.1065/espr2006.12.369 · Cited by 15
Aryl Hydrocarbon Receptor-Dependent and -Independent Pathways Mediate Curcumin Anti-Aging Effects
Brinkmann, V., Romeo, M., Larigot, L., Hemmers, A., Tschage, L., Kleinjohann, J., Schiavi, A., Steinwachs, S., Esser, C., Menzel, R., et al. (2022) · Antioxidants · doi:10.3390/antiox11040613 · Cited by 17
“Of note, many compounds impacting aging or age-related diseases (Sakakibara et al., 2005, Okey et al., 1984, Gao et al., 2015) can modulate AhR activity (Denison et al., 2002, Ashida et al., 2000, Zhang et al., 2003).”
BackgroundSelf-citation
Endocrine disruptor actions through receptor crosstalk
Kiyama, R. (2016) · Environmental Biotechnology · doi:10.14799/ebms262 · Cited by 15
“Abbreviations; AhR: aryl hydrocarbon receptor; AR: androgen receptor; CCR: C-C chemokine receptor; CREB: cAMP response element-binding protein; CXCR1: chemokine (C-X-C motif) receptor 1; CREB: cyclic AMP response element-binding protein; DDE: dichlorodiphenyldichloroethylene; DDT: dichlorodiphenyltrichloroethane; DEHP…”
BackgroundInfluential
Protective effects of bark ethanolic extract from Spondias dulcis Forst F. against DNA damage induced by benzo[a]pyrene and cyclophosphamide
Araujo, C. D. S., Brito, L. D., Tarifa, M. O., da Silva, N. J. F., Rodrigues, K. S., Cavalcante, D. G. S. M., Gomes, A. S., Zocoler, M. A., Yoshihara, E., Camparoto, M. L., et al. (2019) · Genetics and Molecular Biology · doi:10.1590/1678-4685-gmb-2018-0038 · Cited by 14
Specific interactions between aryl hydrocarbon receptor and dioxin congeners: Ab initio fragment molecular orbital calculations
Yoshikawa, E., Miyagi, S., Dedachi, K., Ishihara‐Sugano, M., Itoh, S., & Kurita, N. (2010) · Journal of Molecular Graphics and Modelling · doi:10.1016/j.jmgm.2010.06.008 · Cited by 14
Cytochrome P4501A1 expression in blubber biopsies of endangered false killer whales (Pseudorca crassidens) and nine other odontocete species from Hawai‘i
Foltz, K. M., Baird, R. W., Ylitalo, G. M., & Jensen, B. A. (2014) · Ecotoxicology · doi:10.1007/s10646-014-1300-0 · Cited by 14
Caffeine Induces CYP1A2 Expression in Rat Hepatocytes but not in Human Hepatocytes
Vaynshteyn, D., & Jeong, H. (2012) · Drug Metabolism Letters · doi:10.2174/187231212804096745 · Cited by 14
“Furthermore, the chemical structure of caffeine resembles atypical AhR ligands that have been recently discovered [19].”
Background
A temporal high-resolution investigation of the Ah-receptor pathway during early development of zebrafish (Danio rerio)
Meyer-Alert, H., Ladermann, K., Larsson, M., Schiwy, S., Hollert, H., & Keiter, S. H. (2018) · Aquatic Toxicology · doi:10.1016/j.aquatox.2018.09.007 · Cited by 14
Cinnabarinic Acid-Induced Stanniocalcin 2 Confers Cytoprotection against Alcohol-Induced Liver Injury
Joshi, A., Thinakaran, G., & Elferink, C. J. (2022) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.121.000999 · Cited by 14
“Conventionally, AhR was studied within the context of toxicity in response to various expgenous agonists which are persistant environmental pollutants (Nebert and Gelboin, 1968b; Nebert and Gelboin, 1968a; Hankinson, 1979; Hankinson, 1980; Legraverend et al., 1982; Denison et al., 2002).”
Background
Xenobiotic‐induced alterations in thymocyte development
Drela, N. (2006) · Apmis · doi:10.1111/j.1600-0463.2006.apm_343.x · Cited by 14
“Ligands Endogenous ligands: indoles, AA metabolites, tetrapyroles (47, 49, 62) Dietary ligands: Naturally occurring (flavonoids, carotinoids, phenolics), others such as curcumin, indoles and tryptophan derivatives (46–48, 62, 63) Environmental chemicals: HAHs (polyhalogenated dibenzo-p-dioxins, dibenzofurans, biphenyl…”
Background
Aberrant Kynurenine Signaling Modulates DNA Replication Stress Factors and Promotes Genomic Instability in Gliomas
Bostian, A. C. L., & Eoff, R. L. (2016) · Chemical Research in Toxicology · doi:10.1021/acs.chemrestox.6b00255 · Cited by 14
Quantitative Structure–Activity Relationships Study on the Ah Receptor Binding Affinities of Polybrominated Diphenyl Ethers Using a Support Vector Machine
Zheng, G. F., Xiao, M., & Lü, X. (2006) · QSAR & Combinatorial Science · doi:10.1002/qsar.200610078 · Cited by 14
Implications of xenobiotic-response element(s) and aryl hydrocarbon receptor in health and diseases
Mandal, A., Biswas, N., & Alam, M. N. (2023) · Human Cell · doi:10.1007/s13577-023-00931-5 · Cited by 15
“When AhR is inactive, it remains bound with multifarious protein molecules namely with the heat shock protein HSP90, the XAP2, AIP, or ARA9, and p23 [3].”
Background
Confirmation of Molecular Planarity Disruption Effect on Aqueous Solubility Improvement of β-Naphthoflavone Analogs
Ishikawa, M., Yonehara, M., Kitahara, K., Shimokawa, J., Hashimoto, Y., & Fujita, Y. (2011) · Heterocycles · doi:10.3987/com-11-12352 · Cited by 13

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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