Cited by 134Toxic Organic Pollutants ImpactDevelopmental Biology and Gene RegulationMarine Invertebrate Physiology and Ecology

Diversity as opportunity: Insights from 600 million years of AHR evolution

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Hahn, Mark E., Karchner, Sibel I., Merson, Rebeka R.·2017·Current Opinion in Toxicology

Abstract

The aryl hydrocarbon receptor (AHR) was for many years of interest only to pharmacologists and toxicologists. However, this protein has fundamental roles in biology that are being revealed through studies in diverse animal species. The AHR is an ancient protein. AHR homologs exist in most major groups of modern bilaterian animals, including deuterostomes (chordates, hemichordates, echinoderms) and the two major clades of protostome invertebrates [ecdysozoans (e.g. arthropods and nematodes) and lophotrochozoans (e.g. molluscs and annelids)]. AHR homologs also have been identified in cnidarians such as the sea anemone Nematostella and in the genome of Trichoplax, a placozoan. Bilaterians, cnidarians, and placozoans form the clade Eumetazoa, whose last common ancestor lived approximately 600 million years ago (MYA). The presence of AHR homologs in modern representatives of all these groups indicates that the original eumetazoan animal possessed an AHR homolog. Studies in invertebrates and vertebrates reveal parallel functions of AHR in the development and function of sensory neural systems, suggesting that these may be ancestral roles. Vertebrate animals are characterized by the expansion and diversification of AHRs, via gene and genome duplications, from the ancestral protoAHR into at least five classes of AHR-like proteins: AHR, AHR1, AHR2, AHR3, and AHRR. The evolution of multiple AHRs in vertebrates coincided with the acquisition of high-affinity binding of halogenated and polynuclear aromatic hydrocarbons and the emergence of adaptive functions involving regulation of xenobiotic-metabolizing enzymes and roles in adaptive immunity. The existence of multiple AHRs may have facilitated subfunction partitioning and specialization of specific AHR types in some taxa. Additional research in diverse model and non-model species will continue to enrich our understanding of AHR and its pleiotropic roles in biology and toxicology.

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Crossref · 10.1016/j.cotox.2017.02.003

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  • Differences in receptor size, affinity, sensitivity, and stability have been used to support the idea that the AHR is an evolutionarily malleable molecule that adapts to different chemical environments.

    “These differences in receptor size, affinity, sensitivity, and stability have been used to support the idea that the AHR is an evolutionarily malleable molecule that adapts to different chemical environments (M. S. Denison & Nagy, 2003; M. E. Hahn, 2002; Mark E. Hahn et al., 2017).”

    From Rodent Genetic Models of Ah Receptor Signaling (2021) · cites this paper as Mark E. Hahn et al., 2017

    The Conclusions (section 6; page not provided) describe substantial AHR diversification and link vertebrate adaptive functions to the acquisition of high-affinity ligand binding. Section 5 also describes differences in ligand specificity among AHRs. The copy does not establish receptor size or stability differences as evidence for adaptation to different chemical environments. (LLM, conf=0.85)

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Research works printed but not linked: 7

  1. [1]Poland A Glover E Kende AS Stereospecific, high-affinity binding of 2,3,7,8-tetrachlorodibenzo-p-dioxin by hepatic cytosol J Biol Chem 1976 251 4936 4946 956169
  2. [32]Powell-Coffman JA Qin H Chapter 28. Invertebrate AHR homologs: Ancestral functions in sensory systems The Ah receptor in Biology and Toxicology Pohjanvirta R John Wiley & Sons, Inc 2012 405 411
  3. Butler RB Kelley ML Powell WH Hahn ME Van Beneden RJ An aryl hydrocarbon receptor homologue from the soft-shell clam, Mya arenaria: Evidence that invertebrate AHR homologues lack TCDD and BNF binding Gene 2001 278 223 234 This paper demonstrated the inability of invertebrate AHRs (arthropods, nematodes, and molluscs) to bind typical AHR ligands TCDD and β-naphthoflavone 11707340
  4. [41]Dong PD Dicks JS Panganiban G Distal-less and homothorax regulate multiple targets to pattern the Drosophila antenna Development 2002 129 1967 1974 11934862
  5. [49]Crews ST Brenman JE Spineless provides a little backbone for dendritic morphogenesis Genes Dev 2006 20 2773 2778 17043306
  6. [74]Merson RR Mattingly CJ Planchart AJ Tandem duplication of aryl hydrocarbon receptor (AHR) genes in the genome of the spiny dogfish shark (Squalus acanthias) Bulletin of the Mount Desert Island Biological Laboratory 2009 48 43 44
  7. [103]Petersen SL Curran MA Marconi SA Carpenter CD Lubbers LS McAbee MD Distribution of mRNAs encoding the arylhydrocarbon receptor, arylhydrocarbon receptor nuclear translocator, and arylhydrocarbon receptor nuclear translocator-2 in the rat brain and brainstem J Comp Neurol 2000 427 428 439 11054704

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Authors
Hahn, M. E., Karchner, S. I., & Merson, R. R.
Affiliations
  • Woods Hole Oceanographic Institution (US)
  • Rhode Island College (US)
Corresponding author
Hahn, Mark E.
Venue
Current Opinion in Toxicology
Publisher
Elsevier BV
Published
2017-02
Volume
2
Pages
58-71
ISSN
2468-2020 (ISSN-L)
OpenAlex
W2588953202
Cited by
134
References
149
Citations by year
2026: 11 · 2025: 16 · 2024: 16 · 2023: 23 · 2022: 10 · 2021: 12 · 2020: 13 · 2019: 13 · 2018: 14 · 2017: 6
FWCI
1.31
Type
journal article
Language
en
Open access
Locations
  • Current Opinion in Toxicology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • Digital Commons (Providence College) (submittedVersion)
  • Open Access Server of the Woods Hole Scientific Community (Woods Hole Scientific Community) (submittedVersion)
Funders
  • National Institute of Environmental Health Sciences (R01ES006272, P42ES007381)
  • Andrew W. Mellon Foundation Endowed Fund for Innovative Research
  • NIH National Center for Research Resources (P20RR016457)
  • National Science Foundation EPSCoR Cooperative Agreement
  • ME-INBRE (P20RR016463)
  • NIEHS (P30ES003828)
Topics
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Toxic Organic Pollutants Impact
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
Keywords
aryl hydrocarbon receptor, Eumetazoa, Cnidaria, placozoans, gene duplication, xenobiotic metabolism, adaptive immunity, polycyclic aromatic hydrocarbons, halogenated compounds

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