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An Aryl Hydrocarbon Receptor from the Caecilian Gymnopis multiplicata Suggests Low Dioxin Affinity in the Ancestor of All Three Amphibian Orders

Sarah A. Kazzaz, Sara Giani Tagliabue, Diana G. Franks, Michael S. Denison, Mark E. Hahn, Laura Bonati, View ORCID ProfileWade H. Powell
doi: https://doi.org/10.1101/750653
Sarah A. Kazzaz
1Biology Department, Kenyon College, Gambier, OH 43022 USA
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Sara Giani Tagliabue
2Department of Earth and Environmental Sciences, University of Milano-Bicocca Milan 20126, Italy
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Diana G. Franks
3Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA 02543 USA
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Michael S. Denison
4Department of Environmental Toxicology, University of California-Davis, Davis, CA 95616 USA
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Mark E. Hahn
3Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA 02543 USA
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Laura Bonati
2Department of Earth and Environmental Sciences, University of Milano-Bicocca Milan 20126, Italy
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Wade H. Powell
1Biology Department, Kenyon College, Gambier, OH 43022 USA
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  • ORCID record for Wade H. Powell
  • For correspondence: powellw@kenyon.edu
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Abstract

The aryl hydrocarbon receptor (AHR) plays pleiotropic roles in the development and physiology of vertebrates in conjunction with xenobiotic and endogenous ligands. It is best known for mediating the toxic effects of dioxin-like pollutants such as 2,3,7,8-tetracholordibenzo-p-dioxin (TCDD). While most vertebrates possess at least one AHR that binds TCDD tightly, amphibian AHRs bind TCDD with very low affinity. Previous analyses of AHRs from Xenopus laevis (a frog; order Anura) and Ambystoma mexicanum (a salamander; order Urodela) identified three amino acid residues in the ligand-binding domain (LBD) that underlie low-affinity binding. In X. laevis AHR1β, these are A354, A370, and N325. Here we extend the analysis of amphibian AHRs to the caecilian Gymnopis multiplicata, representing the remaining extant amphibian order, Apoda. G. multiplicata AHR groups with the monophyletic vertebrate AHR/AHR1 clade. The LBD includes all three signature residues of low TCDD affinity, and a structural homology model suggests that its architecture closely resembles those of other amphibians. In transactivation assays, the EC50 for reporter gene induction by TCDD was 17.17 nM, comparable to X. laevis AhR1β (26.23 nM) and Ambystoma AHR (34.09 nM) and dramatically higher than mouse AhR (0.13 nM), a trend generally reflected in direct measures of TCDD binding. These shared properties distinguish amphibian AHRs from the high-affinity proteins typical of both more ancient vertebrate groups (teleost fish) and those that appeared more recently (tetrapods). We suggest that AHRs with low TCDD affinity represent a basal characteristic that evolved in a common ancestor of all three extant amphibian groups.

Research Highlights

  • A caecilian aryl hydrocarbon receptor exhibits low dioxin binding and sensitivity.

  • The protein’s ligand-binding domain resembles frog and salamander AHRs in structure and function.

  • AHR with low dioxin affinity likely evolved in a common ancestor of all three extant amphibian groups.

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Posted September 11, 2019.
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An Aryl Hydrocarbon Receptor from the Caecilian Gymnopis multiplicata Suggests Low Dioxin Affinity in the Ancestor of All Three Amphibian Orders
Sarah A. Kazzaz, Sara Giani Tagliabue, Diana G. Franks, Michael S. Denison, Mark E. Hahn, Laura Bonati, Wade H. Powell
bioRxiv 750653; doi: https://doi.org/10.1101/750653
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An Aryl Hydrocarbon Receptor from the Caecilian Gymnopis multiplicata Suggests Low Dioxin Affinity in the Ancestor of All Three Amphibian Orders
Sarah A. Kazzaz, Sara Giani Tagliabue, Diana G. Franks, Michael S. Denison, Mark E. Hahn, Laura Bonati, Wade H. Powell
bioRxiv 750653; doi: https://doi.org/10.1101/750653

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