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Aryl hydrocarbon receptor (AHR) in the cnidarian Nematostella vectensis: comparative expression, protein interactions, and ligand binding

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Abstract

The aryl hydrocarbon receptor (AHR) is a member of the basic helix-loop-helix/Per-ARNT-Sim (bHLH-PAS) family of transcription factors and has diverse roles in development, physiology, and environmental sensing in bilaterian animals. Studying the expression of conserved genes and function of proteins in outgroups to protostomes and deuterostomes assists in understanding the antiquity of gene function and deciphering lineage-specific differences in these bilaterian clades. We describe the developmental expression of AHR from the sea anemone Nematostella vectensis and compare its expression with three other members of the bHLH-PAS family (AHR nuclear translocator (ARNT), Cycle, and a proto-Single-Minded/Trachealess). NvAHR expression was highest early in the larval stage with spatial expression in the basal portion of the ectoderm that became increasingly restricted to the oral pole with concentrated expression in tentacles of the juvenile polyp. The other bHLH-PAS genes showed a divergent expression pattern in later larval stages and polyps, in which gene expression was concentrated in the aboral end, with broader expression in the endoderm later in development. In co-immunoprecipitation assays, we found no evidence for heterodimerization of AHR with ARNT, contrary to the conservation of this specific interaction in all bilaterians studied to date. Similar to results with other invertebrate AHRs but in contrast to vertebrate AHRs, NvAHR failed to bind two prototypical xenobiotic AHR ligands (2,3,7,8-tetrachlorodibenzo-p-dioxin, β-naphthoflavone). Together, our data suggest that AHR’s original function in Eumetazoa likely involved developmental patterning, potentially of neural tissue. The role of heterodimerization in the function of AHR may have arisen after the cnidarian–bilaterian ancestor. The absence of xenobiotic binding to NvAHR further supports a hypothesis for a derived role of this protein in chemical sensing within the chordates.

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Notes

  1. N. vectensis AHR paralogs are annotated as NvAHRa and NvAHRb to avoid confusion with the numerical annotation of vertebrate AHR paralogs (e.g., AHR1 and AHR2), which resulted from independent duplication events.

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Acknowledgments

This research was supported by Award Number F32HD062178 from the Eunice Kennedy Shriver National Institute of Child Health & Human Development to AMR, the Tropical Research Initiative of the Woods Hole Oceanographic Institution and National Science Foundation Award Number MCB1057354 to AMT, and by Award Number R01ES006272 from the National Institute of Environmental Health Sciences to MEH. AMR was also supported by incentive funds provided by the University of North Carolina at Charlotte.

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Authors and Affiliations

  1. Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USA

    Adam M. Reitzel, Sibel I. Karchner, Diana G. Franks, Ann M. Tarrant & Mark E. Hahn

  2. Department of Biology, University of North Carolina at Charlotte, Charlotte, NC, USA

    Adam M. Reitzel

  3. Kewalo Marine Laboratory, Pacific Biosciences Research Center, University of Hawaii, Honolulu, HI, USA

    Yale J. Passamaneck

  4. Whitney Laboratory for Marine Bioscience, St. Augustine, FL, USA

    Mark Q. Martindale

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  1. Adam M. Reitzel
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  2. Yale J. Passamaneck
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  3. Sibel I. Karchner
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Correspondence to Adam M. Reitzel.

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Reitzel, A.M., Passamaneck, Y.J., Karchner, S.I. et al. Aryl hydrocarbon receptor (AHR) in the cnidarian Nematostella vectensis: comparative expression, protein interactions, and ligand binding. Dev Genes Evol 224, 13–24 (2014). https://doi.org/10.1007/s00427-013-0458-4

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