Dioxin Sensitivity-Related Two Critical Amino Acids of Arylhydrocarbon Receptor May Not Correlate with the Taxonomy or Phylogeny in Avian Species

Fujisawa, Nozomi; Kawai, Yusuke; Nakayama, Shouta M.M.; Ikenaka, Yoshinori; Yamamoto, Hiroki; Ishizuka, Mayumi

doi:10.1292/jvms.13-0179

Cited by 5 publications

(7 citation statements)

References 33 publications

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“…Traditional toxicological testing and risk assessment methods assume that related species share similar xenobiotic sensitivities and extrapolate toxicity data from one species to another based on phylogenetic relatedness 43 . Our results lend support to a growing body of evidence that this is likely an imprecise practice for DLCs, given that AHR1 LBD subtypes, which are strong predictors of avian DLC sensitivity 10 , 11 , 13 , do not correspond well with avian phylogeny 9 , 16 . Our study illustrates the value of trait-based approaches to better understand the evolution of factors that affect species sensitivity with application for conservation.…”

Section: Discussionsupporting

confidence: 71%

“…Remarkably, there appears to be little correspondence between the three AHR1 LBD types and phylogeny, particularly for the high sensitivity type 1 group 9,16 . Hwang et al 9 showed that the transactivation potential of a naturally-occurring dioxin was in the order of type 1 > type 2 > type 3 and demonstrated that factors related to the exposure of birds to naturally occurring dioxins, including a species' habitat and diet, may have contributed to the natural selection of the three AHR1 LBD types in avian species during their evolution.…”

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confidence: 99%

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Species traits predict the aryl hydrocarbon receptor 1 (AHR1) subtypes responsible for dioxin sensitivity in birds

Bianchini

Morrissey

2020

Sci Rep

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Differences in avian sensitivity to dioxin-like compounds (DLCs) are directly attributable to the identities of amino acids at two sites within the ligand binding domain (LBD) of the aryl hydrocarbon receptor 1 (AHR1). Recent work suggests that by influencing avian exposure to naturally occurring dioxins, differences in diet, habitat, and migration may have influenced the evolution of three AHR1 LBD genotypes in birds: type 1 (high sensitivity), type 2 (moderate sensitivity), and type 3 (low sensitivity). Using a boosted regression tree (BRT) analysis, we built on previous work by examining the relationship between a comprehensive set of 17 species traits, phylogeny, and the AHR1 LBD across 89 avian species. The 17 traits explained a combined 74% of the model deviance, while phylogenetic relatedness explained only 26%. The strongest predictors of AHR1 LBD were incubation period and habitat type. We found that type 3 birds tended to occupy aquatic habitats, and, uniquely, we also found that type 3 birds tended to have slower developmental rates. We speculate that this reflects higher evolutionary exposure to naturally occurring dioxins in waterbirds and species with K-selected life histories. This study highlights the value of trait-based approaches in helping to understand differing avian species sensitivities to environmental contaminants.

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Section: Discussionsupporting

confidence: 71%

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confidence: 99%

Species traits predict the aryl hydrocarbon receptor 1 (AHR1) subtypes responsible for dioxin sensitivity in birds

Bianchini

Morrissey

2020

Sci Rep

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“…An earlier study demonstrated that the genotype distribution of key amino acids, corresponding to the 324th and 380th amino acid positions of ck AHR1, in avian AHR isoforms could not be predicted from the phylogenetic tree or previously constructed taxonomy 35 . On the other hand, when we investigated the genotype distribution using our larger data set of 113 avian species, certain AHR1 genotypes were dominant in the Neoaves.…”

Section: Discussionmentioning

confidence: 99%

Ecological factors drive natural selection pressure of avian aryl hydrocarbon receptor 1 genotypes

Hwang

Park

Bak

et al. 2016

Sci Rep

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The aryl hydrocarbon receptor (AHR) mediates dioxin toxicities. Several studies have suggested that two amino acid residues corresponding to the 324th and 380th positions in the ligand binding domain (LBD) of the chicken AHR1 (Ile_Ser as high sensitivity, Ile_Ala as moderate sensitivity, and Val_Ala as low sensitivity), could be an important factor determining dioxin sensitivity in avian species. Here, we analyzed the association between ecological factors and AHR1 LBD genotypes of 113 avian species. Cluster analyses showed that 2 major clusters and sub-clusters of the cluster 3 were associated with specific AHR1 genotypes depending on the food, habitat, and migration of the animal. The majority of the species with Ile_Ala type were the Passeriformes, which are omnivorous or herbivorous feeders in the terrestrial environment. The species with Val_Ala type was primarily composed of raptors and waterbirds, which have been exposed to naturally occurring dioxins. An in vitro reporter gene assay revealed that the sensitivity to a natural dioxin, 1,3,7-tribromodibenzo-p-dioxin was in the order of Ile_Ser > Ile_Ala > Val_Ala. These results suggest that ecological factors related to the exposure of natural dioxins contribute to natural selection of the avian AHR1 genotype, which consequently leads to different sensitivity to man-made dioxins.

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“…For example, carnivorous birds or those living in wet habitats tend to possess fewer sensitive aryl hydrocarbon receptors (AhR), which regulate the expression of genes encoding xenobiotic metabolizing enzymes (e.g., UGT1s and CYP1s). Avian AhRs are divided into three genetic types: highly sensitive (Ile-324 and Ser-380), moderately sensitive (Ile-324 and Ala-380), and less sensitive to dioxin (Val-324 and Ala-380) [ 36 , 37 ]. Certain species may have more of the third genetic type because they receive elevated levels of naturally occurring dioxins through the food web in specific habitats or under specific diets [ 38 ].…”

Section: Discussionmentioning

confidence: 99%

The evolution of UDP-glycosyl/glucuronosyltransferase 1E (UGT1E) genes in bird lineages is linked to feeding habits but UGT2 genes is not

et al. 2018

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UDP-glycosyltransferase (UGT) catalyzes the transfer of glycosyl groups (e.g., glucuronic acid) to exogenous or endogenous chemicals and plays an important role in conjugation reactions. In vertebrates, UGT genes are divided into 5 families: UGT1, UGT2, UGT3, UGT5, and UGT8. Among these UGT enzymes, UGT1 and UGT2 enzymes are known to be important xenobiotic metabolizing enzymes in mammals. However, little is known about UGT1 and UGT2 genes in avian species. In this study, we therefore aimed to classify avian UGT1 and UGT2 genes based on their evolutionary relationships. We also investigated the association between UGT molecular evolution and ecological factors, specifically feeding habits, habitat, and migration. By examining the genomes of 43 avian species with differing ecology, we showed that avian UGT1E genes are divided into 6 groups and UGT2 genes into 3 groups. Correlations between UGT gene count and ecological factors suggested that the number of UGT1E genes is decreasing in carnivorous species. Estimates of selection pressure also support the hypothesis that diet influenced avian UGT1E gene evolution, similar to mammalian UGT1A and UGT2B genes.

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Dioxin Sensitivity-Related Two Critical Amino Acids of Arylhydrocarbon Receptor May Not Correlate with the Taxonomy or Phylogeny in Avian Species

Cited by 5 publications

References 33 publications

Species traits predict the aryl hydrocarbon receptor 1 (AHR1) subtypes responsible for dioxin sensitivity in birds

Species traits predict the aryl hydrocarbon receptor 1 (AHR1) subtypes responsible for dioxin sensitivity in birds

Ecological factors drive natural selection pressure of avian aryl hydrocarbon receptor 1 genotypes

The evolution of UDP-glycosyl/glucuronosyltransferase 1E (UGT1E) genes in bird lineages is linked to feeding habits but UGT2 genes is not

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