Identification and expression of aryl hydrocarbon receptors (AhR1 and AhR2) provide insight in an evolutionary context regarding sensitivity of white sturgeon (Acipenser transmontanus) to dioxin-like compounds

Aquatic Toxicology

Volumn 150, Issue , 2014, Pages 27-35

  Doering, Jon A ^a   Wiseman, Steve ^a   Beitel, Shawn C ^a   Giesy, John P ^a,b,c,d   Hecker, Markus ^a,e  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b CITY UNIVERSITY OF HONG KONG   (Hong Kong)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

^d NANJING UNIVERSITY   (China)

^e University of Saskatchewan   (Canada)

Author keywords

Ancient; Beta naphthoflavone; Dioxin; Endangered; PCB

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; ARYL HYDROCARBON RECEPTOR 1; ARYL HYDROCARBON RECEPTOR 2; BETA NAPHTHOFLAVONE; DIOXIN; UNCLASSIFIED DRUG;

AMINO ACID; BIOACCUMULATION; DIOXIN; ENDANGERED SPECIES; FISH; PCB; POLLUTION EXPOSURE; SENSITIVITY ANALYSIS;

AMINO ACID SEQUENCE; AMPHIBIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIRD; CHEMOSENSITIVITY; CONTROLLED STUDY; ECOTOXICOLOGY; ENDANGERED SPECIES; ENVIRONMENTAL EXPOSURE; EVOLUTION; FISH; HEART; JUVENILE ANIMAL; LIGAND BINDING; LIVER; MAMMAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DENSITY; RECEPTOR UPREGULATION; RISK ASSESSMENT; SALMONID; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SPECIES COMPARISON; SPECIES DIFFERENCE; STURGEON; TETRAPOD; TISSUE DISTRIBUTION; TISSUE SPECIFICITY; WHITE STURGEON;

ANCIENT; BETA-NAPHTHOFLAVONE; DIOXIN; ENDANGERED; PCB;

AMINO ACID SEQUENCE; ANIMALS; DIOXINS; FISHES; GENE EXPRESSION REGULATION; LIVER; MOLECULAR SEQUENCE DATA; PHYLOGENY; RECEPTORS, ARYL HYDROCARBON; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; WATER POLLUTANTS, CHEMICAL;

EID: 84896036936     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2014.02.009     Document Type: Article

References (67)

1. Abnet C.C., Tanguay R.L., Hahn M.E., Heideman W., Peterson R.E. Two forms of aryl hydrocarbon receptor type 2 in rainbow trout (Oncorhynchus mykiss). J. Biol. Chem. 1999, 274:15159-15166.
2. Agradi E., Brevini A.L., Bolla M., Baga R., Favetta L.A. Cytochrome P-450 levels and EROD activity in the Adriatic sturgeon (Acipenser naccarii Chondrostei) and its induction by β-naphthoflavone. J. Appl. Ichthyol. 1999, 15:96-98.
3. Andreasen E.A., Spitsbergen J.M., Tanguay R.L., Stegeman J.J., Heideman W., Peterson R.E. Tissue-specific expression of AHR2 ARNT2, and CYP1A in zebrafish embryos and larvae: effects of developmental stage and 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure. Toxicol. Sci. 2002, 68(2):403-419.
4. Bak S.M., Lida M., Hirano M., Iwata H., Kim E.Y. Potencies of red seabream AHR1- and AHR2-mediated transactivation by dioxins: implications of both AHRs in dioxin toxicity. Environ. Sci. Technol. 2013, 47(6):2877-2885.
5. Birnbaum L.S., DeVito M.J. Use of toxic equivalency factors for risk assessment for dioxins and related compounds. Toxicology 1995, 105:391-401.
6. Birstein V.J. Sturgeons and paddlefishes: threatened fishes in need of conservation. Conserv. Biol. 1993, 7:773-787.
7. Birstein V.J., Hanner R., DeSalle R. Phylogeny of the Acipenseriformes: cytogenetic and molecular approaches. Environ. Biol. Fish. 1997, 48(1-4):127-156.
8. Blair J.E., Hedges S.B. Molecular phylogeny and divergence times of deuterostome animals. Molec. Biol. Evol. 2005, 22(11):2275-2284.
9. Clark B.W., Matson C.W., Jung D., Di Giulio R.T. AHR2 mediates cardiac teratogenesis of polycyclic aromatic hydrocarbons and PCB-126 in Atlantic killifish (Fundulus heteroclitus). Aquat. Toxicol. 2010, 99:232-240.
10. Cohen-Barnhouse A.M., Zwiernik M.J., Link J.E., Fitzgerald S.D., Kennedy S.W., Herve J.C., Giesy J.P., Wiseman S., Yang Y., Jones P.D., Yi W., Collins B., Newsted J.L., Kay D., Bursian S.J. Sensitivity of Japanese quail (Coturnix japonica), common pheasant (Phasianus colchicus), and white leghorn chicken (Gallus gallus domesticus) embryos to in ovo exposure to TCDD, PeCDF, and TCDF. Toxicol. Sci. 2011, 119:93-102.
11. Coutant C.C. A riparian habitat hypothesis for successful reproduction of white sturgeon. Rev. Fish. Sci. 2004, 12:23-73.
12. Doering J.A., Wiseman S., Beitel S.C., Tendler B.J., Giesy J.P., Hecker M. Tissue specificity of aryl hydrocarbon receptor (AhR) mediated responses and relative sensitivity of white sturgeon (Acipenser transmontanus) to an AhR agonist. Aquat. Toxicol. 2012, 114-115:125-133.
13. Doering J.A., Giesy J.P., Wiseman S., Hecker M. Predicting the sensitivity of fishes to dioxin-like compounds: possible role of the aryl hydrocarbon receptor (AhR) ligand binding domain. Environ. Sci. Pollut. Res. Int. 2013, 20(3):1219-1224.
14. Dwyer F.J., Hardesty D.K., Henke C.E., Ingersoll C.G., Whites D.W., Augspurger T., Canfield T.J., Mount D.R., Mayer F.L. Assessing contaminant sensitivity of endangered and threatened aquatic species: Part III. Effluent toxicity tests. Arch. Environ. Contam. Toxicol. 2005, 48:174-183.
15. Farmahin R., Wu D., Crump D., Herve J.C., Jones S.P., Hahn M.E., Karchner S.I., Giesy J.P., Bursian S.J., Zwiernik M.J., Kennedy S.W. Sequence and in vitro function of chicken, ring-necked pheasant, and Japanese quail AHR1 predict in vivo sensitivity to dioxins. Environ. Sci. Toxicol. 2012, 46(5):2967-2975.
16. Farmahin R., Manning G.E., Crump D., Wu D., Mundy L.J., Jones S.P., Hahn M.E., Karchner S.I., Giesy J.P., Bursian S.J., Zwiernik M.J., Fredricks T.B., Kennedy S.W. Amino acid sequence of the ligand-binding domain of the aryl hydrocarbon receptor 1 predicts sensitivity of wild birds to effects of dioxin-like compounds. Toxicol. Sci. 2013, 131(1):139-152.
17. Fernandez-Salguero P.M., Hilbert D.M., Rudikoff S., Ward J.M., Gonzalez F.J. Aryl-hydrocarbon receptor-deficient mice are resistant to 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced toxicity. Toxicol. Appl. Pharmacol. 1996, 140(1):173-190.
18. Foster E.P., Drake D., Farlow R. Polychlorinated dibenzo-p-dioxin and polychlorinated dibenzofuran congener profiles in fish, crayfish, and sediment collected near a wood treating facility and a bleached kraft pulp mill. Bull. Environ. Contam. Toxicol. 1999, 62:239-246.
19. Foster E.P., Fitzpatrick M.S., Feist G.W., Schreck C.B., Yates J., Spitsbergen J.M., Heidel J.R. Plasma androgen correlation, EROD induction, reduced condition factor, and the occurance of organochlorine pollutants in reproductively immature white sturgeon (Acipenser transmontanus) from the Columbia River, USA. Arch. Environ. Contam. Toxicol. 2001, 41:182-191.
20. Fraccalvieri D., Soshilov A.A., Karchner S.I., Franks D.G., Pandini A., Bonati L., Hahn M.E., Dension M.S. Comparative analysis of homology models of the ah receptor ligand binding domain: verification of structure-function predictions by site-directed mutagenesis of a non-functional receptor. Biochemistry 2013, 52:714-725.
21. Giesy J.P., Ludwig J.P., Tillitt D.E. Dioxins, dibenzofurans PCBs and colonial, fish-eating water birds. Dioxin and Health 1994, 254-307. Plenum Press, New York. A. Schecter (Ed.).
22. Giesy J.P., Jones P.D., Kannan K., Newstead J.L., Tillitt D.E., Williams L.L. Effects of chronic dietary exposure to environmentally relevant concentrations to 2,3,7,8-tetrachlorodibenzo-p-dioxin on survival, growth, reproduction and biochemical responses of female rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 2002, 59(1-2):35-53.
23. Gisbert E., Williot P. Advances in the larval rearing of Siberian sturgeon. J. Fish. Biol. 2002, 60:1071-1092.
24. Hahn M.E., Karchner S.I., Shapiro M.A., Perera S.A. Molecular evolution of two vertebrate aryl hydrocarbon (dioxin) receptors (AHR1 and AHR2) and the PAS family. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:13743-13748.
25. Hahn M.E., Woodlin B.R., Stegeman J.J., Tillitt D.E. Aryl hydrocarbon receptor function in early vertebrates: inducibility of cytochrome P450 1A in agnathan and elasmobranch fish. Comp. Biochem. Physiol. C 1998, 120:67-75.
26. Hanno K., Oda S., Mitani H. Effects of dioxin isomers on induction of AhRs and CYP1A1 in early developmental stage embryos of medaka (Oryzias latipes). Chemosphere 2010, 78(7):830-839.
27. Hansson M.C., Hahn M.E. Functional properties of the four Atlantic salmon (Salmo salar) aryl hydrocarbon receptor type 2 (AHR2) isoforms. Aquat. Toxicol. 2008, 86:121-130.
28. Head J.A., Hahn M.E., Kennedy S.W. Key amino acids in the aryl hydrocarbon receptor predict dioxin sensitivity in avian species. Environ. Sci. Technol. 2008, 42:7535-7541.
29. Irvine R.L., Schmidt D.C., Hildebrand L.R. Population status of white sturgeon in the lower Columbia River within Canada. Trans. Am. Fish Soc. 2007, 136:1472-1479.
30. Iwata H., Nagahama N., Kim E., Watanabe M.X., Sudo A. Effects of in ovo exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin on hepatic AHR/ARNT-CYP1A signaling pathways in common cormorants (Phalacrocorax carbo). Comp. Biochem. Physiol. C. 2010, 152(2):224-231.
31. Johnson R.D., Tietge J.E., Jensen K.M., Fernandez J.D., Linnum A.L., Lothenbach D.B., Holcombe G.W., Cook P.M., Christ S.A., Lattier D.L., Gordon D.A. Toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin to early life stage brooke trout (Salvelinus fontinalis) following parental dietary exposure. Environ. Toxicol. Chem. 1998, 17(12):2408-2421.
32. Jonsson M.E., Berg C., Goldstone J.V., Stegeman J.J. New CYP1 genes in the frog Xenopus (Silurana) tropicalis: induction patterns and effects of AHR agonists during development. Toxicol. Appl. Pharmacol. 2011, 250:170-183.
33. Karchner S.I., Franks D.G., Hahn M.E. AHR1B, a new functional aryl hydrocarbon receptor in zebrafish: tandem arrangement of ahr1b and ahr2 genes. Biochem. J. 2005, 392:153-161.
34. Karchner S.I., Powell W.H., Hahn M.E. Identification and functional characterization of two highly divergent aryl hydrocarbon receptors (AHR1 and AHR2) in the teleost Fundulus heteroclitus. J. Biol. Chem. 1999, 274(47):33814-33824.
35. Karchner S.I., Franks D.G., Kennedy S.W., Hahn M.E. The molecular basis for differential dioxin sensitivity in birds: role of the aryl hydrocarbon receptor. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:6252-6257.
36. Kawajiri K., Fujii-Kuriyama Y. Cytochrome P450 gene regulation and physiological functions mediated by the aryl hydrocarbon receptor. Arch. Biochem. Biophys. 2007, 464:207-212.
37. Kruse G.O., Scarnecchia D.L. Assessment of bioaccumulated metal and organochlorine compounds in relation to physiological biomarkers in Kootenai River white sturgeon. J. Appl. Ichthyol. 2002, 18:430-438.
38. Kruse G., Webb M. Upper Columbia river white sturgeon contaminant and deformity evaluation and summary, Technical report 2006, Upper Columbia River White Sturgeon Recovery Team Contaminants Sub-Committee, Revelstoke, BC, Canada.
39. Kumar S., Hedges S.B. A molecular timescale for vertebrate evolution. Nature 1998, 392:917-919.
40. Luk'yanenko V.I., Vasil'ev A.S., Luk'yanenko V.V., Khabarov M.V. On the increasing threat of extermination of the unique Caspian sturgeon populations and the urgent measures required to save them. J. Appl. Ichthyol. 1999, 15:99-102.
41. MacDonald D.D., Ikonomou M.G., Rantalaine A., Rogers I.H., Sutherland D., Oostdam J.V. Contaminants in white sturgeon (Acipenser transmontanus) from the upper Fraser River, British Columbia, Canada. Environ. Toxicol. 1997, 16:479-490.
42. Nault R., Kim S., Zacharewski T.R. Comparison of TCDD-elicited genome-wide hepatic gene expression in Sprague-Dawley rats and C57BL/6 mice. Toxicol. Appl. Pharm. 2013, 267(2):184-191.
43. Okey A.B. An aryl hydrocarbon receptor odyssey to the shores of toxicology: the Deichmann Lecture, International Congress of Toxicology-XI. Toxicol. Sci. 2007, 98:5-38.
44. Paragamian V.L., Hansen M.J. Evaluation of recovery goals for endangered white sturgeon in the Kootenai River, Idaho. N. Am. J. Fish. Manag. 2008, 28:463-470.
45. Prasch A.L., Teraoka H., Carney S.A., Dong W., Hiraga T., Stegeman J.J., Heideman W., Peterson R.E. Aryl hydrocarbon receptor 2 mediated 2,3,7,8-tetrachlorodibenzo-p-dioxin developmental toxicity in zebrafish. Toxicol. Sci. 2003, 76(1):138-150.
46. Rigaud C., Couillard C.M., Pellerin J., Legare B., Gonzalez P., Hodson P.V. Relative potency of PCB126 to TCDD for sublethal embryotoxicity in the mummichog (Fundulus heteroclitus). Aquat. Toxicol. 2013, 128-129:203-214.
47. Roy N.K., Walker N., Chambers R.C., Wirgin I. Characterization and expression of cytochrome P4501A in Atlantic sturgeon and shortnose sturgeon experimentally exposed to coplanar PCB 126 and TCDD. Aquat. Toxicol. 2011, 104:23-31.
48. Rozen S., Skaletsky H.J. Primer3 on the WWW for general users and for biologist programmers. Bioinformatics Methods and Protocols: Methods in Molecular Biology 2000, Humana Press, New Jersey, http://fokker.wi.mit.edu/primer3/. S. Krawetz, S. Misener (Eds.).
49. Rytkonen K.T., Vuori K.A., Primmer C.R., Nikinmaa M. Comparison of hypoxia-inducible factor-1 alpha in hypoxia-sensitive and hypoxia-tolerant fish species. Comp. Biochem. Physiol. Part D Genomics Proteomics 2007, 2(2):177-186.
50. Scott W.B., Crossman E.J. Freshwater fishes of Canada. Bulletin 184 1973, Fisheries Research Board of Canada, Ottawa ON.
51. Shimizu Y., Nakatsuru Y., Ichinose M., Takahashi Y., Kume H., Mimura J., Fujii-Kuriyama Y., Ishikawa T. Benzo[a]pyrene carcinogenicity is lost in mice lacking the aryl hydrocarbon receptor. Proc. Natl. Acad. Sci. U. S. A. 2000, 97(2):779-782.
52. Simon P. Processing quantitative real-time RT-PCR data. Bioinformatics 2003, 19:1439-1440.
53. Subramaniam S. The biology workbench - a seamless database and analysis environment for the biologist. Protein 1998, 32:1-2.
54. Tanguay R.L., Abnett C.C., Heideman W., Peterson R.E. Cloning and characterization of the zebrafish (Danio rerio) aryl hydrocarbon receptor. Biochem. Biophys. Acta 1999, 1444:35-48.
55. Tompsett A.R., Wiseman S., Higley E., Giesy J.P., Hecker M. Effects of exposure to 17α-ethynylestradiol during larval development on growth, sexual differentiation, and abundances of transcripts in the liver of the wood frog (Lithobates sylvaticus). Aquat. Toxicol. 2013, 126:42-51.
56. Toomey B.H., Bello S., Hahn M.E., Cantrell S., Wright P., Tillitt D., Di Giulio R.T. TCDD induces apoptotic cell death and cytochrome P4501A expression in developing Fundulus heteroclitus embryos. Aquat. Toxicol. 2001, 53:127-138.
57. Van den Berg M., Birnbaum L., Bosveld A.T.C., Brunstrom B., Cook P., Feeley M., Giesy J.P., Hanberg A., Hasegawa R., Kennedy S.W., Kubiak T., Larsen J.C., van Leeuwen R.X.R., Liem A.K.D., Nolt C., Peterson R.E., Poellinger L., Safe S., Schrenk D., Tillitt D., Tysklind M., Younes M., Waern F., Zacharewski T. Toxic equivalency factors (TEFs) for PCBs, PCDDs PCDFs for human and wildlife. Environ. Health Perspect. 1998, 106:775-792.
58. Van Tiem L.A., Di Giulio R.T. AHR2 knockdown prevents PAH-mediated cardiac toxicity and XRE- and ARE-associated gene induction in zebrafish (Danio rerio). Toxicol. Appl. Pharmacol. 2011, 254(3):280-287.
59. Vardy D.W., Tompsett A.R., Sigurdson J.L., Doering J.A., Zhang X., Giesy J.P., Hecker M. Effects of subchronic exposure of early life stages of white sturgeon (Acipenser transmontanus) to copper, cadmium, and zinc. Environ. Toxicol. Chem. 2011, 30:2487-2505.
60. Vardy D.W., Oellers J., Doering J.A., Hollert H., Giesy J.P., Hecker M. Sensitivity of early life stages of white sturgeon, rainbow trout, and fathead minnow to copper. Ecotoxicology 2012, 22(1):139-147.
61. Walker M.K., Spitsbergen J.M., Olson J.R., Peterson R.E. 2,3,7,8-tetrachlorodibenzo-para-dioxin (TCDD) toxicity during early life stage development of lake trout (Salvelinus namaycush). Can. J. Fish. Aquat. Sci. 1991, 48:875-883.
62. Wilimovsky N.J. Protoscaphirhyncus squamosus, a new sturgeon from the Upper Cretaceous of Montana. J. Paleontol. 1956, 30:1205-1208.
63. Wiseman S.B., Vijayan M.M. Aryl hydrocarbon receptor signaling in rainbow trout hepatocytes: role of hsp90 and the proteasome. Comp. Biochem. Physiol. C 2007, 146:484-491.
64. Wiseman S.B., Yuhe H., Gamal-El Din M., Martin J.W., Jones P.D., Hecker M., Giesy J.P. Transcriptional responses of male fathead minnows exposed to oil sands process-affected water. Comp. Biochem. Physiol. Part C 2013, 157:227-235.
65. Wisk J.D., Cooper K.R. The stage specific toxicity of 2,3,7,8-tetrachlordibenzo-p-dioxin in embryos of the Japanese Medakafish (Oryzias latipes). Environ. Toxicol. Chem. 1990, 9:1159-1169.
66. Yamauchi M., Kim E.Y., Iwata H., Shima Y., Tanabe S. Toxic effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in developing red seabream (Pagrus major) embryos: an association of morphological deformities with AHR1, AHR2 and CYP1A expressions. Aquat. Toxicol. 2006, 16:166-179.
67. Yasui T., Kim E.Y., Iawata H., Franks D.G., Karchner S.I., Hahn M.E., Tanabe S. Functional characterization and evolutionary history of two aryl hydrocarbon receptor isoforms (AhR1 and AhR2) from avian species. Toxicol. Sci. 2007, 99(1):101-117.