AHR2 mutant reveals functional diversity of aryl hydrocarbon receptors in zebrafish

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Goodale, Britton C ^a   la Du, Jane K ^a   Bisson, William H ^b   Janszen, Derek B ^c   Waters, Katrina M ^c   Tanguay, Robert L ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; AROMATIC HYDROCARBON RECEPTOR 1A; AROMATIC HYDROCARBON RECEPTOR 1B; AROMATIC HYDROCARBON RECEPTOR 2; CYTOCHROME P450 1A; LEFLUNOMIDE; MESSENGER RNA; MUTANT PROTEIN; UNCLASSIFIED DRUG; AHR2 PROTEIN, ZEBRAFISH; ISOPROTEIN; ISOXAZOLE DERIVATIVE; LIGAND; UNSPECIFIC MONOOXYGENASE; ZEBRAFISH PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COMPUTER MODEL; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMBRYO; EMBRYOTOXICITY; ENZYME INDUCTION; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; LIGAND BINDING; MOLECULAR DOCKING; NONHUMAN; PARALOGY; POINT MUTATION; PREDICTION; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PSEUDOGENE; RECEPTOR BINDING; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; ZEBRA FISH; AMINO ACID SEQUENCE; ANIMAL; ANIMAL EMBRYO; BONE; CHEMICAL STRUCTURE; CHEMISTRY; CONGENITAL MALFORMATION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PATHOLOGY; PRENATAL DEVELOPMENT; SKIN; THERMODYNAMICS;

DANIO RERIO;

AMINO ACID SEQUENCE; ANIMALS; ARYL HYDROCARBON HYDROXYLASES; BASE SEQUENCE; BONE AND BONES; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; ISOXAZOLES; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN ISOFORMS; RECEPTORS, ARYL HYDROCARBON; RNA, MESSENGER; SKIN; TETRACHLORODIBENZODIOXIN; THERMODYNAMICS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84855396876     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029346     Document Type: Article

References (59)

1. Fukunaga BN, Probst MR, Reisz-Porszasz S, Hankinson O, (1995) Identification of functional domains of the aryl hydrocarbon receptor. J Biol Chem 270: 29270-29278.
2. Fukunaga BN, Hankinson O, (1996) Identification of a novel domain in the aryl hydrocarbon receptor required for DNA binding. J Biol Chem 271: 3743-3749.
3. Denison MS, Nagy SR, (2003) Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu Rev Pharmacol Toxicol 43: 309-334.
4. Nebert DW, Robinson JR, Niwa A, Kumaki K, Poland AP, (1975) Genetic expression of aryl hydrocarbon hydroxylase activity in the mouse. J Cell Physiol 85: 393-414.
5. Schmidt JV, Bradfield CA, (1996) Ah receptor signaling pathways. Annu Rev Cell Dev Biol 12: 55-89.
6. Nebert DW, Roe AL, Dieter MZ, Solis WA, Yang Y, et al. (2000) Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem Pharmacol 59: 65-85.
7. Sartor MA, Schnekenburger M, Marlowe JL, Reichard JF, Wang Y, et al. (2009) Genomewide analysis of aryl hydrocarbon receptor binding targets reveals an extensive array of gene clusters that control morphogenetic and developmental programs. Environ Health Perspect 117: 1139-1146.
8. Nebert DW, Dalton TP, Okey AB, Gonzalez FJ, (2004) Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J Biol Chem 279: 23847-23850.
9. Gu YZ, Hogenesch JB, Bradfield CA, (2000) The PAS superfamily: sensors of environmental and developmental signals. Annu Rev Pharmacol Toxicol 40: 519-561.
10. Kerkvliet NI, (2009) AHR-mediated immunomodulation: the role of altered gene transcription. Biochem Pharmacol 77: 746-760.
11. Puga A, Ma C, Marlowe JL, (2009) The aryl hydrocarbon receptor cross-talks with multiple signal transduction pathways. Biochem Pharmacol 77: 713-722.
12. Hahn ME, (2002) Aryl hydrocarbon receptors: diversity and evolution. Chem Biol Interact 141: 131-160.
13. Ema M, Ohe N, Suzuki M, Mimura J, Sogawa K, et al. (1994) Dioxin binding activities of polymorphic forms of mouse and human arylhydrocarbon receptors. J Biol Chem 269: 27337-27343.
14. Wirgin I, Roy NK, Loftus M, Chambers RC, Franks DG, et al. Mechanistic basis of resistance to PCBs in Atlantic tomcod from the Hudson River. Science 331: 1322-1325.
15. Hahn ME, Karchner SI, Evans BR, Franks DG, Merson RR, et al. (2006) Unexpected diversity of aryl hydrocarbon receptors in non-mammalian vertebrates: insights from comparative genomics. J Exp Zool A Comp Exp Biol 305: 693-706.
16. Murray IA, Flaveny CA, Chiaro CR, Sharma AK, Tanos RS, et al. (2011) Suppression of cytokine-mediated complement factor gene expression through selective activation of the Ah receptor with 3′,4′-dimethoxy-alpha-naphthoflavone. Mol Pharmacol 79: 508-519.
17. Bisson WH, Koch DC, O'Donnell EF, Khalil SM, Kerkvliet NI, et al. (2009) Modeling of the aryl hydrocarbon receptor (AhR) ligand binding domain and its utility in virtual ligand screening to predict new AhR ligands. J Med Chem 52: 5635-5641.
18. Billiard SM, Hahn ME, Franks DG, Peterson RE, Bols NC, et al. (2002) Binding of polycyclic aromatic hydrocarbons (PAHs) to teleost aryl hydrocarbon receptors (AHRs). Comp Biochem Physiol B Biochem Mol Biol 133: 55-68.
19. Carney SA, Prasch AL, Heideman W, Peterson RE, (2006) Understanding dioxin developmental toxicity using the zebrafish model. Birth Defects Res A Clin Mol Teratol 76: 7-18.
20. Postlethwait J, Amores A, Cresko W, Singer A, Yan YL, (2004) Subfunction partitioning, the teleost radiation and the annotation of the human genome. Trends Genet 20: 481-490.
21. Andreasen EA, Hahn ME, Heideman W, Peterson RE, Tanguay RL, (2002) The zebrafish (Danio rerio) aryl hydrocarbon receptor type 1 is a novel vertebrate receptor. Mol Pharmacol 62: 234-249.
22. Tanguay RL, Abnet CC, Heideman W, Peterson RE, (1999) Cloning and characterization of the zebrafish (Danio rerio) aryl hydrocarbon receptor. Biochim Biophys Acta 1444: 35-48.
23. Karchner SI, Franks DG, Hahn ME, (2005) AHR1B, a new functional aryl hydrocarbon receptor in zebrafish: tandem arrangement of ahr1b and ahr2 genes. Biochem J 392: 153-161.
24. Antkiewicz DS, Peterson RE, Heideman W, (2006) Blocking expression of AHR2 and ARNT1 in zebrafish larvae protects against cardiac toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Sci 94: 175-182.
25. Prasch AL, Teraoka H, Carney SA, Dong W, Hiraga T, et al. (2003) Aryl hydrocarbon receptor 2 mediates 2,3,7,8-tetrachlorodibenzo-p-dioxin developmental toxicity in zebrafish. Toxicol Sci 76: 138-150.
26. Teraoka H, Dong W, Tsujimoto Y, Iwasa H, Endoh D, et al. (2003) Induction of cytochrome P450 1A is required for circulation failure and edema by 2,3,7,8-tetrachlorodibenzo-p-dioxin in zebrafish. Biochem Biophys Res Commun 304: 223-228.
27. Mathew LK, Andreasen EA, Tanguay RL, (2006) Aryl hydrocarbon receptor activation inhibits regenerative growth. Mol Pharmacol 69: 257-265.
28. Billiard SM, Timme-Laragy AR, Wassenberg DM, Cockman C, Di Giulio RT, (2006) The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons to zebrafish. Toxicol Sci 92: 526-536.
29. Hernandez-Ochoa I, Karman BN, Flaws JA, (2009) The role of the aryl hydrocarbon receptor in the female reproductive system. Biochem Pharmacol 77: 547-559.
30. Singh KP, Casado FL, Opanashuk LA, Gasiewicz TA, (2009) The aryl hydrocarbon receptor has a normal function in the regulation of hematopoietic and other stem/progenitor cell populations. Biochem Pharmacol 77: 577-587.
31. Matsumura F, Puga A, Tohyama C, (2009) Biological functions of the arylhydrocarbon receptor: beyond induction of cytochrome P450s. Introduction to this special issue. Biochem Pharmacol 77: 473.
32. Peterson RE, Theobald HM, Kimmel GL, (1993) Developmental and reproductive toxicity of dioxins and related compounds: cross-species comparisons. Crit Rev Toxicol 23: 283-335.
33. Schmidt JV, Su GH, Reddy JK, Simon MC, Bradfield CA, (1996) Characterization of a murine Ahr null allele: involvement of the Ah receptor in hepatic growth and development. Proc Natl Acad Sci U S A 93: 6731-6736.
34. Fernandez-Salguero P, Pineau T, Hilbert DM, McPhail T, Lee SS, et al. (1995) Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 268: 722-726.
35. Lahvis GP, Pyzalski RW, Glover E, Pitot HC, McElwee MK, et al. (2005) The aryl hydrocarbon receptor is required for developmental closure of the ductus venosus in the neonatal mouse. Mol Pharmacol 67: 714-720.
36. Wittkopp N, Huntzinger E, Weiler C, Sauliere J, Schmidt S, et al. (2009) Nonsense-mediated mRNA decay effectors are essential for zebrafish embryonic development and survival. Mol Cell Biol 29: 3517-3528.
37. Cubbage CC, Mabee PM, (1996) Development of the cranium and paired fins in the zebrafish Danio rerio (Ostariophysi, cyprinidae). Journal of Morphology 229: 121-160.
38. Jonsson ME, Jenny MJ, Woodin BR, Hahn ME, Stegeman JJ, (2007) Role of AHR2 in the expression of novel cytochrome P450 1 family genes, cell cycle genes, and morphological defects in developing zebra fish exposed to 3,3′,4,4′,5-pentachlorobiphenyl or 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Sci 100: 180-193.
39. O'Donnell EF, Saili KS, Koch DC, Kopparapu PR, Farrer D, et al. (2010) The anti-inflammatory drug leflunomide is an agonist of the aryl hydrocarbon receptor. PLoS One 5.
40. Pandini A, Denison MS, Song Y, Soshilov AA, Bonati L, (2007) Structural and functional characterization of the aryl hydrocarbon receptor ligand binding domain by homology modeling and mutational analysis. Biochemistry 46: 696-708.
41. Pandini A, Soshilov AA, Song Y, Zhao J, Bonati L, et al. (2009) Detection of the TCDD binding-fingerprint within the Ah receptor ligand binding domain by structurally driven mutagenesis and functional analysis. Biochemistry 48: 5972-5983.
42. Andreasen EA, Spitsbergen JM, Tanguay RL, Stegeman JJ, Heideman W, et al. (2002) 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 68: 403-419.
43. Carney SA, Peterson RE, Heideman W, (2004) 2,3,7,8-Tetrachlorodibenzo-p-dioxin activation of the aryl hydrocarbon receptor/aryl hydrocarbon receptor nuclear translocator pathway causes developmental toxicity through a CYP1A-independent mechanism in zebrafish. Mol Pharmacol 66: 512-521.
44. Dong PD, Munson CA, Norton W, Crosnier C, Pan X, et al. (2007) Fgf10 regulates hepatopancreatic ductal system patterning and differentiation. Nat Genet 39: 397-402.
45. Abbott BD, Schmid JE, Pitt JA, Buckalew AR, Wood CR, et al. (1999) Adverse reproductive outcomes in the transgenic Ah receptor-deficient mouse. Toxicol Appl Pharmacol 155: 62-70.
46. Incardona JP, Carls MG, Teraoka H, Sloan CA, Collier TK, et al. (2005) Aryl hydrocarbon receptor-independent toxicity of weathered crude oil during fish development. Environ Health Perspect 113: 1755-1762.
47. Incardona JP, Day HL, Collier TK, Scholz NL, (2006) Developmental toxicity of 4-ring polycyclic aromatic hydrocarbons in zebrafish is differentially dependent on AH receptor isoforms and hepatic cytochrome P4501A metabolism. Toxicol Appl Pharmacol 217: 308-321.
48. Incardona JP, Linbo TL, Scholz NL., Cardiac toxicity of 5-ring polycyclic aromatic hydrocarbons is differentially dependent on the aryl hydrocarbon receptor 2 isoform during zebrafish development. Toxicol Appl Pharmacol.
49. Scott JA, Incardona JP, Pelkki K, Shepardson S, Hodson PV, (2011) AhR2-mediated, CYP1A-independent cardiovascular toxicity in zebrafish (Danio rerio) embryos exposed to retene. Aquat Toxicol 101: 165-174.
50. Gonzalez FJ, Fernandez-Salguero P, (1998) The aryl hydrocarbon receptor: studies using the AHR-null mice. Drug Metab Dispos 26: 1194-1198.
51. Wienholds E, van Eeden F, Kosters M, Mudde J, Plasterk RH, et al. (2003) Efficient target-selected mutagenesis in zebrafish. Genome Res 13: 2700-2707.
52. Moens CB, Donn TM, Wolf-Saxon ER, Ma TP, (2008) Reverse genetics in zebrafish by TILLING. Brief Funct Genomic Proteomic 7: 454-459.
53. Reimers MJ, La Du JK, Periera CB, Giovanini J, Tanguay RL, (2006) Ethanol-dependent toxicity in zebrafish is partially attenuated by antioxidants. Neurotoxicol Teratol 28: 497-508.
54. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF, (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.
55. Truong L, Harper SL, Tanguay RL, (2011) Evaluation of embryotoxicity using the zebrafish model. Methods Mol Biol 691: 271-279.
56. Team RDC, editor (2010) R: A language and environment for statistical computing. Vienna, Austria.
57. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
58. Hahn ME, (1998) The aryl hydrocarbon receptor: a comparative perspective. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 121: 23-53.
59. Jonsson ME, Franks DG, Woodin BR, Jenny MJ, Garrick RA, et al. (2009) The tryptophan photoproduct 6-formylindolo[3,2-b]carbazole (FICZ) binds multiple AHRs and induces multiple CYP1 genes via AHR2 in zebrafish. Chem Biol Interact.