Cytochrome P450 1 genes in birds: Evolutionary relationships and transcription profiles in chicken and Japanese quail embryos

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Jönsson, Maria E ^a,b   Woodin, Bruce R ^b   Stegeman, John J ^b   Brunström, Björn ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3,3',4,4',5 PENTACHLOROBIPHENYL; AROMATIC HYDROCARBON RECEPTOR; COMPLEMENTARY DNA; CYTOCHROME P450; CYTOCHROME P450 1A4; CYTOCHROME P450 1A5; CYTOCHROME P450 1B1; CYTOCHROME P450 1C1; MESSENGER RNA; UNCLASSIFIED DRUG;

AHR1 GENE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIRD; BRAIN TISSUE; CHICKEN; CONTROLLED STUDY; CYP1B GENE; CYP1C GENE; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; EYE; GENE; GENE DUPLICATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE INDUCTION; GENETIC CONSERVATION; HEART; LAST COMMON ANCESTOR; LIVER PARENCHYMA; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; QUAIL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPECIES DIFFERENCE; SYNTENY; TISSUE DISTRIBUTION; VERTEBRATE;

AMINO ACID SEQUENCE; ANIMALS; ARYL HYDROCARBON HYDROXYLASES; BIOLOGICAL MARKERS; BIRDS; CHICKENS; CLONING, MOLECULAR; COTURNIX; CYTOCHROME P-450 ENZYME SYSTEM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MOLECULAR SEQUENCE DATA; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ARYL HYDROCARBON; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY; TISSUE DISTRIBUTION;

EID: 82555184785     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028257     Document Type: Article

References (63)

1. Choudhary D, Jansson I, Stoilov I, Sarfarazi M, Schenkman JB, (2004) Metabolism of retinoids and arachidonic acid by human and mouse cytochrome P450 1b1. Drug Metab Dispos 32: 840-847.
2. Nebert DW, Dalton TP, (2006) The role of cytochrome P450 enzymes in endogenous signalling pathways and environmental carcinogenesis. Nat Rev Cancer 6: 947-960.
3. Zhou SF, Zhou ZW, Yang LP, Cai JP, (2009) Substrates, inducers, inhibitors and structure-activity relationships of human Cytochrome P450 2C9 and implications in drug development. Curr Med Chem 16: 3480-3675.
4. Nebert DW, Russell DW, (2002) Clinical importance of the cytochromes P450. Lancet 360: 1155-1162.
5. Nebert DW, Karp CL, (2008) Endogenous functions of the aryl hydrocarbon receptor (AHR): intersection of cytochrome P450 1 (CYP1)-metabolized eicosanoids and AHR biology. J Biol Chem 283: 36061-36065.
6. Jönsson ME, Berg C, Goldstone JV, Stegeman JJ, (2011) New CYP1 genes in the frog Xenopus (Silurana) tropicalis: Induction patterns and effects of AHR agonists during development. Toxicol Appl Pharmacol.
7. Jönsson ME, Orrego R, Woodin BR, Goldstone JV, Stegeman JJ, (2007) Basal and 3,3,′4,4′,5-Pentachlorobiphenyl-induced expression of Cytochrome P450 1A, 1B and 1C Genes in Zebrafish. Toxicol Appl Pharmacol 221: 29-41.
8. Chambers D, Wilson L, Maden M, Lumsden A, (2007) RALDH-independent generation of retinoic acid during vertebrate embryogenesis by CYP1B1. Development 134: 1369-1383.
9. Gilday D, Bellward GD, Sanderson JT, Janz DM, Rifkind AB, (1998) 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) induces hepatic cytochrome P450-dependent arachidonic acid epoxygenation in diverse avian orders: regioisomer selectivity and immunochemical comparison of the TCDD-induced P450s to CYP1A4 and 1A5. Toxicol Appl Pharmacol 150: 106-116.
10. Zanette J, Jenny MJ, Goldstone JV, Woodin BR, Watka LA, et al. (2009) New cytochrome P450 1B1, 1C2 and 1D1 genes in the killifish Fundulus heteroclitus: Basal expression and response of five killifish CYP1s to the AHR agonist PCB126. Aquat Toxicol 93: 234-243.
11. Shimada T, Sugie A, Shindo M, Nakajima T, Azuma E, et al. (2003) Tissue-specific induction of cytochromes P450 1A1 and 1B1 by polycyclic aromatic hydrocarbons and polychlorinated biphenyls in engineered C57BL/6J mice of arylhydrocarbon receptor gene. Toxicol Appl Pharmacol 187: 1-10.
12. Uno Y, Uehara S, Murayama N, Yamazaki H, (2011) CYP1D1, pseudogenized in human, is expressed and encodes a functional drug-metabolizing enzyme in cynomolgus monkey. Biochem Pharmacol 81: 442-450.
13. Goldstone JV, Jönsson ME, Behrendt L, Woodin BR, Jenny MJ, et al. (2009) Cytochrome P450 1D1: a novel CYP1A-related gene that is not transcriptionally activated by PCB126 or TCDD. Arch Biochem Biophys 482: 7-16.
14. Brunström B, (1988) Sensitivity of embryos from duck, goose, herring gull, and various chicken breeds to 3,3′,4,4′-tetrachlorobiphenyl. Poultry science 67: 52-57.
15. Head JA, Hahn ME, Kennedy SW, (2008) Key amino acids in the aryl hydrocarbon receptor predict dioxin sensitivity in avian species. Environ Sci Technol 42: 7535-7541.
16. Powell DC, Aulerich RJ, Meadows JC, Tillitt DE, Giesy JP, et al. (1996) Effects of 3,3′,4,4′,5-pentachlorobiphenyl (PCB 126) and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) injected into the yolks of chicken (Gallus domesticus) eggs prior to incubation. Arch Environ Contam Toxicol 31: 404-409.
17. Brunström B, Darnerud PO, (1983) Toxicity and distribution in chick embryos of 3,3′,4,4′-tetrachlorobiphenyl injected into the eggs. Toxicology 27: 103-110.
18. Brunström B, Andersson L, (1988) Toxicity and 7-ethoxyresorufin O-deethylase-inducing potency of coplanar polychlorinated biphenyls (PCBs) in chick embryos. Arch Toxicol 62: 263-266.
19. Brunström B, Halldin K, (1998) EROD induction by environmental contaminants in avian embryo livers. Comp Biochem Physiol C 121: 213-219.
20. Cohen-Barnhouse AM, Zwiernik MJ, Link JE, Fitzgerald SD, Kennedy SW, et al. (2011) 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 119: 93-103.
21. Yang Y, Wiseman S, Cohen-Barnhouse AM, Wan Y, Jones PD, et al. (2010) Effects of in ovo exposure of white leghorn chicken, common pheasant, and Japanese quail to 2,3,7,8-tetrachlorodibenzo-p-dioxin and two chlorinated dibenzofurans on CYP1A induction. Environmental toxicology and chemistry/SETAC 29: 1490-1502.
22. Karchner SI, Franks DG, Kennedy SW, Hahn ME, (2006) The molecular basis for differential dioxin sensitivity in birds: role of the aryl hydrocarbon receptor. Proc Natl Acad Sci U S A 103: 6252-6257.
23. Goldstone HM, Stegeman JJ, (2006) A Revised Evolutionary History of the CYP1A Subfamily: Gene Duplication, Gene Conversion, and Positive Selection. J Mol Evol 62: 708-717.
24. Gilday D, Gannon M, Yutzey K, Bader D, Rifkind AB, (1996) Molecular cloning and expression of two novel avian cytochrome P450 1A enzymes induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin. J Biol Chem 271: 33054-33059.
25. Goldstone JV, Goldstone HM, Morrison AM, Tarrant A, Kern SE, et al. (2007) Cytochrome P450 1 genes in early deuterostomes (tunicates and sea urchins) and vertebrates (chicken and frog): origin and diversification of the CYP1 gene family. Mol Biol Evol 24: 2619-2631.
26. Zeruth G, Pollenz RS, (2007) Functional analysis of cis-regulatory regions within the dioxin-inducible CYP1A promoter/enhancer region from zebrafish (Danio rerio). Chem Biol Interact 170: 100-113.
27. Lee JS, Kim EY, Iwata H, (2009) Dioxin activation of CYP1A5 promoter/enhancer regions from two avian species, common cormorant (Phalacrocorax carbo) and chicken (Gallus gallus): association with aryl hydrocarbon receptor 1 and 2 isoforms. Toxicol Appl Pharmacol 234: 1-13.
28. Kawai Y, Ikenaka Y, Fujita S, Ishizuka M, (2010) The CYP1D subfamily of genes in mammals and other vertebrates. Mamm Genome 21: 320-329.
29. Godard CA, Goldstone JV, Said MR, Dickerson RL, Woodin BR, et al. (2005) The new vertebrate CYP1C family: cloning of new subfamily members and phylogenetic analysis. Biochem Biophys Res Commun 331: 1016-1024.
30. Blair JE, Hedges SB, (2005) Molecular phylogeny and divergence times of deuterostome animals. Mol Biol Evol 22: 2275-2284.
31. Ohno S, (1999) Gene duplication and the uniqueness of vertebrate genomes circa 1970-1999. Semin Cell Dev Biol 10: 517-522.
32. Hackett SJ, Kimball RT, Reddy S, Bowie RC, Braun EL, et al. (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320: 1763-1768.
33. Jönsson 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 zebrafish exposed to 3,3′,4,4′,5-pentachlorobiphenyl or 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Sci 100: 180-193.
34. Jönsson ME, Gao K, Olsson JA, Goldstone JV, Brandt I, (2010) Induction patterns of new CYP1 genes in environmentally exposed rainbow trout. Aquat Toxicol 98: 311-321.
35. Gao K, Brandt I, Goldstone JV, Jönsson ME, (2011) Cytochrome P450 1A, 1B, and 1C mRNA induction patterns in three-spined stickleback exposed to a transient and a persistent inducer. Comp Biochem Physiol C 154: 42-55.
36. Yasui T, Kim EY, Iwata H, Franks DG, Karchner SI, et al. (2007) Functional characterization and evolutionary history of two aryl hydrocarbon receptor isoforms (AhR1 and AhR2) from avian species. Toxicol Sci 99: 101-117.
37. Dey A, Jones JE, Nebert DW, (1999) Tissue- and cell type-specific expression of cytochrome P450 1A1 and cytochrome P450 1A2 mRNA in the mouse localized in situ hybridization. Biochem Pharmacol 58: 525-537.
38. Choudhary D, Jansson I, Stoilov I, Sarfarazi M, Schenkman JB, (2005) Expression patterns of mouse and human CYP orthologs (families 1-4) during development and in different adult tissues. Arch Biochem Biophys 436: 50-61.
39. Choudhary D, Jansson I, Rezaul K, Han DK, Sarfarazi M, et al. (2007) Cyp1b1 protein in the mouse eye during development: An immunohistochemical study. Drug Metab Dispos 35: 987-994.
40. Choudhary D, Jansson I, Sarfarazi M, Schenkman JB, (2006) Physiological significance and expression of P450s in the developing eye. Drug Metab Rev 38: 337-352.
41. Choudhary D, Jansson I, Schenkman JB, Sarfarazi M, Stoilov I, (2003) Comparative expression profiling of 40 mouse cytochrome P450 genes in embryonic and adult tissues. Arch Biochem Biophys 414: 91-100.
42. Chiaro CR, Patel RD, Marcus CB, Perdew GH, (2007) Evidence for an aryl hydrocarbon receptor-mediated cytochrome p450 autoregulatory pathway. Mol Pharmacol 72: 1369-1379.
43. Wei YD, Helleberg H, Rannug U, Rannug A, (1998) Rapid and transient induction of CYP1A1 gene expression in human cells by the tryptophan photoproduct 6-formylindolo(3,2-b)carbazole. Chem-Biol Interact 110: 39-55.
44. Wincent E, Amini N, Luecke S, Glatt H, Bergman J, et al. (2009) The suggested physiologic aryl hydrocarbon receptor activator and cytochrome P4501 substrate 6-formylindolo[3,2-b]carbazole is present in humans. J Biol Chem 284: 2690-2696.
45. 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 305A: 693-706.
46. Poland A, Palen D, Glover E, (1994) Analysis of the four alleles of the murine aryl hydrocarbon receptor. Mol Pharmacol 46: 915-921.
47. Brunström B, Lund J, (1988) Differences between chick and turkey embryos in sensitivity to 3,3′,4,4′-tetrachloro-biphenyl and in concentration/affinity of the hepatic receptor for 2,3,7,8-tetrachlorodibenzo-p-dioxin. Comp Biochem Physiol C 91: 507-512.
48. Lavine JA, Rowatt AJ, Klimova T, Whitington AJ, Dengler E, et al. (2005) Aryl hydrocarbon receptors in the frog Xenopus laevis: two AhR1 paralogs exhibit low affinity for 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol Sci 88: 60-72.
49. Jung RE, Walker MK, (1997) Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on development of anuran amphibians. Environ Toxicol Chem 16: 230-240.
50. Cohen-Barnhouse AM, Zwiernik MJ, Link JE, Fitzgerald SD, Kennedy SW, et al. (2011) Developmental and posthatch effects of in ovo exposure to 2,3,7,8-TCDD, 2,3,4,7,8-PECDF, and 2,3,7,8-TCDF in Japanese quail (Coturnix japonica), common pheasant (Phasianus colchicus), and white leghorn chicken (Gallus gallus domesticus) embryos. Environ Toxicol Chem 30: 1659-1668.
51. Matthews J, Gustafsson JÅ, (2006) Estrogen receptor and aryl hydrocarbon receptor signaling pathways. Nucl Recept Signal 4: e016.
52. Hahn ME, Allan LL, Sherr DH, (2009) Regulation of constitutive and inducible AHR signaling: complex interactions involving the AHR repressor. Biochem Pharmacol 77: 485-497.
53. Hankinson O, (2005) Role of coactivators in transcriptional activation by the aryl hydrocarbon receptor. Arch Biochem Biophys 433: 379-386.
54. Zeruth G, Pollenz RS, (2005) Isolation and characterization of a dioxin-Inducible CYP1A1 promoter/enhancer region from zebrafish (Danio rerio). Zebrafish 2: 197-210.
55. Beedanagari SR, Taylor RT, Bui P, Wang F, Nickerson DW, et al. (2010) Role of epigenetic mechanisms in differential regulation of the dioxin-inducible human CYP1A1 and CYP1B1 genes. Mol Pharmacol 78: 608-616.
56. Hall TA, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95-98.
57. Lewis DF, Gillam EM, Everett SA, Shimada T, (2003) Molecular modelling of human CYP1B1 substrate interactions and investigation of allelic variant effects on metabolism. Chem Biol Interact 145: 281-295.
58. Schmittgen TD, Livak KJ, (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.
59. 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.
60. Ramakers C, Ruijter JM, Deprez RH, Moorman AF, (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339: 62-66.
61. Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, et al. (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37: e45.
62. Grubbs FE, (1969) Procedures for detecting outlying observations in samples. Technometrics 11: 1-21.
63. Hamburger V, Hamilton HL, (1951) A series of normal stages in the development of the chick embryo. Journal of Morphology 88: 49-92.