Cytochrome P450 1A, 1B, and 1C mRNA induction patterns in three-spined stickleback exposed to a transient and a persistent inducer

Comparative Biochemistry and Physiology - C Toxicology and Pharmacology

Volumn 154, Issue 1, 2011, Pages 42-55

  Gao, Kai ^a   Brandt, Ingvar ^a   Goldstone, Jared V ^b   Jönsson, Maria E ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

Author keywords

Biomarkers; CYP1A gene; CYP1B gene; CYP1C gene; Cytochrome P450 1A; Cytochrome P450 1B; Cytochrome P450 1C; Gill EROD activity; Indigo; PCB 126; Three spined stickleback

Indexed keywords

3,3',4,4',5 PENTACHLOROBIPHENYL; CYTOCHROME P450; CYTOCHROME P450 1A; CYTOCHROME P450 1B; CYTOCHROME P450 1C; DIOXIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BRAIN; GILL; KIDNEY; LIVER; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; ZEBRA FISH;

DANIO RERIO; GASTEROSTEUS ACULEATUS;

EID: 79955472743     PISSN: 15320456     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpc.2011.02.005     Document Type: Article

References (67)

1. J. Adachi, Y. Mori, S. Matsui, H. Takigami, J. Fujino, H. Kitagawa, C. Miller Iii, T. Kato, K. Saeki, and T. Matsuda Indirubin and indigo are potent aryl hydrocarbon receptor ligands present in human urine J. Biol. Chem. 276 2001 31475 31478
2. J. Adachi, Y. Mori, S. Matsui, and T. Matsuda Comparison of gene expression patterns between 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin and a natural arylhydrocarbon receptor ligand, indirubin Toxicol. Sci. 80 2004 161 169 (Pubitemid 38967407)
3. T. Andersson, and P. Pärt Benzo (a) pyrene metabolism in isolated perfused rainbow trout gills Mar. Environ. Res. 28 1989 3 7 (Pubitemid 20221462)
4. C. Andersson, I. Katsiadaki, K. Lundstedt-Enkel, and J. Örberg Effects of 17α-ethynylestradiol on EROD activity, spiggin and vitellogenin in three-spined stickleback (Gasterosteus aculeatus) Aquat. Toxicol. 83 2007 33 42 (Pubitemid 46669717)
5. K. Beijer, A. Abrahamson, B. Brunström, and I. Brandt CYP1A inhibition in fish gill filaments: a novel assay applied on pharmaceuticals and other chemicals Aquat. Toxicol. 96 2010 145 150
6. C. Björkblom, P.E. Olsson, I. Katsiadaki, and T. Wiklund Estrogen- and androgen-sensitive bioassays based on primary cell and tissue slice cultures from three-spined stickleback (Gasterosteus aculeatus) Comp. Biochem. Physiol. C Toxicol. Pharmacol. 146 2007 431 442 (Pubitemid 47127018)
7. T. Bucheli, and K. Fent Induction of cytochrome P450 as a biomarker for environmental contamination in aquatic ecosystems Crit. Rev. Environ. Sci. Technol. 25 1995 201 268
8. D. Chambers, L. Wilson, M. Maden, and A. Lumsden RALDH-independent generation of retinoic acid during vertebrate embryogenesis by CYP1B1 Development 134 2007 1369 1383 (Pubitemid 46706043)
9. C.R. Chiaro, R.D. Patel, C.B. Marcus, and G.H. Perdew Evidence for an aryl hydrocarbon receptor-mediated cytochrome p450 autoregulatory pathway Mol. Pharmacol. 72 2007 1369 1379 (Pubitemid 350012610)
10. D. Choudhary, I. Jansson, I. Stoilov, M. Sarfarazi, and J. Schenkman Expression patterns of mouse and human CYP orthologs (families 1-4) during development and in different adult tissues Arch. Biochem. Biophys. 436 2005 50 61 (Pubitemid 40332424)
11. D. Choudhary, I. Jansson, K. Rezaul, D.K. Han, M. Sarfarazi, and J.B. Schenkman Cyp1b1 protein in the mouse eye during development: an immunohistochemical study Drug Metab. Dispos. 35 2007 987 994 (Pubitemid 46798609)
12. Y.-W. Chung-Davidson, C.B. Rees, H. Wu, S.-S. Yun, and W. Li {beta}-naphthoflavone induction of CYP1A in brain of juvenile lake trout (Salvelinus namaycush Walbaum) J. Exp. Biol. 207 2004 1533 1542 (Pubitemid 38571988)
13. A. Conney Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons: GHA Clowes Memorial Lecture Cancer Res. 42 1982 4875 4917 (Pubitemid 13223122)
14. M. Denison, and S. Nagy Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals Annu. Rev. Pharmacol. Toxicol. 43 2003 309 334 (Pubitemid 37372644)
15. M.S. Denison, A. Pandini, S.R. Nagy, E.P. Baldwin, and L. Bonati Ligand binding and activation of the Ah receptor Chem. Biol. Interact. 141 2002 3 24 (Pubitemid 35229988)
16. H.V. Gelboin Benzo[alpha]pyrene metabolism, activation and carcinogenesis: role and regulation of mixed-function oxidases and related enzymes Physiol. Rev. 60 1980 1107 1166
17. F. Geoghegan, I. Katsiadaki, T. Williams, and J. Chipman A cDNA microarray for the three spined stickleback, Gasterosteus aculeatus L., and analysis of the interactive effects of oestradiol and dibenzanthracene exposures J. Fish Biol. 72 2008 2133 2153 (Pubitemid 351814259)
18. C. Godard, J. Goldstone, M. Said, R. Dickerson, B. Woodin, and J. Stegeman The new vertebrate CYP1C family: cloning of new subfamily members and phylogenetic analysis Biochem. Biophys. Res. Commun. 331 2005 1016 1024 (Pubitemid 40692462)
19. J.V. Goldstone, and J.J. Stegeman Gene structure of the novel cytochrome P4501D1 genes in stickleback (Gasterosteus aculeatus) and medaka (Oryzias latipes) Mar. Environ. Res. 66 2008 19 20
20. J. Goldstone, H. Goldstone, A. Morrison, A. Tarrant, S. Kern, B. Woodin, and J. Stegeman 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 2007 2619 2631
21. J.V. Goldstone, M.E. Jönsson, L. Behrendt, B.R. Woodin, M.J. Jenny, D.R. Nelson, and J.J. Stegeman Cytochrome P450 1D1: a novel CYP1A-related gene that is not transcriptionally activated by PCB126 or TCDD Arch. Biochem. Biophys. 482 2009 7 16
22. L. Granberg, A. Östergren, I. Brandt, and E. Brittebo CYP1A1 and CYP1B1 in blood-brain interfaces: CYP1A1-dependent bioactivation of 7, 12-dimethylbenz (a) anthracene in endothelial cells Drug Metab. Dispos. 31 2003 259 265 (Pubitemid 36249679)
23. R.M. Green, N.J. Hodges, J.K. Chipman, M.R. O'Donovan, and M. Graham Reactive oxygen species from the uncoupling of human cytochrome P450 1B1 may contribute to the carcinogenicity of dioxin-like polychlorinated biphenyls Mutagenesis 23 2008 457 463
24. F.E. Grubbs Procedures for detecting outlying observations in samples Technometrics 11 1969 1 21
25. F.P. Guengerich, M. Martin, W. McCormick, L. Nguyen, E. Glover, and C. Bradfield Aryl hydrocarbon receptor response to indigoids in vitro and in vivo Arch. Biochem. Biophys. 423 2004 309 316 (Pubitemid 38328440)
26. T.A. Hall BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucleic Acids Symp. Ser. 41 1999 95 98
27. R. Hoessel, S. Leclerc, J. Endicott, M. Nobel, A. Lawrie, P. Tunnah, M. Leost, E. Damiens, D. Marie, and D. Marko Indirubin, the active constituent of a Chinese antileukaemia medicine, inhibits cyclin-dependent kinases Nat. Cell Biol. 1 1999 60 67 (Pubitemid 129495012)
28. M. Hou, G.L. Baughman, and T.A. Perenich Estimation of water solubility and octanol/water partition coefficient of hydrophobic dyes: Part II: Reverse-phase high performance liquid chromatography Dyes Pigm. 16 1991 291 297 (Pubitemid 21712190)
29. W. Hu, C. Sorrentino, M.S. Denison, K. Kolaja, and M.R. Fielden Induction of cyp1a1 is a nonspecific biomarker of aryl hydrocarbon receptor activation: results of large scale screening of pharmaceuticals and toxicants in vivo and in vitro Mol. Pharmacol. 71 2007 1475 1486 (Pubitemid 47010900)
30. Y. Ishikawa Medakafish as a model system for vertebrate developmental genetics Bioessays 22 2000 487 495 (Pubitemid 30308275)
31. E. Jönsson, I. Brandt, and B. Brunström Gill filament-based EROD assay for monitoring waterborne dioxin-like pollutants in fish Environ. Sci. Technol. 36 2002 3340 3344 (Pubitemid 34847604)
32. E. Jönsson, A. Abrahamson, B. Brunström, and I. Brandt Cytochrome P4501A induction in rainbow trout gills and liver following exposure to waterborne indigo, benzo [a] pyrene and 3, 3, 4, 4, 5-pentachlorobiphenyl Aquat. Toxicol. 79 2006 226 232 (Pubitemid 44279080)
33. M.E. Jönsson, M. Jenny, B. Woodin, M. Hahn, and J. Stegeman 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 2007 180 193 (Pubitemid 47617815)
34. M.E. Jönsson, R. Orrego, B. Woodin, J. Goldstone, and J. Stegeman Basal and 3, 3′, 4, 4′, 5-pentachlorobiphenyl-induced expression of cytochrome P450 1A, 1B and 1C genes in zebrafish Toxicol. Appl. Pharmacol. 221 2007 29 41 (Pubitemid 46702278)
35. M.E. Jönsson, D.G. Franks, B.R. Woodin, M.J. Jenny, R.A. Garrick, L. Behrendt, M.E. Hahn, and J.J. Stegeman 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. 181 2009 447 454
36. M.E. Jönsson, K. Gao, J.A. Olsson, J.V. Goldstone, and I. Brandt Induction patterns of new CYP1 genes in environmentally exposed rainbow trout Aquat. Toxicol. 98 2010 311 321
37. M.E. Jönsson, C. Berg, J.V. Goldstone, and J.J. Stegeman New CYP1 genes in the frog Xenopus (Silurana) tropicalis: induction patterns and effects of AHR agonists during development Toxicol. Appl. Pharmacol. 250 2011 170 183
38. I. Katsiadaki, A. Scott, and I. Mayer The potential of the three-spined stickleback (Gasterosteus aculeatus L.) as a combined biomarker for oestrogens and androgens in European waters Mar. Environ. Res. 54 2002 725 728 (Pubitemid 35286502)
39. X.Q. Kong, D. Shea, R.E. Baynes, J.E. Riviere, and X.-R. Xia Regression method of the hydrophobicity ruler approach for determining octanol/water partition coefficients of very hydrophobic compounds Chemosphere 66 2007 1086 1093 (Pubitemid 44792210)
40. M.J. Leaver, and S.G. George A cytochrome P4501B gene from a fish, Pleuronectes platessa Gene 256 2000 83 91
41. D. Lewis, E. Gillam, S. Everett, and T. Shimada Molecular modelling of human CYP1B1 substrate interactions and investigation of allelic variant effects on metabolism Chem. Biol. Interact. 145 2003 281 295 (Pubitemid 36549112)
42. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(- delta delta C(T)) method Methods 25 2001 402 408 (Pubitemid 34164012)
43. P.K. Mandal Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 175 2005 221 230 (Pubitemid 40764087)
44. G.I. Murray, M.C. Taylor, M.C. McFadyen, J.A. McKay, W.F. Greenlee, M.D. Burke, and W.T. Melvin Tumor-specific expression of cytochrome P450 CYP1B1 Cancer Res. 57 1997 3026 3031 (Pubitemid 27315056)
45. C. Ramakers, J. Ruijter, R. Deprez, and A. Moorman Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data Neurosci. Lett. 339 2003 62 66 (Pubitemid 36263221)
46. A. Rannug, U. Rannug, H. Rosenkranz, L. Winqvist, R. Westerholm, E. Agurell, and A. Grafström Certain photooxidized derivatives of tryptophan bind with very high affinity to the Ah receptor and are likely to be endogenous signal substances J. Biol. Chem. 262 1987 15422 15427
47. J. Ruijter, C. Ramakers, W. Hoogaars, Y. Karlen, O. Bakker, M. van den Hoff, and A. Moorman Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data Nucleic Acids Res. 37 2009 e45
48. W. Sanchez, S. Ait-Aissa, O. Palluel, J.M. Ditche, and J.M. Porcher Preliminary investigation of multi-biomarker responses in three-spined stickleback (Gasterosteus aculeatus L.) sampled in contaminated streams Ecotoxicology 16 2007 279 287 (Pubitemid 46295254)
49. W. Sanchez, B. Piccini, J. Ditche, and J. Porcher Assessment of seasonal variability of biomarkers in three-spined stickleback (Gasterosteus aculeatus L.) from a low contaminated stream: implication for environmental biomonitoring Environ. Int. 34 2008 791 798
50. J. Schlezinger, and J. Stegeman Induction and suppression of cytochrome P450 1A by 3, 3, 4, 4, 5-pentachlorobiphenyl and its relationship to oxidative stress in the marine fish scup (Stenotomus chrysops) Aquat. Toxicol. 52 2001 101 115 (Pubitemid 32063385)
51. T. Schmittgen, and K. Livak Analyzing real-time PCR data by the comparative CT method Nat. Protoc. 3 2008 1101 1108 (Pubitemid 351818697)
52. M.L. Scornaienchi, C. Thornton, K.L. Willett, and J.Y. Wilson Functional differences in the cytochrome P450 1 family enzymes from zebrafish (Danio rerio) using heterologously expressed proteins Arch. Biochem. Biophys. 502 2010 17 22
53. T. Shimada, and Y. Fujii-Kuriyama Metabolic activation of polycyclic aromatic hydrocarbons to carcinogens by cytochromes P450 1A1 and1B1 Cancer Sci. 95 2004 1 6 (Pubitemid 38208399)
54. R. Smolowitz, M. Schultz, and J. Stegeman Cytochrome P4501A induction in tissues, including olfactory epithelium, of topminnows (Poeciliopsis spp.) by waterborne benzo [a] pyrene Carcinogenesis 13 1992 2395 2402 (Pubitemid 23022987)
55. B.C. Spink, M.M. Hussain, B.H. Katz, L. Eisele, and D.C. Spink Transient induction of cytochromes P450 1A1 and 1B1 in MCF-7 human breast cancer cells by indirubin Biochem. Pharmacol. 66 2003 2313 2321 (Pubitemid 37456739)
56. J. Stegeman, B. Woodin, and R. Binder Patterns of benzo [a] pyrene metabolism by varied species, organs, and developmental stages of fish Natl. Cancer Inst. Monogr. 65 1984 371 377 (Pubitemid 14064838)
57. K. Sugihara, S. Kitamura, T. Yamada, T. Okayama, S. Ohta, K. Yamashita, M. Yasuda, Y. Fujii-Kuriyama, K. Saeki, and S. Matsui Aryl hydrocarbon receptor-mediated induction of microsomal drug-metabolizing enzyme activity by indirubin and indigo Biochem. Biophys. Res. Commun. 318 2004 571 578 (Pubitemid 38553817)
58. Y. Uno, S. Uehara, N. Murayama, and H. Yamazaki CYP1D1, pseudogenized in human, is expressed and encodes a functional drug-metabolizing enzyme in cynomolgus monkey Biochem. Pharmacol. 81 2011 442 450
59. L. Wang, B. Scheffler, and K. Willett CYP1C1 messenger RNA expression is inducible by benzo [a] pyrene in Fundulus heteroclitus embryos and adults Toxicol. Sci. 93 2006 331 340 (Pubitemid 44400451)
60. C. Wartman, N. Hogan, L. Hewitt, M. McMaster, M. Landman, S. Taylor, T. Kovacs, and M. van den Heuvel Androgenic effects of a Canadian bleached kraft pulp and paper effluent as assessed using threespine stickleback (Gasterosteus aculeatus) Aquat. Toxicol. 92 2009 131 139
61. J.P. Whitlock Induction of cytochrome p4501A1 Annu. Rev. Pharmacol. Toxicol. 39 1999 103 125
62. J. Whyte, R. Jung, C. Schmitt, and D. Tillitt Ethoxyresorufin-O- deethylase (EROD) activity in fish as a biomarker of chemical exposure CRC Crit. Rev. Toxicol. 30 2000 347 570 (Pubitemid 30636029)
63. T. Williams, H. Wu, E. Santos, J. Ball, I. Katsiadaki, M. Brown, P. Baker, F. Ortega, F. Falciani, and J. Craft Hepatic transcriptomic and metabolomic responses in the stickleback (Gasterosteus aculeatus) exposed to environmentally relevant concentrations of dibenzanthracene Environ. Sci. Technol. 43 2009 6341 6348
64. E. Wincent, N. Amini, S. Luecke, H. Glatt, J. Bergman, C. Crescenzi, A. Rannug, and U. Rannug 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 2009 2690 2696
65. Z. Xiao, Y. Hao, B. Liu, and L. Qian Indirubin and meisoindigo in the treatment of chronic myelogenous leukemia in China Leuk. Lymphoma 43 2002 1763 1768 (Pubitemid 34874008)
66. J. Zanette, M. Jenny, J. Goldstone, B. Woodin, L. Watka, A. Bainy, and J. Stegeman 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 2009 234 243
67. G. ZeRuth, and R. Pollenz Functional analysis of cis-regulatory regions within the dioxin-inducible CYP1A promoter/enhancer region from zebrafish (Danio rerio) Chem. Biol. Interact. 170 2007 100 113 (Pubitemid 47552419)