Brain transcriptomics in response to β-naphthoflavone treatment in rainbow trout: The role of aryl hydrocarbon receptor signaling

Aquatic Toxicology

Volumn 87, Issue 1, 2008, Pages 1-12

  Aluru, Neelakanteswar ^a   Vijayan, Mathilakath M ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Cortisol; Endocrine disruption; Fish; Heat shock proteins; Neurosteroid; Oncorhynchus mykiss; PCBs; Sex steroids; Steroidogenesis; Stress response

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; BETA NAPHTHOFLAVONE; RESVERATROL;

BRAIN; ENDOCRINE DISRUPTOR; ENVIRONMENTAL STRESS; GENE EXPRESSION; HEAT SHOCK; HYDROCARBON; HYPOTHESIS TESTING; PCB; POLLUTION EXPOSURE; PROTEIN; SALMONID; SIGNALING; STEROID;

ANALYTIC METHOD; ANIMAL EXPERIMENT; ARTICLE; ARYL HYDROCARBON RECEPTOR GENE; BRAIN; CONTROLLED STUDY; CYTOCHROME P450 1A1 GENE; DNA MICROARRAY; DOWN REGULATION; FEMALE; GENE; GENE EXPRESSION; MALE; NEUROENDOCRINE SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAINBOW TROUT; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STEROIDOGENESIS; STRESS; TRANSCRIPTOMICS; UNINDEXED SEQUENCE; UPREGULATION;

ANIMALS; BETA-NAPHTHOFLAVONE; BRAIN; CYTOCHROME P-450 CYP1A1; ENZYME INHIBITORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GONADAL STEROID HORMONES; NEUROSECRETORY SYSTEMS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ONCORHYNCHUS MYKISS; POLYMERASE CHAIN REACTION; RECEPTORS, ARYL HYDROCARBON; SIGNAL TRANSDUCTION; STILBENES; STRESS;

ONCORHYNCHUS MYKISS; SALMONIDAE; TELEOST FISH;

EID: 40849119575     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2007.12.012     Document Type: Article

References (62)

1. Abnet C.C., Tanguay R.L., Hahn M.E., Heideman W., and Peterson R.E. Two forms of aryl hydrocarbon receptor type 2 in rainbow trout (Oncorhynchus mykiss). Evidence for differential expression and enhancer specificity. J. Biol. Chem. 274 (1999) 15159-15166
2. Abnet C.C., Tanguay R.L., Heideman W., and Peterson R.E. Transactivation activity of human, zebrafish, and rainbow trout aryl hydrocarbon receptors expressed in COS-7 cells: greater insight into species differences in toxic potency of polychlorinated dibenzo-p-dioxin, dibenzofuran, and biphenyl congeners. Toxicol. Appl. Pharmacol. 159 (1999) 41-51
3. Adachi J., Mori Y., Matsui S., and Matsuda T. Comparison of gene expression patterns between 2,3,7,8-Tetrachlorodibenzo-p-dioxin and a natural aryl hydrocarbon receptor ligand, indirubin. Toxicol. Sci. 80 (2004) 161-169
4. Aluru N., Jorgensen E.H., Maule A.G., and Vijayan M.M. PCB disruption of the hypothalamus-pituitary-interrenal axis involves brain glucocorticoid receptor downregulation in anadromous arctic charr. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287 (2004) R787-R793
5. Aluru N., Renaud R., Leatherland J.F., and Vijayan M.M. Ah Receptor-mediated impairment of interrenal steroidogenesis involves StAR protein and P450scc gene attenuation in rainbow trout. Toxicol. Sci. 84 (2005) 260-269
6. Aluru N., and Vijayan M.M. β-Naphthoflavone disrupts cortisol production and liver glucocorticoid responsiveness in rainbow trout. Aquat. Toxicol. 67 (2004) 273-285
7. Aluru N., and Vijayan M.M. Aryl hydrocarbon receptor activation impairs cortisol response to stress in rainbow trout by disrupting the rate-limiting steps in steroidogenesis. Endocrinol 147 (2006) 1895-1903
8. Aluru N., and Vijayan M.M. Resveratrol affects CYP1A expression in rainbow trout hepatocytes. Aquat. Toxicol. 77 (2006) 291-297
9. Aluru N., and Vijayan M.M. Hepatic transcriptome response to glucocorticoid receptor activation in rainbow trout. Physiol. Genomics. 31 (2007) 483-491
10. Antkiewicz D.S., Peterson R.E., and Heideman W. Blocking expression of AHR2 and ARNT1 in zebrafish larvae protects against cardiac toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Sci. 94 (2006) 175-182
11. Bookstaff R.C., Kamel F., Moore R.W., Bjerke D.L., and Peterson R.E. Altered regulation of pituitary gonadotropin-releasing hormone (GnRH) receptor number and pituitary responsiveness to GnRH in 2,3,7,8-tetrachlorodibenzo-p-dioxin-treated male rats. Toxicol. Appl. Pharmacol. 105 (1990) 78-92
12. Buhler D.R., and Wang-Buhler J.L. Rainbow trout cytochrome P450s: purification, molecular aspects, metabolic activity, induction and role in environmental monitoring. Comp. Biochem. Physiol. C 121 (1998) 107-137
13. Campagnone N.A., and Mellon S.H. Neurosteroids: biosynthesis and function of these novel neuromodulators. Front. Neuroendocrinol. 21 (2000) 1-56
14. Casper R.F., Quesne M., Rogers I.M., Shirota T., Jolivet A., Milgrom E., and Savouret J.F. Resveratrol has antagonist activity on the aryl hydrocarbon receptor: implications for prevention of dioxin activity. Mol. Pharmacol. 56 (1999) 784-790
15. Cok I., Wang-Buhler J.L., Kedzierski M.M., Miranda C.L., Yang Y.H., and Buhler D.R. Expression of CYP2M1, CYP2K1, and CYP3A27 in brain, blood, small intestine, and other tissues of rainbow trout. Biochem. Biophys. Res. Comm. 244 (1998) 790-795
16. DiBartolomeis M.J., Moore R.W., Peterson R.E., Christian B.J., and Jefcoate C.R. Altered regulation of adrenal steroidogenesis in 2,3,7,8-tetrachlorodibenzo-p-dioxin-treated rats. Biochem. Pharmacol. 36 (1987) 59-67
17. Dong W., Teraoka H., Kondo S., and Hiraga T. 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces apoptosis in the dorsal midbrain of zebrafish embryos by activation of arylhydrocarbon receptor. Neurosci. Lett. 303 (2001) 169-172
18. Doostzadeh J., Cotillon A.C., and Morfin R. Dehydroepiandrosterone 7alpha- and 7beta-hydroxylation in mouse brain micrsomes. Effects of cytochrome P450 inhibitors and structure-specific inhibition by steroid hormones. J. Neuroendocrinol. 9 (1997) 923-928
19. Finne E.F., Cooper G.A., Koop B.F., Hylland K., and Tollefsen K.E. Toxicogenomic responses in rainbow trout (Oncorhynchus mykiss) hepatocytes exposed to model chemicals and a synthetic mixture. Aquat. Toxicol. 81 (2007) 293-303
20. Franklin T.B., Krueger-Naug A.M., Clarke D.B., Arrigo A.P., and Currie R.W. The role of heat shock proteins Hsp70 and Hsp27 in cellular protection of the central nervous system. Int. J. Hyperthermia 21 (2005) 379-392
21. Frueh F.W., Hayashibara K.C., Brown P.O., and Whitlock Jr. J.P. Use of cDNA microarrays to analyze dioxin-induced changes in human liver gene expression. Toxicol. Lett. 122 (2001) 189-203
22. Gao X., Mizuyachi K., Terranova P.F., and Rozman K.K. 2,3,7,8-Tetrachlorodibenzo-p-dioxin decreases responsiveness of the hypothalamus to estradiol as a feedback inducer of preovulatory gonadotropin secretion in the immature gonadotropin-primed rat. Toxicol. Appl. Pharmacol. 170 (2001) 181-190
23. Garcia-Ovejero D., Azcoitia I., Doncarlos L.L., Melcangi R.C., and Garcia-Segura L.M. Glia-neuron crosstalk in the neuroprotective mechanisms of sex steroid hormones. Brain Res. Brain Res. Rev. 48 (2005) 273-286
24. Goksøyr A. Use of cytochrome P450 1A (CYP1A) in fish as a biomarker of aquatic pollution. Arch. Toxicol. Suppl. 17 (1995) 80-95
25. Hahn M.E. Dioxin toxicology and the aryl hydrocarbon receptor: insights from fish and other non-traditional models. Mar. Biotechnol. 3 (2001) S224-S238
26. Hightower L.E. Heat shock, stress proteins, chaperones, and proteotoxicity. Cell 66 (1991) 191-197
27. Hill A., Howard C.V., Strahle U., and Cossins A. Neurodevelopmental defects in zebrafish (Danio rerio) at environmentally relevant dioxin (TCDD) concentrations. Toxicol. Sci. 76 (2003) 392-399
28. Hontela A. Stress and the hypothalamo-pituitary-interrenal axis: adrenal toxicology-effects of environmental pollutants on the structure and function of the HPI axis. In: Moon T.W., and Mommsen T.P. (Eds). Biochemical and Molecular Biology of Fishes, vol. 6 Environmental Toxicology (2005), Elsevier, Amsterdam 331-363
29. Hook S.E., Skillman A.D., Small J.A., and Schultz I.R. Gene expression patterns in rainbow trout, Oncorhynchus mykiss, exposed to a suite of model toxicants. Aquat. Toxicol. 77 (2006) 372-385
30. Jorgensen E.H., Vijayan M.M., Aluru N., and Maule A.G. Fasting modifies Aroclor 1254 impact on plasma cortisol, glucose and lactate responses to a handling disturbance in Arctic charr. Comp. Biochem. Physiol. C 132 (2002) 235-245
31. Khan I.A., and Thomas P. Lead and Aroclor 1254 disrupt reproductive neuroendocrine function in Atlantic croaker. Mar. Environ. Res. 50 (2000) 119-123
32. Krasnov A., Koskinen H., Pehkonen P., Rexroad III C.E., Afanasyev S., and Molsa H. Gene expression in the brain and kidney of rainbow trout in response to handling stress. BMC Genomics 6 (2005) 3
33. Kurachi M., Hashimoto S., Obata A., Nagai S., Nagahata T., Inadera H., Sone H., Tohyama C., Kaneko S., Kobayashi K., and Matsushima K. Identification of 2,3,7,8-Tetrachlorodibenzo-p-dioxin in mouse liver by serial analysis of gene expression. Biochem. Biophys. Res. Commun. 292 (2002) 368-377
34. Li X., Johnson D.C., and Rozman K.K. Reproductive effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in female rats: ovulation, hormonal regulation, and possible mechanism(s). Toxicol. Appl. Pharmacol. 133 (1995) 321-327
35. Miksys S.L., and Tyndale R.F. Drug-metabolizing cytochrome P450s in the brain. J. Psychiatry Neurosci. 27 (2002) 406-415
36. Morale M.C., Gallo F., Tirolo C., Testa N., Caniglia S., Marletta N., Spina-Purrello V., Avola R., Caucci F., Tomasi P., Delitala G., Barden N., and Marchetti B. Neuroendocrine-immune (NEI) circuitry from neuron-glial interactions to function: Focus on gender and HPA-HPG interactions on early programming of the NEI system. Immunol. Cell Biol. 79 (2001) 400-417
37. Moran P.W., Aluru N., Black R.W., and Vijayan M.M. Tissue contaminants and associated transcriptional response in trout liver from remote high elevation lakes of Western Washington. Environ. Sci. Tech. 41 (2007) 6591-6597
38. Mutoh J., Taketoh J., Okamura K., Kagawa T., Ishida T., Ishii Y., and Yamada H. Fetal pituitary gonadotropin as an initial target of dioxin in its impairment of cholesterol transportation and steroidogenesis in rats. Endocrinol 147 (2006) 927-936
39. Myllymaki S.A., Karjalainen M., Haavisto T.E., Toppari J., and Paranko J. Infantile 4-tert-octylphenol exposure transiently inhibits rat ovarian steroidogenesis and steroidogenic acute regulatory protein (StAR) expression. Toxicol. Appl. Pharmacol. 207 (2005) 59-68
40. Nebert D.W., Roe A.L., Dieter M.Z., Solis W.A., Yang Y., and Dalton T.P. Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem. Pharmacol. 59 (2000) 65-85
41. Nicholson T.E., and Renton K.W. Modulation of cytochrome P450 by inflammation in astrocytes. Brain Res. 827 (1999) 12-18
42. Petersen S.L., Krishnan S., and Hudgens E.D. The Aryl hydrocarbon receptor pathway and sexual differentiation of neuroendocrine functions. Endocrinol 147 (2006) S33-S42
43. Picard D. Chaperoning steroid hormone action. Trends Endocrinol. Metab. 17 (2006) 229-235
44. Pocar P., Fischer B., Klonisch T., and Hombach-Klonisch S. Molecular interactions of the aryl hydrocarbon receptor and its biological and toxicological relevance for reproduction. Reproduction 129 (2005) 379-389
45. Pollenz R.S., and Buggy C. Ligand-dependent and -independent degradation of the human aryl hydrocarbon receptor (hAHR) in cell culture models. Chem. Biol. Interact. 164 (2006) 49-59
46. Puga A., Maier A., and Medvedovic M. The transcriptional signature of dioxin in human hepatoma HepG2 cells. Biochem. Pharmacol. 60 (2000) 1129-1142
47. Quabius E.S., Balm P.H., and Wendelaar Bonga S.E. Interrenal stress responsiveness of tilapia (Oreochromis mossambicus) is impaired by dietary exposure to PCB 126. Gen. Comp. Endocrinol. 108 (1997) 472-482
48. Rosenbrock H., Hagemeyer C.E., Singec I., Knoth R., and Volk B. Testosterone metabolism in rat brain is differentially enhanced by phentoin-inducible cytochrome P450 isoforms. J. Neuroendocrinol. 11 (1999) 597-604
49. Saeed A.I., Sharov V., White J., Li J., Liang W., Bhagabati N., Braisted J., Klapa M., Currier T., Thiagarajan M., Sturn A., Snuffin M., Rezantsev A., Popov D., Ryltsov A., Kostukovich E., Borisovsky I., Liu Z., Vinsavich A., Trush V., and Quackenbus J. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34 (2003) 374-378
50. Safe S., Wang F., Porter W., Duan R., and McDougal A. Ah receptor agonists as endocrine disruptors: antiestrogenic activity and mechanisms. Toxicol. Lett. 102/103 (1998) 343-347
51. Salama J., Chakraborty T.R., Ng L., and Gore A.C. Effects of polychlorinated biphenyls on estrogen receptor-beta expression in the anteroventral periventricular nucleus. Environ. Health Perspect. 111 (2003) 1278-1282
52. Slezak B.P., Hatch G.E., DeVito M.J., Diliberto J.J., Slade R., Crissman K., Hassoun E., and Birnbaum L.S. Oxidative stress in female B6C3F1 mice following acute and subchronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol. Sci. 54 (2000) 390-398
53. Sridhar S., Farley A., Reid R.L., Foster W.G., and Van Vugt D.A. The effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on corticotrophin-releasing hormone, arginine vasopressin, and pro-opiomelanocortin mRNA levels in the hypothalamus of the cynomolgus monkey. Toxicol. Sci. 63 (2001) 181-188
54. Stocco D.M., and Clark B.J. Regulation of the acute production of steroids in steroidogenic cells. Endocr. Rev. 17 (1996) 221-244
55. Tijet N., Boutros P.C., Moffat I.D., Okey A.B., Tuomisto J., and Pohjanvirta R. Aryl hydrocarbon receptor regulates distinct dioxin-dependent and dioxin independent gene batteries. Mol. Pharmacol. 69 (2006) 140-153
56. Van der Kraak G.J., Munkittrick K.R., McMaster M.E., Portt C.B., and Chang J.P. Exposure to bleached kraft pulp mill effluent disrupts the pituitary-gonadal axis of white sucker at multiple sites. Toxicol. Appl. Pharmacol. 115 (1992) 224-233
57. van der Ven K., Keil D., Moens L.N., Van Leemput K., van Remortel P., and De Coen W.M. Neuropharmaceuticals in the environment: mianserin-induced neuroendocrine disruption in zebrafish (Danio rerio) using cDNA microarrays. Environ. Toxicol. Chem. 25 (2006) 2645-2652
58. Vijayan M.M., Prunet P., and Boone A.N. Xenobiotic impact on corticosteroid signaling. In: Moon T.W., and Mommsen T.P. (Eds). Biochemical and Molecular Biology of Fishes, vol. 6. Environmental Toxicology (2005), Elsevier, Amsterdam 365-394
59. Volz D.C., Bencic D.C., Hinton D.E., Law J.M., and Kullman S.W. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) induces organ-specific differential gene expression in male Japanese medaka (Oryzias latipes). Toxicol. Sci. 85 (2005) 572-584
60. Wentworth J.N., Buzzeo R., and Pollenz R.S. Functional characterization of aryl hydrocarbon receptor (zfAHR2) localization and degradation in zebrafish (Danio rerio). Biochem. Pharmacol. 67 (2004) 1363-1372
61. Wiseman S., Osachoff H., Bassett E., Malhotra J., Bruno J., VanAggelen G., Mommsen T.P., and Vijayan M.M. Gene expression pattern in the liver during recovery from an acute stressor in rainbow trout. Comp. Biochem. Physiol. D 2 (2007) 234-244
62. Wiseman S.B., and Vijayan M.M. Aryl hydrocarbon receptor signaling in rainbow trout hepatocytes: role of hsp90 and the proteasome. Comp. Biochem. Physiol. C 146 (2007) 484-491