Transcriptional response of hepatic largemouth bass (Micropterus salmoides) mRNA upon exposure to environmental contaminants

Journal of Applied Toxicology

Volumn 31, Issue 2, 2011, Pages 108-116

  Sanchez, Brian C ^a,c   Carter, Barbara ^b   Hammers, Heather R ^b   Sepúlveda, María S ^a  

^a PURDUE UNIVERSITY   (United States)

^b EcoArray Inc   (United States)

^c U S FISH AND WILDLIFE SERVICE   (United States)

Author keywords

Aquatic; Atrazine; Cadmium; Fish; PCB 126; Phenanthrene; Toxaphene; Toxicogenomics

Indexed keywords

3,3',4,4',5 PENTACHLOROBIPHENYL; ALCOHOL; ANTIESTROGEN; ATRAZINE; BIOLOGICAL MARKER; CADMIUM CHLORIDE; CAMPHECLOR; CARBON; MESSENGER RNA; OLIGONUCLEOTIDE; PHENANTHRENE;

ALCOHOL METABOLISM; ARTICLE; CARBON METABOLISM; ENVIRONMENTAL EXPOSURE; GENE EXPRESSION; GENE SET ENRICHMENT ANALYSIS; GENETIC TRANSCRIPTION; LARGEMOUTH BASS; LIVER; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLLUTANT; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RNA TRANSCRIPTION;

ANIMALS; BASS; BIOLOGICAL MARKERS; BODY BURDEN; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL POLLUTANTS; GENE EXPRESSION PROFILING; LIVER; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, MESSENGER; STATISTICS AS TOPIC; TRANSCRIPTION, GENETIC;

MICROPTERUS; MICROPTERUS SALMOIDES;

EID: 79951973037     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.1553     Document Type: Article

References (89)

1. Arcaro KF, O'Keefe PW, Yang Y, Clayton W, Gierthy JF. 1999. Antiestrogenicity of environmental polycyclic aromatic hydrocarbons in human breast cancer cells. Toxicology 133: 115-127.
2. Arukwe A, Knudsen FR, Gosksøyr A. 1997. Fish zona radiata (eggshell) protein: a sensitive biomarker for environmental estrogens. Environ. Health Perspect. 105: 418-422.
3. Arukwe A, Yadetie F, Male R, Gosksøyr A. 2001. In vivo modulation of nonylphenol-induced zonagenesis and vitellogenesis by the antiestrogen, 3, 3'4, 4'-tetrachlorobiphenyl (PCB-77). Environ. Toxicol. Phar. 10: 5-15.
4. Arukwe A, Gosksøyr A. 2003. Eggshell and egg yolk proteins in fish: hepatic proteins for the next generation: oogenetic, population, and evolutionary implications of endocrine disruption. Comp. Hepatol. 2: 4.
5. Baker SD, Sepúlveda MS. 2009. Evaluation of the effects of persistent environmental contaminants on the reproductive success of great blue herons (Ardea herodias) in Indiana. Ecotoxicology 18: 271-280; doi:10.1007/s10646-008-0281-2.
6. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Royal Statist. Soc. Ser. B. 57: 289-300.
7. Berg AH, Westerlund L, Olsson PE. 2004. Regulation of Arctic char (Salvelinus alpinus) egg shell proteins and vitellogenin during reproduction and in response to 17β-estradiol and cortisol. Gen. Comp. Endocr. 135: 276-285.
8. Bopp SK, Lettieri T. 2007. Gene regulation in the marine diatom Thalassiosira pseudonana upon exposure to polycyclic aromatic hydrocarbons (PAHs). Gene 396: 293-302.
9. Burchiel SW, Luster MI. 2001. Signalling by environmental polycyclic aromatic hydrocarbons in human lymphocytes. Clin. Immunol. 98: 2-10; doi: 10.1016/j.gene.2007.03.013
10. Chugh LK, Sawhney SK. 1999. Effect of cadmium on activities of some enzymes of glycolysis and pentose phosphate pathway in pea. Biol. Plantarum 42: 401-407.
11. Chung H, Hong DP, Jung JY, Kim HJ, Jang KS, Sheen YY, Ahn JI, Lee YS, Kong G. 2006. Comprehensive analysis of differential gene expression profiles on carbon tetrachloride-induced rat liver and regeneration. Toxicol. Appl. Pharmacol. 206: 27-42.
12. Cohen A, Shmoish M, Levi L, Cheruti U, Levavi-Sivan B, Lubzens E. 2008. Alterations in micro-ribonucleic acid expression profiles reveal a novel pathway for estrogen regulation. Endocrinology 149: 1687-1696; doi: 10.1210/en.2007-0969.
13. Cowper AE, Cáceres JF, Mayeda A, Screaton GR. 2001. Serine-arginine (SR) protein-like factors that antagonize authentic SR proteins and regulate alternative splicing. J. Biol. Chem. 276: 48908-48914; doi: 10.1074/jbc.M103967200.
14. Dong Y, Poellinger L, Okret S, Höög JO, con Bahr-Lindström H, Jörnvall H, Gustafsson JA. 1988. Regulation of gene expression of class I alcohol dehydrogenase by glucocorticoids. Proc. Natl Acad. Sci. USA 85: 767-771.
15. Eisler R, Belisle AA. 1996. Planar PCB Hazards to Fish, Wildlife, and Invertebrates: a Synoptic Review. US Department of the Interior, NBS: Washington, DC.
16. Falahatpisheh H, Nanez A, Montoya-Durango D, Qian Y, Tiffany-Castiglioni E, Ramos KS. 2007. Activation profiles of HSPA5 during the glomular mesangial cell stress response to chemical injury. Cell Stress Chaperon. 12: 209-218.
17. Felder MR, Watson G, O'Malley-Huff M, Ceci JD. 1988. Mechanism of induction of mouse kidney alcohol dehydrogenase by androgen. Androgen-induced stimulation of transcription of the ADH-1 gene. J. Biol. Chem. 263: 14531-14537.
18. Fujikawa A, Shirasaka D, Yamamoto S, Ota H, Yahiro K, Fukuda M, Shintani T, Wada A, Aoyama N, Hirayama T etal. 2003. Mice deficient in protein tyrosine phosphatase receptor type Z are resistant to gastric ulcer induction by VacA of Helicobacter pylori. Nat. Genet. 33: 375-381.
19. Garcia-Reyero N, Denslow ND. 2006. Applications of genomic technologies to the study of organochlorine pesticide-induced reproductive toxicity in fish. J. Pest. Sci. 31: 252-262.
20. García-Rubio M, Chávez S, Huertas P, Tous C, Jimeno S, Luna R, Aguilera A. 2008. Different physiological relevance of yeast THO/TREX subunits in gene expression and genome integrity. Mol. Genet. Genomics 279: 123-132; doi: 10.1007/s00438-007-0301-6.
21. Handley-Goldstone HM, Grow MW, Stegeman JJ. 2005. Cardiovascular gene expression profiles of dioxin exposure in zebrafish embryos. Toxicol. Sci. 85: 683-693.
22. Hankinson O. 2005. Role of coactivators in transcriptional activation by the aryl hydrocarbon receptor. Arch. Biochem. Biophys. 433: 379-386; doi: 10.1016/j.abb.2004.09.031.
23. Harroch S, Furtado GC, Brueck W, Rosenbluth J, Lafaille J, Chao M, Buxbaum JD, Schlessinger J. 2002. A critical role for the protein tyrosine phosphatase receptor type Z in functional recovery from demyelinating lesions. Nat. Genet. 32: 411-414.
24. Hester SD, Nesnow S. 2008. Transcriptional responses in thyroid tissues from rats treated with a tumorigenic and non-tumorigenic triazole conazole fungicide. Toxicol. Appl. Pharmacol. 227: 357-369.
25. Holland DC, Munns RK, Roybal JE, Hurlbut JA, Long AR. 1994. Liquid chromatographic determination of simazine, atrazine, and propazine residues in catfish. J. AOAC Int. 78: 1067-1071.
26. Hook SE, Skillman AD, Small JA, Schultz IR. 2006. Gene expression patterns in rainbow trout, Oncorhynchus mykiss, exposed to a suite of model toxicants. Aquat. Toxicol. 77: 372-385; doi: 10.1016/j.aquatox.2006.01.007.
27. Hurt JA, Silver PA. 2008. mRNA nuclear export and human disease. Dis. Models Mechan. 1: 103-108; doi: 10.1242/dmm.000745.
28. Jarvinen AW, Ankley GT. 1999. Linkage of Effects to Tissue Residues: Development of a Comprehensive Database for Aquatic Organisms Exposed to Inorganic and Organic Chemicals. Pensacola, FL: SETAC Press.
29. Jimeno S, Rondón AG, Luna R, Aguilera A. 2002. The yeast THO complex and mRNA export factors link RNA metabolism with transcription and genome instability. EMBO J. 21: 3526-3535.
30. Kazeto Y, Place AR, Trant JM. 2004. Effects of endocrine disrupting chemicals on the expression of CYP19 genes in zebrafish (Danio rerio) juveniles. Aquat. Toxicol. 69: 25-34; doi: 10.1016/j.aquatox.2004.04.008.
31. Kishimoto T, Kokura K, Ohkawa N, Makino Y, Yoshida M, Hirohashi S, Niwa S, Muramatsu M, Tamura T. 1998. Enhanced expression of a new class of liver-enriched b-zip transcription factors, hepatocellularcarcinogenesis-related transcription factor, in hepatocellular carcinomas of rats and humans. Cell Growth Different. 9: 337-344.
32. Kondoh E, Okamoto T, Higuchi T, Tatsumi K, Baba T, Murphy SK, Takakura K, Konishi I, Fujii S. 2009. Stress affects uterine receptivity through an ovarian-independent pathway. Human Reprod. 1: 1-9; doi: 10.1093/humrep/den461.
33. Koskinen H, Pehkonen P, Vehniäinen E, Krasnov A, Rexroad C, Afanasyev S, Mölsa H, Oikari A. 2004. Response of rainbow trout transcriptome to model chemical contaminants. Biochem. Biophys. Res. Commun. 320: 745-753; doi: 10.1016/j.bbrc.2004.06.024.
34. Langerveld AJ, Celestine R, Zaya R, Mihalko D, Ide CF. 2009. Chronic exposure to high levels of atrazine alters expression of genes that regulate immune and growth-related functions in developing Xenopus laevis tadpoles. Environ. Res. 109: 379-389; doi: 10.1016/j.envres.2009.01.006.
35. Larkin P, Sabo-Atwood T, Kelso J, Denslow ND. 2002. Gene expression analysis of largemouth bass exposed to estradiol, nonylphenol, and p, p'-DDE. Comp. Biochem. Physiol. Part B 133: 543-557.
36. Larkin P, Folmar LC, Hemmer MJ, Poston AJ, Denslow ND. 2003. Expression profiling of estrogenic compounds using a sheepshead minnow cDNA macroarray. Environ. Health Perspect. 111: 839-846; doi: 10.1289/txg.5752.
37. Larkin P, Villeneuve DL, Knoebl I, Miracle AL, Carter BJ, Liu L, Denslow ND, Ankley GT. 2007. Development and validation of a 2, 000-gene microarray for the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 26: 1497-1506.
38. Lee AH, Scapa EF, Cohen DE, Glimcher LH. 2008. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science. 320: 1492-1496; doi: 10.1126/science.1158042.
39. Lee SE, Yoo DH, Son J, Cho K. 2006. Proteomic evaluation of cadmium toxicity on the midge Chironomous riparius Meigen larvae. Proteomics 6: 945-957; doi: 10.1002/pmic.200401349.
40. Lettieri T. 2006. Recent applications of DNA microarray technology to toxicology and ecotoxicology. Environ. Health Perspect. 114: 4-9; doi: 10.1289/ehp.8194.
41. Liu YT, Shang D, Akatsuka S, Ohara H, Dutta KK, Mizushima K, Naito Y, Yoshikawa T, Izumiya M, Abe K etal. 2007. Chronic oxidative stress causes amplification and overexpression of ptprz1 protein tyrosine phophatase to activate β-catenin pathway. Am. J. Pathol. 171: 1978-1988; doi: 10.2353/ajpath.2007-070741.
42. Lyons CE, Payette KL, Price JL, Huang RCC. 1993. Expression and structural-analysis of a teleost homolog of a mammalian zona-pellucida gene. J. Biol. Chem. 268: 21351-21358.
43. Maier MSV, Legare ME, Hanneman WH. 2007. The aryl hydrocarbon receptor agonist 3, 3', 4, 4', 5-pentachlorobiphenyl induces distinct patterns of gene expression between hepatoma and glioma cells: chromatin remodelling as a mechanism for selective effects. Neurotoxicology 28: 594-612; doi: 10.1016/j.neuro.2007.01.002.
44. Oppen-Berntsen DO, Gram-Jensen E, Walther BT. 1992. Eggshell zona radiata proteins are synthesized by rainbow trout (Oncorhynchus mykiss) hepatocytes in response to oestradiol-17β. Endocrinology 135: 293-302.
45. Oppen-Berntsen DO, Arukwe A, Yadetie F, Lorens JB, Male R. 1999. Salmon eggshell protein expression: a marker for environmental estrogens. Mar. Biotechnol. 1: 252-260.
46. Östman A, Hellberg C, Böhmer FD. 2006. Protein-tyrosine phosphatases and cancer. Nat. Rev. Cancer 6: 307-320; doi: 10.1038/nrc1837.
47. Qulali M, Ross RA, Crabb DW. 1991. Estradiol induces class I alcohol dehydrogenase activity and mRNA in kidney of female rats. Arch. Biochem. Biophys. 288: 406-413.
48. Rehwinkel J, Herold A, Gari K, Köcher T, Rode M, Ciccarelli FL, Wilm M, Izaurralde E. 2004. Genome-wide analysis of mRNAs regulated by the THO complex in Drosophila melanogaster. Nat. Struct. Mol. Biol. 11: 558-566; doi: 10.1038/nsmb759.
49. Reimers MJ, Hahn ME, Tanguay RL. 2004. Two zebrafish alcohol dehydrogenases share common ancestry with mammalian class I, II, IV, and V alcohol dehydrogenase genes but have distinct functional characteristics. J. Biol. Chem. 279: 38303-38312; doi: 10.1074/jbc.M401165200.
50. Reimold AM, Etkin A, Clauss I, Perkins A, Friend DS, Zhang J, Horton HF, Scott A, Orkin SH, Byrne MC etal. 2000. An essential role in liver development for transcription factor XBP-1. Genes Devl. 14: 152-157.
51. Rise ML, von Schalburg KR, Brown GD, Mawer MA, Devlin RH, Kuipers N, Busby M, Beetz-Sargent M, Alberto R, Gibbs AR etal. 2004. Development and application of a salmonid EST database and cDNA microarray: data mining and interspecific hybridization characteristics. Genome Res. 14: 478-490; doi: 10.1101/gr.1687304.
52. Romero G, Lasheras B, Sainz Suberviola L, Cenarrauzabeitia E.1994. Protective effects of calcium channel blockers in carbon tetrachloride-induced liver toxicity. Life Sci. 55: 981-990.
53. Rosell A, Valencia E, Parés X, Fita I, Farrés J, Ochoa WF. 2003. Crystal structure of the vertebrate NADP(H)-dependent alcohol dehydrogenase (ADH8). J. Mol. Biol. 330: 75-85.
54. Rutkowski DT, Kaufman RJ. 2007. That which does not kill me makes me stronger: adapting to chronic ER stress. TRENDs Biochem. Sci. 32: 469-476; doi: 0.1016/j.tibs.2007.09.003.
55. Ryu S, Zhou S, Ladurner AG, Tijan R. 1999. The transcriptional cofactor complex CRSP is required for activity of the enhancer-binding protein Sp1. Nature 397: 446-450.
56. Schena M, Shalon D, Davis RW, Brown PO. 1995. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270: 467-470.
57. Schlenk D, Celander M, Gallagher EP, George S, James M, Kullman SW, van den Hurk P, Willett K. 2008. Biotransformation in fishes. In The Toxicology of Fishes, Di Giulio RT, Hinton DE (eds). Boca Raton, FL: CRC Press.
58. Shailaja MS, D'Silva C. 2003. Evaluation of impact of PAH on a tropical fish, Oreochromis mossambicus, using multiple biomarkers. Chemosphere 53: 835-841; doi: 10.1016/S0045-6535903)00667-2.
59. Sharon A, Pratap R, Tripathi B, Srivastava AK, Maulik PR, Ram VJ. 2005. Biaryls and heterobiaryls as α-glucosidase and protein tyrosine phosphatase inhibitors. Bioorg. Med. Chem. Lett. 15: 1341-1344; doi: 10.1016/j.bmcl.2005.01.036.
60. Shin C, Manley J. 2004. Cell signalling and the control of pre-mRNA splicing. Nat. Rev. Mol. Cell Biol. 5: 727-738; doi: 10.1038/nrm1467.
61. Shin C, Feng Y, Manley J. 2004. Dephosphorylated SRp38 acts as a splicing repressor in response to heat shock. Nature 427: 553-558; doi: 10.1038/nature02288.
62. Shuda M, Kondoh N, Imazeki N, Tanaka K, Okada T, Mori K, Hada A, Arai M, Wakatsuki T, Matsubara O etal. 2003. Activation of the ATF6, XBP1 and grp78 genes in human hepatocellular carcinoma: a possible involvement of the ER stress pathway in hepatocarcinogenesis. J. Hepatol. 38: 605-614; doi: 10.1016/S0168-8278(03)00029-1.
63. Spargo SC, Hope RM. 2003. Evolution and nomenclature of the zona pellucida gene family. Biol.Reprod. 68: 358-362.
64. Staal YCM, van Herwijnen MHM, van Schooten FJ, van Delft JHM. 2006. Modulation of gene expression and DNA adduct formation in HepG2 cells by polycyclic aromatic hydrocarbons with different carcinogenic potencies. Carcinogenesis 27: 646-655; doi: 10.1093/carcin/bgi255.
65. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES etal. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102: 15545-15550; doi: 10.1073/pnas.0506580102.
66. Sunaga H, Yamane Y, Aoki Y, Suzuki KT. 1988. The major cadmium-binding protein before induction of metallothioneine in the rat liver is alcohol dehydrogenase. Proceedings of the 14th Symposium on Environmental Pollution and Toxicology, Kumamoto, Japan. Eisei Kagaku.
67. Suske G. 1999. The Sp-family of transcription factors. Gene. 238: 291-300.
68. Suzuki KT, Kawahara S, Sunaga H, Shimojo N. 1990. Efflux of endogenous zinc liberated from metallothioneine and alcohol dehydrogenase in the liver by replacement with cadmium. Toxicol. Appl. Pharmacol. 105: 413-421.
69. Takemura R, Inoue Y, Izawa S. 2004. Stress response in yeast mRNA export factor: reversible changes in Rat8p localization are caused by ethanol stress but not heat shock. J. Cell Sci. 117: 4189-4197; doi: 10.1242/jcs.01296.
70. Tani T, Derby RJ, Hiraoka Y, Spector DL. 1995. Nuclear accumulation of poly(A)+RNA in heat shocked yeast cells: implication of nucleolar involvement in mRNA transport. Molec. Biol. Cell 7: 173-192.
71. Tchounwou PB, Wilson BA, Ishaque AB, Schneider J. 2001. Atrazine potentiation of arsenic trioxide-induced cytotoxicity and gene expression in human liver carcinoma cells (HepG2). Mol. Cell. Biochem. 222: 49-59.
72. Thompson MD, Monga SPS. 2007. WNT/β-catenin signaling in liver health and disease. Hepatology 45: 1298-1305; doi: 10.1002/hep.21651.
73. Tilton SC, Givan SA, Pereira CB, Bailey GS, WIlliams DE. 2006. Toxicogenomic profiling of the hepatic tumor promoters indole-3-carbinol, 17β-estradiol, and α-naphthoflavone in rainbow trout. Toxicol. Sci. 90: 61-72; doi: 10.1093/toxsci/kfi341.
74. USEPA. 2000. Method 6010C. Determination of Inorganic Analytes by Inductively Coupled Plasma-Atomic Emission Spectrometry. US Department of the Interior OOSW: Washington, DC.
75. Vaccaro E, Meucci V, Intorre L, Soldani G, Bello D, Longo V, Gervasi PG, Pretti C. 2005. Effects of 17β, 4-nonylphenol and PCB 126 on the estrogenic activity and phase 1 and 2 biotransformation enzymes in male sea bass (Dicentrarchus labrax). Aquat. Toxicol. 75: 293-305.
76. 1-S-phase transition by polycyclic aromatic hydrocarbons in human breast carcinoma MCF-7 cells. Toxicol. Sci. 70: 193-201.
77. Vinciguerra P, Stutz F. 2004. mRNA export an assembly line from genes to nuclear pores. Curr. Opin. Cell Biol. 16: 285-292.
78. Waku K. 1984. The chemical form of cadmium in subcellular fractions following cadmium exposure. Environ. Health Persp. 54: 37-44.
79. Wang RL, Biales A, Bencic D, Lattier D, Kostich M, Villeneuve DL, Ankley GT, Lazorchak J, Toth G. 2008. DNA microarray application in ecotoxicology: experimental design, microarray scanning, and factors affecting transcriptional profiles in a small fish species. Environ. Toxicol. Chem. 27: 652-663.
80. Watkin RD, Nawrot T, Potts RJ, Hart BA. 2003. Mechanisms regulating the cadmium-mediated suppression of Sp1 transcription factor activity in alveolar epithelial cells. Toxicology 184: 157-178.
81. Weis L, Reinberg D. 1992. Transcription by RNA polymerase II: initiator-directed formation of transcription-competent complexes. FASEB J. 6: 3300-3309.
82. Williams TD, Gensberg K, Minchin SD, Chipman JK. 2003. A DNA expression array to detect toxic stress response in European flounder (Platichthys flesus). Aquat. Toxicol. 65: 141-157; doi: 10.1016/S0166-445X(03)00119-X.
83. Williams TD, Diab A, Ortega F, Sabine VS, Godfrey RE, Falciani F, Chipman JK, George SG. 2008. Transcriptomic responses of European flounder (Platichthys flesus) to model toxicants. Aquat. Toxicol. 90: 83-91; doi: 10.1016/j.aquatox.2008.07.019.
84. Yadetie F, Arukwe A, Gosksøyr A, Male R. 1991. Induction of hepatic estrogen receptor in juvenile Atlantic salmon in vivo by the environmental estrogen, 4-nonylphenol. Sci. Total Environ. 233: 201-210.
85. Yokley RA, Cheung MW. 2000. Analytical method for the determination of atrazine and its dealkylated chlorotriazine metabolites in water using gas chromatography/mass selective detection. J. Agric. Food Chem. 48: 4500-4507; doi: 10.1021/jf991100v.
86. Yost HJ, Petersen RB, Lindquist S. 1990. RNA metabolism: strategies for regulation in the heat shock response. Trends Genet. 6: 223-227.
87. Yu W, Macreadie IG, Winge D. 1991. Protection against cadmium toxicity in yeast by alcohol dehydrogenase. J. Inorg. Biochem. 44: 155-161.11
88. Zeeberg BR, Feng W, Wang G, Wang MD, Fojo AT, Sunshine M, Narasimhan S, Kane DW, Reinhold WC, Lababidi S etal. 2003. GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol. 4: R28.
89. Zhang ZY, Zhou B, Xie L. 2002. Modulation of protein kinase signaling by protein phosphatases and inhibitors. Pharmacol. Ther. 93: 307-317.