Expression profiling and gene ontology analysis in fathead minnow (Pimephales promelas) liver following exposure to pulp and paper mill effluents

Aquatic Toxicology

Volumn 122-123, Issue , 2012, Pages 44-55

  Costigan, Shannon L ^a   Werner, Julieta ^a   Ouellet, Jacob D ^a   Hill, Lauren G ^a   Law, R David ^a  

^a LAKEHEAD UNIVERSITY   (Canada)

Author keywords

DNA microarray; Expression analysis; Fathead minnow; Gene ontology; Pulp and paper mill effluent; Quantitative polymerase chain reaction; Steroid metabolism

Indexed keywords

CHOLESTEROL; ISOPRENOID; STEROID; STEROL;

DNA; EFFLUENT; GENE EXPRESSION; METABOLISM; MOLECULAR ANALYSIS; POLLUTION EFFECT; POLLUTION EXPOSURE; POLYMERASE CHAIN REACTION; STEROID; SURVIVAL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHOLESTEROL SYNTHESIS; COMBINED MILL OUTFALL; CONTROLLED STUDY; DNA MICROARRAY; EFFLUENT; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; FEMALE; GENE EXPRESSION PROFILING; GENE ONTOLOGY ANALYSIS; GENE TARGETING; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; LIVER CELL; LIVER PARENCHYMA; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PIMEPHALES PROMELAS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PUBLICATION; PULP AND PAPER MILL EFFLUENT; REPRODUCTION; STEROIDOGENESIS; STEROL SYNTHESIS; TREATED KRAFT EFFLUENT; WASTE MANAGEMENT; WATER POLLUTANT; WATER POLLUTION;

ANIMALS; CYPRINIDAE; FEMALE; FISH PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEPATOCYTES; INDUSTRIAL WASTE; LIVER; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; WATER POLLUTANTS, CHEMICAL;

PIMEPHALES PROMELAS;

EID: 84862327481     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.05.011     Document Type: Article

References (82)

1. Al-Shahrour F., Minguez P., Tarraga J., Montaner D., Alloza E., Vaquerizas J.M., Conde L., Blaschke C., Vera J., Dopazo J. BABELOMICS: a systems biology perspective in the functional annotation of genome-scale experiments. Nucleic Acids Research 2006, 34:W472-W476.
2. Al-Shahrour F., Minguez P., Vaquerizas J.M., Conde L., Dopazo J. BABELOMICS: a suite of web tools for functional annotation and analysis of groups of genes in high-throughput experiments. Nucleic Acids Research 2005, 33:W460-W464.
3. Ankley G.T., Jensen K.M., Kahl M.D., Korte J.J., Makynen E.A. Description and evaluation of a short-term reproduction test with the fathead minnow (Pimephales promelas). Environmental Toxicology and Chemistry 2001, 20:1276-1290.
4. Arcand-Hoy L.D., Benson W.H. Toxic responses of the reproductive system. Target Organ Toxicity in Marine and Freshwater Teleosts: Systems, II 2001, 177-198. Taylor and Francis, New York. D. Schlenk, W.H. Benson (Eds.).
5. Baer K.N., Bankston C.R., Mosadeghi S., Schlenk D. The effects of pulp and paper mill effluent on physiological and hematological endpoints in fingerling largemouth bass (Micropterus salmoides). Drug and Chemical Toxicology 2009, 32:59-67.
6. Barett T.J., Lowell R.B., Tingley M.A., Munkittrick K.R. Effects of pulp and paper mill effluent on fish: a temporal assessment of fish health across sampling cycles. Environmental Toxicology and Chemistry 2010, 29:440-452.
7. Beggel S., Connon R., Werner I., Geist J. Changes in gene transcription and whole organism responses in larval fathead minnow (Pimephales promelas) following short-term exposure to the synthetic pyrethroid bifenthrin. Aquatic Toxicology 2011, 105:180-188.
8. Benjamini Y., Hochberg Y. On the adaptive control of the false discovery rate in multiple testing with independent statistics. Journal of Educational and Behavioral Statistics 2000, 25:60-83.
9. Bidwell C.A., Carlson D.M. Characterization of vitellogenin from White Sturgeon Acipenser transmontanus. Journal of Molecular Evolution 1995, 41:104-112.
10. Bobe J., Maugars G., Nguyen T., Rime H., Jalabert B. Rainbow trout follicular maturational competence acquisition is associated with an increased expression of follicle stimulating hormone receptor and insulin-like growth factor 2 messenger RNAs. Molecular Reproduction and Development 2003, 66:46-53.
11. Borton D.L., Cook D.L., Bradley W.K., Philbeck R.E., Dube M.G., Brown-Peterson N.J., Streblow W.R. Responses of fathead minnows (Pimephales promelas) during life-cycle exposures to pulp mill effluents at four long-term receiving water study sites. Integrated Environmental Assessment and Management 2009, 5:270-282.
12. Bowron L.K., Munkittrick K.R., McMaster M.E., Tetreault G., Hewitt L.M. Responses of white sucker (Catostomus commersoni) to 20 years of process and waste treatment changes at a bleached kraft pulpmill, and to mill shutdown. Aquatic Toxicology 2009, 95:117-132.
13. Brazma A., Hingamp P., Quackenbush J., Sherlock G., Spellman P., Stoeckert C., Aach J., Ansorge W., Ball C.A., Causton H.C., Gaasterland T., Glenisson P., Holstege F.C., Kim I.F., Markowitz V., Matese J.C., Parkinson H., Robinson A., Sarkans U., Schulze-Kremer S., Stewart J., Taylor R., Vilo J., Vingron M. Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nature Genetics 2001, 29:365-371.
14. Brown G.D. The biosynthesis of steroids and triterpenoids. Natural Products Reports 1998, 15:653-696.
15. Celius T., Matthews J.B., Giesy J.P., Zacharewski T.R.P. Quantification of rainbow trout (Oncorhynchus mykiss) zona radiata and vitellogenin mRNA levels using real-time PCR after in vivo treatment with estradiol-17β or α-zearalenol. Journal of Steroid Biochemistry and Molecular Biology 2000, 75:109-119.
16. Chen T.T. Identification and characterization of estrogen-responsive gene products in the liver of rainbow trout. Canadian Journal of Biochemistry and Cell Biology 1983, 61:802-810.
17. Dai W., Kamei H., Zhao Y., Ding J., Du Z., Duan C. Duplicated zebrafish insulin-like growth factor binding protein-5 genes with split functional domains: evidence for evolutionarily conserved IGF binding, nuclear localization, and transactivation activity. FASEB Journal 2010, 24:2020-2029.
18. Denisov V., Strong W., Walder M., Gingrich J., Wintz H. Development and validation of RQI: an RNA quality indicator for the Experion automated electrophoresis system. Bio-Rad Bulletin 2008, 5761.
19. Denslow N.D., Kocerha J., Sepulveda M.S., Gross T., Holm S.E. Gene expression fingerprints of largemouth bass (Micropterus salmoides) exposed to pulp and paper mill effluents. Mutation Research 2004, 552:19-34.
20. Devlin R.H., Nagahama Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 2002, 208:191-364.
21. Diniz M.S., Peres I., Castro L., Freitas A.C., Rocha-Santos T.A.P., Pereira R., Duarte A.C. Impact of a secondary treated bleached Kraft pulp mill effluent in both sexes of goldfish (Carassius auratus L.). Journal of Environmental Science and Health, Part A 2010, 45:1858-1865.
22. Dorts J., Richter C.A., Wright-Osment M.K., Ellersieck M.R., Carter B.J., Tillitt D.E. The genomic transcriptional response of female fathead minnows (Pimephales promelas) to an acute exposure to the androgen, 17β-trenbolone. Aquatic Toxicology 2009, 91:44-53.
23. Duan C. The insulin like growth factor system and its biological actions in fish. American Zoologist 1997, 37:491-503.
24. Ellis R.J., van den Heuvel M.R., Smith M.A., McCarthy L.H., Stuthridge T.R., Dietrich D.R. In vivo and in vitro assessment of the androgenic potential of a pulp and paper mill effluent. Environmental Toxicology and Chemistry 2003, 22:1448-1456.
25. Environment Canada National Assessment of Pulp and Paper Environmental Effects Monitoring Data: A Report Synopsis. NWRI Scientific Assessment Report Series 2 2003, National Water Research Institute, Burlington, ON.
26. Filby A.L., Tyler C.R. Appropriate 'housekeeping' genes for use in expression profiling the effects of environmental estrogens in fish. BMC Molecular Biology 2007, 8:10.
27. Filby A.L., Santos E.M., Thorpe K.L., Maack G., Tyler C.R. Gene expression profiling for understanding chemical causation of biological effects for complex mixtures: a case study on estrogens. Environmental Science and Technology 2007, 41:8187-8194.
28. Filby A.L., Thorpe K.L., Maack G., Tyler C.R. Gene expression profiles revealing the mechanisms of anti-androgen- and estrogen-induced feminization in fish. Aquatic Toxicology 2007, 81:219-231.
29. Filby A.L., Thorpe K.L., Tyler C.R. Multiple molecular effect pathways of an environmental oestrogen in fish. Journal of Molecular Endocrinology 2006, 37:121-134.
30. Fisheries Act Pulp and paper effluent regulations. Canada Gazette Part II 1992, 126. 967-206.
31. Garcia-Reyero N., Adelman I.R., Martinovic D., Liu L., Denslow N.D. Site-specific impacts on gene expression in fathead minnows (Pimephales promelas) exposed in situ to streams adjacent to sewage treatment plants. BMC Bioinformatics 2009, 10(Suppl 11):S11.
32. Garcia-Reyero N., Adelman I., Liu L., Denslow N. Gene expression profiles of fathead minnows exposed to surface waters above and below a sewage treatment plant in Minnesota. Marine Environment Research 2008, 66:134-136.
33. Gust K.A., Wilbanks M.S., Guan X., Pirooznia M., Habib T., Yoo L., Wintz H., Vulpe C.D., Perkins E.J. Investigations of transcript expression in fathead minnow (Pimephales promelas) brain tissue reveal toxicological impacts of RDX exposure. Aquatic Toxicology 2011, 101:135-145.
34. Hewitt M.L., Kovacs T.G., Dubé M.G., MacLatchy D.L., Martel P.H., McMaster M.E., Paice M.G., Parrot J.L., van den Heuvel M.R., Van Der Kraak G.J. Altered reproduction in fish exposed to pulp and paper mill effluents: roles of individual compounds and mill operating conditions. Environmental Toxicology and Chemistry 2008, 27:682-697.
35. Hyllner S.J., Oppen-Berntsen D.O., Helvik J.V., Walther B.T., Haux C. Oestrogen-17β induces the major vitelline envelope proteins in both sexes in teleosts. Journal of Endocrinology 1991, 131:229-236.
36. Jones J.I., Clemmons D.R. Insulin-like growth factors and their binding proteins: biological actions. Endocrine Reviews 1995, 16:3-34.
37. Kagawa H., Kobayashi M., Hasegawa Y., Aida K. Insulin and insulin-like growth factors I and II induce final maturation of oocytes of red seabream Pagrus major, in vitro. General and Comparative Endocrinology 1994, 95:293-300.
38. Kajimura S., Aida K., Duan C. Insulin-like growth factor-binding protein-1 (IGFBP-1) mediates hypoxia-induced embryonic growth and developmental retardation. PNAS 2005, 105:1240-1245.
39. Kamei H., Lu L., Jiao S., Li Y., Gyrup C., et al. Duplication and diversification of the hypoxia-inducible IGFBP-1 gene in zebrafish. PLoS One 2008, 3:e3091.
40. Kidd K.A., Blanchfield P.J., Mills K.H., Palace V.P., Evans R.E., Lazorchak J.M., Flick R.W. Collapse of a fish population after exposure to a synthetic estrogen. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:8897-8901.
41. Knaut H., Pelegri F., Bohmann K., Schwarz H., Nüsslein-Volhard C. Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification. Journal of Cell Biology 2000, 149:875-888.
42. Kovacs T.G., Martel P.H., O'Conner B.I., Parrott J.L., McMaster M.E., Van Der Kraak G.J., MacLatchy D.L., van den Heuvel M.R., Hewitt L.M. Kraft mill effluent survey: progress toward best management practices for reducing effects on fish reproduction. Environmental Toxicology and Chemistry 2011, 30:1421-1429.
43. Kovacs T., Martel P., Ricci M., Michaud J., Voss R. Further insights into the potential of pulp and paper mill effluents to affect fish reproduction. Journal of Toxicology and Environmental Health, Part A 2005, 68:1621-1641.
44. Lattier D.L., Reddy R.V., Gordon D.A., Lazorchak J.M., Smith M.E., Williams D.E., Wiechman B., Flick R.W., Miracle A.L., Toth G.R. 17α-ethynylestradiol-induced vitellogenin gene transcription quantified in livers of adult males, larvae, and gills of fathead minnows (Pimephales promelas). Environmental Toxicology and Chemistry 2002, 21:2385-2393.
45. Lee K.H., Yamaguchi A., Rashid H., Kadomura K., Yasumoto S., Matsuyama M. Estradiol-17β treatment induces intersexual gonadal development in the pufferfish Takifugu rubripes. Zoological Science 2009, 26:639-645.
46. Maegawa S., Yamashita M., Yasuda K., Inoue K. Zebrafish DAZ-like protein controls translation via the sequence 'GUUC'. Genes to Cells 2002, 7:971-984.
47. Maestro M.A., Planas J.V., Moriyama S., Gutierrez J., Planas J., Swanson P. Ovarian receptors for insulin and insulin-like growth factor-1 (IGF-1) and effects of IGF-1on steroid production by isolated follicular layers of the preovulatory coho salmon ovarian follicle. General and Comparative Endocrinology 1997, 106:189-201.
48. Martinovic-Weigelt D., Wang R.L., Villeneuve D.L., Bencic D.C., Lazorchak J., Ankley G.T. Gene expression profiling of the androgen receptor antagonists flutamide and vinclozolin in zebrafish (Danio rerio) gonads. Aquatic Toxicology 2011, 101:447-458.
49. McMaster M.E., Hewitt L.M., Parrott J.L. A decade of research on the environmental impacts of pulp and paper mill effluents in Canada: field studies and mechanistic research. Journal of Toxicology and Environmental Health. Part B, Critical Reviews 2006, 9:319-339.
50. Mortensen A.S., Arukwe A. Effects of 17a-ethynylestradiol on hormonal responses and xenobiotic biotransformation system of Atlantic salmon (Salmo salar). Aquatic Toxicology 2007, 85:113-123.
51. Munkittrick K.R. Assessment of the effects of endocrine disrupting substances in the Canadian environment. Water Quality Research Journal of Canada 2001, 36:293-302.
52. Munkittrick K.R., McGeachy S.A., McMaster M.E., Courtenay S.C. Overview of freshwater fish studies from the pulp and paper Environmental Effects Monitoring program. Water Quality Research Journal of Canada 2002, 37:49-77.
53. Munkittrick K.R., Van Der Kraak G.J., McMaster M.E., Portt C.B., van den Heuvel M.R., Servos M.R. Survey of receiving water environmental impacts associated with discharges from pulp mills. Environmental Toxicology and Chemistry 1994, 13:1089-1101.
54. Munkittrick K.R., Servos M.R., Carey J.H., Van Der Kraak G.J. Environmental impacts of pulp and paper wastewater: Evidence for a reduction in environmental effects at North American pulp mills since 1992. Water Science and Technology 1997, 35:329-338.
55. Oppen-Berntsen D.O., Gram-Jensen E., Walther B.T. Zona radiata proteins are synthesized by rainbow trout (Oncorhynchus mykiss) hepatocytes in response to oestradiol-17β. Journal of Endocrinology 1992, 135:293-302.
56. Oppen-Berntsen D.O., Hyllner S.J., Haux C., Helvik J.V., Walther B.T. Eggshell zona radiata-proteins from cod (Cadus morhula): extra-ovarian origin and induction by estradiol-17β. International Journal of Developmental Biology 1992, 36:247-254.
57. Orrego R., Burgos A., Moraga-Cid G., Inzunza B., Gonzalez M., Valenzuela A., Barra R., Gavilán J.F. Effects of pulp and paper mill discharges on caged rainbow trout (Oncorhynchus mykiss): biomarker responses along a pollution gradient in the Biobio River, Chile. Environmental Toxicology and Chemistry 2006, 25:2280-2287.
58. Pallittini V., Scalici M., Gibertini G., Marino M., Trentalance A. 3-Hydroxy 3-methylglutaryl coenzyme A reductase: a new biomarker of fish exposure to water pollution. Bulletin of Environmental Contamination and Toxicology 2010, 85:381-384.
59. Parrott J.L., McMaster M.E., Hewitt L.M. A decade of research on the environmental impacts of pulp and paper mill effluents in Canada: development and application of fish bioassays. Journal of Toxicology and Environmental Health Part B: Critical Reviews 2006, 9:297-317.
60. Parrott J.L., Wood C.S., Boutot P., Dunn S. Changes in growth and secondary sex characteristics of fathead minnows exposed to bleached sulfite mill effluent. Environmental Toxicology and Chemistry 2003, 22:2908-2915.
61. Pokhrel D., Viraraghavan T. Treatment of pulp and paper mill wastewater-a review. Science of the Total Environment 2004, 333:37-58.
62. Popesku J.T., Tan E.Y., Martel P.H., Kovacs T.G., Rowan-Carroll A., Williams A., Yauk C., Trudeau V.L. Gene expression profiling of the fathead minnow (Pimephales promelas) neuroendocrine brain in response to pulp and paper mill effluents. Aquatic Toxicology 2010, 99:379-388.
63. Poynton H.C., Vulpe C.D. Ecotoxicogenomics: emerging technologies for emerging contaminants. Journal of the American Water Resources Association 2009, 45:83-96.
64. Raz E. The function and regulation of vasa-like genes in germ-cell development. Genome Biology 2000, 1:1017.
65. Rickwood C.J., Dubé M.G., Hewitt L.M., Kovacs T.G., MacLatchy D.L. Use of paired fathead minnow (Pimephales promelas) reproductive test. Part 2: Source identification of biological effects at a bleached kraft pulp mill. Environmental Toxicology and Chemistry 2006, 25:1847-1856.
66. Riley L.G., Hirano T., Grau E.G. Disparate effects of gonadal steroid hormones on plasma and liver mRNA levels of insulin-like growth factor-I and vitellogenin in the tilapia Oreochromis mossambicus. Fish Physiology and Biochemistry 2002, 26:223-230.
67. Romanov A.A., Altuf'ev Y. Extraregional histogenesis of sexual cells in the Caspian Sea sturgeons. Journal of Ichthyology 1992, 32:145-154.
68. Satoh K., Nagai F., Aoki N. Several environmental pollutants have binding affinities for both androgen receptor and estrogen receptor α. Journal of Health Science 2001, 47:495-501.
69. Schirra F., Richards S.M., Sullivan D.A. Androgen influence on cholesterogenic enzyme mRNA levels in the mouse meibomian gland. Current Eye Research 2007, 32:393-398.
70. Sharpe R.L., MacLatchy D.L. Lipid dynamics in goldfish (Carassius auratus) during a period of gonadal recrudescence: effects of beta-sitosterol and 17beta-estradiol exposure. Comparative Biochemistry and Physiology - Part C: Toxicology & Pharmacology 2007, 145:507-517.
71. Simon R.M., Dobbin K. Experimental design of DNA microarray experiments. BioTechniques 2003, 34:S16-S21.
72. Skolness S.Y., Durhan E.J., Garcia-Reyero N., Jensen K.M., Kahl M.D., Makynen E.A., Martinovic-Weigelt D., Perkins E., Villeneuve D.L., Ankley G.T. Effects of a short-term exposure to the fungicide prochloraz on endocrine function and geneexpression in female fathead minnows (Pimephales promelas). Aquatic Toxicology 2011, 103:170-178.
73. Smyth G.K. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Statistical Applications in Genetics and Molecular Biology 2004, 3. 3 Article.
74. Smyth G.K., Speed T.P. Normalization of cDNA microarray data. Methods 2003, 31:265-273.
75. Smyth G.K., Michaud J., Scott H. The use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 2005, 21:2067-2075.
76. Sonnenschein C., Soto A.M. An updated review of environmental estrogen and androgen mimics and antagonists. The Journal of Steroid Biochemistry and Molecular Biology 1998, 65:143-150.
77. van den Heuvel M.R., Martel P.H., Kovacs T.G., MacLatchy D.L., Van Der Kraak G.J., Parrot J.L., McMaster M.E., O'Connor B.I., Melvin S.D., Hewitt L.M. Evaluation of short-term fish reproductive bioassays for predicting effects of a Canadian bleached kraft mill effluent. Water Quality Research Journal of Canada 2010, 45:175-186.
78. van den Heuvel M.R., Landman M.J., Tremblay L.A. Responses of shortfin eel (Anguilla australis) exposed in situ to pulp and paper effluent. Journal of Toxicology and Environmental Health, Part A 2006, 69:1763-1779.
79. Villeneuve D.L., Blake L.S., Brodin J.D., Greene K.J., Knoebl I., Miracle A.L., Martinovic D., Ankley G.T. Transcription of key genes regulating gonadal steroidogenesis in control and ketoconazole- or vinclozolin-exposed fathead minnows. Toxicological Sciences 2007, 98:395-407.
80. Weech S., Orr S. Cycle 3 Environmental Effects Monitoring Interpretive Report 2004, Minnow Environmental Inc, Mississauga, ON.
81. Werner J., Ouellet J.D., Cheng C.S., Ju Y.J., Law R.D. Pulp and paper mill effluents induce distinct gene expression changes linked to androgenic and estrogenic responses in the fathead minnow (Pimephales promelas). Environmental Toxicology and Chemistry 2010, 29:430-439.
82. Zhou J., Li W., Kamei H., Duan C. Duplication of the IGFBP-2 gene in teleost fish: protein structure and functionality conservation and gene expression divergence. PLoS One 2008, 3:e3926.