Gene expression of fathead minnows (Pimephales promelas) exposed to two types of treated municipal wastewater effluents

Environmental Science and Technology

Volumn 47, Issue 19, 2013, Pages 11268-11277

  Vidal Dorsch, Doris E ^a   Colli Dula, R Cristina ^b   Bay, Steven M ^a   Greenstein, Darrin J ^a   Wiborg, Lan ^c   Petschauer, Dawn ^d   Denslow, Nancy D ^b  

^a SOUTHERN CALIFORNIA COASTAL WATER RESEARCH PROJECT   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c Division of Environmental Management and Technical Services   (United States)

^d City of Los Angeles   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONTAMINANTS OF EMERGING CONCERNS; EXTRACELLULAR MATRICES; FOCAL ADHESION ASSEMBLY; INDUSTRIAL COMPOUNDS; MUNICIPAL WASTEWATERS; PERSONAL CARE PRODUCTS; PHYSIOLOGICAL RESPONSE; PLASMA VITELLOGENIN;

CELL DEATH; DETOXIFICATION; METABOLISM; TRANSCRIPTION; WASTEWATER TREATMENT;

EFFLUENTS;

4 OCTYLPHENOL; 4,4' ISOPROPYLIDENEDIPHENOL; ATENOLOL; ATORVASTATIN; ATRAZINE; BENZOPHENONE; BUTYLATED HYDROXYANISOLE; CAFFEINE; CARBAMAZEPINE; DIAZEPAM; DICLOFENAC; DIETHYLTOLUAMIDE; ESTRADIOL; ESTRONE; ETHINYLESTRADIOL; FLUOXETINE; GEMFIBROZIL; IBUPROFEN; IOPROMIDE; MEPROBAMATE; MUSK KETONE; NAPROXEN; NONYLPHENOL; PHENYTOIN; PRIMIDONE; PROGESTERONE; SULFAMETHOXAZOLE; TESTOSTERONE; TRICLOSAN; TRIMETHOPRIM;

CONCENTRATION (COMPOSITION); CYPRINID; DETOXIFICATION; EFFLUENT; GENE EXPRESSION; GENOTOXICITY; OVIPOSITION; PHYSIOLOGY; POLLUTION EXPOSURE; SECONDARY SEXUAL CHARACTERISTICS; SEWAGE TREATMENT;

APOPTOSIS; ARTICLE; DETOXIFICATION; DRUG INDUSTRY; EFFLUENT; EXTRACELLULAR MATRIX; GENE EXPRESSION; LIPID TRANSPORT; MUNICIPAL SOLID WASTE; NONHUMAN; OXIDATIVE STRESS; PIMEPHALES PROMELAS; STEROID METABOLISM; TRANSCRIPTOMICS; WASTE WATER;

ANIMALS; CYPRINIDAE; GENE EXPRESSION REGULATION; LIVER; MALE; SEX CHARACTERISTICS; VITELLOGENINS; WASTE DISPOSAL, FLUID; WASTE WATER; WATER POLLUTANTS, CHEMICAL;

EID: 84885130120     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es401942n     Document Type: Article

References (61)

1. Kolpin, D. W.; Skopec, M.; Meyer, M. T.; Furlong, E. T.; Zaugg, S. D. Urban contribution of pharmaceuticals and other organic wastewater contaminants to streams during differing flow conditions Sci. Total Environ. 2004, 328 (1-3) 119-130
2. Vidal-Dorsch, D. E.; Bay, S. M.; Maruya, K.; Snyder, S. A.; Trenholm, R. A.; Vanderford, B. J. Contaminants of emerging concern in municipal wastewater effluents and marine receiving water. In SCCWRP Annual Report; Schiff, K.; Miller, K., Eds.; Southern California Coastal Water Research Project (SCCWRP): Costa Mesa, CA, 2011; pp 351-364.
3. Maruya, K. A.; Vidal-Dorsch, D. E.; Bay, S. M.; Kwon, J. W.; Xia, K.; Armbrust, K. L. Organic contaminants of emerging concern in sediments and flatfish collected near outfalls discharging treated wastewater effluent to the Southern California Bight. In SCCWRP Annual Report; Schiff, K.; Miller, K., Eds.; Southern California Coastal Water Research Project (SCCWRP): Costa Mesa, CA, 2011; pp 365-373.
4. Vajda, A. M.; Barber, L. B.; Gray, J. L.; Lopez, E. M.; Bolden, A. M.; Schoenfuss, H. L.; Norris, D. O. Demasculinization of male fish by wastewater treatment plant effluent Aquat. Toxicol. 2011, 103 (3-4) 213-221
5. Garcia-Reyero, N.; Lavelle, C. M.; Escalon, B. L.; Martinović, D.; Kroll, K. J.; Sorensen, P. W.; Denslow, N. D. Behavioral and genomic impacts of a wastewater effluent on the fathead minnow Aquat. Toxicol. 2011, 101 (1) 38-48
6. Björkblom, C.; Högfors, E.; Salste, L.; Bergelin, E.; Olsson, P.-E.; Katsiadaki, I.; Wiklund, T. Estrogenic and androgenic effects of municipal wastewater effluent on reproductive endpoint biomarkers in three-spined stickleback (Gasterousteus aculeatus) Environ. Toxicol. Chem. 2009, 28 (5) 1063-1071
7. Vajda, A. M.; Barber, L. B.; Gray, J. L.; Lopez, E. M.; Woodling, J. D.; Norris, D. O. Reproductive disruption in fish downstream from an estrogenic wastewater effluent Environ. Sci. Technol. 2008, 42 (9) 3407-3414
8. Burkhardt-Holm, P.; Segner, H.; Burki, R.; Peter, A.; Schubert, S.; Suter, M. J. F.; Borsuk, M. E. Estrogenic endocrine disruption in Switzerland: Assessment of fish exposure and effects Chimia 2008, 62 (5) 376-382
9. Gros, M.; Petrovic, M.; Barcelo, D. Wastewater treatment plants as a pathway for aquatic contamination by pharmaceuticals in the Ebro River basin (northeast Spain) Environ. Toxicol. Chem. 2007, 26 (8) 1553-1562
10. 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 Proc. Natl. Acad. Sci., U. S. A. 2007, 104 (21) 8897-8901
11. Folmar, L.; Gardner, G. R.; Schreibman, M. P.; Magliulo, C. L.; Mills, L. J.; Zaroogian, G.; Gutjahr-Gobell, R. E.; Haebler, R.; Horowitz, D. B.; Denslow, N. D. Vitellogenin-induced pathology in male summer flounder (Paralichthys dentatus) Aquat. Toxicol. 2001, 51 (4) 431-441
12. Garcia-Reyero, N.; Kroll, K. J.; Liu, L.; Orlando, E. F.; Watanabe, K. H.; Sepulveda, M. S.; Villeneuve, D. L.; Perkins, E. J.; Ankley, G. T.; Denslow, N. Gene expression responses in male fathead minnows exposed to binary mixtures of an estrogen and antiestrogen BMC Genomics 2009, 10 308
13. Garcia-Reyero, N.; Villeneuve, D. L.; Kroll, K. J.; Liu, L.; Orlando, E. F.; Watanabe, K. H.; Sepulveda, M. S.; Ankley, G. T.; Denslow, N. Expression signatures for a model androgen and antiandrogen in the fathead minnow (Pimephales promelas) ovary Environ. Sci. Technol. 2009, 43 (7) 2614-2619
14. Vidal-Dorsch, D. E.; Bay, S. M.; Mays, M. A.; Greenstein, D. J.; Young, D.; Schlenk, D.; Kelley, K. M. Biological responses of marine flatfish exposed to effluent. In SCCWRP Annual Report; Weisberg, S. B.; Miller, K., Eds.; Southern California Coastal Water Research Project: Costa Mesa, CA, 2010; pp 239-250.
15. Garcia-Reyero, N.; Barber, D.; Gross, T.; Denslow, N. Modeling of gene expression pattern alteration by p, p ′-DDE and dieldrin in largemouth bass Mar. Environ. Res. 2006, 62, S415-S419
16. Russom, C. L.; Bradbury, S. P.; Broderius, S. J.; Hammermeister, D. E.; Drummond, R. A. Predicting modes of action from chemical structure: Acute toxicity in the fathead minnow (Pimephales promelas) Environ. Toxicol. Chem. 1997, 16 (5) 948-967
17. U.S. EPA. Methods for Measuring the Acute Toxicity of Effluents and Receiving Waters to Freshwater and Marine Organisms; EPA-821-R-02-012; U.S. Environmental Protection Agency, Office of Water: Washington, DC, 2002; p 266.
18. U.S. EPA. Short-Term Methods for Estimating the Chronic Toxicity of Effluents and Receiving Waters to Freshwater Organisms; EPA-821-R-02-013; U.S. Environmental Protection Agency: Washington, DC, 2002.
19. Poynton, H. C.; Loguinov, A. V.; Varshavsky, J. R.; Chan, S.; Perkins, E. J.; Vulpe, C. D. Gene expression profiling in Daphnia magna. Part I: Concentration-dependent profiles provide support for the no observed transcriptional effect level Environ. Sci. Technol. 2008, 42 (16) 6250-6256
20. Poynton, H. C.; Zuzow, R.; Loguinov, A. V.; Perkins, E. J.; Vulpe, C. D. Gene expression profiling in Daphnia magna. Part II: Validation of a copper specific gene expression signature with effluent from two copper mines in California Environ. Sci. Technol. 2008, 42 (16) 6257-6263
21. Filby, A. L.; Tyler, C. R. Molecular characterization of estrogen receptors 1, 2a, and 2b and their tissue and ontogenic expression profiles in fathead minnow (Pimephales promelas) Biol. Reprod. 2005, 73 (4) 648-62
22. Filby, A. L.; Shears, J. A.; Drage, B. E.; Churchley, J. H.; Tyler, C. R. Treatments of wastewater effluents on estrogenic and reproductive health impacts in fish Environ. Sci. Technol. 2010, 44 (11) 4348-4354
23. Gunnarsson, L.; Kristiansson, E.; Forlin, L.; Nerman, O.; Larsson, D. G. J. Sensitive and robust gene expression changes in fish exposed to estrogen-A microarray approach BMC Genomics 2007, 8 (1) 149
24. Garcia-Reyero, N.; Adelman, I. R.; Martinović, D.; Liu, L.; Denslow, N. D. Site-specific impacts on gene expression and behavior in fathead minnows (Pimephales promelas) exposed in situ to streams adjacent to sewage treatment plants BMC Bioinform. 2009, 10, 1-12
25. Levine, S. L.; Oris, J. T. CYP1A expression in liver and gill of rainbow trout following waterborne exposure: Implications for biomarker determination Aquat. Toxicol. 1999, 46 (3-4) 279-287
26. Sabo-Attwood, T.; Blum, J. L.; Kroll, K. J.; Patel, V.; Birkholz, D.; Szabo, N. J.; Fisher, S. Z.; McKenna, R.; Campbell-Thompson, M.; Denslow, N. D. Distinct expression and activity profiles of largemouth bass (Micropterus salmoides) estrogen receptors in response to estradiol and nonylphenol J. Mol. Endocrinol. 2007, 39, 223-237
27. 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 J. Toxicol. Environ. Health, Part A 2006, 69 (19) 1763-1779
28. Martyniuk, C. J.; Spade, D. J.; Blum, J. L.; Kroll, K. J.; Denslow, N. D. Methoxychlor affects multiple hormone signaling pathways in the largemouth bass (Micropterus salmoides) liver Aquat. Toxicol. 2011, 101 (3-4) 483-492
29. Gagné, F.; Andre, C.; Cejka, P.; Hausler, R.; Fournier, M. Evidence of neuroendocrine disruption in freshwater mussels exposed to municipal wastewaters Sci. Total Environ. 2011, 409, 3711-3718
30. Thorpe, K. L.; Benstead, R.; Hutchinson, T. H.; Tyler, C. R. Associations between altered vitellogenin concentrations and adverse health effects in fathead minnow (Pimephales promelas) Aquat. Toxicol. 2007, 85, 176-183
31. Vidal-Dorsch, D. E.; Bay, S. M.; Ribecco, C.; Sprague, L. J.; Angert, M.; Ludka, C.; Carnevali, O.; Greenstein, D. J.; Schlenk, D.; Kelley, K. M.; Reyes, J. A.; Snyder, S.; Vanderford, B.; Wiborg, L. C.; Petschauer, D.; Sasik, R.; Baker, M.; Hardiman, G. Genomic and phenotypic response of hornyhead turbot exposed to municipal wastewater effluents. Aquat. Toxicol. 2013, 140-141, 174-184
32. Liao, T.; Guo, Q. L.; Jin, S. W.; Cheng, W.; Xu, Y. Comparative responses in rare minnow exposed to 17ß-estradiol during different life stages Fish Physiol. Biochem. 2008, 600 (35) 341-349
33. Brian, J. V.; Harris, C. A.; Scholze, M.; Backhaus, T.; Booy, P.; Lamoree, M.; Pojana, G.; Jonkers, N.; Runnalls, T.; Bonfà, A.; Marcomini, A.; Sumpter, J. P. Accurate prediction of the response of freshwater fish to a mixture of estrogenic chemicals Environ. Health Perspect. 2005, 113 (6) 721-728
34. Bay, S. M.; Vidal-Dorsch, D. E.; Schlenk, D.; Kelley, K. M.; Maruya, K. A.; Gully, J. R. Integrated coastal effects study: Synthesis of findings Environ. Toxicol. Chem. 2012, 31 (12) 2711-2722
35. Meina, E. G.; Lister, A.; Bosker, T.; Servos, M.; Munkittrick, K.; MacLatchy, D. Effects of 17-ethinylestradiol (EE2) on reproductive endocrine status in mummichog (Fundulus heteroclitus) under differing salinity and temperature conditions Aquat. Toxicol. 2013, 134-135, 92-103
36. Shappell, N. W.; Hyndman, K. M.; Bartell, S. E.; Schoenfuss, H. L. Comparative biological effects and potency of 17a-and 17b-estradiol in fathead minnows Aquat. Toxicol. 2010, 100, 1-8
37. Parrott, J. L. Overview of methodology and endpoints in fathead minnow lifecycle tests assessing pulp and paper mill effluents Water Qual. Res. J. Can. 2005, 40 (3) 334-346
38. Liney, K. E.; Hagger, J. A.; Tyler, C. R.; Depledge, M. H.; Galloway, T. S.; Jobling, S. Health effects in fish of long-term exposure to effluents from wastewater treatment works Environ. Health Perspect. 2006, 114 (1) 81-89
39. Honda, S.; Hjelmeland, L. M.; Handa, J. T. Oxidative stress-induced single-strand breaks in chromosomal telomeres of human retinal pigment epithelial cells in vitro Invest. Ophthalmol. Visual Sci. 2001, 42, 2139-2144
40. Blom, I. E.; Goldschmeding, R.; Leask, A. Gene regulation of connective tissue growth factor: New targets for antifibrotic therapy? Matrix Biol. 2002, 21, 473-482
41. Li, K.; Li, Y.; Shelton, J. M.; Richardson, J. A.; Spencer, E.; Chen, Z. J.; Wang, X.; Williams, R. S. Cytochrome c deficiency causes embryonic lethality and attenuates stress-induced apoptosis Cell 2000, 101, 389-399
42. Thibaut, R.; Schnell, S.; Porte, C. The interference of pharmaceuticals with endogenous and xenobiotic metabolizing enzymes in carp liver: An in-vitro study Environ. Sci. Technol. 2006, 40 (16) 5154-5160
43. Fujii-Kuriyama, Y.; Mimura, J. Molecular mechanisms of AhR functions in the regulation of cytochrome P450 genes Biochem. Biophys. Res. Commun. 2005, 338, 311-317
44. Cuklev, F.; Gunnarsson, L.; Cvijovic, M.; Kristiansson, E.; Rutgersson, C.; Björlenius, B.; Larsson, D. G. J. Global hepatic gene expression in rainbow trout exposed to sewage effluents: A comparison of different sewage treatment technologies Sci. Total Environ. 2012, 106 (114) 427-428
45. Osachoff, H. L.; van Aggelen, G. C.; Mommsen, T. P.; Kennedy, C. J. Concentration-response relationships and temporal patterns in hepatic gene expression of Chinook salmon (Oncorhynchus tshawytscha) exposed to sewage Comp. Biochem. Physiol. 2013, 8 (1) 32-44
46. Wintz, H.; Yoo, L. J.; Loguinov, A.; Wu, Y.-Y.; Steevens, J. A.; Holland, R. D.; Beger, R. D.; Perkins, E. J.; Hughes, O.; Vulpe, C. D. Gene expression profiles in fathead minnow exposed to 2,4-DNT: Correlation with toxicity in mammals Toxicol. Sci. 2006, 94 (1) 71-82
47. Skolness, S. Y.; Durhan, E. J.; Jensen, K. M.; Kahl, M. D.; Makynen, E. A.; Villeneuve, D. L.; Ankley, G. T. Effects of gemfibrozil on lipid metabolism, steroidogenesis, and reproduction in the fathead minnow (Pimephales promelas) Environ. Toxicol. Chem. 2012, 31 (11) 2615-2624
48. Acevedo, R.; Parnell, P. G.; Villanueva, H.; M, C. L.; Gimenez, T.; Gray, S. L.; Baldwin, W. S. The contribution of hepatic steroid metabolism to serum estradiol and estriol concentrations in nonylphenol treated MMTVneu mice and its potential effects on breast cancer incidence and latency J. Appl. Toxicol. 2005, 25 (5) 339-353
49. Livingstone, D. R.; Mitchelmore, C. L.; O'Hara, S. C.; Lemaire, P.; Sturve, J.; Förlin, L. Increased potential for NAD(P)H-dependent reactive oxygen species production of hepatic subcellular fractions of fish species with in vivo exposure to contaminants Mar. Environ. Res. 2000, 50 (1-5) 57-60
50. Poopal, R. K.; Ramesh, M.; Dinesh, B. Short-term mercury exposure on Na(+)/K(+)-ATPase activity and ionoregulation in gill and brain of an Indian major carp, Cirrhinus mrigala J. Trace Elements Med. Biol. 2013, 27 (1) 70-75
51. Hornberger, T. A.; Chu, W. K.; Mak, Y. W.; Hsiung, J. W.; Huang, S. A.; Chien, S. The role of phospholipase D and phosphatidic acid in the mechanical activation of mTOR signaling in skeletal muscle Proc. Natl. Acad. Sci., U. S. A. 2006, 103 (12) 4741-4746
52. Andreasen, E. A.; Mathew, L. K.; Tanguay, R. L. Regenerative growth is impacted by TCDD: Gene expression analysis reveals extracellular matrix modulation Toxicol. Sci. 2006, 92 (1) 254-269
53. Thorpe, K. L.; Cummings, R. I.; Hutchinson, T. H.; Scholze, M.; Brighty, G.; Sumpter, J. P.; Tyler, C. R. Relative potencies and combination effects of steroidal estrogens in fish Environ. Sci. Technol. 2003, 37, 1142-1149
54. Harrisa, C. A.; Briana, J. V.; Pojanab, G.; Lamoreec, M.; Booyc, P.; Marcominib, A.; Sumptera, J. P. The influence of a surfactant, linear alkylbenzene sulfonate, on the estrogenic response to a mixture of (xeno)estrogens in vitro and in vivo Aquat. Toxicol. 2009, 91 (1) 95-98
55. Weisbrod, C. J.; Kunz, P. Y.; Zenker, A. K.; Fent, K. Effects of the UV filter benzophenone-2 on reproduction in fish Toxicol. Appl. Pharmacol. 2007, 225, 255-266
56. Drewes, J. E.; Dickenson, E.; Snyder, S. A. Contributions of Household Chemicals to Sewage and Their Relevance to Municipal Wastewater Systems and the Environment; Report 03-CTS-21UR; Water Environment Research Foundation (WERF): Alexandria, VA, 31 Mar 2009.
57. Pottinger, T. G.; Cook, A.; Jürgens, M. D.; Rhodes, G.; Katsiadaki, I.; Balaam, J. L.; Smith, A. J.; Matthiessen, P. Effects of sewage effluent remediation on body size, somatic RNA: DNA ratio, and markers of chemical exposure in three-spined sticklebacks Environ. Int. 2011, 37 (1) 158-69
58. Vidal-Dorsch, D. E.; Bay, S. M.; Maruya, K.; Snyder, S. A.; Trenholm, R. A.; Vanderford, B. J. Contaminants of emerging concern in municipal wastewater effluents and marine receiving water Environ. Toxicol. Chem. 2012, 31 (12) 2674-2682
59. Ankley, G. T.; Bennett, R. S.; Erickson, R. J.; Hoff, D. J.; Hornung, M. W.; Johnson, R. D.; Mount, D. R.; Nichols, J. W.; Russom, C. L.; Schmieder, P. K.; Serrrano, J. A.; Tietge, J. E.; Villeneuve, D. L. Adverse outcome pathways: A conceptual framework to support ecotoxicology research and risk assessment Environ. Toxicol. Chem. 2010, 29 (3) 730-741
60. Bowman, C. J.; Kroll, K. J.; Folmar, L. C.; Denslow, N. D. Estrogen-induced vitellogenin mRNA and protein in sheepshead minnow (Cyprinodon variegatus) Gen. Comp. Endrocrinol. 2000, 120, 300-313
61. Miller, D. H.; Jensen, K. M.; Villeneuve, D. L.; Kahl, M. D.; Makynen, E. A.; Durhan, E. J.; Ankley, G. T. Linkage of biochemical responses to population-level effects: A case study with vitellogenin in the fathead minnow (Pimephales promelas) Environ. Toxicol. Chem. 2007, 26 (3) 521-527