In vivo and in vitro liver and gill EROD activity in rainbow trout (Oncorhynchus mykiss) exposed to the beta-blocker propranolol

Environmental Toxicology

Volumn 27, Issue 10, 2012, Pages 573-582

  Bartram, Abigail E ^a   Winter, Matthew J ^a   Huggett, Duane B ^b,d   Mccormack, Paul ^a   Constantine, Lisa A ^b   Hetheridge, Malcolm J ^a   Hutchinson, Thomas H ^a,e   Kinter, Lewis B ^a   Ericson, Jon F ^b   Sumpter, John P ^c   Owen, Stewart F ^a,c  

^a ASTRAZENECA   (United Kingdom)

^b PFIZER INC   (United States)

^c BRUNEL UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF NORTH TEXAS   (United States)

^e CENTRE FOR ENVIRONMENT   (United Kingdom)

Author keywords

Cytochrome (CYP); Environmental risk assessment (ERA); Pharmaceuticals in the environment (PIE); Reduction replacement refinement (3Rs); Xenobiotic metabolism

Indexed keywords

ACTIVITY ANALYSIS; ADRENERGIC RECEPTORS; BIOLOGICAL EFFECTS; CELL PREPARATION; ENVIRONMENTAL RISK ASSESSMENT; EROD ACTIVITY; HUMAN THERAPEUTICS; IN-VITRO; IN-VIVO; ONCORHYNCHUS MYKISS; PHYSIOLOGICAL SYSTEMS; RAINBOW TROUT; TIME COURSE; XENOBIOTIC METABOLISM;

FISH; METABOLISM; RISK ASSESSMENT; TISSUE;

PHYSIOLOGY;

ETHOXYRESORUFIN DEETHYLASE; LIVER ENZYME; PROPRANOLOL;

CYTOCHROME; DRUG; ENDOCRINE DISRUPTOR; ENVIRONMENTAL RISK; ENZYME ACTIVITY; METABOLISM; NONTARGET ORGANISM; PHYSIOLOGICAL RESPONSE; POLLUTION EXPOSURE; RISK ASSESSMENT; SALMONID; SURFACE WATER; XENOBIOTICS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG METABOLISM; ENZYME ACTIVITY; ENZYME INDUCTION; FEMALE; FIRST PASS EFFECT; GILL; LIVER CELL; LIVER WEIGHT; NONHUMAN; PRIORITY JOURNAL; RAINBOW TROUT; WATER CONTAMINATION; WATER QUALITY;

ADRENERGIC BETA-ANTAGONISTS; ANIMALS; CELLS, CULTURED; CYTOCHROME P-450 CYP1A1; FEMALE; GILLS; HEPATOCYTES; LIVER; ONCORHYNCHUS MYKISS; PROPRANOLOL;

ANIMALIA; ONCORHYNCHUS MYKISS; SALMONIDAE; VERTEBRATA;

EID: 84866323010     PISSN: 15204081     EISSN: 15227278     Source Type: Journal    
DOI: 10.1002/tox.20684     Document Type: Article

References (48)

1. Andreozzi R, Raffaele M, Nicklas P. 2003. Pharmaceuticals in STP effluents and their solar photodegradation in aquatic environment. Chemosphere 50: 1319-1330.
2. Ashton D, Hilton M, Thomas KV. 2004. Investigating the environmental transport of human pharmaceuticals to streams in the United Kingdom. Sci Total Environ 333: 167-184.
3. Ayscough NJ, Fawell J, Franklin G, Young W. 2000. Review of human pharmaceuticals in the environment. R&D Technical Report P390, Environment Agency, Bristol, UK. 106 p.
4. Bendz D, Paxeus NA, Ginn TR, Loge FJ. 2005. Occurrence and fate of pharmaceutically active compounds in the environment, a case study: Hoje River in Sweden. J Hazard Mater 122: 195-204.
5. Bourne GR. 1981. The metabolism of β-adrenoreceptor blocking drugs. Prog Drug Metab 6: 77-110.
6. Carlsson C, Part P, Brunstrom B. 1999. 7-Ethoxyresorufin O-deethylase induction in cultured gill epithelial cells from rainbow trout. Aquat Toxicol 47: 117-128.
7. Corcoran J, Winter MJ, Tyler CR. 2010. Pharmaceuticals in the aquatic environment: A critical review of the evidence for health effects in fish. Crit Rev Toxicol 40: 287-304.
8. Crooks IR. 2007. Development of a potential in vitro Rainbow trout (Oncorhynchus mykiss) primary hepatocyte assay for use in ecotoxicology. MSc thesis in Toxicology. School of Biosciences, University of Birmingham. 66 p. (Copy available on request from authors)
9. Daughton CG. 2002. Environmental stewardship and drugs as pollutants. Lancet 360: 1035-1036.
10. Daughton CG, Ruhoy IS. 2009. Environmental footprint of pharmaceuticals: The significance of factors beyond direct excretion to sewers. Environ Toxicol Chem 28: 2495-2521.
11. Fent K, Weston AA, Caminada D. 2006. Ecotoxicology of human pharmaceuticals. Aquat Toxicol 79: 122-159.
12. Gagne F, Blaise C, Andre C. 2006. The occurrence of pharmaceutical products in a municipal effluent and toxicity to rainbow trout (Oncorhynchus mykiss) hepatocytes. Ecotoxicol Environ Saf 64: 329-336.
13. Gunnarsson L, Jauhiainen A, Kristiansson E, Nerman O, Larsson DGJ. 2008. Evolutionary conservation of human drug targets in organisms used for environmental risk assessments. Environ Sci Technol 42: 5807-5813.
14. Heilmann LJ, Sheen YY, Bigelow SW, Nebert DW. 1988. Trout P450A1: cDNA and deduced protein sequence, expression in liver and evolutionary significance. DNA 7: 379-387.
15. Hilton MJ, Thomas KV, Ashton D. 2003. Targeted monitoring programme for pharmaceuticals in the aquatic environment. R&D Technical Report P6012/06/TR. Accessed athttp://publications.environment-agency.gov.uk/pdf/SP6012-06-TR-e-p.pdf (04/06/2007).
16. Huggett DB, Ericson JF, Cook JC, Williams RT. 2004. Plasma concentrations of human pharmaceuticals as predictors of pharmacological responses in fish. In: Kummerer K, editor. Pharmaceuticals in the Environment: Sources, Fate, effects and Risks, 2nd ed. Berlin: Springer-Verlag. pp 373-386.
17. Imamura Y, Wu X, Noda A. Noda H. 2002. Side-chain metabolism of monamine oxidase and mitochondrial aldehyde dehydrogenase in the metabolism of N-desisopropylpropranolol to naphthoxylactic acid in rat liver. Life Sci 70: 2687-2697.
18. Jonsson EM, Abrahamson A, Brunstrom B. Brandt I. 2006. 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: 226-232.
19. Kümmerer K. 2009. The presence of pharmaceuticals in the environment due to human use-Present knowledge and future challenges. J Environ Man 90: 2354-2366.
20. Laville N, Aït-Aïssa S, Gomez E, Casellas C, Porcher JM. 2004. Effects of human pharmaceuticals on cytotoxicity. EROD activity and ROS production in fish hepatocytes. Toxicology 196: 41-55.
21. Lin AY, Reinhard M. 2005. Photodegradation of common environmental pharmaceuticals and estrogens in river water. Environ Toxicol Chem 24: 1303-1309.
22. Liu Q.-T, Cumming RI, Sharpe AD. 2009. Photo-induced environmental depletion processes of β-blockers in river waters. Photochem Photobiol Sci 8: 768-777.
23. Masubuchi Y, Hosokawa S, Horie T, Suzuki T, Ohmori S, Kitada M, Narimatsu S. 1994. Cytochrome P450 isozymes involved in propranolol metabolism in human liver microsomes. The role of CYP2D6 as ring-hydroxylase and CYP1A2 as N-desisopropylase. Drug Metab Dispos 22: 909-915.
24. Meton I, Fernandez F, Baanante IV. 2003. Short-and long-term effects of refeeding on the key enzyme activites in glysolysis-gluconogenesis in the liver of gilthead seabream (Sparus aurata). Aquaculture 226: 99-107.
25. Morrison HG, Loeksiak MF, Cornell NW, Sogin ML, Stegeman JJ. 1995. Identification of cytochrome P4501A (CYP1A) genes from two teleost fish, toadfish (Opsanus tau) and scup (Stenotomus chrysops) and phylogenetic analysis of CYP1A genes. Biochem J 308: 97-104.
26. Mosadeghi S, Furnes B, Matsuo AYO, Schlenk D. 2007. Expression and characterisation of cytochrome P450 2X1 in channel catfish (Ictalurus punctatus). Biochim Biophys Acta 1770: 1045-1052.
27. Nabb DL, Mingoia RT, Yang C-H, Han X. 2006. Comparison of basal level metabolic enzyme activities of freshly isolated hepatocytes from rainbow trout (Oncorhynchus mykiss) and rat. Aquat Tox 80: 52-59.
28. Narimatsu S, Mochida M, Ueno K, Horie T, Yamamoto S, Suzuki T. 2002. Induction of cytochrome P450 1A1 in mice by repeated oral administration of propranolol. Drug Metab Pharmacokinet 17: 54-59.
29. Owen SF, Giltrow E, Huggett DB, Hutchinson TH, Saye J-A, Winter MJ, Sumpter JP. 2007. Comparative physiology, pharmacology and toxicology of β-blockers in fish: Mammals versus fish. Aquatic Tox 82: 145-162.
30. Owen SF, Huggett DB, Hutchinson TH, Hetheridge MJ, Kinter LB, Ericson JF, Sumpter JP. 2009. Uptake of propranolol, a cardiovascular pharmaceutical, from water into fish plasma and its effects on growth and organ biometry. Aquatic Tox 93: 217-224.
31. Packard GC, Boardman TJ. 1999. The use of percentages and size specific indices to normalize physiological data for variation in body size: Wasted time, wasted effort? Comp Biochem Physiol Part A: Mol Integr Physiol 122: 37-44.
32. Randall DJ, Connell DW, Yang R, Wu SS. 1998. Concentrations of persistent lipophilic compounds in fish are determined by exchange across the gills, not through the food chain. Chemosphere 37: 1263-1270.
33. Regenthal R, Krueger M, Koeppel C, Preiss R. 1999. Drug levels: Therapeutic and toxic serum/plasma concentrations of common drugs. J Clin Monit 15: 529-544.
34. Roberts PH, Thomas KV. 2005. The occurrence of selected pharmaceuticals in wastewater effluent and surface waters of the lower Tyne catchments. Sci Total Environ 356: 143-153.
35. Sader MD, Ash R, Sundqvist J, Olsson PE, Andersson TB. 1996. Phenobarbital induction of CYP1A1 gene expression in a primary culture of rainbow trout hepatocytes. J Biol Chem 271: 17635-17643.
36. Scholz S, Kordes C, Hamann J, Gutzeit HO. 2004. Induction of vitellogenin in vivo and in vitro in the model teleost medaka (Oryzias latipes): Comparison of gene expression and protein levels. Mar Environ Res 57: 235-244.
37. Sowinski M, Lima JJ, Burlew B.S, Massies JD, Johnson JA. 1996. Racial differences in propranolol enantiomer kinetics following simultaneous i.v. and oral administration. Br J Pharmacol 42: 339-346.
38. Stien X, Amichot M, Berge J-B, Lafaurie M. 1998. Molecular cloning of a CYP1A cDNA from the teleost fish Dicentrarchus labrax. Comp Biochem Physiol Part C: Toxicol Pharmacol 121: 241-248.
39. Ternes TA. 1998. Occurrence of drugs in German sewage treatment plants and rivers. Water Res 32: 3245-3600.
40. Thibaut R, Schnell S. Porte C. 2006. The interference of pharmaceuticals with endogenous and xenobiotic metabolizing enzymes in carp liver: An in vitro study. Environ Sci Technol 40: 5154-5160.
41. van der Oost R. 2003. Fish bioaccumulation and biomarkers in environmental risk assessment: A review. Environ Toxicol Pharmacol 13: 57-149.
42. Walle T, Walle UK, Olanoff LS. 1985. Quantitative account of propranolol metabolism in urine of normal man. Drug Metab Dispos 13: 204-209.
43. Weisbrod AV, Sahi J, Segner H, James MO, Nichols J, Schultz I, Erhardt S, Cowan-Ellsberry C, Bonnell M, Hoeger B. 2009. The state of in vitro science for use in bioaccumulation assessments for fish. Environ Tox Chem 28: 86-96.
44. Whyte JJ, Jung RE, Schmitt CJ, Tillitt DE. 2000. Ethoxyrecorufin-O-deethylase (EROD) activity in fish as a biomarker of chemical exposure. Crit Rev Toxicol 30: 347-570.
45. Winter MJ, Verweij F, Garofalo E, Ceradini S, McKenzie DJ, Williams MA, Taylor EW, Butler PJ, Van der Oost R. Chipman JK. 2005. Tissue levels and biomarkers of organic contaminants in feral and caged chub (Leucisus cephalus) from rivers in the West Midlands, UK. Aquat Toxicol 73: 394-405.
46. Winter MJ, Owen SF, Murray-Smith R, Panter GH, Hetheridge MJ, Kinter LB. 2010. Using data from drug discovery and development to aid the aquatic Environmental Risk Assessment of human pharmaceuticals: Concepts, considerations and challenges. Integ Environ Assess Manage 6; 38-51.
47. Yoshimoto K, Echizen H, Chiba K, Tani M, Ishizaki T. 1995. Identification of human CYP isoforms involved in the metabolism of propranolol enantiomers-N-desisopropylation is mediated mainly by CYP1A2. Br J Clin Pharmacol 39: 421-431.
48. Zuccato E, Castiglioni S, Fanelli R. 2005. Identification of pharmaceuticals for human use contaminating the Italian aquatic environment. J Hazard Mater 122: 205-209.