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Research Article

Ethoxyresorufin-O-deethylase (EROD) Activity in Fish as a Biomarker of Chemical Exposure

J. J. Whyte U.S. Geological Survey (USGS) Cooperative Fish and Wildlife Research Unit, University of Missouri-Columbia, c/o USGS, Columbia Environmetal Research Center (CERC), 4200 New Haven Road, Columbia Missouri 65201
,
R. E. Jung AScI, c/o USGS-CERC. Present Address: USGS, Patuxent Environmental Research Center, 12100 Beech Forest Road, Laurel, MD 20708
,
C. J. Schmitt USGS-CERC
&
D. E. Tillitt USGS-CERC
Pages 347-570 | Published online: 29 Sep 2008

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  • Engwall M, Brunström B, Brewer A, and Norrgren L. 1994. Cytochrome P450IA induction by a coplanar PCB, a PAH mixture, and PCB-contaminated sediment extracts following microinjection of rainbow trout sac-fry. Aquat Toxicol 30:311–24.
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  • Eitzer BD. 1993. Comparison of point and nonpoint sources of polychlorinated dibenzo-p-dioxins and polychlorinated dibenofurans to sediments of the Housatonic River. [Erra- tum]. Environ Sci Technol 27:2919.
  • Elcombe CR and Lech JJ. 1978. Induction of monooxygen- ation in rainbow trout by polybrominated biphenyls: a comparative study. Environ Health Perspect 23:309– 14.
  • Elcombe CR and Lech JJ. 1979. Induction and characterization of hemopro- tein(s) P-450 and monooxygenation in rainbow trout (Salmo gairdneri). Toxicol Appl Pharmacol 49:437- 50.
  • Elonen GE, Spehar RL, Holcombe GW, Johnson RD, Fernandez JD, Erickson RJ, Tietge JE, and Cook PM. 1998. Comparative toxicity of 2,3,7,8-tetrachlorodibenzo- p-dioxin to seven freshwater fish species during early life- stage development. Environ Toxicol Chem 17:472–83.
  • Elskus AA and Stegeman JJ (1989a) Further consideration
  • Elskus AA and Stegeman JJ 1989b. Induced cytochrome P-450 in Fundulus het- eroclitus associated with environmental contamination by polychlorinated biphenyls and polynuclear aromatic hydrocarbons. Mar Environ Res 27:31–50.
  • Elskus AA, Stegeman JJ, Susani LC, Black D, Pruell RJ, and Fluck SJ. 1989. Polychlorinated biphenyls concentration and cytochrome P-450E expression in winter flounder from contaminated environments. Mar Environ Res 28:25–30.
  • Elskus AA, Pruell R, and Stegeman JJ. 1992. Endogenously- mediated, pretranslational suppression of cytochrome P4501A in PCB-contaminated flounder. Mar Environ Res 34:97–101.
  • Enan E and Matsumura F. 1996. Identification of c-Src as the integral component of the cytosolic Ah receptor complex, transducing the signal of 2,3,7,8-tetrachlorodibenzo- p-dioxin (TCDD) through the protein phosphorylation pathway. Biochem Pharmacol 52:1599–612.
  • Engwall M, Brunström B, Brewer A, and Norrgren L. 1994. Cytochrome P450IA induction by a coplanar PCB, a PAH mixture, and PCB-contaminated sediment extracts following microinjection of rainbow trout sac-fry. Aquat Toxicol 30:311–24.
  • Erickson DA, Goodrich MS, and Lech JJ. 1988. The effect of piperonyl butoxide on hepatic cytochrome p450-depen- dent monooxygenase activities in rainbow trout (Salmo gairdneri). Toxicol Appl Pharmacol 94:1–10.
  • Erickson DA, Laib FE, and Lech JJ. 1992. Biotransformation of rotenone by hepatic microsomes following pretreat- ment of rainbow trout with inducers of cytochrome P450. Pestic Biochem Physiol 42:140–50.
  • Ericson G, Liewenborg B, and Balk L. 1995. Comparative 32P-postlabeling analysis of DNA adducts in perch (Perca fluviatilis) from unpolluted and polluted areas in Swed- ish coastal waters. Mar Environ Res 39:303–7.
  • Eufemia NA, Collier TK, Stein JE, Watson DE, and Di Giulio RT. 1997. Biochemical responses to sediment-associated contaminants in brown bullhead (Ameiurus nebulosus) from the Niagara River ecosystem. Ecotoxicology 6: 13–34.
  • Everaarts JM, Sleiderink HM, den Besten PJ, Halbrook RS, and Shugart LR. 1994. Molecular responses as indi- cators of marine pollution: DNA damage and enzyme induction in Limanda limanda and Asterias rubens. En- viron Health Perspect 102:37–43.
  • Fabacher DL. 1982. Hepatic microsomes from freshwater fish. Reduction of benzo(a)pyrene metabolism by the fish anesthetics quinaldine sulfate and tricaine. Comp Bio- chem Physiol 73C:285–8.
  • Fabacher DL and Baumann PC. 1985. Enlarged livers and hepatic microsomal mixed-function oxidase component in tumor-bearing brown bullheads from a chemically contaminated river. Environ Toxicol Chem 4:703–10.
  • Fenet H, Casellas C, and Bontoux J. 1996. Hepatic enzymatic activities of the European eel Anguilla anguilla as a tool for biomonitoring freshwater streams: laboratory and field caging studies. Wat Sci Tech 33:321–9.
  • Fenet H, Casellas C, and Bontoux J. 1998. Laboratory and field-caging studies on hepatic enzymatic activities in European eel and rainbow trout. Ecotoxicol Environ Saf 40:137–43.
  • Fent K and Stegeman JJ. 1993. Effects of tributyltin in vivo on hepatic cytochrome P450 forms in marine fish. Aquat Toxicol 24:219–40.
  • Fent K and Bucheli TD. 1994. Inhibition of hepatic microso- mal monooxygenase system by organotins in vitro in freshwater fish. Aquat Toxicol 28:107–26.
  • Fent K, Woodin B, and Stegeman JJ. 1996. Effects of triphe- nyltin on the hepatic monooxygenase system in marine fish. Mar Environ Res 42:51–2.
  • Firestone D. 1991. Determination of dioxins and furans in foods and biological tissues: review and update. J Assoc Off Anal Chem 74:375–84.
  • Fisk AT, Yarechewski AL, Metner DA, Evans RE, Lockhart WL, and Muir DCG. 1997. Accumulation, depuration and hepatic mixed-function oxidase enzyme induc- tion in juvenile rainbow trout and lake whitefish ex- posed to dietary 2,3,7,8-tetrachlorodibenzo-p-dioxin. Aquat Toxicol 37:201–20.
  • Fitzsimons JD. 1995. A critical review of the effects of contami- nants on early life stage (ELS) mortality of lake trout in the Great Lakes. J Great Lakes Res 21 (Suppl 1):267–76.
  • Flammarion P, Migeon B, and Garric J. 1996. Joint effects of copper sulphate and methidathion on rainbow trout (On- corhynchus mykiss) EROD and AChE activities. Bull Environ Contam Toxicol 56:440–5.
  • Flammarion P, Migeon B, and Garric J 1998. Statistical analysis of cyprinid ethoxyresorufin-O-deethylase data in a large French watershed. Ecotoxicol Environ Saf 40(1/2): 144–153.
  • Flammarion P and Garric J. 1997. Cyprinids EROD activi- ties in low contaminated rivers: a relevant statistical approach to estimate reference levels for EROD bio- marker? Chemosphere 35:2375–88.
  • Flammarion P, Migeon B, Urios S, Morfin P, and Garric J. 1998. Effect of methidathion on the cytochrome P-450 1A in the cyprinid fish gudgeon (Gobio gobio). Aquat Toxicol 42:93–102.
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  • Kloepper-Sams PJ and Stegeman JJ. 1988. Induction of cyto- chrome P-450 in Fundulus heteroclitus: enzyme activ- ity, immunochemical and nucleic acid studies. Mar En- viron Res 24:21–5. 1989. The temporal relationships between P450E protein content, catalytic activity, and mRNA levels in the teleost Fundulus heteroclitus following treatment with β-naphthoflavone. Arch Biochem Biophys 268:525–35.
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  • Kleinow KM, Haasch ML, and Lech JJ. 1986. The effect of tricaine anesthesia upon induction of select P-450 depen- dent monooxygenase activities in rainbow trout (Salmo gairdneri). Aquat Toxicol 8:231–41.
  • Kleinow KM, Melancon MJ, and Lech JJ. 1987. Biotransfor- mation and induction: implications for toxicity, bioaccu- mulation and monitoring of environmental xenobiotics in fish. Environ Health Perspect 71:105–19.
  • Kleinow KM, Droy BF, Buhler DR, and Williams DE. 1990. Interaction of carbon tetrachloride with β-naphthofla- vone-mediated cytochrome P450 induction in winter flounder (Pseudopleuronectes americanus). Toxicol Appl Pharmacol 104:367–74.
  • Kloepper-Sams PJ and Stegeman JJ. 1988. Induction of cyto- chrome P-450 in Fundulus heteroclitus: enzyme activ- ity, immunochemical and nucleic acid studies. Mar En- viron Res 24:21–5. 1989. The temporal relationships between P450E protein content, catalytic activity, and mRNA levels in the teleost Fundulus heteroclitus following treatment with β-naphthoflavone. Arch Biochem Biophys 268:525–35.
  • Kloepper-Sams PJ and Stegeman JJ. 1992. Effects of tempera- ture acclimation on the expression of hepatic cytochrome P4501A mRNA and protein in the fish Fundulus het- eroclitus. Arch Biochem Biophys 299:38–46.
  • Kloepper-Sams PJ, Swanson SM, Marchant T, Schryer R, and Owens JW. 1994. Exposure of fish to biologically treated bleached-kraft effluent. I. Biochemical, physi- ological and pathological assessment of Rocky Moun- tain whitefish (Prosopium williamsoni) and longnose sucker (Catostomus catostomus). Ecotoxicol Environ Saf 13:1469–82.
  • Kloepper-Sams PJ and Benton E. 1994. Exposure of fish to biologically treated bleached-kraft effluent. II. Induc- tion of hepatic cytochrome P4501A in mountain white- fish (Prosopium williamsoni) and other species. Environ Toxicol Chem 13:1483–96.
  • Klotz AV, Stegeman JJ, and Walsh C. 1984. An alternative 7-ethoxyresorufin-O-deethylase activity assay: a con- tinuous visible spectrophotometric method for measure- ment of cytochrome P-450 monooxygenase activity. Anal Biochem 140:138–45.
  • Köhler A and Pluta HJ. 1995. Lysosomal injury and MFO ac- tivity in the liver of flounder (Platichthys flesus L.) in relation to histopathology of hepatic degeneration and carcinogenesis. Mar Environ Res 39:255–60.
  • Kramer VJ and Giesy JP. 1995. Environmental estrogens: a significant risk. Hum Ecol Risk Assess 1:37–42.
  • Kurtz, D. A. 1990. Long-Range Transport of Pesticides. Lewis Publishers, Inc., Chelsea, MI, 462 pp.
  • Kutz FW, Barnes DG, Bretthauer EW, Bottimore DP, and Greim H. 1990. The international toxicity equivalency factors (I-TEF) method of risk assessment for com- plex mixtures of dioxins and related compounds. Toxi- col Environ Chem 26:99–109.
  • Laitinen M, Nieminen M, and Hietanen E. 1982. The effect of pH changes of water on the hepatic metabolism of xenobiotics in fish. Acta Pharmacologica et Toxico- logica 51:24–9.
  • Lange U, Jedamski-Grymlas J, Siebers D, and Karbe L. 1992. Ethoxyresorufin O-deethylase and cytochrome P450 in the liver of dab (Limanda limanda (L.)) from the cen- tral and southern North Sea. Mar Pollut Bull 24:446– 51.
  • Lange U, Danischewski D, and Siebers D. 1993. Regional vari- ability and sexual differences in ethoxyresorufin-O-de- ethylase activities and cytochrome P450 concentrations in the liver of mature dab (Limanda limanda L.) in the German Blight. Heidelberg, Germany, Sept. 25–Sept. 27 1991. Fish: Ecotoxicology and Ecophysiology. Proceedings of an International Symposium.
  • Lange U, Saborowski R, Siebers D, Buchholz F, and Karbe 1998. Temperature as a key factor determining the regional variability of the xenobiotic-inducible ethoxy- resorufin-O-deethylase activity in the liver of dab (Limanda limanda). Can J Fish Aquat Sci 55:328–38.
  • Larsen H, Celander M, and Goksøyr A. 1992. The cytochrome P450 system of Atlantic salmon (Salmo salar). II. Vari- ations in hepatic catalytic activities and isozyme pat- terns during an annual reproductive cycle. Fish Physiol Biochem 10:291–301.
  • Larsson Å, Andersson T, Förlin L, and Härdig J. 1988. Physi- ological disturbances in fish exposed to bleached kraft mill effluents. Wat Sci Tech 20:67–76.
  • Leaver MJ, Pirrit L, and George SG. 1993. Cytochrome P450 1A1 cDNA from plaice (Pleuronectes platessa) and in- duction of P450 1A1 mRNA in various tissues by 3- methylcholanthrene and isosafrole. Mol Mar Biol Bio- technol 2:338–45.
  • Lebo JA, Zajicek JL, Huckins JN, Petty JD, and Peterman PH. 1992. Use of semipermeable membrane devices for in situ monitoring of polycyclic aromatic hydro-carbons in aquatic environments. Chemosphere 25:697–718.
  • Lemaire-Gony S and Lemaire P. 1992. Interactive effects of cadmium and benzo(a)pyrene on cellular structure and biotransformation enzymes of the liver of the European eel Anguilla anguilla. Aquat Toxicol 22:145–60.
  • Lemaire-Gony S, Lemaire P, and Pulsford AL. 1995. Effects of cadmium and benzo(a)pyrene on the immune sys- tem, gill ATPase and EROD activity of European sea bass Dicentrarchus labrax. <i>Aquat Toxicol31:297–313.
  • Lemaire P, Mathieu A, Giudicelli J, and Lafaurie M. 1992a. Effect of benzo[a]pyrene on hepatic biotransformation activities: time course of induction in aquaculture Euro- pean sea bass (Dicentrarchus labrax). Polycyclic Aromat Compd 2:263–73.
  • Lemaire P, Mathieu A, Carrière S, Narbonne JF, Lafaurie M, and Giudicelli J. 1992b. Hepatic biotransformation en- zymes in aquaculture European sea bass (Dicentrarchus labrax): kinetic parameters and induction with benzo(a)py- rene. Comp Biochem Physiol 103B:847–53.
  • Lemaire P, Förlin L, and Livingstone DR. 1996. Responses of hepatic biotransformation and antioxidant enzymes to CYP1A-inducers (3-methylcholanthrene, β-naphtho- flavone) in sea bass (Dicentrarchus labrax), dab (Limanda limanda) and rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 36:141–60.
  • Levine SL, Oris JT, and Wissing TE. 1994. Comparison of P-4501 A1 monooxygenase induction in gizzard shad (Dorosoma cepedianum) following intraperitoneal in- jection or continuous waterborne-exposure with ben- zo[a]pyrene: temporal and dose-dependent studies. Aquat Toxicol 30:61–75. 1995. Influence of environmental factors on the physi- ological condition and hepatic ethoxyresorufin O-de- ethylase (EROD) activity of gizzard shad (Dorosoma cepedianum). Environ Toxicol Chem 14:123–8.
  • Levine SL, Czosnyka H, and Oris JT. 1997. Effect of the fun- gicide clotrimazole on the bioconcentration of ben- zo[a]pyrene in gizzard shad (Dorosoma cepedianum): in vivo and in vitro inhibition of cytochrome P4501A activity. Environ Toxicol Chem 16:306–11.
  • Lindesjöö E, Husoey AM, Petterson I, and Förlin L. 1996. Histopathological and immunohistochemical studies in the roundnose grenadier (Coryphaenoides rupestris) in the Skagerrak, North Sea. Mar Environ Res 421– 4:229–33.
  • Lindström-Seppä P. 1988. Biomonitoring of oil spill in a bo- real archipelago by xenobiotic biotransformation in perch (Perca fluviatilis). Ecotoxicol Environ Saf 15: 162–70.Lindström-Seppä P and Oikari A. 1988. Hepatic xenobiotic biotransformation in fishes exposed to pulpmill effluents. Water Sci Technol 20:167–70.
  • Lindström-Seppä P and Hänninen O. 1988. Sampling and stor- age conditions of rainbow trout liver affects monooxy- genase and conjugation enzymes. Comp Biochem Physiol 89C:221–4.
  • Lindström-Seppä P and Oikari A. 1989a. Biotransformation and other physiological responses in whitefish caged in a lake receiving pulp and paper mill effluents. Ecotoxicol Environ Saf 18:191–203.
  • Lindström-Seppä P and Oikari A. 1989b. Bleached kraft pulpmill effluents and TCDD: effects on biotransformation and testosterone status of mature male rainbow trout (Salmo gairdneri). Mar En- viron Res 28:99–103.
  • Lindström-Seppä P and Oikari A. 1990a. Biotransformation activities of feral fish in waters receiving bleached pulp mill effluents. Environ Toxicol Chem 9:1415–24.
  • Lindström-Seppä P and Oikari A. 1990b. Biotransformation and other toxicological and physiological responses in rainbow trout (Salmo gaird- neri Richardson) caged in a lake receiving effluents of pulp and paper industry. Aquat Toxicol 16:187–204.
  • Lindström-Seppä P, Huuskonen S, Pesonen M, Muona P, and Hänninen O. 1992. Unbleached pulp mill effluents affect cytochrome P450 monooxygenase enzyme activ- ities. Mar Environ Res 34:157–61.
  • Lindström-Seppä P, Korytko PJ, Hahn ME, and Stegeman JJ. 1994. Uptake of waterborne 3,3,4,4-tetrachloro- biphenyl and organ and cell-specific induction of cyto- chrome P4501A in adult and larval fathead minnow Pimephales promelas. Aquat Toxicol 28:147–67.
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