Glutathione, glutathione S-transferase, and glutathione conjugates, complementary markers of oxidative stress in aquatic biota

Environmental Science and Pollution Research

Volumn 19, Issue 6, 2012, Pages 2007-2023

  Hellou, Jocelyne ^a,b   Ross, Neil W ^b,c   Moon, Thomas W ^d  

^a BEDFORD INSTITUTE OF OCEANOGRAPHY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Analyses; Antioxidants; Conjugates; Glutathione; Integration of biomarkers; Metabolites; Oxidative stress; Review

Indexed keywords

BIOLOGICAL MARKER; GLUTATHIONE; GLUTATHIONE TRANSFERASE;

ANTHROPOGENIC SOURCE; ANTIOXIDANT; AQUATIC ORGANISM; BIOMARKER; DRUG; ENVIRONMENTAL FATE; ENZYME ACTIVITY; LITERATURE REVIEW; METABOLITE; METAL; NANOTECHNOLOGY; ORGANIC POLLUTANT; OXIDATION; PESTICIDE; POPULATION PRESSURE; TOXIN; XENOBIOTICS;

ANIMAL; AQUATIC SPECIES; ENVIRONMENTAL MONITORING; METABOLISM; METHODOLOGY; OXIDATIVE STRESS; REVIEW; WATER POLLUTION;

ANIMALS; AQUATIC ORGANISMS; BIOLOGICAL MARKERS; ENVIRONMENTAL MONITORING; GLUTATHIONE; GLUTATHIONE TRANSFERASE; OXIDATIVE STRESS; WATER POLLUTION, CHEMICAL;

EID: 84864101103     PISSN: 09441344     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11356-012-0909-x     Document Type: Review

References (153)

1. Abele D, Puntarulo S (2004) Formation of reactive species and induction of antioxidant defense systems in polar and temperate marine invertebrates and fish. Comp Biochem Physiol 138A: 405-415.
2. Ackman RG (1989) Marine biogenic lipids, fats, and oils, volumes I and II. CRC, Boca Raton, pp 462 and 495.
3. Amado LL, Monserratt JM (2010) Oxidative stress generation by microcystins in aquatic animals: why and how. Environ Int 36: 226-235.
4. Ankley GT, Blazer VS, Reinert RE, Agosin M (1986) Effects of Aroclor 1254 on cytochrome P450-dependent monooxygenase, glutathione-S-transferase and UDP-glucuronyltransferase activities in channel catfish liver. Aquat Toxicol 9: 91-103.
5. Ankley GT, Bennett RS, Erickson RJ, Hoff DJ, Hornung MW, Johnson RD, Mount DR, Nichols JW, Russom CL, Schmieder PK, Serrano JA, Tietge JE, Villeneuve DL (2010) Adverse outcome pathways: a conceptual framework to support ecotoxicology research and risk assessment. Environ Toxicol Chem 29: 730-741.
6. Armknecht SL, Kaattari SL, van Veld PA (1998) An elevated glutathione S-transferase in creosote-resistant mummichog (Fundulus heteroclitus). Aquat Toxicol 41: 1-16.
7. Baganz D, Staaks G, Pfulgmacher S, Steinberg CEW (2004) Comparative study of microcystin-LR-induced changes of two fish species, Danio rerio and Leucaspius delineatus. Environ Toxicol 19: 564-570.
8. Balabaskaran S, Chew S, Segaran M (1986) Studies on glutathione S-transferase in molluscs. Comp Biochem Physiol 85B: 183-192.
9. Ballesteros ML, Wunderlin DA, Bistoni MA (2009) Oxidative stress responses in different organs of Jenynsia multidentata exposed to endosulfan. Ecotoxicol Environ Saf 72: 199-205.
10. Barron MG, Hansen JA, Lipton J (2002) Association between contaminant tissue residue and effects in aquatic organisms. Rev Environ Contam Toxicol 173: 1-37.
11. Baumann PC, Harshbarger JC, Hartman KJ (1990) Relationship between liver tumors and age in brown bullhead populations from two Lake Erie tributaries. Sci Tot Environ 94: 71-87.
12. Beach GB, Quilliam MA, Rouleau C, Croll RP, Hellou J (2010) Bioaccumulation and biotransformation of pyrene and 1-hydroxypyrene by the marine whelk Buccinum undatum. Environ Toxicol Chem 29: 779-788.
13. Beach GB, Hellou J (2011) Bioaccumulation and biotransformation of 1-hydroxypyrene by the marine whelk Neptunea lyrata. Int J Environ Anal Chem 91: 1227-1243.
14. Beattie KA, Ressler J, Wiegand C, Krause E, Codd GA, Steinberg CEW, Pflugmacher S (2003) Comparative effects and metabolism of two microcystins and nodularin in the brine shrimp Artemia salina. Aquat Toxicol 62: 219-226.
15. Biswas SK, Rahman I (2009) Environmental toxicity, redox signaling and lung inflammation: the role of glutathione. Mol Aspects Med 30: 60-76.
16. Blanchette B, Feng X, Singh BR (2007) Marine glutathione S-transferase. Mar Biotechnol 9: 513-542.
17. Campos A, Vasconcelos V (2010) Molecular mechanisms of microcystin toxicity in animal cells. Int J Mol Sci 11: 268-287.
18. Canesi L, Viarengo A (1997) Age-related differences in glutathione metabolism in mussel tissues (Mytilus edulis L). Comp Biochem Physiol 116B: 217-221.
19. Carney Almroth B, Albertsson E, Sturve J, Förlin L (2008) Oxidative stress, evident in antioxidant defences and damage products, in rainbow trout caged outside a sewage treatment plant. Ecotoxicol Environ Safe 70: 370-378.
20. Carney Almroth B, Johansson A, Förlin L, Sturve J (2010) Early-age changes in oxidative stress in brown trout, Salmo trutta. Comp Biochem Physiol 155B: 442-448.
21. Cazenava J, MdlA B, Pesce SF, Wunderlin DA (2006) Differential detoxification and antioxidant response in diverse organs of Corydoras paleatus experimentally exposed to microcystin-LR. Aquat Toxicol 76: 1-12.
22. Chae YJ, Pham CH, Lee J, Bae E, Yi J, Gu MB (2009) Evaluation of the toxic impact of silver nanoparticles on Japanese medaka (Oryzias latipes). Aquat Toxicol 94: 320-327.
23. Cheung CCC, Zheng GT, Li AMY, Richardson BJ, Lam PKS (2001) Relationship between tissue concentrations of polycyclic aromatic hydrocarbons and antioxidative responses of marine mussels, Perna veridis. Aquat Toxicol 52: 189-203.
24. Costa J, Ferreira M, Rey-Salgueiro L, Reis-Henriques MA (2011) Comparison of the waterborne and dietary routes of exposure on the effects of benzo(a)pyrene on biotransformation pathways in Nile tilapia (Oreochromis niloticus). Chemosphere 84: 1452-1460.
25. Crago J, Corsi SR, Weber D, Bannerman R, Klaper R (2011) Linking biomarkers to reproductive success of caged fathead minnows in streams with increasing urbanization. Chemosphere 82: 1669-1674.
26. Da Rocha AM, Salomao de Freita DP, Burns M, Vieira JP, de la Torre FR, Monserrat JM (2009) Seasonal and organ variations in antioxidant capacity, detoxifying competence and oxidative damage in freshwater and estuarine fishes from Southern Brazil. Comp Biochem Physiol 150C: 512-520.
27. Dai M, Ping X, Gaodao L, Chen J, Hehua J (2008) Simultaneous determination of microcystin-LR and its glutathione conjugate in fish tissues by liquid chromatography-mass spectrometry. J Chromatog 862B: 43-50.
28. Dam E, Styrishave B, Rewitz KF, Andersen O (2006) Intermolt duration affects the susceptibility of shore crabs Carcinus maenas (L.) to pyrene and their ability to metabolise it. Aquat Toxicol 80: 290-297.
29. Dettmer K, Aronov PA, Hammock BD (2007) Mass spectrometry based metabolomics. Mass Spectrom Rev 26: 51-78.
30. Dickinson DA, Forman HJ (2002) Glutathione in defense and signaling. Lessons from a small thiol. Ann NY Acad Sci 973: 488-504.
31. Dieckhaus CM, Fernandez-Metzler CL, King R, Krolikowski PH, Bailie TA (2005) Negative ion mass spectrometry for the detection of glutathione conjugates. Chem Res Toxicol 18: 630-638.
32. DiGuilio RT, Meyer JN (2008) Reactive oxygen species and oxidative stress. In: Di Guilio RT, Hinton DE (eds) The toxicology of fishes. CRC, Boca Raton, pp 273-326.
33. Dringen R (2000) Metabolism and functions of glutathione in brain. Prog Neurobiol 62: 649-671.
34. Dunn WB, Bailey NJC, Johnson HE (2005) Measuring the metabolome: current analytical technologies. Analyst 130: 606-625.
35. Eberhardt MK (2001) Reactive oxygen metabolites. Chemistry and medical consequences. CRC, Boca Raton, p 591.
36. Elskus AA, Pruell R, Stegeman JJ (1992) Endogenously-mediated, pretranslational suppression of cytochrome P4501A in PCB-contaminated flounder. Mar Environ Res 34: 97-101.
37. Erskine S, Beach DG, Rouleau C, Hellou J (2010) Fate and distribution of pyrene in Ilyanassa obsoleta exposed through the diet. Inverteb Surv J 7: 67-78.
38. Escartin E, Porte C (1999) Hydroxylated PAHs in bile of deep-sea fish. Relationship with xenobiotic metabolizing enzymes. Environ Sci Technol 33: 2710-2714.
39. Filho DW, Giulivi C, Boveris A (1993) Antioxidant defences in marine fish-I. Teleosts. Comp Biochem Physiol 106C: 409-413.
40. Forbes VE, Palmquist A, Bach L (2006) The use and misuse of biomarkers in ecotoxicology. Environ Toxicol Chem 25: 272-280.
41. Forman HJ, Zhang HQ, Rinna A (2009) Glutathione: overview of its protective roles, measurement and biosynthesis. Mol Aspects Med 30SI: 1-12.
42. Franklin CC, Backos DS, Mohar I, White CC, Forman HJ, Kavanagh TJ (2009) Structure, function, and post-translational regulation of the catalytic and modifier subunits of glutamate cysteine ligase. Mol Aspects Med 30: 86-98.
43. Fraternale A, Paoletti MF, Casabianca A, Nencioni L, Garaci E, Palamara AT, Magnani M (2009) GSH and analogues in antiviral therapy. Mol Aspects Med 30: 99-110.
44. Fu J, Xie P (2006) The acute effects of microcystin LR on the transcription of nine glutathione S-transferase genes in common carp Cyprinus carpio L. Aquat Toxicol 80: 261-266.
45. Fusijawa T, Ichise-Shibuya K, Katagi T (2010) Uptake and transformation of phenol by duckweed. J Pest Sci 35: 456-463.
46. Gagné F, Blaise C, André C, Gagnon C, Salazar M (2007a) Neuroendocrine disruption and health effects in Elliptio complanata mussels exposed to aeration lagoons for wastewater treatment. Chemosphere 68: 731-743.
47. Gagné F, Blaise A, André C, Pellerin J (2007b) Implication of site quality on mitochondrial electron transport activity and its interaction with temperature in feral Mya areneria clams from the Saguenay fjord. Environ Res 103: 238-246.
48. Gagné F, André C, Blaise C, Pellerin J, Sherry J, Talbot A (2009) An investigation of the disruptive effect of pollution in cold- and warm-adapted clam populations. Inverteb Surv J 6: 144-153.
49. Gallagher EP, Sheehy KM (2000) Altered glutathione-S-transferase catalytic activities in female brown bullheads from a contaminated site in central Florida lakes. Mar Environ Res 50: 399-403.
50. George SG (1994) Enzymology and molecular biology of phase II xenobiotic-conjugating enzymes in fish. In: Malins DC, Ostrander GK (eds) Aquatic toxicology: molecular biochemical and cellular perspectives. Lewis, Boca Raton, pp 37-86.
51. Godat E, Madalinski G, Muller L, Hilier JF, Labarre J, Junot C (2010) Mass spectrometry-based methods for the determination of sulfur and related metabolite concentrations in cell extracts. Method Enzym 473: 41-76.
52. Gordon CJ (2005) Temperature and toxicology. An integrative, comparative and environmental approach. Taylor and Francis, CRC, Boca Raton, p 338.
53. Gowland BTG, McIntosh AD, Davies IM, Moffat CF, Webster L (2002) Implications from a field study regarding the relationship between polycyclic aromatic hydrocarbons and glutathione S-transferase activity in mussels. Mar Environ Res 54: 231-235.
54. Guimaraes L, Gravato C, Santos J, Monteiro L, Guilhermino L (2009) Yellow eel (Anguilla anguilla) development in NW Portuguese estuaries with different contamination levels. Ecotox 18: 385-402.
55. Hahn ME, Hestermann EV (2008) Receptor-mediated mechanisms of toxicity. In: Di Guilio RT, Hinton DE (eds) The toxicology of fishes. CRC, Boca Raton, pp 235-272.
56. Harrington CR, Meade TH (1935) Synthesis of glutathione. Biochem J 29: 1602-1611.
57. Hellou J, Payne JF (1988) Assessment of contamination of fish by water-soluble fractions of petroleum: a role for bile metabolites. Environ Toxicol Chem 6: 857-862.
58. Hellou J, Leonard J, Meade J, Sharpe S, Banoub J, Papiernick S, Eglinton L, Whelan J (1999) Presence and metabolism of three heteroaromatic compounds in comparison to a PAH. Polycycl Aromat Comp 14-15: 221-230.
59. Hellou J, Leonard J (2004) PAH bioaccumulation and biotransformation products in trout exposed through food pellets. Polycycl Aromat Comp 24: 697-712.
60. Hellou J, Beach DG, Erskine S, Marklevitz SA, Saunders L (2010) Balanced fates of pyrene and 1-hydroxypyrene in snails, Ilyanassa obsoleta, exposed to spiked sediments. Polycycl Aromat Comp 30: 75-90.
61. Hellou J (2011) Behavioural ecotoxicology, an "early warning" signal to assess environmental quality. Environ Sci Poll Res 18: 1-11.
62. Hellou J, Gagné F (2011) Chapter 8. Integrated impact assessment of mussels health. In: McGevin LE, Editor Mussels: anatomy, habitat and environmental impact. Nova Science, Hauppauge, pp 197-220. ISBN 978-1-61761-763-8.
63. Henson KL, Sheely KM, Gallagher EP (2000) Conservation of a glutathione-S-transferase in marine and freshwater fish. Mar Environ Res 50: 17-21.
64. Hinchman CA, Ballatori N (1994) Glutathione conjugation and conversion to mercapturic acids can occur as an intrahepatic process. J Toxicol Environ Health 41: 387-409.
65. Holcapeck M, Kolarova L, Nobilis M (2008) High-performance liquid chromatography-tandem mass spectrometry in the identification and determination of phase I and phase II drug metabolites. Anal Bioanal Chem 391: 59-78.
66. Holdway DA, Brennan SE, Ahokas JT (1995) Short review of selected fish biomarkers of xenobiotic exposure: example using fish hepatic mixed-function oxidase. Aust J Ecol 20: 34-44.
67. Hughes WW (1996) Essentials of environmental toxicology. The effects of environmentally hazardous substances on human health. Taylor and Francis, Washington, DC, p 176.
68. Ito E, Takai A, Kondo F, Masui H, Imanishi S, Harada K (2002) Comparison of protein phosphatase inhibitory activity and apparent toxicity of microcystins and related compounds. Toxicon 40: 1017-1025.
69. Iwasaki Y, Saito Y, Nakano Y, Mochizuki K, Sakata O, Ito R, Saito K, Nakazawa H (2009) Chromatographic and mass spectrometric analysis of glutathione in biological samples. J Chromatog 877B: 3309-3317.
70. James MO, Bowen ER, Dansette PM, Bend JR (1979) Epoxide hydrase and glutathione S-transferase activities with selected alkene and arene oxides in several marine species. Chem Biol Inter 25: 321-344.
71. Johnson LL, Landahl JT, Kubin LA, Horness BH, Myers MS, Collier TK, Stein JE (1998) Assessing the effects of anthropogenic stressors on Puget Sound flatfish populations. J Sea Res 39: 125-137.
72. Johnson LL, Collier TK, Stein JE (2002) An analysis in support of sediment quality thresholds for polycyclic aromatic hydrocarbons (PAHs) to protect estuarine fish. Aquat Conserv 12: 517-538.
73. Jonsson G, Bechmann RK, Bamber SD, Baussant (2004) Bioconcentration, biotransformation and elimination of polycyclic aromatic hydrocarbons in sheephead minnows (Cypridon variegatus) exposed to contaminated seawater. Environ Toxicol Chem 23: 1538-1548.
74. Jurgella GF, Marwah A, Malison JA, Peterson R, Barry TP (2006) Effects of xenobiotics and steroids on renal and hepatic estrogen metabolism in lake trout. Gen Comp Endoc 148: 273-281.
75. Kellner R, Mermet J-M, Otto M, Valcarcel M, Widmer HM (2004) Analytical chemistry. A modern approach to analytical science, 2nd edn. Wiley-VCH, Germany, p 1181.
76. Kirby GM, Bend JR, Smith IR (1990) The role of glutathione-S-transferase in the hepatic metabolism of benzo[a]pyrene in white suckers (Catostomus commersoni) from polluted and reference sites in the Great Lakes. Comp Biochem Physiol 95C: 25-30.
77. Kleinow KM, Melancon MJ, Lech JJ (1987) Biotransformation and induction: implications for toxicity, bioaccumulation and monitoring of environmental xenobiotics in fish. Environ Health Persp 71: 105-119.
78. Korfmacher WA (2004) Editor. Using mass spectrometry for drug metabolism studies. CRC, Boca Raton, p 370.
79. Krahn MM, Ylitalo GM, Buzitis J, Chan SL, Varanasi U (1993) Rapid high-performance liquid-chromatographic methods that screen aromatic compounds in environmental samples. J Chromatog 642: 15-32.
80. Levsen K, Schiebel H-M, Behnke B, Dotzer R, Dreher W, Elend M, Thiele H (2005) Structure elucidation of phase II metabolites by tandem mass spectrometry: an overview. J Chromatog 1067A: 55-72.
81. Li G, Xie P, Fu J, Hao L, Xiong Q, Li H (2008) Microcystin-induced variations in transcription of GSTs in an omnivorous freshwater fish, goldfish. Aquat Toxicol 88: 261-266.
82. Limón-Pachecoa J, Gonsebatt ME (2009) The role of antioxidants and antioxidant-related enzymes in protective responses to environmentally induced oxidative stress. Mutat Res 674: 137-147.
83. Livingstone DR (1998) The fate of organic xenobiotics in aquatic ecosystems: quantitative and qualitative differences in biotransformation by invertebrates and fish. Comp Biochem Physiol 120A: 43-49.
84. Lu FC (1996) Basic toxicology. Fundamentals, target organs and risk assessment. Taylor and Francis, Washington, DC, p 358.
85. Lu SC (2009) Regulation of glutathione synthesis. Mol Aspects Med 30: 42-59.
86. Lushchak VI (2011a) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101: 13-30.
87. Lushchak VI (2011b) Adaptive response to oxidative stress: bacteria, fungi, plants and animals. Comp Biochem Physiol 153C: 175-190.
88. Ma SG, Chowdury SK, Alton KB (2006) Application of mass spectrometry for metabolite identification. Current Drug Metabolism 7: 503-523.
89. Malbrouck C, Kestemont P (2006) Effects of microcystin in fish. Environ Toxicol Chem 25: 72-86.
90. McKim JM, Nichols JW (1994) Use of physiologically based toxicokinetic models in a mechanistic approach to aquatic toxicology. In: Malins DC, Ostrander GK (eds) Aquatic toxicology, molecular, biochemical and cellular perspectives. Lewis, Boca Raton, pp 469-519.
91. Monostori P, Wittmann G, Karg E, Túri S (2009) Determination of glutathione and glutathione disulfide in biological samples: an in-depth review. J Chromatog 877B: 3331-3346.
92. Muir DCG, Howard PH (2006) Are there other persistent organic pollutants? A challenge for environmental chemists. Environ Toxicol Chem 40: 7157-7166.
93. Mutlib AE (2008) Application of stable isotope-labeled compounds in metabolism and in metabolism-mediated toxicity studies. Chem Res Toxicol 21: 1672-1689.
94. Norris RL, Eaglesham GK, Shaw GR, Smith MJ, Chiswell RK, Seawright AA, Moore MR (2001) A sensitive and specific assay for glutathione with potential application to glutathione disulfide, using high-performance liquid chromatography tandem mass spectrometry. J Chromatog 762B: 17.
95. NRC (National Research Council) (1987) Biological markers in environmental health research. Committee on Biological Markers of the National Research Council. Environ Health Perspect 74: 3-9.
96. Ognjanovic BI, Dordevic NZ, Perendija BR, Despotovic SG, Zikic RV, Stajn AS, Saicic ZS (2008) Concentration of antioxidant compounds and lipid peroxidation in the liver and white muscle of hake (Merluccius merluccius L.) in the Adriatic sea. Arch Biol Sci 60: 601-608.
97. Ownby DR, Belden JB, Lotufo GR, Lydy MJ (2005) Accumulation of trinitrotoluene in aquatic organisms: part I-bioconcentration and distribution in channel catfish (Ictalurus punctatus). Chemosphere 58: 1153-1159.
98. Paetzold SC, Ross NW, Richards RC, Jones M, Hellou J, Bard SM (2009) Up-regulation of hepatic ABCC2, ABCG2, CYP1A1, and GST in multixenobiotic-resistant killifish (Fundulus heteroclitus) from the Sydney Tar Ponds, Nova Scotia, Canada. Mar Environ Res 68: 37-47.
99. Pallante SL, Lisek CA, Dulik DM, Fenseleau C (1986) Glutathione conjugates: immobilized enzyme synthesis and characterization by fast atom bombardment mass spectrometry. Drug Metab Dispos 14: 313-319.
100. Petala M, Kokokiris L, Samaras P, Papadopoulos A, Zouboulis A (2009) Toxicological and ecotoxic impact of secondary and tertiary treated sewage effluents. Wat Res 43: 5063-5074.
101. Petrivalsky M, Machala M, Nezveda K, Piacka V, Svobodova Z, DrabeK P (1997) Glutathione dependent detoxifying enzymes in rainbow trout liver: search for specific biomarkers of chemical stress. Environ Toxicol Chem 16: 1417-1421.
102. Pflugmacher SP, Wiegand C, Oberemm M, Beattie KA, Krause E, Codd GA, Steinberg CEW (1998) Identification of an enzymatically formed glutathione conjugate of the cyanobacterial hepatotoxin microcystin-LR: the first step of detoxification. Biochem Biophys Acta 1425: 527-533.
103. Pflugmacher SP (2004) Promotion of oxidative stress in the aquatic macrophyte Ceratophyllum demersum, during biotransformation of the cyanobacterial toxin microcystin-LR. Aquat Toxicol 70: 169-178.
104. Pflugmacher S, Wiegand C, Werner S, Schroeder H, Kankaanpaeae H (2005) Activity and substrate specificity of cytosolic and microsomal glutathione S-transferase in Australian black tiger prawns (Penaeus monodon) after exposure to cyanobacterial toxins. Aquat Toxicol 20: 301-307.
105. Pinho GLL, Moura de Rosa C, Maciel FE, Bianchini A, Yunes JS, Pronca LAO, Monserrat JM (2005) Antioxidant responses and oxidative stress after microcystin exposure in the hepatopancreas of an estuarine crab species. Ecotox Environ Safe 61: 353-360.
106. Plakunov I, Smolarek TA, Fischer DL, Wiley JC Jr, Baird WM (1987) Separation by ion-pair high-performance liquid chromatography of the glucuronide, sulfate and glutathione conjugates formed from benzo(a)pyrene in cell cultures from rodents, fish and humans. Carcinogenesis 8: 59-66.
107. Powers R (2009) NMR metabolomics and drug discovery. Magn Reson Chem 47: S2-S11.
108. Radi AAR, Hai DQ, Matkovics B, Gabrielak T (1985) Comparative antioxidant enzyme study in freshwater fish with different types of feeding behaviour. Comp Biochem Physiol 81C: 395-399.
109. Ramirez AJ, Brain RA, Usenko S, Mottaleb MA, O'Donnell JG, Stahl LL, Wathen JB, Snyder BD, Pitt JL, Perez-Hutrtado P, Dobbins LL, Brooks BW, Chabliss CK (2009) Occurrence of pharmaceuticals and personal care products in fish: results of a national pilot study in the United States. Environ Toxicol Chem 28: 2587-2597.
110. REACH (Registration, Evaluation, Authorisation and Restriction of Chemicals) (2007) With updates available at the site http://ec. europa. eu/enterprise/sectors/chemicals/reach/index_en. htm.
111. Richardson BJ, Mak E, De Luca-Abbott SB, Martin M, McClella K, Lam PKS (2008) Antioxidant responses to polycyclic aromatic hydrocarbons and organochlorine pesticides in green-lipped mussels (Perna viridis): do mussels "integrate" biomarker responses? Mar Poll Bull 57: 503-514.
112. Reynaud S, Raveton M, Ravanel P (2008) Interactions between immune and biotransformation systems in fish: a review. Aquat Toxicol 87: 139-145.
113. Roberts SC, Noyes PD, Gallagher EP, Stapleton HM (2011) Species-specific differences and structure-activity relationships in the debromination of PBDE congeners in three fish species. Environ Sci Technol 45: 1999-2005.
114. Ross SW, Dalton DA, Kramer S, Christensen BL (2001) Physiological (antioxidant) responses of estuarine fishes to variability in dissolved oxygen. Comp Biochem Physiol 130C: 289-303.
115. Rossi R, Dalle-Donne I, Milzani A, Giustarini D (2006) Oxidized forms of glutathione in peripheral blood as biomarkers of oxidative stress. Clin Chem 52: 1406.
116. Roux A, Lison D, Junot C, Heilier J-F (2011) Applications of liquid chromatography coupled to mass spectrometry-based metabolomics in clinical chemistry and toxicology: a review. Clin Biochem 44: 119-135.
117. Rudneva II, Skuratovskaya EN, Kuzminova NS, Kovyrshina TB (2010) Age composition and antioxidant enzyme activities in blood of Black Sea teleosts. Comp Biochem Physiol 151C: 229-239.
118. Rust AJ, Burgess RM, Brownawell BJ, McElroy AE (2004) Relationship between metabolism and bioaccumulation of benzo[a]pyrene in benthic invertebrates. Environ Toxicol Chem 23: 2587-2593.
119. Ruus A, Sandvik M, Ugland KI, Skaare JU (2002) Factors influencing activities of biotransformation enzymes, concentrations and compositional patterns of organochlorine contaminants in members of a marine food web. Aquat Toxicol 61: 73-87.
120. Salinas AE, Wong MG (1999) Glutathione-S-transferase: a review. Curr Med Chem 6: 279-309.
121. Schlenk D, Handy R, Steinert S, Depledge MH, Benson W (2008) Biomarkers. In: Di Guilio RT, Hinton DE (eds) The toxicology of fishes. CRC, Taylor and Francis, Boca Raton, pp 683-732.
122. Sciuto AM (1997) Antioxidant properties of glutathione and its role in tissue protection. In: Baskin SE, Salem H (eds) Oxidants, antioxidants and free radicals. Taylor and Francis, Washington, DC, pp 171-191.
123. Scown TM, Santos EM, Johnston BD, Gaiser B, Baalousha M, Mitov S, Lead JR, Stone V, Fernandes TF, Jepson M, van Aerle R, Tyler CR (2010) Effects of aqueous exposure to silver nanoparticles of different sizes in rainbow trout. Toxicol Sci 115: 521-534.
124. Snowberger Gray E, Woodin BR, Stegeman JJ (1991) Sex differences in hepatic monooxygenase in winter flounder (Pseudopleuronectes americanus) and scup (Stenotomus chrysops) and regulation of P450 forms by estradiol. J Exp Zool 259: 330-342.
125. Sole M, Rodriguez S, Papiol V, Maynou F, Cartes JE (2009) Xenobiotic metabolism markers in marine fish with different trophic strategies and their relationship to ecological variables. Comp Biochem Physiol 149C: 83-89.
126. Sole M, Anto M, Baena M, Carrasson M, Cartes JE, Maynou F (2010) Hepatic biomarkers of xenobiotic metabolism in eighteen marine fish from the NW Mediterranean slope waters in relation to some of their biological and ecological variables. Mar Environ Res 70: 181-188.
127. Song SB, Xu Y, Zhou BS (2006) Effects of hexachlorobenzene on antioxidant status of liver and brain of the common carp (Cyprinus carpio). Chemosphere 65: 699-706.
128. Speers-Roesch B, Ballantyne JS (2005) Activities of antioxidant enzymes and cytochrome c oxidase in liver of Arctic and temperate teleosts. Comp Biochem Physiol 140A: 487-494.
129. Staack RF, Hopfgartner G (2007) Analytical strategies in studying drug metabolism. Anal Bioanal Chem 388: 1365-1380.
130. Stegeman JJ, Hahn ME (1994) Biochemistry and molecular biology of monooxygenases: current perspectives on forms, functions and regulation of cytochrome P-450 in aquatic species. In: Malins DC, Ostrander GK (eds) Aquatic toxicology: molecular, biochemical and cellular perspective. Lewis, CRC, Boca Raton, pp 87-206.
131. Stenersen J, Kobro S, Bjerke M, Arend U (1987) Glutathione transferases in aquatic and terrestrial animals from nine phyla. Comp Biochem Physiol 86C: 73-82.
132. Stroomberg GJ, Ariese F, van Gestel CAM, van Hattum B, Velthorst NH, van Straalen NM (2003) Pyrene biotransformation products as biomarkers of polycyclic aromatic hydrocarbon exposure in terrestrial isopoda: concentration-response relationship and field study in a contaminated forest. Environ Toxicol Chem 22: 224-231.
133. Tjeerdema RST, Crosby DG (1987) The biotranformation of molinate (Ordram) in stripped bass (Morone saxatilis). Aquat Toxicol 9: 305-317.
134. Upshall C, Payne JF, Hellou J (1993) Investigation of the induction of MFO enzymes and production of bile metabolites in rainbow trout (Salmo gairdneri) exposed to crankcase oil. Environ Toxicol Chem 12: 2105-2112.
135. van Bladeren PJ (2000) Glutathione conjugation as a bioactivation reaction. Chem Biol Inter 129: 61-76.
136. van den Berg M, Sanderson T, Kurihara N, Katayama A (2003) Role of metabolism in the endocrine-disrupting effects of chemicals in aquatic and terrestrial systems. Pure Appl Chem 75: 1917-1932.
137. van der Oost R, Goksoyr A, Celander M, Heida H, Vermeulen NPE (1996) Biomonitoring of aquatic pollution with feral eel (Anguilla anguilla) II. Biomarkers: pollution-induced biochemical responses. Aquat Toxicol 36: 189-222.
138. van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharm 13: 57-149.
139. van Gestel CAM, van Brummelen TC (1996) Incorporation of the biomarker concept in ecotoxicology calls for a redefinition of terms. Ecotoxicology 5: 217-225.
140. van Ravenzwaay B, Coelho-Palermo Cunha G, Leibold E, Looser R, Mellert W, Prokoudine A, Walk T, Wiermer J (2007) The use of metabolomics for the discovery of new biomarkers of effect. Toxicol Lett 172: 21-28.
141. van Veld P, Ko U, Vogelbein W, Westbrook D (1991) Glutathione S-transferase in intestine, liver and hepatic lesions of mummichog (Fundulus heteroclitus) from a creosote-contaminated environment. Fish Physiol Biochem 9: 369-376.
142. van Veld PA, Vogelbein WK, Cochran MK, Goksoyr A, Stegeman JJ (1997) Route-specific cellular expression of cytochrome P4501A (CYP1A) in fish (Funduls heteroclitus) following exposure to aqueous and dietary benzo[a]pyrene. Toxicol Appl Pharmacol 142: 348-359.
143. Viant MR (2007) Metabolomics of aquatic organisms: the new "omics" on the block. Mar Ecol Prog Series 332: 301-306.
144. Vidal ML, Narbonne JF (2000) Characterization of glutathione S-transferase activity in Asiatic clam Corbicula fluminea. Bull Environ Contam Toxicol 64: 455-462.
145. Vuckovick D, Pawliszyn J (2011) Systematic evaluation of solid-phase microextraction coatings for untargeted metabolomic profiling of biological fluids by liquid chromatography-mass spectrometry. Anal Chem 83: 1944-1954.
146. Wiegand C, Krause E, Steinberg C, Pflugmacher S (2001) Toxicokinetics of atrazine in embryos of zebrafish (Danio rerio). Ecotox Environ Safe 49: 199-205.
147. Wiegand C, Pflugmacher S (2005) Biological effects of selected cyanobacterial secondary metabolites: a short review. Toxicol Appl Pharmacol 203: 201-218.
148. Winston GW, DiGuilio RT (1991) Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat Toxicol 19: 131-161.
149. Winters 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 (Leuciscus cephalus) from rivers in the West Midlands, UK. Aquat Toxicol 73: 394-405.
150. Yadwad VB (1989) Effects of endosulfan on glutathione-S-transferase and glutathione content of the premoult field crab, Paratelphusa hydrodromus. Bull Environ Contam Toxicol 43: 597-602.
151. Yeats P, Gagné F, Hellou J (2008) Body burden of contaminants and biological effects in mussels: an integrated approach. Environ Inter 34: 254-264.
152. Young-Mog K, Kunbawui P, Gil-Jae J, Eun-Mo J, Jang-Eok K, In-Koo R (2004) Glutathione-dependent biotranformation of chlorothalonil. J Agr Food Sci 52: 4192-4196.
153. Zhang D, Xie P, Chen J, Dai M, Qiu T, Liang G (2009) Determination of microcystin-LR and its metabolites in snail (Bellamya aeruginosa), shrimp (Macrobrachium nipponensis) and silver carp (Hypophthalmichthys molitrix) from Lake Taihu, China. Chemosphere 76: 974-981.