Characterization of hepatic and extrahepatic glutathione S-transferases in rainbow trout (Oncorhynchus mykiss) and their induction by 3,3',4,4'-tetrachlorobiphenyl

Fish Physiology and Biochemistry

Volumn 22, Issue 1, 2000, Pages 21-32

  Perez Lopez M ^b   Anglade, P ^a   Bec Ferte M P ^a   Debrauwer, L ^a   Perdu, E ^a   Cravedi, J P ^a   Rouimi, P ^a  

^a CEMAGREF   (France)

^b UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

Amino acid sequence; Fish; Glutathiolation; Glutathione; GST; Mass spectrometry; PCB

Indexed keywords

1 CHLORO 2,4 DINITROBENZENE; 3,3',4,4' TETRACHLOROBIPHENYL; GLUTATHIONE; GLUTATHIONE TRANSFERASE; POLYCHLORINATED BIPHENYL;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CHEMICAL ANALYSIS; CHEMICAL MODIFICATION; GILL; KIDNEY; LIVER; MASS SPECTROMETRY; NONHUMAN; OLFACTORY EPITHELIUM; RAINBOW TROUT;

EID: 0343183285     PISSN: 09201742     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1007885332573     Document Type: Article

References (56)

1. Andersson, T., Pesonen, M. and Johansson, C. 1985. Differential induction of cytochrome P450-dependent monooxygenase, epoxide hydrolase, glutathione transferase and UDP glucuronosyl transferase activities in the liver of rainbow trout by β-naphthoflavone or Clophen A50. Biochem. Pharmacol. 34: 3309-3314.
2. Ankley, G.T. and Agosin, M. 1987. Comparative aspects of hepatic UDP-glucuronosyltransferases and glutathione S-transferases in bluegill and channel catfish. Comp. Biochem. Physiol. 87B: 671-673.
3. Bauermeister, A., Lewendon, A., Ramage, P. and Nimmo, I.A. 1983. Distribution and some properties of the glutathione S-transferase and γ-glutamyl transpeptidase activities of rainbow trout. Comp. Biochem. Physiol. 74C: 89-93.
4. Board, P.G. and Baker, R.T., Chelvanayagam, G. and Jermiin, L.S. 1997. Zeta, a novel class of glutathione transferases in a range of species from plants to humans. Biochem. J. 328: 929-935.
5. Boon, J.P., Everaarts, J.M., Hillebrand, M.T.J., Eggens, M.L., Pijnenburg, J. and Goksøyr, A., 1992. Changes in levels of hepatic biotransformation enzymes and haemoglobin levels in female plaice Pleuronectes platessa after oral administration of a technical polychlorinated biphenyl mixture Clophen A40. Sci. Tot. Environ. 114: 113-133.
6. Bradford, M.M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 284-254.
7. Brumley, C.M., Haritos, V.S., Ahokas, J.T. and Holdway, D.A. 1995. Validation of biomarkers of marine pollution exposure in sand flathead using Aroclor 1254. Aquat. Toxicol. 31: 249-262.
8. Buetler, T.M. and Eaton, D.L. 1992. Glutathione S-transferases: aminoacid sequence comparison, classification and phylogenetic relationship. Environ. Carcino. & Ecotox. Revs. C10: 181-203.
9. Cabriscol, E. and Levine, R.L. 1996. The phosphatase activity of carbonic anhydrase III is reversibly regulated by glutathiolation. Proc. Natl. Acad. Sci. USA 93: 4170-4174.
10. Celander, M., Leaver, M.J., George, S.G. and Förlin, L. 1993. Induction of cytochrome P450 IA1 and conjugating enzymes in rainbow trout (Oncorhynchus mykiss) liver: a time course study. Comp. Biochem. Physiol. 106C: 343-349.
11. Cravedi, J.P., Perdu-Durand, E. and Poupin, E. 1998. Effet d'un hydrocarbure aromatique polycyclique et d'un PCB sur les activités de métabolisation des xénobiotiques de la truite arc-en-ciel (O. mykiss). Bull. Fr. Pêche Piscic. 350-351: 563-570.
12. DeJong, J.L., Morgenstern, R., Jörnvall, H., De Pierre, J.W. and Tu, C.-P.D. 1988. Gene expression of rat and human microsomal glutathione S-transferase. J. Biol. Chem. 263: 8430-8436.
13. Dierickx P.J. 1985. Hepatic glutathione S-transferases in rainbow trout and their interaction with 2,4-dichlorophenoxyacetic acid and 1,4-benzoquinone. Comp. Biochem. Physiol. 82C: 495-500.
14. Dominey, R.J., Nimmo, I.A., Cronshaw, A.D. and Hayes, J.D. 1991. The major glutathione S-transferase in salmonid fish livers is homologous to the mammalian pi-class GST. Comp. Biochem. Physiol. 100B: 93-98.
15. Egaas, E., Sandvik, M., Fjeld, E., Källqvist, T., Goksøyr, A. and Svensen, A. 1999. Some effects of the fungicide propiconazole on cytochrome P450 and glutathione S-transferase in brown trout (Salmo trutta). Comp. Biochem. Physiol. 122C: 337-344.
16. Gallagher E.P. and Di Giulio R.T. 1992. A comparison of glutathione-dependent enzymes in liver, gills and posterior kidney of channel catfish (Ictalurus punctatus). Comp. Biochem. Physiol. 102C: 543-547.
17. George S.G. and Buchanan G. 1990. Isolation, properties and induction of plaice liver cytosolic glutathione-S-transferases. Fish Physiol. Biochem. 8: 437-449.
18. George S.G. 1994. Enzymology and molecular biology of phase II xenobiotic-conjugating enzymes in fish. In: Aquatic Toxicology Molecular and Cellular Perspectives, pp. 37-85. Edited by D.C. Malins and G.K. Ostrander. Lewis Publishers, Boca Raton.
19. Gooch, J.W., Elskus, A.A., Kloepper-Sams, P.J., Hahn, M.E. and Stegeman, J.J. 1989. Effects of ortho- and non-orthosubstituted polychlorinated biphenyl congeners on the hepatic monooxygenase system in scup Stenotomus chrysops. Toxicol. Appl. Pharmacol. 98: 422-433.
20. Habig, W.H. Pabst, M.J. and Jakoby, W.B. 1974. Glutathine S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249: 7130-7139.
21. Hayes, J.D. and Pulford, D.J. 1995. The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit. Rev. Biochem. Mol. Biol. 30: 445-600.
22. Huuskonen, S., Lindström-Seppä, P., Koponen, K. and Roy, S. 1996. Effects of non-ortho-substituted polychlorinated biphenyls congeners 77 and 126 on cytochrome P4501A and conjugation activities in rainbow trout Oncorhynchus mykiss. Comp. Biochem. Physiol. 113C: 205-213.
23. Janz, D.M. and Metcalfe, C.D. 1991. Relative induction of aryl hydrocarbon hydroxylase by 2,3,7,8-TCDD and two co-planar PCBs in rainbow trout Oncorhynchus mykiss. Environ. Toxicol. Chem. 10: 917-923.
24. Ketterer, B. Meyer, D.J. and Clarck, A.G. 1988. Soluble glutathione transferase isozymes. In: Glutathione Conjugation, Mechanisms and Biological Significance. pp 74-135. Edited by H. Sies and B. Ketterer. Academic Press, London.
25. Kobayashi, K., Oshima, Y. and Taguchi, C. 1987. Induction of drug-metabolizing enzymes by long-term administration of PCB and duration of their induced activities in carp. Nippon Suisan Gakkaishi 53: 487-491.
26. Kudo, H., Ueda, H., Mochida, K., Adachi, S., Hara, A., Nagasawa, H., Doi, Y., Fugimoto, S. and Ymaushi, K. 1999. Salmonid olfactory system-specific protein (N24) exhibits glutathione S-transferase class pi-like structure. J. Neurochem. 72: 1344-1352.
27. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the heat bacteriophage T4. Nature, London 227: 680-685.
28. Laurén, D.J., Halarnkar, P.P., Hammock, B.D. and Hinton, D.E. 1989. Microsomal and cytosolic epoxide hydrolase and glutathione S-transferase activities in the gill, liver, and kidney of the rainbow trout Salmo gairdneri. Baseline levels and optimization of assay conditions. Biochem. Pharmacol. 38: 881-887.
29. Leaver, M.J., Scott, K. and George, S.G. 1993. Cloning and characterization of the major hepatic glutathione S-transferase from a marine teleost flatfish, the plaice Pleuronectes platessa, with structural similarities to plant, insect and mammalian theta class isoenzymes. Biochem. J. 292: 189-195.
30. Lindström-Seppä, P., Korytko, P.J., Hahn, M.E. and Stegeman, J.J. 1994. Uptake of waterborne 3,3′,4,4′-tetrachlorobiphenyl and organ and cell-specific induction of cytochrome P4501A in adult and larval fathead minnow Pimephales promelas. Aquat. Toxicol. 28: 147-167.
31. Listowsky I. 1993. High capacity binding by glutathione S-transferases and glucocorticoid resistance. In: Structure and Function of Glutathione Transferases. pp. 199-209. Edited by K.D. Tew, C.B. Pickett, T.J. Mantle, B. Mannervik and Hayes, J.D. CRC Press, Boca Raton.
32. Lowry, O.H., Rosebrough, N.J., Fair, A.L. and Randall, R.J. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265-275.
33. Machala, M., Drabek, P., Neca, J., Kolarova, J. and Svobodova, Z. 1998. Biochemical markers for differentiation of exposures to nonplanar polychlorinated biphenyls, organochlorine pesticides or 2,3,7,8-tetrachlorodibenzo-p-dioxin in trout liver. Ecotoxicol. Environ. Saf. 41: 107-111.
34. Mannervik, B. 1985. The isoenzymes of glutathione transferases. Adv. Enzymol. 57: 357-417.
35. Mannervik B., Awasthi, Y.C., Board, P.G., Hayes, J.D., Di Illio, C., Ketterer, B., Listowsky, I., Morgenstern, R., Muramatsu, M., Pearson, W.R., Pickett, C.B., Sato, K., Widersten, M. and Wolf, C.R. 1992. Nomenclature for human glutathione transferases. Biochem. J. 282: 305-308.
36. Mannervik, B. and Danielson, U.H. 1988. Glutathione transferases-structure and catalytic activity. Crit. Rev. Biochem. 23: 283-337.
37. Martínez-Lara, E., George, S.G., López-Barea, J. and Bárcena, J.A. 1997. Purification and characterization of multiple glutathione transferase isoenzymes from grey mullet liver. Cell. Mol. Life Sci. 53: 759-768.
38. Mart́nez-Lara, E., Toribio, F., López-Barea, J. and Bárcena, J.A. 1996. Glutathione-S-transferase isoenzyme patterns in the gilt-head seabream Sparus aurata exposed to environmental contaminants. Comp. Biochem. Physiol. 113C: 215-220.
39. Melancon, M.J. and Lech, J.J. 1983. Dose-effect relationship for induction of hepatic monooxygenase activity in rainbow trout and carp by Arochlor 1254. Aquat. Toxicol. 4: 51-61.
40. Meyer, D.J., Coles, B., Pemble, S.E., Gilmore, K.S., Fraser, G.M. and Ketterer, B. 1991. Theta, a new class of glutathione transferases purified from rat and man. Biochem. J. 274: 409-414.
41. Meyer, D.J. and Yhomas, M. 1995. Characterization of rat spleen prostaglandin-H d-isomerase as a sigma class GSH transferase. Biochem. J. 311: 739-742.
42. Mitchell, A.E., Morin, D., Lamé, M.W. and Jones, A.D. 1995. Purification, mass spectrometric characterization, and covalent modification of murine glutathione S-transferases. Chem. Res. Toxicol. 8: 1054-1062.
43. Monod, G., Devaux, A. and Rivière, J.L. 1988. Effects of chemical pollution on the activities of hepatic xenobiotic metabolizing enzymes in fish from the river Rhône. Sci. Tot. Environ. 73: 189-201.
44. Morgenstern, R. and DePierre, J.W. 1983. Microsomal glutathione transferase. Purification in unactivated form and further characterization of the activation process, substrate specificity and amino acid composition. Eur. J. Biochem. 134: 591-597.
45. Newsted, J.L., Giesy, J.P., Ankley, G.T., Tillitt, D.E., Crawford, R.A., Gooch, J.W, Jone, P.D. and Denison M.S. 1995. Development of toxic equivalency factors for PCB congeners and the assessment of TCDD and PCB mixtures in rainbow trout. Environ. Toxicol. Chem. 14: 861-871.
46. Nimmo, I.A. 1987. The glutathione S-transferases of fish. Fish Physiol. Biochem., 3: 163-172.
47. Nimmo, I.A., Clapp, J.B. and Strange R.C. 1979. A comparison of the glutathione S-transferases of trout and rat liver. Comp. Biochem. Physiol. 63B: 423-427.
48. Otto, D.M.E. and Moon, T.W. 1996. Phase I and II enzymes and antioxidant responses in different tissues of brown bullheads from relatively polluted and non-polluted systems. Arch. Environ. Contam. Toxicol. 31: 141-147.
49. Pascal, S., Debrauwer, L., Ferte, M.-P., Anglade, P., Rouimi, P. and Scalla, R. 1998. Analysis and characterization of glutathione-S-transferase subunits from wheat Triticum aestivum L. Plant Sci., 134: 217-226.
50. Ramage, P.I.N. and Nimmo, I.A. 1984. The substrate specificities and subunit compositions of the hepatic glutathione S-transferases of rainbow trout Salmo gairdneri. Comp. Biochem. Physiol. 78B: 189-194.
51. Rouimi, P., Anglade, P., Debrauwer, L. and Tulliez, J. 1996. Characterization of pig liver glutathione S-transferases using HPLC-electrospray-ionization mass spectrometry. Biochem. J. 317: 879-884.
52. Rouimi, P., Debrauwer, L. and Tulliez, J. 1995. Electrospray Ionization-Mass Spectrometry as a tool for characterization of glutathione S-transferase isozymes. Anal. Biochem. 229: 304-312.
53. Schaffner, W. and Weissmann, C. 1973. A rapid, sensitive, and specific method for the determination of protein in dilute solutions. Anal. Biochem. 56: 502-514.
54. Scott, K., Leaver, M. and George, S. 1992. Regulation of hepatic glutathione S-transferase expression in flounders. Mar. Environ. Res. 34: 233-236.
55. Starcevic, S.L., and Zielinski, B.S. 1995. Inmunohistochemical localization of glutathione S-transferase pi in rainbow trout olfactory receptor neurons. Neurosci. Lett. 183: 175-178.
56. Towbin, H., Staehelin, T. and Gordon, J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76: 4350-4354.