Inhibition of glutathione S-transferase P1-1 in mouse lung epithelial cells by the tumor promoter 2,6-di-tert-butyl-4-methylene-2,5-cyclohexadienone (BHT-quinone methide): Protein adducts investigated by electrospray mass spectrometry

Chemical Research in Toxicology

Volumn 17, Issue 12, 2004, Pages 1675-1683

  Lemercier, Jean Noël ^a   Meier, Brent W ^a   Gomez, Jose D ^a   Thompson, John A ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYLCRESOL; BUTYLCRESOL QUINONE METHIDE; CYSTEINE; GLUTATHIONE S TRANSFERASE P1 1; GLUTATHIONE TRANSFERASE; OXIDIZING AGENT; PHOSPHOTRANSFERASE; POLYCLONAL ANTIBODY; TUMOR PROMOTER; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ALKYLATION; ANIMAL CELL; ARTICLE; CELL GROWTH; CELL LINE; CELL PROTECTION; ELECTROSPRAY MASS SPECTROMETRY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME ISOLATION; ENZYME PHOSPHORYLATION; ION CURRENT; LIQUID CHROMATOGRAPHY; LUNG TUMOR; MOUSE; NONHUMAN; OXIDATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REACTION ANALYSIS; WESTERN BLOTTING;

ALKYLATION; ANIMALS; CARCINOGENS; CELL LINE; CHROMATOGRAPHY, LIQUID; CYTOSOL; EPITHELIAL CELLS; GLUTATHIONE S-TRANSFERASE PI; GLUTATHIONE TRANSFERASE; HUMANS; ISOENZYMES; LUNG; MASS SPECTROMETRY; MICE; QUINONES; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

ANIMALIA;

EID: 10844243976     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx049811x     Document Type: Article

References (50)

1. Wan, P., Barker, B., Diao, L., Fischer, M., Shi, Y., and Yang, C. (1996) Quinone methides: Relevant intermediates in organic synthesis. Can. J. Chem. 74, 465-475.
2. Bolton, J. L., Turnipseed, S. B., and Thompson, J. A. (1997) Influence of quinone methide reactivity on the alkylation of thiol and amino groups in proteins: studies utilizing amino acid and peptide models. Chem.-Biol. Interact. 107, 185-200.
3. Thompson, D. C., Thompson, J. A., Sugumaran, M., and Moldeus, P. (1993) Biological and toxicological consequences of quinone methide formation. Chem.-Biol. Intact. 86, 129-162.
4. McCracken, P. G., Bolton, J. L., and Thatcher, G. R. J. (1997) Covalent modification of proteins and peptides by the quinone methide from 2-tert-butyl-4,6-dimethylphenol: Selectivity and reactivity with respect to competitive hydration. J. Org. Chem. 62, 1820-1825.
5. Marques, M. M., and Beland, F. A. (1997) Identification of tamoxifen-DNA adducts formed by 4-hydroxytamoxifen quinone methide. Carcinogenesis 18, 1949-1954.
6. Boersma, M. G., Vervoort, J., Szymusiak, H., Lemanska, K., Tyrakowska, B., Cenas, N., Segura-Aguilar, J., and Rietjens, I. M. C. M. (2000) Regioselectivity and reversibility of the glutathione conjugation of quercetin quinone methide. Chem. Res. Toxicol. 13, 185-191.
7. Thompson, D. C., Perera, K., and London, R. (1995) Quinone methide formation from para isomers of methylphenol (cresol), ethylphenol, and isopropylphenol: Relationship to toxicity. Chem. Res. Toxicol. 8, 55-60.
8. Bodell, W. J., Deena, Q. Y., Pathak, D. N., and Pongracz, K. (1998) Oxidation of eugenol to form DNA adducts and 8-hydroxy-2′-deoxyguanosine: Role of quinone methide derivatives in DNA adduct formation. Carcinogenesis 19, 437-443.
9. Mizutani, T., Nomura, H., Nakanishi, K., and Fujita, S. (1987) Hepatotoxicity of butylated hydroxytoluene and its analogues in mice depleted of hepatic glutathione. Toxicol. Appl. Pharmacol. 87, 166-176.
10. Witschi, H., Malkinson, A. M., and Thompson, J. A. (1989) Metabolism and pulmonary toxicity of butylated hydroxytoluene (BHT). Pharmacol. Ther. 42, 89-113.
11. Bolton, J. L., Sevestre, H., Ibe, B. O., and Thompson, J. A. (1990) Formation and reactivity of alternative quinone methides from butylated hydroxytoluene: Possible explanation for species-specific pneumotoxicity. Chem. Res. Toxicol. 3, 65-70.
12. Reed, M., and Thompson, D. C. (1997) Immunochemical visualization and identification of rat liver proteins adducted by 2,6-ditert-butyl-4-methylphenol (BHT). Chem. Res. Toxicol. 10, 1109-1117.
13. Thompson, J. A., Carlson, T. J., Sun, Y., Dwyer-Nield, L., and Malkinson, A. M. (2001) Studies using structural analogues and inbred strain differences to support a role for quinone methide metabolites of butylated hydroxytoluene (BHT) in mouse lung tumor promotion. Toxicology 160, 197-205.
14. Mizutani, T., Yamamoto, K., and Tajima, K. (1983) Isotope effects on the metabolism and pulmonary toxicity of butylated hydroxytoluene in mice by deuteration of the 4-methyl group. Toxicol. Appl. Pharmacol. 69, 283-290.
15. Malkinson, A. M., Thaete, L. G., Blumenthal, E. J., and Thompson, J. A. (1989) Evidence for the role of tert-butyl hydroxylation in the induction of pneumotoxicity in mice by butylated hydroxytoluene. Toxicol. Appl. Pharmacol. 101, 196-204.
16. Malkinson, A. M., Koski, K. M., Evans, W. A., and Festing, M. F. W. (1997) Butylated hydroxytoluene exposure is necessary to induce lung tumors in BALB mice treated with 3-methylcholanthrene. Cancer Res. 57, 2832-2834.
17. Malkinson, A. M., Dwyer-Nield, L. D., Rice, P. L., and Dinsdale, D. (1997) Mouse lung epithelial cell lines-tools for the study of differentiation and the neoplastic phenotype. Toxicology 123, 53-100.
18. Thompson, J. A., Schullek, K. M., Fernandez, C. A., and Malkinson, A. M. (1989) A metabolite of butylated hydroxytoluene with potent tumor-promoting activity in mouse lung. Carcinogenesis 10, 773-775.
19. Kupfer, R., Dwyer-Nield, L. D., Malkinson, A. M., Thompson, J. A. (2002) Lung toxicity and tumor promotion by hydroxylated derivatives of 2,6-di-tert-butyl-4-methylphenol (BHT) and 2-tert-butyl-4-methyl-6-iso- propylphenol: Correlation with quinone methide reactivity. Chem. Res. Toxicol. 15, 1106-1112.
20. Guyton, K. Z., Bhan, P., Kuppusamy, P., Zweier, J. L., Trush, M. A., and Kensler, T. W. (1991) Free radical-derived quinone methide mediates skin tumor promotion by butylated hydroxytoluene hydroperoxide: Expanded role for electrophiles in multistage carcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 88, 946-950.
21. Boberg, E. W., Liem, A., Miller, E. C., and Miller, J. A. (1987) Inhibition by pentachlorophenol of the initiating and promoting activities of 1′-hydroxysafrole for the formation of enzyme-altered foci and tumors in rat liver. Carcinogenesis 8, 531-539.
22. Kensler, T., Guyton, K., Egner, P., McCarthy, T., Lesko, S., and Akman, S. (1995) Role of reactive intermediates in tumor promotion and progression. Prog. Clin. Biol. Res. 391, 103-116.
23. Desjardins, J. P., Beard, S. E., Mapoles, J. E., Gee, P., and Thompson, J. A. (1998) Transcriptional activity of quinone methides derived from the tumor promoter butylated hydroxytoluene in HepG2 cells. Cancer Lett. 131, 201-207.
24. Eaton, D. L., and Bammier, T. K. (1999) Concise review of the glutathione S-transferases and their significance to toxicology. Toxicol. Sci. 49, 156-164.
25. Mitchell, A. E., Morin, D., Lakritz, J., and Jones, A. D. (1997) Quantitative profiling of tissue- and gender-related expression of glutathione S-transferase isoenzymes in the mouse. Biochem. J. 325 (Part 1), 207-216.
26. Howie, A. F., Forrester, L. M., Glancey, M. J., Schlager, J. J., Powis, G. J., Beckett, G. J., Hayes, J. D., and Wolf, C. R. (1990) Glutathione S-transferase and glutathione peroxidase expression in normal and tumour human tissues. Carcinogenesis 11, 451-458.
27. Tami, K., Satoh, K., Tsuchida, S., Hatayama, I., Maki, T., and Sato, K. (1990) Specific inactivation of glutathione S-transferases in class pi by SH-modifiers. Biochem. Biophys. Res. Commun. 167, 331-338.
28. Ploemen, J. H. T. M., Bogaards, J. J. P., Veldink, G. A., van Ommen, B., Jansen, D. H. M., and van Bladeren, P. J. (1993) Isozyme selective irreversible inhibition of rat and human glutathione S-transferases by ethacrynic acid and two brominated derivatives. Biochem. Pharmacol. 45, 633-639.
29. Adler, V., Yin, Z., Fuchs, S. Y., Benezra, M., Rosario, L., Tew, K. D., Pincus, M. R., Sardana, M., Henderson, C. J., Wolf, C. R., Davis, R. J., and Ronai, Z. (1999) Regulation of JNK signaling by GSTp. EMBO J. 18, 1321-1334.
30. Sun, Y., Dwyer-Nield, L. D., Malkinson, A. M., Zhang, Y. L., and Thompson, J. A. (2003) Responses of tumorigenic and nontumorigenic mouse lung epithelial cell lines to electrophilic metabolites of the tumor promoter butylated hydroxytoluene. Chem.-Biol. Interact. 145, 41-51.
31. Lewis, M. A., Yoerg, D. G., Bolton, J. L., and Thompson, J. A. (1996) Alkylation of 2′-deoxynucleosides and DNA by quinone methides derived from 2,6-di-tert-butyl-4-methylphenol. Chem. Res. Toxicol. 9, 1368-1374.
32. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
33. Habig, W. H., Pabst, M. J., and Jakoby, W. B. (1974) Glutathione S-transferases: The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 77, 7130-7139.
34. 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.
35. Wilce, M. C. J., and Parker, M. W. (1994) Structure and function of glutathione S-transferases. Biochim. Biophys. Acta 1205, 1-18.
36. Armstrong, R. M. (1994) Glutathione S-transferases: Structure and mechanism of an archetypical detoxication enzyme. In Advances in Enzymology and Related Areas of Molecular Biology (Meister, A., Ed.) pp 1-44, John Wiley and Sons, New York.
37. Lim, H., Eng, J., Yates, J. R., III, Tollaksen, S. L., Giometti, C. S., Holden, J. F., Adams, W. W., Reich, C. I., Olsen, G. J., and Hays, L. G. (2003) Identification of 2D-gel proteins: A comparison of MALDI/TOF mass mapping to μ LC-ESI tandem mass spectrometry. J. Am. Soc. Mass Spectrom. 14, 957-970.
38. Weinmann, W., Stoertzel, M., Vogt, S., and Wendt, J. (2001) Tune compounds for electrospray ionization/in-source collision-induced dissociation with mass spectral library searching. J. Chromatogr. A 926, 199-209.
39. Thompson, D. C., Barhoumi, R., and Burghardt, R. C. (1998) Comparative toxicity of eugenol and its quinone methide metabolite in cultured liver cells using kinetic fluorescence bioassays. Toxicol. Appl. Pharmacol. 149, 55-63.
40. Nakagawa, Y., Hiraga, K., and Suga, T. (1983) On the mechanism of covalent binding of butylated hydroxytoluene to microsomal protein. Biochem. Pharmacol. 32, 1417-1421.
41. Bolton, J. L., and Thompson, J. A. (1991) Oxidation of butylated hydroxytoluene to toxic metabolites. Factors influencing hydroxylation and quinone methide formation by hepatic and pulmonary microsomes. Drug Metab. Dispos. 19, 467-472.
42. van Zanden, J. J., Ben Hamman, O., van Iersel, M. L., Boeren, S., Cnubben, N. H., Lo Bello, M., Vervoort, J., van Bladeren, P. J., and Rietjens, I. M. (2003) Inhibition of human glutathione S-transferase P1-1 by the flavonoid quercetin. Chem.-Biol. Interact. 145, 139-148.
43. Chang, M., Shin, Y. G., van Breemen, R. B., Blond, S. Y., and Bolton, J. L. (2001) Structural and functional consequences of inactivation of human glutathione S-transferase P1-1 mediated by the catechol metabolite of equine estrogens, 4-hydroxyequilenin. Biochemistry 40, 4811-4820.
44. Dirr, H., Reinemer, P., and Huber, R. (1994) X-ray crystal structures of cytosolic glutathione S-transferases. Implications for protein architecture, substrate recognition and catalytic function. Eur. J. Biochem. 220, 645-661.
45. Nishihira, J., Ishibashi, T., Sakai, M., Nishi, S., Kumazaki, T., Hatanaka, Y., Tsuda, S., and Hikichi, K. (1992) Characterization of cysteine residues of glutathione S-transferase P: Evidence for steric hindrance of substrate binding by a bulky adduct to cysteine 47. Biochem. Biophys. Res. Commun. 188, 424-432.
46. Kong, K. H., Inoue, H., and Takahashi, K. (1991) Nonessentiality of cysteine and histidine residues for the activity of human class PI glutathione S-transferase. Biochem. Biophys. Res. Commun. 181, 748-755.
47. Ricci, G., Del Boccio, G., Pennelli, A., Lo Bello, M., Petruzzelli, R., Caccuri, A. M., Barra, D., and Federici, G. (1991) Redox forms of human placenta glutathione transferase. J. Biol. Chem. 266, 21409-21415.
48. Lo Bello, M., Parker, M. W., Desideri, A., Polticelli, F., Falconi, M., Del Boccio, G., Pennelli, A., Federici, G., and Ricci, G. (1993) Peculiar spectroscopic and kinetic properties of Cys-47 in human placental glutathione S-transferase. Evidence for an atypical thiolate ion pair near the active site. J. Biol. Chem. 268, 19033-19038.
49. Stoker, M. G. (1967) Transfer of growth inhibition between normal and virus-transformed cells: Autoradiographic studies using marked cells. J. Cell Sci. 2, 293-304.
50. DiGiovanni, J. (1992) Multistage carcinogenesis in mouse skin. Pharmacol. Ther. 54, 63-128.