Alkylation of cytochrome c by (glutathion-S-yl)-1,4-benzoquinone and iodoacetamide demonstrates compound-dependent site specificity

Chemical Research in Toxicology

Volumn 18, Issue 1, 2005, Pages 41-50

  Person, Maria D ^a   Mason, Daniel E ^b,c   Liebler, Daniel C ^b,d   Monks, Terrence J ^b   Lau, Serrine S ^b  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c Genomic Institute of the Novetis Foundation   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

(GLUTATHION S YL) 1,4 BENZOQUINONE; 1,4 BENZOQUINONE DERIVATIVE; ALKYLATING AGENT; CYSTEINE DERIVATIVE; CYTOCHROME C; GLUTATHIONE; HISTIDINE; IODOACETAMIDE; LYSINE; QUINONE DERIVATIVE; THIOL DERIVATIVE; UNCLASSIFIED DRUG;

ALKYLATION; ARTICLE; CYCLIZATION; MASS SPECTROMETRY; PEPTIDE ANALYSIS; PH; PROTEIN MODIFICATION; SPECTROSCOPY;

ALGORITHMS; ALKYLATING AGENTS; ALKYLATION; AMINO ACID SEQUENCE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYTOCHROMES C; GLUTATHIONE; IODOACETAMIDE; MOLECULAR SEQUENCE DATA; PEPTIDES; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 12144255851     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx049873n     Document Type: Article

References (35)

1. Nerland, D. E., Cai, J., and Benz, F. W. (2003) Selective covalent binding of acrylonitrile to Cys 186 in rat liver carbonic anhydrase III in vivo. Chem. Res. Toxicol. 16, 583-589.
2. Nerland, D. E., Cai, J., Pierce, W. M., Jr., and Benz, F. W. (2001) Covalent binding of acrylonitrile to specific rat liver glutathione S-transferases in vivo. Chem. Res. Toxicol. 14, 799-806.
3. Slaughter, D. E., and Hanzlik, R. P. (1991) Identification of epoxide- and quinone-derived bromobenzene adducts to protein sulfur nucleophiles. Chem. Res. Toxicol. 4, 349-359.
4. Lau, S. S., and Zannoni, V. G. (1981) Bromobenzene epoxidation leading to binding on macromolecular protein sites. J. Pharmacol. Exp. Ther. 219, 563-572.
5. Alderton, A. L., Faustman, C., Liebler, D. C., and Hill, D. W. (2003) Induction of redox instability of bovine myoglobin by adduction with 4-hydroxy-2-nonenal. Biochemistry 42, 4398-4405.
6. Bambal, R. B., and Hanzlik, R. P. (1995) Bromobenzene 3,4-oxide alkylates histidine and lysine side chains of rat liver proteins in vivo. Chem. Res. Toxicol. 8, 729-735.
7. Qi, P. X., Di Stefano, D. L., and Wand, A. J. (1994) Solution structure of horse heart ferrocytochrome c determined by high-resolution NMR and restrained simulated annealing. Biochemistry 33, 6408-6417.
8. Qi, P. X., Beckman, R. A., and Wand, A. J. (1996) Solution structure of horse heart ferricytochrome c and detection of redox-related structural changes by high-resolution 1H NMR. Biochemistry 35, 12275-12286.
9. Bushnell, G. W., Louie, G. V., and Brayer, G. D. (1990) High-resolution three-dimensional structure of horse heart cytochrome c. J. Mol. Biol. 214, 585-595.
10. Banci, L., Bertini, I., Gray, H. B., Luchinat, C., Reddig, T., Rosato, A., and Turano, P. (1997) Solution structure of oxidized horse heart cytochrome c. Biochemistry 36, 9867-9877.
11. Person, M. D., Monks, T. J., and Lau, S. S. (2003) An integrated approach to identifying chemically induced posttranslational modifications using comparative MALDI-MS and targeted HPLC-ESI-MS/MS. Chem. Res. Toxicol. 16, 598-608.
12. Pearson, K. M., Pannell, L. K., and Fales, H. M. (2002) Intramolecular cross-linking experiments on cytochrome c and ribonuclease A using an isotope multiplet method. Rapid Commun. Mass Spectrom. 16, 149-159.
13. Anonymous (1999) 1,4-Benzoquinone (para-quinone). IARC Monogr. Eval. Carcinog. Risks Hum. 71, 1245-1450.
14. Lau, S. S., Hill, B. A., Highet, R. J., and Monks, T. J. (1988) Sequential oxidation and glutathione addition to 1,4-benzoquinone: Correlation of toxicity with increased glutathione substitution. Mol. Pharmacol. 34, 829-836.
15. Lau, S. S., Jones, T. W., Sioco, R., Hill, B. A., Pinon, R. K., and Monks, T. J. (1990) Species differences in renal γ-glutamyl transpeptidase activity do not correlate with susceptibility to 2-bromo-(diglutathion-S-yl)- hydroquinone nephrotoxicity. Toxicology 64, 291-311.
16. Towndrow, K. M., Jia, Z., Lo, H. H., Person, M. D., Monks, T. J., and Lau, S. S. (2003) 11-Deoxy, 16,16-dimethyl prostaglandin E2 induces specific proteins in association with its ability to protect against oxidative stress. Chem. Res. Toxicol. 16, 312-319.
17. Habib, S. L., Phan, M. N., Patel, S. K., Li, D., Monks, T. J., and Lau, S. S. (2003) Reduced constitutive 8-oxoguanine-DNA glycosylase expression and impaired induction following oxidative DNA damage in the tuberin deficient Eker rat. Carcinogenesis 24, 573-582.
18. Kleiner, H. E., Rivera, M. I., Pumford, N. R., Monks, T. J., and Lau, S. S. (1998) Immunochemical detection of quinol-thioether-derived protein adducts. Chem. Res. Toxicol. 11, 1283-1290.
19. Kleiner, H. E., Jones, T. W., Monks, T. J., and Lau, S. S. (1998) Immunochemical analysis of quinol-thioether-derived covalent protein adducts in rodent species sensitive and resistant to quinol-thioether-mediated nephrotoxicity. Chem. Res. Toxicol. 11, 1291-1300.
20. Chen, J., Petersen, D. R., Schenker, S., and Henderson, G. I. (2000) Formation of malondialdehyde adducts in livers of rats exposed to ethanol: Role in ethanol-mediated inhibition of cytochrome c oxidase. Alcohol.: Clin. Exp. Res. 24, 544-552.
21. Hansen, B. T., Jones, J. A., Mason, D. E., and Liebler, D. C. (2001) SALSA: A pattern recognition algorithm to detect electrophile-adducted peptides by automated evaluation of CID spectra in LC-MS-MS analyses. Anal. Chem. 73, 1676-1683.
22. Liebler, D. C. (2002) Proteomic approaches to characterize protein modifications: New tools to study the effects of environmental exposures. Environ. Health Perspect. 110 (Suppl. 1), 3-9.
23. Liebler, D. C., Hansen, B. T., Jones, J. A., Badghisi, H., and Mason, D. E. (2003) Mapping protein modifications with liquid chromatography-mass spectrometry and the SALSA algorithm. Adv. Protein Chem. 65, 195-216.
24. Biemann, K. (1990) Appendix 5. Nomenclature for peptide fragment ions (positive ions). Methods Enzymol. 193, 886-887.
25. Alt, C., and Eyer, P. (1998) Ring addition of the α-amino group of glutathione increases the reactivity of benzoquinone thioethers. Chem. Res. Toxicol. 11, 1223-1233.
26. Monks, T. J., Highet, R. J., and Lau, S. S. (1990) Oxidative cyclization, 1,4-benzothiazine formation and dimerization of 2-bromo-3-(glutathion-S-yl) hydroquinone. Mol. Pharmacol. 38, 121-127.
27. Banci, L., Bertini, I., Bren, K. L., Gray, H. B., Sompornpisut, P., and Turano, P. (1995) Three-dimensional solution structure of the cyanide adduct of a Met80Ala variant of Saccharomyces cerevisiae iso-1-cytochrome c. Identification of ligand-residue interactions in the distal heme cavity. Biochemistry 34, 11385-11398.
28. Kim, J. Y., Kim, K. W., Kwon, H. J., Lee, D. W., and Yoo, J. S. (2002) Probing lysine acetylation with a modification-specific marker ion using high-performance liquid chromatography/electrospray-mass spectrometry with collision-induced dissociation. Anal. Chem. 74, 5443-5449.
29. Hanzlik, R. P., Harriman, S. P., and Frauenhoff, M. M. (1994) Covalent binding of benzoquinone to reduced ribonuclease. Adduct structures and stoichiometry. Chem. Res. Toxicol. 7, 177-184.
30. Musatov, A., Carroll, C. A., Liu, Y. C., Henderson, G. I., Weintraub, S. T., and Robinson, N. C. (2002) Identification of bovine heart cytochrome c oxidase subunits modified by the lipid peroxidation product 4-hydroxy-2-nonenal. Biochemistry 41, 8212-8220.
31. Salemme, F. R. (1976) An hypothetical structure for an intermolecular electron-transfer complex of cytochromes c and b5. J. Mol. Biol. 102, 563-568.
32. Wendoloski, J. J., Matthew, J. B., Weber, P. C., and Salemme, F. R. (1987) Molecular dynamics of a cytochrome c-cytochrome b5 electron-transfer complex. Science 238, 794-797.
33. Liu, X., Kim, C. N., Yang, J., Jemmerson, R., and Wang, X. (1996) Induction of apoptotic program in cell-free extracts: Requirement for dATP and cytochrome c. Cell 86, 147-157.
34. Zou, H., Henzel, W. J., Liu, X., Lutschg, A., and Wang, X. (1997) Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90, 405-413.
35. Yu, T., Wang, X., Purring-Koch, C., Wei, Y., and McLendon, G. L. (2001) A mutational epitope for cytochrome c binding to the apoptosis protease activation factor-1. J. Biol. Chem. 276, 13034-13038.