The frequency of 1,4-Benzoquinone-lysine adducts in cytochrome c correlate with defects in apoptosome activation

Toxicological Sciences

Volumn 122, Issue 1, 2011, Pages 64-72

  Fisher, Ashley A ^a   Labenski, Matthew T ^a   Malladi, Srinivas ^b,c   Chapman, John D ^a   Bratton, Shawn B ^b   Monks, Terrence J ^a   Lau, Serrine S ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

1,4 benzoquinone; Apoptosome formation; Cytochrome c; Fractionation; Liquid IEF separation; Posttranslational modification

Indexed keywords

1,4 BENZOQUINONE; APOPTOSOME; CASPASE 3; CYTOCHROME C; LYSINE; QUINONE DERIVATIVE; REACTIVE OXYGEN METABOLITE; SULFIDE;

ARTICLE; ARYLATION; CHEMICAL STRUCTURE; CIRCULAR DICHROISM; ENZYME ACTIVATION; ISOELECTRIC FOCUSING; MOLECULAR MODEL; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION;

EID: 79960976076     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr085     Document Type: Article

References (32)

1. Bolton, J. L., and Thatcher, G. R. (2008). Potential mechanisms of estrogen quinone carcinogenesis. Chem. Res. Toxicol. 21, 93-101.
2. Bolton, J. L., Trush, M. A., Penning, T. M., Dryhurst, G., and Monks, T. J. (2000). Role of quinones in toxicology. Chem. Res. Toxicol. 13, 135-160.
3. Bratton, S. B., and Salvesen, G. S. (2010). Regulation of the Apaf-1-caspase-9 apoptosome. J. Cell Sci. 123, 3209-3214.
4. Bratton, S. B., Walker, G., Srinivasula, S. M., Sun, X. M., Butterworth, M., Alnemri, E. S., and Cohen, G. M. (2001). Recruitment, activation and retention of caspases-9 and -3 by Apaf-1 apoptosome and associated XIAP complexes. EMBO J. 20, 998-1009.
5. Bushnell, G. W., Louie, G. V., and Brayer, G. D. (1990). High-resolution threedimensional structure of horse heart cytochrome c. J. Mol. Biol. 214, 585-595.
6. Carbone, D. L., Doorn, J. A., Kiebler, Z., and Petersen, D. R. (2005). Cysteine modification by lipid peroxidation products inhibits protein disulfide isomerase. Chem. Res. Toxicol. 18, 1324-1331.
7. Cohen, S. D., Pumford, N. R., Khairallah, E. A., Boekelheide, K., Pohl, L. R., Amouzadeh, H. R., and Hinson, J. A. (1997). Selective protein covalent binding and target organ toxicity. Toxicol. Appl. Pharmacol. 143, 1-12.
8. D'Amici, G. M., Timperio, A. M., and Zolla, L. (2008). Coupling of native liquid phase isoelectrofocusing and blue native polyacrylamide gel electrophoresis a potent tool for native membrane multiprotein complex separation. J. Proteome. Res. 7, 1326-1340.
9. Demozay, D., Mas, J. C., Rocchi, S., and Van Obberghen, E. (2008). Faldh reverses the deleterious action of oxidative stress induced by the lipid peroxidation product, Hne, on insulin signaling in 3t3-L1 adipocytes. Diabetes 57, 1216-1226.
10. Discover 3.0 ESFF (extensible systematic force field). Molecular Mechanics Force Fields, Insight II 2005, Molecular Modeling Software. Accelrys, Inc., San Diego, CA.
11. Fisher, A. A., Labenski, M. T., Malladi, S., Gokhale, V., Bowen, M. E., Milleron, R. S., Bratton, S. B., Monks, T. J., and Lau, S. S. (2007). Quinone electrophiles selectively adduct "electrophile binding motifs" within cytochrome c. Biochemistry 46, 11090-11100.
12. Go, Y. M., Halvey, P. J., Hansen, J. M., Reed, M., Pohl, J., and Jones, D. P. (2007). Reactive aldehyde modification of thioredoxin-1 activates early steps of inflammation and cell adhesion. Am. J. Pathol. 171, 1670-1681.
13. Insight II. (2005). Molecular Modeling Software. Accelrys Inc, San Diego, CA.
14. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935.
15. Kamal, A., Ramu, R., Tekumalla, V., Khanna, G. B., Barkume, M. S., Juvekar, A. S., and Zingde, S. M. (2007). Synthesis, DNA binding, and cytotoxicity studies of pyrrolo[2,1-c][1,4]benzodiazepine-anthraquinone conjugates. Bioorg. Med. Chem. 15, 6868-6875.
16. Koen, Y. M., Yue, W., Galeva, N. A., Williams, T. D., and Hanzlik, R. P. (2006). Site-specific arylation of rat glutathione S-transferase A1 and A2 by bromobenzene metabolites in vivo. Chem. Res. Toxicol. 19, 1426-1434.
17. Liebler, D. C. (2008). Protein damage by reactive electrophiles: targets and consequences. Chem. Res. Toxicol. 21, 117-128.
18. Malladi, S., Challa-Malladi, M., Fearnhead, H. O., and Bratton, S. B. (2009). The Apaf-1*procaspase-9 apoptosome complex functions as a proteolyticbased molecular timer. EMBO J. 28, 1916-1925.
19. Pagano, G. (2002). Redox-modulated xenobiotic action and ROS formation: a mirror or a window? Hum. Exp. Toxicol. 21, 77-81.
20. Person, M. D., Mason, D. E., Liebler, D. C., Monks, T. J., and Lau, S. S. (2005). Alkylation of cytochrome c by (glutathion-S-yl)-1,4-benzoquinone and iodoacetamide demonstrates compound-dependent site specificity. Chem. Res. Toxicol. 18, 41-50.
21. 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.
22. Peters, M. M., Jones, T. W., Monks, T. J., and Lau, S. S. (1997). Cytotoxicity and cell-proliferation induced by the nephrocarcinogen hydroquinone and its nephrotoxic metabolite 2,3,5-(tris-glutathion-S-yl)hydroquinone. Carcinogenesis 18, 2393-2401.
23. Peters, M. M., Rivera, M. I., Jones, T. W., Monks, T. J., and Lau, S. S. (1996). Glutathione conjugates of tert-butyl-hydroquinone, a metabolite of the urinary tract tumor promoter 3-tert-butyl-hydroxyanisole, are toxic to kidney and bladder. Cancer Res. 56, 1006-1011.
24. Poli, G., Biasi, F., and Leonarduzzi, G. (2008). 4-Hydroxynonenal-protein adducts: a reliable biomarker of lipid oxidation in liver diseases. Mol. Aspects Med. 29, 67-71.
25. Price, C. L., and Knight, S. C. (2007). Advanced glycation: a novel outlook on atherosclerosis. Curr. Pharm. Des. 13, 3681-3687.
26. Ross, D. (2000). The role of metabolism and specific metabolites in benzeneinduced toxicity: evidence and issues. J. Toxicol. Environ. Health A 61, 357-372.
27. Sampey, B. P., Carbone, D. L., Doorn, J. A., Drechsel, D. A., and Petersen, D. R. (2007). 4-Hydroxy-2-nonenal adduction of extracellular signal-regulated kinase (Erk) and the inhibition of hepatocyte Erk-Est-like protein-1-activating protein-1 signal transduction. Mol. Pharmacol. 71, 871-883.
28. Sugiyama, Y., Sueyoshi, N., and Kameshita, I. (2006). Two-dimensional expression pattern analysis of protein kinases after separation by Micro-Rotofor/SDS-PAGE. Anal. Biochem. 359, 271-273.
29. Sumi, D., and Kumagai, Y. (2007). Chemical biology of 1,2-naphthoquinone, a novel air pollutant that affects signal transduction pathways. Yakugaku Zasshi 127, 1949-1956.
30. Verrax, J., Delvaux, M., Beghein, N., Taper, H., Gallez, B., and Buc Calderon, P. (2005). Enhancement of quinone redox cycling by ascorbate induces a caspase-3 independent cell death in human leukaemia cells. An in vitro comparative study. Free Radic. Res. 39, 649-657.
31. Wang, G., Ansari, G. A., and Khan, M. F. (2007). Involvement of lipid peroxidation-derived aldehyde-protein adducts in autoimmunity mediated by trichloroethene. J. Toxicol. Environ. Health A 70, 1977-1985.
32. 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.