Protein targets of reactive metabolites of thiobenzamide in rat liver in vivo

Chemical Research in Toxicology

Volumn 21, Issue 7, 2008, Pages 1432-1442

  Ikehata, Keisuke ^a,b   Duzhak, Tatyana G ^a   Galeva, Nadezhda A ^a   Ji, Tao ^a,c   Koen, Yakov M ^a   Hanzlik, Robert P ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

^c ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

THIOBENZAMIDE; TRYPSIN;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CELL ENERGY; COVALENT BOND; CYTOSOL; CYTOTOXICITY; ENZYME INHIBITION; HOMEOSTASIS; HYDROLYSIS; IN VIVO STUDY; LIVER; LIVER TOXICITY; MALE; METABOLITE; MICROSOME; NONHUMAN; OXIDATION; PROTEIN ANALYSIS; PROTEIN TARGETING; RADIOACTIVITY; RAT; TWO DIMENSIONAL GEL ELECTROPHORESIS; UNINDEXED SEQUENCE;

ANIMALS; ANTITUBERCULAR AGENTS; CELL FRACTIONATION; CYTOSOL; DISEASE MODELS, ANIMAL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; INJECTIONS, INTRAPERITONEAL; LIVER; MALE; MICROSOMES, LIVER; PEPTIDE MAPPING; PROTEIN BINDING; PROTEINS; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY; THIOAMIDES;

ANIMALIA; RATTUS;

EID: 49049113052     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx800093k     Document Type: Article

References (79)

1. Hanzlik, R. P., Cashman, J. R., and Traiger, G. J. (1980) Relative hepatotoxicity of substituted thiobenzamides and thiobenzamide-S-oxides in the rat. Toxicol. Appl. Pharmacol. 55, 260-272.
2. Hanzlik, R. P., Vyas, K. P., and Traiger, G. J. (1978) Substituent effects on the hepatotoxicity of thiobenzamide derivatives in the rat. Toxicol. Appl. Pharmacol. 46, 685-694.
3. Cashman, J. R., and Hanzlik, R. P. (1981) Microsomal oxidation of thiobenzamide. A photometric assay for the flavin-containing monooxygenase. Biochem. Biophys. Res. Commun. 98, 147-153.
4. Hanzlik, R. P., and Cashman, J. R. (1983) Microsomal metabolism of thiobenzamide and thiobenzamide-S-oxide. Drug Metab. Dispos. 11, 210-215.
5. Cashman, J. R., and Hanzlik, R. P. (1982) Oxidation and other reactions of thiobenzamide derivatives of relevance to their hepatotoxicity. J. Org. Chem. 47, 4745-4650.
6. Ji, T., Ikehata, K., Koen, Y. M., Esch, S. W., Williams, T. D., and Hanzlik, R. P. (2007) Covalent modification of microsomal lipids by thiobenzamide metabolites in vivo. Chem. Res. Toxicol. 20, 701-708.
7. Park, K. B., Dalton-Brown, E., Hirst, C., and Williams, D. P. (2006) Selection of new chemical entities with decreased potential for adverse drug reactions. Eur. J. Pharmacol. 549, 1-8.
8. Park, K. B., Ketteringham, N. R., Maggs, J. L., Pirmohamed, M., and Williams, D. P. (2005) The role of metabolic activation in drug-induced hepatotoxicity. Annu. Rev. Pharmacol. Toxicol. 45, 177-202.
9. Pumford, N. R., and Halmes, N. C. (1997) Protein targets of xenobiotic reactive intermediates. Annu. Rev. Pharmacol. Toxicol. 37, 91-117.
10. Pohl, L. R., and Gillette, J. R. 1984-85 Determination of toxic pathways of metabolism by deuterium substitution. Drug Metab. Rev. 15, 1335-1351.
11. Hanzlik, R. P. (1982) Effects of substituents on reactivity and toxicity of chemically reactive intermediates. Drug Metab. Rev. 13, 207-234.
12. Cashman, J. R., Parikh, K. K., Traiger, G. J., and Hanzlik, R. P. (1983) Relative hepatotoxicity of ortho and meta monosubstituted thiobenzamides in the rat. Chem.-Biol. Interact. 45, 342-347.
13. Hanzlik, R. P. (1986) Chemistry of covalent binding: studies with bromobenzene and thiobenzamide. Adv. Exp. Med. Biol. 197, 31-40.
14. Cashman, J. R., Traiger, G. J., and Hanzlik, R. P. (1982) Pneumotoxic effects of thiobenzamide derivatives. Toxicology 23, 85-93.
15. Gottschall, D. W., Penney, D. A., Traiger, G. J., and Hanzlik, R. P. (1985) Oxidation of N-methylthiobenzamide and N-methylthiobenzamide S-oxide by liver and lung microsomes. Toxicol. Appl. Pharmacol. 78, 332-344.
16. Penney, D. A., Gottschall, D. W., Hanzlik, R. P., and Traiger, G. J. (1985) The role of metabolism in N-methylthiobenzamide-induced pneumotoxicity. Toxicol. Appl. Pharmacol. 78, 323-331.
17. Cohen, S. D., and Khairallah, E. A. (1997) Selective protein arylation and acetaminophen-induced hepatotoxicity. Drug Metab. Rev. 29, 59-77.
18. Cohen, S. D., Pumford, N. R., Khairallah, E. A., Boekelheide, K., Pohl, L. R., Amouzadeh, H. R., and Hinson, J. A. (1997) Selective potein covalent binding and target organ toxicity. Toxicol. Appl. Pharmacol. 143, 1-12.
19. Qiu, Y., Burlingame, A. L., and Benet, L. Z. (1998) Identification of the hepatic protein targets of reactive metabolites of acetaminophen in vivo in mice using two-dimensional gel electrophoresis and mass spectrometry. J. Biol. Chem. 273, 17940-17953.
20. Koen, Y. M., Gogichaeva, N. V., Alterman, M. A., and Hanzlik, R. P. (2007) A proteomic analysis of bromobenzene reactive metabolite targets in rat liver cytosol in vivo. Chem. Res. Toxicol. 20, 511-519.
21. Koen, Y. M., and Hanzlik, R. P. (2002) Identification of seven proteins in the endoplasmic reticulum as targets for reactive metabolites of bromobenzene. Chem. Res. Toxicol. 15, 699-706.
22. Evans, D. C., Watt, A. P., Nicoll-Griffith, D. A., and Baillie, T. A. (2004) Drug-protein covalent adducts: An industry perspective on minimizing the potential for drug bioactivation in drug discovery and development. Chem. Res. Toxicol. 17, 3-16.
23. 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.
24. Yue, W., Koen, Y. M., Williams, T. D., and Hanzlik, R. P. (2005) Use of isotopic signatures for mass spectral detection of protein adduction by chemically reactive metabolites of bromobenzene: Studies with model proteins. Chem. Res. Toxicol. 18, 1748-1754.
25. 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.
26. Zheng, J., and Hanzlik, R. P. (1991) Premercapturic acid metabolites of bromobenzene derived via its 2,3- and 3,4-oxide metabolites. Xenobiotica 21, 535-546.
27. Nelson, S. D., and Trager, W. F. (2003) The use of deuterium isotope effects to probe the active site properties, mechanism of cytochrome P450-catalyzed reactions, and mechanisms of metabolically dependent toxicity. Drug Metab. Dispos. 31, 1481-1498.
28. Pohl, L. R., and Krishna, G. (1978) Deuterium isotope effect in bioactivation and hepatotoxicity of chloroform. Life Sci. 23, 1067-1072.
29. Dyroff, M. C, and Neal, R. A. (1981) Identification of the major protein adduct formed in rat liver after thioacetamide administration. Cancer Res. 41, 3430-3435.
30. Dyroff, M. C., and Neal, R. A. (1983) Studies of the mechanism of metabolism of thioacetamide S-oxide by rat liver microsomes. Mol. Pharmacol. 233, 219-227.
31. Hanzlik, R. P., Koen, Y. M., Theertham, B., Dong, Y., and Fang, J. (2007) The reactive metabolite Target Protein Database (TPDB)-A web-accessible resource. BMC Bioinformatics 8, 95.
32. Hinman, A., Chuang, H., Bautista, D. M., and Julius, D. (2006) TRP channel activation by reversible covalent modification. Proc. Natl. Acad. Sci. U.S.A. 103, 19564-19568.
33. Macpherson, L. J., Dubin, A. E., Evans, M. J., Marr, F., Schultz, P. G., Cravatt, B. F., and Patapoutian, A. (2007) Noxious compounds activate TRPA1 ion channels through covalent mocification of cysteines. Nature 445, 541-545.
34. Monks, T. J., Hinson, J. A., and Gillette, J. R. (1983) Bromobenzene and p-bromophenol toxicity and covalent binding in vivo. Life Sci. 30, 841-848.
35. Roberts, S. A., and Jollow, D. J. (1978) Acetaminophen structure-toxicity relationships: Why is 3-hydroxyacetanilide not hepatotoxic? Pharmacologist 20, 259.
36. Asif, A. R., Armstrong, V. W., Voland, A., Wieland, E., Oellerich, M., and Shipkova, M. (2007) Proteins identified as targets of the acyl glucuronide metabolite of mycophenolic acid in kidney tissue from mycophenolate mofetil treated rats. Biochemie 89, 393-402.
37. Huang, L., Sun, G., Cobessi, D., Wang, A. C., Shen, J. T., Tung, E. Y., Anderson, V. E., and Berry, E. A. (2006) 3-Nitropropionic acid is a suicide substrate of mitochondrial respiration that, upon osication by complex ii, forms a covalent adduct with a catalytic base arginine in the active site of the enzyme. J. Biol. Chem. 281, 5965-5972.
38. Wallace, K. B., Eells, J. T., Madiera, V. M. C., Cortopassi, G., and Jones, D. P. (1997) Mitochondrial-mediated cell injury. Fundam. Appl. Toxicol. 238, 23-37.
39. Dietze, E. C., Schäfer, A., Omichinski, J. G., and Nelson, S. D. (1997) Inactivation of glyceraldehyde-3-phosphate dehydrogenase by a reactive metabolite of acetaminophen and mass spectral characterization of an arylated active site peptide. Chem. Res. Toxicol. 10, 1097-1103.
40. Barber, D. S., Stevens, S., and LoPachin, R. M. (2007) Proteomic analysis of rat striatal synaptosomes during acrylamide intoxication at a low dose rate. Toxicol. Sci. 100, 156-167.
41. Marx, J. (2006) A stressful situation. Science 313, 1564-1566.
42. Cribb, A. E., Peyrou, M., and Muruganandan, S. (2005) The endoplasmic reticulum in xenobiotic toxicity. Drug Metab. Rev. 37, 405-442.
43. Schröder, M., and Kohno, K. (2007) Recent advances in understanding the unfolded protein response. Antioxid. Redox Signaling 9, 2241-2244.
44. Suzuki, T., Lu, J., Zahed, M., Kita, K., and Suzuki, N. (2007) Reduction of GRP78 expression with siRNA activates unfolded protein response leading to apoptosis in HeLa cells. Arch. Biochem. Biophys. 468, 1-14.
45. Slepak, T. I., Tang, M., Slepak, V. Z., and Lai, K. (2007) Involvement of endoplasmic reticulum stress in a novel classic galactosemia model. Mol. Genet. Metab. 92, 78-87.
46. TPDB. The Reactive Metabolite Target Protein Database is a searchable, annotated compilation of protein targets for reactive metabolites of drugs and chemicals. It can be found at http://tpdb.medchem.ku.edu: 8080/protein_database/ .
47. Høyer-Hansen, M., and Jäättelä, M. (2007) Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ. 14, 1576-1582.
48. Cuevas, B. D., Abell, A. N., and Johnson, G. L. (2007) Role of mitogen-activatged protein kinase kinase kinases in signal integration. Oncogene 26, 3159-3171.
49. Johnson, G. L., and Nakamura, K. (2007) The c-Jun kinase/stress-activated pathway: Regulation, function and role in human disease. Biochim. Biophys. Acta 1773, 1341-1348.
50. Singh, R., and Czaja, M. (2007) Regulation of hepatocyte apoptosis by oxidative stress. J. Gastroenterol. Hepatol. 22, S45-S48.
51. Winter-Vann, A. M., and Johnson, G. L. (2007) Integrated activation of MAP3Ks balances cell fate in response to stress. J. Cell. Biochem. 102, 848-858.
52. Uhlik, M. T., Abell, A. N., Cuevas, B. D.,., Nakamura, K., and Johnson, G. L. (2004) Wiring diagrams of MAPK regulation by MEKK1, 2, and 3. Biochem. Cell Biol. 82, 658-663.
53. Dey, A., and Cederbaum, A. I. (2007) Geldanamycin, an inhibitor of Hsp90 increases cytochrome P450 2E1 mediated toxicity in HepG2 cells through sustained activation of the P38MAPK pathway. Arch. Biochem. Biophys. 461, 275-286.
54. Pimienta, G., and Pascual, J. (2007) Canonical and alternative MAPK signaling. Cell Cycle 6, 2628-2632.
55. Raman, M., Chen, W., and Cobb, M. H. (2007) Differential regulation and properties of MAPKs. Oncogene 26, 3100-3112.
56. Czaja, M. (2007) Cell signaling in oxidtive stress-induced liver injury. Semin. Liver Dis. 27, 378-389.
57. Czaja, M. J. (2002) Induction and regulation of hepatocyte apoptosis by oxidative stress. Antioxid. Redox Signaling 4, 759-767.
58. Genestra, M. (2007) Oxyl radical, redox-sensitive signalling cascades and antioxidants. Cell. Signaling 19, 1807-1819.
59. Reinehr, R., Becker, S., Keitel, V., Eberle, A., Grether-Beck, S., and Häussinger, D. (2005) Bile salt-induced apoptosis involves NADPH oxidase isoform activation. Gastroenterology 129, 2009-2031.
60. Wang, Y., Schattenberg, J. M., Rigoli, R. M., Storz, P., and Czaja, M. J. (2004) Hepatocyte resistance to oxidative stress is dependent on protein kinase C-mediated down-regulation of c-JUN/AP-1. J. Biol. Chem. 279, 31089-31097.
61. Samali, A., Nordgren, H., Zhivotovsky, B., Peterson, E., and Orrenius, S. (1999) A comparative study of apoptosis and necrosis in HepG2 cells: oxidant-induced caspase inactivation leads to necrosis. Biochem. Biophys. Res. Commun. 255, 6-11.
62. Niso-Santo, M., Moran, J. M., Garcia-Rubio, L., Gomez-Martin, A., Gonzalez-Polo, R. A., Soler, G., and Fuentes, J. M. (2006) Low concentrations of paraquat induces early activation of extracellular signal-regulated kinase 1/2, protein kinase B, and c-Jun N-terminal kinase 1/2 pathways: Role of c-Jun N-terminal kinase in paraquat-induced cell death. Toxicol. Sci. 92, 507-515.
63. Lewis, M. D., and Roberts, B. J. (2005) Role of CYP2E1 activity in endoplasmic reticulum ubiquitination, proteasome association, and the unfolded protein response. Arch. Biochem. Biophys. 436, 237-245.
64. Liu, H., Jones, B. E., Bradham, C., and Czaja, M. J. (2002) Increases cytochrome P-450 2E1 expression sensitizes hepatocytes to c-Jun-mediated cell death from TNF-α. Am. J. Physiol. 282, G257-G266.
65. Manibusan, M. K., Odin, M., and Eastmond, D. A. (2007) Postulated carbon tetrachloride mode of action: A review. J. Env. Sci. Health 25, 185-209.
66. Sayre, L. M., Lin, D., Yuan, Q., Zhu, X., and Tang, Z. (2006) Protein adducts generated from products of lipid oxidation: Focus on HNE and ONE. Drug Metab. Rev. 38, 651-675.
67. Ishii, T., Yamada, T., Mori, T., Kumazawa, S., Uchida, K., and Nakayama, T. (2007) Characterization of acrolein-induced protein cross-links. Free Radical Res. 41, 1253-1260.
68. Ishimura, A., Ishige, K., Taira, T., Shimba, S., Ono, S.-I., Ariga, H., Tezuka, M., and Ito, Y. (2008) Comparative study of hudrogen peroxide- and 4-hydroxy-2-nonenal-induced cell death in HT22 cells. Neurochem. Int. 52, 776-785.
69. Uchida, K. (2003) 4-Hydroxy-2-nonenal: A product and mediator of oxidative stress. Prog. Lipid Res. 42, 318-343.
70. Kutuk, O., and Basaga, H. (2007) Apoptosis signalling by 4-hydroxynonenal: A role for JNK-c-Jun/AP-1 pathway. Redox Rep. 12, 30-34.
71. Bochkov, V. N. (2007) Inflammmatory profile of oxidized phospholipids. Thromb. Haemostasis 97, 348-354.
72. Uchida, K. (2007) Lipid peroxidation and redox-sensitive signaling pathways. Curr. Atheroscler. Rep. 9, 216-221.
73. Kang, M.-I., Kobayashi, A., Wakabayashi, N., Kim, S.-G., and Yamamoto, M. (2004) Scaffolding of Keap1 to the actin cytosketleton controls the function of Nrf2 as key regulator of cytoprotective phase 2 genes. Proc. Natl. Acad. Sci. U.S.A. 101, 2046-2051.
74. Kwak, M.-K., Wakabayashi, N., and Kensler, T. W. (2004) Chemoprevention through the Keap1-Nrf2 signaling pathway by phase 2 enzyme inducers. Mutat. Res. 555, 133-148.
75. Dinkova-Kostova, A. T., Holtzclaw, W. D., and Kensler, T. W. (2005) The role of Keap1 in cellular protective responses. Chem. Res. Toxicol. 18, 1779-1791.
76. Nerland, D. E., Cai, J., Pierce, W. M., and Benz, F. W. (2001) Covalent binding of acrylonitrile to specific rat liver glutathione S-transferases in vivo. Chem. Res. Toxicol. 14, 799-806.
77. Cho, S.-G., Lee, Y. H., Park, H.-S., Ryoo, K., Kang, K. W., Park, J., Eom, S.-J., Kim, M. J., Chang, T.-S., Choi, S.-Y., Shim, J., Kim, Y., Dong, M.-S., Lee, M.-J., Kim, S. G., Ichijo, H., and Choi, E.-J. (2001) Glutathione S-transferase mu modulates the stress-activated signals by suppressing apoptosis signal-regulating kinase 1. J. Biol. Chem. 276, 12749-12755.
78. Townsend, D. M., and Tew, K. D. (2003) The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene 22, 7369-7375.
79. Druckova, A., Mernaugh, R. L., Ham, A. L., and Marnett, L. J. (2007) Identification of the protein targets of the reactive metabolite of teucrin A in vivo in the rat. Chem. Res. Toxicol. 20, 1393-1408.