Characterization of rat liver proteins adducted by reactive metabolites of menthofuran

Chemical Research in Toxicology

Volumn 25, Issue 11, 2012, Pages 2301-2309

  Khojasteh, S Cyrus ^a   Hartley, Dylan P ^d   Ford, Kevin A ^a   Uppal, Hirdesh ^a   Oishi, Shimako ^b   Nelson, Sidney D ^c  

^a GENENTECH INC   (United States)

^b Abbott Japan Co Ltd   (Japan)

^c UNIVERSITY OF WASHINGTON   (United States)

^d ARRAY BIOPHARMA INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE ISOENZYME 2; LIVER PROTEIN; MALATE DEHYDROGENASE; MENTHOFURAN; MITOCHONDRIAL ATP SYNTHASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SERUM ALBUMIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; ENZYME ACTIVITY; HOMEOSTASIS; LIQUID CHROMATOGRAPHY; LIVER TOXICITY; MASS SPECTROMETRY; METABOLITE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN ISOLATION; PROTEIN TARGETING; RAT; TWO DIMENSIONAL GEL ELECTROPHORESIS; WESTERN BLOTTING;

ALDEHYDE DEHYDROGENASE; ANIMALS; CYTOPLASM; DOSE-RESPONSE RELATIONSHIP, DRUG; LIVER; MALATE DEHYDROGENASE; MALE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MOLECULAR STRUCTURE; MONOTERPENES; RATS; RATS, SPRAGUE-DAWLEY; SERUM ALBUMIN; STRUCTURE-ACTIVITY RELATIONSHIP;

RATTUS;

EID: 84869390142     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx300144d     Document Type: Article

References (57)

1. Gordon, W. P., Huitric, A. C., Seth, C. L., McClanahan, R. H., and Nelson, S. D. (1987) The metabolism of the abortifacient terpene, (R)-(+)-pulegone, to a proximate toxin, menthofuran Drug Metab. Dispos. 15, 589-594
2. Anderson, I. B., Mullen, W. H., Meeker, J. E., Khojasteh Bakht, S. C., Oishi, S., Nelson, S. D., and Blanc, P. D. (1996) Pennyroyal toxicity: measurement of toxic metabolite levels in two cases and review of the literature Ann. Intern. Med. 124, 726-734
3. Bakerink, J. A., Gospe, S. M., Jr., Dimand, R. J., and Eldridge, M. W. (1996) Multiple organ failure after ingestion of pennyroyal oil from herbal tea in two infants Pediatrics 98, 944-947
4. Allen, W. T. (1897) Note on a case of supposed poisoning by pennyroyal Lancet 1, 1022-1023
5. Sullivan, J. B., Jr., Rumack, B. H., Thomas, H., Jr., Peterson, R. G., and Bryson, P. (1979) Pennyroyal oil poisoning and hepatotoxicity JAMA 242, 2873-2874
6. Nelson, S. D. (1995) Mechanisms of the formation and disposition of reactive metabolites that can cause acute liver injury Drug Metab. Rev 27, 147-177
7. McClanahan, R. H., Thomassen, D., Slattery, J. T., and Nelson, S. D. (1989) Metabolic activation of (R)-(+)-pulegone to a reactive enonal that covalently binds to mouse liver proteins Chem. Res. Toxicol. 2, 349-355
8. Thomassen, D., Knebel, N., Slattery, J. T., McClanahan, R. H., and Nelson, S. D. (1992) Reactive intermediates in the oxidation of menthofuran by cytochromes P-450 Chem. Res. Toxicol. 5, 123-130
9. Thomassen, D., Slattery, J. T., and Nelson, S. D. (1988) Contribution of menthofuran to the hepatotoxicity of pulegone: assessment based on matched area under the curve and on matched time course J. Pharmacol. Exp. Ther 244, 825-829
10. Nelson, S. D. and Pearson, P. G. (1990) Covalent and noncovalent interactions in acute lethal cell injury caused by chemicals Annu. Rev. Pharmacol. Toxicol. 30, 169-195
11. Ikehata, K., Duzhak, T. G., Galeva, N. A., Ji, T., Koen, Y. M., and Hanzlik, R. P. (2008) Protein targets of reactive metabolites of thiobenzamide in rat liver in vivo Chem. Res. Toxicol. 21, 1432-1442
12. Hanzlik, R. P., Fang, J., and Koen, Y. M. (2009) Filling and mining the reactive metabolite target protein database Chem.-Biol. Interact. 179, 38-44
13. Qiu, Y., Benet, L. Z., and Burlingame, A. L. (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
14. Roberts, D. W., Pumford, N. R., Potter, D. W., Benson, R. W., and Hinson, J. A. (1987) A sensitive immunochemical assay for acetaminophen-protein adducts J. Pharmacol. Exp. Ther. 241, 527-533
15. Bartolone, J. B., Sparks, K., Cohen, S. D., and Khairallah, E. A. (1987) Immunochemical detection of acetaminophen-bound liver proteins Biochem. Pharmacol. 36, 1193-1196
16. Pumford, N. R., Myers, T. G., Davila, J. C., Highet, R. J., and Pohl, L. R. (1993) Immunochemical detection of liver protein adducts of the nonsteroidal antiinflammatory drug diclofenac Chem. Res. Toxicol. 6, 147-150
17. Satoh, H., Martin, B. M., Schulick, A. H., Christ, D. D., Kenna, J. G., and Pohl, L. R. (1989) Human anti-endoplasmic reticulum antibodies in sera of patients with halothane-induced hepatitis are directed against a trifluoroacetylated carboxylesterase Proc. Natl. Acad. Sci. U.S.A. 86, 322-326
18. Bonierbale, E., Valadon, P., Pons, C., Desfosses, B., Dansette, P. M., and Mansuy, D. (1999) Opposite behaviors of reactive metabolites of tienilic acid and its isomer toward liver proteins: use of specific anti-tienilic acid-protein adduct antibodies and the possible relationship with different hepatotoxic effects of the two compounds Chem. Res. Toxicol. 12, 286-296
19. Halmes, N. C., McMillan, D. C., Oatis, J. E., Jr., and Pumford, N. R. (1996) Immunochemical detection of protein adducts in mice treated with trichloroethylene Chem. Res. Toxicol. 9, 451-456
20. Druckova, A., Mernaugh, R. L., Ham, A. J., 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
21. Koenigs, L. L., Peter, R. M., Hunter, A. P., Haining, R. L., Rettie, A. E., Friedberg, T., Pritchard, M. P., Shou, M., Rushmore, T. H., and Trager, W. F. (1999) Electrospray ionization mass spectrometric analysis of intact cytochrome P450: identification of tienilic acid adducts to P450 2C9 Biochemistry 38, 2312-2319
22. Koen, Y. M., Sarma, D., Williams, T. D., Galeva, N. A., Obach, R. S., and Hanzlik, R. P. (2012) Identification of protein targets of reactive metabolites of tienilic acid in human hepatocytes Chem. Res. Toxicol. 25, 1868-1877
23. Methogo, Y. M., Dansette, P. M., and KKlarskov, K. (2007) Identification of liver protein targets modified covalently by tienilic acid metabolites using a two dimensional Western blot-mass spectrometry approach Int. J. Mass Spectrom. 268, 284-295
24. Sanchez, J. C., Rouge, V., Pisteur, M., Ravier, F., Tonella, L., Moosmayer, M., Wilkins, M. R., and Hochstrasser, D. F. (1997) Improved and simplified in-gel sample application using reswelling of dry immobilized pH gradients Electrophoresis 18, 324-327
25. Khojasteh, S. C., Oishi, S., and Nelson, S. D. (2010) Metabolism and toxicity of menthofuran in rat liver slices and in rats Chem. Res. Toxicol. 23, 1824-1832
26. Gerlach, R. W., White, R. J., Deming, S. N., Palasota, J. A., and van Emon, J. M. (1993) An evaluation of five commercial immunoassay data analysis software systems Anal. Biochem. 212, 185-193
27. Rabilloud, T., Valette, C., and Lawrence, J. J. (1994) Sample application by in-gel rehydration improves the resolution of two-dimensional electrophoresis with immobilized pH gradients in the first dimension Electrophoresis 15, 1552-1558
28. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels Anal. Chem. 68, 850-858
29. Wang, H., Lim, K. B., Lawrence, R. F., Howald, W. N., Taylor, J. A., Ericsson, L. H., Walsh, K. A., and Hackett, M. (1997) Stability enhancement for peptide analysis by electrospray using the triple quadrupole mass spectrometer Anal. Biochem. 250, 162-168
30. Yates, J. R., III, Eng, J. K., and McCormack, A. L. (1995) Mining genomes: correlating tandem mass spectra of modified and unmodified peptides to sequences in nucleotide databases Anal. Chem. 67, 3202-3210
31. Willis, J. H., Capaldi, R. A., Huigsloot, M., Rodenburg, R. J., Smeitink, J., and Marusich, M. F. (2009) Isolated deficiencies of OXPHOS complexes I and IV are identified accurately and quickly by simple enzyme activity immunocapture assays Biochim. Biophys. Acta 1787, 533-538
32. Li, F. C., Yen, J. C., Chan, S. H., and Chang, A. Y. (2012) Bioenergetics failure and oxidative stress in brain stem mediates cardiovascular collapse associated with fatal methamphetamine intoxication PLoS One 7, e30589
33. Aggeler, R., Coons, J., Taylor, S. W., Ghosh, S. S., Garcia, J. J., Capaldi, R. A., and Marusich, M. F. (2002) A functionally active human F1F0 ATPase can be purified by immunocapture from heart tissue and fibroblast cell lines. Subunit structure and activity studies J. Biol. Chem. 277, 33906-33912
34. Oishi, S. and Nelson, S. D. (1992) Evidence for the formation of heterocyclic arene oxides a g-keto enal by reaction of menthofuran with dimethyldioxirane J. Org. Chem. 57, 2744-2747
35. Khojasteh-Bakht, S. C., Chen, W., Koenigs, L. L., Peter, R. M., and Nelson, S. D. (1999) Metabolism of (R)-(+)-pulegone and (R)-(+)-menthofuran by human liver cytochrome P-450s: evidence for formation of a furan epoxide Drug Metab. Dispos. 27, 574-580
36. Thomassen, D., Slattery, J. T., and Nelson, S. D. (1990) Menthofuran-dependent and independent aspects of pulegone hepatotoxicity: roles of glutathione J. Pharmacol. Exp. Ther. 253, 567-572
37. Thomassen, D., Pearson, P. G., Slattery, J. T., and Nelson, S. D. (1991) Partial characterization of biliary metabolites of pulegone by tandem mass spectrometry. Detection of glucuronide, glutathione, and glutathionyl glucuronide conjugates Drug Metab. Dispos. 19, 997-1003
38. Madyastha, K. M. and Raj, C. P. (1990) Biotransformations of R-(+)-pulegone and menthofuran in vitro: chemical basis for toxicity Biochem. Biophys. Res. Commun. 173, 1086-1092
39. Lindahl, R. and Evces, S. (1984) Comparative subcellular distribution of aldehyde dehydrogenase in rat, mouse and rabbit liver Biochem. Pharmacol. 33, 3383-3389
40. Vasiliou, V. and Nebert, D. W. (2005) Analysis and update of the human aldehyde dehydrogenase (ALDH) gene family Hum. Genomics 2, 138-143
41. Svanas, G. W. and Weiner, H. (1985) Aldehyde dehydrogenase activity as the rate-limiting factor for acetaldehyde metabolism in rat liver Arch. Biochem. Biophys. 236, 36-46
42. Esterbauer, H., Schaur, R. J., and Zollner, H. (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes Free Radical Biol. Med. 11, 81-128
43. Farres, J., Wang, T. T., Cunningham, S. J., and Weiner, H. (1995) Investigation of the active site cysteine residue of rat liver mitochondrial aldehyde dehydrogenase by site-directed mutagenesis Biochemistry 34, 2592-2598
44. Sheikh, S., Ni, L., Hurley, T. D., and Weiner, H. (1997) The potential roles of the conserved amino acids in human liver mitochondrial aldehyde dehydrogenase J. Biol. Chem. 272, 18817-18822
45. Weiner, H. (1982) Aldehyde dehydrogenase Prog. Clin. Biol. Res. 114, 1-9
46. Druckova, A., Mernaugh, R. L., Ham, A. J., 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
47. Landin, J. S., Cohen, S. D., and Khairallah, E. A. (1996) Identification of a 54-kDa mitochondrial acetaminophen-binding protein as aldehyde dehydrogenase Toxicol. Appl. Pharmacol. 141, 299-307
48. 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
49. 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 Biochimie 89, 393-402
50. Williams, K. E., Carver, T. A., Miranda, J. J., Kautiainen, A., Vogel, J. S., Dingley, K., Baldwin, M. A., Turteltaub, K. W., and Burlingame, A. L. (2002) Attomole detection of in vivo protein targets of benzene in mice: evidence for a highly reactive metabolite Mol. Cell. Proteomics 1, 885-895
51. Moon, K. H., Kim, B. J., and Song, B. J. (2005) Inhibition of mitochondrial aldehyde dehydrogenase by nitric oxide-mediated S-nitrosylation FEBS Lett. 579, 6115-6120
52. Williamson, R. L. and Metcalf, R. L. (1967) Salicylanilides: a new group of active uncouplers of oxidative phosphorylation Science 158, 1694-1695
53. Landin, J. S., Cohen, S. D., and Khairallah, E. A. (1996) Identification of a 54-kDa mitochondrial acetaminophen-binding protein as aldehyde dehydrogenase Toxicol. Appl. Pharmacol. 141, 299-307
54. Cunningham, D. and Cross, R. L. (1988) Catalytic site occupancy during ATP hydrolysis by MF1-ATPase. Evidence for alternating high affinity sites during steady-state turnover J. Biol. Chem. 263, 18850-18856
55. Vignais, P. V. and Lunardi, J. (1985) Chemical probes of the mitochondrial ATP synthesis and translocation Annu. Rev. Biochem. 54, 977-1014
56. DeStefano-Shields, C., Morin, D., and Buckpitt, A. (2010) Formation of covalently bound protein adducts from the cytotoxicant naphthalene in nasal epithelium: species comparisons Environ. Health Perspect 118, 647-652
57. Mugford, C. A., Carfagna, M. A., and Kedderis, G. L. (1997) Furan-mediated uncoupling of hepatic oxidative phosphorylation in Fischer-344 rats: an early event in cell death Toxicol. Appl. Pharmacol. 144, 1-11