Detection of drug bioactivation in vivo: Mechanism of nevirapine-albumin conjugate formation in patients

Chemical Research in Toxicology

Volumn 26, Issue 4, 2013, Pages 575-583

  Meng, Xiaoli ^a   Howarth, Alice ^a   Earnshaw, Caroline J ^a   Jenkins, Rosalind E ^a   French, Neil S ^a   Back, David J ^a   Naisbitt, Dean J ^a   Park, B Kevin ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN CONJUGATE; CYSTEINE; GLUTATHIONE TRANSFERASE P1; HAPTEN; HISTIDINE; HUMAN SERUM ALBUMIN; NEVIRAPINE;

ADULT; ARTICLE; CLINICAL ARTICLE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; METABOLITE;

ADULT; AGED; ANTI-HIV AGENTS; BIOTRANSFORMATION; CYSTEINE; GLUTATHIONE S-TRANSFERASE PI; HISTIDINE; HIV INFECTIONS; HIV-1; HUMANS; MIDDLE AGED; NEVIRAPINE; PROTEIN BINDING; SERUM ALBUMIN;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84876272580     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx4000107     Document Type: Article

References (39)

1. Pollard, R. B., Robinson, P., and Dransfield, K. (1998) Safety profile of nevirapine, a nonnucleoside reverse transcriptase inhibitor for the treatment of human immunodeficiency virus infection Clin. Ther. 20, 1071-1092
2. Patel, S. M., Johnson, S., Belknap, S. M., Chan, J., Sha, B. E., and Bennett, C. (2004) Serious adverse cutaneous and hepatic toxicities associated with nevirapine use by non-HIV-infected individuals J. Acquired Immune Defic. Syndr. Hum. Retrovirol. 35, 120-125
3. Kesselring, A. M., Wit, F. W., Sabin, C. A., Lundgren, J. D., Gill, M. J., Gatell, J. M., Rauch, A., Montaner, J. S., de Wolf, F., Reiss, P., Mocroft, A., and Multicohort, N. T. (2009) Risk factors for treatment-limiting toxicities in patients starting nevirapine-containing antiretroviral therapy AIDS 23, 1689-1699
4. Gozalo, C., Gerard, L., Loiseau, P., Morand-Joubert, L., Peytavin, G., Molina, J. M., Dellamonica, P., Becquemont, L., Aboulker, J. P., Launay, O., Verstuyft, C., and Grp, A. S. (2011) Pharmacogenetics of Toxicity, Plasma Trough Concentration and Treatment Outcome with Nevirapine-Containing Regimen in Anti-Retroviral-Naive HIV-Infected Adults: An Exploratory Study of the TRIANON ANRS 081 Trial Basic Clin. Pharmacol. Toxicol. 109, 513-520
5. De Lazzari, E., Leon, A., Arnaiz, J. A., Martinez, E., Knobel, H., Negredo, E., Clotet, B., Montaner, J., Storfer, S., Asenjo, M. A., Mallolas, J., Miro, J. M., and Gatell, J. M. (2008) Hepatotoxicity of nevirapine in virologically suppressed patients according to gender and CD4 cell counts HIV Med. 9, 221-226
6. Shenton, J. M., Teranishi, M., Abu-Asab, M. S., Yager, J. A., and Uetrecht, J. P. (2003) Characterization of a potential animal model of an idiosyncratic drug reaction: Nevirapine-induced skin rash in the rat Chem. Res. Toxicol. 16, 1078-1089
7. Chen, J., Mannargudi, B. M., Xu, L., and Uetrecht, J. (2008) Demonstration of the metabolic pathway responsible for nevirapine-induced skin rash Chem. Res. Toxicol. 21, 1862-1870
8. Chen, X., Tharmanathan, T., Mannargudi, B., Gou, H., and Uetrecht, J. P. (2009) A study of the specificity of lymphocytes in nevirapine-induced skin rash J. Pharmacol. Exp. Ther. 331, 836-841
9. Popovic, M., Caswell, J. L., Mannargudi, B., Shenton, J. M., and Uetrecht, J. P. (2006) Study of the sequence of events involved in nevirapine-induced skin rash in Brown Norway rats Chem. Res. Toxicol. 19, 1205-1214
10. Wen, B., Chen, Y., and Fitch, W. L. (2009) Metabolic activation of nevirapine in human liver microsomes: Dehydrogenation and inactivation of cytochrome P450 3A4 Drug Metab. Dispos. 37, 1557-1562
11. Erickson, D. A., Mather, G., Trager, W. F., Levy, R. H., and Keirns, J. J. (1999) Characterization of the in vitro biotransformation of the HIV-1 reverse transcriptase inhibitor nevirapine by human hepatic cytochromes P-450 Drug Metab. Dispos. 27, 1488-1495
12. Takakusa, H., Masumoto, H., Yukinaga, H., Makino, C., Nakayama, S., Okazaki, O., and Sudo, K. (2008) Covalent binding and tissue distribution/retention assessment of drugs associated with idiosyncratic drug toxicity Drug Metab. Dispos. 36, 1770-1779
13. Srivastava, A., Lian, L. Y., Maggs, J. L., Chaponda, M., Pirmohamed, M., Williams, D. P., and Park, B. K. (2010) Quantifying the metabolic activation of nevirapine in patients by integrated applications of NMR and mass spectrometries Drug Metab. Dispos. 38, 122-132
14. Antunes, A. M., Godinho, A. L., Martins, I. L., Oliveira, M. C., Gomes, R. A., Coelho, A. V., Beland, F. A., and Marques, M. M. (2010) Protein adducts as prospective biomarkers of nevirapine toxicity Chem. Res. Toxicol. 23, 1714-1725
15. Caixas, U., Antunes, A. M., Marinho, A. T., Godinho, A. L., Grilo, N. M., Marques, M. M., Oliveira, M. C., Branco, T., Monteiro, E. C., and Pereira, S. A. (2012) Evidence for nevirapine bioactivation in man: Searching for the first step in the mechanism of nevirapine toxicity Toxicology 301, 33-39
16. Starke, D. W. and Mieyal, J. J. (1989) Hemoglobin catalysis of a monooxygenase-like aliphatic hydroxylation reaction Biochem. Pharmacol. 38, 201-204
17. Mieyal, J. J. and Starke, D. W. (1994) Hydroxylation and dealkylation reactions catalyzed by hemoglobin Methods Enzymol. 231, 573-598
18. Almond, L. M., Edirisinghe, D., Dalton, M., Bonington, A., Back, D. J., and Khoo, S. H. (2005) Intracellular and plasma pharmacokinetics of nevirapine in human immunodeficiency virus-infected individuals Clin. Pharmacol. Ther. 78, 132-142
19. Jenkins, R. E., Meng, X., Elliott, V. L., Kitteringham, N. R., Pirmohamed, M., and Park, B. K. (2009) Characterisation of flucloxacillin and 5-hydroxymethyl flucloxacillin haptenated HSA in vitro and in vivo Proteomics: Clin. Appl. 3, 720-729
20. Chang, M., Bolton, J. L., and Blond, S. Y. (1999) Expression and purification of hexahistidine-tagged human glutathione S-transferase P1-1 in Escherichia coli Protein Expression Purif. 17, 443-448
21. Greenough, C., Jenkins, R. E., Kitteringham, N. R., Pirmohamed, M., Park, B. K., and Pennington, S. R. (2004) A method for the rapid depletion of albumin and immunoglobulin from human plasma Proteomics 4, 3107-3111
22. 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 transferase. Evidence for an atypical thiolate ion pair near the active site J. Biol. Chem. 268, 19033-19038
23. Jenkins, R. E., Kitteringham, N. R., Goldring, C. E., Dowdall, S. M., Hamlett, J., Lane, C. S., Boerma, J. S., Vermeulen, N. P., and Park, B. K. (2008) Glutathione-S-transferase pi as a model protein for the characterisation of chemically reactive metabolites Proteomics 8, 301-315
24. Sharma, A. M., Li, Y., Novalen, M., Hayes, M. A., and Uetrecht, J. (2012) Bioactivation of nevirapine to a reactive quinone methide: Implications for liver injury Chem. Res. Toxicol. 25, 1708-1719
25. Rappaport, S. M., Li, H., Grigoryan, H., Funk, W. E., and Williams, E. R. (2012) Adductomics: Characterizing exposures to reactive electrophiles Toxicol. Lett. 213, 83-90
26. He, X. M. and Carter, D. C. (1992) Atomic structure and chemistry of human serum albumin Nature 358, 209-215
27. Yvon, M., Anglade, P., and Wal, J. M. (1990) Identification of the binding sites of benzyl penicilloyl, the allergenic metabolite of penicillin, on the serum albumin molecule FEBS Lett. 263, 237-240
28. Day, B. W., Skipper, P. L., Zaia, J., Singh, K., and Tannenbaum, S. R. (1994) Enantiospecificity of covalent adduct formation by benzo[a]pyrene anti-diol epoxide with human serum albumin Chem. Res. Toxicol. 7, 829-835
29. Liyasova, M. S., Schopfer, L. M., and Lockridge, O. (2012) Cresyl saligenin phosphate, an organophosphorus toxicant, makes covalent adducts with histidine, lysine, and tyrosine residues of human serum albumin Chem. Res. Toxicol. 25, 1752-1761
30. Szapacs, M. E., Riggins, J. N., Zimmerman, L. J., and Liebler, D. C. (2006) Covalent adduction of human serum albumin by 4-hydroxy-2-nonenal: Kinetic analysis of competing alkylation reactions Biochemistry 45, 10521-10528
31. Presle, N., Lapicque, F., Fournel-Gigleux, S., Magdalou, J., and Netter, P. (1996) Stereoselective irreversible binding of ketoprofen glucuronides to albumin. Characterization of the site and the mechanism Drug Metab. Dispos. 24, 1050-1057
32. Damsten, M. C., Commandeur, J. N., Fidder, A., Hulst, A. G., Touw, D., Noort, D., and Vermeulen, N. P. (2007) Liquid chromatography/tandem mass spectrometry detection of covalent binding of acetaminophen to human serum albumin Drug Metab. Dispos. 35, 1408-1417
33. Wang, Z. and Ramsdell, J. S. (2011) Analysis of interactions of brevetoxin-B and human serum albumin by liquid chromatography/mass spectrometry Chem. Res. Toxicol. 24, 54-64
34. Meng, X., Jenkins, R. E., Berry, N. G., Maggs, J. L., Farrell, J., Lane, C. S., Stachulski, A. V., French, N. S., Naisbitt, D. J., Pirmohamed, M., and Park, B. K. (2011) Direct evidence for the formation of diastereoisomeric benzylpenicilloyl haptens from benzylpenicillin and benzylpenicillenic acid in patients J. Pharmacol. Exp. Ther. 338, 841-849
35. Qiu, Y., Burlingame, A. L., and Benet, L. Z. (1998) Mechanisms for covalent binding of benoxaprofen glucuronide to human serum albumin. Studies by tandem mass spectrometry Drug Metab. Dispos. 26, 246-256
36. Sayre, L. M., Lin, D., Yuan, Q., Zhu, X., and Tang, X. (2006) Protein adducts generated from products of lipid oxidation: Focus on HNE and one Drug Metab. Rev. 38, 651-675
37. Almond, L. M., Boffito, M., Hoggard, P. G., Bonora, S., Raiteri, R., Reynolds, H. E., Garazzino, S., Sinicco, A., Khoo, S. H., Back, D. J., and Di Perri, G. (2004) The relationship between nevirapine plasma concentrations and abnormal liver function tests AIDS Res. Hum. Retroviruses 20, 716-722
38. Yuan, J., Guo, S., Hall, D., Cammett, A. M., Jayadev, S., Distel, M., Storfer, S., Huang, Z., Mootsikapun, P., Ruxrungtham, K., Podzamczer, D., and Haas, D. W. (2011) Toxicogenomics of nevirapine-associated cutaneous and hepatic adverse events among populations of African, Asian, and European descent AIDS 25, 1271-1280
39. Martin, A. M., Nolan, D., James, I., Cameron, P., Keller, J., Moore, C., Phillips, E., Christiansen, F. T., and Mallal, S. (2005) Predisposition to nevirapine hypersensitivity associated with HLA-DRB1*0101 and abrogated by low CD4 T-cell counts AIDS 19, 97-99