Characterization of the formation and localization of sulfamethoxazole and dapsone-associated drug-protein adducts in human epidermal keratinocytes

Journal of Pharmacology and Experimental Therapeutics

Volumn 314, Issue 1, 2005, Pages 43-52

  Roychowdhury, Sanjoy ^a   Vyas, Piyush M ^a   Reilly, Timothy P ^b   Gaspari, Anthony A ^c   Svensson, Craig K ^a  

^a UNIVERSITY OF IOWA   (United States)

^b BRISTOL MYERS SQUIBB COMPANY   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ANTIGEN; ASCORBIC ACID; DAPSONE; DRUG METABOLITE; HAPTEN; N HYDROXYDAPSONE; RABBIT ANTISERUM; SULFAMETHOXAZOLE;

ANTIGEN PRESENTING CELL; ARTICLE; BIOLOGICAL ACTIVITY; CELL DEATH; CELL LINE; CELL MEMBRANE PERMEABILITY; CELL SURFACE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DRUG DISTRIBUTION; DRUG EXPOSURE; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIDERMIS; EPIDERMIS CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; KERATINOCYTE; LABORATORY; PRIORITY JOURNAL; PROTEIN TARGETING;

ACETYLCYSTEINE; ANTI-INFECTIVE AGENTS; ANTIOXIDANTS; ASCORBIC ACID; CELL LINE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DAPSONE; ENZYME ACTIVATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPIDERMIS; FOLIC ACID ANTAGONISTS; HAPTENS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; KERATINOCYTES; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; PROTEIN BINDING; PROTEINS; SULFAMETHOXAZOLE;

EID: 23044473576     PISSN: 00223565     EISSN: None     Source Type: Journal    
DOI: 10.1124/jpet.105.086009     Document Type: Article

References (40)

1. Albanesi C, Cavani A, and Girolomoni G (1998) Interferon-gamma-stimulated human keratinocytes express the genes necessary for the production of peptideloaded MHC class II molecules. J Investig Dermatol 110:138-142.
2. Bour H, Peyron E, Gaucherand M, Garrigue JL, Desvignes C, Kaiserlian D, Revillard JP, and Nicolas JF (1995) Major histocompatibility complex class I-restricted CD8+ T cells and class II-restricted CD4+ T cells, respectively, mediate and regulate contact sensitivity to dinitrofluorobenzene. Eur J Immunol 25:3006-3010.
3. Cribb AE, Lee BL, Trepanier LA, and Spielberg SP (1996a) Adverse reactions to sulphonamide and sulphonamide-trimethoprim antimicrobials: clinical syndromes and pathogenesis. Adverse Drug React Toxicol Rev 15:9-50.
4. Cribb AE, Miller M, Leeder JS, Hill J, and Spielberg SP (1991) Reactions of the nitroso and hydroxylamine metabolites of sulfamethoxazole with reduced glutathione. Implications for idiosyncratic toxicity. Drug Metab Dispos 19:900-906.
5. Cribb AE, Nuss CE, Alberts DW, Lamphere DB, Grant DM, Grossman SJ, and Spielberg SP (1996b) Covalent binding of sulfamethoxazole reactive metabolites to human and rat liver subcellular fractions assessed by immunochemical detection. Chem Res Toxicol 9:500-507.
6. Farrell J, Naisbitt DJ, Drummond NS, Depta JP, Vilar FJ, Pirmohamed M, and Park BK (2003) Characterization of sulfamethoxazole and sulfamethoxazole metabolitespecific T-cell responses in animals and humans. J Pharmacol Exp Ther 306:229-237.
7. Gruchalla RS, Pesenko RD, Do TT, and Skiest DJ (1998) Sulfonamide-induced reactions in desensitized patients with AIDS-the role of covalent protein haptenation by sulfamethoxazole. J Allergy Clin Immunol 101:371-378.
8. Hertl M, Jugert F, and Merk HF (1995) CD8+ dermal T cells from a sulphamethoxazole-induced bullous exanthem proliferate in response to drug-modified liver microsomes. Br J Dermatol 132:215-220.
9. Kehren J, Desvignes C, Krasteva M, Ducluzeau MT, Assossou O, Horand F, Hahne M, Kagi D, Kaiserlian D, and Nicolas JF (1999) Cytotoxicity is mandatory for CD8(+) T cell-mediated contact hypersensitivity. J Exp Med 189:779-786.
10. Manchanda T, Hess D, Dale L, Ferguson SG, and Rieder MJ (2002) Haptenation of sulfonamide reactive metabolites to cellular proteins. Mol Pharmacol 62:1011-1026.
11. Mauri-Hellweg D, Bettens F, Mauri D, Brander C, Hunziker T, and Pichler WJ (1995) Activation of drug-specific CD4+ and CD8+ T cells in individuals allergic to sulfonamides, phenytoin and carbamazepine. J Immunol 155:462-472.
12. Medina I, Mills J, Leoung G, Hopewell PC, Lee B, Modin G, Benowitz N, and Wofsy CB (1990) Oral therapy for Pneumocystis carinii pneumonia in the acquired immunodeficiency syndrome: a controlled trial of trimethoprim-sulfamethoxazole versus trimethoprim-dapsone. N Engl J Med 323:776-782.
13. Naisbitt DJ, Farrell J, Gordon SF, Maggs JL, Burkhart C, Pichler WJ, Pirmohamed M, and Park BK (2002) Covalent binding of the nitroso metabolite of sulfamethoxazole leads to toxicity and major histocompatibility complex-restricted antigen presentation. Mol Pharmacol 62:628-637.
14. Naisbitt DJ, Gordon SF, Pirmohamed M, Burkhart C, Cribb AE, Pichler WJ, and Park BK (2001a) Antigenicity and immunogenicity of sulphamethoxazole: demonstration of metabolism-dependent haptenation and T-cell proliferation in vivo. Br J Pharmacol 133:295-305.
15. Naisbitt DJ, Hough SJ, Gill HJ, Pirmohamed M, Kitteringham NR, and Park BK (1999) Cellular disposition of sulphamethoxazole and its metabolites: implications for hypersensitivity. Br J Pharmacol 126:1393-1407.
16. Naisbitt DJ, Pirmohamed M, and Park BK (2003) Immunopharmacology of hypersensitivity reactions to drugs. Curr Allergy Asthma Rep 3:22-29.
17. Naisbitt DJ, Williams DP, Pirmohamed M, Kitteringham NR, and Park BK (2001b) Reactive metabolites and their role in drug reactions. Curr Opin Allergy Clin Immunol 1:317-325.
18. Nakamura H, Uetrecht J, Cribb AE, Miller MA, Zahid N, Hill J, Josephy PD, Grant DM, and Spielberg SP (1995) In vitro formation, disposition and toxicity of Nacetoxy-sulfamethoxazole, a potential mediator of sulfamethoxazole toxicity. J Pharmacol Exp Ther 274:1099-1104.
19. Park BK and Kitteringham NR (1990) Drug-protein conjugation and its immunological consequences. Drug Metab Rev 22:87-144.
20. Park BK, Pirmohamed M, and Kitteringham NR (1998) Role of drug disposition in drug hypersensitivity: a chemical, molecular and clinical perspective. Chem Res Toxicol 11:969-988.
21. Pertel P and Hirschtick R (1994) Adverse reactions to dapsone in persons infected with human immunodeficiency virus. Clin Infect Dis 18:630-632.
22. Pichler W, Yawalkar N, Schmid S, and Helbling A (2002a) Pathogenesis of druginduced exanthems. Allergy 57:884-893.
23. Pichler WJ, Yawalkar N, Britschgi M, Depta J, Strasser I, Schmid S, Kuechler P, and Naisbitt D (2002b) Cellular and molecular pathophysiology of cutaneous drug reactions. Am J Clin Dermatol 3:229-238.
24. Pohl LR, Satoh H, Christ DD, and Kenna JG (1988) The immunologic and metabolic basis of drug hypersensitivities. Annu Rev Pharmacol Toxicol 28:367-387.
25. Reilly TP, Bellevue FH 3rd, Woster PM, and Svensson CK (1998) Comparison of the in vitro cytotoxicity of hydroxylamine metabolites of sulfamethoxazole and dapsone. Biochem Pharmacol 55:803-810.
26. Reilly TP, Lash LH, Doll MA, Hein DW, Woster PM, and Svensson CK (2000) A role for bioactivation and covalent binding within epidermal keratinocytes in sulfonamide-induced cutaneous drug reactions. J Investig Dermatol 114:1164-1173.
27. Reilly TP, Woster PM, and Svensson CK (1999) Methemoglobin formation by hydroxylamine metabolites of sulfamethoxazole and dapsone: implications for differences in adverse drug reactions. J Pharmacol Exp Ther 288:951-959.
28. Rieder MJ, Uetrecht J, Shear NH, and Spielberg SP (1988) Synthesis and in vitro toxicity of hydroxylamine metabolites of sulfonamides. J Pharmacol Exp Ther 244:724-728.
29. Schnyder B, Mauri-Hellweg D, Zanni M, Bettens F, and Pichler WJ (1997) Direct, MHC-dependent presentation of the drug sulfamethoxazole to human αβ T cell clones. J Clin Investig 100:136-141.
30. Shear NH, Spielberg SP, Grant DM, Tang BK, and Kalow W (1986) Differences in metabolism of sulfonamides predisposing to idiosyncratic toxicity. Ann Intern Med 105:179-184.
31. Svensson CK (2003) Do arylhydroxylamine metabolites mediate idiosyncratic reactions associated with sulfonamides? Chem Res Toxicol 16:1035-1043.
32. Svensson CK, Cowen EW, and Gaspari AA (2001) Cutaneous drug reactions. Pharmacol Rev 53:357-379.
33. Trepanier LA, Yoder AR, Bajad S, Beckwith MD, Bellehumeur JL, and Graziano FM (2004) Plasma ascorbate deficiency is associated with impaired reduction of sulfamethoxazole-nitroso in HIV infection. J Acquir Immune Defic Syndr 36:1041-1050.
34. Uetrecht JP (1999) New concepts in immunology relevant to idiosyncratic drug reactions: the "danger hypothesis" and innate immune system. Chem Res Toxicol 12:387-395.
35. Uetrecht JP, Shear NH, and Zahid N (1993) N-chlorination of sulfamethoxazole and dapsone by the myeloperoxidase system. Drug Metab Dispos 21:830-834.
36. Vage C, Saab N, Woster PM, and Svensson CK (1994) Dapsone-induced hematologic toxicity: comparison of the methemoglobin-forming ability of hydroxylamine metabolites of dapsone in rat and human blood. Toxicol Appl Pharmacol 129:309-316.
37. Vage C and Svensson CK (1994) Evidence that the biotransformation of dapsone and monoacetyldapsone to their respective hydroxylamine metabolites in rat liver microsomes is mediated by cytochrome P450 2C6/2C11 and 3A1. Drug Metab Dispos 22:572-577.
38. Wakita H, Nishimura K, Tokura Y, Furukawa F, and Takigawa M (1996) Inhibitors of sphingolipid synthesis modulate interferon (IFN)-γ-induced intercellular adhesion molecule (ICAM)-1 and human leukocyte antigen (HLA)-DR expression on cultured normal human keratinocytes: possible involvement of ceramide in biologic action of IFN-γ. J Investig Dermatol 107:336-342.
39. Warrington RJ, Sauder PJ, and McPhillips S (1983) Lymphocyte transformation studies in suspected hypersensitivity to trimethoprim- sulphamethoxazole. Clin Allergy 13:235-240.
40. Wikner NE, Huff JC, Norris DA, Boyce ST, Cary M, Kissinger M, and Weston WL (1986) Study of HLA-DR synthesis in cultured human keratinocytes. J Investig Dermatol 87:559-564.