Procainamide, but not N-acetylprocainamide, induces protein free radical formation on myeloperoxidase: A potential mechanism of agranulocytosis

Chemical Research in Toxicology

Volumn 21, Issue 5, 2008, Pages 1143-1153

  Siraki, Arno G ^a   Deterding, Leesa J ^a   Bonini, Marcelo G ^a   Jiang, Jinjie ^a   Ehrenshaft, Marilyn ^a   Tomer, Kenneth B ^a   Mason, Ronald P ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5,5 DIMETHYL 1 PYRROLINE 1 OXIDE; ACECAINIDE; ANTIBODY; AROMATIC AMINE; ASCORBIC ACID; CATION; DRUG METABOLITE; ENZYME INHIBITOR; FREE RADICAL; HYDROGEN PEROXIDE; MYELOPEROXIDASE; NITROGEN; PROCAINAMIDE; RADICAL; ION; PEROXIDASE;

AGRANULOCYTOSIS; ARTICLE; CALCULATION; CELL LYSATE; CELL STRAIN HL 60; CONTROLLED STUDY; COVALENT BOND; DRUG METABOLISM; DRUG OXIDATION; ELECTRON SPIN RESONANCE; HUMAN; HUMAN CELL; HYPOTHESIS; IONIZATION; LEUKEMIA CELL; MASS SPECTROMETRY; PATHOPHYSIOLOGY; PROMYELOCYTIC LEUKEMIA; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DETERMINATION; SPIN TRAPPING; CHEMICAL STRUCTURE; CHEMISTRY; DRUG ANTAGONISM; ENZYME LINKED IMMUNOSORBENT ASSAY; GRANULOCYTE; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ACECAINIDE; ASCORBIC ACID; CELL LINE, TUMOR; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FREE RADICALS; GRANULOCYTES; HUMANS; HYDROGEN PEROXIDE; IONS; MASS SPECTROMETRY; MOLECULAR STRUCTURE; PEROXIDASE; PROCAINAMIDE;

EID: 47549089691     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx700415b     Document Type: Article

References (64)

1. Prystowsky, E. N., Benson, D. W., Jr., Fuster, V., Hart, R. G., Kay, G. N., Myerburg, R. J., Naccarelli, G. V., and Wyse, D. G. (1996) Management of patients with atrial fibrillation. A Statement for Healthcare Professionals. From the Subcommittee on Electrocardiography and Electrophysiology, American Heart Association. Circulation 93, 1262-1277.
2. Ip, J., and Uetrecht, J. P. (2006) In vitro and animal models of drug-induced blood dyscrasias. Environ. Toxicol. Pharmacol. 21, 135-140.
3. Wintrobe, M. M., and Greer J. (2003) Wintrobe's Clinical Hematology (Greer, J. P., Foerster, J., Lukens, J. N., Rodgers, G. M., Paraskevas, F., and Glader, B., Eds.),Lippincott Williams & Wilkins, Philadelphia.
4. Freed, J. S., and Reiner, M. A. (1988) Septic complications of procainamide-induced agranulocytosis: Report of two cases. Mt. Sinai J. Med. 55, 194-197.
5. Dorr, V. J., and Cook, J. (1996) Agranulocytosis and near fatal sepsis due to 'Mexican aspirin' (dipyrone). South. Med. J. 89, 612-614.
6. Young, J. A., Newcomer, L. N., and Keller, A. M. (1984) Amino-glutethimide-induced bone marrow injury. Report of a case and review of the literature. Cancer 54, 1731-1733.
7. van der Klauw, M. M., Wilson, J. H. P., and Stricker, B. H. C. (1998) Drug-associated agranulocytosis: 20 years of reporting in The Netherlands (1974-1994). Am. J. Hematol. 57, 206-211.
8. Ellrodt, A. G., Murata, G. H., Riedinger, M. S., Stewart, M. E., Mochizuki, C., and Gray, R. (1984) Severe neutropenia associated with sustained-release procainamide. Ann. Intern. Med. 100, 197-201.
9. Kaufman, D. W., Kelly, J. P., Jurgelon, J. M., Anderson, T., Issaragrisil, S., Wiholm, B. E., Young, N. S., Leaverton, P., Levy, M., and Shapiro, S. (1996) Drugs in the aetiology of agranulocytosis and aplastic anaemia. Eur. J. Haematol. Suppl. 57, 23-30.
10. Saito, Y. (2003) Acquired Agranulocytosis, In NORD Guide to Rare Disorders pp 361-362, Lippincott Williams & Wilkins, Philadelphia.
11. Uetrecht, J. P. (1992) The role of leukocyte-generated reactive metabolites in the pathogenesis of idiosyncratic drug reactions. Drug. Metab. Rev. 24, 299-366.
12. Gill, H. J., Hough, S. J., Naisbitt, D. J., Maggs, J. L., Kitteringham, N. R., Pirmohamed, M., and Park, B. K. (1997) The relationship between the disposition and immunogenicity of sulfamethoxazole in the rat. J. Pharmacol. Exp. Ther. 282, 795-801.
13. Brown, K. E., Brunt, E. M., and Heinecke, J. W. (2001) Immunohistochemical detection of myeloperoxidase and its oxidation products in Kupffer cells of human liver. Am. J. Pathol. 159, 2081-2088.
14. Dunford, H. B. (1999) Heme peroxidases, John Wiley, New York.
15. O'Brien, P. J. (2000) Peroxidases. Chem. Biol. Interact. 129, 113-139.
16. Nauseef, W. M. (1986) Myeloperoxidase biosynthesis by a human promyelocytic leukemia cell line: insight into myeloperoxidase deficiency. Blood 67, 865-872.
17. Andrews, P. C., and Krinsky, N. I. (1981) The reductive cleavage of myeloperoxidase in half, producing enzymically active hemi-myeloperoxidase. J. Biol. Chem. 256, 4211-4218.
18. Hansson, M., Olsson, I., and Nauseef, W. M. (2006) Biosynthesis, processing, and sorting of human myeloperoxidase. Arch. Biochem. Biophys. 445, 214-224.
19. Kettle, A. J., and Winterbourn, C. C. (1991) Mechanism of inhibition of myeloperoxidase by anti-inflammatory drugs. Biochem. Pharmacol. 41, 1485-1492.
20. Galati, G., Tafazoli, S., Sabzevari, O., Chan, T. S., and O'Brien, P. J. (2002) Idiosyncratic NSAID drug induced oxidative stress. Chem. Biol. Interact. 142, 25-41.
21. Siraki, A. G., Bonini, M. G., Jiang, J., Ehrenshaft, M., and Mason, R. P. (2007) Aminoglutethimide-induced protein free radical formation on myeloperoxidase: A potential mechanism of agranulocytosis. Chem. Res. Toxicol. 20, 1038-1045.
22. Dolman, K. M., Gans, R. O. B., Vervaat, T. J., Zevenbergen, G., Maingay, D., Nikkels, R. E., Donker, A. J. M., von dem Borne, A. E. G. K., and Goldschmeding, R. (1993) Vasculitis and antineutrophil cytoplasmic autoantibodies associated with propylthiouracil therapy. Lancet 342, 651-652.
23. Waldhauser, L., and Uetrecht, J. (1996) Antibodies to myeloperoxidase in propylthiouracil-induced autoimmune disease in the cat. Toxicology 114, 155-162.
24. Hsuanyu, Y., and Dunford, H. B. (1999) Oxidation of clozapine and ascorbate by myeloperoxidase. Arch. Biochem. Biophys. 368, 413-420.
25. Beers, R. F., Jr., and Sizer, I. W. (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem. 195, 133-140.
26. Bonini, M. G., Siraki, A. G., Bhattacharjee, S., and Mason, R. P. (2007) Glutathione-induced radical formation on lactoperoxidase does not correlate with the enzyme's peroxidase activity. Free Radic. Biol. Med. 42, 985-992.
27. Lagercrantz, C. (1971) Spin trapping of some short-lived radicals by the nitroxide method. J. Phys. Chem. 75, 3466-3475.
28. Ramirez, D. C., Gomez Mejiba, S. E., and Mason, R. P. (2005) Mechanism of hydrogen peroxide-induced Cu,Zn-superoxide dismutase-centered radical formation as explored by immuno-spin trapping: The role of copper- and carbonate radical anion-mediated oxidations. Free Radic. Biol. Med. 38, 201-214.
29. Hope, H. R., Remsen, E. E., Lewis, C., Jr., Heuvelman, D. M., Walker, M. C., Jennings, M., and Connolly, D. T. (2000) Large-scale purification of myeloperoxidase from HL60 promyelocytic cells: Characterization and comparison to human neutrophil myeloperoxidase. Protein Expression Purif. 18, 269-276.
30. Detweiler, C. D., Deterding, L. J., Tomer, K. B., Chignell, C. F., Germolec, D., and Mason, R. P. (2002) Immunological identification of the heart myoglobin radical formed by hydrogen peroxide. Free Radic. Biol. Med. 33, 364-349.
31. Marquez, L. A., Huang, J. T., and Dunford, H. B. (1994) Spectral and kinetic studies on the formation of myeloperoxidase compounds I and II: Roles of hydrogen peroxide and superoxide. Biochemistry 33, 1447-1454.
32. Motten, A. G., and Chignell, C. F. (1983) Spectroscopic studies of cutaneous photosensitizing agents - III. Spin trapping of photolysis products from sulfanilamide analogs. Photochem. Photobiol. 37, 17-26.
33. Chignell, C. F., Kalyanaraman, B., Mason, R. P., and Sik, R. H. (1980) Spectroscopic studies of cutaneous photosensitizing agents-I. Spin trapping of photolysis products from sulfanilamide, 4-aminobenzoic acid and related compounds. Photochem. Photobiol. 32, 563-571.
34. Gasanov, R. G., and Freidlina, R. K. (1981) ESR study of the interaction of mononuclear and binuclear metal carbonyls with silicon hydrides and the use of these systems to generate α-chlorine-containing radicals. Russ. Chem. Bull. 30, 980-984.
35. Torssell, K. (1970) Investigation of radical intermediates in organic reactions by use of nitroso compounds as scavengers: The nitroxide method. Tetrahedron 26, 2759-2773.
36. Kadiiska, M. B., De Costa, K. S., Mason, R. P., and Mathews, J. M. (2000) Reduction of 1,3-diphenyl-1-triazene by rat hepatic microsomes, by cecal microflora, and in rats generates the phenyl radical metabolite: An ESR spin-trapping investigation. Chem. Res. Toxicol. 13, 1082-1086.
37. Sinha, B. K. (1983) Enzymatic activation of hydrazine derivatives. A spin-trapping study. J. Biol. Chem. 258, 796-801.
38. Guaiquil, V. H., Farber, C. M., Golde, D. W., and Vera, J. C. (1997) Efficient transport and accumulation of vitamin C in HL-60 cells depleted of glutathione. J. Biol. Chem. 272, 9915-9921.
39. Davies, M. J., and Hawkins, C. L. (2004) EPR spin trapping of protein radicals. Free Radic. Biol. Med. 36, 1072-1086.
40. Uetrecht, J., Zahid, N., and Rubin, R. (1988) Metabolism of procainamide to a hydroxylamine by human neutrophils and mononuclear leukocytes. Chem. Res. Toxicol. 1, 74-78.
41. Uetrecht, J. P., and Zahid, N. (1991) N-Chlorination and oxidation of procainamide by myeloperoxidase: Toxicological implications. Chem. Res. Toxicol. 4, 218-222.
42. 2. J. Phys. Chem. 90, 1193-1198.
43. Ator, M. A., David, S. K., and Ortiz de Montellano, P. R. (1989) Stabilized isoporphyrin intermediates in the inactivation of horseradish peroxidase by alkylhydrazines. J. Biol. Chem. 264, 9250-9257.
44. Huang, L., Colas, C., and Ortiz de Montellano, P. R. (2004) Oxidation of carboxylic acids by horseradish peroxidase results in prosthetic heme modification and inactivation. J. Am. Chem. Soc. 126, 12865-12873.
45. Kettle, A. J., Gedye, C. A., and Winterbourn, C. C. (1997) Mechanism of inactivation of myeloperoxidase by 4-aminobenzoic acid hydrazide. Biochem. J. 321, 503-508.
46. Ortiz de Montellano, P. R., David, S. K., Ator, M. A., and Tew, D. (1988) Mechanism-based inactivation of horseradish peroxidase by sodium azide. Formation of meso-azidoprotoporphyrin IX. Biochemistry 27, 5470-5476.
47. Siraki, A. G., and O'Brien, P. J. (2002) Prooxidant activity of free radicals derived from phenol-containing neurotransmitters. Toxicology 177, 81-90.
48. Rubin, R. L., and Curnutte, J. T. (1989) Metabolism of procainamide to the cytotoxic hydroxylamine by neutrophils activated in vitro. J. Clin. Invest. 83, 1336-1343.
49. Josephy, P. D., Eling, T. E., and Mason, R. P. (1983) An electron spin resonance study of the activation of benzidine by peroxidases. Mol. Pharmacol. 23, 766-770.
50. Zhan, C.-G., Nichols, J. A., and Dixon, D. A. (2003) Ionization potential, electron affinity, electronegativity, hardness, and electron excitation energy: Molecular properties from density functional theory orbital energies. J. Phys. Chem. A 107, 4184-4195.
51. Parker, V. D. (1976) Energetics of electrode reactions II. The relationship between redox potentials, ionization potentials, electron affinities, and solvation energies of aromatic hydrocarbons. J. Am. Chem. Soc. 98, 98-103.
52. Cavalieri, E. L., Rogan, E. G., Roth, R. W., Saugier, R. K., and Hakam, A. (1983) The relationship between ionization potential and horseradish peroxidase/hydrogen peroxide-catalyzed binding of aromatic hydrocarbons to DNA. Chem. Biol. Interact. 47, 87-109.
53. Halliwell, B. (1996) Antioxidants in human health and disease. Annu. Rev. Nutr. 16, 33-50.
54. Halliwell, B. (2007) Dietary polyphenols: Good, bad, or indifferent for your health? Cardiovasc. Res. 73, 341-347.
55. Reidenberg, M. M. (1983) Aromatic amines and the pathogenesis of lupus erythematosus. Am. J. Med. 75, 1037-1042.
56. Perry, H. M., Jr. (1973) Late toxicity to hydralazine resembling systemic lupus erythematosus or rheumatoid arthritis. Am. J. Med. 54, 58-72.
57. Starkebaum, G., Kenyon, C. M., Simrell, C. R., Creamer, J. I., and Rubin, R. L. (1996) Procainamide-induced agranulocytosis differs serologically and clinically from procainamide-induced lupus. Clin. Immunol. Immunopathol. 78, 112-119.
58. Swain, S. D., Rohn, T. T., and Quinn, M. T. (2002) Neutrophil priming in host defense: role of oxidants as priming agents. Antioxid. Redox. Signal. 4, 69-83.
59. Arnljots, K., and Olsson, I. (1987) Myeloperoxidase precursors incorporate heme. J. Biol. Chem. 262, 10430-10433.
60. Koeffler, H. P., Ranyard, J., and Pertcheck, M. (1985) Myeloperoxidase: Its structure and expression during myeloid differentiation. Blood 65, 484-491.
61. Azocar, J. (1984) Anti-myeloid-cell antibody in procainamide-induced agranulocytosis. Lancet 1, 1069-1070.
62. Baker, E. J., Gerard, D. A., Bamberger, E. G., Lozzio, C. B., and Ichiki, A. T. (2002) HL-60 cell growth-conditioned medium is an effective inducer of myeloperoxidase expression in K-562 human leukemia cells. Leuk. Res. 26, 1017-1025.
63. Gardner, I., Popovic, M., Zahid, N., and Uetrecht, J. P. (2005) A comparison of the covalent binding of clozapine, procainamide, and vesnarinone to human neutrophils in vitro and rat tissues in vitro and in vivo. Chem. Res. Toxicol. 18, 1384-1394.
64. Lavergne, S. N., Drescher, N. J., and Trepanier, L. A. (2008) Anti-myeloperoxidase and anti-cathepsin G antibodies in sulphonamide hypersensitivity. Clin. Exp. Allergy 38, 199-207.