Advances in the electrochemical simulation of oxidation reactions mediated by cytochrome P450

Chemical Research in Toxicology

Volumn 27, Issue 10, 2014, Pages 1652-1668

  Bussy, Ugo ^a   Boujtita, Mohammed ^b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITÉ DE NANTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

7 ETHOXYCOUMARIN; ACEBUTOLOL; ALPRENOLOL; AMODIAQUINE; ATORVASTATIN; BENZOQUINONE DERIVATIVE; BENZO[A]PYRENE; CARBON; CLOZAPINE; CRESOL; CYTOCHROME P450; FERROUS GLUCONATE; HALOPERIDOL; HYDROGEN; IRON; LAURIC ACID; MEPHENYTOIN; MEVINOLIN; MITOXANTRONE; NITROGEN; PARACETAMOL; PHENACETIN; REACTIVE OXYGEN METABOLITE; SIMVASTATIN; SKATOLE; TETRAZEPAM; TOREMIFENE; TRIMETHOPRIM; TROGLITAZONE; VERAPAMIL; DRUG;

CHEMICAL STRUCTURE; COVALENT BOND; DEALKYLATION; DRUG METABOLISM; ELECTROCHEMISTRY; ELECTRON TRANSPORT; EPOXIDATION; HYDROXYLATION; OXIDATION; REVIEW; ALKYLATION; ANIMAL; BIOCATALYSIS; CHEMISTRY; ELECTROCHEMICAL ANALYSIS; HUMAN; MASS SPECTROMETRY; METABOLISM; OXIDATION REDUCTION REACTION;

ALKYLATION; ANIMALS; BIOCATALYSIS; CYTOCHROME P-450 ENZYME SYSTEM; ELECTROCHEMICAL TECHNIQUES; ELECTRON TRANSPORT; HUMANS; HYDROGEN; HYDROXYLATION; MASS SPECTROMETRY; OXIDATION-REDUCTION; PHARMACEUTICAL PREPARATIONS;

EID: 84908075090     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx5001943     Document Type: Review

References (109)

1. Wienkers, L. C., and Heath, T. G. (2005) Predicting in vivo drug interactions from in vitro drug discovery data. Nat. Rev. Drug Discovery 4, 825-833.
2. Rydberg, P., Gloriam, D. E., Zaretzki, J., Breneman, C., and Olsen, L. (2010) SMARTCyp: a 2D method for prediction of cytochrome P450-mediated drug metabolism. ACS Med. Chem. Lett. 1, 96-100.
3. Gunter, M. J., and Turner, P. (1991) Metalloporphyrins as models for the cytochromes P-450. Coord. Chem. Rev. 108, 115-161.
4. Chorghade, M. S., Hill, D. R., Lee, E. C., Pariza, R. J., Dolphin, D. H., Hino, F., and Zhang, L.-Y. (1996) Metalloporphyrins as chemical mimics of cytochrome P-450 systems. Pure Appl. Chem. 68, 753-756.
5. Nouri-Nigjeh, E., Bischoff, R., Bruins, A. P., and Permentier, H. P. (2011) Electrochemistry in the mimicry of oxidative drug metabolism by cytochrome P450s. Curr. Drug Metab. 12, 359-371.
6. Faber, H., Jahn, S., Kunnemeyer, J., Simon, H., Melles, D., Vogel, M., and Karst, U. (2011) Electrochemistry/liquid chromatography/mass spectrometry as a tool in metabolism studies. Angew. Chem. 50, A52-58.
7. Jurva, U., Wikstrom, H. V., Weidolf, L., and Bruins, A. P. (2003) Comparison between electrochemistry/mass spectrometry and cytochrome P450 catalyzed oxidation reactions. Rapid Commun. Mass Spectrom. 17, 800-810.
8. Shono, T., Toda, T., and Oshino, N. (1981) Preparation of N-dealkylated drug metabolites by electrochemical simulation of biotransformation. Drug Metab. Dispos. 9, 481-482.
9. Shono, T., Toda, T., and Oshino, N. (1982) Electron transfer from nitrogen in microsomal oxidation of amine and amide. Simulation of microsomal oxidation by anodic oxidation. J. Am. Chem. Soc. 104, 2639-2641.
10. Getek, T. A., Korfmacher, W. A., McRae, T. A., and Hinson, J. A. (1989) Utility of solution electrochemistry mass spectrometry for investigation the formation and detection of biologically important conjugates of acetaminophen. J. Chromatogr. A 474, 245-256.
11. Jurva, U., Wikstrom, H. V., and Bruins, A. P. (2000) In vitro mimicry of metabolic oxidation reactions by electrochemistry/mass spectrometry. Rapid Commun. Mass Spectrom. 14, 529-533.
12. Jurva, U., Wikstrom, H. V., and Bruins, A. P. (2002) Electrochemically assisted Fenton reaction: reaction of hydroxyl radicals with xenobiotics followed by on-line analysis with high-performance liquid chromatography/tandem mass spectrometry. Rapid Commun. Mass Spectrom. 16, 1934-1940.
13. Madsen, K. G., Olsen, J., Skonberg, C., Hansen, S. H., and Jurva, U. (2007) Development and evaluation of an electrochemical method for studying reactive phase-I metabolites: correlation to in vitro drug metabolism. Chem. Res. Toxicol. 20, 821-831.
14. Madsen, K. G., Gronberg, G., Skonberg, C., Jurva, U., Hansen, S. H., and Olsen, J. (2008) Electrochemical oxidation of troglitazone: identification and characterization of the major reactive metabolite in liver microsomes. Chem. Res. Toxicol. 21, 2035-2041.
15. Lohmann, W., and Karst, U. (2006) Simulation of the detoxification of paracetamol using on-line electrochemistry/liquid chromatography/mass spectrometry. Anal. Bioanal. Chem. 386, 1701-1708.
16. Madsen, K. G., Skonberg, C., Jurva, U., Cornett, C., Hansen, S. H., Johansen, T. N., and Olsen, J. (2008) Bioactivation of diclofenac in vitro and in vivo: correlation to electrochemical studies. Chem. Res. Toxicol. 21, 1107-1119.
17. Nouri-Nigjeh, E., Bruins, A. P., Bischoff, R., and Permentier, H. P. (2012) Electrocatalytic oxidation of hydrogen peroxide on a platinum electrode in the imitation of oxidative drug metabolism of lidocaine. Analyst 137, 4698-4702.
18. Permentier, H. P., Bruins, A. P., and Bischoff, R. (2008) Electrochemistry-mass spectrometry in drug metabolism and protein research. Mini-Rev. Med. Chem. 8, 46-56.
19. Jahn, S., and Karst, U. (2012) Electrochemistry coupled to (liquid chromatography/) mass spectrometry - current state and future perspectives. J. Chromatogr. A 1259, 16-49.
20. Guengerich, F. P. (2001) Common and uncommon cytochrome P450 reactions related to metabolism and chemical toxicity. Chem. Res. Toxicol. 14, 611-650.
21. Isin, E. M., and Guengerich, F. P. (2007) Complex reactions catalyzed by cytochrome P450 enzymes. Biochim. Biophys. Acta 1770, 314-329.
22. Meunier, B., de Visser, S. P., and Shaik, S. (2004) Mechanism of oxidation reactions catalyzed by cytochrome P450 enzymes. Chem. Rev. 104, 3947-3980.
23. (2005) Cytochrome P450: Structure, Mechanism, and Biochemistry (Ortiz de Montellano, P. R., Ed.) 3rd ed., Kluwer Academic/Plenum Publishers, New York.
24. (2001) Organic Electrochemistry (Hammerich, O., and Lund, H., Eds.) 4th ed., Marcel Dekker, New York.
25. Fry, A. J. (1989) Synthetic Organic Electrochemistry, 2nd ed., John Wiley & Son, Inc., New York.
26. Li, A. P. (2001) Screening for human ADME/Tox drug properties in drug discovery. Drug Discovery Today 6, 357-366.
27. Zhou, S., Chan, E., Duan, W., Huang, M., and Chen, Y. Z. (2005) Drug bioactivation, covalent binding to target proteins and toxicity relevance. Drug Metab. Rev. 37, 41-213.
28. Guengerich, F. P., and Johnson, W. W. (1997) Kinetics of ferric cytochrome P450 reduction by NADPH-cytochrome P450 reductase: rapid reduction in the absence of substrate and variations among cytochrome P450 systems. Biochemistry 36, 14741-14750.
29. Guengerich, F. P., Ballou, D. P., and Coon, M. J. (1976) Spectral intermediates in the reaction of oxygen with purified liver microsomal cytochrome P-450. Biochem. Biophys. Res. Commun. 70, 951-956.
30. Davydov, R., Makris, T. M., Kofman, V., Werst, D. E., Sligar, S. G., and Hoffman, B. M. (2001) Hydroxylation of camphor by reduced oxy-cytochrome P450cam: mechanistic implications of EPR and ENDOR studies of catalytic intermediates in native and mutant enzymes. J. Am. Chem. Soc. 123, 1403-1415.
31. Brandon, E. F., Raap, C. D., Meijerman, I., Beijnen, J. H., and Schellens, J. H. (2003) An update on in vitro test methods in human hepatic drug biotransformation research: pros and cons. Toxicol. Appl. Pharmacol. 189, 233-246.
32. Bussy, U., Delaforge, M., El-Bekkali, C., Ferchaud-Roucher, V., Krempf, M., Tea, I., Galland, N., Jacquemin, D., and Boujtita, M. (2013) Acebutolol and alprenolol metabolism predictions: comparative study of electrochemical and cytochrome P450-catalyzed reactions using liquid chromatography coupled to high-resolution mass spectrometry. Anal. Bioanal. Chem. 405, 6077-6085.
33. Simon, H., Wehe, C. A., Pajaziti, B., Heinrich, L., and Karst, U. (2013) Simultaneous electrochemical oxidation/ionization of a selenoxanthene revealed by on-line electrospray-high resolution mass spectrometry. Electrochim. Acta 111, 324-331.
34. Lohmann, W., and Karst, U. (2008) Biomimetic modeling of oxidative drug metabolism: strategies, advantages and limitations. Anal. Bioanal. Chem. 391, 79-96.
35. Odijk, M., Baumann, A., Lohmann, W., van den Brink, F. T. G., lthuis, W., Karst, U., and van den Berg, A. (2009) A microfluidic chip for electrochemical conversions in drug metabolism studies. Lab Chip 9, 1687-1693.
36. Odijk, M., Baumann, A., Olthuis, W., van den Berg, A., and Karst, U. (2010) Electrochemistry-on-chip for on-line conversions in drug metabolism studies. Biosens. Bioelectron. 26, 1521-1527.
37. Odijk, M., Olthuis, W., van den Berg, A., Qiao, L., and Girault, H. (2012) Improved conversion rates in drug screening applications using miniaturized electrochemical cells with frit channels. Anal. Chem. 84, 9176-9183.
38. Kertesz, V., and Van Berkel, G. J. (2007) Using the electrochemistry of the electrospray ion source. Anal. Chem. 79, 5510-5520.
39. Karst, U. (2004) Analytical methods: electrochemistry/mass spectrometry (EC/MS) - a new tool to study drug metabolism and reaction mechanisms. Angew. Chem. 43, 2476-2478.
40. Simon, H., Melles, D., Jacquoilleot, S., Sanderson, P., Zazzeroni, R., and Karst, U. (2012) Combination of electrochemistry and nuclear magnetic resonance spectroscopy for metabolism studies. Anal. Chem. 84, 8777-8782.
41. Bussy, U., Giraudeau, P., Silvestre, V., Jaunet-Lahary, T., Ferchaud-Roucher, V., Krempf, M., Akoka, S., Tea, I., and Boujtita, M. (2013) In situ NMR spectroelectrochemistry for the structure elucidation of unstable intermediate metabolites. Anal. Bioanal. Chem. 405, 5817-5824.
42. Baumann, A., Lohmann, W., Schubert, B., Oberacher, H., and Karst, U. (2009) Metabolic studies of tetrazepam based on electrochemical simulation in comparison to in vivo and in vitro methods. J. Chromatogr. A 1216, 3192-3198.
43. Baumann, A., Lohmann, W., Jahn, S., and Karst, U. (2009) Online electrochemistry/electrospray ionization mass spectrometry (EC/ESI-MS) for the generation and identification of nucleotide oxidation products. Electroanalysis 22, 286-292.
44. Bokman, C. F., Zettersten, C., Sjoberg, P. J., and Nyholm, L. (2004) A setup for the coupling of a thin-layer electrochemical flow cell to electrospray mass spectrometry. Anal. Chem. 76, 2017-2024.
45. Bussy, U., Ferchaud-Roucher, V., Tea, I., Krempf, M., Silvestre, V., and Boujtita, M. (2012) Electrochemical oxidation behavior of acebutolol and identification of intermediate species by liquid chromatography and mass spectrometry. Electrochim. Acta 69, 351-357.
46. Liljegren, G., Dahlin, A., Zettersten, C., Bergquist, J., and Nyholm, L. (2005) On-line coupling of a microelectrode array equipped poly(dimethylsiloxane) microchip with an integrated graphite electrospray emitter for electrospray ionisation mass spectrometry. Lab Chip 5, 1008-1016.
47. Nyholm, L. (2005) Electrochemical techniques for lab-on-a-chip applications. Analyst 130, 599-605.
48. Baumann, A., Faust, A., Law, M. P., Kuhlmann, M. T., Kopka, K., Schafers, M., and Karst, U. (2011) Metabolite identification of a radiotracer by electrochemistry coupled to liquid chromatography with mass spectrometric and radioactivity detection. Anal. Chem. 83, 5415-5421.
49. Hambitzer, G., and Heitbaum, J. (1986) Electrochemical thermospray mass spectrometry. Anal. Chem. 58, 1067-1070.
50. Baumann, A., Pfeifer, T., Melles, D., and Karst, U. (2013) Investigation of the biotransformation of melarsoprol by electrochemistry coupled to complementary LC/ESI-MS and LC/ICP-MS analysis. Anal. Bioanal. Chem. 405, 5249-5258.
51. Bussy, U., Boujtita, M. (2014) Review of advances in coupling electrochemistry and liquid state NMR. Talanta, DOI:10.1016/j.talanta.2014.08.033.
52. Bussy, U., Giraudeau, P., Tea, I., and Boujtita, M. (2013) Understanding the degradation of electrochemically-generated reactive drug metabolites by quantitative NMR. Talanta 116, 554-558.
53. Zhang, X., and Zwanziger, J. W. (2011) Design and applications of an in situ electrochemical NMR cell. J. Magn. Reson. 208, 136-147.
54. Stalder, R., and Roth, G. P. (2013) Preparative microfluidic electrosynthesis of drug metabolites. ACS Med. Chem. Lett. 4, 1119-1123.
55. Khera, S., and Hu, N. (2013) Generation of statin drug metabolites through electrochemical and enzymatic oxidations. Anal. Bioanal. Chem. 405, 6009-6018.
56. Johansson, T., Weidolf, L., Castagnoli, J. N., and Jurva, U. (2010) P450-catalyzed vs. electrochemical oxidation of haloperidol studied by ultra-performance liquid chromatography/electrospray ionization mass spectrometry. Rapid Commun. Mass Spectrom. 24, 1231-1240.
57. Jahn, S., Baumann, A., Roscher, J., Hense, K., Zazzeroni, R., and Karst, U. (2011) Investigation of the biotransformation pathway of verapamil using electrochemistry/liquid chromatography/mass spectrometry - a comparative study with liver cell microsomes. J. Chromatogr. A 1218, 9210-9220.
58. Johansson, T., Weidolf, L., and Jurva, U. (2007) Mimicry of phase I drug metabolism - novel methods for metabolite characterization and synthesis. Rapid Commun. Mass Spectrom. 21, 2323-2331.
59. Nouri-Nigjeh, E., Bischoff, R., Bruins, A. P., and Permentier, H. P. (2011) Electrochemical oxidation by square-wave potential pulses in the imitation of phenacetin to acetaminophen biotransformation. Analyst 136, 5064-5067.
60. Bussy, U., Tea, I., Ferchaud-Roucher, V., Krempf, M., Silvestre, V., Galland, N., Jacquemin, D., Andresen-Bergstrom, M., Jurva, U., and Boujtita, M. (2013) Voltammetry coupled to mass spectrometry in the presence of isotope 18O labeled water for the prediction of oxidative transformation pathways of activated aromatic ethers: acebutolol. Anal. Chim. Acta 762, 39-46.
61. Lohmann, W., and Karst, U. (2007) Generation and identification of reactive metabolites by electrochemistry and immobilized enzymes coupled on-line to liquid chromatography/mass spectrometry. Anal. Chem. 79, 6831-6839.
62. Tahara, K., Yano, Y., Kanagawa, K., Abe, Y., Yamada, J., Iijima, S., Mochizuki, M., and Nishikawa, T. (2007) Successful preparation of metabolite of troglitazone by in-flow electrochemical reaction on coulometric electrode. Chem. Pharm. Bull. 55, 1207-1212.
63. Jurva, U., Holmen, A., Groenberg, G., Masimirembwa, C., and Weidolf, L. (2008) Electrochemical generation of electrophilic drug metabolites: characterization of amodiaquine quinoneimine and cysteinyl conjugates by MS, IR, and NMR. Chem. Res. Toxicol. 21, 928-935.
64. Johansson, T., Jurva, U., Groenberg, G., Weidolf, L., and Masimirembwa, C. (2009) Novel metabolites of amodiaquine formed by CYP1A1 and CYP1B1: structure elucidation using electrochemistry, mass spectrometry, and NMR. Drug Metab. Dispos. 37, 571-579.
65. Lohmann, W., and Karst, U. (2009) Electrochemistry meets enzymes: instrumental on-line simulation of oxidative and conjugative metabolism reactions of toremifene. Anal. Bioanal. Chem. 394, 1341-1348.
66. van Leeuwen, S. M., Blankert, B., Kauffmann, J. M., and Karst, U. (2005) Prediction of clozapine metabolism by on-line electrochemistry/liquid chromatography/mass spectrometry. Anal. Bioanal. Chem. 382, 742-750.
67. Jirásko, R., Mikysek, T., Chagovets, V., Vokřál, I., and Holčapek, M. (2013) Structural characterization of electrochemically and in vitro biologically generated oxidation products of atorvastatin using UHPLC/MS/MS. Anal. Bioanal. Chem. 405, 7181-7193.
68. Nozaki, K., Osaka, I., Kawasaki, H., and Arakawa, R. (2009) Application of on-line electrochemistry/electrospray/tandem mass spectrometry to a quantification method for the antipsychotic drug zotepine in human serum. Anal. Sci. 25, 1197-1201.
69. Nouri-Nigjeh, E., Permentier, H. P., Bischoff, R., and Bruins, A. P. (2010) Lidocaine oxidation by electrogenerated reactive oxygen species in the light of oxidative drug metabolism. Anal. Chem. 82, 7625-7633.
70. Nouri-Nigjeh, E., Permentier, H. P., Bischoff, R., and Bruins, A. P. (2011) Electrochemical oxidation by square-wave potential pulses in the imitation of oxidative drug metabolism. Anal. Chem. 83, 5519-5525.
71. Guengerich, F. P. (2013) Kinetic deuterium isotope effects in cytochrome P450 oxidation reactions. J. Labelled Compd. Radiopharm. 56, 428-431.
72. Miwa, G. T., Walsh, J. S., Kedderis, G. L., and Hollenberg, P. F. (1983) The use of intramolecular isotope effects to distinguish between deprotonation and hydrogen-atom abstraction mechnisms in cytochrome P-450-catalyzed and peroxidase-catalyzed N-demethylation reactions. J. Biol. Chem. 258, 4445-4449.
73. Guengerich, F. P., Yun, C. H., and Macdonald, T. L. (1996) Evidence for a 1-electron oxidation mechanism in N-dealkylation of N,N-dialkylanilines by cytochrome P450 2B1. Kinetic hydrogen isotope effects, linear free energy relationships, comparisons with horseradish peroxidase, and studies with oxygen surrogates. J. Biol. Chem. 271, 27321-27329.
74. Watanabe, Y., Oae, S., and Iyanagi, T. (1982) Mechanisms of enzymatic S-oxygenation of thioanisole derivatives and O-demethylation of anisole derivatives promoted by both microsomes and a reconstituted system with purified cytochrome P-450. Bull. Chem. Soc. Jpn. 55, 188-195.
75. Yun, C.-H., Miller, G. P., and Guengerich, F. P. (2000) Rate-determining steps in phenacetin oxidations by human cytochrome P450 1A2 and selected mutants. Biochemistry 39, 11319-11329.
76. Roberts, K. M. (2009) Mechanistic evaluation of N-dealkylation by cytochrome P450 using N,N-dimethylaniline N-oxides and kinetic isotope effects, Ph.D. Thesis, p 146, Washington State University, Pullman, WA.
77. Hinson, J. A., Nelson, S. D., and Gillette, J. R. (1979) Metabolism of [p-18O]-phenacetin: the mechanism of activation of phenacetin to reactive metabolites in hamsters. Mol. Pharmacol. 15, 419-427.
78. Hinson, J. A., Nelson, S. D., and Mitchell, J. R. (1977) Studies on the microsomal formation of arylating metabolites of acetaminophen and phenacetin. Mol. Pharmacol. 13, 625-633.
79. Dahlin, D. C., Miwa, G. T., Lu, A. Y., and Nelson, S. D. (1984) N-Acetyl-p-benzoquinone imine: a cytochrome P-450-mediated oxidation product of acetaminophen. Proc. Natl. Acad. Sci. U.S.A. 81, 1327-1331.
80. James, L. P., Mayeux, P. R., and Hinson, J. A. (2003) Acetaminophen-induced hepatotoxicity. Drug Metab. Dispos. 31, 1499-1506.
81. Yamazaki, H., Inoue, K., Mimura, M., Oda, Y., Guengerich, F. P., and Shimada, T. (1996) 7-Ethoxycoumarin O-deethylation catalyzed by cytochromes P450 1A2 and 2E1 in human liver microsomes. Biochem. Pharmacol. 51, 313-319.
82. Johansson, T., Weidolf, L., Popp, F., Tacke, R., and Jurva, U. (2010) In vitro metabolism of haloperidol and sila-haloperidol: new metabolic pathways resulting from carbon/silicon exchange. Drug Metab. Dispos. 38, 73-83.
83. Novak, M., Pelecanou, M., and Pollack, L. (1986) Hydrolysis of the model carcinogen N-(pivaloyloxy)-4-methoxyacetanilide: involvement of N-acetyl-p-benzoquinone imine. J. Am. Chem. Soc. 108, 112-120.
84. Baer, B. R., DeLisle, R. K., and Allen, A. (2009) Benzylic oxidation of gemfibrozil-1-O-β-glucuronide by P450 2C8 leads to heme alkylation and irreversible inhibition. Chem. Res. Toxicol. 22, 1298-1309.
85. Guroff, G., Daly, J. W., Jerina, D. M., Renson, J., Witkop, B., and Udenfriend, S. (1967) Hydroxylation-induced migration: the NIH shift. Recent experiments reveal an unexpected and general result of enzymatic hydroxylation of aromatic compounds. Science 157, 1524-1530.
86. Kasperek, G. J., Bruice, T. C., Yagi, H., and Jerina, D. M. (1972) Differentiation between the concerted and stepwise mechanisms for aromatization (NIH-shift) of arene epoxides. Chem. Commun., 784-785.
87. Kasperek, G. J., and Bruice, T. C. (1972) Mechanism of the aromatization of arene oxides. J. Am. Chem. Soc. 94, 198-202.
88. Korzekwa, K. R., Swinney, D. C., and Trager, W. F. (1989) Isotopically labeled chlorobenzenes as probes for the mechanism of cytochrome P-450 catalyzed aromatic hydroxylation. Biochemistry 28, 9019-9027.
89. Rietjens, I. M. C. M., Soffers, A. E. M. F., Veeger, C., and Vervoort, J. (1993) Regioselectivity of cytochrome P-450 catalyzed hydroxylation of fluorobenzenes predicted by calculated frontier orbital substrate characteristics. Biochemistry 32, 4801-4812.
90. de Visser, S. P., and Shaik, S. (2003) A proton-shuttle mechanism mediated by the porphyrin in benzene hydroxylation by cytochrome P450 enzymes. J. Am. Chem. Soc. 125, 7413-7424.
91. Bathelt, C. M., Ridder, L., Mulholland, A. J., and Harvey, J. N. (2004) Mechanism and structure-reactivity relationships for aromatic hydroxylation by cytochrome P450. Org. Biomol. Chem. 2, 2998-3005.
92. Bathelt, C. M., Ridder, L., Mulholland, A. J., and Harvey, J. N. (2003) Aromatic hydroxylation by cytochrome P450: model calculations of mechanism and substituent effects. J. Am. Chem. Soc. 125, 15004-15005.
93. Nematollahi, D., Shayani-Jam, H., Alimoradi, M., and Niroomand, S. (2009) Electrochemical oxidation of acetaminophen in aqueous solutions: kinetic evaluation of hydrolysis, hydroxylation and dimerization processes. Electrochim. Acta 54, 7407-7415.
94. Kauffmann, J.-M., Van Antwerpen, P., Sarakbi, A., Feier, B., Tarik, S., and Aydogmus, Z. (2011) Utility of screen printed electrodes for in vitro metabolic stability assays: application to acetaminophen and its thioconjugates. Electroanal 23, 2643-2650.
95. Cavalieri, E. L., Rogan, E. G., Devanesan, P. D., Cremonesi, P., Cerny, R. L., Gross, M. L., and Bodell, W. J. (1990) Binding of benzo[a]pyrene to DNA by cytochrome P-450 catalyzed one-electron oxidation in rat liver microsomes and nuclei. Biochemistry 29, 4820-4827.
96. Halliwell, B. (1991) Reactive oxygen species in living systems: source, biochemistry, and role in human disease. Am. J. Med. 91, S14-S22.
97. Sies, H., and de Groot, H. (1992) Role of reactive oxygen species in cell toxicity. Toxicol. Lett. 64-65, 547-551.
98. Fantel, A. G. (1996) Reactive oxygen species in developmental toxicity: review and hypothesis. Teratology 53, 196-217.
99. Haber, F., and Weiss, J. (1934) The catalytic decomposition of hydrogen peroxide by iron salts. Proc. R. Soc. London, Ser. A 147, 332-351.
100. Paller, M. S., and Jacob, H. S. (1994) Cytochrome P-450 mediates tissue-damaging hydroxyl radical formation during reoxygenation of the kidney. Proc. Natl. Acad. Sci. U.S.A. 91, 7002-7006.
101. Jeong, J., Kim, J. Y., and Yoon, J. (2006) The role of reactive oxygen species in the electrochemical inactivation of microorganisms. Environ. Sci. Technol. 40, 6117-6122.
102. Kugelmann, E., Albert, C. R., Bringmann, G., and Holzgrabe, U. (2011) Fenton's oxidation: a tool for the investigation of potential drug metabolites. J. Pharm. Biomed. Anal. 54, 1047-1058.
103. Isarain-Chávez, E., Rodríguez, R. M., Cabot, P. L., Centellas, F., Arias, C., Garrido, J. A., and Brillas, E. (2011) Degradation of pharmaceutical beta-blockers by electrochemical advanced oxidation processes using a flow plant with a solar compound parabolic collector. Water Res. 45, 4119-4130.
104. Marco-Urrea, E., Radjenovic, J., Caminal, G., Petrovic, M., Vicent, T., and Barcelo, D. (2010) Oxidation of atenolol, propranolol, carbamazepine and clofibric acid by a biological Fenton-like system mediated by the white-rot fungus Trametes versicolor. Water Res. 44, 521-532.
105. Sirés, I., Oturan, N., Oturan, M. A., Rodríguez, R. M., Garrido, J. A., and Brillas, E. (2007) Electro-Fenton degradation of antimicrobials triclosan and triclocarban. Electrochim. Acta 52, 5493-5503.
106. Potter, D. W., Miller, D. W., and Hinson, J. A. (1985) Identification of acetaminophen polymerization products catalyzed by horseradish peroxidase. J. Biol. Chem. 260, 12174-12180.
107. Oberacher, H., Pitterl, F., Erb, R., and Plattner, S. (2014) Mass spectrometric methods for monitoring redox processes in electrochemical cells. Mass Spectrom. Rev., DOI 10.1002/mas.21409.
108. Wasalathanthri, D. P., Mani, V., Tang, C. K., and Rusling, J. F. (2011) Microfluidic electrochemical array for detection of reactive metabolites formed by cytochrome P450 enzymes. Anal. Chem. 83, 9499-9506.
109. Krishnan, S., Wasalathanthri, D., Zhao, L., Schenkman, J. B., and Rusling, J. F. (2011) Efficient bioelectronic actuation of the natural catalytic pathway of human metabolic cytochrome P450s. J. Am. Chem. Soc. 133, 1459-1465.