Whole-cell amperometric biosensor for screening of cytochrome P450 inhibitors

Sensors and Actuators, B: Chemical

Volumn 223, Issue , 2016, Pages 392-399

  Yoetz Kopelman, Tal ^a   Porat Ophir, Carmit ^a   Shacham Diamand, Yosi ^a   Freeman, Amihay ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Aniline; Cytochrome P450 BM3; E. coli; Electrochemical biosensor; Inhibitors screening; Whole cell biosensor

Indexed keywords

ANILINE; COST EFFECTIVENESS; ENZYMES; ESCHERICHIA COLI; PURIFICATION;

CYTOCHROME P450 BM3; CYTOCHROME P450 INHIBITORS; E. COLI; ELECTROCHEMICAL BIOSENSING; ELECTROCHEMICAL BIOSENSOR; ELECTROCHEMICAL SIGNALS; ENVIRONMENTAL MONITORING; WHOLE-CELL BIOSENSORS;

BIOSENSORS;

EID: 84944097455     PISSN: 09254005     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.snb.2015.09.111     Document Type: Article

References (61)

1. P.B. Danielson The cytochrome P450 superfamily: biochemistry, evolution and drug metabolism in humans Curr. Drug Metab. 3 2002 561 597
2. J.A. Williams, R. Hyland, B.C. Jones, D.A. Smith, S. Hurst, T.C. Goosen, and et al. Drug-drug interactions for udp-glucuronosyltransferase substrates: a pharmacokinetic explanation for typically observed low exposure (auci/auc) ratios Drug Metab. Dispos. 32 2004 1201 1208 10.1124/dmd.104.000794
3. D. Nelson The cytochrome P450 homepage Hum. Genom. 4 2009 59 65
4. F.P. Guengerich Cytochrome P450 enzymes in the generation of commercial products Nat. Rev. Drug Discov. 1 2002 359 366
5. A.W. Munro, D.G. Leys, K.J. McLean, K.R. Marshall, T.W.B. Ost, S. Daff, and et al. P450 BM3: the very model of a modern flavocytochrome Trends Biochem. Sci. 27 2002 250 257 10.1016/S0968-0004(02)02086-8
6. C.-H. Yun, K.-H. Kim, D.-H. Kim, H.-C. Jung, and J.-G. Pan The bacterial P450 BM3: a prototype for a biocatalyst with human P450 activities Trends Biotechnol. 25 2007 289 298 10.1016/j.tibtech.2007.05.003
7. R. Bernhardt Encyclopedia of Biological Chemistry 2004 Elsevier 10.1016/B0-12-443710-9/00143-5
8. G. Di Nardo, A. Fantuzzi, A. Sideri, P. Panicco, C. Sassone, C. Giunta, and et al. Wild-type CYP102A1 as a biocatalyst: turnover of drugs usually metabolised by human liver enzymes J. Biol. Inorg. Chem. 12 2007 313 323 10.1007/s00775-006-0188-4
9. L.P. Wen, and A.J. Fulco Cloning of the gene encoding a catalytically self-sufficient cytochrome P-450 fatty acid monooxygenase induced by barbiturates in Bacillus megaterium and its functional expression and regulation in heterologous (Escherichia coli) and homologous (Bacillus) J. Biol. Chem. 262 1987 6676 6682
10. A.J. Warman, O. Roitel, R. Neeli, H.M. Girvan, H.E. Seward, S.A. Murray, and et al. Flavocytochrome P450 BM3: an update on structure and mechanism of a biotechnologically important enzyme Biochem. Soc. Trans. 33 2005 747 753 10.1042/BST0330747
11. M.C. Damsten, B.M. van Vugt-Lussenburg, T. Zeldenthuis, J.S.B. de Vlieger, J.N.M. Commandeur, and N.P.E. Vermeulen Application of drug metabolising mutants of cytochrome P450 BM3 (CYP102A1) as biocatalysts for the generation of reactive metabolites Chem. Biol. Interact. 171 2008 96 107 10.1016/j.cbi.2007.09.007
12. S. Fowler, and H. Zhang In vitro evaluation of reversible and irreversible cytochrome P450 inhibition: current status on methodologies and their utility for predicting drug-drug interactions AAPS J. 10 2008 410 424 10.1208/s12248-008-9042-7
13. J. Wu, C.S. Hughes, P. Picard, S. Letarte, M. Gaudreault, J.-F. Lévesque, and et al. High-throughput cytochrome P450 inhibition assays using laser diode thermal desorption-atmospheric pressure chemical ionization-tandem mass spectrometry Anal. Chem. 79 2007 4657 4665 10.1021/ac070221o
14. R. Xu, M. Manuel, J. Cramlett, and D.B. Kassel A high throughput metabolic stability screening workflow with automated assessment of data quality in pharmaceutical industry J. Chromatogr. A 1217 2010 1616 1625 10.1016/j.chroma.2010.01.009
15. K. Lim, C. Ozbal, and D. Kassel High-throughput mass spectrometric cytochrome P450 inhibition screening I.R. Phillips, E.A. Shephard, P.R. Ortiz de Montellano, Cytochrome P450 Protoc. SE - 3 2013 Humana Press 25 50 10.1007/978-1-62703-321-3-3
16. M.J. Traylor, J.D. Ryan, E.S. Arnon, J.S. Dordick, and D.S. Clark Rapid and quantitative measurement of metabolic stability without chromatography or mass spectrometry J. Am. Chem. Soc. 133 2011 14476 14479 10.1021/ja203172c
17. O.V. Trubetskoy, J.R. Gibson, and B.D. Marks Highly miniaturized formats for in vitro drug metabolism assays using vivid fluorescent substrates and recombinant human cytochrome P450 enzymes J. Biomol. Screen. 10 2005 56 66 10.1177/1087057104269731
18. B.M.A. Lussenburg, L.C. Babel, N.P.E. Vermeulen, and J.N.M. Commandeur Evaluation of alkoxyresorufins as fluorescent substrates for cytochrome P450 BM3 and site-directed mutants Anal. Biochem. 341 2005 148 155 10.1016/j.ab.2005.02.025
19. J.J. Cali, D. Ma, M. Sobol, D.J. Simpson, S. Frackman, T.D. Good, and et al. Luminogenic cytochrome P450 assays Expert Opin. Drug Metab. Toxicol. 2 2006 629 645 10.1517/17425255.2.4.629
20. A. Di Marco, I. Marcucci, M. Verdirame, J. Perez, M. Sanchez, F. Pelaez, and et al. Development and validation of a high-throughput radiometric CYP3A4/5 inhibition assay using tritiated testosterone Drug Metab. Dispos. 33 2005 349 358 10.1124/dmd.104.002873
21. A.K. Udit, and H.B. Gray Electrochemistry of heme-thiolate proteins Biochem. Biophys. Res. Commun. 338 2005 470 476 10.1016/j.bbrc.2005.08.087
22. V. Urlacher, and R.D. Schmid Biotransformations using prokaryotic P450 monooxygenases Curr. Opin. Biotechnol. 13 2002 557 564 10.1016/S0958-1669(02)00357-9
23. V. Reipa, M.P. Mayhew, and V.L. Vilker A direct electrode-driven P450 cycle for biocatalysis Proc. Natl. Acad. Sci. 94 1997 13554 13558
24. R.W. Estabrook, K.M. Faulkner, M.S. Shet, and C.W. Fisher Cytochrome P450, Part B 1996 Elsevier 10.1016/S0076-6879(96)72007-4
25. E. Schneider, and D.S. Clark Cytochrome P450 (CYP) enzymes and the development of CYP biosensors Biosens. Bioelectron. 39 2013 1 13 10.1016/j.bios.2012.05.043
26. S.J. Sadeghi, A. Fantuzzi, and G. Gilardi Breakthrough in P450 bioelectrochemistry and future perspectives Biochim. Biophys. Acta 1814 2011 237 248 10.1016/j.bbapap.2010.07.010
27. S.-K. Yim, D.-H. Kim, H.-C. Jung, J.-G. Pan, H.-S. Kang, T. Ahn, and et al. Surface display of heme- and diflavin-containing cytochrome P450 BM3 in Escherichia coli: a whole cell biocatalyst for oxidation J. Microbiol. Biotechnol. 20 2010 712 717
28. I.D.G. Macdonald, W. Ewen Smith, and A.W. Munro Inhibitor/fatty acid interactions with cytochrome P-450 BM3 FEBS Lett. 396 1996 196 200 10.1016/0014-5793(96)01095-2
29. G.E. Tsotsou, A.E.G. Cass, and G. Gilardi High throughput assay for cytochrome P450 BM3 for screening libraries of substrates and combinatorial mutants Biosens. Bioelectron. 17 2002 119 131 10.1016/S0956-5663(01)00285-8
30. A. Fantuzzi, M. Fairhead, and G. Gilardi Direct electrochemistry of immobilized human cytochrome P450 2E1 J. Am. Chem. Soc. 126 2004 5040 5041 10.1021/ja049855s
31. K. Yagi Applications of whole-cell bacterial sensors in biotechnology and environmental science Appl. Microbiol. Biotechnol. 73 2007 1251 1258 10.1007/s00253-006-0718-6
32. H. Ben-Yoav, A. Biran, R. Pedahzur, S. Belkin, S. Buchinger, G. Reifferscheid, and et al. A whole cell electrochemical biosensor for water genotoxicity bio-detection Electrochim. Acta 54 2009 6113 6118 10.1016/j.electacta.2009.01.061
33. R. Popovtzer, T. Neufeld, D. Biran, E.Z. Ron, J. Rishpon, and Y. Shacham-Diamand Novel integrated electrochemical nano-biochip for toxicity detection in water Nano Lett. 5 2005 1023 1027 10.1021/nl0503227
34. S. Vernick, A. Freeman, J. Rishpon, Y. Niv, A. Vilkin, and Y. Shacham-Diamand Electrochemical biosensing for direct biopsy slices screening for colorectal cancer detection J. Electrochem. Soc. 158 2011 P1 P4 10.1149/1.3507268
35. S. Kumar, S. Kundu, K. Pakshirajan, and V.V. Dasu Cephalosporins determination with a novel microbial biosensor based on permeabilized pseudomonas aeruginosa whole cells Appl. Biochem. Biotechnol. 151 2008 653 664 10.1007/s12010-008-8280-6
36. A.M. Ferrini, V. Mannoni, G. Carpico, and G.E. Pellegrini Detection and identification of β-lactam residues in milk using a hybrid biosensor J. Agric. Food Chem. 56 2008 784 788 10.1021/jf071479i
37. M.P. Byfield, and R.A. Abuknesha Biochemical aspects of biosensors Biosens. Bioelectron. 9 1994 373 399 10.1016/0956-5663(94)80038-3
38. L. Su, W. Jia, C. Hou, and Y. Lei Microbial biosensors: a review Biosens. Bioelectron. 26 2011 1788 1799 10.1016/j.bios.2010.09.005
39. C. Porat-Ophir Study of Conductive Coatings of Enzymes and Cells for Electrochemical Synthesis (Ph.D. Thesis) 2012 Tel Aviv University
40. Y. Lu, and L. Mei Co-expression of P450 BM3 and glucose dehydrogenase by recombinant Escherichia coli and its application in an NADPH-dependent indigo production system J. Ind. Microbiol. Biotechnol. 34 2007 247 253 10.1007/s10295-006-0193-1
41. R.K. Gudiminchi, and M.S. Smit Identification and characterization of 4-hexylbenzoic acid and 4-nonyloxybenzoic acid as substrates of CYP102A1 Appl. Microbiol. Biotechnol. 90 2011 117 126 10.1007/s00253-010-3029-x
42. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
43. Y. Paitan, I. Biran, N. Shechter, D. Biran, J. Rishpon, and E.Z. Ron Monitoring aromatic hydrocarbons by whole cell electrochemical biosensors Anal. Biochem. 335 2004 175 183 10.1016/j.ab.2004.08.032
44. A.J.F.L.R. Bard Electrochemical Methods Fundamentals and Applications 2001 John Wiley & Sons, Inc. New York
45. E. Gileady Electrode Kinetics for Chemists, Chemical Engineers and Materials Scientists 1993 Wiley-VCH New York
46. H. Yamazaki, M. Nakano, E.M.J. Gillam, L.C. Bell, F.P. Guengerich, and T. Shimada Requirements for cytochrome b5 in the oxidation of 7-ethoxycoumarin, chlorzoxazone, aniline, and N-nitrosodimethylamine by recombinant cytochrome P450 2E1 and by human liver microsomes Biochem. Pharmacol. 52 1996 301 309 10.1016/0006-2952(96)00208-0
47. C.A. Wijayawardhana, H.B. Halsall, and W.R. Heineman Electroanalytical Methods of Biological Materials 2002 Marcel Dekker, Inc.
48. J.S. Miles, A.W. Munro, B.N. Rospendowski, W.E. Smith, J. McKnight, and A.J. Thomson Domains of the catalytically self-sufficient cytochrome P-450 BM-3. Genetic construction, overexpression, purification and spectroscopic characterization Biochem. J. 288 1992 503 509
49. D. Kupfer, and L.L. Bruggeman Determination of enzymic demethylation of p-chloro-N-methylaniline. Assay of aniline and p-chloroaniline Anal. Biochem. 17 1966 502 512 10.1016/0003-2697(66)90185-0
50. A. Kausaite-Minkstimiene, V. Mazeiko, A. Ramanaviciene, and A. Ramanavicius Evaluation of amperometric glucose biosensors based on glucose oxidase encapsulated within enzymatically synthesized polyaniline and polypyrrole Sens. Actuators B: Chem. 158 2011 278 285 10.1016/j.snb.2011.06.019
51. J.B. Houston, and K.E. Kenworthy In vitro-in vivo scaling of CYP kinetic data not consistent with the classical Michaelis-Menten model Drug Metab. Dispos. 28 2000 246 254
52. T.R. Van Vleet, D.W. Bombick, and R.A. Coulombe Inhibition of human cytochrome P450 2E1 by nicotine, cotinine, and aqueous cigarette tar extract in vitro Toxicol. Sci. 64 2001 185 191 10.1093/toxsci/64.2.185
53. S.J. Smith, A.W. Munro, and W.E. Smith Resonance Raman scattering of cytochrome P450 BM3 and effect of imidazole inhibitors Biopolymers 70 2003 620 627 10.1002/bip.10502
54. M.A. Correia, and P.R. Ortiz de Montellano Cytochrome P450: Structure, Mechanism, and Biochemistry third ed. 2005 Springer Science & Business Media
55. P.R. Ortiz de Montellano, and J.M. Mathews Autocatalytic alkylation of the cytochrome P-450 prosthetic haem group by 1-aminobenzotriazole Isolation of an NN-bridged benzyne-protoporphyrin IX adduct Biochem. J. 195 1981 761 764
56. C.D. Linder, N.A. Renaud, and J.M. Hutzler Is 1-aminobenzotriazole an appropriate in vitro tool as a nonspecific cytochrome P450 inactivator? Drug Metab. Dispos. 37 2009 10 13 10.1124/dmd.108.024075
57. S. Karkola, A. Lilienkampf, and K. Wahala Recent Advances in Polyphenol Research vol. 1 2009 John Wiley & Sons
58. J.C. Hackett, Y.-W. Kim, B. Su, and R.W. Brueggemeier Synthesis and characterization of azole isoflavone inhibitors of aromatase Bioorg. Med. Chem. 13 2005 4063 4070 10.1016/j.bmc.2005.03.050
59. Q. Shi, X. Yang, J. Greenhaw, and W.F. Salminen Hepatic cytochrome P450s attenuate the cytotoxicity induced by leflunomide and its active metabolite A77 1726 in primary cultured rat hepatocytes Toxicol. Sci. 122 2011 579 586 10.1093/toxsci/kfr106
60. E.H. Seymour, N.S. Lawrence, E.L. Beckett, J. Davis, and R.G. Compton Electrochemical detection of aniline: an electrochemically initiated reaction pathway Talanta 57 2002 233 242
61. T. Spətaru, N. Spətaru, and A. Fujishima Detection of aniline at boron-doped diamond electrodes with cathodic stripping voltammetry Talanta 73 2007 404 406