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Can peroxygenase and microperoxidase substitute cytochrome P450 in biosensors

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Bioanalytical Reviews

Abstract

Aromatic peroxygenase (APO) from the basidiomycetous mushroom Agrocybe aegerita (AaeAPO) and microperoxidases (MPs) obtained from cytochrome c exhibit a broad substrate spectrum including hydroxylation of selected aromatic substrates, demethylation and epoxidation by means of hydrogen peroxide. It overlaps with that of cytochrome P450 (P450), making MPs and APOs to alternate recognition elements in biosensors for the detection of typical P450 substrates. Here, we discuss recently developed approaches using microperoxidases and peroxygenases in view of their potential to supplement P450 enzymes as recognition elements in biosensors for aromatic compounds. Starting as early as the 1970s, the direct electron transfer between electrodes and the heme group of heme peptides called microperoxidases has been used as a model of oxidoreductases. These MP-modified electrodes are used as hydrogen peroxide detectors based on the catalytic current generated by electrically contacted microperoxidase molecules. A similar catalytic reaction has been obtained for the electrode-immobilised heme protein AaeAPO. However, up to now, no MP-based sensors for substrates have been described. In this review, we present biosensors which indicate 4-nitrophenol, aniline, naphthalene and p-aminophenol based on the peroxide-dependent substrate conversion by electrode-immobilised MP and AaeAPO. In these enzyme electrodes, the signal is generated by the conversion of all substrates, thus representing in complex media an overall parameter. The performance of these sensors and their further development are discussed in comparison with P450-based electrodes.

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Notes

  1. In previous publications, the enzymes were named A. aegerita peroxidase/peroxygenase (AaeAPO), haloperoxidase or haloperoxidase–peroxygenase [36, 37, 45, 48]. Because of the discovery of more and more peroxygenases, they should be systematically abbreviated by the capital letter of the fungal genus plus the first and second letters of the species identifier (epitheton) and a suitable acronym such as APO (which stands for aromatic peroxygenase), e.g. Agrocybe aegerita aromatic peroxygenase = AaeAPO.

References

  1. Lohmann W, Karst U (2008) Biomimetic modelling of oxidative drug metabolism: strategies, advantages and limitations. Anal Bioanal Chem 391:79–96

    Article  CAS  Google Scholar 

  2. Nagatsu Y, Higuchi T, Hirobe M (1990) Application of chemical P-450 systems to study drug metabolism. III. The metabolism of 3-isobutyryl-2-isopropylpayrazolo[1,5-α]pyridine. Chem Pharm Bull 38:400–403

    CAS  Google Scholar 

  3. Hofrichter M, Ullrich R, Pecyna M, Kinne M, Kluge M, Aranda E, Liers C et al. (2009) Aromatic peroxygenases from mushrooms: extracellular heme-thiolate proteins of a new enzyme sub-subclass? In: Shoun H, Ohkawa H (eds) 16th International Conference on Cytochrome P450 (Nago, Okinawa, Japan), Medimond (International Proceedings), Bologna, Italy, pp 83–88

  4. Renneberg R, Scheller F, Ruckpaul K, Pirrwitz J, Mohr P (1978) NADPH and H2O2-dependent reactions of cytochrome P-450LM compared with peroxidase catalysis. FEBS Lett 96:349–353

    Article  CAS  Google Scholar 

  5. Bistolas N, Wollenberger U, Jung C, Scheller FW (2005) Cytochrome P450 biosensors—a review. Biosens Bioelectron 20:2408–2423

    Article  CAS  Google Scholar 

  6. Rabe KS, Gandubert VJ, Spengler M, Erkelenz M, Niemeyer CM (2008) Engineering and assaying of cytochrome P450 biocatalysts. Anal Bioanal Chem 392:1059–1073

    Article  CAS  Google Scholar 

  7. Sadeghi SJ, Fantuzzi A, Gilardi G (2011) Breakthrough in P450 bioelectrochemistry and future perspectives. Biochim Biophys Acta 1814:237–248

    CAS  Google Scholar 

  8. Shumyantseva VV, Bulko TV, Suprun EV, Chalenko YM, Vagin MY, Rudakov YO, Shatskaya MA, Archakov AI (2011) Electrochemical investigations of cytochrome P450. BBA 1814:94–101

    CAS  Google Scholar 

  9. Denisov IG, Makris TM, Sligar SG, Schlichting I (2005) Structure and chemistry of cytochromes P450. Chem Rev 105:2253–2277

    Article  CAS  Google Scholar 

  10. Theâvenot DR, Toth K, Durst RA, Wilson GS (1999) Electrochemical biosensors: recommended definitions and classification. Pure Appl Chem 71:2333–2348

    Article  Google Scholar 

  11. Clark LC, Lyons C (1962) Electrode systems for continuous monitoring in cardiovascular surgery. Ann N Y Acad Sci Bd 102:29–45

    Article  CAS  Google Scholar 

  12. Brandon EFA, RAaeAPO CD, Meijerman I, Beijnen JH, Schellens JHM (2003) An update on in vitro test methods in human hepatic drug biotransformation research: pros and cons. Toxicaol Appl Pharmacol 189:233–246

    Article  CAS  Google Scholar 

  13. Pelkonen O, Turpeinen M, Uusitalo J, Rautio A, Raunio H (2005) Prediction of drug metabolism and interactions on the basis of in vitro investigations. Basic Clin Pharmacol Toxicol 96:167–175

    Article  CAS  Google Scholar 

  14. Lewis DFV (2001) Guide to cytochromes P450: structure and function. Taylor and Francis, New York

    Book  Google Scholar 

  15. Ortiz de Montellano PR (2004) Cytochrome P450: structure, mechanism, and biochemistry, 3rd edn. Springer, New York, p 689

    Google Scholar 

  16. Cirino PC, Arnold FH (2003) A self-sufficient peroxide-driven hydroxylation biocatalyst. Angew Chem Int Ed Engl 28:3299–3301

    Article  CAS  Google Scholar 

  17. Scheller F, Renneberg R, Strnad G, Pommerening K, Mohr P (1977) Electrochemical aspects of cytochrome P-450 system from liver microsomes. Bioelectrochem Bioenerg 4:500–507

    Article  CAS  Google Scholar 

  18. Tsotsou GE, Cass AEG, Gilardi G (2002) High throughput assay for cytochrome P450 BM3 for screening libraries of substrates and combinatorial mutants. Biosens Bioelectron 17:113–119

    Article  Google Scholar 

  19. Eggers HM, Halsall HB, Heineman WR (1982) Enzyme immunoassay with flow-amperometric detection of NADH. Clin Chem 28:1848–1851

    CAS  Google Scholar 

  20. Elving PJ, Bresnahan W, Moiroux J, Samec Z (1982) NAD/NADH as a model redox system: mechanism, mediation, modification by the environment. Bioelectrochem Bioenerg 2:365–378

    Article  Google Scholar 

  21. Wodnicka M, Guarino RD, Hemperly JJ, Timmins MR, Stitt D, Pitner JB (2000) Novel fluorescent technology platform for high throughput cytotoxicity and proliferation assays. J Biomol Screen 5:141–152

    Article  CAS  Google Scholar 

  22. Yu D, Blankert B, Bodoki E, Viré J-C, Sandulescu R, Nomura A, Kauffmann J-M (2006) Amperometric biosensors based on horseradish peroxidase-immobilised magnetic microparticles. Sens Actuators, B 113:149–154

    Article  CAS  Google Scholar 

  23. Yu D, Blankert B, Kauffmann J-M (2007) Development of amperometric horseradish peroxidase based biosensors for clozapine and for the screening for thiol compounds. Biosens Bioelectron 22:2707–2711

    Article  CAS  Google Scholar 

  24. Yu D, Renedo OD, Blankert B, Bodoki E, Sima V, Sandulescu R, Arcos J, Kauffmann J-M (2006) A peroxidase-based biosensor supported by nanoporous silica microparticles for acetaminophen biotransformation and inhibition studies. Electroanalysis 18:1637–1642

    Article  CAS  Google Scholar 

  25. Scheller W, Jin W, Ehrentreich-Förster E, Ge B, Lisdat F, Büttemeier R, Wollenberger U, Scheller FW (1999) Cytochrome C based superoxide sensor for in vivo application. Electroanalysis 11:703–706

    Article  CAS  Google Scholar 

  26. Wu Y, Liu X, Wang C (2011) An amperometric biosensor based on rat cytochrome p450 1A1 for benzo[a]pyrene determination. Biosens Bioelectron 26:2177–2182

    Article  CAS  Google Scholar 

  27. Estabrook RW, Faulkner KM, Shet MJ, Fisher CW (1996) In: Waterman MR, Johnson EF (eds) Methods in enzymology, vol 272. Cytochrome P450 (Part B). Academic Press, pp 44–51

  28. Eddowes MJ, Hill HAO (1977) Novel method for the investigation of the electrochemistry of metalloproteins: cytochrome c. J Chem Soc Chem Commun 21:771b–772

    Article  Google Scholar 

  29. Yeh P, Kuwana T (1977) Reversible electron reaction of cytochrome c. Chem Lett 10:1145–1148

    Article  Google Scholar 

  30. Ikeda T (1992) Electrochemical bionsensors based on biocatalyst electrodes. Bull Electrochem 8:45–159

    Google Scholar 

  31. Degani Y, Heller A (1987) Direct electrical communication between chemically modified enzymes and metal-electrodes. 1. Electron-transfer from glucose-oxidase to metal-electrodes via electron relays, bound covalently to the enzyme. J Phys Chem 91:1285–1289

    Article  CAS  Google Scholar 

  32. Shumyantseva VV, Bulko TV, Bachmann TT, Bilitewski U, Schmid RD, Archakov AI (2000) Electrochemical reduction of flavocytochromes 2B4 and 1A2 and their catalytic activity. Arch Biochem Biophys 377:43–48

    Article  CAS  Google Scholar 

  33. Gilardi G, Fantuzzi A, Sadeghi SJ (2001) Engineering and design in the bioelectrochemistry of metalloproteins. Curr Opin Struct Biol 11:491–499

    Article  CAS  Google Scholar 

  34. Gilardi G, Meharenna YT, Tsotsou GE, Sadeghi SJ, Fairhead M, Giannini S (2002) Molecular Lego: design of molecular assemblies of P450 enzymes for nanobiotechnology. Biosens Bioelectron 17:133–145

    Article  CAS  Google Scholar 

  35. Wong TS, Schwaneberg U (2003) Protein engineering in bioelectrocatalysis. Curr Opin Biotech 14:590–596

    Article  CAS  Google Scholar 

  36. Ullrich R, Nüske J, Scheibner K, Spantzel J, Hofrichter M (2004) Novel haloperoxidase from the agaric basidiomycete Agrocybe aegerita oxidizes aryl alcohols and aldehydes. Appl Environ Microbiol 70:4575–4581

    Article  CAS  Google Scholar 

  37. Ullrich R, Hofrichter M (2005) The haloperoxidase of the agaric fungus Agrocybe aegerita hydroxylates toluene and naphthalene. FEBS Lett 579:6247–6250

    Article  CAS  Google Scholar 

  38. Kinne M, Poraj-Kobielska M, Aranda E, Ullrich R, Hammel KE, Scheibner K, Hofrichter M (2009) Regioselective preparation of 5-hydroxypropranolol and 4′-hydroxydiclofenac with a fungal peroxygenase. Bioorg Med Chem Lett 19:3085–3087

    Article  CAS  Google Scholar 

  39. Kinne M, Poraj-Kobielska M, Ralph SA, Ullrich R, Hofrichter M, Hammel KE (2009) Oxidative cleavage of diverse ethers by an extracellular fungal peroxygenase. J Biol Chem 284:29343–29349

    Article  CAS  Google Scholar 

  40. Hofrichter M, Ullrich R (2010) New trends in fungal biooxidation. In: Hofrichter M, Esser K (eds) The Mycota, volume X. Industrial applications, 2nd edn. Springer, Berlin, pp 425–449

    Google Scholar 

  41. Kluge M, Ullrich R, Dolge C, Scheibner K, Hofrichter M (2009) Hydroxylation of naphthalene by aromatic peroxygenase from Agrocybe aegerita proceeds via oxygen transfer from H2O2 and intermediary epoxidation. Appl Microbiol Biotechnol 81:1071–1076

    Article  CAS  Google Scholar 

  42. Aranda E, Ullrich R, Hofrichter M (2010) Conversion of polycyclic aromatic hydrocarbons, methyl naphthalenes and dibenzofuran by two fungal peroxygenases. Biodegradation 21:267–281

    Article  CAS  Google Scholar 

  43. Pecyna MJ, Ullrich R, Bittner B, Clemens A, Scheibner K, Schubert R, Hofrichter M (2009) Molecular characterization of aromatic peroxygenase from Agrocybe aegerita. Appl Microbiol Biotechnol 84:885–897

    Article  CAS  Google Scholar 

  44. Hofrichter M, Ullrich R, Pecyna MJ, Liers C, Lundell T (2010) New and classic families of secreted fungal heme peroxidases. Appl Microbiol Biotechnol 87:871–897

    Article  CAS  Google Scholar 

  45. Hofrichter M, Ullrich R (2006) Heme-thiolate haloperoxidases: versatile biocatalysts with biotechnological and environmental significance. Appl Microbiol Biotechnol 71:276–288

    Article  CAS  Google Scholar 

  46. Ullrich R, Liers C, Schimpke S, Hofrichter M (2009) Purification of homogeneous forms of fungal peroxygenase. Biotechnol J 4:1619–1626

    Article  CAS  Google Scholar 

  47. Kinne M, Zeisig C, Ullrich R, Kayser G, Hammel KE, Hofrichter M (2010) Stepwise oxygenations of toluene and 4-nitrotoluene by a fungal peroxygenase. Biochem Biophys Res Commun 397:18–21

    Article  CAS  Google Scholar 

  48. Kluge MG, Ullrich R, Scheibner K, Hofrichter M (2007) Spectrophotometric assay for detection of aromatic hydroxylation catalysed by fungal haloperoxidase-peroxygenase. Appl Microbiol Biotechnol 75:1473–1478

    Article  CAS  Google Scholar 

  49. Gonzalez FJ (2005) Role of cytochromes P450 in chemical toxicity and oxidative stress: studies with P4502E1. Mutat Res 569:101–110

    Article  CAS  Google Scholar 

  50. Peng L, Wollenberger U, Hofrichter M, Ullrich R, Scheibner K, Scheller FW (2010) Bioelectrocatalytic properties of Agrocybe aegerita peroxygenase. Electrochim Acta 55:7809–7813

    Article  CAS  Google Scholar 

  51. Tassaneeyakul W, Veronese ME, Birkett DJ, Gonzalez FJ, Miners JO (1993) Validation of 4-nitrophenol as an in vitro substrate probe for human liver P4502E1 using cDNA expression and microsomal kinetic techniques. Biochem Pharmacol 46:1975–1981

    Article  CAS  Google Scholar 

  52. Kinne M, Ullrich R, Hammel KE, Hofrichter M (2008) Regioselective preparation of (R)-2-(4-Hydroxyphenoxy)propionic acid with a fungal peroxygenase. Tetrahedron Lett 49:5950–5953

    Article  CAS  Google Scholar 

  53. Ullrich R, Dolge C, Kluge M, Hofrichter M (2008) Pyridine as novel substrate for regioselective oxygenation with aromatic peroxygenase from Agrocybe aegerita. FEBS Lett 582:4100–4106

    Article  CAS  Google Scholar 

  54. Ullrich R, Hofrichter M (2007) Enzymatic hydroxylation of aromatic compounds. Cell Mol Life Sci 64:271–293

    Article  CAS  Google Scholar 

  55. Makris TM, Denisov I, Schlichting I, Sligar SG (2005) Activation of molecular oxygen by cytochrome P450. In: Ortiz De Montellano PR (ed) Cytochrome P450 - Structure, Mechanism and Biochemistry, 3rd edn. Kluwer Academic/Plenum Publishers, New York, pp 149–182

    Google Scholar 

  56. Piontek K, Ullrich R, Liers C, Diederichs K, Plattner D, Hofrichter M (2010) Crystallization of a 45 kDa peroxygenase/peroxidase from the mushroom Agrocybe aegerita and structure determination by SAD utilizing only the heme iron. Acta Crystallogr Sect F Struct Biol Cryst Commun 66:693–698

    Article  CAS  Google Scholar 

  57. Kinne M, Poraj-Kobielska M, Ullrich R, Nousiainen P, Sipilä J, Scheibner K, Hammel K, Hofrichter M (2011) Oxidative cleavage of non-phenolic beta-O-4 lignin model dimers by an extracellular aromatic peroxygenase. Holzforschung, in press

  58. Oku Y, Ohtaki A, Kamitori S, Nakamura N, Yohda M, Ohno H, Kawarabayashi Y (2004) Structure and direct electrochemistry of cytochrome P-450 from the thermoacidophilic crenarchaeon, Sulfolobus tokodaii strain 7. J Inorg Biochem 98:1194–1197

    Article  CAS  Google Scholar 

  59. Estavillo C, Lu Z, Jansson I, Schenkman JB, Rusling JF (2003) Epoxidation of styrene by human cyt P-450 1A2 by thin film electrolysis and peroxide activation compared to solution reactions. Biophysical Chem 104:291–296

    Article  CAS  Google Scholar 

  60. Shumyantseva VV, Ivanov YD, Bistolas N, Scheller FW, Archakov AI, Wollenberger U (2004) Direct electron transfer of cytochrome P450 2B4 at electrodes modified with non-ionic detergent and colloidal clay nanoparticles. Anal Chem 76:6046–6052

    Article  CAS  Google Scholar 

  61. Rusling JF, Zhou L, Munge B, Yang J, Estavillo C, Schenkmann JB (2000) Applications of polyion filmss containing biomolecules to sensing toxicity. Faraday Discuss 116:77–87

    Article  CAS  Google Scholar 

  62. Laviron E (1979) General expression of the linear potential sweep voltammogram in the case of diffusionless electrochemical systems. J Electroanal Chem 101:19–28

    Article  CAS  Google Scholar 

  63. Kamin RA, Wilson GS (1980) Rotating ring-disk enzyme electrode for biocatalysis kinetic studies and characterization of the immobilised enzyme layer. Anal Chem 52:1198–1205

    Article  CAS  Google Scholar 

  64. Xiao Y, Ju HX, Chen HY (2000) Direct Electrochemistry of Horseradish Peroxidase İmmobilised on a Colloid/Cysteamine-Modified Gold Electrode. Anal Biochem 278:22–28

    Article  CAS  Google Scholar 

  65. Anh DH, Ullrich R, Benndorf D, Svatoś A, Muck A, Hofrichter M (2007) The coprophilous mushroom Coprinus radians secretes a haloperoxidase that catalyzes aromatic peroxygenation. Appl Eviron Microbiol 73:5477–5485

    Article  CAS  Google Scholar 

  66. Veeger C (2002) Does P450-type catalysis proceed through a peroxo-iron intermediate?A review of studies with microperoxidase. J Inorg Biochem 91:35–45

    Article  CAS  Google Scholar 

  67. Peng L, Wollenberger U, Kinne M, Hofrichter Ullrich R, Schreibner K, Fischer A, Scheller FW (2010) Peroxygenase based sensor for aromatic compounds. Biosens Bioelectron 26:1432–1436

    Article  CAS  Google Scholar 

  68. Kafi AKM, Chen AC (2009) A novel amperometric biosensor for the detection of nitrophenol. Talanta 79:97–102

    Article  CAS  Google Scholar 

  69. England PA, Harford-Cross CF, Stevenson JA, Rouch DA, Wong LL (1998) The oxidation of naphthalene and pyrene by cytochrome P450cam. FEBS Lett 424:271–274

    Article  CAS  Google Scholar 

  70. Durliat H, Courteix A, Comtat M (1992) Role of horseradish peroxidase in the catalytic hydroxylation of phenol. J Mol Catal 75:357–369

    Article  CAS  Google Scholar 

  71. Monostory K, Hazai E, Vereczkey L (2004) Inhibition of cytochrome P450 enzymes participating in p-nitrophenol hydroxylation by drugs known as CYP2E1 inhibitors. Chem Biol Interact 147:331–340

    Article  CAS  Google Scholar 

  72. Adams PA (2001) In: Everse J, Everse KE, Grisham MB (eds) Peroxidases in chemistry and biology, vol II. CRC, Boca Raton, pp 174–176

  73. Marques MH (2007) Insights into porphyrin chemistry provided by the microperoxidases, the haempeptides derived from cytochrome c. Dalton Trans 39:4371–4385

    Article  CAS  Google Scholar 

  74. Wilson MT, Ranson J, Masiakowski P, Czarnecka E, Brunori M (1977) A kinetic study of the pH dependent properties of the ferric undecapeptide of cytochrome c (microperoxidase). Eur J Biochem 77:193–199

    Google Scholar 

  75. Braun M, Thöny-Meyer L (2004) Biosynthesis of artificial microperoxidases by exploiting the secretion and cytochrome c maturation apparatuses of Escherichia coli. PNAS 101:12830–12835

    Article  CAS  Google Scholar 

  76. Ni TW, Tezcan FA (2010) Structural characterization of a microperoxidase inside a metal-directed protein cage. Angew Chem Int Ed 49:7014–7018

    Article  CAS  Google Scholar 

  77. Laszlo JA, Compton DL (2002) Comparison of peroxidase activities of hemin, cytochrome c and microperoxidase-11 in molecular solvents and imidazolium-based ionic liquids. J Mol Catal B: Enzym 18:109–120

    Article  CAS  Google Scholar 

  78. Vazquez-Duhalt R (1999) Cytochrome c as a biocatalyst. J Mol Catal B: Enzym 7:241–249

    Article  CAS  Google Scholar 

  79. Deere J, Magner E, Wall EJ, Hodnett BK (2003) Oxidation of ABTS by silicate-immobilised cytochrome c in nonaqueous solutions. Biotechnol Prog 19:1238–1243

    Article  CAS  Google Scholar 

  80. Adams PA (1990) The peroxidasic activity of the haem octapeptide microperoxidase-8 (MP-8): the kinetic mechanism of the catalytic reduction of H2O2 by MP-8 using 2,2′-azinobis-(3-ethylbenzothiazoline-6-sulphonate) (ABTS) as reducing substrate. J Chem Soc, Perkin Trans 2:1407–1414

    Google Scholar 

  81. Spee JH, Boersma MG, Veeger C, Samyn B, Van Beeumen J, Warmerdam G, Canters GW, Van Dongen WMAM, Rietjens IMCM (1996) The influence of the peptide chain on the kinetics and stability of microperoxidases. Eur J Biochem 24:215–220

    Article  Google Scholar 

  82. Osman AM, Koerts J, Boersma MG, Boeren S, Veeger C, Rietjens IMCM (1996) Heme-(hydro)peroxide mediated O- and N-dealkylation: a study with microperoxidase. Eur J Biochem 240:232–238

    Article  CAS  Google Scholar 

  83. Boersma MG, Primus J-L, Koerts J, Veeger C, Rietjens IMCM (2000) Heme-(hydro)peroxide mediated O- and N-dealkylation: a study with microperoxidase. Eur J Biochem 267:6673–6678

    Article  CAS  Google Scholar 

  84. Rusvaia E, Végha M, Kramera M, Horvátha I (1988) Hydroxylation of aniline mediated by heme-bound oxy-radicals in a heme peptide model system. Biochem Pharmacol 37:4574–4577

    Article  Google Scholar 

  85. Sharma VS, Isaacson RA, John ME, Waterman MR, Chevion M (1983) Reaction of nitric oxide with heme proteins: studies on metmyoglobin, opossum methemoglobin, and microperoxidase. Bioelectrochemistry 22:3897–3902

    CAS  Google Scholar 

  86. Dorosvka-Taran V, Posthumus MA, Boeren S, Boersma MG, Teunis CJ, Rietjens IMCM, Veegere C (1998) Oxygen exchange with water in heme-oxo intermediates during H2O2-driven oxygen incorporation in aromatic hydrocarbons catalysed by microperoxidase-8. Eur J Biochem 253:659–668

    Article  Google Scholar 

  87. Reszka KJ, McCormick ML, Britigan BE (2003) Oxidation of anthracycline antiicancer agents by the peroxidase mimic microperoxidase 11 and hydrogen peroxide. Free Radical Biol Med 35:78–93

    Article  CAS  Google Scholar 

  88. Reszka KJ, O’Malley Y, McCormick ML, Denning GM, Britigan BE (2003) Oxidation of pyocyanin, a cytotoxic product from Pseudomonas aeruginase, by microperoxidase 11 and hydrogen peroxide. Free Radical Biol Med 11:1448–1459

    Google Scholar 

  89. Rodriguez M, Claparols C, Robert A, Meunier B (2002) Alkylation of microperoxidase-11 by the antimalarial drug artemisinin. ChemBioChem 11:1147–1149

    Article  Google Scholar 

  90. Mohajerani B, Soleymani-Jamarani M, Nazari K, Mahmoudib A, Moosavi-Movahedi AA (2008) Microperoxidase-11-NH2-FSM16 biocatalyst: a heterogeneous enzyme model for peroxidative reactions. J Mol Catal Chem 296:28–35

    Article  CAS  Google Scholar 

  91. Jeng WY, Tsai YH, Chuang WJ (2004) The catalase activity of Nalpha-acetyl-microperoxidase-8. Peptide Res 64:104–109

    Article  CAS  Google Scholar 

  92. Ranweiler JS, Wilson GS (1976) Structural effects on cytochrome electron transfer: properties of HPI-65 from horse heart cytochrome C. Biolectrochem Bioenerg 3:113–122

    Article  CAS  Google Scholar 

  93. Lötzbeyer T, Schuhmann W, Schmidt H-L (1997) Minienzymes: a review for the development of reagentless amperometric biosensors based on direct electron-transfer process. Bioelectrochem Bioenerg 42:1–6

    Article  Google Scholar 

  94. Santucci R, Reinhard H, Brunori M (1988) Direct electrochemistry of the undecapeptide from cytochrome c (microperoxidase) at a glassy carbon electrode. J Am Chem Soc 110:8536–8537

    Article  CAS  Google Scholar 

  95. Razumas V, Kazlauskaite J, Ruzgas T, Kulys J (1992) Bioelectrochemistry of microperoxidases. Bioelectrochem Bioenerg 28:159–176

    Article  CAS  Google Scholar 

  96. Ruzgas T, Gaigalas A, Gorton L (1999) Diffusionless electron transfer of microperoxidase-11 on gold electrodes. J Electroanal Chem 469:123–131

    Article  CAS  Google Scholar 

  97. Kulys J, Drungiliene A, Wollenberger U, Scheller F (1998) Membrane covered carbon paste electrode for the electrochemical determination of peroxidase and microperoxidase in a flow system. Bioelectrochem Bioenerg 45:227–232

    Article  CAS  Google Scholar 

  98. Tatsuma T, Watanabe T (1991) Peroxidase model electrodes: sensing of imidazole derivatives with heme peptide-modified electrode. Anal Chem 64:143–147

    Article  Google Scholar 

  99. Tatsuma T, Watanabe T (1992) Peroxidase model electrodes: heme peptide modified electrodes as reagentless sensors for hydrogen peroxide. Anal Chem 63:1580–1585

    Article  Google Scholar 

  100. Patolsky F, Gabriel T, Willner I (1999) Controlled electrocatalysis by microperoxidase-11 and Au-nanoparticle superstructures on conductive supports. J Electroanal Chem 479:69–73

    Article  CAS  Google Scholar 

  101. Renault C, Haris KD, Brett MJ, Balland V, Limoges B (2011) Time-resolved UV–visible spectroelectrochemistry using 3D-transparent mesoporous nanocrystalline ITO electrodes. Chem Commun 47:1863–1865

    Article  CAS  Google Scholar 

  102. Wan J, Ding J, Wang M (2010) Preparation of gold nanotube by direct electrodeposition for biosensors. J Clust Sci 21:669–677

    Article  CAS  Google Scholar 

  103. Wang M, Shen Y, Liu Y, Wang T, Zhao F, Liu F, Dong S (2005) Direct electrochemistry of microperoxidase 11 using carbon nanotube modified electrodes. J Electroanal Chem 578:121–127

    Article  CAS  Google Scholar 

  104. Mazzei F, Favero G, Frasconi M, Tata A, Pepi F (2009) Electron-transfer kinetics of microperoxidase-11 covalently immobilised onto the surface of multi-walled carbon nanotubes by reactive landing of mass-selected ions. Chem Eur J 15:7359–7367

    Article  CAS  Google Scholar 

  105. Astuti Y, Topoglidis E, Gilardi G, Durrant JR (2004) Cyclic voltammetry and voltabsorptometry studies of redox proteins immobilised on nanocrystalline tin dioxide electrodes. Bioelectrochemistry 63:55–59

    Article  CAS  Google Scholar 

  106. Santucci R, Brunori M, Campanella L, Tranchida G (1992) Electrochemical behaviour of horse heart cytochrome c and microperoxidase at a gold electrode chemically modified with sulphur-containing compounds. Bioelectrochem Bioenerg 29:177–184

    Article  CAS  Google Scholar 

  107. Lötzbeyer T, Schuhmann W, Schmidt H-L (1996) Electron transfer principles in amperometric biosensors: direct electron transfer between enzymes and electrode surface. Sens Actuators, B 23:50–54

    Article  Google Scholar 

  108. Razumas VJ, Gudavičius AV, Kazlauskaite JD, Kulys JJ (1989) Redox conversions of microperoxidase-11 on a silver electrode. J Electroanal Chem Interfac 271:155–160

    Article  CAS  Google Scholar 

  109. Wollenberger U, Drungiliene A, Stöcklein W, Kulys JJ, Scheller FW (1996) Direct electrocatalytic determination of dissolved peroxidases. Anal Chim Acta 329:231–237

    Article  CAS  Google Scholar 

  110. Huang W, Zhang Z, Han X, Tang J, Peng Z, Dong S, Wang E (2001) Electrochemistry and spectroscopy study on the interaction of microperoxidase-11 with lipid membrane. Biophys Chem 94:165–173

    Article  CAS  Google Scholar 

  111. Qi Z, Li X, Sun D, Li C, Lu T, Ding X, Huang X (2006) Effect of Tris on cacatalytic activity of MP-11. Bioelectrochemistry 68:40–47

    Article  CAS  Google Scholar 

  112. Lötzbeyer T, Schuhmann W, Katz E, Falter J, Schmidt H-L (1994) Direct electron transfer between the covalently immobilised enzyme microperoxidase MP-11 and a cystamine-modified gold electrode. J Electroanal Chem 377:291–294

    Article  Google Scholar 

  113. Jiang L, Glidle A, McNeil JC, Cooper MJ (1997) Characterization of electron transfer reactions of microperoxidase assembled at short-chain thiol-monolayers on gold. Biosens Bioelectron 12:1143–1155

    Article  CAS  Google Scholar 

  114. Gooding JJ, Erokhin P, Losic D, Yang W, Policarpio V, Liu J, Ho FM, Situmorang M, Hibbert DB, Shapter JG (2001) Parameters important in fabricating enzyme electrodes using self-assembled monolayers of alkanethiols. Anal Sci 17:3–9

    Article  CAS  Google Scholar 

  115. Liu Y, Wang M, Zhao F, Guo Z, Chen H, Dong S (2005) Direct electron transfer and electrocatalysis of microperoxidase immobilised on nanohybrid film. J Electroanal Chem 581:1–10

    Article  CAS  Google Scholar 

  116. Yarman A, Nagel T, Gajovic-Eichelmann N, Fischer A, Wollenberger U, Scheller FW (2011) Bioelectrocatalysis by microperoxidase-11 in a multilayer architecture of chitosan embedded gold nanoparticles. Electroanalysis 23:611–618

    CAS  Google Scholar 

  117. Narvaez A, Dominguez E, Katakis I, Katz E, Ranjit KT, Ben-Dov I, Willner I (1997) Microperoxidase-11-mediated reduction of hemoproteins: electrocatalysed reduction of cytochrome c, myoglobin and hemoglobin and electrocatalytic reduction of nitrate in the presence of cytochrome-dependent nitrate reductase. J Electroanal Chem 430:227–233

    Article  CAS  Google Scholar 

  118. Katz E, Heleg-Shabtai V, Bardea A, Willner I, Rau HK, Haehnel W (1998) Fully integrated biocatalytic electrodes based on bioaffinity interactions. Biosens Bioelectron 13:741–756

    Article  CAS  Google Scholar 

  119. Mabrouk PA (1995) First direct interfacial electron transfer between a biomolecule and a solid electrode in non-aqueous media: direct electrochemistry of microperoxidase-11 at glassy carbon in dimethyl sulfoxide solution. Anal Chim Acta 307:245–251

    Article  CAS  Google Scholar 

  120. Moore ANJ, Katz E, Willner I (1996) Electrocatalytic reduction of organic peroxides in organic solvents by microperoxidase-11 immobilised as a monolayer on a gold electrode. J Electroanal Chem 417:189–192

    Article  CAS  Google Scholar 

  121. Katz E, Filanovsky B, Willner I (1999) A biofuel cell based on two immiscible solvents and glucose oxidase and microperoxidase-11 monolayer-functionalized electrodes. New J Chem 23:481–487

    Article  CAS  Google Scholar 

  122. Ramanavicius A, Kausaite A, Ramanaviciene A (2008) Enzymatic biofuelcell based on anode and cathode powered by ethanol. Biosens Bioelectron 24:761–766

    Article  CAS  Google Scholar 

  123. Katz E, Willner I (1996) Amperometric amplification of antigen–antibody association at monolayer interfacess: design of immunosensor. J Electroanal Chem 418:67–72

    Article  CAS  Google Scholar 

  124. Abdelwahab AA, Koh WCA, Noh H-B, Shim Y-B (2010) A selective nitric oxide nanocomposite biosensor based on direct electron transfer of microperoxidase: removal of interferences by co-immobilised enzymes. Biosens Bioelectron 91:35–45

    Google Scholar 

  125. Wollenberger U, Lisdat F, Rose A, Streffer K (2008) In: Bartlett P (ed) Bioelectrochemistry: fundamentals, experimental techniques and applications. Wiley, New York, pp 219–248

  126. Wollenberger U, Neumann B (1997) Quinoprotein glucose dehydrogenase modified carbon paste electrode for the detection of phenolic compounds. Electroanalysis 9:366–371

    Article  CAS  Google Scholar 

  127. Mie Y, Kowata K, Hirano Y, Niwa O, Mizutani F (2008) Comparison of enzymatic recycling electrodes for measuring aminophenol: development of a highly sensitive natriuretic peptide assay system. Anal Sci 24:577–582

    Article  CAS  Google Scholar 

  128. Solná R, Skládal P (2005) Amperometric flow-injection determination of phenolic compounds using a biosensor with immobilised laccase, peroxidase and tyrosinase. Electroanalysis 17:2137–2146

    Article  CAS  Google Scholar 

  129. Haghighi B, Gorton L, Ruzgas T, Jönsson LJ (2003) Characterization of graphite electrodes modified with laccase from Trametes versicolor and their use for bioelectrochemical monitoring of phenolic compounds in flow injection analysis. Anal Chim Acta 487:3–14

    Article  CAS  Google Scholar 

  130. Munteanu FD, Lindgren A, Emnéus J, Gorton L, Ruzgas T, Csöregi E, Ciucu A, Van Huystee RB, Gazaryan IG, Lagrimini LM (1998) Bioelectrochemical monitoring of phenols and aromatic amines in flow injection using novel plant peroxidases. Anal Chem 70:2596–2600

    Article  CAS  Google Scholar 

  131. Scheller F, Schubert F (1992) In: Techniques and instrumentation in analytical chemistry: biosensors, vol 11. Elsevier, Amsterdam, pp 53–56

  132. O’Donoghue D, Magner E (2007) The electrochemical response of microperoxidase in non-aqueous solvents. Electrochim Acta 53:1134–1139

    Article  CAS  Google Scholar 

  133. Sartori LR, Santos WR, Kubota LT, Segatelli MG, Tarley CRT (2010) Flow-based method for epinephrine determination using a solid reactor based on molecularly imprinted poly(FePP–MAA–EGDMA). Mater Sci Eng C 31:114–119

    Article  CAS  Google Scholar 

  134. Kazlauskaite J, Westlake ACG, Wong L-L, Hill HAO (1996) Direct electrochemistry of cytochrome P40cam. Chem Commun 1996:2189–2190

    Article  Google Scholar 

  135. Fantuzzi A, Fairhead M, Gilardi G (2004) Direct electrochemistry of immobilised human cytochrome CYP2E1. J Am Chem Soc 126:5040–5041

    Article  CAS  Google Scholar 

  136. Iwuoha EI, Joseph S, Zhang Z, Smyth MR, Fuhr U, Ortiz de Montellano PR (1998) Drug metabolism biosensors: electrochemical reactivities of cytochrome CYP101 immobilised in synthetic vesicular systems. J Pharm Biom Anal 17:1101–1110

    Article  CAS  Google Scholar 

  137. Zhang Z, Nassar A-EF, Lu Z, Schenkman JB, Rusling JF (1997) Direct electron injection from electrodes to cytochrome CYP101 in biomembrane-like films. J Chem Soc Faraday Trans 93:1769–1774

    Article  CAS  Google Scholar 

  138. Iwuoha EI, Wilson A, Howel M, Mathebe NGR, Montane-Jaime K, Narinesingh D, Gueseppi-Elie A (2004) Cytochrome P-4502D6 (CYP2D6) bioelectrode for fluoxetine. Anal Lett 37:929–941

    Article  CAS  Google Scholar 

  139. Matsumura H, Wiwatchaiwong S, Nakamura N, Yohda M, Ohno H (2006) A novel method for direct electrochemistry of a thermoacidophilic cytochrome P450. Electrochem Commun 8:1245–1249

    Article  CAS  Google Scholar 

  140. Matsumura H, Nakamura N, Yohda M, Ohno H (2007) The electrochemical properties of thermophilic cytochrome. P450 CYP119A2 at extremely high temperatures in poly(ethylene oxide). Electrochem Commun 9:361–364

    Article  CAS  Google Scholar 

  141. Shumyantseva VV, Bulko TV, Rudakov YO, Kuznetsova GP, Samenkova NF, Lisitsa AV, Karuzina IT, Archakov AI (2007) Electrochemical properties of cytochroms P450 using nanostructured electrodes: direct electron transfer and electro catalysis. J Inorg Biochem 101:859–865

    Article  CAS  Google Scholar 

  142. Shumyantseva VV, Bulko TV, Kumetsova GP, Lisitsa AV, Ponomarenko EA, Karuzina II, Archakov AI (2007) Electrochemical reduction of sterol-14 alpha-demethylase from Mycobacterium tuberculosis (CYP51b1). Biochem Mosc 72:658–663

    Article  CAS  Google Scholar 

  143. Liu SQ, Peng L, Yang XD, Wu YF, He L (2008) Electrochemistry of cytochrome P450 enzyme on nanoparticle-containing membrane-coated electrode and its applications for drug sensing. Anal Biochem 375:209–216

    Article  CAS  Google Scholar 

  144. Peng L, Yang X, Zhang Q, Liu S (2008) Electrochemistry of cytochrome P4502B6 on electrodes modified with zirconium dioxide nanoparticles and platin components. Electroanalysis 20:803–807

    Article  CAS  Google Scholar 

  145. Yang ML, Kabulski JL, Wollenberg L, Chen XQ, Subramanian M, Tracy TS, Lederman D, Gannett PM, Wu N (2009) Electrocatalytic drug metabolism by CYP2C9 bonded to a self-assembled monolayer-modified electrode. Drug Metab Dispos 37:892–899

    Article  CAS  Google Scholar 

  146. Rhieu SY, Ludwig DR, Siu VS, Palmore GTR (2009) Direct electrochemistry of cytochrome P450 27B1 in surfactant films. Electrochem Commun 11:1857–1860

    Article  CAS  Google Scholar 

  147. Mie Y, Ikegami M, Komatsu Y (2010) Gold sputtered electrode surfaces enhance direct electron transfer reactions of human cytochrome P450s. Electrochem Commun 12:680–683

    Article  CAS  Google Scholar 

  148. Mak LH, Sadeghi SJ, Fantuzzi A, Gilardi G (2010) Control of human cytochrome P450 2E1 electrocatalytic response as a result of unique orientation on gold electrodes. Anal Chem 82:5357–5362

    Article  CAS  Google Scholar 

  149. Fantuzzi A, Capria E, Mak LH, Dodhia VR, Sadeghi SJ, Collins S, Somers G, Hug E, Gilardi G (2010) An electrochemical microfluidic platform for human P450 drug metabolism profiling. Anal Chem 82:10222–10227

    Article  CAS  Google Scholar 

  150. Lvov YM, Lu Z, Schenkman JB, Zu X, Rusling JF (1998) Direct electrochemistry of myoglobin and cytochrome CYP101 in alternate layer-by-layer films with DNA and other polyions. J Am Chem Soc 120:4073–4080

    Article  CAS  Google Scholar 

  151. Munge B, Estavillo C, Schenkman JB, Rusling JF (2003) Optimization of electrochemical and peroxide-driven oxidation of styrene with ultrathin polyion films containing cytochrome CYP101 and myoglobin. Chem Biol Biological Chem 4:82–89

    CAS  Google Scholar 

  152. Rusling JF, Zhou L, Munge B, Yang J, Estavillo C, Schenkmann JB (2000) Applications of polyion filmss containing biomolecules to sensing toxicity. Faraday Discuss 116:1–11

    Article  Google Scholar 

  153. Zu X, Lu Z, Zhang Z, Schenkman JB, Rusling JF (1999) Electroenzyme-catalysed oxidation of styrene and cis-β-methylstyrene using thin films of cytochrome CYP101 and myoglobin. Langmuir 15:7372–7377

    Article  CAS  Google Scholar 

  154. Joseph S, Rusling JF, Lvov YM, Fredberg T, Fuhr U (2003) An amperometric biosensor with human CYP3A4 as a novel drug screening tool. Biochem Pharmacol 65:1817–1826

    CAS  Google Scholar 

  155. Reipa V, Mayhew MP, Holden MJ, Vilker VL (2002) Redox control of the CYP101 catalytic cycle: effects of Y96F active site mutations and binding of a non-natural substrate. Chem Commun 4:318–319

    Google Scholar 

  156. Faulkner KM, Shet MS, Fisher CW, Eastbrook RW (1995) Electrocatalytically driven w-hydroxylation of fatty acids using cytochrome CYP 4A1. Proc Nat Acad Science USA 92:7705–7709

    Article  CAS  Google Scholar 

  157. Shumyantseva VV, Bulko TV, Usanov SA, Schmid RD, Nicolini C, Archakov AI (2001) Construction and characterization of bioelectrocatalytic sensors based on cytochromes P450. J Inorg Biochem 87:185–190

    Article  CAS  Google Scholar 

  158. Nazor J, Dannenmann S, Adjei RO, Fordjour YB, Ghampson IT, Blanusa M, Roccatano D, Schwaneberg U (2008) Laboratory evolution of P450BM3 for mediated electron transfer yielding an activity-improved and reductase independent variant. Protein Eng Des Sel 21:29–35

    Article  CAS  Google Scholar 

  159. Nouri-Nigjeh E, Permentier HP, Bischoff R, Bruins AP (2010) Lidocaine oxidation by electrogenerated reactive oxygen species in the light of oxidative drug metabolism. Anal Chem 82:7625–7633

    Article  CAS  Google Scholar 

  160. Reipa V, Mayhew MP, Vilker VL (1997) A direct electrode-driven CYP cycle for biocatalysis. Proc Nat Acad Science USA 94:13554–13558

    Article  CAS  Google Scholar 

  161. Mayhew MP, Reipa V, Holden MJ, Vilker VL (2000) Improving the cytochrome CYP enzyme for electrode-driven biocatalysis of styrene epoxidation. Biotech Prog 16:610–616

    Article  CAS  Google Scholar 

  162. Dodhia VR, Sassone C, Fantuzzi A, Di Nardo G, Sadeghi SJ, Gilardi G (2008) Modulating the coupling efficiency of human cytochrome P450 CYP3A4 at electrode surfaces through protein engineering. Electro Chem 10:1744–1747

    Article  CAS  Google Scholar 

  163. Krishnan S, Wasalathanthri D, Zhao LL, Schenkman JB, Rusling JF (2011) Efficient bioelectronic actuation of the natural catalytic pathway of human metabolic cytochrome P450s. JACS 133:1459–1465

    Article  CAS  Google Scholar 

  164. Panicco P, Dodhia VR, Fantuzzi A, Gilardi G (2011) Enzyme-based amperometric platform to determine the polymorphic response in drug metabolism by cytochromes P450. Anal Chem 83:2179–2186

    Article  CAS  Google Scholar 

  165. Makings LR, Zlokarnik G (2000) Aurora Biosciences Corporation, San Diego, CA, USA

  166. Hara M, Yasuda Y, Toyotama H, Ohkawa H, Nozawa T, Miyake J (2002) A novel isfet-type biosensor based on P-450 monooxygenases. Biosens Bioelectron 17:173–179

    Article  CAS  Google Scholar 

  167. Zhou Y, Liu S, Jiang H-J, Yang H, Chen HY (2010) Direct electrochemistry and bioelectrocatalysis of microperoxidase-11 immobilised on chitosan–graphene nanocomposite. Electroanalysis 22:1323–1328

    Article  CAS  Google Scholar 

  168. Liu Y, Offenhäuser A, Meyer D (2010) Electrochemical current rectification at bio-functionalized electrodes. Bioelectrochemistry 77:89–93

    Article  CAS  Google Scholar 

  169. Zhu X, Yuri I, Gan X, Suzuki I, Li G (2007) Electrochemical study of the effect of nano-zinc oxide on microperoxidase and its application to more sensitive hydrogen peroxide biosensor preparation. Biosens Bioelectron 22:1600–1604

    Article  CAS  Google Scholar 

  170. Razumas V, Kazlauskaitė J, Vidžiūnaitė R (1996) Electrocatalytic reduction of hydrogen peroxide on the microperoxidase-11 modified carbon paste and graphite electrodes. Bioelectrochem Bioenerg 39:139–143

    Article  CAS  Google Scholar 

  171. Youssoufi-Korri H, Desbenoit N, Ricoux R, Mahy JP, Lecomte S (2008) Eleboration of a new hydrogen peroxide biosensor using microperoxidase 8 (MP8) immobilised on a polypyyrole coated electrode. Mat Sci Eng C 28:855–860

    Article  CAS  Google Scholar 

  172. Huang W, Jia J, Zhang Z, Han X, Tang J, Wang J, Dong S, Wang E (2003) Hydrogen peroxide biosensor based on microperoxidase-11 entrapped in lipid membrane. Biosens Bioelectron 18:1225–1230

    Article  CAS  Google Scholar 

  173. Cipriano TC, Takahashi PM, de Lima D, Oliveira VX, Souza JA, Martinho H, Alves WA (2010) Spatial organization of peptide nanotubes for electrochemical devices. J Mater Sci 45:5101–5108

    Article  CAS  Google Scholar 

  174. Csöregi E, Jönsson-Petterson G, Gorton L (1993) Mediatorless electrocatalytic reduction of hydrogen peroxide at graphite electrodes chemically modified with peroxidases. J Biotechnol 30:315–337

    Article  Google Scholar 

  175. Scheller FW, Schubert F, Renneberg R, Jänchen M, Weise H (1985) Bioesensors: trends and commercialization. Biosensors 1:135–160

    Article  CAS  Google Scholar 

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Acknowledgements

The authors gratefully acknowledge the financial support of BMBF (0311993) of Germany. This work is a part of UniCat, the Cluster of Excellence in the field of catalysis coordinated by TU Berlin and financially supported by Deutsche Forschungsgemeinschaft (DFG) within the framework of the German Excellence Initiative (EXC 314).

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Authors and Affiliations

  1. Fraunhofer Institute for Biomedical Engineering IBMT, 14476, Potsdam, Germany

    Aysu Yarman, Amay Bandodkar, Nenad Gajovic-Eichelmann & Frieder W. Scheller

  2. Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24-25, 14476, Potsdam, Germany

    Lei Peng, Yunhua Wu, Ulla Wollenberger & Frieder W. Scheller

  3. Unit of Environmental Biotechnology, International Graduate School of Zittau, 0276, Zittau, Germany

    Martin Hofrichter & René Ullrich

  4. Department of Biotechnology, Lausitz University of Applied Sciences, Senftenberg, Germany

    Katrin Scheibner

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  1. Aysu Yarman
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Correspondence to Frieder W. Scheller.

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This review paper is dedicated to Reinhard Renneberg on the occasion of his 60th birthday.

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Yarman, A., Peng, L., Wu, Y. et al. Can peroxygenase and microperoxidase substitute cytochrome P450 in biosensors. Bioanal Rev 3, 67–94 (2011). https://doi.org/10.1007/s12566-011-0023-4

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