Features and applications of bilirubin oxidases

Applied Microbiology and Biotechnology

Volumn 96, Issue 2, 2012, Pages 301-307

  Mano, Nicolas ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Bilirubin detection; Bilirubin oxidases; Biofuel cells; Decolorization of dyes; Mutlicopper oxidases; Oxygen reduction

Indexed keywords

ACID MEDIA; BILIRUBIN OXIDASE; BIOCHEMICAL PROPERTIES; CHLORIDE ANIONS; DEPOLLUTION; HIGH ACTIVITY; HIGH THERMAL; LACCASES; MULTICOPPER OXIDASE; MUTLICOPPER OXIDASES; NEUTRAL PH; OXYGEN REDUCTION; PH CONDITION; PULP BLEACHING;

CHLORINE COMPOUNDS; ELECTROLYTIC REDUCTION; HEALTH CARE; POLLUTION CONTROL;

BIOLOGICAL FUEL CELLS;

BILIRUBIN OXIDASE; BIOFUEL; CHELATING AGENT; LACCASE; OXIDOREDUCTASE; OXYGEN; UNCLASSIFIED DRUG;

BIOCHEMICAL OXYGEN DEMAND; BIOFUEL; CATALYSIS; COPPER; DATA SET; ENZYME ACTIVITY; ION; OXIDATION; OXYGEN; PH; TEMPERATURE TOLERANCE;

AMINO ACID SEQUENCE; BIOSENSOR; BIOTECHNOLOGY; BLEACHING; CHEMICAL ANALYSIS; DECOLORIZATION; HEALTH CARE; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PH MEASUREMENT; PULP MILL; REVIEW;

BACTERIA; BACTERIAL PROTEINS; BIODEGRADATION, ENVIRONMENTAL; BIOELECTRIC ENERGY SOURCES; BIOTECHNOLOGY; FUNGAL PROTEINS; FUNGI; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS;

EID: 84866514236     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-012-4312-9     Document Type: Review

References (89)

1. Ackermann Y, Guschin DA, Eckhard K, Shleev S, Schuhmann W (2010) Design of a bioelectrocatalytic electrode interface for oxygen reduction in biofuel cells based on a specifically adapted Os-complex containing redox polymer with entrapped Trametes hirsuta laccase. Electrochem Commun 12(5):640-643
2. Artiss JD, McEnroe RJ, Zak B (1984) Bilirubin interference in a peroxidase-coupled procedure for creatinine eliminated by bilirubin oxidase. Clin Chem 30(8):1389-1392 (Pubitemid 15087803)
3. Barriere F, Kavanagh P, Leech D (2006) A laccase-glucose oxidase biofuel cell prototype operating in a physiological conditions. Electrochim Acta 51:5187-5192 (Pubitemid 43927722)
4. Barton SC, Pickard M, Vasquez-Duhalf R, Heller A (2002) Electroreduction of O2 to water at 0.6V (SHE) at pH 7 on the 'wired' Pleurotus ostreatus laccase cathode. Biosens. Bioelec. 17(11-12): 1071-1074 (Pubitemid 35232480)
5. Barton SC, Gallaway J, Atanassov P (2004) Enzymatic biofuel cells for implantable and microscale devices. Chem Rev 104:4867-4886
6. Boland S, Leech D (2012) A glucose/oxygen enzymatic fuel cell based on redox polymer and enzyme immobilisation at highly-ordered macroporous gold electrodes. Analyst 137(1):113-117
7. Brissos V, Pereira L, Munteanu FD, Cavaco-Paulo A, Martins LO (2009) Expression system of CotA-laccase for directed evolution and high-throughput screenings for the oxidation of high-redox potential dyes. Biotechnol J 4(4):558-563
8. Cracknell JA, McNamara TP, Lowe ED, Blanford CF (2011) Bilirubin oxidase from Myrothecium verrucaria: X-ray determination of the complete crystal structure and a rational surface modification for enhanced electrocatalytic O2 reduction. Dalton Trans 40 (25):6668-6675
9. Dos Santos L, Climent V, Blanford CF, Armstrong FA (2010) Mechanistic studies of the 'blue' Cu enzyme, bilirubin oxidase, as a highly efficient electrocatalyst for the oxygen reduction reaction. Phys Chem Chem Phys 12(42):13962-13974
10. Doumas BT, Perry B, Jendrzejczak B, Davis L (1987) Measurement of direct bilirubin by use of bilirubin oxidase. Clin Chem 33 (8):1349-1353 (Pubitemid 18041968)
11. Doumas BT, Yein F, Perry B, Jendrzejczak B, Kessner A (1999) Determination of the sum of bilirubin sugar conjugates in plasma by bilirubin oxidase. Clin Chem 45(8):1255-1260 (Pubitemid 29424265)
12. Durand F, Gounel S, Kjaergaard C, Solomon E, Mano N (2012a) Bilirubin oxidase from Magnaporthe oryzae: An attractive enzyme for biotechnological application. Appl Microbiol Biotechnol. doi:10.1007/s00253-012-3926-2
13. Durand F, Kjaergaard CH, Suraniti E, Gounel S, Hadt RG, Solomon EI, Mano N (2012b) Bilirubin oxidase from Bacillus pumilus: A promising enzyme for the elaboration of efficient cathodes in biofuel cells. Biosens Bioelectron 35(1):140-146
14. Durao P, Chen Z, Fernandes AT, Hildebrandt P,Murgida DH, Todorovic S, Pereira MM, Melo EP, Martins LO (2008) Copper incorporation into recombinant CotA laccase from Bacillus subtilis: Characterization of fully copper loaded enzymes. J Biol Inorg Chem 13(2):183-193 (Pubitemid 351172176)
15. Edembe L, Gounel S, Cadet M, Durand F, Mano N (2012) A highly efficient O2 cathode based on bilirubin oxidase from Bacillus pumilus operating in serum. Electrochem Commun: 10.1016/j.elecom.2012.1007.1013
16. Falk M, Andoralov V, Blum Z, Sotres J, Suyatin DB, Ruzgas T, Arnebrant T, Shleev S (2012) Biofuel cell as a power source for electronic contact lenses. Biosens Bioelectron 37:38-45
17. Fortuney A, Guibault GG (1996) Enzyme electrode for the determination of bilirubin. Electroanalysis 8(3):229-232 (Pubitemid 126419515)
18. Fu Y, Viraraghavan T (2001) Fungal decolorization of dye wastewaters: A review. Bioresour Technol 79:251-262 (Pubitemid 32633765)
19. Gallaway J, Wheeldon I, Rincon R, Atanassov P, Banta S, Barton SC (2008) Oxygen-reducing enzyme cathodes produced from SLAC, a small laccase from Streptomyces coelicolor. Biosens Bioelectron 23:1229-1235
20. Gao F, Viry L, Maugey M, Poulin P, Mano N (2010) Engineering hybrid nanotube wires for high-power biofuel cells. Nat Commun 1(1): 10.1038/ncomms1000
21. Goldfinch ME, Maguire GA (1988) Investigation of the use of bilirubin oxidase to measure the apparent unbound bilirubin concentration in human plasma. Ann Clin Biochem 25(Pt 1):73-77
22. Guo J, Liang XX, Mo PS, Li GX (1991) Purification and properties of bilirubin oxidase from Myrothecium verrucaria. Appl Biochem Biotechnol 31(2):135-143
23. Gupta S, Lau C, Rajendran A, Colon F, Branch B, Ivnitski D, Atanassov P (2011) Direct electron transfer catalyzed by bilirubin oxidase for air breathing gas-diffusion electrodes. Electrochem Comm 13:247-249
24. Halamkova L, Halamek J, Bocharova V, Szczupak A, Alfonta L, Katz E (2012) Implanted biofuel cell in a living snail. J Am Chem Soc 134:5040-5043
25. Hilden K, Hakala TK, Lundell T (2009) Thermotolerant and thermostable laccases. Biotechnol Lett 31(8):1117-1128
26. Hiromi K, Yamaguchi S, Sugiura Y, Iwamoto H, Hirose J (1992) Bilirubin oxidase from Trachyderma tsunodae K-2593, a multicopper enzyme. Biosci Biotech Biochem 56:1349-1350
27. Kamitaka Y, Tsujimura S, Kataoka K, Sakurai T, Ikeda T, Kano K (2007a) Effects of axial ligand mutation of the type I copper site in bilirubin oxidase on direct electron transfer type bioelectrocatalytic reduction of oxygen. J Electroanal Chem 601:119-124 (Pubitemid 46330313)
28. Kamitaka Y, Tsujimura S, Setoyama N, Kajino T, Kano K (2007b) Fructose/dioxygen biofuel cell based on direct electron transfertype bioelectrocatalysis. Phys Chem Chem Phys 9(15):1793-1801
29. Karaskiewicz M, Nazruk E, Zelechowska K, Biernat JF, Rogalski J, Bilewicz R (2012) Fully enzymatic mediatorless fuel cell with efficient naphtylated cabon nanotube-laccases composites cathodes. Electrochem Commun 20:124-127
30. Kataoka K, Kitagawa R, Inoue M, Naruse D, Sakurai T, Huang HW (2005a) Point mutations at the type I Cu ligands, Cys457 and Met467, and at the putative proton donor, Asp105, in Myrothecium verrucaria bilirubin oxidase and reactions with dioxygen. Biochemistry 44(18):7004-7012 (Pubitemid 40632418)
31. Kataoka K, Tanaka K, Sakai Y, Sakurai T (2005b) High-level expression of Myrothecium verrucaria bilirubin oxidase in Pichia pastoris, and its facile purification and characterization. Protein Expr Purif 41(1):77-83 (Pubitemid 40406366)
32. Kirihigashi K, Tatsumi N, Hino M, Yamane T, Ohta K (2000) Basic and clinical evaluation of a newly-developed enzymatic bilirubin assay. Osaka City Med J 46(1):55-70
33. Kirk JM (2008) Neonatal jaundice: A critical review of the role and practice of bilirubin analysis. Ann Clin Biochem 45:452-462
34. Kjaergaard CH, Durand F, Tasca F, Qayyum MF, Kauffmann B, Gounel S, Suraniti E, Hodgson KO, Hedman B, Mano N, Solomon EI (2012) Spectroscopic and crystallographic characterization of "alternative resting" and "resting oxidized" enzyme forms of bilirubin oxidase: Implications for activity and electrochemical behavior of multicopper oxidases. J Am Chem Soc 134(12):5548-5551
35. Klemm J, Prodromidis MI, Karayannis MI (2000) An enzymatic method for the determination of bilirubin using an oxygen electrode. Electroanalysis 12(4):292-295
36. Koikeda S, Ando K, Kaji H, Inoue T, Murao S, Takeuchi K, Samejima T (1993) Molecular cloning of the gene for bilirubin oxidase from Myrothecium verrucaria and its expression in yeast. J Biol Chem 268(25):18801-18809 (Pubitemid 23273825)
37. Kosaka A, Yamamoto A, Morishita Y, Nakane K (1987) Enzymatic determination of bilirubin fractions in serum. Clin Biochem 20:451-458 (Pubitemid 18035418)
38. Koschorreck K, Richter SM, Ene AB, Roduner E, Schmid RD, Urlacher VB (2008) Cloning and characterization of a new laccase from Bacillus licheniformis catalyzing dimerization of phenolic acids. Appl Microbiol Biotechnol 79(2):217-224
39. Kurosakaa K, Senbaa S, Tsubotab T, Kondoa H (1998) A new enzymatic assay for selectively measuring conjugated bilirubin concentration in serum with use of bilirubin oxidase. Clinica Chimica Acta 269:125-136
40. Leech D, Kavanagh P, Schuhmann W (2012) Enzymatic fuel cells: Recent progress. Electrochim. Acta. http://dx.doi.org/10.1016/j.electacta.2012.02.087
41. Liu Y, Huang J, Zhang X (2009) Decolorization and biodegradation of remazol brilliant blue R by bilirubin oxidase. J Biosci Bioeng 108 (6):496-500
42. Mano N, Kim HH, Zhang Y, Heller A (2002) An oxygen cathode operating in a physiological solution. J Am Chem Soc 124:6480-6486 (Pubitemid 34579400)
43. Mano N, Fernandez JL, Kim Y, Shin W, Bard AJ, Heller A (2003) Oxygen is electroreduced to water on a "wired" enzyme electrode at a lesser overpotential than on platinum. J Am Chem Soc 125:15290-15291 (Pubitemid 37532162)
44. Mano N, Soukharev VS, Heller A (2006) A laccase-wiring redox hydrogel for efficient catalysis of O2 electroreduction. J Phys Chem B 110:11180-11187 (Pubitemid 43999478)
45. Masuda-Nishimura I, Ichikawa K, Hatamoto O, Abe K, Koyama Y (1999) cDNA cloning of bilirubin oxidase from Pleurotus ostreatus strain Shinshu and its expression in Aspergillus sojae: An efficient screening of transformants, using the laccase activity of bilirubin oxidase. J Gen Appl Microbiol 45:93-97 (Pubitemid 29408233)
46. Mayer AM, Staples RC (2002) Laccase: New functions for an old enzyme. Phytochemistry 60(6):551-565 (Pubitemid 34832184)
47. Million CJ, Klibanov AM, Langer R (1988) Kinetics of bilirubin oxidase and modeling of an immobilized bilirubin oxidase reactor for bilirubin detoxification. Biotechnol Bioeng 31(6):536-546 (Pubitemid 18594974)
48. Mizutani K, Toyoda M, Sagara K, Takahashi N, Sato A, Kamitaka Y, Tsujimura S, Nakanishi Y, Sugiura T, Yamaguchi S, Kano K, Mikami B (2010) X-ray analysis of bilirubin oxidase from Myrothecium verrucaria at 2.3 A resolution using a twinned crystal. Acta Crystallogr Sect F Struct Biol Cryst Commun 66(Pt 7):765-770
49. Mohammadian M, Fathi-Roudsari M, Mollania N, Badoei-Dalfard A, Kjhajed K (2010) Enhanced expression of a recombinant bacterial laccase at low temperature and microaerobic conditions: Purification and biochemical characterization. J Ind Microbiol Biotechnol 37:863-869
50. Mullon CJ, Langer R (1987) Determination of conjugated and total bilirubin in serum of neonates, with use of bilirubin oxidase. Clin Chem 33(10):1822-1825 (Pubitemid 19097553)
51. Mullon CJ, Tosone CM, Langer R (1989) Simulation of bilirubin detoxification in the newborn using an extracorporeal bilirubin oxidase reactor. Pediatr Res 26(5):452-457 (Pubitemid 19267296)
52. Murao S, Tanaka N (1981) A new enzyme "bilirubin oxidase" produced by Myrothecium verrucaria MT-1. Agric Biol Chem 45:2383-2384
53. Murao S, Tanaka N (1982) Isolation and identification of a microorganism producing bilirubin oxidase. Agric Biol Chem 46 (8):2031-2034
54. Nakamura H, Lee Y (1977) Microdetermination of unbound bilirubin in icteric newborn sera: An enzymatic method employing peroxidase and glucose oxidase. Clin Chim Acta 79(2):411-417 (Pubitemid 8168487)
55. Pereira L, Coelho AV, Viegas CA, Santos MM, Robalo MP, Martins LO (2009) Enzymatic biotransformation of the azo dye Sudan Orange G with bacterial CotA-laccase. J Biotechnol 139(1):68-77
56. Perry B, Doumas BT, Buffone G, Glick M, Ou CN, Ryder K (1986) Measurement of total bilirubin by use of bilirubin oxidase. Clin Chem 32(2):329-332 (Pubitemid 17025651)
57. Ramirez P, Mano N, Andreu R, Ruzgas T, Heller A, Gorton L, Shleev S (2008) Direct electron transfer from graphite and functionalized gold electrodes to T1 and T2/T3 copper centers of bilirubin oxidase. Biochim Biophys Acta 1777:1364-1369
58. Rasmussen M, Ritzmann RE, Lee I, Pollack AJ, Scherson D (2012) An implantable biofuel cell for a live insect. J Am Chem Soc 134 (3):1458-1460
59. Robinson T, McMullan G, Marchant R, Nigam P (2001) Remediation of dyes in textile effluent: A critical review on current treatment technologies with a proposed alternative. Bioresour Technol 77:247-255 (Pubitemid 32015869)
60. Rowinski P, Bilewicz R, Stebe MJ, Rogalska EE (2004) Electrodes modified with monoolein cubic phases hosting laccases for the catalytic reduction of dioxygen. Anal Chem 76(2):283-291 (Pubitemid 38090763)
61. Sakasegawa S, Ishikawa H, Imamura S, Sakuraba H, Goda S, Ohshima T (2006) Bilirubin oxidase activity of Bacillus subtilis CotA. Appl Environ Microbiol 72(1):972-975
62. Sakurai T, Kataoka K (2007) Basic and applied features of multicopper oxidases, CueO, bilirubin oxidase, and laccase. Chem Rec 7 (4):220-229
63. Sakurai T, Zhan L, Fujita T, Kataoka K, Shimizu A, Samejima T, Yamakguchi S (2003) Autenthic and recombinant bilirubin oxidases are in different resting forms. Biosci Biotechnol Biochem 67(5):1157-1159 (Pubitemid 39251881)
64. Salaj-Kosla U, Poller S, Beyl Y, Scanlon MD, Belochapkin S, Shleev S, Schuhmann W, Magner E (2012) Direct electron transfer of bilirubin oxidase (Myrothecium verrucaria) at an unmodified nanopoorus gold biocathode. Electrochem Comm 16:92-95
65. Satomura S, Miki Y, Hamanaka T, Sakata Y (1985) Kinetic assay of gamma-glutamyltransferase with use of bilirubin oxidase as a coupled enzyme. Clin Chem 31(8):1380-1383 (Pubitemid 16041938)
66. Seki Y, Takeguchi M, Okura I (1996) Purification and properties of bilirubin oxidase from Penicillium janthinellum. J Biotechnol 46:145-151 (Pubitemid 26178180)
67. Shimizu A, Kwon JH, Sasaki T, Satoh T, Sakurai N, Sakurai T, Yamaguchi S, Samejima T (1999a) Myrothecium verrucaria bilirubin oxidase and its mutants for potential copper ligands. Biochemistry 38(10):3034-3042
68. Shimizu A, Sasaki T, Kwon JH, Odaka A, Satoh T, Sakurai N, Sakurai T, Yamaguchi S, Samejima T (1999b) Site-directed mutagenesis of a possible type 1 copper ligand of bilirubin oxidase; a Met467Gln mutant shows stellacyanin-like properties. J Biochem 125(4):662-668 (Pubitemid 29192485)
69. Shimizu A, Samejima T, Hirota S, Yamaguchi S, Sakurai N, Sakurai T (2003) Type III Cu mutants of Myrothecium verrucaria bilirubin oxidase. J Biochem 133(6):767-772 (Pubitemid 36898648)
70. Shleev S, Nikitina O, Christenson A, Reimann CT, Yaropolov AI, Ruzgas T, Gorton L (2007) Characterization of two new multiforms of Trametes pubescens laccase. Bioorg Chem 35 (1):35-49 (Pubitemid 46108993)
71. Shleev S, Andoralov V, Falk M, Reimann CT, Ruzgas T, Srnec M, Ryde U, Rulisek L (2012) On the possibility of uphill intramolecular electron transfer in multicopper oxidases: Electrochemical and quantum chemical study of bilirubin oxidase. Electroanalysis 24:1524-1540
72. Solomon EI, Sundaram UM, Machonkin TE (1996) Multicopper oxidases and oxygenases. Chem Rev 96:2563-2605 (Pubitemid 126641113)
73. Solomon EI, Chen P, Metz M, Lee SK, Palmer AE (2001) Oxygen binding, activation, and reduction to water by copper proteins. Angew Chem Int Ed Engl 40(24):4570-4590 (Pubitemid 34032186)
74. Soltys PJ, Mullon C, Langer R (1992) Oral treatment for jaundice using immobilized bilirubin oxidase. Artif Organs 16(4):331-335
75. Suraniti E, Abintou M, Durand F, Mano N (2012) Heat and drying time modulate the O2 reduction current of modified glassy carbon electrodes with bilirubin oxidases. Bioelectrochemistry 88:65-69
76. Takeguchi M, Seki Y, Murao S, Shin T, Okura I (1995) On the molecular weight of bilirubin oxidase from Penicillum janthinellum. J Mol Cat A: Chemical 97:L3-L5
77. Tanaka N,Murao S (1981) A new enzyme bilirubin oxidase produced by Myrothecium verrucaria MT-1. Agric Biol Chem 45:2383-2384
78. Tanaka N, Murao S (1985) Reaction of bilirubin oxidase produced by Myrothecium verrucaria MT-1. Agric Biol Chem 49:843-844
79. Tarasevich M, Yaropolov A, Bogdanovskaya VA, Varfolomeev S (1979) Electrocatalysis of a cathodic oxygen reduction by laccase J. Electroanal Chem 104:393-403
80. Tasca F, Gorton L, Kujawa M, Patel I, Harreither W, Peterbauer CK, Ludwig R, Noll G (2010) Increasing the coulombic efficiency of glucose biofuel cell anodes by combination of redox enzymes. Biosens Bioelectron 25(7):1710-1716
81. Tsujimura S, Tatsumi H, Ogawa J, Shimizu S, Kano K, Ikeda T (2001) Bioelectrocatalytic reduction of dioxygen to water at neutral pH using bilirubin oxidase as an enzyme and 2,2'-azinobis(3-ethylbenzothiazolin-6-silfonate) as an electron transfer mediator. J Electroanal Chem 496:69-75 (Pubitemid 32195695)
82. Tsujimura S, Nakagawa T, Kano K, Ikeda T (2004) Kinetic study of direct bioelectrocatalysis of dioxygen reduction with bilirubin oxidase at carbon electrodes. Electrochemistry 72(6):437-439
83. Wang X, Falk M, Ortiz R, Matsumura H, Bobacka J, Ludwig R, Bergelin M, Gorton L, Shleev S (2012) Mediatorless sugar/oxygen enzymatic fuel cells based on gold nanoparticle-modified electrodes. Biosens Bioelectron 31(1):219-225
84. Weisburger JH (2002) Comments on the history and importance of aromatic and heterocyclic amines in public health. Mutat Res 506:9-20 (Pubitemid 35291144)
85. Xu F (2001) Dioxygen reactivity of laccase: Dependence on laccase source, pH, and anion inhibition. Appl Biochem Biotechnol 95:125-133 (Pubitemid 32953613)
86. Yoshino EM, JP), Imamura SS, JP), Matsuura KS, JP), Misaki HS, JP) 1988. Thermostable bilirubin oxidase and production process thereof. Toyo Jozo Co., Ltd. (Shizuoka, JP) Japan
87. Zebda A, Gondran C, Le Goff A, Holzinger M, Cosnier S (2011) Mediatorless high-power glucose biofuel cells based on compressed carbon nanotube-enzyme electrodes. Nat. Commun.: DOI: 10.1038/ncomms1365
88. Zloczewska A, Jonsson-Niedziolka M, Rogalski J, Opallo M (2011) Vertically aligned carbon nanotube film electrodes for bioelectrocatalytic dioxygen reduction. Electrochim Acta 56:3947-3953
89. Zoppellaro G, Sakurai N, Kataoka K, Sakurai T (2004) The reversible change in the redox state of type I Cu in Myrothecium verrucaria bilirubin oxidase depending on pH. Biosci Biotechnol Biochem 68(9):1998-2000 (Pubitemid 39415273)