Extracellular tyrosinase from the fungus Trichoderma reesei shows product inhibition and different inhibition mechanism from the intracellular tyrosinase from Agaricus bisporus

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1824, Issue 4, 2012, Pages 598-607

  Gasparetti, Chiara ^a   Nordlund, Emilia ^a   Jänis, Janne ^b   Buchert, Johanna ^a   Kruus, Kristiina ^a  

^a VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Agaricus bisporus; Dopachrome; End product inhibition; Ki; Trichoderma reesei; Tyrosinase

Indexed keywords

ARBUTIN; CAFFEIC ACID; CATECHOL; DOPACHROME; KOJIC ACID; LEVODOPA; MONOPHENOL MONOOXYGENASE; PARA COUMARIC ACID; POTASSIUM CYANIDE; SODIUM AZIDE;

AGARICUS BISPORUS; ARTICLE; CATALYSIS; ENZYME ACTIVITY; HYPOCREA JECORINA; NEGATIVE FEEDBACK; NONHUMAN; OXIDATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL;

AGARICUS; CAFFEIC ACIDS; CATECHOLS; COUMARIC ACIDS; ENZYME INHIBITORS; FUNGAL PROTEINS; INDOLEQUINONES; INTRACELLULAR FLUID; KINETICS; LEVODOPA; MONOPHENOL MONOOXYGENASE; OXIDATION-REDUCTION; POTASSIUM CYANIDE; PYRONES; SODIUM AZIDE; SPECTROPHOTOMETRY, ULTRAVIOLET; TRICHODERMA;

AGARICUS BISPORUS; FUNGI; HYPOCREA JECORINA;

EID: 84857304751     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2011.12.012     Document Type: Article

References (65)

1. D.A. Robb Tyrosinase R. Lontie, Copper Proteins and Copper Enzymes Vol. 2 1984 CRC Press Inc. Boca Raton, FL 207 241
2. K. Lerch Neurospora tyrosinase: structural, spectroscopic and catalytic properties Mol. Cell. Biochem. 52 1983 125 138
3. A.A. Bell, and M.H. Wheeler Biosynthesis and functions of fungal melanins Annu. Rev. Phytopathol. 24 1986 411 451
4. C. Soler-Rivas, N. Arpin, J.M. Olivier, and H.J. Wichers Activation of tyrosinase in Agaricus bisporus strains following infection by Pseudomonas tolaasii or treatment with a tolaasin-containing preparation Mycol. Res. 101 1997 375 382
5. C.W.G. van Gelder, W.H. Flurkey, and H.J. Wichers Sequence and structural features of plant and fungal tyrosinases Phytochemistry 45 1997 1309 1323
6. A.M. Mayer Polyphenol oxidases in plants-recent progress Phytochemistry 26 1987 11 20
7. M. Sugumaran Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects Pigment Cell Res. 15 2002 2 9
8. M. Sugumaran Molecular mechanisms for mammalian melanogenesis: comparison with insect cuticular sclerotization FEBS Lett. 295 1991 233 239
9. J.D. Nosanchuk, and A. Casadevall The contribution of melanin to microbial pathogenesis Cell. Microbiol. 5 2003 203 223
10. K. Lerch, and L. Ettinger Purification and characterization of a tyrosinase from Streptomyces glaucescens Eur. J. Biochem. 31 1972 427 437
11. Y. Matoba, T. Kumagai, A. Yamamoto, H. Yoshitsu, and M. Sugiyama Crystallographic evidence that the dinuclear copper center of tyrosinase is flexible during catalysis J. Biol. Chem. 281 2006 8981 8990
12. M. Fling, N.H. Horowitz, and S.F. Heinenmann The isolation and properties of crystalline tyrosinase from Neurospora J. Biol. Chem. 238 1963 2045 2053
13. U. Kupper, D.M. Niedermann, G. Travaglini, and K. Lerch Isolation and characterization of the tyrosinase gene from Neurospora crassa J. Biol. Chem. 264 1989 17250 17258
14. T. Nakamura, S. Sho, and Y. Ogura On the purification and properties of mushroom tyrosinase J. Biochem. 59 1966 481 486
15. H.J. Wichers, Y.A.M. Gerritsen, and C.G.J. Chapelon Tyrosinase isoforms from the fruitbodies of Agaricus bisporus Phytochemistry 43 1996 333 337
16. D.A. Robb, and S. Gutteridge Polypeptide composition of two fungal tyrosinases Phytochemistry 20 1981 1481 1485
17. T.S. Chang An updated review of tyrosinase inhibitors Int. J. Mol. Sci. 10 2009 2440 2475
18. H. Decker, T. Schweikardt, D. Nillius, U. Salzbrunn, E. Jaenicke, and F. Tuczek Similar enzyme activation and catalysis in hemocyanins and tyrosinases Gene 398 2007 183 191
19. E.I. Solomon, U.M. Sundaram, and T.E. Machonkin Multicopper oxidases and oxygenases Chem. Rev. 96 1996 2563 2606
20. R.L. Jolley Jr., L.H. Evans, and H.S. Mason Reversible oxygenation of tyrosinase Biochem. Biophys. Res. Commun. 46 1972 878 884
21. R.L. Jolley Jr., L.H. Evans, N. Makino, and H.S. Mason Oxytyrosinase J. Biol. Chem. 249 1974 335 345
22. N. Makino, and H.S. Mason Reactivity of oxytyrosinase toward substrates J. Biol. Chem. 248 1973 5731 5735
23. H.S. Raper The tyrosinase-tyrosine reaction: production from tyrosine of 5:6-dihydroxyindole and 5:6-dihydroxyindole-2-carboxylic acid-the precursors of melanin Biochem. J. 21 1927 89 96
24. H.S. Mason The chemistry of melanin; mechanism of the oxidation of dihydroxyphenylalanine by tyrosinase J. Biol. Chem. 172 1948 83 99
25. J.N. Rodriguez-Lopez, J. Tudela, R. Varón, and F.G. García-Cánovas Kinetic study on the effect of pH on the melanin biosynthesis pathway Biochim. Biophys. Acta 1076 1991 379 386
26. Y.J. Kim, and H. Uyama Tyrosinase inhibitors from natural and synthetic sources: structure, inhibition mechanism and perspective for the future Cell. Mol. Life Sci. 62 2005 1707 1723
27. H. Claus, and H. Decker Bacterial tyrosinases Syst. Appl. Microbiol. 29 2006 3 14
28. S. Ito, and K. Wakamatsu Chemistry of mixed melanogenesis-pivotal roles of dopaquinone Photochem. Photobiol. 84 2008 582 592
29. S.Y. Seo, V.K. Sharma, and N. Sharma Mushroom tyrosinase: recent prospects J. Agric. Food Chem. 51 2003 2837 2853
30. S. Parvez, M. Kang, H.S. Chung, and H. Bae Naturally occurring tyrosinase inhibitors: mechanism and applications in skin health, cosmetics and agriculture industries Phytother. Res. 21 2007 805 816
31. A. Rescigno, F. Sollai, B. Pisu, A. Rinaldi, and E. Sanjust Tyrosinase inhibition: general and applied aspects J. Enzyme Inhib. Med. Chem. 17 2002 207 218
32. M. Mattinen, R. Lantto, E. Selinheimo, K. Kruus, and J. Buchert Oxidation of peptides and proteins by Trichoderma reesei and Agaricus bisporus tyrosinases J. Biotechnol. 133 2008 395 402
33. G. Freddi, A. Anghileri, S. Sampaio, J. Buchert, P. Monti, and P. Taddei Tyrosinase-catalyzed modification of Bombyx mori silk fibroin: grafting of chitosan under heterogeneous reaction conditions J. Biotechnol. 125 2006 281 294
34. S. Halaouli, M. Asther, K. Kruus, L. Guo, M. Hamdi, J.C. Sigoillot, M. Asther, and A. Lomascolo Characterization of a new tyrosinase from Pycnoporus species with high potential for food technological applications J. Appl. Microbiol. 98 2005 332 343
35. C.M. Aberg, T. Chen, A. Olumide, S.R. Raghavan, and G.F. Payne Enzymatic grafting of peptides from casein hydrolysate to chitosan. Potential for value-added byproducts from food-processing wastes J. Agric. Food Chem. 52 2004 788 793
36. R. Lantto, E. Puolanne, K. Kruus, J. Buchert, and K. Autio Tyrosinase-aided protein cross-linking: effects on gel formation of chicken breast myofibrils and texture and water-holding of chicken breast meat homogenate gels J. Agric. Food Chem. 55 2007 1248 1255
37. E. Selinheimo, K. Autio, K. Kruus, and J. Buchert Elucidating the mechanism of laccase and tyrosinase in wheat bread making J. Agric. Food Chem. 55 2007 6357 6365
38. A. Anghileri, R. Lantto, K. Kruus, C. Arosio, and G. Freddi Tyrosinase-catalyzed grafting of sericin peptides onto chitosan and production of protein-polysaccharide bioconjugates J. Biotechnol. 127 2007 508 519
39. E. Selinheimo, M. Saloheimo, E. Ahola, A. Westerholm-Parvinen, N. Kalkkinen, J. Buchert, and K. Kruus Production and characterization of a secreted, C-terminally processed tyrosinase from the filamentous fungus Trichoderma reesei FEBS J. 273 2006 4322 4335
40. E. Selinheimo, D. NiEidhin, C. Steffensen, J. Nielsen, A. Lomascolo, S. Halaouli, E. Record, D. O'Beirne, J. Buchert, and K. Kruus Comparison of the characteristics of fungal and plant tyrosinases J. Biotechnol. 130 2007 471 480
41. E. Selinheimo, C. Gasparetti, M. Mattinen, C.L. Steffensen, J. Buchert, and K. Kruus Comparison of substrate specificity of tyrosinases from Trichoderma reesei and Agaricus bisporus Enzyme Microb. Technol. 44 2009 1 10
42. J. Jänis, P. Pulkkinen, J. Rouvinen, and P. Vainiotalo Determination of steady-state kinetic parameters for a xylanase-catalyzed hydrolysis of neutral underivatized xylooligosaccharides by mass spectrometry Anal. Biochem. 365 2007 165 173
43. A. Cornish-Bowden A simple graphical method for determining the inhibition constants of mixed, uncompetitive and non-competitive inhibitors Biochem. J. 137 1974 143 144
44. J.C. Espín, P.A. García-Ruíz, J. Tudela, and F.G. García-Cánovas Study of stereospecificity in mushroom tyrosinase Biochem. J. 331 1998 547 551
45. J.C. Espín, R. Varón, L.G. Fenoll, M.A. Gilabert, P.A. García-Ruíz, J. Tudela, and F.G. García-Cánovas Kinetic characterization of the substrate specificity and mechanism of mushroom tyrosinase Eur. J. Biochem. 267 2000 1270
46. H.J. Wichers, K. Recourt, M. Hendriks, C.E. Ebbelaar, G. Biancone, F.A. Hoeberichts, H. Mooibroek, and C. Soler-Rivas Cloning, expression and characterisation of two tyrosinase cDNAs from Agaricus bisporus Appl. Environ. Microbiol. 61 2003 336 341
47. W.T. Ismaya, H.J. Rozeboom, A. Weijn, J.J. Mes, F. Fusetti, H.J. Wichers, and B.W. Dijkstra Crystal structure of Agaricus bisporus mushroom tyrosinase: identity of the tetramer subunits and interaction with tropolone Biochemistry 50 2011 5477 5486
48. J.Y. Lim, K. Ishiguro, and I. Kubo Tyrosinase inhibitory p-coumaric acid from ginseng leaves Phytother. Res. 13 1999 371 375
49. C.J. Cooksey, P.J. Garratt, E.J. Land, S. Pavel, C.A. Ramsden, P.A. Riley, and N.P. Smit Evidence of the indirect formation of the catecholic intermediate substrate responsible for the autoactivation kinetics of tyrosinase J. Biol. Chem. 272 1997 26226 26235
50. B. Kågedal, P. Konradsson, T. Shibata, and Y. Mishima High-performance liquid-chromatographic analysis of dopachrome and dihydroxyphenylalanine Anal. Biochem. 225 1995 264 269
51. J.L. Muñoz-Muñoz, F.J. Garcia-Molina, R. Varón, P.A. García-Ruíz, J. Tudela, F.G. García-Cánovas, and J.N. Rodriguez-Lopez Suicide inactivation of the diphenolase and monophenolase activities of tyrosinase IUBMB Life 62 2010 539 547
52. J.L. Muñoz-Muñoz, F.J. Garcia-Molina, P.A. García-Ruíz, M. Molina-Alarcón, J. Tudela, F.G. García-Cánovas, and J.N. Rodriguez-Lopez Phenolic substrates and suicide inactivation of tyrosinase: kinetics and mechanism Biochem. J. 416 2008 431 440
53. J.S. Chen, C.I. Wei, and M.R. Marshall Inhibition mechanism of kojic acid on polyphenol oxidase J. Agric. Food Chem. 39 1991 1897 1901
54. J. Cabanes, S. Chazarra, and F. García Carmona Kojic acid, a cosmetic skin whitening agent, is a slow-binding inhibitor of catecholase activity of tyrosinase J. Pharm. Pharmacol. 46 1994 982 985
55. J.C. Espín, and H.J. Wichers Slow-binding inhibition of mushroom (Agaricus bisporus) tyrosinase isoforms by tropolone J. Agric. Food Chem. 47 1999 2638 2644
56. M. Funayama, H. Arakawa, R. Yamamoto, T. Nishino, T. Shin, and S. Murao Effects of alpha- and beta-arbutin on activity of tyrosinases from mushroom and mouse melanoma Biosci. Biotechnol. Biochem. 59 1995 143 144
57. I. Kubo, and I. Kinst-Hori Tyrosinase inhibitors from cumin J. Agric. Food Chem. 46 1998 5338 5341
58. J.S. Conrad, S.R. Dawso, E.R. Hubbard, T.E. Meyers, and K.G. Strothkamp Inhibitor binding to the binuclear active site of tyrosinase: temperature, pH, and solvent deuterium isotope effects Biochemistry 33 1994 5739 5744
59. D.E. Wilcox, A.G. Porras, Y.T. Hwang, K. Lerch, M.E. Winkler, and E.I. Solomon Substrate analogue binding to the coupled binuclear copper active site in tyrosinase J. Am. Chem. Soc. 107 1985 4015 4027
60. M. Sendovski, M. Kanteev, V.S. Ben-Yosef, N. Adir, and A. Fishman First structures of an active bacterial tyrosinase reveal copper plasticity J. Mol. Biol. 405 2011 227 237
61. K. Nihei, and I. Kubo Identification of oxidation product of arbutin in mushroom tyrosinase assay system Bioorg. Med. Chem. Lett. 13 2003 2409 2412
62. L.G. Fenoll, J.N. Rodriguez-Lopez, F. Garcia-Sevilla, P.A. García-Ruíz, R. Varón, F.G. García-Cánovas, and J. Tudela Analysis and interpretation of the action mechanism of mushroom tyrosinase on monophenols and diphenols generating highly unstable o-quinones Biochim. Biophys. Acta 1548 2001 1 22
63. I. Kubo, and I. Kinst-Hori Tyrosinase inhibitory activity of the olive oil flavor compounds J. Agric. Food Chem. 47 1999 4574 4578
64. D.F. Healey, and K.G. Strothkamp Inhibition of the catecholase and cresolase activity of mushroom tyrosinase by azide Arch. Biochem. Biophys. 211 1981 86 91
65. M. Sugumaran A caution about the azide inhibition of enzymes associated with electrophilic metabolites Biochem. Biophys. Res. Commun. 212 1995 834 839