Enzyme, protein, carbohydrate, and phenolic contaminants in commercial tyrosinase preparations: Potential problems affecting tyrosinase activity and inhibition studies

Journal of Agricultural and Food Chemistry

Volumn 56, Issue 12, 2008, Pages 4760-4768

  Flurkey, Allison ^a   Cooksey, Jena ^a   Reddy, Akhila ^a   Spoonmore, Kelli ^a   Rescigno, Antonio ^b   Inlow, Jennifer ^a   Flurkey, William H ^a  

^a INDIANA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Agaricus bisporus; Carbohydrates; Glycosidases; Inhibitors; Phenolics; Proteins; Tyrosinase

Indexed keywords

CARBOHYDRATE; ENZYME; ENZYME INHIBITOR; MONOPHENOL MONOOXYGENASE; PHENOL DERIVATIVE; PROTEIN;

AGARICUS; ARTICLE; CHEMISTRY; DRUG CONTAMINATION; ENZYMOLOGY; METABOLISM;

AGARICUS; CARBOHYDRATES; DRUG CONTAMINATION; ENZYME INHIBITORS; ENZYMES; MONOPHENOL MONOOXYGENASE; PHENOLS; PROTEINS;

AGARICUS BISPORUS; BASIDIOMYCOTA;

EID: 47349132380     PISSN: 00218561     EISSN: None     Source Type: Journal    
DOI: 10.1021/jf800109a     Document Type: Article

References (57)

1. Claus, H.; Decker, H. Bacterial tyrosinases. Syst. Appl. Microbiol. 2006, 29, 3-14.
2. Halaouli, S.; Asther, M.; Sigoillot, J. C.; Hamdi, M.; Lomascolo, A. Bacterial tyrosinases: new prospects in molecular characteristics, bioengineering and biotechnological applications. J. Appl. Microbiol. 2006, 100, 219-232.
3. van Gelder, C. W. G.; Flurkey, W. H.; Wichers, H. J. Sequence and structural features of plant and fungal tyrosinase. Phytochemistry 1997, 45, 1309-1323.
4. Marusek, C. M.; Trobaugh, N. M.; Flurkey, W. H.; Inlow, J. K. Comparative analysis of polyphenol oxidase from plant and fungal species. J. Inorg. Biochem. 2006, 100, 108-123.
5. Yoruk, R.; Marshall, M. R. Physicochemical properties and function of plant poly-phenol oxidase: a review. J. Food Biochem. 2003, 27, 361-422.
6. Sugumaran, M. Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. Pigment Cell Res. 2002, 15, 2-9.
7. del Marmol, V.; Beermann, F. Tyrosinase and related proteins in mammalian pigmentation. FEBS Lett. 1996, 381, 165-168.
8. Gandio-Herrero, F.; Escribano, J.; Garcia-Carmona, F. Betaxanthins as substrates for tyrosinase. An approach to the role of tyrosinase in the biosynthetic pathway of betalains. Plant Physiol. 2005, 138, 421-432.
9. Kim, Y. J.; Umaya, H. Tyrosinase inhibitors from natural and synthetic sources: structure, inhibition mechanism and perspective for the future. Cell. Mol. Life Sci. 2005, 62, 1707-1723.
10. Rescigno, A.; Solli, F.; Pisu, B.; Rinaldi, A.; Sanjust, E. Tyrosinase inhibition: general and applied aspects. J. Enzyme Inhib. Med. Chem. 2002, 17, 207-218.
11. Seo, S. Y.; Sharma, V. K.; Sharma, N. J. Mushroom tyrosinase: recent prospects. J. Agric. Food Chem. 2003, 51, 2837-2853.
12. Valero, E.; Carrion, P.; Varon, R.; Garcia-Carmona, F. Quantification of acetamino-phen by oxidation with tyrosinase in the presence of Besthorn's hydrazone. Anal. Biochem. 2003, 318, 187-195.
13. Kahn, M. T.; Choudhary, M. I.; Khan, K. M.; Rani, M.; Rahman, A. Structure activity relationships of tyrosinase inhibitory combinatorial library of 2,5-disubstituted-1,3,4-oxadiazole analogues. Bioorg. Med. Chem. 2005, 13, 3385-3395.
14. Karbassi, F.; Haghbeen, K.; Saboury, A. A.; Ranjbar, B.; Moosavi-Movahedi, A. A. Activity, structural and stability changes of mushroom tyrosinase by sodium dodecyl sulfate. Colloids Surf. B: Biointerfaces 2003, 32, 137-143.
15. Li, B.; Huang, Y.; Paskewitz, S. M. Hen white lysozyme as an inhibitor of mushroom tyrosinase. FEBS Lett. 2006, 580, 1877-1882.
16. Borojerdi, S. S.; Haghbeen, K.; Karkhane, A. A.; Fazli, M.; Saboury, A. A. Successful resonance Raman study of cresolase activity of mushroom tyrosinase. Biochem. Biophys. Res. Commun. 2004, 314, 925-930.
17. Marrero-Ponce, Y.; Khan, M. T. H.; Martin, G. M. C.; Ather, A.; Sultankhodzhaev, M. N.; Torrens, F.; Rotondo, R. Prediction of tyrosinase inhibition activity using atom-based bilinear indices. Chem. Med. Chem. 2007, 2, 449-478.
18. Ratcliff, B.; Flurkey, W. H.; Kuglin, J.; Dawley, R. Tyrosinase, laccase, and peroxidase in mushrooms (agaricus, crimini, oyster, and shiitake). J. Food Sci. 1994, 59, 824-827.
19. Kumar, M.; Flurkey, W. H. Phenolic oxidative enzymes in Agaricus bisporus. Phytochem. (Life Sci. Adv.) 1992, 11, 97-103.
20. Flurkey, W. H.; Ratcliff, B.; Lopez, L.; Kuglin, J.; Dawley, R. Differentiation of fungal tyrosinases and laccases using selective inhibitors and substrates. In Enzymatic Browning and its Prevention; ACS Symposium Series 600; Lee, C. Y., Whitaker, J. R. Eds.; American Chemical Society: Washington, DC, 1995; pp 81-89.
21. Sugumaran, M.; Bolton, J. L. Laccase - and not tyrosinase - is the enzyme responsible for quinone methide production from 2,6-dimethoxy-4-allyl phenol. Arch. Biochem. Biophys. 1998, 353, 207-212.
22. Rescigno, A.; Zucca, P.; Flurkey, A.; Inlow, J.; Flurkey, W. H. Identification and discrimination between some contaminant enzyme activities in commercial preparations of mushroom tyrosinase. Enzyme Microbiol. Technol. 2007, 41, 620-627.
23. Espin, J. C.; van Leeuwen, J.; Wicher, H. J. Kinetic study of the activation process of latent mushroom tyrosinase by serine proteases. J. Agric. Food Chem. 1999, 47, 3509-3517.
24. Chen, L.; Flurkey, W. H. Effect of protease inhibitors on the extraction of crimini mushroom tyrosinase isoforms. Curr. Top. Phytochem. 2002, 5, 109-120.
25. Fu, B.; Li, H.; Wang, X.; Lee, F. S. C.; Cui, S. Isolation and identification of flavonoids in licorice and a study of their inhibitory effects on tyrosinase. J. Agric. Food Chem. 2005, 53, 7408-7414.
26. Masamoto, Y.; Ando, H.; Murata, Y.; Shimoishi, Y.; Tada, M.; Takahata, K. Mushroom tyrosinase inhibitory activity of esculetin isolated from seeds of Euphorbia lathysis L. Biosci., Biotechnol., Biochem. 2003, 67, 631-634.
27. Friedman, M. Food browning and its prevention: an overview. J. Agric. Food Chem. 1966, 44, 631-653.
28. van Leeuwen, J.; Wichers, H. J. Tyrosinase activity and isoform composition in separate tissues during development of Agaricus bisporus fruit bodies. Mycol. Res. 1999, 103, 413-418.
29. Singleton, V.; Orthofer, R.; Lamuela-Raventos, R. M. Analysis of total phenol and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol. 1999, 299, 152-158.
30. Chaplin, M. F. Monosaccharides. In Carbohydrate Analysis: A Practical Approach; Chaplin, M. F., Kennedy, J. F. Eds.; IRL Press: Oxford, U.K., 1986; pp 1-36.
31. Lowry, O.; Rosebrough, N.; Farr, A.; Randall, R. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193, 265-275.
32. Fan, Y.; Flurkey, W. H. Purification and characterization of tyrosinase from gill tissue of portabella mushrooms. Phytochemistry 2004, 65, 671-678.
33. Horn, S. J.; Eijsink, V. G. H. A reliable reducing end assay for chito-oligosaccharides. Carbohydr. Polym. 2004, 56, 35-59.
34. Olianas, A.; Sanjust, E.; Pellegrini, M.; Rescigno, A. Tyrosinase activity and hemocyanin in the hemolymph of the slipper lobster Scyllarides liatus. J. Comp. Physiol. B 2005, 175, 405-411.
35. Kwon, K. S.; Lee, J.; Hyung, G. K.; Yung Chil, H. Detection of β-glucosidase activity in polyacrylamide gels with esculin as substrate. Appl. Environ. Microbiol. 1994, 60, 4584-4586.
36. Schwarz, W. E.; Bronnenmeier, K.; Grabnitz, F.; Staudenbauer, W. L. Activity staining of cellulases in polyacrylamide gel containing mixed linkage β-glucans. Anal. Biochem. 1987, 164, 72-77.
37. Wichers, H. J.; Recourt, K.; Hendriks, M.; Ebbelaar, C. E. M.; Biancone, G.; Hoeberichts, F. A.; Mooibroek, H.; Soler-Rivas, C. Cloning, expression and characterization of two tyrosinase cDNAs from Agaricus bisporus. Appl. Microbiol. Biotechnol. 2003, 61, 36-341.
38. Tang, C. M.; Waterman, L. D.; Smith, M. H.; Thurston, C. F. The cel4 gene of Agaricus bisporus encodes a β mannanase. Appl. Environ. Microbiol. 2001, 67, 2298-2303.
39. Carrizo, M. E.; Irazoqui, F. J.; Lardone, R. D.; Nores, G. A.; Curtino, J. A.; Capaldi, S.; Perduca, M.; Monaco, H. L. Crystallization and prelimary X-ray study of the common edible mushroom (Agaricus bisporus) lectin. Acta Crystallogr. 2004, D60, 718-720.
40. Hammond, J. B. W.; Nichols, R. Carbohydrate metabolism in Agaricus bisporus (Lange) Sing.: changes in soluble carbohydrates during growth of mycelium and sporophore. J. Gen. Microbiol. 1976, 93, 309-320.
41. Hammond, J. B. W. Changes in composition of harvested mushroom (Agaricus bisporus). Phytochemistry 1979, 18, 415-418.
42. Kumar, M.; Flurkey, W. H. Activity, isoenzymes, and purity of mushroom tyrosinase in commercial preparations. Phytochemistry 1991, 30, 3899-3902.
43. 4. J. Food Biochem. 2000, 24, 399-415.
44. Kahn, V.; Andrawis, A. Inhibition of mushroom tyrosinase by tropolone. Phytochemistry 1985, 24, 905-908.
45. Andrawis, A.; Kahn, V. Effect of methimazole on the activity of mushroom tyrosinase. Biochem. J. 1986, 235, 91-96.
46. Park, K.; Park, Y.; Lee, J.; Hahn, H.; Lee, S.; Bae, C.; Yang, J.; Kim, D.; Hahn, M. Inhibition kinetics of mushroom tyrosinase by copper-chelating ammonium tetrathiomolybdate. Biochim. Biophys. Acta 2005, 1726, 115-120.
47. Chen, Q.; Ke, L.; Song, K.; Huang, H.; Liu, X. Inhibitory effects of hexylresorcinol and dodecylresorcinol on mushroom (Agaricus bisporus) tyrosinase. Protein J. 2004, 23, 35-141.
48. Jacobsohn, G. M.; Jacobsohn, M. K. Incorporation and binding of estrogens in melanin: comparison of mushroom and mammalian tyrosinases. Biochim. Biophys. Acta 1992, 1116, 173-182.
49. Galindo, J. D.; Martinez, J. J.; Lopez-Ballester, J. A.; Penafiel, R.; Solano, F.; Lozano, J. A. The effect of polyamines on tyrosinase activity. Biochem. Int. 1987, 15, 1151-1158.
50. Schurink, M.; van Berkel, W. J. H.; Wichers, H. J.; Boeriu, C. G. Novel peptides with tyrosinase inhibitory activity. Peptides 2007, 28, 485-495.
51. Strothkamp, K. G.; Jolley, R. L.; Mason, H. S. Quaternary structure of mushroom tyrosinase. Biochem. Biophys. Res. Commun. 1976, 70, 519-524.
52. Robinson, S. P.; Dry, I. E. Broad bean leaf polyphenol oxidase is a 60 kilodalton protein susceptible to proteolytic cleavage. Plant Physiol. 1992, 99, 317-323.
53. Morales, P.; Thurston, C. F. Efficient isolation of genes differentially expressed on cellulose by suppression subtractive hybridization in Agaricus bisporus. Mycol. Res. 2003, 107, 401-407.
54. Whiteford, J. R.; Wood, D. A.; Thurston, C. F. Characterization of xylanases in liquid and compost cultures of the cultivated mushroom Agaricus bisporus. Mycol. Res. 2000, 104, 810-819.
55. Galan, B.; Garcia-Mendoza, C.; Calonje, M.; Novaes-Ledieu, M. Production, purification, and properties of an endo 1,3-β-glucanase from the basidiomycete Agaricus bisporus. Curr. Microbiol. 1999, 38, 190-193.
56. Sassoon, J.; Mooibrock, H. A system categorizing enzyme cell-wall associations in Agaricus bisporus using operational criteria. Appl. Microbiol. Biotechnol. 2001, 55, 613-622.
57. Yague, E.; Mehak-Zunic, M.; Morgan, L.; Wood, D. A. Expression of CEL2 and CEL4, two proteins from Agaricus bisporus with similarity to fungal cellobiohydrolase 1 and β mannanase, respectively, is regulated by the carbon source. Microbiology 1997, 143, 239-244.