Crystal structure of agaricus bisporus mushroom tyrosinase: Identity of the tetramer subunits and interaction with tropolone

Biochemistry

Volumn 50, Issue 24, 2011, Pages 5477-5486

  Ismaya, Wangsa T ^a   Rozeboom, Henritte J ^a   Weijn, Amrah ^b   Mes, Jurriaan J ^b   Fusetti, Fabrizia ^a   Wichers, Harry J ^b   Dijkstra, Bauke W ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

3D STRUCTURE; ACTIVE SITE; AGARICUS BISPORUS; BROWNING REACTIONS; CALCIUM IONS; CARBOHYDRATE BINDING; COPPER BINDING; COPPER IONS; COPPER SITES; ENZYME COMPLEXES; FOOD INDUSTRIES; FUNGAL TYROSINASE; HISTIDINE RESIDUES; LIVING ORGANISMS; MOLECULAR LEVELS; MUSHROOM TYROSINASE; PHENOLIC COMPOUNDS; SIDE-CHAINS; TETRAMERS; THIOETHERS; TROPOLONE; TYROSINASE INHIBITORS;

AMINO ACIDS; BINDING SITES; BIOLOGY; CARBOHYDRATES; COPPER; ENZYMES; GENES; HYDROGEN BONDS; METAL IONS; OLIGOMERS; PHENOLS;

CRYSTAL STRUCTURE;

CALCIUM ION; CARBOHYDRATE; COPPER; HISTIDINE; LECTIN; MELANIN; MONOPHENOL MONOOXYGENASE; PHENOL DERIVATIVE; QUINONE DERIVATIVE; SULFIDE; TETRAMER; TROPOLONE;

AGARICUS BISPORUS; ARTICLE; BINDING SITE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME MECHANISM; ENZYME STABILITY; ENZYME STRUCTURE; ENZYME SUBUNIT; FOOD INDUSTRY; FUNGAL GENE; HYDROGEN BOND; MUSHROOM; NONHUMAN; OPEN READING FRAME; PPO3 GENE; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY;

AGARICUS; AMINO ACID SEQUENCE; BASE SEQUENCE; BINDING SITES; CATALYTIC DOMAIN; COPPER; CRYSTALLOGRAPHY, X-RAY; DNA, FUNGAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MONOPHENOL MONOOXYGENASE; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; TROPOLONE;

AGARICUS BISPORUS; BASIDIOMYCOTA;

EID: 79959257956     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200395t     Document Type: Article

References (60)

1. Sanchez-Ferrer, A., Rodriguez-Lopez, J. N., Garcia-Canovas, F., and Garcia-Carmona, F. (1995) Tyrosinase: a comprehensive review of its mechanism Biochim. Biophys. Acta 1247, 1-11
2. Wichers, H. J., Recourt, K., Hendriks, M., Ebbelaar, C. E. M., Biancone, G., Hoeberichts, F. A., Mooibroek, H., and Soler-Rivas, C. (2003) Cloning, expression and characterisation of two tyrosinase cDNAs from Agaricus bisporus Appl. Microbiol. Biotechnol. 61, 336-341 (Pubitemid 36683529)
3. Wu, J., Chen, H., Gao, J., Liu, X., Cheng, W., and Ma, X. (2010) Cloning, characterization and expression of two new polyphenol oxidase cDNAs from Agaricus bisporus Biotechnol. Lett. 32, 1439-1447
4. Strothkamp, K. G., Jolley, R. L., and Mason, H. S. (1976) Quarternary structure of mushroom tyrosinase Biochem. Biophys. Res. Commun. 70, 519-524
5. Wichers, H. J., Gerritsen, Y. A. M., and Chapelon, C. G. J. (1996) Tyrosinase isoforms from the fruitbodies of Agaricus bisporus Phytochemistry 43, 333-337 (Pubitemid 27065544)
6. Schurink, M., van Berkel, W. J. H., Wichers, H. J., and Boeriu, C. G. (2007) Novel peptides with tyrosinase inhibitory activity Peptides 28, 485-495 (Pubitemid 46205013)
7. Flurkey, W. H. and Inlow, J. K. (2008) Proteolytic processing of polyphenol oxidase from plants and fungi J. Inorg. Biochem. 102, 2160-2170
8. Klabunde, T., Eicken, C., Sacchettini, J. C., and Krebs, B. (1998) Crystal structure of a plant catechol oxidase containing a dicopper center Nat. Struct. Biol. 5, 1084-1090 (Pubitemid 28546272)
9. Matoba, Y., Kumagai, T., Yamamoto, A., Yoshitsu, H., and Sugiyama, M. (2006) Crystallographic evidence that the dinuclear copper center of tyrosinase is flexible during catalysis J. Biol. Chem. 281, 8981-8990 (Pubitemid 43848005)
10. Decker, H., Schweikardt, T., and Tuczek, F. (2006) The first crystal structure of tyrosinase: All questions answered? Angew. Chem., Int. Ed. 45, 4546-4550 (Pubitemid 44106069)
11. Van Gelder, C. W. G., Flurkey, W. H., and Wichers, H. J. (1997) Sequence and structural features of plant and fungal tyrosinases Phytochemistry 45, 1309-1323 (Pubitemid 27294948)
12. Lerch, K. (1982) Primary structure of tyrosinase from Neurospora crassa. II. Complete amino acid sequence and chemical structure of a tripeptide containing an unusual thioether J. Biol. Chem. 257, 6414-6419
13. Ismaya, W. T., Rozeboom, H. J., Schurink, M., Boeriu, C. G., Wichers, H., and Dijkstra, B. W. (2011) Crystallization and preliminary X-ray crystallographic analysis of mushroom Agaricus bisporus tyrosinase Acta Crystallogr. F67, 575-578
14. Kabsch, W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants J. Appl. Crystallogr. 26, 795-800
15. Leslie, A. G. W. (2006) The integration of macromolecular diffraction data Acta Crystallogr. D62, 48-57
16. Evans, P. (2006) Scaling and assessment of data quality Acta Crystallogr. D62, 72-82
17. Collaborative Computational Project Number 4. ((1994) The CCP4 suite: programs for protein crystallography, Acta Crystallogr. D50, 760-763.
18. Matthews, B. W. (1968) Solvent content of protein crystals J. Mol. Biol. 33, 491-497
19. Vagin, A. and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement J. Appl. Crystallogr. 30, 1022-1025 (Pubitemid 127485985)
20. The UniProt Consortium. ((2007) The universal protein resource (UniProt), Nucleic Acids Res. 35, D193-D197.
21. Saller, M. J., Fusetti, F., and Driessen, A. J. M. (2009) Bacillus subtilis SpoIIIJ and YqjG function in membrane protein biogenesis J. Bacteriol. 191, 6749-6757
22. Jaroszewski, L., Rychlewski, L., Li, Z. W., Li, W. Z., and Godzik, A. (2005) FFAS03: a server for profile-profile sequence alignments Nucl. Acid Res. 33, W284-W288
23. Cuff, M. E., Miller, K. I., van Holde, K. E., and Hendrickson, W. A. (1998) Crystal structure of a functional unit from Octopus hemocyanin J. Mol. Biol. 278, 885-870
24. Perbandt, M., Guthöhrlein, E. W., Rypniewski, W., Idakieva, K., Stoeva, S., Voelter, W., Genov, N., and Betzel, C. (2003) The structure of a functional unit from the wall of a gastropod hemocyanin offers a possible mechanism for cooperativity Biochemistry 42, 6341-6346 (Pubitemid 36665807)
25. Canutescu, A. A., Shelenkov, A. A., and Dubrack, R. L. (2003) A graph theory for protein side-chain prediction Protein Sci. 12, 2001-2014 (Pubitemid 37022822)
26. McCoy, A. J., Grosse-Kunstleve, R. W., Storoni, L. C., and Read, R. J. (2005) Likelihood-enhanced fast translation functions Acta Crystallogr. D61, 458-464 (Pubitemid 43934606)
27. Terwilliger, T. C. (2003) Automated main-chain model building by template matching and interative fragment extension Acta Crystallogr. D59, 38-44 (Pubitemid 36117204)
28. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr. D66, 486-501
29. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53, 240-255 (Pubitemid 27235885)
30. Lamzin, V. S., Perrakis, A., and Wilson, K. S. (2001) The ARP/wARP suite for automated construction and refinement of protein models in International Tables for Crystallography (Rossmann, M. G. and Arnold, E., Eds.) pp 720-722, Kluwer Academic Publishers, Dordrecht, The Netherlands.
31. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search tool J. Mol. Biol. 215, 403-410
32. Winn, M. D., Isupov, M. N., and Murshudov, G. N. (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement Acta Crystallogr. D57, 122-133 (Pubitemid 32062682)
33. Lovell, S. C., Davis, I. W., Arendall, W. B., de Bakker, P. I. W., Word, J. M., Prisant, M. G., Richardson, J. S., and Richardson, D. C. (2003) Structure validation by C-alpha geometry: phi, psi, and C-beta deviation Proteins: Struct., Funct., Genet. 50, 437-450
34. Schüttelkopf, A. W. and van Aalten, D. M. F. (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr. D60, 1355-1363 (Pubitemid 41079731)
35. Shimanouchi, H. and Sasada, Y. (1973) Crystal and molecular structure of tropolone Acta Crystallogr. B29, 81-90
36. Bond, C. S. and Schüttelkopf, A. W. (2009) ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments Acta Crystallogr. D65, 510-512
37. Gouet, P., Robert, X., and Courcelle, E. (2003) ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins Nucleic Acids Res. 31, 3320-3323 (Pubitemid 37442149)
38. DeLano, W. L. (2008) The PyMOL molecular graphics system, Delano Scientific LLC, Palo Alto, CA.
39. Flurkey, A., Cooksey, J., Reddy, A., Spoonmore, K., Rescigno, A., Inlow, J., and Flurkey, W. H. (2008) Enzyme, protein, carbohydrate, and phenolic contaminants in commercial tyrosinase preparations: Potential problems affecting tyrosinase activity and inhibition studies J. Agric. Food Chem. 56, 4760-4768 (Pubitemid 351999408)
40. Jolley, R. L., Robb, D. A., and Mason, H. S. (1969) Multiple forms of mushroom tyrosinase-Association-dissociation phenomena J. Biol. Chem. 244, 1593-1598
41. Jolley, R. L., Nelson, R. M., and Robb, D. A. (1969) Multiple forms of mushroom tyrosinase-Structural studies on isozymes J. Biol. Chem. 244, 3251-3257
42. Marusek, C. M., Trobaugh, N. M., Flurkey, W. H., and Inlow, J. K. (2006) Comparative analysis of polyphenol oxidase from plant and fungal species J. Inorg. Biochem. 100, 108-123 (Pubitemid 43005023)
43. Kawamura-Konishi, Y., Tsuji, M., Hatana, S., Asanuma, M., Kakuta, D., Kawano, T., Mukouyama, E. B., Goto, H., and Suzuki, H. (2007) Purification, characterization, and molecular cloning of tyrosinase from Pholiota nameko Biosci. Biotechnol. Biochem. 71, 1752-1760 (Pubitemid 47358724)
44. Holm, L., Kaariainen, S., Rosenstrom, P., and Schenkel, A. (2008) Searching protein structure databases with DaliLite v.3 Bioinformatics 24, 2780-2781 (Pubitemid 352722625)
45. Arndt, J. W., Gu, J., Jaroszewski, L., Schwarzenbacher, R., Hanson, M. A., Lebeda, F. J., and Stevens, R. C. (2005) The structure of the neurotoxin-associated protein HA33/A from Clostridium botulinum suggests a reoccurring ß-trefoil fold in the progenitor toxin complex J. Mol. Biol. 346, 1083-1093 (Pubitemid 40215532)
46. Satoh, A., Konishi, S., Tamura, H., Stickland, H. G., Whitney, H. M., Smith, A. G., Matsumura, H., and Inoue, T. (2010) Substrate-induced closing of the active site revealed by the crystal structure of pantothenate synthetase from Staphylococcus aureus Biochemistry 49, 6400-6410
47. Hazes, B., Magnus, K. A., Bonaventura, C., Bonaventura, J., Dauter, Z., Kalk, K. H., and Hol, W. G. J. (1993) Crystal structure of deoxygenated Limulus polyphemus subunit II haemocyanin at 2.18 Å resolution: clues for a mechanism for allosteric regulation Protein Sci. 2, 597-619 (Pubitemid 23119310)
48. Yoon, J., Fujii, S., and Solomon, E. I. (2009) Geometric and electronic structure differences between the type 3 copper sites of the multicopper oxidases and hemocyanin/tyrosinase Proc. Natl. Acad. Sci. U.S.A. 106, 6585-6590
49. Li, Y. C., Wang, Y., Jiang, H. B., and Deng, J. P. (2009) Crystal structure of Manduca sexta prophenoloxidase provides insights into the mechanism of type 3 copper enzymes Proc. Natl. Acad. Sci. U.S.A. 106, 17002-17006
50. Kahn, V. and Andrawis, A. (1985) Inhibition of mushroom tyrosinase by tropolone Phytochemistry 24, 905-908
51. Espin, J. C. and Wichers, H. J. (1999) Slow-binding inhibition of mushroom (Agaricus bisporus) tyrosinase isoforms by tropolone J. Agric. Food Chem. 47, 2638-2644 (Pubitemid 29396332)
52. Macintyre, W. M., Robertson, J. M., and Zahrobski, R. F. (1966) Crystal structure of cupric tropolone-a refinement Proc. R. Soc. London, A 289, 161-170
53. Sendovski, M., Kanteev, M., Shuster Ben-Yosef, V., Adir, N., and Fishman, A. (2011) First structures of an active bacterial tyrosinase reveal copper plasticity J. Mol. Biol. 405, 227-237
54. Woerdenbag, H. J., Pras, N., Frijlink, H. W., Lerk, C. F., and Malingré, T. M. (1990) Cyclodextrin-facilitated bioconversion of 17-ß-estradiol by a phenoloxidase from Mucuna pruriens cell cultures Phytochemistry 29, 1551-1554
55. Ito, N., Phillips, S. E. V., Stevens, C., ögel, Z. B., McPherson, M. J., Keen, J. N., Yadav, K. D. S., and Knowles, P. F. (1991) Nover thioether bond revealed by a 1.7 Å crystal structure of galactosidase Nature 350, 87-90 (Pubitemid 21926129)
56. Decker, H., Schweikardt, T., Nillius, D., Salzbrunn, U., Jaenicke, E., and Tuczek, F. (2007) Similar enzyme activation and catalysis in hemocyanins and tyrosinases Gene 398, 183-191 (Pubitemid 47068888)
57. Kim, Y.-J. and Uyama, H. (2005) Tyrosinase inhibitors from natural and synthetic sources: structure, inhibition mechanism and perspective for the future Cell. Mol. Life Sci. 62, 1707-1723 (Pubitemid 41176052)
58. Chang, T. S. (2009) An updated review of tyrosinase inhibitors Int. J. Mol. Sci. 10, 2440-2475
59. Espin, J. C., van Leeuwen, J., and Wichers, H. J. (1999) Kinetic study of the activation process of a latent mushroom (Agaricus bisporus) tyrosinase by serine proteases J. Agric. Food Chem. 47, 3509-3517 (Pubitemid 29449461)
60. Espin, J. C., Soler-Rivas, C., and Wichers, H. J. (2000) Maturation and activation of latent tyrosinase from Agaricus bisporus Mushroom Sci. 15, 79-86