Manganese oxidation site in Pleurotus eryngii versatile peroxidase: A site-directed mutagenesis, kinetic, and crystallographic study

Biochemistry

Volumn 46, Issue 1, 2007, Pages 66-77

  Ruiz Dueñas, Francisco J ^a   Morales, María ^a   Pérez Boada, Marta ^a   Choinowski, Thomas ^b   Martínez, María Jesús ^a   Piontek, Klaus ^b   Martínez, Ángel T ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MUTATION; PEROXIDASE; PHANEROCHAETE CHRYSOSPORIUM;

CONFORMATIONS; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENZYMES; MANGANESE; MUTAGENESIS; OXIDATION; RATE CONSTANTS;

ENZYME KINETICS;

ASPARTIC ACID; CARBOXYLIC ACID; GLUTAMIC ACID; MANGANESE; MANGANESE PEROXIDASE; PEROXIDASE; RECOMBINANT ENZYME; TRYPTOPHAN; UNCLASSIFIED DRUG; VERSATILE PEROXIDASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTALLOGRAPHY; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME REPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; PHANEROCHAETE; PLEUROTUS; PLEUROTUS ERYNGII; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS;

BINDING SITES; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; FUNGAL PROTEINS; KINETICS; LIGANDS; MANGANESE; MUTAGENESIS, SITE-DIRECTED; MUTATION; OXIDATION-REDUCTION; PEROXIDASES; PLEUROTUS;

PHANEROCHAETE CHRYSOSPORIUM; PLEUROTUS ERYNGII;

EID: 33846173370     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061542h     Document Type: Article

References (53)

1. Gold, M. H., Youngs, H. L., and Gelpke, M. D. (2000) Manganese peroxidase, Met. Ions Biol. Syst. 37, 559-586.
2. Magliozzo, R. S., and Marcinkeviciene, J. A. (1997) The role of Mn(II)-peroxidase activity of mycobacterial catalase-peroxidase in activation of the antibiotic isoniazid, J. Biol. Chem. 272, 8867-8870.
3. 2+ oxidation, Appl. Environ. Microbiol. 63, 2166-2174.
4. Martínez, A. T. (2002) Molecular biology and structure-function of lignin-degrading heme peroxidases, Enzyme Microb. Technol. 30, 425-444.
5. Kirk, T. K., and Cullen, D. (1998) Enzymology and molecular genetics of wood degradation by white-rot fungi, in Environmentally friendly technologies for the pulp and paper industry (Young, R. A., and Akhtar, M., Eds.) pp 273-308, TAPPI Press, Atlanta, GA.
6. Kirk, T. K., and Farrell, R. L. (1987) Enzymatic "combustion": The microbial degradation of lignin, Annu. Rev. Microbiol. 41, 465-505.
7. Lobos, S., Tello, M., Polanco, R., Larrondo, L. F., Manubens, A., Salas, L., and Vicuña, R. (2001) Enzymology and molecular genetics of the ligninolytic system of the basidiomycete Ceriporiopsis subvermispora, Curr. Sci. 81, 992-997.
8. Martínez, A. T., Camarero, S., Guillén, F., Gutiérrez, A., Muñoz, C., Varela, E., Martínez, M. J., Barrasa, J. M., Ruel, K., and Pelayo, M. (1994) Progress in biopulping of non-woody materials: Chemical, enzymatic and ultrastructural aspects of wheat-straw delignification with ligninolytic fungi from the genus Pleurotus, FEMS Microbiol. Rev. 13, 265-274.
9. Ruiz-Dueñas, F. J., Camarero, S., Pérez-Boada, M., Martínez, M. J., and Martínez, A. T. (2001) A new versatile peroxidase from Pleurotus, Biochem. Soc. Trans. 29, 116-122.
10. Ruiz-Dueñas, F. J., Martínez, M. J., and Martínez, A. T. (1999) Molecular characterization of a novel peroxidase isolated from the ligninolytic fungus Pleurotus eryngii, Mol. Microbiol. 31, 223-236.
11. Camarero, S., Ruiz-Dueñas, F. J., Sarkar, S., Martínez, M. J., and Martínez, A. T. (2000) The cloning of a new peroxidase found in lignocellulose cultures of Pleurotus eryngii and sequence comparison with other fungal peroxidases, FEMS Microbiol. Lett. 191, 37-43.
12. Moreira, P. R., Duez, C., Dehareng, D., Antunes, A., Almeida-Vara, E., Frère, J. M., Malcata, F. X., and Duarte, J. C. (2005) Molecular characterisation of a versatile peroxidase from a Bjerkandera strain, J. Biotechnol. 118, 339-352.
13. Heinfling, A., Ruiz-Dueñas, F. J., Martínez, M. J., Bergbauer, M., Szewzyk, U., and Martínez, A. T. (1998) A study on reducing substrates of manganese-oxidizing peroxidases from Pleurotus eryngii and Bjerkandera adusta, FEBS Lett. 428, 141-146.
14. Caramelo, L., Martínez, M. J., and Martínez, A. T. (1999) A search for ligninolytic peroxidases in the fungus Pleurotus eryngii involving α-keto-γ-thiomethylbutyric acid and lignin model dimers, Appl. Environ. Microbiol. 65, 916-922.
15. Flournoy, D. S., Paul, J. A., Kirk, T. K., and Highley, T. L. (1993) Changes in the size and volume of pores in sweetgum wood during simultaneous rot by Phanerochaete chrysosporium Burds, Holzforschung 47, 297-301.
16. Bao, W. L., Fukushima, Y., Jensen, K. A., Moen, M. A., and Hammel, K. E. (1994) Oxidative degradation of non-phenolic lignin during lipid peroxidation by fungal manganese peroxidase, FEBS Lett. 354, 297-300.
17. Bourbonnais, R., and Paice, M. G. (1990) Oxidation of non-phenolic substrates. An expanded role for laccase in lignin biodegradation, FEBS Lett. 267, 99-102.
18. Harvey, P. J., Schoemaker, H. E., and Palmer, J. M. (1986) Veratryl alcohol as a mediator and the role of radical cations in lignin biodegradation by Phanerochaete chrysosporium, FEBS Lett. 195, 242-246.
19. Glenn, J. K., Akileswaran, L., and Gold, M. H. (1986) Mn(II) oxidation is the principal function of the extracellular Mn-peroxidase from Phanerochaete chrysosporium, Arch. Biochem. Biophys. 251, 688-696.
20. Poulos, T. L., Edwards, S. L., Wariishi, H., and Gold, M. H. (1993) Crystallographic refinement of lignin peroxidase at 2 Å, J. Biol. Chem. 268, 4429-4440.
21. Sundaramoorthy, M., Kishi, K., Gold, M. H., and Poulos, T. L. (1994) The crystal structure of manganese peroxidase from Phanerochaete chrysosporium at 2.06-Å resolution, J. Biol. Chem. 269, 32759-32767.
22. Harris, R. Z., Wariishi, H., Gold, M. H., and Ortiz de Montellano, P. R. (1991) The catalytic site of manganese peroxidase. Regiospecific addition of sodium azide and alkylhydrazines to the heme group, J. Biol. Chem. 266, 8751-8758.
23. Sundaramoorthy, M., Kishi, K., Gold, M. H., and Poulos, T. L. (1997) Crystal structures of substrate binding site mutants of manganese peroxidase, J. Biol. Chem. 272, 17574-17580.
24. Kusters-van Someren, M., Kishi, K., Lundell, T., and Gold, M. H. (1995) The manganese binding site of manganese peroxidase: Characterization of an Asp179Asn site-directed mutant protein, Biochemistry 34, 10620-10627.
25. Kishi, K., Kusters-van Someren, M., Mayfield, M. B., Sun, J., Loehr, T. M., and Gold, M. H. (1996) Characterization of manganese(II) binding site mutants of manganese peroxidase, Biochemistry 35, 8986-8994.
26. Gelpke, M. D. S., Moënne-Loccoz, P., and Gold, M. H. (1999) Arginine 177 is involved in Mn(II) binding by manganese peroxidase, Biochemistry 38, 11482-11489.
27. II binding site of manganese peroxidase. Studies with R177D, R177E, R177N, and R177Q mutants, Eur. J. Biochem. 267, 7038-7045.
28. 2+ by both compound I and compound II, Biochemistry 36, 9766-9773.
29. Mester, T., and Tien, M. (2001) Engineering of a manganese-binding site in lignin peroxidase isozyme H8 from Phanerochaete chrysosporium, Biochem. Biophys. Res. Commun. 284, 723-728.
30. Wilcox, S. K., Putnam, C. D., Sastry, M., Blankenship, J., Chazin, W. J., McRee, D. E., and Goodin, D. B. (1998) Rational design of a functional metalloenzyme: Introduction of a site for manganese binding and oxidation into a heme peroxidase, Biochemistry 37, 16853-16862.
31. Yeung, B. K. S., Wang, X. T., Sigman, J. A., Petillo, P. A., and Lu, Y. (1997) Construction and characterization of a manganese-binding site in cytochrome c peroxidase: Towards a novel manganese peroxidase, Chem. Biol. 4, 215-221.
32. Banci, L., Camarero, S., Martínez, A. T., Martínez, M. J., Pérez-Boada, M., Pierattelli, R., and Ruiz-Dueñas, F. J. (2003) NMR study of Mn(II) binding by the new versatile peroxidase from the white-rot fungus Pleurotus eryngii, J. Biol. Inorg. Chem. 8, 751-760.
33. Pérez-Boada, M., Doyle, W. A., Ruiz-Dueñas, F. J., Martínez, M. J., Martínez, A. T., and Smith, A. T. (2002) Expression of Pleurotus eryngii versatile peroxidase in Escherichia coli and optimisation of in vitro folding, Enzyme Microb. Technol. 30, 518-524.
34. Pogni, R., Baratto, M. C., Teutloff, C., Giansanti, S., Ruiz-Dueñas, F. J., Choinowski, T., Piontek, K., Martínez, A. T., Lendzian, F., and Basosi, R. (2006) A tryptophan neutral radical in the oxidized state of versatile peroxidase from Pleurotus eryngii: a combined multi-frequency EPR and DFT study, J. Biol. Chem. 281, 9517-9526.
35. Pérez-Boada, M., Ruiz-Dueñas, F. J., Pogni, R., Basosi, R., Choinowski, T., Martinez, M. J., Piontek, K., and Martínez, A. T. (2005) Versatile peroxidase oxidation of high redox potential aromatic compounds: Site-directed mutagenesis, spectroscopic and crystallographic investigations of three long-range electron transfer pathways, J. Mol. Biol. 354, 385-402.
36. Doyle, W. A., Blodig, W., Veitch, N. C., Piontek, K., and Smith, A. T. (1998) Two substrate interaction sites in lignin peroxidase revealed by site-directed mutagenesis, Biochemistry 37, 15097-15105.
37. Weiner, M. P., Costa, G. L., Schoettlin, W., Cline, J., Mathur, E., and Bauer, J. C. (1994) Site-directed mutagenesis of double-stranded DNA by the polymerase chain reaction, Gene 151, 119-123.
38. Sambrook, J., and Russell, D. W. (2001) Molecular cloning, CSHL Press, Cold Spring Harbor, NY.
39. 4, Nature 227, 680-685.
40. Martínez, M. J., Ruiz-Dueñas, F. J., Guillén, F., and Martínez, A. T. (1996) Purification and catalytic properties of two manganese-peroxidase isoenzymes from Pleurotus eryngii, Eur. J. Biochem. 237, 424-432.
41. Kabsch, W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants, J. Appl. Crystallogr. 26, 795-800.
42. Navaza, J. (1994) Amore-An automated package for molecular replacement, Acta Crystallogr. A 50, 157-163.
43. Collaborative Computational Project No. 4 (1994) The CCP4 suite: programs from protein crystallography, Acta Crystallogr. D 50, 760-763.
44. Hatakka, A. (1994) Lignin-modifying enzymes from selected white-rot fungi-Production and role in lignin degradation, FEMS Microbiol Rev. 13, 125-135.
45. Hilden, K., Martínez, A. T., Hatakka, A., and Lundell, T. (2005) The two manganese peroxidases Pr-MnP2 and Pr-MnP3 of Phlebia radiata, a lignin-degrading basidiomycete, are phylogenetically and structurally divergent, Fungal Genet. Biol. 42, 403-419.
46. Stewart, P., Whitwam, R. E., Kersten, P. J., Cullen, D., and Tien, M. (1996) Efficient expression of a Phanerochaete chrysosporium manganese peroxidase gene in Aspergillus oryzae, Appl. Environ. Microbiol. 62, 860-864.
47. Pease, E. A., Aust, S. D., and Tien, M. (1991) Heterologous expression of active manganese peroxidase from Phanerochaete chrysosporium using the baculovirus expression system, Biochem. Biophys. Res. Commun. 179, 897-903.
48. Whitwam, R. E., Gazarian, I. G., and Tien, M. (1995) Expression of fungal Mn peroxidase in E. coli and refolding yield active enzyme, Biochem. Biophys. Res. Commun. 216, 1013-1017.
49. Ambert-Balay, K., Dougherty, M., and Tien, M. (2000) Reactivity of manganese peroxidase: Site-directed mutagenesis of residues in proximity to the porphyrin ring, Arch. Biochem. Biophys. 382, 89-94.
50. Youngs, H. L., Gelpke, M. D. S., Li, D. M., Sundaramoorthy, M., and Gold, M. H. (2001) The role of Glu39 in Mn-II binding and oxidation by manganese peroxidase from Phanerochaete chrysosporium, Biochemistry 40, 2243-2250.
51. Maeda, Y., Kajiwara, S., and Ohtaguchi, K. (2001) Manganese peroxidase gene of the perennial mushroom Elfvingia applanata: cloning and evaluation of its relationship with lignin degradation, Biotechnol. Lett. 23, 103-109.
52. Sundaramoorthy, M., Youngs, H. L., Gold, M. H., and Poulos, T. L. (2005) High-resolution crystal structure of manganese peroxidase: substrate and inhibitor complexes, Biochemistry 44, 6463-6470.
53. II is not a productive, substrate for wild-type or recombinant lignin peroxidase isozyme H2, Arch. Biochem. Biophys. 381, 16-24.