Kinetic and thermodynamic characterization of the functional properties of a hybrid versatile peroxidase using isothermal titration calorimetry: Insight into manganese peroxidase activation and lignin peroxidase inhibition

Biochimie

Volumn 94, Issue 5, 2012, Pages 1221-1231

  Ertan, Haluk ^a,b   Siddiqui, Khawar Sohail ^a   Muenchhoff, Julia ^a   Charlton, Tim ^a   Cavicchioli, Ricardo ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b ISTANBUL UNIVERSITY   (Turkey)

Author keywords

Allosteric substrate activation and inhibition; Azo dye; Bjerkandera adusta peroxidase; Enzyme kinetics and activation thermodynamics; Methylene blue

Indexed keywords

DYE; HYBRID PROTEIN; LIGNIN PEROXIDASE; MANGANESE PEROXIDASE; PEROXIDASE;

ACCURACY; ARTICLE; BINDING AFFINITY; BINDING SITE; BJERKANDERA; CATALYSIS; ENERGY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME KINETICS; ENZYME STRUCTURE; ENZYME SUBSTRATE; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; PH; THERMODYNAMICS;

CALORIMETRY; CORIOLACEAE; FUNGAL PROTEINS; KINETICS; PEROXIDASES; THERMODYNAMICS;

BJERKANDERA; BJERKANDERA ADUSTA;

EID: 84859420715     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2012.02.012     Document Type: Article

References (45)

1. D.W.S. Wong Structure and action mechanism of ligninolytic enzymes Appl. Biochem. Biotechnol. 157 2009 174 209
2. I. Morgenstern, S. Klopman, and D.S. Hibbett Molecular evolution and diversity of lignin degrading heme peroxidases in the Agaricomycetes J. Mol. Evol. 66 2008 243 257
3. Q. Husain Peroxidase mediated decolorization and remediation of wastewater containing industrial dyes: a review Rev. Environ. Sci. Biotechnol. 9 2010 117 140
4. Y. Wang, R. Vazquez-Duhalt, and M.A. Pickard Manganese-lignin peroxidase hybrid from Bjerkandera adusta oxidizes polycyclic aromatic hydrocarbons more actively in the absence of manganese Can. J. Microbiol. 49 2003 675 682
5. M.R. Mauk, K. Kishi, M.H. Gold, and A.G. Mauk pH-linked binding of Mn(II) to manganese peroxidase Biochemistry 37 1998 6767 6771
6. M. Sundaramoorthy, H.L. Youngs, M.H. Gold, and T.H. Poulos High-resolution crystal structure of manganese peroxidase: substrate and inhibitor complexes Biochemistry 44 2005 6463 6470
7. B. Valderrama, H. García-Arellano, S. Giansanti, M.C. Baratto, R. Pogni, and R. Vazquez-Duhalt Oxidative stabilization of iso-1-cytochrome c by redox-inspired protein engineering FASEB J. 20 2006 1233 1235
8. R. Pogni, M.C. Baratto, S. Giansanti, C. Teutloff, J. Verdin, B. Valderrama, F. Lendzian, W. Lubitz, R. Vazquez-Duhalt, and R. Basosi Tryptophan-based radical in the catalytic mechanism of versatile peroxidase from Bjerkandera adusta Biochemistry 44 2005 4267 4274
9. F.J. Ruiz-Dueñas, M. Morales, E. Garcia, Y. Miki, M.J. Martinez, and A.T. Martinez Substrate oxidation sites in versatile peroxidase and other basidiomycetes peroxidases J. Exp. Bot. 60 2009 441 452
10. T.L. Poulos, S.L. Edwards, H. Wariishi, and M.H. Gold Crystallographic refinement of lignin peroxidise at 2Δ J. Biol. Chem. 268 1993 4429 4440
11. M. Pérez-Boada, F.J. Ruiz-Dueñas, R. Pogni, R. Basosi, T. Choinowski, M.J. Martínez, K. Piontek, and A.T. Martínez Versatile peroxidase oxidation of high redox potential aromatic compounds: site-directed mutagenesis, spectroscopic and crystallographic investigation of three long-range electron transfer pathways J. Mol. Biol. 354 2005 385 402
12. F.J. Ruiz-Dueñas, M. Morales, M.J. Mate, A. Romero, M.J. Martínez, A.T. Smith, and A.T. Martínez Site-directed mutagenesis of the catalytic tryptophan environment in Pleurotus eryngii versatile peroxidase Biochemistry 47 2008 1685 1695
13. A. Heinfling, F.J. Ruiz-Dueñas, M.J. Martinez, M. Bergbauer, U. Szrwzyk, and A.T. Martinez A study on reducing substrates of manganese-oxidizing peroxidases from Pleurotus eryngii and Bjerkandera adusta FEBS Lett. 428 1998 141 146
14. T. Mester, and J.A. Field Characterization of a novel manganese peroxidase-lignin peroxidase hybrid isozyme produced by Bjerkandera species strain BOS55 in the absence of manganese J. Biol. Chem. 273 1998 15412 15417
15. S. Camarero, S. Sarkar, F.J. Ruiz-Dueñas, M.J. Martínez, and A.T. Martínez Description of a versatile peroxidase involved in the natural degradation of lignin that has both manganese peroxidase and lignin peroxidase substrate interaction sites J. Biol. Chem. 274 1999 10324 10330
16. P.R. Moreira, F. Bouillenne, E. Almeida-Vara, J.M. Frre, F.X. Malcata, J.M. Frere, and J.C. Duarte Purification, kinetics and spectral characterization of a new versatile peroxidase from a Bjerkandera sp. Isolate Enzym. Microb. Tech. 38 2006 28 33
17. T. Tsukihara, Y. Honda, R. Sakai, T. Watanabe, and T. Watanabe Mechanism for oxidation of high-molecular-weight substrates by a fungal versatile peroxidase, MnP2 Appl. Environ. Microbiol. 74 2008 2873 2881
18. Y. Suga, T. Yomo, and I. Urabe Heme content of catalase I from Bacillus stearothermophilus J. Ferment. Bioeng. 81 1996 259 261
19. G. Nie, S. Reading, and S.D. Aust Relative stability of recombinant versus native peroxidases from Phanerochaete chrysosporium Arch. Biochem. Biophys. 365 1999 328 334
20. K. Arnold, L. Bordoli, J. Kopp, and T. Schwede The SWISS-MODEL Workspace: a web-based environment for protein structure homology modelling Bioinformatics 22 2006 195 201
21. D.B. Magalhaes, M.E.A. De Carvalho, E. Bon, J.S.A. Neto, and S.H. Kling Colorimetric assay for lignin peroxidase activity determination using methylene blue as substrate Biotechnol. Techniques 10 1996 273 276
22. M.P. Castillo, J. Stenström, and P. Ander Determination of manganese peroxidase activity with 3-methyl-2-benzothiazolinone hydrazone and 3-(dimethylamino)benzoic acid Anal. Biochem. 218 1994 399 404
23. M.W. Freyer, and E.A. Lewis Isothermal titration calorimetrey: experimental design, data analysis and probing macromolecular/ligand binding and kinetic interactions Method. Cell Biol. 84 2008 79 113
24. M.J. Todd, and J. Gomez Enzyme kinetics determined using calorimetry: a general assay for enzyme activity Anal. Biochem. 296 2001 179 187
25. The Calorimetry Experts Use of Isothermal Titration Calorimetry to Measure Enzyme Kinetics Parameters 2003 ITC Application Note (October) available at: www.microcalorimetry.com
26. M. Lakomek, M. Scharnetzky, W. Tillmann, W. Schröter, and H. Winkler On the temperature- and salt-dependent conformation change in human erythrocyte pyruvate kinase Hoppe Seylers Z. Physiol. Chem. 364 1983 787 792
27. A. Giordano, F. Febbraio, C. Russo, M. Rossi, and C.A. Raia Evidence for co-operativity in coenzyme binding to tetrameric Sulfolobus solfataricus alcohol dehydrogenase and its structural basis: fluorescence, kinetic and structural studies of the wild-type enzyme and non-co-operative N249Y mutant Biochem. J. 388 2005 657 667
28. O. Kolaj-Robin, S.R. O'Kane, W. Nitschke, C. Léger, F. Baymann, and T. Soulimane Biochemical and biophysical characterization of succinate: quinone reductase from Thermus thermophilus Biochim. Biophys. Acta 1807 2011 68 79
29. K.S. Siddiqui, D.M. Parkin, P.M.G. Curmi, D. De Francisci, A. Poljak, K. Barrow, M.H. Noble, J. Trewhella, and R. Cavicchioli A novel approach for enhancing the catalytic efficiency of a protease at low temperature: reduction in substrate inhibition by chemical modification Biotechnol. Bioeng. 103 2009 676 686
30. E. Niday, C.-S. Wang, and P. Alaupovic Kinetic evidence for the allosteric substrate inhibition of human erythrocyte acetylcholinesterase Biochim. Biophys. Acta 612 1980 67 72
31. K.S. Siddiqui, R. Cavicchioli, and T. Thomas Thermodynamic activation properties of elongation factor 2 (EF-2) proteins from psychrotolerant and thermophilic Archaea Extremophiles 6 2002 143 150
32. I.H. Segal Multisite and allosteric enzymes Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-state Enzyme Systems 1993 John Wiley and Sons New York 346 464
33. K.S. Siddiqui, A. Poljak, D. De Francisci, G. Guerriero, O. Pilak, D. Burg, M.J. Raftery, D.M. Parkin, J. Trewhella, and R. Cavicchioli A chemically modified alpha-amylase with a molten-globule state has entropically driven enhanced thermal stability Protein Eng. Des. Sel 23 2010 769 780
34. R. Tinoco, J. Verdin, and R. Vazquez-Duhalt Role of oxidizing mediators and tryptophan 172 in the decoloration of industrial dyes by the versatile peroxidise from Bjerkandera adusta J. Mol. Catal. B-Enzy 46 2007 1 7
35. L. Murphy, M.J. Baumann, K. Borch, M. Sweeney, and P. Westh An enzymatic signal amplification system for calorimetric studies of cellobiohydrolases Anal. Biochem. 404 2010 140 148
36. T. Lonhienne, C. Gerday, and G. Feller Psychrophilic enzymes: revisiting the thermodynamic parameters of activation may explain local flexibility Biochim. Biophys. Acta 1543 2000 1 10
37. K.S. Siddiqui, and R. Cavicchioli Cold-adapted enzymes Annu. Rev. Biochem. 75 2006 403 433
38. F.J. Ruiz-Dueñas, M. Morales, M. Pérez-Boada, T. Choinowski, M.J. Martinez, K. Piontek, and A.T. Martinez Manganese oxidation site in Pleurotus eryngii versatile peroxidase: a site-directed mutagenesis, kinetic and crystallographic study Biochemistry 46 2007 66 77
39. F. Krieger, M. Spinka, R. Golbik, G. Hubner, and S. Konig Pyruvate decarboxylase from Kluyveromyces lactis. An enzyme with an extraordinary substrate activation behavior Eur. J. Biochem. 269 2002 3256 3263
40. T. Traut Regulatory Allosteric Enzymes 2008 Springer New York
41. M.D. Aitken, and R.L. Irvine Characterization of reactions catalyzed by manganese peroxidase from Phanerochaete chrysosporium Arch. Biochem. Biophys. 276 1990 405 414
42. M.D. Gelpke, H.L. Youngs, and M.H. Gold Role of arginine 177 in the MnII binding site of manganese peroxidase. Studies with R177D, R177E, R177N, and R177Q mutants Eur. J. Biochem. 267 2000 7038 7045
43. S. Augustin, H. Stephanowitz, B. Wolff, J. Schroder, and E. Hoffmann Manganese in tree rings of Norway spruce as an indicator for soil chemical changes in the past Eur. J. For. Res. 124 2005 313 318
44. R.A. Blanchette Manganese accumulation in wood decayed by white rot fungi Ecol. Epidem 74 1984 725 730
45. G. Daniel, and O. Bergman White rot and manganese deposition in TnBTO-AAC preservative treated pine stakes from field tests Holz als Roh- und Werkstoff 55 1997 197 201