Purification and basic biochemical characterization of 19 recombinant plant peroxidase isoenzymes produced in Pichia pastoris

Protein Expression and Purification

Volumn 95, Issue , 2014, Pages 104-112

  Krainer, Florian W ^a   Pletzenauer, Robert ^b   Rossetti, Laura ^b   Herwig, Christoph ^b   Glieder, Anton ^c   Spadiut, Oliver ^b  

^a GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^b VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

^c AUSTRIAN CENTRE OF INDUSTRIAL BIOTECHNOLOGY   (Austria)

Author keywords

Glycosylation; Horseradish peroxidase; Monolith; Negative chromatography; Pichia pastoris; Protein purification

Indexed keywords

HORSERADISH PEROXIDASE; ISOENZYME; RECOMBINANT PROTEIN; VEGETABLE PROTEIN;

AFFINITY CHROMATOGRAPHY; ARTICLE; CHEMICAL PHENOMENA; CHEMISTRY; ENZYME STABILITY; GENETICS; GLYCOSYLATION; ISOLATION AND PURIFICATION; METABOLISM; MONOLITH; NEGATIVE CHROMATOGRAPHY; PICHIA; PICHIA PASTORIS; PROTEIN PURIFICATION;

GLYCOSYLATION; HORSERADISH PEROXIDASE; MONOLITH; NEGATIVE CHROMATOGRAPHY; PICHIA PASTORIS; PROTEIN PURIFICATION;

CHROMATOGRAPHY, AFFINITY; ENZYME STABILITY; HORSERADISH PEROXIDASE; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; ISOENZYMES; PICHIA; PLANT PROTEINS; RECOMBINANT PROTEINS;

EID: 84891699480     PISSN: 10465928     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pep.2013.12.003     Document Type: Article

References (57)

1. B. Chance The kinetics and stoichiometry of the transition from the primary to the secondary peroxidase peroxide complexes Arch. Biochem. Biophys. 41 1952 416 424
2. P. George Chemical nature of the secondary hydrogen peroxide compound formed by cytochrome-c peroxidase and horseradish peroxidase Nature 169 1952 612 613
3. P. George The chemical nature of the second hydrogen peroxide compound formed by cytochrome c peroxidase and horseradish peroxidase. I. Titration with reducing agents Biochem. J. 54 1953 267 276
4. L.A. Planche Note sur la sophistication de la résine de jalap et sur les moyens de la reconnaître Bull. Pharm. 2 1810 578 580
5. J.F. Kratochvil, R.H. Burris, M.K. Seikel, and J.M. Harkin Isolation and characterization of α-guaiaconic acid and the nature of guaiacum blue Phytochemistry 10 1971 2529 2531
6. A.J. Gross, and I.W. Sizer The oxidation of tyramine, tyrosine, and related compounds by peroxidase J. Biol. Chem. 234 1959 1611 1614
7. F. Passardi, C. Penel, and C. Dunand Performing the paradoxical: how plant peroxidases modify the cell wall Trends Plant Sci. 9 2004 534 540 (Pubitemid 39408748)
8. F. Passardi, C. Cosio, C. Penel, and C. Dunand Peroxidases have more functions than a Swiss army knife Plant Cell Rep. 24 2005 255 265 (Pubitemid 41116471)
9. M.C. Hoyle High resolution of peroxidase-indoleacetic acid oxidase isoenzymes from horseradish by isoelectric focusing Plant Physiol. 60 1977 787 793
10. M.A. Jermyn Horseradish peroxidase Nature 169 1952 488 489
11. M.A. Jermyn, and R. Thomas Multiple components in horseradish peroxidase Biochem. J. 56 1954 631 639
12. L.M. Shannon, E. Kay, and J.Y. Lew Peroxidase isozymes from horseradish roots. I. Isolation and physical properties J. Biol. Chem. 241 1966 2166 2172
13. E. Kay, L.M. Shannon, and J.Y. Lew Peroxidase isozymes from horseradish roots. II. Catalytic properties J. Biol. Chem. 242 1967 2470 2473
14. S. Marklund, P.I. Ohlsson, A. Opara, and K.G. Paul The substrate profiles of the acidic and slightly basic horseradish peroxidases Biochim. Biophys. Acta 350 1974 304 313
15. S. Aibara, T. Kobayashi, and Y. Morita Isolation and properties of basic isoenzymes of horseradish peroxidase J. Biochem. 90 1981 489 496
16. S. Aibara, H. Yamashita, E. Mori, M. Kato, and Y. Morita Isolation and characterization of five neutral isoenzymes of horseradish peroxidase J. Biochem. 92 1982 531 539
17. K. Fujiyama, H. Takemura, S. Shibayama, K. Kobayashi, J.K. Choi, and A. Shinmyo et al. Structure of the horseradish peroxidase isozyme C genes Eur. J. Biochem. 173 1988 681 687
18. M. Gajhede, D.J. Schuller, A. Henriksen, A.T. Smith, and T.L. Poulos Crystal structure of horseradish peroxidase C at 2.15 A resolution Nat. Struct. Biol. 4 1997 1032 1038 (Pubitemid 27525808)
19. K.G. Welinder Amino acid sequence studies of horseradish peroxidase. Amino and carboxyl termini, cyanogen bromide and tryptic fragments, the complete sequence, and some structural characteristics of horseradish peroxidase C Eur. J. Biochem. 96 1979 483 502
20. B.Y. Yang, J.S. Gray, and R. Montgomery The glycans of horseradish peroxidase Carbohydr. Res. 287 1996 203 212 (Pubitemid 26266989)
21. J.W. Tams, and K.G. Welinder Mild chemical deglycosylation of horseradish peroxidase yields a fully active, homogeneous enzyme Anal. Biochem. 228 1995 48 55
22. J.W. Tams, and K.G. Welinder Glycosylation and thermodynamic versus kinetic stability of horseradish peroxidase FEBS Lett. 421 1998 234 236 (Pubitemid 28045761)
23. C.B. Lavery, M.C. Macinnis, M.J. Macdonald, J.B. Williams, C.A. Spencer, and A.A. Burke et al. Purification of peroxidase from Horseradish (Armoracia rusticana) roots J. Agric. Food Chem. 58 2010 8471 8476
24. 2+ and heme J. Biol. Chem. 265 1990 13335 13343
25. V. Grigorenko, T. Chubar, Y. Kapeliuch, T. Börchers, F. Spener, and A. Egorov New approaches for functional expression of recombinant horseradish peroxidase C in Escherichia coli Biocatalysis Biotransformation 17 1999 359 379 (Pubitemid 30019205)
26. C. Hartmann, and P.R. Ortiz de Montellano Baculovirus expression and characterization of catalytically active horseradish peroxidase Arch. Biochem. Biophys. 297 1992 61 72
27. M. de las, M. Segura, G. Levin, M.V. Miranda, F.M. Mendive, H.M. Targovnik, and O. Cascone High-level expression and purification of recombinant horseradish peroxidase isozyme C in SF-9 insect cell culture Process Biochem. 40 2005 795 800 (Pubitemid 39437884)
28. A. Vlamis-Gardikas, A.T. Smith, J.M. Clements, and J.F. Burke Expression of active horseradish peroxidase in Saccharomyces cerevisiae Biochem. Soc. Trans. 20 1992 111S
29. B. Morawski, Z. Lin, P. Cirino, H. Joo, G. Bandara, and F.H. Arnold Functional expression of horseradish peroxidase in Saccharomyces cerevisiae and Pichia pastoris Protein Eng. 13 2000 377 384 (Pubitemid 30339361)
30. B. Morawski, S. Quan, and F.H. Arnold Functional expression and stabilization of horseradish peroxidase by directed evolution in Saccharomyces cerevisiae Biotechnol. Bioeng. 76 2001 99 107
31. F.W. Krainer, C. Dietzsch, T. Hajek, C. Herwig, O. Spadiut, and A. Glieder Recombinant protein expression in Pichia pastoris strains with an engineered methanol utilization pathway Microb. Cell Factor 11 2012 22 35
32. C. Dietzsch, O. Spadiut, and C. Herwig A dynamic method based on the specific substrate uptake rate to set up a feeding strategy for Pichia pastoris Microb. Cell Factor 10 2011 14 22
33. O. Spadiut, L. Rossetti, C. Dietzsch, and C. Herwig Purification of a recombinant plant peroxidase produced in Pichia pastoris by a simple 2-step strategy Protein Expr. Purif. 86 2012 89 97
34. M.G. Brattain, M.E. Marks, and T.G. Pretlow The purification of horseradish peroxidase by affinity chromatography on Sepharose-bound concanavalin A1,2 Anal. Biochem. 72 1976 346 352
35. M.V. Miranda, H.M. Fernández-Lahore, J. Dobrecky, and O. Cascone The extractive purification of peroxidase from plant raw materials in aqueous two-phase systems Acta Biotechnol. 18 1998 179 188 (Pubitemid 28488374)
36. W. Guo, and E. Ruckenstein Separation and purification of horseradish peroxidase by membrane affinity chromatography J. Membr. Sci. 211 2003 101 111 (Pubitemid 35448117)
37. L.F. Fraguas, F. Batista-Viera, and J. Carlsson Preparation of high-density concanavalin A adsorbent and its use for rapid, high-yield purification of peroxidase from horseradish roots J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 803 2004 237 241 (Pubitemid 38452444)
38. A. Glieder, F.W. Krainer, M. Kulterer, L. Näätsaari, V. Reichel, Horseradish peroxidase isoenzymes, EP2584035 A1, 2013.
39. S.K. Sharma, N. Sehgal, and A. Kumar A quick and simple biostrip technique for detection of lactose Biotechnol. Lett. 24 2002 1737 1739 (Pubitemid 35326058)
40. C.C. Chiou, P.Y. Chang, E.C. Chan, T.L. Wu, K.C. Tsao, and J.T. Wu Urinary 8-hydroxydeoxyguanosine and its analogs as DNA marker of oxidative stress: development of an ELISA and measurement in both bladder and prostate cancers Clin. Chim. Acta 334 2003 87 94 (Pubitemid 36836061)
41. A. Singh, D. Ma, and D.L. Kaplan Enzyme-mediated free radical polymerization of styrene Biomacromolecules 1 2000 592 596
42. N. Vasileva, T. Godjevargova, D. Ivanova, and K. Gabrovska Application of immobilized horseradish peroxidase onto modified acrylonitrile copolymer membrane in removing of phenol from water Int. J. Biol. Macromol. 44 2009 190 194
43. O. Greco, S. Rossiter, C. Kanthou, L.K. Folkes, P. Wardman, and G.M. Tozer et al. Horseradish peroxidase-mediated gene therapy: choice of prodrugs in oxic and anoxic tumor conditions Mol. Cancer Ther. 1 2001 151 160
44. L. Näätsaari, B. Mistlberger, C. Ruth, T. Hajek, F.S. Hartner, and A. Glieder Deletion of the Pichia pastoris KU70 homologue facilitates platform strain generation for gene expression and synthetic biology PLoS One 7 2012 e39720
45. R. Weis, R. Luiten, W. Skranc, H. Schwab, M. Wubbolts, and A. Glieder Reliable high-throughput screening with Pichia pastoris by limiting yeast cell death phenomena FEMS Yeast Res. 5 2004 179 189 (Pubitemid 39360920)
46. O. Spadiut, C. Leitner, C. Salaheddin, B. Varga, B.G. Vertessy, and T.-C. Tan et al. Improving thermostability and catalytic activity of pyranose 2-oxidase from Trametes multicolor by rational and semi-rational design FEBS J. 276 2009 776 792
47. D. Mattanovich, A. Graf, J. Stadlmann, M. Dragosits, A. Redl, and M. Maurer et al. Genome, secretome and glucose transport highlight unique features of the protein production host Pichia pastoris Microb. Cell Factor 8 2009 29
48. C.-J. Huang, L.M. Damasceno, K.A. Anderson, S. Zhang, L.J. Old, and C.A. Batt A proteomic analysis of the Pichia pastoris secretome in methanol-induced cultures Appl. Microbiol. Biotechnol. 90 2011 235 247
49. H. Podgornik, A. Podgornik, and A. Perdih A method of fast separation of lignin peroxidases using convective interaction media disks Anal. Biochem. 272 1999 43 47 (Pubitemid 29343380)
50. H. Podgornik, A. Podgornik, P. Milavec, and A. Perdih The effect of agitation and nitrogen concentration on lignin peroxidase (LiP) isoform composition during fermentation of Phanerochaete chrysosporium J. Biotechnol. 88 2001 173 176 (Pubitemid 32524254)
51. H. Podgornik, and A. Podgornik Separation of manganese peroxidase isoenzymes on strong anion-exchange monolithic column using pH-salt gradient J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 799 2004 343 347 (Pubitemid 37510238)
52. M. Barut, A. Podgornik, P. Brne, and A. Strancar Convective interaction media short monolithic columns: enabling chromatographic supports for the separation and purification of large biomolecules J. Sep. Sci. 28 2005 1876 1892 (Pubitemid 41614722)
53. A.N. Hiner, J. Hernández-Ruíz, M.B. Arnao, F. García-Cánovas, and M. Acosta A comparative study of the purity, enzyme activity, and inactivation by hydrogen peroxide of commercially available horseradish peroxidase isoenzymes A and C Biotechnol. Bioeng. 50 1996 655 662 (Pubitemid 26152238)
54. D.J. Gilfoyle, J.N. Rodriguez-Lopez, and A.T. Smith Probing the aromatic-donor-binding site of horseradish peroxidase using site-directed mutagenesis and the suicide substrate phenylhydrazine Eur. J. Biochem. 236 1996 714 722 (Pubitemid 26098854)
55. B. Bjellqvist, G.J. Hughes, C. Pasquali, N. Paquet, F. Ravier, and J.C. Sanchez et al. The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences Electrophoresis 14 1993 1023 1031 (Pubitemid 23359589)
56. B. Bjellqvist, B. Basse, E. Olsen, and J.E. Celis Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions Electrophoresis 15 1994 529 539 (Pubitemid 24151853)
57. R. Gupta, E. Jung, S. Brunak, Prediction of N-glycosylation sites in human proteins, 2004 (in preparation).