An updated view on horseradish peroxidases: recombinant production and biotechnological applications

Applied Microbiology and Biotechnology

Volumn 99, Issue 4, 2015, Pages 1611-1625

  Krainer, Florian W ^a   Glieder, Anton ^a  

^a GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

Biosensor; Cancer treatment; Diagnostics; Horseradish peroxidase; Indole 3 acetic acid; Plant peroxidase; Recombinant protein production

Indexed keywords

BIOCHEMISTRY; BIOREMEDIATION; BIOSENSORS; BIOTECHNOLOGY; CATALYSIS; DIAGNOSIS; DISEASES; ISOENZYMES; ONCOLOGY; PLASMA DIAGNOSTICS; RECOMBINANT PROTEINS;

BIOCHEMICAL PROPERTIES; BIOTECHNOLOGICAL APPLICATIONS; ENVIRONMENTAL CONDITIONS; HORSE-RADISH PEROXIDASE; HORSERADISH PEROXIDASE ENZYMES; INDOLE-3-ACETIC ACID; PLANT PEROXIDASE; RECOMBINANT PROTEIN PRODUCTIONS;

FOOD PRODUCTS;

HORSERADISH PEROXIDASE; ISOENZYME; PEROXIDASE; RECOMBINANT PROTEIN;

ACETIC ACID; BIOCHEMICAL COMPOSITION; BIOTECHNOLOGY; CANCER; CATALYSIS; DICOTYLEDON; ENZYME ACTIVITY; PROTEIN; RECOMBINATION;

BIOCATALYSIS; BIOREMEDIATION; BIOTECHNOLOGICAL PRODUCTION; ENZYME SYNTHESIS; ESCHERICHIA COLI; HUMAN; NONHUMAN; OXIDATION REDUCTION STATE; PROTEIN STRUCTURE; REVIEW; BIOTECHNOLOGY; ENZYMOLOGY; GENETICS; HORSERADISH; METABOLISM; PROCEDURES;

ARMORACIA RUSTICANA;

ARMORACIA; BIOTECHNOLOGY; PEROXIDASES; RECOMBINANT PROTEINS;

EID: 84922496820     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-6346-7     Document Type: Review

References (180)

1. Ahammad AJS, Sarker S, Lee J-J (2011) Immobilization of horseradish peroxidase onto a gold-nanoparticle-adsorbed poly(thionine) film for the construction of a hydrogen peroxide biosensor. J Nanosci Nanotechnol 11:5670–5
2. Aibara S, Kobayashi T, Morita Y (1981) Isolation and properties of basic isoenzymes of horseradish peroxidase. J Biochem 90:489–96
3. Aibara S, Yamashita H, Mori E, Kato M, Morita Y (1982) Isolation and characterization of five neutral isoenzymes of horseradish peroxidase. J Biochem 92:531–9
4. Alemzadeh I, Nejati S (2009) Phenols removal by immobilized horseradish peroxidase. J Hazard Mater 166:1082–6. doi:10.1016/j.jhazmat.2008.12.026
5. Alonso-Lomillo MA, Ruiz JG, Pascual FJM (2005) Biosensor based on platinum chips for glucose determination. Anal Chim Acta 547:209–214. doi:10.1016/j.aca.2005.05.037
6. Antipov E, Cho AE, Klibanov AM (2009) How a single-point mutation in horseradish peroxidase markedly enhances enantioselectivity. J Am Chem Soc 131:11155–60. doi:10.1021/ja903482u
7. Arnao MB, Acosta M, del Río JA, García-Cánovas F (1990a) Inactivation of peroxidase by hydrogen peroxide and its protection by a reductant agent. Biochim Biophys Acta 1038:85–9
8. Arnao MB, Acosta M, del Río JA, Varón R, García-Cánovas F (1990b) A kinetic study on the suicide inactivation of peroxidase by hydrogen peroxide. Biochim Biophys Acta 1041:43–7
9. Asad S, Dabirmanesh B, Ghaemi N, Etezad SM, Khajeh K (2013) Studies on the refolding process of recombinant horseradish peroxidase. Mol Biotechnol 54:484–92. doi:10.1007/s12033-012-9588-6
10. Azevedo AM, Martins VC, Prazeres DM, Vojinović V, Cabral JM, Fonseca LP (2003) Horseradish peroxidase: a valuable tool in biotechnology. Biotechnol Annu Rev 9:199–247. doi:10.1016/S1387-2656(03)09003-3
11. Azevedo AM, Prazeres DMF, Cabral JMS, Fonseca LP (2005) Ethanol biosensors based on alcohol oxidase. Biosens Bioelectron 21:235–47. doi:10.1016/j.bios.2004.09.030
12. Bagger S, Williams RJP, Schroll G, Lindberg AA, Lagerlund I, Ehrenberg L (1971) Intermediates in the reaction between hydrogen peroxide and horseradish peroxidase. Acta Chem Scand 25:976–982. doi:10.3891/acta.chem.scand. 25-0976
13. Barber JEB, Damry AM, Calderini GF, Walton CJW, Chica RA (2014) Continuous colorimetric screening assay for detection of d-amino acid aminotransferase mutants displaying altered substrate specificity. Anal Biochem 463:23–30. doi:10.1016/j.ab.2014.06.006
14. Bartonek-Roxå E, Eriksson H, Mattiasson B (1991) The cDNA sequence of a neutral horseradish peroxidase. Biochim Biophys Acta 1088:245–50
15. Bayramoğlu G, Arica MY (2008) Enzymatic removal of phenol and p-chlorophenol in enzyme reactor: horseradish peroxidase immobilized on magnetic beads. J Hazard Mater 156:148–55. doi:10.1016/j.jhazmat.2007.12.008
16. Bayramoglu G, Altintas B, Yakup Arica M (2012) Cross-linking of horseradish peroxidase adsorbed on polycationic films: utilization for direct dye degradation. Bioprocess Biosyst Eng 35:1355–65. doi:10.1007/s00449-012-0724-2
17. Berglund GI, Carlsson GH, Smith AT, Szöke H, Henriksen A, Hajdu J (2002) The catalytic pathway of horseradish peroxidase at high resolution. Nature 417:463–8. doi:10.1038/417463a
18. Bjellqvist B, Hughes GJ, Pasquali C, Paquet N, Ravier F, Sanchez JC, Frutiger S, Hochstrasser D (1993) The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. Electrophoresis 14:1023–31
19. Bjellqvist B, Basse B, Olsen E, Celis JE (1994) 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 15:529–39
20. Bódalo A, Bastida J, Máximo MF, Montiel MC, Gómez M, Murcia MD (2008) A comparative study of free and immobilized soybean and horseradish peroxidases for 4-chlorophenol removal: protective effects of immobilization. Bioprocess Biosyst Eng 31:587–93. doi:10.1007/s00449-008-0207-7
21. Boucher J, Vadon S, Tomas A, Viossat B, Mansuy D (1996) Oxidation of arylamidoximes by hydrogen peroxide and horseradish peroxidase in water: easy preparation and X-ray structure of O-(arylimidoyl)arylamidoximes. Tetrahedron Lett 37:3113–3116
22. Burke JF, Smith A, Santama N, Bray RC, Thorneley RN, Dacey S, Griffiths J, Catlin G, Edwards M (1989) Expression of recombinant horseradish peroxidase C in Escherichia coli. Biochem Soc Trans 17:1077–8
23. Cao X, Chen C, Yu H, Wang P (2014) Horseradish peroxidase-encapsulated chitosan nanoparticles for enzyme-prodrug cancer therapy. Biotechnol Lett. doi:10.1007/s10529-014-1664-5
24. Capone S, Pletzenauer R, Maresch D, Metzger K, Altmann F, Herwig C, Spadiut O (2014) Glyco-variant library of the versatile enzyme horseradish peroxidase. Glycobiology. doi:10.1093/glycob/cwu047
25. Chance B (1952) The kinetics and stoichiometry of the transition from the primary to the secondary peroxidase peroxide complexes. Arch Biochem Biophys 41:416–24
26. Chen H, Jiang C, Yu C, Zhang S, Liu B, Kong J (2009) Protein chips and nanomaterials for application in tumor marker immunoassays. Biosens Bioelectron 24:3399–411. doi:10.1016/j.bios.2009.03.020
27. Cheng J, Ming Yu S, Zuo P (2006) Horseradish peroxidase immobilized on aluminium-pillared inter-layered clay for the catalytic oxidation of phenolic wastewater. Water Res 40:283–90. doi:10.1016/j.watres.2005.11.017
28. Chiswell DJ, Ortlepp SA (1988) DNA sequence coding for HRP enzyme. EP0299682A1
29. Colonna S, Gaggero N, Carrea G, Pasta P (1992) Horseradish peroxidase catalysed sulfoxidation is enantioselective. J Chem Soc Chem Commun 357. doi: 10.1039/c39920000357
30. Colonna S, Gaggero N, Richelmi C, Pasta P (1999) Recent biotechnological developments in the use of peroxidases. Trends Biotechnol 17:163–8
31. Da Silva MR, de Sá LRV, Russo C, Scio E, Ferreira-Leitão VS (2011) The use of HRP in decolorization of reactive dyes and toxicological evaluation of their products. Enzym Res 2010:703824. doi:10.4061/2010/703824
32. Dai M, Liu J, Chen D-E, Rao Y, Tang Z-J, Ho W-Z, Dong C-Y (2012) Tumor-targeted gene therapy using Adv-AFP-HRPC/IAA prodrug system suppresses growth of hepatoma xenografted in mice. Cancer Gene Ther 19:77–83. doi:10.1038/cgt.2011.65
33. Dalal S, Gupta MN (2007) Treatment of phenolic wastewater by horseradish peroxidase immobilized by bioaffinity layering. Chemosphere 67:741–7. doi:10.1016/j.chemosphere.2006.10.043
34. Dalmazzo LFF, Santana-Lemos BA, Jácomo RH, Garcia AB, Rego EM, da Fonseca LM, Falcão RP (2011) Antibody-targeted horseradish peroxidase associated with indole-3-acetic acid induces apoptosis in vitro in hematological malignancies. Leuk Res 35:657–62. doi:10.1016/j.leukres.2010.11.025
35. Das PK, Caaveiro JMM, Luque S, Klibanov AM (2002) Binding of hydrophobic hydroxamic acids enhances peroxidase’s stereoselectivity in nonaqueous sulfoxidations. J Am Chem Soc 124:782–787. doi:10.1021/ja012075o
36. de las Segura M, Levin G, Miranda MV, Mendive FM, Targovnik HM, Cascone O (2005) High-level expression and purification of recombinant horseradish peroxidase isozyme C in SF-9 insect cell culture. Process Biochem 40:795–800. doi:10.1016/j.procbio.2004.02.009
37. De Melo MP, de Lima TM, Pithon-Curi TC, Curi R (2004) The mechanism of indole acetic acid cytotoxicity. Toxicol Lett 148:103–11. doi:10.1016/j.toxlet.2003.12.067
38. Derat E, Shaik S (2006) The Poulos-Kraut mechanism of compound I formation in horseradish peroxidase: a QM/MM study. J Phys Chem B 110:10526–33. doi:10.1021/jp055412e
39. Derat E, Shaik S, Rovira C, Vidossich P, Alfonso-Prieto M (2007) The effect of a water molecule on the mechanism of formation of compound 0 in horseradish peroxidase. J Am Chem Soc 129:6346–7. doi:10.1021/ja0676861
40. Dietzsch C, Spadiut O, Herwig C (2011a) A fast approach to determine a fed batch feeding profile for recombinant Pichia pastoris strains. Microb Cell Factories 10:85–94. doi:10.1186/1475-2859-10-85
41. Dietzsch C, Spadiut O, Herwig C (2011b) A dynamic method based on the specific substrate uptake rate to set up a feeding strategy for Pichia pastoris. Microb Cell Factories 10:14–22. doi:10.1186/1475-2859-10-14
42. Egorov AM, Gazaryan IG, Savelyev SV, Fechina VA, Veryovkin AN, Kim BB (1991) Horseradish peroxidase gene expression in Escherichia coli. Ann N Y Acad Sci 646:35–40
43. 2 nanoparticles using scanning electrochemical microscopy. Biosens Bioelectron 47:373–8. doi:10.1016/j.bios.2013.03.027
44. Flocco CG, Giulietti M (2003) Effect of chitosan on peroxidase activity and isoenzyme profile in hairy root cultures of Armoracia lapathifolia. Appl Biochem Biotechnol 110:175–83
45. Flocco CG, Alvarez MA, Giulietti AM (1998) Peroxidase production in vitro by Armoracia lapathifolia (horseradish)-transformed root cultures: effect of elicitation on level and profile of isoenzymes. Biotechnol Appl Biochem 28:33–8
46. Folkes LK, Wardman P (2001) Oxidative activation of indole-3-acetic acids to cytotoxic species—a potential new role for plant auxins in cancer therapy. Biochem Pharmacol 61:129–36
47. Folkes LK, Candeias LP, Wardman P (1998) Toward targeted “oxidation therapy” of cancer: peroxidase-catalysed cytotoxicity of indole-3-acetic acids. Int J Radiat Oncol Biol Phys 42:917–20. doi:10.1021/bi970384e
48. Folkes LK, Dennis MF, Stratford MR, Candeias LP, Wardman P (1999) Peroxidase-catalyzed effects of indole-3-acetic acid and analogues on lipid membranes, DNA, and mammalian cells in vitro. Biochem Pharmacol 57:375–82
49. Fujiyama K, Takemura H, Shibayama S, Kobayashi K, Choi JK, Shinmyo A, Takano M, Yamada Y, Okada H (1988) Structure of the horseradish peroxidase isozyme C genes. Eur J Biochem 173:681–7
50. Fujiyama K, Takemura H, Shinmyo A, Okada H, Takano M (1990) Genomic DNA structure of two new horseradish-peroxidase-encoding genes. Gene 89:163–9
51. Gajhede M, Schuller DJ, Henriksen A, Smith AT, Poulos TL (1997) Crystal structure of horseradish peroxidase C at 2.15 A resolution. Nat Struct Biol 4:1032–8
52. Galston AW, Bonner J, Baker RS (1953) Flavoprotein and peroxidase as components of the indoleacetic acid oxidase system of peas. Arch Biochem Biophys 42:456–70
53. Gasser B, Maurer M, Gach J, Kunert R, Mattanovich D (2006) Engineering of Pichia pastoris for improved production of antibody fragments. Biotechnol Bioeng 94:353–61. doi:10.1002/bit.20851
54. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) The proteomics protocols handbook: protein identification and analysis tools on the ExPASy server, 1st ed. Biochemical 71:571–607. doi:10.1134/S0006297906060150
55. Gazarian IG, Lagrimini LM, Mellon FA, Naldrett MJ, Ashby GA, Thorneley RN (1998) Identification of skatolyl hydroperoxide and its role in the peroxidase-catalysed oxidation of indol-3-yl acetic acid. Biochem J 333:223–32
56. George P (1952) Chemical nature of the secondary hydrogen peroxide compound formed by cytochrome-c peroxidase and horseradish peroxidase. Nature 169:612–3
57. George P (1953) The chemical nature of the second hydrogen peroxide compound formed by cytochrome c peroxidase and horseradish peroxidase. I. Titration with reducing agents. Biochem J 54:267–76
58. Greco O, Rossiter S, Kanthou C, Folkes LK, Wardman P, Tozer GM, Dachs GU (2001) Horseradish peroxidase-mediated gene therapy: choice of prodrugs in oxic and anoxic tumor conditions. Mol Cancer Ther 1:151–60
59. Greco O, Dachs GU, Tozer GM, Kanthou C (2002) Mechanisms of cytotoxicity induced by horseradish peroxidase/indole-3-acetic acid gene therapy. J Cell Biochem 87:221–232. doi:10.1002/jcb.10292
60. Grigorenko V, Chubar T, Kapeliuch Y, Börchers T, Spener F, Egorov A (1999) New approaches for functional expression of recombinant horseradish peroxidase C in Escherichia coli. Biocatal Biotransformation 17:359–379
61. Guerfal M, Ryckaert S, Jacobs PP, Ameloot P, Van Craenenbroeck K, Derycke R, Callewaert N (2010) The HAC1 gene from Pichia pastoris: characterization and effect of its overexpression on the production of secreted, surface displayed and membrane proteins. Microb Cell Factories 9:49. doi:10.1186/1475-2859-9-49
62. Hartmann C, Ortiz de Montellano PR (1992) Baculovirus expression and characterization of catalytically active horseradish peroxidase. Arch Biochem Biophys 297:61–72
63. Hartner FS, Ruth C, Langenegger D, Johnson SN, Hyka P, Lin-Cereghino GP, Lin-Cereghino J, Kovar K, Cregg JM, Glieder A (2008) Promoter library designed for fine-tuned gene expression in Pichia pastoris. Nucleic Acids Res 36:e76. doi:10.1093/nar/gkn369
64. Heggie L, Jansen MAK, Burbridge EM, Kavanagh TA, Thorneley RNF, Dix PJ (2005) Transgenic tobacco (Nicotiana tabacum L. cv. Samsun-NN) plants over-expressing a synthetic HRP-C gene are altered in growth, development and susceptibility to abiotic stress. Plant Physiol Biochem 43:1067–73. doi:10.1016/j.plaphy.2005.11.002
65. Henriksen A, Schuller DJ, Meno K, Welinder KG, Smith AT, Gajhede M (1998) Structural interactions between horseradish peroxidase C and the substrate benzhydroxamic acid determined by X-ray crystallography. Biochemistry 37:8054–60. doi:10.1021/bi980234j
66. 2. Biochem J 354:107–14
67. Hiner AN, Hernández-Ruíz J, García-Cánovas F, Smith AT, Arnao MB, Acosta M (1995) A comparative study of the inactivation of wild-type, recombinant and two mutant horseradish peroxidase isoenzymes C by hydrogen peroxide and m-chloroperoxybenzoic acid. Eur J Biochem 234:506–12
68. Hiner AN, Hernández-Ruíz J, Arnao MB, García-Cánovas F, Acosta M (1996) A comparative study of the purity, enzyme activity, and inactivation by hydrogen peroxide of commercially available horseradish peroxidase isoenzymes A and C. Biotechnol Bioeng 50:655–62. doi:10.1002/(SICI)1097-0290(19960620)50:6<655::AID-BIT6>3.0.CO;2-J
69. Hiner ANP, Hernández-Ruiz J, Rodríguez-López JN, Arnao MB, Varón R, García-Cánovas F, Acosta M (2001a) The inactivation of horseradish peroxidase isoenzyme A2 by hydrogen peroxide: an example of partial resistance due to the formation of a stable enzyme intermediate. J Biol Inorg Chem 6:504–16. doi:10.1007/s007750100219
70. Hiner AN, Hernández-Ruiz J, Williams GA, Arnao MB, García-Cánovas F, Acosta M (2001b) Catalase-like oxygen production by horseradish peroxidase must predominantly be an enzyme-catalyzed reaction. Arch Biochem Biophys 392:295–302. doi:10.1006/abbi.2001.2460
71. Hoyle MC (1977) High resolution of peroxidase-indoleacetic acid oxidase isoenzymes from horseradish by isoelectric focusing. Plant Physiol 60:787–93
72. Huang C, Liu L-Y, Song T-S, Ni L, Yang L, Hu X-Y, Hu J-S, Song L-P, Luo Y, Si L-S (2005) Apoptosis of pancreatic cancer BXPC-3 cells induced by indole-3-acetic acid in combination with horseradish peroxidase. World J Gastroenterol 11:4519–23
73. Jeong Y-M, Oh MH, Kim SY, Li H, Yun H-Y, Baek KJ, Kwon NS, Kim WY, Kim D-S (2010) Indole-3-acetic acid/horseradish peroxidase induces apoptosis in TCCSUP human urinary bladder carcinoma cells. Pharmazie 65:122–6
74. Jermyn MA (1952) Horseradish peroxidase. Nature 169:488–9
75. Jermyn MA, Thomas R (1954) Multiple components in horseradish peroxidase. Biochem J 56:631–9
76. Joo H, Lin Z, Arnold FH (1999) Laboratory evolution of peroxide-mediated cytochrome P450 hydroxylation. Nature 399:670–3. doi:10.1038/21395
77. Kafi AKM, Chen A (2009) A novel amperometric biosensor for the detection of nitrophenol. Talanta 79:97–102. doi:10.1016/j.talanta.2009.03.015
78. Kafi AKM, Wu G, Chen A (2008) A novel hydrogen peroxide biosensor based on the immobilization of horseradish peroxidase onto Au-modified titanium dioxide nanotube arrays. Biosens Bioelectron 24:566–71. doi:10.1016/j.bios.2008.06.004
79. Kagliwal LD, Singhal RS (2014) Enzyme-polysaccharide interaction: a method for improved stability of horseradish peroxidase. Int J Biol Macromol 69:329–35. doi:10.1016/j.ijbiomac.2014.05.065
80. Kalliney S, Zaks A (1995) An efficient peroxidase-catalyzed oxidation of hydroxylaminoeverninomicin in aqueous-organic media. Tetrahedron Lett 36:4163–4166. doi:10.1016/0040-4039(95)00713-M
81. Kalra B, Gross RA (2000) Horseradish peroxidase mediated free radical polymerization of methyl methacrylate. Biomacromolecules 1:501–5
82. Kanofsky JR (1988) Singlet oxygen production from the peroxidase-catalyzed oxidation of indole-3-acetic acid. J Biol Chem 263:14171–5
83. Kawaoka A, Kawamoto T, Moriki H, Murakami A, Murakami K, Yoshida K, Sekine M, Takano M, Shinmyo A (1994) Growth-stimulation of tobacco plant introduced the horseradish peroxidase gene prxC1a. J Ferment Bioeng 78:49–53. doi:10.1016/0922-338X(94)90177-5
84. Kawaoka A, Matsunaga E, Endo S, Kondo S, Yoshida K, Shinmyo A, Ebinuma H (2003) Ectopic expression of a horseradish peroxidase enhances growth rate and increases oxidative stress resistance in hybrid aspen. Plant Physiol 132:1177–85
85. Kay E, Shannon LM, Lew JY (1967) Peroxidase isozymes from horseradish roots. II. Catalytic properties. J Biol Chem 242:2470–3
86. Keilin D, Hartree EF (1951) Purification of horse-radish peroxidase and comparison of its properties with those of catalase and methaemoglobin. Biochem J 49:88–104
87. Kim D-S, Jeon S-E, Park K-C (2004) Oxidation of indole-3-acetic acid by horseradish peroxidase induces apoptosis in G361 human melanoma cells. Cell Signal 16:81–8. doi:10.1016/S0898-6568(03)00091-3
88. Kim D-S, Jeon S-E, Jeong Y-M, Kim S-Y, Kwon S-B, Park K-C (2006a) Hydrogen peroxide is a mediator of indole-3-acetic acid/horseradish peroxidase-induced apoptosis. FEBS Lett 580:1439–46. doi:10.1016/j.febslet.2006.01.073
89. Kim D-S, Kim S-Y, Jeong Y-M, Jeon S-E, Kim M-K, Kwon S-B, Park K-C (2006b) Indole-3-acetic acid/horseradish peroxidase-induced apoptosis involves cell surface CD95 (Fas/APO-1) expression. Biol Pharm Bull 29:1625–9
90. Kim SJ, Joo JC, Song BK, Yoo YJ, Kim YH (2014a) Engineering a horseradish peroxidase C stable to radical attacks by mutating multiple radical coupling sites. Biotechnol Bioeng 1–28. doi: 10.1002/bit.25483
91. Kim J, Kim J, Rho THD, Lee JH (2014b) Rapid chemiluminescent sandwich enzyme immunoassay capable of consecutively quantifying multiple tumor markers in a sample. Talanta 129:106–12. doi:10.1016/j.talanta.2014.05.020
92. Kis M, Burbridge E, Brock IW, Heggie L, Dix PJ, Kavanagh TA (2004) An N-terminal peptide extension results in efficient expression, but not secretion, of a synthetic horseradish peroxidase gene in transgenic tobacco. Ann Bot 93:303–10. doi:10.1093/aob/mch045
93. Koliasnikov OV, Grigorenko VG, Egorov AM, Lange S, Schmid RD (2011) Recombinant production of horseradish peroxidase conjugates with Fab antibodies in Pichia pastoris for analytical applications. Acta Nat 3:85–92
94. Krainer FW, Dietzsch C, Hajek T, Herwig C, Spadiut O, Glieder A (2012) Recombinant protein expression in Pichia pastoris strains with an engineered methanol utilization pathway. Microb Cell Factories 11:22–35. doi:10.1186/1475-2859-11-22
95. Krainer FW, Gmeiner C, Neutsch L, Windwarder M, Pletzenauer R, Herwig C, Altmann F, Glieder A, Spadiut O (2013a) Knockout of an endogenous mannosyltransferase increases the homogeneity of glycoproteins produced in Pichia pastoris. Sci Rep 3:3279–91. doi:10.1038/srep03279
96. Krainer FW, Pletzenauer R, Rossetti L, Herwig C, Glieder A, Spadiut O (2013b) Purification and basic biochemical characterization of 19 recombinant plant peroxidase isoenzymes produced in Pichia pastoris. Protein Expr Purif 95C:104–112. doi:10.1016/j.pep.2013.12.003
97. Kubota K, Mizukoshi T, Miyano H (2013) A new approach for quantitative analysis of L-phenylalanine using a novel semi-sandwich immunometric assay. Anal Bioanal Chem 405:8093–103. doi:10.1007/s00216-013-7081-0
98. Kulterer M, Reichel V, Ribitsch V, Glieder A, Krainer F (2013) Degradation of hormones using recombinant HRP isoenzymes. EP2628713A1
99. Kurokawa Y, Yanagi H, Yura T (2000) Overexpression of protein disulfide isomerase DsbC stabilizes multiple-disulfide-bonded recombinant protein produced and transported to the periplasm in Escherichia coli. Appl Environ Microbiol 66:3960–5. doi:10.1128/AEM. 66.9.3960-3965.2000
100. Levin G, Mendive F, Targovnik HM, Cascone O, Miranda MV (2005) Genetically engineered horseradish peroxidase for facilitated purification from baculovirus cultures by cation-exchange chromatography. J Biotechnol 118:363–9. doi:10.1016/j.jbiotec.2005.05.015
101. Li H, Zhao H, Liu C, Li Y, Cao H, Zhang Y (2013) A novel mechanism of bisphenol A removal during electro-enzymatic oxidative process: chain reactions from self-polymerization to cross-coupling oxidation. Chemosphere 92:1294–300. doi:10.1016/j.chemosphere.2013.04.071
102. Li T, Lin H, Yu L, Xue M, Ge S, Zhao Q, Zhang J, Xia N (2014) Development of an enzyme-linked immunospot assay for determination of rotavirus infectivity. J Virol Methods 209:7–14. doi:10.1016/j.jviromet.2014.08.012
103. Lin-Cereghino GP, Stark CM, Kim D, Chang J, Shaheen N, Poerwanto H, Agari K, Moua P, Low LK, Tran N, Huang AD, Nattestad M, Oshiro KT, Chang JW, Chavan A, Tsai JW, Lin-Cereghino J (2013) The effect of α-mating factor secretion signal mutations on recombinant protein expression in Pichia pastoris. Gene 519:311–7. doi:10.1016/j.gene.2013.01.062
104. Liu X, Luo L, Ding Y, Xu Y (2011) Amperometric biosensors based on alumina nanoparticles-chitosan-horseradish peroxidase nanobiocomposites for the determination of phenolic compounds. Analyst 136:696–701. doi:10.1039/c0an00752h
105. Loughran NB, O’Connell MJ, O’Connor B, O’Fágáin C (2014) Stability properties of an ancient plant peroxidase. Biochimie 104:156–9. doi:10.1016/j.biochi.2014.05.012
106. Malani RS, Khanna S, Moholkar VS (2013) Sonoenzymatic decolourization of an azo dye employing immobilized horse radish peroxidase (HRP): a mechanistic study. J Hazard Mater 256–257:90–7. doi:10.1016/j.jhazmat.2013.04.023
107. Marklund S, Ohlsson PI, Opara A, Paul KG (1974) The substrate profiles of the acidic and slightly basic horseradish peroxidases. Biochim Biophys Acta 350:304–13
108. Matsui T, Nakayama H, Yoshida K, Shinmyo A (2003) Vesicular transport route of horseradish C1a peroxidase is regulated by N- and C-terminal propeptides in tobacco cells. Appl Microbiol Biotechnol 62:517–22. doi:10.1007/s00253-003-1273-z
109. Matsui T, Hori M, Shizawa N, Nakayama H, Shinmyo A, Yoshida K (2006) High-efficiency secretory production of peroxidase C1a using vesicular transport engineering in transgenic tobacco. J Biosci Bioeng 102:102–9. doi:10.1263/jbb.102.102
110. Matsui T, Tabayashi A, Iwano M, Shinmyo A, Kato K, Nakayama H (2011) Activity of the C-terminal-dependent vacuolar sorting signal of horseradish peroxidase C1a is enhanced by its secondary structure. Plant Cell Physiol 52:413–20. doi:10.1093/pcp/pcq205
111. Miller VP, Goodin DB, Friedman AE, Hartmann C, Ortiz de Montellano PR (1995) Horseradish peroxidase Phe172 —> Tyr mutant. Sequential formation of compound I with a porphyrin radical cation and a protein radical. J Biol Chem 270:18413–9
112. Morawski B, Lin Z, Cirino P, Joo H, Bandara G, Arnold FH (2000) Functional expression of horseradish peroxidase in Saccharomyces cerevisiae and Pichia pastoris. Protein Eng 13:377–84
113. Morawski B, Quan S, Arnold FH (2001) Functional expression and stabilization of horseradish peroxidase by directed evolution in Saccharomyces cerevisiae. Biotechnol Bioeng 76:99–107
114. Morita Y, Mikami B, H. Y, Lee JY, Aibara S, Sato M, Katsube Y, Tanaka N (1991) Biochemical, molecular, and physiological aspects of plant peroxidases: primary and crystal structures of horseradish peroxidase isozyme E5. 81–88
115. Näätsaari L, Krainer FW, Schubert M, Glieder A, Thallinger GG (2014) Peroxidase gene discovery from the horseradish transcriptome. BMC Genomics 15:227. doi:10.1186/1471-2164-15-227
116. Newmyer SL, Ortiz de Montellano PR (1995) Horseradish peroxidase His-42 —> Ala, His-42 —> Val, and Phe-41 —> Ala mutants. Histidine catalysis and control of substrate access to the heme iron. J Biol Chem 270:19430–8
117. Newmyer SL, Ortiz de Montellano PR (1996) Rescue of the catalytic activity of an H42A mutant of horseradish peroxidase by exogenous imidazoles. J Biol Chem 271:14891–6
118. Newmyer SL, Sun J, Loehr TM, Ortiz de Montellano PR (1996) Rescue of the horseradish peroxidase His-170 —> Ala mutant activity by imidazole: importance of proximal ligand tethering. Biochemistry 35:12788–95. doi:10.1021/bi9609331
119. Nielsen KL, Indiani C, Henriksen A, Feis A, Becucci M, Gajhede M, Smulevich G, Welinder KG (2001) Differential activity and structure of highly similar peroxidases. Spectroscopic, crystallographic, and enzymatic analyses of lignifying Arabidopsis thaliana peroxidase A2 and horseradish peroxidase A2. Biochemistry 40:11013–21
120. O’Brien AM, O’Fágáin C, Nielsen PF, Welinder KG (2001) Location of crosslinks in chemically stabilized horseradish peroxidase: implications for design of crosslinks. Biotechnol Bioeng 76:277–84. doi:10.1002/bit.1194
121. Ortlepp SA, Pollard-Knight D, Chiswell DJ (1989) Expression and characterisation of a protein specified by a synthetic horseradish peroxidase gene in Escherichia coli. J Biotechnol 11:353–364. doi:10.1016/0168-1656(89)90019-9
122. Ozaki S, Ortiz de Montellano PR (1994) Molecular engineering of horseradish peroxidase. Highly enantioselective sulfoxidation of aryl alkyl sulfides by the Phe-41 —> Leu mutant. J Am Chem Soc 116:4487–4488. doi:10.1021/ja00089a052
123. Ozaki S, Ortiz de Montellano PR (1995) Molecular engineering of horseradish peroxidase: thioether sulfoxidation and styrene epoxidation by Phe-41 leucine and threonine mutants. J Am Chem Soc 117:7056–7064. doi:10.1021/ja00132a003
124. Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24:255–65. doi:10.1007/s00299-005-0972-6
125. Patris S, De Pauw P, Vandeput M, Huet J, Van Antwerpen P, Muyldermans S, Kauffmann J-M (2014) Nanoimmunoassay onto a screen printed electrode for HER2 breast cancer biomarker determination. Talanta 130:164–70. doi:10.1016/j.talanta.2014.06.069
126. Pereira AR, da Costa RS, Yokoyama L, Alhadeff EM, Teixeira LAC (2014) Evaluation of textile dye degradation due to the combined action of enzyme horseradish peroxidase and hydrogen peroxide. Appl Biochem Biotechnol 174:2741–7. doi:10.1007/s12010-014-1222-6
127. Planche LA (1810) Note sur la sophistication de la résine de jalap et sur les moyens de la reconnaître. Bull Pharm 2:578–580
128. Poulos TL, Kraut J (1980) The stereochemistry of peroxidase catalysis. J Biol Chem 255:8199–205
129. Preethi S, Anumary A, Ashokkumar M, Thanikaivelan P (2013) Probing horseradish peroxidase catalyzed degradation of azo dye from tannery wastewater. Springerplus 2:341. doi:10.1186/2193-1801-2-341
130. Raghu P, Madhusudana Reddy T, Reddaiah K, Jaidev LR, Narasimha G (2013) A novel electrochemical biosensor based on horseradish peroxidase immobilized on Ag-nanoparticles/poly(l-arginine) modified carbon paste electrode toward the determination of pyrogallol/hydroquinone. Enzym Microb Technol 52:377–385. doi:10.1016/j.enzmictec.2013.02.010
131. Regalado C, García-Almendárez BE, Duarte-Vázquez MA (2004) Biotechnological applications of peroxidases. Phytochem Rev 3:243–256. doi:10.1023/B:PHYT.0000047797.81958.69
132. Romero L, Targovnik A, Wolman F, Fogar M, Simonella M, Cascone O, Miranda M (2010) Recombinant peroxidase production in species of lepidoptera frequently found in Argentina. N Biotechnol 27:857–61. doi:10.1016/j.nbt.2010.06.019
133. Romero LV, Targovnik AM, Wolman FJ, Cascone O, Miranda MV (2011) Rachiplusia nu larva as a biofactory to achieve high level expression of horseradish peroxidase. Biotechnol Lett 33:947–56. doi:10.1007/s10529-011-0540-9
134. Ruiz-Valdepeñas Montiel V, Campuzano S, Conzuelo F, Torrente-Rodríguez RM, Gamella M, Reviejo AJ, Pingarrón JM (2015) Electrochemical magnetoimmunosensing platform for determination of the milk allergen β-lactoglobulin. Talanta 131:156–62. doi:10.1016/j.talanta.2014.07.076
135. Ryan BJ, O’Fágáin C (2007a) Effects of single mutations on the stability of horseradish peroxidase to hydrogen peroxide. Biochimie 89:1029–32. doi:10.1016/j.biochi.2007.03.013
136. Ryan BJ, O’Fágáin C (2007b) Arginine-to-lysine substitutions influence recombinant horseradish peroxidase stability and immobilisation effectiveness. BMC Biotechnol 7:86. doi:10.1186/1472-6750-7-86
137. Ryan BJ, O’Fágáin C (2008) Effects of mutations in the helix G region of horseradish peroxidase. Biochimie 90:1414–21. doi:10.1016/j.biochi.2008.05.008
138. Ryan BJ, Carolan N, O’Fágáin C (2006) Horseradish and soybean peroxidases: comparable tools for alternative niches? Trends Biotechnol 24:355–63. doi:10.1016/j.tibtech.2006.06.007
139. Ryan BJ, O’Connell MJ, O’Fágáin C (2008) Consensus mutagenesis reveals that non-helical regions influence thermal stability of horseradish peroxidase. Biochimie 90:1389–96. doi:10.1016/j.biochi.2008.04.009
140. Saikrishnan D, Goyal M, Rossiter S, Kukol A (2014) A cellulose-based bioassay for the colorimetric detection of pathogen DNA. Anal Bioanal Chem 406:7887–98. doi:10.1007/s00216-014-8257-y
141. Sakai S, Khanmohammadi M, Khoshfetrat AB, Taya M (2014) Horseradish peroxidase-catalyzed formation of hydrogels from chitosan and poly(vinyl alcohol) derivatives both possessing phenolic hydroxyl groups. Carbohydr Polym 111:404–9. doi:10.1016/j.carbpol.2014.05.010
142. Savenkova MI, Ortiz de Montellano PR (1998) Horseradish peroxidase: partial rescue of the His-42 —> Ala mutant by a concurrent Asn-70 —> Asp mutation. Arch Biochem Biophys 351:286–93. doi:10.1006/abbi.1997.0559
143. Savenkova MI, Newmyer SL, Ortiz de Montellano PR (1996) Rescue of His-42 —> Ala horseradish peroxidase by a Phe-41 —> His mutation. Engineering of a surrogate catalytic histidine. J Biol Chem 271:24598–603
144. Savenkova MI, Kuo JM, Ortiz de Montellano PR (1998) Improvement of peroxygenase activity by relocation of a catalytic histidine within the active site of horseradish peroxidase. Biochemistry 37:10828–36. doi:10.1021/bi9725780
145. Shannon LM, Kay E, Lew JY (1966) Peroxidase isozymes from horseradish roots. I. Isolation and physical properties. J Biol Chem 241:2166–72
146. Shih JHC, Shannon LM, Kay E, Lew JY (1971) Peroxidase isoenzymes from horseradish roots. IV. Structural relationships. J Biol Chem 246:4546–4551
147. Silva E, Edwards AM, Faljoni-Alario A (1990) Enzymatic generation of triplet acetone by deglycosylated horseradish peroxidase. Arch Biochem Biophys 276:527–30
148. Singh A, Ma D, Kaplan DL (2000) Enzyme-mediated free radical polymerization of styrene. Biomacromolecules 1:592–6
149. 2+ and heme. J Biol Chem 265:13335–43
150. Spadiut O, Rossetti L, Dietzsch C, Herwig C (2012) Purification of a recombinant plant peroxidase produced in Pichia pastoris by a simple 2-step strategy. Protein Expr Purif 86:89–97. doi:10.1016/j.pep.2012.09.008
151. Strickland EH, Kay E, Shannon LM, Horwitz J (1968) Peroxidase isoenzymes from horseradish roots. 3. Circular dichroism of isoenzymes and apoisoenzymes. J Biol Chem 243:3560–5
152. Tams JW, Welinder KG (1995) Mild chemical deglycosylation of horseradish peroxidase yields a fully active, homogeneous enzyme. Anal Biochem 228:48–55. doi:10.1006/abio.1995.1313
153. Tams JW, Welinder KG (1998) Glycosylation and thermodynamic versus kinetic stability of horseradish peroxidase. FEBS Lett 421:234–6
154. Theorell H, Maehly AC, Dam H, Kinell P-O (1950) Untersuchungen an künstlichen Peroxydasen. Acta Chem Scand 4:422–434. doi:10.3891/acta.chem.scand. 04-0422
155. Tognolli M, Penel C, Greppin H, Simon P (2002) Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 288:129–38
156. Tran HV, Piro B, Reisberg S, Huy Nguyen L, Dung Nguyen T, Duc HT, Pham MC (2014) An electrochemical ELISA-like immunosensor for miRNAs detection based on screen-printed gold electrodes modified with reduced graphene oxide and carbon nanotubes. Biosens Bioelectron 62:25–30. doi:10.1016/j.bios.2014.06.014
157. US Food and Drug Administration (2006) Phospholipase C enzyme preparation from Pichia pastoris expressing a heterologous phospholipase C gene. http://www.accessdata.fda.gov/scripts/fdcc/?set=GRASNotices&id=204 (Accessed Dec 2014)
158. Ulson de Souza SMAG, Forgiarini E, Ulson de Souza AA (2007) Toxicity of textile dyes and their degradation by the enzyme horseradish peroxidase (HRP). J Hazard Mater 147:1073–8. doi:10.1016/j.jhazmat.2007.06.003
159. Uozumi N, Kato Y, Nakashimada Y, Kobayashi T (1992) Excretion of peroxidase from horseradish hairy root in combination with ion supplementation. Appl Microbiol Biotechnol 37:560–565. doi:10.1007/BF00240725
160. Utashima Y, Matsumoto H, Masaki K, Iefuji H (2014) Heterologous production of horseradish peroxidase C1a by the basidiomycete yeast Cryptococcus sp. S-2 using codon and signal optimizations. Appl Microbiol Biotechnol 98:7893–900. doi:10.1007/s00253-014-5856-7
161. Varnado CL, Goodwin DC (2004) System for the expression of recombinant hemoproteins in Escherichia coli. Protein Expr Purif 35:76–83. doi:10.1016/j.pep.2003.12.001
162. Vasileva N, Godjevargova T, Ivanova D, Gabrovska K (2009) Application of immobilized horseradish peroxidase onto modified acrylonitrile copolymer membrane in removing of phenol from water. Int J Biol Macromol 44:190–4. doi:10.1016/j.ijbiomac.2008.12.002
163. Veillette M, Coutu M, Richard J, Batraville L-A, Désormeaux A, Roger M, Finzi A (2014) Conformational evaluation of HIV-1 trimeric envelope glycoproteins using a cell-based ELISA assay. J Vis Exp 91:51995. doi:10.3791/51995
164. Veitch NC, Smith AT (2001) Horseradish peroxidase. Adv Inorg Chem 51(51):107–162
165. Vidossich P, Fiorin G, Alfonso-Prieto M, Derat E, Shaik S, Rovira C (2010) On the role of water in peroxidase catalysis: a theoretical investigation of HRP compound I formation. J Phys Chem B 114:5161–9. doi:10.1021/jp911170b
166. Virel A, Saa L, Köster SD, Pavlov V (2010) Ultrasensitive optical detection of hydrogen peroxide by triggered activation of horseradish peroxidase. Analyst 135:2291–5. doi:10.1039/c0an00095g
167. Vlamis-Gardikas A, Smith AT, Clements JM, Burke JF (1992) Expression of active horseradish peroxidase in Saccharomyces cerevisiae. Biochem Soc Trans 20:111S
168. Vlasits J, Jakopitsch C, Bernroitner M, Zamocky M, Furtmüller PG, Obinger C (2010) Mechanisms of catalase activity of heme peroxidases. Arch Biochem Biophys 500:74–81. doi:10.1016/j.abb.2010.04.018
169. Walwyn DR, Huddy SM, Rybicki EP (2014) Techno-economic analysis of horseradish peroxidase production using a transient expression system in Nicotiana benthamiana. Appl Biochem Biotechnol. doi:10.1007/s12010-014-1320-5
170. Wang J, Fang B-S, Chou K-Y, Chen C-C, Gu Y (2014) A two-stage enzymatic synthesis of conductive poly(3,4-ethylenedioxythiophene). Enzym Microb Technol 54:45–50. doi:10.1016/j.enzmictec.2013.10.002
171. Welinder KG (1976) Covalent structure of the glycoprotein horseradish peroxidase (EC 1.11.1.7). FEBS Lett 72:19–23
172. Welinder KG (1979) 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 96:483–502
173. Willies SC, White JL, Turner NJ (2012) Development of a high-throughput screening method for racemase activity and its application to the identification of alanine racemase variants with activity towards l-arginine. Tetrahedron 68:7564–7567. doi:10.1016/j.tet.2012.06.062
174. Xu Y, Hou J, Liu Z, Yu H, Sun W, Xiong J, Liao Z, Zhou F, Xie C, Zhou Y (2011) Gene therapy with tumor-specific promoter mediated suicide gene plus IL-12 gene enhanced tumor inhibition and prolonged host survival in a murine model of Lewis lung carcinoma. J Transl Med 9:39. doi:10.1186/1479-5876-9-39
175. Yamazaki H, Yamazaki I (1973) The reaction between indole 3-acetic acid and horseradish peroxidase. Arch Biochem Biophys 154:147–59
176. Yang BY, Gray JS, Montgomery R (1996) The glycans of horseradish peroxidase. Carbohydr Res 287:203–12
177. Yin H, Wang M, Li B, Yang Z, Zhou Y, Ai S (2015) A sensitive electrochemical biosensor for detection of protein kinase A activity and inhibitors based on Phos-tag and enzymatic signal amplification. Biosens Bioelectron 63:26–32. doi:10.1016/j.bios.2014.07.016
178. Yu J-H, Klibanov AM (2006) Co-lyophilization with D-proline greatly enhances peroxidase’s stereoselectivity in a non-aqueous medium. Biotechnol Lett 28:555–8. doi:10.1007/s10529-006-0018-3
179. Zachetti VGL, Granero AM, Robledo SN, Zon MA, Fernández H (2013) Development of an amperometric biosensor based on peroxidases to quantify citrinin in rice samples. Bioelectrochemistry 91:37–43. doi:10.1016/j.bioelechem.2012.12.004
180. 2 nanoparticles. Bioprocess Biosyst Eng 34:923–930. doi:10.1007/s00449-011-0543-x