This investigation is aimed at understanding the specific role of pH and calcium
ions on the activity and stability of wild-type
recombinant Phlebia radiata manganese
peroxidase 3 (rPr-MnP3).
The pH-dependent cycle of reactions for rPr-MnP3 was evaluated by investigating
time-dependent changes in the activity and electronic absorption spectrum of rPr-MnP3.The rPr-MnP3 had maximum efficacy (kcat/Km) for Mn (II)
oxidation at pH 5.0 and 3.0 for oxidation of ABTS. Raising the pH of a solution
of resting rPr-MnP3 from pH 6.7 (form XH) to pH 8.6 (form X−),
a rapid alkaline transition occurs. Leaving the X− form of the enzyme
at pH 8.6, it slowly becomes converted to a third form of the enzyme Y−,
which returned to the original XH form of the enzyme at pH 6.7. Recovery of form
XH from form Y− occurred through an intermediate Z form. The pH inactivation
of rPr-MnP3 followed first-order kinetics. The rate of formation of XH from Z is
pH-dependent and biphasic in nature, with measured rate constants (k) = 0.25 min−1,
and half-life (T1/2) = 2.8 min. The pH-dependent properties observed
may be indicative of a greater degree of conformational flexibility at rPr-MnP3
active site due to disruption of the haem-linked hydrogen-bonding network in the
distal haem pocket. Calcium ions were observed
to significantly stabilised the enzyme’s spectral features and reduce the loss of
activity during the alkaline pH transition. Calcium ions enhance the recovery of
the initial activity but cannot prevent
the final time-dependent
irreversible denaturation and aggregation.
References
[1]
Vares, T., Kalsi, M. and Hatakka, A. (1995) Lignin Peroxidases, Manganese Peroxidases, and Other Ligninolytic Enzymes Produced by Phlebia radiata during Solid-State Fermentation Of Wheat-Straw. Applied and Environmental Microbiology, 61, 3515-3520. https://doi.org/10.1128/aem.61.10.3515-3520.1995
[2]
Hatakka, A., Lundell, T., Hofrichter, M. and Maijala, P. (2003) Manganese Peroxidase and Its Role in the Degradation of Wood Lignin. In: Mansfield, S.D. and Saddler, J.N., Eds., Applications of Enzymes to Lignocellulosics, American Chemical Society (ACS) Symposium Series 855, Washington DC, 230-243.
https://doi.org/10.1021/bk-2003-0855.ch014
[3]
Lundell, T., Leonowicz, A., Rogalski, J. and Hatakka, A. (1990) Formation and Action of Lignin Modifying Enzymes in Cultures of Phlebia radiata Supplemented with Veratric Acid. Applied and Environmental Microbiology, Journal, 56, 2623-2629. https://doi.org/10.1128/aem.56.9.2623-2629.1990
[4]
Niemenmaa, O., Uusi-Rauva, A.K. and Hatakka, A. (2006) Wood Stimulates the Demethoxylation of [O14CH3]-Labeled Lignin Model Compounds by the White-Rot Fungi Phanerochaete chrysosporium and Phlebia radiata. Archives of Microbiology, 185, 307-315. https://doi.org/10.1007/s00203-006-0097-5
[5]
Hatakka, A.I. and Uusi-Rauva, A.K. (1983) Degradation of IT Labelled Poplar Wood Lignin by Selected White-Rot Fungi. European Journal of Applied Microbiology and Biotechnology, 17, 235-242. https://doi.org/10.1007/BF00510422
[6]
Hammel, K.E. and Cullen, D. (2008) Role of Fungal Peroxidases in Biological Ligninolysis. Current Opinion in Plant Biology, 11, 349-355.
https://doi.org/10.1016/j.pbi.2008.02.003
[7]
Pollegioni, L., Tonin, F. and Rosini, E. (2015) Lignin-Degrading Enzymes. The FEBS Journal, 282, 1190-1213. https://doi.org/10.1111/febs.13224
[8]
Hatakka, A.I. (1994) Lignin-Modifying Enzymes from Selected White-Rot Fungi—Production and Role in Lignin Degradation. Federation of European Microbiological Societies (FEMS), 13, 125-135.
https://doi.org/10.1111/j.1574-6976.1994.tb00039.x
[9]
Wariishi, H., Akileswaran, L. and Gold, M.H. (1988) Manganese Peroxidase from the Basidiomycete Phanerochaete chrysosporium: Spectral Characterization of the Oxidized States and the Catalytic Cycle. Biochemistry, 27, 5365-5370.
https://doi.org/10.1021/bi00414a061
[10]
Shin, K.S., Kim, Y.H. and Lim, J.S. (2005) Purification and Characterization of Manganese Peroxidase of the White-Rot Fungus Irpex lacteus. Journal of Microbiology, 43, 503-509.
[11]
Glenn, J.K. and Gold, M.H. (1985) Purification and Characterization of an Extracellular Mn(II)-Dependent Peroxidase from the Lignin-Degrading Basidiomycete, Phanerochaete chrysosporium. Archives of Biochemistry and Biophysics, 242, 329-341. https://doi.org/10.1016/0003-9861(85)90217-6
[12]
Lisov, A., Leontievsky, A. and Golovleva, A. (2003) Hybrid Mn, A-Peroxidase from the Ligninolytic Fungus Panus tigrinus 8/18. Isolation, Substrate Specificity, and Catalytic Cycle. Biochemistry, 68, 1027-1035.
[13]
Hoshino, F., Kajino, T., Sugiyama, H., et al. (2002) Thermally Stable and Hydrogen Peroxide Tolerant Manganese Peroxidase (MnP) from Lenzites betulinus. FEBS Letters, 530, 249-252. https://doi.org/10.1016/S0014-5793(02)03454-3
[14]
Lankinen, P.V., Bonnen, A.M., Anton, L.H., Wood, D.A., Kalkkinen, N., Hatakka, A. and Thurston, C.F. (2001) Characteristics and N-Terminal Amino Acid Sequence of Manganese Peroxidase from Solid Substrate Cultures of Agaricus bisporusi. Applied Microbiology and Biotechnology, 55, 170-176.
https://doi.org/10.1007/s002530000509
[15]
Palma, C., Martinez, A.T., Lema, J.M., et al. (2000) Different Fungal Manganese-Oxidizing Peroxidases: A Comparison between Bjerkandera sp and Phanerochaete chrysosporium. Journal of Biotechnology, 77, 235-245.
https://doi.org/10.1016/S0168-1656(99)00218-7
[16]
Hilden, K., Martinez, 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 Genetics and Biology, 42, 403-419. https://doi.org/10.1016/j.fgb.2005.01.008
[17]
Hilden, K.S., Bortfeldt, R., Hofrichter, M., et al. (2008) Molecular Characterization of the Basidiomycete Isolate Nematoloma frowardii b19 and Its Manganese Peroxidase Places the Fungus in the Corticioid Genus Phlebia. Microbiology, 154, 2371-2379. https://doi.org/10.1099/mic.0.2008/018747-0
[18]
de Oliveira, P.L., Duarte, M.C., Ponezi, A.N., et al. (2009) Purification and Partial Characterization of Manganese Peroxidase from Bacillus pumilus and Paenibacillus sp. Brazilian Journal of Microbiology, 40, 818-826.
https://doi.org/10.1590/S1517-83822009000400012
[19]
Kupriashina, M.A., Selivanov, N. and Nikitina, V.E. (2012) Isolation and Purification of Mn-Peroxidase from Azospirillum brasilense Sp245. Prikladnaia Biokhimiia i Mikrobiologiia, 48, 23-26. https://doi.org/10.1134/S0003683812010097
[20]
Niladevi, K.N. and Prema, P. (2005) Mangrove Actinomycetes as the Source of Ligninolytic Enzymes. Actinomycetologica, 19, 40-47. https://doi.org/10.3209/saj.19.40
[21]
Janusz, G., Pawlik, A., Sulej, J., Swiderska-Burek, U., Anna Jarosz-Wilkolazka, A. and Paszczynski, A. (2017) Lignin Degradation: Microorganisms, Enzymes Involved, Genomes Analysis and Evolution. FEMS Microbiology Reviews, 41, 941-962.
https://doi.org/10.1093/femsre/fux049
[22]
Xu, H., Guo, M., Gao, Y., Bai, X. and Zhou, X. (2017) Expression and Characteristics of Manganese Peroxidase from Ganoderma lucidum in Pichia pastoris and Its Application in the Degradation of Four Dyes and Phenol. BMC Biotechnology, 17, Article No. 19. https://doi.org/10.1186/s12896-017-0338-5
[23]
Twala, P.P., Mitema, A., Baburam, C. and Feto, N.A. (2020) Breakthroughs in the Discovery and Use of Different Peroxidase Isoforms of Microbial Origin. AIMS Microbiology, 6, 330-349. https://doi.org/10.3934/microbiol.2020020
[24]
Sundaramoorthy, M., Kiishi, K., Gold, M.H., Thomas, L. and Poulos, T.L. (1994) The Crystal Structure of Manganese Peroxidase from Phanerochaete chrysosporium at 2.06-A Resolution. Journal of Biological Chemistry, 269, 32759-32767.
https://doi.org/10.1016/S0021-9258(20)30056-9
[25]
Sutherland, G.R.J., Zapanta, L.S., Tien, M. and Aust, S.D. (1997) Thermodynamics of Binding of the Distal Calcium to Manganese Peroxidase. Biochemistry, 36, 3654-3662. https://doi.org/10.1021/bi962195m
[26]
Carmona-Ribeiro, A.M., Prieto, T. and Nantes, I. (2015) Nanostructures for Peroxidases. Frontiers in Molecular Biosciences, 2, Article No. 50.
https://doi.org/10.3389/fmolb.2015.00050
[27]
Nie, G. and Aust, S.D. (1997) Effect of Calcium on the Reversible Thermal Inactivation of Lignin Peroxidase. Archives of Biochemistry and Biophysics, 337, 225-231.
https://doi.org/10.1006/abbi.1996.9770
[28]
Howest, B.D., Feis, A., Raimond, L., Indiani, C. and Smulevich, G. (2001) The Critical Role of the Proximal Calcium Ion in the Structural Properties of Horseradish Peroxidase. Journal of Biological Chemistry, 276, 40704-40711.
https://doi.org/10.1074/jbc.M107489200
[29]
Dunford, H.B. (1991) Horseradish Peroxidase: Structure and Kinetic Properties. In: Everse, J., Everse, K.E. and Grisham, M.B., Eds., Peroxidases in Chemistry and Biology, CRC Press, Boca Raton, 1-24.
[30]
Kirk, T.K. and Cullen, D. (1998) Enzymology and Molecular Genetics of Wood Degradation by White-Rot Fungi. In: Young, R.A. and Akthar, M., Eds., Environmentally Friendly Technologies for the Pulp and Paper Industry, John Wiley & Sons, New York, 273-307.
[31]
Wariishi, H., Valli, K. and Gold, M.H. (1992) Manganese (II) Oxidation by Manganese Peroxidase from the Basidiomycete Phanerochaete chrysosporium Kinetic Mechanism and Role of Chelators. Journal of Biological Chemistry, 267, 23688-23695.
https://doi.org/10.1016/S0021-9258(18)35893-9
[32]
Kishi, K., Wariishi, H., Marquez, L., Dunford, B.H. and Gold, M.H. (1994) Mechanism of Manganese Peroxidase II Reduction. Effect of Organic Acid and Chelators and pH. Biochemistry, 34, 8694-8701. https://doi.org/10.1021/bi00195a010
[33]
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. Archives of Biochemistry and Biophysics, 251, 688-696.
https://doi.org/10.1016/0003-9861(86)90378-4
[34]
Wariishi, H., Dunford, H.B., MacDonald, I.D. and Gold, M.H. (1989) Thiol-Mediated Oxidation of Nonphenolic Lignin Model Compounds by Manganese Peroxidase of Phanerochaete chrysosporium. Journal Biological Chemistry, 264, 3335-3340.
https://doi.org/10.1016/S0021-9258(18)94070-6
[35]
Paszczynski, A., Huynh, V.B. and Crawford, R. (1986) Comparison of Ligninase-I and Peroxidase-M2 from the White-Rot Fungus Phanerochaete chrysosporium. Archives of Biochemistry and Biophysics, 244, 750-765.
https://doi.org/10.1016/0003-9861(86)90644-2
[36]
Kuan, I.C. and Tien, M. (1993) Stimulation of MnP Peroxidase Activity: A Possible Role for Oxalate in Lignin Biodegradation. Proceedings of the National Academy of Sciences of the United States of America, 90, 1242-1246.
https://doi.org/10.1073/pnas.90.4.1242
[37]
Pintus, F., Spanò, D., Medda, R. and Floris, G. (2011) Calcium Ions and a Secreted Peroxidase in Euphorbia characias Latex Are Made for Each Other. Protein Journal, 30, 115-123. https://doi.org/10.1007/s10930-011-9310-8
[38]
Plieth, C. and Vollbehr, S. (2012) Calcium Promotes Activity and Confers Heat Stability on Plant Peroxidases. Plant Signaling & Behavior, 7, 650-660.
https://doi.org/10.4161/psb.20065
[39]
Sutherland, G.R.J. and Aust, S.D. (1996) The Effects of Calcium on the Thermal Stability and Activity of Manganese Peroxidase. Archives of Biochemistry and Biophysics, 332, 128-134. https://doi.org/10.1006/abbi.1996.0324
[40]
Estevez, R.L., Sartorio Chambo, A.P., Stangarlin, J.R. and Kuhn, O.J. (2020) Doses of Calcium Sulphate Increase the Peroxidase Activity and the Rooting of Eucalyptus Clones. Clencia Florestral, Santa Maria, 30, 396-405.
https://doi.org/10.5902/1980509834369
[41]
Mura, A., Medda, R., Longu, S., Floris, G., Rinaldi, A.C. and Padiglia, A.A. (2005) A Ca2+/Calmodulin-Binding Peroxidase from Euphorbia Latex: Novel Aspects of Calcium-Hydrogen Peroxide Cross-Talk in the Regulation of Plant Defenses. Biochemistry, 44, 14120-14130. https://doi.org/10.1021/bi0513251
[42]
Mura, A., Pintus, F., Lai, P., Padiglia, A., Bellelli, A., Floris, G., et al. (2006) Catalytic pathways of Euphorbia characias Peroxidase Reacting with Hydrogen Peroxide. Biological Chemistry, 387, 559-567. https://doi.org/10.1515/BC.2006.072
[43]
Peterson, J.A. and Graham, S.E. (1998) A Close Family Resemblance: The Importance of Structure in Understanding Cytochromes P450. Structure, 6, 1079-1085.
https://doi.org/10.1016/S0969-2126(98)00109-9
[44]
Rasmussen, C.B., Hiner, A.N.P., Smith, A.T. and Welinder, K.G. (1998) Effect of Calcium, Other Ions, and pH on Reactions of Barley Peroxidase with Hydrogen Peroxidase and Fluoride: Control of Activity through Conformational Change. Journal of Biological Chemistry, 273, 2232-2240. https://doi.org/10.1074/jbc.273.4.2232
[45]
Sanders, S.A., Brays, R.C. and Smith, A.T. (1994) pH-Dependent Properties of a Mutant Horseradish Peroxidase Isoenzyme C in Which Arg38 Has Been Replaced with Lysine. European Journal of Biochemistry, 224, 1029-1037.
https://doi.org/10.1111/j.1432-1033.1994.01029.x
[46]
Zamorano, L.S., Vilarmau, S.B., Arellano, J.B., Zhadan, G.G., Cuadrado, N., Bursakov, S.A., Roig, M.G. and Shnyrov, V.L. (2009) Thermal Stability of Peroxidase from Chamaerops excelsa Palm Tree at pH 3. International Journal of Biological Macromolecules, 44, 326-332. https://doi.org/10.1016/j.ijbiomac.2009.01.004
[47]
Colonna, S., et al. (1999) Recent Biotechnological Developments in the Use of Peroxidase. Trends Biotechnology, 17, 163-168.
https://doi.org/10.1016/S0167-7799(98)01288-8
[48]
Sellami, K., Couvert, A., Nasrallah, N., Maach, R., Abouseoud, M. and Amrane, A. (2022) Peroxidase Enzymes as Green Catalysts for Bioremediation and Biotechnological Applications: A Review. Science of the Total Environment, 806, Article ID: 150500. https://doi.org/10.1016/j.scitotenv.2021.150500
[49]
Ufot, U.F. and Akpanabiatu, M.I. (2012) An Engineered Phlebia radiata Manganese Peroxidase: Expression, Refolding, Purification and Preliminary Characterization. American Journal of Molecular Biology, 2, 359-370.
https://doi.org/10.4236/ajmb.2012.24037
[50]
Ufot, U.F. and Akpanabiatu, M.I. (2014) Influence of CaCl2 and EDTA on Reversible Thermal Inactivation of Recombinant Wild-Type and Mutant (E40H/E44H) Phlebia radiata Manganese Peroxidase 3(rPr-MnP3). African Journal of Biochemistry Research, 8, 118-126. https://doi.org/10.5897/AJBR2014.0788
[51]
Ufot, U.F., Ite, A.E., Usoh, I.H. and Akpanabiatu, M.I. (2016) Role of Some Metal Ions on Steady-State Kinetics of Engineered Wild-Type and Manganese(II) Binding Site Mutants of Recombinant Phlebia radiata Manganese Peroxidase 3 (rPr-MnP3). American Journal of Medical and Biological Research, 4, 42-52.
[52]
Lundell, T.K., Bentley, E., Hilden, S.K., Rytioja, J.T., Kuuskeri, J.T., Ufot, U., Nousiainen, P.A., Hofrichter, M., Wahlsten, M.P., Doyle, W. and Smith, A. (2016) Engineering towards Catalytic Use of Fungal Class-II Peroxidases for Dye-Decolorizing and Conversion of Lignin Model Compounds. Current Biotechnology, 5, 1-12.
[53]
Ufot, U.F., Akpanabiatu, I., Cali, K., Uffia, I.D. and Udosen, I. (2022) pH-Dependence of Manganese(II) Oxidation Reaction by Novel Wild-Type and Mutants Recombinant Phlebia radiata Manganese Peroxidase 3 (rPr-MnP3) Enzymes. American Journal of Molecular Biology, 12, 67-84. https://doi.org/10.4236/ajmb.2022.122007
[54]
Tam, J.W. and Welinder, K.G. (1996) Unfolding and Refolding of Coprinus cinereus Peroxidase at High pH, in Urea, and at High Temperature. Effect of Organic and Ionic Additives on These Processes. Biochemistry, 35, 7573-7579.
https://doi.org/10.1021/bi953067l
[55]
Ogawa, S., Shiro, Y. and Morishma, J. (1979) Calcium Binding by Horseradish Peroxidase c and the Heme Environmental Structure. Biochemical and Biophysical Research Communications, 90, 674-678.
https://doi.org/10.1016/0006-291X(79)91288-9
[56]
Whitaker, J.R. (1994) Effect of pH on Enzyme Catalysed Reactions. In: Principles of Enzymology for the Food Science, 2nd Edition, Marcel Dekker, New York, 271-300.
https://doi.org/10.1201/9780203742136-10
[57]
Youngs, H.L., Gelpke, M.D.S., Li, D.M., et al. (2001) The Role of Glu39 in Mn-II Binding and Oxidation by Manganese Peroxidase from Phanerochaete chrysosporium. Biochemistry, 40, 2243-2250. https://doi.org/10.1021/bi002104s
[58]
Feis, A., Rodriguez-Lopez, J.N., Thorneley, R.N.F. and Smulevich, G. (1998) The Distal Cavity Structure of Carbonyl Horseradish Peroxidase as Probed by the Resonance Raman Spectra of His-42-Leu and Arg-38-Leu Mutants. Biochemistry, 37, 13575-13581. https://doi.org/10.1021/bi981399v
[59]
de Ropp, J.S., Mandal, P., Brauer, S.L. and La Mar, G.N. (1997) Solution NMR Study of the Electronic and Molecular Structure of the Haem Cavity in High-Spin, Resting State Horseradish Peroxidase. Journal of the American Chemical Society, 119, 4732-4739. https://doi.org/10.1021/ja9642018
[60]
George, S.J., Kvaratskhelia, M., Dilworth, M.J. and Thorneley, R.N.F. (1999) Reversible Alkaline Inactivation of Lignin Peroxidase Involves the Release of both the Distal and Proximal Site Calcium Ions and Bishistidine Co-Ordination of the Haem. Biochemical Journal, 344, 237-244. https://doi.org/10.1042/bj3440237
[61]
Converso, D.A. and Fernandez, M.E. (1996) Ca2+ Activation of Wheat Peroxidase: A Possible Physiological Mechanism of Control. Archives of Biochemistry and Biophysics, 33, 59-65. https://doi.org/10.1006/abbi.1996.0364
[62]
Henriksen, A., Welinder, K.G. and Gajhede, M. (1998) Structure of Barley Grain Peroxidase Refined at 1.9-A° Resolution: A Plant Peroxidase Reversibly Inactivated at Neutral pH. The Journal of Biological Chemistry, 273, 2241-2248.
https://doi.org/10.1074/jbc.273.4.2241
[63]
van Huystee, R.B., Roi, M.G., Shnyrov, V.L. and Sakharov, I.Y. (2004) Peroxidase Stability Related to Its Calcium and Glycans. Phytochemistry Reviews, 3, 19-28.
https://doi.org/10.1023/B:PHYT.0000047802.79211.32
[64]
Neves-Petersen, M.T., Klitgaard, S., Carvalho, A.S.L., Petersen, S.B., de Barros, M.R.A. and Pinho e Melo, E. (2007) Photophysics and Photochemistry of Horseradish Peroxidase A2 upon Ultraviolet Illumination. Biophysical Journal, 92, 2016-2027. https://doi.org/10.1529/biophysj.106.095455
[65]
Araiso, T. and Yamazaki, I. (1978) Kinetic Analysis of the Acid-Alkaline Conversion of Horseradish Peroxidases. Biochemistry, 17, 942-946.
https://doi.org/10.1021/bi00598a031
[66]
Job, D., Ricard, J. and Dunford, H.B. (1977) The Alkaline Transition of Turnip Peroxidases. Archives of Biochemistry and Biophysics, 179, 95-99.
https://doi.org/10.1016/0003-9861(77)90090-X
[67]
Tams, J.W. and Welinder, K.G. (1998) Glycosylation and Thermodynamic versus Kinetic Stability of Horseradish Peroxidase. FEBS Letter, 421, 234-236.
https://doi.org/10.1016/S0014-5793(97)01573-1
[68]
Lige, B., Ma, S.W. and Huystee, R.B. (2001) Glycosylation of the Cationic Peanut Peroxidase Gene Expressed in Transgenic Tobacco. Plant Science, 156, 55-63.
https://doi.org/10.1016/S0168-9452(00)00233-8
[69]
Mc Eldoon, J.P. and Dordick, J.S. (1996) Unusual Thermal Stability of Soybean Peroxidase. Biotechnology Progress, 12, 555-558. https://doi.org/10.1021/bp960010x
[70]
Askari, H., Rahimian, A. and Aminian, M. (2022) Purification and Biochemical Characterization of Two Anionic Peroxidase Isoenzymes from Raphanus sativus L. var niger Roots. Applied Biochemistry and Biotechnology, 194, 2219-2235.
https://doi.org/10.1007/s12010-021-03736-0
[71]
Smith, D.W. and Williams, R.J.P. (1970) The Spectra of Ferric Haem and Haemproteins. Structure and Bonding, 7, 1-45. https://doi.org/10.1007/BFb0118898
[72]
Dunford, H.B. and Stillman, J.S. (1976) On the Function and Mechanism of Action of Peroxidases. Coordination Chemistry Reviews, 19, 187-251.
https://doi.org/10.1016/S0010-8545(00)80316-1
[73]
Miller, M.A., Coletta, M., Mauro, J.M., Putman, I.D., Farnum, M.F., Kraut, J. and Traylor, T.G. (1990) Carbon Monoxide Recombination in Cytochrome c Peroxidase: Effect of the Local Heme Environment on Carbon Monoxide Binding Explored through Site-Directed Mutagenesis. Biochemistry, 29, 1777-1791.
https://doi.org/10.1021/bi00459a017
[74]
Vitello, L.B., Erman, J.E., et al. (1992) Effect of Asp-235→Asn Substitution on the Absorption Spectrum and Hydrogen Peroxide Reactivity of Cytochrome c Peroxidase. Biochemistry, 31, 11524-11535. https://doi.org/10.1021/bi00161a034
[75]
Foote, N., Gadsby, P.M.A., Berry, M.J., Greenwood, C. and Thompson, A.J. (1987) The Formation of Ferric Haem during the Low Temperature Photolysis of Horseradish Peroxidase Compound I. Biochemical Journal, 246, 659-668.
https://doi.org/10.1042/bj2460659
[76]
Sitter, A.J., Shifflet, J.R. and Terner, J. (1988) Resonance Raman Spectroscopic Evidence for Heme Iron-Hydroxide Ligation in Peroxidase Alkaline Forms. Journal of Biological Chemistry, 263, 13032-13038.
https://doi.org/10.1016/S0021-9258(18)37667-1
