Abstract
Aniline was polymerised enzymatically in aqueous solution at pH = 4.3 and 25°C in the presence of submicrometer-sized vesicles formed from sodium bis(2-ethylhexyl)sulphosuccinate (AOT). H2O2 served as oxidant and the enzyme used was either horseradish peroxidase isoenzyme C (HRPC) or soybean peroxidase (SBP), both being class III peroxidases. From previous studies with HRPC, it is known that stable vesicle suspensions containing the emeraldine salt form of polyaniline (PANI-ES) can be obtained within 1–2 days with a 90–95 % yield, provided that optimal reaction conditions are applied. Unfortunately, HRPC becomes inactivated during polymerisation. In the present study, a linear dendritic block copolymer was added to HRPC, resulting in higher operational enzyme stability; the stabilising effect, however, was too small to afford a substantial decrease in the required amount of enzyme. Moreover, replacing HRPC with SBP was of no advantage, although SBP is known to be more stable towards inactivation by H2O2 than HRPC. By contrast, SBP was found to be much slower in oxidising aniline, and complete inactivation of SBP occurred before all the aniline monomers were oxidised, leading to low yields and the formation of over-oxidised products. The same was observed for HRP isoenzyme A2. Reactions without vesicles indicated that peroxidase inactivation was probably caused by PANI-ES.
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Aibara, S., Yamashita, H., Mori, E., Kato, M., & Morita, Y. (1982). Isolation and characterization of five neutral isoenzymes of horseradish peroxidase. The Journal of Biochemistry, 92, 531–539.
Ator, M. A., & Ortiz de Montellano, P. R. (1987). Protein control of prosthetic heme reactivity. Reaction of substrates with the heme edge of horseradish peroxidase. The Journal of Biological Chemistry, 262, 1542–1551.
Berglund, G. I., Carlsson, G. H., Smith, A. T., Szöke, H., Henriksen, A., & Hajdu, J. (2002). The catalytic pathway of horseradish peroxidase at high resolution. Nature, 417, 463–468. DOI: 10.1038/417463a.
Cao, Y., Smith, P., & Heeger, A. J. (1989). Spectroscopic studies of polyaniline in solution and in spin-cast films. Synthetic Metals, 32, 263–281. DOI: 10.1016/0379-6779(89)90770-4.
Caramyshev, A. V., Evtushenko, E. G., Ivanov, V. F., Barceló, A. R., Roig, M. G., Shnyrov, V. L., van Hystee, R. B., Kurochinkin, I. N., Vorobiev, A. Kh., & Sakharov, I. Yu. (2005). Synthesis of conducting polyelectrolyte complexes of polyaniline and poly(2-acrylamido-3-methyl-1-propanesulfonic acid) catalyzed by pH-stable palm tree peroxidase. Biomacromolecules, 6, 1360–1366. DOI: 10.1021/bm049370 w.
Caramyshev, A. V., Lobachov, V. M., Selivanov, D. V., Sheval, E. V., Vorobiev, A. Kh., Katasova, O. N., Polyakov, V. Y., Makarov, A. A., & Sakharov, I. Yu. (2007). Micellar peroxidase-catalyzed synthesis of chiral polyaniline. Biomacromolecules, 8, 2549–2555. DOI: 10.1021/bm070212p.
Carvalho, A. S. L., Sommer Ferreira, B., Neves-Petersen, M. T., Petersen, S. B., Aires-Barros, M. R., & Melo, E. P. (2007). Thermal denaturation of HRPA2: pH-dependent conformational changes. Enzyme and Microbial Technology, 40, 696–703. DOI: 10.1016/j.enzmictec.2006.05.029.
Chiang, J. C., & MacDiarmid, A. G. (1986). ’Polyaniline’: Protonic acid doping of the emeraldine form to the metallic regime. Synthetic Metals, 13, 193–205: DOI: 10.1016/0379-6779(86)90070-6
Cruz-Silva, R., Roman, P., & Romero, J. (2011). Enzymatic synthesis of polyaniline and other electrically conductive polymers. In K. Loos (Ed.), Biocatalysis in polymer chemistry (chapter 8, pp. 187–210). Weinheim, Germany: Wiley-VCH. DOI: 10.1002/9783527632534.ch8.
Ding, Y., Padias, A. B., & Hall, H. K., Jr. (1999). Chemical trapping experiments support a cation-radical mechanism for the oxidative polymerisation of aniline. Journal of Polymer Science Part A: Polymer Chemistry, 37, 2569–2579. DOI: 10.1002/(SICI)1099-0518(19990715)37:14〈2569::AIDPOLA30〉3.0.CO;2-N.
Dmitrieva, E., & Dunsch, L. (2011). How linear is “linear” polyaniline? The Journal of Physical Chemistry B, 115, 6401–6411. DOI: 10.1021/jp200599f.
do Nascimento, G. M., & de Souza, M. A. (2010). Spectroscopy of nanostructured conductive polymers. In A. Eftekhari (Ed.), Nanostructured conductive polymers (chapter 8, pp. 341–373). Chichester, UK: Wiley.
Dunford, H. B. (2010). Peroxidases and catalases: Biochemistry, biophysics, biotechnology, and physiology (2nd ed.). Hoboken, NJ, USA: Wiley.
Duroux, L., & Welinder, K. G. (2003). The peroxidase gene family in plants: A phyolgenetic overview. Journal of Molecular Evolution, 57, 397–407. DOI: 10.1007/s00239-003-2489-3.
Gajhede, M., Schuller, D. J., Henriksen, A., Smith, A. T., & Poulos, T. L. (1997). Crystal struture of horseradish peroxidase C at 2.15 Å resolution. Nature Structural & Molecular Biology, 4, 1032–1038. DOI: 10.1038/nsb1297-1032.
Geniès, E. M., & Tsintavis, C. (1985). Redox mechanism and elctrochemical behaviour of polyaniline deposites. Journal of Electroanalytical Chemistry, 195, 109–128. DOI: 10.1016/0022-0728(85)80009-7.
Geni`es, E. M., Boyle, A., Lapkowski, M., & Tsintavis, C. (1990). Polyaniline: A historical survey. Synthetic Metals, 36, 139–182. DOI: 10.1016/0379-6779(90)90050-u.
Gillikin, J. W., & Graham, J. S. (1991). Purification and developmental analysis of the major anionic peroxidase from the seed coat of Glycine max. Plant Physiology, 96, 214–220. DOI: 10.1104/pp.96.1.214.
Gitsov, I., Simonyan, A., & Vladimirov, N. G. (2007). Synthesis of novel asymmetric dendritic-linear-dendritic block copolymers via “living” anionic polymerisation of ethylene oxide initiated by dendritic macroinitiators. Journal of Polymer Science Part A: Polymer Chemistry, 45, 5136–5148. DOI: 10.1002/pola.22258.
Gitsov, I., Hamzik, J., Ryan, J., Simonyan, A., Nakas, J. P., Omori, S., Krastanov, A., Cohen, T., & Tannenbaum, S. W. (2008). Enzymatic nanoreactors for environmentally benign biotransformations. 1. Formation and catalytic activity of supramolecular complexes of laccase and lineardendritic block copolymers. Biomacromolecules, 9, 804–811. DOI: 10.1021/bm701081m.
Gitsov, I., Simonyan, A., Wang, L., Krastanov, A., Tanenbaum, S. W., & Kiemle, D. (2012). Polymer-assisted biocatalysis: Unprecedented enzymatic oxidation of fullerene in aqueous medium. Journal of Polymer Science Part A: Polymer Chemistry, 50, 119–126. DOI: 10.1002/pola.24995.
Gray, J. S. S., Yang, B. Y., Hull, S. R., Venzke, D. P., & Montgomery, R. (1996). The glycans of soybean peroxidase. Glycobiology, 6, 23–32. DOI: 10.1093/glycob/6.1.23.
Gray, J. S. S., Yang, B. Y., & Montgomery, R. (1998). Heterogeneity of glycans at each N-glycosylation site of horseradish peroxidase. Carbohydrate Research, 311, 61–69. DOI: 10.1016/s0008-6215(98)00209-2.
Gray, J. S. S., & Montgomery, R. (2006). Asymmetric glycosylation of soybean seed coat peroxidase. Carbohydrate Research, 341, 198–209. DOI: 10.1016/j.carres.2005.11.016.
Guo, Z., Rüegger, H., Kissner, R., Ishikawa, T., Willeke, M., & Walde, P. (2009). Vesicles as soft templates for the enzyamtic polymerisation of aniline. Langmuir, 25, 11390–11405. DOI: 10.1021/la901510m.
Guo, Z., Hauser, N., Moreno, A., Ishikawa, T., & Walde, P. (2011). AOT vesicles as templates for the horseradish peroxidase-triggered polymerisation of aniline. Soft Matter, 7, 180–193. DOI: 10.1039/c0sm00599a.
Henriksen, A., Mirza, O., Indiani, C., Teilum, K., Smulevich, G., Welinder, K. G., & Gajhede, M. (2001). Structure of soybean seed coat peroxidase: A plant peroxidase with unusual stability and haem-apoprotein interactions. Protein Science, 10, 108–115. DOI: 10.1110/ps.37301.
Hidalgo Cuadrado, N., Arellano, J. B., Calvete, J. J., Sanz, L., Zhadan, G. G., Textor, L. C., Polikarpov, I., Bursakov, S., Roig, M. R., & Shnyrov, V. L. (2011). Palm peroxidases: The most robust enzymes. Current Topics in Biochemical Research, 13(2), 67–79.
Hiner, A. N. P., Hernández-Ruíz, J., Arnao, M. B., 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. Biotechnology and Bioengineering, 50, 655–662. DOI: 10.1002/(SICI)1097-0290(19960620)50:6〈655::AID-BIT6〉3.0.CO;2-J.
Hollmann, F., & Arends, I. W. C. E. (2012). Enzyme initiated radical polymerisations. Polymers, 4, 759–793. DOI: 10.3390/polym4010759.
Huang, W. S., & MacDiarmid, A. G. (1993). Optical properties of polyaniline. Polymer, 34, 1833–1845. DOI: 10.1016/0032-3861(93)90424-9.
Junker, K., Zandomeneghi, G., Guo, Z., Kissner, R., Ishikawa, T., Kohlbrecher, J., & Walde, P. (2012). Mechanistic aspects of the horseradish peroxidase-catalysed polymerisation of aniline in the presence of AOT vesicles as templates. RSC Advances, 2, 6478–6495. DOI: 10.1039/c2ra20566a.
Kamal, J. K. A., & Behere, D. V. (2002). Thermal and conformational stability of seed coat soybean peroxidase. Biochemistry, 41, 9034–9042. DOI: 10.1021/bi025621e.
Kamal, J. K. A., & Behere, D. V. (2003). Activity, stability and conformational flexibility of seed coat soybean peroxidase. Journal of Inorganic Biochemistry, 94, 236–242. DOI: 10.1016/s0162-0134(03)00004-7.
Kamal, J. K. A., & Behere, D. V. (2008). Kinetic stabilities of soybean and horseradish peroxidases. Biochemical Engineering Journal, 38, 110–114. DOI: 10.1016/j.bej.2007.07.019.
Karamyshev, A. V., Shleev, S. V., Koroleva, O. V., Yaropolov, A. I., & Sakharov, I. Yu. (2003). Laccase-catalyzed synthesis of conducting polyaniline. Enzyme and Microbial Technology, 33, 556–564. DOI: 10.1016/s0141-0229(03)00163-7.
Kausaite, A., Ramanaviciene, A., & Ramanavicius, A. (2009). Polyaniline synthesis catalysed by glucose oxidase. Polymer, 50, 1864–1851. DOI: 10.1016/j.polymer.2009.02.013.
Lavery, C. B., MacInnis, M. C., MacDonald, M. J., Williams, J. B., Spencer, C. A., Burke, A.A., Irwin, D. J. G., & D’Cunha, G. B. (2010). Purification of peroxidase from horseradish (Armoracia rusticana) roots. Journal of Agricultural and Food Chemistry, 58, 8471–8476. DOI: 10.1021/jf100786h.
Lehmann Nielsen, K., Indiani, C., Henriksen, A., Feis, A., Becucci, M., Gajhede, M., Smulevich, G., & Welinder, K. G. (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, 11013–11021. DOI: 10.1021/bi010661o.
Liu, W., Cholli, A. L., Nagarajan, R., Kumar, J., Tripathy, S., Bruno, F. F., & Samuelson, L. (1999a). The role of template in the enzymatic synthesis of conducting polyaniline. Journal of the American Chemical Society, 121, 11345–11355. DOI: 10.1021/ja9926156.
Liu, W., Kumar, J., Tripathy, S., Senecal, K. J., & Samuelson, L. (1999b). Enzymatically synthesized conducting polyaniline. Journal of the American Chemical Society, 121, 71–78. DOI: 10.1021/ja982270b.
Liu, W., Kumar, J., Tripathy, S., & Samuelson, L. A. (2002). Enzymatic synthesis of conducting polyaniline in micelle solution. Langmuir, 18, 9696–9704. DOI: 10.1021/la0206357.
McEldoon, J. P., Pokora, A. R., & Dordick, J. S. (1995). Lignin peroxidase-type activity of soybean peroxidase. Enzyme and Microbial Technology, 17, 359–365. DOI: 10.1016/0141-0229(94)00060-3.
McEldoon, J. P., & Dordick, J. S. (1996). Unusual thermal stability of soybean peroxidase. Biotechnology Progress, 12, 555–558. DOI: 10.1021/bp960010x.
Nagarajan, R., Tripathy, S., Kumar, J., Bruno, F. F., & Samuelson, L. (2000). An enzymatically synthesized conducting molecular complex of polyaniline and poly(vinylphosphonic acid). Macromolecules, 33, 9542–9547. DOI: 10.1021/ma000954+.
Namani, T., & Walde, P. (2005). From decanoate micelles to decanoic acid/dodecylbenzensulfonate vesicles. Langmuir, 21, 6210–6219. DOI: 10.1021/la047028z.
Nissum, M., Schiødt, C. B., & Welinder, K. G. (2001). Reactions of soybean peroxidase and hydrogen peroxide pH 2.4–12.0, and veratryl alcohol at pH 2.4. Biochimica et Biophysica Acta, 1545, 339–348. DOI: 10.1016/s0167-4838(00)00295-8.
Ortiz de Montellano, P. R. (2010). Catalytic mechanisms of heme peroxidases. In E. Torres, & M. Ayala (Eds.), Biocatalysis based on heme peroxidases: Peroxidases as potential industrial biocatalysts (chapter 5, pp. 79–107). Heidelberg, Germany: Springer. DOI: 10.1007/978-3-642-12627-7.
Rumbau, V., Pomposo, J. A., Alduncin, J. A., Grande, H., Mecerreyes, D., & Ochoteco, E. (2007). A new bifunctional template for the enzymatic synthesis of conducting polyaniline. Enzyme and Microbial Technology, 40, 1412–1421. DOI: 10.1016/j.enzmictec.2006.10.024.
Ryan, B. J., Carolan, N., & Ó’Fágáin, C. (2006). Horseradish and soybean peroxidases: comparable tools for alternative niches? Trends in Biotechnology, 24, 355–363. DOI: 10.1016/j.tibtech.2006.06.007.
Sahoo, S. K., Nagarajan, R., Chakraborty, S., Samuelson, L. A., Kumar, J., & Cholli, A. L. (2002). Variation in the structure of conducting polyaniline with and without the presence of template during enzymatic polymerisation: A solid-state NMR study. Journal of Macromolecular Science Part A. Pure and Applied Chemistry, 39, 1223–1240. DOI: 10.1081/ma-120014848.
Sakharov, I. Yu., Vesgac, B. M. K., Galaev, I. Yu., Sakharova, I. V., & Pletjushkina, O. Yu. (2001). Peroxidase from leaves of royal palm tree Roystonea regia: purification and some properties. Plant Science, 161, 853–860. DOI: 10.1016/s0168-9452(01)00466-6.
Sakharov, I. Yu., Vorobiev, A. Ch., & Castillo Leon, J. J. (2003). Synthesis of polyelectrolyte complexes of polyaniline and sulfonated polystyrene by palm tree peroxidase. Enzyme and Microbial Technology, 33, 661–667. DOI: 10.1016/s0141-0229(03)00188-1.
Samuelson, L. A., Anagnostopoulos, A., Alva, K. S., Kumar, J., & Tripathy, S. K. (1998). Biologically derived conducting and water soluble polyaniline. Macromolecules, 31, 4376–4378. DOI: 10.1021/ma980258y.
Schmitz, N., Gijzen, M., & van Huystee, R. (1997). Characterization of anionic soybean (Glycine max) seed coat peroxidase. Canadian Journal of Botany, 75, 1336–1341. DOI: 10.1139/b97-845.
Shannon, L. M., Kay, E., & Lew, J. Y. (1966). Peroxidase isoenzymes from horseradish roots. I. Isolation and physical properties. The Journal of Biological Chemistry, 241, 2166–2172.
Shen, Y. P., Sun, J. Z., Wu, J. G., & Zhou, Q. Y. (2005). Synthesis and characterization of water-soluble conducting polyaniline by enzyme catalysis. Journal of Applied Polymer Science, 96, 814–817. DOI: 10.1002/app.21574.
Stejskal, J., Kratochvíl, P., & Radhakrishnan, N. (1993) Polyaniline dispersions. 2. UV-Vis absorption spectra. Synthetic Metals, 61, 225–231. DOI: 10.1016/0379-6779(93)91266-5.
Stejskal, J., & Gilbert, R. G. (2002). Polyaniline. Preparation of a conductive polymer (IUPAC technical report). Pure and Applied Chemistry, 74, 857–867. DOI: 10.1351/pac200274050857.
Stejskal, J., Omastová, M., Fedorova, S., Prokeš, J., & Trchová, M. (2003). Polyaniline and polypyrrole prepared in the presence of surfactants: a comparative conductivity study. Polymer, 44, 1353–1358. DOI: 10.1016/s0032-3861(02)00906-0.
Stejskal, J., Sapurina, I., & Trchová, M. (2010). Polyaniline nanostructures and the role of aniline oligomers in their formation. Progress in Polymer Science, 35, 1420–1481. DOI: 10.1016/s0162-0134(03)00004-7.
Stejskal, J., & Trchová, M. (2012). Aniline oligomers versus polyaniline. Polymer International, 61, 240–251. DOI: 10.1002/pi.3179.
Strickland, E. H., Kay, E., Shannon, L. M., & Horwitz, J. (1968). Peroxidase isoenzymes from horseradish roots. III. Circular dichroism of isoenzymes and apoisoenzymes. The Journal of Biological Chemistry, 243, 3560–3565.
Torres, E., Bustos-Jaimes, I., & Le Borgne, S. (2003). Potential use of oxidative enzymes for the detoxification of organic pollutants. Applied Catalysis B: Environmental, 46, 1–15. DOI: 10.1016/s0926-3373(03)00228-5.
Veitch, N. C., & Smith, A. T. (2000). Horseradish peroxidase. Advances in Inorganic Chemistry, 51, 107–162. DOI: 10.1016/s0898-8838(00)51002-2.
Veitch, N. C. (2004). Horseradish peroxidase: a modern view of a classic enzyme. Phytochemistry, 65, 249–259. DOI: 10.1016/j.phytochem.2003.10.022.
Walde, P., & Guo, Z. (2011). Enzyme-catalyzed chemical structure-controlling template polymerisation. Soft Matter, 7, 316–331. DOI: 10.1039/c0sm00259c.
Wallace, G. D., Spinks, G. M., Kane-Maguire, L. A. P., & Teasdale, P. R. (2009). Synthesis of polyanilines. In Conductive electroactive polymers: Intelligent polymer systems (3rd ed., chapter 4, pp. 137–178). Boca Raton, FL, USA: CRC Press.
Watanabe, L., Ribeiro de Moura, P., Bleicher, L., Nascimento, A. S., Zamorano, L. S., Calvete, J. J., Sanz, L., Pérez, A., Bursakov, S., Roig, M. G., Shnyrov, V. L., & Polikarpov, I. (2010). Crystal structure and statistical coupling analysis of highly glycosylated peroxidase from royal palm tree (Roystonea regia). Journal of Structural Biology, 169, 226–242. DOI: 10.1016/j.jsb.2009.10.009.
Welinder, K. G. (1976). Covalent structure of glycoprotein horseradish peroxidase (EC 1.11.1.7). FEBS Letters, 72, 19–23. DOI: 10.1016/0014-5793(76)80804-6.
Welinder, K. G., & Larsen, Y. B. (2004). Covalent structure of soybean seed coat peroxidase. Biochimica et Biophysica Acta — Proteins and Proteomics, 1698, 121–126. DOI: 10.1016/j.bbapap.2003.11.005.
Wright, H., & Nicell, J. A. (1999). Characterization of soybean peroxidase for the treatment of aqueous phenols. Bioresource Technology, 70, 69–79. DOI: 10.1016/s0960-8524(99)00007-3.
Wudl, F., Angus, R. O., Jr., Lu, F. L., Allemand, P. M., Vachon, D. J., Nowak, M., Liu, Z. X., Schaffer, H., & Heeger, A. J. (1987). Poly(p-phenyleneamineimine): Synthesis and comparison to polyaniline. Journal of the American Chemical Society, 109, 3677–3684. DOI: 10.1021/ja00246a026.
Xia, Y. N., Wiesinger, J. M., MacDiarmid, A. G., & Epstein, A. J. (1995). Camphorsulfonic acid fully doped polyaniline emeraldine salt: Conformations in different solvents studied by an ultraviolet/visible/near-infrared spectroscopic method. Chemistry of Materials, 7, 443–445. DOI: 10.1021/cm00051a002.
Xu, P., Singh, A., & Kaplan, D. L. (2006). Enzymatic catalysis in the synthesis of polyanilines and derivatives of polyanilines. Advances in Polymer Science, 194, 69–94. DOI: 10.1007/12 036.
Yang, B. Y., Gray, J. S. S., & Montgomery, R. (1996). The glycans of horseradish peroxidase. Carbohydrate Research, 287, 203–212. DOI: 10.1016/0008-6215(96)00073-0.
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Junker, K., Gitsov, I., Quade, N. et al. Preparation of aqueous polyaniline-vesicle suspensions with class III peroxidases. Comparison between horseradish peroxidase isoenzyme C and soybean peroxidase. Chem. Pap. 67, 1028–1047 (2013). https://doi.org/10.2478/s11696-013-0307-y
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DOI: https://doi.org/10.2478/s11696-013-0307-y