1,123
Views
54
CrossRef citations to date
0
Altmetric
Articles

Molecular docking and dynamics simulation analyses unraveling the differential enzymatic catalysis by plant and fungal laccases with respect to lignin biosynthesis and degradation

, , , &
Pages 1835-1849 | Received 28 Aug 2014, Accepted 07 Oct 2014, Published online: 06 Nov 2014

References

  • Accelrys Software Inc. 2013. Discovery studio modeling environment (Release 3.5). San Diego, CA: Author.
  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.10.1016/S0022-2836(05)80360-2
  • Ander, P., & Eriksson, K. E. (1976). The importance of phenol oxidase activity in lignin degradation by the white-rot fungus Sporotrichum pulverulentum. Archives of Microbiology, 109, 1–8.10.1007/BF00425105
  • Bao, W., O’Malley, D. M., Whetten, R., & Sederoff, R. R. (1993). A laccase associated with lignification in loblolly pine xylem. Science, 260, 672–674.10.1126/science.260.5108.672
  • Berthet, S., Demont-Caulet, N., Pollet, B., Bidzinski, P., Cezard, L., Le Bris, P., … Jouanin, L. (2011). Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. The Plant Cell, 23, 1124–1137.10.1105/tpc.110.082792
  • Berthet, S., Thevenin, J., Baratiny, D., Demont-Caulet, N., Debeaujon, I., Bidzinski, P., … Jouanin, L. (2012). Role of plant laccases in lignin polymerization. Advances in Botanical Research, 61, 145–172.10.1016/B978-0-12-416023-1.00005-7
  • Bleve, G., Lezzi, C., Spagnolo, S., Tasco, G., Tufariello, M., Casadio, R., … Grieco, F. (2013). Role of the C-terminus of Pleurotus eryngii ery4 laccase in determining enzyme structure, catalytic properties and stability. Protein Engineering, Design & Selection, 26, 1–13.
  • Camarero, S., Galletti, G. C., & Martinez, A. T. (1994). Preferential degradation of phenolic lignin units by two white rot fungi. Applied and Environmental Microbiology, 60, 4509–4516.
  • Camarero, S., Ibarra, D., Martinez, M. J., & Martinez, A. T. (2005). Lignin-derived compounds as efficient laccase mediators for decolorization of different types of recalcitrant dyes. Applied and Environmental Microbiology, 71, 1775–1784.10.1128/AEM.71.4.1775-1784.2005
  • Cañas, A. I., Alcalde, M., Plou, F., Martínez, M. J., Martínez, A. T., & Camarero, S. (2007). Transformation of polycyclic aromatic hydrocarbons by laccase is strongly enhanced by phenolic compounds present in soil. Environmental Science and Technology, 8, 2964–2971.
  • Chabanet, A., Coldberg, R., Catesson, A. M., Quinet-Szely, M., Delaunay, A. M., & Faye, L. (1994). Characterization and localization of a phenoloxidase in mung bean hypocotyl cell walls. Plant Physiology, 106, 1095–1102.
  • Claus, H. (2004). Laccases: Structure, reactions, distribution. Micron, 35, 93–96.10.1016/j.micron.2003.10.029
  • Colaneri, M. J., & Vitali, J. (2014). Copper dynamics in doped metal–bis(histidine) complexes. The Journal of Physical Chemistry A, 118, 4688–4694.10.1021/jp500981c
  • Davin, L. B., Bedgar, D. L., Katayama, T., & Lewis, N. G. (1992). On the stereoselective synthesis of (+)-pinoresinol in Forsythia suspensa from its achiral precursor, coniferyl alcohol. Phytochemistry, 31, 3869–3874.10.1016/S0031-9422(00)97544-7
  • Driouich, A., Laine, A. C., Vian, B., & Faye, L. (1992). Characterization and localization of laccase forms in stem and cell cultures of sycamore. The Plant Journal, 2, 13–24.10.1111/tpj.1992.2.issue-1
  • Dwivedi, U. N., Singh, P., Pandey, V. P., & Kumar, A. (2011). Structure-function relationship among bacterial, fungal and plant laccases. Journal of Molecular Catalysis B: Enzymatic, 68, 117–128.10.1016/j.molcatb.2010.11.002
  • Eggert, C., Temp, U., Dean, J. F., & Eriksson, K. E. (1996). A fungal metabolite mediates degradation of non-phenolic lignin structures and synthetic lignin by laccase. FEBS Letters, 391, 144–148.10.1016/0014-5793(96)00719-3
  • Frasconi, M., Favero, G., Boer, H., Koivula, A., & Mazzei, F. (2010). Kinetic and biochemical properties of high and low redox potential laccases from fungal and plant origin. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, 1804, 899–908.10.1016/j.bbapap.2009.12.018
  • Gianfreda, L., Xu, F., & Bollag, J. M. (1999). Laccases: A useful group of oxidoreductive enzymes. Bioremediation Journal, 3, 1–26.10.1080/10889869991219163
  • Gorbacheva, M. A., Shumakovich, G. P., Morozova, O. V., Strel’tsov, A. V., Zaitseva, E. A., & Shleev, S. V. (2008). Comparative study of biocatalytic reactions of high and low redox potential fungal and plant laccases in homogeneous and heterogeneous reactions. Moscow University Chemistry Bulletin, 63, 94–98.10.3103/S0027131408020107
  • Hakulinen, N., Kiiskinen, L. L., Kruus, K., Saloheimo, M., Paananen, A., Koivula, A., & Rouvinen, J. (2002). Crystal structure of a laccase from Melanocarpus albomyces with an intact trinuclear copper site. Natural Structural Biology, 9, 601–605.
  • Hoegger, P. J., Kilaru, S., James, T. Y., Thacker, J. R., & Kues, U. (2006). Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS Journal, 273, 2308–2326.10.1111/ejb.2006.273.issue-10
  • Jaiswal, N., Pandey, V. P., & Dwivedi, U. N. (2014). Purification of a thermostable laccase from Leucaena leucocephala using a copper alginate entrapment approach and the application of the laccase in dye decolorization. Process Biochemistry, 49, 1196–1204.
  • Jaiswal, N., Pandey, V. P., & Dwivedi, U. N. (2015). Purification of a thermostable alkaline laccase from papaya (Carica papaya) using affinity chromatography. International Journal of Biological Macromolecules, 72, 326–336.
  • Kallio, J. P., Auer, S., Jänis, J., Andberg, M., Kruus, K., Rouvinen, J., Koivula, A., & Hakulinen, N. J. (2009). Structure–function studies of a Melanocarpus albomyces laccase suggest a pathway for oxidation of phenolic compounds. Journal of Molecular Biology, 392, 895–909.10.1016/j.jmb.2009.06.053
  • Kallio, J. P., Gasparetti, C., Andberg, M., Boer, H., Koivula, A., Kruus, K., … Hakulinen, N. (2011). Crystal structure of an ascomycete fungal laccase from Thielavia arenaria-common structural features of asco-laccases. FEBS Journal, 278, 2283–2295.10.1111/j.1742-4658.2011.08146.x
  • Kirk, T. K., Harkin, J. M., & Cowling, E. B. (1968). Degradation of the lignin model compount springgylglycol-β-guaiacyl ether by Polyporus versicolor and Stereum frustulatum. Biochimica et Biophysica Acta (BBA) - General Subjects, 165, 145–163.10.1016/0304-4165(68)90199-2
  • Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., … Cheatham, T. E. (2000). Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models. Accounts of Chemical Research, 33, 889–897.10.1021/ar000033j
  • Kumari, R., Kumar, R., Open Source Drug Discovery Consortium, & Lynn, A. (2014). g_mmpbsa – A GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information and Modeling, 54, 1951–1962.10.1021/ci500020m
  • Lange, L., & Grell, M. N. (2014). The prominent role of fungi and fungal enzymes in the ant-fungus biomass conversion symbiosis. Applied Microbiology and Biotechnology, 98, 4839–4851.10.1007/s00253-014-5708-5
  • Li, K., Xu, F., & Eriksson, K. E. (1999). Comparison of fungal laccases and redox mediators in oxidation of a nonphenolic lignin model compound. Applied and Environment Microbiology, 65, 2654–2660.
  • Li, M., Zhang, G., Wang, H., & Ng, T. (2010). Purification and characterization of a laccase from the edible wild mushroom Tricholoma mongolicum. Journal of Microbiology and Biotechnology, 20, 1069–1076.
  • Lindley, P. F. (2001). Multi-copper oxidases. In I. Bertini, A. Sigel, & H. Sigel (Eds.), Handbook on metalloproteins (pp. 763–911). New York, NY: Marcel Dekker.
  • Liu, L., Dean, J. F. D., Friedman, W. E., & Eriksson, K. E. L. (1994). A laccase-like phenoloxidase is correlated with lignin biosynthesis in Zinnia elegans stem tissues. The Plant Journal, 6, 213–224.10.1046/j.1365-313X.1994.6020213.x
  • Madhavi, V., & Lele, S. S. (2009). Laccase: Properties and applications. BioResources, 4, 1694–1717.
  • Madzak, C., Mimmi, M. C., Caminade, E., Brault, A., Baumberger, S., Briozzo, P., … Jolivalt, C. (2006). Shifting the optimal pH of activity for a laccase from the fungus Trametes versicolor by structure-based mutagenesis. Protein Engineering, Design & Selection, 19, 77–84.
  • McDougall, G. J., & Morrison lan, M. (1996). Extraction and partial purification of cell-wall-associated coniferyl alcohol oxidase from developing xylem of sitka spruce. Holzforschung-International Journal of the Biology, Chemistry, Physics, and Technology of Wood, 50, 549–543.
  • Messerschmidt, A., & Huber, R. (1990). The blue oxidases, ascorbate oxidase, laccase and ceruloplasmin modelling and structural relationships. European Journal of Biochemistry, 187, 341–352.10.1111/ejb.1990.187.issue-2
  • Morozova, O. V., Shumakovich, G. P., Gorbacheva, M. A., Shleev, S. V., & Yaropolov, A. I. (2007). Blue laccases. Biochemistry (Moscow), 72, 1136–1150.10.1134/S0006297907100112
  • Nicolini, C., Bruzzese, D., Cambria, M. T., Bragazzi, N. L., & Pechkova, E. (2013). Recombinant laccase: I. Enzyme cloning and characterization. Journal of Cellular Biochemistry, 114, 599–605.10.1002/jcb.v114.3
  • Nitta, K., Kataoka, K., & Sakurai, T. (2002). Primary structure of a Japanese lacquer tree laccase as a prototype enzyme of multicopper oxidases. Journal of Inorganic Biochemistry, 91, 125–131.10.1016/S0162-0134(02)00440-3
  • Nousiainen, P., Maijala, P., Hatakka, A., Martínez, A. T., & Holzforschung, J. S. (2009). Syringyl-type simple plant phenolics as mediating oxidants in laccase catalyzed degradation of lignocellulosic materials. Holzforschung, 63, 699–704.
  • Papadopoulos, J. S., & Agarwala, R. (2007). COBALT: Constraint-based alignment tool for multiple protein sequences. Bioinformatics, 23, 1073–1079.10.1093/bioinformatics/btm076
  • Piontek, K., Antorini, M., & Choinowski, T. (2002). Crystal structure of a laccase from the fungus Trametes versicolor at 1.90 Å resolution containing a full complement of coppers. Journal of Biological Chemistry, 277, 37663–37669.10.1074/jbc.M204571200
  • Pronk, S., Pall, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., … Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics, 29, 845–854.10.1093/bioinformatics/btt055
  • Ralph, S., Ralph, J., & Landucci, L. (2004). NMR database of lignin and cell wall model compounds. Retrieved from; http://ars.usda.gov/Services/docs.htm?docid=10491
  • Ranocha, P., Matthieu, C., Simon, C., Danoun, S., Jauneau, A., Boudet, Alain-M, & Goffner, D. (2002). Laccase down-regulation causes alterations in phenolic metabolism and cell wall structure in poplar. Plant Physiology, 129, 145–155.10.1104/pp.010988
  • Ranocha, P., McDougall, G., Hawkins, S., Sterjiades, R., Borderies, G., Stewart, D., … Goffner, D. (1999). Biochemical characterization, molecular cloning and expression of laccases – A divergent gene family-in poplar. European Journal of Biochemistry, 259, 485–495.10.1046/j.1432-1327.1999.00061.x
  • Rocha, M. V. J., Ramalho, T. C., Caetano, M. S., & da Cunha, E. F. F. (2013). Construction and assessment of reaction models between F1F0-synthase and organotin compounds: Molecular docking and quantum calculations. Journal of Biomolecular Structure & Dynamics, 31, 1175–1181.
  • Rodríguez Couto, S., Herrera, J., & Toca, L. (2006). Industrial and biotechnological applications of laccases: A review. Biotechnology Advances, 24, 500–513.10.1016/j.biotechadv.2006.04.003
  • Sato, Y., Wuli, B., Sederoff, R., & Whetten, R. (2001). Molecular cloning and expression of eight laccase cDNAs in Loblolly Pine (Pinus taeda). Journal of Plant Research, 114, 147–155.10.1007/PL00013978
  • Satpathy, R., Behera, R., Padhi, S. K., & Guru, R. K. (2013). Computational phylogenetic study and data mining approach to laccase enzyme sequences. Journal of Phylogenetics & Evolutionary Biology, 1, 108.
  • SchuÈttelkopf, A. W., & van Aalten, D. M. (2004). PRODRG: A tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallographic, D60, 1355–1363.
  • Solomon, E. I., Heppner, D. E., Johnston, E. M., Ginsbach, J. W., Cirera, J., Qayyum, M., … Tian, L. (2014). Copper active sites in biology. Chemical Reviews, 114, 3659–3853.10.1021/cr400327t
  • Solomon, E. I., Sundaram, U. M., & Machonkin, T. E. (1996). Multicopper oxidases and oxygenases. Chemical Reviews, 96, 2563–2606.10.1021/cr950046o
  • Sterjiades, R., Dean, J. F., & Eriksson, K. E. (1992). Laccase from sycamore maple (Acer pseudoplatanus) polymerizes monolignols. Plant Physiology, 99, 1162–1168.10.1104/pp.99.3.1162
  • Torres-Duarte, C., Roman, R., Tinoco, R., & Vazquez-Duhalt, R. (2009). Halogenated pesticide transformation by a laccase-mediator system. Chemosphere, 77, 687–692.10.1016/j.chemosphere.2009.07.039
  • Valderrama, B., Oliver, P., Medrano-Soto, A., & Vazquez-Duhalt, R. (2003). Evolutionary and structural diversity of fungal laccases. Antonie van Leeuwenhoek, 84, 289–299.10.1023/A:1026070122451
  • Wariishi, H., Morohoshi, N., & Haraguchi, T. (1987). Degradation of lignin by the extracellular enzymes of Coriolus versicolor VII. Effective degradation of syringyl type ß-aryl ether lignin model compound by Laccase III. Mokuzai Gakkaishi, 33, 892–898.
  • Xu, F. (1996). Oxidation of phenols, anilines, and benzenethiols by fungal laccases: Correlation between activity and redox potentials as well as halide inhibition. Biochemistry, 35, 7608–7614.10.1021/bi952971a
  • Xu, F., Berka, R. M., Walheithner, J. A., Nelson, B. A., Shuster, J. R., Brown, S. H., … Solomon, E. I. (1998). Site-directed mutations in fungal laccase: Effect on redox potential, activity and pH profile. Biochemical Journal, 334, 63–70.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.