Laccase engineering by rational and evolutionary design

Cellular and Molecular Life Sciences

Volumn 72, Issue 5, 2015, Pages 897-910

  Pardo, Isabel ^a   Camarero, Susana ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Computational simulation; Directed evolution; Laccase; Protein engineering; Random mutagenesis; Site directed mutagenesis

Indexed keywords

LACCASE; MULTICOPPER OXIDASE; OXIDOREDUCTASE; UNCLASSIFIED DRUG; OXYGEN;

BIOCATALYST; BIOTECHNOLOGY; CATALYST; DIRECTED MOLECULAR EVOLUTION; ENZYME ACTIVITY; ENZYME ENGINEERING; ENZYME MECHANISM; ENZYME STABILITY; REVIEW; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; BINDING SITE; BIOCATALYSIS; CHEMISTRY; ENZYME SPECIFICITY; GENETICS; METABOLISM; PROTEIN ENGINEERING; PROTEIN TERTIARY STRUCTURE;

BINDING SITES; BIOCATALYSIS; DIRECTED MOLECULAR EVOLUTION; LACCASE; OXYGEN; PROTEIN ENGINEERING; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 84949114843     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1824-8     Document Type: Review

References (76)

1. Baldrian P (2006) Fungal laccases-occurrence and properties. FEMS Microbiol Rev 30:215-242
2. Skalova T, Dohnalek J, Ostergaard LH, Osteryaard PR, Kolenko P, Duskova J, StepankovaA, Hasek J (2009) The structure of the small laccase from Streptomyces coelicolor reveals a link between laccases and nitrite reductases. J Mol Biol 385:1165-1178
3. Mot A, Silaghi-Dumitrescu R (2012) Laccases: complex architectures for one-electron oxidations. Biochemistry (Mosc) 77(1395-1407):6
4. Alcalde M, Bulter T (2003) Colorimetric assays for screening laccases. Methods Mol Biol 230:193-201
5. Pardo I, Chanaga X, Vicente AI, Alcalde M, Camarero S (2013) New colorimetric screening assays for the directed evolution of fungal laccases to improve the conversion of plant biomass. BMC Biotechnol 13:90
6. Sakurai T, Kataoka K (2007) Structure and function of type I copper in multicopper oxidases. Cell Mol Life Sci 64:2642-2656
7. Hall JF, Kanbi LD, Strange RW, Hasnain SS (1999) Role of the axial ligand in type 1 Cu centers studied by point mutations of Met148 in rusticyanin. Biochemistry 38:12675-12680
8. Durao P, Bento I, Fernandes AT, Melo EP, Lindley PF, Martins LO (2006) Perturbations of the T1 copper site in the CotA laccase from Bacillus subtilis: structural, biochemical, enzymatic and stability studies. J Biol Inorg Chem 11:514-526
9. Xu F, Berka RM, Wahleithner JA, Nelson BA, Shuster JR, Brown SH, Palmer AE, Solomon EI (1998) Site-directed mutations in fungal laccase: effect on redox potential, activity and pH profile. Biochem J 334:63-70
10. Xu F, Palmer AE, Yaver DS, Berka RM, Gambetta GA, Brown SH, Solomon EI (1999) Targeted mutations in a Trametes villosa laccase-axial perturbations of the T1 copper. J Biol Chem 274:12372-12375
11. Miura Y, Tsujimura S, Kurose S, Kamitaka Y, Kataoka K, Sakurai T, Kano K (2009) Direct electrochemistry of CueO and its mutants at residues to and near type I Cu for oxygen-reducing biocathode. Fuel Cells 9:70-78
12. Palmer AE, Szilagyi RK, Cherry JR, Jones A, Xu F, Solomon EI (2003) Spectroscopic characterization of the Leu513His variant of fungal laccase: effect of increased axial ligand interaction on the geometric and electronic structure of the type 1 Cu site. Inorg Chem 42:4006-4017
13. Shimizu A, Sasaki T, Kwon JH, Odaka A, Satoh T, Sakurai N, Sakurai T, Yamaguchi S, Samejima T (1999) Site-directed mutagenesis of a possible type 1 copper ligand of bilirubin oxidase; a Met467Gln mutant shows stellacyanin-like properties. J Biochem Tokyo 125:662-668
14. Kataoka K, Kitagawa R, Inoue M, Naruse D, Sakurai T, Huang HW (2005) Point mutations at the type ICu ligands, Cys457 and Met467, and at the putative proton donor, Asp105, in Myrothecium verrucaria bilirubin oxidase and reactions with dioxygen. Biochemistry 44:7004-7012
15. Li H, Webb SP, Ivanic J, Jensen JH (2004) Determinants of the relative reduction potentials of type-1 copper sites in proteins. J Am Chem Soc 126:8010-8019
16. Hong G, Ivnitski DM, Johnson GR, Atanassov P, Pachter R (2011) Design parameters for tuning the type 1 Cu multicopper oxidase redox potential: insight from a combination of first principles and empirical molecular dynamics simulations. J Am Chem Soc 133:4802-4809
17. Piontek K, Antorini M, Choinowski T (2002) Crystal structure of a laccase from the fungus Trametes versicolor at 1.90-A° resolution containing a full complement of coppers. J Biol Chem 277:37663-37669
18. Garavaglia S, Cambria MT, Miglio M, Ragusa S, Lacobazzi V, Palmieri F, D'Ambrosio C, Scaloni A, Rizzi M (2004) The structure of Rigidoporus lignosus laccase containing a full complement of copper ions, reveals an asymmetrical arrangement for the T3 copper pair. J Mol Biol 342:1519-1531
19. Cambria MT, Gullotto D, Garavaglia S, Cambria A (2012) In silico study of structural determinants modulating the redox potential of Rigidoporus lignosus and other fungal laccases. J Biomol Struct Dyn 30:89-101
20. Tadesse MA, d'Annibale A, Galli C, Gentili P, Sergi F (2008) An assessment of the relative contributions of redox and steric issues to laccase specificity towards putative substrates. Org Biomol Chem 6:868-878
21. Galli C, Gentili P, Jolivalt C, Madzak C, Vadala R (2011) How is the reactivity of laccase affected by single-point mutations? Engineering laccase for improved activity towards sterically demanding substrates. Appl Microbiol Biotechnol 91:123-131
22. Koschorreck K, Richter SM, Swierczek A, Beifuss U, Schmid RD, Urlacher VB (2008) Comparative characterization of four laccases from Trametes versicolor concerning phenolic C-C coupling and oxidation of PAHs. Arch Biochem Biophys 474:213-219
23. Cambria MT, Di Marino D, Falconi M, Garavaglia S, Cambria A (2010) Docking simulation and competitive experiments validate the interaction between the 2,5-xylidine inhibitor and Rigidoporus lignosus laccase. J Biomol Struct Dyn 27:501-509
24. Bertrand T, Jolivalt C, Briozzo P, Caminade E, Joly N, Madzak C, Mougin C (2002) Crystal structure of a four-copper laccase complexed with an arylamine: insights into substrate recognition and correlation with kinetics. Biochemistry 41:7325-7333
25. Kallio JP, Gasparetti C, Andberg M, Boer H, Koivula A, Kruus K, Rouvinen J, Hakulinen N (2011) Crystal structure of an ascomycete fungal laccase from Thielavia arenaria-common structural features of asco-laccases. FEBS J 278:2283-2295
26. Matera I, Gullotto A, Tilli S, Ferraroni M, Scozzafava A, Briganti F (2008) Crystal structure of the blue multicopper oxidase from the white-rot fungus Trametes trogii complexed with p-toluate. Inorg Chim Acta 361:4129-4137
27. Galli C, Madzak C, Vadala R, Jolivalt C, Gentili P (2013) Concerted electron/proton transfer mechanism in the oxidation of phenols by laccase. Chembiochem 14:2500-2505
28. Madzak C, Mimmi MC, Caminade E, Brault A, Baumberger S, Briozzo P, Mougin C, Jolivalt C (2006) Shifting the optimal pH of activity for a laccase from the fungus Trametes versicolor by structure-based mutagenesis. Protein Eng Des Sel 19:77-84
29. Kallio JP, Auer S, Janis J, Andberg M, Kruus K, Rouvinen J, Koivula A, Hakulinen N (2009) Structure-function studies of a Melanocarpus albomyces laccase suggest a pathway for oxidation of phenolic compounds. J Mol Biol 392:895-909
30. Cantarella G, Galli C, Gentili P (2003) Free radical versus electron-transfer routes of oxidation of hydrocarbons by laccasemediator systems. Catalytic and stoichiometric procedures. J Mol Catal B Enzym 22:135-144
31. Christensen NJ, Kepp KP (2014) Setting the stage for electron transfer: molecular basis of ABTS-binding to four laccases from Trametes versicolor at variable pH and protein oxidation state. J Mol Catal B Enzym 100:68-77
32. Autore F, Del Vecchio C, Fraternali F, Giardina P, Sannia G, Faraco V (2009) Molecular determinants of peculiar properties of a Pleurotus ostreatus laccase: analysis by site-directed mutagenesis. Enzyme Microb Technol 45:507-513
33. Ferraroni M, Myasoedova NM, Schmatchenko V, Leontievsky AA, Golovleva LA, Scozzafava A, Briganti F (2007) Crystal structure of a blue laccase from Lentinus tigrinus: evidences for intermediates in the molecular oxygen reductive splitting by multicopper oxidases. BMC Struct Biol 7:60
34. Yoon JJ, Solomon EI (2007) Electronic structure of the peroxy intermediate and its correlation to the native intermediate in the multicopper oxidases: insights into the reductive cleavage of the O-O bond. J Am Chem Soc 129:13127-13136
35. Gupta A, Nederlof I, Sottini S, Tepper AW, Groenen EJ, Thomassen EA, Canters GW (2012) Involvement of tyr108 in the enzyme mechanism of the small laccase from Streptomyces coelicolor. J Am Chem Soc 134:18213-18216
36. Augustine AJ, Kragh ME, Sarangi R, Fujii S, Liboiron BD, Stoj CS et al (2008) Spectroscopic studies of perturbed T1 Cu sites in the multicopper oxidases Saccharomyces cerevisiae Fet3p and Rhus vernicifera laccase: allosteric coupling between the T1 and trinuclear Cu sites. Biochemistry 47:2036-2045
37. Bento I, Martins LO, Lopes GG, Carrondo MA, Lindley PF (2005) Dioxygen reduction by multi-copper oxidases; a structural perspective. Dalton Trans 21:3507-3513
38. Silva CS, Damas JM, Chen Z, Brissos V, Martins LO, Soares CM, Lindley PF, Bento I (2012) The role of Asp116 in the reductive cleavage of dioxygen to water in CotA laccase: assistance during the proton-transfer mechanism. Acta Crystallogr Sect D Biol Crystallogr 68:186-193
39. Brissos V, Chen Z, Martins LO (2012) The kinetic role of carboxylate residues in the proximity of the trinuclear centre in the O-2 reactivity of CotA-laccase. Dalton Trans 41:6247-6255
40. Chen Z, Durao P, Silva CS, Pereira MM, Todorovic S, Hildebrandt P, Bento I, Lindley PF, Martins LO (2010) The role of Glu(498) in the dioxygen reactivity of CotA-laccase from Bacillus subtilis. Dalton Trans 39:2875-2882
41. Ueki Y, Inoue M, Kurose S, Kataoka K, Sakurai T (2006) Mutations at Asp112 adjacent to the trinuclear Cu center in CueO as the proton donor in the four-electron reduction of dioxygen. FEBS Lett 580:4069-4072
42. Komori H, Kajikawa T, Kataoka K, Higuchi Y, Sakurai T (2013) Crystal structure of the CueO mutants at Glu506, the key amino acid located in the proton transfer pathway for dioxygen reduction. Biochem Biophys Res Commun 438:686-690
43. Kataoka K, Sugiyama R, Hirota S, Inoue M, Urata K, Minagawa Y, Seo D, Sakurai T (2009) Four-electron reduction of dioxygen by a multicopper oxidase, CueO, and roles of Asp112 and Glu506 located adjacent to the trinuclear copper center. J Biol Chem 284:14405-14413
44. Augustine AJ, Quintanar L, Stoj CS, Kosman DJ, Solomon EI (2007) Spectroscopic and kinetic studies of perturbed trinuclear copper clusters: the role of protons in reductive cleavage of the O-O bond in the multicopper oxidase Fet3p. J Am Chem Soc 129:13118-13126
45. Quintanar L, Stoj C, Wang TP, Kosman DJ, Solomon EJ (2005) Role of aspartate 94 in the decay of the peroxide intermediate in the multicopper oxidase Fet3p. Biochemistry 44:6081-6091
46. Messerschmidt A, Huber A (1990) The blue oxidases, ascorbate oxidase, laccase and ceruloplasmin. Modelling and structural relationships. Eur J Biochem 187:341-352
47. Nitta K, Kataoka K, Sakurai T (2002) Primary structure of a Japanese lacquer tree laccase as a prototype enzyme of multicopper oxidases. J Inorg Biochem 91:125-131
48. Koschorreck K, Schmid RD, Urlacher VB (2009) Improving the functional expression of a Bacillus licheniformis laccase by random and site-directed mutagenesis. BMC Biotechnol 9:12
49. Nasoohi N, Khajeh K, Mohammadian M, Ranjbar B (2013) Enhancement of catalysis and functional expression of a bacterial laccase by single amino acid replacement. Int J Biol Macromol 60:56-61
50. Bulter T, Alcalde M, Sieber V, Meinhold P, Schlachtbauer C, Arnold FH (2003) Functional expression of a fungal laccase in Saccharomyces cerevisiae by directed evolution. Appl Environ Microbiol 69:987-995
51. Andberg M, Hakulinen N, Auer S, Saloheimo M, Koivula A, Rouvinen J, Kruus K (2009) Essential role of the C-terminus in Melanocarpus albomyces laccase for enzyme production, catalytic properties and structure. FEBS J 276:6285-6300
52. Fernández-Larrea J, Stahl U (1996) Isolation and characterization of a laccase gene from Podospora anserina. Mol Gen Genet 252:539-551
53. Camarero S, Pardo I, Cañas AI, Molina P, Record E, Martínez AT, Martínez MJ, Alcalde M (2012) Engineering platforms for directed evolution of laccase from Pycnoporus cinnabarinus. Appl Environ Microbiol 78:1370-1384
54. Maté D, García-Burgos C, García-Ruiz E, Ballesteros A, Camarero S, Alcalde M (2010) Laboratory evolution of high redox potential laccases. Chem Biol 17:1030-1041
55. Mate D, García-Ruiz E, Camarero S, Shubin V, Falk M, Shleev S, Alcalde M (2013) Switching from blue to yellow: altering the spectral properties of a high redox potential laccase by directed evolution. Biocatal Biotransform 31:8-21
56. Toscano MD, De Maria L, Lobedanz S, Ostergaard LH (2013) Optimization of a small laccase by active-site redesign. Chembiochem 14:1209-1211
57. GuptaN, Lee FS, FarinasET(2010) Laboratory evolution of laccase for substrate specificity. J Mol Catal B Enzym 62:230-234
58. Pardo I, Vicente AI, Alcalde M, Camarero S (2012) Development of chimeric laccases by directed evolution. Biotechnol Bioeng 109:2978-2986
59. Cañas AI, Camarero S (2010) Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol Adv 28:694-705
60. Bleve G, Lezzi C, Spagnolo S, Tasco G, Tufariello M, Casadio R, Mita G, Rampino P, Grieco F (2013) Role of the C-terminus of Pleurotus eryngii Ery4 laccase in determining enzyme structure, catalytic properties and stability. Protein Eng Des Sel 26:1-13
61. Torres-Salas P, Mate DM, Ghazi I, Plou FJ, Ballesteros AO, Alcalde M (2013) Widening the pH activity profile of a fungal laccase by directed evolution. Chembiochem 14:934-937
62. Zumárraga M, Bulter T, Shleev S, Polaina J, Martinez-Arias A, Plou FJ, Ballesteros A, Alcalde M (2007) In vitro evolution of a fungal laccase in high concentrations of organic cosolvents. Chem Biol 14:1052-1064
63. Zumárraga M, Domínguez CV, Camarero S, Shleev S, Polaina J, Martínez-Arias A et al (2008) Combinatorial saturation mutagenesis of the Myceliophthora thermophila laccase T2 mutant: the connection between the C-terminal plug and the conserved (509)VSG(511) tripeptide. Comb Chem High Throughput Screen 11:807-816
64. Zumárraga M, Camarero S, Shleev S, Martinez-Arias A, Ballesteros A, Plou FJ, Alcalde M (2007) Altering the laccase functionality by in vivo assembly of mutant libraries with different mutational spectra. Proteins 71:250-260
65. Festa G, Autore F, Fraternali F, Giardina P, Sannia G (2008) Development of new laccases by directed evolution: functional and computational analyses. Proteins 72:25-34
66. Miele A, Giardina P, Notomista E, Piscitelli A, Sannia G, Faraco V (2010) A semi-rational approach to engineering laccase enzymes. Mol Biotechnol 46:149-156
67. Miele A, Giardina P, Sannia G, Faraco V (2010) Random mutants of a Pleurotus ostreatus laccase as new biocatalysts for industrial effluents bioremediation. J Appl Microbiol 108:998-1006
68. Bleve G, Lezzi C, Mita G, Rampino P, Perrotta C, Villanova L, Grieco F (2008) Molecular cloning and heterologous expression of a laccase gene from Pleurotus eryngii in free and immobilized Saccharomyces cerevisiae cells. Appl Microbiol Biotechnol 79:731-741
69. García-Ruiz E, Maté D, Ballesteros A, Martínez AT, Alcalde M (2010) Evolving thermostability in mutant libraries of ligninolytic oxidoreductases expressed in yeast. Microb Cell Fact 9:17
70. Alcalde M, Bulter T, Zumárraga M, García-Arellano H, Mencia M, Plou FJ, Ballesteros A (2005) Screening mutant libraries of fungal laccases in the presence of organic solvents. J Biomol Screen 10:624-631
71. Romero PA, Arnold FH (2009) Exploring protein fitness landscapes by directed evolution. Nat Rev Mol Cell Biol 10:866-876
72. Nakagawa Y, Sakamoto Y, Kikuchi S, Sato T, Yano A (2010) A chimeric laccase with hybrid properties of the parental Lentinula edodes laccases. Microbiol Res 165:392-401
73. Bleve G, Lezzi C, Spagnolo S, Rampino P, Perrotta C, Mita G, Grieco F (2014) Construction of a laccase chimerical gene: recombinant protein characterization and gene expression via yeast surface display. Appl Biochem Biotechnol 172:2916-2931
74. Pardo I, Camarero S (2014) Domain swapping between two high redox potential laccases: effect on enzyme properties. In: Proceedings of 13th EWLP, Sevilla, 24-27 June, 631-634
75. Cusano AM, Mekmouche Y, Meglecz E, Tron T (2009) Plasticity of laccase generated by homeologous recombination in yeast. FEBS J 276:5471-5480
76. Mate D, González-Pérez D, Falk M, Kittl R, Pita M, De Lacey AL, Ludwig R, Shleev S, Alcalde M (2013) Blood tolerant laccase by directed evolution. Chem Biol 20(2):223-231