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Laccases: a never-ending story

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Abstract

Laccases (benzenediol:oxygen oxidoreductases, EC 1.10.3.2) are blue multicopper oxidases that catalyze the oxidation of an array of aromatic substrates concomitantly with the reduction of molecular oxygen to water. In fungi, laccases carry out a variety of physiological roles during their life cycle. These enzymes are being increasingly evaluated for a variety of biotechnological applications due to their broad substrate range. In this review, the most recent studies on laccase structural features and catalytic mechanisms along with analyses of their expression are reported and examined with the aim of contributing to the discussion on their structure–function relationships. Attention has also been paid to the properties of enzymes endowed with unique characteristics and to fungal laccase multigene families and their organization.

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References

  1. Solomon EI, Sundaram UM, Machonkin TE (1996) Multicopper oxidases and oxygenases. Chem Rev 96:2563–2605

    Article  CAS  PubMed  Google Scholar 

  2. Messerschmidt A (1997) Multi-copper oxidases. World Scientific, Singapore

    Book  Google Scholar 

  3. Yoshida H (1883) Chemistry of lacquer (urushi). Part I. J Chem Soc 43:472–486

    CAS  Google Scholar 

  4. Thurston CF (1994) The structure and function of fungal laccases. Microbiology 140:19–26

    Article  CAS  Google Scholar 

  5. Gianfreda L, Xu F, Bollag JM (1999) Laccases: a useful group of oxidoreductive enzymes. Bioremediat J 3:1–26

    Article  CAS  Google Scholar 

  6. Heinzkill M, Messner K (1997) The ligninolytic system of fungi. In: Anke T (ed) Fungal biotechnology. Chapman & Hall, Weinheim, pp 213–226

    Google Scholar 

  7. Bao W, O’Malley DM, Whetten R, Sederoff RR (1993) A laccase associated with lignification in loblolly pine xylem. Science 260:672–674

    Article  CAS  PubMed  Google Scholar 

  8. Sato Y, Bao W, Sederoff R, Whetten R (2001) Molecular cloning and expression of eight laccase cDNAs in loblolly pine (Pinus taeda). J Plant Res 114:147–155

    Article  CAS  Google Scholar 

  9. Sharma P, Goel R, Capalash N (2007) Bacterial laccases. World J Microbiol Biotechnol 23:823–832

    Article  CAS  Google Scholar 

  10. Roberts SA, Weichsel A, Grass G, Thakali K, Hazzard JT, Tollin G, Rensing C, Montfort WR (2002) Crystal structure and electron transfer kinetics of CueO, a multicopper oxidase required for copper homeostasis in Escherichia coli. Proc Natl Acad Sci USA 99:2766–2771

    Article  CAS  PubMed  Google Scholar 

  11. Enguita FJ, Martins LO, Henriques AO, Carrondo MA (2003) Crystal structure of a bacterial endospore coat component. A laccase with enhanced thermostability properties. J Biol Chem 278:19416–19425

    Article  CAS  PubMed  Google Scholar 

  12. Dittmer NT, Suderman RJ, Jiang H, Zhu YC, Gorman MJ, Kramer KJ, Kanost MR (2004) Characterization of cDNAs encoding putative laccase-like multicopper oxidases and developmental expression in the tobacco hornworm, Manduca sexta, and the malaria mosquito, Anopheles gambiae. Insect Biochem Mol Biol 34:29–41

    Article  CAS  PubMed  Google Scholar 

  13. Parkinson NM, Conyers CM, Keen JN, MacNicoll AD, Smith I, Weaver RJ (2003) cDNAs encoding large venom proteins from the parasitoid wasp Pimpla hypochondriaca identified by random sequence analysis. Comp Biochem Physiol C Toxicol Pharmacol 134:513–520

    Article  PubMed  CAS  Google Scholar 

  14. Yaropolov AI, Skorobogat’ko OV, Vartanov SS, Varfolomeev SD (1994) Laccase: properties, catalytic mechanism, and applicability. Appl Biochem Biotechnol 49:257–280

    Article  CAS  Google Scholar 

  15. Sakurai T (1992) Anaerobic reactions of Rhus vernicifera laccase and its type-2 copper-depleted derivatives with hexacyanoferrate(II). Biochem J 284:681–685

    CAS  PubMed  Google Scholar 

  16. Hofer C, Schlosser D (1999) Novel enzymatic oxidation of Mn2+ to Mn3+ catalyzed by a fungal laccase. FEBS Lett 451:186–190

    Article  CAS  PubMed  Google Scholar 

  17. Schlosser D, Hofer C (2002) Laccase-catalyzed oxidation of Mn2+ in the presence of natural Mn3+ chelators as a novel source of extracellular H2O2 production and its impact on manganese peroxidase. Appl Environ Microbiol 68:3514–3521

    Article  CAS  PubMed  Google Scholar 

  18. De Souza CGM, Peralta RM (2003) Purification and characterization of the main laccase produced by the white-rot fungus Pleurotus pulmonarius on wheat bran solid state medium. J Basic Microbiol 43:278–286

    Article  Google Scholar 

  19. Shleev SV, Morozova O, Nikitina O, Gorshina ES, Rusinova T, Serezhenkov VA, Burbaev DS, Gazaryan IG, Yaropolov AI (2004) Comparison of physico-chemical characteristics of four laccases from different basidiomycetes. Biochimie 86:693–703

    Article  CAS  PubMed  Google Scholar 

  20. Kumar SVS, Phale PS, Durani S, Wangikar PP (2003) Combined sequence and structure analysis of the fungal laccase family. Biotechnol Bioeng 83:386–394

    Article  CAS  PubMed  Google Scholar 

  21. Larrondo LF, Salas L, Melo F, Vicuna R, Cullen D (2003) A novel extracellular multicopper oxidase from Phanerochaete chrysosporium with ferroxidase activity. Appl Environ Microbiol 69:6257–6263

    Article  CAS  PubMed  Google Scholar 

  22. Ducros V, Brzozowski AM, Wilson KS, Brown SH, Østergaard P, Schneider P, Yaver DS, Pedersen AH, Davies GJ (1998) Crystal structure of the type-2 Cu depleted laccase from Coprinus cinereus at 2.2 Å resolution. Nat Struct Biol 5:310–316

    Article  CAS  PubMed  Google Scholar 

  23. 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. J Biol Chem 277:37663–37669

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  25. Garavaglia S, Cambria MT, Miglio M, Ragusa S, Iacobazzi 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

    Article  CAS  PubMed  Google Scholar 

  26. 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 7:60–72

    Article  PubMed  CAS  Google Scholar 

  27. 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

    Article  CAS  Google Scholar 

  28. Hakulinen N, Kiiskinen LL, 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. Nat Struct Biol 9:601–605

    CAS  PubMed  Google Scholar 

  29. Hakulinen N, Andberg M, Kallio J, Koivula A, Kruus K, Rouvinen J (2008) A near atomic resolution structure of a Melanocarpus albomyces laccase. J Struc Biol 162:29–39

    Article  CAS  Google Scholar 

  30. Murphy MEP, Lindley PF, Adman ET (1997) Structural comparison of cupredoxin domains: domain recycling to construct proteins with novel functions. Protein Sci 6:761–770

    Article  CAS  PubMed  Google Scholar 

  31. Messerschmidt A, Ladenstein R, Huber R, Bolognesi M, Avigliano L, Petruzzelli R, Rossi A, Finazzi Agrò A (1992) Refined crystal structure of ascorbate oxidase at 1.9 Å resolution. J Mol Biol 224:179–205

    Article  CAS  PubMed  Google Scholar 

  32. Zaitsev I, Zaitsev V, Card G, Moshkov K, Bax B, Ralph A, Lindley P (1996) The nature of the copper centres in human ceruloplasmin. J Biol Inorg Chem 1:15–23

    Article  Google Scholar 

  33. Lee SK, George SD, Antholine WE, Hedman B, Hodgson KO, Solomon EI (2002) Nature of the intermediate formed in the reduction of O2 to H2O at the trinuclear copper cluster active site in native laccase. J Am Chem Soc 124:6180–6193

    Article  CAS  PubMed  Google Scholar 

  34. Solomon EI, Augustine AJ, Yoon J (2008) O2 reduction to H2O by the multicopper oxidases. Dalton Trans 30:3921–3932

    Article  PubMed  CAS  Google Scholar 

  35. Marcus RA, Sutin N (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811:265–322

    CAS  Google Scholar 

  36. Xu F, Shin W, Brown SH, Wahleithner JA, Sundaram UM, Solomon EI (1996) A study of a series of recombinant fungal laccases and birilubin oxidase that exhibit significant differences in redox potential, substrate specificity and stability. Biochim Biophys Acta 1292:303–311

    PubMed  Google Scholar 

  37. 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

    Article  CAS  PubMed  Google Scholar 

  38. Klonowska A, Gaudin C, Fournel A, Asso M, Le Petit J, Giorgi M, Tron T (2002) Characterization of a low redox potential laccase from the basidiomycete C30. Eur J Biochem 269:6119–6125

    Article  CAS  PubMed  Google Scholar 

  39. Gray HB, Malmstrom BG, Williams RJ (2000) Copper coordination in blue proteins. J Biol Inorg Chem 5:551–559

    Article  CAS  PubMed  Google Scholar 

  40. Durao P, Bento I, Fernandes AT, Melo EP, Lindley PF, Martins LO (2006) Perturbation of the T1 copper site in CotA-laccase from Bacillus subtilis: structural, biochemical, enzymatic and stability studies. J Biol Inorg Chem 11:514–526

    Article  CAS  PubMed  Google Scholar 

  41. Enguita FJ, Marcal D, Martins LO, Grenha R, Henriques AO, Lindley PF, Carrondo MA (2004) Substrate and dioxygen binding to the endospore coat laccase from Bacillus subtilis. J Biol Chem 279:23472–23476

    Article  CAS  PubMed  Google Scholar 

  42. Xu F (1997) Effects of redox potential and hydroxide inhibition on the pH activity profile of fungal laccases. J Biol Chem 272:924–928

    CAS  PubMed  Google Scholar 

  43. 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

    CAS  PubMed  Google Scholar 

  44. 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

    Article  CAS  PubMed  Google Scholar 

  45. Bonomo RP, Boudet AM, Cozzolino R, Rizzarelli E, Santoro AM, Sterjiades R, Zappala R (1998) A comparative study of two isoforms of laccase secreted by the “white-rot” fungus Rigidoporus lignosus, exhibiting significant structural and functional differences. J Inorg Biochem 71:205–211

    Article  CAS  PubMed  Google Scholar 

  46. Tadesse MA, D’Annibale A, Galli C, Gentilia P, Sergia 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

    Article  CAS  PubMed  Google Scholar 

  47. Torres J, Svistunenko D, Karlsson B, Cooper CE, Wilson MT (2002) Fast reduction of a copper center in laccase by nitric oxide and formation of a peroxide intermediate. J Am Chem Soc 124:963–967

    Article  CAS  PubMed  Google Scholar 

  48. Yoon J, 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

    Article  CAS  PubMed  Google Scholar 

  49. Yoon J, Liboiron BD, Sarangi R, Hodgson KO, Hedman B, Solomon EI (2007) The two oxidized forms of the trinuclear Cu cluster in the multicopper oxidases and mechanism for the decay of the native intermediate. Proc Natl Acad Sci USA 104:13609–13614

    Article  CAS  PubMed  Google Scholar 

  50. Palmer AE, Lee SK, Solomon EI (2001) Decay of the peroxide intermediate in laccase: reductive cleavage of the O–O bond. J Am Chem Soc 123:6591–6599

    Article  CAS  PubMed  Google Scholar 

  51. Zoppellaro G, Sakurai T, Huang H (2001) A novel mixed valence form of Rhus vernicifera laccase and its reaction with dioxygen to give a peroxide intermediate bound to the trinuclear center. J Biochem 129:949–953

    CAS  PubMed  Google Scholar 

  52. 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

    Article  CAS  PubMed  Google Scholar 

  53. Augustine AJ, Kragh ME, Sarangi R, Fujii S, Liboiron BD, Stoj CS, Kosman DJ, Hodgson KO, Hedman B, Solomon EI (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

    Article  CAS  PubMed  Google Scholar 

  54. Quintanar L, Yoon J, Aznar CP, Palmer AE, Andersson KK, Britt RD, Solomon EI (2005) Spectroscopic and electronic structure studies of the trinuclear Cu cluster active site of the multicopper oxidase laccase: nature of its coordination unsaturation. J Am Chem Soc 127:13832–13845

    Article  CAS  PubMed  Google Scholar 

  55. 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

    Article  PubMed  CAS  Google Scholar 

  56. Kyritsis P, Messerschmidt A, Huber R, Salmon GA, Sykes AG (1993) Pulse-radiolysis studies on the oxidized form of the multicopper enzyme ascorbate oxidase—evidence for 2 intramolecular electron-transfer steps. Dalton Trans 5:731–735

    Google Scholar 

  57. Fernandez Larrea J, Stahl U (1996) Isolation and characterization of a laccase gene from Podospora anserina. Mol Gen Genet 252:539–551

    CAS  PubMed  Google Scholar 

  58. Germann UA, Muller G, Hunziker PE, Lerch K (1988) Characterization of 2 allelic forms of Neurospora crassa laccase amino-terminal and carboxyl-terminal processing of a precursor. J Biol Chem 263:885–896

    CAS  PubMed  Google Scholar 

  59. Kiiskinen LL, Saloheimo M (2004) Molecular cloning and expression in Saccharomyces cerevisiae of a laccase gene from the ascomycete Melanocarpus albomyces. Appl Environ Microb 70:137–144

    Article  CAS  Google Scholar 

  60. 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 Microb 69:987–995

    Article  CAS  Google Scholar 

  61. Zumárraga M, Camarero S, Shleev S, Martínez-Arias A, Ballesteros A, Plou FJ, Alcalde M (2008) Altering the laccase functionality by in vivo assembly of mutant libraries with different mutational spectra. Proteins 71:250–260

    Article  PubMed  CAS  Google Scholar 

  62. Gelo-Pujic M, Kim HH, Butlin NG, Palmore GT (1999) Electrochemical studies of a truncated laccase produced in Pichia pastoris. Appl Environ Microbiol 65:5515–5521

    CAS  PubMed  Google Scholar 

  63. Giardina P, Palmieri G, Scaloni A, Fontanella B, Faraco V, Cennamo G, Sannia G (1999) Protein and gene structure of a blue laccase from Pleurotus ostreatus. Biochem J 341:655–663

    Article  CAS  PubMed  Google Scholar 

  64. Piscitelli A, Giardina P, Mazzoni C, Sannia G (2005) Recombinant expression of Pleurotus ostreatus laccases in Kluyveromyces lactis and Saccharomyces cerevisiae. Appl Microbiol Biotechnol 69:428–439

    Article  CAS  PubMed  Google Scholar 

  65. Festa G, Autore F, Fraternali F, Giardina P, Sannia G (2007) Development of new laccases by directed evolution: functional and computational analyses. Proteins 72:25–34

    Article  CAS  Google Scholar 

  66. Kawai S, Umezawa T, Higuchi T (1988) Degradation mechanisms of phenolic beta-1 lignin substructure model compounds by laccase of Coriolus versicolor. Arch Biochem Biophys 262:99–110

    Article  CAS  PubMed  Google Scholar 

  67. Xu F (1996) Oxidation of phenols, anilines, and benzenethiols by fungal laccases: correlation between activity and redox potentials as well as halide inhibition. Biochem 35:7608–7614

    Article  CAS  Google Scholar 

  68. Garzillo AM, Colao MC, Caruso C, Caporale C, Celletti D, Buonocore V (1998) Laccase from the white-rot fungus Trametes trogii. Appl Microbiol Biotechnol 49:545–551

    Article  CAS  PubMed  Google Scholar 

  69. Bajpai P (1999) Application of enzymes in the pulp and paper industry. Biotechnol Prog 15:147–157

    Article  CAS  PubMed  Google Scholar 

  70. Durán N, Esposito E (2000) Potential applications of oxidative enzymes and phenoloxidase-like compounds in wastewater and soil treatment: a review. Appl Catal B Environ 28:83–99

    Article  Google Scholar 

  71. Abadulla E, Tzanov T, Costa S, Robra KH, Cavaco-Paulo A, Gübitz GM (2000) Decolorization and detoxification of textile dyes with a laccase from Trametes hirsuta. Appl Environ Microbiol 66:3357–3362

    Article  CAS  PubMed  Google Scholar 

  72. Minussi R, Pastore GM, Duran N (2002) Potential applications of laccase in the food industry. Trends Food Sci Technol 13:205–216

    Article  CAS  Google Scholar 

  73. Amir L, Tam TK, Pita M, Meijler MM, Alfonta L, Katz E (2009) Biofuel cell controlled by enzyme logic systems. J Am Chem Soc 131:826–832

    Article  CAS  PubMed  Google Scholar 

  74. Pereira L, Coelho AV, Viegas CA, Santos MM, Robalo MP, Martins LO (2009) Enzymatic biotransformation of the azo dye Sudan Orange G with bacterial CotA-laccase. J Biotechnol 139:68–77

    Article  CAS  PubMed  Google Scholar 

  75. Couto SR (2007) Decolouration of industrial azo dyes by crude laccase from Trametes hirsuta. J Hazard Mater 148:768–770

    Article  CAS  PubMed  Google Scholar 

  76. Palmieri G, Cennamo G, Sannia G (2005) Remazol Brilliant Blue R decolourisation by the fungus Pleurotus ostreatus and its oxidative enzymatic system. Enzyme Microb Technol 36:17–24

    Article  CAS  Google Scholar 

  77. Palmieri G, Giardina P, Sannia G (2005) Laccase-mediated Remazol Brilliant Blue R decolorization in a fixed-bed bioreactor. Biotechnol Prog 21:1436–1441

    Article  CAS  PubMed  Google Scholar 

  78. Vanhulle S, Trovaslet M, Enaud E, Lucas M, Sonveaux M, Decock C, Onderwater R, Schneider YJ, Corbisier AM (2008) Cytotoxicity and genotoxicity evolution during decolourisation of dyes by white rot fungi. World J Microbiol Biotechnol 24:337–344

    Article  CAS  Google Scholar 

  79. Vanhulle S, Trovaslet M, Enaud E, Lucas M, Taghavi S, Van Der Lelie D, Van Aken B, Foret M, Onderwater R, Wesenberg D, Agathos S, Schneider YJ, Corbisier AM (2008) Decolourisation, cytotoxicity and genotoxicity reduction during a combined ozonation/fungal treatment of dye contaminated wastewater. Environ Sci Technol 42:584–589

    Article  CAS  PubMed  Google Scholar 

  80. Kunamneni A, Camarero S, García-Burgos C, Plou FJ, Ballesteros A, Alcalde M (2008) Engineering and applications of fungal laccases for organic synthesis. Microb Cell Fact 7:32–49

    Article  PubMed  CAS  Google Scholar 

  81. Aktaş N, Tanyolaç A (2003) Reaction conditions for laccase catalyzed polymerization of catechol. Bioresour Technol 87:209–214

    Article  PubMed  Google Scholar 

  82. Ceylan H, Kubilay S, Aktas N, Sahiner N (2008) An approach for prediction of optimum reaction conditions for laccase-catalyzed bio-transformation of 1-naphthol by response surface methodology (RSM). Bioresour Technol 99:2025–2031

    Article  CAS  PubMed  Google Scholar 

  83. Ikeda R, Tanaka H, Oyabu H, Uyama H, Kobayashi S (2001) Preparation of artificial urushi via an environmentally benign process. Bull Chem Soc Jpn 74:1067–1073

    Article  CAS  Google Scholar 

  84. Bruyneel F, Enaud E, Billottet L, Vanhulle S, Marchand-Brynaert J (2008) Regioselective synthesis of 3-hydroxyorthanilic acid and its biotransformation with laccase into a novel phenoxazinone dye. Eur J Org Chem 1:72–79

    Article  Google Scholar 

  85. Ossiadacz J, Al-Adhami AJH, Bajraszewska D, Fischer P, Peczynska-Czoch W (1999) On the use of Trametes versicolor laccase for the conversion of 4-methyl-3-hydroxyanthranilic acid to actinocin chromophore. J Biotechnol 72:141–149

    Article  Google Scholar 

  86. Nicotra S, Cramarossa MR, Mucci A, Pagnoni UM, Riva S, Forti L (2004) Biotransformation of resveratrol: synthesis of trans-dehydrodimers catalyzed by laccases from Myceliophtora thermophyla and from Trametes pubescens. Tetrahedron 60:595–600

    Article  CAS  Google Scholar 

  87. Bourbonnais R, Paice MG, Freiermuth B, Bodie E, Borneman S (1997) Reactivities of various mediators and laccases with kraft pulp and lignin model compounds. Appl Environ Microbiol 63:4627–4632

    CAS  PubMed  Google Scholar 

  88. Bourbonnais R, Paice MG (1990) Oxidation of nonphenolic substrates—an expanded role for laccase in lignin biodegradation. FEBS Lett 267:99–102

    Article  CAS  PubMed  Google Scholar 

  89. Barreca AM, Fabbrini M, Galli C, Gentili P, Ljunggren S (2003) Laccase-mediated oxidation of lignin model for improved delignification procedures. J Mol Cat B Enzym 26:105–110

    Article  CAS  Google Scholar 

  90. Li K, Xu F, Eriksson KE (1999) Comparison of fungal laccases and redox mediators in oxidation of a nonphenolic lignin model compound. Appl Environ Microbiol 65:2654–2660

    CAS  PubMed  Google Scholar 

  91. Xu F, Kulys JJ, Duke K, Li K, Krikstopaitis K, Deussen HJW, Abbate E, Galinyte V, Schneider P (2000) Redox chemistry in laccase-catalyzed oxidation of N-hydroxy compounds. Appl Environ Microbiol 66:2052–2056

    Article  CAS  PubMed  Google Scholar 

  92. Fabbrini M, Galli C, Gentili P (2002) Comparing the catalytic efficiency of some mediators of laccase. J Mol Cat B Enzym 16:231–240

    Article  CAS  Google Scholar 

  93. Brogioni B, Biglino D, Sinicropi A, Reijerse EJ, Giardina P, Sannia G, Lubitz W, Basosi R, Pogni R (2008) Characterization of radical intermediates in laccase-mediator systems. A multifrequency EPR, ENDOR and DFT/PCM investigation. Phys Chem Chem Phys 10:7284–7292

    Article  CAS  PubMed  Google Scholar 

  94. Collins PJ, Kotterman MJJ, Field JA, Dobson ADW (1996) Oxidation of anthracene and benzo[a]pyrene by laccases from Trametes versicolor. Appl Environ Microbiol 62:4563–4567

    CAS  PubMed  Google Scholar 

  95. Camarero S, García O, Vidal T, Colom J, del Río JC, Gutiérrez A, Gras JM, Monje R, Martínez MJ, Martínez T (2004) Efficient bleaching of non-wood high-quality paper pulp using laccase-mediator system. Enzyme Microbiol Technol 35:113–120

    Article  CAS  Google Scholar 

  96. Gutiérrez A, del Río JC, Ibarra D, Rencoret J, Romero J, Speranza M, Camarero S, Martínez MJ, Martínez AT (2006) Enzymatic removal of free and conjugated sterols forming pitch deposits in environmentally sound bleaching of eucalypt paper pulp. Environ Sci Technol 40:3416–3422

    Article  PubMed  CAS  Google Scholar 

  97. Hu MR, Chao YP, Zhang GQ, Xue ZQ, Qian S (2009) Laccase-mediator system in the decolorization of different types of recalcitrant dyes. J Ind Microbiol Biotechnol 36:45–51

    Article  CAS  PubMed  Google Scholar 

  98. Galante YM, Formantici C (2003) Enzyme applications in detergency and in manufacturing industries. Curr Org Chem 7:1399–1422

    Article  CAS  Google Scholar 

  99. Camarero S, Cañas AI, Nousiainen P, Record E, Lomascolo A, Martínez MJ, Martínez AT (2008) P-hydroxycinnamic acids as natural mediators for laccase oxidation of recalcitrant compounds. Environ Sci Technol 42:6703–6709

    Article  CAS  PubMed  Google Scholar 

  100. Camarero S, Ibarra D, Martínez AT, Romero J, Gutiérrez A, del Río JC (2007) Paper pulp delignification using laccase and natural mediators. Enzyme Microb Technol 40:1264–1271

    Article  CAS  Google Scholar 

  101. Cañas A, Alcalde M, Plou FJ, Martínez MJ, Martínez AT, Camarero S (2007) Transformation of polycyclic aromatic hydrocarbons by laccase is strongly enhanced by phenolic compounds present in soil. Environ Sci Technol 41:2964–2971

    Article  PubMed  CAS  Google Scholar 

  102. Jeon JR, Murugesan K, Kim YM, Kim EJ, Chang YS (2008) Synergistic effect of laccase mediators on pentachlorophenol removal by Ganoderma lucidum laccase. Appl Microbiol Biotechnol 81:783–790

    Article  CAS  PubMed  Google Scholar 

  103. Nakamura K, Go N (2005) Function and molecular evolution of multicopper blue proteins. Cell Mol Life Sci 62:2050–2066

    Article  CAS  PubMed  Google Scholar 

  104. Pezet R (1998) Purification and characterization of a 32-kDa laccase-like stilbene oxidase produced by Botrytis cinerea Pers.:Fr. FEMS Microbiol Lett 167:203–208

    Article  CAS  Google Scholar 

  105. Wang HX, Ng TB (2004) Purification of a novel low molecular-mass laccase with HIV-1 reverse transcriptase inhibitory activity from the mushroom Tricholoma giganteum. Biochem Biophys Res Commun 315:450–454

    Article  CAS  PubMed  Google Scholar 

  106. Yaver DS, Xu F, Golightly EJ, Brown KM, Brown SH, Rey MW, Schneider P, Halkier T, Mondorf K, Dalboge H (1996) Purification, characterization, molecular cloning, and expression of two laccase genes from the white rot basidiomycete Trametes villosa. Appl Environ Microbiol 62:834–841

    CAS  PubMed  Google Scholar 

  107. Min KL, Kim YH, Kim YW, Jung HS, Hah YC (2001) Characterization of a novel laccase produced by the wood-rotting fungus Phellinus ribis. Arch Biochem Biophys 392:279–286

    Article  CAS  PubMed  Google Scholar 

  108. Wahleithner JA, Xu F, Brown KM, Brown SH, Golightly EJ, Halkier T, Kauppinen S, Pederson A, Schneider P (1996) The identification and characterization of four laccases from the plant pathogenic fungus Rhizoctonia solani. Curr Genet 29:395–403

    Article  CAS  PubMed  Google Scholar 

  109. Edens WA, Goins TQ, Dooley D, Henson JM (1999) Purification and characterization of a secreted laccase of Gaeumannomyces graminis var. tritici. Appl Environ Microbiol 65:3071–3074

    CAS  PubMed  Google Scholar 

  110. Junghanns C, Pecyna MJ, Böhm D, Jehmlich N, Martin C, von Bergen M, Schauer F, Hofrichter M, Schlosser D (2009) Biochemical and molecular genetic characterisation of a novel laccase produced by the aquatic ascomycete Phoma sp. UHH 5-1-03. Appl Microbiol Biotechnol. doi:10.1007/s00253-009-2028-2

  111. Wang HX, Ng TB (2006) Purification of a laccase from fruiting bodies of the mushroom Pleurotus eryngii. Appl Microbiol Biotechnol 69:521–525

    Article  CAS  PubMed  Google Scholar 

  112. Ng TB, Wang HX (2004) A homodimeric laccase with unique characteristics from the yellow mushroom Cantharellus cibarius. Biochem Biophys Res Commun 313:37–41

    Article  CAS  PubMed  Google Scholar 

  113. Lawton TJ, Sayavedra-Soto LA, Arp DJ, Rosenzweig AC (2009) Crystal structure of a two-domain multicopper oxidase: implications for the evolution of multicopper blue proteins. J Biol Chem 284:10174–10180

    Article  CAS  PubMed  Google Scholar 

  114. Skálová T, Dohnálek J, Østergaard LH, Østergaard PR, Kolenko P, Dušková J, Štepánková A, Hašek 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

    Article  PubMed  CAS  Google Scholar 

  115. Komori H, Miyazaki K, Higuchi Y (2009) X-ray structure of a two-domain type laccase: a missing link in the evolution of multi-copper proteins. FEBS Lett 583:1189–1195

    Article  CAS  PubMed  Google Scholar 

  116. Wood DA (1980) Production, purification and properties of extracellular laccase of Agaricus bisporus. J Gen Microbiol 117:327–338

    CAS  Google Scholar 

  117. Curir P, Thurston CF, Daquila F, Pasini C, Marchesini A (1997) Characterization of a laccase secreted by Armillaria mellea pathogenic for Genista. Plant Physiol Biochem 35:147–153

    CAS  Google Scholar 

  118. Minuth W, Klischies M, Esser K (1978) The phenoloxidases of the ascomycete Podospora anserina. Structural differences between laccases of high and low molecular weight. Eur J Biochem 90:73–82

    Article  CAS  PubMed  Google Scholar 

  119. Kurtz MB, Champe SP (1982) Purification and characterization of the conidial laccase of Aspergillus nidulans. J Bacteriol 151:1338–1345

    CAS  PubMed  Google Scholar 

  120. Thakker GD, Evans CS, Rao KK (1992) Purification and characterization of laccase from Monocillium indicum Saxena. Appl Microbiol Biotechnol 37:321–323

    Article  CAS  Google Scholar 

  121. Perry CR, Matcham SE, Wood DA, Thurston CF (1993) The structure of laccase protein and its synthesis by the commercial mushroom Agaricus bisporus. J Gen Microbiol 139:171–178

    CAS  PubMed  Google Scholar 

  122. Palmieri G, Cennamo G, Faraco V, Amoresano A, Sannia G, Giardina P (2003) Atypical laccase isoenzymes from copper supplemented Pleurotus ostreatus cultures. Enzyme Microb Technol 33:220–230

    Article  CAS  Google Scholar 

  123. Giardina P, Autore F, Faraco V, Festa G, Palmieri G, Piscitelli A, Sannia G (2007) Structural characterization of heterodimeric laccases from Pleurotus ostreatus. Appl Microbiol Biotechnol 75:1293–1300

    Article  CAS  PubMed  Google Scholar 

  124. Hoegger PJ, Kilaru S, James TY, Thacker JR, Kues U (2006) Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J 273:2308–2326

    Article  CAS  PubMed  Google Scholar 

  125. Pezzella C, Autore F, Giardina P, Piscitelli A, Sannia G, Faraco V (2009) The Pleurotus ostreatus laccase multi-gene family: isolation and heterologous expression of new family members. Curr Genet 55:45–57

    Article  CAS  PubMed  Google Scholar 

  126. Faraco V, Ercole C, Festa G, Giardina P, Piscitelli A, Sannia G (2008) Heterologous expression of heterodimeric laccase from Pleurotus ostreatus in Kluyveromyces lactis. Appl Microbiol Biotechnol 77:1329–1335

    Article  CAS  PubMed  Google Scholar 

  127. Mei G, Di Venere A, Buganza M, Vecchini P, Rosato N, Finazzi-Agrò A (1997) Role of quaternary structure in the stability of dimeric proteins: the case of ascorbate oxidase. Biochemistry 36:10917–10922

    Article  CAS  PubMed  Google Scholar 

  128. Nicolai E, Di Venere A, Rosato N, Rossi A, Finazzi Agrò A, Mei G (2006) Physico-chemical properties of molten dimer ascorbate oxidase. FEBS J 273:5194–5204

    Article  CAS  PubMed  Google Scholar 

  129. Vries OMH, Kooistra WHCF, Wessels GH (1986) Formation of an extracellular laccase by Schizophyllum commune dikaryon. J Gen Microbiol 132:2817–2826

    Google Scholar 

  130. Leontievsky A, Myasoedova N, Pozdnyakova N, Golovleva L (1997) “Yellow” laccase of Panus tigrinus oxidizes nonphenolic substrates without electron-transfer mediators. FEBS Lett 413:446–448

    Article  CAS  PubMed  Google Scholar 

  131. Leontievsky AA, Vares T, Lankinen P, Shergill JK, Pozdnyakova NN, Myasoedova NM, Kalkkinen N, Golovleva LA, Cammack R, Thurston CF, Hatakka A (1997) Blue and yellow laccases of ligninolytic fungi. FEMS Microbiol Lett 156:9–14

    Article  CAS  PubMed  Google Scholar 

  132. Pozdnyakova NN, Rodakiewicz-Nowak J, Turkovskaya OV (2004) Catalytic properties of yellow laccase from Pleurotus ostreatus D1. J Mol Catal B 30:19–24

    Article  CAS  Google Scholar 

  133. Pozdnyakova NN, Turkovskaya OV, Yudina EN, Rodakiewicz-Nowak Ya (2006) Yellow laccase from the fungus Pleurotus ostreatus D1: purification and characterization. Appl Biochem Microbiol 42:56–61

    Article  CAS  Google Scholar 

  134. Palmieri G, Giardina P, Bianco C, Scaloni A, Capasso A, Sannia G (1997) A novel white laccase from Pleurotus ostreatus. J Biol Chem 272:31301–31307

    Article  CAS  PubMed  Google Scholar 

  135. Litthauer D, Jansen van Vuuren M, van Tonder A, Wolfaardt FW (2007) Purification and kinetics of a thermostable laccase from Pycnoporus sanguineus (SCC 108). Enzyme MicrobTechnol 40:563–568

    Article  CAS  Google Scholar 

  136. Haibo Z, Yinglong Z, Feng H, Peiji G, Jiachuan C (2009) Purification and characterization of a thermostable laccase with unique oxidative characteristics from Trametes hirsuta. Biotechnol Lett 31:837–843

    Article  PubMed  CAS  Google Scholar 

  137. Kaneko S, Cheng M, Murai H, Takenaka S, Murakami S, Aoki K (2009) Purification and characterization of an extracellular laccase from Phlebia radiata strain BP-11-2 that decolorizes fungal melanin. Biosci Biotechnol Biochem 73:939–942

    Article  CAS  PubMed  Google Scholar 

  138. Chernykh A, Myasoedova N, Kolomytseva M, Ferraroni M, Briganti F, Scozzafava A, Golovleva L (2008) Laccase isoforms with unusual properties from the basidiomycete Steccherinum ochraceum strain 1833. J Appl Microbiol 105:2065–2075

    Article  CAS  PubMed  Google Scholar 

  139. Hoshida H, Nakao M, Kanazawa H, Kubo K, Hakukawa T, Morimasa K, Akada R, Nishizawa Y (2001) Isolation of five laccase gene sequences from the white-rot fungus Trametes sanguinea by PCR, and cloning, characterization and expression of the laccase cDNA in yeasts. J Biosci Bioeng 92:372–380

    Article  CAS  PubMed  Google Scholar 

  140. Mansur M, Suárez T, Fernández-Larrea JB, Brizuela MA, González AE (1997) Identification of a laccase gene family in the new lignin-degrading basidiomycete CECT 20197. Appl Environ Microbiol 63:2637–2646

    CAS  PubMed  Google Scholar 

  141. Xiao YZ, Hong YZ, Li JF, Hang J, Tong PG, Fang W, Zhou CZ (2006) Cloning of novel laccase isozyme genes from Trametes sp. AH28–2 and analyses of their differential expression. Appl Microbiol Biotechnol 71:493–501

    Article  CAS  PubMed  Google Scholar 

  142. Litvintseva AP, Henson JM (2002) Cloning, characterization, and transcription of three laccase genes from Gaeumannomyces graminis var. tritici, the take-all fungus. Appl Environ Microbiol 68:1305–1311

    Article  CAS  PubMed  Google Scholar 

  143. Soden DM, Dobson AD (2001) Differential regulation of laccase gene expression in Pleurotus sajor-caju. Microbiology 147:1755–1763

    CAS  PubMed  Google Scholar 

  144. Rodríguez E, Ruiz-Dueñas FJ, Kooistra R, Ram A, Martínez AT, Martínez MJ (2008) Isolation of two laccase genes from the white-rot fungus Pleurotus eryngii and heterologous expression of the pel3 encoded protein. J Biotechnol 134:9–19

    Article  PubMed  CAS  Google Scholar 

  145. Kilaru S, Hoegger PJ, Kües U (2006) The laccase multi-gene family in Coprinopsis cinerea has seventeen different members that divide into two distinct subfamilies. Curr Genet 50:45–60

    Article  CAS  PubMed  Google Scholar 

  146. Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Duenas FJ, Martinez AT, Kersten P, Hammel KE, Vanden Wymelenberg A, Gaskell J, Lindquist E, Sabat G, Bondurant SS, Larrondo LF, Canessa P, Vicuna R, Yadav J, Doddapaneni H, Subramanian V, Pisabarro AG, Lavín JL, Oguiza JA, Master E, Henrissat B, Coutinho PM, Harris P, Magnuson JK, Baker SE, Bruno K, Kenealy W, Hoegger PJ, Kües U, Ramaiya P, Lucas S, Salamov A, Shapiro H, Tu H, Chee CL, Misra M, Xie G, Teter S, Yaver D, James T, Mokrejs M, Pospisek M, Grigoriev IV, Brettin T, Rokhsar D, Berka R, Cullen D (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci USA 106:1954–1959

    Article  CAS  PubMed  Google Scholar 

  147. Courty PE, Hoegger PJ, Kilaru S, Kohler A, Buée M, Garbaye J, Martin F, Kües U (2009) Phylogenetic analysis, genomic organization, and expression analysis of multi-copper oxidases in the ectomycorrhizal basidiomycete Laccaria bicolor. New Phytol 182:736–750

    Article  CAS  PubMed  Google Scholar 

  148. Chen S, Ge W, Buswell JA (2004) Molecular cloning of a new laccase from the edible straw mushroom Volvariella volvacea: possible involvement in fruit body development. FEMS Microbiol Lett 30:171–176

    Article  CAS  Google Scholar 

  149. Tsai HF, Wheeler MH, Chang YC, Kwon-Chung KJ (1999) A developmentally regulated gene cluster involved in conidial pigment biosynthesis in Aspergillus fumigatus. J Bacteriol 181:6469–6477

    CAS  PubMed  Google Scholar 

  150. Missal TA, Moran JM, Corbett JA, Lodge JK (2005) Distinct stress responses of two functional laccases in Cryptococcus neoformans are revealed in the absence of the thiol-specific antioxidant Tsa1. Eukaryot Cell 4:202–208

    Article  CAS  Google Scholar 

  151. Iakovlev A, Stenlid J (2000) Spatiotemporal patterns of laccase activity in interacting mycelia of wood-decaying basidiomycete fungi. Microb Ecol 39:236–245

    CAS  PubMed  Google Scholar 

  152. Luis P, Kellner H, Zimdars B, Langer U, Martin F, Buscot F (2005) Patchiness and spatial distribution of laccase genes of ectomycorrhizal, saprotrophic, and unknown basidiomycetes in the upper horizons of a mixed forest cambisol. Microb Ecol 50:570–579

    Article  CAS  PubMed  Google Scholar 

  153. Terrón MC, González T, Carbajo JM, Yagüe S, Arana-Cuenca A, Téllez A, Dobson AD, González AE (2004) Structural close-related aromatic compounds have different effects on laccase activity and on lcc gene expression in the ligninolytic fungus Trametes sp. I-62. Fungal Genet Biol 41:954–962

    Article  PubMed  CAS  Google Scholar 

  154. Solé M, Kellner H, Brock S, Buscot F, Schlosser D (2008) Extracellular laccase activity and transcript levels of putative laccase genes during removal of the xenoestrogen technical nonylphenol by the aquatic hyphomycete Clavariopsis aquatica. FEMS Microbiol Lett 288:47–54

    Article  PubMed  CAS  Google Scholar 

  155. Galhaup C, Goller S, Peterbauer CK, Strauss J, Haltrich D (2002) Characterization of the major laccase isoenzyme from Trametes pubescens and regulation of its synthesis by metal ions. Microbiology 148:2159–2169

    CAS  PubMed  Google Scholar 

  156. Collins PJ, Dobson A (1997) Regulation of laccase gene transcription in Trametes versicolor. Appl Environ Microbiol 63:3444–3450

    CAS  PubMed  Google Scholar 

  157. Karahanian E, Corsini G, Lobos S, Vicuña R (1998) Structure and expression of a laccase gene from the ligninolytic basidiomycete Ceriporiopsis subvermispora. Biochim Biophys Acta 26:65–74

    Google Scholar 

  158. Palmieri G, Giardina P, Bianco C, Fontanella B, Sannia G (2000) Copper induction of laccase isoenzymes in the ligninolytic fungus Pleurotus ostreatus. Appl Environ Microbiol 66:920–924

    Article  CAS  PubMed  Google Scholar 

  159. Baldrian P, Gabriel J (2002) Copper and cadmium increase laccase activity in Pleurotus ostreatus. FEMS Microbiol Lett 206:69–74

    Article  CAS  PubMed  Google Scholar 

  160. Manubens A, Canessa P, Folch C, Avila M, Salas L, Vicuña R (2007) Manganese affects the production of laccase in the basidiomycete Ceriporiopsis subvermispora. FEMS Microbiol Lett 275:139–145

    Article  PubMed  CAS  Google Scholar 

  161. Faraco V, Giardina P, Sannia G (2003) Metal-responsive elements in Pleurotus ostreatus laccase gene promoters. Microbiology 149:2155–2162

    Article  CAS  PubMed  Google Scholar 

  162. Buchman C, Scroch P, Welch J, Fogel S, Karin M (1989) The CUP2 gene product, regulator of yeast metallothionein expression, is a copper-activated DNA-binding protein. Mol Cell Biol 9:4091–4095

    CAS  PubMed  Google Scholar 

  163. Alvarez JM, Canessa P, Mancilla RA, Polanco R, Santibáñez PA, Vicuña R (2009) Expression of genes encoding laccase and manganese-dependent peroxidase in the fungus Ceriporiopsis subvermispora is mediated by an ACE1-like copper-fist transcription factor. Fungal Genet Biol 46:104–111

    Article  CAS  PubMed  Google Scholar 

  164. Giatti Marques De Souza C, Tychanowicz GK, Farani De Souza D, Peralta RM (2004) Production of laccase isoforms by Pleurotus pulmonarius in response to presence of phenolic and aromatic compounds. J Basic Microbiol 44:129–136

    Article  CAS  Google Scholar 

  165. Vanhulle S, Enaud E, Trovaslet M, Nouaimeh N, Bols CM, Keshavarz T, Tron T, Sannia G, Corbisier AM (2007) Overlap of laccases/cellobiose dehydrogenase activities during the decolourisation of anthraquinonic dyes with close chemical structures by Pycnoporus strains. Enzyme Microb Technol 40:1723–1731

    Article  CAS  Google Scholar 

  166. Eggert C, Temp U, Eriksson KE (1996) The ligninolytic system of the white rot fungus Pycnoporus cinnabarinus: purification and characterization of the laccase. Appl Environ Microbiol 62:1151–1158

    CAS  PubMed  Google Scholar 

  167. Mansur M, Suárez T, González AE (1998) Differential gene expression in the laccase gene family from basidiomycete I-62 (CECT 20197). Appl Environ Microbiol 64:771–774

    CAS  PubMed  Google Scholar 

  168. Colao MC, Garzillo AM, Buonocore V, Schiesser A, Ruzzi M (2003) Primary structure and transcription analysis of a laccase-encoding gene from the basidiomycete Trametes trogii. Appl Microbiol Biotechnol 63:153–158

    Article  CAS  PubMed  Google Scholar 

  169. Strauss J, Horvath HK, Abdallah BM, Kindermann J, Mach RL, Kubicek CP (1999) The function of CreA, the carbon catabolite repressor of Aspergillus nidulans, is regulated at the transcriptional and post-transcriptional level. Mol Microbiol 32:169–178

    Article  CAS  PubMed  Google Scholar 

  170. Ohga S, Smith M, Thurston CF, Wood DA (1999) Transcriptional regulation of laccase and cellulase genes in the mycelium of Agaricus bisporus during fruit body development on a solid substrate. Mycol Res 103:1557–1560

    Article  CAS  Google Scholar 

  171. Ohga S, Royse DJ (2001) Transcriptional regulation of laccase and cellulose genes during growth and fruiting of Lentinula edodes on supplemented sawdust. FEMS Microbiol Lett 201:111–115

    Article  CAS  PubMed  Google Scholar 

  172. Zhang S, Hacham M, Panepinto J, Hu G, Shin S, Zhu X, Williamson PR (2006) The Hsp70 member, Ssa1, acts as a DNA-binding transcriptional co-activator of laccase in Cryptococcus neoformans. Mol Microbiol 62:1090–1101

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work is supported by grants from the Ministero dell’Università e della Ricerca Scientifica (Progetti di Rilevante Interesse Nazionale, PRIN) and from COST Action FP0602 “Biotechnology for lignocellulose biorefineries” (BIOBIO).

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  1. Dipartimento di Chimica Organica e Biochimica, Complesso Universitario Monte S. Angelo, via Cintia 4, 80126, Naples, Italy

    Paola Giardina, Vincenza Faraco, Cinzia Pezzella, Alessandra Piscitelli & Giovanni Sannia

  2. Microbiology Unit, Université catholique de Louvain, Croix du Sud 3/6, 1348, Louvain-la-Neuve, Belgium

    Sophie Vanhulle

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  1. Paola Giardina
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  2. Vincenza Faraco
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Correspondence to Paola Giardina.

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Dedicated to the memory of our missed friend and colleague Sophie Vanhulle who died suddenly and tragically.

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Giardina, P., Faraco, V., Pezzella, C. et al. Laccases: a never-ending story. Cell. Mol. Life Sci. 67, 369–385 (2010). https://doi.org/10.1007/s00018-009-0169-1

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