Degradation of aflatoxins by means of laccases from trametes versicolor: An in silico insight

Toxins

Volumn 9, Issue 1, 2017, Pages

  Dellafiora, Luca ^a   Galaverna, Gianni ^a   Reverberi, Massimo ^b   Dall’Asta, Chiara ^a  

^a UNIVERSITY OF PARMA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Aflatoxins; Biotransformation; Enzymatic detoxification; Food safety; Laccase; Mild technologies; Mycotoxins mitigation

Indexed keywords

2,2' AZINOBIS(3 ETHYLBENZOTHIAZOLINE 6 SULFONIC ACID); AFLATOXIN; AFLATOXIN B1; AFLATOXIN M1; LACCASE; SYRINGOL; FUNGAL PROTEIN; ISOENZYME;

ARTICLE; BINDING SITE; BIOTRANSFORMATION; CHEMICAL STRUCTURE; COMPUTER MODEL; CONTROLLED STUDY; DETOXIFICATION; ENZYMATIC DEGRADATION; ENZYME ACTIVITY; FOOD SAFETY; MOLECULAR DOCKING; MOLECULAR MODEL; NONHUMAN; PROTEIN ENGINEERING; SEQUENCE ANALYSIS; TRAMETES VERSICOLOR; CHEMISTRY; DRUG INACTIVATION; ENZYME SPECIFICITY; ENZYMOLOGY; METABOLISM; PROTEIN CONFORMATION; STRUCTURE ACTIVITY RELATION; TRAMETES;

AFLATOXIN B1; AFLATOXIN M1; FUNGAL PROTEINS; INACTIVATION, METABOLIC; ISOENZYMES; LACCASE; MOLECULAR DOCKING SIMULATION; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; TRAMETES;

EID: 85008425525     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins9010017     Document Type: Article

References (51)

1. Berthiller, F.; Crews, C.; Dall’Asta, C.; Saeger, S.D.; Haesaert, G.; Karlovsky, P.; Oswald, I.P.; Seefelder, W.; Speijers, G.; Stroka, J. Masked mycotoxins: A review. Mol. Nutr. Food Res. 2013, 57, 165-168.
2. Dellafiora, L.; Perotti, A.; Galaverna, G.; Buschini, A.M.; Dall’Asta, C. On the masked mycotoxin zearalenone-14-glucoside. Does the mask truly hide? Toxicon 2016, 111, 139-142.
3. Wu, F.; Guclu, H. Aflatoxin regulations in a network of global maize trade. PLoS ONE 2012, 7, e45151.
4. Jard, G.; Liboz, T.; Mathieu, F.; Guyonvarc’h, A.; Lebrihi, A. Review of mycotoxin reduction in food and feed: From prevention in the field to detoxification by adsorption or transformation. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess. 2011, 28, 1590-1609.
5. Karlovsky, P. Detoxification strategies for mycotoxins in plant breeding. In Masked Mycotoxins in Food: Formation, Occurrence and Toxicological Relevance; Dall’Asta, C., Berthiller, F., Eds.; Royal Society of Chemistry: London, UK, 2016.
6. Dellafiora, L.; Paolella, S.; Dall’Asta, C.; Dossena, A.; Cozzini, P.; Galaverna, G. Hybrid in silico/in vitro approach for the identification of angiotensin I converting enzyme inhibitory peptides from Parma dry-cured ham. J. Agric. Food Chem. 2015, 22, 6366-6375.
7. Kalyanaraman, C.; Jacobson, M.P. Studying enzyme-substrate specificity in silico: A case study of the Escherichia coli glycolysis pathway. Biochemistry 2010, 49, 4003-4005.
8. Wu, F.; Groopman, J.D.; Pestka, J.J. Public health impacts of foodbornemycotoxins. Annu. Rev. Food Sci. Technol. 2014, 5, 351-372.
9. European Food Safety Authority (EFSA). Opinion of the scientific panel on contaminants in the food chain [contam] related to the potential increase of consumer health risk by a possible increase of the existing maximum levels for aflatoxins in almonds, hazelnuts and pistachios and derived products. EFSA J. 2007, 446.
10. Raiola, A.; Tenore, G.C.; Manyes, L.; Meca, G.; Ritieni, A. Risk analysis of main mycotoxins occurring in food for children: An overview. Food Chem. Toxicol. 2015, 84, 169-180.
11. Prandini, A.; Tansini, G.; Sigolo, S.; Filippi, L.; Laporta, M.; Piva, G. On the occurrence of aflatoxin M1 in milk and dairy products. Food Chem. Toxicol. 2009, 47, 984-991.
12. Perrone, G.; Gallo, A.; Logrieco, A.F. Biodiversity of Aspergillus section Flavi in Europe in relation to the management of aflatoxin risk. Front. Microbiol. 2014, 5, 377.
13. Mate, D.M.; Alcalde, M. Laccase: A multi-purpose biocatalyst at the forefront of biotechnology. Microb. Biotechnol. 2016.
14. Scarpari, M.; Bello, C.; Pietricola, C.; Zaccaria, M.; Bertocchi, L.; Angelucci, A.; Ricciardi, M.R.; Scala, V.; Parroni, A.; Fabbri, A.A. et al. Aflatoxin control in maize by Trametes versicolor. Toxins (Basel) 2014, 6, 3426-3437.
15. Zeinvand-Lorestani, H.; Sabzevari, O.; Setayesh, N.; Amini, M.; Nili-Ahmadabadi, A.; Faramarzi, M.A. Comparative study of in vitro prooxidative properties and genotoxicity induced by aflatoxin B1 and its laccase-mediated detoxification products. Chemosphere 2015, 135, 1-6.
16. Bertrand, T.; Jolivalt, C.; Briozzo, P.; Caminade, E.; Joly, N.; Madzak, C.; Mouqin, C. Crystal structure of a four-copper laccase complexed with an arylamine: Insights into substrate recognition and correlation with kinetics. Biochemistry 2002, 41, 7325-7333.
17. Dellafiora, L.; Mena, P.; Cozzini, P.; Brighenti, F.; Del Rio, D. Modelling the possible bioactivity of ellagitannin-derived metabolites. In silico tools to evaluate their potential xenoestrogenic behavior. Food Funct. 2013, 4, 1442-1451.
18. Dellafiora, L.; Mena, P.; Del Rio, D.; Cozzini, P. Modeling the effect of phase II conjugations on topoisomerase I poisoning: Pilot study with luteolin and quercetin. J. Agric. Food Chem. 2014, 62, 5881-5886.
19. Dellafiora, L.; Dall’Asta, C.; Cozzini, P. Ergot alkaloids: From witchcraft till in silico analysis. Multi-receptor analysis of ergotamine metabolites. Toxicol. Rep. 2015, 2, 535-545.
20. Madzak, C.; Mimmi, M.C.; Caminade, E.; Brault, A.; Baumberger, S.; Briozzo, P.; Mougin, C.; Jolivalt, C. Shifting the optimal pH of activity for a laccase from the fungus Trametes versicolor by structure-based mutagenesis. Protein Eng. Des. Sel. 2006, 19, 77-84.
21. Cozzini, P.; Dellafiora, L. In silico approach to evaluate molecular interaction between mycotoxins and the estrogen receptors ligand binding domain: A case study on zearalenone and its metabolites. Toxicol. Lett. 2012, 214, 81-85.
22. Cozzini, P.; Fornabaio, M.; Marabotti, A.; Abraham, D.J.; Kellogg, G.E.; Mozzarelli, A. Simple, intuitive calculations of free energy of binding for protein-ligand complexes. 1. Modelswithout explicit constrainedwater. J.Med. Chem. 2002, 45, 2469-2483.
23. Dellafiora, L.; Dall’Asta, C.; Cruciani, G.; Galaverna, G.; Cozzini, P. Molecular modelling approach to evaluate poisoning of topoisomerase I by alternariol derivatives. Food Chem. 2015, 189, 93-101.
24. Fornabaio, M.; Cozzini, P.; Mozzarelli, A.; Abraham, D.J.; Kellogg, G.E. Simple, intuitive calculations of free energy of binding for protein-ligand complexes. 2. Computational titration and pH effects in molecular models of neuraminidase-inhibitor complexes. J. Med. Chem. 2003, 46, 4487-4500.
25. Fornabaio, M.; Spirakis, F.; Mozzarelli, A.; Cozzini, P.; Abraham, D.J.; Kellogg, G.E. Simple, intuitive calculations of free energy of binding for protein-ligand complexes. 3. The free energy contribution of structural water molecules in HIV-1 protease complexes. J. Med. Chem. 2004, 47, 4507-4516.
26. Christensen, N.J.; Kepp, K.P. 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. 2014, 100, 68-77.
27. Galli, C.; Madzak, C.; Vadalà, R.; Jolivalt, C.; Gentili, P. Concerted electron/proton transfer mechanism in the oxidation of phenols by laccase. ChemBioChem 2013, 14, 2500-2505.
28. Lee, D.; Redfern, O.; Orengo, C. Predicting protein function from sequence and structure. Nat. Rev. Mol. Cell Biol. 2007, 8, 995-1005.
29. Enguita, F.J.; Marçal, D.; Martins, L.O.; Grenha, R.; Henriques, A.O.; Lindley, P.F.; Carrondo, M.A. Substrate and dioxygen binding to the endospore coat laccase from Bacillus subtilis. J. Biol. Chem. 2004, 279, 23472-23476.
30. Hahn, I.; Thamhesl, M.; Apfelthaler, E.; Klingenbrunner, V.; Hametner, C.; Krska, R.; Schatzmayr, G.; Moll, W-D.; Berthiller, F.; Schwartz-Zimmermann, H.E. Characterisation and determination of metabolites formed by microbial and enzymatic degradation of ergot alkaloids. World Mycotoxins J. 2015, 8, 393-404.
31. Igawa, T.; Takahashi-Ando, N.; Ochiai, N.; Ohsato, S.; Shimizu, T.; Kudo, T.; Yamaguchi, I.; Kimura, M. Reduced contamination by the Fusarium mycotoxin zearalenone in maize kernels through genetic modification with a detoxification gene. Appl. Environ. Microbiol. 2007, 73, 1622-1629.
32. Munkvold, G.P. Cultural and genetic approaches to managing mycotoxins in maize. Annu. Rev. Phytopathol. 2003, 44, 99-116.
33. Gerike, U.; Danson, M.J.; Hough, D.W. Cold-active citrate synthase: Mutagenesis of active-site residues. Protein Eng. 2001, 14, 655-661.
34. Leferink, N.G.; Antonyuk, S.V.; Houwman, J.A.; Scrutton, N.S.; Eady, R.R.; Hasnain, S.S. Impact of residues remote from the catalytic centre on enzyme catalysis of copper nitrite reductase. Nat. Commun. 2014, 5, 4395.
35. Bleve, G.; Lezzi, C.; Spagnolo, S.; Tasco, G.; Tufariello, M.; Casadio, R.; Mita, G.; Rampino, P.; Grieco, F. Role of the C-terminus of Pleurotus eryngii Ery4 laccase in determining enzyme structure, catalytic properties and stability. Protein Eng. Des. Sel. 2013, 26, 1-13.
36. Andberg, M.; Hakulinen, N.; Auer, S.; Saloheimo, M.; Koivula, A.; Rouvinen, J.; Kruus, K. Essential role of the C-terminus in Melanocarpus albomyces laccase for enzyme production, catalytic properties and structure. FEBS J. 2009, 276, 6285-6300.
37. Reiss, R.; Ihssen, J.; Richter, M.; Eichhorn, E.; Schilling, B.; Thöny-Meyer, L. Laccase versus laccase-like multi-copper oxidase: A comparative study of similar enzymes with diverse substrate spectra. PLoS ONE 2013, 8, e65633.
38. Loi, M.; Fanelli, F.; Zucca, P.; Liuzzi, V.C.; Quintieri, L.; Cimmarusti, M.T.; Monaci, L.; Haidukowski, M.; Logrieco, A.F.; Sanjust, E. et al. Aflatoxin B1 and M1 degradation by lac2 from Pleurotus pulmonarius and redox mediators. Toxins (Basel) 2016, 8, E245.
39. Cambria, M.T.; Di Marino, D.; Falconi, M.; Garavaglia, S.; Cambria, A. Docking simulation and competitive experiments validate the interaction between the 2,5-xylidine inhibitor and Rigidoporus lignosus laccase. J. Biomol. Struct. Dyn. 2010, 27, 501-510.
40. Suresh, P.S.; Kumar, A.; Kumar, R.; Singh, V.P. An in silico [correction of insilico] approach to bioremediation: Laccase as a case study. J. Mol. Graph. Model. 2008, 26, 845-849.
41. Sali, A.; Blundell, T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 1993, 234, 779-815.
42. Baroni, M.; Cruciani, G.; Sciabola, S.; Perruccio, F.; Mason, J.S. A common reference framework for analyzing/comparing proteins and ligands. Fingerprints for ligands and proteins (FLAP): Theory and application. J. Chem. Inf. Model. 2007, 47, 279-294.
43. Goodford, P.J. A computational procedure for determining energetically favourable binding sites on biologically important macromolecules. J. Med. Chem. 1985, 28, 849-857.
44. Carosati, E.; Sciabola, S.; Cruciani, G. Hydrogen bonding interactions of covalently bonded fluorine atoms: From crystallographic data to a new angular function in the GRID force field. J. Med. Chem. 2004, 47, 5114-5125.
45. Kellogg, E.G.; Abraham, D.J. Hydrophobicity: Is LogPo/w more than the sum of its parts? Eur. J. Med. Chem. 2000, 37, 651-661.
46. Dellafiora, L.; Galaverna, G.; Dall’Asta, C.; Cozzini, P. Hazard identification of cis/trans-zearalenone through the looking-glass. Food Chem. Toxicol. 2015, 86, 65-71.
47. Ehrlich, V.A.; Dellafiora, L.; Mollergues, J.; Dall’Asta, C.; Serrant, P.; Marin-Kuan, M.; Lo Piparo, E.; Schilter, B.; Cozzini, P. Hazard assessment through hybrid in vitro/in silico approach: The case of zearalenone. ALTEX 2015, 32, 275-286.
48. Marabotti, A.; Spyrakis, F.; Facchiano, A.; Cozzini, P.; Alberti, S.; Kellogg, G.E.; Mozzarelli, A. Energy-based prediction of amino acid-nucleotide base recognition. J. Comput. Chem. 2008, 29, 1955-1969.
49. Kellogg, G.E.; Burnett, J.C.; Abraham, D.J. Very empirical treatment of solvation and entropy: A force field derived from LogPo/w. J. Comput. Aided Mol. Des. 2001, 15, 381-393.
50. Kellogg, G.E.; Fornabaio, M.; Spyrakis, F.; Lodola, A.; Cozzini, P.; Mozzarelli, A.; Abraham, D.J. Getting it right: Modeling of pH, solvent and “Nearly” Everything else in virtual screening of biological targets. J. Mol. Graph. Model. 2004, 22, 479-486.
51. Sarkar, A.; Kellogg, G.E. Hydrophobicity-shake flasks, protein folding and drug discovery. Curr. Top. Med. Chem. 2010, 10, 67-83.