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Protein & Peptide Letters

Author(s): Binbin Li, Yuan Wang, Linlin Xue and Shiling Lu*

DOI: 10.2174/0929866527666200616160859

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Heterologous Expression and Application of Multicopper Oxidases from Enterococcus spp. for Degradation of Biogenic Amines

Page: [183 - 194] Pages: 12

  • * (Excluding Mailing and Handling)

Abstract

Background: Biogenic amines are harmful to human health at a certain extent. As a kind of biogenic amine oxidase, multicopper oxidase can be used to degrade them. Currently, the literature about enzyme from Enterococcus spp. are limited, and recombinant multicopper oxidase might be an effective way to degrade biogenic amines.

Objective: (i) Select and identify strains that can degrade biogenic amines, (ii) overexpress enzyme from Enterococcus spp., (iii) measure gene expression and probe amine-degradation differences among strains (native, E. coli DH5α, and L. delbruckii), and (iv) examine the biochemical properties of recombinant multicopper oxidase, (v) apply the recombinant enzyme into smoked horsemeat sausage.

Methods: Reverse transcription PCR and high-performance liquid chromatography were performed to examine gene expression and amine degradation rate.

Results: The results demonstrated that target enzymes were successfully overexpressed, accompanied by increased amine-degrading activity (P <0.05). Gene from E. faecalis M5B was expressed in L. delbrueckii resulted in degradation rates for phenylethylamine, putrescine, histamine and tyramine of 54%, 52%, 70% and 40%, respectively, significantly higher than achieved by other recombinant strains.

Conclusion: In this work, gene expression levels were higher in recombinant M5B than recombinant M2B, regardless of host. E. coli is more stable to express multicopper oxidase. Besides, the amine-degrading ability was markedly increased in the two recombinant strains. After prolonged incubation, the recombinant enzyme could degrade three amines, and it displayed high alkali resistance and thermostability.

Keywords: Biogenic amine, recombinant enzyme, Enterococcus spp., multicopper oxidase, amine degradation, recombinant strains.

Graphical Abstract

[1]
Gobbetti, M.; De Angelis, M.; Di Cagno, R.; Mancini, L.; Fox, P.F. Pros and cons for using non-starter lactic acid bacteria (NSLAB) as secondary/adjunct starters for cheese ripening. Trends Food Sci. Technol., 2015, 45(2), 167-178.
[http://dx.doi.org/10.1016/j.tifs.2015.07.016]
[2]
Harada, R.; Yuzuki, M.; Ito, K.; Shiga, K.; Bamba, T.; Fukusaki, E. Influence of yeast and lactic acid bacterium on the constituent profile of soy sauce during fermentation. J. Biosci. Bioeng., 2017, 123(2), 203-208.
[http://dx.doi.org/10.1016/j.jbiosc.2016.08.010] [PMID: 27939139]
[3]
Bezerra, T.K.A.; de Oliveira Arcanjo, N.M.; Garcia, E.F.; Gomes, A.M.P.; de Cássia Ramos do Egypto Queiroga, R.; de Souza, E.L.; Madruga, M.S. Effect of supplementation with probiotic lactic acid bacteria, separately or combined, on acid and sugar production in goat ‘coalho’ cheese. Lebensm. Wiss. Technol., 2017, 75, 710-718.
[http://dx.doi.org/10.1016/j.lwt.2016.10.023]
[4]
du Toit, M.; Engelbrecht, L.; Lerm, E.; Krieger-Weber, S. Lactobacillus: the next generation of malolactic fermentation starter cultures—an overview. Food Bioprocess Technol., 2010, 4(6), 876-906.
[http://dx.doi.org/10.1007/s11947-010-0448-8]
[5]
Willems, R.J.L.; Top, J.; van Santen, M.; Robinson, A.D., Coque, T.M.; Baquero, F.; Grundmann, H.; Bonten, M.J.M. Global Spread of Vancomycin resistant Enterococcus faecium from Distinct Nosocomial Genetic Complex. Emerg. Infect. Dis., 2005, 11, 821-828.
[http://dx.doi.org/10.3201/1106.041204]
[6]
Gardiner, G.E.; Ross, R.P.; Wallace, J.M.; Scanlan, F.P.; Jägers, P.P.J.M.; Fitzgerald, G.F.; Collins, J.K.; Stanton, C. Influence of a probiotic adjunct culture of Enterococcus faecium on the quality of cheddar cheese. J. Agric. Food Chem., 1999, 47(12), 4907-4916.
[http://dx.doi.org/10.1021/jf990277m] [PMID: 10606551]
[7]
Hugas, M.; Garriga, M.; Aymerich, M.T. Functionality of enterococci in meat products. Int. J. Food Microbiol., 2003, 88(2-3), 223-233.
[http://dx.doi.org/10.1016/S0168-1605(03)00184-3] [PMID: 14596994]
[8]
Fernández, M.; Linares, D.M.; Rodríguez, A.; Alvarez, M.A. Factors affecting tyramine production in Enterococcus durans IPLA 655. Appl. Microbiol. Biotechnol., 2007, 73(6), 1400-1406.
[http://dx.doi.org/10.1007/s00253-006-0596-y] [PMID: 17043827]
[9]
Henríquez-Aedo, K.; Duran, D.; Garcia, A.; Hengst, M.B.; Aranda, M. Identification of biogenic amines-producing lactic acid bacteria isolated from spontaneous malolactic fermentation of chilean red wines. LWT: Food Sci. Technol., 2016, 68, 183-189.
[http://dx.doi.org/10.1016/j.lwt.2015.12.003]
[10]
Pereira, C.I.; Matos, D.; San Romão, M.V.; Crespo, M.T. Dual role for the tyrosine decarboxylation pathway in Enterococcus faecium E17: response to an acid challenge and generation of a proton motive force. Appl. Environ. Microbiol., 2009, 75(2), 345-352.
[http://dx.doi.org/10.1128/AEM.01958-08] [PMID: 19011061]
[11]
Ayala, D.I.; Cook, P.W.; Campos, D.L.; Franco, J.G.; Brashears, M.M.; den Bakker, H.; Nightingale, K.K. Draft Genome Sequence of Enterococcus faecium Strain J19, Isolated from Cabbage. Genome Announc., 2018, 6(14), e00213-e00218.
[http://dx.doi.org/10.1128/genomeA.00213-18] [PMID: 29622613]
[12]
Cho, S.Y.; Park, Y.J.; Cho, H.; Park, D.J.; Yu, J.K.; Oak, H.C.; Lee, D.G. Comparison of Enterococcus faecium Bacteremic Isolates from Hematologic and Non-hematologic Patients: Differences in Antimicrobial Resistance and Molecular Characteristics. Ann. Lab. Med., 2018, 38(3), 226-234.
[http://dx.doi.org/10.3343/alm.2018.38.3.226] [PMID: 29401557]
[13]
Jahansepas, A.; Ahangarzadeh Rezaee, M.; Hasani, A.; Sharifi, Y.; Rahnamaye Farzami, M.; Dolatyar, A.; Aghazadeh, M. Molecular epidemiology of vancomycin-resistant Enterococcus faecalis and Enterococcus faecium isolated from clinical specimens in the northwest of Iran. Microb. Drug Resist., 2018, 24(8), 1165-1173.
[http://dx.doi.org/10.1089/mdr.2017.0380] [PMID: 29708837]
[14]
Lu, S.; Xu, X.; Zhou, G.; Zhu, Z.; Meng, Y.; Sun, Y. Effect of starter cultures on microbial ecosystem and biogenic amines in fermented sausage. Food Control, 2010, 21(4), 444-449.
[http://dx.doi.org/10.1016/j.foodcont.2009.07.008]
[15]
Spano, G.; Russo, P.; Lonvaud-Funel, A.; Lucas, P.; Alexandre, H.; Grandvalet, C.; Coton, E.; Coton, M.; Barnavon, L.; Bach, B.; Rattray, F.; Bunte, A.; Magni, C.; Ladero, V.; Alvarez, M.; Fernández, M.; Lopez, P.; de Palencia, P.F.; Corbi, A.; Trip, H.; Lolkema, J.S. Biogenic amines in fermented foods. Eur. J. Clin. Nutr., 2010, 64(Suppl. 3), S95-S100.
[http://dx.doi.org/10.1038/ejcn.2010.218] [PMID: 21045859]
[16]
Taylor, S.L.; Eitenmiller, R.R. Histamine food poisoning: toxicology and clinical aspects. Crit. Rev. Toxicol., 1986, 17(2), 91-128.
[http://dx.doi.org/10.3109/10408448609023767] [PMID: 3530640]
[17]
Kalač, P. Kalacˇ. Health effects and occurrence of dietary polyamines: a review for the period 2005-mid 2013. Food Chem., 2014, 161, 27-39.
[http://dx.doi.org/10.1016/j.foodchem.2014.03.102] [PMID: 24837918]
[18]
Zhang, H.; Chen, Y.; Yin, D. DENG, Y.; Ma, Y.; Ju, L., Discussion on risk factors of Kazakh esophageal cancer in Xinjiang. Mod. Prev. Med., 2009, 36(10), 1804-1806.
[19]
Gezginc, Y.; Akyol, I.; Kuley, E.; Özogul, F. Biogenic amines formation in Streptococcus thermophilus isolated from home-made natural yogurt. Food Chem., 2013, 138(1), 655-662.
[http://dx.doi.org/10.1016/j.foodchem.2012.10.138] [PMID: 23265537]
[20]
Nie, X.; Zhang, Q.; Lin, S. Biogenic amine accumulation in silver carp sausage inoculated with Lactobacillus plantarum plus Saccharomyces cerevisiae. Food Chem., 2014, 153(9), 432-436.
[http://dx.doi.org/10.1016/j.foodchem.2013.12.093] [PMID: 24491750]
[21]
Nei, D. Evaluation of Non-bacterial factors contributing to histamine accumulation in fish fillets. Food Control, 2014, 35(1), 142-145.
[http://dx.doi.org/10.1016/j.foodcont.2013.06.037]
[22]
Alan, Y.; Topalcengiz, Z.; Diğrak, M. Production of biogenic amines and fermentation metabolites by Lactobacillus plantarum isolated from naturally fermented pickles. The 3rd International Symposium on EuroAsian Biodiversity Minsk - Belarus , 2017.
[23]
Bartkiene, E.B.V.; Mozuriene, E.; Krungleviciute, V.; Novoslavskij, A.; Santini, A.; Rozentale, I.; Juodeikiene, G.; Cizeikiene, D. The impact of lactic acid bacteria with antimicrobial properties on biodegradation of polycyclic aromatic hydrocarbons and biogenic amines in cold smoked pork sausages. Food Control, 2017, 2017(71), 285-292.
[http://dx.doi.org/10.1016/j.foodcont.2016.07.010]
[24]
Capozzi, V.; Russo, P.; Ladero, V.; Fernández, M.; Fiocco, D.; Alvarez, M.A.; Grieco, F.; Spano, G. Biogenic amines degradation by Lactobacillus plantarum: toward a potential application in wine. Front. Microbiol., 2012, 3, 122.
[http://dx.doi.org/10.3389/fmicb.2012.00122] [PMID: 22485114]
[25]
Yagodina, O.V.; Nikol’skaya, E.B.; Khovanskikh, A.E.; Kormilitsyn, B.N. Amine oxidases of microorganisms. J. Evol. Biochem. Physiol., 2002, 38(3), 251-258.
[http://dx.doi.org/10.1023/A:1020714607203]
[26]
Schilling, B.; Lerch, K. Amine oxidases from Aspergillus niger: identification of a novel flavin-dependent enzyme. Biochim. Biophys. Acta, 1995, 1243(3), 529-537.
[http://dx.doi.org/10.1016/0304-4165(94)00183-X] [PMID: 7727530]
[27]
Ihssen, J.; Reiss, R.; Luchsinger, R.; Thöny-Meyer, L.; Richter, M. Biochemical properties and yields of diverse bacterial laccase-like multicopper oxidases expressed in Escherichia coli. Sci. Rep., 2015, 5(1), 10465.
[http://dx.doi.org/10.1038/srep10465] [PMID: 26068013]
[28]
Guarcello, R.; De Angelis, M.; Settanni, L.; Formiglio, S.; Gaglio, R.; Minervini, F.; Moschetti, G.; Gobbetti, M.; Björkroth, J. Selection of amine-oxidizing dairy lactic acid bacteria and identification of the enzyme and gene involved in the decrease of biogenic amines. Appl. Environ. Microbiol., 2016, 82(23), 6870-6880.
[http://dx.doi.org/10.1128/AEM.01051-16] [PMID: 27637883]
[29]
Callejón, S.; Sendra, R.; Ferrer, S.; Pardo, I. Identification of a novel enzymatic activity from lactic acid bacteria able to degrade biogenic amines in wine. Appl. Microbiol. Biotechnol., 2014, 98(1), 185-198.
[http://dx.doi.org/10.1007/s00253-013-4829-6] [PMID: 23515835]
[30]
Ye, Y-X.; Pan, P-L.; Kang, D.; Lu, J-B.; Zhang, C-X. The multicopper oxidase gene family in the brown planthopper, Nilaparvata lugens. Insect Biochem. Mol. Biol., 2015, 63, 124-132.
[http://dx.doi.org/10.1016/j.ibmb.2015.06.010] [PMID: 26107750]
[31]
Ausec, L.; Črnigoj, M.; Šnajder, M.; Ulrih, N.P.; Mandic-Mulec, I. Characterization of a novel high-pH-tolerant laccase-like multicopper oxidase and its sequence diversity in Thioalkalivibrio sp. Appl. Microbiol. Biotechnol., 2015, 99(23), 9987-9999.
[http://dx.doi.org/10.1007/s00253-015-6843-3] [PMID: 26227413]
[32]
Solano, F.; Lucas-Elío, P.; López-Serrano, D.; Fernández, E.; Sanchez-Amat, A. Dimethoxyphenol oxidase activity of different microbial blue multicopper proteins. FEMS Microbiol. Lett., 2001, 204(1), 175-181.
[http://dx.doi.org/10.1111/j.1574-6968.2001.tb10882.x] [PMID: 11682198]
[33]
Li, Y.; Zuo, W.; Li, Y.; Wang, X. Cloning of multicopper oxidase gene from Ochrobactrum sp. 531 and characterization of its alkaline laccase activity towards phenolic substrates. Adv. Biol. Chem., 2012, 02(03), 248-255.
[http://dx.doi.org/10.4236/abc.2012.23031]
[34]
Lee, J.I.; Kim, Y.W. Characterization of amine oxidases from Arthrobacter aurescens and application for determination of biogenic amines. World J. Microbiol. Biotechnol., 2013, 29(4), 673-682.
[http://dx.doi.org/10.1007/s11274-012-1223-y] [PMID: 23225177]
[35]
Sugawara, A.; Matsui, D.; Komeda, H.; Asano, Y.; Isobe, K. Characterization and application of aminoamide-oxidizing enzyme from Aspergillus carbonarius AIU 205. J. Biosci. Bioeng., 2014, 117(3), 263-268.
[http://dx.doi.org/10.1016/j.jbiosc.2013.08.019] [PMID: 24113361]
[36]
Boonen, F.; Vandamme, A.M.; Etoundi, E.; Pigneur, L.M.; Housen, I. Identification and characterization of a novel multicopper oxidase from Acidomyces acidophilus with ferroxidase activity. Biochimie, 2014, 102, 37-46.
[http://dx.doi.org/10.1016/j.biochi.2014.02.009] [PMID: 24582726]
[37]
Zhao, L.; Xue, L.; Li, B.; Wang, Q.; Li, B.; Lu, S.; Fan, Q. Ferulic acid reduced histamine levels in the smoked horsemeat sausage. Int. J. Food Sci. Technol., 2018, 53, 2256-2264.
[http://dx.doi.org/10.1111/ijfs.13814]
[38]
Lee, Y-C.; Kung, H-F.; Huang, C-Y.; Huang, T-C.; Tsai, Y-H. Reduction of histamine and biogenic amines during salted fish fermentation by Bacillus polymyxa as a starter culture. Yao Wu Shi Pin Fen Xi, 2016, 24(1), 157-163.
[http://dx.doi.org/10.1016/j.jfda.2015.02.002] [PMID: 28911399]
[39]
Eom, J.S.; Seo, B.Y.; Choi, H.S. Biogenic amine degradation by Bacillus species isolated from traditional fermented soybean food and detection of decarboxylase-related genes. J. Microbiol. Biotechnol., 2015, 25(9), 1519-1527.
[http://dx.doi.org/10.4014/jmb.1506.06006] [PMID: 26165318]
[40]
Kung, H-F.; Lee, Y-C.; Huang, Y-L.; Huang, Y-R.; Su, Y-C.; Tsai, Y-H. Degradation of Histamine by Lactobacillus plantarum Isolated from Miso Products. J. Food Prot., 2017, 80(10), 1682-1688.
[http://dx.doi.org/10.4315/0362-028X.JFP-17-135] [PMID: 28885051]
[41]
Deng, H.; Lu, S.; Li, K. Isolation and Identification of Biogenic Amines Oxidase-producing Strains in Traditional Chinese Sausage. Shipin Yu Fajiao Gongye, 2012, (02), 57-60.
[42]
Lu, S.; Ji, H.; Wang, Q.; Li, B.; Li, K.; Xu, C.; Jiang, C. The effects of starter cultures and plant extracts on the biogenic amine accumulation in traditional Chinese smoked horsemeat sausages Food Control 2015, 50 (ISSN), 2015, 869-875.
[http://dx.doi.org/10.1016/j.foodcont.2014.08.015]
[43]
Palomino, M.M.; Allievi, M.C.; Prado-Acosta, M.; Sanchez-Rivas, C.; Ruzal, S.M. New method for electroporation of Lactobacillus species grown in high salt. J. Microbiol. Methods, 2010, 83(2), 164-167.
[http://dx.doi.org/10.1016/j.mimet.2010.08.017] [PMID: 20807556]
[44]
Marco, M.L.; Bongers, R.S.; de Vos, W.M.; Kleerebezem, M. Spatial and temporal expression of Lactobacillus plantarum genes in the gastrointestinal tracts of mice. Appl. Environ. Microbiol., 2007, 73(1), 124-132.
[http://dx.doi.org/10.1128/AEM.01475-06] [PMID: 17071785]
[45]
Marco, M.L.; Kleerebezem, M. Assessment of real-time RT-PCR for quantification of Lactobacillus plantarum gene expression during stationary phase and nutrient starvation. J. Appl. Microbiol., 2008, 104(2), 587-594.
[http://dx.doi.org/10.1111/j.1365-2672.2007.03578.x] [PMID: 18081777]
[46]
Foster, A.; Barnes, N.; Speight, R.; Keane, M.A. Genomic organisation, activity and distribution analysis of the microbial putrescine oxidase degradation pathway. Syst. Appl. Microbiol., 2013, 36(7), 457-466.
[http://dx.doi.org/10.1016/j.syapm.2013.06.008] [PMID: 23906496]
[47]
Moshides, J.S. Enzymic determination of the free cholesterol fraction of high-density lipoprotein in plasma with use of 2,4,6-tribromo-3-hydroxybenzoic acid. Clin. Chem., 1988, 34(9), 1799-1804.
[http://dx.doi.org/10.1093/clinchem/34.9.1794] [PMID: 2843306]
[48]
Callejón, S.; Sendra, R.; Ferrer, S.; Pardo, I. Ability of Kocuria varians LTH 1540 to degrade putrescine: identification and characterization of a novel amine oxidase. J. Agric. Food Chem., 2015, 63(16), 4170-4178.
[http://dx.doi.org/10.1021/jf5026967] [PMID: 25817823]
[49]
Li, J.; Lawton, T.J.; Kostecki, J.S.; Nisthal, A.; Fang, J.; Mayo, S.L.; Rosenzweig, A.C.; Jewett, M.C. Cell-free protein synthesis enables high yielding synthesis of an active multicopper oxidase. Biotechnol. J., 2016, 11(2), 212-218.
[http://dx.doi.org/10.1002/biot.201500030] [PMID: 26356243]
[50]
Huichao, Z.; Binbin, L.; Lili, Z.; Qingling, W.; Baokun, L.; Shiling, L. The effects of amine oxidase-producing starter culture on biogenic amine accumulation in traditional Chinese smoked horsemeat sausages. J. Food Saf., 2019, 39(3)e12638
[http://dx.doi.org/10.1111/jfs.12638]
[51]
Nout, M.J.R. Fermented foods and food safety. Food Res. Int., 1994, 27(3), 291-298.
[http://dx.doi.org/10.1016/0963-9969(94)90097-3]
[52]
Summers, D. Timing, self-control and a sense of direction are the secrets of multicopy plasmid stability. Mol. Microbiol., 1998, 29(5), 1137-1145.
[http://dx.doi.org/10.1046/j.1365-2958.1998.01012.x] [PMID: 9767582]
[53]
Xiong, Z.Q.; Wang, Q.H.; Kong, L.H.; Song, X.; Wang, G.Q.; Xia, Y.J.; Zhang, H.; Sun, Y.; Ai, L.Z. Short communication: Improving the activity of bile salt hydrolases in Lactobacillus casei based on in silico molecular docking and heterologous expression. J. Dairy Sci., 2017, 100(2), 975-980.
[http://dx.doi.org/10.3168/jds.2016-11720] [PMID: 28012620]
[54]
Gasser, B.; Saloheimo, M.; Rinas, U.; Dragosits, M.; Rodríguez-Carmona, E.; Baumann, K.; Giuliani, M.; Parrilli, E.; Branduardi, P.; Lang, C.; Porro, D.; Ferrer, P.; Tutino, M.L.; Mattanovich, D.; Villaverde, A. Protein folding and conformational stress in microbial cells producing recombinant proteins: a host comparative overview. Microb. Cell Fact., 2008, 7(1), 11.
[http://dx.doi.org/10.1186/1475-2859-7-11] [PMID: 18394160]
[55]
Brémond, P.; Pasteur, N.; Combes, C.; Renaud, F.; Théron, A. Experimental host-induced selection in Schistosoma mansoni strains from Guadeloupe and comparison with natural observations. Heredity, 1993, 70(Pt 1), 33-37.
[http://dx.doi.org/10.1038/hdy.1993.5] [PMID: 8432659]
[56]
Celik, E.; Calık, P. Production of recombinant proteins by yeast cells. Biotechnol. Adv., 2012, 30(5), 1108-1118.
[http://dx.doi.org/10.1016/j.biotechadv.2011.09.011] [PMID: 21964262]
[57]
Ranka, K. C. B. B., Biochemical characterisation of two novel laccases from Magnaporthe grisea. Journal of Yeast and Fungal Research, 2011, 2(10), 153-164.
[58]
Koschorreck, K.; Richter, S.M.; Ene, A.B.; Roduner, E.; Schmid, R.D.; Urlacher, V.B. Cloning and characterization of a new laccase from Bacillus licheniformis catalyzing dimerization of phenolic acids. Appl. Microbiol. Biotechnol., 2008, 79(2), 217-224.
[http://dx.doi.org/10.1007/s00253-008-1417-2] [PMID: 18330561]
[59]
Ruijssenaars, H.J.; Hartmans, S. A cloned Bacillus halodurans multicopper oxidase exhibiting alkaline laccase activity. Appl. Microbiol. Biotechnol., 2004, 65(2), 177-182.
[http://dx.doi.org/10.1007/s00253-004-1571-0] [PMID: 15293032]
[60]
Sondhi, S.; Sharma, P.; George, N.; Chauhan, P. S.; Puri, N.; Gupta, N. An extracellular thermo-alkali-stable laccase from Bacillus tequilensis SN4, with a potential to biobleach softwood pulp 3 Biotech, 2015, 5(2), 175-185.
[61]
Durão, P.; Chen, Z.; Fernandes, A.T.; Hildebrandt, P.; Murgida, D.H.; Todorovic, S.; Pereira, M.M.; Melo, E.P.; Martins, L.O. Copper incorporation into recombinant CotA laccase from Bacillus subtilis: characterization of fully copper loaded enzymes. J. Biol. Inorg. Chem., 2008, 13(2), 183-193.
[http://dx.doi.org/10.1007/s00775-007-0312-0] [PMID: 17957391]
[62]
Lončar, N.; Božić, N.; Vujčić, Z. Expression and characterization of a thermostable organic solvent-tolerant laccase from Bacillus licheniformis ATCC 9945a. J. Mol. Catal., B Enzym., 2016, 134, 390-395.
[http://dx.doi.org/10.1016/j.molcatb.2016.06.005]
[63]
Lu, L.; Zeng, G.; Fan, C.; Ren, X.; Wang, C.; Zhao, Q.; Zhang, J.; Chen, M.; Chen, A.; Jiang, M. Characterization of a laccase-like multicopper oxidase from newly isolated Streptomyces sp. C1 in agricultural waste compost and enzymatic decolorization of azo dyes. Biochem. Eng. J., 2013, 72, 70-76.
[http://dx.doi.org/10.1016/j.bej.2013.01.004]
[64]
Messerschmidt, A.; Huber, R. The blue oxidases, ascorbate oxidase, laccase and ceruloplasmin Modelling and structural relationships. FEBS J., 2010, 187(2), 341-352.
[PMID: 21134129]
[65]
Quintanar, L.; Stoj, C.; Taylor, A.B.; Hart, P.J.; Kosman, D.J.; Solomon, E.I. Shall we dance? How a multicopper oxidase chooses its electron transfer partner. Acc. Chem. Res., 2007, 40(6), 445-452.
[http://dx.doi.org/10.1021/ar600051a] [PMID: 17425282]
[66]
Miyazaki, K. A hyperthermophilic laccase from Thermus thermophilus HB27. Extremophiles, 2005, 9(6), 415-425.
[http://dx.doi.org/10.1007/s00792-005-0458-z] [PMID: 15999224]
[67]
Galli, I.; Musci, G.; Bonaccorsi di Patti, M.C. Sequential reconstitution of copper sites in the multicopper oxidase CueO. J. Biol. Inorg. Chem., 2004, 9(1), 90-95.
[http://dx.doi.org/10.1007/s00775-003-0501-4] [PMID: 14648285]
[68]
Jaiswal, N.; Pandey, V.P.; Dwivedi, U.N. Purification of a thermostable laccase from Leucaena leucocephala using a copper alginate entrapment approach and the application of the laccase in dye decolorization. Process Biochem., 2014, 49(7), 1196-1204.
[http://dx.doi.org/10.1016/j.procbio.2014.04.002]
[69]
Vantamuri, A. B.; Kaliwal, B. B. Purification and characterization of laccase from Marasmius species BBKAV79 and effective decolorization of selected textile dyes 3 Biotech, 2016, 6(2), 189.
[70]
Alcalde, M. Biological functions, molecular structure and industrial Applications.2007, , 461-476.
[71]
Sun, Q.; Chen, Q.; Li, F.; Zheng, D.; Kong, B. Biogenic amine inhibition and quality protection of Harbin dry sausages by inoculation with Staphylococcus xylosus and Lactobacillus plantarum. Food Control, 2016, 68, 358-366.
[http://dx.doi.org/10.1016/j.foodcont.2016.04.021]
[72]
Fadda, S.; Vignolo, G.; Oliver, G. Tyramine degradation and tyramine/histamine production by lactic acid bacteria and Kocuria strains. Biotechnol. Lett., 2001, 23(24), 2015-2019.
[http://dx.doi.org/10.1023/A:1013783030276]
[73]
Landete, J.M.; de Las Rivas, B.; Marcobal, A.; Muñoz, R. Molecular methods for the detection of biogenic amine-producing bacteria on foods. Int. J. Food Microbiol., 2007, 117(3), 258-269.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2007.05.001] [PMID: 17532497]
[74]
Griswold, A.R.; Jameson-Lee, M.; Burne, R.A. Regulation and physiologic significance of the agmatine deiminase system of Streptococcus mutans UA159. J. Bacteriol., 2006, 188(3), 834-841.
[http://dx.doi.org/10.1128/JB.188.3.834-841.2006] [PMID: 16428386]
[75]
Perez, M.; Calles-Enríquez, M.; Nes, I.; Martin, M.C.; Fernandez, M.; Ladero, V.; Alvarez, M.A. Tyramine biosynthesis is transcriptionally induced at low pH and improves the fitness of Enterococcus faecalis in acidic environments. Appl. Microbiol. Biotechnol., 2015, 99(8), 3547-3558.
[http://dx.doi.org/10.1007/s00253-014-6301-7] [PMID: 25529314]
[76]
Tasić, T.; Ikonić, P.; Mandić, A.; Jokanović, M.; Tomović, V.; Savatić, S.; Petrović, L. Biogenic amines content in traditional dry fermented sausage Petrovská klobása as possible indicator of good manufacturing practice. Food Control, 2012, 23(1), 107-112.
[http://dx.doi.org/10.1016/j.foodcont.2011.06.019]