L-Amino acid oxidases from microbial sources: Types, properties, functions, and applications

Applied Microbiology and Biotechnology

Volumn 98, Issue 4, 2014, Pages 1507-1515

  Hossain, Gazi Sakir ^a,b,c   Li, Jianghua ^a,c   Shin, Hyun Dong ^d   Du, Guocheng ^a,c   Liu, Long ^a,b,c   Chen, Jian ^a  

^a JIANGNAN UNIVERSITY   (China)

^b EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c Synergetic Innovation Center of Food Safety and Nutrition   (China)

^d Georgia Institute of Technology   (United States)

Author keywords

Biotechnological applications; Function; l Amino acid oxidase; Properties; Structure

Indexed keywords

AMINO ACID OXIDOREDUCTASES; AMINO ACIDS; BIOTECHNOLOGY; L-AMINO ACID OXIDASE;

EID: 84894330298     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-5444-2     Document Type: Review

References (104)

1. Ahn MY, Ryu KS, Lee YW, Kim YS (2000) Cytotoxicity and l-amino acid oxidase activity of crude insect drugs. Arch Pharm Res 23:477-481
2. Anraku Y, Gennis RB (1987) The aerobic respiratory chain of Escherichia coli. Trends Biochem Sci 12:262-266
3. Arima J, Tamura T, Kusakabe H, Ashiuchi M, Yagi T, Tanaka H, Inagaki K (2003) Recombinant expression, biochemical characterization and stabilization through proteolysis of an l- glutamate oxidase from Streptomyces sp. X-119-6. J Biochem 134:805-812
4. Arima J, Sasaki C, Sakaguchi C, Mizuno H, Tamura T, Kashima A, Kusakabe H, Sugio S, Inagaki K (2009) Structural characterization of l-glutamate oxidase from Streptomyces sp. X-119-6. FEBS J 276:3894-3903
5. Arinbasarova A, Ashin VV, Makrushin KV, Medentsev AG, Lukasheva EV, Berezov TT (2012) Isolation and properties of l-lysine-alpha-oxidase from the fungus Trichoderma cf. aureoviride RIFAI VKM F-4268D tion. Mikrobiologiia 81:594-599
6. Baek JO, Seo JW, Kwon O, Seong S, Kim IH, Kim CH (2008) Heterologous expression and characterization of l-amino acid deaminase from Proteus mirabilis in Escherichia coli. Chi J Biotech 24:21-29
7. Baek JO, Seo JW, Kwon O, Seong SI, Kim IH, Kim CH (2011) Expression and characterization of a second l-amino acid deaminase isolated from Proteus mirabilis in Escherichia coli. J Basic Microbiol 51:129-135
8. Blaschko H, Hope DB (1956) The oxidation of l-amino acids by Mytilus edulis. Biochem J 62:335-339
9. Bockholt R, Masepohl B, Kruft V, Wittmann-Liebold B, Pistorius EK (1995) Partial amino acid sequence of a l-amino acid oxidase from the cyanobacterium Synechococcus PCC6301, cloning and DNA sequence analysis of the aoxA gene. Biochim Biophys Acta 1264:289-293
10. Böhmer A, Müller A, Passarge M, Liebs P, Honeck H, Müller HG (1989) A novel l-glutamate oxidase from Streptomyces endus purification and properties. Eur J Biochem 182:327-332
11. Bossi RT, Negri A, Tedeschi G, Mattevi A (2002) Structure of FAD-bound l-aspartate oxidase: insight into substrate specificity and catalysis. Biochem 41:3018-3024
12. Braun M, Kim JM, Schmid RD (1992) Purification and some properties of an extracellular l-amino acid oxidase from Cellulomonas cellulans AM8 isolated from soil. Appl Microbiol Biotechnol 37:594-598
13. Brearley GM, Price CP, Atkinson T, Hammond PM (1994) Purification and partial characterization of a broad-range l-amino acid oxidase from Bacillus carotarum 2Pfa isolated from soil. Appl Microbiol Biotechnol 41:670-676
14. Carbonnelle-Puscian A, Copie-Bergman C, Baia M, Martin-Garcia N, Allory Y, Haioun C, Crémades A, Abd-Alsamad I, Farcet JP, Gaulard P, Castellano F, Molinier-Frenkel V (2009) The novel immunosuppressive enzyme IL4I1 is expressed by neoplastic cells of several B-cell lymphomas and by tumor associated macrophages. Leukemia 23:952-960
15. Chauhan N, Narang J, Sunny, Pundir CS (2013) Immobilization of lysine oxidase on a gold-platinum nanoparticles modified Au electrode for detection of lysine. Enzyme Microb Technol 52:265-271
16. Chen WM, Lin CY, Che CA, Wang JT, Sheu SY (2010) Involvement of an l-amino acidoxidase in the activity of the marine bacterium Pseudoalteromonas flavipulchra against methicillin resistant Staphylococcus aureus. Enzym Microb Tech 47:52-58
17. Cheng CH, Yang CA, Liu SY, Lo CT, Huang HC, Liao FC, Peng KC (2011) Cloning of a novel l-amino acid oxidase from Trichoderma harzianum ETS 323 and bioactivity analysis of overexpressed l-amino acid oxidase. J Agric Food Chem 59:9142-9149
18. Christiansen L, Budolfsen G (2002) Preparation of baked product from dough. US patent 6,890,570, 10 May 2005.
19. Coudert M, Vandecasteele JP (1975) Characterization and physiological function of a soluble l- amino acid oxidase in Corynebacterium. Arch Microbiol 102:151-153
20. Curti B, Massey V, Zmudka M (1968) Inactivation of snake venom l-amino acid oxidase by freezing. J Biol Chem 243:2306-2314
21. Davis MA, Askin MC, Hynes MJ (2005) Amino acid catabolism by an area-regulated gene encoding an l-amino acid oxidase with broad substrate specificity in Aspergillus nidulans. Appl Environ Microbiol 71:3551-3555
22. DeBusk RM, Ogilvie S (1984a) Participation of an extracellular deaminase in amino acid utilization by Neurospora crassa. J Bacteriol 159:583-589
23. DeBusk RM, Ogilvie S (1984b) Nitrogen regulation of amino acid utilization by Neurospora crassa. J Bacteriol 160:493-498
24. DeBusk RM, Ogilvie S (1984c) Regulation of amino acid utilization in Neurospora crassa: effect of nmr-1 and ms-5 mutations. J Bacteriol 60:656-661
25. Du XY, Clemetson KJ (2002) Snake venom L-amino acid oxidases. Toxicon 40:659-665
26. Duerre JA, Chakrabarty S (1975) l-amino acid oxidases of Proteus rettgeri. J Bacteriol 121:656-663
27. Ehara T, Kitajima S, Kanzawa N, Tamiya T, Tsuchiya T (2002) Antimicrobial action of achacin is mediated by l-amino acid oxidase activity. FEBS Lett 531:509-512
28. Faust A, Geueke B, Niefind K, Hummel W, Schomburg D (2006) Crystallization and preliminary x-ray analysis of a bacterial l-amino-acid oxidase from Rhodococcus opacus. Acta Crystallogr Sect F: Struct Biol Cryst Commun 62:279-281
29. Faust A, Niefind K, Hummel W, Schombur D (2007) The structure of a bacterial l-amino acid oxidase from Rhodococcus opacus gives new evidence for the hydride mechanism for dehydrogenation. J Mol Biol 367:234-248
30. Findrik Z, Geueke B, Hummel W, Vasić-Rački D (2006) Modelling of LDOPA enzymatic oxidation catalyzed by l-amino acid oxidases from Crotalus adamanteus and Rhodococcus opacus. Biochem Eng J 27:275-286
31. Fitzpatrick PF (2004) Carbanion versus hydride transfer mechanisms in flavoprotein-catalyzed dehydrogenations. Bioorg Chem 32:125-139
32. Franklin FC, Venables WA (1976) Biochemical, genetic, and regulatory studies of alanine catabolism in Escherichia coli K12. Mol Gen Genet 149:229-237
33. Gau AE, Heindl A, Nodop A, Kahmann U, Pistorius EK (2007) l-Amino acid oxidases with specificity for basic l-amino acids in cyanobacteria. Z Naturforsch C 62:273-284
34. Genet R, Bénetti PH, Hammadi A, Ménez A (1995) l-Tryptophan 2′,3′-oxidase from Chromobacterium violaceum. J Biol Chem 270:23540-23545
35. Geueke B, Hummel W (2002) A new bacterial l-amino acid oxidase with a broad substrate specificity: purification and characterization. Enzym Microb Technol 31:77-87
36. Geueke B, Hummel W (2003) Heterologous expression of Rhodococcus opacus l-amino acid oxidase in Streptomyces lividans. Protein Expr Purif 28:303-309
37. Hanson RL, Bembenek KS, Patel RN, Szarka LJ (1992) Transformation of N epsilon-CBZ- l-lysine to CBZ-l-oxylysine using l-amino acid oxidase from Providencia alcalifaciens and l-2-hydroxy-isocaproate dehydrogenase from Lactobacillus confusus. Appl Microbiol Biotechnol 37:599-603
38. Hossain GS, Liu L, Shin HD, Du G, Chen J (2013) Bioconversion of α-ketoglutaric acid to l-glutamic acid by an immobilized whole-cell biocatalyst expressing l-amino acid deaminase from Proteus mirabilis. J Biotechnol. doi: 10.1016/j.jbiotec.2013.10.026
39. Huang T, Warsinke A, Kuwana T, Scheller FW (1998) Determination of l-phenylalanine based on an NADH-detecting biosensor. Anal Chem 70:991-997
40. Huang YL, Li M, Yu Z, Qian PY (2011) Correlation between pigmentation and larval settlement deterrence by Pseudoalteromonas sp. sf57. Biofouling 27:287-293
41. Ida K, Kurabayashi M, Suguro M, HirumaY HT, Yamomoto M, Suzuki H (2008) Structural basis of proteolytic activation of l-phenylalanine oxidase from Pseudomonas sp. P-501. J Biol Chem 24:16584-16590
42. Ida K, Suguro M, Suzuki H (2011) High resolution x-ray crystal structures of l-phenylalanine oxidase (deaminating and decarboxylating) from Pseudomonas sp. P-501. Structures of the enzyme-ligand complex and catalytic mechanism. J Biol Chem 150:659-669
43. Isobe K, Fukuda N, Nagasawa S (2008) Analysis of selective production of N-alpha-benzyloxycarbonyl- l- aminoadipate-delta-semialdehyde and N-alpha-benzyloxycarbonyl- l-aminoadipic acid by Rhodococcus sp. AIU Z-35-1. J Biosci Bioeng 105:152-156
44. James SG, Holmstrom C, Kjelleberg S (1996) Purification and characterization of a novel antibacterial protein from marine bacterium D2. Appl Environ Microbiol 62:2783-2788
45. Jang D, Kim K, Park D, Kim G (2012) Efficient optical resolution of amino acid by alanine racemaze chiral analogue supported on mesoporous carbon. IOP Conf Ser: Mater Sci Eng 40:012024
46. Jones H, Venables WA (1983) Effects of solubilization on some properties of the membrane-bound respiratory enzyme D-amino acid dehydrogenase of Escherichia coli. FEBS Lett 151:189-192
47. Kacaniklic V, Johansson K, Marko-Varga G, Gorton L, Jonssön- Pettersson G, Csöregi E (1994) Amperometric biosensors for detection of l- and D-amino acids based on coimmobilized peroxidase and l-and D-amino acid oxidases in carbon paste electrodes. Electroanalysis 6:381-390
48. Koyama H (1982) Purification and characterization of a novel l-phenylalanine oxidase (Deaminating and decarboxylating) from Pseudomonas sp. P-501. J Bio Chem 92:1235-1240
49. Kusakabe H, Kodama K, Kuninaka A, Yoshino H (1980) A new antitumor enzyme, l-lysine oxidase from Trichoderma viride: purification and enzymological properties. J Biol Chem 255:976-981
50. Kwan RCH, Chan CY, Renneberg R (2002) An amperometric biosensor for determining amino acids using a bienzymatic system containing amino acid oxidase and protease. Biotechnol Lett 24:1203-1207
51. Lee YC, Huh MH (1999) Development of a biosensor with immobilized l-amino acid oxidase for determination of l-amino acids. J Food Bio Chem 23:173-185
52. Leese C, Fotheringham I, Escalettes F, Speight R, Grogan G (2012) Cloning, expression, characterization and mutational analysis of l-aspartate oxidase from Pseudomonas putida. J Mol Catal B Enzym 85-86:17-22
53. Liu L, Hossain GS, Shin HD, Li J, Du G, Chen J (2013) One-step production of α-ketoglutaric acid from glutamic acid with an engineered l-amino acid deaminase from Proteus mirabilis. J Biotechnol 164:97-104
54. Lucas-Elio P, Hernandez P, Sanchez-Amat A, Solano F (2005) Purification and partial characterization of marinocine, a new broad-spectrum antibacterial protein produced by Marinomonas mediterranea. Biochim Biophys Acta 1721:193-203
55. Lucas-Elio P, Gomez D, Solano F, Sanchez-Amat A (2006) The antimicrobial activity of marinocine, synthesized by Marinomonas mediterranea, is due to hydrogen peroxide generated by its lysine oxidase activity. J Bacteriol 188:2493-2501
56. Macheroux P, Seth O, Bollschweiler C, Schwarz M, Kurfürst M, Au LC, Ghisla S (2001) l-amino-acid oxidase from the Malayan pit viper Calloselasma rhodostoma. Comparative sequence analysis and characterization of active and inactive forms of the enzyme. Eur J Biochem 268:1679-1686
57. Mandal S, Bhattacharyya D (2008) Two l-amino acid oxidase isoenzymes from Russell's viper (Daboia russelli russelli) venom with different mechanism of inhibition by substrate analogs. FEBS J 275:2078-2095
58. Massad G, Zhao H, Mobley HL (1995) Proteus mirabilis amino acid deaminase: cloning, nucleotide sequence, and characterization of aad. J Bacteriol 177:5878-5883
59. Moynihan K, Elion BG, Pegram C, Reist CJ, Wellner D, Bigner DD, Griffith OW, Friedman HS (1997) l-amino acid oxidase (LOX) modulation of melphalan activity against intracranial glioma. Cancer Chemother Pharmacol 39:179-186
60. Muñoz-Blanco J, Hidalgo-Martínez J, Cárdenas J (1990) Extracellular deamination of l-amino acids by Chlamydomonas reinhadtii cells. Planta 182:194-198
61. Mutaguchi Y, Ohmori T, Sakuraba H, Yoneda K, Doi K, Ohshima T (2011) Visible wavelength spectrophotometric assays of l-aspartate and D-aspartate using hyperthermophilic enzyme systems. Anal Chem 409:1-6
62. Nakano M, Danowski TS (1966) Crystalline mammalian l-amino acid oxidase from rat kidney mitochondria. J Biol Chem 241:2075-2083
63. Neidermann DM, Lerch K (1990) Molecular cloning of the l-amino-acid oxidase gene from Neurospora crassa. J Biol Chem 265:17246-17251
64. Neidermann DM, Lerch K (1991) Regulation of biosynthesis of l-amino acid oxidase by Neurospora crassa. FEMS Microbiol Lett 79:309-314
65. Nishiya Y, Imanaka T (1998) Purification and characterization of a novel glycine oxidase from Bacillus subtilis. FEBS Lett 438:263-266
66. Nuutinen JT, Timoneni S (2008) Identification of nitrogen mineralization enzymes, l-amino acidoxidases, from the ectomycorrhizal fungi Hebeloma spp. and Laccaria bicolor. Mycol Res 112:1453-1464
67. Nuutinen JT, Marttinen E, Soliymani R, Hildén K, Timonen S (2012) l-amino acid oxidase of the fungus Hebeloma cylindrosporum displays substrate preference towards glutamate. Microbiol 158:272-283
68. Okubo BM, Silva ON, Migliolo L, Gomes DG, Porto WF, Batista CL, Ramos CS, Holanda HH, Dias SC, Franco OL, Moreno SE (2012) Evaluation of an antimicrobial l-amino acid oxidase and peptide derivatives from Bothropoides mattogrosensis pit viper venom. PLoS ONE 7:e33639
69. Olsiewski PJ, Kaczorowski GJ, Walsh C (1980) Purification and properties of D-amino acid dehydrogenase, an inducible membrane bound iron-sulfur flavoenzyme from Escherichia coli. J Biol Chem 255:4487-4494
70. Pawelek PD, Cheah J, Coulombe R, Macheroux P, Ghisla S, Vrielink A (2000) The structure of l-amino acid oxidase reveals the substrate trajectory into an enantiomerically conserved active site. EMBO J 19:4204-4215
71. 6 modified electrode. Fresenius J Anal Chem 367:707-713
72. Pelmont J, Arlaud G, Rossat AM (1972) l-amino acid oxydases des envelopes de Proteus mirabilis: proprie' te'sge' nerales. Biochemie 54:1359-1374
73. Pistorius EK, Voss H (1980) Some properties of a basic l-amino-acid oxidase from Anacystis nidulans. Biochim Biophys Acta 611:227-240
74. Pistorius EK, Voss H (1982) Presence of an amino acid oxidase in photosystem II of Anacystis nidulans. Eur J Biochem 126:203-209
75. Pokrovsky VS, Treshalina HM, Lukasheva EV, Sedakova LA, Medentzev AG, Arinbasarova AY, Berezov TT (2013) Enzymatic properties and anticancer activity of l-lysine α-oxidase from Trichoderma cf. aureoviride Rifai BKMF-4268D. Anticancer Drugs 24:846-851
76. Pollegioni L, Molla G (2011) New biotech applications from evolved D-amino acid oxidases. Trends Biotechnol 29:276-283
77. Preuschoff F, Spohn U, Weber E, Unverhau K, Mohr KH (1993) Chemiluminometric l-lysine determination with immobilized lysine oxidase by flow-injection analysis. Anal Chimi Acta 280:185-189
78. Puiffe ML, Lachaise I, Molinier-Frenkel V, Castellano F (2013) Antibacterial properties of the mammalian l-amino acid oxidase IL4I1. PLoS ONE 8:e54589
79. Qi L, Qiao J, Yang G, Chen Y (2009) Chiral ligand-exchange CE assays for separation of amino acid enantiomers and determination of enzyme kinetic constant. Electrophoresis 30:2266-2272
80. Ralph EC, Anderson MA, Cleland WW, Fitzpatrick PF (2006) Mechanistic studies of the flavoenzyme tryptophan 2-monooxygenase: deuterium and 15 N kinetic isotope effects on alanine oxidation by a l-amino acid oxidase. Biochem 45:15844-15852
81. Rau JE, Fischer U (2011) In-gel detection of l-amino acid oxidases based on the visualization of hydrogen peroxide production. J Microbiol Methods 85:228-229
82. Roth M (1971) Fluorescence reaction for amino acids. Anal Chem 43:880-882
83. Sakurai Y, Takatsuka H, Yoshioka A, Matsui T, Suzuki M, Titani K, Fujimura Y (2001) Inhibition of human platelet aggregation by l-amino acid oxidase purified from Naja naja kaouthia venom. Toxicon 39:1827-1833
84. Sarkar P, Tothill IE, Setford SJ, Turner AP (1999) Screen-printed amperometric biosensors for the rapid measurement of l-and D-amino acids. Analyst 124:865-870
85. Scheller FW, Schubert F (1989) Biosensors, 2nd edn. Amsterdam: Elsevier, pp. 157-159
86. Schneider P, Pedersen AH, Hansen SA (1998) l-amino acid oxidase. US Patent 5,801,035, 1 Sept 1998
87. Sikora L, Marzluf GA (1982) Regulation of l-amino acid oxidase and D-amino acid oxidase in Neurospora crassa. Mol Gen Genet 186:33-39
88. Simonian AL, Badalian IE, Berezov TT, Smirnova IP, Khaduev SH (1994) Flow-injection amperometric biosensor based on immobilized l-lysine-a-oxidase for l-lysine determination. Anal Lett 27:2849-2860
89. Singh S, Gogoi BK, Bezbaruah RL (2009) Optimization of medium and cultivation conditions for l-amino acid oxidase production by Aspergillus fumigatus. Can J Microbiol 55:1096-1102
90. Stumpf PK, Green DE (1944) l-amino acid oxidase of Proteus vulgaris. J Biol Chem 153:387-399
91. Takahashi E, Ito K, Yoshimoto T (1999) Cloning of l-amino acid deaminase gene from Proteus vulgaris. Biosci Biotechnol Biochem 63:2244-2247
92. Timmer B, Olthuis W, van den Berg A (2005) Ammonia sensors and their applications - a review. Sensor Actuat B 107:666-677
93. 2 from peptone. J Bacteriol 190:4716-4721
94. Treshalina HM, Lukasheva EV, Sedakova LA, Firsova GA, Guerassimova GK, Gogichaeva NV, Berezov TT (2000) Anticancer enzyme l-lysine α-oxidase: properties, application and perspectives. Appl Biochem Biotechnol 88:267-273
95. Vallon O (2000) New sequence motifs in flavoproteins: evidence for common ancestry and tools to predict structure. Proteins 38:95-114
96. Vallon O, Bulte L, Kuras R, Olive J, Wollman FA (1993) Extensive accumulation of an extracellular l-amino-acid oxidase during gametogenesis of Chlumydomonas reinhardtii. Eur J Biochem 215:351-360
97. Varadi M, Adányi N, Szabó EE, Trummer N (1999) Determination of the ratio of D- and l-amino acids in brewing by an immobilized amino acid oxidase enzyme reactor coupled to amperometric detection. Biosens Bioelectron 14:335-340
98. Wellner D (1966) Evidence for conformational changes in l-amino acid oxidase associated with reversible inactivation. Biochemical 5:1585-1591
99. Yang H, Johnson PM, Ko KC, Kamio M, Germann MW, Derby CD, Tai PC (2005) Cloning, characterization and expression of escapin, a broadly antimicrobial FAD-containing l-amino acid oxidase from ink of the sea hare Aplysia californica. J Exp Biol 208:609-622
100. Yang CA, Cheng CH, Lo CT, Liu SY, Lee JW, Peng KC (2011) A novel l-amino acid oxidase from Trichoderma harzianum ETS 323 associated with antagonism of Rhizoctonia solani. J Agric Food Chem 59:4519-4526
101. Yang CA, Cheng CH, Lee JW, Lo CT, Liu SY, Peng KC (2012) Monomeric l-amino acid oxidase-induced mitochondrial dysfunction in Rhizoctonia solani reveals a novel antagonistic mechanism of Trichoderma harzianum ETS 323. J Agric Food Chem 60:2464-2471
102. Yu EK, DeVoe IW (1981) l-Cysteine oxidase activity in the membrane of Neisseria meningitidis. J Bacteriol 145:280-287
103. Yu Z, Zhou N, Zhao C, Qiu J (2013) In-gel determination of l-amino acid oxidase activity based on the visualization of Prussian blue-forming reaction. PLoS One 8:e55548
104. Zeller A, Maritz A (1944) Ubereineneue l-aminosaure-oxidase. Helv Chim Acta 27:1888-1902