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Advances in Detection Methods of l-Amino Acid Oxidase Activity

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Abstract

l-Amino acid oxidase (LAAO) is widely distributed in many different organisms and found to play important biological roles, thus attracting a great deal of attention for characterization of its activity. Diverse detection methods with their own properties have been established. This review advanced different LAAO activity assays based on substrate consumption, cofactor amount, and product accumulation. The description of benefits and drawbacks of each method is expected to help researchers find appropriate detection method of LAAO activity for their own purpose.

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References

  1. Gómez, D., Espinosa, E., Bertazzo, M., Lucas-Elío, P., Solano, F., & Sanchez-Amat, A. (2008). The macromolecule with antimicrobial activity synthesized by Pseudoalteromonas luteoviolacea strains is an l-amino acid oxidase. Applied Microbiology and Biotechnology, 79, 925–930.

    Article  Google Scholar 

  2. James, S. G., Holmstrom, C., & Kjelleberg, S. (1996). Purification and characterization of a novel antibacterial protein from marine bacterium D2. Applied and Environmental Microbiology, 62, 2783–2788.

    CAS  Google Scholar 

  3. Kitani, Y., Mori, T., Nagai, H., Toyooka, K., Ishizaki, S., Shimakura, K., et al. (2007). Gene expression and distribution of antibacterial l-amino acid oxidase in the rockfish Sebastes schlegeli. Fish & Shellfish Immunology, 23, 1178–1186.

    Article  CAS  Google Scholar 

  4. Zhang, Y. J., Wang, J. H., Lee, W. H., Wang, Q., Liu, H., Zheng, Y. T., et al. (2003). Molecular characterization of Trimeresurus stejnegeri venom l-amino acid oxidase with potential anti-HIV activity. Biochemical and Biophysical Research Communications, 309(3), 598–604.

    Article  CAS  Google Scholar 

  5. Treshalina, H. M., Lukasheva, E. V., Sedakova, L. A., Firsova, G. A., Guerassimova, G. K., Gogichaeva, N. V., et al. (2000). Anticancer enzyme L-lysine α-oxidase: Properties and application perspectives. Applied Biochemistry and Biotechnology, 88, 267–273.

    Article  CAS  Google Scholar 

  6. Suhr, M., & Kim, D. S. (1996). Identification of the snake venom substance that induces apoptosis. Biochemical and Biophysical Research Communications, 224(1), 134–139.

    Article  CAS  Google Scholar 

  7. Sakurai, Y., Takatsuka, H., Yoshioka, A., Matsui, T., Suzuki, M., Titani, K., et al. (2001). Inhibition of human platelet aggregation by l-amino acid oxidase purified from Naja naja kaouthia venom. Toxicon, 39(12), 1827–1833.

    Article  CAS  Google Scholar 

  8. Iijima, R., Kisugi, J., & Yamazaki, M. (2003). A novel antimicrobial peptide from the sea hare Dolabella auricularia. Developmental and Comparative Immunology, 27(4), 305–311.

    Article  CAS  Google Scholar 

  9. Davis, M. A., Askin, M. C., & Hynes, M. J. (2005). Amino acid catabolism by an areA-regulated gene encoding an l-amino acid oxidase with broad substrate specificity in Aspergillus nidulans. Applied and Environmental Microbiology, 71(7), 3551–3555.

    Article  CAS  Google Scholar 

  10. Huang, Y. L., Li, M., Yu, Z., & Qian, P. Y. (2011). Correlation between pigmentation and larval settlement deterrence by Pseudoalteromonas sp. sf57. Biofouling, 27(3), 287–293.

    Article  CAS  Google Scholar 

  11. Bouvrette, P., & Luong, J. H. (1994). Isolation, purification and further characterization of an l-phenylalanine oxidase from Morganella morganii. Applied Biochemistry and Biotechnology, 48, 61–73.

    Article  CAS  Google Scholar 

  12. Vallon, O., Bulté, L., Kuras, R., Olive, J., & Wollman, F. A. (1993). Extensive accumulation of an extracellular l-amino-acid oxidase during gametogenesis of Chlamydomonas reinhardtii. European Journal of Biochemistry, 215, 351–360.

    Article  CAS  Google Scholar 

  13. Okazaki, S., Nakano, S., Matsui, D., Akaji, S., Inagaki, K., & Asano, Y. (2013). X-ray crystallographic evidence for the presence of the cysteine tryptophylquinone cofactor in l-lysine ε-oxidase from Marinomonas mediterranea. Journal of Biochemistry, 154(3), 233–236.

    Article  CAS  Google Scholar 

  14. Chacón-Verdú, M. D., Gómez, D., Solano, F., Lucas-Elío, P., & Sánchez-Amat, A. (2013). LodB is required for the recombinant synthesis of the quinoprotein l-lysine-ε-oxidase from Marinomonas mediterranea. Applied Microbiology and Biotechnology, 98(7), 2981–2989.

    Article  Google Scholar 

  15. Hafner, E. W., & Wellner, D. (1971). Demonstration of imino acids as products of the reactions catalyzed by d- and l-amino acid oxidases. Proceedings of National Academy of Sciences of the United States of America, 68(5), 987–991.

    Article  CAS  Google Scholar 

  16. Hafner, E. W., & Wellner, D. (1979). Reactivity of the imino acids formed in the amino acid oxidase reaction. Biochemistry, 18(4), 411–417.

    Article  CAS  Google Scholar 

  17. Schriek, S., Rückert, C., Staiger, D., Pistorius, E. K., & Michel, K. P. (2007). Bioinformatic evaluation of l-arginine catabolic pathways in 24 cyanobacteria and transcriptional analysis of genes encoding enzymes of l-arginine catabolism in the cyanobacterium Synechocystis sp. PCC 6803. BMC Genomics, 8, 437.

    Article  Google Scholar 

  18. Furuya, Y., Sawada, H., Hirahara, T., Ito, K., Ohshiro, T., & Izumi, Y. (2000). A novel enzyme, l-tryptophan oxidase, from a basidiomycete, Coprinus sp. SF-1: Purification and characterization. Bioscience, Biotechnology, and Biochemistry, 64(7), 1486–1493.

    Article  CAS  Google Scholar 

  19. Puiffe, M. L., Lachaise, I., Molinier-Frenkel, V., & Castellano, F. (2013). Antibacterial properties of the mammalian l-amino acid oxidase IL4I1. PloS One, 8(1), e54589.

    Article  CAS  Google Scholar 

  20. Ralph, E. C., Anderson, M. A., Cleland, W. W., & Fitzpatrick, P. F. (2006). Mechanistic studies of the flavoenzyme tryptophan 2-monooxygenase: Deuterium and 15 N kinetic isotope effects on alanine oxidation by an l-amino acid oxidase. Biochemistry, 45(51), 15844–15852.

    Article  CAS  Google Scholar 

  21. Sobrado, P., & Fitzpatrick, P. F. (2003). Analysis of the role of the active site residue Arg98 in the flavoprotein tryptophan 2-monooxygenase, a member of the l-amino oxidase family. Biochemistry, 42(47), 13826–13832.

    Article  CAS  Google Scholar 

  22. Nishizawa, T., Aldrich, C. C., & Sherman, D. H. (2005). Molecular analysis of the Rebeccamycin l-amino acid oxidase from Lechevalieria aerocolonigenes ATCC 39243. Journal of Bacteriology, 187(6), 2084–2092.

    Article  CAS  Google Scholar 

  23. Yang, H., Johnson, P. M., Ko, K. C., Kamio, M., Germann, M. W., Derby, C. D., et al. (2005). Cloning, characterization and expression of escapin, a broadly antimicrobial FAD-containing l-amino acid oxidase from ink of the sea hare Aplysia californica. The Journal of Experimental Biology, 208, 3609–3622.

    Article  CAS  Google Scholar 

  24. Ponnudurai, G., Chung, M. C., & Tan, N. H. (1994). Purification and properties of the l-amino acid oxidase from Malayan pit viper (Calloselasma rhodostoma) venom. Archives of Biochemistry and Biophysics, 313(2), 373–378.

    Article  CAS  Google Scholar 

  25. Lu, Q. M., Wei, Q., Jin, Y., Wei, J. F., Wang, W. Y., & Xiong, Y. L. (2002). l-amino acid oxidase from Trimeresurus jerdonii snake venom: Purification, characterization, platelet aggregation-inducing and antibacterial effects. Journal of Natural Toxins, 11(4), 345–352.

    CAS  Google Scholar 

  26. Saurina, J., Hernandez-Cassou, S., Fabregas, E., & Alegret, S. (1998). Potentiometric biosensor for lysine analysis based on a chemically immobilized lysine oxidase membrane. Analytica Chimica Acta, 371(1), 49–56.

    Article  CAS  Google Scholar 

  27. El-Sayed, A. S. (2011). Purification and characterization of a new l-methioninase from solid cultures of Aspergillus flavipes. The Journal of Microbiology, 49(1), 130–140.

    Article  CAS  Google Scholar 

  28. El-Sayed, A. S., Shindia, A. A., & Zaher, Y. (2012). l-Amino acid oxidase from filamentous fungi: Screening and optimization. Annals of Microbiology, 62(2), 773–784.

    Article  CAS  Google Scholar 

  29. Ghauch, A., Rima, J., Charef, A., Suptil, J., Fachinger, C., & Martin-Bouyer, M. (1999). Quantitative measurements of ammonium, hydrogenophosphate and Cu(II) by diffuse reflectance spectroscopy. Talanta, 48, 385–392.

    Article  CAS  Google Scholar 

  30. Timmer, B., Wouter Olthuis, W., & van den Berg, A. (2005). Ammonia sensors and their applications-a review. Sensors and Actuators B, 107, 666–677.

    Article  CAS  Google Scholar 

  31. Weinberger, F., Pohnert, G., Berndt, M. L., Bouarab, K., Kloareg, B., & Potin, P. (2005). Apoplastic oxidation of l-asparagine is involved in the control of the green algal endophyte Acrochaete operculata Correa & Nielsen by the red seaweed Chondrus crispus Stackhouse. Journal of Experimental Botany, 56(415), 1317–1326.

    Article  CAS  Google Scholar 

  32. Saurina, J., Hernandez-Cassou, S., Fabregas, E., & Alegret, S. (1998). Potentiometric biosensor for lysine analysis based on a chemically immobilized lysine oxidase membrane. Analytica Chimica Acta, 371, 49–56.

    Article  CAS  Google Scholar 

  33. Singh, S., Gogoi, B. K., & Bezbaruah, R. L. (2009). Optimization of medium and cultivation conditions for l-amino acid oxidase production by Aspergillus fumigatus. Canadian Journal of Microbiology, 55(9), 1096–1102.

    Article  CAS  Google Scholar 

  34. Danson, J. W., Trawick, M. L., & Cooper, A. J. (2002). Spectrophotometric assays for l-lysine α-oxidase and γ-glutamylamine cyclotransferase. Analytical Biochemistry, 303, 120–130.

    Article  CAS  Google Scholar 

  35. Tong, H. C., Chen, W., Shi, W. Y., Qi, F. X., & Dong, X. Z. (2008). SO-LAAO, a novel l-amino acid oxidase that enables Streptococcus oligofermentans to over-compete Streptococcus mutans by generating H2O2 from peptone. Journal of Bacteriology, 190(13), 4716–4721.

    Article  CAS  Google Scholar 

  36. Lee, M. L., Tan, N. H., Fung, S. Y., & Sekaran, S. D. (2011). Antibacterial action of a heat-stable form of l-amino acid oxidase isolated from king cobra (Ophiophagus hannah) venom. Comparative Biochemistry and Physiology, Part C: Toxicology & Pharmacology, 153, 237–242.

    Google Scholar 

  37. Zhang, H., Yang, Q., Sun, M., Teng, M., & Niu, L. (2004). Hydrogen peroxide produced by two amino acid oxidases mediates antibacterial actions. The Journal of Microbiology, 42(4), 336–339.

    CAS  Google Scholar 

  38. Avrameas, S., & Guilbart, B. (1972). Enzyme-immunoassay for the measurement of antigens using peroxidase conjugates. Biochimie, 54, 837–842.

    Article  CAS  Google Scholar 

  39. Chen, H. S., Wang, Y. M., Huang, W. T., Huang, K. F., & Tsai, I. H. (2012). Cloning, characterization and mutagenesis of Russell’s viper venom l-amino acid oxidase: Insights into its catalytic mechanism. Biochimie, 94(2), 335–344.

    Article  CAS  Google Scholar 

  40. Yang, C. A., Cheng, C. H., Lo, C. T., Liu, S. Y., Lee, J. W., & Peng, K. C. (2011). A novel l-amino acid oxidase from Trichoderma harzianum ETS 323 associated with antagonism of Rhizoctonia solani. Journal of Agricultural and Food Chemistry, 59, 4519–4526.

    Article  CAS  Google Scholar 

  41. Butzke, D., Hurwitz, R., Thiede, B., Goedert, S., & Rudel, T. (2005). Cloning and biochemical characterization of APIT, a new l-amino acid oxidase from Aplysia punctata. Toxicon, 46(5), 479–489.

    Article  CAS  Google Scholar 

  42. Nagashima, Y., Tsukamoto, C., Kitani, Y., Ishizaki, S., Nagai, H., & Yanagimoto, T. (2009). Isolation and cDNA cloning of an antibacterial l-amino acid oxidase from the skin mucus of the great sculpin Myoxocephalus polyacanthocephalus. Comparative Biochemistry and Physiology Part B, Biochemistry and Molecular Biology, 154, 55–61.

    Article  Google Scholar 

  43. Okubo, B. M., Silva, O. N., Migliolo, L., Gomes, D. G., Porto, W. F., Batista, C. L., et al. (2012). Evaluation of an antimicrobial l-amino acid oxidase and peptide derivatives from Bothropoides mattogrosensis pitviper venom. PloS One, 7(3), e33639.

    Article  CAS  Google Scholar 

  44. Naumann, G. B., Silva, L. F., Silva, L., Faria, G., Richardson, M., Evangelista, K., et al. (2011). Cytotoxicity and inhibition of platelet aggregation caused by an l-amino acid oxidase from Bothrops leucurus venom. Biochimica et Biophysica Acta, 1810, 683–694.

    Article  CAS  Google Scholar 

  45. Frey, A., Meckelein, B., Externest, D., & Schmidt, M. A. (2000). A stable and highly sensitive 3,3′,5,5′-tetramethylbenzidine-based substrate reagent for enzyme-linked immunosorbent assays. Journal of Immunological Methods, 233, 47–56.

    Article  CAS  Google Scholar 

  46. Wilming, M., Iffland, A., Tafelmeyer, P., Arrivoli, C., Saudan, C., & Johnsson, K. (2002). Examining reactivity and specificity of cytochrome c peroxidase by using combinatorial mutagenesis. ChemBioChem, 3, 1097–1104.

    Article  CAS  Google Scholar 

  47. Porstmann, T., & Kiessig, S. T. (1992). Enzyme immunoassay techniques. An overview. Journal of Immunological Methods, 150(1–2), 5–12.

    Article  CAS  Google Scholar 

  48. Gallati, H., & Pracht, I. (1985). Horseradish peroxidase: kinetic studies and optimization of peroxidase activity determination using the substrates H2O2 and 3,3',5,5'-tetramethylbenzidine. Journal of Clinical Chemistry and Clinical Biochemistry, 23, 453–460.

    CAS  Google Scholar 

  49. Joseph, P. D., Eling, T., & Mason, R. P. (1982). The horseradish peroxidase-catalyzed oxidation of 3,5,3′,5′-tetramethylbenzidine. Free radical and charge-transfer complex intermediates. The Journal of Biological Chemistry, 257(7), 3669–3675.

    Google Scholar 

  50. Azevedo, A. M., Fonseca, L. P., Graham, D. L., Cabral, J. M., & Prazeres, D. M. (2001). Behaviour of horseradish peroxidase in AOT reversed micelles. Biocatalysis and Biotransformation, 19(1), 213–233.

    Article  CAS  Google Scholar 

  51. Goodwin, D. C., Yamazaki, I., Aust, S. D., & Grover, T. A. (1995). Determination of rate constants for rapid peroxidase reactions. Analytical Biochemistry, 231, 333–338.

    Article  CAS  Google Scholar 

  52. Gómez, D., Lucas-Elío, P., Sanchez-Amat, A., & Solano, F. (2006). A novel type of lysine oxidase: l-lysine-ε-oxidase. Biochimica et Biophysica Acta, 1764(10), 1577–1585.

    Article  Google Scholar 

  53. Palamakumbura, A. H., & Trackman, P. C. (2002). A fluorometric assay for detection of l-lysine α-oxidase enzyme activity in biological samples. Analytical Biochemistry, 300, 245–251.

    Article  CAS  Google Scholar 

  54. Wang, B. Q., & Dong, S. J. (2000). Sol-gel-derived amperometric biosensor for hydrogen peroxide based on methylene green incorporated in Nafion film. Talanta, 51, 565–572.

    Article  CAS  Google Scholar 

  55. Liu, S. Q., & Ju, H. X. (2002). Renewable reagentless hydrogen peroxide sensor based on direct electron transfer of horseradish peroxidase immobilized on colloidal gold-modified electrode. Analytical Biochemistry, 307, 110–116.

    Article  CAS  Google Scholar 

  56. Geueke, B., & Hummel, W. (2002). A new bacterial l-amino acid oxidase with a broad substrate specificity: Purification and characterization. Enzyme and Microbial Technology, 31, 77–87.

    Article  CAS  Google Scholar 

  57. Saito, M., Seki, M., Lida, K., Nakayama, H., & Yoshiada, S. (2007). A novel agar medium to detect hydrogen peroxide-producing bacteria based on the prussian blue-forming reaction. Microbiology and Immunology, 51(9), 889–892.

    Article  CAS  Google Scholar 

  58. 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(2), e55548.

    Article  CAS  Google Scholar 

  59. Ehara, T., Kitajima, S., Kanzawa, N., Tamiya, T., & Tsuchiya, T. (2002). Antimicrobial action of achacin is mediated by l-amino acid oxidase activity. FEBS Letters, 531, 509–512.

    Article  CAS  Google Scholar 

  60. Hermes-Lima, M., Willmore, W. G., & Storey, K. B. (1995). Quantification of lipid peroxidation in tissue extracts based on Fe(III)xylenol orange complex formation. Free Radical Biology & Medicine, 19(3), 271–280.

    Article  CAS  Google Scholar 

  61. Chen, W. M., Lin, C. Y., & Sheu, S. Y. (2010). Investigating antimicrobial activity in Rheinheimera sp. due to hydrogen peroxide generated by l-lysine oxidase activity. Enzyme and Microbial Technology, 46, 487–493.

    Article  CAS  Google Scholar 

  62. Chen, W. M., Lin, C. Y., Chen, C. A., Wang, J. T., & Sheu, S. Y. (2010). Involvement of an l-amino acid oxidase in the activity of the marine bacterium Pseudoalteromonas flavipulchra against methicillin-resistant Staphylococcus aureus. Enzyme and Microbial Technology, 47, 52–58.

    Article  CAS  Google Scholar 

  63. Rau, J. E., & Fischer, U. (2011). In-gel detection of l-amino acid oxidases based on the visualisation of hydrogen peroxide production. Journal of Microbiological Methods, 85, 228–229.

    Article  CAS  Google Scholar 

  64. Yu, Z., & Qiao, H. (2012). Advances in non-snake venom l-amino acid oxidase. Applied Biochemistry and Biotechnology, 167(1), 1–13.

    Article  CAS  Google Scholar 

  65. Yu, Z., Zhou, N., Qiao, H., & Qiu, J. (2014). Identification, cloning and expression of l-amino acid oxidase from marine Pseudoalteromonas sp. B3. Scientific World Journal, 979858.

  66. Zhou, M., Diwu, Z., Panchuk-Voloshina, N., & Haugland, R. P. (1997). A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: Applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Analytical Biochemistry, 253, 162–168.

    Article  CAS  Google Scholar 

  67. Friedman, M. (2004). Applications of the ninhydrin reaction for analysis of amino acids, peptides, and proteins to agricultural and biomedical sciences. Journal of Agricultural and Food Chemistry, 52(3), 385–406.

    Article  CAS  Google Scholar 

  68. Roth, M. (1971). Fluorescence reaction for amino acids. Analytical Chemistry, 43(7), 880–882.

    Article  CAS  Google Scholar 

  69. Burton, K. (1951). The l-amino acid oxidase of Neurospora. Biochemical Journal, 50(2), 258–268.

    CAS  Google Scholar 

  70. Böhmer, A., Müller, A., Passarge, M., Liebs, P., Honeck, H., & Müller, H. G. (1989). A novel l-glutamate oxidase from Streptomyces endus: Purification and properties. European Journal of Biochemistry, 182, 327–332.

    Article  Google Scholar 

  71. Gay, C., Collins, J., & Gebicki, J. M. (1999). Hydroperoxide assay with the ferric-xylenol orange complex. Analytical Biochemistry, 273(2), 149–155.

    Article  CAS  Google Scholar 

  72. Yu, Z., Wang, J., Zhou, N., Zhao, C., & Qiu, J. (2013). A highly sensitive method for quantitative determination of l-amino acid oxidase activity based on the visualization of ferric-xylenol orange formation. PloS One, 8(12), e82483.

    Article  Google Scholar 

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Acknowledgments

This work was supported by Regional Demonstration of Marine Economy Innovative Development Project, China (No. 12PYY001SF08).

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Authors and Affiliations

  1. College of Biological and Environmental Engineering, Zhejiang University of Technology, Hangzhou, China

    Zhiliang Yu, Yangsheng Wang, Ning Zhou, Minyan Zhao & Juanping Qiu

  2. Department of Electrical Engineering, Columbia University, New York, NY, USA

    Jianxun Lin

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  1. Zhiliang Yu
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Yu, Z., Wang, Y., Zhou, N. et al. Advances in Detection Methods of l-Amino Acid Oxidase Activity. Appl Biochem Biotechnol 174, 13–27 (2014). https://doi.org/10.1007/s12010-014-1005-0

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