The effect of antioxidants on xanthine oxidase activity in fresh ovine milk
Keywords:antioxidant, molybdenum, tungsten, phospholipids, nitrate, nitrite
In the present, the consequences of nitrate pollution of the environment are very pronounced. In humans and animals, microorganisms can reduce nitrates to nitrites, which cause cancer. Purified and homogeneous xanthine oxidase (XO) of cow's milk can restore these compounds, which makes the article extremely relevant. The purpose of the article is to determine the effect of antioxidants on the activity of xanthine oxidase in fresh ovine milk. Various natural and artificial antioxidants were examined for the detection of xanthine oxidase (XO) activity in ovine milk. Among the natural antioxidants, L-cysteine was more effective in the stabilization of XO in heated milk. XO of sheep milk activated by heat treatment in the presence of cysteine and molybdenum became able to convert nitrate and nitrite to nitric oxide (NO). Therefore, L-cysteine was used for double purposes: as the protector of enzyme active center against the oxidation during heat treatment of milk and as a reagent for S-nitrosothiol formation. Hypoxanthine, as a natural substrate of XO, is an effective electron donor for nitrate reductase (NR) and nitrite reductase (NiR) activities. Heat treatment of the milk in the presence of exogenous lecithin increased the activity of NR and NiR of XO and CysNO formation. Thus, during the heat treatment: a) excess of exogenous phospholipids disintegrates the structure of milk fat globule membrane (MFGM) and b) enzyme molecules denatured partially and their active center became available for exogenous cysteine, molybdenum, hypoxanthine, and nitrate or nitrite.
Abadeh, S., Killacky, J., Benboubetra, M., Harrison, R. 1992. Purification and partial characterization of xanthine oxidase from human milk. Biochimica et Biophysica Acta, vol. 1117, no. 1, p. 25-32. https://doi.org/10.1016/0304-4165(92)90157-p
Alikulov, Z. A., Lvov, N. P., Kretovich, V. L. 1980. Nitrate and nitrite reductase activity of milk xanthine oxidase. Biokhimiia, vol. 45, no. 9, p. 1714-1718.
Alikulov, Z. A., Mendel, R. R. 1984. Molybdenum cofactor from tobacco cell cultures and milk xanthine oxidase: involvement of sulfhydryl groups in dimerization activity of cofactor. Biochemie und Physiologie der Pflanzen, vol. 179, no. 8, p. 693-705. https://doi.org/10.1016/S0015-3796(84)80026-8
Atmani, D., Benboubetra, M., Harrison, R. 2004. Goat’s milk xanthine oxidoreductase is grossly deficient in molybdenum. Journal of Dairy Research, vol. 71, no. 1, p. 7-13. https://doi.org/10.1017/S0022029903006514
Beedham, C. 2001. Molybdenum hydroxylases. Ioannides, C. In Ioannides, C. Enzyme systems that metabolize drug and xenobiotics. New York, USA: John Wiley & Sons Ltd., p. 147-187. ISBN 9780470846308. https://doi.org/10.1002/0470846305.ch5
Bray, R. S., Lowe, D., Godber, B., Harrison, R., Eisenthal, R. 1999. Properties of xanthine oxidase from human milk: grossly deficient in molybdenum and substantially deficient in iron-sulfur centers. In Ghisla, S., Kroneck, P., Macheroux, P., Sund, H. Flavins and Flavoproteins, Berlin: Weber, p. 775-778.
Bryan, N. S. 2006. Nitrite in nitric oxide biology: cause or consequence? A systems-based review. Free Radical Biology and Medicine, vol. 41, no. 5, p. 691-701. https://doi.org/10.1016/j.freeradbiomed.2006.05.019
Bryan, N. S., Bian, K., Murad, F. 2009. Discovery of the nitric oxide signaling pathway and targets for drug development. Frontiers in Bioscience, vol. 14, p. 1-18. https://doi.org/10.2741/3228
Garcia, C., Lutz, N. W., Confort-Gouny, S., Cozzone, P. J., Armand, M., Bernard, M. 2012. Phospholipid fingerprints of milk from different mammalians determined by 31P NMR: Towards specific interest in human health. Food Chemistry, vol. 135, p. 1777-1783. https://doi.org/10.1016/j.foodchem.2012.05.111
Gladwin, M., Schechter, A., Kim-Shapiro, D., Patel, R., Hogg, N., Shiva, S., Cannon III, R. O., Kelm, M., Wink, D., Graham Espey, M., Oldfield, E. H., Pluta, R. M., Freeman, B. A., Lancaster Jr, J. R., Feelisch, M., Lundberg, J. O. 2005. The emerging biology of the nitrite anion. Nature Chemical Biology, vol. 1, no. 6, p. 308-314. https://doi.org/10.1038/nchembio1105-308
Godber, B., Doel, J., Sapkota, G., Blake, D., Stevens, C., Eisenthal, R., Harrison, R. 2000. Reduction of Nitrite to Nitric Oxide Catalyzed by Xanthine Oxidoreductase. The Journal of biological chemistry, vol. 275, no. 11, p. 7757-7763. https://doi.org/10.1074/jbc.275.11.7757
Godber, B., Sanders, S., Harrison, R., Eisenthal, R., Bray, R. C. 1997. More or=95% of xanthine oxidase in human milk is present as the demolybdo form, lacking molybdopterin. Biochemical Society Transactions, vol. 25, no. 3, p. 519S-519S. https://doi.org/10.1042/bst025519s
Harrison, R. 2006. Milk xanthine oxidase: Properties and physiological roles. International Dairy Journal, vol. 16, no. 6, p. 546-554. https://doi.org/10.1016/j.idairyj.2005.08.016
Harrison, R. 2004. Physiological Roles of Xanthine Oxidoreductase. Drug Metabolism Reviews, vol. 36, p. 363-375. https://doi.org/10.1081/DMR-120037569
Hord, N. G., Ghannam, J. S., Garg, H. K., Berens, P. D., Bryan, N. S. 2011. Nitrate and nitrite content of human, formula, bovine, and soy milks: implications for dietary nitrite and nitrate recommendations. Breastfeed Medicine, vol. 6, no. 6, p. 393-399. https://doi.org/10.1089/bfm.2010.0070
Kisker, C., Schindelin, H., Rees, D. C. 1997. Molybdenum-cofactor-containing enzymes: structure and mechanism. Annual Review of Biochemistry, vol. 66, no. 1, p. 233-267. https://doi.org/10.1146/annurev.biochem.66.1.233
Kletzin, A., Adams, M. W. 1996. Tungsten in biological systems. FEMS Microbiology Reviews, vol. 18, no. 1, p. 5-63. https://doi.org/10.1111/j.1574-6976.1996.tb00226.x
Kramer, S. P., Johnson, J. L., Ribeiro, A. A., Millington, D. S., Rajagopalan, K. V. 1987. The Structure of the Molybdenum Cofactor. The Journal of Biological Chemistry, vol. 262, no. 34, p. 16357-16363. https://doi.org/10.1016/S0021-9258(18)49263-0
Kuo, W. N., Kocis, J. M., Nibbs, J. 2003. Nitrosation of cysteine and reduced glutathione by nitrite at physiological pH. Frontiers in Bioscience, vol. 8, no. 1, p. 62-69. https://doi.org/10.2741/1032
Marley, R., Patel, R. P., Orie, N., Ceaser, E., Darley-Usmar, V., Moore, K. 2001. Formation of nanomolar concentrations of S-nitroso-albumin in human plasma by nitric oxide. Free Radical Biology & Medicine, vol. 31, no. 5, p. 688-696. https://doi.org/10.1016/S0891-5849(01)00627-X
Milkowski, A., Garg, H., Couglin, J., Bryan, N. 2010. Nutritional epidemiology in the context of nitric oxide biology: Risk-Benefit evaluation for dietary nitrite and nitrate. Nitric Oxide, vol. 22, no. 2, p. 110-119. https://doi.org/10.1016/j.niox.2009.08.004
Millar, T. M., Stevens, C. R., Benjamin, N., Eisenthal, R., Harrison, R., Blake, D. R. 1998. Xanthine oxidoreductase catalyses the reduction of nitrates and nitrite to nitric oxide under hypoxic conditions. FEBS Letters, vol. 427, p. 225-228. https://doi.org/10.1016/s0014-5793(98)00430-x
Mondy, B. L., Keenan, T. W. 1993. Butyrophilin and xanthine oxidase occur in constant molar proportions in milk lipid globule membrane but vary in amount with breed and stage of lactation. Protoplasma, vol. 177, p. 32-36. https://doi.org/10.1007/BF01403396
Poje, M., Sokolić-Maravić, L. 1986. The Mechanism for the Conversion of Uric Acid into Allantoin and Dehydro-Allantoin. A New Look at an old Problem. Tetrahedron, vol. 42, no. 2, p. 747-751. https://doi.org/10.1016/S0040-4020(01)87480-9
Porras, A. G., Olson, J. S., Palmer, G. 1981. The reaction of reduced xanthine oxidase with oxygen. Kinetics of peroxide and superoxide formation. Journal of Biological Chemistry, vol. 256, no. 17, p. 9096-9103. https://doi.org/10.1016/S0021-9258(19)52513-3
Reynolds, J. D., Ahearn, G. S., Angelo, M., Zhang, J., Cobb, F., Stamler, J. S. 2007. S-nitrosohemoglobin deficiency: A mechanism for loss of physiological activity in banked blood. Proceedings of the National Academy of Sciences, vol. 104, no. 43, p. 17058-17062. https://doi.org/10.1073/pnas.0707958104
Rochette, L., Ghibu, S., Richard, C., Zeller, M., Cottin, Y., Vergely, C. 2013. Direct and indirect antioxidant properties of α-lipoic acid and therapeutic potential. Molecular Nutrition & Food Research, vol. 57, no. 1, p. 114-125. https://doi.org/10.1002/mnfr.201200608
Stsiapura, V. I., Bederman, I., Stepuro, I. I., Morozkina, T. S., Lewis, S. J., Smith, L., Gaston, B., Marozkina, N. 2018. S-Nitrosoglutathione formation at gastric pH is augmented by ascorbic acid and by the antioxidant vitamin complex. Resiston Journal Pharmaceutical Biology, vol. 56, no. 1, p. 86-93. https://doi.org/10.1080/13880209.2017.1421674
Suzuki, G., Okamoto, K., Kusano, T., Matsuda, Y., Fuse, A., Yokota, H. 2015. Evaluation of Neuronal Protective Effects of Xanthine Oxidoreductase Inhibitors on Severe Whole-brain Ischemia in Mouse Model and Analysis of Xanthine Oxidoreductase Activity in the Mouse Brain. Neurologia Medico-Chirurgica, vol. 55, no. 1, p. 7785. https://doi.org/10.2176/nmc.oa.2013-0307
Taibi, G., Nicotra, C. M. 2007. Xanthine oxidase catalyzes the oxidation of retinol. Journal of Enzyme Inhibition and Medicinal Chemistry, vol. 22, no. 4, p. 471-476. https://doi.org/10.1080/14756360701408739
Taibi, G., Paganini, A., Gueli, M. C., Ampola, F., Nicotra, C. M. 2001. Xanthine oxidase catalyzes the synthesis of retinoic acid. Journal of Enzyme Inhibition and Medicinal Chemistry, vol. 16, no. 3, p. 275-85. https://doi.org/10.1080/14756360109162376
Vogels, G., Van der Drift, C. 1970. Differential analyses of glyoxylate derivatives. Analytical Biochemistry, vol. 33, no. 1, p. 143-157. https://doi.org/10.1016/0003-2697(70)90448-3
Zhang, Z., Nauthon, D., Winyard, P. G., Benjamin, N. 1998. Generation of nitric oxide by a nitrite reductase activity of xanthine oxidase: a potential pathway for nitric oxide formation in the absence of nitric oxide synthase activity. Biochemical and Biophysical Research Communications, vol. 249, no. 3, p. 767-772. https://doi.org/10.1006/bbrc.1998.9226
How to Cite
Copyright (c) 2021 Potravinarstvo Slovak Journal of Food Sciences
This work is licensed under a Creative Commons Attribution 4.0 International License.Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).