The effect of antioxidants on xanthine oxidase activity in fresh ovine milk

Authors

  • Akmaral Mukhamejanova L. N. Gumilyov Eurasian National University, Department of Biotechnology and Microbiology, Kazhymukan Str., 5, 010008, Nur-Sultan, Republic of Kazakhstan, Tel.: +77172709500 https://orcid.org/0000-0001-9611-3269
  • Zerekbay Alikulov L. N. Gumilyov Eurasian National University, Department of Biotechnology and Microbiology, Kazhymukan Str., 5, 010008, Nur-Sultan, Republic of Kazakhstan, Tel.: + 77172709457
  • Nelya Shapekova L. N. Gumilyov Eurasian National University, Department of Biotechnology and Microbiology, Kazhymukan Str., 5, 010008, Nur-Sultan, Republic of Kazakhstan, Tel.: +77172709483
  • Karlygash Aubakirova L. N. Gumilyov Eurasian National University, Department of Biotechnology and Microbiology, Kazhymukan Str., 5, 010008, Nur-Sultan, Republic of Kazakhstan, Tel.: + 77172708488
  • Abilkhas Mukhtarov L. N. Gumilyov Eurasian National University, Department of Biotechnology and Microbiology, Kazhymukan Str., 5, 010008, Nur-Sultan, Republic of Kazakhstan, Tel.: +77172709512

DOI:

https://doi.org/10.5219/1662

Keywords:

antioxidant, molybdenum, tungsten, phospholipids, nitrate, nitrite

Abstract

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.

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References

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

Published

2021-07-12

How to Cite

Mukhamejanova, A., Alikulov, Z., Shapekova, N., Aubakirova, K., & Mukhtarov, A. (2021). The effect of antioxidants on xanthine oxidase activity in fresh ovine milk. Potravinarstvo Slovak Journal of Food Sciences, 15, 599–607. https://doi.org/10.5219/1662