The Efficacy of Stabilizers on Lactoperoxidase System’s Antibacterial Activity and Stability: A Review

Document Type : Research Paper

Authors

1 Department of Biology, Faculty of Sciences, University of Guilan, Rasht, Iran.

2 Department of Biochemistry, Falavarjan Branch, Islamic Azad University, Isfahan, Iran

3 Department of Microbiology, Falavarjan Branch, Islamic Azad University, Isfahan, Iran.

Abstract

The lactoperoxidase System holds significant prominence as a pivotal protein within milk, assuming a defensive role in combating diverse strains of microorganisms, particularly those with deleterious implications for milk quality. The stabilization process of the lactoperoxidase enzyme offers numerous advantages and benefits within an academic context and allows for controlled modulation of the enzyme's effects. Stabilized enzymes have attracted considerable research attention due to their favorable attributes, including easy separation from reaction mixtures, and the potential for reusing enzymes from multiple sources, to find and improve valuable methodologies. This review summarized the role of stabilizers in enhancing the efficacy and stability of the lactoperoxidase system and antibacterial applications in cosmetics, pharmaceutical, food, and health industries. This enzyme possesses characteristics that make it an effective natural antibacterial agent, leading to the extension of the lifespan and improvement of the stability of diverse types of dairy products and milk. It is used especially in remote areas where farmers are not close to the market. The common findings confirmed the ability of stabilizers to enhance enzyme stability in unfavorable environmental conditions that result in the extension of the activity period of the enzyme. Therefore, this characteristic indirectly enhances the enzyme's remarkable effectiveness against bacteria. Finally, according to various studies, the main function of stabilizing agents is the enhancement of enzyme stability as well as the longevity of the enzyme. Overall, it seems the stabilizers have a supplementary function in improving the enzyme's ability to kill bacteria through increased enzymatic activity.

Keywords

Main Subjects

References

Al-Baarri, A.N., Damayanti, N.T., Legowo, A.M., Tekiner, İ.H., Hayakawa, S. (2019). Enhanced Antibacterial Activity of Lactoperoxidase-Thiocyanate-Hydrogen Peroxide System in Reduced-Lactose Milk Whey. International Journal of Food Science, 2019, 8013402. doi: 10.1155/2019/8013402.
Al-Baarri, A. N. M., Damayanti, N. T., Legowo, A. M., Tekiner, İ. H., & Hayakawa, S. (2019). Enhanced antibacterial activity of lactoperoxidase–thiocyanatehydrogen peroxide system in reduced-lactose milk whey. International Journal of Food Science, 2019 https://doi.org/10.1155/2019/8013402
Al-Baarri, A., Agawa, M., Hayakawa, S. (2010). Scaleup studies on immobilization of lactoperoxidase using milk whey for producing antimicrobial agent. Journal of the Indonesian Tropical Animal Agriculture, 35(3),185-91. https://doi.org/10.14710/jitaa.35.3.185-191
Akbari, E., Beheshti-Maal, K., & Nayeri, H. (2016). Production and optimization of alkaline lipase by a novel psychrotolerant and halotolerant strain Planomicrobium okeanokoites ABN-IAUF-2 isolated from Persian Gulf. International Journal of Medical Research and Health Sciences, 5(4), 139-48.
Akbari, E., Beheshti-Maal, K., & Nayeri, H. (2018). A novel halo-alkalo-tolerant bacterium, Marinobacter alkaliphilus ABN-IAUF-1, isolated from Persian Gulf suitable for alkaline lipase production. International Journal of Environmental Science and Technology, 15, 1767-1776. https://doi.org/10.1007/s13762-017-1503-z
Althaus, R.L., Molina, M.P., Rodríguez, M., Fernández, N. (2001). Analysis time and lactation stage influence on lactoperoxidase system components in dairy ewe milk. Journal of Dairy Science 84(8),1829-35. https://doi.org/10.3168/jds.S0022-0302(01)74622-X
Amiri Fahliyani, S., Beheshti Maal, K., Ghandehari, F. (2020). Isolation and identification of bovine mastitis producing bacteria in dairy cows in Isfahan city. Applied Biology, 32(4), 9-22. doi: 10.22051/jab.2020.4650
Babadaie Samani, N., Nayeri, H., & Amiri, G. A. (2016). Effects of cadmium chloride as inhibitor on stability and kinetics of immobilized Lactoperoxidase (LPO) on silica-coated magnetite nanoparticles versus free LPO. Nanomedicine Journal, 3(4), 230-239. Doi:10.22038/nmj.2016.7579
Bafort, F., Parisi, O., Perraudin, J.P., Jijakli, M.H. (2014). Mode of Action of lactoperoxidase as related to its antimicrobial activity: a review. Enzyme Research, 2014, 517164. https://doi.org/10.1155/2014/517164
Barrett, N.E., Grandison, A.S., Lewis, M.J. (1999). Contribution of the lactoperoxidase system to the keeping quality of pasteurized milk. Journal of Dairy Research, 66(1),73-80. https://doi.org/10.1017/S0022029998003252
Beheshti-Maal, K., Emtiazi, G., & Nahvi, I. (2009). Production of alkaline protease by Bacillus cereus and Bacillus polymixa in new industrial culture mediums and its immobilization. African Journal of Microbiology Research, 3(9), 491-497.
Beheshti-Maal, K., Emtiazi, G., & Nahvi, I. (2011). Increasing the alkaline protease activity of Bacillus cereus and Bacillus polymyxa simultaneously with the start of sporulation phase as a defense mechanism. African Journal of Biotechnology, 10(19), 3894-3901.
Benkerroum, N. (2008). Antimicrobial activity of lysozyme with special relevance to milk. African Journal of Biotechnology, 7, 4856–4867.
Björck, L., Rosen, C., Marshall, V., Reiter, B. (1975). Antibacterial activity of the lactoperoxidase system in milk against pseudomonads and other gram-negative bacteria. Applied Microbiology, 30(2),199-204. https://doi.org/10.1128/am.30.2.199-204.1975
Björck, L. (1978). Antibacterial effect of the lactoperoxidase system on psychrotrophic bacteria in milk. Journal of Dairy Research, 45(1), 109-118. https://doi.org/10.1017/S0022029900016253
Borjian-Boroujeni, M., Nayeri, H. (2021). Interaction of bovine lactoperoxidase with hydroxyectoine: stabilizing effect study. Biologia, 76, 1285–1296. DOI: 10.2478/s11756-020-00674-w
Borjian-Boroujeni, M., Nayeri, H. (2018). Stabilization of bovine lactoperoxidase in the presence of ectoine. Food Chemistry, 265, 208-215. doi: 10.1016/j.foodchem.2018.05.067.
Bostock, M.P., Prasad, A.R., Chaouni, R., Yuen, A.C., Sousa-Nunes, R., Amoyel, M., et al. (2020). An immobilization technique for long-term time-lapse imaging of explanted Drosophila tissues. Frontiers in Cell and Developmental Biology, 8,1074. doi.org/10.3389/fcell.2020.590094
Cankaya, M., Sişecioğlu, M., Bariş, O., Güllüce, M., Ozdemir, H. (2010). Effects of bovine milk lactoperoxidase system on some bacteria. Applied Biochemistry and Microbiology, 46, 57-60. https://doi.org/10.1134/S0003683810010096
Cass, A., Cass, T., Ligler, F.S. (1998). Immobilized biomolecules in Analysis: A Practical Approach: Practical Approach, 198, Oxford University Press
Claeys, W.L., Cardoen, S., Daube, G., De Block, J., Dewettinck, K., Dierick, K., et al. (2013). Raw or heated cow milk consumption: Review of risks and benefits. Food control, 31(1),251-62. https://doi.org/10.1016/j.foodcont.2012.09.035
Contesini, FJ, de Alencar Figueira, J, Kawaguti, HY, de Barros Fernandes, PC, de Oliveira Carvalho, P, da Graça Nascimento, M, et al. (2013). Potential applications of carbohydrases immobilization in the food industry. International Journal of Molecular Sciences,14(1),1335-69. https://doi.org/10.3390/ijms14011335
Cooper, R.A. (2013). Inhibition of biofilms by glucose oxidase, lactoperoxidase and guaiacol: the active antibacterial component in an enzyme alginogel. International Wound Journal, 10(6),630-7. https://doi.org/10.1111/iwj.12083
Dawoodi, E., Beheshtimaal, K., Nayeri, H. (2015). Screening of Alkaline Protease-Producing Streptomyces diastaticus and Optimization of Enzyme Production. Iranian Journal of Medical Microbiology, 8(4) ,50-58.
Ebrahimi, A., Moosavy, M.H., Khatibi, S.A., Barabadi, Z., Hajibemani, A. (2021). A comparative study of the antibacterial properties of milk from different domestic animals. International Journal of Dairy Technology,74(2),425-30. 0307.12757. https://doi.org/10.1111/1471
Ehsani, A., Hashemi, M., Afshari, A., Aminzare, M., Raeisi, M., Zeinali, T. (2020). Effect of different types of active biodegradable films containing lactoperoxidase system or sage essential oil on the shelf life of fish burger during refrigerated storage. LWT, 117,108633. doi: 10.1016/j.lwt.2019.108633
Emtiazi, G., Nahvi, I., & Beheshti-Maal, K. (2005). Production and immobilization of alkaline protease by Bacillus polymyxa which degrades various proteins. International Journal of Environmental Studies, 62(1), 101107. https://doi.org/10.1080/0020723042000261722
Ericsno, T., Bratt, P. (1987). Interactions between peroxide and salivary glycoprotein: protection by peroxidase. Journal Medicine,16(8),421-4. 0714.1987.tb02079.x of Oral Pathology & https://doi.org/10.1111/j.1600
Fernandes, P., Marques, M.P., Carvalho, F., Cabral, J.M. (2009). A simple method for biocatalyst immobilization using PVA‐based hydrogel particles. Journal of Chemical Technology & Biotechnology: International Research in Process, Environmental & Clean Technology,84(4),561-4. https://doi.org/10.1002/jctb.2080
Fuglsang, C. C., Johansen, C., Christgau, S., & Adler-Nissen, J. (1995). Antimicrobial enzymes: applications and future potential in the food industry. Trends in Food Science & Technology, 6(12), 390-396. https://doi.org/10.1016/S0924-2244(00)89217-1
Giansanti, F., Panella, G., Leboffe, L., Antonini, G. (2016). Lactoferrin from milk: Nutraceutical and pharmacological properties. Pharmaceuticals,9(4),61. https://doi.org/10.3390/ph9040061
Gruden, Š., Oberčkal, J., Matijašić, B. B., & Ulrih, N. P. (2023). Insights into factors affecting lactoperoxidase conformation stability and enzymatic activity. International Dairy Journal, 138, https://doi.org/10.1016/j.idairyj.2022.105537 105537.
Guisan, J. M. (Ed.). (2006). Immobilization of enzymes and cells (Vol. 22). Totowa, NJ: Humana Press.
Gupta, C., Prakash, D. (2017). Therapeutic Potential of Whey. Beverages, 3(3),31. https://doi.org/10.3390/beverages3030031
Hancock, J.T., Salisbury, V., Ovejero-Boglione, M.C., Cherry, R., Hoare, C., Eisenthal, R., et al. (2002). Antimicrobial properties of milk: dependence on presence of xanthine oxidase and nitrite. Antimicrobial Agents and Chemotherapy,46(10),3308-3310. https://doi.org/10.1128/aac.46.10.3308-3310.2002
Jooyandeh, H., Aberoumand, A., & Nasehi, B. (2011). Application of lactoperoxidase system in fish and food products: a review. American-Eurasian Journal of Agricultural & Environmental Sciences, 10, 89-96.
Köksal, Z., Alim, Z. (2020). Lactoperoxidase, an antimicrobial enzyme, is inhibited by some indazoles. Drug and Chemical Toxicology,43(1),22-6. https://doi.org/10.1080/01480545.2018.148886135 M
Koksal, Z., Gulcin, I., & Ozdemir, H. (2016). An important milk enzyme: lactoperoxidase. Milk proteins-from structure to biological properties and health aspects, 141-156., https://dox.doi.org/ 10.5772/64416
Koksal, Z., Kalin, R., Kalin, P., Karaman, M., Gulcin, İ., & Ozdemir, H. (2020). Lactoperoxidase inhibition of some natural phenolic compounds: Kinetics and molecular docking studies. Journal of food Biochemistry, 44(2), e13132. https://doi.org/10.1111/jfbc.13132 of food
Król, J., Litwinczuk, Z., Brodziak, A., & Barlowska, J. (2010). Lactoferrin, lysozyme and immunoglobulin G content in milk of four breeds of cows managed under intensive production system. Polish Journal of Veterinary Sciences, 13(2), 357-361.
Kussendrager, K.D., van Hooijdonk, A.C. (2000). Lactoperoxidase: Physico-chemical properties, occurrence, mechanism of action and applications. British Journal of Nutrition, 84(S. 1), https://doi.org/10.1017/S0007114500002208 19–25.
Lee, H., & Min, S. C. (2013). Antimicrobial edible defatted soybean meal-based films incorporating the lactoperoxidase system. LWT-Food Science and Technology, 54(1), 42-50.https://doi.org/10.1016/j.lwt.2013.05.012
León-López, A., Pérez-Marroquín, X. A., Estrada-Fernández, A. G., Campos-Lozada, G., Morales-Peñaloza, A., Campos-Montiel, R. G., & Aguirre-Álvarez, G. (2022). Milk whey hydrolysates as high value-added natural polymers: Functional properties and applications. Polymers, 14(6), 1258. https://doi.org/10.3390/polym14061258
Lotfi, M., Beheshti-Maal, K., & Nayeri, H. (2015). Evaluation of alkaline protease production and optimization of culture medium by Yarrowia lipolytica. Biological Journal of Microorganism, 4(14), 61-70. Lotfi, M, Beheshti-Maal, K, Nayeri, H. (2014). Isolation, identification and optimization of alkaline protease production by Candida viswanathii. Iranian Journal of Medical Microbiology,7 (4),36-42.
Magacz, M., Alatorre-Santamaría, S., Kędziora, K., Klasa, K., Mamica, P., Pepasińska, W., & Krzyściak, W. (2023). Modified Lactoperoxidase System as a Promising Anticaries Agent: In Vitro Studies on Streptococcus mutans Biofilms. International Journal of Molecular Sciences, 24(15), 12136. https://doi.org/10.3390/ijms241512136
Magacz, M., Kędziora, K., Sapa, J., Krzyściak, W. (2019). The Significance of Lactoperoxidase System in Oral Health: Application and Efficacy in Oral Hygiene Products. International Journal of Molecular Sciences, 20 (6),1443. https://doi.org/10.3390/ijms20061443
Marangoni, F., Pellegrino, L., Verduci, E., Ghiselli, A., Bernabei, R., Calvani, R., Cetin, I., Giampietro, M., Perticone, F., Piretta, L., et al. (2019). Cow’s milk consumption and health: A health professional’s guide. Journal of the American College of Nutrition, 38,197-208.
Min, S., Harris, L.J., Krochta, J.M. (2005). Antimicrobial effects of lactoferrin, and the lactoperoxidase system and edible whey protein films incorporating the lactoperoxidase system against Salmonella enterica and Escherichia coli O157: H7. Journal of Food Science, 70(2):m332-m338. https://doi.org/10.1111/j.13652621.2005.tb11476.x
Miroliaei, M., Nayeri, H., Samsam-Shariat, S.Z., Atar, M. (2007). 'Biospecific Immobilization of Lactoperoxidase on Con A-Sepharose 4B', Scientia Iranica, 14(4), 303-307.
Min, S., Harris, L.J., Krochta, J.M. (2005a). Listeria monocytogenes inhibition by whey protein films and coatings incorporating the lactoperoxidase system. Journal of Food Science, 70(7), m317-m324. https://doi.org/10.1111/j.1365-2621.2005.tb11474.x
Mohamad, N.R., Marzuki, N.H.C., Buang, N.A., Huyop, F, Wahab, R.A. (2015). An overview of technologies for immobilization of enzymes and surface analysis techniques for immobilized enzymes. Biotechnology & Biotechnological Equipment,29(2),20520. https://doi.org/10.1080/13102818.2015.1008192
Molayi, R., Ehsani, A, Yousefi, M. (2018). The antibacterial effect of whey protein–alginate coating incorporated with the lactoperoxidase system on chicken thigh meat. Food Science & Nutrition, 6,878–83. https://doi.org/10.1002/fsn3.634
Munsch-Alatossava, P., Gursoy, O., Lorilla, P. M., Gauchi, J. P., & Alatossava, T. (2018). Antibacterial effects and modes of action of the activated lactoperoxidase system (LPS), of CO2 and N2 gas as food-grade approaches to control bovine raw milk–associated bacteria. In Food Control and Biosecurity (pp. 519-541). Academic Press. https://doi.org/10.1016/B978-0-12-811445-2.00015-5
Nayeri, H., Fattahi, A., Iranpoor-mobarakeh, M., Nori, P. (2015). Stabilization of lactoperoxidase by tragacanthchitosan nano biopolymer. International Journal of Biosciences, 6(2). http://dx.doi.org/10.12692/ijb/6.2.418-426 418-426.
Nunes, M.A., Vila-Real, H., Fernandes, P.C., Ribeiro, M.H. (2010). Immobilization of naringinase in PVAalginate matrix using an innovative technique. Applied Biochemistry and Biotechnology,160(7),2129-47. https://doi.org/10.1007/s12010-009-8733-6
Jafari, F., Kashanian, S., Samsam Sharieat, S.Z. (2013). Purification, immobilization, and characterization of bovine lactoperoxidase. International Journal of Food Properties,16(4),905-16. https://doi.org/10.1080/10942912.2011.566400
Jayaram, P. N., Roy, G., & Mugesh, G. (2008). Effect of thione—thiol tautomerism on the inhibition of lactoperoxidase by anti-thyroid drugs and their analogues. Journal of Chemical Sciences, 120(1), 143-154.https://doi.org/10.1007/s12039-008-0017-0 143-154.
Pellegrino, L., Marangoni, F., Muscogiuri, G., D’Incecco, P., Duval, G. T., Annweiler, C., & Colao, A. (2021). Vitamin D fortification of consumption cow’s milk: Health, nutritional and technological aspects. A multidisciplinary lecture of the recent scientific evidence. Molecules, 26(17), 5289. https://doi.org/10.3390/molecules26175289
Puspitarini, O. R., Al-Baarri, A. N., Legowo, A. M., Bintoro, P., & Hintono, A. (2013). The activation method of LPs to inhibit microbial activity in fresh milk. Animal Production, 15(2), 119–126.
Rostami, H., Abbaszadeh, S., Shokri, S. (2017). Combined effects of lactoperoxidase system-whey protein coating and modified atmosphere packaging on the microbiological, chemical and sensory attributes of PikePerch fillets. Journal of Food Science and Technology, 54,3243–50. https://doi.org/10.1007/s13197-017-2767-5
Saravani, M., Ehsani, A., Aliakbarlu, J., Ghasempour, Z. Gouda cheese spoilage prevention: biodegradable coating induced by Bunium persicum essential oil and lactoperoxidase system. Food Science & Nutrition, 7(3), 959-968. https://doi.org/10.1002/fsn3.888
Sarikaya, S.B.O., Sisecioglu, M., Cankaya, M., Gulcin, İ., Ozdemir, H. (2015). Inhibition profile of a series of phenolic acids on bovine lactoperoxidase enzyme. Journal of Enzyme Inhibition and Medicinal Chemistry, 30(3),479-83. https://doi.org/10.3109/14756366.2014.949254
Samsam Shariat, S.Z.A.S., Borzouee, F., Mofid, M.R., Varshosaz, J. (2018). Immobilization of lactoperoxidase on graphene oxide nanosheets with improved activity and stability. Biotechnology Letters,40(9),1343-53. https://doi.org/10.1007/s10529-018-2583-7
Seifu, E., Buys, E. M., & Donkin, E. F. (2005). Significance of the lactoperoxidase system in the dairy industry and its potential applications: a review. Trends in Food Science & Technology, 16(4), 137-154. https://doi.org/10.1016/j.tifs.2004.11.002
Sheikh, I.A., Yasir, M., Khan, I., Khan, S.B., Azum, N., E.H., et al. (2018). Lactoperoxidase immobilization on silver nanoparticles enhances its antimicrobial activity. Journal of Dairy Research, 85(4), 460-4. https://doi.org/10.1017/S0022029918000730
Silva, E., Oliveira, J., Silva, Y., Urbano, S., Sales, D., Moraes, E., et al. (2020). Lactoperoxidase system in the dairy industry: challenges and opportunities. Czech Journal of Food Sciences, 38,337–46.
doi: 10.17221/103/2020CJFS
Sisecioglu, M., Kirecci, E., Cankaya, M., Ozdemir, H., Gulcin, I., Atasever, A. (2010). The prohibitive effect of lactoperoxidase system (LPS) on some pathogen fungi and bacteria. African Journal Pharmacology, 4(9), 671-677.
Thallinger, B., Argirova, M., Lesseva, M., Ludwig, R., Sygmund, C., Schlick, A., et al. (2014). Preventing microbial colonisation of catheters: antimicrobial and antibiofilm activities of cellobiose dehydrogenase. International Journal of Antimicrobial Agents, 44,402–8. https://doi.org/10.1016/j.ijantimicag.2014.06.016
Tiwari, B.K., Valdramidis, V.P., O'Donnell, C.P., Muthukumarappan, K., Bourke, P., Cullen, P.J. (2009). Application of natural antimicrobials for food preservation. Journal Of Agricultural and Food Chemistry, 57(14),59876000. https://doi.org/10.1021/jf900668n.
Urtasun, N., Baieli, M.F., Hirsch, D.B., MartínezCeron, M.C., Cascone, O. & Wolman, F.J. (2017). Lactoperoxidase purification from whey by using dye affinity chromatography. Processing,103,58-65. Food and Bioproducts https://doi.org/10.1016/j.fbp.2017.02.011
Villa, V.Y., Legowo, A.M., Priyo Bintoro, V. & AlBaarri, A.N. (2014). Quality of Fresh Bovine Milk after Addition of Hypothiocyanite-rich-solution from Lactoperoxidase System. International Journal of Dairy Science, 9(1),24-31. DOI: 10.3923/ijds.2014.24.31
Welk, A., Patjek, S., Gärtner, M., Baguhl, R., Schwahn, C., & Below, H. (2021). Antibacterial and antiplaque efficacy of a lactoperoxidase-thiocyanatehydrogen-peroxide-system-containing lozenge. BMC Microbiology, 21, 1-12. https://doi.org/10.1186/s12866021-02333-9
Wolfson, L. M., & Sumner, S. S. (1993). Antibacterial activity of the lactoperoxidase system: a review. Journal of Food Protection, 56(10), https://doi.org/10.4315/0362-028X-56.10.887 887-892.
Woźniak, D., Cichy, W., Dobrzyńska, M., Przysławski, J., & Drzymała-Czyż, S. (2022). Reasonableness of enriching cow’s milk with vitamins and minerals. Foods, 11(8), 1079.
https://doi.org/10.3390/foods11081079 11(8),1079.
Yener, F.Y., Korel, F. & Yemenicioglu, A. (2009). Antimicrobial activity of lactoperoxidase system incorporated into cross-linked alginate films. Journal of Food Science,74, M73–M79. https://doi.org/10.1111/j.1750-3841.2009.01057.x
Yousefi, M., Farshidi, M.  & Ehsani, A. (2018). Effects of lactoperoxidase system-alginate coating on chemical, microbial, and sensory properties of chicken breast fillets during cold storage. Journal of Food Safety, 38, e12449. https://doi.org/10.1111/jfs.12449
Yousefi, M., Nematollahi, A., Shadnoush, M., Mortazavian, A.M. & Khorshidian, N. (2022). Antimicrobial Activity of Films and Coatings Containing Lactoperoxidase System: A Review. Frontiers in Nutrition, 9,828065. https://doi.org/10.3389/fnut.2022.828065
Zhou, Y. & Lim, L.T. (2009). Activation of lactoperoxidase system in milk by glucose oxidase immobilized in electrospun polylactide microfibers. Journal of Food Science, 74(2), C170-C176. https://doi.org/10.1111/j.1750-3841.2009.01071.x
Microbiology, Metabolites and Biotechnology
Volume 6, Issue 2
November 2023
Pages 17-36

Files

Share

How to cite

Statistics