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Lipopolysaccharide challenge of the mammary gland in cows induces nitrosative stress that impairs milk oxidative stability

Published online by Cambridge University Press:  23 February 2012

N. Silanikove ,
A. Rauch-Cohen ,
F. Shapiro ,
A. Arieli ,
U. Merin  and
G. Leitner
N. Silanikove*
Affiliation:
Biology of Lactation Laboratory, Institute of Animal Science, The Volcani Center, P.O. Box 6, Bet Dagan 50250, Israel
A. Rauch-Cohen
Affiliation:
Biology of Lactation Laboratory, Institute of Animal Science, The Volcani Center, P.O. Box 6, Bet Dagan 50250, Israel
F. Shapiro
Affiliation:
Biology of Lactation Laboratory, Institute of Animal Science, The Volcani Center, P.O. Box 6, Bet Dagan 50250, Israel
A. Arieli
Affiliation:
Department of Animal Science, Faculty of Agricultural, Food and Environmental Sciences, Hebrew University of Jerusalem, Rehovot 76-100, Israel
U. Merin
Affiliation:
Food Quality and Safety, Institute of Postharvest and Food Sciences, The Volcani Center, P.O. Box 6, Bet Dagan 50250, Israel
G. Leitner
Affiliation:
National Mastitis Reference Center, Kimron Veterinary Institute, Ministry of Agriculture and Rural Development, P.O. Box 12, Bet Dagan 50250, Israel
*
†E-mail: [email protected]
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Abstract

The aim of this work was to study the effects of mastitis induced by intramammary lipopolysaccharide (LPS) challenge on milk oxidative stability, as well as to understand the underlying biochemical processes that cause such changes. LPS challenge was associated with nitric oxide burst from the surrounding mammary epithelial cells and consequently induced nitrosative stress that was induced by the formation of NO2• from nitrite by lactoperoxidase. This response was associated with an ∼3-fold increased formation of hazardous compounds: nitrotyrosines, carbonyls and lipid peroxides. We sustained the involvement of xanthine oxidase as a major source of hydrogen peroxide. In consistent with previous findings, catalase has been shown to play a major role in modulating the nitrosative stress by oxidizing nitrite to nitrate. The current hygienic quality criteria cannot detect mixing of low-quality milk, such as milk with high somatic cells, and nitrite with high-quality milk. Thus, development of an improved quality control methodology may be important for the production of high-quality milk.

Keywords

milkcowmastitisNO and NO2•plasmin system
Type
Full Paper
Information
animal , Volume 6 , Issue 9 , September 2012 , pp. 1451 - 1459
Copyright
Copyright © The Animal Consortium 2012

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References

Ara, N, Iijima, K, Asanuma, K, Yoshitake, T, Ohara, S, Shimosegawa, T, Yoshimura, T 2008. Disruption of gastric barrier function by luminal nitrosative stress: a potential chemical insult to the human gastro-oesophageal junction. Gut 57, 306–313.Google Scholar
Boulanger, V, Bouchard, L, Zhao, X, Lacasse, P 2001. Induction of nitric oxide production by bovine mammary epithelial cells and blood leukocytes. Journal of Dairy Science 84, 1430–1437.CrossRefGoogle ScholarPubMed
Bruckmaier, RM 2005. Gene expression of factors related to the immune reaction in response to intramammary Escherichia coli lipopolysaccharide challenge. Journal of Dairy Research 72, 120–124.CrossRefGoogle Scholar
Drewnowski, IA, Fulgoni, V 2008. Nutrient profiling of foods: creating a nutrient-rich food index. Nutrition Review 66, 23–39.CrossRefGoogle ScholarPubMed
EEC Council Directive 94/71/EC 1994. Directive amending Directive 92/46/EC laying down the health rules for the production and placing on the market of raw milk, heat-treated milk and milk-based products. Official Journal of the European Community L368, 33–37.Google Scholar
Fridovich, I 1970. Quantitative aspects of the production of superoxide anion radical by milk xanthine oxidase. Journal of Biological Chemistry 245, 4053–4057.Google Scholar
Forsback, L, Lindmark-Mansson, H, Andren, A, Akerstedt, M, Svennersten-Sjaunja, K 2009. Udder quarter milk composition at different levels of somatic cell count in cow composite milk. Animal 3, 710–717.Google Scholar
Forsback, L, Lindmark-Mansson, H, Andren, A, Svennersten-Sjaunja, K 2010. Evaluation of quality changes in udder quarter milk from cows with low-to-moderate somatic cell counts. Animal 4, 617–626.CrossRefGoogle ScholarPubMed
Heumann, D, Roger, T 2002. Initial responses to endotoxins and Gram-negative bacteria. Clinical et Chimica Acta 323, 59–72.CrossRefGoogle ScholarPubMed
Ibeagha-Awemu, EM, Ibeagha, AE, Messier, S, Zhao, X 2010. Proteomics, genomics, and pathway analyses of Escherichia coli and Staphylococcus aureus infected milk whey reveal molecular pathways and networks involved in mastitis. Journal of Proteome Research 9, 4604–4619.CrossRefGoogle ScholarPubMed
Ito, H, Iijima, K, Ara, N, Asanuma, K, Endo, H, Asano, N, Koike, T, Abe, Y, Imatani, A, Shimosegawa, T 2010. Reactive nitrogen oxide species induce dilatation of the intercellular space of rat esophagus. Scandinavian Journal of Gastroenterology 45, 282–291.Google Scholar
Johnston, BD, DeMaster, EG 2003. Suppression of nitric oxide oxidation to nitrite by curcumin is due to the sequestration of the reaction intermediate nitrogen dioxide, not nitric oxide. Nitric Oxide-Biology and Chemistry 8, 231–234.Google Scholar
Jung, T, Engels, M, Klotz, LO, Kroncke, KD, Grune, T 2007. Nitrotyrosine and protein carbonyls are equally distributed in HT22 cells after nitrosative stress. Free Radical in Biology and Medicine 42, 773–786.CrossRefGoogle ScholarPubMed
Kelley, EE, Khoo, NKH, Hundley, NJ, Malik, UZ, Freeman, BA, Tarpey, MM 2010. Hydrogen peroxide is the major oxidant product of xanthine oxidase. Free Radical in Biology and Medicine 48, 493–498.CrossRefGoogle ScholarPubMed
Leitner, G, Chaffer, M, Shamay, A, Shapiro, F, Merin, U, Ezra, E, Saran, A, Silanikove, N 2004a. Changes in milk composition as affected by subclinical mastitis in sheep. Journal of Dairy Science 87, 46–52.CrossRefGoogle ScholarPubMed
Leitner, G, Merin, U, Silanikove, N 2004b. Changes in milk composition as affected by subclinical mastitis in goats. Journal of Dairy Science 87, 1719–1726.Google Scholar
Leitner, G, Merin, U, Silanikove, N, Ezra, E, Chaffer, M, Gollop, N, Winkler, M, Glikman, A, Saran, A 2004c. Effect of subclinical intramammary infection on somatic cell counts, NAGase activity and gross composition of goats’ milk. Journal of Dairy Research 71, 311–315.Google Scholar
Leitner, G, Krifucks, O, Merin, U, Lavi, U, Silanikove, N 2006. Interactions between bacteria type, proteolysis of casein and physico-chemical properties of bovine milk. International Dairy Journal 16, 648–654.CrossRefGoogle Scholar
Leitner, G, Silanikove, N, Jacobi, S, Weisblit, L, Bernstein, S, Merin, U 2008. The influence of storage on the farm and in dairy silos on milk quality for cheese production. International Dairy Journal 18, 109–113.CrossRefGoogle Scholar
Leitner, G, Merin, U, Silanikove, N 2011. Effects of glandular bacterial infection and stage of lactation on milk clotting parameters: comparison among cows, goats and sheep. International Dairy Journal 21, 279–285.CrossRefGoogle Scholar
McLaughlin, F 2006. A brief comparison of United States and European Union standards for fluid dairy production. Retrieved May 5, 2007, from http://www.iflr.msu.edu/uploads/files/109/Student%20Papers/A_Brief_Comparison_of_United_States_and_European_Union_Standards_for_Fluid_Dairy_Products.pdf Google Scholar
Merin, U, Fleminger, G, Komanovsky, J, Silanikove, N, Bernstein, S, Leitner, G 2008. Subclinical udder infection with Streptococcus dysgalactiae impairs milk coagulation, properties: the emerging role of proteose-petones. Dairy Science and Technology 88, 407–419.CrossRefGoogle Scholar
Milkowski, A, Garg, HK, Coughlin, JR, Bryan, NS 2010. Nutritional epidemiology in the context of nitric oxide biology: a risk-benefit evaluation for dietary nitrite and nitrate. Nitric Oxide-Biology and Chemistry 22, 110–119.Google Scholar
Moussaoui, F, Michelutti, I, Le Roux, Y, Laurent, F 2002. Mechanisms involved in milk endogenous proteolysis induced by a lipopolysaccharide experimental mastitis. Journal of Dairy Science 85, 2562–2570.Google Scholar
Oliveira, CAF, Fernandes, AM, Neto, OCC, Fonseca, LFL, Silva, EOT, Balian, SC 2002. Composition and sensory evaluation of whole yogurt produced from milk with different somatic cell counts. Australian Journal of Dairy Technology 57, 192–196.Google Scholar
Ohshima, H, Tatemichi, M, Sawa, T 2003. Chemical basis of inflammation-induced carcinogenesis. Archives of Biochemistry and Biophysics 417, 3–11.Google Scholar
PMO 2007. Grade “A” pasteurized milk ordinance. US Department of Health and Human Services, Public Health Service, Food and Drug Administration, Washington, DC, USA.Google Scholar
Rainard, P, Riollet, C 2006. Innate immunity of the bovine mammary gland. Veterinary Research 37, 369–400.Google Scholar
Rossi, L, Galante, F, Fusi, E, Luini, M, Dell'Orto, V, Baldi, A 2009. Evaluation the of PL–PG–PA system in relation to quality of bovine milk. Veterinary Research Communications 33, S293–S295.Google Scholar
Sala, A, Nicolis, S, Roncone, R, Casella, L, Monzani, E 2004. Peroxidase catalyzed nitration of tryptophan derivatives – mechanism, products and comparison with chemical nitrating agents. European Journal of Biochemistry 271, 2841–2852.CrossRefGoogle ScholarPubMed
SAS Institute 1990. SAS/STAT user's guide, version 6, 4th edition, vol. 2. SAS Institute Inc., Cary, NC, USA.Google Scholar
Seraphim, KR, Bastos De Siqueira, MEP, Galego, G, de Fernicola, NA 1988. Nitrates and nitrites in crude and pasteurized milk commercialized in the Alfena's City, Minas Gerais, Brazil. Alimentaria 35, 49–52.Google Scholar
Shamay, A, Shapiro, F, Mabjees, SJ, Silanikove, N 2002. Casein-derived phosphopeptides disrupt tight junction integrity, and precipitously dry up milk secretion in goats. Life Sciences 70, 2707–2719.Google Scholar
Shamay, A, Shapiro, F, Leitner, G, Silanikove, N 2003. Infusions of casein hydrolyzates into the mammary gland disrupt tight junction integrity and induce involution in cows. Journal of Dairy Science 86, 1250–1258.Google Scholar
Shamay, A, Homans, R, Fuerman, Y, Levin, I, Barash, H, Silanikove, N, Mabjeesh, SJ 2005. Expression of albumin in nonhepatic tissues and its synthesis by the bovine mammary gland. Journal of Dairy Science 88, 569–576.Google Scholar
Silanikove, N, Shapiro, F 2007. Distribution of xanthine oxidase and xanthine dehydrogenase activity in bovine milk: physiological and technological implications. International Dairy Journal 17, 1188–1194.CrossRefGoogle Scholar
Silanikove, N, Merin, U, Leitner, G 2006. Physiological role of indigenous milk enzymes: an overview of an evolving picture. International Dairy Journal 16, 533–545.Google Scholar
Silanikove, N, Shapiro, F, Leitner, G 2007. Posttranslational ruling of xanthine oxidase activity in bovine milk by its substrates. Biochemical and Biophysical Research Communications 363, 561–565.Google Scholar
Silanikove, N, Shamay, A, Shinder, D, Moran, A 2000. Stress down regulates milk yield in cows by plasmin induced β-casein product that blocks K+ channels on the apical membranes. Life Sciences 67, 2201–2212.Google Scholar
Silanikove, N, Shapiro, F, Shamay, A, Leitner, G 2005. Role of xanthine oxidase, lactoperoxidase, and NO in the innate immune system of mammary secretion during active involution in dairy cows: manipulation with casein hydrolysates. Free Radical in Biology and Medicine 38, 1139–1151.Google Scholar
Silanikove, N, Shapiro, F, Shinder, D 2009a. Acute heat stress brings down milk secretion in dairy cows by up-regulating the activity of the milk-borne negative feedback regulatory system. BMC Physiology 9, 13.Google Scholar
Silanikove, N, Shapiro, F, Silanikove, M, Merin, U, Leitner, G 2009b. Hydrogen peroxide-dependent conversion of nitrite to nitrate as a crucial feature of bovine milk catalase. Journal of Agriculture and Food Chemistry 57, 8018–8025.CrossRefGoogle ScholarPubMed
Silanikove, N, Leitner, G, Merin, U, Prosser, GC 2010. Recent advances in exploiting goat's milk: quality, safety and production aspects. Small Ruminant Research 89, 110–124.CrossRefGoogle Scholar
Silanikove, N, Rauch-Cohen, A, Shapiro, F, Blum, S, Arieli, A, Leitner, G 2011. Lipopolysaccharide challenge of the mammary gland in bovine induced a transient glandular shift to anaerobic metabolism. Journal of Dairy Science 94, 4468–4475.Google Scholar
Titov, V Yu, Kosenko, OV, Fisinin, VI, Klimov, NT 2010. Content of nitric oxide metabolites in cow milk in health and mastitis. Russian Journal of Agricultural Science 36, 288–290.Google Scholar
Zheng, JM, Watson, AD, Kerr, DE 2006. Genome-wide expression analysis of lipopolysaccharide-induced mastitis in a mouse model. Infection and Immunity 74, 1907–1915.Google Scholar