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Mammary immunity of White Park and Highland cattle compared with Brown Swiss and Red Holstein

Published online by Cambridge University Press:  04 April 2013

D. Sorg ,
E. Fandrey ,
K. Frölich ,
H.H.D. Meyer  and
H. Kliem
D. Sorg
Affiliation:
Physiology Weihenstephan, Technische Universität München, Freising, Germany ZIEL – Research Center for Nutrition and Food Sciences, Technische Universität München, Freising, Germany
E. Fandrey
Affiliation:
Arche Warder, Zentrum für alte Haus- und Nutztierrassen e.V, Warder, Germany
K. Frölich
Affiliation:
Arche Warder, Zentrum für alte Haus- und Nutztierrassen e.V, Warder, Germany
H.H.D. Meyer
Affiliation:
Physiology Weihenstephan, Technische Universität München, Freising, Germany ZIEL – Research Center for Nutrition and Food Sciences, Technische Universität München, Freising, Germany
H. Kliem*
Affiliation:
Physiology Weihenstephan, Technische Universität München, Freising, Germany ZIEL – Research Center for Nutrition and Food Sciences, Technische Universität München, Freising, Germany
*
Correspondence to: H. Kliem, Physiology Weihenstephan, Technische Universität München, Freising, Germany. email: [email protected]
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Summary

Mastitis is a frequent disease in modern dairy cows, but ancient cattle breeds seem to be naturally more resistant to it. Primary bovine mammary epithelial cells from the ancient Highland and White Park (n = 5) cattle and the modern dairy breeds Brown Swiss and Red Holstein (n = 6) were non-invasively isolated from milk, cultured, and stimulated with the heat-inactivated mastitis pathogens Escherichia coli and Staphylococcus aureus to compare the innate immune response in vitro. With reverse transcription quantitative polymerase chain reaction (RT-qPCR), the breeds differed in the basal expression of 16 genes. Notably CASP8, CXCL8, Toll-like receptors 2 and 4 (TLR2 and TLR4) expression were higher in the ancient breeds (P < 0.05). In the modern breeds, more genes were regulated after stimulation. Breed differences (P < 0.05) were detected in C3, CASP8, CCL2, CD14, LY96 and transforming growth factor β1 (TGFβ1) regulation. Principal component analysis separated the ancient from the modern breeds in their basal expression, but not after stimulation. ELISA of lactoferrin and serum amyloid A protein revealed breed differences in control and S. aureus treated levels. The immune reaction of ancient breeds seemed less intensive because of a higher basal expression, which has been shown before to be beneficial for the animal. For the first time, the innate immune response of these ancient breeds was studied. Previous evidence of breed and animal variation in innate immunity was confirmed.

Résumé

La mastite est une maladie fréquente chez les vaches laitières modernes. Or, les races bovines anciennes semblent être naturellement plus résistantes. Dans le présent travail, des cellules primaires bovines épithéliales mammaires des races anciennes Highland et White Park (n = 5), ainsi que des races laitières modernes Brown Swiss et Red Holstein (n = 6) ont été isolées du lait de façon non-invasive. Ensuite, elles ont été cultivées, puis stimulées avec les pathogènes de la mastite Escherichia coli et Staphylocoque doré – tous les deux préalablement inactivés par la chaleur – pour ainsi comparer la réponse immunitaire innée in vitro, utilisant la technique reverse transcription quantitative polymerase chain reaction (RT-qPCR). Il s'avère que les races diffèrent dans l'expression basale de 16 gènes. Notamment, les expressions de CASP8, CXCL8, TLR2 et TLR4 étaient élevées dans les races anciennes (P < 0.05). Dans les races modernes, c'est le nombre global des gènes régulés après stimulation qui était plus élevé. Des différences entre les races (P < 0.05) ont été détectées quant à la régulation de C3, CASP8, CCL2, CD14, LY96 et TGFβ1. L'analyse des composantes principales a permis de cloisonner les races anciennes des races modernes dans l'expression basale, mais pas après stimulation. Les mesures ELISA de lactoferrin et de sérum amyloïde A protéine ont dévoilé des différences interraciales entre le groupe du contrôle et du groupe Staphylocoque doré. Dans son ensemble, la réaction immunitaire de races anciennes apparaissait moins intensive en fonction d'une expression basale plus grande. Une telle atténuation avait préalablement été décrite comme étant bénéfique pour l'animal. Pour la première fois la réponse immunitaire innée de ces races anciennes a été étudiée ici. De précédentes preuves de la variation interraciale, ainsi qu'inter-animale, ont pu être confirmées par le présent travail.

Resumen

La mastitis es una enfermedad de gran incidencia en ganado bovino moderno destinado a producción lechera. Sin embargo, razas más ancestrales y hoy en día casi en desuso parecen poseer una mayor resistencia natural a esta enfermedad. En el presente estudio se establecieron cultivos celulares de celulas mamarias provenientes de las razas ancestrales Highland y White Park (n = 5) y de las razas modernas Brown Swiss y Red Holstein (n = 6), para después ser infectados con los patógenos Escherichia coli y Staphylococcus aureus. Mediante reverse transcription quantitative polymerase chain reaction (RT-qPCR) se pudo determinar que la expresión basal de 16 genes era diferente en las distintas razas. Los genes CASP8, CXCL8, TLR2 y TLR4 demonstran una mayor expresión en las razas ancestrales (P < 0.05). Un mayor número de genes sufría una estimulación de su expresión tras la infección con los patógenos en las razas modernas. Asi mismo fueron encontradas diferencias significativas (P < 0.05) entre razas en la regulación de C3, CASP8, CCL2, CD14, LY96 y TGFβ1. La concentración de las proteínas lactoferrina y serum amyloid A también es diferente en las distintas razas en células control y tratadas con Staphylococcus aureus. La reacción inmune tras infección fue generalmente menos intensa en células provenientes de razas ancestrales, posiblemente debido a una mayor expresión basal en estas razas, un hecho que ha sido demostrado beneficioso para el animal en trabajos previos. En resumen, los datos de este trabajo confirman la hipótesis previa de una mayor inmunidad innata en razas bovinas ancestrales en comparación con las razas modernas empleadas hoy en día.

Keywords

breed comparisonprimary bovine mammary epithelial cellsinnate immune responseancient and modern cattle breedsmastitiscomparaison de racescellules primaires épithéliales mammaires bovinesréponse immunitaire innéeraces bovines anciennes et modernesmastitecomparación de razascélulas primarias epiteliales mamarias bovinasrespuesta inmune innatarazas bovinas antiguas y modernasmastitis
Type
Research Article
Information
Animal Genetic Resources/Resources génétiques animales/Recursos genéticos animales , Volume 52 , June 2013 , pp. 91 - 104
Copyright
Copyright © Food and Agriculture Organization of the United Nations 2013 

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Footnotes

†

Prof. Dr H.H.D. Meyer, who supervised this research, passed away before publication of this work.

References

Alderson, G.L.H. 1997. A breed of distinction: White Park cattle ancient and modern. Countrywide Livestock Ltd., Shrewsbury, UK.Google Scholar
Bannerman, D.D., Paape, M.J., Lee, J.W., Zhao, X., Hope, J.C. & Rainard, P. 2004. Escherichia coli and Staphylococcus aureus elicit differential innate immune responses following intramammary infection. Clinical and Diagnostic Laboratory Immunology 11: 463–472.Google Scholar
Bannerman, D.D., Kauf, A.C., Paape, M.J., Springer, H.R. & Goff, J.P. 2008a. Comparison of Holstein and Jersey innate immune responses to Escherichia coli intramammary infection. Journal of Dairy Science 91: 2225–2235.Google Scholar
Bannerman, D.D., Springer, H.R., Paape, M.J., Kauf, A.C. & Goff, J.P. 2008b. Evaluation of breed-dependent differences in the innate immune responses of Holstein and Jersey cows to Staphylococcus aureus intramammary infection. Journal of Dairy Research 75: 291–301.Google Scholar
Biedermann, G., Hecht, W., Fandrey, E., Rudolph, H. & Frolich, K. 2009. Population genetic analysis of White Park cattle in Germany. Archiv Fur Tierzucht-Archives of Animal Breeding 52: 561–573.Google Scholar
BLE. 2012. Central documentation on animal genetic resources in Germany – domestic animals. Bundesanstalt für Landwirtschaft und Ernährung (BLE), Bonn, Germany (available at http://tgrdeu.genres.de/hausundnutztiere/rind).Google Scholar
Buehring, G.C. 1990. Culture of mammary epithelial cells from bovine milk. Journal of Dairy Science 73: 956–963.Google Scholar
Burvenich, C., Van Merris, V., Mehrzad, J., Diez-Fraile, A. & Duchateau, L. 2003. Severity of E. coli mastitis is mainly determined by cow factors. Veterinary Research 34: 521–564.CrossRefGoogle ScholarPubMed
Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M.W., Shipley, G.L., Vandesompele, J. & Wittwer, C.T. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55: 611–622.Google Scholar
Carroll, J.A., Burdick, N.C., Reuter, R.R., Chase, C.C. Jr, Spiers, D.E., Arthington, J.D. & Coleman, S.W. 2011. Differential acute phase immune responses by Angus and Romosinuano steers following an endotoxin challenge. Domestic Animal Endocrinology 41: 163–173.Google Scholar
Danowski, K., Sorg, D., Gross, J., Meyer, H.H.D. & Kliem, H. 2012a. Innate defense capability of challenged primary bovine mammary epithelial cells after an induced negative energy balance in vivo . Czech Journal of Animal Science 57: 207–220.Google Scholar
Danowski, K., Gross, J.J., Meyer, H.H.D. & Kliem, H. 2012b. Effects of induced energy deficiency on lactoferrin concentration in milk and the lactoferrin reaction of primary bovine mammary epithelial cells in vitro . Journal of Animal Physiology and Animal Nutrition [Epub ahead of Print], DOI: 10.1111/j.1439-0396.2012.01305.x.Google Scholar
Dimmer, E.C., Huntley, R.P., Alam-Faruque, Y., Sawford, T., O'Donovan, C., Martin, M.J., Bely, B., Browne, P., Mun Chan, W., Eberhardt, R., Gardner, M., Laiho, K., Legge, D., Magrane, M., Pichler, K., Poggioli, D., Sehra, H., Auchincloss, A., Axelsen, K., Blatter, M.C., Boutet, E., Braconi-Quintaje, S., Breuza, L., Bridge, A., Coudert, E., Estreicher, A., Famiglietti, L., Ferro-Rojas, S., Feuermann, M., Gos, A., Gruaz-Gumowski, N., Hinz, U., Hulo, C., James, J., Jimenez, S., Jungo, F., Keller, G., Lemercier, P., Lieberherr, D., Masson, P., Moinat, M., Pedruzzi, I., Poux, S., Rivoire, C., Roechert, B., Schneider, M., Stutz, A., Sundaram, S., Tognolli, M., Bougueleret, L., Argoud-Puy, G., Cusin, I., Duek-Roggli, P., Xenarios, I. & Apweiler, R. 2012. The UniProt-GO Annotation database in 2011. Nucleic Acids Research 40: D565–D570.CrossRefGoogle ScholarPubMed
Dohner, J. 2001. The encyclopedia of historic and endangered livestock and poultry breeds. Yale University Press, New Haven, USA.Google Scholar
European Brown Swiss Federation. 2012. Brown Swiss from Europe means: protein, longevity, functionality. European Brown Swiss Federation, Bussolengo, Italia (available at http://www.brown-swiss.org/WhyBrownSwiss/brochure_ING.pdf).Google Scholar
FAO. 2000. World watch list for domestic animal diversity. Food and Agriculture Organization of the United Nations, Rome, Italy (available at http://www.fao.org/docrep/009/x8750e/x8750e00.htm).Google Scholar
German Holstein Association. 2010. German Holsteins 2010 facts & figures. German Holstein Association, Bonn, Germany (available at http://www.holstein-dhv.de/downloads.html).Google Scholar
Glass, E.J., Crutchley, S. & Jensen, K. 2012. Living with the enemy or uninvited guests: functional genomics approaches to investigating host resistance or tolerance traits to a protozoan parasite, Theileria annulata, in cattle. Veterinary Immunology and Immunopathology 148: 178–189.Google Scholar
Glass, E.J., Preston, P.M., Springbett, A., Craigmile, S., Kirvar, E., Wilkie, G. & Brown, C.G.D. 2005. Bos taurus and Bos indicus (Sahiwal) calves respond differently to infection with Theileria annulata and produce markedly different levels of acute phase proteins. International Journal for Parasitology 35: 337–347.Google Scholar
Griesbeck-Zilch, B., Meyer, H.H., Kuhn, C.H., Schwerin, M. & Wellnitz, O. 2008. Staphylococcus aureus and Escherichia coli cause deviating expression profiles of cytokines and lactoferrin messenger ribonucleic acid in mammary epithelial cells. Journal of Dairy Science 91: 2215–2224.Google Scholar
Griesbeck-Zilch, B., Osman, M., Kuhn, C., Schwerin, M., Bruckmaier, R.H., Pfaffl, M.W., Hammerle-Fickinger, A., Meyer, H.H. & Wellnitz, O. 2009. Analysis of key molecules of the innate immune system in mammary epithelial cells isolated from marker-assisted and conventionally selected cattle. Journal of Dairy Science 92: 4621–4633.Google Scholar
Groebner, A.E., Schulke, K., Schefold, J.C., Fusch, G., Sinowatz, F., Reichenbach, H.D., Wolf, E., Meyer, H.H. & Ulbrich, S.E. 2011. Immunological mechanisms to establish embryo tolerance in early bovine pregnancy. Reproduction, Fertility and Development 23: 619–632.Google Scholar
Gunther, J., Esch, K., Poschadel, N., Petzl, W., Zerbe, H., Mitterhuemer, S., Blum, H. & Seyfert, H.M. 2011. Comparative kinetics of Escherichia coli- and Staphylococcus aureus-specific activation of key immune pathways in mammary epithelial cells demonstrates that S. aureus elicits a delayed response dominated by interleukin-6 (IL-6) but not by IL-1A or tumor necrosis factor alpha. Infection and Immunity 79L: 695–707.Google Scholar
Gunther, J., Koczan, D., Yang, W., Nurnberg, G., Repsilber, D., Schuberth, H.J., Park, Z., Maqbool, N., Molenaar, A. & Seyfert, H.M. 2009. Assessment of the immune capacity of mammary epithelial cells: comparison with mammary tissue after challenge with Escherichia coli . Veterinary Research 40: 31.Google Scholar
Hayes, B.J., Pryce, J., Chamberlain, A.J., Bowman, P.J. & Goddard, M.E. 2010. Genetic architecture of complex traits and accuracy of genomic prediction: coat colour, milk-fat percentage, and type in Holstein cattle as contrasting model traits. PLoS Genetics 6: e1001139.Google Scholar
Heringstad, B., Klemetsdal, G. & Steine, T. 2003. Selection responses for clinical mastitis and protein yield in two Norwegian dairy cattle selection experiments. Journal of Dairy Science 86: 2990–2999.Google Scholar
Hsu, K., Champaiboon, C., Guenther, B.D., Sorenson, B.S., Khammanivong, A., Ross, K.F., Geczy, C.L. & Herzberg, M.C. 2009. Anti-infective protective properties of S100 calgranulins. Anti-inflammatory and Anti-allergy Agents in Medicinal Chemistry 8: 290–305.Google Scholar
Kandasamy, S., Green, B.B., Benjamin, A.L. & Kerr, D.E. 2012. Between-cow variation in dermal fibroblast response to lipopolysaccharide reflected in resolution of inflammation during Escherichia coli mastitis. Journal of Dairy Science 94: 5963–5975.Google Scholar
Krol, 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: 357–361.Google Scholar
Liao, Y., Du, X. & Lonnerdal, B. 2010. miR-214 regulates lactoferrin expression and pro-apoptotic function in mammary epithelial cells. Journal of Nutrition 140: 1552–1556.Google Scholar
Livak, K.J. & Schmittgen, T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25: 402–408.Google Scholar
Longley, D.B., Steel, D.M. & Whitehead, A.S. 1999. Posttranscriptional regulation of acute phase serum amyloid A2 expression by the 5′- and 3′-untranslated regions of its mRNA. Journal of Immunology 163: 4537–4545.Google Scholar
Mason, I.L. 2002. Mason's world dictionary of livestock breeds, types and varieties. 5th ed. CABI Publication, Wallingford, Oxfordshire, UK.Google Scholar
O'Halloran, F., Bahar, B., Buckley, F., O'Sullivan, O., Sweeney, T. & Giblin, L. 2009. Characterisation of single nucleotide polymorphisms identified in the bovine lactoferrin gene sequences across a range of dairy cow breeds. Biochimie 91: 68–75.Google Scholar
Ogorevc, J., Kunej, T., Razpet, A. & Dovc, P. 2009. Database of cattle candidate genes and genetic markers for milk production and mastitis. Animal Genetics 40: 832–851.CrossRefGoogle ScholarPubMed
Petzl, W., Zerbe, H., Gunther, J., Yang, W., Seyfert, H.M., Nurnberg, G. & Schuberth, H.J. 2008. Escherichia coli, but not Staphylococcus aureus triggers an early increased expression of factors contributing to the innate immune defense in the udder of the cow. Veterinary Research 39: 18.Google Scholar
Rainard, P. & Riollet, C. 2006. Innate immunity of the bovine mammary gland. Veterinary Research 37: 369–400.Google Scholar
Riollet, C., Rainard, P. & Poutrel, B. 2001. Cell subpopulations and cytokine expression in cow milk in response to chronic Staphylococcus aureus infection. Journal of Dairy Science 84: 1077–1084.Google Scholar
Shah, C., Hari-Dass, R. & Raynes, J.G. 2006. Serum amyloid A is an innate immune opsonin for Gram-negative bacteria. Blood 108: 1751–1757.Google Scholar
Sharma, A., Kumar, M., Aich, J., Hariharan, M., Brahmachari, S.K., Agrawal, A. & Ghosh, B. 2009. Posttranscriptional regulation of interleukin-10 expression by hsa-miR-106a. Proceedings of the National Academy of Sciences of the United States of America 106: 5761–5766.Google Scholar
Singh, K., Erdman, R.A., Swanson, K.M., Molenaar, A.J., Maqbool, N.J., Wheeler, T.T., Arias, J.A., Quinn-Walsh, E.C. & Stelwagen, K. 2010. Epigenetic regulation of milk production in dairy cows. Journal of Mammary Gland Biology and Neoplasia 15: 101–112.Google Scholar
Smith, P.K., Krohn, R.I., Hermanson, G.T., Mallia, A.K., Gartner, F.H., Provenzano, M.D., Fujimoto, E.K., Goeke, N.M., Olson, B.J. & Klenk, D.C. 1985. Measurement of protein using bicinchoninic acid. Analytical Biochemistry 150: 76–85.Google Scholar
Sorg, D., Potzel, A., Beck, M., Meyer, H., Viturro, E. & Kliem, H. 2012. Effects of cell culture techniques on gene expression and cholesterol efflux in primary bovine mammary epithelial cells derived from milk and tissue. In Vitro Cellular and Developmental Biology – Animal 48: 550–553.Google Scholar
Spurgeon, S.L., Jones, R.C. & Ramakrishnan, R. 2008. High throughput gene expression measurement with real time PCR in a microfluidic dynamic array. PLoS ONE 3: e1662.Google Scholar
Strandberg, E. & Shook, G.E. 1989. Genetic and economic responses to breeding programs that consider mastitis. Journal of Dairy Science 72: 2136–2142.Google Scholar
Strandberg, Y., Gray, C., Vuocolo, T., Donaldson, L., Broadway, M. & Tellam, R. 2005. Lipopolysaccharide and lipoteichoic acid induce different innate immune responses in bovine mammary epithelial cells. Cytokine 31: 72–86.Google Scholar
Tsuji, S., Hirata, Y., Mukai, F. & Ohtagaki, S. 1990. Comparison of lactoferrin content in colostrum between different cattle breeds. Journal of Dairy Science 73: 125–128.Google Scholar
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