Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-16T20:51:48.643Z Has data issue: false hasContentIssue false
  • English
  • Français

Administration of a live culture of Lactococcus lactis DPC 3147 into the bovine mammary gland stimulates the local host immune response, particularly IL-1β and IL-8 gene expression

Published online by Cambridge University Press:  18 May 2009

Christine Beecher ,
Mairéad Daly ,
Donagh P Berry ,
Katja Klostermann ,
James Flynn ,
William Meaney ,
Colin Hill ,
Tommie V McCarthy ,
R Paul Ross  and
Linda Giblin
Christine Beecher
Affiliation:
Moorepark Food Research Centre, Teagasc, Fermoy, Co. Cork, Ireland Biochemistry Department, University College Cork, Cork, Ireland
Mairéad Daly
Affiliation:
Moorepark Food Research Centre, Teagasc, Fermoy, Co. Cork, Ireland
Donagh P Berry
Affiliation:
Moorepark Production Research Centre, Teagasc, Fermoy, Co. Cork, Ireland
Katja Klostermann
Affiliation:
Moorepark Food Research Centre, Teagasc, Fermoy, Co. Cork, Ireland Microbiology Department, University College Cork, Cork, Ireland
James Flynn
Affiliation:
Moorepark Production Research Centre, Teagasc, Fermoy, Co. Cork, Ireland
William Meaney
Affiliation:
Moorepark Production Research Centre, Teagasc, Fermoy, Co. Cork, Ireland
Colin Hill
Affiliation:
Microbiology Department, University College Cork, Cork, Ireland
Tommie V McCarthy
Affiliation:
Biochemistry Department, University College Cork, Cork, Ireland
R Paul Ross
Affiliation:
Moorepark Food Research Centre, Teagasc, Fermoy, Co. Cork, Ireland
Linda Giblin*
Affiliation:
Moorepark Food Research Centre, Teagasc, Fermoy, Co. Cork, Ireland
*
*For correspondence; e-mail: linda.giblin@teagasc.ie
Get access Rights & Permissions [Opens in a new window]

Abstract

Mastitis is one of the most costly diseases to the dairy farming industry. Conventional antibiotic therapy is often unsatisfactory for successful treatment of mastitis and alternative treatments are continually under investigation. We have previously demonstrated, in two separate field trials, that a probiotic culture, Lactococcus lactis DPC 3147, was comparable to antibiotic therapy to treat bovine mastitis. To understand the mode of action of this therapeutic, we looked at the detailed immune response of the host to delivery of this live strain directly into the mammary gland of six healthy dairy cows. All animals elicited signs of udder inflammation 7 h post infusion. At this time, clots were visible in the milk of all animals in the investigation. The most pronounced increase in immune gene expression was observed in Interleukin (IL)-1β and IL-8, with highest expression corresponding to peaks in somatic cell count. Infusion with a live culture of a Lc. lactis leads to a rapid and considerable innate immune response.

Keywords

MastitisLactococcus lactisprobiotic treatment
Type
Research Article
Information
Journal of Dairy Research , Volume 76 , Issue 3 , August 2009 , pp. 340 - 348
Copyright
Copyright © Proprietors of Journal of Dairy Research 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Al-Qumber, M & Tagg, JR 2006 Commensal bacilli inhibitory to mastitis pathogens isolated from the udder microbiota of healthy cows. Journal of Applied Microbiology 101 1152–1160CrossRefGoogle ScholarPubMed
Alluwaimi, AM 2004 The cytokines of bovine mammary gland: prospects for diagnosis and therapy. Research in Veterinary Science 77 211–222CrossRefGoogle ScholarPubMed
Bannerman, DD, Paape, MJ, Goff, JP, Kimura, K, Lippolis, JD & Hope, JC 2004a Innate immune response to intramammary infection with Serratia marcescens and Streptococcus uberis. Veterinary Research 35 681–700CrossRefGoogle ScholarPubMed
Bannerman, DD, Paape, MJ, Lee, JW, Zhao, X, Hope, JC & Rainard, P 2004b Escherichia coli and Staphylococcus aureus elicit differential innate immune responses following intramammary infection. Clinical Diagnostic Laboratory Immunology 11 463–472Google ScholarPubMed
Barkema, HW, Schukken, YH & Zadoks, RN 2006 Invited Review: The role of cow, pathogen, and treatment regimen in the therapeutic success of bovine Staphylococcus aureus mastitis. Journal of Dairy Science 89 1877–1895CrossRefGoogle ScholarPubMed
Berry, DP & Meaney, WJ 2006 Interdependence and distribution of subclinical mastitis and intramammary infection among udder quarters in dairy cattle. Preventive Veterinary Medicine 75 81–91CrossRefGoogle ScholarPubMed
Bonizzi, G & Karin, M 2004 The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends in Immunology 25 280–288CrossRefGoogle ScholarPubMed
Boutinaud, M, Rulquin, H, Keisler, DH, Djiane, J & Jammes, H 2002 Use of somatic cells from goat milk for dynamic studies of gene expression in the mammary gland. Journal of Animal Science 80 1258–1269CrossRefGoogle ScholarPubMed
Crispie, F, Alonso-Gomez, M, O'Loughlin, C, Klostermann, K, Flynn, J, Arkins, S, Meaney, W, Ross, P & Hill, C 2008 Intramammary infusion of a live culture for treatment of bovine mastitis: effect of live lactococci on the mammary immune response. Journal of Dairy Research 75 374–384CrossRefGoogle ScholarPubMed
Cross, ML 2002 Microbes versus microbes: immune signals generated by probiotic lactobacilli and their role in protection against microbial pathogens. FEMS Immunology and Medical Microbiology 34 245–253CrossRefGoogle ScholarPubMed
Diarra, MS, Petitclerc, D, Deschenes, E, Lessard, N, Grondin, G, Talbot, BG & Lacasse, P 2003 Lactoferrin against Staphylococcus aureus mastitis. Lactoferrin alone or in combination with penicillin G on bovine polymorphonuclear function and mammary epithelial cells colonisation by Staphylococcus aureus. Veterinary Immunology and Immunopathology 95 33–42CrossRefGoogle ScholarPubMed
Gill, JJ, Pacan, JC, Carson, ME, Leslie, KE, Griffiths, MW & Sabour, PM 2006a Efficacy and pharmacokinetics of bacteriophage therapy in treatment of subclinical Staphylococcus aureus mastitis in lactating dairy cattle. Antimicrobial Agents in Chemotherapy 50 2912–2918CrossRefGoogle ScholarPubMed
Gill, JJ, Sabour, PM, Leslie, KE & Griffiths, MW 2006b Bovine whey proteins inhibit the interaction of Staphylococcus aureus and bacteriophage K. Journal of Applied Microbiology 101 377–386CrossRefGoogle ScholarPubMed
Goldammer, T, Zerbe, H, Molenaar, A, Schuberth, HJ, Brunner, RM, Kata, SR & Seyfert, HM 2004 Mastitis increases mammary mRNA abundance of beta-defensin 5, toll-like-receptor 2 (TLR2), and TLR4 but not TLR9 in cattle. Clinical Diagnostic Laboratory Immunology 11 174–185Google Scholar
Greene, WA, Gano, AM, Smith, KL, Hogan, JS & Todhunter, DA 1991 Comparison of probiotic and antibiotic intramammary therapy of cattle with elevated somatic cell counts. Journal of Dairy Science 74 2976–2981CrossRefGoogle ScholarPubMed
Jimenez, E, Fernandez, L, Maldonado, A, Martin, R, Olivares, M, Xaus, J & Rodriguez, JM 2008 Oral administration of Lactobacillus strains isolated from breast milk as an alternative for the treatment of infectious mastitis during lactation. Applied and Environmental Microbiology 74 4650–4655CrossRefGoogle ScholarPubMed
Kauf, AC, Vinyard, BT & Bannerman, DD 2007 Effect of intramammary infusion of bacterial lipopolysaccharide on experimentally induced Staphylococcus aureus intramammary infection. Research in Veterinary Science 82 39–46CrossRefGoogle ScholarPubMed
Klostermann, K, Crispie, F, Flynn, J, Ross, RP, Hill, C & Meaney, W 2008 Intramammary infusion of a live culture of Lactococcus lactis for treatment of bovine mastitis: comparison with antibiotic treatment in field trials. Journal of Dairy Research 75 365–373CrossRefGoogle ScholarPubMed
Lacasse, P, Lauzon, K, Diarra, MS & Petitclerc, D 2008 Utilization of lactoferrin to fight antibiotic-resistant mammary gland pathogens. Journal of Animal Science 86 (Suppl. 13) 66–71CrossRefGoogle ScholarPubMed
Middleton, JR, Luby, CD & Adams, DS 2009 Efficacy of vaccination against staphylococcal mastitis: A review and new data. Veterinary Microbiology 134 192–198CrossRefGoogle ScholarPubMed
O'Flaherty, S, Coffey, A, Meaney, WJ, Fitzgerald, GF & Ross, RP 2005 Inhibition of bacteriophage K proliferation on Staphylococcus aureus in raw bovine milk. Letters in Appied Microbiology 41 274–279CrossRefGoogle ScholarPubMed
Oviedo-Boyso, J, Cardoso-Correa, BI, Cajero-Juarez, M, Bravo-Patino, A, Valdez-Alarcon, JJ & Baizabal-Aguirre, VM 2008 The capacity of bovine endothelial cells to eliminate intracellular Staphylococcus aureus and Staphylococcus epidermidis is increased by the proinflammatory cytokines TNF-alpha and IL-1beta. FEMS Immunology and Medical Microbiology 54 53–59CrossRefGoogle ScholarPubMed
Ozinsky, A, Underhill, DM, Fontenot, JD, Hajjar, AM, Smith, KD, Wilson, CB, Schroeder, L & Aderem, A 2000 The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proceedings of National Academy of Sciences of the USA 97 13766–13771CrossRefGoogle ScholarPubMed
Pfaffl, MWH 2001 Validities of mRNA quantification using recombinant RNA and recombinant DNA external calibratiopn curves in real-time RT-PCR. Biotechnology Letters 23 275–282CrossRefGoogle Scholar
Rainard, P, Riollet, C, Berthon, P, Cunha, P, Fromageau, A, Rossignol, C & Gilbert, FB 2008 The chemokine CXCL3 is responsible for the constitutive chemotactic activity of bovine milk for neutrophils. Molecular Immunology 45 4020–4027CrossRefGoogle ScholarPubMed
Ryan, MP, Flynn, J, Hill, C, Ross, RP & Meaney, WJ 1999 The natural food grade inhibitor, lacticin 3147, reduced the incidence of mastitis after experimental challenge with Streptococcus dysgalactiae in nonlactating dairy cows. Journal of Dairy Science 82 2625–2631CrossRefGoogle ScholarPubMed
Ryan, MP, Meaney, WJ, Ross, RP & Hill, C 1998 Evaluation of lacticin 3147 and a teat seal containing this bacteriocin for inhibition of mastitis pathogens. Applied and Environmental Microbiology 64 2287–2290CrossRefGoogle Scholar
SABRE 2006 Cutting edge genomics for sustainable animal breeding. In Framework 6 Report. (Ed. Faraday, G). Farm Animal Genetics and Genomics Faraday Partnership LtdGoogle 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 72–86CrossRefGoogle ScholarPubMed
Twomey, DP, Wheelock, AI, Flynn, J, Meaney, WJ, Hill, C & Ross, RP 2000 Protection against Staphylococcus aureus mastitis in dairy cows using a bismuth-based teat seal containing the bacteriocin, lacticin 3147. Journal of Dairy Science 83 1981–1988CrossRefGoogle ScholarPubMed
Wedlock, DN, Denis, M, Lacy-Hulbert, J & Buddle, BM 2008 Interleukin-1beta infusion in bovine mammary glands prior to challenge with Streptococcus uberis reduces bacterial growth but causes sterile mastitis. Veterinary Research Communications 32 439–447CrossRefGoogle ScholarPubMed
Wright, SD, Ramos, RA, Tobias, PS, Ulevitch, RJ & Mathison, JC 1990 CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249 1431–1433CrossRefGoogle ScholarPubMed
Yang, W, Zerbe, H, Petzl, W, Brunner, RM, Gunther, J, Draing, C, von Aulock, S, Schuberth, HJ & Seyfert, HM 2008 Bovine TLR2 and TLR4 properly transduce signals from Staphylococcus aureus and E. coli, but S. aureus fails to both activate NF-kappaB in mammary epithelial cells and to quickly induce TNFalpha and interleukin-8 (CXCL8) expression in the udder. Molecular Immunology 45 1385–1397CrossRefGoogle Scholar
Zecconi, A, Piccinini, R, Fiorina, S, Cabrini, L, Daprà, V & Amadori, M 2008 Evaluation of interleukin-2 treatment for prevention of intramammary infections in cows after calving. Comparative Immunology, Microbiology and Infectious Diseases. In PressGoogle ScholarPubMed