Journal of Dairy Science
Volume 91, Issue 6 , Pages 2215-2224 , June 2008

Staphylococcus aureus and Escherichia coli Cause Deviating Expression Profiles of Cytokines and Lactoferrin Messenger Ribonucleic Acid in Mammary Epithelial Cells

  • B. Griesbeck-Zilch

      Affiliations

    • Physiology Weihenstephan, Technical University Munich, D-85350 Freising, Germany
  • ,
  • H.H.D. Meyer

      Affiliations

    • Physiology Weihenstephan, Technical University Munich, D-85350 Freising, Germany
  • ,
  • Ch. Kühn

      Affiliations

    • Research Institute for the Biology of Farm Animals, D-18196 Dummerstorf, Germany
  • ,
  • M. Schwerin

      Affiliations

    • Research Institute for the Biology of Farm Animals, D-18196 Dummerstorf, Germany
  • ,
  • O. Wellnitz

      Affiliations

    • Veterinary Physiology, Vetsuisse Faculty, University of Bern, CH-1725 Posieux, Switzerland
    • Corresponding Author InformationCorresponding author.

Received 5 October 2007 ,Accepted 6 February 2008.

References 

  1. Aderem A, Ulevitch RJ. Toll-like receptors in the induction of the innate immune response. Nature. 2000;406:782–787
  2. Bannerman DD, Paape MJ, Lee JW, Zhao X, Hope JC, Rainard P. Escherichia coli and Staphylococcus aureus elicit differential innate immune responses following intramammary infection. Clin. Diagn. Lab. Immunol. 2004;11:463–472
  3. Barkema HW, Schukken YH, Zadoks RN. The role of cow, pathogen, and treatment regimen in the therapeutic success of bovine Staphylococcus aureus mastitis. J. Dairy Sci. 2006;89:1877–1895
  4. Berlutti F, Schippa S, Morea C, Sarli S, Perfetto B, Donnarumma G, et al. Lactoferrin downregulates pro-inflammatory cytokines upexpressed in intestinal epithelial cells infected with invasive or noninvasive Escherichia coli strains. Biochem. Cell Biol. 2006;84:351–357
  5. Boudjellab N, Chan-Tang HS, Zhao X. Bovine interleukin-1 expression by cultured mammary epithelial cells (MAC-T) and its involvement in the release of MAC-T derived interleukin-8. Comp. Biochem. Physiol. A. 2000;127:191–199
  6. Bramley AJ, Patel AH, O’Reilly M, Foster R, Foster TJ. Roles of alpha-toxin and beta-toxin in virulence of Staphylococcus aureus for the mouse mammary gland. Infect. Immun. 1989;57:2489–2494
  7. Burvenich C, van Merris V, Mehrzad J, Diez-Fraile A, Duchateau L. Severity of E. coli mastitis is mainly determined by cow factors. Vet. Res. 2003;34:521–564
  8. Chennazhy KP, Krishnan LK. Effect of passage number and matrix characteristics on differentiation of endothelial cells cultured for tissue engineering. Biomaterials. 2005;26:5658–5667
  9. Curran CS, Demick KP, Mansfield JM. Lactoferrin activates macrophages via TLR4-dependent and -independent signaling pathways. Cell. Immunol. 2006;242:23–30
  10. Dinarello CA. Cytokines as mediators in the pathogenesis of septic shock. Curr. Top. Microbiol. Immunol. 1996;216:133–165
  11. Frank MM, Fries LF. The role of complement in inflammation and phagocytosis. Immunol. Today. 1991;12:322–326
  12. Goldammer T, Zerbe H, Molenaar A, Schuberth HJ, Brunner RM, Kata SR, et al. Mastitis increases mammary mRNA abundance of beta-defensin 5, Toll-like-receptor 2 (TLR2), and TLR4 but not TLR9 in cattle. Clin. Diagn. Lab. Immunol. 2004;11:174–185
  13. Hagiwara S, Kawai K, Anri A, Nagahata H. Lactoferrin concentrations in milk from normal and subclinical mastitic cows. J. Vet. Med. Sci. 2003;65:319–323
  14. Hagiwara K, Yamanaka H, Hisaeda K, Taharaguchi S, Kirisawa R, Iwai H. Concentrations of IL-6 in serum and whey from healthy and mastitic cows. Vet. Res. Commun. 2001;25:99–108
  15. Hoeben D, Burvenich C, Trevisi E, Bertoni G, Hamann J, Bruckmaier RM, et al. Role of endotoxin and TNF-alpha in the pathogenesis of experimentally induced coliform mastitis in periparturient cows. J. Dairy Res. 2000;67:503–514
  16. Hogan J, Smith KL. Coliform mastitis. Vet. Res. 2003;34:507–519
  17. Kawai K, Hagiwara S, Anri A, Nagahata H. Lactoferrin concentration in milk of bovine clinical mastitis. Vet. Res. Commun. 1999;23:391–398
  18. Korhonen H, Marnila P, Gill HS. Milk immunoglobulins and complement factors. Br. J. Nutr. 2000;84(Suppl. 1):75–80
  19. Kutila T, Suojala L, Lehtolainen T, Saloniemi H, Kaartinen L, Tahti M, et al. The efficacy of bovine lactoferrin in the treatment of cows with experimentally induced Escherichia coli mastitis. J. Vet. Pharmacol. Ther. 2004;27:197–202
  20. Lacasse P, Lauzon K, Diarra MS, Petitclerc D. Utilization of lactoferrin to fight antibiotic resistant mammary gland pathogens. J. Anim. Sci. 2007;
  21. Lahouassa H, Moussay E, Rainard P, Riollet C. Differential cytokine and chemokine responses of bovine mammary epithelial cells to Staphylococcus aureus and Escherichia coli. Cytokine. 2007;38:12–21
  22. Lee NY, Kawai K, Nakamura I, Tanaka T, Kumura HK, Shimazaki Susceptibilities against bovine lactoferrin with microorganisms isolated from mastitic milk. J. Vet. Med. Sci. 2004;66:1267–1269
  23. Legrand D, Elass E, Pierce A, Mazurier J. Lactoferrin and host defence: An overview of its immuno-modulating and anti-inflammatory properties. Biometals. 2004;17:225–229
  24. Liang Y, Zhou Y, Shen P. NF-kappaB and its regulation on the immune system. Cell. Mol. Immunol. 2004;1:343–350
  25. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods. 2001;25:402–408
  26. McManaman JL, Neville MC. Mammary physiology and milk secretion. Adv. Drug Deliv. Rev. 2003;55:629–641
  27. Menzies M, Ingham A. Identification and expression of Toll-like receptors 1–10 in selected bovine and ovine tissues. Vet. Immunol. Immunopathol. 2006;109:23–30
  28. Okada H, Ito T, Ohtsuka H, Kirisawa R, Iwai H, Yamashita K, et al. Detection of interleukin-1 and interleukin-6 on cryopreserved bovine mammary epithelial cells in vitro. J. Vet. Med. Sci. 1997;59:503–507
  29. Orsi N. The antimicrobial activity of lactoferrin: Current status and perspectives. Biometals. 2004;17:189–196
  30. Pahl HL. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene. 1999;18:6853–6866
  31. Pandey S, Agrawal DK. Immunobiology of Toll-like receptors: Emerging trends. Immunol. Cell Biol. 2006;84:333–341
  32. Pareek R, Wellnitz O, van Dorp R, Burton J, Kerr D. Immunorelevant gene expression in LPS-challenged bovine mammary epithelial cells. J. Appl. Genet. 2005;46:171–177
  33. Perissutti S, Tedesco F. Effect of cytokines on the secretion of the fifth and eighth complement components by HepG2 cells. Int. J. Clin. Lab. Res. 1994;24:45–48
  34. Persson Waller K, Colditz IG, Lun S, Ostensson K. Cytokines in mammary lymph and milk during endotoxin-induced bovine mastitis. Res. Vet. Sci. 2003;74:31–36
  35. Pfaffl MW, Wittmann SL, Meyer HH, Bruckmaier RM. Gene expression of immunologically important factors in blood cells, milk cells, and mammary tissue of cows. J. Dairy Sci. 2003;86:538–545
  36. Rainard P. The complement in milk and defense of the bovine mammary gland against infections. Vet. Res. 2003;34:647–670
  37. Rainard P, Riollet C. Innate immunity of the bovine mammary gland. Vet. Res. 2006;37:369–400
  38. Riollet C, Rainard P, Poutrel B. Differential induction of complement fragment C5a and inflammatory cytokines during intramammary infections with Escherichia coli and Staphylococcus aureus. Clin. Diagn. Lab. Immunol. 2000;7:161–167
  39. Schmitz S, Pfaffl MW, Meyer HH, Bruckmaier RM. Short-term changes of mRNA expression of various inflammatory factors and milk proteins in mammary tissue during LPS-induced mastitis. Domest. Anim. Endocrinol. 2004;26:111–126
  40. Seegers H, Fourichon CF, Beaudeau Production effects related to mastitis and mastitis economics in dairy cattle herds. Vet. Res. 2003;34:475–491
  41. Srivastava MD, Srivastava A, Brouhard B, Saneto R, Groh-Wargo S, Kubit J. Cytokines in human milk. Res. Commun. Mol. Pathol. Pharmacol. 1996;93:263–287
  42. Strandberg Y, Gray C, Vuocolo T, Donaldson L, Broadway M, Tellam R. Lipopolysaccharide and lipoteichoic acid induce different innate immune responses in bovine mammary epithelial cells. Cytokine. 2005;31:72–86
  43. Sutra L, Poutrel B. Virulence factors involved in the pathogenesis of bovine intramammary infections due to Staphylococcus aureus. J. Med. Microbiol. 1994;40:79–89
  44. Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu. Rev. Immunol. 2003;21:335–376
  45. Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, Ogawa T, et al. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity. 1999;11:443–451
  46. Teng CT. Regulation of lactoferrin gene expression by estrogen and epidermal growth factor: Molecular mechanism. Cell Biochem. Biophys. 1999;31:49–64
  47. Teng CT. Lactoferrin gene expression and regulation: An overview. Biochem. Cell Biol. 2002;80:7–16
  48. van der Kraan MI, van Marle J, Nazmi K, Groenink J, van’t Hof W, Veerman EC, et al. Ultrastructural effects of antimicrobial peptides from bovine lactoferrin on the membranes of Candida albicans and Escherichia coli. Peptides. 2005;26:1537–1542
  49. Ward PP, Paz E, Conneely OM. Multifunctional roles of lactoferrin: A critical overview. Cell. Mol. Life Sci. 2005;62:2540–2548
  50. Wellnitz O, Kerr DE. Cryopreserved bovine mammary cells to model epithelial response to infection. Vet. Immunol. Immunopathol. 2004;101:191–202
  51. Wyble CW, Hynes KL, Kuchibhotla J, Marcus BC, Hallahan D, Gewertz BL. TNF-alpha and IL-1 upregulate membrane-bound and soluble E-selectin through a common pathway. J. Surg. Res. 1997;73:107–112
  52. Yang W, Zerbe H, Petzl W, Brunner RM, Günther J, Draing C, et al. 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. Mol. Immunol. 2008;45:1385–1397
  53. Zheng J, Ather JL, Sonstegard TS, Kerr DE. Characterization of the infection-responsive bovine lactoferrin promoter. Gene. 2005;353:107–117

PII: S0022-0302(08)71172-X

doi: 10.3168/jds.2007-0752

Journal of Dairy Science
Volume 91, Issue 6 , Pages 2215-2224 , June 2008