Streptococcus uberis strains isolated from the bovine mammary gland evade immune recognition by mammary epithelial cells, but not of macrophages

Veterinary Research

Volumn 47, Issue 1, 2016, Pages

  Günther, Juliane ^a   Czabanska, Anna ^b   Bauer, Isabel ^a   Leigh, James A ^c   Holst, Otto ^b   Seyfert, Hans Martin ^a  

^a LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

^b RESEARCH CENTER BORSTEL   (Germany)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BOVINE; BOVINE MASTITIS; CATTLE DISEASE; CELL LINE; CLASSIFICATION; CYTOLOGY; EPITHELIUM CELL; FEMALE; IMMUNOLOGY; MACROPHAGE; MICROBIOLOGY; MOUSE; PHYSIOLOGY; STREPTOCOCCUS; STREPTOCOCCUS INFECTION; UDDER; VETERINARY;

ANIMALS; CATTLE; CATTLE DISEASES; CELL LINE; EPITHELIAL CELLS; FEMALE; MACROPHAGES; MAMMARY GLANDS, ANIMAL; MASTITIS, BOVINE; MICE; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS;

EID: 84954027475     PISSN: 09284249     EISSN: 12979716     Source Type: Journal    
DOI: 10.1186/s13567-015-0287-8     Document Type: Article

References (68)

1. Ericsson Unnerstad H, Lindberg A, Persson Waller K, Ekman T, Artursson K, Nilsson-Öst M, Bengtsson B (2009) Microbial aetiology of acute clinical mastitis and agent-specific risk factors. Vet Microbiol 137:90-97
2. Zadoks R, Middleton J, McDougall S, Katholm J, Schukken Y (2011) Molecular epidemiology of mastitis pathogens of dairy cattle and comparative relevance to humans. J Mammary Gland Biol Neoplasia 16:357-372
3. Zadoks RN, Gillespie BE, Barkema HW, Sampimon OC, Oliver SP, Schukken YH (2003) Clinical, epidemiological and molecular characteristics of Streptococcus uberis infections in dairy herds. Epidemiol Infect 130:335-349
4. Douglas VL, Fenwick SG, Pfeiffer DU, Williamson NB, Holmes CW (2000) Genomic typing of Streptococcus uberis isolates from cases of mastitis, in New Zealand dairy cows, using pulsed-field gel electrophoresis. Vet Microbiol 75:27-41
5. Hossain M, Egan SA, Coffey T, Ward PN, Wilson R, Leigh JA, Emes RD (2015) Virulence related sequences; insights provided by comparative genomics of Streptococcus uberis of differing virulence. BMC Genomics 16:334
6. Hill AW (1988) Pathogenicity of two strains of Streptococcus uberis infused into lactating and non-lactating bovine mammary glands. Res Vet Sci 45:400-404
7. Tassi R, McNeilly TN, Fitzpatrick JL, Fontaine MC, Reddick D, Ramage C, Lutton M, Schukken YH, Zadoks RN (2013) Strain-specific pathogenicity of putative host-adapted and nonadapted strains of Streptococcus uberis in dairy cattle. J Dairy Sci 96:5129-5145
8. Rato MG, Bexiga R, Nunes SF, Cavaco LM, Vilela CL, Santos-Sanches I (2008) Molecular epidemiology and population structure of bovine Streptococcus uberis. J Dairy Sci 91:4542-4551
9. Abureema S, Smooker P, Malmo J, Deighton M (2014) Molecular epidemiology of recurrent clinical mastitis due to Streptococcus uberis: evidence of both an environmental source and recurring infection with the same strain. J Dairy Sci 97:285-290
10. Lundberg A, Nyman A, Unnerstad H, Waller K (2014) Prevalence of bacterial genotypes and outcome of bovine clinical mastitis due to Streptococcus dysgalactiae and Streptococcus uberis. Acta Vet Scand 56:80
11. Tomita T, Meehan B, Wongkattiya N, Malmo J, Pullinger G, Leigh J, Deighton M (2008) Identification of Streptococcus uberis multilocus sequence types highly associated with mastitis. Appl Environ Microbiol 74:114-124
12. Bannerman DD, Paape MJ, Goff JP, Kimura K, Lippolis JD, Hope JC (2004) Innate immune response to intramammary infection with Serratia marcescens and Streptococcus uberis. Vet Res 35:681-700
13. Leigh JA, Egan SA, Ward PN, Field TR, Coffey TJ (2010) Sortase anchored proteins of Streptococcus uberis play major roles in the pathogenesis of bovine mastitis in dairy cattle. Vet Res 41:63
14. Swanson KM, Stelwagen K, Dobson J, Henderson HV, Davis SR, Farr VC, Singh K (2009) Transcriptome profiling of Streptococcus uberis-induced mastitis reveals fundamental differences between immune gene expression in the mammary gland and in a primary cell culture model. J Dairy Sci 92:117-129
15. Moyes K, Drackley J, Morin D, Bionaz M, Rodriguez-Zas S, Everts R, Lewin H, Loor J (2009) Gene network and pathway analysis of bovine mammary tissue challenged with Streptococcus uberis reveals induction of cell proliferation and inhibition of PPARgamma signaling as potential mechanism for the negative relationships between immune response and lipid metabolism. BMC Genomics 10:542
16. de Greeff A, Zadoks R, Ruuls L, Toussaint M, Nguyen TKA, Downing A, Rebel J, Stockhofe-Zurwieden N, Smith H (2013) Early host response in the mammary gland after experimental Streptococcus uberis challenge in heifers. J Dairy Sci 96:3723-3736
17. Günther J, Koczan D, Yang W, Nürnberg G, Repsilber D, Schuberth HJ, Park Z, Macbool 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. Vet Res 40:31
18. Mitterhuemer S, Petzl W, Krebs S, Mehne D, Klanner A, Wolf E, Zerbe H, Blum H (2010) Escherichia coli infection induces distinct local and systemic transcriptome responses in the mammary gland. BMC Genomics 11:138
19. Petzl W, Zerbe H, Günther J, Yang W, Seyfert H-M, Schuberth HJ (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. Vet Res 39:18
20. Leigh JA, Field TR, Williams MR (1990) Two strains of Streptococcus uberis, of differing ability to cause clinical mastitis, differ in their ability to resist some host defence factors. Res Vet Sci 49:85-87
21. Capuco AV, Akers RM, Smith JJ (1997) Mammary growth in Holstein cows during the dry period: quantification of nucleic acids and histology. J Dairy Sci 80:477-487
22. Capuco AV, Wood DL, Baldwin R, Mcleod K, Paape MJ (2001) Mammary cell number, proliferation, and apoptosis during a bovine lactation: relation to milk production and effect of bST. J Dairy Sci 84:2177-2187
23. Rainard P, Riollet C (2006) Innate immunity of the bovine mammary gland. Vet Res 37:369-400
24. Schukken YH, Günther J, Fitzpatrick J, Fontaine MC, Goetze L, Holst O, Leigh J, Petzl W, Schuberth HJ, Sipka A, Smith DGE, Quesnell R, Watts J, Yancey R, Zerbe H, Gurjar A, Zadoks RN, Seyfert HM (2011) Host-response patterns of intramammary infections in dairy cows. Vet Immunol Immunopathol 144:270-289
25. 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
26. Goldammer T, Zerbe H, Molenaar A, Schuberth HJ, Brunner RM, Kata SR, Seyfert HM (2004) Mastitis increases mammary mRNA abundance of β-defensin 5, toll-like-receptor 2 (TLR2), and TLR4 but not TLR9 in cattle. Clin Diagn Lab Immunol 11:174-185
27. Yang W, Molenaar AJ, Kurts-Ebert B, Seyfert HM (2006) NF-κB factors are essential, but not the switch, for pathogen-related induction of the bovine β-defensin 5-encoding gene in mammary epithelial cells. Mol Immunol 43:210-225
28. Porcherie A, Cunha P, Trotereau A, Roussel P, Gilbert F, Rainard P, Germon P (2012) Repertoire of Escherichia coli agonists sensed by innate immunity receptors of the bovine udder and mammary epithelial cells. Vet Res 43:14
29. Wellnitz O, Berger U, Schaeren W, Bruckmaier R (2012) Mastitis severity induced by two Streptococcus uberis strains is reflected by the mammary immune response in vitro. Schweiz Arch Tierheilkd 154:317-323
30. Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140:805-820
31. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124:783-801
32. Karin M, Lin A (2002) NF-kappaB at the crossroads of life and death. Nat Immunol 3:221-227
33. Hoesel B, Schmid J (2013) The complexity of NF-kappaB signaling in inflammation and cancer. Mol Cancer 12:86
34. Oeckinghaus A, Hayden MS, Ghosh S (2011) Crosstalk in NF-κB signaling pathways. Nat Immunol 12:695-708
35. Drennan MB, Nicolle D, Quesniaux VJF, Jacobs M, Allie N, Mpagi J, Fremond C, Wagner H, Kirschning C, Ryffel B (2004) Toll-like receptor 2-deficient mice succumb to Mycobacterium tuberculosis infection. Am J Pathol 164:49-57
36. Elson G, Dunn-Siegrist I, Daubeuf B, Pugin J (2006) Contribution of Toll-like receptors to the innate immune response to Gram-negative and Gram-positive bacteria. Blood 109:1574-1583
37. Asplin IR, Carl DJ, Way SS, Jones AL (2008) Role of Toll-like receptor 2 in innate resistance to Group B Streptococcus. Microb Pathog 44:43-51
38. Jin MS, Kim SE, Heo JY, Lee ME, Kim HM, Paik SG, Lee H, Lee JO (2007) Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130:1071-1082
39. Uematsu S, Akira S (2008) Toll-Like receptors (TLRs) and their ligands. Handb Exp Pharmacol 2008:1-20
40. Flo TH, Halaas Ø, Lien E, Ryan L, Teti G, Golenbock DT, Sundan A, Espevik T (2000) Human toll-like receptor 2 mediates monocyte activation by Listeria monocytogenes, but not by group B streptococci or lipopolysaccharide. J Immunol 164:2064-2069
41. Farhat K, Sauter KS, Brcic M, Frey J, Ulmer AJ, Jungi TW (2008) The response of HEK293 cells transfected with bovine TLR2 to established pathogen-associated molecular patterns and to bacteria causing mastitis in cattle. Vet Immunol Immunopathol 125:326-336
42. Ward PN, Field TR, Ditcham WGF, Maguin E, Leigh JA (2001) Identification and disruption of two discrete loci encoding hyaluronic acid capsule biosynthesis genes hasA, hasB, and hasC in Streptococcus uberis. Infect Immun 69:392-399
43. Czabanska A (2013) Immunochemical investigations of the cell envelope components isolated from Streptococcus uberis. PhD Thesis, University of Lübeck, Germany
44. Peterson GL (1979) Review of the Folin phenol protein quantitation method of Lowry, Rosebrough, Farr and Randall. Anal Biochem 100:201-220
45. Morath S, Geyer A, Hartung T (2001) Structure-function relationship of cytokine induction by lipoteichoic acid from Staphylococcus aureus. J Exp Med 193:393-398
46. Czabanska A, Neiwert O, Lindner B, Leigh J, Holst O, Duda KA (2012) Structural analysis of the lipoteichoic acids isolated from bovine mastitis Streptococcus uberis 233, Streptococcus dysgalactiae 2023 and Streptococcus agalactiae 0250. Carbohyd Res 361:200-205
47. Seo HS, Nahm MH (2009) Lipoprotein lipase and hydrofluoric acid deactivate both bacterial lipoproteins and lipoteichoic acids, but platelet-activating factor-acetylhydrolase degrades only lipoteichoic acids. Clin Vaccine Immunol 16:1187-1195
48. Bauer I, Günther J, Wheeler TT, Engelmann S, Seyfert H-M (2015) Extracellular milieu grossly alters pathogen-specific immune response of mammary epithelial cells. BMC Vet Res 11:67
49. Yang W, Zerbe H, Petzl W, Brunner RM, Günther 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-κ B in mammary epithelial cells and to quickly induce TNFα and interleukin-8 (CXCL8) expression in the udder. Mol Immunol 45:1385-1397
50. Ito S, Chen C, Satoh J, Yim S, Gonzalez FJ (2007) Dietary phytochemicals regulate whole-body CYP1A1 expression through an arylhydrocarbon receptor nuclear translocator-dependent system in gut. J Clin Invest 117:1940-1950
51. Fujii-Kuriyama Y, Kawajiri K (2010) Molecular mechanisms of the physiological functions of the aryl hydrocarbon (dioxin) receptor, a multifunctional regulator that senses and responds to environmental stimuli. Proc Jpn Acad Ser B Phys Biol Sci 86:40-53
52. Badal S, Delgoda R (2014) Role of the modulation of CYP1A1 expression and activity in chemoprevention. J Appl Toxicol 34:743-753
53. Field TR, Ward PN, Pedersen LH, Leigh JA (2003) The hyaluronic acid capsule of streptococcus uberis is not required for the development of infection and clinical mastitis. Infect Immun 71:132-139
54. Günther J, Esch K, Poschadel N, Petzl W, Zerbe H, Mitterhuemer S, Blum H, Seyfert HM (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. Infect Immun 79:695-707
55. Okumura CY, Nizet V (2014) Subterfuge and sabotage: evasion of host innate defenses by invasive gram-positive bacterial pathogens. Annu Rev Microbiol 68:439-458
56. Foster TJ (2009) Colonization and infection of the human host by staphylococci: adhesion, survival and immune evasion. Vet Dermatol 20:456-470
57. Moschioni M, Pansegrau W, Barocchi MA (2010) Adhesion determinants of the Streptococcus species. Microb Biotechnol 3:370-388
58. Sander LE, Davis MJ, Boekschoten MV, Amsen D, Dascher CC, Ryffel B, Swanson JA, Muller M, Blander JM (2011) Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 474:385-389
59. Fedtke I, Mader D, Kohler T, Moll H, Nicholson G, Biswas R, Henseler K, Götz F, Zähringer U, Peschel A (2007) A Staphylococcus aureus ypfP mutant with strongly reduced lipoteichoic acid (LTA) content: LTA governs bacterial surface properties and autolysin activity. Mol Microbiol 65:1078-1091
60. Ray A, Cot M, Puzo G, Gilleron M, Nigou J (2013) Bacterial cell wall macroamphiphiles: pathogen-/microbe-associated molecular patterns detected by mammalian innate immune system. Biochimie 95:33-42
61. Henneke P, Morath S, Uematsu S, Weichert S, Pfitzenmaier M, Takeuchi O, Müller A, Poyart C, Akira S, Berner R, Teti G, Geyer A, Hartung T, Trieu-Cuot P, Kasper DL, Golenbock DT (2005) Role of lipoteichoic acid in the phagocyte response to group B Streptococcus. J Immunol 174:6449-6455
62. Schröder NWJ, Morath S, Alexander C, Hamann L, Hartung T, Zähringer U, Göbel UB, Weber JR, Schumann RR (2003) Lipoteichoic acid (LTA) of Streptococcus pneumoniae and Staphylococcus aureus activates immune cells via Toll-like receptor (TLR)-2, lipopolysaccharide-binding protein (LBP), and CD14, whereas TLR-4 and MD-2 are not involved. J Biol Chem 278:15587-15594
63. Schmidt RR, Pedersen CM, Qiao Y, Zähringer U (2011) Chemical synthesis of bacterial lipoteichoic acids: an insight on its biological significance. Org Biomol Chem 9:2040-2052
64. Grant RG, Finch JM (1997) Phagocytosis of Streptococcus uberis by bovine mammary gland macrophages. Res Vet Sci 62:74-78
65. Almeida RA, Oliver SP (1995) Phagocytosis of Streptococcus uberis by bovine mammary macrophages: opsonizing effect of bovine antiserum. Zentralbl Veterinarmed B 42:331-337
66. Matthews KR, Almeida RA, Oliver SP (1994) Bovine mammary epithelial cell invasion by Streptococcus uberis. Infect Immun 62:5641-5646
67. Ki Shibata, Hasebe A, Sasaki T, Watanabe T (1997) Mycoplasma salivarium induces interleukin-6 and interleukin-8 in human gingival fibroblasts. FEMS Immunol Med Microbiol 19:275-283
68. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911-917