Innate immune response of bovine mammary gland to pathogenic bacteria responsible for mastitis

Journal of Infection

Volumn 54, Issue 4, 2007, Pages 399-409

  Oviedo Boyso, Javier ^a   Valdez Alarcón, Juan J ^a   Cajero Juárez, Marcos ^a   Ochoa Zarzosa, Alejandra ^a   López Meza, Joel E ^a   Bravo Patiño, Alejandro ^a   Baizabal Aguirre, Víctor M ^a  

^a UNIVERSIDAD MICHOACANA DE SAN NICOLÁS DE HIDALGO   (Mexico)

Author keywords

Bovine; Innate immunity; Mammary gland; Mastitis; Pathogenic bacteria

Indexed keywords

ANTIBIOTIC AGENT; CYTOKINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; INTERLEUKIN 8; RECOMBINANT INTERLEUKIN 8; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL FOOD; ARCANOBACTERIUM; ARTICLE; BACILLUS; BACTERIAL VIRULENCE; BREEDING LINE; CATTLE DISEASE; CYTOKINE PRODUCTION; DAIRY CATTLE; DRUG DESIGN; DRUG EFFICACY; ERADICATION THERAPY; ESCHERICHIA COLI; IMMUNE RESPONSE; INFECTION CONTROL; INFECTION SENSITIVITY; INNATE IMMUNITY; KLEBSIELLA PNEUMONIAE; LACTATION; MACROPHAGE; MAMMARY GLAND; MASTITIS; MILK PRODUCTION; MOLECULAR MECHANICS; NATURAL KILLER CELL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PARITY; PATHOGENESIS; PATHOLOGICAL ANATOMY; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS DYSGALACTIAE; STREPTOCOCCUS UBERIS;

ANIMALS; CATTLE; CYTOKINES; FEMALE; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE COCCI; IMMUNITY, NATURAL; MAMMARY GLANDS, ANIMAL; MASTITIS, BOVINE;

EID: 33947160550     PISSN: 01634453     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinf.2006.06.010     Document Type: Article

References (113)

1. Crist W.L., Harmon R.J., O'Leary J., and McAllister A.J. Mastitis and its control (1997), University of Kentucky Cooperative Extension Service
2. Dego O.K., van Dijk J.E., and Nederbragt H. Factors involved in the early pathogenesis of bovine Staphylococcus aureus mastitis with emphasis on bacterial adhesion and invasion. Vet Quart 24 (2002) 181-198
3. Bannerman D.D., Paape M.J., Lee J.W., Zhao X., Hope J.C., and Rainard P. Escherichia coli and Staphylococcus aureus elicit differential innate immune responses following intramammary infection. Clin Diagn Lab Immunol 11 (2004) 463-472
4. Schroeder J.W. Bovine mastitis and milking management. Mastitis control programs (April 1997), National Mastitis Council
5. Barkema H.W., Schukken Y.H., Lam T.J.M., Galligan D.T., Beiboer M.L., and Brand A. Estimation of interdependence among quarters of the bovine udder with subclinical mastitis and implications for analysis. J Dairy Sci 80 (1997) 1592-1599
6. Smith K.L., Hogan J.S., and Weiss W.P. Dietary vitamin E and selenium affect mastitis and milk quality. J Anim Sci 75 (1997) 1659-1665
7. Barkema H.W., Schukken Y.H., Lam T.J.G.M., Beiboer M.L., Benedictus G., and Brand A. Management practices associated with the incidence rate. J Dairy Sci 82 (1999) 1643-1654
8. Zadoks R.N., Allore H.G., Barkema H.W., Sampimon O.C., Wellenberg G.J., Gröhn Y.T., et al. Cow and quarter level risk factors for Streptococcus uberis and Staphylococcus aureus mastitis. J Dairy Sci 84 (2001) 2649-2663
9. Wagter L.C., Mallard B.A., Wilkie B.N., Leslie K.E., Boettcher P.J., and Dekkers J.C.M. A quantitative approach to classifying Holstein cows based on antibody responsiveness and its relationship to peripartum mastitis occurrence. J Dairy Sci 83 (2000) 488-498
10. Burvenich C., Van Merris V., Mehrzad J., Diez-Fraile A., and Duchateau L. Severity of E. coli mastitis is mainly determined by cow factors. Vet Res 34 (2003) 521-564
11. Mallard B.A., Dekkers J.C., Ireland M.J., Leslie K.E., Sharif S., Vankampen C.L., et al. Alteration in immune responsiveness during the peripartum period and its ramification on dairy cow and calf health. J Dairy Sci 81 (1998) 585-595
12. Hogan J.S., and Smith K.L. A practical look at environmental mastitis. Current concepts of bovine mastitis (August 1998), National Mastitis Council
13. Tollersrud T., Kenny K., Reitz Jr. A.J., and Lee J.C. Genetic and serologic evaluation of capsule production by bovine mammary isolates of Staphylococcus aureus and other Staphylococcus spp. from Europe and the United States. J Clin Microbiol 38 (2000) 2998-3003
14. Bradley A.J. Bovine mastitis: an evolving disease. Vet J 164 (2002) 116-128
15. Janeway Jr. C.A., and Medzhitov R. Innate immune recognition. Annu Rev Immunol 20 (2002) 197-216
16. Sordillo L.M., Shafer-Weaver K., and DeRosa D. Immunobiology of the mammary gland. J Dairy Sci 80 (1997) 1851-1865
17. Rivas A.L., Tadevosyan R., Quimby F.W., Coksaygan T., and Lein D.H. Identification of subpopulation of bovine mammary-gland phagocytes and evaluation of sensitivity and specificity of morphologic and functional indicators of bovine mastitis. Can J Vet Res 66 (2002) 165-172
18. Han S.H., Kim J.H., Martin M., Michalek S.M., and Nahm Moon H. Pneumococcal lipoteichoic acid (LTA) is not as potent as staphylococcal LTA in stimulating Toll-like receptor 2. Infect Immun 71 (2003) 5541-5548
19. Rosenberger C.M., and Finlay B.B. Phagocyte sabotage: disruption of macrophages signalling by bacterial pathogens. Nature Rev Mol Cell Biol 4 (2003) 385-396
20. Lembo A., Kalis C., Kirschning C.J., Mitolo V., Jirillo E., Wagner H., et al. Differential contribution of Toll-like receptors 4 and 2 to the cytokine response to Salmonella enterica serovar typhimurium and Staphylococcus aureus in mice. Infect Immun 71 (2003) 6058-6062
21. Takeuchi O., Hoshino K., and Akira S. Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J Immunol 165 (2000) 5392-5396
22. Beutler B. Interferences, questions and possibilities in Toll-like receptor signalling. Nature 430 (2004) 257-263
23. Wagner H. The immunobiology of the TLR9 subfamily. Trends Immunol 25 (2004) 381-386
24. Akira S. Toll-like receptor signaling. J Biol Chem 40 (2003) 38105-38108
25. Rooijakkers S.H.M., van Kessel K.P.M., and van Strijp J.A.G. Staphylococcal innate immune evasion. Trends Microbiol 13 (2005) 596-601 10.1016/j.tim.2005.10.002
26. Fournier B., and Philpott D.J. Recognition of Staphylococcus aureus by the innate immune system. Clin Microbiol Rev 3 (2005) 521-540
27. Gómez M.I., Lee A., Reddy B., Muir A., Soong G., Pitt A., et al. Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1. Nat Med 8 (2004) 842-848
28. Sordillo L.M., and Streicher K.L. Mammary gland immunity and mastitis susceptibility. J Mammary Gland Biol Neoplasia 7 (2002) 135-146
29. Myllys V., and Honkanen-Buzalski T. Effect of abrasion of teat orifice epithelium on development of bovine staphylococcal mastitis. J Dairy Sci 77 (1994) 446-452
30. Capuco A.V., Mein G.A., Nickerson S.C., Jack L.J.W., Wood D.L., Bright S.A., et al. Influence of pulsationless milking on teat canal keratin and mastitis. J Dairy Sci 77 (1994) 64-74
31. Miller R.H., Bitman J., Bright S.A., Wood D.L., and Capuco A.V. Effect of clinical and subclinical mastitis on lipid composition of teat canal keratin. J Dairy Sci 75 (1992) 1436-1442
32. Paulrud C.O. Basic concepts of the bovine teat canal. Vet Res Commun 29 (2005) 215-245
33. Soltys J., and Quinn M.T. Selective recruitment of T-cell subsets to the udder during staphylococcal and streptococcal mastitis: analysis of lymphocyte subsets and adhesion molecule expression. Infect Immun 67 (1999) 6293-6302
34. Zhang H., and Issekutz A.C. Down-regulation of monocyte transendothelial migration and endothelial adhesion molecule expression by fibroblast growth factor. Am J Pathol 160 (2002) 2219-2230
35. Rainard P. The complement in milk and defense of the bovine mammary gland against infections. Vet Res 34 (2003) 647-670
36. Boulanger D., Bureau F., Mélotte D., Mainil J., and Lekeux P. Increased nuclear factor κB activity in milk cells of mastitis-affected cows. J Dairy Sci 86 (2003) 1259-1267
37. Stein B.N., Gamble J.R., Pitson S.M., Vadas M.A., and Khew-Goodall Y. Activation of endothelial extracellular signal-regulated kinase is essential for neutrophil transmigration: potential involvement of a soluble neutrophil factor in endothelial activation. J Immunol 171 (2003) 6097-6104
38. Rainard P., and Riollet C. Mobilization of neutrophils and defense of the bovine mammary gland. Reprod Nutr Dev 43 (2003) 436-457
39. Nishimura T. Expression of potential lymphocyte trafficking mediator molecules in the mammary gland. Vet Res 34 (2003) 3-10
40. Cytokines. In: Abbas A.K., and Lichtman A.H. (Eds). Cellular and molecular immunology (2003), WB Saunders 243-274
41. Strindhall J., Lingren P.E., Löfgren S., and Kihlström E. Clinical isolates of Staphylococcus aureus vary in ability to stimulate cytokine expression in human. Scand J Immunol 67 (2005) 57-62
42. Mehrzad J., Duchateau L., Pyörälä S., and Burvenich C. Blood and milk neutrophil chemiluminescence and viability in primiparous and pluriparous dairy cows during late pregnancy, around parturition and early lactating period. J Dairy Sci 85 (2002) 3268-3276
43. Paape M.J., Bannerman D.D., Zhao X., and Lee J.W. The bovine neutrophil: structure and function in blood and milk. Vet Res 34 (2003) 597-627
44. Park Y.H., Joo Y.S., Park J.Y., Moon J.S., Kim S.H., Kwon N.H., et al. Characterization of lymphocytes subpopulations and major histocompatibility complex haplotypes of mastitis-resistant and susceptible cows. J Vet Sci 5 (2004) 29-39
45. Ohtsuka H., Koiwa M., Fukuda S., Satoh Y., Hayashi T., Hoshi F., et al. Changes in peripheral leukocyte subsets in dairy cows with inflammatory diseases after calving. J Vet Med Sci 66 (2004) 905-909
46. Dosogne H., Vangroenweghe F., and Burvenich C. Potential mechanism of action of J5 vaccine in protection against severe coliform mastitis. Vet Res 33 (2002) 1-12
47. + memory T cells. J Immunol 171 (2003) 5853-5864
48. Yamaguchi T., Hiratsuka M., Asai K., Kai K., and Kumagai K. Differential distribution of T lymphocytes subpopulations in the bovine mammary gland during lactating period. J Dairy Sci 82 (1999) 1459-1464
49. Alluwaimi A.M., and Cullor J.S. Cytokines gene expression patterns of bovine milk during middle and late stages of lactating period. J Vet Med B Infect Dis Vet Public Health 49 (2002) 105-110
50. Sordillo L.M., Snider M., Hughes H., Afseth G., Campos M., and Babiuk L.A. Pathological changes in bovine mammary glands following intramammary infusion of recombinant interleukin-2. J Dairy Sci 74 (1991) 4164-4174
51. Hornef M.W., Wick M.J., Rhen M., and Normark S. Bacterial strategies for overcoming host innate and adaptative immune responses. Nat Immunol 3 (2002) 1033-1040
52. Alluwaimi A.M. The cytokine of bovine mammary gland: prospects for diagnosis and therapy. Res Vet Sci 77 (2004) 211-222 10.1016/j.rvsc.2004.04.006
53. Havell E.A. Evidence that tumor necrosis factor has an important role in antibacterial resistance. J Immunol 143 (1989) 2894-2899
54. 3), tumor necrosis factor-α (TNF-α) and interleukin-6 (IL-6) in milk from healthy and naturally infected quarters of cows. Res Vet Sci 72 (2002) 17-21
55. Persson Waller K., Colditz I.G., Lun S., and Östensson K. Cytokines in mammary lymph and milk during endotoxin-induced bovine mastitis. Res Vet Sci 74 (2003) 31-36
56. Strichman R., and Samuel C.E. The role of gamma interferon in antimicrobial immunity. Curr Opin Microbiol 4 (2001) 251-259
57. Nonnecke B.J., Kimura K., Goff J.P., and Kehrli Jr. M.E. Effects of the mammary gland on functional capacities of blood mononuclear leukocyte populations from periparturient cows. J Dairy Sci 86 (2003) 2359-2368
58. Yamanaka H., Hisaeda K., Hagiwara K., Kirisawa R., and Iwai H. ELISA for bovine interleukin-1 receptor antagonist and its application to mastitic sera and whey. J Vet Med Sci 62 (2000) 661-664
59. Ohtsuka H., Kudo K., Mori K., Nagai F., Hatsugaya A., Tajima M., et al. Acute phase response in naturally occurring coliform mastitis. J Vet Med Sci 63 (2001) 675-678
60. Lee N.Y., Kawai K., Nakamura I., Tanaka T., Kumura H., and Shimazaki K. Susceptibilities against bovine lactoferrin with microorganisms isolated from mastitic milk. J Vet Med Sci 66 (2004) 1267-1269
61. Kai K., Komine Y., Komine K., Asai K., Kuroishi T., Kozutsumi T., et al. Effects of bovine lactoferrin by the intramammary infusion in cows with staphilococcal mastitis during the early non-lactating period. J Vet Med Sci 64 (2002) 873-878
62. Korhonen H., Marnila P., and Gill H.S. Milk immunoglobulins and complement factors. Br J Nutr Supply 84 (2000) S75-S80
63. Rainard P., and Poutrel B. Generation of complement fragment C5a in milk is variable among cows. J Dairy Sci 83 (2000) 945-951
64. Barrio M.B., Rainard P., and Poutrel B. Milk complement and the opsonophagocytosis and killing of Staphylococcus aureus mastitis isolates by bovine neutrophils. Microb Pathog 34 (2003) 1-9
65. Shuster D.E., Kehrli Jr. M.E., Rainard P., and Paape M. Complement fragment C5a and inflammatory cytokines in neutrophil recruitment during intramammary infection with Escherichia coli. Infect Immun 65 (1997) 3286-3292
66. Vangroenweghe F., Ducheteau L., and Burvenich C. Moderate inflammatory reaction during experimental Escherichia coli mastitis in primiparous cows. J Dairy Sci 87 (2004) 886-895
67. Mehrzad J., Duchateau L., and Burvenich C. Viability of milk neutrophils and severity of bovine coliform mastitis. J Dairy Sci 87 (2004) 4150-4162
68. Mehrzad J., Duchateau L., and Burvenich C. High milk neutrophil chemiluminescence limits the severity of bovine coliform mastitis. Vet Res 36 (2005) 101-116
69. Riollet C., Rainar P., and Poutrel B. Differential induction of complement fragment C5a and inflammatory cytokines during intramammary infections with Escherichia coli and Staphylococcus aureus. Clin Diagn Lab Immunol 7 (2000) 161-167
70. Hisaeda K., Hagiwara K., Eguchi J., Yamanaka H., Kirisawa R., and Iwai H. Interferon-γ and tumor necrosisi factor-α levels in sera and whey of cattle with naturally occurring mastitis. J Vet Med Sci 63 (2001) 1009-1011
71. Lee J.W., Paape M.J., Elsasser T.H., and Zhao X. Elevated milk soluble CD14 in bovine mammary glands challenged with Escherichia coli lipopolysaccharide. J Dairy Sci 86 (2003) 2382-2389
72. Lee J.W., Paape M.J., Elsasser T.H., and Zhao X. Recombinant soluble CD14 reduce severity of intramammary infection by Escherichia coli. Infect Immun 71 (2003) 4034-4039
73. Bannerman D.D., Paape M.J., Hare W.R., and Sohn E.J. Increased levels of LPS-binding protein in bovine blood and milk following bacterial lipopolysaccharide challenge. J Dairy Sci 86 (2003) 3128-3137
74. Rambeaud M., Almeida R.A., Pghetti G.M., and Oliver S.P. Dynamics of leukocytes and cytokines during experimentally induced Streptococcus uberis mastitis. Vet Immunol Immunopathol 96 (2003) 193-205 10.1016/j.vetimm.2003.08.008
75. Bannerman D.D., Paape M.J., Goff J.P., Kimura K., Lippolis J.D., and Hope J.C. Innate immune response to intramammary infection with Serratia marcescens and Streptococcus uberis. Vet Res 35 (2004) 681-700
76. Bannerman D.D., Paape M.J., Hare W.R., and Hope J.C. Characterization of the bovine innate immune response to intramammary infection with Klebsiella pneumoniae. J Dairy Sci 87 (2004) 2420-2432
77. Bannerman D.D., Chockalingam A., Paape M.J., and Hope J.C. The bovine innate immune response during experimentally-induced Pseudomonas aeruginosa mastitis. Vet Immunol Immunopathol 107 (2005) 201-215 10.1016/j.vetimm.2005.04.012
78. Erskine R.J., Walker R.D., Bolin C.A., Bartlett P.C., and White D.G. Trends in antibacterial susceptibility of mastitis pathogens during a seven-year period. J Dairy Sci 85 (2002) 1111-1118
79. Leitner G., Eligulashvily R., Krifucks O., Perl S., and Saran A. Immune cell differentiation in mammary gland tissues and milk of cows chronically infected with Staphylococcus aureus. J Vet Med B Infect Dis Vet Public Health 50 (2003) 45-52
80. Riollet C., Rainard P., and Poutrel B. Cell subpopulations and cytokine expression in cow milk in response to chronic Staphylococcus aureus infection. J Dairy Sci 84 (2001) 1077-1084
81. Zecconi A., Binda E., Borromeo V., and Piccinini R. Relationship between some Staphylococcus aureus pathogenic factors and growth rates somatic cell counts. J Dairy Res 72 (2005) 203-208
82. Foster T.J. The Staphylococcus aureus superbug. J Clin Invest 12 (2004) 1693-1696
83. Götz F. Staphylococcus and biofilms. Mol Microbiol 43 (2002) 1367-1378
84. Almeida R.A., Matthews K.R., Cifrian E., Guidry A.J., and Oliver S.P. Staphylococcus aureus invasion of bovine mammary epithelial cells. J Dairy Sci 79 (1996) 1021-1026
85. Hensen S.M., Pavicic M.J.A.M.P., Lohuis J.A.C.M., and Poutrel B. Use of bovine primary mammary epithelial cells for the comparison of adherence and invasion ability of Staphylococcus aureus strain. J Dairy Sci 83 (2000) 418-429
86. Dziewanowska K., Patti J.M., Deobald C.F., Bayles K.W., Trumble W.R., and Bohach G.A. Fibronectin binding protein and cell tyrosine kinase are required for internalization of Staphylococcus aureus by epithelial cells. Infect Immun 67 (1999) 4673-4678
87. Peacock S.J., Foster T.J., Cameron B.J., and Berendt A.R. Bacterial fibronectin-binding proteins and endothelial cell surface fibronectin mediate adherence of Staphylococcus aureus to resting endothelial cells. Microbiology 145 (1999) 3477-3486
88. Massey R.C., Kantzanou M.N., Fowler T., Day N.P.J., Schofield K., Wann E.R., et al. Fibronectin-binding protein A of Staphylococcus aureus has multiple, substituting, binding regions that mediate adherence to fibronectin and invasion of endothelial cells. Cell Microbiol 3 (2001) 839-851
89. Alexander E.H., and Hudson M.C. Factors influencing the internalization of Staphylococcus aureus and impacts on the course of infections in humans. Appl Microbiol Biotechnol 56 (2001) 361-366
90. Haggar A., Hussain M., Lönnies H., Herrmann M., Norrby-Teglund A., and Flock J.I. Extracellular adherence protein from Staphylococcus aureus enhances internalization into eukaryotic cells. Infect Immun 5 (2003) 2310-2317
91. Harraghy N., Hussain M., Haggar A., et al. The adhesive and immunomodulating properties of the multifunctional Staphylococcus aureus protein Eap. Microbiology 149 (2003) 2701-2707
92. Brouillette E., Grondin G., Shkreta L., Lacasse P., and Talbot B.G. In vivo and in vitro demonstration that Staphylococcus aureus is an intracellular pathogen in the presence or absence of fibronectin-binding proteins. Microb Pathog 35 (2003) 159-168
93. Lee L.Y.L., Höök M., Haviland D., Wetsel R.A., Yonter E.O., Syribeys P., et al. Inhibition of complement activation by a secreted Staphylococcus aureus protein. J Infect Dis 190 (2004) 571-579
94. Chavakis T., Hussain M., Kanse S.M., Peters G., Bretzel R.G., Flock J.I., et al. Staphylococcus aureus extracellular adherence protein serves as anti-inflammatory factor by inhibiting the recruitment of host leukocytes. Nat Med 7 (2002) 687-693
95. Jin T., Bokarewa M., Foster T., Mitchel J., Higgins J., and Tarkowski A. Staphylococcus aureus resists human defensins by production of staphylokinase, a novel bacterial evasion mechanism. J Immunol 172 (2004) 1169-1176
96. Rooijakkers H.M.S., van Wamel W.J.B., Ruyken M., van Kessel K.P.M., and van Strijp J.A.G. Anti-opsonic properties of staphylokinase. Microb Infect 7 (2005) 476-484
97. Ferens W.A., Davis W.C., Hamilton M.Y., Park Y.H., Deobald C.F., Fox L., et al. Activation of bovine lymphocyte subpopulations by staphylococal enterotoxin C. Infect Immun 66 (1998) 573-580
98. Kuroishi T., Komine K., Kai K., Itagaki M., Kobayashi J., Ohta M., et al. Concentrations and specific antibodies to staphylococcal enterotixin-C and toxic shock syndrome toxin-1 in bovine glands secretions, and inflammatory response to the intramammary inoculation of these toxins. J Vet Med Sci 65 (2003) 899-906
99. Ebling T.L., Fox L.K., Bayles K.W., Bohach G.A., Byrne K.M., Davis W.C., et al. Bovine mammary immune response to an experimental intramammary infection with a Staphylococcus aureus strain containing a gene from staphylococcal esterotoxin C1. J Dairy Sci 84 (2001) 2044-2050
100. Orwin P.M., Fitzgerald J.R., Leung D.Y.M., Gutiérrez J.A., Bohach G.A., and Schlievert P.M. Characterization of Staphylococcus aureus enterotoxin L. Infect Immun 71 (2003) 2916-2919
101. Alluwaimi A.M., Leutenegger C.M., Farver T.B., Rossitto P.V., Smith W.L., and Cullor J.S. The cytokine markers in Staphylococcus aureus mastitis of bovine mammary gland. J Vet Med B Infect Dis Vet Public Health 50 (2003) 105-111
102. Leitner G., Yadlin B., Glickman A., Chaffer M., and Saran A. Systemic and local immune response of cows to intramammary infection with Staphylococcus aureus. Res Vet Sci 69 (2000) 181-184
103. Rivas A.L., Tadevosyan R., Quimby F.W., and Lein D.H. Blood and milk cellular immune responses of mastitic non-periparturient cows inoculated with Staphylococcus aureus. Can J Vet Res 66 (2002) 125-131
104. Grönlund U., Johannisson A., and Persson Waller K. Changes in blood and milk lymphocyte sub-populations during acute and chronic phases of Staphylococcus aureus induced bovine mastitis. Res Vet Sci 80 (2006) 147-154
105. Bayles K.W., Wesson C.A., Liou L.E., Fox L.K., Bohach G.A., and Trumble W.R. Intracellular Staphylococcus aureus escapes the endosome and induces apoptosis in epithelial cells. Infect Immun 66 (1998) 336-342
106. Anaya-López J.L., Contreras-Guzmán O.E., Cárabez-Trejo A., Baizabal-Aguirre V.M., López-Meza J.E., Valdez-Alarcón J.J., et al. Invasive potential of bacterial isolates associated with subclinical bovine mastitis. Res Vet Sci (2006) 10.1016/j.rvsc.2006.02.002
107. Hamill R.J., Vann J.M., and Proctor R.A. Phagocytosis of Staphylococcus aureus by cultured bovine aortic endothelial cells: model for postadherence events in endovascular infections. Infect Immun 54 (1986) 833-836
108. Vann J.M., and Proctor R.A. Ingestion of Staphylococcus aureus by bovine endothelial cells results in time and inoculum-dependent damage to endothelial cell monolayers. Infect Immun 55 (1987) 2155-2163
109. Strandberg Y., Gray C., Vuocolo T., Donaldson L., Broadway M., and Tellam R. Lipopolysaccharide and lipoteichoic acid induce different innate immune responses in ovine mammary epithelial cells. Cytokine 31 (2005) 72-86 10.1016/j.cyto.2005.02.010
110. Yao L., Benguadil V., Lowy F.D., Gibbons J.J., Hatcher V.B., and Berman J.W. Internalization of Staphylococcus aureus by endothelial cells induces cytokine gene expression. Infect Immun 63 (1995) 1835-1839
111. Erskine R.J., Bartlett P.C., Tavernier S.R., Fowler L.H., Walker R.D., Seguin J.H., et al. Recombinant bovine interleukin-2 and dry cow therapy: efficacy to cure and prevent intramammary infections, safety, and effect on gestation. J Dairy Sci 81 (1998) 107-115
112. Takahashi H., Odai M., Mitani K., Inumaru S., Arai S., Horino R., et al. Effect of intramammary injection of rboGM-CSF on milk levels of chemiluminescence activity, somatic cell count, and Staphylococcus aureus count in Holstein cows with S. aureus subclinical mastitis. Can J Vet Res 68 (2004) 182-187
113. Takahashi H., Komatsu T., Hodate K., Horino R., and Yokomiso Y. Effect of intramammary injection of rboIL-8 on milk levels of somatic cell count, chemiluminescence activity and shedding patterns of total bacteria and S. aureus in Holstein cows with naturally infected-subclinical mastitis. J Vet Med B Infect Dis Vet Public Health 52 (2005) 32-37