Vet Med - Czech, 2006, 51(9):437-447 | DOI: 10.17221/5571-VETMED

The role of neutrophil apoptosis during experimentally induced Streptococcus uberismastitis

Z. Sladek1, D. Rysanek2, H. Ryznarova1, M. Faldyna2
1 Mendel University of Agriculture and Forestry, Brno, Czech Republic
2 Veterinary Research Institute, Brno, Czech Republic

The object of the study was to determine if apoptosis of neutrophils and their subsequent elimination from the mammary gland by macrophages are modulated by an infection of Streptococcus uberis. The experiments were carried out in 5 clinically normal Holstein × Bohemian Red Pied crossbred heifers, aged 14 to 18 months. Before the experimental infection mammary glands were stimulated by PBS as a control. The samples of cell populations were obtained by lavages of the mammary glands in 4 intervals (24, 48, 72 and 168 h) after the PBS and after the experimental infection. Flow cytometry was used to determine the Annexin V positive and propidium jodide negative neutrophils (Annexin V+/PI-). The light microscopy was used to determine apoptotic neutrophils and myeloperoxidase (MPO) positive macrophages. After PBS and S. uberis administration the total number of both Annexin V+/PI- neutrophils and karyopycnotic neutrophils peaked at 24 hours. The highest percentages of Annexin V+/PI- neutrophils were detected at 72 h after PBS and S. uberis, respectively. The highest percentages of karyopycnotic neutrophils were detected at 72 h after PBS and 168 h after S. uberis, respectively. The total number of MPO+ macrophages was the highest at 24 h after PBS and 72 h after S. uberis. The percentage of MPO+ macrophages was the highest at 72 h after PBS and S. uberis. The results of this study demonstrate that during experimental infection of the mammary gland by S. uberis, the apoptosis of neutrophils is modulated. Apoptosis of neutrophils and the subsequent phagocytosis of apoptotic neutrophils by macrophages were delayed. This may cause the transition of the acute inflammatory reaction to a chronic state.

Keywords: Streptococcus uberis; experimental infection; neutrophil apoptosis

Published: September 30, 2006  Show citation

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Sladek Z, Rysanek D, Ryznarova H, Faldyna M. The role of neutrophil apoptosis during experimentally induced Streptococcus uberismastitis. Vet Med - Czech. 2006;51(9):437-447. doi: 10.17221/5571-VETMED.
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    References

    1. Alluwaimi A.M. (2004): The cytokines of bovine mammary gland: prospects for diagnosis and therapy. Research in Veterinary Science, 77, 211-222. Go to original source... Go to PubMed...
    2. Bannerman D.D., Paape M.J., Goff J.P., Kimura K., Lippolis J.D., Hope J.C. (2004a): Innate immune response to intramammary infection with Serratia marcescens and Streptococcus uberis. Veterinary Research, 35, 681-700. Go to original source... Go to PubMed...
    3. Bannerman D.D., Paape M.J., Hare W.R., Hope J.C. (2004b): Characterization of the bovine innate immune response to intramammary infection with Klebsiella pneumoniae. Journal of Dairy Science, 87, 2420-2432. Go to original source... Go to PubMed...
    4. Bannerman D.D., Paape M.J., Lee J.W., Zhao X., Hope J.C., Rainard P. (2004c): Escherichia coli and Staphylococcus aureus elicit differential innate immune responses following intramammary infection. Clinical and Diagnostic Laboratory Imunology, 11, 463-472. Go to original source... Go to PubMed...
    5. Boutet P., Boulanger D., Gillet L., Vanderplasschen A., Closset R., Bureau F., Lekeux P. (2004): Delayed neutrophil apoptosis in bovine subclinical mastitis. Journal of Dairy Science, 87, 4104-4114. Go to original source... Go to PubMed...
    6. DeLeo F.R. (2004): Modulation of phagocyte apoptosis by bacterial pathogens. Apoptosis, 9, 399-413. Go to original source... Go to PubMed...
    7. Duffield J.S. (2003): The inflammatory macrophage: a story of Jekyll and Hyde. Clinical Science (London), 104, 27-38. Go to original source... Go to PubMed...
    8. Engelich G., White M., Hartshorn K.L. (2001): Neutrophil survival is markedly reduced by incubation with influenza virus and Streptococcus pneumoniae: role of respiratory burst. Journal of Leukocyte Biology, 69, 50-56. Go to original source...
    9. Grant R.G., Finch J.M. (1996): Phagocytosis of Streptococcus uberis by bovine mammary gland macrophages. Research in Veterinary Science, 62, 74-78. Go to original source... Go to PubMed...
    10. Haslett C., Savill J.S., Whyte M.K., Stern M., Dransfield I., Meagher L.C. (1994): Granulocyte apoptosis and the control of inflammation. Philosophical Transactions of the Royal Society of London. Series B, Biological Science, 327-333.
    11. Henson P.M., Zanolari B., Schwartzman N.A, Hong S.R. (1978): Intracellular control of human neutrophil secretion. I. C5a-induced stimulus-specific desensitisation and effect of cytochalasin B. Journal of Imunology, 121, 851-855. Go to original source...
    12. Hill A.W. (1988): Pathogenicity of two strains of Streptococcus uberis infused into lactating and non-lactating bovine mammary glands. Research in Veterinary Science, 45, 400-404. Go to original source... Go to PubMed...
    13. Hill A.W., Shears A.L., Hibbitt K.G. (1978): The elimination of serum-resistant Escherichia coli from experimentally infected single mammary glands of healthy cows. Research in Veterinary Science, 25, 89-93. Go to original source... Go to PubMed...
    14. Hill A.W., Finch J.M., Field T.R., Leigh J.A. (1994): Immune modification of the pathogenesis of Streptococcus uberis mastitis in the dairy cow. FEMS Immunology and Medical Mikrobiology, 8, 109-117. Go to original source... Go to PubMed...
    15. IDF (1995): International Dairy Federation, Milk-Enumeration of somatic cells. International IDF Standard 148A, 8 pp.
    16. Jayarao B.M., Gillespie B.E., Lewis M.J., Dowlen H.H., Oliver S.P. (1999): Epidemiology of Streptococcus uberis intramammary infections in a dairy herd. Zentralblatt fur Veterinarmedizin, Reihe B, 46, 433-442. Go to original source... Go to PubMed...
    17. Kettritz R., Gaido M.L., Haller H., Luft F.C., Jennette C.J., Falk R.J. (1998): Interleukin-8 delays spontaneous and tumor necrosis factor-alpha-mediated apoptosis of human neutrophils. Kidney International, 53, 84-91. Go to original source... Go to PubMed...
    18. King J.S. (1981): Streptococcus uberis: a review of its role as a causative organism of bovine mastitis. II. Control of infection. The British Veterinary Journal, 137, 160-165. Go to original source... Go to PubMed...
    19. Kobayashi S.D., DeLeo F.R. (2004): An apoptosis differentiation programme in human polymorphonuclear leucocytes. Biochemical Society Transactions, 32, 474-476. Go to original source... Go to PubMed...
    20. Kobayashi S.D., Braughton K.R., Whitney A.R., Voyich J.M., Schwan T.G., Musser J.M., DeLeo F.R. (2003): Bacterial pathogens modulate an apoptosis differentiation program in human neutrophils. Proceedings of the National Academy of Sciences of the U. S. A., 100, 10948-10953. Go to original source... Go to PubMed...
    21. Koch C.C., Esteban D.J., Chin A.C., Olson M.E., Read R.R., Ceri H., Morck D.W., Buret A.G. (2000): Apoptosis, oxidative metabolism and interleukin-8 production in human neutrophils exposed to azithromycin: effects of Streptococcus pneumoniae. The Journal of Antimicrobial Chemotherapy, 46, 19-26. Go to original source... Go to PubMed...
    22. Mantovani A., Sica A., Sozzani S., Allavena P., Vecchi A., Locati M. (2004): The chemokine system in diverse forms of macrophage activation and polarization. Trends in Imunology, 25, 677-686. Go to original source... Go to PubMed...
    23. Matouskova O., Chalupa J., Cigler M., Hruska K. (1992): STAT Plus - Manual 1.01 (in Czech). 1st ed. Veterinary Research Institute, Brno. 168 pp.
    24. Murray J., Barbara J.A., Dunkley S.A., Lopez A.F., Van Ostade X., Condliffe A.M., Dransfield I., Haslett C., Chilvers E.R. (1997): Regulation of neutrophil apoptosis by tumor necrosis factor-alpha: requirement for TNFR55 and TNFR75 for induction of apoptosis in vitro. Blood, 90, 2772-2783. Go to original source...
    25. Oliver S.P., Almeida R.A., Gillespie B.E., Headrick S.J., Dowlen H.H., Johnson D.L., Lamar K.C., Chester S.T., Moseley W.M. (2004): Extended ceftiofur therapy for treatment of experimentally-induced Streptococcus uberis mastitis in lactating dairy cattle. Journal of Dairy Science, 87, 3322-3329. Go to original source... Go to PubMed...
    26. Paape M.J., Bannerman D.D., Zhao X., Lee J.W. (2003): The bovine neutrophil: Structure and function in blood and milk. Veterinary Research, 34, 597-627. Go to original source... Go to PubMed...
    27. Phuektes P., Mansell P.D., Dyson R.S., Hooper N.D., Dick J.S., Browning G.F. (2001): Molecular epidemiology of Streptococcus uberis isolates from dairy cows with mastitis. Journal of Clinical Mikrobiology, 39, 1460- 1466. Go to original source... Go to PubMed...
    28. Rambeaud M., Almeida R.A., Pighetti G.M., Oliver S.P. (2003): Dynamics of leukocytes and cytokines during experimentally induced Streptococcus uberis mastitis. Veterinary Immunology and Immunopathology, 96, 193-205. Go to original source... Go to PubMed...
    29. Riollet C., Rainard P., Poutrel B. (2000): Differential induction of complement fragment C5a and inflammatory cytokines during intramammary infections with Escherichia coli and Staphylococcus aureus. Clinical and Diagnostic Laboratory Imunology, 7, 161-167. Go to original source... Go to PubMed...
    30. Rysanek D., Sladek Z., Vasickova D., Faldyna M. (2005): Effect of certain inducers of neutrophils migration into the bovine mammary gland on their apoptosis expression in a subsequent in vitro cultivation. Physiological Research, 54, 305-312. Go to original source... Go to PubMed...
    31. Savill J. (1992): Macrophage recognition of senescent neutrophils. Clinical Science (London), 83, 649-655. Go to original source... Go to PubMed...
    32. Savill J., Wyllie A.H., Henson J.E., Walport M.J., Henson P.M., Haslett CH. (1989): Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. The Journal of Clinical Investigation, 83, 865-867. Go to original source... Go to PubMed...
    33. Schalm O.W., Lasmanis J., Jain N.C. (1976): Conversion of chronic staphylococcal mastitis to acute gangrenous mastitis after neutropenia in blood and bone marrow produced by an equine anti-bovine leukocyte serum. American Journal of Veterinary Research, 37, 885-890.
    34. Sladek Z., Rysanek D. (1999): Ultrastructure of phagocytes from mammary glands of non-pregnant heifers. Anatomia, Histologia, Embryologia, 28, 291-298. Go to original source... Go to PubMed...
    35. Sladek Z., Rysanek D. (2000a): Morphology of apoptosis of polymorphonuclear leukocytes isolated from mammary glands of unbred heifers. Veterinarni Medicina, 45, 71-81.
    36. Sladek Z., Rysanek D. (2000b): Apoptosis of poly-morphonuclear leukocytes of the juvenile bovine mammary glands during induced influx. Veterinary Research, 31, 553-563. Go to original source... Go to PubMed...
    37. Sladek Z., Rysanek D. (2001): Neutrophil apoptosis during resolution of bovine mammary gland injury. Research in Veterinary Science, 70, 41-46. Go to original source... Go to PubMed...
    38. Sladek Z., Rysanek D., Faldyna M. (2002): Activation of phagocytes during initiation and resolution of mammary gland injury induced by lipopolysaccharide. Veterinary Research, 33, 191-204. Go to original source... Go to PubMed...
    39. Sladek Z., Rysanek D., Faldyna, M. (2005a): Effect of Staphylococcus aureus and Streptococcus uberis on apoptosis of bovine mammary gland tissue pool neutrophils in vitro. Veterinarni Medicina, 50, 11-23. Go to original source...
    40. Sladek Z., Rysanek D., Ryznarova H., Faldyna M. (2005b): Neutrophil apoptosis during experimentally induced Staphylococcus aureus mastitis. Veterinary Research, 36, 629-643. Go to original source... Go to PubMed...
    41. Tatsuta T., Cheng J., Mountz J.D. (1996): Intracellular IL-1beta is an inhibitor of Fas-mediated apoptosis. Journal of Imunology, 157, 3949-3957. Go to original source...
    42. Thomas L.H., Haider W., Hill A.W., Cook R.S. (1994): Pathologic findings of experimentally induced Streptococcus uberis infection in the mammary gland of cows. American Journal of Veterinary Research, 55, 1723-1728. Go to original source...
    43. Ulett G.C., Adderson E.E. (2005): Nitric oxide is a key determinant of group B streptococcus-induced murine macrophage apoptosis. The Journal of Infectious Diseases, 191, 1761-1770. Go to original source... Go to PubMed...
    44. Van Oostveldt K., Dosogne H., Burvenich C., Paape M.J., Brochez V., Van den Eeckhout E. (1999): Flow cytometric procedure to detect apoptosis of bovine polymorphonuclear leukocytes in blood. Veterinar y Immunology and Immunopathology, 70, 125-133. Go to original source... Go to PubMed...
    45. Van Oostveldt K., Paape M.J., Dosogne H., Burvenich C. (2002): Effect of apoptosis on phagocytosis, respiratory burst and CD18 adhesion receptor expression of bovine neutrophils. Domestic Animal Endocrinology, 22, 37-50. Go to original source... Go to PubMed...
    46. Vermes I., Haanen C., Stefferns-Naaken H., Reutelingsperger C.P. (1995): A novel assay for apoptosis: flow cytometry detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. Journal of Imunology, 184, 39-51. Go to original source... Go to PubMed...
    47. Wang P.L., Shirasu S., Daito M., Ohura K. (2001): Streptococcus mutans lipoteichoic acid-induced apoptosis in cultured dental pulp cells from human deciduous teeth. Biochemical and Biophysical Research Communications, 281, 957-961. Go to original source... Go to PubMed...
    48. Weiss S.J. (1989): Tissue destruction by neutrophils. The New England Journal of Medicine, 320, 365-376. Go to original source... Go to PubMed...
    49. Yamamoto A., Taniuchi S., Tsuji S., Hasui M., Kobayashi Y. (2002): Role of reactive oxygen species in neutrophil apoptosis following ingestion of heat-killed Staphylococcus aureus. Clinical and Experimental Imunology, 129, 479-484. Go to original source... Go to PubMed...
    50. Zysk G., Bejo L., Schneider-Wald B.K., Nau R., Heinz H. (2000): Induction of necrosis and apoptosis of neutrophil granulocytes by Streptococcus pneumoniae. Clinical and Experimental Imunology, 122, 61-66. Go to original source... Go to PubMed...

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