Local immunization impacts the response of dairy cows to Escherichia coli mastitis

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Herry, Vincent ^a   Gitton, Christophe ^b   Tabouret, Guillaume ^a   Répérant, Maryline ^b   Forge, Laurine ^a   Tasca, Christian ^a   Gilbert, Florence B ^b   Guitton, Edouard ^c   Barc, Céline ^c   Staub, Christophe ^c   Smith, David G E ^d   Germon, Pierre ^b   Foucras, Gilles ^a   Rainard, Pascal ^b  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b UNIVERSITÉ DE TOURS   (France)

^c CEMAGREF   (France)

^d HERIOT WATT UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE;

ANIMAL; BLOOD; BOVINE; BOVINE MASTITIS; ESCHERICHIA COLI; FEMALE; IMMUNIZATION; IMMUNOLOGY; MICROBIOLOGY; PATHOGENICITY; PROCEDURES; RANDOMIZATION;

ANIMALS; CATTLE; CYTOKINES; ESCHERICHIA COLI; FEMALE; IMMUNIZATION; MASTITIS, BOVINE; RANDOM ALLOCATION;

EID: 85020541794     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-03724-7     Document Type: Article

References (59)

1. Hogan, J., & Smith, K. L. Coliform mastitis. Vet. Res. 34, 507-519 (2003).
2. Hill, A. W. Factors influencing the outcome of Escherichia coli mastitis in the dairy cow. Res. Vet. Sci. 31, 107-112 (1981).
3. Van Werven, T., et al. Preinfection in vitro chemotaxis, phagocytosis, oxidative burst, and expression of CD11/CD18 receptors and their predictive capacity on the outcome of mastitis induced in dairy cows with Escherichia coli. J. Dairy Sci. 80, 67-74 (1997).
4. Dosogne, H., Vangroenweghe, F., & Burvenich, C. Potential mechanism of action of J5 vaccine in protection against severe bovine coliform mastitis. Vet. Res. 33, 1-12 (2002).
5. Aujla, S. J., Dubin, P. J., & Kolls, J. K. Th17 cells and mucosal host defense. Semin. Immunol. 19, 377-382 (2007).
6. Khader, S. A., Gaffen, S. L., & Kolls, J. K. Th17 cells at the crossroads of innate and adaptive immunity against infectious diseases at the mucosa. Mucosal Immunol 2, 403-411 (2009).
7. Zhao, Y., et al. Shifted T Helper Cell Polarization in a Murine Staphylococcus aureus Mastitis Model. PLoS ONE 10, e0134797, doi:10.1371/journal.pone.0134797 (2015).
8. Porcherie, A., et al. IL-17A Is an Important Effector of the Immune Response of the Mammary Gland to Escherichia coli Infection. J. Immunol. 196, 803-812, doi:10.4049/jimmunol.1500705 (2016).
9. Rainard, P., et al. Antigen-Specific Mammary Inflammation Depends on the Production of IL-17A and IFN-gamma by Bovine CD4+T Lymphocytes. PLoS ONE 10, e0137755 (2015).
10. Agabriel, J. Almentation des bovins, ovins et caprins: besoins des animaux. Valeur des aliments. Tables INRA 2007. Mise a jour 2010. p. (Editions Quae, 2010).
11. Bramley, A. J. Variations in the susceptibility of lactating and non-lactating bovine udders to infection when infused with Escherichia coli. J. Dairy Res. 43, 205-211 (1976).
12. Hill, A. W., Shears, A. L., & Hibbitt, K. G. The survival of serum resistant Escherichia coli in the bovine mammary gland following experimental infection. Res. Vet. Sci. 26, 32-37 (1979).
13. Bannerman, D. D., et al. Escherichia coli and Staphylococcus aureus elicit differential innate immune responses following intramammary infection. Clin. Diagn. Lab. Immunol. 11, 463-472 (2004).
14. Shpigel, N. Y., et al. Efficacy of cefquinome for treatment of cows with mastitis experimentally induced using Escherichia coli. J. Dairy Sci. 80, 318-323 (1997).
15. Blum, S., Sela, N., Heller, E. D., Sela, S., & Leitner, G. Genome Analysis of Bovine-Mastitis-Associated Escherichia coli O32:H37 Strain P4. J. Bacteriol. 194, 3732 (2012).
16. Bougarn, S., et al. Muramyl dipeptide synergizes with Staphylococcus aureus lipoteichoic acid to recruit neutrophils in the mammary gland and to stimulate mammary epithelial cells. Clin. Vaccine Immunol. 17, 1797-1809 (2010).
17. Bouvier-Muller, J., et al. Response to dietary-induced energy restriction in dairy sheep divergently selected for resistance or susceptibility to mastitis. Journal of Dairy Science 99, 480-492 (2016).
18. Rainard, P., Sarradin, P., Paape, M. J., & Poutrel, B. Quantification of C5a/C5a(desArg) in bovine plasma, serum and milk. Vet. Res. 29, 73-88 (1998).
19. Rainard, P., et al. The chemokine CXCL3 is responsible for the constitutive chemotactic activity of bovine milk for neutrophils. Mol. Immunol. 45, 4020-4027 (2008).
20. Rainard, P., & Paape, M. J. Sensitization of the bovine mammary gland to Escherichia coli endotoxin. Vet.Res. 28, 231-238 (1997).
21. Rainard, P., et al. T helper 17-Associated cytokines are produced during antigen-specific inflammation in the mammary gland. PLoS ONE 8, e63471 (2013).
22. Auboiron, S., et al. Characterization and amino-Terminal sequence of apolipoprotein AI from plasma high density lipoproteins in the preruminant calf, Bos spp. Biochem. Biophys. Res. Commun. 166, 833-839 (1990).
23. Iwaki, T., & Castellino, F. J. A single plasmid transfection that offers a significant advantage associated with puromycin selection in Drosophila Schneider S2 cells expressing heterologous proteins. Cytotechnology 57, 45-49 (2008).
24. Bougarn, S., et al. Staphylococcal-Associated molecular patterns enhance expression of immune defense genes induced by IL-17 in mammary epithelial cells. Cytokine 56, 749-759 (2011).
25. Barrio, M. B., Rainard, P., Gilbert, F. B., & Poutrel, B. Assessment of the opsonic activity of purified bovine sIgA following intramammary immunization of cows with Staphylococcus aureus. J. Dairy Sci. 86, 2884-2894 (2003).
26. Rainard, P. Experimental mastitis with Escherichia coli: sequential response of leukocytes and opsonic activity in milk of immunised and unimmunised cows. Annales de Recherches Veterinaires 14, 281-286 (1983).
27. Metsalu, T., & Vilo, J. ClustVis: a web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap. Nucleic Acids Res 43, W566-W570 (2015).
28. Rainard, P., & Poutrel, B. Deposition of complement components on Streptococcus agalactiae in bovine milk in the absence of inflammation. Infect. Immun. 63, 3422-3427 (1995).
29. Harmon, R. J., & Newbould, F. H. S. Neutrophil leukocyte as a source of lactoferrin in bovine milk. Am. J. Vet. Res. 41, 1603-1606 (1980).
30. Harmon, R. J., Schanbacher, F. L., Ferguson, L. C., & Smith, K. L. Changes in lactoferrin, immunoglobulin G, bovine serum albumin, and alpha-lactalbumin during acute experimental and natural coliform mastitis in cows. Infect. Immun. 13, 533-542 (1976).
31. 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. 7, 161-167 (2000).
32. Vangroenweghe, F., Duchateau, L., & Burvenich, C. Moderate inflammatory reaction during experimental Escherichia coli mastitis in primiparous cows. J. Dairy Sci. 87, 886-895 (2004).
33. Suojala, L., Orro, T., Jarvinen, H., Saatsi, J., & Pyörälä, S. Acute phase response in two consecutive experimentally induced E. coli intramammary infections in dairy cows. Acta Vet. Scand. 50, 18 (2008).
34. Kehrli, M. E. Jr., & Harp, J. A. Immunity in the mammary gland. Vet. Clin. North Am. Food Anim. Pract 17, 495-516 (2001).
35. Sordillo, L. M., & Babiuk, L. A. Controlling acute Escherichia coli mastitis during the periparturient period with recombinant bovine interferon gamma. Vet. Microbiol. 28, 189-198 (1991).
36. Sordillo, L. M., & Peel, J. E. Effect of interferon-gamma on the production of tumor necrosis factor during acute Escherichia coli mastitis. J. Dairy Sci. 75, 2119-2125 (1992).
37. Cua, D. J., & Tato, C. M. Innate IL-17-producing cells: the sentinels of the immune system. Nat Rev Immunol 10, 479-489 (2010).
38. Peckham, R. K., et al. Two distinct populations of bovine IL-17(+) T-cells can be induced and WC1(+)IL-17(+)gammadelta T-cells are effective killers of protozoan parasites. Sci. Rep. 4, 5431 (2014).
39. Ferretti, S., Bonneau, O., Dubois, G. R., Jones, C. E., & Trifilieff, A. IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. J. Immunol. 170, 2106-2112 (2003).
40. Zindl, C. L., et al. IL-22-producing neutrophils contribute to antimicrobial defense and restitution of colonic epithelial integrity during colitis. Proc Natl Acad Sci USA 110, 12768-12773, doi:10.1073/pnas.1300318110 (2013).
41. Dudakov, J. A., Hanash, A. M., & van den Brink, M. R. Interleukin-22: immunobiology and pathology. Annu. Rev. Immunol. 33, 747-785 (2015).
42. 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. 34, 521-564 (2003).
43. Rainard, P., Cunha, P., & Gilbert, F. B. Innate and Adaptive Immunity Synergize to Trigger Inflammation in the Mammary Gland. PLoS ONE 11, e0154172 (2016).
44. Nemali, S., et al. Molecular analysis of the bovine anaphylatoxin C5a receptor. J. Leukoc. Biol. 84, 537-549 (2008).
45. Lahouassa, H., Rainard, P., Caraty, A., & Riollet, C. Identification and characterization of a new interleukin-8 receptor in bovine species. Mol. Immunol. 45, 1153-1164 (2008).
46. Hill, A. W., Heneghan, D. J., Field, T. R., & Williams, M. R. Increase in specific opsonic activity in bovine milk following experimental Escherichia coli mastitis. Res. Vet. Sci. 35, 222-226 (1983).
47. Burton, J. L., & Erskine, R. J. Immunity and mastitis. Some new ideas for an old disease. Vet. Clin. North Am. Food Anim. Pract 19, 1-45 (2003).
48. Steinbeck, M. J., Roth, J. A., & Kaeberle, M. L. Activation of bovine neutrophils by recombinant interferon-gamma. Cell Immunol. 98, 137-144 (1986).
49. Pennington, J. E., & Menkes, E. Type-specific vs. cross-protective vaccination for gram-negative bacterial pneumonia. J. Infect. Dis. 144, 599-603 (1981).
50. Van Dijk, W. C., Verbrugh, H. A., van der Tol, M. E., Peters, R., & Verhoef, J. Role of Escherichia coli K capsular antigens during complement activation, C3 fixation, and opsonization. Infect. Immun. 25, 603-609 (1979).
51. Vreede, R. W., et al. Complement activating and opsonic capacity of monoclonal antibodies raised against Escherichia coli O111 and its rough mutant J5. Eur J Clin Microbiol 5, 141-147 (1986).
52. Kim, K. S., et al. Functional activities of monoclonal antibodies to the O side chain of Escherichia coli lipopolysaccharides in vitro and in vivo. J. Infect. Dis. 157, 47-53 (1988).
53. Jiang, X., et al. Skin infection generates non-migratory memory CD8+ T(RM) cells providing global skin immunity. Nature 483, 227-231 (2012).
54. Iijima, N., & Iwasaki, A. T cell memory. A local macrophage chemokine network sustains protective tissue-resident memory CD4 T cells. Science 346, 93-98 (2014).
55. Stary, G., et al. A mucosal vaccine against Chlamydia trachomatis generates two waves of protective memory T cells. Science 348, aaa8205 (2015).
56. Isobe, N., Morimoto, K., Nakamura, J., Yamasaki, A., & Yoshimura, Y. Intramammary challenge of lipopolysaccharide stimulates secretion of lingual antimicrobial peptide into milk of dairy cows. J. Dairy Sci. 92, 6046-6051 (2009).
57. Smith, J. L., Hogan, J. S., & Smith, K. L. Efficacy of intramammary immunization with an Escherichia coli J5 bacterin. J. Dairy Sci. 82, 2582-2588 (1999).
58. Pomeroy, B., et al. Intramammary immunization with ultraviolet-killed Escherichia coli shows partial protection against late gestation intramammary challenge with a homologous strain. J. Dairy Sci, doi:10.3168/jds.2016-11149 (2016).
59. Petzl, W., et al. Lipopolysaccharide pretreatment of the udder protects against experimental Escherichia coli mastitis. Innate immunity 18, 467-477 (2012).