1887

Abstract

The aim of this study was to examine changes in the systemic immune response during the incubation period and following the onset of clinical swine dysentery, including the recovery period. Ten healthy conventional pigs were inoculated with . Blood was sampled at pre-inoculation, at days 4 and 14 post-inoculation, during the first 4 days with clinical signs of dysentery and at days 1, 3, 7, 11 and 15 of the recovery period. Eight pigs developed haemorrhagic diarrhoea. Flow-cytometric analyses of lymphocyte subpopulations showed that all animals, including the two that remained healthy, had an increase in CD8 CD4 cells and T cells at days 4 and 14 post-inoculation. In addition, an increase in CD4 CD8 cells and CD8 CD8 cells was observed at days 4 and 14 post-inoculation in animals that developed dysentery. During clinical signs of dysentery, the acute-phase protein serum amyloid A was increased. There was a two- to threefold increase in both neutrophils and monocytes during signs of dysentery and at the beginning of the recovery period. The numbers of CD8 CD8 CD4, CD45RA lymphocytes also increased during the dysentery period. Circulating CD21 cells and CD21 CD45RA cells decreased at the end of the incubation period, during signs of dysentery and at the beginning of the recovery period. The dysentery-affected animals developed antibodies to -specific antigens (∼16 kDa and ∼30 kDa) from the first day of recovery, and T cells showed an increase during the recovery period. In comparison with pre-inoculation, increased numbers of monocytes, neutrophils, CD8 CD8 CD4 lymphocytes and CD45RA lymphocytes were observed during clinical dysentery. Increased numbers of neutrophils, T cells and specific antibodies were seen during the recovery period.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.46538-0
2006-07-01
2019-10-20
Loading full text...

Full text loading...

/deliver/fulltext/jmm/55/7/845.html?itemId=/content/journal/jmm/10.1099/jmm.0.46538-0&mimeType=html&fmt=ahah

References

  1. Albassam, M. A., Olander, H. J., Thacker, H. L. & Turek, J. J. ( 1985; ). Ultrastructural characterization of colonic lesions in pigs inoculated with Treponema hyodysenteriae. Can J Comp Med 49, 384–390.
    [Google Scholar]
  2. Badolato, R., Wang, J. M., Murphy, W. J., Lloyd, A. R., Michiel, D. F., Bausserman, L. L., Kelvin, D. J. & Oppenheim, J. J. ( 1994; ). Serum amyloid A is a chemoattractant: induction of migration, adhesion, and tissue infiltration of monocytes and polymorphonuclear leukocytes. J Exp Med 180, 203–209.[CrossRef]
    [Google Scholar]
  3. Bassaganya-Riera, J., Hontecillas, R., Zimmerman, D. R. & Wannemuehler, M. J. ( 2001; ). Dietary conjugated linoleic acid modulates phenotype and effector functions of porcine CD8(+) lymphocytes. J Nutr 131, 2370–2377.
    [Google Scholar]
  4. Beutler, B., Milsark, I. W. & Cerami, A. C. ( 1985; ). Passive immunization against cachectin/tumor necrosis factor protects mice from lethal effect of endotoxin. Science 229, 869–871.[CrossRef]
    [Google Scholar]
  5. Constant, P., Davodeau, F., Peyrat, M. A., Poquet, Y., Puzo, G., Bonneville, M. & Fournie, J. J. ( 1994; ). Stimulation of human gamma delta T cells by nonpeptidic mycobacterial ligands. Science 264, 267–270.[CrossRef]
    [Google Scholar]
  6. de Bruin, M. G., van Rooij, E. M., Voermans, J. J., de Visser, Y. E., Bianchi, A. T. & Kimman, T. G. ( 1997; ). Establishment and characterization of porcine cytolytic cell lines and clones. Vet Immunol Immunopathol 59, 337–347.[CrossRef]
    [Google Scholar]
  7. de Bruin, T. G., van Rooij, E. M., de Visser, Y. E., Voermans, J. J., Samsom, J. N., Kimman, T. G. & Bianchi, A. T. ( 2000; ). Discrimination of different subsets of cytolytic cells in pseudorabies virus immune and naive pigs. J Gen Virol 81, 1529–1537.
    [Google Scholar]
  8. Dhiman, T. R., Satter, L. D., Pariza, M. W., Galli, M. P., Albright, K. & Tolosa, M. X. ( 2000; ). Conjugated linoleic acid (CLA) content of milk from cows offered diets rich in linoleic and linolenic acid. J Dairy Sci 83, 1016–1027.[CrossRef]
    [Google Scholar]
  9. Fellström, C. & Gunnarsson, A. ( 1995; ). Phenotypical characterisation of intestinal spirochaetes isolated from pigs. Res Vet Sci 59, 1–4.[CrossRef]
    [Google Scholar]
  10. Fujihashi, K., Taguchi, T., McGhee, J. R., Eldridge, J. H., Bruce, M. G., Green, D. R., Singh, B. & Kiyono, H. ( 1990; ). Regulatory function for murine intraepithelial lymphocytes. Two subsets of CD3+, T cell receptor-1+ intraepithelial lymphocyte T cells abrogate oral tolerance. J Immunol 145, 2010–2019.
    [Google Scholar]
  11. Greer, J. M. & Wannemuehler, M. J. ( 1989; ). Pathogenesis of Treponema hyodysenteriae: induction of interleukin-1 and tumor necrosis factor by a treponemal butanol/water extract (endotoxin). Microb Pathog 7, 279–288.[CrossRef]
    [Google Scholar]
  12. Guy-Grand, D. & Vassalli, P. ( 1993; ). Gut intraepithelial T lymphocytes. Curr Opin Immunol 5, 247–252.[CrossRef]
    [Google Scholar]
  13. Harris, D. L. & Glock, R. D. ( 1981; ). Swine dysentery. In Diseases of Swine, pp. 432–444. Edited by A. D. Leman, R. D. Glock, W. L. Mengeling, R. H. C. Penny, E. Scholl & B. Straw. Ames, IA: Iowa State University Press.
  14. Hayday, A. C. ( 2000; ). γδ cells: a right time and a right place for a conserved third way of protection. Annu Rev Immunol 18, 975–1026.[CrossRef]
    [Google Scholar]
  15. Heegaard, P. M., Klausen, J., Nielsen, J. P., Gonzalez-Ramon, N., Pineiro, M., Lampreave, F. & Alava, M. A. ( 1998; ). The porcine acute phase response to infection with Actinobacillus pleuropneumoniae. Haptoglobin, C-reactive protein, major acute phase protein and serum amyloid A protein are sensitive indicators of infection. Comp Biochem Physiol B Biochem Mol Biol 119, 365–373.[CrossRef]
    [Google Scholar]
  16. Hershkoviz, R., Preciado-Patt, L., Lider, O., Fridkin, M., Dastych, J., Metcalfe, D. D. & Mekori, Y. A. ( 1997; ). Extracellular matrix-anchored serum amyloid A preferentially induces mast cell adhesion. Am J Physiol 273, 179–187.
    [Google Scholar]
  17. Hontecillas, R., Wannemeulher, M. J., Zimmerman, D. R., Hutto, D. L., Wilson, J. H., Ahn, D. U. & Bassaganya-Riera, J. ( 2002; ). Nutritional regulation of porcine bacterial-induced colitis by conjugated linoleic acid. J Nutr 132, 2019–2027.
    [Google Scholar]
  18. Hontecillas, R., Bassaganya-Riera, J., Wilson, J., Hutto, D. L. & Wannemuehler, M. J. ( 2005; ). CD4+ T-cell responses and distribution at the colonic mucosa during Brachyspira hyodysenteriae-induced colitis in pigs. Immunology 115, 127–135.[CrossRef]
    [Google Scholar]
  19. Hutto, D. L. & Wannemuehler, M. J. ( 1999; ). A comparison of the morphologic effects of Serpulina hyodysenteriae or its beta-hemolysin on the murine cecal mucosa. Vet Pathol 36, 412–422.[CrossRef]
    [Google Scholar]
  20. Jacobson, M., Fellström, C., Lindberg, R., Wallgren, P. & Jensen-Waern, M. ( 2004; ). Experimental swine dysentery: comparison between infection models. J Med Microbiol 53, 273–280.[CrossRef]
    [Google Scholar]
  21. Janeway, C. A., Jr ( 1992; ). The T cell receptor as a multicomponent signalling machine: CD4/CD8 coreceptors and CD45 in T cell activation. Annu Rev Immunol 10, 645–674.[CrossRef]
    [Google Scholar]
  22. Jensen, L. E. & Whitehead, A. S. ( 1998; ). Regulation of serum amyloid A protein expression during the acute-phase response. Biochem J 334, 489–503.
    [Google Scholar]
  23. Joens, L. A., Harris, D. L. & Baum, D. H. ( 1979; ). Immunity to swine dysentery in recovered pigs. Am J Vet Res 40, 1352–1354.
    [Google Scholar]
  24. Joens, L. A., Whipp, S. C., Glock, R. D. & Neussen, M. E. ( 1983; ). Serotype-specific protection against Treponema hyodysenteriae infection in ligated colonic loops of pigs recovered from swine dysentery. Infect Immun 39, 460–462.
    [Google Scholar]
  25. Joens, L. A., de Young, D. W., Cramer, J. C. & Glock, R. D. ( 1984; ). The immune response of the porcine colon to swine dysentery. In Proceedings of the International Pig Veterinary Society, Ghent, Belgium, p. 187. Ghent, Belgium: International Pig Veterinary Society.
  26. Joens, L. A., de Young, D. W., Glock, R. D., Mapother, M. E., Cramer, J. D. & Wilcox, H. E., III ( 1985; ). Passive protection of segmented swine colonic loops against swine dysentery. Am J Vet Res 46, 2369–2371.
    [Google Scholar]
  27. Jonasson, R., Johannisson, A., Jacobson, M., Fellström, C. & Jensen-Waern, M. ( 2004; ). Differences in lymphocyte subpopulations and cell counts before and after experimentally induced swine dysentery. J Med Microbiol 53, 267–272.[CrossRef]
    [Google Scholar]
  28. Jones, H. P., Tabor, L., Sun, X., Woolard, M. D. & Simecka, J. W. ( 2002; ). Depletion of CD8+ T cells exacerbates CD4+ Th cell-associated inflammatory lesions during murine mycoplasma respiratory disease. J Immunol 168, 3493–3501.[CrossRef]
    [Google Scholar]
  29. Komano, H., Fujiura, Y., Kawaguchi, M. & 7 other authors ( 1995; ). Homeostatic regulation of intestinal epithelia by intraepithelial gamma delta T cells. Proc Natl Acad Sci U S A 92, 6147–6151.[CrossRef]
    [Google Scholar]
  30. La, T., Phillips, N. D., Reichel, M. P. & Hampson, D. J. ( 2004; ). Protection of pigs from swine dysentery by vaccination with recombinant BmpB, a 29.7 kDa outer-membrane lipoprotein of Brachyspira hyodysenteriae. Vet Microbiol 102, 97–109.[CrossRef]
    [Google Scholar]
  31. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.[CrossRef]
    [Google Scholar]
  32. Lee, B. J., La, T., Mikosza, A. S. & Hampson, D. J. ( 2000; ). Identification of the gene encoding BmpB, a 30 kDa outer envelope lipoprotein of Brachyspira (Serpulina) hyodysenteriae, and immunogenicity of recombinant BmpB in mice and pigs. Vet Microbiol 76, 245–257.[CrossRef]
    [Google Scholar]
  33. Lobova, D., Smola, J. & Cizek, A. ( 2004; ). Decreased susceptibility to tiamulin and valnemulin among Czech isolates of Brachyspira hyodysenteriae. J Med Microbiol 53, 287–291.[CrossRef]
    [Google Scholar]
  34. Murray, H. W. ( 1990; ). Gamma interferon, cytokine-induced macrophage activation, and antimicrobial host defense. In vitro, in animal models, and in humans. Diagn Microbiol Infect Dis 13, 411–421.[CrossRef]
    [Google Scholar]
  35. Neef, N. A., Lysons, R. J., Trott, D. J., Hampson, D. J., Jones, P. W. & Morgan, J. H. ( 1994; ). Pathogenicity of porcine intestinal spirochetes in gnotobiotic pigs. Infect Immun 62, 2395–2403.
    [Google Scholar]
  36. Nibbelink, S. K., Sacco, R. E. & Wannemuehler, M. J. ( 1997; ). Pathogenicity of Serpulina hyodysenteriae: in vivo induction of tumor necrosis factor and interleukin-6 by a serpulinal butanol/water extract (endotoxin). Microb Pathog 23, 181–187.[CrossRef]
    [Google Scholar]
  37. Nuessen, M. E., Birmingham, J. R. & Joens, L. A. ( 1982; ). Biological activity of a lipopolysaccharide extracted from Treponema hyodysenteriae. Infect Immun 37, 138–142.
    [Google Scholar]
  38. Pescovitz, M. D., Sakopoulos, A. G., Gaddy, J. A., Husmann, R. J. & Zuckermann, F. A. ( 1994; ). Porcine peripheral blood CD4+/CD8+ dual expressing T-cells. Vet Immunol Immunopathol 43, 53–62.[CrossRef]
    [Google Scholar]
  39. Rees, A. S., Lysons, R. J., Stokes, C. R. & Bourne, F. J. ( 1989; ). Antibody production by the pig colon during infection with Treponema hyodysenteriae. Res Vet Sci 47, 263–269.
    [Google Scholar]
  40. Sacco, R. E., Nibbelink, S. K., Baarsch, M. J., Murtaugh, M. P. & Wannemuehler, M. J. ( 1996; ). Induction of interleukin (IL)-1beta and IL-8 mRNA expression in porcine macrophages by lipopolysaccharide from Serpulina hyodysenteriae. Infect Immun 64, 4369–4372.
    [Google Scholar]
  41. Sacco, R. E., Hutto, D. L., Waters, W. R., Xiasong, L., Kehrli, M. E., Jr, Zuckermann, F. A. & Wannemuehler, M. J. ( 2000; ). Reduction in inflammation following blockade of CD18 or CD29 adhesive pathways during the acute phase of a spirochetal-induced colitis in mice. Microb Pathog 29, 289–299.[CrossRef]
    [Google Scholar]
  42. Schild, H., Mavaddat, N., Litzenberger, C., Ehrich, E. W., Davis, M. M., Bluestone, J. A., Matis, L., Draper, R. K. & Chien, Y. H. ( 1994; ). The nature of major histocompatibility complex recognition by gamma delta T cells. Cell 76, 29–37.[CrossRef]
    [Google Scholar]
  43. Schoel, B., Sprenger, S. & Kaufmann, S. H. ( 1994; ). Phosphate is essential for stimulation of Vγ9Vδ2 T lymphocytes by mycobacterial low molecular weight ligand. Eur J Immunol 24, 1886–1892.[CrossRef]
    [Google Scholar]
  44. Solano-Aguilar, G. I., Vengroski, K. G., Beshah, E., Douglass, L. W. & Lunney, J. K. ( 2001; ). Characterization of lymphocyte subsets from mucosal tissues in neonatal swine. Dev Comp Immunol 25, 245–263.[CrossRef]
    [Google Scholar]
  45. Steele, C., Zheng, M., Young, E., Marrero, L., Shellito, J. E. & Kolls, J. K. ( 2002; ). Increased host resistance against Pneumocystis carinii pneumonia in γδ T-cell-deficient mice: protective role of gamma interferon and CD8+ T cells. Infect Immun 70, 5208–5215.[CrossRef]
    [Google Scholar]
  46. Taguchi, T., McGhee, J. R., Coffman, R. L., Beagley, K. W., Eldridge, J. H., Takatsu, K. & Kiyono, H. ( 1990; ). Analysis of Th1 and Th2 cells in murine gut-associated tissues. Frequencies of CD4+ and CD8+ T cells that secrete IFN-gamma and IL-5. J Immunol 145, 68–77.
    [Google Scholar]
  47. Tanaka, Y., Morita, C. T., Nieves, E., Brenner, M. B. & Bloom, B. R. ( 1995; ). Natural and synthetic non-peptide antigens recognized by human gamma delta T cells. Nature 375, 151–158.[CrossRef]
    [Google Scholar]
  48. Taylor, D. J. & Alexander, T. J. ( 1971; ). The production of dysentery in swine by feeding cultures containing a spirochaete. Br Vet J 127, 58–61.
    [Google Scholar]
  49. Thomas, W. & Sellwood, R. ( 1993; ). Molecular cloning, expression, and DNA sequence analysis of the gene that encodes the 16-kilodalton outer membrane lipoprotein of Serpulina hyodysenteriae. Infect Immun 61, 1136–1140.
    [Google Scholar]
  50. Thomas, W., Sellwood, R. & Lysons, R. J. ( 1992; ). A 16-kilodalton lipoprotein of the outer membrane of Serpulina (Treponema) hyodysenteriae. Infect Immun 60, 3111–3116.
    [Google Scholar]
  51. Towbin, H., Staehelin, T. & Gordon, J. ( 1979; ). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76, 4350–4354.[CrossRef]
    [Google Scholar]
  52. Van Snick, J. ( 1990; ). Interleukin-6: an overview. Annu Rev Immunol 8, 253–278.[CrossRef]
    [Google Scholar]
  53. Waters, W. R., Pesch, B. A., Hontecillas, R., Sacco, R. E., Zuckermann, F. A. & Wannemuehler, M. J. ( 1999a; ). Cellular immune responses of pigs induced by vaccination with either a whole cell sonicate or pepsin-digested Brachyspira (Serpulina) hyodysenteriae bacterin. Vaccine 18, 711–719.[CrossRef]
    [Google Scholar]
  54. Waters, W. R., Sacco, R. E., Dorn, A. D., Hontecillas, R., Zuckermann, F. A. & Wannemuehler, M. J. ( 1999b; ). Systemic and mucosal immune responses of pigs to parenteral immunization with a pepsin-digested Serpulina hyodysenteriae bacterin. Vet Immunol Immunopathol 69, 75–87.[CrossRef]
    [Google Scholar]
  55. Waters, W. R., Hontecillas, R., Sacco, R. E., Zuckermann, F. A., Harkins, K. R., Bassaganya-Riera, J. & Wannemuehler, M. J. ( 2000; ). Antigen-specific proliferation of porcine CD8αα cells to an extracellular bacterial pathogen. Immunology 101, 333–341.[CrossRef]
    [Google Scholar]
  56. Whipp, S. C., Robinson, I. M., Harris, D. L., Glock, R. D., Matthews, P. J. & Alexander, T. J. ( 1979; ). Pathogenic synergism between Treponema hyodysenteriae and other selected anaerobes in gnotobiotic pigs. Infect Immun 26, 1042–1047.
    [Google Scholar]
  57. Wilcock, B. P. & Olander, H. J. ( 1979; ). Studies on the pathogenesis of swine dysentery. I. Characterization of the lesions in colons and colonic segments inoculated with pure cultures or colonic content containing Treponema hyodysenteriae. Vet Pathol 16, 450–465.
    [Google Scholar]
  58. Wright, J. C., Wilt, G. R., Reed, R. B. & Powe, T. A. ( 1989; ). Use of an enzyme-linked immunosorbent assay for detection of Treponema hyodysenteriae infection in swine. J Clin Microbiol 27, 411–416.
    [Google Scholar]
  59. Xu, L., Badolato, R., Murphy, W. J., Longo, D. L., Anver, M., Hale, S., Oppenheim, J. J. & Wang, J. M. ( 1995; ). A novel biologic function of serum amyloid A. Induction of T lymphocyte migration and adhesion. J Immunol 155, 1184–1190.
    [Google Scholar]
  60. Yang, H. & Parkhouse, R. M. ( 1996; ). Phenotypic classification of porcine lymphocyte sub-populations in blood and lymphoid tissues. Immunology 98, 76–83.
    [Google Scholar]
  61. Zuckermann, F. A. & Husmann, R. J. ( 1996; ). Functional and phenotypic analysis of porcine peripheral blood CD4/CD8 double-positive T cells. Immunology 87, 500–512.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.46538-0
Loading
/content/journal/jmm/10.1099/jmm.0.46538-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error