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Parasitology Research

, Volume 101, Issue 3, pp 591–598 | Cite as

Eimeria bovis infection enhances adhesion of peripheral blood mononuclear cells to and their transmigration through an infected bovine endothelial cell monolayer in vitro

  • Anja TaubertEmail author
  • Horst Zahner
  • Carlos Hermosilla
Original Paper

Abstract

The first schizogony of Eimeria bovis takes place in lymphatic endothelial cells of the ileum, resulting in the formation of macroschizonts within 2–3 weeks. In this study, we analyse early cellular immune responses to infected host cells on the basis of peripheral blood mononuclear cell (PBMC) adhesion on and transmigration through infected bovine umbilical vein endothelial cell (BUVEC) monolayers. Adhesion of PBMC was upregulated by an E. bovis infection. Most marked effects were observed 1 day p.i.; thereafter, PBMC adhesion declined reaching control levels from day 8 p.i. onward. CD8+ T cells adhered more frequently to infected BUVEC (42%) than CD4+ T cells (25%). About one third of attached PBMC were represented by γδ-TCR+ T cells. Adhesion of T cells was not restricted to parasitised host cells, but occurred almost equally on non-infected BUVEC within the same monolayer. Furthermore, we found moderately enhanced levels of PBMC transmigration through infected BUVEC monolayers, in particular on day 2 p.i. The data presented here suggest that E. bovis infection of BUVEC induces endothelial cell-derived proinflammatory reactions, which appear suitable for the initiation of both adaptive and innate immune responses.

Keywords

Peripheral Blood Mononuclear Cell Roswell Park Memorial Institute Infected Calf Bovine Umbilical Vein Endothelial Cell Eimeria Infection 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We are indebted to Prof. Dr. H. Bollwein and Dr. A. Koch (University of Veterinary Medicine, Hannover) for their kind cooperation and constant supply of bovine umbilical cords. Further, we acknowledge Brigitte Hofmann, Christina Scheld and Birgit Reinhardt for their excellent technical assistance in cell culture. We also thank K. Failing (Giessen) for support in statistical analyses of the data.

This work was supported by the German Research Foundation (DFG; project TA 291/1–2).

References

  1. Bumstead J, Tomley F (2000) Induction of secretion and surface capping of microneme proteins in Eimeria tenella. Mol Biochem Parasitol 110:311–321PubMedCrossRefGoogle Scholar
  2. Butcher EC, Picker LJ (1996) Lymphocyte homing and homeostasis. Science 272:60–66PubMedCrossRefGoogle Scholar
  3. Daugschies A, Bürger HJ, Akimaru M (1998) Apparent digestibility of nutrients and nitrogen balance during experimental infection of calves with Eimeria bovis. Vet Parasitol 77(2–3):93–102PubMedCrossRefGoogle Scholar
  4. Dengler TJ, Raftery MJ, Werle M, Zimmermann R, Schonrich G (2000) Cytomegalovirus infection of vascular cells induces expression of pro-inflammatory adhesion molecules by paracrine action of secreted interleukin-1beta. Transplantation 69(6):1160–1168PubMedCrossRefGoogle Scholar
  5. Dixon WJ (1993) BMDP statistical software manual, University of California Press, Berkeley, Los Angeles, OxfordGoogle Scholar
  6. Ebnet K, Vestweber D (1999) Molecular mechanisms that control leukocyte extravasation: the selectins and the chemokines. Histochem Cell Biol 112(1):1–23PubMedCrossRefGoogle Scholar
  7. Epperson DE, Pober JS (1994) Antigen-presenting function of human endothelial cells. Direct activation of resting CD8 T cells. J Immunol 153(12):5402–5412PubMedGoogle Scholar
  8. Fabbri M, Bianchi E, Fumagalli L, Pardi R (1999) Regulation of lymphocyte traffic by adhesion molecules. Inflamm Res 48(5):239–246PubMedCrossRefGoogle Scholar
  9. Fiege N, Klatte D, Kollmann D, Zahner H, Burger HJ (1992) Eimeria bovis in cattle: colostral transfer of antibodies and immune response to experimental infections. Parasitol Res 78(1):32–38PubMedCrossRefGoogle Scholar
  10. Fitzgerald PR (1980) The economic impact of coccidiosis in domestic animals. Adv Vet Sci Comp Med 24:121–143PubMedGoogle Scholar
  11. Hammond DM, Davis LR, Bowmann L (1964) Experimental infections with Eimeria bovis in calves. Am J Vet Res 5:303–311Google Scholar
  12. Hermosilla C, Bürger HJ, Zahner H (1999) T cell responses in calves to a primary Eimeria bovis infection: phenotypical and functional changes. Vet Parasitol 84(1–2):49–64PubMedCrossRefGoogle Scholar
  13. Hermosilla C, Barbisch B, Heise A, Kowalik S, Zahner H (2002) Development of Eimeria bovis in vitro: suitability of several bovine, human and porcine endothelial cell lines, bovine fetal gastrointestinal, Madin–Darby bovine kidney (MDBK) and African green monkey kidney (VERO) cells. Parasitol Res 88(4):301–307PubMedCrossRefGoogle Scholar
  14. Hermosilla C, Zahner H, Taubert A (2006) Eimeria bovis modulates adhesion molecule gene transcription in and PMN adhesion to infected bovine endothelial cells. Int J Parasitol 36(4):423–431PubMedCrossRefGoogle Scholar
  15. Hughes HP, Thomas KR, Speer CA (1988) Antigen-specific lymphocyte transformation induced by oocyst antigens of Eimeria bovis. Infect Immun 56(6):1518–1525PubMedGoogle Scholar
  16. Hughes HP, Whitmire WM, Speer CA (1989) Immunity patterns during acute infection by Eimeria bovis. J Parasitol 75(1):86–91PubMedCrossRefGoogle Scholar
  17. Jaffe E, Nachman R, Becker C, Mimnick C (1973) Culture of human endothelial cells derived from umbilical veins: identification by morphologic and immunologic criteria. J Clin Invest 52:2745PubMedCrossRefGoogle Scholar
  18. Lawrence MB, Springer TA (1991) Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell 65(5):859–873PubMedCrossRefGoogle Scholar
  19. Ma W, Pober JS (1998) Human endothelial cells effectively costimulate cytokine production by, but not differentiation of, naive CD4+ T cells. J Immunol 161(5):2158–2167PubMedGoogle Scholar
  20. Maly P, Thall AD, Petryniak B, Rogers CE, Smith PL, Marks RM, Kelly RJ, Gersten KM, Cheng G, Saunders TL, Camper SA, Camphausen RT, Sullivan FX, Isogai Y, Hindsgaul O, von Andrian UH, Lowe JB (1996) The (alpha)(1,3) fucosyltransferase Fuc-TVII controls leukocyte trafficking through an essential role in L-, E- and P-selectin ligand biosynthesis. Cell 87(4):1037–1047Google Scholar
  21. Pober JS, Cotran RS (1991) Immunologic interactions of T lymphocytes with vascular endothelium. Adv Immunol 50:261–302PubMedCrossRefGoogle Scholar
  22. Radeke HH, Ludwig RJ, Boehncke WH (2005) Experimental approaches to lymphocyte migration in dermatology in vitro and in vivo. Exp Dermatol 14(9):641–666PubMedCrossRefGoogle Scholar
  23. Rodig N, Ryan T, Allen JA, Pang H, Grabie N, Chernova T, Greenfield EA, Liang SC, Sharpe AH, Lichtman AH, Freeman GJ (2003) Endothelial expression of PD-L1 and PD-L2 down-regulates CD8+ T cell activation and cytolysis. Eur J Immunol 33(11):3117–3126PubMedCrossRefGoogle Scholar
  24. Rose ME, Hesketh P (1982) Coccidiosis: T-lymphocyte-dependent effects of infection with Eimeria nieschulzi in rats. Vet Immunol Immunopathol 3(5):499–508PubMedCrossRefGoogle Scholar
  25. Rose ME, Joysey HS, Hesketh P, Grencis RK, Wakelin D (1988a) Mediation of immunity to Eimeria vermiformis in mice by L3T4+ T cells. Infect Immun 56(7):1760–1765PubMedGoogle Scholar
  26. Rose ME, Wakelin D, Joysey HS, Hesketh P (1988b) Immunity to coccidiosis: adoptive transfer in NIH mice challenged with Eimeria vermiformis. Parasite Immunol 10(1):59–69PubMedCrossRefGoogle Scholar
  27. Rose ME, Wakelin D, Hesketh P (1990) Eimeria vermiformis: differences in the course of primary infection can be correlated with lymphocyte responsiveness in the BALB/c and C57BL/6 mouse, Mus musculus. Exp Parasitol 71(3):276–283PubMedCrossRefGoogle Scholar
  28. Rose ME, Hesketh P, Wakelin D (1992a) Immune control of murine coccidiosis: CD4+ and CD8+ T lymphocytes contribute differentially in resistance to primary and secondary infections. Parasitology 105(Pt 3):349–354PubMedCrossRefGoogle Scholar
  29. Rose ME, Millard BJ, Hesketh P (1992b) Intestinal changes associated with expression of immunity to challenge with Eimeria vermiformis. Infect Immun 60(12):5283–5290PubMedGoogle Scholar
  30. Shi M, Huther S, Burkhardt E, Zahner H (2001) Lymphocyte subpopulations in the caecum mucosa of rats after infections with Eimeria separata: early responses in naive and immune animals to primary and challenge infections. Int J Parasitol 31(1):49–55PubMedCrossRefGoogle Scholar
  31. Speer CA, Reduker DW, Burgess DE, Whitmire WM, Splitter GA (1985) Lymphokine-induced inhibition of growth of Eimeria bovis and Eimeria papillata (Apicomplexa) in cultured bovine monocytes. Infect Immun 50(2):566–571PubMedGoogle Scholar
  32. St Louis JD, Lederer JA, Lichtman AH (1993) Costimulator deficient antigen presentation by an endothelial cell line induces a nonproliferative T cell activation response without anergy. J Exp Med 178(5):1597–1605PubMedCrossRefGoogle Scholar
  33. Taubert A, Krüll M, Zahner H, Hermosilla C (2006a) Toxoplasma gondii and Neospora caninum infections of bovine endothelial cells induce endothelial adhesion molecule gene transcription and subsequent PMN adhesion. Vet Immunol Immunopathol 112(3–4):272–283PubMedCrossRefGoogle Scholar
  34. Taubert A, Zahner H, Hermosilla C (2006b) Dynamics of transcription of immunoregulatory genes in endothelial cells infected with different coccidian parasites. Vet Parasitol 142(3–4):214–222PubMedCrossRefGoogle Scholar
  35. Tedder TF, Steeber DA, Chen A, Engel P (1995) The selectins: vascular adhesion molecules. FASEB J 9(10):866–873PubMedGoogle Scholar
  36. von Andrian UH, Mackay CR (2000) T-cell function and migration. Two sides of the same coin. N Engl J Med 343(14):1020–1034CrossRefGoogle Scholar
  37. Wagner JG, Roth RA (2000) Neutrophil migration mechanisms, with an emphasis on the pulmonary vasculature. Pharmacol Rev 52(3):349–374PubMedGoogle Scholar
  38. Yang GX, Hagmann WK (2003) VLA-4 antagonists: potent inhibitors of lymphocyte migration. Med Res Rev 23(3):369–392PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Institute of Parasitology, Justus Liebig University GiessenGiessenGermany

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