Folia Parasitologica, vol. 51 (2004), issue 4

Folia Parasitologica 51[4] 367-372 (2004) | 10.14411/fp.2004.046

Effect of tick salivary gland extract on the cytokine production by mouse epidermal cells

Jitka Pechová, Jan Kopecký, Jiří Salát
Institute of Parasitology, Academy of Sciences of the Czech Republic, and Faculty of Biological Sciences, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic

Previous studies have demonstrated that both tick saliva and Borrelia burgdorferi sensu lato antigens modulate the cytokine response of the host. In this paper, the effect of salivary gland extract (SGE) from Ixodes ricinus (L., 1758) ticks on cytokine production by primary cultures of mouse epidermal cells stimulated with Borrelia afzelii Canica, Nato, du Merle, Mazie, Baranton et Postic, 1993 spirochetes was analysed. Epidermal cells were derived from C3H/HeN mice, susceptible to Lyme disease, and BALB/c mice, which are resistant. In cultures from C3H/HeN mice, SGE down regulated production of tumour necrosis factor alpha (TNF-α) and up regulated Th2 cytokine, interleukin 4 (IL-4). Cultures from BALB/c mice produced higher basal levels of monitored cytokines, but their production was affected by SGE a different way. While Th2 cytokines IL-6 and IL-10 were down regulated, the effect on TNF-α and IL-4 was ambiguous. These results indicate that the effect of tick saliva on the epidermal cells of Lyme disease-susceptible C3H/HeN mice mirrors its effect on other cells of the immune system.

Keywords: Ixodes ricinus, salivary gland extract, Borrelia afzelii, mouse epidermal cells, cytokines

Received: February 16, 2004; Accepted: May 21, 2004; Published: December 1, 2004


References

  1. ASKENASE P.W., GRAZIANO F., WORMS M. 1979: Immunobiology of cutaneous basophil reactions. Monogr. Allergy 14: 222-235 Go to PubMed...
  2. BARTHOLD S.W., BECK D.S., HANSEN G.M., TERWILLIGER G.A., MOODY D. 1990: Lyme borreliosis in selected strains and ages of laboratory mice. J. Infect. Dis. 162: 133-138 Go to original source... Go to PubMed...
  3. ELBE A., FOSTER C.A., STINGL G. 1997: Isolation of T cells from mouse and human skin. In: I. Lefkovits (Ed.), Immunology Methods Manual. Academic Press, New York, pp. 1490-1501
  4. ENK A.H., ANGELONI V.L., UDEY M.C., KATZ S.I. 1993: Inhibition of Langerhans cell antigen-presenting function by IL-10. A role of IL-10 in induction of tolerance. J. Immunol. 151: 2390-2398 Go to PubMed...
  5. FERREIRA B.R., SILVA J.S. 1999: Successive tick infestations selectively promote a T-helper 2 cytokine profile in mice. Immunology 96: 434-439 Go to original source... Go to PubMed...
  6. FERREIRA B.R., SZABO M.J., CAVASSANI K.A., BECHARA G.H., SILVA J.S. 2003: Antigens from Rhipicephalus sanguineus ticks elicit potent cell-mediated immune responses in resistant but not in susceptible animals. Vet. Parasitol. 115: 35-48 Go to original source... Go to PubMed...
  7. GWAKISA P., YOSHIHARA K., LONG TO T., GOTOH H., AMANO F., MOMOTANI E. 2001: Salivary gland extract of Rhipicephalus appendiculatus ticks inhibits in vitro transcription and secretion of cytokines and production of nitric oxide by LPS-stimulated JA-4 cells. Vet. Parasitol. 99: 35-61 Go to original source... Go to PubMed...
  8. HIRSCHFELD M., KIRSCHNING C.J., SCHWANDNER R., WESCHE H., WEIS J.H., WOOTEN R.M., WEIS J.J. 1999: Cutting edge: inflammatory signalling by Borrelia burgdorferi lipoproteins is mediated by toll-like receptor 2. J. Immunol. 163: 2382-2386 Go to PubMed...
  9. KOPECKY J., KUTHEJLOVA M., PECHOVA J. 1999: Salivary gland extract from Ixodes ricinus ticks inhibits production of interferon-gamma by upregulation of interleukin-10. Parasite Immunol. 21: 351-356 Go to original source... Go to PubMed...
  10. KOVAR L., KOPECKY J., RIHOVA B. 2001: Salivary gland extract from Ixodes ricinus ticks polarizes the cytokine profile toward Th2 and suppresses proliferation of T lymphocytes in human PBMC culture. J. Parasitol. 87: 1342-1348 Go to original source... Go to PubMed...
  11. KOVAR L., KOPECKY J., RIHOVA B. 2002: Salivary gland extract from Ixodes ricinus tick modulates the host immune response towards the Th2 cytokine profile. Parasitol. Res. 88: 1066-1072 Go to original source... Go to PubMed...
  12. KURODA E., SUGIURA T., ZEKI K., YOSHIDA Y., YAMASHITA U. 2000: Sensitivity difference to the suppressive effect of prostaglandin E2 among mouse strains: a possible mechanism to polarize Th2 type response in BALB/c mice. J. Immunol. 164: 2386-2395 Go to original source... Go to PubMed...
  13. KUTHEJLOVA M., KOPECKY J., STEPANOVA G., MACELA A. 2001: Tick salivary gland extract inhibits killing of Borrelia afzelii spirochetes by mouse macrophages. Infect. Immun. 69: 575-578 Go to original source... Go to PubMed...
  14. MATYNIAK J.E., REINER S.L. 1995: T helper phenotype and genetic susceptibility in experimental Lyme disease. J. Exp. Med. 181: 1251-1254 Go to original source... Go to PubMed...
  15. MBOW M.L., CHRISTE M., RUTTI B., BROSSARD M. 1994a: Absence of acquired resistance to nymphal Ixodes ricinus ticks in BALB/c mice developing cutaneous reactions. J. Parasitol. 80: 81-87 Go to original source... Go to PubMed...
  16. MBOW M.L., RUTTI B., BROSSARD M. 1994b: Infiltration of CD4+ CD8+ T cells, and expression of ICAM-1, Ia antigens, IL-1 alpha and TNF-alpha in the skin lesion of BALB/c mice undergoing repeated infestations with nymphal Ixodes ricinus ticks. Immunology 82: 596-602 Go to PubMed...
  17. MODOLELL M., SCHAIBLE U.E., RITTIG M., SIMON M.M. 1994: Killing of Borrelia burgdorferi by macrophages is dependent on oxygen radicals and nitric oxide and can be enhanced by antibodies to outer surface proteins of the spirochete. Immunol. Lett. 40: 139-146 Go to original source... Go to PubMed...
  18. PECHOVA J., STEPANOVA G., KOVAR L., KOPECKY J. 2002: Tick salivary gland extract-activated transmission of Borrelia afzelii spirochetes. Folia Parasitol. 49: 153-159 Go to original source... Go to PubMed...
  19. RAMACHANDRA R.N., WIKEL S.K. 1992: Modulation of host-immune responses by ticks (Acari: Ixodidae): effect of salivary gland extract on host macrophages and lymphocyte cytokine production. J. Med. Entomol. 29: 818- 826 Go to original source... Go to PubMed...
  20. SALAZAR J.C., POPE C.D., SELATTI T.J., FEDER H.M. Jr., KIELY T.G., DARDICK K.R., BUCKMAN R.L., MOORE M.V., CAIMANO M.J., POPE J.G., KRAUSE P.J., RADOLF J.D. 2003: Coevolution of markers of innate and adaptive immunity in skin and peripheral blood of patients with erythema migrans. J. Immunol. 171: 2660-2670 Go to original source... Go to PubMed...
  21. SCHOELER G.B., MANWEILER S.A., WIKEL S.K. 1999: Ixodes scapularis: effect of repeated infestation with pathogen-free nymphs on macrophage and T-lymphocyte cytokine responses of BALB/c and C3H/HeN mice. Exp. Parasitol. 92: 239-248 Go to original source... Go to PubMed...
  22. SHREEDHAR V., GIESE T., SUNG V.W., ULLRICH S.E. 1998: A cytokine cascade including prostaglandin E2, IL4, and IL-10 is responsible for UV-induced systemic immune suppression. J. Immunol. 160: 3783-3789 Go to PubMed...
  23. STEERE A.C. 1989: Lyme disease. N. Engl. J. Med. 321: 586-596 Go to original source... Go to PubMed...
  24. STREILEIN J.W. 1983: Skin-associated lymphoid tissues (SALT): origins and functions. J. Invest. Dermatol. 80: 12S-16S Go to original source... Go to PubMed...
  25. STEPANOVA-TRESOVA G., KOPECKY J., KUTHEJLOVA M. 1999: Identification of Borrelia burgdorferi sensu stricto, Borrelia garinii and Borrelia afzelii in Ixodes ricinus ticks from Southern Bohemia using monoclonal antibodies. Zentralbl. Bakteriol. 289: 797-806 Go to original source... Go to PubMed...
  26. WEIS J.J., MA Y., ERDILE L.F. 1994: Biological activities of native and recombinant Borrelia burgdorferi outer surface protein A: dependence on lipid modification. Infect. Immun. 62: 4632-4636 Go to PubMed...
  27. WHEELER C.M., COLEMAN J.L., HABICHT G.S., BENACH J.L. 1989: Adult Ixodes dammini on rabbits: development of acute inflammation in the skin and immune responses to salivary gland, midgut, and spirochetal components. J. Infect. Dis. 159: 265-273 Go to original source... Go to PubMed...
  28. WIKEL S.K. 1996: Immunology of the skin. In: S.K. Wikel (Ed.), The Immunology of Host-Ectoparasitic Arthropod Relationships. CAB International, Wallingford, Oxon, pp. 1-29
  29. WIKEL S.K. 1999: Tick modulation of host immunity: an important factor in pathogen transmission. Int. J. Parasitol. 29: 851-859 Go to original source... Go to PubMed...
  30. WOOD L.C., JACKSON S.M., ELIAS P.M., GRUNFELD C., FEINGOLD K.R. 1992: Cutaneous barrier perturbation stimulates cytokine production in epidermis of mice. J. Clin. Invest. 90: 482-487 Go to original source... Go to PubMed...
  31. ZEIDNER N., DREITZ M., BELASCO D., FISH D. 1996: Suppression of acute Ixodes scapularis-induced Borrelia burgdorferi infection using tumour necrosis factor-α, interleukin-2 and interferon-γ. J. Infect. Dis. 173: 187- 195 Go to original source... Go to PubMed...
  32. ZEIDNER N., MBOW M.L., DOLAN M., MASSUNG R., BACA E., PIESMAN J. 1997: Effects of Ixodes scapularis and Borrelia burgdorferi on the modulation of the host immune response: induction of a Th2 cytokine response in Lyme disease susceptible (C3H/HeJ) but not in disease resistant (BALB/c) mice. Infect. Immun. 65: 3100-3106 Go to PubMed...