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Co-inoculation ofBorrelia afzelii with tick salivary gland extract influences distribution of immunocompetent cells in the skin and lymph nodes of mice

Abstract

The impact ofIxodes ricinus salivary gland extract (SGE) on inflammatory changes in the skin and draining lymph nodes of mice, elicited by the infection with the important human pathogen,B. afzelii, was determined using flow cytometry. SGE injected together with spirochetes reduced the numbers of leukocytes and γδ-T lymphocytes in infected epidermis at early time-points post infection. In draining lymph nodes, the anti-inflammatory effect of SGE was manifested by the decrease of total cell count compared with that in mice treated with inactivated SGE. Changes in subpopulations of immunocompetent cells apparently reflected the effect of SGE on the proliferation of spirochetes in the host. The significance of tick saliva anti-inflammatory effect for saliva activated transmission ofB. afzelii is shown.

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Abbreviations

BP:

band pass

FACS:

fluorescein-activated cell sorter

FCS:

fetal calf serum

FITC:

fluorescein isothiocyanate

PBS:

phosphate-buffered saline

p.i.:

post infection

PMNs:

polymorphonuclear cells

RPE:

rhodamine-phycoerythrin

SAT:

saliva-activated transmission

SGE:

salivary gland extract

TCR:

T-cell receptor

References

  • Alekseev N., Chunikhin S.P., Rukhkyan M.Y., Stefutkina L.F.: Possible role ofIxodidae salivary gland substrate as an adjuvant enhancing arbovirus transmission.Med.Parazitol. 1, 28–31 (1991).

    Google Scholar 

  • Bloom W.H.: γδ-T cells andMycobacterium tuberculosis.Microbes Infect. 1, 187–195 (1999).

    Article  Google Scholar 

  • Chong-Cerillo C., Shang E.S., Blanco D.R., Lovett M.A., Miller J.M.: Immunohistochemical analysis of Lyme disease in the skin of naïve and infection-immune rabbits following challenge.Infect.Immun. 6, 14094–14102 (2001).

    Google Scholar 

  • Ferreira B.R., Silva J.S.: Successive tick infestations selectively promote a T-helper 2 cytokine profile in mice.Immunology 96, 434–439 (1999).

    PubMed  Article  CAS  Google Scholar 

  • Glatzel A., Entschladen F.T., Zollner M., Kraiczy P., Brade V., Kaufmann R., Janssen O., Lengl-Janssen B., Wesch D., Kabelitz D.: The responsiveness of human Vδ1γ-T cells toBorrelia burgdorferi is largely restricted to synovial-fluid cells from patients with Lyme arthritis.J.Infect.Dis. 186, 1043–1046 (2002).

    PubMed  Article  CAS  Google Scholar 

  • Hajnická V., Kocáková P., Slovák M., Labuda M., Fuchsberger N., Nuttall P.A.: Inhibition of the antiviral action of interferon by tick salivary gland extract.Parasite Immunol. 22, 201–206 (2000).

    PubMed  Article  Google Scholar 

  • Hiromatshu K., Yoshikai Y., Matsuzaki G., Ohga S., Muramori K., Matsumoto K., Bluestone J.A., Nomoto K.: A protective role of γ/δ-T cells in primary infection withListeria monocytogenes in mice.J.Exp.Med. 175, 49–56 (1992).

    Article  Google Scholar 

  • Hisaeda H., Nagasawa H., Maeda K., Maekawa Y., Ishikawa H., Ito Y., Good R.A., Kimeno K.: γδ-T cells play an important role in hsp65 expression and in acquiring protective immune responses against infection withToxoplasma gondii.J.Immunol. 155, 244–251 (1995).

    PubMed  CAS  Google Scholar 

  • Honarvar N., Schaible U.E., Galanos C., Wallich R., Simon M.M.: A 14000 MW lipoprotein and a glycolipid-like structure ofBorrelia burgdorferi induce proliferation and immunoglobulin production in mouse B cells at high frequencies.Immunology 82, 389–396 (1994).

    PubMed  CAS  Google Scholar 

  • Hume D.A., Robinson A.P., MacPherson G.G., Gordon S.: The mononuclear phagocyte system of the mouse defined by immuno-histochemical localization of antigen F4/80. Relationship between macrophages, Langerhans cells, reticular cells, and dendritic cells in lymphoid and hematopoietic organs.J.Exp.Med. 158, 1522–1536 (1983).

    PubMed  Article  CAS  Google Scholar 

  • Jameson J., Witherden D., Havran W.L.: T-cell effector mechanisms: γδ and CD1d-restricted subsets.Curr.Opin.Immunol. 15, 349–353 (2003).

    PubMed  Article  CAS  Google Scholar 

  • Jones L.D., Hodgson E., Nuttall P.A.: Enhancement of virus transmission by tick salivary glands.J.Gen.Virol. 70, 1895–1898 (1989).

    PubMed  Article  Google Scholar 

  • Kabelitz D., Glatzel A., Wesch D.: Antigen recognition by human γδ-T lymphocytes.Internat.Arch.Allergy Immunol. 122, 1–7 (2000).

    Article  CAS  Google Scholar 

  • Kopecký J., Kuthejlová M.: Suppressive effect ofIxodes ricinus salivary gland extract on mechanisms of natural immunityin vitro.Parasite Immunol. 20, 169–174 (1998).

    PubMed  Google Scholar 

  • Kopecký J., Kuthejlová M., Pechová J.: Salivary gland extract fromIxodes ricinus ticks inhibits production of interferon-γ by the upregulation of interleukin-10.Parasite Immunol. 21, 351–356 (1999).

    PubMed  Article  Google Scholar 

  • Kovář L., Kopecký J., Říhová B.: Salivary gland extract fromIxodes ricinus tick polarizes the cytokine profile toward TH2 and suppresses proliferation of T lymphocytes in human PBL culture.J.Parasitol. 87, 1342–1348 (2001).

    PubMed  Article  Google Scholar 

  • Kovář L., Kopecky J., Říhová B.: Salivary gland extract fromIxodes ricinus tick modulates the host immune response towards the TH2 cytokine profile.Parasitol.Res. 88, 1066–1072 (2002).

    PubMed  Article  Google Scholar 

  • Kročová Z., Macela A., Hernychová L., Kroča M., Pechová J., Kopecký J.: Tick salivary gland extract accelerates proliferation ofFranciscella tularensis in the host.J.Parasitol. 89, 14–20 (2003).

    PubMed  Article  Google Scholar 

  • Kuthejlová M., Pechová J., Braunfuchsová P., Kopecký J.: Effect of salivary gland extract fromIxodes ricinus ticks on the production of various cytokinesin vitro, pp. 165–171 in M. Kazimírová, M. Labuda, P.A. Nuttall (Eds):Proc. 3rd Internat. Conf. Ticks and Tick-borne Pathogens: Into the 21st Century, High Tatra Mountains (Slovakia) 2000. Institute of Zoology SAV, Bratislava (Slovakia) 2000.

    Google Scholar 

  • Kuthejlová M., Kopecký J., Štěpánová G., Macela A.: Tick salivary gland extract inhibits killing ofBorrelia afzelii spirochetes by mouse macrophages.Infect.Immun. 69, 575–578 (2001).

    PubMed  Article  Google Scholar 

  • Labuda M., Jones L.D., Williams T., Nuttall P.A.: Enhancement of tick-borne encephalitis virus transmission by tick salivary gland extracts.Med.Vet.Entomol. 7, 193–196 (1993).

    PubMed  Article  CAS  Google Scholar 

  • Ladel H., Blum C., Draher A., Reifenberg K., Kaufmann S.H.: Protective role of γ/δ-T cells and α/β-T cells in tuberculosis.Eur.J.Immunol. 25, 2877–2881 (1995).

    PubMed  Article  CAS  Google Scholar 

  • Mbow M.L., Zeidner N., Gilmore R.D., Dolan M., Piesman J., Titus R.G.: Major histocompability complex class II-independent generation of neutralizing antibodies against T-cell-dependentBorrelia burgdoferi antigens presented by dendritic cells: regulation by NK and γδ-T cells.Infect.Immun. 4, 2407–2415 (2001).

    Article  Google Scholar 

  • Mukasa A., Lahn M., Fleming S., Freiberg B., Pflum E., Vollmer M., Kupfer A., O’Brien R., Born W.: Extensive and preferential Fas/Fas ligand-dependent death of γδ-T cells following infection withListeria monocytogenes.Scand.J.Immunol. 56, 233–247 (2002).

    PubMed  Article  CAS  Google Scholar 

  • Nuttall P.A.: Pathogen-tick-host interactions:Borrelia burgdorferi and TBE virus.Zbl.Bakteriol. 289, 492–505 (1999).

    CAS  Google Scholar 

  • Nuttall P.A., Jones L.D.: Non-viremic tick-borne virus transmission: mechanism and significance, pp. 3–6 in F. Dusbábek, V. Bukva (Eds):Modern Acarology. Academia, Prague-SPB Academic Publishing, The Hague 1991.

    Google Scholar 

  • Paesen C., Adams P.L., Harlos K., Nuttall P.A., Stuart D.I.: Tick histamine-binding proteins: isolation, cloning and three dimensional structure.Mol.Cell 3, 661–671 (1999).

    PubMed  Article  CAS  Google Scholar 

  • Pechová J., Štěpánová G., Kovář L., Kopecký J.: Tick salivary gland extract-activated transmission ofBorrelia afzelii spirochetes.Folia Parasitol. 49, 153–159 (2002).

    PubMed  Google Scholar 

  • Ribeiro J.M.C.:Ixodes dammini: salivary anti-complement activity.Exp.Parasitol. 64, 347–353 (1987).

    PubMed  Article  CAS  Google Scholar 

  • Ribeiro J.M.C., Spielman A.:Ixodes dammini: salivary anaphylatoxin inactivating activity.Exp.Parasitol. 62, 292–297 (1986).

    PubMed  Article  CAS  Google Scholar 

  • Ribeiro J.M.C., Weiss J.J., Telford S.R. III: Saliva of the tickIxodes dammini inhibits neutrophil function.Exp.Parasitol. 70, 382–388 (1990).

    PubMed  Article  CAS  Google Scholar 

  • Schoeler G.B., Manweiler S.A., Wikel S.K.:Ixodes scapularis: effects of repeated infestations with pathogen-free nymphs on macrophage and T lymphocyte cytokine responses of BALB/c and C3H/HeN mice.Exp.Parasitol. 92, 239–248 (1999).

    PubMed  Article  CAS  Google Scholar 

  • Schwarzová K., Čižnár I.: Immunochemical analysis of lipopolysaccharide-like component extracted fromBorrelia burgdorferi sensu lato.Folia Microbiol. 49, 625–629 (2004).

    Article  Google Scholar 

  • Silberer M., Koszik F., Stingl G., Aberer E.: Downregulation of class II molecules on epidermal Langerhans cells in Lyme borreliosis.Brit.J.Dermatol. 143, 786–794 (2000).

    Article  CAS  Google Scholar 

  • Štěpánová-Tresová G., Kopecký J., Kuthejlová M.: Identification ofBorrelia burgdorferi sensu stricto,Borrelia garinii andBorrelia afzelii inIxodes ricinus ticks from Southern Bohemia using monoclonal antibodies.Zbl.Bakteriol. 289, 797–806 (1999).

    Google Scholar 

  • Summers B.A., Straubinger A.F., Jacobson R.H., Chang Y.F., Appel M.J., Straubinger R.K.: Histopathological studies of experimental lyme disease in the dog.J.Comp.Pathol. 133, 1–13 (2005).

    PubMed  Article  CAS  Google Scholar 

  • Vincent M.S., Roessner K., Lynch D., Wilson D., Cooper S.M., Schopp J., Sigal L.H., Budd R.C.: Apoptosis of Fas high CD4+ synovial T cells by borrelia-reactive Fas-ligand (high) γδ-T cells in Lyme arthritis.J.Exp.Med. 184, 2109–2117 (1996).

    PubMed  Article  CAS  Google Scholar 

  • Wikel S.K.: Influence ofDermacentor andersoni infestation on lymphocyte responsiveness to mitogens.Ann.Trop.Med.Parasitol. 76, 627–632 (1982).

    PubMed  CAS  Google Scholar 

  • Zeidner N.S., Schneider B.S., Nuncio M.S., Gern L., Piesman J.: Coinoculation ofBorrelia spp. with tick salivary gland lysate enhances spirochete load in mice and is tick species-specific.J.Parasitol. 88, 1276–1278 (2002).

    PubMed  CAS  Google Scholar 

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This work was supported by grant of theGrant Agency of the Czech Republic (no. 524/02/0901) and by grant of theMinistry of Education, Youth and Sports of the Czech Republic (no. MSM 123100003). This study is a part of the research project of theInstitute of Parasitology, Academy of Sciences of the Czech Republic (Z6 022 909). Experiments comply with the current laws of the Czech Republic.

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Severinová, J., Salát, J., Kročová, Z. et al. Co-inoculation ofBorrelia afzelii with tick salivary gland extract influences distribution of immunocompetent cells in the skin and lymph nodes of mice. Folia Microbiol 50, 457–463 (2005). https://doi.org/10.1007/BF02931430

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  • DOI: https://doi.org/10.1007/BF02931430

Keywords

  • Drain Lymph Node
  • Infected Group
  • Borrelia Burgdorferi
  • Immunocompetent Cell
  • Salivary Gland Extract