Folia Parasitologica, vol. 64 (2017)

Folia Parasitologica 64:032 (2017) | DOI: 10.14411/fp.2017.032

Anti-tumour necrosis factor activity in saliva of various tick species and its appearance during the feeding period

Markéta Rezková, Jan Kopecký
Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic

Tumour necrosis factor (TNF) plays a central role in the inflammatory process. In the skin, it contributes to immune containment of tick-transmitted pathogens like Borrelia burgdorferi. In the saliva of some tick species, active compounds are present that inhibit detection of TNF in specific ELISA. We compared the presence of anti-TNF activity in saliva or salivary gland extract from 11 tick species from the family Ixodidae and demonstrated it in genera Ixodes Latreille, 1795 and Haemaphysalis Koch, 1844. Analysis of anti-TNF activity in Ixodes ricinus (Linnaeus, 1758) saliva during the feeding period showed that it is present in the late, rapid phase of engorgement. Significance of anti-TNF activity for tick feeding and transmission of tick-borne pathogens is discussed.

Keywords: ixodid ticks, cytokine, immunomodulation

Received: June 13, 2017; Accepted: September 14, 2017; Published online: October 20, 2017


References

  1. Bernard Q., Gallo R.L., Jaulhac B., Nakatsuji T., Luft B., Yang X., Boulanger N. 2016: Ixodes tick saliva suppresses the keratinocyte cytokine response to TLR2/TLR3 ligands during early exposure to Lyme borreliosis. Exp. Dermatol. 25: 26-31. Go to original source... Go to PubMed...
  2. Bonvin P., Power C.A., Proudfoot A.E. 2016: Evasins: therapeutic potential of a new family of chemokine-binding proteins from ticks. Front. Immunol. 7: 208. Go to original source... Go to PubMed...
  3. Bradley J.R. 2008: TNF-mediated inflammatory disease. J. Pathol. 214: 149-160. Go to original source... Go to PubMed...
  4. Cumberbatch M., Kimber I. 1995: Tumour necrosis factor-alpha is required for accumulation of dendritic cells in draining lymph nodes and for optimal contact sensitization. Immunology 84: 31-35. Go to PubMed...
  5. Déruaz M., Frauenschuh A., Alessandri A.L., Dias J.M., Coelho F.M., Russo R.C., Ferreira B.R., Graham G.J., Shaw J.P., Wells T.N., Teixeira M.M., Power C.A., Proudfoot A.E. 2008: Ticks produce highly selective chemokine binding proteins with antiinflammatory activity. J. Exp. Med. 205: 2019-2031. Go to original source... Go to PubMed...
  6. Eisen L., Lane R.S. 2002: Vectors of Borrelia burgdorferi sensu lato. In: J. Gray, O. Kahl, R.S. Lane and G. Stanek (Eds.), Lyme Borreliosis: Biology, Epidemiology and Control. CABI Publishing, Wallingford, pp. 92-99.
  7. Estrada A., Van Kessel A., Yun C.M., Li B. 1998: Effect of endotoxin on cytokine production and cell dynamics in mice. Immunopharmacol. Immunotoxicol. 20: 217-231. Go to original source... Go to PubMed...
  8. Ferreira B.R., Szabó 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...
  9. Francischetti I.M., Sa-Nunes A., Mans B.J., Santos I.M., Ribeiro J.M. 2009: The role of saliva in tick feeding. Front. Biosci. 14: 2051-2088. Go to original source...
  10. Fuchsberger N., Kita M., Hajnická V., Imanishi J., Labuda M., Nuttall P.A. 1995: Ixodid tick salivary gland extracts inhibit production of lipopolysaccharide-induced mRNA of several different human cytokines. Exp. Appl. Acarol. 19: 671-676. Go to original source... Go to PubMed...
  11. Gillespie R.D., Dolan M.C., Piesman J., Titus R.G. 2001: Identification of an IL-2 binding protein in the saliva of the Lyme disease vector tick, Ixodes scapularis. J. Immunol. 166: 4319-4326. Go to original source... Go to PubMed...
  12. 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 secretionof cytokines and production of nitric oxide by LPS-stimulated JA-4 cells. Vet. Parasitol. 99: 53-61. Go to original source... Go to PubMed...
  13. Hajnická V., Vančová I., Kocáková P., Slovák M., Gasperík J., Sláviková M., Hails R.S., Labuda M., Nuttall P.A. 2005: Manipulation of host cytokine network by ticks: a potential gateway for pathogen transmission. Parasitology 130: 333-342. Go to original source... Go to PubMed...
  14. Hehlgans T., Pfeffer K. 2005: The intriguing biology of the tumour necrosis factor/tumour necrosis factor receptor superfamily: players, rules and the games. Immunology 115: 1-20. Go to original source... Go to PubMed...
  15. Kern A., Collin E., Barthel C., Michel C., Jaulhac B., Boulanger N. 2011: Tick saliva represses innate immunity and cutaneous inflammation in a murine model of Lyme disease. Vector Borne Zoonotic Dis. 11: 1343-1350. Go to original source... Go to PubMed...
  16. Koník P., Slavíková V., Salát J., Řezníčková J., Dvorožňáková E., Kopecký J. 2006: Anti-tumour necrosis factor-alpha activity in Ixodes ricinus saliva. Parasite Immunol. 28: 649-656. Go to original source... Go to PubMed...
  17. Marchal C., Schramm F., Kern A., Luft B.J., Yang X., Schuijt T.J., Hovius J.W., Jaulhac B., Boulanger N. 2011: Antialarmin effect of tick saliva during the transmission of Lyme disease. Infect. Immun. 79: 774-785. Go to original source... Go to PubMed...
  18. Michelet L., Delannoy S., Devillers E., Umhang G., Aspan A., Juremalm M., Chirico J., van der Wal F.J., Sprong H., Boye Pihl T.P., Klitgaard K., Bødker R., Fach P., Moutailler S. 2014: High-throughput screening of tick-borne pathogens in Europe. Front. Cell. Infect. Microbiol. 4: 103. Go to original source... Go to PubMed...
  19. Nawroth P.P., Stern D.M. 1986: Modulation of endothelial cell hemostatic properties by tumor necrosis factor. J. Exp. Med. 163: 740-745. Go to original source... Go to PubMed...
  20. Paesen G.C., Adams P.L., Harlos K., Nuttall P.A., Stuart D.I. 1999: Tick histamine-binding proteins: isolation, cloning, and three-dimensional structure. Mol. Cell 3: 661-671. Go to original source... Go to PubMed...
  21. Peetre C., Thysell H., Grubb A., Olsson I. 1988: A tumor necrosis factor binding protein is present in human biological fluids. Eur. J. Haematol. 41: 414-419. Go to original source... Go to PubMed...
  22. Prevot P.P., Beschin A., Lins L., Beaufays J., Grosjean A., Bruys L., Adam B., Brossard M., Brasseur R., Zouaoui Boudjeltia K., Vanhamme L., Godfroid E. 2009: Exosites mediate the anti-inflammatory effects of a multifunctional serpin from the saliva of the tick Ixodes ricinus. FEBS J. 276: 3235-3246. Go to original source... Go to PubMed...
  23. Rahman M.M., McFadden G. 2006: Modulation of tumor necrosis factor by microbial pathogens. PLoS Pathog. 2: e4. Go to original source... Go to PubMed...
  24. Ramachandra R.N., Wikel S.K. 1992: Modulation of host-immune responses by ticks (Acari: Ixodidae): effect of salivary gland extracts on host macrophages and lymphocyte cytokine production. J. Med. Entomol. 29: 818-826. Go to original source... Go to PubMed...
  25. Ribeiro J.M. 1987: Ixodes dammini: salivary anti-complement activity. Exp. Parasitol. 64: 347-353. Go to original source... Go to PubMed...
  26. Severinová J., Salát J., Kročová Z., Řezníčková J., Demová H., Horká H., Kopecký J. 2005: Co-inoculation of Borrelia afzelii with tick salivary gland extract influences distribution of immunocompetent cells in the skin and lymph nodes of mice. Folia Microbiol. 50: 457-463. Go to original source... Go to PubMed...
  27. Singh K., Davies G., Alenazi Y., Eaton J.R.O., Kawamura A., Bhattacharya S. 2017: Yeast surface display identifies a family of evasins from ticks with novel polyvalent CC chemokine-binding activities. Sci. Rep. 7: 4267. Go to original source... Go to PubMed...
  28. Steen N.A., Barker S.C., Alewood P.F. 2006: Proteins in the saliva of the Ixodida (ticks): pharmacological features and biological significance. Toxicon 47: 1-20. Go to original source... Go to PubMed...
  29. Steere A.C., Coburn J., Glickstein L. 2004: The emergence of Lyme disease. J. Clin. Invest. 113: 1093-1101. Go to original source... Go to PubMed...
  30. Sun Y., Xu R. 2003: Ability of Ixodes persulcatus, Haemaphysalis concinna and Dermacentor silvarum ticks to acquire and transstadially transmit Borrelia garinii. Exp. Appl. Acarol. 31: 151-160. Go to original source... Go to PubMed...
  31. Vachiery N., Puech C., Cavelier P., Rodrigues V., Aprelon R., Lefrançois T., Martinez D., Epardaud M. 2015: An in vitro model to assess the immunosuppressive effect of tick saliva on the mobilization of inflammatory monocyte-derived cells. Vet. Res. 46: 117. Go to original source... Go to PubMed...
  32. Vančová I., Hajnická V. Slovák M., Nuttall P.A. 2010: Anti-chemokine activities of ixodid ticks depend on tick species, developmental stage, and duration of feeding. Vet. Parasitol. 167: 274-278. Go to original source... Go to PubMed...
  33. Wikel S. 2013: Ticks and tick-borne pathogens at the cutaneous interface: host defences, tick countermeasures, and a suitable environment for pathogen establishment. Front. Microbiol. 4: 337. Go to original source... Go to PubMed...
  34. Zeidner N., Dreitz M., Belasco D., Fish D. 1996: Suppression of acute Ixodes scapularis-induced Borrelia burgdorferi infection using tumor necrosis factor-alpha, interleukin-2, and interferon-gamma. J. Infect. Dis. 173: 187-195. Go to original source... Go to PubMed...