European Journal of Dermatology

, Volume 25, Supplement 1, pp 18–22 | Cite as

Skin and arthropods: an effective interaction used by pathogens in vector-borne diseases

  • Quentin Bernard
  • Benoît Jaulhac
  • Nathalie Boulanger
SPIM 2014 Proceedings


In the last years, the skin has been described as a major interface in arthropod borne diseases. Although it constitutes an efficient immune and physical barrier, pathogens have developed effective strategies to thwart the host. In this process, the arthropod plays a major role. For mosquitoes, the quick blood meal is made through an efficient inoculation process directly into the blood vessel. For the long lasting blood meal of hard ticks, the sophisticated biting pieces and the tick saliva provide potent tools to help pathogen transmission. Lyme borreliosis and leishmaniases have been particularly well investigated in this context.


keratinocytes fibroblasts dendritic cell arthropod saliva vector-borne diseases leishmaniasis Lyme borreliosis 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Knols BG, Jong R De BG. Limburger cheese as an attractant for the malaria mosquito Anopheles gambiae s.s. Parasitol Today 1996; 12: 159–61.PubMedCrossRefGoogle Scholar
  2. 2.
    Bernard Q, Jaulhac B, Boulanger N. Smuggling across the Border: How Arthropod-Borne Pathogens Evade and Exploit the Host Defense System of the Skin. J Invest Dermatol 2014; 134: 1211–9.PubMedCrossRefGoogle Scholar
  3. 3.
    Vizioli J, Bulet P, Hoffmann J, et al. Gambicin: a novel immune responsive antimicrobial peptide from the malaria vector Anopheles gambiae. Proc Natl Acad Sci USA 2001; 98: 12630–5.PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Boulanger N, Bulet P, Lowenberger C. Antimicrobial peptides in the interactions between insects and flagellate parasites. Trends Parasitol 2006; 22: 262–8.PubMedCrossRefGoogle Scholar
  5. 5.
    Hajdu?sek O, Síma R, Ayllón N, et al. Interaction of the tick immune system with transmitted pathogens. Front Cell Infect Microbiol 2013; 3: 26.Google Scholar
  6. 6.
    Nestle FO, Meglio P Di FO, Qin JZ, et al. Skin immune sentinels in health and disease. Nat Rev Immunol 2009; 9: 679–91.PubMedCentralPubMedGoogle Scholar
  7. 7.
    Sonenshine D. Biology of ticks: vol.1. 1991.Google Scholar
  8. 8.
    Elston DM. Tick bites and skin rashes. Curr Opin Infect Dis 2010; 23: 132–8.PubMedCrossRefGoogle Scholar
  9. 9.
    Burke G, Wikel SK, Spielman A, et al. Hypersensitivity to ticks and Lyme disease risk. Emerg Infect Dis 2005; 11: 36–41.PubMedCentralPubMedGoogle Scholar
  10. 10.
    Titus RG, Bishop JV, Mejia JS. The immunomodulatory factors of arthropod saliva and the potential for these factors to serve as vaccine targets to prevent pathogen transmission. Parasite Immunol 2006; 28: 131–41.PubMedGoogle Scholar
  11. 11.
    Francischetti IM1, Sa-Nunes A, Mans BJ, Santos IMRJ. NIH Public Access. Front Biosci 2010; 14: 2051–88.Google Scholar
  12. 12.
    Wikel S. Ticks and tick-borne pathogens at the cutaneous interface: host defenses, tick countermeasures, and a suitable environment for pathogen establishment. Front Microbiol 2013; 4: 337.PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Titus RG, Ribeiro JM. Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 1988; 239: 1306–8.PubMedCrossRefGoogle Scholar
  14. 14.
    Patramool S, Choumet V, Surasombatpattana P, et al. Update on the proteomics of major arthropod vectors of human and animal pathogens. Proteomics 2012; 12: 3510–23.PubMedCrossRefGoogle Scholar
  15. 15.
    Gomes R, Oliveira F. The immune response to sand fly salivary proteins and its influence on leishmania immunity. Front Immunol 2012; 3: 110.PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    SKazimírová M, ?tibrániová I. Tick salivary compounds: their role in modulation of host defences and pathogen transmission. Front Cell Infect Microbiol 2013; 3: 43.Google Scholar
  17. 17.
    Liu XY, Bonnet SI. Hard Tick Factors Implicated in Pathogen Transmission. PLoS Negl Trop Dis 2014; 8: e2566.PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Ramamoorthi N, Narasimhan S, Pal U, et al. The Lyme disease agent exploits a tick protein to infect the mammalian host. Nature 2005; 436: 573–7.PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Hovius JWR, Levi M, Fikrig E. Salivating for knowledge: Potential pharmacological agents in tick saliva. PLoS Med 2008; 5: e43.PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Kebaier C, Voza T, Vanderberg J. Neither mosquito saliva nor immunity to saliva has a detectable effect on the infectivity of Plasmodium sporozoites injected into mice. Infect Immun 2010; 78: 545–51.PubMedCentralPubMedCrossRefGoogle Scholar
  21. 21.
    Guilbride DL, Guilbride PDL, Gawlinski P. Malaria’s deadly secret: a skin stage. Trends Parasitol 2012; 28: 142–50.PubMedCrossRefGoogle Scholar
  22. 22.
    Peters NC, Egen JG, Secundino N, et al. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 2008; 321: 970–4.PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Ribeiro-Gomes FL, Peters NC, Debrabant A, et al. Efficient capture of infected neutrophils by dendritic cells in the skin inhibits the early anti-leishmania response. PLoS Pathog 2012; 8: e1002536.PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Gueirard P, Tavares J, Thiberge S, et al. Development of the malaria parasite in the skin of the mammalian host. Proc Natl Acad Sci USA 2010; 107: 18640–5.PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Ménard R, Tavares J, Cockburn I, Markus M, Zavala FAR. Looking under the skin: the first steps in malarial infection and immunity. Nat Rev Microbiol 2013; 11: 701–12.PubMedCrossRefGoogle Scholar
  26. 26.
    Mac-Daniel L, Buckwalter M, Berthet M, et al. Local immune response to injection of Plasmodium sporozoites into the skin. J Immunol 2014; 193: 1246–57.PubMedCrossRefGoogle Scholar
  27. 27.
    Tassaneetrithep B, Burgess TH, Granelli-Piperno A, et al. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 2003; 197: 823–9.PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Surasombatpattana P, Patramool S, Luplertlop N, et al. Aedes aegypti saliva enhances dengue virus infection of human keratinocytes by suppressing innate immune responses. J Invest Dermatol 2012; 132: 2103–5.PubMedCrossRefGoogle Scholar
  29. 29.
    Bustos-Arriaga J, García-Machorro J, León-Juárez M, et al. Activation of the innate immune response against DENV in normal nontransformed human fibroblasts. PLoS Negl Trop Dis 2011; 5: e1420.PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    McCracken M, Christofferson RC, Grasperge B, Calvo E, et al. Aedes aegypti salivary protein “aegyptin” co-inoculation modulates dengue virus infection in the vertebrate host. Virology 2014; 468-470: 133–9.PubMedCrossRefGoogle Scholar
  31. 31.
    Radolf JD, Caimano MJ, Stevenson B, et al. Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes. Nat Rev Microbiol 2012; 10: 87–99.PubMedCentralPubMedGoogle Scholar
  32. 32.
    Kern A, Collin E, Barthel C, et al. Tick saliva represses innate immunity and cutaneous inflammation in a murine model of lyme disease. Vector Borne Zoonotic Dis 2011; 11: 1343–50.PubMedCrossRefGoogle Scholar
  33. 33.
    Brisson D, Baxamusa N, Schwartz I, et al. Biodiversity of Borrelia burgdorferi strains in tissues of Lyme disease patients. PLoS One 2011; 6: e22926.PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Marchal CMP, Luft BJ, Yang X, et al. Defensin is suppressed by tick salivary gland extract during the in vitro interaction of resident skin cells with Borrelia burgdorferi. J Invest Dermatol 2009; 129: 2515–7.PubMedCrossRefGoogle Scholar
  35. 35.
    Schramm F, Kern A, Barthel C, et al. Microarray analyses of inflammation response of human dermal fibroblasts to different strains of Borrelia burgdorferi sensu stricto. PLoS One 2012; 7: e40046.PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    Stanek G, Wormser G, Gray J, et al. Lyme borreliosis. Lancet 2012; 379: 461–73.PubMedCrossRefGoogle Scholar
  37. 37.
    Mansfield KL, Johnson N, Phipps LP, et al. Tick-borne encephalitis virus- a review of an emerging zoonosis. J Gen Virol 2009; 90: 1781–94.PubMedCrossRefGoogle Scholar
  38. 38.
    Dörrbecker B, Dobler G, Spiegel M, et al. Tick-borne encephalitis virus and the immune response of the mammalian host. Travel Med Infect Dis 2010; 8: 213–22.PubMedCrossRefGoogle Scholar
  39. 39.
    Fialová A, Cimburek Z, Iezzi G, et al. Ixodes ricinus tick saliva modulates tick-borne encephalitis virus infection of dendritic cells. Microbes Infect 2010; 12: 580–5.PubMedCrossRefGoogle Scholar
  40. 40.
    Labuda M, Trimnell A, Licková M, et al. An antivector vaccine protects against a lethal vector-borne pathogen. PLoS Pathog 2006; 2: e27.PubMedCentralPubMedCrossRefGoogle Scholar
  41. 41.
    Fontaine A, Diouf I, Bakkali N, et al. Implication of haematophagous arthropod salivary proteins in host-vector interactions. Parasit Vectors 2011; 28: 187.CrossRefGoogle Scholar
  42. 42.
    Gallo RL, Nakatsuji T. Microbial symbiosis with the innate immune defense system of the skin. J Invest Dermatol 2011; 131: 1974–80.PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Verhulst N, Beijleveld H, Knols B, et al. Cultured skin microbiota attracts malaria mosquitoes. Malar J 2009; 17: 302.CrossRefGoogle Scholar

Copyright information

© John Libbey Eurotext 2015

Authors and Affiliations

  • Quentin Bernard
    • 1
  • Benoît Jaulhac
    • 1
    • 2
  • Nathalie Boulanger
    • 1
    • 2
  1. 1.EA7290: Virulence bactérienne précoce: groupe borréliose de Lymeuniversité de StrasbourgStrasbourgFrance
  2. 2.Centre national de référence Borreliacentre hospitalier UniversitaireStrasbourgFrance

Personalised recommendations