Tick saliva represses innate immunity and cutaneous inflammation in a Murine model of lyme disease

Vector-Borne and Zoonotic Diseases

Volumn 11, Issue 10, 2011, Pages 1343-1350

  Kern, Aurélie ^a   Collin, Elody ^a   Barthel, Cathy ^a   Michel, Chloé ^a,b   Jaulhac, Benoît ^a   Boulanger, Nathalie ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Borrelia; Cathelicidin; Cutaneous inflammation; Defensin; Innate immunity; Ixodes ricinus; Tick saliva

Indexed keywords

CATHELICIDIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL TRANSMISSION; BACTERIUM CONTAMINATION; BORRELIA BURGDORFERI; CONTROLLED STUDY; DISEASE CARRIER; HOST PATHOGEN INTERACTION; INNATE IMMUNITY; INOCULATION; LYME DISEASE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SALIVA ANALYSIS; SKIN INFLAMMATION; TICK; TICK INFESTATION;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; ARACHNID VECTORS; BORRELIA BURGDORFERI; DEFENSINS; DERMATITIS; DISEASE MODELS, ANIMAL; HEART; IMMUNITY, INNATE; JOINTS; LYME DISEASE; MICE; MICE, INBRED C3H; POLYMERASE CHAIN REACTION; SALIVA; SKIN; TICKS; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA; URINARY BLADDER;

ARTHROPODA; BACTERIA (MICROORGANISMS); BORRELIA; IXODES; IXODES RICINUS; IXODIDA; MURINAE; VERTEBRATA;

EID: 80053628360     PISSN: 15303667     EISSN: 15577759     Source Type: Journal    
DOI: 10.1089/vbz.2010.0197     Document Type: Article

References (47)

1. Adusumilli, S, Booth, CJ, Anguita, J, Fikrig, E. Passage through Ixodes scapularis ticks enhances the virulence of a weakly pathogenic isolate of Borrelia burgdorferi. Infect Immun 2010; 78:138-144.
2. Amino, R, Thiberge, S, Martin, B, Celli, S, et al. Quantitative imaging of Plasmodium transmission from mosquito to mammal. Nat Med 2006; 12:220-224. (Pubitemid 43214749)
3. Antonara, S, Ristow, L, McCarthy, J, Coburn, J. Effect of Borrelia burgdorferi OspC at the site of inoculation in mouse skin. Infect Immun 2010; 78:4723-4733.
4. Braff, MH, Gallo, RL. Antimicrobial peptides: An essential component of the skin defensive barrier. Curr Top Microbiol Immunol 2006; 306:91-110. (Pubitemid 47400319)
5. Brossard, M, Wikel, SK. Tick immunobiology. Parasitology 2004; 129 Suppl:S161-S176. (Pubitemid 40780694)
6. Crippa, M, Rais, O, Gern, L. Investigations on the mode and dynamics of transmission and infectivity of Borrelia burgdorferi sensu stricto and Borrelia afzelii in Ixodes ricinus ticks. Vector Borne Zoonot Dis 2002; 2:3-9.
7. Dinulos, JG, Mentele, L, Fredericks, LP, Dale, BA, et al. Keratinocyte expression of human beta defensin 2 following bacterial infection: Role in cutaneous host defense. Clin Diagn Lab Immunol 2003; 10:161-166. (Pubitemid 36133844)
8. Dorschner, RA, Lin, KH, Murakami, M, Gallo, RL. Neonatal skin in mice and humans expresses increased levels of antimicrobial peptides: Innate immunity during development of the adaptive response. Pediatr Res 2003; 53:566-572. (Pubitemid 36406725)
9. Dorschner, RA, Pestonjamasp, VK, Tamakuwala, S, Ohtake, T, et al. Cutaneous injury induces the release of cathelicidin antimicrobial peptides active against group A Streptococcus. J Invest Dermatol 2001; 117:91-97. (Pubitemid 32652444)
10. Frischknecht. The skin as interface in the transmission of arthropod- borne pathogens. Cell Microbiol 2007; 9:1630-1640.
11. Garg, R, Juncadella, IJ, Ramamoorthi, N, Ananthanarayanan, SK, et al. Cutting edge: CD4 is the receptor for the tick saliva immunosuppressor, Salp15. J Immunol 2006; 177: 6579-6583. (Pubitemid 44715018)
12. Gillespie, RD, Dolan, MC, Piesman, J, Titus, RG. Identification of an IL-2 binding protein in the saliva of the Lyme disease vector tick, Ixodes scapularis. J Immunol 2001; 166:4319-4326.
13. Giulietti, A, Overbergh, L, Valckx, D, Decallonne, B, et al. An overview of real-time quantitative PCR: Applications to quantify cytokine gene expression. Methods 2001; 25:386-401. (Pubitemid 34164011)
14. Gueirard, P, Tavares, J, Thiberge, S, Bernex, F, et al. Development of the malaria parasite in the skin of the mammalian host. Proc Natl Acad Sci USA 2010; 107:18640-18645.
15. Hinrichsen, K, Podschun, R, Schubert, S, Schrö der, JM, et al. Mouse beta-defensin-14, an antimicrobial ortholog of human beta-defensin-3. Antimicrob Agents Chemother 2008; 52: 1876-1879. (Pubitemid 351614694)
16. Hodzic, E, Feng, S, Freet, KJ, Barthold, SW. Borrelia burgdorferi population dynamics and prototype gene expression during infection of immunocompetent and immunodeficient mice. Infect Immun 2003; 71:5042-5055. (Pubitemid 37070747)
17. Hojgaard, A, Eisen, RJ, Piesman, J. Transmission dynamics of Borrelia burgdorferi s.s. during the key third day of feeding by nymphal Ixodes scapularis (Acari: Ixodidae). J Med Entomol 2008; 45:732-736.
18. Hovius, JW, Schuijt, TJ, de Groot, KA, Roelofs, JJ, et al. Preferential protection of Borrelia burgdorferi sensu stricto by a Salp15 homologue in Ixodes ricinus saliva. J Infect Dis 2008; 198:1189-1197.
19. Hovius, JW, van Dam, AP, Fikrig, E. Tick-host-pathogen interactions in Lyme borreliosis. Trends Parasitol 2007; 23:434-438. (Pubitemid 47271975)
20. Jaulhac, B, Heller, R, Limbach, FX, Hansmann, Y, et al. Direct molecular typing of Borrelia burgdorferi sensu lato species in synovial samples from patients with Lyme arthritis. J Clin Microbiol 2000; 38:1895-1900. (Pubitemid 30253934)
21. Krause, PJ, Grant-Kels, JM, Tahan, SR, Dardick, KR, et al. Dermatologic changes induced by repeated Ixodes scapularis bites and implications for prevention of tick-borne infection.Vector Borne Zoonot Dis 2009; 9:603-610.
22. Lee, YR, Liu, MT, Lei, HY, Liu, CC, et al. MCP-1, a highly expressed chemokine in dengue haemorrhagic fever/dengue shock syndrome patients, may cause permeability change, possibly through reduced tight junctions of vascular endothelium cells. J Gen Virol 2006; 87:3623-3630. (Pubitemid 44816994)
23. Marchal, C, Schramm, F, Kern, A, Luft, BJ, et al. Antialarmin effect of tick saliva during the transmission of Lyme disease. Infect Immun 2011; 79:774-785.
24. Marchal, CM, Luft, BJ, Yang, X, Sibilia, J, 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; 129:2515-2517.
25. Mbow, ML, Christe, M, Rutti, B, Brossard, M. Absence of acquired resistance to nymphal Ixodes ricinus ticks in BALB/c mice developing cutaneous reactions. J Parasitol 1994; 80: 81-87. (Pubitemid 24058888)
26. Nakazawa, T, Nakazawa, C, Matsubara, A, Noda, K, et al. Tumor necrosis factor-alpha mediates oligodendrocyte death and delayed retinal ganglion cell loss in a mouse model of glaucoma. J Neurosci 2006; 26:12633-12641. (Pubitemid 44904557)
27. Nizet, V, Ohtake, T, Lauth, X, Trowbridge, J, et al. L Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 2001; 414:454-457. (Pubitemid 34173727)
28. Ohnishi, J, Piesman, J, de Silva, AM. Antigenic and genetic heterogeneity of Borrelia burgdorferi populations transmitted by ticks. Proc Natl Acad Sci USA 2001; 98:670-675. (Pubitemid 32105101)
29. Ong, PY, Ohtake, T, Brandt, C, Strickland, I, et al. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 2002; 347:1151-1160.
30. Pechová , J, Stêpánová , G, Ková r, L, Kopecký , J. Tick salivary gland extract-activated transmission of Borrelia afzelii spirochaetes. Folia Parasitol (Praha) 2002; 49:153-159. (Pubitemid 34780670)
31. Piesman, J, Mather, TN, Sinsky, RJ, Spielman, A. Duration of tick attachment and Borrelia burgdorferi transmission. J Clin Microbiol 1987; 25:557-558. (Pubitemid 17015570)
32. Piesman, J, Schneider, BS, Zeidner, NS. Use of quantitative PCR to measure density of Borrelia burgdorferi in the midgut and salivary glands of feeding tick vectors. J Clin Microbiol 2001; 39:4145-4148. (Pubitemid 33029796)
33. Schrö der, JM, Harder, J. Antimicrobial skin peptides and proteins. Cell Mol Life Sci 2006; 63:469-486.
34. Schuijt, TJ, Hovius, JW, van der Poll, T, van Dam, AP, et al. Lyme borreliosis vaccination: The facts, the challenge and the future. Trends Parasitol 2011; 27:40-47.
35. Sinnis, P, Zavala, F. The skin stage of malaria infection: Biology and relevance to the malaria vaccine effort. Future Microbiol 2008; 3:275-278. (Pubitemid 352003138)
36. Skallová , A, Iezzi, G, Ampenberger, F, Kopf, M, Kopecky, J. Tick saliva inhibits dendritic cell migration, maturation, and function while promoting development of Th2 responses. J Immunol 2008; 180:6186-6192.
37. Soulas, P, Woods, A, Jaulhac, B, Knapp, AM, et al. Autoantigen, innate immunity, and T cells cooperate to break B cell tolerance during bacterial infection. J Clin Investig 2005; 115:2257-2267. (Pubitemid 41134168)
38. Steere, AC, Coburn, J, Glickstein, L. The emergence of Lyme disease. J Clin Invest 2004; 113:1093-1101. (Pubitemid 38544091)
39. Sumikawa, Y, Asada, H, Hoshino, K, Azukizawa, H, et al. Induction of beta-defensin 3 in keratinocytes stimulated by bacterial lipopeptides through toll-like receptor 2. Microbes Infect 2006; 8:1513-1521. (Pubitemid 44192354)
40. Tilly, K, Krum, JG, Bestor, A, Jewett, MW, et al. Borrelia burgdorferi OspC protein required exclusively in a crucial early stage of mammalian infection. Infect Immun 2006; 74:3554-3564. (Pubitemid 43794547)
41. Tyson, KR, Elkins, C, de Silva, AM. A novel mechanism of complement inhibition unmasked by a tick salivary protein that binds to properdin. J Immunol 2008; 180:3964-3968.
42. Valenzuela, JG, Charlab, R, Mather, TN, Ribeiro, JM. Purification, cloning, and expression of a novel salivary anticomplement protein from the tick, Ixodes scapularis. J Biol Chem 2000; 275:18717-18723. (Pubitemid 30422830)
43. Wikel, SK. Tick modulation of host immunity: An important factor in pathogen transmission. Int J Parasitol 1999; 29:851-859. (Pubitemid 29352326)
44. Wikel, SK, Graham, JE, Allen, JR. Acquired resistance to ticks. Skin reactivity and in vitro lymphocyte responsiveness to salivary gland antigen. Immunology 1978; 34:257-263. (Pubitemid 8287089)
45. Woods, A, Soulas-Sprauel, P, Jaulhac, B, Arditi, B, et al. MyD88 negatively controls hypergammaglobulinemia with autoantibody production during bacterial infection. Infect Immun 2008; 76:1657-1667. (Pubitemid 351562010)
46. Zeidner, NS, Schneider, BS, Dolan, MC, Piesman, J. An analysis of spirochete load, strain, and pathology in a model of ticktransmitted Lyme borreliosis. Vector Borne Zoonot Dis 2001; 1:35-44.
47. Zhao, Z, McCloud, B, Fleming, R, Klempner, MS. Borrelia burgdorferi-induced monocyte chemoattractant protein-1 production in vivo and in vitro. Biochem Biophys Res Commun 2007; 358:528-533. (Pubitemid 46766598)