Tick saliva induces regulatory dendritic cells: MAP-kinases and Toll-like receptor-2 expression as potential targets

Veterinary Parasitology

Volumn 167, Issue 2-4, 2010, Pages 288-297

  Oliveira, Carlo José F ^a   Carvalho, Wanessa A ^a   Garcia, Gustavo R ^a   Gutierrez, Fredy R S ^a   de Miranda Santos, Isabel K F ^a   Silva, João S ^a   Ferreira, Beatriz R ^a,b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Laboratory of Pharmacology   (Brazil)

Author keywords

Dendritic cells; MAP kinases; Rhipicephalus sanguineus; Tick saliva; Toll like receptors

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 12P70; LIPOPOLYSACCHARIDE; LIPOTEICHOIC ACID; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW; CELL MATURATION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DOG; ENZYME INHIBITION; GENE EXPRESSION REGULATION; HOST SUSCEPTIBILITY; IMMUNE RESPONSE; IMMUNOMODULATION; INFESTATION; MOUSE; NONHUMAN; PROTEIN TARGETING; RHIPICEPHALUS SANGUINEUS; SALIVA; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; CHEMOKINES; DENDRITIC CELLS; FEMALE; GENE EXPRESSION REGULATION; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; RATS; RHIPICEPHALUS; SALIVA; TOLL-LIKE RECEPTOR 2;

ACARI; ARTHROPODA; IXODIDA; IXODIDAE; RHIPICEPHALUS SANGUINEUS;

EID: 74449091935     PISSN: 03044017     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetpar.2009.09.031     Document Type: Article

References (56)

1. Agrawal S., Agrawal A., Doughty B., Gerwitz A., Blenis J., Van Dyke T., and Pulendran B. Cutting edge: different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos. J. Immunol. 171 (2003) 4984-4989
2. An H., Yu Y., Zhang M., Xu H., Qi R., Yan X., Liu S., Wang W., Guo Z., Guo J., Qin Z., and Cao X. Involvement of ERK, p38 and NF-kappa B signal transduction in regulation of TLR2, TLR4 and TLR9 gene expression induced by lipopolysaccharide in mouse dendritic cells. Immunology 106 (2002) 38-45
3. Arrighi J.F., Rebsamen M., Rousset F., Kindler V., and Hauser C. A critical role for p38 mitogen-activated protein kinase in the maturation of human blood-derived dendritic cells induced by lipopolysaccharide, TNF-α, and contact sensitizers. J. Immunol. 166 (2001) 3837-3845
4. Babu S., Blauvelt C.P., Kumaraswami V., and Nutman T.B. Diminished expression and function of TLR in lymphatic filariasis: a novel mechanism of immune dysregulation. J. Immunol. 175 (2005) 1170-1176
5. Beaman M.H., Hunter C.A., and Remington J.S. Enhancement of intracellular replication of Toxoplasma gondii by IL-6: interactions with IFN-γ and TNF-α. J. Immunol. 153 (1994) 4583-4588
6. Bermudez L.E., Wu M., Petrofsky M., and Young L.S. Interleukin-6 antagonizes tumor necrosis factor-mediated mycobacteriostatic and mycobactericidal activities in macrophages. Infect. Immun. 60 (1992) 4245-4252
7. Bihl F., Salez L., Beaubier M., Torres D., Larivière L., Laroche L., Benedetto A., Martel D., Lapointe J.M., Ryffel B., and Malo D. Overexpression of Toll-like receptor 4 amplifies the host response to lipopolysaccharide and provides a survival advantage in transgenic mice. J. Immunol. 170 (2003) 6141-6150
8. Boehmer E.D., Goral J., Faunce D.E., and Kovacs E.J. Age-dependent decrease in Toll-like receptor 4-mediated proinflammatory cytokine production and mitogen-activated protein kinase expression. J. Leukoc. Biol. 75 (2004) 342-349
9. Bowman A.S., Coons L.B., Needham G.R., and Sauer J.R. Tick saliva: recent advances and implications for vector competence. Med. Vet. Entomol. 11 (1997) 277-285
10. Cavassani K.A., Aliberti J.C., Dias A.R.V., Silva J.S., and Ferreira B.R. Tick saliva inhibits differentiation, maturation and function of murine bone-marrow-derived dendritic cells. Immunology 114 (2005) 235-245
11. Chandra D., and Naik S. Leishmania donovani infection down-regulates TLR2-stimulated IL-12p40 and activates IL-10 in cells of macrophage/monocytic lineage by modulating MAPK pathways through a contact-dependent mechanism. Clin. Exp. Immunol. 154 (2008) 224-234
12. D'Andrea A., Aste-Amezaga M., Valiante N.M., Ma X., Kubin M., and Trinchieri G. Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J. Exp. Med. 178 (1993) 1041-1048
13. Demma L.J., Eremeeva M., Nicholson W.L., Traeger M., Blau D., Paddock C., Levin M., Dasch G., Cheek J., Swerdlow D., and McQuiston J. An outbreak of Rocky Mountain spotted fever associated with a novel tick vector, Rhipicephalus sanguineus, in Arizona, 2004: preliminary report. Ann. N. Y. Acad. Sci. 1078 (2006) 342-343
14. Diehl S., and Rincon M. The two faces of IL-6 on Th1/Th2 differentiation. Mol. Immunol. 39 (2002) 531-536
15. Ferreira B.R., and Silva J.S. Saliva of Rhipicephalus sanguineus tick impairs T cell proliferation and IFN-γ-induced macrophage microbicidal activity. Vet. Immunol. Immunopathol. 64 (1998) 279-293
16. Ferreira B.R., and Silva J.S. Successive tick infestations selectively promote a T helper 2 cytokine profile in mice. Immunology 96 (1999) 434-439
17. Ferreira K.S., Bastos K.R., Russo M., and Almeida S.R. Interaction between Paracoccidioides brasiliensis and pulmonary dendritic cells induces interleukin-10 production and toll-like receptor-2 expression: possible mechanisms of susceptibility. J. Infect. Dis. 196 (2007) 108-115
18. Filippi C.M., and von Herrath M.G. IL-10 and the resolution of infections. J. Pathol. 214 (2008) 224-230
19. Flechtmann, C.H.W., 1973. Ácaros de importância médico-veterinária, Ed. Livraria Nobel S.A., São Paulo, 104 pp.
20. Frauenschuh A., Power C.A., Déruaz M., Ferreira B.R., Silva J.S., Teixeira M.M., Dias J.M., Martin T., Wells T.N., and Proudfoot A.E. Molecular cloning and characterization of a highly selective chemokine-binding protein from the Tick Rhipicephalus sanguineus. J. Biol. Chem. 282 (2007) 27250-27258
21. Hajnická V., Kocáková P., Sláviková M., Slovák M., Gašperík J., Fuchsberger N., and Nuttall P.A. Anti-interleukin-8 activity of tick salivary gland extracts. Parasite Immunol. 9 (2001) 483-489
22. Hoarau C., Lagaraine C., Martin L., Velge-Roussel F., and Lebranchu Y. Supernatant of Bifidobacterium breve induces dendritic cell maturation, activation, and survival through a Toll-like receptor 2 pathway. J. Allergy Clin. Immunol. 117 (2006) 696-702
23. Keber M.M., Gradisar H., and Jerala R. MD-2 and Der p 2-a tale of two cousins or distant relatives?. J. Endotoxin Res. 11 (2005) 186-192
24. Kim H.K., Lee J.J., Lee J.S., Park Y.M., and Yoon T.R. Rosmarinic acid down-regulates the LPS-induced production of monocyte chemoattractant protein-1 (MCP-1) and macrophage inflammatory protein-1 alpha (MIP-1 alpha) via the MAPK pathway in bone-marrow derived dendritic cells. Mol. Cells 26 (2008) 583-589
25. Kishimoto T. Interleukin-6: from basic science to medicine-40 years in immunology. Annu. Rev. Immunol. 23 (2005) 1-21
26. Kramer C., Nahmias Z., Norman D.D., Mulvihill T.A., Coons L.B., and Cole J.A. Dermacentor variabilis: regulation of fibroblast migration by tick salivary gland extract and saliva. Exp. Parasitol. 119 (2008) 391-397
27. Kubes M., Fuchsberger N., Labuda M., Zuffová E., and Nuttall P.A. Salivary gland extracts of partially fed Dermacentor reticulatus ticks decrease natural killer cell activity in vitro. Immunology 82 (1994) 113-116
28. Lutz M.B., Kukutsch N., Ogilvie A.L., Rossner S., Koch F., Romani N., and Schuler G. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223 (1999) 77-92
29. Mejri N., Franscini N., Rutti B., and Brossard M. Th2 polarization of the immune response of BALB/c mice to Ixodes ricinus instars, importance of several antigens in activation of specific Th2 subpopulations. Parasite Immunol. 23 (2001) 61-69
30. Murray H.W. Accelerated control of visceral Leishmania donovani infection in interleukin-6-deficient mice. Infect. Immun. 76 (2008) 4088-4089
31. Nakahara T., Moroi Y., Uchi H., and Furue M. Differential role of MAPK signalling in human dendritic cell maturation and Th1/Th2 engagement. J. Dermatol. Sci. 42 (2006) 1-11
32. Netea M.G., Sutmuller R., Hermann C., Van der Graaf C.A., Van der Meer J.W., van Krieken J.H., Hartung T., Adema G., and Kullberg B.J. Toll-like receptor 2 suppresses immunity against Candida albicans through induction of IL-10 and regulatory T cells. J. Immunol. 172 (2004) 3712-3718
33. Ninomiya-Tsuji J., Kishimoto K., Hiyama A., Inoue J., Cao Z., and Matsumoto K. The kinase TAK1 can activate the NIK-I kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 398 (1999) 252-256
34. Oliveira C.J., Cavassani K.A., Moré D.D., Garlet G.P., Aliberti J.C., Silva J.S., and Ferreira B.R. Tick saliva inhibits the chemotactic function of MIP-1α and selectively impairs chemotaxis of immature dendritic cells by down-regulating cell-surface CCR5. Int. J. Parasitol. 38 (2008) 705-716
35. Privé C., and Descoteaux A. Leishmania donovani promastigotes evade the activation of mitogen-activated protein kinases p38, c-Jun N-terminal kinase, and extracellular signal-regulated kinase-1/2 during infection of naive macrophages. Eur. J. Immunol. 30 (2000) 2235-2244
36. Pulendran B. Variegation of the immune response with dendritic cells and pathogen recognition receptors. J. Immunol. 174 (2005) 2457-2465
37. Ramachandra R.N., and Wikel S.K. 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 (1992) 818-826
38. Ramachandra R.N., and Wikel S.K. Effects of Dermacentor andersoni (Acari: Ixodidae) salivary gland extracts on Bos indicus and B. taurus lymphocytes and macrophages: in vitro cytokine elaboration and lymphocyte blastogenesis. J. Med. Entomol. 32 (1995) 338-345
39. Renshaw M., Rockwell J., Engleman C., Gewirtz A., Katz J., and Sambhara S. Cutting edge: impaired Toll-like receptor expression and function in aging. J. Immunol. 169 (2002) 4697-4701
40. Rescigno M., Martino M., Sutherland C.L., Gold M.R., and Ricciardi-Castagnoli P. Dendritic cell survival and maturation are regulated by different signalling pathways. J. Exp. Med. 188 (1998) 2175-2180
41. Ribeiro J.M. Ixodes dammini: salivary anti-complement activity. Exp. Parasitol. 64 (1987) 347-353
42. Ribeiro J.M., Weiss J.J., and Telford III S.R. Saliva of the tick Ixodes dammini inhibits neutrophil function. Exp. Parasitol. 70 (1990) 382-388
43. Ribeiro J.M. How ticks make a living. Parasitol. Today 113 (1995) 91-93
44. Rincón M., Anguita J., Nakamura T., Fikrig E., and Flavell R.A. Interleukin (IL)-6 directs the differentiation of IL-4-producing CD4+ T cells. J. Exp. Med. 185 (1997) 461-469
45. Rudenko N., Golovchenko M., Edwards M.J., and Grubhoffer L. Differential expression of Ixodes ricinus tick genes induced by blood feeding or Borrelia burgdorferi infection. J. Med. Entomol. 42 (2005) 36-41
46. Sá-Nunes A., Bafica A., Lucas D.A., Conrads T.P., Veenstra T.D., Andersen J.F., Mather T.N., Ribeiro J.M., and Francischetti I.M. Prostaglandin E2 is a major inhibitor of dendritic cell maturation and function in Ixodes scapularis saliva. J. Immunol. 179 (2007) 1497-1505
47. Schoeler G.B., Manweiler S.A., and 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 (1999) 239-248
48. Sing A., Rost D., Tvardovskaia N., Roggenkamp A., Wiedemann A., Kirschning C.J., Aepfelbacher M., and Heesemann J. Yersinia V-antigen exploits toll-like receptor 2 and CD14 for interleukin 10-mediated immunosuppression. J. Exp. Med. 196 (2002) 1017-1024
49. Skallová A., Iezzi G., Ampenberger F., Kopf M., and Kopecky J. Tick saliva inhibits dendritic cell migration, maturation, and function while promoting development of Th2 responses. J. Immunol. 180 (2008) 6186-6192
50. Trinchieri G. Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity. Annu. Rev. Immunol. 13 (1995) 251-276
51. Uchi H., Arrighi J.F., Aubry J.P., Furue M., and Hauser C. The sesquiterpene lactone parthenolide inhibits LPS- but not TNF-alpha-induced maturation of human monocyte-derived dendritic cells by inhibition of the p38 mitogen-activated protein kinase pathway. J. Allergy. Clin. Immunol. 110 (2002) 269-276
52. Urioste S., Hall L.R., Telford S.R.3rd., and Titus R.G. Saliva of the Lyme disease vector, Ixodes dammini, blocks cell activation by a nonprostaglandin E2-dependent mechanism. J. Exp. Med. 180 (1994) 1077-1085
53. Valenzuela J.G. Exploring tick saliva: from biochemistry to 'sialomes' and functional genomics. Parasitology 129 Suppl. (2004) S83-S94
54. Vancová I., Slovák M., Hajnická V., Labuda M., Simo L., Peterková K., Hails R.S., and Nuttall P.A. Differential anti-chemokine activity of Amblyomma variegatum adult ticks during blood-feeding. Parasite Immunol. 29 (2007) 1-9
55. van der Kleij D., Latz E., Brouwers J.F., Kruize Y.C., Schmitz M., Kurt-Jones E.A., Espevik T., de Jong E.C., Kapsenberg M.L., Golenbock D.T., Tielens A.G., and Yazdanbakhsh M. A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. J. Biol. Chem. 277 (2002) 48122-48129
56. Walker J.B., Keirans J.E., and Horak I.G. The Genus Rhipicephalus (Acari, Ixodidae). A Guide to the Brown Ticks of the World (2000), Cambridge University Press, New York 643 p.