Helminth antigens modulate immune responses in cells from multiple sclerosis patients through TLR2-dependent mechanisms

Journal of Immunology

Volumn 183, Issue 9, 2009, Pages 5999-6012

  Correale, Jorge ^a   Farez, Mauricio ^a  

^a Instituto de Investigaciones Neurologicas Raul Carrera   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; CD40 ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; LYMPHOTOXIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYELOID DIFFERENTIATION FACTOR 88; PARASITE ANTIGEN; SMALL INTERFERING RNA; SYNAPTOPHYSIN; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA;

ADULT; AMEBIASIS; ARTICLE; B LYMPHOCYTE; CELL STIMULATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DOWN REGULATION; DRUG POTENCY; ENZYME PHOSPHORYLATION; FEMALE; GENE SILENCING; GIARDIASIS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; LEISHMANIASIS; MALE; MULTIPLE SCLEROSIS; PARASITOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SCHISTOSOMA MANSONI; SIGNAL TRANSDUCTION; TOXOPLASMOSIS; TRYPANOSOMIASIS;

ADULT; ANIMALS; ANTIGENS, HELMINTH; B-LYMPHOCYTE SUBSETS; CELLS, CULTURED; CYSTEINE; DENDRITIC CELLS; FEMALE; HUMANS; LIGANDS; LIPOPROTEINS; MALE; MULTIPLE SCLEROSIS; OVUM; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2;

EID: 77954161382     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900897     Document Type: Article

References (60)

1. McFarland, H. F., and R. Martin. 2007. Multiple sclerosis: a complicated picture of autoimmunity. Nat. Immunol. 8: 913-919.
2. Marrie, R. A. 2004. Environmental risk factors in multiple sclerosis aetiology. Lancet Neurol. 3: 709-718.
3. Oksenberg, J. R., S. E. Baranzini, S. Sawcer, and S. L. Hauser. 2008. The genetics of multiple sclerosis: SNP to pathways to pathogenesis. Nat. Rev. Genet. 9: 516-526.
4. Dyment, D. A., G. A. Ebers, and A. D. Sadovnik. 2004. Genetics of multiple sclerosis. Lancet Neurol. 4: 104-110.
5. Sadovnik, A. D., H. Armstrong, G. P. A. Rice, D. Bulman, L. Hashimoto, D. W. Paty, S. A. Hashimoto, S. Warren, W. Hader, T. J. Murray, et al. 1993. A population based study of multiple sclerosis in twins: update. Ann. Neurol. 33: 281-285.
6. Poser, S., B. Stickel, U. Krtsch, D. Burckhardt, and B. Nordman. 1989. Increasing evidence of multiple sclerosis in South Lower Saxony. Germany. Neuroepidemiology 8: 207-213. (Pubitemid 19157046)
7. EURODIAB ACE Study Group. 2000. Variations and trends in incidence of childhood diabetes in Europe. Lancet 355: 873-876.
8. Swarbrick, E. T., F. Farrokhyar, and E. J. Irvine. 2001. A critical review of epidemiological studies in inflammatory bowel disease. Scand. J. Gastroenterol. 36: 2-15. (Pubitemid 32147176)
9. Bach, J. F. 2002. The effect of infections on susceptibility to autoimmune and allergic diseases. N. Engl. J. Med. 347: 911-920.
10. Correale, J., and M. Farez. 2007. Association between parasite infection and immune responses in multiple sclerosis. Ann. Neurol. 61: 97-108.
11. Correale, J., M. Farez, and G. Razzite. 2008. Helminth infections associated with multiple sclerosis induce regulatory B cells. Ann. Neurol. 64: 187-199.
12. Gay, N. J., and M. Gangloff. 2007. Structure and function of Toll receptors and their ligands. Annu. Rev. Biochem. 76: 141-165.
13. Medzhitov, R. 2001. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1: 135-145.
14. Akira, S. 2003. Mammalian Toll-like receptors. Curr. Opin. Immunol. 15: 5-11.
15. O'Neill, L. A., and A. G. Bowie. 2007. The family of five: TIR-domain-containing adaptors in Toll-like receptor signaling. Nat. Rev. Immunol. 7: 353-364.
16. O'Neill, L. A. J. 2008. When signaling pathways collide: positive and negative regulation of Toll-like receptor signal transduction. Immunity 29: 12-20.
17. Boros, D. L., R. Tomford, and K. S. Warren. 1977. Induction of granulomatous and elicitation of cutaneous sensitivity by partially purified SEA of Schistosoma mansoni. J. Immunol. 118: 373-376.
18. Sallusto, F., and A. Lanzavecchia. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor α. J. Exp. Med. 179: 1109-1118. (Pubitemid 24983498)
19. Stumhofer, J. S., A. Laurence, E. H. Wilson, E. Huang, C. M. Tato, L. M. Johnson, A. V. Villarino, Q. Huang, A. Yoshimura, D. Sehy, et al. 2006. Interleukin 27 negatively regulates the development of interleukin 17-producing cells during chronic inflammation of the central nervous system. Nat. Immunol. 7: 937-945.
20. Betten, M., J. Li, S. Yi, N. M. Kljavin, D. M. Danilenko, S. Lucas, J. Lee, F. J. de Sauvage, and N. Ghilardi. 2006. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat. Immunol. 7: 929-936.
21. Betelli, E., Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, and V. K. Kuchroo. 2006. Reciprocal development pathways for the generation of pathogenic effector Th17 and regulatory T cells. Nature 441: 235-238.
22. Veldhoen, M., R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Strockinger. 2006. TGF-β in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17 producing T cells. Immunity 24: 179-189.
23. Jankovic, D., S. Steinfleder, M. C. Kullberg, and A. Sher. 2006. Mechanisms underlying helminth-induced Th2 polarization: default, negative or positive pathways. Chem. Immunol. Allergy. 90: 65-81. (Pubitemid 43265668)
24. Fallon, P. G., and N. E. Mangan. 2007. Suppression of Th2-type allergic reactions by helminth infection. Nat. Rev. Immunol. 7: 220-230.
25. Sewell, D., Z. Qing, E. Reinke, D. Elliot, J. Weinstock, M. Sandor, and Z. Fabry. 2003. Immunomodulation of experimental autoimmune encephalomyelitis by helminth ova immunization. Int. Immunol. 15: 59-69.
26. La Flamme, A. C., K. Ruddenklau, and B. T. Bäckström. 2003. Schistosomiasis decreases central nervous system inflammation and alters the progression of experimental autoimmune encephalomyelitis. Infect. Immun. 71: 4996-5004.
27. Alvarez, J. I. 2005. Inhibition of Toll like receptor immune responses by microbial pathogens. Front. Biosci. 10: 582-587.
28. Hartgers, F. C., B. B. Obeng, A. Voskamp, I. A. Larbi, A. S. Amoah, A. J. F. Luty, D. Boakye, and M. Yazdanbakhsh. 2008. Enhanced Toll-like receptor responsiveness associated with mitogen-activated protein kinase activation in Plasmodium falciparum-infected children. Infect. Immun. 76: 5149-5157.
29. Maldonado, C., W. Trejo, A. Ramirez, M. Carrera, J. Sánchez, C. Lopez-Macias, and A. Isibasi. 2000. Lipophosphopeptidoglycan of induces an antiinflammatory innate immune response and downregulation of Entamoeba histolytica Toll-like receptor 2 (TLR-2) gene expression in human monocytes. Arch. Med. Res. 31: S71-S-73.
30. Babu, S., C. P. Blauvelt, V. Kumaraswami, and T. B. Nutman. 2005. Diminished expression and function of TLR in lymphatic filariasis: a novel mechanism of immune dysregulation. J. Immunol. 175: 1170-1176.
31. Lotz, M., D. Gütle, S. Walther, S. Menard, C. Bogdan, and M. W. Hornef. 2006. Postnatal acquisition of endotoxin tolerance in intestinal epithelial cells. J. Exp. Med. 203: 973-984.
32. Cook, D. N., D. S. Pisetsky, and D. A. Schwartz. 2004. Toll-like receptors in the pathogenesis of human disease. Nat. Immunol. 5: 975-979.
33. Lorenz, E., J. P. Mira, K. L. Cornish, N. C. Arbour, and D. A. Schwartz. 2000. A novel polymorphism in the Toll-like receptor 2 gene and its potential association with staphylococcal infection. Infect. Immun. 68: 6398-6401.
34. Arcaroli, J., E. Silva, J. P. Maloney, Q. He, D. Svetkauskaite, J. R. Murphy, and E. Abraham. 2006. Variant IRAK-1 haplotype is associated with increased nuclear factor-κB activation and worse outcomes in sepsis. Am. J. Resp. Crit. Care Med. 173: 1335-1341.
35. Zhang, X., J. P. Edwards, and D. M. Mosser. 2006. Dynamic and transient remodelling of the macrophage IL-10 promoter during transcription. J. Immunol. 177: 1282-1288. (Pubitemid 44036634)
36. Takeuchi, O., K. Hoshino, K. Kawai, T. Sanjo, H. Takada, T. Ogawa, K. Takeda, and S. Akira. 1999. Differential roles of TLR2 and TLR4 in recognition of Gram-negative and gram-positive bacterial cell wall components. Immunity 11: 443-451.
37. van der Kleij, D., E. Latz, J. F. H. M. Brouwers, Y. C. M. Kruize, M. Schmitz, E. A. Kurt-Jones, T. Espevik, E. C de Jong, M. L. Kapsenberg, D. T. Golenbock, et al. 2002. A novel host-parasite lipid cross-talk. J. Biol. Chem. 277: 48122-48129.
38. Layland, L. E., R. Rad, H. Wagner, and C. U. da Costa. 2007. Immunopathology in schistosomiasis is controlled by antigen-specific regulatory T cells primed in the presence of TLR2. Eur. J. Immunol. 37: 2174-2184.
39. Aksoy, E., C. S. Zouain, F. Vanhoutte, J. Fontaine, N. Pavelka, N. Thiebelemont, F. Willems, P. Ricciardi-Castiglioni, M. Goldman, M. Capron, et al. 2005. Double-stranded RNAs from the helminth parasite schistosoma activate TLR3 in dendritic cells. J. Biol. Chem. 280: 277-283.
40. Becker, I., N. Salaiza, M. Aguirre, J. Delgado, N. Carrillo-Carrasco, L. G. Kobe, A. Ruiz, R. Cervantes, A. P. Torres, N. Cabrera, et al. 2003. Leishmania lipophosphoglycan (LPG) activates NK cells through Toll-like recpetor-2. Mol. Biochem. Parasitol. 130: 65-74.
41. Kane, C. M., E. Jung, and E. J. Pearce. 2008. Schistosoma mansoni egg antigen-mediated modulation of Toll-like receptor (TLR)-induced activation occurs independently of TLR2. TLR4, and MyD88. Infect. Immun. 76: 5754-5759.
42. Hokke, C. H., and A. M. Deelder. 2001. Schistosome glycoconjugates in host-parasite interplay. Glyconconj. J. 18: 573-587.
43. Thomas, P. G., M. R. Carter, O. Atochina, A. A. Da'Dara, D. Piskorska, E. McGuire, and D. A. Harn. 2003. Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-dependent mechanism. J. Immunol. 171: 5837-5841.
44. Kawai, T., and S. Akira. 2005. Pathogen recognition with Toll-like receptors. Curr. Opin. Immunol. 17: 338-344.
45. Kreider, T., R. M. Anthony, J. F. Urban, and W. C. Gause. 2007. Alternatively activated macrophages in helminth infections. Curr. Opin. Immunol. 19: 448-453.
46. Carvalho, L., J. Sun, C. Kane, F. Marshall, C. Krawczyk, and E. J. Pearce. 2009. Review series on helminthes, immune modulation and the hygiene hypothesis: mechanisms underlying helminth modulation of dendritic cell function. Immunology 126: 28-34.
47. Agrawal, S., A. Agrawal, B. Doughty, A. Gerwitz, J. Belnis, T. Van Dyke, and B. Pulendran. 2003. 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: 4984-4989.
48. Mizoguchi, A., E. Mizoguchi, H. Takedatsu, R. S. Blumberg, and A. K. Bhan. 2002. Chronic intestinal inflammatory condition generates IL-10 producing regulatory B cell subset characterized by CD1d upregulation. Immunity 16: 219-230.
49. Fillatreau, S., C. H. Sweenie, M. J. McGeachy, D. Gray, and S. M. Anderton. 2002. B cells regulate autoimmunity by provision of IL-10. Nat. Immunol. 3: 944-950.
50. Mauri, C., D. Gray, N. Mushtaq, and M. Londei. 2003. Prevention of arthritis by interleukin 10-producing B cells. J. Exp. Med. 197: 489-501.
51. Lampropoulou, V., K. Hoehlig, T. Roch, P. Neves, E. Calderón Gómez, C. H. Sweenie, Y. Hao, A. A. Freitas, U. Steinhoff, S. M. Anderton, and S. Fillatreau. 2008. TLR-activated B cells suppress T-cell mediated autoimmunity. J. Immunol. 180: 4763-4773.
52. Prinz, M., F. Garbe, H. Schmidt, A. Mildner, I. Gutcher, K. Wolter, M. Piesche, R. Schroers, E. Weiss, C. J. Kirschning, et al. 2006. Innate immunity mediated by TLR9 modulates pathogenicity in an animal model of multiple sclerosis. J. Clin. Invest. 116: 456-464.
53. Mangan, N. E., R. E. Fallon, P. Smith, N. van Rooijen, A. N. McKenzie, and P. G. Fallon. 2004. Helminth infection protects mice from anaphylaxis via IL-10 producing B cells. J. Immunol. 173: 6346-6356.
54. Yi, A. K., J. G. Yoon, S. Y. Yeo, S. C. Hong, B. K. English, and A. M. Krieg. 2002. Role of mitogen-activated protein kinases in CpG DNA-mediated IL-10 and IL-12 production: central role of extracellular signal-regulated kinase in the negative feed-back loop of the CpG DNA-mediated Th1 response. J. Immunol. 168: 4711-4720.
55. Marthur, R. K., A. Awasthi, P. Wadhone, B. Ramanamurthy, and B. Saha. 2004. Reciprocal CD40 signals through p38MAPK and ERK-1/2 induce counteracting immune responses. Nat. Med. 10: 540-544.
56. Rincón, M., H. Enslen, J. Raingeaud, M. Recht, T. Zapton, M. S. Su, L. A. Penix, R. J. Davis, and R. A. Flavell. 1998. Interferon-γ expression by Th1 effector T cells mediated by the p38MAP kinase signalling pathway. EMBO. J. 17: 2817-2829.
57. Kamda, J. D., and S. M. Singer. 2009. Phosphoinositide 3-kinase-dependent inhibition of dendritic cell interleukin-12 production by Giardia lamblia. Infect. Immun. 77: 685-693.
58. Kaisho, T., O. Takeuchi, T. Kawai, K. Hoshino, and S. Akira. 2001. Endotoxin-induced maturation of MyD88-deficient dendritic cells. J. Immunol. 166: 5688-5694. (Pubitemid 32374193)
59. Rescigno, M., M. Martino, C. L. Sutherland, M. R. Gold, and P. Ricciardi-Castagnoli. 1998. Dendritic cell survival and maturation are regulated by different signalling pathways. J. Exp. Med. 188: 2175-2180.
60. Yazdanbakhsh, M., A. van den Biggelaar, and R. M. Maizels. 2001. Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol. 22: 372-377.