Tlrs, Treg, and B cells, an interplay of regulation during helminth infection

Frontiers in Immunology

Volumn 3, Issue FEB, 2012, Pages

  Ludwig Portugall, Isis ^a   Layland, Laura E ^a,b,c  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY HOSPITAL BONN   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

B cells; Helminth; Immune regulation; Regulatoryt cells; TLR

Indexed keywords

EID: 84873733702     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00008     Document Type: Short Survey

References (82)

1. Adjobimey, T., and Hoerauf, A. (2010). Induction of immunoglobulin G4 in human filariasis: an indicator of immunoregulation. Ann. Trop. Med. Parasitol. 104, 455-464.
2. Aksoy, E., Zouain, C. S., Vanhoutte, F., Fontaine, J., Pavelka, N., Thieblemont, N., Willems, F., Ricciardi-Castagnoli, P., Goldman, M., Capron, M., Ryffel, B, and Trottein, F. (2005). Double-stranded RNAs from the helminth parasite Schistosoma activate TLR3 in dendritic cells. J. Biol. Chem. 280, 277-283.
3. Allen, J. E., and Maizels, R. M. (2011). Diversity and dialogue in immunity to helminths. Nat. Rev. Immunol. 11, 375-388.
4. Amu, S., Saunders, S. P., Kronenberg, M., Mangan, N. E., Atzberger, A., and Fallon, P. G. (2010). Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J. Allergy Clin. Immunol. 125, 1114-1124.e8.
5. Anthony, R. M., Rutitzky, L. I., Urban, J. F. Jr., Stadecker, M. J., and Gause, W. C. (2007). Protective immune mechanisms in helminth infection. Nat. Rev. Immunol. 7, 975-987.
6. Asahi, H., and Stadecker, M. J. (2003). Analysis of egg antigens inducing hepatic lesions in schistosome infection. Parasitol. Int. 52, 361-367.
7. Blackwell,N. M.,and Else,K. J. (2001). B cells and antibodies are required for resistance to the parasitic gastrointestinal nematode Trichuris muris. Infect. Immun. 69, 3860-3868.
8. Blankenhaus, B., Klemm, U., Eschbach, M. L., Sparwasser, T., Huehn, J., Kuhl, A. A., Loddenkemper, C., Jacobs, T., and Breloer, M. (2011). Strongyloides ratti infection induces expansion of Foxp3+ regulatory T cells that interfere with immune response and parasite clearance in BALB/c mice. J. Immunol. 186, 4295-4305.
9. Brattig, N. W., Bazzocchi, C., Kirschning, C. J., Reiling, N., Buttner, D. W., Ceciliani, F., Geisinger, F., Hochrein, H., Ernst, M., Wagner, H., Bandi, C., and Hoerauf, A. (2004). The major surface protein of Wolbachia endosymbionts in filarial nematodes elicits immune responses through TLR2 and TLR4. J. Immunol. 173, 437-445.
10. Conroy, H., Marshall, N. A., and Mills, K. H. (2008). TLR ligand suppression or enhancement of Treg cells? A double-edged sword in immunity to tumours. Oncogene 27, 168-180.
11. Correale, J., and Farez, M. (2009). Helminth antigens modulate immune responses in cells from multiple sclerosis patients through TLR2-dependent mechanisms. J. Immunol. 183, 5999-6012.
12. Correale, J., Farez, M., and Razzitte, G. (2008). Helminth infections associated with multiple sclerosis induce regulatory B cells. Ann. Neurol. 64, 187-199.
13. D'Elia, R., Behnke, J. M., Bradley, J. E., and Else, K. J. (2009). Regulatory T cells: a role in the control of helminth-driven intestinal pathology and worm survival. J. Immunol. 182, 2340-2348.
14. Doetze, A., Satoguina, J., Burchard, G., Rau, T., Loliger, C., Fleischer, B., and Hoerauf, A. (2000). Antigenspecific cellular hyporesponsiveness in a chronic human helminth infection is mediated by T(h)3/T(r)1type cytokines IL-10 and transforming growth factor-beta but not by a T(h)1 to T(h)2 shift. Int. Immunol. 12, 623-630.
15. Everts, B., Smits, H. H., Hokke, C. H., and Yazdanbakhsh, M. (2010). Helminths and dendritic cells: sensing and regulating via pattern recognition receptors, Th2 and Treg responses. Eur. J. Immunol. 40, 1525-1537.
16. Fillatreau, S., Gray, D., and Anderton, S. M. (2008). Not always the bad guys: B cells as regulators of autoimmune pathology. Nat. Rev. Immunol. 8, 391-397.
17. Gillan, V., and Devaney, E. (2005). Regulatory T cells modulate Th2 responses induced by Brugia pahangi third-stage larvae. Infect. Immun. 73, 4034-4042.
18. Goodridge, H. S., Marshall, F. A., Else, K. J., Houston, K. M., Egan, C., Al-Riyami, L., Liew, F. Y., Harnett, W., and Harnett, M. M. (2005). Immunomodulation via novel use of TLR4 by the filarial nematode phosphorylcholinecontaining secreted product, ES-62. J. Immunol. 174, 284-293.
19. Goodridge, H. S., McGuiness, S., Houston, K. M., Egan, C. A., Al-Riyami, L., Alcocer, M. J., Harnett, M. M., and Harnett, W. (2007). Phosphorylcholine mimics the effects of ES-62 on macrophages and dendritic cells. Parasite Immunol. 29, 127-137.
20. Grainger, J. R., Smith, K. A., Hewitson, J. P., McSorley, H. J., Harcus, Y., Filbey, K. J., Finney, C. A., Greenwood, E. J., Knox,D. P.,Wilson, M. S., Belkaid, Y., Rudensky, A. Y., and Maizels, R. M. (2010). Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-beta pathway. J. Exp. Med. 207, 2331-2341.
21. Haczku, A., Takeda, K., Hamelmann, E., Loader, J., Joetham, A., Redai, I., Irvin, C. G., Lee, J. J., Kikutani, H., Conrad, D., and Gelfand, E. W. (2000). CD23 exhibits negative regulatory effects on allergic sensitization and airway hyperresponsiveness. Am. J. Respir. Crit. Care Med. 161, 952-960.
22. Hall, J. A., Bouladoux, N., Sun, C. M., Wohlfert, E. A., Blank, R. B., Zhu, Q., Grigg, M. E., Berzofsky, J. A., and Belkaid,Y. (2008). Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses. Immunity 29, 637-649.
23. Harris, N., and Gause, W. C. (2010). To B or not to B: B cells and the Th2type immune response to helminths. Trends Immunol. 32, 80-88.
24. Hernandez, H. J., Wang, Y., and Stadecker, M. J. (1997). In infection with Schistosoma mansoni,B cells are required for T helper type 2 cell responses but not for granuloma formation. J. Immunol. 158, 4832-4837.
25. Hesse, M., Piccirillo, C. A., Belkaid, Y., Prufer, J., Mentink-Kane, M., Leusink, M., Cheever, A. W., Shevach, E. M., and Wynn, T. A. (2004). The pathogenesis of schistosomiasis is controlled by cooperating IL-10producing innate effector and regulatory T cells. J. Immunol. 172, 3157-3166.
26. Hoffmann, K. F., Cheever, A. W., and Wynn, T. A. (2000). IL-10 and the dangers of immune polarization: excessive type 1 and type 2 cytokine responses induce distinct forms of lethal immunopathology in murine schistosomiasis. J. Immunol. 164, 6406-6416.
27. Hori, S. (2010). Developmental plasticity of Foxp3+ regulatory T cells. Curr. Opin. Immunol. 22, 575-582.
28. Hotez,P. J.,Brindley,P. J.,Bethony,J. M., King, C. H., Pearce, E. J., and Jacobson, J. (2008). Helminth infections: the great neglected tropical diseases. J. Clin. Invest. 118, 1311-1321.
29. Hussaarts, L., van der Vlugt, L. E., Yazdanbakhsh, M., and Smits, H. H. (2011). Regulatory B-cell induction by helminths: implications for allergic disease. J. Allergy Clin. Immunol. 128, 733-739.
30. Kamradt, T. (2005). Can infections prevent or cure allergy and autoimmunity? Discov. Med. 5, 283-287.
31. Kane, C. M., Cervi, L., Sun, J., McKee,A. S., Masek, K. S., Shapira, S., Hunter, C. A., and Pearce, E. J. (2004). Helminth antigens modulate TLRinitiated dendritic cell activation. J. Immunol. 173, 7454-7461.
32. Korten, S., Badusche, OM., Buttner, D. W., Hoerauf, A., Brattig, N., and Fleischer, B. (2008). Natural death of adult Onchocerca volvulus and filaricidal effects of doxycycline induce local FOXP3+/CD4+ regulatory T cells and granzyme expression. Microbes Infect. 10, 313-324.
33. Kubo, T., Hatton, R. D., Oliver, J., Liu, X., Elson, C. O., and Weaver, C. T. (2004). Regulatory T cell suppression and anergy are differentially regulated by proinflammatory cytokines produced by TLRactivated dendritic cells. J. Immunol. 173, 7249-7258.
34. Layland, L. E., Mages, J., Loddenkemper, C., Hoerauf, A., Wagner, H., Lang, R., and da Costa, C. U. (2010). Pronounced phenotype in activated regulatory T cells during a chronic helminth infection. J. Immunol. 184, 713-724.
35. Layland, L. E., Rad, R., Wagner, H., and da Costa, C. U. (2007). Immunopathology in schistosomiasis is controlled by antigen-specific regulatory T cells primed in the presence of TLR2. Eur. J. Immunol. 37, 2174-2184.
36. Linton, P. J., Bautista, B., Biederman, E., Bradley, E. S., Harbertson, J., Kondrack, R. M., Padrick, R. C., and Bradley, L. M. (2003). Costimulation via OX40L expressed by B cells is sufficient to determine the extent of primary CD4 cell expansion and Th2 cytokine secretion in vivo. J. Exp. Med. 197, 875-883.
37. Liu, Q., Kreider, T., Bowdridge, S., Liu, Z., Song,Y., Gaydo,A. G., Urban, J. F. Jr., and Gause, W. C. (2010). B cells have distinct roles in host protection against different nematode parasites. J. Immunol. 184, 5213-5223.
38. Lundy, S. K., and Boros, D. L. (2002). Fas ligand-expressing B-1a lymphocytes mediate CD4(+)-T-cell apoptosis during schistosomal infection: induction by interleukin 4 (IL4) and IL-10. Infect. Immun. 70, 812-819.
39. Mahanty, S., Mollis, S. N., Ravichandran, M., Abrams, J. S., Kumaraswami, V., Jayaraman, K., Ottesen, E. A., and Nutman, T. B. (1996). High levels of spontaneous and parasite antigen-driven interleukin-10 production are associated with antigen-specific hyporesponsiveness in human lymphatic filariasis. J. Infect. Dis. 173, 769-773.
40. Maizels, R. M., Balic, A., GomezEscobar, N., Nair, M., Taylor, M. D., and Allen, J. E. (2004). Helminth parasites - masters of regulation. Immunol. Rev. 201, 89-116.
41. Maizels, R. M., Pearce, E. J., Artis, D., Yazdanbakhsh, M., and Wynn, T. A. (2009). Regulation of pathogenesis and immunity in helminth infections. J. Exp. Med. 206, 2059-2066.
42. Maizels, R. M., and Yazdanbakhsh, M. (2003). Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat. Rev. Immunol. 3, 733-744.
43. Mangan, N. E., Fallon, R. E., Smith, P., van Rooijen, N., McKenzie, A. N., and Fallon, P. G. (2004). Helminth infection protects mice from anaphylaxis via IL-10-producing B cells. J. Immunol. 173, 6346-6356.
44. McSorley, H. J., Harcus, Y. M., Murray, J., Taylor, M. D., and Maizels, R. M. (2008). Expansion of Foxp3+ regulatory T cells in mice infected with the filarial parasite Brugia malayi. J. Immunol. 181, 6456-6466.
45. Medzhitov, R., and Janeway, C. A. Jr. (1997). Innate immunity: the virtues of a nonclonal system of recognition. Cell 91, 295-298.
46. Meyer, S., van Liempt, E., Imberty, A., van Kooyk, Y., Geyer, H., Geyer, R., and van Die, I. (2005). DC-SIGN mediates binding of dendritic cells to authentic pseudo-LewisY glycolipids of Schistosoma mansoni cercariae, the first parasite-specific ligand of DC-SIGN. J. Biol. Chem. 280, 37349-37359.
47. Mills, K. H. (2008). TLR9 turns the tide on Treg cells. Immunity 29, 518-520.
48. Mitre, E., Chien, D., and Nutman, T. B. (2008). CD4(+) (and not CD25+) T cells are the predominant interleukin-10-producing cells in the circulation of filariainfected patients. J. Infect. Dis. 197, 94-101.
49. Moreau, E., and Chauvin, A. (2010). Immunity against helminths: interactions with the host and the intercurrent infections. J. Biomed. Biotechnol. 2010, 428593.
50. Moulin, V., Andris, F., Thielemans, K., Maliszewski, C., Urbain, J., and Moser, M. (2000). B lymphocytes regulate dendritic cell (DC) function in vivo: increased interleukin 12 production by DCs from B celldeficient mice results in T helper cell type 1 deviation. J. Exp. Med. 192, 475-482.
51. Okano,M.,Satoskar,A. R.,Nishizaki,K., Abe, M., and Harn, D. A. Jr. (1999). Induction of Th2 responses and IgE is largely due to carbohydrates functioning as adjuvants on Schistosoma mansoni egg antigens. J. Immunol. 163, 6712-6717.
52. Okano, M., Satoskar, A. R., Nishizaki, K., and Harn, D. A. Jr. (2001). Lacto-N-fucopentaose III found on Schistosoma mansoni egg antigens functions as adjuvant for proteins by inducing Th2-type response. J. Immunol. 167, 442-450.
53. Onguru, D., Liang,Y., Griffith, Q., Nikolajczyk, B., Mwinzi, P., and GanleyLeal, L. (2011). Human schistosomiasis is associated with endotoxemia and Toll-like receptor 2and 4-bearing B cells. Am. J. Trop. Med. Hyg. 84, 321-324.
54. Onishi, Y., Fehervari, Z., Yamaguchi, T., and Sakaguchi, S. (2008). Foxp3+ natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc. Natl. Acad. Sci. U.S.A. 105, 10113-10118.
55. Othman, A. A., El-Shourbagy, S. H., and Soliman, R. H. (2011). Kinetics of Foxp3-expressing regulatory cells in experimental Toxocara canis infection. Exp. Parasitol. 127, 454-459.
56. Pasare, C., and Medzhitov, R. (2005). Control of B-cell responses by Tolllike receptors. Nature 438, 364-368.
57. Pennock, J. L., and Grencis, R. K. (2006). The mast cell and gut nematodes: damage and defence. Chem. Immunol. Allergy 90, 128-140.
58. Perona-Wright, G., Jenkins, S. J., Crawford, A., Gray, D., Pearce, E. J., and MacDonald, A. S. (2006). Distinct sources and targets of IL-10 during dendritic cell-driven Th1 and Th2 responses in vivo. Eur. J. Immunol. 36, 2367-2375.
59. Ritter, M., Gross, O., Kays, S., Ruland, J., Nimmerjahn, F., Saijo, S., Tschopp, J., Layland, L. E., and Prazeres da Costa, C. (2010). Schistosoma mansoni triggers Dectin-2, which activates the Nlrp3 inflammasome and alters adaptive immune responses. Proc. Natl. Acad. Sci. U.S.A. 107, 20459-20464.
60. Rudensky, A. Y. (2011). Regulatory T cells and Foxp3. Immunol. Rev. 241, 260-268.
61. Rutitzky, L. I., and Stadecker, M. J. (2011). Exacerbated egg-induced immunopathology in murine Schistosoma mansoni infection is primarily mediated by IL-17 and restrained by IFN-gamma. Eur. J. Immunol. 41, 2677-2687.
62. Rzepecka, J., Rausch, S., Klotz, C., Schnoller, C., Kornprobst, T., Hagen, J., Ignatius, R., Lucius, R., and Hartmann, S. (2009). Calreticulin from the intestinal nematode Heligmosomoides polygyrus is a Th2skewing protein and interacts with murine scavenger receptor-A. Mol. Immunol. 46, 1109-1119.
63. Satoguina, J., Mempel, M., Larbi, J., Badusche, M., Loliger, C., Adjei, O., Gachelin,G.,Fleischer,B.,and Hoerauf, A. (2002). Antigen-specific T regulatory-1 cells are associated with immunosuppression in a chronic helminth infection (onchocerciasis). Microbes Infect. 4, 1291-1300.
64. Satoguina, J. S., Adjobimey, T., Arndts, K., Hoch, J., Oldenburg, J., Layland, L. E., and Hoerauf, A. (2008). Tr1 and naturally occurring regulatory T cells induce IgG4 in B cells through GITR/GITR-L interaction, IL-10 and TGF-beta. Eur. J. Immunol. 38, 3101-3113.
65. Schabussova, I., Amer, H., van Die, I., Kosma, P., and Maizels, R. M. (2007). O-methylated glycans from Toxocara are specific targets for antibody binding in human and animal infections. Int. J. Parasitol. 37, 97-109.
66. Schenten, D., and Medzhitov, R. (2011). The control of adaptive immune responses by the innate immune system. Adv. Immunol. 109, 87-124.
67. Smits, H. H., Everts, B., Hartgers, F. C., and Yazdanbakhsh, M. (2010). Chronic helminth infections protect against allergic diseases by active regulatory processes. Curr. Allergy Asthma Rep. 10, 3-12.
68. Tawill, S., Le Goff, L., Ali, F., Blaxter, M., and Allen, J. E. (2004). Both free-living and parasitic nematodes induce a characteristic Th2 response that is dependent on the presence of intact glycans. Infect. Immun. 72, 398-407.
69. Taylor, M. D., Harris, A., Babayan, S. A., Bain, O., Culshaw, A., Allen, J. E., and Maizels, R. M. (2007). CTLA4 and CD4+ CD25+ regulatory T cells inhibit protective immunity to filarial parasites in vivo. J. Immunol. 179, 4626-4634.
70. Taylor, M. D., van der Werf, N., Harris, A., Graham, A. L., Bain, O., Allen, J. E., and Maizels, R. M. (2009). Early recruitment of natural CD4+ Foxp3+ Treg cells by infective larvae determines the outcome of filarial infection. Eur. J. Immunol. 39, 192-206.
71. Taylor, M. J., Hoerauf, A., and Bockarie, M. (2010). Lymphatic filariasis and onchocerciasis. Lancet 376, 1175-1185.
72. 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. (2002). A novel hostparasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. J. Biol. Chem. 277, 48122-48129.
73. van Die, I., van Vliet, S. J., Nyame, A. K., Cummings, R. D., Bank, C. M., Appelmelk, B., Geijtenbeek, T. B., and van Kooyk, Y. (2003). The dendritic cell-specific C-type lectin DC-SIGN is a receptor for Schistosoma mansoni egg antigens and recognizes the glycan antigen Lewis x. Glycobiology 13, 471-478.
74. van Liempt, E., van Vliet, S. J., Engering, A., Garcia Vallejo, J. J., Bank, C. M., Sanchez-Hernandez, M., van Kooyk, Y., and van Die, I. (2007). Schistosoma mansoni soluble egg antigens are internalized by human dendritic cells through multiple C-type lectins and suppress TLR-induced dendritic cell activation. Mol. Immunol. 44, 2605-2615.
75. van Riet, E., Everts, B., Retra, K., Phylipsen, M., van Hellemond, J. J., Tielens,A. G.,van der Kleij,D.,Hartgers, F. C., and Yazdanbakhsh, M. (2009). Combined TLR2 and TLR4 ligation in the context of bacterial or helminth extracts in human monocyte derived dendritic cells: molecular correlates for Th1/Th2 polarization. BMC Immunol. 10, 9. doi:10.1186/1471-2172-10-9
76. Venugopal, P. G., Nutman, T. B., and Semnani, R. T. (2009). Activation and regulation of toll-like receptors (TLRs) by helminth parasites. Immunol. Res. 43, 252-263.
77. Voehringer, D. (2009). The role of basophils in helminth infection. Trends Parasitol. 25, 551-556.
78. Voo, K. S., Wang, Y. H., Santori, F. R., Boggiano, C., Wang, Y. H., Arima, K., Bover, L., Hanabuchi, S., Khalili, J., Marinova, E., Zheng, B., Littman, D. R., and Liu, Y. J. (2009). Identification of IL-17producing FOXP3+ regulatory T cells in humans. Proc. Natl. Acad. Sci. U.S.A. 106, 4793-4798.
79. Whelan, M., Harnett, M. M., Houston, K. M., Patel, V., Harnett, W., and Rigley, K. P. (2000). A filarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J. Immunol. 164, 6453-6460.
80. Wilson, M. S., Mentink-Kane, M. M., Pesce, J. T., Ramalingam, T. R., Thompson, R., and Wynn, T. A. (2007). Immunopathology of schistosomiasis. Immunol. Cell Biol. 85, 148-154.
81. Wilson, M. S., Taylor, M. D., O'Gorman, M. T., Balic, A., Barr, T. A., Filbey, K., Anderton, S. M., and Maizels, R. M. (2010). Helminthinduced CD19+CD23hi B cells modulate experimental allergic and autoimmune inflammation. Eur. J. Immunol. 40, 1682-1696.
82. Yanaba, K., Bouaziz, J. D., Matsushita, T., Tsubata, T., and Tedder, T. F. (2009). The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J. Immunol. 182, 7459-7472.