Helminth-conditioned dendritic cells prime CD4+T cells to IL-4 production in vivo

Journal of Immunology

Volumn 193, Issue 6, 2014, Pages 2709-2717

  Connor, Lisa M ^a   Tang, Shiau Choot ^a   Camberis, Mali ^a   Gros, Graham Le ^a   Ronchese, Franca ^a  

^a MALAGHAN INSTITUTE OF MEDICAL RESEARCH   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON REGULATORY FACTOR 4; INTERLEUKIN 4; OX40 LIGAND; PROGRAMMED DEATH 1 LIGAND 2; THYMIC STROMAL LYMPHOPOIETIN; CYTOKINE; GLYCOPROTEIN P 15095; GREEN FLUORESCENT PROTEIN; HLA ANTIGEN CLASS 2; INTERFERON REGULATORY FACTOR; INTERFERON REGULATORY FACTOR-4; INTERLEUKIN DERIVATIVE; INTERLEUKIN-33, MOUSE; LECTIN; LY ANTIGEN; LY-6C ANTIGEN, MOUSE; MEMBRANE PROTEIN; MGL2 PROTEIN, MOUSE; PDCD1LG2 PROTEIN, MOUSE; TNFSF4 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL EXPANSION; CELL INTERACTION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DENDRITIC CELL; IN VIVO STUDY; MOUSE; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; TH2 CELL; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LARVA; LYMPH NODE; LYMPHOCYTE ACTIVATION; NIPPOSTRONGYLUS;

ANIMALS; ANTIGENS, CD11C; ANTIGENS, LY; CELL DIFFERENTIATION; CYTOKINES; DENDRITIC CELLS; GREEN FLUORESCENT PROTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS II; INTERFERON REGULATORY FACTORS; INTERLEUKIN-4; INTERLEUKINS; LARVA; LECTINS, C-TYPE; LYMPH NODES; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NIPPOSTRONGYLUS; PROGRAMMED CELL DEATH 1 LIGAND 2 PROTEIN; TH2 CELLS; TUMOR NECROSIS FACTORS;

EID: 84907069894     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400374     Document Type: Article

References (55)

1. Paul, W. E., and J. Zhu. 2010. How are T(H)2-type immune responses initiated and amplified? Nat. Rev. Immunol. 10: 225-235
2. Pulendran, B., and D. Artis. 2012. New paradigms in t ype 2 immunity. Science 337: 431-435
3. MacDonald, A. S., A. D. Straw, B. Bauman, and E. J. Pearce. 2001. CD8-dendritic cell activation status plays an integral role in influencing Th2 response development. J. Immunol. 167: 1982-1988
4. Ohnmacht, C., C. Schwartz, M. Panzer, I. Schiedewitz, R. Naumann, and D. Voehringer. 2010. Basophils orchestrate chronic allergic dermatitis and protect ive immunity against helminths. Immunity 33: 364-374
5. Perrigoue, J. G., S. A. Saenz, M. C. Siracusa, E. J. Allenspach, B. C. Taylor, P. R. Giacomin, M. G. Nair, Y. Du, C. Zaph, N. van Rooijen, et al. 2009. MHC class II-dependent basophil-CD4+ T cell interactions promote T(H)2 cytokinedependent immunity. Nat. Immunol. 10: 697-705
6. Sokol, C. L., N.-Q. Chu, S. Yu, S. A. Nish, T. M. Laufer, and R. Medzhitov. 2009. Basophils function as antigen-presenting cells for an allergen-induced T helper type 2 response. Nat. Immunol. 10: 713-720
7. Tang, H., W. Cao, S. P. Kasturi, R. Ravindran, H. I. Nakaya, K. Kundu, N. Murthy, T. B. Kepler, B. Malissen, and B. Pulendran. 2010. The T helper type 2 response to cysteine proteases requires dendritic cell-basophil cooperation via ROS-mediated signaling. Nat. Immunol. 11: 608-617
8. Yoshimoto, T., K. Yasuda, H. Tanaka, M. Nakahira, Y. Imai, Y. Fujimori, and K. Nakanishi. 2009. Basophils contribute to T(H)2-IgE responses in vivo via IL-4 production and presentation of peptide-MHC clas s II complexes to CD4+ T cells. Nat. Immunol. 10: 706-712
9. Phythian-Adams, A. T., P. C. Cook, R. J. Lundie, L. H. Jones, K. A. Smith, T. A. Barr, K. Hochweller, S. M. Anderton, G. J. Hämmerling, R. M. Maizels, and A. S. MacDonald. 2010. CD11c depletion severely disrupts Th2 induction and development in vivo. J. Exp. Med. 207: 2089-2096
10. Smith, K. A., Y. Harcus, N. Garbi, G. J. Hämmerling, A. S. MacDonald, and R. M. Maizels. 2012. Type 2 innate immunity in helminth infection is induced redundantly and acts autonomously following CD11c(+) cell depletion. Infect. Immun. 80: 3481-3489
11. Smith, K. A., K. Hochweller, G. J. Hämmerling, L. Boon, A. S. MacDonald, and R. M. Maizels. 2011. Chronic helminth infection promotes immune regulation in vivo through dominance of CD11cloCD103-dendritic ce lls. J. Immunol. 186: 7098-7109
12. Hammad, H., M. Plantinga, K. Deswarte, P. Pouliot, M. A. M. Willart, M. Kool, F. Muskens, and B. N. Lambrecht. 2010. Inflammatory dendritic cells-not basophils-are necessary and sufficient for induction of Th2 immunity to inhaled house dust mite allergen. J. Exp. Med. 207: 2097-2111
13. Chu, D. K., A. Llop-Guevara, T. D. Walker, K. Flader, S. Goncharova, J. E. Boudreau, C. L. Moore, T. Seunghyun In, S. Waserman, A. J. Coyle, R. Kolbeck, A. A. Humbles, and M. Jordana. 2013. IL-33, but not thym ic stromal lymphopoietin or IL-25, is central to mite and peanut allergic sensitization. J. Allergy Clin. Immunol. 131: 187-200.e181-188
14. Ito, T., Y. H. Wang, O. Duramad, T. Hori, G. J. Delespesse, N. Watanabe, F. X. Qin, Z. Yao, W. Cao, and Y. J. Liu. 2005. TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J. Exp. Med. 202: 1213-1223
15. W ang, Y. H., and Y. J. Liu. 2009. Thymic stromal lymphopoietin, OX40-ligand, and interleukin-25 in allergic responses. Clin. Exp. Allergy 39: 798-806
16. Hoshino, A., Y. Tanaka, H. Akiba, Y. Asakura, Y. Mita, T. Sakurai, A. Takaoka, S. Nakaike, N. Ishii, K. Sugamura, et al. 2003. Critical role for OX40 ligand in the development of pathogenic Th2 cells in a murine model of asthma. Eur. J. Immunol. 33: 861-869
17. Seshasayee, D., W. P. Lee, M. Zhou, J. Shu, E. Suto, J. Zhang, L. Diehl, C. D. Austin, Y. G. Meng, M. Tan, et al. 2007. In vivo blockade of OX40 ligand inhibits thym ic stromal lymphopoietin driven atopic inflammation. J. Clin. Invest. 117: 3868-3878
18. Ekkens, M. J., Z. Liu, Q. Liu, J. Whitmire, S. Xiao, A. Foster, J. Pesce, J. VanNoy, A. H. Sharpe, J. F. Urban, and W. C. Gause. 2003. The role of OX40 ligand interactions in the development of the Th2 response to the gastrointestinal nematode parasite Heligmosomoides polygyrus. J. Immunol. 170: 384-393
19. Pippig, S. D., C. Pen?a-Rossi, J. Long, W. R. Godfrey, D. J. Fowell, S. L. Reiner, M. L. Birkeland, R. M. Locksley, A. N. Barclay, and N. Killeen. 1999. Robust B cell immunity but impaired T cell prolifer ation in the absence of CD134 (OX40). J. Immunol. 163: 6520-6529.
20. Croft M, 2010. Control of immunity by the TNFR-related molecule OX40 (CD134). Annu. Rev. Immunol, 28, 57-78.
21. Jenkins, S. J., G. Perona-Wright, A. G. F. Worsley, N. Ishii, and A. S. MacDonald. 2007. Dendritic cell expression of OX40 ligand acts as a costimulatory, not polarizing, signal for optimal Th2 priming and memory induction in vivo. J. Immunol. 179: 3515-3523
22. León, B., A. Ballesteros-Tato, J. L. Browning, R. Dunn, T. D. Randall, and F. E. Lund. 2012. Regulation of T(H)2 development by CXCR5+ dendritic cells and lymphotoxin-expressing B cells. Nat. Immunol. 13: 681-690
23. Halim, T. Y., C. A. Steer, L. Mathä, M. J. Gold, I. Martinez-Gonzalez, K. M. McNagny, A. N. McKenzie, and F. Takei. 20 14. Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity 40: 425-435
24. Kumamoto, Y., M. Linehan, J. S. Weinstein, B. J. Laidlaw, J. E. Craft, and A. Iwasaki. 2013. CD301b? dermal dendritic cells drive T helper 2 cell-mediated immunity. Immunity 39: 733-743
25. Gao, Y., S. A. Nish, R. Jiang, L. Hou, P. Licona-Limón, J. S. Weinstein, H. Zhao, and R. Medzhitov. 2013. Control of T helper 2 responses by transcription factor IRF4-dependent dendritic cells. Immunity 39: 722-732
26. Murakami, R., K. Denda-Nagai, S. Hashimoto, S. Nagai, M. Hattori, and T. Irimura. 2013. A unique dermal dendritic cell subset that skews the immune response toward Th2. PLoS ONE 8: e73270
27. Mesnil, C., C. M. Sabatel, T. Marichal, M. Toussaint, D. Cataldo, P. V. Drion, P. Lekeux, F. Bureau, and C. J. Desmet. 2012. Resident CD11b(+)Ly6C(-) lung dendritic cells are responsible for allergic airway sensitization to house dust mite in mice. PLoS ONE 7: e53242
28. Plantinga, M., M. Guilliams, M. Vanheerswynghels, K. Deswarte, F. Branco-Madeira, W. Toussaint, L. Vanhoutte, K. Neyt, N. Killeen, B. Malissen, et al. 2013. Conventional and monocyte-derived CD11b(+) dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity 38: 322-335
29. van Panhuys, N., S. C. Tang, M. Prout, M. Camberis, D. Scarlett, J. Roberts, J. Hu-Li, W. E. Paul, and G. Le Gros. 2008. In vivo studies fail to reveal a role for IL-4 or STAT6 signaling in Th2 lymphocyte differentiation. Proc. Natl. Acad. Sc i. USA 105: 12423-12428
30. Camberis, M., M. Prout, S. C. Tang, E. Forbes-Blom, M. Robinson, R. Kyle, Y. Belkaid, W. Paul, and G. Le Gros. 2013. Evaluating the in vivo Th2 priming potential am ong common allergens. J. Immunol. Methods 394: 62-72
31. Hu-Li, J., C. Pannetier, L. Guo, M. Löhning, H. Gu, C. Watson, M. Assenmacher, A. Radbruch, and W. E. Paul. 2001. Regulation of expression of IL-4 alleles: analysis using a chimeric GFP/IL-4 gene. Immunity 14: 1-11
32. Al-Shami, A., R. Spolski, J. Kelly, T. Fry, P. L. Schwartzberg, A. Pandey, C. L. Mackall, and W. J. Leonard. 2004. A role for thymic stromal lymphopoietin in CD4(+) T cell development. J. Exp. Med. 200: 159-168
33. Ma, J. Z., S. N. Lim, J. S. Qin, J. Yang, N. Enomoto, C. Ruedl, and F. Ronchese. 2012. Murine CD4+ T cell responses are inhibited by cytotoxic T cell-mediated killing of dendritic cells and are restored by antigen transfer. PLoS ONE 7: e37481
34. Besnard, A. G., D. Togbe, N. Guillou, F. Erard, V. Quesniaux, and B. Ryffel. 2011. IL-33-activated dendritic cells are critical for allergic airway inflammation. Eur. J. Immunol. 41: 1675-1686
35. Balic, A., Y. Harcus, M. J. Holland, and R. M. Maizels. 2004. Selective maturation of dendritic cells by Nippostrongylus brasiliensis-secreted proteins drives Th2 immune responses. Eur. J. Immunol. 34: 3047-3059
36. Lambrecht, B. N., M. De Veerman, A. J. Coyle, J. C. Gutierrez-Ramos, K. Thielemans, and R. A. Pauwels. 2000. Myeloid dendritic cells induce Th2 responses to inhaled antigen, leading to eosinoph ilic airway inflammation. J. Clin. Invest. 106: 551-559
37. MacDonald, A. S., A. D. Straw, N. M. Dalton, and E. J. Pearce. 2002. Cutting edge: Th2 response induction by dendritic cells: a role for CD40. J. Immunol. 168: 537-540
38. Whelan, M., M. M. Harnett, K. M. Houston, V. Patel, W. Harnett, and K. P. Rigley. 2000. A filarial nematode-secreted product signals dendritic cells to acquir e a phenotype that drives development of Th2 cells. J. Immunol. 164: 6453-6460
39. Constant, S. L., and K. Bottomly. 1997. Induction of Th1 and Th2 CD4+ T cell responses: the alternative approaches. Annu. Rev. Immunol. 15: 297-322
40. Massacand, J. C., R. C. Stettler, R. Meier, N. E. Humphreys, R. K. Grencis, B. J. Marsland, and N. L. Harris. 2009. Helminth products bypass the need for TSLP in Th2 immune responses by directly modulating dendritic cell function. Proc. Natl. Acad. Sci. USA 106: 13968-13973
41. Mearns, H., E. E. F orbes-Blom, M. Camberis, S.-C. Tang, R. Kyle, M. Harvie, M. A. Kleinschek, and G. Le Gros. 2014. IL-25 exhibits disparate roles during Th2-cell differentiation versus effector function. Eur. J. Immunol. 44: 1976 -1980.
42. Moussion C.,N. Ortega,J.P. Girard, 2008, The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: a novel ?alarmin', PLoS ONE, 3, e3331
43. Hung, L. Y., I. P. Lewkowich, L. A. Dawson, J. Downey, Y. Yang, D. E. Smith, and D. R. Herbert. 2013. IL-33 drives biphasic IL-13 production for noncanonical Type 2 immunity against hookworm s. Proc. Natl. Acad. Sci. USA 110: 282-287
44. Harris, N. L., R. J. Peach, and F. Ronchese. 1999. CTLA4-Ig inhibits optimal T helper 2 cell development but not protective immunity or memory response to Nippostrongylus brasiliensis. Eur. J. Immunol. 29: 311-316
45. Harris, N. L., and F. Ronchese. 1999. The role of B7 costimulation in T-cell immunity. Immunol. Cell Biol. 77: 304-311
46. Berney, C., S. Herren, C. A. Power, S. Gordon, L. Martinez-Pomares, and M. H. Kosco-Vilbois. 1999. A member of the dendritic cell family that enters B cell follicles and stimulates primary antibody responses ident ified by a mannose receptor fusion protein. J. Exp. Med. 190: 851-860
47. Saeki, H., M. T. Wu, E. Olasz, and S. T. Hwang. 2000. A migratory population of skin-derived dendritic cells expresses CXCR5, responds to B lymphocyte chemoattractant in vitro, and co-localizes to B cell zones in lymph nodes in vivo. Eur. J. Immunol. 30: 2808-2814
48. Ronchese, F., B. Hausmann, and G. Le Gros. 1994. Interferon -gamma-and interleukin-4-producing T cells can be primed on dendritic cells in vivo and do not require the presence of B cells. Eur. J. Immunol. 24: 1148-1154
49. Bajan? a, S., K. Roach, S. Turner, J. Paul, and S. Kovats. 2012. IRF4 promotes cutaneous dendritic cell migration to lymph nodes during homeostasis and inflammation. J. Immunol. 189: 3368-3377
50. Vander Lugt, B., A. A. Khan, J. A. Hackney, S. A grawal, J. Lesch, M. Zhou, W. P. Lee, S. Park, M. Xu, J. Devoss, et al. 2014. Transcriptional programming of dendritic cells for enhanced MHC class II antigen presentation. Nat. Immunol. 15: 161-167
51. Williams, J. W., M. Y. Tjota, B. S. Clay, B. Vander Lugt, H. S. Bandukwala, C. L. Hrusch, D. C. Decker, K. M. Blaine, B. R. Fixsen, H. Singh, et al. 2013. Transcription factor IRF4 drives dendrit ic cells to promote Th2 differentiation. Nat. Commun. 4: 2990
52. Roediger, B., R. Kyle, K. H. Yip, N. Sumaria, T. V. Guy, B. S. Kim, A. J. Mitchell, S. S. Tay, R. Jain, E. Forbes-Blom, et al. 2013. Cutaneous immunosurveillance and regulation of inflammation by group 2 innate lymphoid cells. Nat. Immunol. 14: 564-573
53. Randolph, G. J., K. Inaba, D. F. Robbiani, R. M. Steinman, and W. A. Muller. 1999. Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity 11: 753-761
54. Tamoutounour, S., M. Guilliams, F. Montanana Sanchis, H. Liu, D. Terhorst, C. Malosse, E. Pollet, L. Ardouin, H. Luche, C. Sanchez, et al. 2013. Origins and functional specialization of macrophages and of conventional and monocytederived dendritic cells in mouse skin. Immunity 39: 925-938
55. Ingulli, E., D. R. Ulman, M. M. Lucido, and M. K. Jenkins. 2002. In situ analysis reve als physical interactions between CD11b+ dendritic cells and antigenspecific CD4 T cells after subcutaneous injection of antigen. J. Immunol. 169: 2247-2252