Thymic stromal lymphopoietin-dependent basophils promote Th2 cytokine responses following intestinal helminth infection

Journal of Immunology

Volumn 189, Issue 9, 2012, Pages 4371-4378

  Giacomin, Paul R ^a,b   Siracusa, Mark C ^a   Walsh, Kevin P ^a,h   Grencis, Richard K ^c   Kubo, Masato ^d,e   Comeau, Michael R ^f   Artis, David ^a,g  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b JAMES COOK UNIVERSITY   (Australia)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d RIKEN YOKOHAMA INSTITUTE   (Japan)

^e TOKYO UNIVERSITY OF SCIENCE   (Japan)

^f AMGEN INC   (United States)

^g UNIVERSITY OF PENNSYLVANIA   (United States)

^h TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CYTOKINE RECEPTOR; INTERLEUKIN 3; INTERLEUKIN 3 RECEPTOR; THYMIC STROMAL LYMPHOPOIETIN; THYMIC STROMAL LYMPHOPOIETIN RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASOPHIL; CELL FUNCTION; CONTROLLED STUDY; CYTOKINE RESPONSE; DEPLETION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; TH2 CELL; TRICHINELLA SPIRALIS; TRICHINOSIS;

ANIMALS; BASOPHILS; CYTOKINES; INFLAMMATION; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; STROMAL CELLS; TH2 CELLS; THYMUS GLAND; TRICHINELLA SPIRALIS; TRICHINELLOSIS;

EID: 84867913372     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200691     Document Type: Article

References (51)

1. Anthony, R. M., L. I. Rutitzky, J. F. Urban, Jr., M. J. Stadecker, and W. C. Gause. 2007. Protective immune mechanisms in helminth infection. Nat. Rev. Immunol. 7: 975-987. (Pubitemid 350166058)
2. Artis, D., and R. K. Grencis. 2008. The intestinal epithelium: sensors to effectors in nematode infection. Mucosal Immunol. 1: 252-264. (Pubitemid 351850532)
3. Finkelman, F. D., T. Shea-Donohue, J. Goldhill, C. A. Sullivan, S. C. Morris, K. B. Madden, W. C. Gause, and J. F. Urban, Jr. 1997. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu. Rev. Immunol. 15: 505-533. (Pubitemid 27169291)
4. Maizels, R. M., E. J. Pearce, D. Artis, M. Yazdanbakhsh, and T. A. Wynn. 2009. Regulation of pathogenesis and immunity in helminth infections. J. Exp. Med. 206: 2059-2066.
5. Urban, J. F., Jr., K. B. Madden, A. Svetić, A. Cheever, P. P. Trotta, W. C. Gause, I. M. Katona, and F. D. Finkelman. 1992. The importance of Th2 cytokines in protective immunity to nematodes. Immunol. Rev. 127: 205-220.
6. Kim, H. Y., R. H. DeKruyff, and D. T. Umetsu. 2010. The many paths to asthma: phenotype shaped by innate and adaptive immunity. Nat. Immunol. 11: 577-584.
7. Maizels, R. M. 2005. Infections and allergy - helminths, hygiene and host immune regulation. Curr. Opin. Immunol. 17: 656-661. (Pubitemid 41506912)
8. Hammad, H., M. Plantinga, K. Deswarte, P. Pouliot, M. A. 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.
9. Kim, S., M. Prout, H. Ramshaw, A. F. Lopez, G. LeGros, and B. Min. 2010. Cutting edge: basophils are transiently recruited into the draining lymph nodes during helminth infection via IL-3, but infection-induced Th2 immunity can develop without basophil lymph node recruitment or IL-3. J. Immunol. 184: 1143-1147.
10. Ohnmacht, C., C. Schwartz, M. Panzer, I. Schiedewitz, R. Naumann, and D. Voehringer. 2010. Basophils orchestrate chronic allergic dermatitis and protective immunity against helminths. Immunity 33: 364-374.
11. 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 cytokine-dependent immunity. Nat. Immunol. 10: 697-705.
12. 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.
13. 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.
14. Sullivan, B. M., H. E. Liang, J. K. Bando, D. Wu, L. E. Cheng, J. K. McKerrow, C. D. Allen, and R. M. Locksley. 2011. Genetic analysis of basophil function in vivo. Nat. Immunol. 12: 527-535.
15. 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.
16. Torrero, M. N., M. P. Hübner, D. Larson, H. Karasuyama, and E. Mitre. 2010. Basophils amplify type 2 immune responses, but do not serve a protective role, during chronic infection of mice with the filarial nematode Litomosoides sigmodontis. J. Immunol. 185: 7426-7434.
17. 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 class II complexes to CD4+ T cells. Nat. Immunol. 10: 706-712.
18. Lantz, C. S., J. Boesiger, C. H. Song, N. Mach, T. Kobayashi, R. C. Mulligan, Y. Nawa, G. Dranoff, and S. J. Galli. 1998. Role for interleukin-3 in mast-cell and basophil development and in immunity to parasites. Nature 392: 90-93. (Pubitemid 28150595)
19. Lantz, C. S., B. Min, M. Tsai, D. Chatterjea, G. Dranoff, and S. J. Galli. 2008. IL-3 is required for increases in blood basophils in nematode infection in mice and can enhance IgE-dependent IL-4 production by basophils in vitro. Lab. Invest. 88: 1134-1142.
20. Valent, P., G. Schmidt, J. Besemer, P. Mayer, G. Zenke, E. Liehl, W. Hinterberger, K. Lechner, D. Maurer, and P. Bettelheim. 1989. Interleukin-3 is a differentiation factor for human basophils. Blood 73: 1763-1769. (Pubitemid 19145104)
21. Siracusa, M. C., S. A. Saenz, D. A. Hill, B. S. Kim, M. B. Headley, T. A. Doering, E. J. Wherry, H. K. Jessup, L. A. Siegel, T. Kambayashi, et al. 2011. TSLP promotes interleukin-3-independent basophil haematopoiesis and type 2 inflammation. Nature 477: 229-233.
22. Lee, T. D., R. K. Grencis, and D. Wakelin. 1982. Specific cross-immunity between Trichinella spiralis and Trichuris muris: immunization with heterologous infections and antigens and transfer of immunity with heterologous immune mesenteric lymph node cells. Parasitology 84: 381-389. (Pubitemid 12083926)
23. Wakelin, D., and M. M. Wilson. 1977. Transfer of immunity to Trichinella spiralis in the mouse with mesenteric lymph node cells: time of appearance of effective cells in donors and expression of immunity in recipients. Parasitology 74: 215-224. (Pubitemid 8122999)
24. Despommier, D. D. 1993. Trichinella spiralis and the concept of niche. J. Parasitol. 79: 472-482. (Pubitemid 23249732)
25. Arinobu, Y., H. Iwasaki, M. F. Gurish, S. Mizuno, H. Shigematsu, H. Ozawa, D. G. Tenen, K. F. Austen, and K. Akashi. 2005. Developmental checkpoints of the basophil/mast cell lineages in adult murine hematopoiesis. Proc. Natl. Acad. Sci. USA 102: 18105-18110. (Pubitemid 41798509)
26. Urban, J. F., Jr., L. Schopf, S. C. Morris, T. Orekhova, K. B. Madden, C. J. Betts, H. R. Gamble, C. Byrd, D. Donaldson, K. Else, and F. D. Finkelman. 2000. Stat6 signaling promotes protective immunity against Trichinella spiralis through a mast cell- and T cell-dependent mechanism. J. Immunol. 164: 2046-2052. (Pubitemid 30108762)
27. Ohnmacht, C., and D. Voehringer. 2010. Basophils protect against reinfection with hookworms independently of mast cells and memory Th2 cells. J. Immunol. 184: 344-350.
28. Obata, K., K. Mukai, Y. Tsujimura, K. Ishiwata, Y. Kawano, Y. Minegishi, N. Watanabe, and H. Karasuyama. 2007. Basophils are essential initiators of a novel type of chronic allergic inflammation. Blood 110: 913-920. (Pubitemid 47267429)
29. Sawaguchi, M., S. Tanaka, Y. Nakatani, Y. Harada, K. Mukai, Y. Matsunaga, K. Ishiwata, K. Oboki, T. Kambayashi, N. Watanabe, et al. 2012. Role of mast cells and basophils in IgE responses and in allergic airway hyperresponsiveness. J. Immunol. 188: 1809-1818.
30. Vallance, B. A., K. Croitoru, and S. M. Collins. 1998. T lymphocyte-dependent and -independent intestinal smooth muscle dysfunction in the T. spiralis-infected mouse. Am. J. Physiol. 275: G1157-G1165.
31. Perrigoue, J. G., F. A. Marshall, and D. Artis. 2008. On the hunt for helminths: innate immune cells in the recognition and response to helminth parasites. Cell. Microbiol. 10: 1757-1764.
32. Neill, D. R., S. H. Wong, A. Bellosi, R. J. Flynn, M. Daly, T. K. Langford, C. Bucks, C. M. Kane, P. G. Fallon, R. Pannell, et al. 2010. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464: 1367-1370.
33. Paul, W. E., and J. Zhu. 2010. How are T(H)2-type immune responses initiated and amplified? Nat. Rev. Immunol. 10: 225-235.
34. Saenz, S. A., M. Noti, and D. Artis. 2010. Innate immune cell populations function as initiators and effectors in Th2 cytokine responses. Trends Immunol. 31: 407-413.
35. Saenz, S. A., M. C. Siracusa, J. G. Perrigoue, S. P. Spencer, J. F. Urban, Jr., J. E. Tocker, A. L. Budelsky, M. A. Kleinschek, R. A. Kastelein, T. Kambayashi, et al. 2010. IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature 464: 1362-1366.
36. Al-Shami, A., R. Spolski, J. Kelly, A. Keane-Myers, and W. J. Leonard. 2005. A role for TSLP in the development of inflammation in an asthma model. J. Exp. Med. 202: 829-839. (Pubitemid 41345971)
37. Taylor, B. C., C. Zaph, A. E. Troy, Y. Du, K. J. Guild, M. R. Comeau, and D. Artis. 2009. TSLP regulates intestinal immunity and inflammation in mouse models of helminth infection and colitis. J. Exp. Med. 206: 655-667.
38. Ziegler, S. F., and D. Artis. 2010. Sensing the outside world: TSLP regulates barrier immunity. Nat. Immunol. 11: 289-293.
39. Ramalingam, T. R., J. T. Pesce, M. M. Mentink-Kane, S. Madala, A.W. Cheever, M. R. Comeau, S. F. Ziegler, and T. A. Wynn. 2009. Regulation of helminth-induced Th2 responses by thymic stromal lymphopoietin. J. Immunol. 182: 6452-6459.
40. 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. (Pubitemid 41586952)
41. Le Gros, G., S. Z. Ben-Sasson, D. H. Conrad, I. Clark-Lewis, F. D. Finkelman, M. Plaut, andW. E. Paul. 1990. IL-3 promotes production of IL-4 by splenic non-B, non-T cells in response to Fc receptor cross-linkage. J. Immunol. 145: 2500-2506. (Pubitemid 20374570)
42. Ohnmacht, C., and D. Voehringer. 2009. Basophil effector function and homeostasis during helminth infection. Blood 113: 2816-2825.
43. Shen, T., S. Kim, J. S. Do, L. Wang, C. Lantz, J. F. Urban, G. Le Gros, and B. Min. 2008. T cell-derived IL-3 plays key role in parasite infection-induced basophil production but is dispensable for in vivo basophil survival. Int. Immunol. 20: 1201-1209.
44. Kroeger, K. M., B. M. Sullivan, and R. M. Locksley. 2009. IL-18 and IL-33 elicit Th2 cytokines from basophils via a MyD88- and p38alpha-dependent pathway. J. Leukoc. Biol. 86: 769-778.
45. Schneider, E., A. F. Petit-Bertron, R. Bricard, M. Levasseur, A. Ramadan, J. P. Girard, A. Herbelin, and M. Dy. 2009. IL-33 activates unprimed murine basophils directly in vitro and induces their in vivo expansion indirectly by promoting hematopoietic growth factor production. J. Immunol. 183: 3591-3597.
46. Suzukawa, M., M. Iikura, R. Koketsu, H. Nagase, C. Tamura, A. Komiya, S. Nakae, K. Matsushima, K. Ohta, K. Yamamoto, and M. Yamaguchi. 2008. An IL-1 cytokine member, IL-33, induces human basophil activation via its ST2 receptor. J. Immunol. 181: 5981-5989.
47. Hill, D. A., M. C. Siracusa, M. C. Abt, B. S. Kim, D. Kobuley, M. Kubo, T. Kambayashi, D. F. Larosa, E. D. Renner, J. S. Orange, et al. 2012. Commensal bacteria-derived signals regulate basophil hematopoiesis and allergic inflammation. Nat. Med. 18: 538-546.
48. Ishizaka, T., R. De Bernardo, H. Tomioka, L. M. Lichtenstein, and K. Ishizaka. 1972. Identification of basophil granulocytes as a site of allergic histamine release. J. Immunol. 108: 1000-1008.
49. Chen, K., W. Xu, M. Wilson, B. He, N. W. Miller, E. Bengtén, E. S. Edholm, P. A. Santini, P. Rath, A. Chiu, et al. 2009. Immunoglobulin D enhances immune surveillance by activating antimicrobial, proinflammatory and B cell-stimulating programs in basophils. Nat. Immunol. 10: 889-898.
50. Siraganian, R. P., andW. A. Hook. 1976. Complement-induced histamine release from human basophils. II. Mechanism of the histamine release reaction. J. Immunol. 116: 639-646.
51. Charles, N., D. Hardwick, E. Daugas, G. G. Illei, and J. Rivera. 2010. Basophils and the T helper 2 environment can promote the development of lupus nephritis. Nat. Med. 16: 701-707.