Basophils protect against reinfection with hookworms independently of mast cells and memory Th2 cells

Journal of Immunology

Volumn 184, Issue 1, 2010, Pages 344-350

  Ohnmacht, Caspar ^a   Voehringer, David ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN E; STEM CELL FACTOR; STEM CELL FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASOPHIL; BLOOD SAMPLING; CELLULAR IMMUNITY; CONTROLLED STUDY; HOOKWORM; HOOKWORM INFECTION; IMMUNE RESPONSE; IMMUNOGLOBULIN BLOOD LEVEL; MAST CELL; MEMORY T LYMPHOCYTE; MOUSE; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; PRIMARY INFECTION; PRIORITY JOURNAL; REINFECTION; SECONDARY INFECTION; STEADY STATE; T CELL DEPLETION; TH2 CELL; WILD TYPE; WORM EXPULSION; ANIMAL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; MOUSE MUTANT; NIPPOSTRONGYLUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; BASOPHILS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HOOKWORM INFECTIONS; IMMUNOLOGIC MEMORY; MAST CELLS; MICE; MICE, KNOCKOUT; NIPPOSTRONGYLUS; PROTO-ONCOGENE PROTEINS C-KIT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TH2 CELLS;

EID: 73949111782     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901841     Document Type: Article

References (38)

1. Hotez, P. J., B. Zhan, J. M. Bethony, A. Loukas, A. Williamson, G. N. Goud, J. M. Hawdon, A. Dobardzic, R. Dobardzic, K. Ghosh, et al. 2003. Progress in the development of a recombinant vaccine for human hookworm disease: the Human Hookworm Vaccine Initiative. Int. J. Parasitol. 33: 1245-1258.
2. 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.
3. Mitchell, L. A., R. B. Wescott, and L. E. Perryman. 1983. Kinetics of expulsion of the nematode, Nippostrongylus brasiliensis, in mast-cell deficient W/WV mice. Parasite Immunol. 5: 1-12.
4. Behm, C. A., and K. S. Ovington. 2000. The role of eosinophils in parasitic helminth infections: insights from genetically modified mice. Parasitol. Today 16: 202-209.
5. Anthony, R. M., J. F. Urban Jr., F. Alem, H. A. Hamed, C. T. Rozo, J. L. Boucher, N. Van Rooijen, and W. C. Gause. 2006. Memory T(H)2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat. Med. 12: 955-960.
6. 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.
7. Voehringer, D., T. A. Reese, X. Huang, K. Shinkai, and R. M. Locksley. 2006. Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic non-eosinophil cells of the innate immune system. J. Exp. Med. 203: 1435-1446.
8. Katona, I. M., J. F. Urban Jr., and F. D. Finkelman. 1988. The role of L3T4+ and Lyt-2+ T cells in the IgE response and immunity to Nippostrongylus brasiliensis. J. Immunol. 140: 3206-3211.
9. Knott, M. L., K. I. Matthaei, P. R. Giacomin, H. Wang, P. S. Foster, and L. A. Dent. 2007. Impaired resistance in early secondary Nippostrongylus brasiliensis infections in mice with defective eosinophilopoeisis. Int. J. Parasitol. 37: 1367-1378.
10. Zhao, A., J. F. Urban, Jr., R. M. Anthony, R. Sun, J. Stiltz, N. van Rooijen, T. A. Wynn, W. C. Gause, and T. Shea-Donohue. 2008. Th2 cytokine-induced alterations in intestinal smooth muscle function depend on alternatively activated macrophages. Gastroenterology 135:217-225.e1.
11. Denzel, A., U. A. Maus, M. Rodriguez Gomez, C. Moll, M. Niedermeier, C. Winter, R. Maus, S. Hollingshead, D. E. Briles, L. A. Kunz-Schughart, et al. 2008. Basophils enhance immunological memory responses. Nat. Immunol. 9: 733-742.
12. Mack, M., M. A. Schneider, C. Moll, J. Cihak, H. Brühl, J. W. Ellwart, M. P. Hogarth, M. Stangassinger, and D. Schlöndorff. 2005. Identification of antigen-capturing cells as basophils. J. Immunol. 174: 735-741.
13. 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.
14. 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.
15. 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.
16. Ohnmacht, C., and D. Voehringer. 2009. Basophil effector function and homeostasis during helminth infection. Blood 113: 2816-2825.
17. Kitamura, Y., S. Go, and K. Hatanaka. 1978. Decrease of mast cells in W/Wv mice and their increase by bone marrow transplantation. Blood 52: 447-452. (Pubitemid 8395558)
18. Maeda, H., A. Yamagata, S. Nishikawa, K. Yoshinaga, S. Kobayashi, K. Nishi, and S. Nishikawa. 1992. Requirement of c-kit for development of intestinal pacemaker system. Development 116: 369-375.
19. Lyon, M. F., and P. H. Glenister. 1982. A new allele sash (Wsh) at the W-locus and a spontaneous recessive lethal in mice. Genet. Res. 39: 315-322.
20. Kaplan, M. H., U. Schindler, S. T. Smiley, and M. J. Grusby. 1996. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 4: 313-319.
21. McKenzie, G. J., P. G. Fallon, C. L. Emson, R. K. Grencis, and A. N. McKenzie. 1999. Simultaneous disruption of interleukin (IL)-4 and IL-13 defines individual roles in T helper cell type 2-mediated responses. J. Exp. Med. 189: 1565-1572.
22. Tono, T., T. Tsujimura, U. Koshimizu, T. Kasugai, S. Adachi, K. Isozaki, S. Nishikawa, M. Morimoto, Y. Nishimune, S. Nomura, et al. 1992. c-kit Gene was not transcribed in cultured mast cells of mast cell-deficient Wsh/Wsh mice that have a normal number of erythrocytes and a normal c-kit coding region. Blood 80: 1448-1453.
23. Lantz, C. S., and T. F. Huff. 1995. Differential responsiveness of purified mouse c-kit+ mast cells and their progenitors to IL-3 and stem cell factor. J. Immunol. 155: 4024-4029.
24. Huntley, J. F., C. Gooden, G. F. Newlands, A. Mackellar, D. A. Lammas, D. Wakelin, M. Tuohy, R. G. Woodbury, and H. R. Miller. 1990. Distribution of intestinal mast cell proteinase in blood and tissues of normal and Trichinella-infected mice. Parasite Immunol. 12: 85-95.
25. Ikeda, R. K., M. Miller, J. Nayar, L. Walker, J. Y. Cho, K. McElwain, S. McElwain, E. Raz, and D. H. Broide. 2003. Accumulation of peribronchial mast cells in a mouse model of ovalbumin allergen induced chronic airway inflammation: modulation by immunostimulatory DNA sequences. J. Immunol. 171: 4860-4867.
26. Voehringer, D., K. Shinkai, and R. M. Locksley. 2004. Type 2 immunity reflects orchestrated recruitment of cells committed to IL-4 production. Immunity 20: 267-277.
27. Miller, H. R., and A. D. Pemberton. 2002. Tissue-specific expression of mast cell granule serine proteinases and their role in inflammation in the lung and gut. Immunology 105: 375-390.
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.
29. Urban, J. F., Jr., N. Noben-Trauth, L. Schopf, K. B. Madden, and F. D. Finkelman. 2001. Cutting edge: IL-4 receptor expression by non-bone marrow-derived cells is required to expel gastrointestinal nematode parasites. J. Immunol. 167: 6078-6081.
30. Crowle, P. K., and N. D. Reed. 1981. Rejection of the intestinal parasite Nippostrongylus brasiliensis by mast cell-deficient W/Wv anemic mice. Infect. Immun. 33: 54-58.
31. Khodoun, M. V., T. Orekhova, C. Potter, S. Morris, and F. D. Finkelman. 2004. Basophils initiate IL-4 production during a memory T-dependent response. J. Exp. Med. 200: 857-870.
32. McCoy, K. D., M. Stoel, R. Stettler, P. Merky, K. Fink, B. M. Senn, C. Schaer, J. Massacand, B. Odermatt, H. C. Oettgen, et al. 2008. Polyclonal and specific antibodies mediate protective immunity against enteric helminth infection. Cell Host Microbe 4: 362-373.
33. Wojciechowski, W., D. P. Harris, F. Sprague, B. Mousseau, M. Makris, K. Kusser, T. Honjo, K. Mohrs, M. Mohrs, T. Randall, et al. 2009. Cytokine-producing effector B cells regulate type 2 immunity to H. polygyrus. Immunity 30: 421-433.
34. Mitre, E., R. T. Taylor, J. Kubofcik, and T. B. Nutman. 2004. Parasite antigen-driven basophils are a major source of IL-4 in human filarial infections. J. Immunol. 172: 2439-2445. (Pubitemid 38182393)
35. Manz, R. A., A. Thiel, and A. Radbruch. 1997. Lifetime of plasma cells in the bone marrow. Nature 388: 133-134.
36. Slifka, M. K., R. Antia, J. K. Whitmire, and R. Ahmed. 1998. Humoral immunity due to long-lived plasma cells. Immunity 8: 363-372.
37. Miller, H. R. 1980. Expulsion of Nippostrongylus brasiliensis from rats protected with serum. I. The efficacy of sera from singly and multiply infected donors related to time of administration and volume of serum injected. Immunology 40: 325-334.
38. Ahmad, A., C. H. Wang, and R. G. Bell. 1991. A role for IgE in intestinal immunity. Expression of rapid expulsion of Trichinella spiralis in rats transfused with IgE and thoracic duct lymphocytes. J. Immunol. 146: 3563-3570.