Identification of semaphorin 4B as a negative regulator of basophil-mediated immune responses

Journal of Immunology

Volumn 186, Issue 5, 2011, Pages 2881-2888

  Nakagawa, Yukinobu ^a,b   Takamatsu, Hyota ^a   Okuno, Tatsusada ^a,b   Kang, Sujin ^a   Nojima, Satoshi ^a,b   Kimura, Tetsuya ^a   Kataoka, Tatsuki R ^c   Ikawa, Masahito ^d   Toyofuku, Toshihiko ^a   Katayama, Ichiro ^b   Kumanogoh, Atsushi ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c KYOTO UNIVERSITY HOSPITAL   (Japan)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; IMMUNOGLOBULIN E; INTERLEUKIN 3; INTERLEUKIN 4; PAPAIN; SEMAPHORIN; SEMAPHORIN 4B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; BASOPHIL; CD4+ T LYMPHOCYTE; CELL CONTACT; CELL FUNCTION; CONTROLLED STUDY; CROSS LINKING; CYTOKINE PRODUCTION; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOGLOBULIN PRODUCTION; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TH2 CELL;

ANIMALS; B-LYMPHOCYTES; BASOPHILS; CYTOKINES; DOWN-REGULATION; GENE EXPRESSION REGULATION; IMMUNE TOLERANCE; IMMUNOGLOBULIN E; IMMUNOLOGIC MEMORY; INTERLEUKIN-4; INTERLEUKIN-6; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NUDE; MICE, TRANSGENIC; SEMAPHORINS; T-LYMPHOCYTES; TH2 CELLS;

EID: 79952774427     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003485     Document Type: Article

References (47)

1. Kawakami, T., and S. J. Galli. 2002. Regulation of mast-cell and basophil function and survival by IgE. Nat. Rev. Immunol. 2: 773-786.
2. 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.
3. Min, B. 2008. Basophils: what they 'can do' versus what they 'actually do'. Nat. Immunol. 9: 1333-1339.
4. Sullivan, B. M., and R. M. Locksley. 2009. Basophils: a nonredundant contributor to host immunity. Immunity 30: 12-20.
5. Hida, S., M. Tadachi, T. Saito, and S. Taki. 2005. Negative control of basophil expansion by IRF-2 critical for the regulation of Th1/Th2 balance. Blood 106: 2011-2017. (Pubitemid 41291714)
6. Charles, N., W. T. Watford, H. L. Ramos, L. Hellman, H. C. Oettgen, G. Gomez, J. J. Ryan, J. J. O'Shea, and J. Rivera. 2009. Lyn kinase controls basophil GATA-3 transcription factor expression and induction of Th2 cell differentiation. Immunity 30: 533-543.
7. 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.
8. Seder, R. A., W. E. Paul, A. M. Dvorak, S. J. Sharkis, A. Kagey-Sobotka, Y. Niv, F. D. Finkelman, S. A. Barbieri, S. J. Galli, and M. Plaut. 1991. Mouse splenic and bone marrow cell populations that express high-affinity Fc epsilon receptors and produce interleukin 4 are highly enriched in basophils. Proc. Natl. Acad. Sci. USA 88: 2835-2839.
9. Sokol, C. L., G. M. Barton, A. G. Farr, and R. Medzhitov. 2008. A mechanism for the initiation of allergen-induced T helper type 2 responses. Nat. Immunol. 9: 310-318.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. Kolodkin, A. L., D. J. Matthes, and C. S. Goodman. 1993. The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75: 1389-1399.
18. Serini, G., D. Valdembri, S. Zanivan, G. Morterra, C. Burkhardt, F. Caccavari, L. Zammataro, L. Primo, L. Tamagnone, M. Logan, et al. 2003. Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 424: 391-397. (Pubitemid 36917481)
19. Toyofuku, T., H. Zhang, A. Kumanogoh, N. Takegahara, F. Suto, J. Kamei, K. Aoki, M. Yabuki, M. Hori, H. Fujisawa, and H. Kikutani. 2004. Dual roles of Sema6D in cardiac morphogenesis through region-specific association of its receptor, Plexin-A1, with off-track and vascular endothelial growth factor receptor type 2. Genes Dev. 18: 435-447. (Pubitemid 38316350)
20. Neufeld, G., and O. Kessler. 2008. The semaphorins: versatile regulators of tumour progression and tumour angiogenesis. Nat. Rev. Cancer 8: 632-645.
21. Suzuki, K., A. Kumanogoh, and H. Kikutani. 2008. Semaphorins and their receptors in immune cell interactions. Nat. Immunol. 9: 17-23.
22. Capparuccia, L., and L. Tamagnone. 2009. Semaphorin signaling in cancer cells and in cells of the tumor microenvironment - two sides of a coin. J. Cell Sci. 122: 1723-1736.
23. Kumanogoh, A., C. Watanabe, I. Lee, X. Wang, W. Shi, H. Araki, H. Hirata, K. Iwahori, J. Uchida, T. Yasui, et al. 2000. Identification of CD72 as a lymphocyte receptor for the class IV semaphorin CD100: a novel mechanism for regulating B cell signaling. Immunity 13: 621-631.
24. Kumanogoh, A., S. Marukawa, K. Suzuki, N. Takegahara, C. Watanabe, E. Ch'ng, I. Ishida, H. Fujimura, S. Sakoda, K. Yoshida, and H. Kikutani. 2002. Class IV semaphorin Sema4A enhances T-cell activation and interacts with Tim-2. Nature 419: 629-633.
25. Takegahara, N., H. Takamatsu, T. Toyofuku, T. Tsujimura, T. Okuno, K. Yukawa, M. Mizui, M. Yamamoto, D. V. Prasad, K. Suzuki, et al. 2006. Plexin-A1 and its interaction with DAP12 in immune responses and bone homeostasis. Nat. Cell Biol. 8: 615-622.
26. Kumanogoh, A., T. Shikina, K. Suzuki, S. Uematsu, K. Yukawa, S. Kashiwamura, H. Tsutsui, M. Yamamoto, H. Takamatsu, E. P. Ko-Mitamura, et al. 2005. Nonredundant roles of Sema4A in the immune system: defective T cell priming and Th1/Th2 regulation in Sema4A-deficient mice. Immunity 22: 305-316. (Pubitemid 40387473)
27. Takamatsu, H., N. Takegahara, Y. Nakagawa, M. Tomura, M. Taniguchi, R. H. Friedel, H. Rayburn, M. Tessier-Lavigne, Y. Yoshida, T. Okuno, et al. 2010. Semaphorins guide the entry of dendritic cells into the lymphatics by activating myosin II. Nat. Immunol. 11: 594-600.
28. Sato, T., T. Sasahara, Y. Nakamura, T. Osaki, T. Hasegawa, T. Tadakuma, Y. Arata, Y. Kumagai, M. Katsuki, and S. Habu. 1994. Naive T cells can mediate delayed-type hypersensitivity response in T cell receptor transgenic mice. Eur. J. Immunol. 24: 1512-1516.
29. Yoshimoto, T., H. Tsutsui, K. Tominaga, K. Hoshino, H. Okamura, S. Akira, W. E. Paul, and K. Nakanishi. 1999. IL-18, although antiallergic when administered with IL-12, stimulates IL-4 and histamine release by basophils. Proc. Natl. Acad. Sci. USA 96: 13962-13966.
30. Hida, S., S. Yamasaki, Y. Sakamoto, M. Takamoto, K. Obata, T. Takai, H. Karasuyama, K. Sugane, T. Saito, and S. Taki. 2009. Fc receptor gammachain, a constitutive component of the IL-3 receptor, is required for IL-3-induced IL-4 production in basophils. Nat. Immunol. 10: 214-222.
31. Inaba, K., R. M. Steinman, M. W. Pack, H. Aya, M. Inaba, T. Sudo, S. Wolpe, and G. Schuler. 1992. Identification of proliferating dendritic cell precursors in mouse blood. J. Exp. Med. 175: 1157-1167.
32. Doi, T., K. Obayashi, T. Kadowaki, H. Fujii, and S. Koyasu. 2008. PI3K is a negative regulator of IgE production. Int. Immunol. 20: 499-508.
33. Shi, W., A. Kumanogoh, C. Watanabe, J. Uchida, X. Wang, T. Yasui, K. Yukawa, M. Ikawa, M. Okabe, J. R. Parnes, et al. 2000. The class IV semaphorin CD100 plays nonredundant roles in the immune system: defective B and T cell activation in CD100-deficient mice. Immunity 13: 633-642.
34. Paradis, S., D. B. Harrar, Y. Lin, A. C. Koon, J. L. Hauser, E. C. Griffith, L. Zhu, L. F. Brass, C. Chen, and M. E. Greenberg. 2007. An RNAi-based approach identifies molecules required for glutamatergic and GABAergic synapse development. Neuron 53: 217-232.
35. Geha, R. S., H. H. Jabara, and S. R. Brodeur. 2003. The regulation of immunoglobulin E class-switch recombination. Nat. Rev. Immunol. 3: 721-732.
36. Reddy, E. P., A. Korapati, P. Chaturvedi, and S. Rane. 2000. IL-3 signaling and the role of Src kinases, JAKs and STATs: a covert liaison unveiled. Oncogene 19: 2532-2547. (Pubitemid 30339209)
37. Martinez-Moczygemba, M., and D. P. Huston. 2003. Biology of common beta receptor-signaling cytokines: IL-3, IL-5, and GM-CSF. J. Allergy Clin. Immunol. 112: 653-665, quiz 666.
38. Sokol, C. L., and R. Medzhitov. 2010. Emerging functions of basophils in protective and allergic immune responses. Mucosal Immunol. 3: 129-137.
39. Burkhardt, C., M. Müller, A. Badde, C. C. Garner, E. D. Gundelfinger, and A. W. Püschel. 2005. Semaphorin 4B interacts with the post-synaptic density protein PSD-95/SAP90 and is recruited to synapses through a C-terminal PDZ-binding motif. FEBS Lett. 579: 3821-3828.
40. Affaticati, P., O. Mignen, F. Jambou, M. C. Potier, I. Klingel-Schmitt, J. Degrouard, S. Peineau, E. Gouadon, G. L. Collingridge, R. Liblau, et al. 2011. Sustained calcium signalling and caspase-3 activation involve NMDA receptors in thymocytes in contact with dendritic cells. Cell Death Differ. 18: 99-108.
41. 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.
42. Kuroda, E., V. Ho, J. Ruschmann, F. Antignano, M. Hamilton, M. J. Rauh, A. Antov, R. A. Flavell, L. M. Sly, and G. Krystal. 2009. SHIP represses the generation of IL-3-induced M2 macrophages by inhibiting IL-4 production from basophils. J. Immunol. 183: 3652-3660.
43. Paling, N. R., and M. J. Welham. 2002. Role of the protein tyrosine phosphatase SHP-1 (Src homology phosphatase-1) in the regulation of interleukin-3-induced survival, proliferation and signalling. Biochem. J. 368: 885-894.
44. Minoo, P., M. M. Zadeh, R. Rottapel, J. J. Lebrun, and S. Ali. 2004. A novel SHP-1/Grb2-dependent mechanism of negative regulation of cytokine-receptor signaling: contribution of SHP-1 C-terminal tyrosines in cytokine signaling. Blood 103: 1398-1407. (Pubitemid 38168655)
45. Kraft, S., and J. P. Kinet. 2007. New developments in FcepsilonRI regulation, function and inhibition. Nat. Rev. Immunol. 7: 365-378.
46. Pasterkamp, R. J., and A. L. Kolodkin. 2003. Semaphorin junction: making tracks toward neural connectivity. Curr. Opin. Neurobiol. 13: 79-89.
47. Toyofuku, T., M. Yabuki, J. Kamei, M. Kamei, N. Makino, A. Kumanogoh, and M. Hori. 2007. Semaphorin-4A, an activator for T-cell-mediated immunity, suppresses angiogenesis via Plexin-D1. EMBO J. 26: 1373-1384. (Pubitemid 46398711)