Fc receptor γ-chain, a constitutive component of the IL-3 receptor, is required for IL-3-induced IL-4 production in basophils

Nature Immunology

Volumn 10, Issue 2, 2009, Pages 214-222

  Hida, Shigeaki ^a   Yamasaki, Sho ^b   Sakamoto, Yuzuru ^a   Takamoto, Masaya ^a   Obata, Kazushige ^c   Takai, Toshiyuki ^d   Karasuyama, Hajime ^c   Sugane, Kazuo ^a   Saito, Takashi ^b   Taki, Shinsuke ^a  

^a SHINSHU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b RIKEN Center for Integrative Medical Sciences   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^d TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; INTERLEUKIN 3; INTERLEUKIN 3 RECEPTOR; INTERLEUKIN 4; PROTEIN KINASE SYK;

ANIMAL CELL; ARTICLE; BASOPHIL; BETA CHAIN; COMPLEMENT SYSTEM; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENETIC COMPLEMENTATION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RETROVIRUS; SIGNAL TRANSDUCTION; TH2 CELL;

ANIMALS; BASOPHILS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; FLOW CYTOMETRY; IMMUNOPRECIPITATION; INTERLEUKIN-3; INTERLEUKIN-4; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, TRANSGENIC; PROTEIN-TYROSINE KINASES; RECEPTORS, IGG; RECEPTORS, INTERLEUKIN-3; SIGNAL TRANSDUCTION; TH2 CELLS; TRANSCRIPTIONAL ACTIVATION;

EID: 58549089167     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.1686     Document Type: Article

References (49)

1. Nicola, N.A. Cytokine pleiotropy and redundancy: A view from the receptor. Stem Cells 12 Suppl 1, 3-12 (1994).
2. Sugamura, K. et al. The interleukin-2 receptor γ chain: Its role in the multiple cytokine receptor complexes and T cell development in XSCID. Annu. Rev. Immunol. 14, 179-205 (1996).
3. Taniguchi, T. Cytokine signaling through nonreceptor protein tyrosine kinases. Science 268, 251-255 (1995).
4. Taga, T. & Kishimoto, T. Gp130 and the interleukin-6 family of cytokines. Annu. Rev. Immunol. 15, 797-819 (1997).
5. Geijsen, N., Koenderman, L. & Coffer, P.J. Specificity in cytokine signal transduction: Lessons learned from the IL-3/IL-5/GM-CSF receptor family. Cytokine Growth Factor Rev. 12, 19-25 (2001).
6. Miyajima, A., Kitamura, T., Harada, N., Yokota, T. & Arai, K. Cytokine receptors and signal transduction. Annu. Rev. Immunol. 10, 295-331 (1992).
7. Takatsu, K. Interleukin 5 and B cell differentiation. Cytokine Growth Factor Rev. 9, 25-35 (1998).
8. Bezbradica, J.S. et al. Granulocyte-macrophage colony-stimulating factor regulates effector differentiation of invariant natural killer T cells during thymic ontogeny. Immunity 25, 487-497 (2006).
9. Falcone, F.H., Haas, H. & Gibbs, B.F. The human basophil: A new appreciation of its role in immune responses. Blood 96, 4028-4038 (2000).
10. Lopez, A.F. et al. Stimulation of proliferation, differentiation, and function of human cells by primate interleukin 3. Proc. Natl. Acad. Sci. USA 84, 2761-2765 (1987).
11. Reddy, E.P., Korapati, A., Chaturvedi, P. & Rane, S. IL-3 signaling and the role of Src kinases, JAKs and STATs: A covert liaison unveiled. Oncogene 19, 2532-2547 (2000).
12. Yousefi, S., Hoessli, D.C., Blaser, K., Mills, G.B. & Simon, H.U. Requirement of Lyn and Syk tyrosine kinases for the prevention of apoptosis by cytokines in human eosinophils. J. Exp. Med. 183 1407-1414 (1996).
13. Pazdrak, K., Schreiber, D., Forsythe, P., Justement, L. & Alam, R. The intracellular signal transduction mechanism of interleukin 5 in eosinophils: The involvement of lyn tyrosine kinase and the Ras-Raf-1- MEK-microtubule-associated protein kinase pathway. J. Exp. Med. 181, 1827-1834 (1995).
14. Lach-Trifilieff, E., Menear, K., Schweighoffer, E., Tybulewicz, V.L.J. & Walker, C. Syk-deficient eosinophils show normal interleukin-5-mediated differentiation, maturation, and survival but no longer respond to FcgR activation. Blood 96, 2506-2510 (2000).
15. Chan, A.C. & Shaw, A.S. Regulation of antigen receptor signal transduction by protein tyrosine kinases. Curr. Opin. Immunol. 8, 394-401 (1996).
16. Fodor, S., Jakus, Z. & Mocsai, A. ITAM-based signaling beyond the adaptive immune response. Immunol. Lett. 104, 29-37 (2006).
17. Tsubokawa, M. et al. Interleukin-3 activates Syk in a human myeloblastic leukemia cell line, AML193. Eur. J. Biochem. 249 792-796 (1997).
18. Falcone, F.H., Zillikens, D. & Gibbs, B.F. The 21st century renaissance of the basophil? Current insights into its role in allergic responses and innate immunity. Exp. Dermatol. 15, 855-864 (2006).
19. Oh, K., Shen, T., Le Gros, G. & Min, B. Induction of Th2 type immunity in a mouse system reveals a novel immunoregulatory role of basophils. Blood 109, 2921-2927 (2007).
20. Hida, S., Tadachi, M., Saito, T. & Taki, S. Negative control of basophil expansion by IRF-2 critical for the regulation of Th1/Th2 balance. Blood 106, 2011-2017 (2005).
21. Sokol, C.L., Barton, G.M., Farr, A.G. & Medzhitov, R. A mechanism for the initiation of allergen-induced T helper type 2 responses. Nat. Immunol. 9, 310-318 (2008).
22. Schramm, G. et al. Cutting edge: IPSE/alpha-1, a glycoprotein from Schistosoma mansoni eggs, induces IgE-dependent, antigen-independent IL-4 production by murine basophils in vivo. J. Immunol. 178 6023-6027 (2007).
23. Mohrs, K., Wakil, A.E., Killeen, N., Locksley, R.M. & Mohrs, M. A two-step process for cytokine production revealed by IL-4 dual-reporter mice. Immunity 23, 419-429 (2005).
24. Park, S.Y. et al. Resistance of Fc receptor-deficient mice to fatal glomerulonephritis. J. Clin. Invest. 102, 1229-1238 (1998).
25. Min, B. et al. Basophils produce IL-4 and accumulate in tissues after infection with a Th2-inducing parasite. J. Exp. Med. 200 507-517 (2004).
26. Mukai, K. et al. Basophils play a critical role in the development of IgE-mediated chronic allergic inflammation independently of T cells and mast cells. Immunity 23, 191-202 (2005).
27. Takeda, K. et al. Essential role of Stat6 in IL-4 signalling. Nature 380, 627-630 (1996).
28. Yoshimoto, T. et al. 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 (1999).
29. Denzel, A. et al. Basophils enhance immunological memory responses. Nat. Immunol. 9, 733-742 (2008).
30. Kojima, T. et al. Mast cells and basophils are selectively activated in vitro and in vivo through CD200R3 in an IgE-independent manner. J. Immunol. 179, 7093-7100 (2007).
31. Mita, S. et al. Molecular characterization of the β chain of the murine interleukin 5 receptor. Int. Immunol. 3, 665-672 (1991).
32. Sakurai, D. et al. FceRIγ-ITAM Is differentially required for mast cell function in vivo. J. Immunol. 172, 2374-2381 (2004).
33. Wines, B.D., Trist, H.M., Ramsland, P.A. & Hogarth, P.M. A common site of the Fc receptor g subunit interacts with the unrelated immunoreceptors FcaRI and FceRI. J. Biol. Chem. 281, 17108-17113 (2006).
34. Padigel, U.M. & Farrell, J.P. Control of infection with Leishmania major in susceptible BALB/c mice lacking the common γ-chain for FcR is associated with reduced production of IL-10 and TGF-β by parasitized cells. J. Immunol. 174, 6340-6345 (2005).
35. Kitamura, K. et al. Critical role of the Fc receptor γ-chain on APCs in the development of allergen-induced airway hyperresponsiveness and inflammation. J. Immunol. 178, 480-488 (2007).
36. Finkelman, F.D. et al. Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol. Rev. 201, 139-155 (2004).
37. Schmitz, J. et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptorrelated protein ST2 and induces T helper type 2-associated cytokines. Immunity 23, 479-490 (2005).
38. Tassiulas, I. et al. Amplification of IFN-α-induced STAT1 activation and inflammatory function by Syk and ITAM-containing adaptors. Nat. Immunol. 5, 1181-1189 (2004).
39. Mocsai, A. et al. Integrin signaling in neutrophils and macrophages uses adaptors containing immunoreceptor tyrosine-based activation motifs. Nat. Immunol. 7, 1326-1333 (2006).
40. Feng, J., Garrity, D., Call, M.E., Moffett, H. & Wucherpfennig, K.W. Convergence on a distinctive assembly mechanism by unrelated families of activating immune receptors. Immunity 22, 427-438 (2005).
41. Launay, P. et al. Alternative endocytic pathway for immunoglobulin A Fc receptors (CD89) depends on the lack of FcRγ association and protects against degradation of bound ligand. J. Biol. Chem. 274, 7216-7225 (1999).
42. Honorio-Franca, A.C., Launay, P., Carneiro-Sampaio, M.M.S. & Monteiro, R.C. Colostral neutrophils express Fcα receptors (CD89) lacking γ chain association and mediate noninflammatory properties of secretory IgA. J. Leukoc. Biol. 69, 289-296 (2001).
43. Nicola, N.A. et al. Functional inactivation in mice of the gene for the interleukin-3 (IL- 3)-specific receptor β-chain: Implications for IL-3 function and the mechanism of receptor transmodulation in hematopoietic cells. Blood 87, 2665-2674 (1996).
44. Min, B. & Paul, W.E. Basophils and type 2 immunity. Curr. Opin. Hematol. 15, 59-63 (2008).
45. Bieneman, A.P., Chichester, K.L., Chen, Y.H. & Schroeder, J.T. Toll-like receptor 2 ligands activate human basophils for both IgE-dependent and IgE-independent secretion. J. Allergy Clin. Immunol. 115, 295-301 (2005).
46. Phillips, C., Coward, W.R., Pritchard, D.I. & Hewitt, C.R.A. Basophils express a type 2 cytokine profile on exposure to proteases from helminths and house dust mites. J. Leukoc. Biol. 73, 165-171 (2003).
47. Koga, T. et al. Costimulatory signals mediated by the ITAM motif cooperate with RANKL for bone homeostasis. Nature 428, 758-763 (2004).
48. Shi, Y. et al. Protein-tyrosine kinase Syk is required for pathogen engulfment in complement-mediated phagocytosis. Blood 107, 4554-4562 (2006).
49. Tian, X., Takamoto, M. & Sugane, K. Bisphenol A promotes IL-4 production by Th2 cells. Int. Arch. Allergy Immunol. 132, 240-247 (2003).