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PMID: 19465908 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

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.

Nature immunology ·Vol. 10 ·No. 7 ·2009-07-00 ·Pages 706-12

Yoshimoto T, Yasuda K, Tanaka H, Nakahira M, Imai Y, Fujimori Y, Nakanishi K

Abstract

Basophils express major histocompatibility complex class II, CD80 and CD86 and produce interleukin 4 (IL-4) in various conditions. Here we show that when incubated with IL-3 and antigen or complexes of antigen and immunoglobulin E (IgE), basophils internalized, processed and presented antigen as complexes of peptide and major histocompatibility complex class II and produced IL-4. Intravenous administration of ovalbumin-pulsed basophils into naive mice 'preferentially' induced the development of naive ovalbumin-specific CD4+ T cells into T helper type 2 (T(H)2) cells. Mice immunized in this way, when challenged by intravenous administration of ovalbumin, promptly produced ovalbumin-specific IgG1 and IgE. Finally, intravenous administration of IgE complexes rapidly induced T(H)2 cells only in the presence of endogenous basophils, which suggests that basophils are potent antigen-presenting cells that 'preferentially' augment T(H)2-IgE responses by capturing IgE complex.

MeSH Terms
Adoptive Transfer Animals Antigen-Presenting Cells/cytology,immunology,metabolism Basophils/immunology,metabolism,transplantation CD4-Positive T-Lymphocytes/cytology,immunology,metabolism Flow Cytometry Histocompatibility Antigens Class II/chemistry,immunology Immunoglobulin E/immunology Interleukin-4/genetics,metabolism Mice Mice, Inbred BALB C Mice, Knockout Ovalbumin/immunology Peptides/chemistry,immunology Spleen/cytology,immunology Strongyloides/immunology Strongyloidiasis/immunology,parasitology Th2 Cells/immunology
Chemicals
Histocompatibility Antigens Class II Peptides Interleukin-4 Immunoglobulin E Ovalbumin
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Yoshimoto Tomohiro
Department of Immunology and Medical Zoology, Hyogo College of Medicine, Nishinomiya, Hyogo, Japan.
Yasuda Koubun
Tanaka Hidehisa
Nakahira Masakiyo
Imai Yasutomo
Fujimori Yoshihiro
Nakanishi Kenji
References (49)
49 references, click to expand
  1. Basophils produce IL-4 and accumulate in tissues after infection with a Th2-inducing parasite.
    J Exp Med. 2004 Aug 16;200(4):507-17 PMID: 15314076
  2. Interleukin-12 and the regulation of innate resistance and adaptive immunity.
    Nat Rev Immunol. 2003 Feb;3(2):133-46 PMID: 12563297
  3. Type 2 immunity reflects orchestrated recruitment of cells committed to IL-4 production.
    Immunity. 2004 Mar;20(3):267-77 PMID: 15030771
  4. Interleukin-18 is a unique cytokine that stimulates both Th1 and Th2 responses depending on its cytokine milieu.
    Cytokine Growth Factor Rev. 2001 Mar;12(1):53-72 PMID: 11312119
  5. IL-18, although antiallergic when administered with IL-12, stimulates IL-4 and histamine release by basophils.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13962-6 PMID: 10570181
  6. Regulatory T cells selectively express toll-like receptors and are activated by lipopolysaccharide.
    J Exp Med. 2003 Feb 17;197(4):403-11 PMID: 12591899
  7. Immunohistochemical detection of human basophils in late-phase skin reactions.
    J Allergy Clin Immunol. 1998 Mar;101(3):354-62 PMID: 9525452
  8. Airway basophil and mast cell density in patients with bronchial asthma: relationship to bronchial hyperresponsiveness.
    J Asthma. 1996;33(2):89-95 PMID: 8609103
  9. Studies of hypersensitivity to low molecular weight substances. III. The 2,4-dinitrophenyl group as a determinant in the preciptin reaction.
    J Immunol. 1954 Nov;73(5):296-308 PMID: 13212051
  10. Basophils: a nonredundant contributor to host immunity.
    Immunity. 2009 Jan 16;30(1):12-20 PMID: 19144314
  11. Cross-linking Fc receptors stimulate splenic non-B, non-T cells to secrete interleukin 4 and other lymphokines.
    Proc Natl Acad Sci U S A. 1990 Feb;87(4):1421-5 PMID: 2106135
  12. IL-18 with IL-2 protects against Strongyloides venezuelensis infection by activating mucosal mast cell-dependent type 2 innate immunity.
    J Exp Med. 2005 Sep 5;202(5):607-16 PMID: 16129701
  13. IL-27 suppresses Th2 cell development and Th2 cytokines production from polarized Th2 cells: a novel therapeutic way for Th2-mediated allergic inflammation.
    J Immunol. 2007 Oct 1;179(7):4415-23 PMID: 17878337
  14. Mast cells as "tunable" effector and immunoregulatory cells: recent advances.
    Annu Rev Immunol. 2005;23:749-86 PMID: 15771585
  15. Basophils play a critical role in the development of IgE-mediated chronic allergic inflammation independently of T cells and mast cells.
    Immunity. 2005 Aug;23(2):191-202 PMID: 16111637
  16. TIM-1 and TIM-3 enhancement of Th2 cytokine production by mast cells.
    Blood. 2007 Oct 1;110(7):2565-8 PMID: 17620455
  17. Isolation of transcriptionally active umbilical cord blood-derived basophils expressing Fc epsilon RI, HLA-DR and CD203c.
    Allergy. 2006 Sep;61(9):1063-70 PMID: 16918508
  18. Regulation of expression of IL-4 alleles: analysis using a chimeric GFP/IL-4 gene.
    Immunity. 2001 Jan;14(1):1-11 PMID: 11163225
  19. Toll-like receptors.
    Annu Rev Immunol. 2003;21:335-76 PMID: 12524386
  20. IgE enhances mouse mast cell Fc(epsilon)RI expression in vitro and in vivo: evidence for a novel amplification mechanism in IgE-dependent reactions.
    J Exp Med. 1997 Feb 17;185(4):663-72 PMID: 9034145
  21. New targets for drug development in asthma.
    Lancet. 2008 Sep 20;372(9643):1073-87 PMID: 18805336
  22. Induction of Th2 type immunity in a mouse system reveals a novel immunoregulatory role of basophils.
    Blood. 2007 Apr 1;109(7):2921-7 PMID: 17132717
  23. Induction of human IgE synthesis in B cells by mast cells and basophils.
    Nature. 1993 Sep 23;365(6444):340-3 PMID: 7690905
  24. Basophils: what they 'can do' versus what they 'actually do'.
    Nat Immunol. 2008 Dec;9(12):1333-9 PMID: 19008933
  25. Developmental checkpoints of the basophil/mast cell lineages in adult murine hematopoiesis.
    Proc Natl Acad Sci U S A. 2005 Dec 13;102(50):18105-10 PMID: 16330751
  26. Basophils play a pivotal role in immunoglobulin-G-mediated but not immunoglobulin-E-mediated systemic anaphylaxis.
    Immunity. 2008 Apr;28(4):581-9 PMID: 18342553
  27. Basophils, eosinophils, and mast cells in atopic and nonatopic asthma and in late-phase allergic reactions in the lung and skin.
    J Allergy Clin Immunol. 2000 Jan;105(1 Pt 1):99-107 PMID: 10629459
  28. Basophil effector function and homeostasis during helminth infection.
    Blood. 2009 Mar 19;113(12):2816-25 PMID: 18941115
  29. Critical role of IL-15-IL-15R for antigen-presenting cell functions in the innate immune response.
    Nat Immunol. 2001 Dec;2(12):1138-43 PMID: 11702064
  30. Mast cells and basophils.
    Curr Opin Hematol. 2000 Jan;7(1):32-9 PMID: 10608502
  31. Basophils: a potential liaison between innate and adaptive immunity.
    Allergol Int. 2006 Jun;55(2):99-104 PMID: 17075245
  32. CD4pos, NK1.1pos T cells promptly produce interleukin 4 in response to in vivo challenge with anti-CD3.
    J Exp Med. 1994 Apr 1;179(4):1285-95 PMID: 7908323
  33. Basophils and type 2 immunity.
    Curr Opin Hematol. 2008 Jan;15(1):59-63 PMID: 18043247
  34. Regulation of mast-cell and basophil function and survival by IgE.
    Nat Rev Immunol. 2002 Oct;2(10):773-86 PMID: 12360215
  35. Anti-IgE antibody therapy for Japanese cedar pollinosis: omalizumab update.
    Allergol Int. 2008 Sep;57(3):205-9 PMID: 18724074
  36. The relationship between serum IgE and surface levels of FcepsilonR on human leukocytes in various diseases: correlation of expression with FcepsilonRI on basophils but not on monocytes or eosinophils.
    J Allergy Clin Immunol. 2000 Sep;106(3):514-20 PMID: 10984372
  37. Basophils enhance immunological memory responses.
    Nat Immunol. 2008 Jul;9(7):733-42 PMID: 18516038
  38. Interferon-gamma is a therapeutic target molecule for prevention of postoperative adhesion formation.
    Nat Med. 2008 Apr;14(4):437-41 PMID: 18345012
  39. Administration of IL-33 induces airway hyperresponsiveness and goblet cell hyperplasia in the lungs in the absence of adaptive immune system.
    Int Immunol. 2008 Jun;20(6):791-800 PMID: 18448455
  40. Entry of naive CD4 T cells into peripheral lymph nodes requires L-selectin.
    J Exp Med. 1994 Dec 1;180(6):2401-6 PMID: 7525854
  41. IgE regulates mouse basophil Fc epsilon RI expression in vivo.
    J Immunol. 1997 Mar 15;158(6):2517-21 PMID: 9058781
  42. Interleukin-18 regulates both Th1 and Th2 responses.
    Annu Rev Immunol. 2001;19:423-74 PMID: 11244043
  43. Increased numbers of both airway basophils and mast cells in sputum after allergen inhalation challenge of atopic asthmatics.
    Am J Respir Crit Care Med. 2000 May;161(5):1473-8 PMID: 10806141
  44. T1/ST2 is preferentially expressed on murine Th2 cells, independent of interleukin 4, interleukin 5, and interleukin 10, and important for Th2 effector function.
    Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6930-5 PMID: 9618516
  45. Identification of antigen-capturing cells as basophils.
    J Immunol. 2005 Jan 15;174(2):735-41 PMID: 15634893
  46. Acquisition of lymphokine-producing phenotype by CD4+ T cells.
    Annu Rev Immunol. 1994;12:635-73 PMID: 7912089
  47. Newly discovered roles for basophils: a neglected minority gains new respect.
    Nat Rev Immunol. 2009 Jan;9(1):9-13 PMID: 19039320
  48. A mechanism for the initiation of allergen-induced T helper type 2 responses.
    Nat Immunol. 2008 Mar;9(3):310-8 PMID: 18300366
  49. Anti-IgE for the treatment of allergic rhinitis--and eventually nasal polyps?
    Int Arch Allergy Immunol. 2009;148(2):87-98 PMID: 18799888
Article Info
Journal
Nature immunology
Abbr.
Nat Immunol
ISSN
1529-2916
Published
2009-07-00
Epub
2009-00-24
Pages
706-12
Language
English
Region
United States
NLM ID
100941354
Subset
IM
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