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PMID: 20067531 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Toll-like receptors--sentries in the B-cell response.

Immunology ·Vol. 128 ·No. 3 ·2009-11-00 ·Pages 311-23

Bekeredjian-Ding I, Jego G

Abstract

Toll-like receptors (TLR) play a central role in the initiation of the innate immune response to pathogens. Upon recognition of molecular motifs specific for microbial molecules TLR mediate pro-inflammatory cytokine secretion and enhance antigen presentation; in B cells they further promote expansion, class switch recombination and immunoglobulin secretion. As a result of their adjuvant properties, TLR ligands have become an integral component of antimicrobial vaccines. In spite of this, little is known of the direct effects of TLR engagement on B-lymphocyte function. The scope of this review is to outline the differences in TLR expression and reactivity in murine and human B-cell subsets and to provide an overview of the currently available literature. We will further discuss the possible roles of TLR in regulating B-cell effector functions and shaping antibody-mediated defence against microbial pathogens in vivo.

MeSH Terms
Animals Antibody Formation B-Lymphocytes/metabolism,pathology Host-Pathogen Interactions Humans Immunity, Innate Immunoglobulin Class Switching Immunomodulation Mice Toll-Like Receptors/genetics,immunology,metabolism
Chemicals
Toll-Like Receptors
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Bekeredjian-Ding Isabelle
Department of Medical Microbiology and Hygiene, University Hospital Heidelberg, Germany. bekeredjian-ding@uni-heidelberg.de
Jego Gaetan
References (132)
132 references, click to expand
  1. Induction of germ-line immunoglobulin heavy chain transcripts by mitogens and interleukins prior to switch recombination.
    Eur J Immunol. 1990 May;20(5):1079-84 PMID: 1972677
  2. Induction of IgG3 to LPS via Toll-like receptor 4 co-stimulation.
    PLoS One. 2008;3(10):e3509 PMID: 18946502
  3. Activation of autoreactive B cells by CpG dsDNA.
    Immunity. 2003 Dec;19(6):837-47 PMID: 14670301
  4. TLR9 stimulation drives naïve B cells to proliferate and to attain enhanced antigen presenting function.
    Eur J Immunol. 2007 Aug;37(8):2205-13 PMID: 17621369
  5. BCR-mediated uptake of antigen linked to TLR9 ligand stimulates B-cell proliferation and antigen-specific plasma cell formation.
    Blood. 2009 Apr 23;113(17):3969-77 PMID: 19144984
  6. Type I interferons protect neonates from acute inflammation through interleukin 10-producing B cells.
    J Exp Med. 2007 May 14;204(5):1107-18 PMID: 17485512
  7. TLR-9 activation of marginal zone B cells in lupus mice regulates immunity through increased IL-10 production.
    J Clin Immunol. 2005 Jan;25(1):29-40 PMID: 15742155
  8. B cells from p50/NF-kappa B knockout mice have selective defects in proliferation, differentiation, germ-line CH transcription, and Ig class switching.
    J Immunol. 1996 Jan 1;156(1):183-91 PMID: 8598461
  9. Vesicular stomatitis virus glycoprotein displaying retrovirus-like particles induce a type I IFN receptor-dependent switch to neutralizing IgG antibodies.
    J Immunol. 2007 May 1;178(9):5839-47 PMID: 17442968
  10. T-bet regulates T-independent IgG2a class switching.
    Int Immunol. 2003 Aug;15(8):937-44 PMID: 12882831
  11. Plasmacytoid dendritic cells control TLR7 sensitivity of naive B cells via type I IFN.
    J Immunol. 2005 Apr 1;174(7):4043-50 PMID: 15778362
  12. Antiinfective applications of toll-like receptor 9 agonists.
    Proc Am Thorac Soc. 2007 Jul;4(3):289-94 PMID: 17607015
  13. Superantigen- and TLR-dependent activation of tonsillar B cells after receptor-mediated endocytosis.
    J Immunol. 2009 Apr 15;182(8):4713-20 PMID: 19342647
  14. Signaling in transitional type 2 B cells is critical for peripheral B-cell development.
    Immunol Rev. 2004 Feb;197:161-78 PMID: 14962194
  15. Viral double-stranded RNA triggers Ig class switching by activating upper respiratory mucosa B cells through an innate TLR3 pathway involving BAFF.
    J Immunol. 2008 Jul 1;181(1):276-87 PMID: 18566393
  16. B cells lacking RelB are defective in proliferative responses, but undergo normal B cell maturation to Ig secretion and Ig class switching.
    J Exp Med. 1996 Oct 1;184(4):1537-41 PMID: 8879226
  17. CpG DNA induces IgG class switch DNA recombination by activating human B cells through an innate pathway that requires TLR9 and cooperates with IL-10.
    J Immunol. 2004 Oct 1;173(7):4479-91 PMID: 15383579
  18. TLR agonists selectively promote terminal plasma cell differentiation of B cell subsets specialized in thymus-independent responses.
    J Immunol. 2007 Jun 15;178(12):7779-86 PMID: 17548615
  19. MyD88 is required for the formation of long-term humoral immunity to virus infection.
    J Immunol. 2007 Apr 15;178(8):5124-31 PMID: 17404295
  20. TLR agonists promote marginal zone B cell activation and facilitate T-dependent IgM responses.
    J Immunol. 2008 Mar 15;180(6):3882-8 PMID: 18322196
  21. Human lupus autoantibody-DNA complexes activate DCs through cooperation of CD32 and TLR9.
    J Clin Invest. 2005 Feb;115(2):407-17 PMID: 15668740
  22. CpG oligonucleotides enhance proliferative and effector responses of B Cells in HIV-infected individuals.
    J Immunol. 2008 Jul 15;181(2):1199-206 PMID: 18606673
  23. Toll-like receptors.
    Annu Rev Immunol. 2003;21:335-76 PMID: 12524386
  24. CpG drives human transitional B cells to terminal differentiation and production of natural antibodies.
    J Immunol. 2008 Jan 15;180(2):800-8 PMID: 18178818
  25. T-bet regulates IgG class switching and pathogenic autoantibody production.
    Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5545-50 PMID: 11960012
  26. Role of TLR in B cell development: signaling through TLR4 promotes B cell maturation and is inhibited by TLR2.
    J Immunol. 2005 Jun 1;174(11):6639-47 PMID: 15905502
  27. The agonists of TLR4 and 9 are sufficient to activate memory B cells to differentiate into plasma cells in vitro but not in vivo.
    J Immunol. 2008 Aug 1;181(3):1746-52 PMID: 18641311
  28. IRAK4 kinase activity is redundant for interleukin-1 (IL-1) receptor-associated kinase phosphorylation and IL-1 responsiveness.
    J Biol Chem. 2004 Jun 18;279(25):26748-53 PMID: 15084582
  29. IL-12p70-dependent Th1 induction by human B cells requires combined activation with CD40 ligand and CpG DNA.
    J Immunol. 2004 Jan 15;172(2):954-63 PMID: 14707068
  30. Polyinosinic acid is a ligand for toll-like receptor 3.
    J Biol Chem. 2007 Aug 24;282(34):24759-66 PMID: 17573354
  31. Type I IFN as a natural adjuvant for a protective immune response: lessons from the influenza vaccine model.
    J Immunol. 2002 Jul 1;169(1):375-83 PMID: 12077267
  32. The p65 subunit of NF-kappa B is redundant with p50 during B cell proliferative responses, and is required for germline CH transcription and class switching to IgG3.
    J Immunol. 1999 Feb 15;162(4):1941-6 PMID: 9973462
  33. A distinct Toll-like receptor repertoire in human tonsillar B cells, directly activated by PamCSK, R-837 and CpG-2006 stimulation.
    Immunology. 2006 Aug;118(4):539-48 PMID: 16780564
  34. IL-10 interrupts memory B cell expansion in the germinal center by inducing differentiation into plasma cells.
    Eur J Immunol. 1998 Feb;28(2):508-15 PMID: 9521060
  35. Identification of two subpopulations of purified human blood B cells, CD27- CD23+ and CD27high CD80+, that strongly express cell surface Toll-like receptor 9 and secrete high levels of interleukin-6.
    Immunology. 2008 Nov;125(3):430-7 PMID: 18445007
  36. Regulation of B-cell entry into the cell cycle.
    Immunol Rev. 2008 Aug;224:183-200 PMID: 18759927
  37. Evidence for a large compartment of IgM-expressing memory B cells in humans.
    Blood. 1997 Feb 15;89(4):1288-98 PMID: 9028952
  38. Herpes simplex virus encephalitis in human UNC-93B deficiency.
    Science. 2006 Oct 13;314(5797):308-12 PMID: 16973841
  39. Pyogenic bacterial infections in humans with MyD88 deficiency.
    Science. 2008 Aug 1;321(5889):691-6 PMID: 18669862
  40. The toll-like receptor repertoire of human B lymphocytes: inducible and selective expression of TLR9 and TLR10 in normal and transformed cells.
    Blood. 2003 Aug 1;102(3):956-63 PMID: 12689944
  41. TLR accessory molecules.
    Curr Opin Immunol. 2008 Aug;20(4):420-5 PMID: 18625310
  42. Pathogen-associated molecular patterns are growth and survival factors for human myeloma cells through Toll-like receptors.
    Leukemia. 2006 Jun;20(6):1130-7 PMID: 16628189
  43. TLR signaling fine-tunes anti-influenza B cell responses without regulating effector T cell responses.
    J Immunol. 2007 Feb 15;178(4):2182-91 PMID: 17277123
  44. B cell receptor cross-talk: exposure to lipopolysaccharide induces an alternate pathway for B cell receptor-induced ERK phosphorylation and NF-kappa B activation.
    J Immunol. 2007 Jul 1;179(1):229-35 PMID: 17579042
  45. CpG DNA activation and plasma-cell differentiation of CD27- naive human B cells.
    Blood. 2007 Feb 15;109(4):1611-9 PMID: 17032927
  46. Toll-like receptors in systemic autoimmune disease.
    Nat Rev Immunol. 2006 Nov;6(11):823-35 PMID: 17063184
  47. TLR9 signaling in B cells determines class switch recombination to IgG2a.
    J Immunol. 2007 Feb 15;178(4):2415-20 PMID: 17277148
  48. Regulating B-cell activation and survival in response to TLR signals.
    Immunol Cell Biol. 2007 Aug-Sep;85(6):471-5 PMID: 17637697
  49. The B cell receptor governs the subcellular location of Toll-like receptor 9 leading to hyperresponses to DNA-containing antigens.
    Immunity. 2008 Jun;28(6):799-809 PMID: 18513998
  50. TLR9-activating DNA up-regulates ZAP70 via sustained PKB induction in IgM+ B cells.
    J Immunol. 2008 Dec 15;181(12):8267-77 PMID: 19050243
  51. Toll-like receptor stimulation as a third signal required for activation of human naive B cells.
    Eur J Immunol. 2006 Apr;36(4):810-6 PMID: 16541472
  52. BAFF costimulation of Toll-like receptor-activated B-1 cells.
    Eur J Immunol. 2006 Jul;36(7):1837-46 PMID: 16791880
  53. IL-4 induction of IgE class switching by lipopolysaccharide-activated murine B cells occurs predominantly through sequential switching.
    J Immunol. 1993 Jan 15;150(2):407-18 PMID: 8419474
  54. TLR-activated B cells suppress T cell-mediated autoimmunity.
    J Immunol. 2008 Apr 1;180(7):4763-73 PMID: 18354200
  55. Interleukin receptor-associated kinase (IRAK-4) deficiency associated with bacterial infections and failure to sustain antibody responses.
    J Pediatr. 2004 Apr;144(4):524-6 PMID: 15069404
  56. Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides.
    J Immunol. 2002 May 1;168(9):4531-7 PMID: 11970999
  57. Toll-like receptors mediate proliferation and survival of multiple myeloma cells.
    Leukemia. 2006 Jun;20(6):1138-44 PMID: 16617319
  58. Functional outcome of B cell activation by chromatin immune complex engagement of the B cell receptor and TLR9.
    J Immunol. 2007 Dec 1;179(11):7397-405 PMID: 18025183
  59. Staphylococcus aureus protein A triggers T cell-independent B cell proliferation by sensitizing B cells for TLR2 ligands.
    J Immunol. 2007 Mar 1;178(5):2803-12 PMID: 17312124
  60. UNC93B1 delivers nucleotide-sensing toll-like receptors to endolysosomes.
    Nature. 2008 Mar 13;452(7184):234-8 PMID: 18305481
  61. Toll-like receptor expression and responsiveness of distinct murine splenic and mucosal B-cell subsets.
    PLoS One. 2007 Sep 12;2(9):e863 PMID: 17848994
  62. Toll-like receptor 9 can be expressed at the cell surface of distinct populations of tonsils and human peripheral blood mononuclear cells.
    Infect Immun. 2004 Dec;72(12):7202-11 PMID: 15557645
  63. Role of phosphoinositide 3-kinase p110 delta in TLR4- and TLR9-mediated B cell cytokine production and differentiation.
    Mol Immunol. 2009 Jun;46(10):1970-8 PMID: 19362372
  64. Toll-like receptor 2-mediated human B cell differentiation.
    Clin Immunol. 2006 Sep;120(3):272-84 PMID: 16766226
  65. Enhanced B-cell activation mediated by TLR4 and BCR crosstalk.
    Eur J Immunol. 2008 Sep;38(9):2475-87 PMID: 18819072
  66. The mucosal adjuvant macrophage-activating lipopeptide-2 directly stimulates B lymphocytes via the TLR2 without the need of accessory cells.
    J Immunol. 2005 May 15;174(10):6308-13 PMID: 15879130
  67. Toll-like receptor 2 is required for innate, but not acquired, host defense to Borrelia burgdorferi.
    J Immunol. 2002 Jan 1;168(1):348-55 PMID: 11751980
  68. The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via Toll-like receptors 3, 7 and 9.
    Nat Immunol. 2006 Feb;7(2):156-64 PMID: 16415873
  69. Mitogen- and IL-4-regulated expression of germ-line Ig gamma 2b transcripts: evidence for directed heavy chain class switching.
    Cell. 1988 Apr 22;53(2):177-84 PMID: 2834063
  70. TLR-mediated stimulation of APC: Distinct cytokine responses of B cells and dendritic cells.
    Eur J Immunol. 2007 Nov;37(11):3040-53 PMID: 17918201
  71. Regulation and functions of Blimp-1 in T and B lymphocytes.
    Annu Rev Immunol. 2008;26:133-69 PMID: 18370921
  72. NF-kappa B RelA-deficient lymphocytes: normal development of T cells and B cells, impaired production of IgA and IgG1 and reduced proliferative responses.
    J Exp Med. 1997 Mar 3;185(5):953-61 PMID: 9120401
  73. Myeloid differentiation antigen 88 deficiency impairs pathogen clearance but does not alter inflammation in Borrelia burgdorferi-infected mice.
    Infect Immun. 2004 Jun;72(6):3195-203 PMID: 15155621
  74. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6.
    Immunity. 2003 Aug;19(2):225-34 PMID: 12932356
  75. Resident enteric microbiota and CD8+ T cells shape the abundance of marginal zone B cells.
    Eur J Immunol. 2008 Dec;38(12):3411-25 PMID: 19009526
  76. Toll-like receptors control activation of adaptive immune responses.
    Nat Immunol. 2001 Oct;2(10):947-50 PMID: 11547333
  77. Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelial-cell secretion of the cytokine APRIL.
    Immunity. 2007 Jun;26(6):812-26 PMID: 17570691
  78. Plasmacytoid dendritic cells, antigen, and CpG-C license human B cells for plasma cell differentiation and immunoglobulin production in the absence of T-cell help.
    Blood. 2004 Apr 15;103(8):3058-64 PMID: 15070685
  79. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE.
    Nat Immunol. 2007 May;8(5):487-96 PMID: 17417641
  80. Type I IFN receptor signals directly stimulate local B cells early following influenza virus infection.
    J Immunol. 2006 Apr 1;176(7):4343-51 PMID: 16547272
  81. IRAK-4- and MyD88-dependent pathways are essential for the removal of developing autoreactive B cells in humans.
    Immunity. 2008 Nov 14;29(5):746-57 PMID: 19006693
  82. Inherited disorders of human Toll-like receptor signaling: immunological implications.
    Immunol Rev. 2005 Feb;203:10-20 PMID: 15661018
  83. Comparison of human B cell activation by TLR7 and TLR9 agonists.
    BMC Immunol. 2008 Jul 24;9:39 PMID: 18652679
  84. Human blood IgM "memory" B cells are circulating splenic marginal zone B cells harboring a prediversified immunoglobulin repertoire.
    Blood. 2004 Dec 1;104(12):3647-54 PMID: 15191950
  85. Toll-like receptor 9-dependent and -independent dendritic cell activation by chromatin-immunoglobulin G complexes.
    J Exp Med. 2004 Jun 21;199(12):1631-40 PMID: 15197227
  86. Induction of secretory immunity and memory at mucosal surfaces.
    Vaccine. 2007 Jul 26;25(30):5467-84 PMID: 17227687
  87. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors.
    Nature. 2002 Apr 11;416(6881):603-7 PMID: 11948342
  88. A role for Toll-like receptors in acquired immunity: up-regulation of TLR9 by BCR triggering in naive B cells and constitutive expression in memory B cells.
    Blood. 2003 Jun 1;101(11):4500-4 PMID: 12560217
  89. TLR9/MyD88 signaling is required for class switching to pathogenic IgG2a and 2b autoantibodies in SLE.
    J Exp Med. 2006 Mar 20;203(3):553-61 PMID: 16492804
  90. Toll-like receptors: lessons to learn from normal and malignant human B cells.
    Blood. 2008 Sep 15;112(6):2205-13 PMID: 18591383
  91. Expression of toll-like receptors on B lymphocytes.
    Cell Immunol. 2005 Jul-Aug;236(1-2):140-5 PMID: 16188245
  92. CD36 is differentially expressed on B cell subsets during development and in responses to antigen.
    J Immunol. 2008 Jan 1;180(1):230-7 PMID: 18097024
  93. Transcription factor Mef2c is required for B cell proliferation and survival after antigen receptor stimulation.
    Nat Immunol. 2008 Jun;9(6):603-12 PMID: 18438409
  94. Toll-like receptor 7-induced naive human B-cell differentiation and immunoglobulin production.
    J Allergy Clin Immunol. 2009 Jan;123(1):224-230.e4 PMID: 18995892
  95. Bruton's tyrosine kinase is required for TLR-induced IL-10 production.
    J Immunol. 2006 Nov 15;177(10):7203-10 PMID: 17082638
  96. B cell intrinsic TLR signals amplify but are not required for humoral immunity.
    J Exp Med. 2007 Dec 24;204(13):3095-101 PMID: 18039950
  97. Endogenous pro- and anti-inflammatory cytokines differentially regulate an in vivo humoral response to Streptococcus pneumoniae.
    Infect Immun. 2002 Feb;70(2):749-61 PMID: 11796608
  98. Antiviral defense in mice lacking both alpha/beta and gamma interferon receptors.
    J Virol. 1995 Aug;69(8):4792-6 PMID: 7609046
  99. MyD88- and Bruton's tyrosine kinase-mediated signals are essential for T cell-independent pathogen-specific IgM responses.
    J Immunol. 2007 Mar 15;178(6):3740-9 PMID: 17339472
  100. The perfect mix: recent progress in adjuvant research.
    Nat Rev Microbiol. 2007 Jul;5(7):505-17 PMID: 17558426
  101. High levels of susceptibility and T helper 2 response in MyD88-deficient mice infected with Leishmania major are interleukin-4 dependent.
    Infect Immun. 2003 Dec;71(12):7215-8 PMID: 14638820
  102. Induction of interferon-alpha production in plasmacytoid dendritic cells by immune complexes containing nucleic acid released by necrotic or late apoptotic cells and lupus IgG.
    Arthritis Rheum. 2004 Jun;50(6):1861-72 PMID: 15188363
  103. Human splenic marginal zone B cells lack expression of activation-induced cytidine deaminase.
    Eur J Immunol. 2005 Oct;35(10):3002-7 PMID: 16180254
  104. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement.
    J Exp Med. 2005 Nov 7;202(9):1171-7 PMID: 16260486
  105. T-independent activation-induced cytidine deaminase expression, class-switch recombination, and antibody production by immature/transitional 1 B cells.
    J Immunol. 2007 Mar 15;178(6):3593-601 PMID: 17339456
  106. Both innate immunity and type 1 humoral immunity to Streptococcus pneumoniae are mediated by MyD88 but differ in their relative levels of dependence on toll-like receptor 2.
    Infect Immun. 2005 Jan;73(1):298-307 PMID: 15618166
  107. Control of B-cell responses by Toll-like receptors.
    Nature. 2005 Nov 17;438(7066):364-8 PMID: 16292312
  108. Evidence that marginal zone B cells possess an enhanced secretory apparatus and exhibit superior secretory activity.
    J Immunol. 2006 Sep 15;177(6):3791-8 PMID: 16951340
  109. Different kinetics of blimp-1 induction in B cell subsets revealed by reporter gene.
    J Immunol. 2007 Apr 1;178(7):4104-11 PMID: 17371965
  110. CpG inhibits IgE class switch recombination through suppression of NF kappa B activity, but not through Id2 or Bcl6.
    Biochem Biophys Res Commun. 2005 Mar 11;328(2):499-506 PMID: 15694375
  111. Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells.
    Immunity. 2003 Oct;19(4):607-20 PMID: 14563324
  112. Upon TLR9 signaling, CD5+ B cells control the IL-12-dependent Th1-priming capacity of neonatal DCs.
    Immunity. 2005 Apr;22(4):467-77 PMID: 15845451
  113. Immunology: Toll-like receptors and antibody responses.
    Nature. 2006 May 18;441(7091):E4; discussion E4 PMID: 16710369
  114. Defective Toll-like receptor 9-mediated cytokine production in B cells from Bruton's tyrosine kinase-deficient mice.
    Immunology. 2008 Feb;123(2):239-49 PMID: 17725607
  115. Resistance to and recovery from lethal influenza virus infection in B lymphocyte-deficient mice.
    J Exp Med. 1997 Dec 15;186(12):2063-8 PMID: 9396777
  116. Bruton's tyrosine kinase separately regulates NFkappaB p65RelA activation and cytokine interleukin (IL)-10/IL-12 production in TLR9-stimulated B Cells.
    J Biol Chem. 2008 Apr 25;283(17):11189-98 PMID: 18276597
  117. Immune complexes present in the sera of autoimmune mice activate rheumatoid factor B cells.
    J Immunol. 2000 Aug 1;165(3):1626-33 PMID: 10903773
  118. Staphylococcus aureus-induced plasmacytoid dendritic cell activation is based on an IgG-mediated memory response.
    J Immunol. 2008 Sep 15;181(6):3823-33 PMID: 18768836
  119. A new population of cells lacking expression of CD27 represents a notable component of the B cell memory compartment in systemic lupus erythematosus.
    J Immunol. 2007 May 15;178(10):6624-33 PMID: 17475894
  120. Human TLR10 is a functional receptor, expressed by B cells and plasmacytoid dendritic cells, which activates gene transcription through MyD88.
    J Immunol. 2005 Mar 1;174(5):2942-50 PMID: 15728506
  121. Adjuvant-enhanced antibody responses in the absence of toll-like receptor signaling.
    Science. 2006 Dec 22;314(5807):1936-8 PMID: 17185603
  122. Lymphocyte-specific TRAF3 transgenic mice have enhanced humoral responses and develop plasmacytosis, autoimmunity, inflammation, and cancer.
    Blood. 2009 May 7;113(19):4595-603 PMID: 19074733
  123. B cells genetically deficient in the c-Rel transactivation domain have selective defects in germline CH transcription and Ig class switching.
    J Immunol. 1997 Oct 1;159(7):3133-9 PMID: 9317110
  124. Endocytic sequestration of the B cell antigen receptor and toll-like receptor 9 in anergic cells.
    Proc Natl Acad Sci U S A. 2009 Apr 14;106(15):6262-7 PMID: 19332776
  125. CpG DNA redirects class-switching towards "Th1-like" Ig isotype production via TLR9 and MyD88.
    Eur J Immunol. 2004 May;34(5):1483-7 PMID: 15114682
  126. Regulation of terminal differentiation of human B-cells by IL-6.
    Curr Top Microbiol Immunol. 1995;194:189-98 PMID: 7895492
  127. Selective predisposition to bacterial infections in IRAK-4-deficient children: IRAK-4-dependent TLRs are otherwise redundant in protective immunity.
    J Exp Med. 2007 Oct 1;204(10):2407-22 PMID: 17893200
  128. IRAK4 and NEMO mutations in otherwise healthy children with recurrent invasive pneumococcal disease.
    J Med Genet. 2007 Jan;44(1):16-23 PMID: 16950813
  129. TLR signaling.
    Semin Immunol. 2007 Feb;19(1):24-32 PMID: 17275323
  130. CpG directly induces T-bet expression and inhibits IgG1 and IgE switching in B cells.
    Nat Immunol. 2003 Jul;4(7):687-93 PMID: 12766768
  131. Role of IgM antibodies versus B cells in influenza virus-specific immunity.
    Eur J Immunol. 2002 Aug;32(8):2229-36 PMID: 12209635
  132. Translating innate immunity into immunological memory: implications for vaccine development.
    Cell. 2006 Feb 24;124(4):849-63 PMID: 16497593
Article Info
Journal
Immunology
Abbr.
Immunology
ISSN
1365-2567
DOI
10.1111/j.1365-2567.2009.03173.x
Email
bekeredjian-ding@uni-heidelberg.de
Published
2009-11-00
Pages
311-23
Language
English
Region
England
NLM ID
0374672
PMCID
PMC2770679
Subset
IM
External Links
PubMed source DOI: 10.1111/j.1365-2567.2009.03173.x PMC Full Text View journal details
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