Abstract
Although innate signals driven by Toll-like receptors (TLRs) play a crucial role in T-dependent immune responses and serological memory, the precise cellular and time-dependent requirements for such signals remain poorly defined. To directly address the role for B cell-intrinsic TLR signals in these events, we compared the TLR response profile of germinal center (GC) versus naive mature B cell subsets. TLR responsiveness was markedly up-regulated during the GC reaction, and this change correlated with altered expression of the key adaptors MyD88, Mal, and IRAK-M. To assess the role for B cell-intrinsic signals in vivo, we transferred MyD88 wild-type or knockout B cells into B cell-deficient microMT mice and immunized recipient animals with 4-hydroxy-3-nitrophenylacetyl (NP) chicken gamma globulin. All recipients exhibited similar increases in NP-specific antibody titers during primary, secondary, and long-term memory responses. The addition of lipopolysaccharide to the immunogen enhanced B cell-intrinsic, MyD88-dependent NP-specific immunoglobulin (Ig)M production, whereas NP-specific IgG increased independently of TLR signaling in B cells. Our data demonstrate that B cell-intrinsic TLR responses are up-regulated during the GC reaction, and that this change significantly promotes antigen-specific IgM production in association with TLR ligands. However, B cell-intrinsic TLR signals are not required for antibody production or maintenance.
MeSH Terms
Animals
Antibody Formation
B-Lymphocytes/metabolism
Cell Proliferation
Humans
Immune System
Leukosialin/biosynthesis
Mice
Mice, Inbred C57BL
Mice, Knockout
Myeloid Differentiation Factor 88/metabolism
Signal Transduction
Spleen/cytology,metabolism
T-Lymphocytes/metabolism
Toll-Like Receptors/metabolism
Chemicals
Leukosialin
Myd88 protein, mouse
Myeloid Differentiation Factor 88
Toll-Like Receptors
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Meyer-Bahlburg Almut
Seattle Children's Hospital Research Institute, Seattle, WA 98101, USA.
Khim Socheath
Rawlings David J
References (30)
30 references, click to expand
-
Mycobacterium tuberculosis lipoarabinomannan-mediated IRAK-M induction negatively regulates Toll-like receptor-dependent interleukin-12 p40 production in macrophages.
J Biol Chem. 2005 Dec 30;280(52):42794-800
PMID: 16263713
-
Intravenous polyclonal IgM-enriched immunoglobulin therapy in sepsis: a review of clinical efficacy in relation to microbiological aetiology and severity of sepsis.
J Intern Med. 2006 Dec;260(6):509-16
PMID: 17116001
-
Toll-like receptors: critical proteins linking innate and acquired immunity.
Nat Immunol. 2001 Aug;2(8):675-80
PMID: 11477402
-
Innate and acquired humoral immunities to influenza virus are mediated by distinct arms of the immune system.
Proc Natl Acad Sci U S A. 1999 Mar 2;96(5):2250-5
PMID: 10051627
-
Memory B-cell persistence is independent of persisting immunizing antigen.
Nature. 2000 Oct 5;407(6804):636-42
PMID: 11034213
-
Toll-like receptor control of the adaptive immune responses.
Nat Immunol. 2004 Oct;5(10):987-95
PMID: 15454922
-
Nitric oxide activates the expression of IRAK-M via the release of TNF-alpha in human monocytes.
Nitric Oxide. 2004 Jun;10(4):213-20
PMID: 15275867
-
Humoral immunity due to long-lived plasma cells.
Immunity. 1998 Mar;8(3):363-72
PMID: 9529153
-
Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens.
Immunity. 2001 May;14(5):617-29
PMID: 11371363
-
Requirement for MD-1 in cell surface expression of RP105/CD180 and B-cell responsiveness to lipopolysaccharide.
Blood. 2002 Mar 1;99(5):1699-705
PMID: 11861286
-
Unresponsiveness of MyD88-deficient mice to endotoxin.
Immunity. 1999 Jul;11(1):115-22
PMID: 10435584
-
TLR9 signaling in B cells determines class switch recombination to IgG2a.
J Immunol. 2007 Feb 15;178(4):2415-20
PMID: 17277148
-
Maintenance of serological memory by polyclonal activation of human memory B cells.
Science. 2002 Dec 13;298(5601):2199-202
PMID: 12481138
-
Endotoxin can induce MyD88-deficient dendritic cells to support T(h)2 cell differentiation.
Int Immunol. 2002 Jul;14(7):695-700
PMID: 12096028
-
IRAK-M is a negative regulator of Toll-like receptor signaling.
Cell. 2002 Jul 26;110(2):191-202
PMID: 12150927
-
A critical role of natural immunoglobulin M in immediate defense against systemic bacterial infection.
J Exp Med. 1998 Dec 21;188(12):2381-6
PMID: 9858525
-
Toll-like receptors control activation of adaptive immune responses.
Nat Immunol. 2001 Oct;2(10):947-50
PMID: 11547333
-
A new mathematical model for relative quantification in real-time RT-PCR.
Nucleic Acids Res. 2001 May 1;29(9):e45
PMID: 11328886
-
A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene.
Nature. 1991 Apr 4;350(6317):423-6
PMID: 1901381
-
Antiviral antibody responses: the two extremes of a wide spectrum.
Nat Rev Immunol. 2006 Mar;6(3):231-43
PMID: 16498452
-
B cells move to centre stage: novel opportunities for autoimmune disease treatment.
Nat Rev Drug Discov. 2006 Jul;5(7):564-76
PMID: 16816838
-
Identification of murine germinal center B cell subsets defined by the expression of surface isotypes and differentiation antigens.
J Immunol. 2000 Jun 1;164(11):5729-38
PMID: 10820250
-
IRAK-M is a novel member of the Pelle/interleukin-1 receptor-associated kinase (IRAK) family.
J Biol Chem. 1999 Jul 2;274(27):19403-10
PMID: 10383454
-
Maintenance of serum antibody levels.
Annu Rev Immunol. 2005;23:367-86
PMID: 15771575
-
Autoreactivity by design: innate B and T lymphocytes.
Nat Rev Immunol. 2001 Dec;1(3):177-86
PMID: 11905826
-
Control of B-cell responses by Toll-like receptors.
Nature. 2005 Nov 17;438(7066):364-8
PMID: 16292312
-
Pyogenic bacterial infections in humans with IRAK-4 deficiency.
Science. 2003 Mar 28;299(5615):2076-9
PMID: 12637671
-
Immunology: Toll-like receptors and antibody responses.
Nature. 2006 May 18;441(7091):E4; discussion E4
PMID: 16710369
-
TLR signaling.
Cell Death Differ. 2006 May;13(5):816-25
PMID: 16410796
-
Up-regulation of MyD88s and SIGIRR, molecules inhibiting Toll-like receptor signaling, in monocytes from septic patients.
Crit Care Med. 2006 Sep;34(9):2377-85
PMID: 16850005