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Department of Host Defense, Research Institute for Microbial Diseases, Osaka University, Osaka, Japan; and Core Research for Evolutional Science and Technology, Japan Science and Technology Corporation, Osaka, Japan
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResultsDiscussionReferences |
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B and
mitogen-activated protein kinase cascades, although the biological
significance of this activation is not clear. In this study, we have
examined the effects of LPS on dendritic cells (DCs) from wild-type and
several mutant mice. LPS-induced cytokine production from DCs was
dependent on MyD88. However, LPS could induce functional maturation of
MyD88-deficient DCs, including up-regulation of costimulatory molecules
and enhancement of APC activity. MyD88-deficient DCs could not maturate
in response to bacterial DNA, the ligand for Toll-like receptor (TLR)9,
indicating that MyD88 is differentially required for TLR family
signaling. MyD88-dependent and -independent pathways originate at the
intracytoplasmic region of TLR4, because both cytokine induction and
functional maturation were abolished in DCs from C3H/HeJ mice carrying
the point mutation in the region. Finally, in vivo analysis revealed
that MyD88-, but not TLR4-, deficient splenic CD11c+ DCs
could up-regulate their costimulatory molecule expression in response
to LPS. Collectively, the present study provides the first evidence
that the MyD88-independent pathway downstrem of TLR4 can lead to
functional DC maturation, which is critical for a link between innate
and adaptive immunity. |
Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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B and mitogen-activated protein kinase (MAPK) cascades in
response to LPS (16). It remains unclear at present
whether the activation is biologically significant. In addition to macrophages, dendritic cells (DCs) with highly potent APC activity function as critical sentinels in antimicrobial immune responses (18, 19). Exposure to microbial components such as LPS can induce DC maturation characterized by cytokine production, up-regulation of costimulatory molecules, and an increased ability to activate T cells (20, 21, 22). Together with macrophage activation, the DC maturation is critical for a link between innate and adaptive immunity.
In this study, we have investigated the effects of LPS on DCs from wild-type and several mutant mice. MyD88-deficient DCs can respond to LPS in terms of up-regulation of costimulatory molecule expression and enhanced Ag-presenting activity. Our study for the first time demonstrates that the MyD88-independent pathway through TLR4 can lead to the innate immune response, i.e., DC maturation.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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C57BL/6, BALB/c, C3H/HeN, and C3H/HeJ mice were purchased from Japan SLC (Shizuoka, Japan). TLR4- and MyD88-deficient mice were established as described previously (8). The BALB/c-background DO11.10 TCR-transgenic mice (23), which recognize the 323–339 peptide of chicken OVA in the context of I-Ad, were kindly provided by Dr. K. M. Murphy. MyD88-deficient mice with a BALB/c background were obtained by backcrossing them to BALB/c mice for five to six generations.
Reagents
LPS derived from Escherichia coli O55:B5 was purchased from Sigma (St. Louis, MO) (16). Synthetic E. coli-type lipid A (compound 506) was purchased from Dai-ichi Pure Chemicals (Tokyo, Japan) (16). Phosphorothioate-stabilized oligodeoxynucleotides containing unmethylated CpG motifs were purchased from TIB MOLBIOL (Berlin, Germany) (24).
Bone marrow (BM) DC culture
BM cells from femurs and tibias were plated at 1 x 106 cells/ml in 24-well plates with 10% FCS-RPMI 1640 supplemented with 10 ng/ml murine GM-CSF (PeproTech, London, U.K.) as described previously (25). At day 6, loosely adherent cells were harvested by gentle pipeting, plated at 5 x 105 cells/ml in 24-well plates, and cultured with or without 100 ng/ml LPS, 1 µg/ml synthetic lipid A, or 0.1 µM CpG DNA in a fresh medium for 2 more days.
ELISA
At day 8 of the DC culture, cell supernatants were harvested for
measuring TNF-
and IL-12 p40 production by ELISA kits (Genzyme,
Minneapolis, MN).
Flow cytometry
DCs were incubated with anti-CD16/32 (2.4G2; BD PharMingen, San Diego, CA) to minimize nonspecific staining. They were then stained with biotinylated mAbs for 20 min at 4°C and developed with streptavidine-PE (BD PharMingen). The following biotinylated mAbs were also purchased from BD PharMingen: CD3 (145-2C11), CD11c (HL3), CD40 (3/23), CD80 (16-10A1), and CD86 (GL1). Flow cytometric analysis was performed using a FACSCalibur (BD Biosciences, Mountain View, CA) with CellQuest software (BD Biosciences).
MLR assay
Unstimulated or stimulated BM DCs were harvested at day 8, washed, irradiated at a dose of 30 Gy, and plated at 3-fold serial dilutions in 96-well round-bottom plates. These stimulator DCs were incubated for 3 days with 5 x 104/well of splenic CD4+ T cells, which were isolated by using MACS with CD4 microbeads (Miltenyi Biotec, Bergisch Gladbach, Germany). The resulting population of CD4+ T cells after MACS was >95% positive for CD4, as determined by flow cytometry. [3H]Thymidine was added for the last 15 h.
Ag presentation assay
Unstimulated or LPS-stimulated BM DCs were generated from wild-type BALB/c or MyD88-deficient mice with a BALB/c background. The DCs at day 8 were irradiated and cocultured with CD4+ T cells from DO11.10 TCR-transgenic mice (23) in the presence of 1 µM of chicken OVA peptide (residues 323–339) for 3 days. [3H]Thymidine was added for the last 15 h.
In vitro kinase assay and EMSA
At day 6 of the DC culture, harvested cells were stimulated with 100 ng/ml LPS for indicated periods, lysed, and immunoprecipitated with anti-IL-1R-associated kinase (IRAK) Ab or rabbit anti-c-Jun N-terminal kinase (JNK)1 Ab (Santa Cruz Biotechnology, Santa Cruz, CA). The in vitro kinase assay and EMSA were performed as described previously (16).
LPS injection and splenic DC analysis
LPS (200 ng/head) derived from E. coli O55:B5 was i.v. injected into wild-type, TLR4-deficient, and MyD88-deficient mice. Control mice were injected with PBS. Six hours later, spleens were dissected and incubated with RPMI 1640 medium containing 400 U/ml collagenase (Wako, Osaka, Japan) and 15 µg/ml DNase I (Sigma) for 20 min at 37°C. For the last 5 min of the incubation period, 5 mM EDTA was added. Single-cell suspensions were prepared and stained with biotinylated anti-CD11c followed by streptavidin-PE and FITC-conjugated anti-CD40 or anti-CD86 (BD PharMingen). Stained cells were subjected to flow cytometric analysis.
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Results |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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To assess the effects of LPS on DCs, immature DCs were generated
in vitro by culturing BM cells with GM-CSF. First, we measured
proinflammatory cytokine production in response to LPS. When wild-type
immature BM DCs were stimulated with LPS, they produced more amounts of
TNF- and IL-12 p40 than those without LPS (Fig. 1
). Meanwhile, the cytokine induction was
abolished in TLR4- or MyD88-deficient BM DCs. The results suggest that
LPS stimulates cytokine production in BM DCs through TLR4 in a
MyD88-dependent manner.
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Next, we analyzed surface expression of costimulatory molecules on
LPS-stimulated and unstimulated BM DCs. LPS could enhance surface
expression of CD40, CD80, and CD86 in wild-type BM DCs (Fig. 2). Meanwhile, CD11c expression was
significantly decreased in response to LPS. This phenotype typically
represents DC maturation (21). TLR4-deficient BM DCs
showed no modulation of these surface molecules in response to LPS.
However, upon LPS stimulation, MyD88-deficient DCs showed up-regulation
of CD40, CD80, and CD86 and down-regulation of CD11c (Fig. 2). These
results clearly indicate that LPS-induced DC maturation is dependent on
TLR4 but can proceed in the absence of MyD88.
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A). Similarly, the
allostimulatory activity of MyD88-deficient BM DCs was also enhanced
with LPS stimulation. However, LPS did not enhance the ability of
TLR4-deficient BM DCs to stimulate allogeneic T cells. Next, we
investigated whether LPS could enhance APC activity of BM DCs. BM DCs
from wild-type or MyD88-deficient mice were irradiated and cocultured
with CD4+ T cells from cOVA-specific
TCR-transgenic mice (23) in the presence of cOVA peptide.
Both wild-type and MyD88-deficient BM DCs without LPS stimulation could
augment cOVA-specific T cell proliferation in a DC number-dependent
manner (Fig. 3B, 
). When stimulated with LPS, both BM DCs
showed enhanced ability to stimulate T cell proliferation (Fig. 3B, •). Taken together, LPS could not only modulate
costimulatory molecule expression but also enhance the T cell
stimulatory activity of MyD88-deficient BM DCs.
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A, lipid
A-induced cytokine production was dependent on MyD88. However, lipid A
could significantly enhance not only CD40 expression but also
allostimulatory activity of MyD88-deficient BM DCs (Fig. 4, B and C). All of these effects were dependent on
TLR4, because lipid A showed no effects on TLR4-deficient BM
DCs.
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Bacteria-derived DNA containing CpG motifs can also induce
cytokine production and DC maturation through another TLR family
member, TLR9 (24). CpG DNA-induced cytokine induction from
macrophages and DCs is dependent on MyD88 (26, 27).
Therefore, we tested the effects of CpG DNA on wild-type and
MyD88-deficient DCs. CpG DNA could induce cytokine production, surface
expression of costimulatory molecules such as CD40, CD80, and CD86, and
allostimulatory activity of wild-type DCs (Fig. 5 and data not shown). However, all of
these effects were abolished in not only TLR9-deficient
(24) but also in MyD88-deficient DCs (Fig. 5). The results
clearly suggest that TLR9-mediated signaling can induce DC maturation
in a MyD88-dependent manner.
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Mice of the C3H/HeJ strain show defective responses to LPS and
were found to carry the point mutation in the Tlr4 gene
locus, which results in the replacement of a conserved proline residue
with a histidine residue in the cytoplasmic region of TLR4 (6, 7). This point mutation is responsible for diminished responses
to LPS (8). We have investigated whether C3H/HeJ DCs can
mature in response to LPS. LPS-induced cytokine production was severely
impaired in C3H/HeJ DCs as in TLR4- and MyD88-deficient DCs (Fig. 1
and 6A). Unlike MyD88-deficient
DCs, C3H/HeJ DCs did not show either up-regulation of CD40, CD80, and
CD86, nor down-regulation of CD11c in response to LPS (Fig. 6B and data not shown). C3H/HeJ DCs also showed severe
impairment of LPS-induced allostimulatory activity (Fig. 6C). Taken together, LPS could induce neither cytokine
induction nor DC maturation in C3H/HeJ DCs.
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We next examined the LPS signaling pathways of wild-type and
mutant DCs. MyD88 interacts with TLR4 through a TIR domain and recruits
IRAK to the receptor complex through a death domain, and then IRAK is
sequentially activated (14, 15). LPS could not induce IRAK
activation in either TLR4- or MyD88-deficient DCs, indicating that
MyD88 is essential for LPS-induced IRAK activation (Fig. 7A). Activated IRAK
subsequently activates NF-B via TNFR-associated factor (TRAF)6
(14, 15). Next, LPS-induced NF-B activation in DCs was
examined by EMSA (Fig. 7B). NF-B DNA binding activity was
detected in wild-type DC nuclear extracts at 10 min after LPS
stimulation and gradually increased thereafter (Fig. 7B).
This NF-B activation is dependent on TLR4, because it was not
observed in TLR4-deficient DCs. NF-B activation was detected at 60
min after LPS stimulation in MyD88-deficient DCs in a similar level to
that observed in wild-type DCs. However, kinetics of NF-B activation
showed delayed induction in MyD88-deficient DCs as compared with that
in wildtype DCs. Furthermore, LPS-induced JNK activation, which is
dependent on TLR4, was also detected in MyD88-deficient DCs with
delayed kinetics (Fig. 7C). Meanwhile, LPS-induced
activation of IRAK, NF-B, and JNK was abolished in both
TLR4-deficient and C3H/HeJ DCs (Fig. 7). The results show a close
correlation of NF-B and JNK activation with DC maturation in
response to LPS and strongly suggest that residual biochemical
responses in MyD88-deficient DCs are involved in LPS-induced DC
maturation.
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We next investigated in vivo effects of LPS on splenic DCs from
wild-type and mutant mice. Intravenous injection of LPS can induce
up-regulation of costimulatory molecule expression on splenic DCs
(28). Splenic CD11c+ cells from
LPS-injected wild-type mice showed increased expression of CD40 and
CD86 compared with those from PBS-injected wild-type mice (Fig. 8A). LPS-induced up-regulation
of costimulatory molecules was abolished in TLR4-deficient mice (Fig. 8B). However, in MyD88-deficient mice, splenic DCs
significantly increased their surface expression levels of CD40 and
CD86 in response to LPS injection (Fig. 8C). Serum IL-12 p40
levels reached 718 ± 27 pg/ml in LPS-injected wild-type mice,
whereas levels were <10 pg/ml not only in PBS-injected wild-type mice,
but also in LPS-injected TLR4- and MyD88-deficient mice. Thus, these in
vivo experiments clearly indicate that LPS can induce up-regulation of
costimulatory molecules on splenic DCs in a TLR4-dependent and
MyD88-independent manner.
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Expression levels of costimulatory molecules and T cell activating
ability on LPS-stimulated MyD88-deficient DCs were not as high as those
observed on LPS-stimulated wild-type DCs (Figs. 2 and 3). However,
different from no responses to LPS in TLR4-deficient as well as C3H/HeJ
DCs, MyD88-deficient DCs consistently showed significant enhancement of
these activities in response to LPS (Figs. 2, 3, and 6). In
contrast, LPS could not stimulate production from MyD88-deficient BM
DCs, which is consistent with our previous study about MyD88-deficient
macrophages (16). Like MyD88-deficient macrophages, both NF-B and
JNK were activated with delayed kinetics in MyD88-deficient BM DCs,
although IRAK activation was abolished.
Commercial preparations of LPS are often contaminated with some TLR2
agonist (30). However, it is unlikely that some
contaminants contribute to MyD88-independent DC maturation. First, we
used LPS derived from E. coli serotype O55:B5, which is
phenol-extracted and then chromatographically purified by gel
filtration (16). The effects of this LPS on
MyD88-deficient BM DCs were completely abolished by addition of
polymyxin B (data not shown). Furthermore, we have also used synthetic
E. coli-type lipid A (compound 506) in our culture system.
The lipid A could induce CD40 up-regulation and enhancement of
allostimulatory activity on both wild-type and MyD88-deficient BM DCs
(Fig. 4). Therefore, we can exclude the possibility that LPS-induced
maturation is due to some contaminants in the LPS preparation. It is
also noteworthy that, in contrast to TLR4 signaling, TLR2 signaling can
induce activation of NF-B and MAPK cascades in a MyD88-dependent
manner (31). Together with the fact that DC maturation
observed in this study is dependent on TLR4, these results clearly
indicate that the MyD88-independent pathway is located downstream
of TLR4.
Neither TLR4-deficient nor C3H/HeJ DCs showed any responses to LPS.
This indicates that the conserved proline residue in the cytoplasmic
region of TLR4 is essential for both cytokine induction and DC
maturation signals and that LPS-induced, MyD88-dependent and
independent pathways originate at the TLR4 cytoplasmic region. Because
IRAK activation is dependent on MyD88 (16 and Fig. 7A), it is integrated in the MyD88-dependent pathway. In
this context, it should be noted that LPS can induce activation of
NF-B and MAPK cascades with delayed kinetics in IRAK-deficient
macrophages (32). Furthermore, delayed activation of
NF-B in response to LPS was also observed in TRAF6-deficient
embryonic fibroblasts (data not shown). Taken together, it can be
reasonably assumed that sequential activation of MyD88, IRAK, and TRAF6
is involved in MyD88-dependent pathway. Meanwhile, such sequential
activation does not seem to be involved in the MyD88-independent
pathway, although both pathways can lead to NF-B activation. With
serine protease inhibitors such as
N-tosyl-L-phenylalanine chloromethyl
ketone or
N--p-tosyl-L-lysine
chloromethyl ketone, Rescigno et al. argued that LPS-induced DC
maturation assesed by up-regulation of costimulatory molecules such as
MHC and CD86 is dependent on NF-B activation (33). We
have also found that
N-tosyl-L-phenylalanine chloromethyl
ketone and
N--p-tosyl-L-lysine
chloromethyl ketone could decrease the up-regulation of surface CD40
expression in response to LPS in both wild-type and MyD88-deficient BM
DCs (our unpublished data). However, although the reagents can block
nuclear translocation of NF-B by preventing of the inhibitor of B
(IB)- degradation (34), it is unclear at present
whether they affect other signaling cascades. Thus, further studies are
necessary to clarify whether NF-B activation is essential for
LPS-induced DC maturation.
The receptor for bacterial DNA, TLR9, possesses the conserved proline
in the cytoplasmic region and shows a similar overall molecular
structure to TLR4. However, signaling through TLR4 is significantly
distinct from that through TLR9, in the respect that the former can
activate the MyD88-independent pathway, leading to NF-B activation.
At present, the molecular mechanism of this pathway remains to be
clarified. In Drosophila, Tube functions as an adaptor
protein in Toll-signaling and is considered to be a homologue of MyD88.
However, Drosophila genome sequencing identified the
homologue of mammalian MyD88 (DDBJ/GenBank/EMBL accession number
AAF58953). Drosophila MyD88 carries the TIR and death
domain-like mammalian MyD88, whereas Tube does not carry a TIR domain.
It is an interesting possibility that a mammalian homologue of Tube
functions as an adaptor for the TLR family. A future challenge will be
the identification and characterization of signaling molecules involved
in the MyD88-independent pathway.
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Acknowledgments |
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Footnotes |
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2 Address correspondence and reprint requests to Dr. Shizuo Akira, Department of Host Defense, Research Institute for Microbial Diseases, Osaka University, Yamadaoka 3-1, Suita, Osaka 565-0871, Japan.
3 Abbreviations used in this paper: TLR, Toll-like receptor; MAPK, mitogen-activated protein kinase; DC, dendritic cell; TIR, Toll/IL-1R homology; BM, bone marrow; IRAK, IL-1R-associated kinase; TRAF, TNFR-associated factor; JNK, c-Jun N-terminal kinase.
Received for publication October 10, 2001. Accepted for publication February 20, 2001.
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B. Lemmers, L. Salmena, N. Bidere, H. Su, E. Matysiak-Zablocki, K. Murakami, P. S. Ohashi, A. Jurisicova, M. Lenardo, R. Hakem, et al. Essential Role for Caspase-8 in Toll-like Receptors and NF{kappa}B Signaling J. Biol. Chem., March 9, 2007; 282(10): 7416 - 7423. [Abstract] [Full Text] [PDF]
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 M. Pevsner-Fischer, V. Morad, M. Cohen-Sfady, L. Rousso-Noori, A. Zanin-Zhorov, S. Cohen, I. R. Cohen, and D. Zipori Toll-like receptors and their ligands control mesenchymal stem cell functions Blood, February 15, 2007; 109(4): 1422 - 1432. [Abstract] [Full Text] [PDF]
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R. Yadav, D. J. Zammit, L. Lefrancois, and A. T. Vella Effects of LPS-mediated bystander activation in the innate immune system J. Leukoc. Biol., December 1, 2006; 80(6): 1251 - 1261. [Abstract] [Full Text] [PDF]
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B. Liu, Y. Yang, J. Dai, R. Medzhitov, M. A. Freudenberg, P. L. Zhang, and Z. Li TLR4 Up-Regulation at Protein or Gene Level Is Pathogenic for Lupus-Like Autoimmune Disease J. Immunol., November 15, 2006; 177(10): 6880 - 6888. [Abstract] [Full Text] [PDF]
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S.-a. Ha, M. Tsuji, K. Suzuki, B. Meek, N. Yasuda, T. Kaisho, and S. Fagarasan Regulation of B1 cell migration by signals through Toll-like receptors J. Exp. Med., October 30, 2006; 203(11): 2541 - 2550. [Abstract] [Full Text] [PDF]
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W. E. Walker, I. W. Nasr, G. Camirand, B. M. Tesar, C. J. Booth, and D. R. Goldstein Absence of Innate MyD88 Signaling Promotes Inducible Allograft Acceptance J. Immunol., October 15, 2006; 177(8): 5307 - 5316. [Abstract] [Full Text] [PDF]
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C. Chassin, J.-M. Goujon, S. Darche, L. du Merle, M. Bens, F. Cluzeaud, C. Werts, E. Ogier-Denis, C. Le Bouguenec, D. Buzoni-Gatel, et al. Renal Collecting Duct Epithelial Cells React to Pyelonephritis-Associated Escherichia coli by Activating Distinct TLR4-Dependent and -Independent Inflammatory Pathways J. Immunol., October 1, 2006; 177(7): 4773 - 4784. [Abstract] [Full Text] [PDF]
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Y. Yao, Q. Xu, M.-J. Kwon, R. Matta, Y. Liu, S.-C. Hong, and C.-H. Chang ERK and p38 MAPK Signaling Pathways Negatively Regulate CIITA Gene Expression in Dendritic Cells and Macrophages J. Immunol., July 1, 2006; 177(1): 70 - 76. [Abstract] [Full Text] [PDF]
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K. A. Archer and C. R. Roy MyD88-Dependent Responses Involving Toll-Like Receptor 2 Are Important for Protection and Clearance of Legionella pneumophila in a Mouse Model of Legionnaires' Disease. Infect. Immun., June 1, 2006; 74(6): 3325 - 3333. [Abstract] [Full Text] [PDF]
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 A. E. Medvedev, I. Sabroe, J. D. Hasday, and S. N. Vogel Invited review: Tolerance to microbial TLR ligands: molecular mechanisms and relevance to disease Innate Immunity, June 1, 2006; 12(3): 133 - 150. [Abstract] [PDF]
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D. C. Rowe, A. F. McGettrick, E. Latz, B. G. Monks, N. J. Gay, M. Yamamoto, S. Akira, L. A. O'Neill, K. A. Fitzgerald, and D. T. Golenbock The myristoylation of TRIF-related adaptor molecule is essential for Toll-like receptor 4 signal transduction PNAS, April 18, 2006; 103(16): 6299 - 6304. [Abstract] [Full Text] [PDF]
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A. M. van der Sar, O. W. Stockhammer, C. van der Laan, H. P. Spaink, W. Bitter, and A. H. Meijer MyD88 Innate Immune Function in a Zebrafish Embryo Infection Model Infect. Immun., April 1, 2006; 74(4): 2436 - 2441. [Abstract] [Full Text] [PDF]
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 F.-S. X. Yu and L. D. Hazlett Toll-like Receptors and the Eye. Invest. Ophthalmol. Vis. Sci., April 1, 2006; 47(4): 1255 - 1263. [Full Text] [PDF]
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M. Ahmed, K. L. Brzoza, and E. M. Hiltbold Matrix Protein Mutant of Vesicular Stomatitis Virus Stimulates Maturation of Myeloid Dendritic Cells J. Virol., March 1, 2006; 80(5): 2194 - 2205. [Abstract] [Full Text] [PDF]
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T. B. Thornley, M. A. Brehm, T. G. Markees, L. D. Shultz, J. P. Mordes, R. M. Welsh, A. A. Rossini, and D. L. Greiner TLR Agonists Abrogate Costimulation Blockade-Induced Prolongation of Skin Allografts J. Immunol., February 1, 2006; 176(3): 1561 - 1570. [Abstract] [Full Text] [PDF]
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M. Yasutomi, Y. Ohshima, N. Omata, A. Yamada, H. Iwasaki, Y. Urasaki, and M. Mayumi Erythromycin Differentially Inhibits Lipopolysaccharide- or Poly(I:C)-Induced but Not Peptidoglycan-Induced Activation of Human Monocyte-Derived Dendritic Cells J. Immunol., December 15, 2005; 175(12): 8069 - 8076. [Abstract] [Full Text] [PDF]
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Y. Gao, J. Tao, M. O. Li, D. Zhang, H. Chi, O. Henegariu, S. M. Kaech, R. J. Davis, R. A. Flavell, and Z. Yin JNK1 Is Essential for CD8+ T Cell-Mediated Tumor Immune Surveillance J. Immunol., November 1, 2005; 175(9): 5783 - 5789. [Abstract] [Full Text] [PDF]
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H. Qin, C. A. Wilson, S. J. Lee, X. Zhao, and E. N. Benveniste LPS induces CD40 gene expression through the activation of NF-{kappa}B and STAT-1{alpha} in macrophages and microglia Blood, November 1, 2005; 106(9): 3114 - 3122. [Abstract] [Full Text] [PDF]
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M. Cohen-Sfady, G. Nussbaum, M. Pevsner-Fischer, F. Mor, P. Carmi, A. Zanin-Zhorov, O. Lider, and I. R. Cohen Heat Shock Protein 60 Activates B Cells via the TLR4-MyD88 Pathway J. Immunol., September 15, 2005; 175(6): 3594 - 3602. [Abstract] [Full Text] [PDF]
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M. Shingai, N. Inoue, T. Okuno, M. Okabe, T. Akazawa, Y. Miyamoto, M. Ayata, K. Honda, M. Kurita-Taniguchi, M. Matsumoto, et al. Wild-Type Measles Virus Infection in Human CD46/CD150-Transgenic Mice: CD11c-Positive Dendritic Cells Establish Systemic Viral Infection J. Immunol., September 1, 2005; 175(5): 3252 - 3261. [Abstract] [Full Text] [PDF]
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M. B. Drennan, B. Stijlemans, J. Van Den Abbeele, V. J. Quesniaux, M. Barkhuizen, F. Brombacher, P. De Baetselier, B. Ryffel, and S. Magez The Induction of a Type 1 Immune Response following a Trypanosoma brucei Infection Is MyD88 Dependent J. Immunol., August 15, 2005; 175(4): 2501 - 2509. [Abstract] [Full Text] [PDF]
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M. Ohmura, M. Yamamoto, C. Tomiyama-Miyaji, Y. Yuki, Y. Takeda, and H. Kiyono Nontoxic Shiga Toxin Derivatives from Escherichia coli Possess Adjuvant Activity for the Augmentation of Antigen-Specific Immune Responses via Dendritic Cell Activation Infect. Immun., July 1, 2005; 73(7): 4088 - 4097. [Abstract] [Full Text] [PDF]
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F. Ossendorp, N. Fu, M. Camps, F. Granucci, S. J. P. Gobin, P. J. van den Elsen, D. Schuurhuis, G. J. Adema, G. B. Lipford, T. Chiba, et al. Differential Expression Regulation of the {alpha} and {beta} Subunits of the PA28 Proteasome Activator in Mature Dendritic Cells J. Immunol., June 15, 2005; 174(12): 7815 - 7822. [Abstract] [Full Text] [PDF]
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J. A. Perry, C. S. Olver, R. C. Burnett, and A. C. Avery Cutting Edge: The Acquisition of TLR Tolerance during Malaria Infection Impacts T Cell Activation J. Immunol., May 15, 2005; 174(10): 5921 - 5925. [Abstract] [Full Text] [PDF]
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S. M. Zughaier, S. M. Zimmer, A. Datta, R. W. Carlson, and D. S. Stephens Differential Induction of the Toll-Like Receptor 4-MyD88-Dependent and -Independent Signaling Pathways by Endotoxins Infect. Immun., May 1, 2005; 73(5): 2940 - 2950. [Abstract] [Full Text] [PDF]
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A. R. Weatherill, J. Y. Lee, L. Zhao, D. G. Lemay, H. S. Youn, and D. H. Hwang Saturated and Polyunsaturated Fatty Acids Reciprocally Modulate Dendritic Cell Functions Mediated through TLR4 J. Immunol., May 1, 2005; 174(9): 5390 - 5397. [Abstract] [Full Text] [PDF]
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J.-N. Tournier, A. Quesnel-Hellmann, J. Mathieu, C. Montecucco, W.-J. Tang, M. Mock, D. R. Vidal, and P. L. Goossens Anthrax Edema Toxin Cooperates with Lethal Toxin to Impair Cytokine Secretion during Infection of Dendritic Cells J. Immunol., April 15, 2005; 174(8): 4934 - 4941. [Abstract] [Full Text] [PDF]
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D. W. Smith and C. Nagler-Anderson Preventing Intolerance: The Induction of Nonresponsiveness to Dietary and Microbial Antigens in the Intestinal Mucosa J. Immunol., April 1, 2005; 174(7): 3851 - 3857. [Abstract] [Full Text] [PDF]
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P. Decker, H. Singh-Jasuja, S. Haager, I. Kotter, and H.-G. Rammensee Nucleosome, the Main Autoantigen in Systemic Lupus Erythematosus, Induces Direct Dendritic Cell Activation via a MyD88-Independent Pathway: Consequences on Inflammation J. Immunol., March 15, 2005; 174(6): 3326 - 3334. [Abstract] [Full Text] [PDF]
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T. E. Singleton, P. Massari, and L. M. Wetzler Neisserial Porin-Induced Dendritic Cell Activation Is MyD88 and TLR2 Dependent J. Immunol., March 15, 2005; 174(6): 3545 - 3550. [Abstract] [Full Text] [PDF]
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 H. Bjorkbacka, K. A. Fitzgerald, F. Huet, X. Li, J. A. Gregory, M. A. Lee, C. M. Ordija, N. E. Dowley, D. T. Golenbock, and M. W. Freeman The induction of macrophage gene expression by LPS predominantly utilizes Myd88-independent signaling cascades Physiol Genomics, February 7, 2005; 19(3): 319 - 330. [Abstract] [Full Text] [PDF]
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H. S. Goodridge, F. A. Marshall, K. J. Else, K. M. Houston, C. Egan, L. Al-Riyami, F.-Y. Liew, W. Harnett, and M. M. Harnett Immunomodulation via Novel Use of TLR4 by the Filarial Nematode Phosphorylcholine-Containing Secreted Product, ES-62 J. Immunol., January 1, 2005; 174(1): 284 - 293. [Abstract] [Full Text] [PDF]
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 M. Yamamoto, K. Yaginuma, H. Tsutsui, J. Sagara, X. Guan, E. Seki, K. Yasuda, M. Yamamoto, S. Akira, K. Nakanishi, et al. ASC is essential for LPS-induced activation of procaspase-1 independently of TLR-associated signal adaptor molecules Genes Cells, November 1, 2004; 9(11): 1055 - 1067. [Abstract] [Full Text] [PDF]
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K. Honda, H. Yanai, T. Mizutani, H. Negishi, N. Shimada, N. Suzuki, Y. Ohba, A. Takaoka, W.-C. Yeh, and T. Taniguchi Role of a transductional-transcriptional processor complex involving MyD88 and IRF-7 in Toll-like receptor signaling PNAS, October 26, 2004; 101(43): 15416 - 15421. [Abstract] [Full Text] [PDF]
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K. Hiraoka, S. Yamamoto, S. Otsuru, S. Nakai, K. Tamai, R. Morishita, T. Ogihara, and Y. Kaneda Enhanced Tumor-Specific Long-Term Immunity of Hemaggluttinating Virus of Japan-Mediated Dendritic Cell-Tumor Fused Cell Vaccination by Coadministration with CpG Oligodeoxynucleotides J. Immunol., October 1, 2004; 173(7): 4297 - 4307. [Abstract] [Full Text] [PDF]
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S.-J. Park, T. Nakagawa, H. Kitamura, T. Atsumi, H. Kamon, S.-i. Sawa, D. Kamimura, N. Ueda, Y. Iwakura, K. Ishihara, et al. IL-6 Regulates In Vivo Dendritic Cell Differentiation through STAT3 Activation J. Immunol., September 15, 2004; 173(6): 3844 - 3854. [Abstract] [Full Text] [PDF]
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N. Sato, N. Takahashi, K. Suda, M. Nakamura, M. Yamaki, T. Ninomiya, Y. Kobayashi, H. Takada, K. Shibata, M. Yamamoto, et al. MyD88 But Not TRIF Is Essential for Osteoclastogenesis Induced by Lipopolysaccharide, Diacyl Lipopeptide, and IL-1{alpha} J. Exp. Med., September 7, 2004; 200(5): 601 - 611. [Abstract] [Full Text] [PDF]
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 Y. Emori, T. Ikeda, T. Ohashi, T. Masuda, T. Kurimoto, M. Takei, and M. Kannagi Inhibition of human immunodeficiency virus type 1 replication by Z-100, an immunomodulator extracted from human-type tubercle bacilli, in macrophages J. Gen. Virol., September 1, 2004; 85(9): 2603 - 2613. [Abstract] [Full Text] [PDF]
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S. Mukhopadhyay, L. Peiser, and S. Gordon Activation of murine macrophages by Neisseria meningitidis and IFN-{gamma} in vitro: distinct roles of class A scavenger and Toll-like pattern recognition receptors in selective modulation of surface phenotype J. Leukoc. Biol., September 1, 2004; 76(3): 577 - 584. [Abstract] [Full Text] [PDF]
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S. Datta, M. Novotny, X. Li, J. Tebo, and T. A. Hamilton Toll IL-1 Receptors Differ in Their Ability to Promote the Stabilization of Adenosine and Uridine-Rich Elements Containing mRNA J. Immunol., August 15, 2004; 173(4): 2755 - 2761. [Abstract] [Full Text] [PDF]
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K. W. Boehme and T. Compton Innate Sensing of Viruses by Toll-Like Receptors J. Virol., August 1, 2004; 78(15): 7867 - 7873. [Full Text] [PDF]
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 J. A. Whitsett, C. J. Bachurski, K. C. Barnes, P. A. Bunn Jr., L. M. Case, D. N. Cook, D. Crooks, M. W. Duncan, L. Dwyer-Nield, R. C. Elston, et al. Functional Genomics of Lung Disease Am. J. Respir. Cell Mol. Biol., August 1, 2004; 31(2/S1): S1 - S81. [Full Text] [PDF]
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D. D. Bolz, R. S. Sundsbak, Y. Ma, S. Akira, C. J. Kirschning, J. F. Zachary, J. H. Weis, and J. J. Weis MyD88 Plays a Unique Role in Host Defense but Not Arthritis Development in Lyme Disease J. Immunol., August 1, 2004; 173(3): 2003 - 2010. [Abstract] [Full Text] [PDF]
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S. Epelman, D. Stack, C. Bell, E. Wong, G. G. Neely, S. Krutzik, K. Miyake, P. Kubes, L. D. Zbytnuik, L. L. Ma, et al. Different Domains of Pseudomonas aeruginosa Exoenzyme S Activate Distinct TLRs J. Immunol., August 1, 2004; 173(3): 2031 - 2040. [Abstract] [Full Text] [PDF]
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A. K. Perry, E. K. Chow, J. B. Goodnough, W.-C. Yeh, and G. Cheng Differential Requirement for TANK-binding Kinase-1 in Type I Interferon Responses to Toll-like Receptor Activation and Viral Infection J. Exp. Med., June 21, 2004; 199(12): 1651 - 1658. [Abstract] [Full Text] [PDF]
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M. Drakes, T. Blanchard, and S. Czinn Bacterial Probiotic Modulation of Dendritic Cells Infect. Immun., June 1, 2004; 72(6): 3299 - 3309. [Abstract] [Full Text] [PDF]
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A. Didierlaurent, I. Ferrero, L. A. Otten, B. Dubois, M. Reinhardt, H. Carlsen, R. Blomhoff, S. Akira, J.-P. Kraehenbuhl, and J.-C. Sirard Flagellin Promotes Myeloid Differentiation Factor 88-Dependent Development of Th2-Type Response J. Immunol., June 1, 2004; 172(11): 6922 - 6930. [Abstract] [Full Text] [PDF]
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 S. Basu and M. J. Fenton Toll-like receptors: function and roles in lung disease Am J Physiol Lung Cell Mol Physiol, May 1, 2004; 286(5): L887 - L892. [Abstract] [Full Text] [PDF]
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J. Y. Lee, L. Zhao, H. S. Youn, A. R. Weatherill, R. Tapping, L. Feng, W. H. Lee, K. A. Fitzgerald, and D. H. Hwang Saturated Fatty Acid Activates but Polyunsaturated Fatty Acid Inhibits Toll-like Receptor 2 Dimerized with Toll-like Receptor 6 or 1 J. Biol. Chem., April 23, 2004; 279(17): 16971 - 16979. [Abstract] [Full Text] [PDF]
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D. Palliser, H. Ploegh, and M. Boes Myeloid Differentiation Factor 88 Is Required for Cross-Priming In Vivo J. Immunol., March 15, 2004; 172(6): 3415 - 3421. [Abstract] [Full Text] [PDF]
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E. Andreakos, S. M. Sacre, C. Smith, A. Lundberg, S. Kiriakidis, T. Stonehouse, C. Monaco, M. Feldmann, and B. M. Foxwell Distinct pathways of LPS-induced NF-{kappa}B activation and cytokine production in human myeloid and nonmyeloid cells defined by selective utilization of MyD88 and Mal/TIRAP Blood, March 15, 2004; 103(6): 2229 - 2237. [Abstract] [Full Text] [PDF]
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N. M. Tsuji, H. Tsutsui, E. Seki, K. Kuida, H. Okamura, K. Nakanishi, and R. A. Flavell Roles of caspase-1 in Listeria infection in mice Int. Immunol., February 1, 2004; 16(2): 335 - 343. [Abstract] [Full Text] [PDF]
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 T. Akazawa, H. Masuda, Y. Saeki, M. Matsumoto, K. Takeda, K. Tsujimura, K. Kuzushima, T. Takahashi, I. Azuma, S. Akira, et al. Adjuvant-Mediated Tumor Regression and Tumor-Specific Cytotoxic Response Are Impaired in MyD88-Deficient Mice Cancer Res., January 15, 2004; 64(2): 757 - 764. [Abstract] [Full Text] [PDF]
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J.-L. Imler and L. Zheng Biology of Toll receptors: lessons from insects and mammals J. Leukoc. Biol., January 1, 2004; 75(1): 18 - 26. [Abstract] [Full Text] [PDF]
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H. Oshiumi, M. Sasai, K. Shida, T. Fujita, M. Matsumoto, and T. Seya TIR-containing Adapter Molecule (TICAM)-2, a Bridging Adapter Recruiting to Toll-like Receptor 4 TICAM-1 That Induces Interferon-{beta} J. Biol. Chem., December 12, 2003; 278(50): 49751 - 49762. [Abstract] [Full Text] [PDF]
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V. Buatois, M. Baillet, S. Becart, N. Mooney, L. Leserman, and P. Machy MHC Class II-Peptide Complexes in Dendritic Cell Lipid Microdomains Initiate the CD4 Th1 Phenotype J. Immunol., December 1, 2003; 171(11): 5812 - 5819. [Abstract] [Full Text] [PDF]
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N. Suzuki, S. Suzuki, U. Eriksson, H. Hara, C. Mirtosis, N.-J. Chen, T. Wada, D. Bouchard, I. Hwang, K. Takeda, et al. IL-1R-Associated Kinase 4 Is Required for Lipopolysaccharide- Induced Activation of APC J. Immunol., December 1, 2003; 171(11): 6065 - 6071. [Abstract] [Full Text] [PDF]
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R. Kalupahana, A. R. Emilianus, D. Maskell, and B. Blacklaws Salmonella enterica Serovar Typhimurium Expressing Mutant Lipid A with Decreased Endotoxicity Causes Maturation of Murine Dendritic Cells Infect. Immun., November 1, 2003; 71(11): 6132 - 6140. [Abstract] [Full Text] [PDF]
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M. Boes, N. Bertho, J. Cerny, M. Op den Brouw, T. Kirchhausen, and H. Ploegh T Cells Induce Extended Class II MHC Compartments in Dendritic Cells in a Toll-Like Receptor-Dependent Manner J. Immunol., October 15, 2003; 171(8): 4081 - 4088. [Abstract] [Full Text] [PDF]
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S. Sato, M. Sugiyama, M. Yamamoto, Y. Watanabe, T. Kawai, K. Takeda, and S. Akira Toll/IL-1 Receptor Domain-Containing Adaptor Inducing IFN-{beta} (TRIF) Associates with TNF Receptor-Associated Factor 6 and TANK-Binding Kinase 1, and Activates Two Distinct Transcription Factors, NF-{kappa}B and IFN-Regulatory Factor-3, in the Toll-Like Receptor Signaling J. Immunol., October 15, 2003; 171(8): 4304 - 4310. [Abstract] [Full Text] [PDF]
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L. Franchi, I. Condo, B. Tomassini, C. Nicolo, and R. Testi A caspaselike activity is triggered by LPS and is required for survival of human dendritic cells Blood, October 15, 2003; 102(8): 2910 - 2915. [Abstract] [Full Text] [PDF]
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K. A. Fitzgerald, D. C. Rowe, B. J. Barnes, D. R. Caffrey, A. Visintin, E. Latz, B. Monks, P. M. Pitha, and D. T. Golenbock LPS-TLR4 Signaling to IRF-3/7 and NF-{kappa}B Involves the Toll Adapters TRAM and TRIF J. Exp. Med., October 6, 2003; 198(7): 1043 - 1055. [Abstract] [Full Text] [PDF]
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 A J Stagg, A L Hart, S C Knight, and M A Kamm The dendritic cell: its role in intestinal inflammation and relationship with gut bacteria Gut, October 1, 2003; 52(10): 1522 - 1529. [Abstract] [Full Text] [PDF]
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J. Y. Lee, J. Ye, Z. Gao, H. S. Youn, W. H. Lee, L. Zhao, N. Sizemore, and D. H. Hwang Reciprocal Modulation of Toll-like Receptor-4 Signaling Pathways Involving MyD88 and Phosphatidylinositol 3-Kinase/AKT by Saturated and Polyunsaturated Fatty Acids J. Biol. Chem., September 26, 2003; 278(39): 37041 - 37051. [Abstract] [Full Text] [PDF]
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J. Uehori, M. Matsumoto, S. Tsuji, T. Akazawa, O. Takeuchi, S. Akira, T. Kawata, I. Azuma, K. Toyoshima, and T. Seya Simultaneous Blocking of Human Toll-Like Receptors 2 and 4 Suppresses Myeloid Dendritic Cell Activation Induced by Mycobacterium bovis Bacillus Calmette-Guerin Peptidoglycan Infect. Immun., August 1, 2003; 71(8): 4238 - 4249. [Abstract] [Full Text] [PDF]
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S.-i. Fujii, K. Shimizu, C. Smith, L. Bonifaz, and R. M. Steinman Activation of Natural Killer T Cells by {alpha}-Galactosylceramide Rapidly Induces the Full Maturation of Dendritic Cells In Vivo and Thereby Acts as an Adjuvant for Combined CD4 and CD8 T Cell Immunity to a Coadministered Protein J. Exp. Med., July 21, 2003; 198(2): 267 - 279. [Abstract] [Full Text] [PDF]
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S. S. Way, T. R. Kollmann, A. M. Hajjar, and C. B. Wilson Cutting Edge: Protective Cell-Mediated Immunity to Listeria monocytogenes in the Absence of Myeloid Differentiation Factor 88 J. Immunol., July 15, 2003; 171(2): 533 - 537. [Abstract] [Full Text] [PDF]
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) or
without (
) 100 ng/ml LPS for 2 more days. Amounts of TNF-
