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*
Division of Dermatology and
Pulmonary Medicine,
Department of Microbiology and Immunology, and Molecular Biology Institute, University of California School of Medicine, Los Angeles, CA 90095;
§
Genentech Incorporated, South San Francisco, CA 94080; and
¶
Department of Microbiology, University of Texas Southwestern Medical Center, Dallas, TX 75235
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResultsDiscussionReferences |
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, CD40 ligand, or LPS are required for complete maturation and
maximum APC function. Because we recently found that microbial
lipoproteins can activate monocytes and DC through Toll-like receptor
(TLR) 2, we also investigated whether lipoproteins can drive DC
maturation. Immature DC were cultured with or without lipoproteins and
were monitored for expression of cell surface markers indicative of
maturation. Stimulation with lipopeptides increased expression of CD83,
MHC class II, CD80, CD86, CD54, and CD58, and decreased CD32 expression
and endocytic activity; these lipopeptide-matured DC also displayed
enhanced T cell stimulatory capacity in MLR, as measured by T cell
proliferation and IFN-
secretion. The lipid moiety of the
lipopeptide was found to be essential for induction of maturation.
Preincubation of maturing DC with an anti-TLR2 blocking Ab before
addition of lipopeptide blocked the phenotypic and functional changes
associated with DC maturation. These results demonstrate that
lipopeptides can stimulate DC maturation via TLR2, providing a
mechanism by which products of bacteria can participate in the
initiation of an immune response. |
Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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In vitro studies of DC maturation have been conducted using cells
derived from peripheral blood monocytes cultured in the presence of
GM-CSF and IL-4 (2, 3, 4, 5). Such cells are relatively
immature, having a high rate of endocytosis and expressing low levels
of MHC class II (MHC-II), CD83, and costimulatory molecules CD80 and
CD86 (1). Upon maturation with TNF-, CD40 ligand, or
LPS, DC down-regulate mechanisms of Ag capture, including endocytic
activity and expression of Fc receptors, while increasing expression of
costimulatory and adhesion molecules (6, 7). Similar
changes indicative of maturation have also been reported following
infection with mycoplasma, viruses, intracellular bacteria, and
parasites (8, 9, 10). These phenotypic changes parallel the
functional transition of DC from Ag-capturing cells to APCs. Although
it is known that microbes and microbial products, particularly LPS,
induce the maturation of DC, the mechanism by which this occurs is not
known.
Recent work in our laboratory has revealed that DC express Toll-like receptor (TLR) 2 and that this receptor mediates lipopeptide-induced IL-12 production, but little is known of other processes mediated by TLRs (11). Although there is currently no direct evidence that TLRs mediate DC maturation, TLRs or other pattern recognition receptors have been predicted to mediate DC maturation events (1, 12). In this study, we examined whether microbial lipopeptides can induce the phenotypic and functional changes associated with DC maturation, and whether this process is dependent upon TLR2.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Peripheral blood was collected from healthy volunteers and fractionated over Ficoll-Paque (Amersham Pharmacia, Uppsala, Sweden) by a standard procedure. To derive DC, total PBMCs were cultured at 2 x 106 cells/ml in complete media (RPMI 1640, 0.1 mM sodium pyruvate, 2 mM penicillin, 50 µg/ml streptomycin; Life Technologies, Grand Island, NY) supplemented with 1% FCS (Omega Scientific, Tarzana, CA) for 1.5 h in tissue culture flasks. Following incubation, nonadherent cells were removed by extensive washing with a 1x solution of HBSS (Life Technologies). The remaining adherent cells were then cultured in complete media containing 10% FCS, 200 U/ml GM-CSF (Genetics Institute, Cambridge MA), and 100 U/ml IL-4 (Schering-Plough, Madison, NJ) for 3–4 days in a CO2 incubator at 37°C. The resulting cells were semi- to nonadherent and MHC II+ CD14+ CD83-/low and displayed DC morphology.
For further maturation, adherent and nonadherent DC were harvested from T-75 flasks by incubation in PBS-EDTA (1 mM) for 30 min. The cells recovered were counted and recultured at 5 x 105 cells/ml in fresh media containing GM-CSF and IL-4. Salmonella typhosa LPS (Sigma; St. Louis, MO), the synthetic lipopeptide Pam3CysSerLys4 (Boehringer Mannheim, Indianapolis, IN), the 19-kDa lipoprotein from Mycobacterium tuberculosis (13) (courtesy of John Belisle, Colorado State University, Ft. Collins, CO), a synthetic 19-kDa lipopeptide, a synthetic lipopeptide based on the sequence of the 47-kDa lipoprotein from Treponema pallidum (14), or unlipidated forms of the synthetic lipopeptides were added to some DC cultures for 24–48 h (15). All lipopeptides contained <40 pg/µg of LPS, as determined by the Limulus Amoebocyte Assay (BioWhittaker, Walkersville, MD). Cells were cultured for an additional 24–48 h before analysis by flow cytometry.
Blocking of TLR2
Blocking experiments with anti-TLR2 mAb were performed on DC 3 days after the initiation of the culture from PBMCs. Anti-TLR2 Ab (16) or IgG1 isotype control Ab (10 µg/ml) was added to the cells 30 min before the addition of the lipopeptides or LPS. Cells were harvested with PBS-EDTA 40–48 h later and analyzed for expression of cell surface molecules by flow cytometry, or used directly in a MLR.
Mixed leukocyte reactions
DC for use in MLRs were harvested from T-75 flasks following the initial 3-day culture period, and recultured in the same media in 96-well round-bottom plates (Costar, Corning, NY) at 1 x 104, 4 x 103, or 2 x 103 cells/well. Lipopeptides were added to some cultures, and the DC were incubated for an additional 2 days in a total volume of 100 µl. On day 5 after initiation of the cells from PBMC, the DC were irradiated (3000 rad from a 137Cs source) and cocultured with purified T cells. Blocking of TLR2 was performed as described above.
T cells from an unrelated donor were prepared from total PBMC by negative selection using Ab depletion and magnetic beads. Briefly, total PBMCs were prepared as described above and diluted to 5 x 106 cells/ml in RPMI 1640 plus 10% human serum (Omega Scientific). The cells were then cultured for 30 min in tissue culture flasks to remove the adherent cells. The nonadherent cells were collected and incubated for 20 min at 4°C with anti-CD14, anti-CD16, and anti-CD19 mAb (no azide, low endotoxin (NA/LE); PharMingen, San Diego, CA) at a concentration of 0.4 µg Ab/106 nonadherent cells. Following two washes with PBS plus 2% serum, cells were incubated with sheep anti-mouse IgG-conjugated Dynabeads (10:1 bead:cell ratio; Dynal, Lake Success, NY) for 20 min at 4°C. The nonmagnetic fraction was collected and contained >95% CD3+ T cells, as assessed by flow cytometry.
Purified T cells were added to the lipopeptide-matured DC at 2 x
105 cells/well to give final ratios of 1:100,
1:50, or 1:20 DC:T cells and incubated for 5–6 days. Culture
supernatant fluids were collected from some cultures for use in an
IFN- ELISA. To measure T cell-proliferative responses,
[3H]thymidine was added at 1 µCi/well and
incubated for an additional 18 h. The assay was then harvested,
and the incorporation of [3H]thymidine was
measured in a liquid scintillation counter.
IFN- ELISA
IFN- in culture supernatant fluids was assessed by a standard
sandwich ELISA. Microtiter plates (Costar) were coated with an
unconjugated anti-IFN- capture Ab (clone NIB42, 5 µg/ml), and
detection was achieved using a biotinylated Ab (clone 4s.B3, 2 µg/ml;
PharMingen). The plate was developed using Immunopure HRP-conjugated
streptavidin (Pierce, Rockford, IL) and an ABTS Microwell Peroxidase
Substrate System (Kirkegaard & Perry Laboratories, Gaithersburg, MD).
The absorbance at 405 nm was read using a microtiter plate reader,
and concentrations of IFN- were calculated from a standard curve of
recombinant human IFN- (PharMingen).
Flow cytometry
Standard flow cytometric analysis was used to assess surface expression of various markers. Surface expression of TLR2 was determined using a mAb (clone 2392, IgG1) and a PE-conjugated goat anti-mouse IgG secondary Ab. The following mAbs directly conjugated with either PE or FITC were used in single-color flow cytometric analysis: PE-CD14 (clone TUK4, IgG2a), PE-CD54 (clone MEM111, IgG2a), PE-CD58 (clone 1C3, IgG2a), PE-CD80 (clone L3007.4, IgG1), PE-CD83 (clone HB15e, IgG1), PE-CD86 (clone IT2.2, IgG1), FITC-HLA-DR (clone TU36, IgG2b), and FITC-CD32 (clone FLI8.26, IgG2b). Isotype control Abs (mouse IgG1, PE-IgG2a, PE-IgG1, FITC-IgG2b) were used in all experiments. All conjugated Abs were purchased from Caltag (South San Francisco, CA) or PharMingen. After staining, cells were washed and fixed in 1% paraformaldehyde before analysis on a Becton Dickinson (Mountain View, CA) FacsScan or FacsCa1ibur Flow Cytometer. Gating was on large granular cells, and 2000–5000 gated events were collected from each sample. Data were analyzed using WinMDI 2.8 (Joseph Trotter, Scripps Research Institute, San Diego, CA). Histograms were drawn from and median fluorescence intensity (MFI) values were determined on the gated population. In some experiments, the percentage of cells positive for a particular marker was determined.
Endocytic activity
Endocytic activity of DC was measured by the uptake of fluorescein-conjugated dextran (F-Dx; m.w. 40,000; Molecular Probes, Eugene, OR) as previously described (2). Briefly, DC at various states of maturation were incubated in complete media plus 10% FCS plus 1 mg/ml F-Dx for 1 h at 4°C to measure nonspecific binding, or at 37°C to measure specific uptake. Cells were then washed extensively and analyzed by flow cytometry as described above.
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Results |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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It has previously been shown that both LPS and lipopeptides induce
cytokine secretion in monocytes via TLRs (11, 13, 17, 18),
and that LPS induces maturation of DC (1). Hence, we asked
whether lipopeptides can also induce DC maturation and whether TLR2
mediates this process. To this end, we used an in vitro culture system
for the derivation of DC from adherent PBMCs cultured with GM-CSF and
IL-4 (2). As shown in Fig. 1
, cells cultured in this manner for 3
days stably expressed MHC-II. The monocyte marker CD14 was also
expressed, whereas there was little or no expression of CD83, a marker
expressed on DC. With additional days in culture, cells became more
differentiated and acquired a DC morphology. After 5 days in culture,
the MFI of cells stained with anti-CD14 expression decreased 5-fold
relative to cells cultured for 3 days (Fig. 1); in some donors, we
observed a concomitant increase in CD83 expression (data not shown).
These cells also expressed TLR2, as we have previously shown (Fig. 1)
(11).
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Final maturation of DC has been shown to occur upon
treatment with TNF-, CD40 ligand, or LPS (6). This
maturation results in increased expression of CD83. To determine
whether lipopeptides also mediate DC maturation, immature DC were
cultured with various concentrations of the synthetic lipopeptide
PAM3CysSerLys4. As shown in
Fig. 2, immature DC cultured with
increasing doses of lipopeptide had increasing levels of CD83
expression, as assessed by flow cytometry. At the maximum dose of
10,000 ng/ml the MFI of cells stained with anti-CD83 Ab was 3.5
times greater than unstimulated cells. A similar dose-dependent effect
was also observed with a 19-kDa lipoprotein from M.
tuberculosis and a synthetic 19-kDa lipopeptide (data not shown).
This finding suggests that lipopeptides can induce DC maturation.
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1.5–10
times higher on DC cultured with
PAM3CysSerLys4 or a
synthetic 19-kDa lipopeptide from M. tuberculosis, relative
to unstimulated cells (Fig. 3). In
contrast, levels of FcRII (CD32), which mediates uptake of Ag-Ab
complexes, was 2-fold lower on DC matured with lipopeptides. In
addition, IL-12 could be detected in the culture supernatant fluids of
lipopeptide-stimulated DC (data not shown). Stimulation with the
T. pallidum 47-kDa lipopeptide (Fig. 4; data not shown) and LPS yielded
similar results, although the absolute fold increase of MFI observed
showed some donor variability. Overall, these data support the notion
that lipopeptides and LPS have a similar biological effect on the
activation and maturation of DC.
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8-fold lower than
untreated cells (Fig. 5). This finding
provides further evidence that microbial lipopeptides can drive DC
maturation.
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Previous work describing the biological properties of lipopeptides
has revealed that the lipid portion of the molecule is required for
activity (11, 13, 14, 17, 19). To determine whether
microbial lipopeptide-induced DC maturation was dependent upon the
lipid moiety of the molecule, synthetic 19-kDa lipopeptide and
synthetic 47-kDa lipopeptide were compared with unlipidated peptides
with the same amino acid sequences. DC matured for 2 days in the
presence of the lipidated 19-kDa or 47-kDa peptides showed increased
levels of CD83, CD80, CD86, and MHC-II expression, whereas unlipidated
control peptides induced only small or no increases in levels of
expression of these molecules relative to untreated cells (Fig. 4
).
Together, these results confirm that the lipid portion of the
lipopeptide is required for the induction of DC maturation.
TLR2 mediates lipopeptide-induced DC maturation
TLR2 has previously been shown to mediate responses to
lipopeptides in cells of the monocyte lineage (11, 13, 17, 18). Consequently, the role of TLR2 in mediating
lipopeptide-induced DC maturation was tested. Immature DC were
preincubated with anti-TLR2 Ab or an IgG1 isotype control Ab for 30
min before the addition of suboptimal concentrations of lipopeptide and
subsequent maturation. Preincubation of DC with anti-TLR2 before
the addition of lipopeptide blocked the up-regulation of CD80 and CD86
induced by the 19-kDa lipopeptide or
PAM3CysSerLys4 by 90–100%
(Fig. 6A), relative to
untreated cells or cells treated with IgG1 alone. In some cultures, the
IgG1 Ab was slightly stimulatory and enhanced expression of CD80 and
CD86, as indicated by increases in MFI.
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7-fold fewer CD80-positive cells compared with
cells cultured with lipopeptide alone (Fig. 6B). However,
the relative percentage of CD86-positive cells did not change
significantly (Fig. 6B), as nearly all immature and mature
DC expressed CD86. Anti-TLR2 also blocked the decrease in endocytic
activity observed in lipopeptide-matured DC (Fig. 6C).
Additionally, IL-12 was not detected in culture supernatant fluids of
cells incubated with the anti-TLR Ab (data not shown) as we have
previously shown (11). In summary, anti-TLR2 blocked
the lipopeptide-induced increase in CD80 MFI and the increase in the
percentage of cells positive for CD80. Anti-TLR2 blocked increases in
the CD86 MFI, but not the percentage of cells positive for CD86. In
whole, these results indicate that lipopeptide activation of immature
DC via TLR2 leads to increases of cell surface markers associated with
mature DC and decreases in endocytic function, suggesting that TLR2
regulates multiple factors associated with lipopeptide-induced DC
maturation. Lipopeptide-matured DC have increased stimulatory potential in MLRs
We observed that lipopeptide-matured DC expressed increased levels
of Ag-presenting and costimulatory molecules. To determine whether, as
a result of these phenotypic changes, lipopeptide-matured DC had
enhanced functional properties, we compared the capacity of immature
and lipopeptide-matured DC to stimulate T cells in an MLR. DC were
treated with PAM3CysSerLys4
or 19- kDa lipopeptide for 2 days before coculture with T cells from an
unrelated donor. Lipopeptide-matured DC were more effective at
stimulating a MLR, as observed by a 1.5- to 3-fold increase in T
cell-proliferative responses compared with untreated DC (Fig. 7A). Again, treatment of DC
with an unlipidated peptide did not result in enhanced T cell
proliferation. We also measured the ability of these DC to stimulate a
MLR by measuring the production of IFN- by T cells.
Lipopeptide-matured DC stimulated 3- to 11-fold greater levels of
IFN- production relative to control cultures (Fig. 7B).
Together, these data demonstrate that lipopeptide-matured DC have
greater T cell-stimulatory activity than immature DC. The addition of
anti-TLR2 Ab before the maturation of DC with lipopeptides
abrogated the ability of the DC to stimulate enhanced T cell
proliferation and IFN- production in a MLR (Fig. 7, C and
D). In summary, these results demonstrate that
lipopeptide-matured DC have enhanced T cell-stimulatory activity, and
induction of this activity is dependent upon TLR2.
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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During the immune response to infectious agents, DC concentrate microbial ligands and Ags and mature into highly effective APCs. Previous studies have demonstrated that stimulation with LPS or live bacteria induces DC maturation. In these studies, culture of immature DC with LPS from Escherichia coli (2) induced increases in a number of cell surface markers, including MHC-II, CD80, CD40, CD54, and CD58, whereas expression of CD14, CD32, and endocytic activity was reduced. Additionally, infection of human DC with live bacillus Calmette-Guérin (20), M. tuberculosis (21), Listeria monocytogenes (9), Streptococcus gordonii (22), or Leishmania major (10) results in an increase in MHC and costimulatory molecule expression and enhanced T cell-stimulatory activity (20). Similar results were obtained with murine DC; these cells also demonstrated an enhanced ability to induce T cell responses in mice (23). In our studies, we found that the 19-kDa lipoprotein from M. tuberculosis, as well as synthetic lipopeptides, induced DC maturation. The resulting mature DC had increased cell surface expression of MHC-II, CD80, CD83, CD86, CD54, and CD58, suggesting that the lipopeptide alone is sufficient to induce maturation events. Lipopeptide-matured DC were also more potent than immature DC in stimulating T cells in a MLR. Together, these findings provide a mechanism by which cells of the innate immune system can recognize and be activated by microbial products, leading to the initiation of an adaptive immune response.
Many studies with LPS-matured DC give an indication of the relevance of such maturation events as we have described herein. Recent work has revealed that LPS treatment of DC enhances peptide-MHC-II complex formation and its trafficking to the cell surface (24). This trafficking also results in the clustering of peptide-MHC-II/costimulatory molecules on the surface of DC, which enhances the T cell-stimulatory capacity of these cells. Furthermore, surface MHC-II molecules on LPS-matured DC have a longer half-life than that of immature DC, and mature DC maintain their in vitro T cell-stimulatory capacity for several days longer in culture compared with immature cells (25). Because of the functional similarity of LPS and lipopeptides, we predict that lipopeptides will have a similar effect on peptide loading and MHC-II stability, although this remains to be determined.
Before this work, the mechanism by which microbe-induced DC maturation
occurs had not been identified. However, the recent identification of
TLRs as CD14-associated signaling molecules has shed new light on the
mechanisms by which cells of the immune system respond to microbial
products. TLRs are a family of transmembrane proteins that are
evolutionarily conserved in species ranging from insects to mammals
(26). In Drosophila, Toll is involved in
dorsal-ventral patterning, as well as induction of innate immune
responses to microbial pathogens (27). Humans have at
least 10 different TLRs that are expressed primarily on cells of
myeloid origin, but TLRs have also been found on epithelial cells
(26). Of these receptors, TLR2 and TLR4 have been shown to
mediate cellular responses to LPS from Gram-negative bacteria
(16, 28), lipopeptides from mycobacteria
(13), as well as peptidoglycans and lipoteichoic acids
from Gram-positive bacteria (29). The result of such
activation includes induction of the NF-
B signaling pathway and the
production of cytokines (13, 16, 30, 31).
Here we have described a role for TLR2 in mediating DC maturation, thereby providing a mechanism by which lipopeptides act as adjuvants. The increase in DC expression of Ag-presenting and costimulatory molecules has been shown to allow DC, cells of the innate immune system, to instruct the adaptive immune response by stimulating naive T cells. This finding may have important implications in the rational design of vaccines that could exploit the adjuvant properties of lipopeptides for enhancing DC-mediated induction of cellular immune responses.
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Acknowledgments |
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Footnotes |
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2 Address correspondence and reprint requests to Dr. Robert Modlin, University of California Division of Dermatology, 52-121 CHS, 10833 Le Conte Avenue, Los Angeles, CA 90095.
3 Abbreviations used in this paper: DC, dendritic cell(s); MFI, median fluorescence intensity; F-Dx, fluorescein-conjugated dextran; TLR, Toll-like receptor; MHC-II, MHC class II.
Received for publication June 22, 2000. Accepted for publication December 7, 2000.
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References |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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. J. Exp. Med. 179:1109. B. Infect. Immun. 64:3845.[Abstract]
-independent activation of dendritic cells following treatment with Mycobacterium bovis bacillus Calmette-Guerin. Immunology 97:626.[Medline]
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N. D. Pecora, A. J. Gehring, D. H. Canaday, W. H. Boom, and C. V. Harding Mycobacterium tuberculosis LprA Is a Lipoprotein Agonist of TLR2 That Regulates Innate Immunity and APC Function J. Immunol., July 1, 2006; 177(1): 422 - 429. [Abstract] [Full Text] [PDF]
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 L. Romics Jr, G. Szabo, J. C. Coffey, J. H. Wang, and H. P. Redmond The Emerging Role of Toll-Like Receptor Pathways in Surgical Diseases Arch Surg, June 1, 2006; 141(6): 595 - 601. [Abstract] [Full Text] [PDF]
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 M. Stasiolek, A. Bayas, N. Kruse, A. Wieczarkowiecz, K. V. Toyka, R. Gold, and K. Selmaj Impaired maturation and altered regulatory function of plasmacytoid dendritic cells in multiple sclerosis Brain, May 1, 2006; 129(5): 1293 - 1305. [Abstract] [Full Text] [PDF]
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S. O. Dionne, A. B. Podany, Y. W. Ruiz, N. M. Ampel, J. N. Galgiani, and D. F. Lake Spherules Derived from Coccidioides posadasii Promote Human Dendritic Cell Maturation and Activation Infect. Immun., April 1, 2006; 74(4): 2415 - 2422. [Abstract] [Full Text] [PDF]
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C. Nicolo, G. Di Sante, M. Orsini, S. Rolla, S. Columba-Cabezas, V. R. Spica, G. Ricciardi, B. M. C. Chan, and F. Ria Mycobacterium tuberculosis in the adjuvant modulates the balance of Th immune response to self-antigen of the CNS without influencing a "core" repertoire of specific T cells Int. Immunol., February 1, 2006; 18(2): 363 - 374. [Abstract] [Full Text] [PDF]
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 R. E. LaFond and S. A. Lukehart Biological Basis for Syphilis Clin. Microbiol. Rev., January 1, 2006; 19(1): 29 - 49. [Abstract] [Full Text] [PDF]
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S. E. Lee, S. Y. Kim, B. C. Jeong, Y. R. Kim, S. J. Bae, O. S. Ahn, J.-J. Lee, H.-C. Song, J. M. Kim, H. E. Choy, et al. A Bacterial Flagellin, Vibrio vulnificus FlaB, Has a Strong Mucosal Adjuvant Activity To Induce Protective Immunity Infect. Immun., January 1, 2006; 74(1): 694 - 702. [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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J. E. Butler, D. H. Francis, J. Freeling, P. Weber, and A. M. Krieg Antibody Repertoire Development in Fetal and Neonatal Piglets. IX. Three Pathogen-Associated Molecular Patterns Act Synergistically to Allow Germfree Piglets to Respond to Type 2 Thymus-Independent and Thymus-Dependent Antigens J. Immunol., November 15, 2005; 175(10): 6772 - 6785. [Abstract] [Full Text] [PDF]
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 S. Meyer, E. van Liempt, A. Imberty, Y. van Kooyk, H. Geyer, R. Geyer, and I. van Die DC-SIGN Mediates Binding of Dendritic Cells to Authentic Pseudo-LewisY Glycolipids of Schistosoma mansoni Cercariae, the First Parasite-specific Ligand of DC-SIGN J. Biol. Chem., November 11, 2005; 280(45): 37349 - 37359. [Abstract] [Full Text] [PDF]
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Z. Zhang, J.-P. Louboutin, D. J. Weiner, J. B. Goldberg, and J. M. Wilson Human Airway Epithelial Cells Sense Pseudomonas aeruginosa Infection via Recognition of Flagellin by Toll-Like Receptor 5 Infect. Immun., November 1, 2005; 73(11): 7151 - 7160. [Abstract] [Full Text] [PDF]
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A. M. C. van Rossum, E. S. Lysenko, and J. N. Weiser Host and Bacterial Factors Contributing to the Clearance of Colonization by Streptococcus pneumoniae in a Murine Model Infect. Immun., November 1, 2005; 73(11): 7718 - 7726. [Abstract] [Full Text] [PDF]
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R. Vankayalapati, A. Garg, A. Porgador, D. E. Griffith, P. Klucar, H. Safi, W. M. Girard, D. Cosman, T. Spies, and P. F. Barnes Role of NK Cell-Activating Receptors and Their Ligands in the Lysis of Mononuclear Phagocytes Infected with an Intracellular Bacterium J. Immunol., October 1, 2005; 175(7): 4611 - 4617. [Abstract] [Full Text] [PDF]
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 S. Radhakrishnan, E. Celis, and L. R. Pease B7-DC cross-linking restores antigen uptake and augments antigen-presenting cell function by matured dendritic cells PNAS, August 9, 2005; 102(32): 11438 - 11443. [Abstract] [Full Text] [PDF]
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E. Porter, H. Yang, S. Yavagal, G. C. Preza, O. Murillo, H. Lima, S. Greene, L. Mahoozi, M. Klein-Patel, G. Diamond, et al. Distinct Defensin Profiles in Neisseria gonorrhoeae and Chlamydia trachomatis Urethritis Reveal Novel Epithelial Cell-Neutrophil Interactions Infect. Immun., August 1, 2005; 73(8): 4823 - 4833. [Abstract] [Full Text] [PDF]
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N. Craft, K. W. Bruhn, B. D. Nguyen, R. Prins, J. W. Lin, L. M. Liau, and J. F. Miller The TLR7 Agonist Imiquimod Enhances the Anti-Melanoma Effects of a Recombinant Listeria monocytogenes Vaccine J. Immunol., August 1, 2005; 175(3): 1983 - 1990. [Abstract] [Full Text] [PDF]
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S. Bluml, S. Kirchberger, V. N. Bochkov, G. Kronke, K. Stuhlmeier, O. Majdic, G. J. Zlabinger, W. Knapp, B. R. Binder, J. Stockl, et al. Oxidized Phospholipids Negatively Regulate Dendritic Cell Maturation Induced by TLRs and CD40 J. Immunol., July 1, 2005; 175(1): 501 - 508. [Abstract] [Full Text] [PDF]
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 G. Mastrangelo, J. M. Grange, E. Fadda, U. Fedeli, A. Buja, and J. H. Lange Lung Cancer Risk: Effect of Dairy Farming and the Consequence of Removing that Occupational Exposure Am. J. Epidemiol., June 1, 2005; 161(11): 1037 - 1046. [Abstract] [Full Text] [PDF]
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Y. Maeda, T. Mukai, J. Spencer, and M. Makino Identification of an Immunomodulating Agent from Mycobacterium leprae Infect. Immun., May 1, 2005; 73(5): 2744 - 2750. [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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M. Iqbal, V. J. Philbin, G. S. K. Withanage, P. Wigley, R. K. Beal, M. J. Goodchild, P. Barrow, I. McConnell, D. J. Maskell, J. Young, et al. Identification and Functional Characterization of Chicken Toll-Like Receptor 5 Reveals a Fundamental Role in the Biology of Infection with Salmonella enterica Serovar Typhimurium Infect. Immun., April 1, 2005; 73(4): 2344 - 2350. [Abstract] [Full Text] [PDF]
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M. Buettner, C. Meinken, M. Bastian, R. Bhat, E. Stossel, G. Faller, G. Cianciolo, J. Ficker, M. Wagner, M. Rollinghoff, et al. Inverse Correlation of Maturity and Antibacterial Activity in Human Dendritic Cells J. Immunol., April 1, 2005; 174(7): 4203 - 4209. [Abstract] [Full Text] [PDF]
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G.-X. Yang, Z.-X. Lian, K. Kikuchi, Y.-J. Liu, A. A. Ansari, S. Ikehara, and M. E. Gershwin CD4- Plasmacytoid Dendritic Cells (pDCs) Migrate in Lymph Nodes by CpG Inoculation and Represent a Potent Functional Subset of pDCs J. Immunol., March 15, 2005; 174(6): 3197 - 3203. [Abstract] [Full Text] [PDF]
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G. Hajishengallis, R. I. Tapping, M. H. Martin, H. Nawar, E. A. Lyle, M. W. Russell, and T. D. Connell Toll-Like Receptor 2 Mediates Cellular Activation by the B Subunits of Type II Heat-Labile Enterotoxins Infect. Immun., March 1, 2005; 73(3): 1343 - 1349. [Abstract] [Full Text] [PDF]
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H. Revets, G. Pynaert, J. Grooten, and P. De Baetselier Lipoprotein I, a TLR2/4 Ligand Modulates Th2-Driven Allergic Immune Responses J. Immunol., January 15, 2005; 174(2): 1097 - 1103. [Abstract] [Full Text] [PDF]
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K. U. Saikh, T. L. Kissner, A. Sultana, G. Ruthel, and R. G. Ulrich Human Monocytes Infected with Yersinia pestis Express Cell Surface TLR9 and Differentiate into Dendritic Cells J. Immunol., December 15, 2004; 173(12): 7426 - 7434. [Abstract] [Full Text] [PDF]
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O. A. Skorokhod, M. Alessio, B. Mordmuller, P. Arese, and E. Schwarzer Hemozoin (Malarial Pigment) Inhibits Differentiation and Maturation of Human Monocyte-Derived Dendritic Cells: A Peroxisome Proliferator-Activated Receptor-{gamma}-Mediated Effect J. Immunol., September 15, 2004; 173(6): 4066 - 4074. [Abstract] [Full Text] [PDF]
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S. M. Fortune, A. Solache, A. Jaeger, P. J. Hill, J. T. Belisle, B. R. Bloom, E. J. Rubin, and J. D. Ernst Mycobacterium tuberculosis Inhibits Macrophage Responses to IFN-{gamma} through Myeloid Differentiation Factor 88-Dependent and -Independent Mechanisms J. Immunol., May 15, 2004; 172(10): 6272 - 6280. [Abstract] [Full Text] [PDF]
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S. A. Fulton, S. M. Reba, R. K. Pai, M. Pennini, M. Torres, C. V. Harding, and W. H. Boom Inhibition of Major Histocompatibility Complex II Expression and Antigen Processing in Murine Alveolar Macrophages by Mycobacterium bovis BCG and the 19-Kilodalton Mycobacterial Lipoprotein Infect. Immun., April 1, 2004; 72(4): 2101 - 2110. [Abstract] [Full Text] [PDF]
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T. Okusawa, M. Fujita, J.-i. Nakamura, T. Into, M. Yasuda, A. Yoshimura, Y. Hara, A. Hasebe, D. T. Golenbock, M. Morita, et al. Relationship between Structures and Biological Activities of Mycoplasmal Diacylated Lipopeptides and Their Recognition by Toll-Like Receptors 2 and 6 Infect. Immun., March 1, 2004; 72(3): 1657 - 1665. [Abstract] [Full Text] [PDF]
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 M. B. Drennan, D. Nicolle, V. J. F. Quesniaux, M. Jacobs, N. Allie, J. Mpagi, C. Fremond, H. Wagner, C. Kirschning, and B. Ryffel Toll-Like Receptor 2-Deficient Mice Succumb to Mycobacterium tuberculosis Infection Am. J. Pathol., January 1, 2004; 164(1): 49 - 57. [Abstract] [Full Text] [PDF]
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M. Fujita, T. Into, M. Yasuda, T. Okusawa, S. Hamahira, Y. Kuroki, A. Eto, T. Nisizawa, M. Morita, and K.-i. Shibata Involvement of Leucine Residues at Positions 107, 112, and 115 in a Leucine-Rich Repeat Motif of Human Toll-Like Receptor 2 in the Recognition of Diacylated Lipoproteins and Lipopeptides and Staphylococcus aureus Peptidoglycans J. Immunol., October 1, 2003; 171(7): 3675 - 3683. [Abstract] [Full Text] [PDF]
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J. Colino and C. M. Snapper Two Distinct Mechanisms For Induction of Dendritic Cell Apoptosis in Response to Intact Streptococcus pneumoniae J. Immunol., September 1, 2003; 171(5): 2354 - 2365. [Abstract] [Full Text] [PDF]
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K. Tschoep, T. C. Manning, H. Harlin, C. George, M. Johnson, and T. F. Gajewski Disparate functions of immature and mature human myeloid dendritic cells: implications for dendritic cell-based vaccines J. Leukoc. Biol., July 1, 2003; 74(1): 69 - 80. [Abstract] [Full Text] [PDF]
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K. W. Schjetne, K. M. Thompson, N. Nilsen, T. H. Flo, B. Fleckenstein, J.-G. Iversen, T. Espevik, and B. Bogen Cutting Edge: Link Between Innate and Adaptive Immunity: Toll-Like Receptor 2 Internalizes Antigen for Presentation to CD4+ T Cells and Could Be an Efficient Vaccine Target J. Immunol., July 1, 2003; 171(1): 32 - 36. [Abstract] [Full Text] [PDF]
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T. K. Means, F. Hayashi, K. D. Smith, A. Aderem, and A. D. Luster The Toll-Like Receptor 5 Stimulus Bacterial Flagellin Induces Maturation and Chemokine Production in Human Dendritic Cells J. Immunol., May 15, 2003; 170(10): 5165 - 5175. [Abstract] [Full Text] [PDF]
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D. J. Shedlock, J. K. Whitmire, J. Tan, A. S. MacDonald, R. Ahmed, and H. Shen Role of CD4 T Cell Help and Costimulation in CD8 T Cell Responses During Listeria monocytogenes Infection J. Immunol., February 15, 2003; 170(4): 2053 - 2063. [Abstract] [Full Text] [PDF]
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P. A. Sieling, W. Chung, B. T. Duong, P. J. Godowski, and R. L. Modlin Toll-Like Receptor 2 Ligands as Adjuvants for Human Th1 Responses J. Immunol., January 1, 2003; 170(1): 194 - 200. [Abstract] [Full Text] [PDF]
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V. K. Latchumanan, B. Singh, P. Sharma, and K. Natarajan Mycobacterium tuberculosis Antigens Induce the Differentiation of Dendritic Cells from Bone Marrow J. Immunol., December 15, 2002; 169(12): 6856 - 6864. [Abstract] [Full Text] [PDF]
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D. van der Kleij, E. Latz, J. F. H. M. Brouwers, Y. C. M. Kruize, M. Schmitz, E. A. Kurt-Jones, T. Espevik, E. C. de Jong, M. L. Kapsenberg, D. T. Golenbock, et al. A Novel Host-Parasite Lipid Cross-talk. SCHISTOSOMAL LYSO-PHOSPHATIDYLSERINE ACTIVATES TOLL-LIKE RECEPTOR 2 AND AFFECTS IMMUNE POLARIZATION J. Biol. Chem., December 6, 2002; 277(50): 48122 - 48129. [Abstract] [Full Text] [PDF]
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W. Zeng, S. Ghosh, Y. F. Lau, L. E. Brown, and D. C. Jackson Highly Immunogenic and Totally Synthetic Lipopeptides as Self-Adjuvanting Immunocontraceptive Vaccines J. Immunol., November 1, 2002; 169(9): 4905 - 4912. [Abstract] [Full Text] [PDF]
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S. J. McSorley, B. D. Ehst, Y. Yu, and A. T. Gewirtz Bacterial Flagellin Is an Effective Adjuvant for CD4+ T Cells In Vivo J. Immunol., October 1, 2002; 169(7): 3914 - 3919. [Abstract] [Full Text] [PDF]
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S. E. Applequist, R. P. A. Wallin, and H.-G. Ljunggren Variable expression of Toll-like receptor in murine innate and adaptive immune cell lines Int. Immunol., September 1, 2002; 14(9): 1065 - 1074. [Abstract] [Full Text] [PDF]
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 K. Bieback, E. Lien, I. M. Klagge, E. Avota, J. Schneider-Schaulies, W. P. Duprex, H. Wagner, C. J. Kirschning, V. ter Meulen, and S. Schneider-Schaulies Hemagglutinin Protein of Wild-Type Measles Virus Activates Toll-Like Receptor 2 Signaling J. Virol., July 29, 2002; 76(17): 8729 - 8736. [Abstract] [Full Text] [PDF]
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A. Ouaissi, E. Guilvard, Y. Delneste, G. Caron, G. Magistrelli, N. Herbault, N. Thieblemont, and P. Jeannin The Trypanosoma cruzi Tc52-Released Protein Induces Human Dendritic Cell Maturation, Signals Via Toll-Like Receptor 2, and Confers Protection Against Lethal Infection J. Immunol., June 15, 2002; 168(12): 6366 - 6374. [Abstract] [Full Text] [PDF]
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 K. Edfeldt, J. Swedenborg, G. K. Hansson, and Z.-q. Yan Expression of Toll-Like Receptors in Human Atherosclerotic Lesions: A Possible Pathway for Plaque Activation Circulation, March 12, 2002; 105(10): 1158 - 1161. [Abstract] [Full Text] [PDF]
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 M. F. Lipscomb and B. J. Masten Dendritic Cells: Immune Regulators in Health and Disease Physiol Rev, January 1, 2002; 82(1): 97 - 130. [Abstract] [Full Text] [PDF]
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N. V. Serbina, V. Lazarevic, and J. L. Flynn CD4+ T Cells Are Required for the Development of Cytotoxic CD8+ T Cells During Mycobacterium tuberculosis Infection J. Immunol., December 15, 2001; 167(12): 6991 - 7000. [Abstract] [Full Text] [PDF]
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 N. Kadowaki, S. Ho, S. Antonenko, R. de Waal Malefyt, R. A. Kastelein, F. Bazan, and Y.-J. Liu Subsets of Human Dendritic Cell Precursors Express Different Toll-like Receptors and Respond to Different Microbial Antigens J. Exp. Med., September 17, 2001; 194(6): 863 - 870. [Abstract] [Full Text] [PDF]
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J. R. Bleharski, K. R. Niazi, P. A. Sieling, G. Cheng, and R. L. Modlin Signaling Lymphocytic Activation Molecule Is Expressed on CD40 Ligand-Activated Dendritic Cells and Directly Augments Production of Inflammatory Cytokines J. Immunol., September 15, 2001; 167(6): 3174 - 3181. [Abstract] [Full Text] [PDF]
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R. T. Semnani, H. Sabzevari, R. Iyer, and T. B. Nutman Filarial Antigens Impair the Function of Human Dendritic Cells during Differentiation Infect. Immun., September 1, 2001; 69(9): 5813 - 5822. [Abstract] [Full Text] [PDF]
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R. A. Silva, T. F. Pais, and R. Appelberg Blocking the Receptor for IL-10 Improves Antimycobacterial Chemotherapy and Vaccination J. Immunol., August 1, 2001; 167(3): 1535 - 1541. [Abstract] [Full Text] [PDF]
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C. Neufert, R. K. Pai, E. H. Noss, M. Berger, W. H. Boom, and C. V. Harding Mycobacterium tuberculosis 19-kDa Lipoprotein Promotes Neutrophil Activation J. Immunol., August 1, 2001; 167(3): 1542 - 1549. [Abstract] [Full Text] [PDF]
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E. H. Noss, R. K. Pai, T. J. Sellati, J. D. Radolf, J. Belisle, D. T. Golenbock, W. H. Boom, and C. V. Harding Toll-Like Receptor 2-Dependent Inhibition of Macrophage Class II MHC Expression and Antigen Processing by 19-kDa Lipoprotein of Mycobacterium tuberculosis J. Immunol., July 15, 2001; 167(2): 910 - 918. [Abstract] [Full Text] [PDF]
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), or preincubated with anti-TLR2 (
) or an IgG1 isotype control
Ab (
) for 30 min before the addition of suboptimal concentrations of
the 19-kDa lipopeptide or Pam3CysSerLys4. DC
were matured for an additional 2 days with lipopeptide before the
addition of T cells. C, Proliferation of T cells in MLR
as assessed by [3H]thymidine uptake (cpm). Background
proliferation (cpm) of wells containing T cells alone was subtracted
from cpm obtained in wells containing DC plus T cells. The
concentrations of 19-kDa lipopeptide (5 µg/ml) and
Pam3CysSerLys4 (0.5 µg/ml) were optimal for
demonstrating a block in proliferative responses. D,
IFN-