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CUTTING EDGE |
,§
,§
*
Department of Host Defense, Research Institute for Microbial Diseases, Osaka University, Osaka, Japan;
Department of Immunology and Medical Zoology, Hyogo College of Medicine, Hyogo, Japan;
Department of Immunology, Saga Medical School, Saga, Japan; and
§
Core Research for Evolutional Science and Technology, Japan Science and Technology Corporation, Tokyo, Japan
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResults and DiscussionReferences |
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B was observed in macrophages that became tolerant by
LPS pretreatment, indicating that the proximal event in Toll-like
receptor 4 (TLR4)-MyD88-dependent signaling is affected in tolerant
macrophages. Although TLR4 mRNA expression significantly decreased
within a few hours of LPS pretreatment and returned to the original
level at 24 h, the surface TLR4 expression began to decrease
within 1 h, with a gradual decrease after that, and remained
suppressed over 24 h. A decrease in inflammatory cytokine
production in tolerant macrophages well correlates with down-regulation
of the surface TLR4 expression, which may explain one of the mechanisms
for LPS tolerance. |
Introduction |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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, IL-6, and IL-12, which, when in excess,
leads to serious systemic disorders with a high mortality rate.
Pre-exposure to LPS is shown to induce a reduced sensitivity to
subsequent challenge of LPS. This phenomenon is termed LPS tolerance
(also called LPS hyporesponsiveness or refractoriness). LPS tolerance
was observed in vivo with a decreased febrile response and an escape
from lethality as well as in vitro with a reduced production of
inflammatory cytokines in response to a secondary stimulation with
LPS.
Molecular
mechanisms for LPS tolerance have long been investigated
(1). Several reports described that expression of the LPS
receptor such as CD14 was not altered in LPS-tolerant monocytes and
macrophages (2, 3). In contrast, LPS-signaling pathways
have been shown to be affected in several aspects. It has been reported
that activation of proteins kinase C was compromised in LPS-tolerant
macrophages (4). Several other reports demonstrated that
there is a predominant accumulation of p50/p50 homodimers of NF-B
transcription factors in LPS-tolerant cells (3, 5, 6). In
normal cells, NF-B mainly consists of p50/p65 heterodimers, and this
complex induces expression of target genes. On the other hand, p50/p50
homodimers do not have transactivation property and prevent DNA binding
of p50/p65 heterodimers. Thus, it is hypothesized that LPS tolerance
occurs through alteration of the intracellular signaling pathways of
LPS. However, a precise mechanism for LPS tolerance remains
unclear.
It has recently been demonstrated that the genetically
LPS-hyporesponsive C3H/HeJ mice has a mutation in the Tlr4
gene (7, 8). Toll-like receptor 4
(TLR4)3 is a member of
the Toll-like receptor family, which is an expanding large family in
mammals (9, 10, 11, 12). Drosophila Toll has been shown
to have a critical role in antifungal and antibacterial responses
(13, 14, 15, 16). Several recent reports have also demonstrated
that Toll-like receptors are involved in recognition of bacterial cell
wall components (8, 17, 18, 19, 20, 21, 22, 23). TLR4-deficient mice showed
hyporesponsiveness to LPS, demonstrating that TLR4 is a critical
receptor for LPS signaling (20). The TLR4-mediated
signaling pathway is homologous to that of IL-1 signaling (10, 24, 25). An adaptor molecule MyD88 binds to TLR4. Upon
stimulation, MyD88 recruits IL-1 receptor-associated kinase (IRAK) to
TLR4. IRAK then activates TNFR-associated factor 6 (TRAF6), leading to
activation of NF-B and c-Jun N-terminal kinase. Indeed, MyD88- and
TRAF6-deficient mice displayed hyporesponsiveness to both IL-1 and LPS
(26, 27). Especially, MyD88-deficient mice are almost
completely unresponsive to LPS (26). Thus, analyses of
gene-targeted mice demonstrate that the pathway via TLR4-MyD88 is
essential for LPS response.
In this study, we investigated whether the pathway via TLR4-MyD88 is involved in LPS tolerance. We show that TLR4 expression on the surface of LPS-tolerant macrophages is down-regulated, which explains one of the molecular mechanisms for LPS tolerance.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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Peritoneal macrophages were isolated from C57BL/6J mice essentially as described. Briefly, mice were i.p. injected with 2 ml of 4% thioglycollate. After 3 days of injection, peritoneal exudate cells were isolated by washing the peritoneal cavity with ice-cold HBSS. These cells were incubated for 2 h, and adherent cells were used as peritoneal macrophages.
Phenol-extracted LPS (Escherichia coli O55:B5) was purchased from Sigma (St. Louis, MO). PE-conjugated Abs to IL-6 and IL-12 were purchased from PharMingen (San Diego, CA).
Intracellular staining of macrophages
Peritoneal macrophages were preincubated with 1, 10, or 100 ng/ml LPS for the indicated periods and washed with HBSS twice. Cells were stimulated with 10 ng/ml LPS in the presence of 10 µg/ml brefeldin A (Sigma) for 6 h. Cells were harvested and incubated with 4% paraformaldehyde. Then cells were incubated with PE-conjugated anti-cytokine Abs. Stained cells were analyzed on a FACSCalibur using CellQuest software (Becton Dickinson, San Jose, CA).
Electrophoretic mobility shift assay and in vitro kinase assay
Peritoneal macrophages were incubated with 100 ng/ml LPS for the indicated periods and washed with HBSS. Cells were cultured with culture media alone for 1 h and then stimulated with 10 ng/ml LPS for 10 or 20 min. An electrophoretic mobility shift assay and in vitro kinase assay were performed as described previously (26).
Northern blot analysis
Peritoneal macrophages and RAW264.7 cells were incubated with 100 ng/ml LPS for the indicated periods. Total RNA was extracted with an RNeasy kit (Qiagen, Hilden, Germany). RNA (20 µg) was electrophoresed, transferred to nylon membrane, and hybridized with cDNA probe for mouse TLR4. The same membrane was stripped and rehybridized with GAPDH cDNA probe.
Establishment of a mAb to mouse TLR4
A rat was immunized with Ba/F3 cells expressing mouse TLR4 and MD-2 and used for hybridoma production. The MTS 510 mAb (rat IgG2a/k) that specifically reacted with the immunized transfectant but not with the original Ba/F3 line was selected for further analysis. The mAb was purified from ascites obtained from severe combined immunodeficient mice. Detailed characterization of the mAb will be described elsewhere (29).
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Results and Discussion |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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When mouse peritoneal macrophages were stimulated with 10
ng/ml LPS, these cells displayed a significant increase in production
of inflammatory cytokines such as IL-12 and IL-6 (Fig. 1
). However, when the cells were
preincubated with 100 ng/ml LPS for 1 h, IL-12 production was
dramatically reduced (30.6 to 4.6% positive). When the cells were
preincubated for 24 h, IL-12 production was almost completely
blocked. Pre-exposure to LPS for 1 h also partially reduced
production of IL-6 (15.1 to 8.8%). In addition, production of IL-6
reduced with the lapse of pre-exposure time, and production was
severely reduced after 24 h of pre-exposure (0.8%). Thus,
suppression of inflammatory cytokine production from LPS-pretreated
macrophages was observed in a time-dependent manner.
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, 100 ng/ml LPS dramatically reduced the production of
IL-12 and IL-6. However, when preincubated with 10 ng/ml, the reduction
was partial, and further 1 ng/ml LPS did not cause significant
reduction (Fig. 1). These results suggest that suppression of
inflammatory cytokine production was observed in a dose-dependent
manner. Thus, when we used a system to detect intracellular cytokines,
LPS tolerance does occur in a time-dependent and a dose-dependent
manner. Reduced activation of LPS-signaling cascade after exposure to LPS
The results from intracellular cytokine production indicate that a
24-h exposure to LPS results in almost complete LPS tolerance, but it
is partial after a 3-h exposure. To assess LPS-induced activation of
signaling molecules during LPS tolerance, we analyzed LPS-induced
NF-B activation by gel mobility shift assay (Fig. 2A). In nontreated cells,
DNA-binding activity of NF-B transcription factors was slightly
observed, and LPS stimulation induced a significant increase in their
DNA-binding activity. When pretreated with LPS for 3 h, basal
NF-B activity was still observed; however, LPS-induced increase was
not observed. In the 24-h pretreated cells, neither basal NF-B
activity nor LPS-induced activation was observed. Thus, LPS
pre-exposure significantly reduced NF-B DNA-binding activity.
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B). However, IRAK
activation was not observed in cells pre-exposed to LPS for 3 and
24 h. Thus, LPS-induced IRAK activation was severely reduced in
cells pre-exposed to LPS. We have previously shown that LPS-induced
IRAK activation was not observed in both MyD88-deficient and
TLR4-deficient mice (22, 26). Both strains of knockout
mice are unresponsive to LPS. TLR4 knockout mice also displayed no
LPS-induced NF-B activation. These findings are quite similar
to the data in the macrophages pre-exposed to LPS for 24 h.
Therefore, we hypothesized that tolerant macrophages are affected
in the MyD88-dependent pathway, which is essential for LPS
responsiveness. Decreased expression of TLR4 after exposure to LPS
We analyzed expression of TLR4, an essential signaling receptor
for LPS. The former study demonstrated that LPS stimulation transiently
reduced mRNA expression of TLR4 in the macrophage cell line RAW264.7
(7). We also obtained similar results in RAW264.7 cells.
When cells were stimulated with 100 ng/ml LPS for 2.5 h, TLR4 mRNA
expression was severely reduced; however, the expression returned
to the original level after a 20-h stimulation (Fig. 3A). When mouse peritoneal
macrophages were stimulated with 100 ng/ml LPS, TLR4 mRNA expression
was also transiently suppressed (Fig. 3B). In both types of
cells, TLR4 mRNA expression at 24-h LPS treatment was almost the same
level as that of nontreated cells. Thus, the mRNA expression pattern of
TLR4 seems not to correlate with LPS tolerance.
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B activation and TNF production
(28, 29). Almost all nontreated macrophages were positive
for this Ab (Fig. 4A). The
specificity of this Ab was confirmed by the staining of macrophages
from TLR4 knockout mice. In TLR4 knockout mice, macrophages were
negatively stained with this Ab, indicating that a positive staining by
MTS510 reflects a surface TLR4 expression (Fig. 4A). When
macrophages were stimulated with 100 ng/ml LPS for 1 h, expression
of TLR4 was partially decreased. In addition, the surface expression of
TLR4 was gradually decreased as the culture time continued. At the 24-h
culture period, the surface expression of TLR4 was severely reduced
(Fig. 4B). This was in sharp contrast with the surface
expression of CD14, an LPS-binding receptor. The surface CD14
expression was not significantly changed by LPS treatment, although the
24-h culture induced a slight decrease. When the LPS concentration was
decreased, the reduction of TLR4 expression was partial (Fig. 4C). These results completely parallel with the production
of inflammatory cytokine shown in Fig. 1, indicating that LPS tolerance
occurs mainly by suppression of surface TLR4 expression. We further
analyzed TLR4 expression after treatment with other stimuli such as
IL-1ß and peptidoglycan (PGN), both of which activate the
MyD88-dependent pathway via other receptors than TLR4. IL-1ß and PGN
are shown to utilize the IL-1R and TLR2 as the signaling receptor,
respectively (22). Both stimulations for 24 h did not
affect surface TLR4 expression, indicating that the reduced expression
of surface TLR4 is induced only when macrophages are exposed to LPS,
although all of these stimuli activate the same MyD88-dependent pathway
(Fig. 4D). Interestingly, reduction of surface TLR4
expression after LPS treatment was observed even in C3H/HeJ mice in a
manner similar to that in C3H/HeN mice (Fig. 4E). C3H/HeJ
mice are shown to have a mutation in the Tlr4 gene, leading
to the impaired LPS-mediated MyD88-dependent signaling pathway
(7, 8, 20). These observations indicate that
down-regulation of TLR4 expression occurs independently of the
MyD88-dependent signaling pathway.
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However, there seems to exist other mechanisms for LPS tolerance than
down-regulation of TLR4 expression. Although intracellular production
of inflammatory cytokines was not completely blocked during 1–12-h
pre-exposure, secretion of these cytokines into the culture
supernatants in these periods was not observed (our unpublished data).
This suggests that LPS tolerance does not occur solely due to
suppression of the surface expression of TLR4. There must be some
modifications of intracellular transport or stability of newly
synthesized proteins in the LPS-tolerant macrophages. Interestingly,
the nuclear extract from the macrophages pretreated for 24 h did
not show the basal NF-B-binding activity that is observed in the
nuclear extract from untreated macrophages. Thus, although
down-regulation of TLR4 expression is responsible for LPS tolerance,
other mechanisms along with it seem to operate toward LPS tolerance
during LPS pretreatment.
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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, 3-1 Yamadaoka, Suita, Osaka 565-0871, Japan. E-mail address:
3 Abbreviations used in this paper: TLR4, Toll-like receptor 4; IRAK, IL-1 receptor-associated kinase; TRAF6, TNFR-associated factor 6; PGN, peptidoglycan.
Received for publication November 18, 1999. Accepted for publication February 2, 2000.
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K. A. Powers, K. Szaszi, R. G. Khadaroo, P. S. Tawadros, J. C. Marshall, A. Kapus, and O. D. Rotstein Oxidative stress generated by hemorrhagic shock recruits Toll-like receptor 4 to the plasma membrane in macrophages J. Exp. Med., August 7, 2006; 203(8): 1951 - 1961. [Abstract] [Full Text] [PDF]
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J. D. Turner, R. S. Langley, K. L. Johnston, G. Egerton, S. Wanji, and M. J. Taylor Wolbachia Endosymbiotic Bacteria of Brugia malayi Mediate Macrophage Tolerance to TLR- and CD40-Specific Stimuli in a MyD88/TLR2-Dependent Manner J. Immunol., July 15, 2006; 177(2): 1240 - 1249. [Abstract] [Full Text] [PDF]
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M. K. Mohammad, M. Morran, B. Slotterbeck, D. W. Leaman, Y. Sun, H. v. Grafenstein, S.-C. Hong, and M. F. McInerney Dysregulated Toll-like receptor expression and signaling in bone marrow-derived macrophages at the onset of diabetes in the non-obese diabetic mouse Int. Immunol., July 1, 2006; 18(7): 1101 - 1113. [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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G. Gatti, V. Rivero, R. D. Motrich, and M. Maccioni Prostate epithelial cells can act as early sensors of infection by up-regulating TLR4 expression and proinflammatory mediators upon LPS stimulation J. Leukoc. Biol., May 1, 2006; 79(5): 989 - 998. [Abstract] [Full Text] [PDF]
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 I. Jou, J. H. Lee, S. Y. Park, H. J. Yoon, E.-H. Joe, and E. J. Park Gangliosides Trigger Inflammatory Responses via TLR4 in Brain Glia Am. J. Pathol., May 1, 2006; 168(5): 1619 - 1630. [Abstract] [Full Text] [PDF]
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C. H. Li, J. H. Wang, and H. P. Redmond Bacterial lipoprotein-induced self-tolerance and cross-tolerance to LPS are associated with reduced IRAK-1 expression and MyD88-IRAK complex formation J. Leukoc. Biol., April 1, 2006; 79(4): 867 - 875. [Abstract] [Full Text] [PDF]
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M. Muthukuru and C. W. Cutler Upregulation of Immunoregulatory Src Homology 2 Molecule Containing Inositol Phosphatase and Mononuclear Cell Hyporesponsiveness in Oral Mucosa during Chronic Periodontitis Infect. Immun., February 1, 2006; 74(2): 1431 - 1435. [Abstract] [Full Text] [PDF]
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C. Tsatsanis, A. Androulidaki, T. Alissafi, I. Charalampopoulos, E. Dermitzaki, T. Roger, A. Gravanis, and A. N. Margioris Corticotropin-Releasing Factor and the Urocortins Induce the Expression of TLR4 in Macrophages via Activation of the Transcription Factors PU.1 and AP-1 J. Immunol., February 1, 2006; 176(3): 1869 - 1877. [Abstract] [Full Text] [PDF]
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Q. Zhao, X. Wang, L. D. Nelin, Y. Yao, R. Matta, M. E. Manson, R. S. Baliga, X. Meng, C. V. Smith, J. A. Bauer, et al. MAP kinase phosphatase 1 controls innate immune responses and suppresses endotoxic shock J. Exp. Med., January 23, 2006; 203(1): 131 - 140. [Abstract] [Full Text] [PDF]
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H. Yumoto, H.-H. Chou, Y. Takahashi, M. Davey, F. C. Gibson III, and C. A. Genco Sensitization of Human Aortic Endothelial Cells to Lipopolysaccharide via Regulation of Toll-Like Receptor 4 by Bacterial Fimbria-Dependent Invasion Infect. Immun., December 1, 2005; 73(12): 8050 - 8059. [Abstract] [Full Text] [PDF]
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L. C. Parker, E. C. Jones, L. R. Prince, S. K. Dower, M. K. B. Whyte, and I. Sabroe Endotoxin tolerance induces selective alterations in neutrophil function J. Leukoc. Biol., December 1, 2005; 78(6): 1301 - 1305. [Abstract] [Full Text] [PDF]
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 P. S. Thorne, K. Kulhankova, M. Yin, R. Cohn, S. J. Arbes Jr., and D. C. Zeldin Endotoxin Exposure Is a Risk Factor for Asthma: The National Survey of Endotoxin in United States Housing Am. J. Respir. Crit. Care Med., December 1, 2005; 172(11): 1371 - 1377. [Abstract] [Full Text] [PDF]
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 W. Jiang, R. Sun, H. Wei, and Z. Tian Toll-like receptor 3 ligand attenuates LPS-induced liver injury by down-regulation of toll-like receptor 4 expression on macrophages PNAS, November 22, 2005; 102(47): 17077 - 17082. [Abstract] [Full Text] [PDF]
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D. M. Underhill, E. Rossnagle, C. A. Lowell, and R. M. Simmons Dectin-1 activates Syk tyrosine kinase in a dynamic subset of macrophages for reactive oxygen production Blood, October 1, 2005; 106(7): 2543 - 2550. [Abstract] [Full Text] [PDF]
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 T. V. Pedchenko, G. Y. Park, M. Joo, T. S. Blackwell, and J. W. Christman Inducible binding of PU.1 and interacting proteins to the Toll-like receptor 4 promoter during endotoxemia Am J Physiol Lung Cell Mol Physiol, September 1, 2005; 289(3): L429 - L437. [Abstract] [Full Text] [PDF]
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H.-S. Mun, F. Aosai, K. Norose, L.-X. Piao, H. Fang, S. Akira, and A. Yano Toll-Like Receptor 4 Mediates Tolerance in Macrophages Stimulated with Toxoplasma gondii-Derived Heat Shock Protein 70 Infect. Immun., August 1, 2005; 73(8): 4634 - 4642. [Abstract] [Full Text] [PDF]
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D. S. Weiss, K. Takeda, S. Akira, A. Zychlinsky, and E. Moreno MyD88, but Not Toll-Like Receptors 4 and 2, Is Required for Efficient Clearance of Brucella abortus Infect. Immun., August 1, 2005; 73(8): 5137 - 5143. [Abstract] [Full Text] [PDF]
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S. Yang, N. Takahashi, T. Yamashita, N. Sato, M. Takahashi, M. Mogi, T. Uematsu, Y. Kobayashi, Y. Nakamichi, K. Takeda, et al. Muramyl Dipeptide Enhances Osteoclast Formation Induced by Lipopolysaccharide, IL-1{alpha}, and TNF-{alpha} through Nucleotide-Binding Oligomerization Domain 2-Mediated Signaling in Osteoblasts J. Immunol., August 1, 2005; 175(3): 1956 - 1964. [Abstract] [Full Text] [PDF]
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C. Feterowski, A. Novotny, S. Kaiser-Moore, P. F. Muhlradt, T. Rossmann-Bloeck, M. Rump, B. Holzmann, and H. Weighardt Attenuated pathogenesis of polymicrobial peritonitis in mice after TLR2 agonist pre-treatment involves ST2 up-regulation Int. Immunol., August 1, 2005; 17(8): 1035 - 1046. [Abstract] [Full Text] [PDF]
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L. C. Parker, M. K. B. Whyte, S. K. Dower, and I. Sabroe The expression and roles of Toll-like receptors in the biology of the human neutrophil J. Leukoc. Biol., June 1, 2005; 77(6): 886 - 892. [Abstract] [Full Text] [PDF]
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A. S. Damazo, S. Yona, F. D'Acquisto, R. J. Flower, S. M. Oliani, and M. Perretti Critical Protective Role for Annexin 1 Gene Expression in the Endotoxemic Murine Microcirculation Am. J. Pathol., June 1, 2005; 166(6): 1607 - 1617. [Abstract] [Full Text] [PDF]
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J. Wang, R. Alvarez, G. Roderiquez, E. Guan, Q. Caldwell, J. Wang, M. Phelan, and M. A. Norcross CpG-Independent Synergistic Induction of {beta}-Chemokines and a Dendritic Cell Phenotype by Orthophosphorothioate Oligodeoxynucleotides and Granulocyte-Macrophage Colony-Stimulating Factor in Elutriated Human Primary Monocytes J. Immunol., May 15, 2005; 174(10): 6113 - 6121. [Abstract] [Full Text] [PDF]
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D. Y. Jung, H. Lee, B.-Y. Jung, J. Ock, M.-S. Lee, W.-H. Lee, and K. Suk TLR4, but Not TLR2, Signals Autoregulatory Apoptosis of Cultured Microglia: A Critical Role of IFN-{beta} as a Decision Maker J. Immunol., May 15, 2005; 174(10): 6467 - 6476. [Abstract] [Full Text] [PDF]
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A. Uhrig, R. Banafsche, M. Kremer, S. Hegenbarth, A. Hamann, M. Neurath, G. Gerken, A. Limmer, and P. A. Knolle Development and functional consequences of LPS tolerance in sinusoidal endothelial cells of the liver J. Leukoc. Biol., May 1, 2005; 77(5): 626 - 633. [Abstract] [Full Text] [PDF]
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P. A. Hopkins, J. D. Fraser, A. C. Pridmore, H. H. Russell, R. C. Read, and S. Sriskandan Superantigen recognition by HLA class II on monocytes up-regulates toll-like receptor 4 and enhances proinflammatory responses to endotoxin Blood, May 1, 2005; 105(9): 3655 - 3662. [Abstract] [Full Text] [PDF]
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M. W. Hornef and C. Bogdan The role of epithelial Toll-like receptor expression in host defense and microbial tolerance Innate Immunity, April 1, 2005; 11(2): 124 - 128. [Abstract] [PDF]
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P. A. Ruiz, A. Shkoda, S. C. Kim, R. B. Sartor, and D. Haller IL-10 Gene-Deficient Mice Lack TGF-{beta}/Smad Signaling and Fail to Inhibit Proinflammatory Gene Expression in Intestinal Epithelial Cells after the Colonization with Colitogenic Enterococcus faecalis J. Immunol., March 1, 2005; 174(5): 2990 - 2999. [Abstract] [Full Text] [PDF]
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A. De Creus, M. Abe, A. H. Lau, H. Hackstein, G. Raimondi, and A. W. Thomson Low TLR4 Expression by Liver Dendritic Cells Correlates with Reduced Capacity to Activate Allogeneic T Cells in Response to Endotoxin J. Immunol., February 15, 2005; 174(4): 2037 - 2045. [Abstract] [Full Text] [PDF]
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M. Muthukuru, R. Jotwani, and C. W. Cutler Oral Mucosal Endotoxin Tolerance Induction in Chronic Periodontitis Infect. Immun., February 1, 2005; 73(2): 687 - 694. [Abstract] [Full Text] [PDF]
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M. R.-E.-I. Benhnia, D. Wroblewski, M. N. Akhtar, R. A. Patel, W. Lavezzi, S. C. Gangloff, S. M. Goyert, M. J. Caimano, J. D. Radolf, and T. J. Sellati Signaling through CD14 Attenuates the Inflammatory Response to Borrelia burgdorferi, the Agent of Lyme Disease J. Immunol., February 1, 2005; 174(3): 1539 - 1548. [Abstract] [Full Text] [PDF]
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J. Mostecki, B. M. Showalter, and P. B. Rothman Early Growth Response-1 Regulates Lipopolysaccharide-induced Suppressor of Cytokine Signaling-1 Transcription J. Biol. Chem., January 28, 2005; 280(4): 2596 - 2605. [Abstract] [Full Text] [PDF]
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G. C. O'Brien, J. H. Wang, and H. P. Redmond Bacterial Lipoprotein Induces Resistance to Gram-Negative Sepsis in TLR4-Deficient Mice via Enhanced Bacterial Clearance J. Immunol., January 15, 2005; 174(2): 1020 - 1026. [Abstract] [Full Text] [PDF]
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K. Takeda and S. Akira Toll-like receptors in innate immunity Int. Immunol., January 1, 2005; 17(1): 1 - 14. [Abstract] [Full Text] [PDF]
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G. Grutz New insights into the molecular mechanism of interleukin-10-mediated immunosuppression J. Leukoc. Biol., January 1, 2005; 77(1): 3 - 15. [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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S. Shirasawa, S. Sugiyama, I. Baba, J. Inokuchi, S. Sekine, K. Ogino, Y. Kawamura, T. Dohi, M. Fujimoto, and T. Sasazuki Dermatitis due to epiregulin deficiency and a critical role of epiregulin in immune-related responses of keratinocyte and macrophage PNAS, September 21, 2004; 101(38): 13921 - 13926. [Abstract] [Full Text] [PDF]
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N. Nilsen, U. Nonstad, N. Khan, C. F. Knetter, S. Akira, A. Sundan, T. Espevik, and E. Lien Lipopolysaccharide and Double-stranded RNA Up-regulate Toll-like Receptor 2 Independently of Myeloid Differentiation Factor 88 J. Biol. Chem., September 17, 2004; 279(38): 39727 - 39735. [Abstract] [Full Text] [PDF]
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M. Siedlar, M. Frankenberger, E. Benkhart, T. Espevik, M. Quirling, K. Brand, M. Zembala, and L. Ziegler-Heitbrock Tolerance Induced by the Lipopeptide Pam3Cys Is Due to Ablation of IL-1R-Associated Kinase-1 J. Immunol., August 15, 2004; 173(4): 2736 - 2745. [Abstract] [Full Text] [PDF]
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E. Lorenz, D. C. Chemotti, K. Vandal, and P. A. Tessier Toll-Like Receptor 2 Represses Nonpilus Adhesin-Induced Signaling in Acute Infections with the Pseudomonas aeruginosa pilA Mutant Infect. Immun., August 1, 2004; 72(8): 4561 - 4569. [Abstract] [Full Text] [PDF]
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J. Dai, N. J. Megjugorac, S. B. Amrute, and P. Fitzgerald-Bocarsly Regulation of IFN Regulatory Factor-7 and IFN-{alpha} Production by Enveloped Virus and Lipopolysaccharide in Human Plasmacytoid Dendritic Cells J. Immunol., August 1, 2004; 173(3): 1535 - 1548. [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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 S.-I. Hayashi, M. Tsuneto, T. Yamada, M. Nose, M. Yoshino, L. D. Shultz, and H. Yamazaki Lipopolysaccharide-Induced Osteoclastogenesis in Src Homology 2-Domain Phosphatase-1-Deficient Viable Motheaten Mice Endocrinology, June 1, 2004; 145(6): 2721 - 2729. [Abstract] [Full Text] [PDF]
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S. L. McCoy, S. E. Kurtz, F. A. Hausman, D. R. Trune, R. M. Bennett, and S. H. Hefeneider Activation of RAW264.7 Macrophages by Bacterial DNA and Lipopolysaccharide Increases Cell Surface DNA Binding and Internalization J. Biol. Chem., April 23, 2004; 279(17): 17217 - 17223. [Abstract] [Full Text] [PDF]
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 Y. Masubuchi and T. Horie ENDOTOXIN-MEDIATED DISTURBANCE OF HEPATIC CYTOCHROME P450 FUNCTION AND DEVELOPMENT OF ENDOTOXIN TOLERANCE IN THE RAT MODEL OF DEXTRAN SULFATE SODIUM-INDUCED EXPERIMENTAL COLITIS Drug Metab. Dispos., April 1, 2004; 32(4): 437 - 441. [Abstract] [Full Text] [PDF]
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Hongkuan Fan and J. A. Cook Review: Molecular mechanisms of endotoxin tolerance Innate Immunity, April 1, 2004; 10(2): 71 - 84. [Abstract] [PDF]
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D. S. Weiss, B. Raupach, K. Takeda, S. Akira, and A. Zychlinsky Toll-Like Receptors Are Temporally Involved in Host Defense J. Immunol., April 1, 2004; 172(7): 4463 - 4469. [Abstract] [Full Text] [PDF]
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T. J. Murphy, H. M. Paterson, J. A. Mannick, and J. A. Lederer Injury, sepsis, and the regulation of Toll-like receptor responses J. Leukoc. Biol., March 1, 2004; 75(3): 400 - 407. [Abstract] [Full Text] [PDF]
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K. S. Kobayashi and R. A. Flavell Shielding the double-edged sword: negative regulation of the innate immune system J. Leukoc. Biol., March 1, 2004; 75(3): 428 - 433. [Abstract] [Full Text] [PDF]
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L. Kim, B. A. Butcher, and E. Y. Denkers Toxoplasma gondii Interferes with Lipopolysaccharide-Induced Mitogen-Activated Protein Kinase Activation by Mechanisms Distinct from Endotoxin Tolerance J. Immunol., March 1, 2004; 172(5): 3003 - 3010. [Abstract] [Full Text] [PDF]
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K. Nakayama, S. Okugawa, S. Yanagimoto, T. Kitazawa, K. Tsukada, M. Kawada, S. Kimura, K. Hirai, Y. Takagaki, and Y. Ota Involvement of IRAK-M in Peptidoglycan-induced Tolerance in Macrophages J. Biol. Chem., February 20, 2004; 279(8): 6629 - 6634. [Abstract] [Full Text] [PDF]
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G. Hajishengallis and R. J. Genco Downregulation of the DNA-Binding Activity of Nuclear Factor-{kappa}B p65 Subunit in Porphyromonas gingivalis Fimbria-Induced Tolerance Infect. Immun., February 1, 2004; 72(2): 1188 - 1191. [Abstract] [Full Text] [PDF]
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D. Burzyn, J. C. Rassa, D. Kim, I. Nepomnaschy, S. R. Ross, and I. Piazzon Toll-Like Receptor 4-Dependent Activation of Dendritic Cells by a Retrovirus J. Virol., January 15, 2004; 78(2): 576 - 584. [Abstract] [Full Text] [PDF]
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E. LeBouder, J. E. Rey-Nores, N. K. Rushmere, M. Grigorov, S. D. Lawn, M. Affolter, G. E. Griffin, P. Ferrara, E. J. Schiffrin, B. P. Morgan, et al. Soluble Forms of Toll-Like Receptor (TLR)2 Capable of Modulating TLR2 Signaling Are Present in Human Plasma and Breast Milk J. Immunol., December 15, 2003; 171(12): 6680 - 6689. [Abstract] [Full Text] [PDF]
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D. Frleta, R. J. Noelle, and W. F. Wade CD40-mediated up-regulation of Toll-like receptor 4-MD2 complex on the surface of murine dendritic cells J. Leukoc. Biol., December 1, 2003; 74(6): 1064 - 1073. [Abstract] [Full Text]
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S.-I. Hayashi, T. Yamada, M. Tsuneto, T. Yamane, M. Takahashi, L. D. Shultz, and H. Yamazaki Distinct Osteoclast Precursors in the Bone Marrow and Extramedullary Organs Characterized by Responsiveness to Toll-Like Receptor Ligands and TNF-{alpha} J. Immunol., November 15, 2003; 171(10): 5130 - 5139. [Abstract] [Full Text] [PDF]
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