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The Journal of Immunology, 2000, 164: 5564-5574.
Copyright © 2000 by The American Association of Immunologists

Inhibition of Lipopolysaccharide-Induced Signal Transduction in Endotoxin-Tolerized Mouse Macrophages: Dysregulation of Cytokine, Chemokine, and Toll-Like Receptor 2 and 4 Gene Expression1

Andrei E. Medvedev, Karen M. Kopydlowski and Stefanie N. Vogel2

Department of Microbiology and Immunology, Uniformed Services University of the Health Sciences, Bethesda, MD 20814

In this study, the effect of in vitro endotoxin tolerance on LPS-induced mitogen-activated protein kinase activation, transcription factor induction, and cytokine, chemokine, and Toll-like receptor (TLR) 2 and 4 gene expression, as well as the involvement of TNF and IL-1 signaling pathways in tolerance, were examined. Pretreatment of mouse macrophages with LPS inhibited phosphorylation of the extracellular signal-regulated kinases, c-Jun NH2-terminal kinases, and p38 kinase; degradation of I-{kappa}B{alpha} (inhibitory protein that dissociates from NF-{kappa}B) and I-{kappa}Bß; and activation of the transcription factors NF-{kappa}B and AP-1 in response to subsequent LPS stimulation. These changes were accompanied by suppression of LPS-induced expression of mRNA for GM-CSF, IFN-{gamma}-inducible protein-10, KC, JE/monocyte chemoattractant protein-1, macrophage-inflammatory protein-1ß, and macrophage-inflammatory protein-2, with concurrent inhibition of chemokine secretion. In contrast to control cells, endotoxin-tolerant macrophages exhibited an increased basal level of TLR2 mRNA, and failed to increase levels of TLR2 mRNA or to down-regulate TLR4 gene expression upon restimulation with LPS. As judged by transcription factor activation, LPS and IL-1 were found to induce a state of cross-tolerance against each other, while no such reciprocal effect was seen for LPS and TNF-{alpha}. In addition, macrophages from TNFR I/II double knockout mice were LPS tolerizable, and blocking of endogenous TNF-{alpha} with TNFR-Fc fusion protein did not affect the capacity of LPS to tolerize macrophages. These data extend our understanding of LPS-signaling mechanisms that are inhibited in endotoxin-tolerized macrophages and suggest that endotoxin tolerance might result from impaired expression and/or functions of common signaling intermediates involved in LPS and IL-1 signaling.




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N. Qureshi, P.-Y. Perera, J. Shen, G. Zhang, A. Lenschat, G. Splitter, D. C. Morrison, and S. N. Vogel
The Proteasome as a Lipopolysaccharide-Binding Protein in Macrophages: Differential Effects of Proteasome Inhibition on Lipopolysaccharide-Induced Signaling Events
J. Immunol., August 1, 2003; 171(3): 1515 - 1525.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
H. Ogawa, P. Rafiee, J. Heidemann, P. J. Fisher, N. A. Johnson, M. F. Otterson, B. Kalyanaraman, K. A. Pritchard Jr., and D. G. Binion
Mechanisms of Endotoxin Tolerance in Human Intestinal Microvascular Endothelial Cells
J. Immunol., June 15, 2003; 170(12): 5956 - 5964.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
S. B. Mizel, A. N. Honko, M. A. Moors, P. S. Smith, and A. P. West
Induction of Macrophage Nitric Oxide Production by Gram-Negative Flagellin Involves Signaling Via Heteromeric Toll-Like Receptor 5/Toll-Like Receptor 4 Complexes
J. Immunol., June 15, 2003; 170(12): 6217 - 6223.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
J. Pocock, C. Gomez-Guerrero, S. Harendza, M. Ayoub, P. Hernandez-Vargas, G. Zahner, R. A. K. Stahl, and F. Thaiss
Differential Activation of NF-{kappa}B, AP-1, and C/EBP in Endotoxin-Tolerant Rats: Mechanisms for In Vivo Regulation of Glomerular RANTES/CCL5 Expression
J. Immunol., June 15, 2003; 170(12): 6280 - 6291.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
Y. Tsutsumi-Ishii and I. Nagaoka
Modulation of Human {beta}-Defensin-2 Transcription in Pulmonary Epithelial Cells by Lipopolysaccharide-Stimulated Mononuclear Phagocytes Via Proinflammatory Cytokine Production
J. Immunol., April 15, 2003; 170(8): 4226 - 4236.
[Abstract] [Full Text] [PDF]


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Infect. Immun.Home page
J. D. Schilling, S. M. Martin, D. A. Hunstad, K. P. Patel, M. A. Mulvey, S. S. Justice, R. G. Lorenz, and S. J. Hultgren
CD14- and Toll-Like Receptor-Dependent Activation of Bladder Epithelial Cells by Lipopolysaccharide and Type 1 Piliated Escherichia coli
Infect. Immun., March 1, 2003; 71(3): 1470 - 1480.
[Abstract] [Full Text] [PDF]


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Innate ImmunityHome page
A. E. Medvedev and S. N. Vogel
Overexpression of CD14, TLR4, and MD-2 in HEK 293T cells does not prevent induction of in vitro endotoxin tolerance
Innate Immunity, February 1, 2003; 9(1): 60 - 64.
[Abstract] [PDF]


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BloodHome page
H. Tsujimura, T. Tamura, C. Gongora, J. Aliberti, C. Reis e Sousa, A. Sher, and K. Ozato
ICSBP/IRF-8 retrovirus transduction rescues dendritic cell development in vitro
Blood, February 1, 2003; 101(3): 961 - 969.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
S.-J. Yeo, J.-G. Yoon, S.-C. Hong, and A.-K. Yi
CpG DNA Induces Self and Cross-Hyporesponsiveness of RAW264.7 Cells in Response to CpG DNA and Lipopolysaccharide: Alterations in IL-1 Receptor-Associated Kinase Expression
J. Immunol., January 15, 2003; 170(2): 1052 - 1061.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
M. A. Dobrovolskaia, A. E. Medvedev, K. E. Thomas, N. Cuesta, V. Toshchakov, T. Ren, M. J. Cody, S. M. Michalek, N. R. Rice, and S. N. Vogel
Induction of In Vitro Reprogramming by Toll-Like Receptor (TLR)2 and TLR4 Agonists in Murine Macrophages: Effects of TLR "Homotolerance" Versus "Heterotolerance" on NF-{kappa}B Signaling Pathway Components
J. Immunol., January 1, 2003; 170(1): 508 - 519.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
I. Friedrich, J. Spillner, E.-X. Lu, M. Barnscheidt, O. Kuss, A. Sablotzki, F. U. Schade, and J. Borgermann
Induction of endotoxin tolerance improves lung function after warm ischemia in dogs
Am J Physiol Lung Cell Mol Physiol, January 1, 2003; 284(1): L224 - L231.
[Abstract] [Full Text] [PDF]


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Infect. Immun.Home page
G. Hajishengallis, M. Martin, R. E. Schifferle, and R. J. Genco
Counteracting Interactions between Lipopolysaccharide Molecules with Differential Activation of Toll-Like Receptors
Infect. Immun., December 1, 2002; 70(12): 6658 - 6664.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
A. E. Medvedev, A. Lentschat, L. M. Wahl, D. T. Golenbock, and S. N. Vogel
Dysregulation of LPS-Induced Toll-Like Receptor 4-MyD88 Complex Formation and IL-1 Receptor-Associated Kinase 1 Activation in Endotoxin-Tolerant Cells
J. Immunol., November 1, 2002; 169(9): 5209 - 5216.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
R. D. Erwert, R. K. Winn, J. M. Harlan, and D. D. Bannerman
Shiga-like Toxin Inhibition of FLICE-like Inhibitory Protein Expression Sensitizes Endothelial Cells to Bacterial Lipopolysaccharide-induced Apoptosis
J. Biol. Chem., October 18, 2002; 277(43): 40567 - 40574.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
J. H. Wang, M. Doyle, B. J. Manning, Q. Di Wu, S. Blankson, and H. P. Redmond
Induction of Bacterial Lipoprotein Tolerance Is Associated with Suppression of Toll-like Receptor 2 Expression
J. Biol. Chem., September 20, 2002; 277(39): 36068 - 36075.
[Abstract] [Full Text] [PDF]


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Infect. Immun.Home page
K. Ruckdeschel and K. Richter
Lipopolysaccharide Desensitization of Macrophages Provides Protection against Yersinia enterocolitica-Induced Apoptosis
Infect. Immun., September 1, 2002; 70(9): 5259 - 5264.
[Abstract] [Full Text] [PDF]


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BloodHome page
E. A. Kurt-Jones, L. Mandell, C. Whitney, A. Padgett, K. Gosselin, P. E. Newburger, and R. W. Finberg
Role of Toll-like receptor 2 (TLR2) in neutrophil activation: GM-CSF enhances TLR2 expression and TLR2-mediated interleukin 8 responses in neutrophils
Blood, August 13, 2002; 100(5): 1860 - 1868.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
M. Adib-Conquy and J.-M. Cavaillon
Gamma Interferon and Granulocyte/Monocyte Colony-stimulating Factor Prevent Endotoxin Tolerance in Human Monocytes by Promoting Interleukin-1 Receptor-associated Kinase Expression and Its Association to MyD88 and Not by Modulating TLR4 Expression
J. Biol. Chem., July 26, 2002; 277(31): 27927 - 27934.
[Abstract] [Full Text] [PDF]


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Int ImmunolHome page
S. Sato, O. Takeuchi, T. Fujita, H. Tomizawa, K. Takeda, and S. Akira
A variety of microbial components induce tolerance to lipopolysaccharide by differentially affecting MyD88-dependent and -independent pathways
Int. Immunol., July 1, 2002; 14(7): 783 - 791.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
R. Jacinto, T. Hartung, C. McCall, and L. Li
Lipopolysaccharide- and Lipoteichoic Acid-Induced Tolerance and Cross-Tolerance: Distinct Alterations in IL-1 Receptor-Associated Kinase
J. Immunol., June 15, 2002; 168(12): 6136 - 6141.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
S. B. Mizel and J. A. Snipes
Gram-negative Flagellin-induced Self-tolerance Is Associated with a Block in Interleukin-1 Receptor-associated Kinase Release from Toll-like Receptor 5
J. Biol. Chem., June 14, 2002; 277(25): 22414 - 22420.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
J. Fan, A. Kapus, P. A. Marsden, Y. H. Li, G. Oreopoulos, J. C. Marshall, S. Frantz, R. A. Kelly, R. Medzhitov, and O. D. Rotstein
Regulation of Toll-Like Receptor 4 Expression in the Lung Following Hemorrhagic Shock and Lipopolysaccharide
J. Immunol., May 15, 2002; 168(10): 5252 - 5259.
[Abstract] [Full Text] [PDF]


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CVIHome page
T. K. Varma, C. Y. Lin, T. E. Toliver-Kinsky, and E. R. Sherwood
Endotoxin-Induced Gamma Interferon Production: Contributing Cell Types and Key Regulatory Factors
Clin. Vaccine Immunol., May 1, 2002; 9(3): 530 - 543.
[Abstract] [Full Text] [PDF]


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Eur Respir JHome page
E. Israel-Assayag and Y. Cormier
Adaptation to organic dust exposure: a potential role of l-selectin shedding?
Eur. Respir. J., May 1, 2002; 19(5): 833 - 837.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
I. Sabroe, E. C. Jones, L. R. Usher, M. K. B. Whyte, and S. K. Dower
Toll-Like Receptor (TLR)2 and TLR4 in Human Peripheral Blood Granulocytes: A Critical Role for Monocytes in Leukocyte Lipopolysaccharide Responses
J. Immunol., May 1, 2002; 168(9): 4701 - 4710.
[Abstract] [Full Text] [PDF]


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BloodHome page
D. Bosisio, N. Polentarutti, M. Sironi, S. Bernasconi, K. Miyake, G. R. Webb, M. U. Martin, A. Mantovani, and M. Muzio
Stimulation of toll-like receptor 4 expression in human mononuclear phagocytes by interferon-gamma : a molecular basis for priming and synergism with bacterial lipopolysaccharide
Blood, May 1, 2002; 99(9): 3427 - 3431.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
J. Hu, R. Jacinto, C. McCall, and L. Li
Regulation of IL-1 Receptor-Associated Kinases by Lipopolysaccharide
J. Immunol., April 15, 2002; 168(8): 3910 - 3914.
[Abstract] [Full Text] [PDF]


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Innate ImmunityHome page
A. S. Cross
Invited review: Endotoxin tolerance -- current concepts in historical perspective
Innate Immunity, April 1, 2002; 8(2): 83 - 98.
[PDF]


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Infect. Immun.Home page
G. Sebastiani, V. Blais, V. Sancho, S. N. Vogel, M. M. Stevenson, P. Gros, J.-M. Lapointe, S. Rivest, and D. Malo
Host Immune Response to Salmonella enterica Serovar Typhimurium Infection in Mice Derived from Wild Strains
Infect. Immun., April 1, 2002; 70(4): 1997 - 2009.
[Abstract] [Full Text] [PDF]


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Innate ImmunityHome page
B. K. Yoza, J. Y.-Q. Hu, and C. E. McCall
Inhibition of histone deacetylation enhances endotoxin-stimulated transcription but does not reverse endotoxin tolerance
Innate Immunity, April 1, 2002; 8(2): 109 - 114.
[Abstract] [PDF]


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CVIHome page
G. Hajishengallis, M. Martin, H. T. Sojar, A. Sharma, R. E. Schifferle, E. DeNardin, M. W. Russell, and R. J. Genco
Dependence of Bacterial Protein Adhesins on Toll-Like Receptors for Proinflammatory Cytokine Induction
Clin. Vaccine Immunol., March 1, 2002; 9(2): 403 - 411.
[Abstract] [Full Text] [PDF]


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JEMHome page
M. W. Hornef, T. Frisan, A. Vandewalle, S. Normark, and A. Richter-Dahlfors
Toll-like Receptor 4 Resides in the Golgi Apparatus and Colocalizes with Internalized Lipopolysaccharide in Intestinal Epithelial Cells
J. Exp. Med., February 25, 2002; 195(5): 559 - 570.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
J. C. Rassa, J. L. Meyers, Y. Zhang, R. Kudaravalli, and S. R. Ross
Murine retroviruses activate B cells via interaction with toll-like receptor 4
PNAS, February 19, 2002; 99(4): 2281 - 2286.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
M. J. Sweet, C. C. Campbell, D. P. Sester, D. Xu, R. C. McDonald, K. J. Stacey, D. A. Hume, and F. Y. Liew
Colony-Stimulating Factor-1 Suppresses Responses to CpG DNA and Expression of Toll-Like Receptor 9 but Enhances Responses to Lipopolysaccharide in Murine Macrophages
J. Immunol., January 1, 2002; 168(1): 392 - 399.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
M. Ferlito, O. G. Romanenko, S. Ashton, F. Squadrito, P. V. Halushka, and J. A. Cook
Effect of cross-tolerance between endotoxin and TNF-{alpha} or IL-1{beta} on cellular signaling and mediator production
J. Leukoc. Biol., November 1, 2001; 70(5): 821 - 829.
[Abstract] [Full Text] [PDF]




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