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*
Pulmonary Center, Boston University School of Medicine, and
Infectious Disease Section, Boston Medical Center, Boston, MA 02118
Recent studies have implicated a family of mammalian Toll-like receptors (TLR) in the activation of macrophages by Gram-negative and Gram-positive bacterial products. We have previously shown that different TLR proteins mediate cellular activation by the distinct CD14 ligands Gram-negative bacterial LPS and mycobacterial glycolipid lipoarabinomannan (LAM). Here we show that viable Mycobacterium tuberculosis bacilli activated both Chinese hamster ovary cells and murine macrophages that overexpressed either TLR2 or TLR4. This contrasted with Gram-positive bacteria and Mycobacterium avium, which activated cells via TLR2 but not TLR4. Both virulent and attenuated strains of M. tuberculosis could activate the cells in a TLR-dependent manner. Neither membrane-bound nor soluble CD14 was required for bacilli to activate cells in a TLR-dependent manner. We also assessed whether LAM was the mycobacterial cell wall component responsible for TLR-dependent cellular activation by M. tuberculosis. We found that TLR2, but not TLR4, could confer responsiveness to LAM isolated from rapidly growing mycobacteria. In contrast, LAM isolated from M. tuberculosis or Mycobacterium bovis bacillus Calmette-Guérin failed to induce TLR-dependent activation. Lastly, both soluble and cell wall-associated mycobacterial factors were capable of mediating activation via distinct TLR proteins. A soluble heat-stable and protease-resistant factor was found to mediate TLR2-dependent activation, whereas a heat-sensitive cell-associated mycobacterial factor mediated TLR4-dependent activation. Together, our data demonstrate that Toll-like receptors can mediate cellular activation by M. tuberculosis via CD14-independent ligands that are distinct from the mycobacterial cell wall glycolipid LAM.
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Z. Darieva, E. B. Lasunskaia, M. N. N. Campos, T. L. Kipnis, and W. D. da Silva Activation of phosphatidylinositol 3-kinase and c-Jun-N-terminal kinase cascades enhances NF-{kappa}B-dependent gene transcription in BCG-stimulated macrophages through promotion of p65/p300 binding J. Leukoc. Biol., April 1, 2004; 75(4): 689 - 697. [Abstract] [Full Text] [PDF]
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V. J. Quesniaux, D. M. Nicolle, D. Torres, L. Kremer, Y. Guerardel, J. Nigou, G. Puzo, F. Erard, and B. Ryffel Toll-Like Receptor 2 (TLR2)-Dependent-Positive and TLR2-Independent-Negative Regulation of Proinflammatory Cytokines by Mycobacterial Lipomannans J. Immunol., April 1, 2004; 172(7): 4425 - 4434. [Abstract] [Full Text] [PDF]
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F. A. W. Verreck, T. de Boer, D. M. L. Langenberg, M. A. Hoeve, M. Kramer, E. Vaisberg, R. Kastelein, A. Kolk, R. de Waal-Malefyt, and T. H. M. Ottenhoff Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria PNAS, March 30, 2004; 101(13): 4560 - 4565. [Abstract] [Full Text] [PDF]
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R. E. Weir, G. F. Black, H. M. Dockrell, S. Floyd, P. E. M. Fine, S. D. Chaguluka, S. Stenson, E. King, B. Nazareth, D. K. Warndorff, et al. Mycobacterial Purified Protein Derivatives Stimulate Innate Immunity: Malawians Show Enhanced Tumor Necrosis Factor Alpha, Interleukin-1{beta} (IL-1{beta}), and IL-10 Responses Compared to Those of Adolescents in the United Kingdom Infect. Immun., March 1, 2004; 72(3): 1807 - 1811. [Abstract] [Full Text] [PDF]
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 J. Branger, J. C. Leemans, S. Florquin, S. Weijer, P. Speelman, and T. van der Poll Toll-like receptor 4 plays a protective role in pulmonary tuberculosis in mice Int. Immunol., March 1, 2004; 16(3): 509 - 516. [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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 B.-C. Chiu, C. M. Freeman, V. R. Stolberg, J. S. Hu, E. Komuniecki, and S. W. Chensue The Innate Pulmonary Granuloma: Characterization and Demonstration of Dendritic Cell Recruitment and Function Am. J. Pathol., March 1, 2004; 164(3): 1021 - 1030. [Abstract] [Full Text] [PDF]
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 A.C. Ogus, B. Yoldas, T. Ozdemir, A. Uguz, S. Olcen, I. Keser, M. Coskun, A. Cilli, and O. Yegin The Arg753Gln polymorphism of the human Toll-like receptor 2 gene in tuberculosis disease Eur. Respir. J., February 1, 2004; 23(2): 219 - 223. [Abstract] [Full Text] [PDF]
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M. A. Campos, G. M. S. Rosinha, I. C. Almeida, X. S. Salgueiro, B. W. Jarvis, G. A. Splitter, N. Qureshi, O. Bruna-Romero, R. T. Gazzinelli, and S. C. Oliveira Role of Toll-Like Receptor 4 in Induction of Cell-Mediated Immunity and Resistance to Brucella abortus Infection in Mice Infect. Immun., January 1, 2004; 72(1): 176 - 186. [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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G. R. Alvarez, B. S. Zwilling, and W. P. Lafuse Mycobacterium avium Inhibition of IFN-{gamma} Signaling in Mouse Macrophages: Toll-Like Receptor 2 Stimulation Increases Expression of Dominant-Negative STAT1{beta} by mRNA Stabilization J. Immunol., December 15, 2003; 171(12): 6766 - 6773. [Abstract] [Full Text] [PDF]
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A.-S. W. Moller, R. Ovstebo, A.-B. Westvik, G. B. Joo, K.-B. F. Haug, and P. Kierulf Effects of bacterial cell wall components (PAMPs) on the expression of monocyte chemoattractant protein-1 (MCP-1), macrophage inflammatory protein-1{alpha} (MIP-1{alpha}) and the chemokine receptor CCR2 by purified human blood monocytes Innate Immunity, December 1, 2003; 9(6): 349 - 360. [Abstract] [PDF]
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C. L. Fuller, J. L. Flynn, and T. A. Reinhart In Situ Study of Abundant Expression of Proinflammatory Chemokines and Cytokines in Pulmonary Granulomas That Develop in Cynomolgus Macaques Experimentally Infected with Mycobacterium tuberculosis Infect. Immun., December 1, 2003; 71(12): 7023 - 7034. [Abstract] [Full Text] [PDF]
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P. L. Fisette, S. Ram, J. M. Andersen, W. Guo, and R. R. Ingalls The Lip Lipoprotein from Neisseria gonorrhoeae Stimulates Cytokine Release and NF-{kappa}B Activation in Epithelial Cells in a Toll-like Receptor 2-dependent Manner J. Biol. Chem., November 21, 2003; 278(47): 46252 - 46260. [Abstract] [Full Text] [PDF]
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C. G. Feng, C. A. Scanga, C. M. Collazo-Custodio, A. W. Cheever, S. Hieny, P. Caspar, and A. Sher Mice Lacking Myeloid Differentiation Factor 88 Display Profound Defects in Host Resistance and Immune Responses to Mycobacterium avium Infection Not Exhibited by Toll-Like Receptor 2 (TLR2)- and TLR4-Deficient Animals J. Immunol., November 1, 2003; 171(9): 4758 - 4764. [Abstract] [Full Text] [PDF]
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K. J. C. Gibson, L. Eggeling, W. N. Maughan, K. Krumbach, S. S. Gurcha, J. Nigou, G. Puzo, H. Sahm, and G. S. Besra Disruption of Cg-Ppm1, a Polyprenyl Monophosphomannose Synthase, and the Generation of Lipoglycan-less Mutants in Corynebacterium glutamicum J. Biol. Chem., October 17, 2003; 278(42): 40842 - 40850. [Abstract] [Full Text] [PDF]
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S. Shi, C. Nathan, D. Schnappinger, J. Drenkow, M. Fuortes, E. Block, A. Ding, T. R. Gingeras, G. Schoolnik, S. Akira, et al. MyD88 Primes Macrophages for Full-Scale Activation by Interferon-{gamma} yet Mediates Few Responses to Mycobacterium tuberculosis J. Exp. Med., October 6, 2003; 198(7): 987 - 997. [Abstract] [Full Text] [PDF]
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S. K. Sukumaran, H. Shimada, and N. V. Prasadarao Entry and Intracellular Replication of Escherichia coli K1 in Macrophages Require Expression of Outer Membrane Protein A Infect. Immun., October 1, 2003; 71(10): 5951 - 5961. [Abstract] [Full Text] [PDF]
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A. Kariyone, T. Tamura, H. Kano, Y. Iwakura, K. Takeda, S. Akira, and K. Takatsu Immunogenicity of Peptide-25 of Ag85B in Th1 development: role of IFN-{gamma} Int. Immunol., October 1, 2003; 15(10): 1183 - 1194. [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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Y. Guerardel, E. Maes, V. Briken, F. Chirat, Y. Leroy, C. Locht, G. Strecker, and L. Kremer Lipomannan and Lipoarabinomannan from a Clinical Isolate of Mycobacterium kansasii: NOVEL STRUCTURAL FEATURES AND APOPTOSIS-INDUCING PROPERTIES J. Biol. Chem., September 19, 2003; 278(38): 36637 - 36651. [Abstract] [Full Text] [PDF]
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 F. Sandor, E. Latz, F. Re, L. Mandell, G. Repik, D. T. Golenbock, T. Espevik, E. A. Kurt-Jones, and R. W. Finberg Importance of extra- and intracellular domains of TLR1 and TLR2 in NF{kappa}B signaling J. Cell Biol., September 15, 2003; 162(6): 1099 - 1110. [Abstract] [Full Text] [PDF]
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M. Gilleron, V. F. J. Quesniaux, and G. Puzo Acylation State of the Phosphatidylinositol Hexamannosides from Mycobacterium bovis Bacillus Calmette Guerin and Mycobacterium tuberculosis H37Rv and Its Implication in Toll-like Receptor Response J. Biol. Chem., August 8, 2003; 278(32): 29880 - 29889. [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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A. J. Gehring, R. E. Rojas, D. H. Canaday, D. L. Lakey, C. V. Harding, and W. H. Boom The Mycobacterium tuberculosis 19-Kilodalton Lipoprotein Inhibits Gamma Interferon-Regulated HLA-DR and Fc{gamma}R1 on Human Macrophages through Toll-Like Receptor 2 Infect. Immun., August 1, 2003; 71(8): 4487 - 4497. [Abstract] [Full Text] [PDF]
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R. I. Tapping and P. S. Tobias Mycobacterial lipoarabinomannan mediates physical interactions between TLR1 and TLR2 to induce signaling Innate Immunity, August 1, 2003; 9(4): 264 - 268. [Abstract] [PDF]
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 J. Indrigo, R. L. Hunter Jr, and J. K. Actor Cord factor trehalose 6,6'-dimycolate (TDM) mediates trafficking events during mycobacterial infection of murine macrophages Microbiology, August 1, 2003; 149(8): 2049 - 2059. [Abstract] [Full Text] [PDF]
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K. A. Heldwein, M. D. Liang, T. K. Andresen, K. E. Thomas, A. M. Marty, N. Cuesta, S. N. Vogel, and M. J. Fenton TLR2 and TLR4 serve distinct roles in the host immune response against Mycobacterium bovis BCG J. Leukoc. Biol., August 1, 2003; 74(2): 277 - 286. [Abstract] [Full Text] [PDF]
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A. Bafica, C. A. Scanga, M. L. Schito, S. Hieny, and A. Sher Cutting Edge: In Vivo Induction of Integrated HIV-1 Expression by Mycobacteria Is Critically Dependent on Toll-Like Receptor 2 J. Immunol., August 1, 2003; 171(3): 1123 - 1127. [Abstract] [Full Text] [PDF]
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A. A. R. Tobian, N. S. Potter, L. Ramachandra, R. K. Pai, M. Convery, W. H. Boom, and C. V. Harding Alternate Class I MHC Antigen Processing Is Inhibited by Toll-Like Receptor Signaling Pathogen-Associated Molecular Patterns: Mycobacterium tuberculosis 19-kDa Lipoprotein, CpG DNA, and Lipopolysaccharide J. Immunol., August 1, 2003; 171(3): 1413 - 1422. [Abstract] [Full Text] [PDF]
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E. S. Van Amersfoort, T. J. C. Van Berkel, and J. Kuiper Receptors, Mediators, and Mechanisms Involved in Bacterial Sepsis and Septic Shock Clin. Microbiol. Rev., July 1, 2003; 16(3): 379 - 414. [Abstract] [Full Text] [PDF]
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A. B. Kamath, J. Alt, H. Debbabi, and S. M. Behar Toll-Like Receptor 4-Defective C3H/HeJ Mice Are Not More Susceptible than Other C3H Substrains to Infection with Mycobacterium tuberculosis Infect. Immun., July 1, 2003; 71(7): 4112 - 4118. [Abstract] [Full Text] [PDF]
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G. Fenhalls, G. R. Squires, L. Stevens-Muller, J. Bezuidenhout, G. Amphlett, K. Duncan, and P. T. Lukey Associations between Toll-Like Receptors and Interleukin-4 in the Lungs of Patients with Tuberculosis Am. J. Respir. Cell Mol. Biol., July 1, 2003; 29(1): 28 - 38. [Abstract] [Full Text] [PDF]
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M. Sato, H. Sano, D. Iwaki, K. Kudo, M. Konishi, H. Takahashi, T. Takahashi, H. Imaizumi, Y. Asai, and Y. Kuroki Direct Binding of Toll-Like Receptor 2 to Zymosan, and Zymosan-Induced NF-{kappa}B Activation and TNF-{alpha} Secretion Are Down-Regulated by Lung Collectin Surfactant Protein A J. Immunol., July 1, 2003; 171(1): 417 - 425. [Abstract] [Full Text] [PDF]
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S. Heinz, V. Haehnel, M. Karaghiosoff, L. Schwarzfischer, M. Muller, S. W. Krause, and M. Rehli Species-specific Regulation of Toll-like Receptor 3 Genes in Men and Mice J. Biol. Chem., June 6, 2003; 278(24): 21502 - 21509. [Abstract] [Full Text] [PDF]
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O. Equils, M. L. Schito, H. Karahashi, Z. Madak, A. Yarali, K. S. Michelsen, A. Sher, and M. Arditi Toll-Like Receptor 2 (TLR2) and TLR9 Signaling Results in HIV-Long Terminal Repeat Trans-Activation and HIV Replication in HIV-1 Transgenic Mouse Spleen Cells: Implications of Simultaneous Activation of TLRs on HIV Replication J. Immunol., May 15, 2003; 170(10): 5159 - 5164. [Abstract] [Full Text] [PDF]
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