International Immunology, Vol. 13, No. 7, 933-940,
July 2001
© 2001 Japanese Society for Immunology
Discrimination of bacterial lipoproteins by Toll-like receptor 6
2 Core Research for Evolutional Science and Technology (CREST) of Japan Science and Technology Corp., 3-1 Yamada-oka, Suita, Osaka 565-0871, Japan
3 Immunobiology Research Group, Gesellschaft für Biotechnologische Forschung, Mascheroderweg 1, 38124 Braunschweig, Germany
4 Center for Microbial Pathogenesis, University of Connecticut Health Center, 263 Farmington Avenue, Farmington, CT 06030, USA
5 Skirball Institute and Department of Microbiology, New York University School of Medicine, 540 First Avenue, New York, NY 10016, USA
Correspondence to: S. Akira
Bacterial lipoproteins (BLP) trigger immune responses via Toll-like receptor 2 (TLR2) and their immunostimulatory properties are attributed to the presence of a lipoylated N-terminus. Most BLP are triacylated at the N-terminus cysteine residue, but mycoplasmal macrophage-activating lipopeptide-2 kD (MALP-2) is only diacylated. Here we show that TLR6-deficient (TLR6–/–) cells are unresponsive to MALP-2 but retain their normal responses to lipopeptides of other bacterial origins. Reconstitution experiments in TLR2–/– TLR6–/– embryonic fibroblasts reveal that co-expression of TLR2 and TLR6 is absolutely required for MALP-2 responsiveness. Taken together, these results show that TLR6 recognizes MALP-2 cooperatively with TLR2, and appears to discriminate between the N-terminal lipoylated structures of MALP-2 and lipopeptides derived from other bacteria.
Keywords: cytokine, inflammatory mediator, knockout, macrophage, monocyte, transgenic
Transmitting editor: T. Watanabe
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J.-S. Chang, J. F. Huggett, K. Dheda, L. U. Kim, A. Zumla, and G. A. W. Rook Myobacterium tuberculosis Induces Selective Up-Regulation of TLRs in the Mononuclear Leukocytes of Patients with Active Pulmonary Tuberculosis. J. Immunol., March 1, 2006; 176(5): 3010 - 3018. [Abstract] [Full Text] [PDF]
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N. Banaiee, E. Z. Kincaid, U. Buchwald, W. R. Jacobs Jr., and J. D. Ernst Potent Inhibition of Macrophage Responses to IFN-{gamma} by Live Virulent Mycobacterium tuberculosis Is Independent of Mature Mycobacterial Lipoproteins but Dependent on TLR2. J. Immunol., March 1, 2006; 176(5): 3019 - 3027. [Abstract] [Full Text] [PDF]
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P. Massari, A. Visintin, J. Gunawardana, K. A. Halmen, C. A. King, D. T. Golenbock, and L. M. Wetzler Meningococcal Porin PorB Binds to TLR2 and Requires TLR1 for Signaling J. Immunol., February 15, 2006; 176(4): 2373 - 2380. [Abstract] [Full Text] [PDF]
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M. Hashimoto, K. Tawaratsumida, H. Kariya, K. Aoyama, T. Tamura, and Y. Suda Lipoprotein is a predominant Toll-like receptor 2 ligand in Staphylococcus aureus cell wall components Int. Immunol., February 1, 2006; 18(2): 355 - 362. [Abstract] [Full Text] [PDF]
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 T. Hubschle, J. Mutze, P. F. Muhlradt, S. Korte, R. Gerstberger, and J. Roth Pyrexia, anorexia, adipsia, and depressed motor activity in rats during systemic inflammation induced by the Toll-like receptors-2 and -6 agonists MALP-2 and FSL-1 Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2006; 290(1): R180 - R187. [Abstract] [Full Text] [PDF]
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K. O. Omueti, J. M. Beyer, C. M. Johnson, E. A. Lyle, and R. I. Tapping Domain Exchange between Human Toll-like Receptors 1 and 6 Reveals a Region Required for Lipopeptide Discrimination J. Biol. Chem., November 4, 2005; 280(44): 36616 - 36625. [Abstract] [Full Text] [PDF]
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K. Honda, H. Yanai, A. Takaoka, and T. Taniguchi Regulation of the type I IFN induction: a current view Int. Immunol., November 1, 2005; 17(11): 1367 - 1378. [Abstract] [Full Text] [PDF]
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R. Dziarski and D. Gupta Peptidoglycan recognition in innate immunity Innate Immunity, October 1, 2005; 11(5): 304 - 310. [Abstract] [PDF]
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T. Shimizu, Y. Kida, and K. Kuwano A Dipalmitoylated Lipoprotein from Mycoplasma pneumoniae Activates NF-{kappa}B through TLR1, TLR2, and TLR6 J. Immunol., October 1, 2005; 175(7): 4641 - 4646. [Abstract] [Full Text] [PDF]
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 N. Verjan, I. Hirono, and T. Aoki Genetic Loci of Major Antigenic Protein Genes of Edwardsiella tarda Appl. Envir. Microbiol., September 1, 2005; 71(9): 5654 - 5658. [Abstract] [Full Text] [PDF]
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B. C. Cole, H.-H. Mu, N. D. Pennock, A. Hasebe, F. V. Chan, L. R. Washburn, and M. R. Peltier Isolation and Partial Purification of Macrophage- and Dendritic Cell-Activating Components from Mycoplasma arthritidis: Association with Organism Virulence and Involvement with Toll-Like Receptor 2 Infect. Immun., September 1, 2005; 73(9): 6039 - 6047. [Abstract] [Full Text] [PDF]
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 H. Weigt, C. Nassenstein, T. Tschernig, P. F. Muhlradt, N. Krug, and A. Braun Efficacy of Macrophage-activating Lipopeptide-2 Combined with Interferon-{gamma} in a Murine Asthma Model Am. J. Respir. Crit. Care Med., September 1, 2005; 172(5): 566 - 572. [Abstract] [Full Text] [PDF]
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N. W. J. Schroder, I. Diterich, A. Zinke, J. Eckert, C. Draing, V. v. Baehr, D. Hassler, S. Priem, K. Hahn, K. S. Michelsen, et al. Heterozygous Arg753Gln Polymorphism of Human TLR-2 Impairs Immune Activation by Borrelia burgdorferi and Protects from Late Stage Lyme Disease J. Immunol., August 15, 2005; 175(4): 2534 - 2540. [Abstract] [Full Text] [PDF]
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R. Dziarski and D. Gupta Staphylococcus aureus Peptidoglycan Is a Toll-Like Receptor 2 Activator: a Reevaluation Infect. Immun., August 1, 2005; 73(8): 5212 - 5216. [Abstract] [Full Text] [PDF]
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 B. Fournier and D. J. Philpott Recognition of Staphylococcus aureus by the Innate Immune System Clin. Microbiol. Rev., July 1, 2005; 18(3): 521 - 540. [Abstract] [Full Text] [PDF]
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S. Borsutzky, K. Kretschmer, P. D. Becker, P. F. Muhlradt, C. J. Kirschning, S. Weiss, and C. A. Guzman The Mucosal Adjuvant Macrophage-Activating Lipopeptide-2 Directly Stimulates B Lymphocytes via the TLR2 without the Need of Accessory Cells J. Immunol., May 15, 2005; 174(10): 6308 - 6313. [Abstract] [Full Text] [PDF]
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P. Henneke, S. Morath, S. Uematsu, S. Weichert, M. Pfitzenmaier, O. Takeuchi, A. Muller, C. Poyart, S. Akira, R. Berner, et al. Role of Lipoteichoic Acid in the Phagocyte Response to Group B Streptococcus J. Immunol., May 15, 2005; 174(10): 6449 - 6455. [Abstract] [Full Text] [PDF]
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 J. Sun, F. Wiklund, S. L. Zheng, B. Chang, K. Balter, L. Li, J.-E. Johansson, G. Li, H.-O. Adami, W. Liu, et al. Sequence Variants in Toll-Like Receptor Gene Cluster (TLR6-TLR1-TLR10) and Prostate Cancer Risk J Natl Cancer Inst, April 6, 2005; 97(7): 525 - 532. [Abstract] [Full Text] [PDF]
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H. Stoll, J. Dengjel, C. Nerz, and F. Gotz Staphylococcus aureus Deficient in Lipidation of Prelipoproteins Is Attenuated in Growth and Immune Activation Infect. Immun., April 1, 2005; 73(4): 2411 - 2423. [Abstract] [Full Text] [PDF]
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T. E. Singleton, P. Massari, and L. M. Wetzler Neisserial Porin-Induced Dendritic Cell Activation Is MyD88 and TLR2 Dependent J. Immunol., March 15, 2005; 174(6): 3545 - 3550. [Abstract] [Full Text] [PDF]
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S. Totemeyer, P. Kaiser, D. J. Maskell, and C. E. Bryant Sublethal Infection of C57BL/6 Mice with Salmonella enterica Serovar Typhimurium Leads to an Increase in Levels of Toll-Like Receptor 1 (TLR1), TLR2, and TLR9 mRNA as Well as a Decrease in Levels of TLR6 mRNA in Infected Organs Infect. Immun., March 1, 2005; 73(3): 1873 - 1878. [Abstract] [Full Text] [PDF]
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 P. Tobias and L. K. Curtiss Thematic review series: The Immune System and Atherogenesis. Paying the price for pathogen protection: toll receptors in atherogenesis J. Lipid Res., March 1, 2005; 46(3): 404 - 411. [Abstract] [Full Text] [PDF]
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Q. Zhou, T. Desta, M. Fenton, D. T. Graves, and S. Amar Cytokine Profiling of Macrophages Exposed to Porphyromonas gingivalis, Its Lipopolysaccharide, or Its FimA Protein Infect. Immun., February 1, 2005; 73(2): 935 - 943. [Abstract] [Full Text] [PDF]
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A. C. Johnson, F. P. Heinzel, E. Diaconu, Y. Sun, A. G. Hise, D. Golenbock, J. H. Lass, and E. Pearlman Activation of Toll-Like Receptor (TLR)2, TLR4, and TLR9 in the Mammalian Cornea Induces MyD88-Dependent Corneal Inflammation Invest. Ophthalmol. Vis. Sci., February 1, 2005; 46(2): 589 - 595. [Abstract] [Full Text] [PDF]
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Y. Nakao, K. Funami, S. Kikkawa, M. Taniguchi, M. Nishiguchi, Y. Fukumori, T. Seya, and M. Matsumoto Surface-Expressed TLR6 Participates in the Recognition of Diacylated Lipopeptide and Peptidoglycan in Human Cells J. Immunol., February 1, 2005; 174(3): 1566 - 1573. [Abstract] [Full Text] [PDF]
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A. Q. Khan, Q. Chen, Z.-Q. Wu, J. C. Paton, and C. M. Snapper Both Innate Immunity and Type 1 Humoral Immunity to Streptococcus pneumoniae Are Mediated by MyD88 but Differ in Their Relative Levels of Dependence on Toll-Like Receptor 2 Infect. Immun., January 1, 2005; 73(1): 298 - 307. [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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D. Nicolle, C. Fremond, X. Pichon, A. Bouchot, I. Maillet, B. Ryffel, and V. J. F. Quesniaux Long-Term Control of Mycobacterium bovis BCG Infection in the Absence of Toll-Like Receptors (TLRs): Investigation of TLR2-, TLR6-, or TLR2-TLR4-Deficient Mice Infect. Immun., December 1, 2004; 72(12): 6994 - 7004. [Abstract] [Full Text] [PDF]
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E. A. Kurt-Jones, F. Sandor, Y. Ortiz, G. N. Bowen, S. L. Counter, T. C. Wang, and R. W. Finberg Use of murine embryonic fibroblasts to define Toll-like receptor activation and specificity Innate Immunity, December 1, 2004; 10(6): 419 - 424. [Abstract] [PDF]
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D. C. Jackson, Y. F. Lau, T. Le, A. Suhrbier, G. Deliyannis, C. Cheers, C. Smith, W. Zeng, and L. E. Brown A totally synthetic vaccine of generic structure that targets Toll-like receptor 2 on dendritic cells and promotes antibody or cytotoxic T cell responses PNAS, October 26, 2004; 101(43): 15440 - 15445. [Abstract] [Full Text] [PDF]
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 F. Gao, A. Barchowsky, A. A. Nemec, and J. P. Fabisiak Microbial Stimulation by Mycoplasma fermentans Synergistically Amplifies IL-6 Release by Human Lung Fibroblasts in Response to Residual Oil Fly Ash (ROFA) and Nickel Toxicol. Sci., October 1, 2004; 81(2): 467 - 479. [Abstract] [Full Text] [PDF]
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