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International Immunology, Vol. 13, No. 7, 933-940, July 2001
© 2001 Japanese Society for Immunology

Discrimination of bacterial lipoproteins by Toll-like receptor 6

Osamu Takeuchi1,2, Taro Kawai1,2, Peter F. Mühlradt3, Michael Morr3, Justin D. Radolf4, Arturo Zychlinsky5, Kiyoshi Takeda1,2 and Shizuo Akira1,2 1 Department of Host Defense, Research Institute for Microbial Diseases, Osaka University, and
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. Biol. Chem.Home page
U. Buwitt-Beckmann, H. Heine, K.-H. Wiesmuller, G. Jung, R. Brock, S. Akira, and A. J. Ulmer
TLR1- and TLR6-independent Recognition of Bacterial Lipopeptides
J. Biol. Chem., April 7, 2006; 281(14): 9049 - 9057.
[Abstract] [Full Text] [PDF]


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IOVSHome page
F.-S. X. Yu and L. D. Hazlett
Toll-like Receptors and the Eye.
Invest. Ophthalmol. Vis. Sci., April 1, 2006; 47(4): 1255 - 1263.
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Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
B. Schmeck, S. Huber, K. Moog, J. Zahlten, A. C. Hocke, B. Opitz, S. Hammerschmidt, T. J. Mitchell, M. Kracht, S. Rosseau, et al.
Pneumococci induced TLR- and Rac1-dependent NF-{kappa}B-recruitment to the IL-8 promoter in lung epithelial cells
Am J Physiol Lung Cell Mol Physiol, April 1, 2006; 290(4): L730 - L737.
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J. Biol. Chem.Home page
S. Suram, G. D. Brown, M. Ghosh, S. Gordon, R. Loper, P. R. Taylor, S. Akira, S. Uematsu, D. L. Williams, and C. C. Leslie
Regulation of Cytosolic Phospholipase A2 Activation and Cyclooxygenase 2 Expression in Macrophages by the beta-Glucan Receptor
J. Biol. Chem., March 3, 2006; 281(9): 5506 - 5514.
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J. Leukoc. Biol.Home page
T. Basler, S. Jeckstadt, P. Valentin-Weigand, and R. Goethe
Mycobacterium paratuberculosis, Mycobacterium smegmatis, and lipopolysaccharide induce different transcriptional and post-transcriptional regulation of the IRG1 gene in murine macrophages
J. Leukoc. Biol., March 1, 2006; 79(3): 628 - 638.
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J. Immunol.Home page
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.
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J. Immunol.Home page
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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J. Immunol.Home page
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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Int ImmunolHome page
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.
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Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
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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J. Biol. Chem.Home page
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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Int ImmunolHome page
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.
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Innate ImmunityHome page
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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J. Immunol.Home page
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.
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Appl. Environ. Microbiol.Home page
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.
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Infect. Immun.Home page
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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Am. J. Respir. Crit. Care Med.Home page
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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J. Immunol.Home page
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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Infect. Immun.Home page
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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Clin. Microbiol. Rev.Home page
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.
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J. Immunol.Home page
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.
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J. Immunol.Home page
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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JNCI J Natl Cancer InstHome page
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.
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Infect. Immun.Home page
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.
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J. Immunol.Home page
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.
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Infect. Immun.Home page
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.
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J. Lipid Res.Home page
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.
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Infect. Immun.Home page
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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IOVSHome page
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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J. Immunol.Home page
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.
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Infect. Immun.Home page
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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Int ImmunolHome page
K. Takeda and S. Akira
Toll-like receptors in innate immunity
Int. Immunol., January 1, 2005; 17(1): 1 - 14.
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Infect. Immun.Home page
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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Innate ImmunityHome page
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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Proc. Natl. Acad. Sci. USAHome page
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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Toxicol SciHome page
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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