Gram-positive bacterial lipoglycans based on a glycosylated diacylglycerol lipid anchor are microbe-associated molecular patterns recognized by TLR2

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Blanc, Landry ^a,b   Castanier, Romain ^a,b   Mishra, Arun K ^c   Ray, Aurélie ^a,b,f   Besra, Gurdyal S ^d   Sutcliffe, Iain ^e   Vercellone, Alain ^a,b   Nigou, Jérôme ^a,b  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^d UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^e NORTHUMBRIA UNIVERSITY   (United Kingdom)

^f TRANSGENE S A   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 ANTIGEN; DIACYLGLYCEROL; GLYCOLIPID; INTERLEUKIN 6; INTERLEUKIN 8; LIPOGLYCAN; LIPOTEICHOIC ACID; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; LIPOPOLYSACCHARIDE; PATTERN RECOGNITION RECEPTOR; PROTEIN BINDING;

ANTIGEN RECOGNITION; ARTICLE; BACTERIAL IMMUNITY; CONTROLLED STUDY; CORYNEBACTERIUM GLUTAMICUM; CYTOKINE PRODUCTION; EMBRYO; HUMAN; HUMAN CELL; INNATE IMMUNITY; MACROPHAGE; MICROCOCCUS LUTEUS; NONHUMAN; PROTEIN EXPRESSION; ROTHIA MUCILAGINOSA; SIGNAL TRANSDUCTION; CELL LINE; GRAM POSITIVE BACTERIUM; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MACROPHAGE ACTIVATION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

CELL LINE; GRAM-POSITIVE BACTERIA; HOST-PATHOGEN INTERACTIONS; HUMANS; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES; PROTEIN BINDING; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2;

EID: 84896704198     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081593     Document Type: Article

References (40)

1. Medzhitov R (2007) Recognition of microorganisms and activation of the immune response. Nature 449: 819-826.
2. Iwasaki A, Medzhitov R (2010) Regulation of adaptive immunity by the innate immune system. Science 327: 291-295.
3. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124: 783-801. (Pubitemid 43261452)
4. Moresco EM, LaVine D, Beutler B (2011) Toll-like receptors. Curr Biol 21: R488-493.
5. Thomas CJ, Schroder K (2013) Pattern recognition receptor function in neutrophils. Trends Immunol 34: 317-328.
6. O'Neill LA, Golenbock D, Bowie AG (2013) The history of Toll-like receptors - redefining innate immunity. Nat Rev Immunol 13: 453-460.
7. Zahringer U, Lindner B, Inamura S, Heine H, Alexander C (2008) TLR2 - promiscuous or specific? A critical re-evaluation of a receptor expressing apparent broad specificity. Immunobiology 213: 205-224.
8. Ray A, Cot M, Puzo G, Gilleron M, Nigou J (2013) Bacterial cell wall macroamphiphiles: pathogen-/microbe-associated molecular patterns detected by mammalian innate immune system. Biochimie 95: 33-42.
9. Rahman O, Dover LG, Sutcliffe IC (2009) Lipoteichoic acid biosynthesis: two steps forwards, one step sideways? Trends Microbiol 17: 219-225.
10. Fischer W (1994) Lipoteichoic acids and lipoglycans. In:, editors. Bacterial cell wall. Amsterdam, The Netherlands.: Elsevier Science B.V. pp. 199-215.
11. Jin MS, Lee JO (2008) Structures of the toll-like receptor family and its ligand complexes. Immunity 29: 182-191.
12. Kang JY, Lee JO (2011) Structural biology of the Toll-like receptor family. Annu Rev Biochem 80: 917-941.
13. Ozinsky A, Underhill DM, Fontenot JD, Hajjar AM, Smith KD, et al. (2000) The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proc Natl Acad Sci U S A 97: 13766-13771.
14. Takeuchi O, Kawai T, Muhlradt PF, Morr M, Radolf JD, et al. (2001) Discrimination of bacterial lipoproteins by Toll-like receptor 6. Int Immunol 13: 933-940. (Pubitemid 32685205)
15. Takeuchi O, Sato S, Horiuchi T, Hoshino K, Takeda K, et al. (2002) Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins. J Immunol 169: 10-14. (Pubitemid 34686113)
16. Jin MS, Kim SE, Heo JY, Lee ME, Kim HM, et al. (2007) Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130: 1071-1082. (Pubitemid 47410281)
17. Kang JY, Nan X, Jin MS, Youn SJ, Ryu YH, et al. (2009) Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6 heterodimer. Immunity 31: 873-884.
18. Sutcliffe IC, Shaw N (1991) Atypical lipoteichoic acids of gram-positive bacteria. J Bacteriol 173: 7065-7069.
19. Sutcliffe IC (1994) The lipoteichoic acids and lipoglycans of Gram-positive Bacteria: A chemotaxonomic perspective. System Appl Microbiol 17: 467-480.
20. Chatterjee D, Khoo KH (1998) Mycobacterial lipoarabinomannan: an extraordinary lipoheteroglycan with profound physiological effects. Glycobiology 8: 113-120. (Pubitemid 28098211)
21. Nigou J, Gilleron M, Puzo G (2003) Lipoarabinomannans: from structure to biosynthesis. Biochimie 85: 153-166. (Pubitemid 36625990)
22. Torrelles JB, Schlesinger LS (2010) Diversity in Mycobacterium tuberculosis mannosylated cell wall determinants impacts adaptation to the host. Tuberculosis (Edinb) 90: 84-93.
23. Briken V, Porcelli SA, Besra GS, Kremer L (2004) Mycobacterial lipoarabinomannan and related lipoglycans: from biogenesis to modulation of the immune response. Mol Microbiol 53: 391-403. (Pubitemid 38998163)
24. Henneke P, Morath S, Uematsu S, Weichert S, Pfitzenmaier M, et al. (2005) Role of lipoteichoic acid in the phagocyte response to group B streptococcus. J Immunol 174: 6449-6455. (Pubitemid 40663839)
25. Bunk S, Sigel S, Metzdorf D, Sharif O, Triantafilou K, et al. (2010) Internalization and coreceptor expression are critical for TLR2-mediated recognition of lipoteichoic acid in human peripheral blood. J Immunol 185: 3708-3717.
26. Gilleron M, Nigou J, Nicolle D, Quesniaux V, Puzo G (2006) The acylation state of mycobacterial lipomannans modulates innate immunity response through toll-like receptor 2. Chem Biol 13: 39-47. (Pubitemid 43099923)
27. Pakkiri LS, Waechter CJ (2005) Dimannosyldiacylglycerol serves as a lipid anchor precursor in the assembly of the membrane-associated lipomannan in Micrococcus luteus . Glycobiology 15: 291-302. (Pubitemid 40347355)
28. Pakkiri LS, Wolucka BA, Lubert EJ, Waechter CJ (2004) Structural and topological studies on the lipid-mediated assembly of a membrane-associated lipomannan in Micrococcus luteus. Glycobiology 14: 73-81. (Pubitemid 38159410)
29. Sutcliffe IC, Old LA (1995) Stomatococcus mucilaginosus produces a mannose-containing lipoglycan rather than lipoteichoic acid. Arch Microbiol 163: 70-75.
30. Tatituri RV, Illarionov PA, Dover LG, Nigou J, Gilleron M, et al. (2007) Inactivation of Corynebacterium glutamicum NCgl0452 and the role of MgtA in the biosynthesis of a novel mannosylated glycolipid involved in lipomannan biosynthesis. J Biol Chem 282: 4561-4572. (Pubitemid 47100964)
31. Mishra AK, Klein C, Gurcha SS, Alderwick LJ, Babu P, et al. (2008) Structural characterization and functional properties of a novel lipomannan variant isolated from a Corynebacterium glutamicum pimB' mutant. Antonie Van Leeuwenhoek 94: 277-287.
32. Krishna S, Ray A, Dubey SK, Larrouy-Maumus G, Chalut C, et al. (2011) Lipoglycans contribute to innate immune detection of mycobacteria. PLoS One 6: e28476.
33. Buwitt-Beckmann U, Heine H, Wiesmuller KH, Jung G, Brock R, et al. (2005) Toll-like receptor 6-independent signaling by diacylated lipopeptides. Eur J Immunol 35: 282-289. (Pubitemid 40123875)
34. Buwitt-Beckmann U, Heine H, Wiesmuller KH, Jung G, Brock R, et al. (2006) TLR1- and TLR6-independent recognition of bacterial lipopeptides. J Biol Chem 281: 9049-9057. (Pubitemid 43864617)
35. Nigou J, Vasselon T, Ray A, Constant P, Gilleron M, et al. (2008) Mannan chain length controls lipoglycans signaling via and binding to TLR2. J Immunol 180: 6696-6702.
36. Hermann C, Spreitzer I, Schroder NW, Morath S, Lehner MD, et al. (2002) Cytokine induction by purified lipoteichoic acids from various bacterial species - role of LBP, sCD14, CD14 and failure to induce IL-12 and subsequent IFN-gamma release. Eur J Immunol 32: 541-551. (Pubitemid 34173345)
37. Schroder NW, Morath S, Alexander C, Hamann L, Hartung T, et al. (2003) Lipoteichoic acid (LTA) of Streptococcus pneumoniae and Staphylococcus aureus activates immune cells via Toll-like receptor (TLR)-2, lipopolysaccharidebinding protein (LBP), and CD14, whereas TLR-4 and MD-2 are not involved. J Biol Chem 278: 15587-15594. (Pubitemid 36799667)
38. Hoebe K, Georgel P, Rutschmann S, Du X, Mudd S, et al. (2005) CD36 is a sensor of diacylglycerides. Nature 433: 523-527. (Pubitemid 40204309)
39. Cot M, Ray A, Gilleron M, Vercellone A, Larrouy-Maumus G, et al. (2011) Lipoteichoic acid in Streptomyces hygroscopicus: structural model and immunomodulatory activities. PLoS One 6: e26316.
40. Elson G, Dunn-Siegrist I, Daubeuf B, Pugin J (2007) Contribution of Toll-like receptors to the innate immune response to Gram-negative and Gram-positive bacteria. Blood 109: 1574-1583. (Pubitemid 46239591)