Inhibitory role for D-alanylation of wall teichoic acid in activation of insect toll pathway by peptidoglycan of Staphylococcus aureus

Journal of Immunology

Volumn 185, Issue 4, 2010, Pages 2424-2431

  Tabuchi, Yukichika ^a   Shiratsuchi, Akiko ^a   Kurokawa, Kenji ^b,c   Gong, Ji Hee ^c   Sekimizu, Kazuhisa ^b   Lee, Bok Luel ^c   Nakanishi, Yoshinobu ^a  

^a KANAZAWA UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c Pusan National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOMYCIN; MESSENGER RNA; PEPTIDOGLYCAN; POLYPEPTIDE ANTIBIOTIC AGENT; TEICHOIC ACID; TOLL LIKE RECEPTOR; ALANINE; BACTERIAL PROTEIN; DROSOMYCIN PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; LIGASE; TL PROTEIN, DROSOPHILA;

ARTICLE; BACTERIAL CELL WALL; BACTERIAL GROWTH; BACTERIAL VIRULENCE; DROSOPHILA; FLY; HUMORAL IMMUNITY; IN VITRO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; SURVIVAL; ANIMAL; CELL WALL; CHEMISTRY; DROSOPHILA MELANOGASTER; GENETICS; HOST PATHOGEN INTERACTION; MALE; METABOLISM; MICROBIOLOGY; MUTATION; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME; WESTERN BLOTTING;

ALANINE; ANIMALS; BACTERIAL PROTEINS; BLOTTING, WESTERN; CARBON-OXYGEN LIGASES; CELL WALL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HOST-PATHOGEN INTERACTIONS; MALE; MUTATION; PEPTIDOGLYCAN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; TEICHOIC ACIDS; TIME FACTORS; TOLL-LIKE RECEPTORS;

EID: 77956909955     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000625     Document Type: Article

References (38)

1. Ernst, J. D. 2000. Bacterial inhibition of phagocytosis. Cell. Microbiol. 2: 379-386.
2. Rosenberger, C. M., and B. B. Finlay. 2003. Phagocyte sabotage: disruption of macrophage signalling by bacterial pathogens. Nat. Rev. Mol. Cell Biol. 4: 385-396.
3. Coombes, B. K., Y. Valdez, and B. B. Finlay. 2004. Evasive maneuvers by secreted bacterial proteins to avoid innate immune responses. Curr. Biol. 14: R856-R867.
4. Bhavsar, A. P., J. A. Guttman, and B. B. Finlay. 2007. Manipulation of host-cell pathways by bacterial pathogens. Nature 449: 827-834.
5. Sansonetti, P. J., and J. P. Di Santo. 2007. Debugging how bacteria manipulate the immune response. Immunity 26: 149-161.
6. Nizet, V. 2007. Understanding how leading bacterial pathogens subvert innate immunity to reveal novel therapeutic targets. J. Allergy Clin. Immunol. 120: 13-22.
7. Diacovich, L., and J.-P. Gorvel. 2010. Bacterial manipulation of innate immunity to promote infection. Nat. Rev. Microbiol. 8: 117-128.
8. Watanabe, I., M. Ichiki, A. Shiratsuchi, and Y. Nakanishi. 2007. TLR2-mediated survival of Staphylococcus aureus in macrophages: a novel bacterial strategy against host innate immunity. J. Immunol. 178: 4917-4925.
9. Shiratsuchi, A., K. Shimizu, I. Watanabe, Y. Hashimoto, K. Kurokawa, I. M. Razanajatovo, K. H. Park, H. K. Park, B. L. Lee, K. Sekimizu, and Y. Nakanishi. 2010. Auxiliary role for D-alanylated wall teichoic acid in Toll-like receptor 2-mediated survival of Staphylococcus aureus in macrophages. Immunology 129: 268-277.
10. Mylonakis, E., and A. Aballay. 2005. Worms and flies as genetically tractable animal models to study host-pathogen interactions. Infect. Immun. 73: 3833-3841.
11. Lemaitre, B., and J. Hoffmann. 2007. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25: 697-743.
12. Strand, M. R. 2008. The insect cellular immune response. Insect Sci. 15: 1-14.
13. Kim, C.-H., S.-J. Kim, H. Kan, H.-M. Kwon, K.-B. Roh, R. Jiang, Y. Yang J.-W. Park, H.-H. Lee, N.-C. Ha, et al. 2008. A three-step proteolytic cascade mediates the activation of the peptidoglycan-induced Toll pathway in an insect. J. Biol. Chem. 283: 7599-7607.
14. Roh, K.-B., C.-H. Kim, H. Lee, H.-M. Kwon, J.-W. Park, J.-H. Ryu, K. Kurokawa, N.-C. Ha, W.-J. Lee, B. Lemaitre, et al. 2009. Proteolytic cascade for the activation of the insect Toll pathway induced by the fungal cell wall component. J. Biol. Chem. 284: 19474-19481.
15. Hashimoto, Y., Y. Tabuchi, K. Sakurai, M. Kutsuna, K. Kurokawa, T. Awasaki, K. Sekimizu, Y. Nakanishi, and A. Shiratsuchi. 2009. Identification of lipoteichoic acid as a ligand for Draper in the phagocytosis of Staphylococcus aureus by Drosophila hemocytes. J. Immunol. 183: 7451-7460.
16. Anderson, K. V., G. Jürgens, and C. Nüsslein-Volhard. 1985. Establishment of dorsal-ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product. Cell 42: 779-789.
17. Park, J.-W., C.-H. Kim, J.-H. Kim, B.-R. Je, K.-B. Roh, S.-J. Kim, H.-H. Lee J.-H. Ryu, J.-H. Lim, B.-H. Oh, et al. 2007. Clustering of peptidoglycan recognition protein-SA is required for sensing lysine-type peptidoglycan in insects. Proc. Natl. Acad. Sci. USA 104: 6602-6607.
18. Neuhaus, F. C., and J. Baddiley. 2003. A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol. Mol. Biol. Rev. 67: 686-723.
19. Kurokawa, K., C. Kaito, and K. Sekimizu. 2007. Two-component signaling in the virulence of Staphylococcus aureus: a silkworm larvae-pathogenic agent infection model of virulence. Methods Enzymol. 422: 233-244. (Pubitemid 47030652)
20. Herbert, S., A. Bera, C. Nerz, D. Kraus, A. Peschel, C. Goerke, M. Meehl, A. Cheung, and F. Götz. 2007. Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in staphylococci. PLoS Pathog. 3: e102. (Pubitemid 47203994)
21. Peschel, A., M. Otto, R. W. Jack, H. Kalbacher, G. Jung, and F. Götz. 1999. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274: 8405-8410.
22. Shia, A. K. H., M. Glittenberg, G. Thompson, A. N. Weber, J.-M. Reichhart, and P. Ligoxygakis. 2009. Toll-dependent antimicrobial responses in Drosophila larval fat body require Spätzle secreted by haemocytes. J. Cell Sci. 122: 4505-4515.
23. Shimada, T., B. G. Park, A. J. Wolf, C. Brikos, H. S. Goodridge, C. A. Becker, C. N. Reyes, E. A. Miao, A. Aderem, F. Götz, et al. 2010. Staphylococcus aureus evades lysozyme-based peptidoglycan digestion that links phagocytosis, inflammasome activation, and IL-1β secretion. Cell Host Microbe 7: 38-49.
24. Bera, A., S. Herbert, A. Jakob, W. Vollmer, and F. Götz. 2005. Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol. Microbiol. 55: 778-787.
25. Weidenmaier, C., and A. Peschel. 2008. Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat. Rev. Microbiol. 6: 276-287.
26. 2 and human β-defensin 3. Infect. Immun. 76: 2169-2176.
27. Peschel, A., C. Vuong, M. Otto, and F. Götz. 2000. The D-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes. Antimicrob. Agents Chemother. 44: 2845-2847.
28. Sieradzki, K., and A. Tomasz. 2003. Alterations of cell wall structure and metabolism accompany reduced susceptibility to vancomycin in an isogenic series of clinical isolates of Staphylococcus aureus. J. Bacteriol. 185: 7103-7110.
29. Weidenmaier, C., A. Peschel, V. A. J. Kempf, N. Lucindo, M. R. Yeaman, and A. S. Bayer. 2005. DltABCD- and MprF-mediated cell envelope modifications of Staphylococcus aureus confer resistance to platelet microbicidal proteins and contribute to virulence in a rabbit endocarditis model. Infect. Immun. 73: 8033-8038.
30. Boyd, D. A., D. G. Cvitkovitch, A. S. Bleiweis, M. Y. Kiriukhin, D. V. Debabov, F. C. Neuhaus, and I. R. Hamilton. 2000. Defects in D-alanyl-lipoteichoic acid synthesis in Streptococcus mutans results in acid sensitivity. J. Bacteriol. 182: 6055-6065.
31. Abachin, E., C. Poyart, E. Pellegrini, E. Milohanic, F. Fiedler, P. Berche, and P. Trieu-Cuot. 2002. Formation of D-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Mol. Microbiol. 43: 1-14.
32. Kurokawa, K., H. Lee, K.-B. Roh, M. Asanuma, Y. S. Kim, H. Nakayama, A. Shiratsuchi, Y. Choi, O. Takeuchi, H. J. Kang, et al. 2009. The triacylated ATP binding cluster transporter substrate-binding lipoprotein of Staphylococcus aureus functions as a native ligand for Toll-like receptor 2. J. Biol. Chem. 284: 8406-8411.
33. Novick, R. P., H. F. Ross, S. J. Projan, J. Kornblum, B. Kreiswirth, and S. Moghazeh. 1993. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J. 12: 3967-3975.
34. Kaito, C., and K. Sekimizu. 2007. Colony spreading in Staphylococcus aureus. J. Bacteriol. 189: 2553-2557.
35. Kajimura, J., T. Fujiwara, S. Yamada, Y. Suzawa, T. Nishida, Y. Oyamada, I. Hayashi, J. Yamagishi, H. Komatsuzawa, and M. Sugai. 2005. Identification and molecular characterization of an N-acetylmuramyl-L-alanine amidase Sle1 involved in cell separation of Staphylococcus aureus. Mol. Microbiol. 58: 1087-1101.
36. Takahashi, J., H. Komatsuzawa, S. Yamada, T. Nishida, H. Labischinski, T. Fujiwara, M. Ohara, J. Yamagishi, and M. Sugai. 2002. Molecular characterization of an atl null mutant of Staphylococcus aureus. Microbiol. Immunol. 46: 601-612.
37. Ichihashi, N., K. Kurokawa, M. Matsuo, C. Kaito, and K. Sekimizu. 2003. Inhibitory effects of basic or neutral phospholipid on acidic phospholipid-mediated dissociation of adenine nucleotide bound to DnaA protein, the initiator of chromosomal DNA replication. J. Biol. Chem. 278: 28778-28786.
38. Oku, Y., K. Kurokawa, M. Matsuo, S. Yamada, B.-L. Lee, and K. Sekimizu. 2009. Pleiotropic roles of polyglycerolphosphate synthase of lipoteichoic acid in growth of Staphylococcus aureus cells. J. Bacteriol. 191: 141-151.