Wall Teichoic Acids of Limit Recognition by the Drosophila Peptidoglycan Recognition Protein-SA to Promote Pathogenicity

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The cell wall of Gram-positive bacteria is a complex network of surface proteins, capsular polysaccharides and wall teichoic acids (WTA) covalently linked to Peptidoglycan (PG). The absence of WTA has been associated with a reduced pathogenicity of Staphylococcus aureus (S. aureus). Here, we assessed whether this was due to increased detection of PG, an important target of innate immune receptors. Antibiotic-mediated or genetic inhibition of WTA production in S. aureus led to increased binding of the non-lytic PG Recognition Protein-SA (PGRP-SA), and this was associated with a reduction in host susceptibility to infection. Moreover, PGRP-SD, another innate sensor required to control wild type S. aureus infection, became redundant. Our data imply that by using WTA to limit access of innate immune receptors to PG, under-detected bacteria are able to establish an infection and ultimately overwhelm the host. We propose that different PGRPs work in concert to counter this strategy.

Vyšlo v časopise: Wall Teichoic Acids of Limit Recognition by the Drosophila Peptidoglycan Recognition Protein-SA to Promote Pathogenicity. PLoS Pathog 7(12): e32767. doi:10.1371/journal.ppat.1002421
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002421

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Zdroje

1. FosterTJ 2005 Immune evasion by staphylococci. Nat Rev Microbiol 3 948 958

2. ChaputCBonecaIG 2007 Peptidoglycan detection by mammals and flies. Microbes Infect 9 637 647

3. VollmerWBlanotDde PedroMA 2008 Peptidoglycan structure and architecture. FEMS Microbiol Rev 32 149 167

4. SchleiferKHKandlerO 1972 Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36 407 477

5. ScottJRBarnettTC 2006 Surface proteins of gram-positive bacteria and how they get there. Annu Rev Microbiol 60 397 423

6. KadiogluAWeiserJNPatonJCAndrewPW 2008 The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol 6 288 301

7. WeidenmaierCPeschelA 2008 Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 6 276 287

8. HumannJLenzLL 2009 Bacterial peptidoglycan degrading enzymes and their impact on host muropeptide detection. J Innate Immun 1 88 97

9. VollmerW 2008 Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol Rev 32 287 306

10. BonecaIGDussurgetOCabanesDNahoriMASousaS 2007 A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proc Natl Acad Sci U S A 104 997 1002

11. TabuchiYShiratsuchiAKurokawaKGongJHSekimizuK 2010 Inhibitory role for D-alanylation of wall teichoic acid in activation of insect Toll pathway by peptidoglycan of Staphylococcus aureus. J Immunol 185 2424 2431

12. KurokawaKGongJHRyuKHZhengLChaeJH 2011 Biochemical characterization of evasion from peptidoglycan recognition by Staphylococcus aureus D-alanylated wall teichoic acid in insect innate immunity. Dev Comp Immunol 35 835 839

13. FilipeSRTomaszALigoxygakisP 2005 Requirements of peptidoglycan structure that allow detection by the Drosophila Toll pathway. EMBO Rep 6 327 333

14. WangLGilbertRJAtilanoMLFilipeSRGayNJ 2008 Peptidoglycan recognition protein-SD provides versatility of receptor formation in Drosophila immunity. Proc Natl Acad Sci U S A 105 11881 11886

15. BischoffVVignalCBonecaIGMichelTHoffmannJA 2004 Function of the drosophila pattern-recognition receptor PGRP-SD in the detection of Gram-positive bacteria. Nat Immunol 5 1175 1180

16. MichelTReichhartJMHoffmannJARoyetJ 2001 Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature 414 756 759

17. GobertVGottarMMatskevichAARutschmannSRoyetJ 2003 Dual activation of the Drosophila toll pathway by two pattern recognition receptors. Science 302 2126 2130

18. LemaitreBHoffmannJ 2007 The host defense of Drosophila melanogaster. Annu Rev Immunol 25 697 743

19. WangLWeberANAtilanoMLFilipeSRGayNJ 2006 Sensing of Gram-positive bacteria in Drosophila: GNBP1 is needed to process and present peptidoglycan to PGRP-SA. EMBO J 25 5005 5014

20. KashyapDRWangMLiuLHBoonsGJGuptaD 2011 Peptidoglycan recognition proteins kill bacteria by activating protein-sensing two-component systems. Nat Med 17 676 683

21. SchlagMBiswasRKrismerBKohlerTZollS 2010 Role of staphylococcal wall teichoic acid in targeting the major autolysin Atl. Mol Microbiol 75 864 873

22. GrundlingAMissiakasDMSchneewindO 2006 Staphylococcus aureus mutants with increased lysostaphin resistance. J Bacteriol 188 6286 6297

23. SteenABuistGLeenhoutsKJEl KhattabiMGrijpstraF 2003 Cell wall attachment of a widely distributed peptidoglycan binding domain is hindered by cell wall constituents. J Biol Chem 278 23874 23881

24. DavisonALBaddileyJ 1963 The Distribution of Teichoic Acids in Staphylococci. J Gen Microbiol 32 271 276

25. SwobodaJGCampbellJMeredithTCWalkerS 2010 Wall teichoic acid function, biosynthesis, and inhibition. Chembiochem 11 35 45

26. WangYHuebnerJTzianabosAOMartirosianGKasperDL 1999 Structure of an antigenic teichoic acid shared by clinical isolates of Enterococcus faecalis and vancomycin-resistant Enterococcus faecium. Carbohydr Res 316 155 160

27. SaltonMRJ 1994 The bacterial cell envelope -⁠ a historical perspective. GhuysenJ-MHakenbeckR Bacterial Cell Wall Elsevier 1 22

28. CampbellJSinghAKSanta MariaJPJrKimYBrownS 2011 Synthetic lethal compound combinations reveal a fundamental connection between wall teichoic acid and peptidoglycan biosyntheses in Staphylococcus aureus. ACS Chem Biol 6 106 116

29. AtilanoMLPereiraPMYatesJReedPVeigaH 2010 Teichoic acids are temporal and spatial regulators of peptidoglycan cross-linking in Staphylococcus aureus. Proc Natl Acad Sci U S A 107 18991 18996

30. BrownSZhangYHWalkerS 2008 A revised pathway proposed for Staphylococcus aureus wall teichoic acid biosynthesis based on in vitro reconstitution of the intracellular steps. Chem Biol 15 12 21

31. ArcherGL 1998 Staphylococcus aureus: a well-armed pathogen. Clin Infect Dis 26 1179 1181

32. GalacMRLazzaroBP 2011 Comparative pathology of bacteria in the genus Providencia to a natural host, Drosophila melanogaster. Microbes Infect 13 673 683

33. PeschelAOttoMJackRWKalbacherHJungG 1999 Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274 8405 8410

34. BeraABiswasRHerbertSKulauzovicEWeidenmaierC 2007 Influence of wall teichoic acid on lysozyme resistance in Staphylococcus aureus. J Bacteriol 189 280 283

35. DziarskiRGuptaD 2006 The peptidoglycan recognition proteins (PGRPs). Genome Biol 7 232

36. ChangCIPili-FlourySHervéMParquetCChelliahY 2004 A Drosophila pattern recognition receptor contains a peptidoglycan docking groove and unusual L,D-carboxypeptidase activity. PLoS Biol 2 e277

37. WangLWeberANAtilanoMLFilipeSRGayNJ 2006 Sensing of Gram-positive bacteria in Drosophila:GNBP1 is needed to process and present peptidoglycan to PGRP-SA. EMBO J 25 5005 14

38. ParkJWJeBRPiaoSInamuraSFujimotoY 2006 A synthetic peptidoglycan fragment as a competitive inhibitor of the melanization cascade. J Biol Chem 281 7747 7755

39. LeonePBischoffVKellenbergerCHetruCRoyetJ 2008 Crystal structure of Drosophila PGRP-SD suggests binding to DAP-type but not lysine-type peptidoglycan. Mol Immunol 45 2521 2530

40. WeidenmaierCKokai-KunJFKulauzovicEKohlerTThummG 2008 Differential roles of sortase-anchored surface proteins and wall teichoic acid in Staphylococcus aureus nasal colonization. Int J Med Microbiol 298 505 513

41. SuzukiTCampbellJSwobodaJGWalkerSGilmoreMS 2011 Role of wall teichoic acids in Staphylococcus aureus endophthalmitis. Invest Ophthalmol Vis Sci 52 3187 3192

42. FerrandonDJungACCriquiMLemaitreBUttenweiler-JosephS 1998 A drosomycin-GFP reporter transgene reveals a local immune response in Drosophila that is not dependent on the Toll pathway. EMBO J 17 1217 1227

43. LemaitreBNicolasEMichautLReichhartJMHoffmannJA 1996 The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86 973 983

44. LindsleyDLZimmGG 1992 The Genome of Drosophila melanogaster. San Diego Academic Press

45. RutschmannSKilincAFerrandonD 2002 Cutting edge: the toll pathway is required for resistance to gram-positive bacterial infections in Drosophila. J Immunol 168 1542 1546

46. Vergara-IrigarayMMaira-LitranTMerinoNPierGBPenadesJR 2008 Wall teichoic acids are dispensable for anchoring the PNAG exopolysaccharide to the Staphylococcus aureus cell surface. Microbiology 154 865 877

47. WieserMDennerEBKampferPSchumannPTindallB 2002 Emended descriptions of the genus Micrococcus, Micrococcus luteus (Cohn 1872) and Micrococcus lylae (Kloos, et al. 1974). Int J Syst Evol Microbiol 52 629 637

48. JacobAEHobbsSJ 1974 Conjugal transfer of plasmid-borne multiple antibiotic resistance in Streptococcus faecalis var. zymogenes. J Bacteriol 117 360 372

49. HenriquesAOGlaserPPiggotPJMoranCPJr 1998 Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol Microbiol 28 235 247

50. GlittenbergMTSilasSMacCallumDMGowNALigoxygakisP 2011 Wild-type Drosophila melanogaster as an alternative model system for investigating the pathogenicity of Candida albicans. Dis Model Mech 4 504 514

51. AbramoffMMagalhaesPRamS 2004 Image processing with ImageJ. Biophoton Int 11 36 42

52. MeredithTCSwobodaJGWalkerS 2008 Late-stage polyribitol phosphate wall teichoic acid biosynthesis in Staphylococcus aureus. J Bacteriol 190 3046 3056