Toll-like receptor 2 activation depends on lipopeptide shedding by bacterial surfactants

Nature Communications

Volumn 7, Issue , 2016, Pages

  Hanzelmann, Dennis ^a   Joo, Hwang Soo ^b   Franz Wachtel, Mirita ^a   Hertlein, Tobias ^c   Stevanovic, Stefan ^a   Macek, Boris ^a   Wolz, Christiane ^a   Götz, Friedrich ^a   Otto, Michael ^b   Kretschmer, Dorothee ^a   Peschel, Andreas ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPEPTIDE; PHENOL; SURFACTANT; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR AGONIST; BACTERIAL PROTEIN; PHENOL DERIVATIVE;

BACTERIAL DISEASE; BACTERIUM; GENETIC ANALYSIS; INFECTIOUS DISEASE; PATHOGEN; PROTEIN; SURFACTANT; VIRULENCE;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL SHEDDING; CELL MEMBRANE; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE SEVERITY; EMBRYO; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN SECRETION; SEPSIS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; VIRULENCE; WILD TYPE; ANIMAL; BONE MARROW CELL; CELL LINE; DRUG EFFECT; INFLAMMATION; MACROPHAGE; METABOLISM; MICROBIOLOGY; NEUTROPHIL; PATHOGENICITY; PATHOLOGY; SOLUBILITY;

BACTERIA (MICROORGANISMS); MUS; POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

ANIMALS; BACTERIAL PROTEINS; BONE MARROW CELLS; CELL LINE; HUMANS; INFLAMMATION; LIPOPEPTIDES; MACROPHAGES; MICE; NEUTROPHILS; PHENOLS; SEPSIS; SOLUBILITY; STAPHYLOCOCCUS AUREUS; SURFACE-ACTIVE AGENTS; TOLL-LIKE RECEPTOR 2; VIRULENCE;

EID: 84982728043     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12304     Document Type: Article

References (51)

1. Angus, D. C. & van der Poll, T. Severe sepsis and septic shock. N. Engl. J. Med. 369, 840-851 (2013).
2. Plociennikowska, A., Hromada-Judycka, A., Borzecka, K. & Kwiatkowska, K. Co-operation of TLR4 and raft proteins in LPS-induced pro-inflammatory signaling. Cell. Mol. Life Sci. 72, 557-581 (2015).
3. Kawai, T. & Akira, S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373-384 (2010).
4. Hashimoto, M. et al. Not lipoteichoic acid but lipoproteins appear to be the dominant immunobiologically active compounds in Staphylococcus aureus. J. Immunol. 177, 3162-3169 (2006).
5. Takeuchi, O., Hoshino, K. & Akira, S. Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J. Immunol. 165, 5392-5396 (2000).
6. Nachtigall, I. et al. Polymorphisms of the toll-like receptor 2 and 4 genes are associated with faster progression and a more severe course of sepsis in critically ill patients. J. Int. Med. Res. 42, 93-110 (2014).
7. Stappers, M. H. et al. TLR1, TLR2, and TLR6 gene polymorphisms are associated with increased susceptibility to complicated skin and skin structure infections. J. Infect. Dis. 210, 311-318 (2014).
8. Lachance, C., Segura, M., Gerber, P. P., Xu, J. & Gottschalk, M. Toll-like receptor 2-independent host innate immune response against an epidemic strain of Streptococcus suis that causes a toxic shock-like syndrome in humans. PLoS ONE 8, e65031 (2013).
9. Edelson, B. T. & Unanue, E. R. MyD88-dependent but Toll-like receptor 2-independent innate immunity to Listeria: no role for either in macrophage listericidal activity. J. Immunol. 169, 3869-3875 (2002).
10. Loof, T. G., Goldmann, O. & Medina, E. Immune recognition of Streptococcus pyogenes by dendritic cells. Infect. Immun. 76, 2785-2792 (2008).
11. Schmaler, M. et al. Lipoproteins in Staphylococcus aureus mediate inflammation by TLR2 and iron-dependent growth in vivo. J. Immunol. 182, 7110-7118 (2009).
12. Peres, A. G. et al. Uncoupling of pro- and anti-inflammatory properties of Staphylococcus aureus. Infect. Immun. 83, 1587-1597 (2015).
13. Basto, A. P. & Leitao, A. Targeting TLR2 for vaccine development. J. Immunol. Res. 2014, 619410 (2014).
14. Tong, S. Y., Davis, J. S., Eichenberger, E., Holland, T. L. & Fowler, Jr V. G. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin. Microbiol. Rev. 28, 603-661 (2015).
15. Thammavongsa, V., Kim, H. K., Missiakas, D. & Schneewind, O. Staphylococcal manipulation of host immune responses. Nat. Rev. Microbiol. 13, 529-543 (2015).
16. Spaan, A. N., Surewaard, B. G., Nijland, R. & van Strijp, J. A. Neutrophils versus Staphylococcus aureus: a biological tug of war. Annu. Rev.Microbiol. 67, 629-650 (2013).
17. Nakayama, H., Kurokawa, K. & Lee, B. L. Lipoproteins in bacteria: structures and biosynthetic pathways. FEBS J. 279, 4247-4268 (2012).
18. Buddelmeijer, N. The molecular mechanism of bacterial lipoprotein modification-how, when and why? FEMS Microbiol. Rev. 39, 246-261 (2015).
19. Muller, P. et al. The Staphylococcus aureus lipoprotein SitC colocalizes with Toll-like receptor 2 (TLR2) in murine keratinocytes and elicits intracellular TLR2 accumulation. Infect. Immun. 78, 4243-4250 (2010).
20. Sheldon, J. R. & Heinrichs, D. E. The iron-regulated staphylococcal lipoproteins. Front. Cell. Infect. Microbiol. 2, 41 (2012).
21. Stoll, H., Dengjel, J., Nerz, C. & Gotz, F. Staphylococcus aureus deficient in lipidation of prelipoproteins is attenuated in growth and immune activation. Infect. Immun. 73, 2411-2423 (2005).
22. Otto, M. Staphylococcus aureus toxins. Curr. Opin. Microbiol. 17, 32-37 (2014).
23. Singh, R. & Ray, P. Quorum sensing-mediated regulation of staphylococcal virulence and antibiotic resistance. Future Microbiol. 9, 669-681 (2014).
24. Wang, R. et al. Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat. Med. 13, 1510-1514 (2007).
25. Queck, S. Y. et al. RNAIII-independent target gene control by the agr quorumsensing system: insight into the evolution of virulence regulation in Staphylococcus aureus. Mol. Cell. 32, 150-158 (2008).
26. Peschel, A. & Otto, M. Phenol-soluble modulins and staphylococcal infection. Nat. Rev. Microbiol. 11, 667-673 (2013).
27. Kretschmer, D. et al. Human formyl peptide receptor 2 senses highly pathogenic Staphylococcus aureus. Cell Host Microbe 7, 463-473 (2010).
28. Bloes, D. A., Kretschmer, D. & Peschel, A. Enemy attraction: bacterial agonists for leukocyte chemotaxis receptors. Nat. Rev. Microbiol. 13, 95-104 (2015).
29. Rautenberg, M., Joo, H. S., Otto, M. & Peschel, A. Neutrophil responses to staphylococcal pathogens and commensals via the formyl peptide receptor 2 relates to phenol-soluble modulin release and virulence. FASEB J. 25, 1254-1263 (2011).
30. Chambers, H. F. Community-associated MRSA-resistance and virulence converge. N. Engl. J. Med. 352, 1485-1487 (2005).
31. Cheung, G. Y., Wang, R., Khan, B. A., Sturdevant, D. E. & Otto, M. Role of the accessory gene regulator agr in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. Infect. Immun. 79, 1927-1935 (2011).
32. Joo, H. S., Cheung, G. Y. & Otto, M. Antimicrobial activity of communityassociated methicillin-resistant Staphylococcus aureus is caused by phenolsoluble modulin derivatives. J. Biol. Chem. 286, 8933-8940 (2011).
33. Diep, B. A. et al. Identifying potential therapeutic targets of methicillin-resistant Staphylococcus aureus through in vivo proteomic analysis. J. Infect. Dis. 209, 1533-1541 (2014).
34. Chatterjee, S. S. et al. Essential Staphylococcus aureus toxin export system. Nat. Med. 19, 364-367 (2013).
35. Vesy, C. J., Kitchens, R. L., Wolfbauer, G., Albers, J. J. & Munford, R. S. Lipopolysaccharide-binding protein and phospholipid transfer protein release lipopolysaccharides from gram-negative bacterial membranes. Infect. Immun. 68, 2410-2417 (2000).
36. Hajjar, A. M. et al. Cutting edge: functional interactions between toll-like receptor (TLR) 2 and TLR1 or TLR6 in response to phenol-soluble modulin. J. Immunol. 166, 15-19 (2001).
37. Valour, F. et al. Delta-toxin production deficiency in Staphylococcus aureus: a diagnostic marker of bone and joint infection chronicity linked with osteoblast invasion and biofilm formation. Clin. Microbiol. Infect. 21, 568.e1-568.e11 (2015).
38. Bardoel, B. W. et al. Evasion of toll-like receptor 2 activation by staphylococcal superantigen-like protein 3. J. Mol. Med. (Berl) 90, 1109-1120 (2012).
39. Koymans, K. J. et al. Structural basis for inhibition of TLR2 by staphylococcal superantigen-like protein 3 (SSL3). Proc. Natl Acad. Sci. USA 112, 11018-11023 (2015).
40. Hengge, U. R., Benninghoff, B., Ruzicka, T. & Goos, M. Topical immunomodulators-progress towards treating inflammation, infection, and cancer. Lancet Infect. Dis. 1, 189-198 (2001).
41. Savva, A. & Roger, T. Targeting toll-like receptors: promising therapeutic strategies for the management of sepsis-associated pathology and infectious diseases. Front. Immunol. 4, 387 (2013).
42. Kim, L. H., Jung, Y., Yu, H. W., Chae, K. J. & Kim, I. S. Physicochemical interactions between rhamnolipids and pseudomonas aeruginosa biofilm layers. Environ. Sci. Technol. 49, 3718-3726 (2015).
43. Wooten, R. M. et al. Toll-like receptor 2 is required for innate, but not acquired, host defense to Borrelia burgdorferi. J. Immunol. 168, 348-355 (2002).
44. Siegfried, A. et al. IFIT2 is an effector protein of type I IFN-mediated amplification of lipopolysaccharide (LPS)-induced TNF-alpha secretion and LPS-induced endotoxin shock. J. Immunol. 191, 3913-3921 (2013).
45. Geiger, T. et al. The stringent response of Staphylococcus aureus and its impact on survival after phagocytosis through the induction of intracellular PSMs expression. PLoS Pathog. 8, e1003016 (2012).
46. Carpy, A. et al. Absolute proteome and phosphoproteome dynamics during the cell cycle of Schizosaccharomyces pombe (Fission Yeast). Mol. Cell. Proteomics 13, 1925-1936 (2014).
47. Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372 (2008).
48. Cox, J. et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome. Res. 10, 1794-1805 (2011).
49. Luber, C. A. et al. Quantitative proteomics reveals subset-specific viral recognition in dendritic cells. Immunity 32, 279-289 (2010).
50. Chen, K. et al. A critical role for the g protein-coupled receptor mFPR2 in airway inflammation and immune responses. J. Immunol. 184, 3331-3335 (2010).
51. Vizcaino, J. A. et al. 2016 update of the PRIDE database and its related tools. Nucleic Acids Res 44, D447-456 (2016).