Staphylococcus aureus phenol-soluble modulin peptides modulate dendritic cell functions and increase in vitro priming of regulatory T cells

Journal of Immunology

Volumn 190, Issue 7, 2013, Pages 3417-3426

  Schreiner, Jens ^a   Kretschmer, Dorothee ^a   Klenk, Juliane ^a   Otto, Michael ^b   Bühring, Hans Jörg ^a   Stevanovic, Stefan ^a   Wang, Ji Ming ^c   Beer Hammer, Sandra ^a   Peschel, Andreas ^a   Autenrieth, Stella E ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

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

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; FORMYLPEPTIDE RECEPTOR; FORMYLPEPTIDE RECEPTOR 1; FORMYLPEPTIDE RECEPTOR 2; GUANINE NUCLEOTIDE BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; MODULIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CHEMOTAXIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; DENDRITIC CELL; ENDOCYTOSIS; FEMALE; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR BINDING; REGULATORY T LYMPHOCYTE; STAPHYLOCOCCUS AUREUS; T LYMPHOCYTE ACTIVATION; TH1 CELL;

ANIMALS; BACTERIAL TOXINS; CHEMOTAXIS; CLATHRIN; CYTOKINES; DENDRITIC CELLS; ENDOCYTOSIS; FEMALE; LYMPHOCYTE ACTIVATION; MICE; PEPTIDES; RECEPTORS, FORMYL PEPTIDE; STAPHYLOCOCCUS AUREUS; T-LYMPHOCYTES, REGULATORY; TOLL-LIKE RECEPTOR 2;

EID: 84875423196     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202563     Document Type: Article

References (54)

1. Lowy, F. D. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339: 520- 532.
2. Fridkin, S. K., J. C. Hageman, M. Morrison, L. T. Sanza, K. Como-Sabetti, J. A. Jernigan, K. Harriman, L. H. Harrison, R. Lynfield, and M. M. Farley; Active Bacterial Core Surveillance Program of the Emerging Infections Program Network. 2005. Methicillin-resistant Staphylococcus aureus disease in three communities. N. Engl. J. Med. 352: 1436-1444.
3. Otto, M. 2010. Basis of virulence in community-associated methicillin-resistant Staphylococcus aureus. Annu. Rev. Microbiol. 64: 143-162.
4. Bubeck Wardenburg, J., T. Bae, M. Otto, F. R. Deleo, and O. Schneewind. 2007. Poring over pores: alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat. Med. 13: 1405-1406.
5. Kretschmer, D., A. K. Gleske, M. Rautenberg, R. Wang, M. Köberle, E. Bohn, T. Schöneberg, M. J. Rabiet, F. Boulay, S. J. Klebanoff, et al. 2010. Human formyl peptide receptor 2 senses highly pathogenic Staphylococcus aureus. Cell Host Microbe 7: 463-473.
6. Wang, R., K. R. Braughton, D. Kretschmer, T. H. Bach, S. Y. Queck, M. Li, A. D. Kennedy, D. W. Dorward, S. J. Klebanoff, A. Peschel, et al. 2007. Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat. Med. 13: 1510-1514.
7. Diep, B. A., L. Chan, P. Tattevin, O. Kajikawa, T. R. Martin, L. Basuino, T. T. Mai, H. Marbach, K. R. Braughton, A. R. Whitney, et al. 2010. Polymorphonuclear leukocytes mediate Staphylococcus aureus Panton-Valentine leukocidin-induced lung inflammation and injury. Proc. Natl. Acad. Sci. USA 107: 5587-5592.
8. Migeotte, I., D. Communi, and M. Parmentier. 2006. Formyl peptide receptors: a promiscuous subfamily of G protein-coupled receptors controlling immune responses. Cytokine Growth Factor Rev. 17: 501-519.
9. Laarman, A., F. Milder, J. van Strijp, and S. Rooijakkers. 2010. Complement inhibition by Gram-positive pathogens: molecular mechanisms and therapeutic implications. J. Mol. Med. 88: 115-120.
10. Bestebroer, J., C. J. De Haas, and J. A. Van Strijp. 2010. How microorganisms avoid phagocyte attraction. FEMS Microbiol. Rev. 34: 395-414.
11. Peschel, A., and H. G. Sahl. 2006. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat. Rev. Microbiol. 4: 529-536.
12. Bröker, B. M., and A. van Belkum. 2011. Immune proteomics of Staphylococcus aureus. Proteomics 11: 3221-3231.
13. Kim, H. K., V. Thammavongsa, O. Schneewind, and D. Missiakas. 2012. Recurrent infections and immune evasion strategies of Staphylococcus aureus. Curr. Opin. Microbiol. 15: 92-99.
14. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
15. Iwasaki, A., and R. Medzhitov. 2004. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5: 987-995.
16. Cho, J. S., E. M. Pietras, N. C. Garcia, R. I. Ramos, D. M. Farzam, H. R. Monroe, J. E. Magorien, A. Blauvelt, J. K. Kolls, A. L. Cheung, et al. 2010. IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J. Clin. Invest. 120: 1762-1773.
17. Lin, L., A. S. Ibrahim, X. Xu, J. M. Farber, V. Avanesian, B. Baquir, Y. Fu, S. W. French, J. E. Edwards, Jr., and B. Spellberg. 2009. Th1-Th17 cells mediate protective adaptive immunity against Staphylococcus aureus and Candida albicans infection in mice. PLoS Pathog. 5: e1000703.
18. McLoughlin, R. M., J. C. Lee, D. L. Kasper, and A. O. Tzianabos. 2008. IFNgamma regulated chemokine production determines the outcome of Staphylococcus aureus infection. J. Immunol. 181: 1323-1332.
19. Miller, L. S., and J. S. Cho. 2011. Immunity against Staphylococcus aureus cutaneous infections. Nat. Rev. Immunol. 11: 505-518.
20. Zhao, Y. X., I. M. Nilsson, and A. Tarkowski. 1998. The dual role of interferongamma in experimental Staphylococcus aureus septicaemia versus arthritis. Immunology 93: 80-85.
21. Barnden, M. J., J. Allison, W. R. Heath, and F. R. Carbone. 1998. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and betachain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76: 34-40.
22. Takeuchi, O., K. Hoshino, T. Kawai, H. Sanjo, H. Takada, T. Ogawa, K. Takeda, and S. Akira. 1999. Differential roles of TLR2 and TLR4 in recognition of Gramnegative and Gram-positive bacterial cell wall components. Immunity 11: 443-451.
23. Chen, K., Y. Le, Y. Liu, W. Gong, G. Ying, J. Huang, T. Yoshimura, L. Tessarollo, and J. M. Wang. 2010. A critical role for the G protein-coupled receptor mFPR2 in airway inflammation and immune responses. J. Immunol. 184: 3331-3335.
24. Konrad, S., S. R. Ali, K. Wiege, S. N. Syed, L. Engling, R. P. Piekorz, E. Hirsch, B. Nürnberg, R. E. Schmidt, and J. E. Gessner. 2008. Phosphoinositide 3-kinases gamma and delta, linkers of coordinate C5a receptor-Fcgamma receptor activation and immune complex-induced inflammation. J. Biol. Chem. 283: 33296-33303.
25. Wang, Y., A. Kissenpfennig, M. Mingueneau, S. Richelme, P. Perrin, S. Chevrier, C. Genton, B. Lucas, J. P. DiSanto, H. Acha-Orbea, et al. 2008. Th2 lymphoproliferative disorder of LatY136F mutant mice unfolds independently of TCRMHC engagement and is insensitive to the action of Foxp3+ regulatory T cells. J. Immunol. 180: 1565-1575.
26. Schlag, M., R. Biswas, B. Krismer, T. Kohler, S. Zoll, W. Yu, H. Schwarz, A. Peschel, and F. Götz. 2010. Role of staphylococcal wall teichoic acid in targeting the major autolysin Atl. Mol. Microbiol. 75: 864-873.
27. Joo, H. S., G. Y. Cheung, and M. Otto. 2011. Antimicrobial activity of community-associated methicillin-resistant Staphylococcus aureus is caused by phenol-soluble modulin derivatives. J. Biol. Chem. 286: 8933-8940.
28. Erfurth, S. E., S. Gröbner, U. Kramer, D. S. Gunst, I. Soldanova, M. Schaller, I. B. Autenrieth, and S. Borgmann. 2004. Yersinia enterocolitica induces apoptosis and inhibits surface molecule expression and cytokine production in murine dendritic cells. Infect. Immun. 72: 7045-7054.
29. Lutz, M. B., N. Kukutsch, A. L. Ogilvie, S. Rössner, F. Koch, N. Romani, and G. Schuler. 1999. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223: 77-92.
30. de Haas, C. J., K. E. Veldkamp, A. Peschel, F. Weerkamp, W. J. Van Wamel, E. C. Heezius, M. J. Poppelier, K. P. Van Kessel, and J. A. van Strijp. 2004. Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory agent. J. Exp. Med. 199: 687-695.
31. Somerville, G. A., A. Cockayne, M. Dürr, A. Peschel, M. Otto, and J. M. Musser. 2003. Synthesis and deformylation of Staphylococcus aureus delta-toxin are linked to tricarboxylic acid cycle activity. J. Bacteriol. 185: 6686-6694.
32. Autenrieth, S. E., P. Warnke, G. H. Wabnitz, C. Lucero Estrada, K. A. Pasquevich, D. Drechsler, M. Günter, K. Hochweller, A. Novakovic, S. Beer-Hammer, et al. 2012. Depletion of dendritic cells enhances innate antibacterial host defense through modulation of phagocyte homeostasis. PLoS Pathog. 8: e1002552.
33. Oellerich, M. F., C. A. Jacobi, S. Freund, K. Niedung, A. Bach, J. Heesemann, and K. Trülzsch. 2007. Yersinia enterocolitica infection of mice reveals clonal invasion and abscess formation. Infect. Immun. 75: 3802-3811.
34. Demangel, C., P. Bertolino, and W. J. Britton. 2002. Autocrine IL-10 impairs dendritic cell (DC)-derived immune responses to mycobacterial infection by suppressing DC trafficking to draining lymph nodes and local IL-12 production. Eur. J. Immunol. 32: 994-1002.
35. Bebien, M., M. E. Hensler, S. Davanture, L. C. Hsu, M. Karin, J. M. Park, L. Alexopoulou, G. Y. Liu, V. Nizet, and T. Lawrence. 2012. The pore-forming toxin b hemolysin/cytolysin triggers p38 MAPK-dependent IL-10 production in macrophages and inhibits innate immunity. PLoS Pathog. 8: e1002812.
36. Autenrieth, S. E., I. Soldanova, R. Rösemann, D. Gunst, N. Zahir, M. Kracht, K. Ruckdeschel, H. Wagner, S. Borgmann, and I. B. Autenrieth. 2007. Yersinia enterocolitica YopP inhibits MAP kinase-mediated antigen uptake in dendritic cells. Cell. Microbiol. 9: 425-437.
37. Burgdorf, S., A. Kautz, V. Böhnert, P. A. Knolle, and C. Kurts. 2007. Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316: 612-616.
38. Burgdorf, S., V. Lukacs-Kornek, and C. Kurts. 2006. The mannose receptor mediates uptake of soluble but not of cell-associated antigen for cross-presentation. J. Immunol. 176: 6770-6776.
39. Husebye, H., O. Halaas, H. Stenmark, G. Tunheim, O. Sandanger, B. Bogen, A. Brech, E. Latz, and T. Espevik. 2006. Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J. 25: 683- 692.
40. Volz, T., M. Nega, J. Buschmann, S. Kaesler, E. Guenova, A. Peschel, M. Rocken, F. Gotz, and T. Biedermann. 2010. Natural Staphylococcus aureusderived peptidoglycan fragments activate NOD2 and act as potent costimulators of the innate immune system exclusively in the presence of TLR signals. FASEB J. 24: 4089-4102.
41. Koyasu, S. 2003. The role of PI3K in immune cells. Nat. Immunol. 4: 313- 319.
42. Kang, H. K., H. Y. Lee, M. K. Kim, K. S. Park, Y. M. Park, J. Y. Kwak, and Y. S. Bae. 2005. The synthetic peptide Trp-Lys-Tyr-Met-Val-D-Met inhibits human monocyte-derived dendritic cell maturation via formyl peptide receptor and formyl peptide receptor-like 2. J. Immunol. 175: 685-692.
43. Nakane, A., M. Okamoto, M. Asano, M. Kohanawa, and T. Minagawa. 1995. Endogenous gamma interferon, tumor necrosis factor, and interleukin-6 in Staphylococcus aureus infection in mice. Infect. Immun. 63: 1165-1172.
44. Hultgren, O., H. P. Eugster, J. D. Sedgwick, H. Körner, and A. Tarkowski. 1998. TNF/lymphotoxin-alpha double-mutant mice resist septic arthritis but display increased mortality in response to Staphylococcus aureus. J. Immunol. 161: 5937-5942.
45. Manicassamy, S., and B. Pulendran. 2011. Dendritic cell control of tolerogenic responses. Immunol. Rev. 241: 206-227.
46. McGuirk, P., C. McCann, and K. H. Mills. 2002. Pathogen-specific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: a novel strategy for evasion of protective T helper type 1 responses by Bordetella pertussis. J. Exp. Med. 195: 221-231.
47. Depaolo, R. W., F. Tang, I. Kim, M. Han, N. Levin, N. Ciletti, A. Lin, D. Anderson, O. Schneewind, and B. Jabri. 2008. Toll-like receptor 6 drives differentiation of tolerogenic dendritic cells and contributes to LcrV-mediated plague pathogenesis. Cell Host Microbe 4: 350-361.
48. Couper, K. N., D. G. Blount, and E. M. Riley. 2008. IL-10: the master regulator of immunity to infection. J. Immunol. 180: 5771-5777.
49. Lutz, M. B. 2012. Therapeutic potential of semi-mature dendritic cells for tolerance induction. Front. Immunol. 3: 123.
50. Mathews, W. C., J. C. Caperna, R. E. Barber, F. J. Torriani, L. G. Miller, S. May, and J. A. McCutchan. 2005. Incidence of and risk factors for clinically significant methicillin-resistant Staphylococcus aureus infection in a cohort of HIVinfected adults. J. Acquir. Immune Defic. Syndr. 40: 155-160.
51. Zhao, Y. X., and A. Tarkowski. 1995. Impact of interferon-gamma receptor deficiency on experimental Staphylococcus aureus septicemia and arthritis. J. Immunol. 155: 5736-5742.
52. Tae, Y. M., H. T. Park, H. G. Moon, Y. S. Kim, S. G. Jeon, T. Y. Roh, Y. S. Bae, Y. S. Gho, S. H. Ryu, H. S. Kwon, and Y. K. Kim. 2012. Airway activation of formyl peptide receptors inhibits Th1 and Th17 cell responses via inhibition of mediator release from immune and inflammatory cells and maturation of dendritic cells. J. Immunol. 188: 1799-1808.
53. Belkaid, Y. 2007. Regulatory T cells and infection: a dangerous necessity. Nat. Rev. Immunol. 7: 875-888.
54. Kane, M. M., and D. M. Mosser. 2001. The role of IL-10 in promoting disease progression in leishmaniasis. J. Immunol. 166: 1141-1147.