Lipoteichoic acid-induced lung inflammation depends on TLR2 and the concerted action of TLR4 and the platelet-activating factor receptor

Journal of Immunology

Volumn 180, Issue 5, 2008, Pages 3478-3484

  Knapp, Sylvia ^a,b   Von Aulock, Sonja ^c   Leendertse, Masja ^a   Haslinger, Isabella ^b   Draing, Christian ^c   Golenbock, Douglas T ^d   Van Der Poll, Tom ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF KONSTANZ   (Germany)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; INITIATION FACTOR; INTERLEUKIN 10; KERATINOCYTE DERIVED CHEMOKINE; LIPOPOLYSACCHARIDE BINDING PROTEIN; LIPOTEICHOIC ACID; MACROPHAGE INFLAMMATORY PROTEIN 2; THROMBOCYTE ACTIVATING FACTOR RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; FIBRINOGEN RECEPTOR; G PROTEIN COUPLED RECEPTOR; LIPOPOLYSACCHARIDE; TEICHOIC ACID; THROMBOCYTE ACTIVATING FACTOR; TLR2 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN FUNCTION; ARTICLE; BACTERIAL INFECTION; CELL FUNCTION; CELL WALL; CONTROLLED STUDY; DOSE RESPONSE; EMBRYO; FEMALE; GRAM POSITIVE BACTERIUM; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MEDIATOR; MOUSE; NONHUMAN; PHENOTYPE; PNEUMONIA; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN DEFICIENCY; ACUTE DISEASE; ANIMAL; BACTERIAL PNEUMONIA; C57BL MOUSE; CELL LINE; GENETICS; IMMUNOLOGY; LUNG; LUNG ALVEOLUS; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY;

ACUTE DISEASE; ANIMALS; ANTIGENS, CD14; CELL LINE; FEMALE; HUMANS; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; LUNG; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLATELET ACTIVATING FACTOR; PLATELET MEMBRANE GLYCOPROTEINS; PNEUMONIA, BACTERIAL; PULMONARY ALVEOLI; RECEPTORS, G-PROTEIN-COUPLED; TEICHOIC ACIDS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

EID: 46349097273     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.5.3478     Document Type: Article

References (57)

1. 2005. Deaths: leading causes for 2002. Nat. Vital Stat. Rep. 53: 1-90.
2. Ginsburg, I. 2002. Role of lipoteichoic acid in infection and inflammation. Lancet Infect. Dis. 2: 171-179.
3. Kengatharan, K. M., S. De Kimpe, C. Robson, S. J. Foster, and C. Thiemermann. 1998. Mechanism of Gram-positive shock: identification of peptidoglycan and lipoteichoic acid moieties essential in the induction of nitric oxide synthase, shock, and multiple organ failure. J. Exp. Med. 188: 305-315.
4. von Aulock, S., S. Morath, L. Hareng, S. Knapp, K. P. van Kessel, J. A. van Strijp, and T. Hartung. 2003. Lipoteichoic acid from Staphylococcus aureus is a potent stimulus for neutrophil recruitment. Immunobiology 208: 413-422.
5. Ellingsen, E., S. Morath, T. Flo, A. Schromm, T. Hartung, C. Thiemermann, T. Espevik, D. Golenbock, D. Foster, R. Solberg, et al. 2002. Induction of cytokine production in human T cells and monocytes by highly purified lipoteichoic acid: involvement of Toll-like receptors and CD14. Med. Sci. Monit. 8: BR149-BR156.
6. Leemans, J. C., M. J. Vervoordeldonk, S. Florquin, K. P. Van Kessel, and T. Van Der Poll. 2002. Differential role of interleukin-6 in lung inflammation induced by lipoteichoic acid and peptidoglycan from Staphylococcus aureus. Am. J. Respir. Crit. Care Med. 165: 1445-1450.
7. Wang, J. E., P. F. Jorgensen, M. Almlof, C. Thiemermann, S. J. Foster, A. O. Aasen, and R. Solberg. 2000. Peptidoglycan and lipoteichoic acid from Staphylococcus aureus induce tumor necrosis factor α, interleukin 6 (IL-6), and IL-10 production in both T cells and monocytes in a human whole blood model. Infect. Immun. 68: 3965-3970.
8. Opitz, B., N. W. Schroder, I. Spreitzer, K. S. Michelsen, C. J. Kirschning, W. Hallatschek, U. Zahringer, T. Hartung, U. B. Gobel, and R. R. Schumann. 2001. Toll-like receptor-2 mediates Treponema glycolipid and lipoteichoic acid-induced NF-κB translocation. J. Biol. Chem. 276: 22041-22047.
9. Michelsen, K. S., A. Aicher, M. Mohaupt, T. Hartung, S. Dimmeler, C. J. Kirschning, and R. R. Schumann. 2001. The role of Toll-like receptors (TLRs) in bacteria-induced maturation of murine dendritic cells (DCs): peptidoglycan and lipoteichoic acid are inducers of DC maturation and require TLR2. J. Biol. Chem. 276: 25680-25686.
10. Triantafilou, M., M. Manukyan, A. Mackie, S. Morath, T. Hartung, H. Heine, and K. Triantafilou. 2004. Lipoteichoic acid and Toll-like receptor 2 internalization and targeting to the Golgi are lipid raft-dependent. J. Biol. Chem. 279: 40882-40889.
11. Schroder, N. W., S. Morath, C. Alexander, L. Hamann, T. Hartung, U. Zahringer, U. B. Gobel, J. R. Weber, and R. R. Schumann. 2003. Lipoteichoic acid (LTA) of Streptococcus pneumoniae and Staphylococcus aureus activates immune cells via Toll-like receptor (TLR)-2, lipopolysaccharide- binding protein (LBP), and CD14, whereas TLR-4 and MD-2 are not involved. J. Biol. Chem. 278: 15587-15594.
12. Han, S. H., J. H. Kim, M. Martin, S. M. Michalek, and M. H. Nahm. 2003. Pneumococcal lipoteichoic acid (LTA) is not as potent as staphylococcal LTA in stimulating Toll-like receptor 2. Infect. Immun. 71: 5541-5548.
13. Knapp, S., C. W. Wieland, C. van 't Veer, O. Takeuchi, S. Akira, S. Florquin, and T. van der Poll. 2004. Toll-like receptor 2 plays a role in the early inflammatory response to murine pneumococcal pneumonia but does not contribute to antibacterial defense. J. Immunol. 172: 3132-3138.
14. 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 Gram-negative and Gram-positive bacterial cell wall components. Immunity 11: 443-451.
15. Yang, S., R. Tamai, S. Akashi, O. Takeuchi, S. Akira, S. Sugawara, and H. Takada. 2001. Synergistic effect of muramyldipeptide with lipopolysaccharide or lipoteichoic acid to induce inflammatory cytokines in human monocytic cells in culture. Infect. Immun. 69: 2045-2053.
16. Morath, S., A. Geyer, and T. Hartung. 2001. Structure-function relationship of cytokine induction by lipoteichoic acid from Staphylococcus aureus. J. Exp. Med. 193: 393-397.
17. Lotz, S., E. Aga, I. Wilde, G. van Zandbergen, T. Hartung, W. Solbach, and T. Laskay. 2004. Highly purified lipoteichoic acid activates neutrophil granulocytes and delays their spontaneous apoptosis via CD14 and TLR2. J. Leukocyte Biol. 75: 467-477.
18. Hattar, K., U. Grandel, A. Moeller, L. Fink, J. Iglhaut, T. Hartung, S. Morath, W. Seeger, F. Grimminger, and U. Sibelius. 2006. Lipoteichoic acid (LTA) from Staphylococcus aureus stimulates human neutrophil cytokine release by a CD14-dependent, Toll-like-receptor-independent mechanism: autocrine role of tumor necrosis factor-α in mediating LTA-induced interleukin-8 generation. Crit. Care Med. 34: 835-841.
19. Hermann, C., I. Spreitzer, N. W. Schroder, S. Morath, M. D. Lehner, W. Fischer, C. Schutt, R. R. Schumann, and T. Hartung. 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-γ release. Eur. J. Immunol. 32: 541-551.
20. Hamann, L., C. Stamme, A. J. Ulmer, and R. R. Schumann. 2002. Inhibition of LPS-induced activation of alveolar macrophages by high concentrations of LPS-binding protein. Biochem. Biophys. Res. Commun. 295: 553-560.
21. Martin, T. R., G. D. Rubenfeld, J. T. Ruzinski, R. B. Goodman, K. P. Steinberg, D. J. Leturcq, A. M. Moriarty, G. Raghu, R. P. Baughman, and L. D. Hudson. 1997. Relationship between soluble CD14, lipopolysaccharide binding protein, and the alveolar inflammatory response in patients with acute respiratory distress syndrome. Am. J. Respir. Crit. Care Med. 155: 937-944.
22. Wright, S. D., R. A. Ramos, P. S. Tobias, R. J. Ulevitch, and J. C. Mathison. 1990. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249: 1431-1433.
23. Martin, T. R., J. C. Mathison, P. S. Tobias, D. J. Leturcq, A. M. Moriarty, R. J. Maunder, and R. J. Ulevitch. 1992. Lipopolysaccharide binding protein enhances the responsiveness of alveolar macrophages to bacterial lipopolysaccharide: implications for cytokine production in normal and injured lungs. J. Clin. Invest. 90: 2209-2219.
24. Wurfel, M. M., B. G. Monks, R. R. Ingalls, R. L. Dedrick, R. Delude, D. Zhou, N. Lamping, R. R. Schumann, R. Thieringer, M. J. Fenton, et al. 1997. Targeted deletion of the lipopolysaccharide (LPS)-binding protein gene leads to profound suppression of LPS responses ex vivo, whereas in vivo responses remain intact. J. Exp. Med. 186: 2051-2056.
25. Dentener, M. A., A. C. Vreugdenhil, P. H. Hoet, J. H. Vernooy, F. H. Nieman, D. Heumann, Y. M. Janssen, W. A. Buurman, and E. F. Wouters. 2000. Production of the acute-phase protein lipopolysaccharide-binding protein by respiratory type II epithelial cells: implications for local defense to bacterial endotoxins. Am. J. Respir. Cell Mol. Biol. 23: 146-153.
26. Knapp, S., S. Florquin, D. T. Golenbock, and T. van der Poll. 2006. Pulmonary lipopolysaccharide (LPS)-binding protein inhibits the LPS-induced lung inflammation in vivo. J. Immunol. 176: 3189-3195.
27. Fan, X., F. Stelter, R. Menzel, R. Jack, I. Spreitzer, T. Hartung, and C. Schutt. 1999. Structures in Bacillus subtilis are recognized by CD14 in a lipopolysaccharide binding protein-dependent reaction. Infect. Immun. 67: 2964-2968.
28. Lemjabbar, H., and C. Basbaum. 2002. Platelet-activating factor receptor and ADAM10 mediate responses to Staphylococcus aureus in epithelial cells. Nat. Med. 8: 41-46.
29. Han, S. H., J. H. Kim, H. S. Seo, M. H. Martin, G.-H. Chung, S. M. Michalek, and M. H. Nahm. 2006. Lipoteichoic acid-induced nitric oxide production depends on the activation of platelet-activating factor receptor and Jak2. J. Immunol. 176: 573-579.
30. Muir, A., G. Soong, S. Sokol, B. Reddy, M. I. Gomez, A. van Heeckeren, and A. Prince. 2004. Toll-like receptors in normal and cystic fibrosis airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 30: 777-783.
31. Sha, Q., A. Q. Truong-Tran, J. R. Plitt, L. A. Beck, and R. P. Schleimer. 2004. Activation of airway epithelial cells by Toll-like receptor agonists. Am. J. Respir. Cell Mol. Biol. 31: 358-364.
32. Moore, K. J., L. P. Andersson, R. R. Ingalls, B. G. Monks, R. Li, M. A. Arnaout, D. T. Golenbock, and M. W. Freeman. 2000. Divergent response to LPS and bacteria in CD14-deficient murine macrophages. J. Immunol. 165: 4272-4280.
33. Hoshino, K., O. Takeuchi, T. Kawai, H. Sanjo, T. Ogawa, Y. Takeda, K. Takeda, and S. Akira. 1999. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol. 162: 3749-3752.
34. Ishii, S., T. Kuwaki, T. Nagase, K. Maki, F. Tashiro, S. Sunaga, W.-H. Cao, K. Kume, Y. Fukuchi, K. Ikuta, et al. 1998. Impaired anaphylactic responses with intact sensitivity to endotoxin in mice lacking a platelet-activating factor receptor. J. Exp. Med. 187: 1779-1788.
35. Rijneveld, A. W., G. P. van den Dobbelsteen, S. Florquin, T. J. Standiford, P. Speelman, L. van Alphen, and T. van der Poll. 2002. Roles of interleukin-6 and macrophage inflammatory protein-2 in pneumolysin-induced lung inflammation in mice. J. Infect. Dis. 185: 123-126.
36. von Aulock, S., T. Hartung, and C. Hermann. 2007. Comment on "Not Lipoteichoic Acid but Lipoproteins Appear to Be the Dominant Immunobiologically Active Compounds in Staphylococcus aureus." J. Immunol. 178: 2610.
37. Latz, E., A. Visintin, E. Lien, K. A. Fitzgerald, B. G. Monks, E. A. Kurt-Jones, D. T. Golenbock, and T. Espevik. 2002. Lipopolysaccharide rapidly traffics to and from the Golgi apparatus with the Toll-like receptor 4-MD-2-CD14 complex in a process that is distinct from the initiation of signal transduction. J. Biol. Chem. 277: 47834-47843.
38. Divanovic, S., A. Trompette, S. F. Atabani, R. Madan, D. T. Golenbock, A. Visintin, R. W. Finberg, A. Tarakhovsky, S. N. Vogel, Y. Belkaid, et al. 2005. Negative regulation of Toll-like receptor 4 signaling by the Toll-like receptor homolog RP105. Nat. Immunol. 6: 571-578.
39. Tobias, P., and L. K. Curtiss. 2005. Thematic Review Series: The Immune System and Atherogenesis: paying the price for pathogen protection: Toll receptors in atherogenesis. J. Lipid Res. 46: 404-411.
40. Jiang, D., J. Liang, J. Fan, S. Yu, S. Chen, Y. Luo, G. D. Prestwich, M. M. Mascarenhas, H. G. Garg, D. A. Quinn, et al. 2005. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat. Med. 11: 1173-1179.
41. Jiang, D., J. Liang, Y. Li, and P. W. Noble. 2006. The role of Toll-like receptors in non-infectious lung injury. Cell Res. 16: 693-701.
42. Walton, K. A., X. Hsieh, N. Gharavi, S. Wang, G. Wang, M. Yeh, A. L. Cole, and J. A. Berliner. 2003. Receptors involved in the oxidized 1-palmitoyl-2-arachidonoyl-sn-glycero-3-phosphorylcholine-mediated synthesis of interleukin-8: a role for Toll-like receptor 4 and a glycosylphosphatidylinositol-anchored protein. J. Biol. Chem. 278: 29661-29666.
43. Schaefer, L., A. Babelova, E. Kiss, H.-J. Hausser, M. Baliova, M. Krzyzankova, G. Marsche, M. F. Young, D. Mihalik, M. Gotte, et al. 2005. The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J. Clin. Invest. 115: 2223-2233.
44. Ohashi, K., V. Burkart, S. Flohe, and H. Kolb. 2000. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the Toll-like receptor-4 complex. J. Immunol. 164: 558-561.
45. Vabulas, R. M., P. Ahmad-Nejad, S. Ghose, C. J. Kirschning, R. D. Issels, and H. Wagner. 2002. HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J. Biol. Chem. 277: 15107-15112.
46. Hasty, D. L., S. Meron-Sudai, K. H. Cox, T. Nagorna, E. Ruiz-Bustos, E. Losi, H. S. Courtney, E. A. Mahrous, R. Lee, and I. Ofek. 2006. Monocyte and macrophage activation by lipoteichoic acid is independent of alanine and is potentiated by hemoglobin. J. Immunol. 176: 5567-5576.
47. Cox, K. H., I. Ofek, and D. L. Hasty. 2007. Enhancement of macrophage stimulation by lipoteichoic acid and the costimulant hemoglobin is dependent on Toll-like receptors 2 and 4. Infect. Immun. 75: 2638-2641.
48. Juffermans, N. P., A. Verbon, J. T. Belisle, P. J. Hill, P. Speelman, S. J. van Deventer, and T. van der Poll. 2000. Mycobacterial lipoarabinomannan induces an inflammatory response in the mouse lung: a role for interleukin-1. Am. J. Respir. Crit. Care Med. 162: 486-489.
49. Wiersinga, W. J., C. W. Wieland, M. C. Dessing, N. Chantratita, A. C. Cheng, D. Limmathurotsakul, W. Chierakul, M. Leendertse, S. Florquin, A. F. de Vos, et al. 2007. Toll-like receptor 2 impairs host defense in gram-negative sepsis caused by Burkholderia pseudomallei (melioidosis). PLoS Med. 4: e248.
50. Zimmerman, G. A., T. M. McIntyre, S. M. Prescott, and D. M. Stafforini. 2002. The platelet-activating factor signaling system and its regulators in syndromes of inflammation and thrombosis. Crit. Care Med. 30: S294-301.
51. Bonfield, T., M. Konstan, P. Burfeind, J. Panuska, J. Hilliard, and M. Berger. 1995. Normal bronchial epithelial cells constitutively produce the anti- inflammatory cytokine interleukin-10, which is downregulated in cystic fibrosis. Am. J. Respir. Cell Mol. Biol. 13: 257-261.
52. Fernandez, S., P. Jose, M. G. Avdiushko, A. M. Kaplan, and D. A. Cohen. 2004. Inhibition of IL-10 receptor function in alveolar macrophages by Toll-like receptor agonists. J. Immunol. 172: 2613-2620.
53. Strieter, R. M., J. A. Belperio, and M. P. Keane. 2002. Cytokines in innate host defense in the lung. J. Clin. Invest. 109: 699-705.
54. van der Poll, T., A. Marchant, C. V. Keogh, M. Goldman, and S. F. Lowry. 1996. Interleukin-10 impairs host defense in murine pneumococcal pneumonia. J. Infect. Dis. 174: 994-1000.
55. Steinhauser, M. L., C. M. Hogaboam, S. L. Kunkel, N. W. Lukacs, R. M. Strieter, and T. J. Standiford. 1999. IL-10 is a major mediator of sepsis-induced impairment in lung antibacterial host defense. J. Immunol. 162: 392-399.
56. Greenberger, M. J., R. M. Strieter, S. L. Kunkel, J. M. Danforth, R. E. Goodman, and T. J. Standiford. 1995. Neutralization of IL-10 increases survival in a murine model of Klebsiella pneumonia. J. Immunol. 155: 722-729.
57. Netea, M. G., J. W. M. Van der Meer, R. P. Sutmuller, G. J. Adema, and B.-J. Kullberg. 2005. From the Th1/Th2 paradigm towards a Toll-like receptor/Thelper bias. Antimicrob. Agents Chemother. 49: 3991-3996.