Toll-like receptor 2- and 6-mediated stimulation by macrophage-activating lipopeptide 2 induces lipopolysaccharide (LPS) cross tolerance in mice, which results in protection from tumor necrosis factor alpha but in only partial protection from lethal LPS doses

Infection and Immunity

Volumn 71, Issue 8, 2003, Pages 4456-4462

  Deiters, Ursula ^a   Gumenscheimer, Marina ^b   Galanos, Chris ^b   Mühlradt, Peter F ^a,c  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^c Wound Healing Research Group   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GALACTOSAMINE; INTERLEUKIN 6; LIPOPEPTIDE; LIPOPOLYSACCHARIDE; MACROPHAGE ACTIVATING LIPOPEPTIDE 2; PYROGEN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 6; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADOLESCENT; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CROSS TOLERANCE; CYTOKINE RELEASE; FEMALE; LETHAL DOSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROVOCATION TEST; RABBIT; SENSITIZATION; SHOCK; SURVIVAL;

ANIMALS; DRUG TOLERANCE; FEMALE; GALACTOSAMINE; HUMANS; LIPOPOLYSACCHARIDES; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; OLIGOPEPTIDES; PYROGENS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0042265135     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.8.4456-4462.2003     Document Type: Article

References (67)

1. Arbibe, L., J.-P. Mira, N. Teusch, L. Kline, M. Guha, N. Mackman, P. J. Godowski, R. J. Ulevitch, and U. G. Knaus. 2000. Toll-like receptor 2-mediated NF-κB activation requires a Rac1-dependent pathway. Nat. Immunol. 1:533-540.
2. Basu, S., A. R. Dunn, M. W. Marino, H. Savoia, G. Hodgson, G. J. Lieschke, and J. Cebon. 1997. Increased tolerance to endotoxin by granulocyte-macrophage colony-stimulating factor-deficient mice. J. Immunol. 159:1412-1417.
3. Berg, D. J., R. Kühn, K. Rajewsky, W. Müller, S. Menon, N. Davidson, G. Grünig, and D. Rennick. 1995. Interleukin-10 is a central regulator of the response to LPS in murine models of endotoxic shock and the Schartzman reaction but not to endotoxin tolerance. J. Clin. Investig. 96:2339-2347.
4. Car, B. D., V. M. Eng, B. Schnyder, L. Ozmen, S. Huang, P. Gallay, D. Heumann, M. Aguet, and B. Ryffel. 1994. Interferon-γ receptor deficient mice are resistant to endotoxic shock. J. Exp. Med. 179:1437-1444.
5. Carson, W. E., H. Yu, J. Dierksheide, K. Pfeffer, P. Bouchard, R. Clark, J. Durbin, A. S. Baldwin, J. Peschon, P. R. Johnson, G. Ku, H. Baumann, and M. A. Caligiuri. 1999. A fatal cytokine-induced systemic inflammatory response reveals a critical role for NK cells. J. Immunol. 162:4943-4951.
6. Deitch, E. A. 1998. Animal models of sepsis and shock: a review and lessons learned. Shock 9:1-11.
7. Deiters, U., and P. F. Mühlradt. 1999. Mycoplasmal lipopeptide MALP-2 induces the chemoattractant proteins MIP-1α, MCP-1, and MIP-2 and promotes leukocyte infiltration in mice. Infect. Immun. 67:3390-3398.
8. Di Santo, E., C. Meazza, M. Sironi, P. Fruscella, A. Mantovani, J. D. Sipe, and P. Ghezzi. 1997. IL-13 inhibits TNF production but potentiates that of IL-6 in vivo and ex vivo in mice. J. Immunol. 159:379-382.
9. Doherty, G. M., J. R. Lange, H. N. Langstein, H. R. Alexander, C. M. Buresh, and J. A. Norton. 1992. Evidence for IFN-γ as a mediator of the lethality of endotoxin and tumor necrosis factor-alpha. J. Immunol. 149:1666-1670.
10. Faure, E., O. Equils, P. A. Sieling, L. Thomas, F. X. Zhang, C. J. Kirschning, N. Polentarutti, M. Muzio, and M. Arditi. 2000. Bacterial lipopolysaccharide activates NF-κB through Toll-like receptor 4 (TLR-4) in cultured human dermal endothelial cells. Differential expression of TLR-4 and TLR-2 in endothelial cells. J. Biol. Chem. 275:11058-11063.
11. Fiedler, V. B., I. Loof, E. Sander, V. Voehringer, C. Galanos, and M. A. Fournel. 1992. Monoclonal antibody to tumor necrosis factor-alpha prevents lethal endotoxin sepsis in adult rhesus monkeys. J. Lab. Clin. Med. 120:574-588.
12. Flo, T. H., O. Halaas, S. Torp, L. Ryan, E. Lien, B. Dybdahl, A. Sundan, and T. Espevik. 2001. Differential expression of Toll-like receptor 2 in human cells. J. Leukoc. Biol. 69:474-481.
13. Freudenberg, M. A., and C. Galanos. 1985. Alterations in rats in vivo of the chemical structure of lipopolysaccharide from Salmonella abortus equi. Eur. J. Biochem. 152:353-359.
14. Freudenberg, M. A., and C. Galanos. 1988. Induction of tolerance to lipopolysaccharide (LPS)-D-galactosamine lethality by pretreatment with LPS is mediated by macrophages. Infect. Immun. 56:1352-1357.
15. Freudenberg, M. A., and C. Galanos. 1991. Tumor necrosis factor alpha mediates lethal activity of killed gram-negative and gram-positive bacteria in D-galactosamine-treated mice. Infect. Immun. 59:2110-2115.
16. Freudenberg, M. A., R. Salomao, A. Sing, I. Mitov, and C. Galanos. 1998. Reconciling the concepts of endotoxin sensitization and tolerance. Prog. Clin. Biol. Res. 397:261-268.
17. Galanos, C., O. Lüderitz, and O. Westphal. 1979. Preparation and properties of a standardized lipopolysaccharide from Salmonella abortus equi (Novo-Pyrexal). Zentbl. Bakteriol. Infektkrankh. Hyg. Abt. 1 Orig. Reihe A 243:226-244.
18. Galanos, C., M. A. Freudenberg, T. Katschinski, R. Salomao, H. Mossmann, and Y. Kumazawa. 1992. Tumor necrosis factor and host response to endotoxin, p. 75-104. In J. L. Ryan, and D. C. Morrison (ed.), Bacterial endotoxic lipopolysaccharides, vol. III. Immunopharmacology and pathophysiology. CRC Press, Boca Raton, Fla.
19. Hauschildt, S., H. U. Beuscher, G. Jung, W. Bessler, and A. Ulmer. 1994. Intraperitoneal injection of synthetic bacterial lipopeptides does not cause a rise in circulating inflammatory cytokines. FEMS Immunol. Med. Microbiol. 8:77-82.
20. Heremans, H., C. Dillen, J. van Damme, and A. Billiau. 1994. Essential role for natural killer cells in the lethal lipopolysaccharide-induced Shwartzman-like reaction in mice. Eur. J. Immunol. 24:1155-1160.
21. Horng, T., G. M. Barton, and R. Medzhitov. 2001. TIRAP: an adaptor molecule in the toll signaling pathway. Nature Immunol. 2:835-841.
22. Hornung, V., S. Rothenfusser, S. Britsch, A. Krug, B. Jahrsdörfer, T. Giese, S. Endres, and G. Hartmann. 2002. Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J. Immunol. 168:4531-4537.
23. Jacinto, R., T. Hartung, C. McCall, and L. Li. 2002. Lipopolysaccharide- and lipoteichoic acid-induced tolerance and cross-tolerance: distinct alterations in IL-1 receptor-associated kinase. J. Immunol. 168:6136-6141.
24. Jin, L., D. P. Raymond, T. D. Crabtree, S. J. Pelletier, C. K. Rudy, T. L. Pruett, and R. G. Sawyer. 2002. Preexposure of murine macrophages to CpG-containing oligonucleotides results in nuclear factor κB p50 homodimer-associated hyporesponsiveness. Surgery 132:245-251.
25. Karp, C. L., M. Wysocka, X. Ma, M. Marovich, R. E. Factor, T. Nutman, M. Armant, L. Wahl, P. Cuomo, and G. Trinchieri. 1998. Potent suppression of IL-12 production from monocytes and dendritic cells during endotoxin tolerance. Eur. J. Immunol. 28:3128-3136.
26. Katschinski, T., C. Galanos, A. Coumbos, and M. A. Freudenberg. 1992. Gamma interferon mediates Propionibacterium acnes-induced hypersensitivity to lipopolysaccharide in mice. Infect. Immun. 60:1994-2001.
27. Kaufmann, A., E. Rischkowsky, P. F. Mühlradt, D. Gemsa, and H. Sprenger. 1999. Induction of cytokines and chemokines in human monocytes by Mycoplasma fermentans-derived lipoprotein MALP-2. Infect. Immun. 67:6303-6308.
28. Kawai, T., O. Adachi, T. Ogawa, K. Takeda, and S. Akira. 1999. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11:115-122.
29. Kawai, T., O. Takeuchi, T. Fujita, J. Inoue, P. F. Mühlradt, S. Sato, K. Hoshino, and S. Akira. 2001. Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J. Immunol. 167:5887-5894.
30. Kiani, A., A. Tschiersch, E. Gaboriau, F. Otto, A. Seiz, H. P. Knopf, P. Stutz, L. Faber, U. Haus, C. Galanos, R. Mertelsmann, and R. Engelhadt. 1997. Downregulation of the proinflammatory cytokine response to endotoxin by pretreatment with the nontoxic lipid A analog SDZ MRL 953 in cancer patients. Blood 90:1673-1683.
31. Kobayashi, K., L. D. Hernandez, J. E. Galán, C. A. Janeway, Jr., R. Medzhitov, and R. A. Flavell. 2002. IRAK-M is a negative regulator of toll-like receptor signaling. Cell 110:191-202.
32. Kraatz, J., L. Clair, J. L. Rodriguez, and M. A. West. 1999. Macrophage TNF secretion in endotoxin tolerance: role of SAPK, p38, and MAPK. J. Surg. Res. 83:158-164.
33. Kreutz, M., U. Ackermann, S. Hauschildt, S. W. Krause, D. Riedel, W. Bessler, and R. Andreesen. 1997. A comparative analysis of cytokine production and tolerance induction by bacterial lipopeptides, lipopolysaccharides and Staphylococcus aureus in human monocytes. Immunology 92:396-401.
34. Lehmann, V., M. A. Freudenberg, and C. Galanos. 1987. Lethal toxicity of lipopolysaccharide and tumor necrosis factor in normal and D-galactosamine-treated mice. J. Exp. Med. 165:657-663.
35. Lehner, M. D., S. Morath, K. S. Michelsen, R. R. Schumann, and T. Hartung. 2001. Induction of cross-tolerance by lipopolysaccharide and highly purified lipoteichoic acid via different toll-like receptors independent of paracrine mediators. J. Immunol. 166:5161-5167.
36. Lehner, M. D., and T. Hartung. 2002. Endotoxin tolerance mechanisms and beneficial effects in bacterial infections. Rev. Physiol. Biochem. Pharmacol. 144:95-141.
37. Li, L., S. Cousart, J. Hu, and C. E. McCall. 2000. Characterization of interleukin-1 receptor associated kinase in normal and endotoxin-tolerant cells. J. Biol. Chem. 275:23340-23345.
38. Lührmann, A., U. Deiters, J. Skokowa, M. Hanke, J. E. Gessner, P. F. Mühlradt, R. Papst, and T. Tschernig. 2002. In vivo effects of a synthetic 2-kilodalton macrophage-activating lipopeptide of Mycoplasma fermentans after pulmonary application. Infect. Immun. 70:3785-3792.
39. Madonna, G. S., and S. N. Vogel. 1985. Early endotoxin tolerance is associated with alterations in bone marrow-derived macrophage precursor pools. J. Immunol. 135:3763-3771.
40. Matsugushi, T., K. Takagi, T. Musikacharoen, and Y. Yoshikai. 2000. Gene expression of lipopolysaccharide receptors, toll-like receptors 2 and 4, are differently regulated in mouse T lymphocytes. Blood 95:1378-1385.
41. Medvedev, A. E., A. Lentschat, L. M. Wahl, D. T. Golenbock, and S. N. Vogel. 2002. Dysregulation of LPS-induced toll-like receptor 4-MyD88 complex formation and IL-1 receptor-associated kinase 1 activation in endotoxin-tolerant cells. J. Immunol. 169:5209-5216.
42. d C57BL/10ScCr mouse. J. Immunol. 166:566-573.
43. Metzger, J. W., K.-H. Wiesmüller, and G. Jung. 1991. Synthesis of N-alpha-Fmoc protected derivatives of S-(2,3-dihydroxypropyl)-cysteine and their application in peptide synthesis. Int. J. Pept. Protein Res. 38:545-554.
44. Morr, M., O. Takeuchi, S. Akira, M. M. Simon, and P. F. Mühlradt. 2002. Differential recognition of structural details of bacterial lipopeptides by toll-like receptors. Eur. J. Immunol. 32:3337-3347.
45. Mühlradt, P. F., and U. Schade. 1991. MDHM, a macrophage-stimulatory product of Mycoplasma fermentans, leads to in vitro interleukin-1 (IL-1), IL-6, tumor necrosis factor, and prostaglandin production and is pyrogenic in rabbits. Infect. Immun. 59:3969-3974.
46. Mühlradt, P. F., and M. Frisch. 1994. Purification and partial biochemical characterization of a Mycoplasma fermentans-derived substance that activates macrophages to release nitric oxide, TNF, and IL-6. Infect. Immun. 62:3801-3807.
47. Mühlradt, P. F., M. Kieß, H. Meyer, R. Süßmuth, and G. Jung. 1997. Isolation, structure elucidation, and synthesis of a macrophage stimulatory lipopeptide from Mycoplasma fermentans acting at picomolar concentration. J. Exp. Med. 185:1951-1958.
48. Muzio, M., J. Ni, P. Feng, and V. M. Dixit. 1997. IRAK (Pelle) family member IRAK-2 and MyD88 as proximal mediators of IL-1 signaling. Science 278:1612-1615.
49. Muzio, M., D. Bosisio, N. Polentarutti, G. D'Amico, A. Stoppacciaro, R. Mancinelli, C. van't Veer, G. Penton-Rol, L. P. Ruco, P. Allavena, and A. Mantovani. 2000. Differential expression and regulation of toll-like receptors (TLR) in human leukocytes: selective expression of TLR3 in dendritic cells. J. Immunol. 164:5998-6004.
50. Nose, M., A. Uzawa, M. Nomura, Y. Ikarashi, Y. Nakata, M. Akashi, and G. Suzuki. 1998. Control of endotoxin shock by the dried preparation of low virulent Streptococcus pyogenes OK-432. Cell. Immunol. 188:97-104.
51. Passlick, B., M. O. Labeta, J. R. Izbicki, P. Ostertag, T. Loffler, M. Siebeck, U. Pichlmeier, L. Schweiberer, and H. W. Ziegler-Heitbrock. 1995. Prevention of experimental endotoxin shock by a monocyte activator. Antimicrob. Agents Chemother. 39:2535-2540.
52. Poltorak, A., X. He, I. Smirnova, M.-Y. Liu, C. V. Huffel, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, M. A. Freudenberg, P. Ricciardi-Castagnoli, B. Layton, and B. Beutler. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085-2088.
53. Roth, J., T. Aslan, B. Störr, and E. Zeisberger. 1997. Lack of cross tolerance between LPS and muramyl dipeptide in induction of circulating TNF-α and IL-6 in guinea pigs. Am. J. Physiol. 273: R1529-R1533.
54. Sakao, Y., K. Takeda, H. Tsutsui, T. Kaisho, F. Nomura, H. Okamura, K. Nakanishi, and S. Akira. 1999. IL-18-deficient mice are resistant to endotoxin-induced liver injury but highly susceptible to endotoxin shock. Int. Immunol. 11:471-480.
55. Sato, S., F. Nomura, T. Kawai, O. Takeuchi, P. F. Mühlradt, K. Takeda, and S. Akira. 2000. Synergy and cross-tolerance between toll-like receptor (TLR)2- and TLR4-mediated signaling pathways. J. Immunol. 165:7096-7101.
56. Sato, S., O. Takeuchi, T. Fujita, H. Tomizawa, K. Takeda, and S. Akira. 2002. A variety of microbial components induce tolerance to lipopolysaccharide by differentially affecting MyD88-dependent and -independent pathways. Int. Immunol. 14:783-791.
57. Senaldi, G., C. L. Shaklee, J. Guo, L. Martin, T. Boone, T. W. Mak, and T. R. Ulich. 1999. Protection against the mortality associated with disease models mediated by TNF and IFN-γ in mice lacking IFN regulatory factor-1. J. Immunol. 163:6820-6826.
58. Szabó, C., C. Thiemermann, C. C. Wu, M. Perretti, and J. R. Vane. 1994. Attenuation of the induction of nitric oxide synthase by endogenous glucocorticoids accounts for endotoxin tolerance in vivo. Proc. Natl. Acad. Sci. USA 91:271-275.
59. Takeuchi, O., A. Kaufmann, K. Grote, T. Kawai, K. Hoshino, M. Morr, P. F. Mühlradt, and S. Akira. 2000. Cutting edge: preferentially the R-stereoisomer of the mycoplasmal lipopeptide macrophage-activating lipopeptide-2 activates immune cells through a Toll-like receptor 2- and MyD88-dependent signaling pathway. J. Immunol. 164:554-557.
60. Takeuchi, O., T. Kawai, P. F. Mühlradt, M. Morr, J. D. Radolf, A. Zychlinsky, Y. Takeda, and S. Akira. 2001. Discrimination of microbial lipoproteins by Toll-like receptor (TLR) 6. Int. Immunol. 13:933-940.
61. Toshchakov, V., B. W. Jones, P.-Y. Perera, K. Thomas, M. J. Cody, S. Zhang, B. R. G. Williams, J. Major, T. A. Hamilton, M. J. Fenton, and S. N. Vogel. 2002. TLR4, but not TLR2, mediates IFN-β-induced STAT1α/β-dependent gene expression in macrophages. Nat. Immunol. 3:392-398.
62. Werts, C., R. I. Tapping, J. C. Mathison, T. H. Chuang, V. Kravchenko, I. Saint Girons, D. A. Haake, P. J. Godowski, F. Hayashi, A. Ozinsky, D. M. Underhill, C. J. Kirschning, H. Wagner, A. Aderem, P. S. Tobias, and R. J. Ulevitch. 2001. Leptospiral lipopolysaccharide activates cells through a TLR2-dependent mechanism. Nat. Immunol. 2:346-352.
63. West, M. A., and W. Heagy. 2002. Endotoxin tolerance: a review. Crit. Care Med. 30:S64-S73.
64. Westphal, O., and K. Jann. 1965. Bacterial lipopolysaccharides. Extraction with phenol-water and further applications of the procedure. Methods Carbohydr. Chem. 5:83-91.
65. Yaegashi, Y., P. Nielsen, A. Sing, C. Galanos, and M. A. Freudenberg. 1995. Interferon beta, a cofactor in the interferon gamma production induced by gram-negative bacteria in mice. J. Exp. Med. 181:953-960.
66. Ziegler-Heitbrock, H. W. L., A. Wedel, W. Schraut, M. Ströbel, P. Wendelgass, T. Sternsdorf, P. Bäuerle, J. G. Haas, and G. Riethmüller. 1994. Tolerance to lipopolysaccharide involves mobilization of nuclear factor κB with predominance of p50 homodimers. J. Biol. Chem. 269:17001-17004.
67. Ziegler-Heitbrock, H. W. L. 1995. Molecular mechanism in tolerance to lipopolysaccharide. J. Inflamm. 45:13-26.