Cellular reprogramming by gram-positive bacterial components: A review

Journal of Leukocyte Biology

Volumn 80, Issue 4, 2006, Pages 731-741

  Buckley, Julliette M ^a   Jiang, Huai Wang ^a   Redmond, H Paul ^a  

^a University College Cork and INFANT Centre   (Ireland)

Author keywords

Cross tolerance; Lipopolysaccharide; Lipoprotein; TLR signaling; Tolerance

Indexed keywords

CD14 ANTIGEN; CELL SURFACE RECEPTOR; CYTOKINE; I KAPPA B KINASE; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 10; LIPOPOLYSACCHARIDE; LIPOPROTEIN; LIPOTEICHOIC ACID; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN MD 2; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

BACTERIAL CELL WALL; CROSS TOLERANCE; CYTOKINE PRODUCTION; GENE EXPRESSION; GRAM POSITIVE BACTERIUM; HUMAN; IMMUNOLOGICAL TOLERANCE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CYTOKINES; GRAM-POSITIVE BACTERIA; HUMANS; IMMUNE TOLERANCE; LIPOPOLYSACCHARIDES; LIPOPROTEINS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TEICHOIC ACIDS;

BACTERIA (MICROORGANISMS); POSIBACTERIA;

EID: 33751520650     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0506312     Document Type: Review

References (88)

1. Navarre, W. W., Schneewind, O. (1999) Surface proteins of gram positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol. Mol. Biol. Rev. 63, 174-229.
2. Beveridge, T. J. (1999) Structures of gram negative cell walls and their derived membrane vesicles. J. Bacteriol. 181, 4725-4733.
3. Medzhitov, R., Janeway Jr., C. A. (1997) Innate immunity: the virtues of a nonclonal system of recognition. Cell 91, 295-298.
4. Beeson, P. B. (1946) Development of tolerance to typhoid bacterial pyrogen and its abolition by reticuloendothelial blockade. Proc. Soc. Exp. Biol. Med. 61, 248-250.
5. Virca, G. D., Kim, S. Y., Glaser, K. B., Ulevitch, R. J. (1989) Lipopolysaccharide induces hyporesponsiveness to its own action in RAW 264.7 cells. J. Biol. Chem. 264, 21951-21956.
6. Zeisberger, E., Roth, J. (1998) Tolerance to pyrogens. Ann. N. Y. Acad. Sci. 856, 116-131.
7. Fan, H., Cook, J. A. (2004) Molecular mechanisms of endotoxin tolerance. J. Endotoxin Res. 10, 71-84.
8. Zhang, X., Morrison, D. C. (1993) Lipopolysaccharide structure-function relationship in activation versus reprogramming of mouse peritoneal macrophages. J. Leukoc. Biol. 54, 444-450.
9. Hashimoto, C., Hudson, K. L., Anderson, K. V. (1988) The Toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell 52, 269-279.
10. Medzhitov, R., Preston-Hulbert, P., Janeway, C. A. (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388, 394-397.
11. Akira, S., Takeda, K., Kaisho, T. (2001) Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2, 675-680.
12. Swantek, J. L., Tsen, M. F., Cobb, M. H., Thomas, J. A. (2000) IL-1 receptor-associated kinase modulates host responsiveness to endotoxin. J. Immunol. 164, 4301-4306.
13. Lomaga, M. A., Yeh, W. C., Sarosi, I., Duncan, G. S., Furlonger, C., Ho, A., Moroney, S., Capparelli, C., Van, G., Kaufman, S., Van der Heiden, A., Itie, A., Wakeham, A., Khoo, W., Sasaki, T., Cao, Z., Penninger, J. M., Paige, C. J., Lacey, D. L., Dunstan, C. R., Boyle, W. J., Goeddel, D. V., Mak, T. W. (1999) TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev. 13, 1015-1024.
14. Takeuchi, O., Akira, S. (2001) Toll-like receptors: their physiological role and signal transduction system. Int. Immunopharmacol. 1, 625-635.
15. Tapping, R. I., Akashi, S., Miyake, K., Godowski, P. J., Tobias, P. S. (2000) Toll-like receptor 4 but not Toll-like receptor 2 is a signaling receptor for Escherichia and Salmonella lipopolysaccharides. J. Immunol. 165, 5780-5787.
16. Akashi, S., Shimazu, R., Ogata, H., Nagai, Y., Takeda, K., Kimoto, M., Miyake, K. (2000) Cell surface expression and lipopolysaccharide signaling via the Toll-like receptor 4-MD2 complex on mouse peritoneal macrophages. J. Immunol. 164, 3471-3475.
17. Poltorak, A., He, X., Smirnova, I., Liu, M. Y., Van Huffel, C., Du, X., Birdwell, D., Alejos, E., Silva, M., Galanos, C., Freudenberg, M., Ricciardi-Castagnoli, P., Layton, B., Beutler, B. (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in the TLR4 gene. Science 282, 2085-2088.
18. Iwaki, D., Mitsuzawa, H., Murakami, S., Sano, H., Konishi, M., Akino, T., Kuroki, Y. (2002) The extracellular TLR2 domain directly binds peptidoglycan derived from Staphlycoccus aureus. J. Biol. Chem. 277, 24315-24320.
19. Schwandner, R., Dziarski, R., Wesche, H., Rothe, M., Kirschning, C. J. (1999) Peptidoglycan and lipoteichoic acid-induced activation is mediated via TLR2. J. Biol. Chem. 274, 17406-17409.
20. Yoshimura, A., Lien, E., Ingalls, R. R., Tuomanen, E., Dziarski, R., Golenbock, D. (1999) Recognition of gram positive cell wall components by the innate immune system occurs via Toll-like receptor 2. J. Immunol. 163, 1-5.
21. Brightbill, H. D., Libraty, D. H., Krutzik, S. R., Yang, R. B., Belisle, J. T., Bleharski, J. R., Maitland, M., Norgard, M. V., Plevy, S. E., Smale, S. T., Brennan, P. J., Bloom, B. R., Godowski, P. J., Modlin, R. L. (1999) Host defense mechanisms triggered by lipoproteins through Toll like receptors. Science 285, 732-736.
22. Takeuchi, O., Hoshino, K., Akira, S. (2000) Cutting edge: TLR2 deficient and MyD88 deficient mice are highly susceptible to Staphlycoccus aureus infection. J. Immunol. 165, 5392-5396.
23. Zhang, H., Neisel, D. W., Peterson, J. W., Klimpel, G. R. (1998) Lipoprotein release by bacteria: potential factor in bacterial pathogenesis. Infect. Immun. 66, 5196-5201.
24. Aliprantis, A. O., Yang, R. B., Mark, M. R., Suggett, S., Devaux, B., Radolf, J. D., Klimpel, G. R., Godowski, P., Zychlinsky, A. (1999) Cell activation and apoptosis by bacterial lipoproteins through Toll-like receptor 2. Science 285, 736-739.
25. Kreutz, M., Ackermann, U., Hauschildt, S., Krause, S. W., Reidel, D., Bessler, W., Andreesen, R. (1997) A comparative analysis of cytokine production and tolerance induction by bacterial lipopeptides, LPS and S. aureus in human monocytes. Immunology 92, 396-401.
26. Jacinto, R., Hartung, T., McCall, C., Li, L. (2002) Lipopolysaccharide and lipoteichoic acid-induced tolerance and cross tolerance: distinct alterations in IL-1 receptor associated kinase. J. Immunol. 168, 6136-6141.
27. Sato, S., Nomura, F., Kawai, T., Takeuchi, O., Muhlradt, P. F., Takeda, K., Akira, S. (2000) Synergy and cross tolerance between TLR2 and TLR4 mediated signaling pathways. J. Immunol. 165, 7096-7101.
28. Ausobsky, J. R., Cheadle, W. D., Brosky, B. G., Polk Jr., H. C. (1984) Muramyl dipeptide increases tolerance to shock and bacterial challenge in mice. Br. J. Surg. 71, 151-153.
29. Wang, J. H., Doyle, M., Manning, B. J., Blankson, S., Wu, Q. D., Power, C., Cahill, R. A., Redmond, H. P. (2003) Cutting edge: bacterial lipoprotein induces endotoxin-independent tolerance to septic shock. J. Immunol. 170, 14-18.
30. Deiters, U., Gumenscheimer, M., Galanos, C., Muhlradt, P. F. (2003) Toll-like receptor 2 and 6 mediated stimulation by macrophage activating lipopeptide 2 induces LPS cross tolerance in mice which results in protection from tumor necrosis factor α but only partial protection from lethal LPS doses. Infect. Immun. 71, 4456-4462.
31. Freudenberg, M. A., Galanos, C. (1991) Tumor necrosis factor α mediates lethal activity of killed gram negative and gram positive bacteria in D-galactosamine treated mice. Infect. Immun. 59, 2110-2115.
32. O'Brien, G. C., Wang, J. H., Redmond, H. P. (2005) Bacterial lipoprotein induces resistance to gram negative sepsis in TLR4 deficient mice via enhanced bacterial clearance. J. Immunol. 174, 1020-1026.
33. Lehner, M. D., Morath, S., Michelson, K. S., Schumann, R. R., Hartung, T. (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.
34. Frey, E. A., Miller, D. S., Jahr, T. G., Sundan, A., Bazil, V., Espevik, T., Finlay, B. B., Wright, S. D. (1992) Soluble CD14 participates in the response of cells to LPS. J. Exp. Med. 176, 1665-1671.
35. Haziot, A., Rong, G. W., Silver, J., Goyert, S. M. (1993) Recombinant soluble CD14 mediates the activation of endothelial cells by lipopolysaccharide. J. Immunol. 151, 1500-1507.
36. Wright, S. D., Ramos, R. A., Tobias, P. S., Ulevitch, R. J., Mathison, J. C. (1990) CD14, a receptor for complexes of lipopolysaccharide and LPS binding protein. Science 249, 1431-1433.
37. Wooten, R. M., Morrisson, T. B., Weis, J. H., Wright, S. D., Thieringer, R., Weis, J. J. (1998) The role of CD14 in signaling mediated by outer membrane lipoproteins of Borrelia burgdorferi. J. Immunol. 160, 5485-5492.
38. Hirschfeld, M., Kirschning, C. J., Schwandner, R., Wesche, H., Weis, J. H., Wooten, R. M., Weis, J. J. (1999) Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by Toll like receptor 2. J. Immunol. 163, 2382-2386.
39. Cleveland, M. G., Gorham, J. D., Muphy, T. L., Tuomanen, L., Murphy, K. M. (1996) Lipoteichoic acid preparations of gram positive bacteria induce interleukin-12 through a CD14 dependent pathway. Infect. Immun. 64, 1906-1912.
40. Wang, J. H., Doyle, M., Manning, B. J., Wu, Q. D., Blankson, S., Redmond, H. P. (2002) Induction of bacterial lipoprotein tolerance is associated with suppression of Toll like receptor 2 expression. J. Biol. Chem. 277, 36068-36075.
41. Siedlar, M., Frankenberger, M., Benkhart, E., Espevik, T., Quirling, M., Brand, K., Zimbala, M., Zeigler-Heitbrock, L. (2004) Tolerance induced by the lipopeptide Pam3Cys is due to ablation of IL-IR-associated kinase-1. J. Immunol. 173, 2736-2745.
42. Medvedev, A. E., Henneke, P., Schromm, A., Lien, E., Ingalls, R., Fenton, M., Golenbock, D., Vogel, S. (2001) Induction of tolerance to lipopolysaccharide and mycobacterial components in Chinese hamster ovary/CD14 cells is not affected by overexpression of Toll-like receptors 2 or 4. J. Immunol. 167, 2257-2267.
43. Nakayama, K., Okugawa, S., Yanagimoto, S., Kitazawa, T., Tsukada, K., Kawada, M., Kimura, S., Hirai, K., Takagaki, Y., Ota, Y. (2004) Involvement of IRAK-M in peptidoglycan-induced tolerance in macrophages. J. Biol. Chem. 279, 6629-6634.
44. Li, C. H., Wang, J. H., Redmond, H. P. (2006) Bacterial lipoprotein-induced self tolerance and cross tolerance to LPS are associated with reduced IRAK-1 expression and MyD88-IRAK complex formation. J. Leukoc. Biol. 79, 867-875.
45. Medvedev, A. E., Lentschat, A., Wahl, L. M., Golenbock, D. T., Vogel, S. N. (2002) Dysregulation of LPS-Toll-like receptor 4-MyD88 complex formation and IL-1R associated kinase-1 activation in endotoxin-tolerant cells. J. Immunol. 169, 5209-5216.
46. Matsuguchi, T., Musikacharoen, T., Ogawa, T., Yoshikai, Y. (2000) Gene expression of Toll-like receptor 2, but not Toll-like receptor 4, is induced by LPS and inflammatory cytokines in mouse macrophages. J. Immunol. 165, 5767-5772.
47. Faure, E., Thomas, L., Xu, H., Medvedev, A. E., Equils, O., Arditi, M. (2001) Bacterial lipopolysaccharide and IFN-γ induce Toll-like receptor 2 and Toll-like receptor 4 expression in human endothelial cells: the role of NF-κ B activation. J. Immunol. 166, 2018-2024.
48. Takeda, K., Akira, S. (2004) TLR signaling pathways. Semin. Immunol. 16, 3-9.
49. Kawai, T., Adachi, O., Ogawa, T., Takeda, K., Akira, S. (1999) Unresponsiveness of MyD88 deficient mice to endotoxin. Immunity 11, 115-122.
50. Takeuchi, O., Takeda, K., Hoshino, K., Adachi, O., Ogawa, T., Akira, S. (2000) Cellular responses to bacterial cell wall components are mediated through MyD88 signaling cascades. Int. Immunol. 12, 113-117.
51. Takeuchi, O., Kaufmann, A., Grote, K., Kawai, T., Hoshino, K., Morr, M., Muhlradt, P. F., Akira, S. (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.
52. Adib-Conquy, M., Cavaillon, J. M. (2002) γ Interferon and granulocyte/monocyte colony stimulating factor prevent endotoxin tolerance in human monocytes by promoting interleukin-1 receptor-associated kinase expression and its association to MyD88 and not by modulation TLR4 expression. J. Biol. Chem. 277, 27927-27934.
53. Janssens, S., Beyaert, R. (2003) Functional diversity and regulation of interleukin-1 receptor-associated kinase (IRAK) family members. Mol. Cell 11, 293-302.
54. Wesche, H., Gao, X., Li, X., Kirschning, C. J., Stark, G. R., Cao, Z. (1999) IRAK M is a novel member of the Pelle/interleukin-1 receptor-associated kinase (IRAK) family. J. Biol. Chem. 274, 19403-19410.
55. Medzhitov, R., Preston-Hurlburt, P., Kopp, E., Stadlen, A., Chen, C., Ghosh, S., Janeway Jr., C. A. (1998) MyD88 is an adaptor protein in hToll/IL-1 receptor family signaling pathways. Mol. Cell 2, 253-258.
56. Li, S., Strelow, A., Fontana, E. J., Wesche, H. (2002) IRAK-4: a novel member of the IRAK family with properties of an IRAK kinase. Proc. Natl. Acad. Sci. USA 99, 5567-5572.
57. Dobrovolskaia, M. A., Medvedev, A. E., Thomas, K. E., Cuesta, N., Toshchakov, V., Ren, T., Cody, M. J., Michalek, S. M., Rice, N. R., Vogel, S. N. (2003) Induction of in-vitro reprogramming by Toll-like receptor (TLR) 2 and TLR4 agonists in murine macrophages: effect of TLR homo-tolerance vs. heterotolerance on the NF-κB signaling pathway components. J. Immunol. 170, 508-519.
58. Suzuki, N., Suzuki, S., Duncan, G. S., Miller, D. G., Wada, T., Mirtsos, C., Takeda, H., Wakeham, A., Itie, A., Li, S., Penninger, J. M., Wesche, H., Ohashi, P. S., Mak, T. W., Yeh, W. C. (2002) Severe impairment of interleukin-1 and Toll-like receptor signaling in mice lacking IRAK-4. Nature 416, 750-756.
59. Kobayashi, K., Hernandez, L. D., Galen, J. E., Janeway Jr., C. A., Medzhitov, R., Flavell, R. A. (2002) IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 110, 191-202.
60. Escoll, P., del Fresno, C., Garcia, L., Valles, G., Ledenez, M. J., Amalich, F., Lopez-Collazo, E. (2003) Rapid upregulation of IRAK-M expression following a second endotoxin challenge in human monocytes and in monocytes isolated from septic patients. Biochem. Biophys. Res. Commun. 311, 465-472.
61. Karin, M. (1999) How NF-κB is activated: the role of the IκB kinase (IKK) complex. Oncogene 18, 6867-6874.
62. Ferlito, M., Squadrito, F., Halushka, P. V., Cook, J. A. (2001) Signal transduction events in Chinese hamster ovary cells expressing human CD14; effect of endotoxin desensitization. Shock 15, 291-296.
63. Kraatz, J., Clair, L., Rodriguez, J. L., West, M. A. (1999) In-vitro macrophage endotoxin tolerance: defective in vitro macrophage MAP kinase signal transduction after LPS pretreatment is not present in macrophages from C3H/HeJ endotoxin resistant mice. Shock 11, 58-63.
64. Medvedev, A. E., Kopydlowski, K. M., Vogel, S. N. (2000) Inhibition of lipopolysaccharide-induced signal transduction in endotoxin tolerized mouse macrophages: dysregulation of cytokine, chemokine and Toll-like receptor 2 and 4 gene expression. J. Immunol. 164, 5564-5574.
65. Ferlito, M., Romanenko, O. G., Ashton, S., Squadrito, F., Halushka, P. V., Cook, J. A. (2001) Effect of cross tolerance between endotoxin and TNF-α or IL-1β on cellular signaling and mediator production. J. Leukoc. Biol. 70, 821-829.
66. De Martin, R., Vanhove, B., Cheng, Q., Hofer, E., Czismadia, V., Winkler, H., Bach, F. H. (1993) Cytokine inducible expression in endothelial cells of an IκB-α like gene is regulated by NF-κB. EMBO J. 12, 2773-2779.
67. Zhang, G., Ghosh, S. (2001) Toll-like receptor mediated NF-κB activation: a phylogenetically conserved paradigm in innate immunity. J. Clin. Invest. 107, 13-19.
68. Ropert, C., Almeida, I. C., Clossel, M., Travassos, L. R., Ferguson, M. A., Cohen, P., Gazzinelli, R. T. (2001) Requirement of mitogen activated protein kinases and IκB phosphorylation for proinflammatory cytokine synthesis by macrophages indicates functional similarity of receptors triggered by glycosylphosphatidylinositol anchors from parasitic protozoa and bacterial lipopolysaccharide. J. Immunol. 166, 3423-3431.
69. Chang, L., Karin, M. (2001) Mammalian MAP kinase signaling cascades. Nature 410, 37-40.
70. Ropert, C., Closel, M., Chaves, A. C. L., Gazzinelli, R. T. (2003) Inhibition of p38/stress-activated protein kinase-2-dependent phosphatase restores function of interleukin-1 receptor-associated kinase-1, and reverses Toll-like receptor 2 and 4 dependent tolerance in macrophages. J. Immunol. 171, 1456-1465.
71. Campos, M. A., Almeida, I. C., Takeuchi, O., Akira, S., Valente, P., Procopio, D. O., Travassos, L. R., Smith, J. A., Golenbock, D. T., Gazzinelli, R. T. (2001) Activation of Toll-like receptor 2 by glycosylphophotidylinositol anchors from a protozoan parasite. J. Immunol. 167, 416-423.
72. Ropert, C., Ferreira, L. R., Campos, M. A., Procopio, D. O., Travassos, L. R., Ferguson, M. A., Reis, L. F., Tiexeira, M. M., Almeida, I. C., Gazzinelli, R. T. (2002) Macrophage signaling by glycosylphosphatidylinositol- anchored mucin-like glycoproteins derived from Trypanosoma cruzi trypomastigotes. Microbes Infect. 4, 1015-1025.
73. Wahlstrom, K., Bellingham, J., Rodriguez, J. L., West, M. A. (1999) Inhibitory κB α control of nuclear factor κB is dysregulated in endotoxin-tolerant macrophages. Shock 11, 242-247.
74. Tominaga, K., Saito, S., Matsuura, M., Nakano, M. (1999) Lipopolysaccharide tolerance in murine peritoneal macrophages induces downregulation of the lipopolysaccharide signal transduction pathway through mitogen-activated protein kinase and nuclear factor κB cascades but not lipopolysaccharide-incorporation steps. Biochim. Biophys. Acta 1450, 130-144.
75. Goldring, C. E., Reveneau, S., Pinard, D., Jeannin, J. F. (1998) Hyporesponsiveness to lipopolysaccharide alters the composition of NF-κB binding to the regulatory regions of inducible nitric oxide synthase gene. Eur. J. Immunol. 28, 2960-2970.
76. Ryseck, R. P., Bull, P., Takamiya, M., Bours, V., Siebenlist, U., Dobrzanski, P., Bravo, R. (1992) Rel B, a new Rel family transcription activator that can interact with p50-NF-κ-B. Mol. Cell. Biol. 12, 674-684.
77. Schmitz, M. L., Baeuerle, P. A. (1991) The p65 subunit is responsible for the strong transcription activating potential of NF-κ-B. EMBO J. 10, 3805-3817.
78. Ziegler-Heitbrock, H. W., Wedel, L. A., Schraut, W., Strobel, M., Wendelgass, P., Sternsdorf, T., Bauerle, P., Hass, J. G., Reithmuller, G. (1994) Tolerance to lipopolysaccharide involves mobilization of nuclear factor-κ-B with predominance of p50 homodimers. J. Biol. Chem. 269, 17001-17004.
79. Kastenbauer, S., Ziegler-Heitbrock, H. W. (1999) NF-κ-B1 (p50) is up-regulated in lipopolysaccharide tolerance and can block tumor necrosis factor gene expression. Infect. Immun. 67, 1553-1559.
80. Ziegler-Heitbrock, L. (2001) The p50 homodimer mechanism in tolerance to LPS. J. Endotoxin Res. 7, 219-222.
81. Chan, C., Li, L., McCall, C. E., Yoza, B. K. (2005) Endotoxin tolerance disrupts chromation remodeling and NF-κ-B transactivation at the IL-1β promoter. J. Immunol. 175, 461-468.
82. Feterowski, C., Novotny, A., Kaiser-Moore, S., Muhlradt, P., Robmann-Bloeck, T., Rump, M., Holzmann, B., Wieghardt, H. (2005) Attenuated pathogenesis of polymicrobial peritonitis after TLR2 agonist pretreatment involves ST2 up-regulation. Int. Immunol. 17, 1035-1046.
83. Lehner, M. D., Ittner, J. A., Bundschuh, D. S., Van Rooijen, N., Wendel, A., Hartung, T. (2001) Improved innate immunity of endotoxin-tolerant mice increases resistance to Salmonella enterica Serovar typhimurium infection despite attenuated cytokine response. Infect. Immun. 69, 463-471.
84. Varma, T. K., Durham, M., Murphey, E. D., Cui, W., Huang, Z., Lin, C. Y., Toliver-Kinsky, T., Sherwood, E. R. (2005) Endotoxin priming improves clearance of Pseudomonas aeruginosa in wild-type and interleukin-10 knockout mice. Infect. Immun. 73, 7340-7347.
85. Ruggiero, G., Andreana, A., Utili, R., Galante, D. (1980) Enhanced phagocytosis and bactericidal activity of hepatic reticuloendothelial system during endotoxin tolerance. Infect. Immun. 27, 798-803.
86. Moore, K. W., de Waal Malefyt, R., Coffman, R. L., O'Garra, A. (2001) Interleukin 10 and the interleukin 10 receptor. Annu. Rev. Immunol. 19, 683-765.
87. Berg, D. J., Kuhn, R., Rajewsky, K., Muller, W., Menon, S., Davidson, N., Grunig, G., Rennick, D. (1995) Interleukin 10 is a central regulator of the response to LPS in murine models of endotoxic shock and the Shwartzman reaction but not endotoxin tolerance. J. Clin. Invest. 96, 2339-2347.
88. Wysocka, M., Robertson, S., Riemann, H., Caamano, J., Hunter, C., Mackiewicz, A., Montaner, J., Trinchieri, G., Karp, C. L. (2001) IL-12 suppression during experimental endotoxin tolerance: dendritic cell loss and macrophage hyporesponsiveness. J. Immunol. 166, 7504-7513.