Inhibition of a p38/stress-activated protein kinase-2-dependent phosphatase restores function of IL-1 receptor-associated kinase-1 and reverses Toll-like receptor 2- and 4-dependent tolerance of macrophages

Journal of Immunology

Volumn 171, Issue 3, 2003, Pages 1456-1465

  Ropert, Catherine ^a,b   Closel, Meire ^a   Chaves, Andréa C L ^a   Gazzinelli, Ricardo T ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CYTOKINE; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 12; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE; OKADAIC ACID; PHOSPHATASE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL LYSATE; CROSS TOLERANCE; ENZYME ACTIVATION; ENZYME ASSAY; ENZYME INHIBITION; GENE EXPRESSION; GENETIC TRANSCRIPTION; IMMUNOBLOTTING; IMMUNOLOGICAL TOLERANCE; IMMUNOPRECIPITATION; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERITONEUM MACROPHAGE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRYPANOSOMA CRUZI; TRYPANOSOMIASIS; TRYPOMASTIGOTE;

EID: 0042346123     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.3.1456     Document Type: Article

References (64)

1. Medzhitov, R., and C. A. Janeway, Jr. 1997. Innate immunity: the virtues of a nonclonal system of recognition. Cell 91:295.
2. McKnight, A. J., and S. Gordon. 2000. Innate recognition systems in host defense. Microbes Infect. 3:239.
3. Lemaitre, B., E. Nicolas, L. Michaut, J. M. Reichhart, and J. A. Hoffmann. 1996. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86:973.
4. Lemaitre, B., J. M. Reichhart, and J. A. Hoffmann. 1997. Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc. Natl. Acad. Sci. USA 94:14614.
5. Medzhitov, R., P. Preston-Hurlburt, and C. A. Janeway Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394.
6. Aderem, A., and R. J. Ulevitch. 2000. Toll-like receptors in the induction of the innate immune response. Nature 406:782.
7. Medzhitov, R. 2001. Toll-Like receptors and innate immunity. Nat. Rev. Immunol. 1:135.
8. Kawai, T., O. Adachi, T. Ogawa, K. Takeda, and S. Akira. 1999. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11:115.
9. Seki, E., H. Tsutsui, N. M. Tsuji, N. Hayashi, K. Adachi, H. Nakano, S. Futatsugi-Yumikura, O. Takeuchi, K. Hoshino, S. Akira, J. Fujimoto, and K. Nakanishi. 2002. Critical roles of myeloid differentiation factor 88-dependent proinflammatory cytokine release in early phase clearance of Listeria monocytogenes in mice. J. Immunol. 169:3863.
10. Zhang, G., and S. Ghosh. 2001. Toll-like receptor-mediated NF-κB activation: a phylogenetically conserved paradigm in innate immunity. J. Clin. Invest. 107:13.
11. West, M. A., and W. Heagy. 2002. Endotoxin tolerance: a review. Crit. Care Med. 30:S64.
12. Schwartz, D. A., C. L. Wohlford-Lenane, T. J. Quinn, and A. M. Krieg. 1999. Bacterial DNA or oligonucleotides containing unmethylated CpG motifs can minimize lipopolysaccharide-induced inflammation in the lower respiratory tract through an IL-12-dependent pathway. J. Immunol. 163:224.
13. 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 Staphyloccous aureus in human monocytes. Immunology 92:396.
14. Sato, S., F. Nomura, T. Kawai, O. Takeuchi, P. F. Muhlradt, 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.
15. 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.
16. Campos, M. A., I. C. Almeida, O. Takeuchi, S. Akira, E. P. Valente, D. O. Procópio, L. R. Travassos, J. A. Smith, D. T. Golenbock, and R. T. Gazzinelli. 2001. Activation of Toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite. J. Immunol. 167:416.
17. Ropert, C., L. R. Ferreira, M. A. Campos, D. O. Procópio, L. R. Travassos, M. A. Ferguson, L. F. Reis, M. M. Teixeira, I. C. Almeida, and R. T. Gazzinelli. 2002. Macrophage signaling by glycosylphosphatidylinositol-anchored mucin-like glycoproteins derived from Trypanosoma cruzi trypomastigotes. Microbes Infect. 4:1015.
18. Ropert, C., I. C. Almeida, M. Closel, L. R. Travassos, M. A. Ferguson, P. Cohen. and R. T. Gazzinelli. 2001. Requirement of mitogen-activated protein kinases and IKB phosphorylation for induction of proinflammatory cytokine synthesis by macrophages indicates functional similarity of receptors triggered by glycosylphosphatidylinositol anchors from parasitic protozoa and bacterial lipopolysaccharide. J. Immunol. 166:3423.
19. Whalstrom, K., J. Bellingham, J. L. Rodriguez, and M. A. West. 1999. Inhibitory κB α control of nuclear factor-κB is dysregulated in endotoxin tolerant macrophages. Shock 11:242.
20. Kohler, N. G., and A. Joly. 1997. The involvement of a LPS inducible IKB kinase in endotoxin tolerance. Biochem. Biophys. Res. Commun. 232:602.
21. 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.
22. Medvedev, A. E., K. M. Kopydlowski, and S. N. Vogel. 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.
23. Wysocka, M., S. Robertson, H. Riemann, J. Caamano, C. Hunter, A. Mackiewicz, L. J. Montaner, G. Trinchieri, and C. L. Karp. 2001. IL-12 suppression during experimental endotoxin tolerance: dendritic cell loss and macrophage hyporesponsiveness. J. Immunol. 166:7504.
24. Ziegler-Heitbrock, H. W., A. Wedel, W. Schraut, M. Strobel, P. Wendelgass, T. Sternsdorf, P. A. Bauerle, J. G. Haas, G. Riethmuller. 1994. Tolerance to lipopolysaccharide involves mobilization of nuclear factor KB with predominance of p50 homodimers. J. Biol. Chem. 269:17001.
25. Tominaga, K., S. Saito, M. Matsuura, and M. Nakano. 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.
26. Shnyra, A., R. Brewington, A. Alipio, C. Amura, and D. C. Morrison. 1998. Reprogramming of lipopolysaccharide-primed macrophages is controlled by a counterbalanced production of IL-10 and IL-12. J. Immunol. 160:372.
27. Randow, F., U. Syrbe, C. Meisel, D. Krausch, H. Zuckermann, C. Platzer, and H. D. Volk. 1995. Mechanism of endotoxin desensitization: involvement of interleukin 10 and transforming growth factor β. J. Exp. Med. 181:1887.
28. Medvedev, A. E., P. Henneke, A. Schromm, E. Lien, R. Ingalls, M. J. Fenton, D. T. Golenbock, and S. N. Vogel. 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.
29. Kastenbauer, S., and H. W. L. Ziegler-Heitbrock. 1999. NF-κB I (p50) is upregulated in lipopolysaccharide tolerance and can block tumor necrosis factor gene expression. Infect. Immun. 67:1553.
30. Nomura, F., S. Akashi, Y. Sakao, S. Sato, T. Kawai, M. Matsumoto, K. Nakanishi, M. Kimoto, K. Miyake, K. Takeda, and S. Akira. 2000. Cutting edge: endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface Toll-like receptor 4 expression. J. Immunol. 164:3476.
31. Swantek, J. L., M. F. Tsen, M. H. Cobb, and J. A. Thomas. 2000. IL-1 receptor-associated kinase modulates host responsiveness to endotoxin. J. Immunol. 164:4301.
32. Medvedev, A. E., A. Lentschat, L. M. Whal, 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.
33. 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.
34. Mizel, S. B., and J. A. Snipes. 2002. Gram negative flagellin-induced self tolerance is associated with a block in interleukin-1 receptor-associated kinase release from Toll-like receptor 5. J. Biol. Chem. 277:22414.
35. Schade, F. U., R. Flash, S. Flohe, M. Majetschak, E. Kreuzfelder, E. Dominguez-Femandez, J. Borgermann, M. Reuter, and U. Obertacke. 1999. Endotoxin tolerance. In Endotoxin in Health and Disease. H. Brade, S. M. Opal, S. N. Vogel, and D. C. Morrison, eds. Dekker, New York, p. 50.
36. Cohen, P. 1997. The search for physiological substrates of MAP and SAP kinases in mammalian cells. Trends Cell Biol. 7:353.
37. Chang, L., and M. Karin. 2001. Mammalian MAP kinase signaling cascades. Nature 410:37.
38. Hunter, T. 1995. Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80:225.
39. Keyse, S. M. 2000. Protein phosphatases and the regulation of mitogen-activated protein kinase signalling. Curr. Opin. Cell Biol. 12:186.
40. Camps, M., A. Nichols, and S. Arkinstall. 2000. Dual specificity phosphatases: a gene family for control of MAP kinase function. FASEB J. 14:6.
41. Almeida. I. C., M. A. J. Ferguson, S. Schenkman, and L. R. Travassos. 1994. Lyric anti-α-galactosyl antibodies from patients with chronic Chagas' disease recognize novel O-linked oligosaccharides on mucin-like glycosyl-phosphatidylinositol-anchored glycoproteins of Trypanosoma cruzi. Biochem. J. 304:793.
42. Rouse, J., P. Cohen, S. Trigon, M. Morange, A. Alonso Llamazares, D. Zamanillo, T. Hunt, and A. R. Nebreda. 1994. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP-kinase-2. Cell 78:1027.
43. Furuya, T., L. Zhong, J. R. Meyer-Fernandes, H.-G. Lu, S. N. J. Moreno, and R. Docampo. 1998. Ecto-protein tyrosine phosphatase activity in Trypanosoma cruzi infective stages. Mol. Biochem. Parasitol. 92:339.
44. Bialojan, C., and A. Takai. 1988. Inhibitory effect of marine sponge toxin, okadaic acid on protein phosphatases. Biochem. J. 256:283.
45. Takai, A., and G. Mieskes. 1991. Inhibitory effect of okadaic acid on the pnitrophenyl phosphatase activity of protein phosphatases. Biochem. J. 275:233.
46. Zhang, X., and D. C. Morrisson. 1993. Lipopolysaccharide-induced selective priming effects on tumor necrosis factor-α and nitric oxide production in mouse peritoneal macrophages. J. Exp. Med. 177:511.
47. Seatter, S. C., T. Bennet, M. H. Li, M. P. Bubrick, and M. A. West. 1994. Macrophage endotoxin tolerance: tumor necrosis factor and interleukin-1 regulation by lipopolysaccharide pretreatment. Arch. Surg. 129:1263.
48. Mathison, J. C., G. D. Virca, E. Wolfson, P. S. Tobias, K. Glaser, and R. J. Ulevitch. 1990. Adaptation to bacterial lipopolysaccharide controls lipopolysaccharide-induced tumor necrosis factor production in rabbit macrophages. J. Clin. Invest. 85:1108.
49. Hirohashi, N., and D. C. Morrison. 1996. Low-dose lipopolysaccharide (LPS) pretreatment of mouse macrophages modulates LPS-dependent interleukin-6 production in vitro. Infect. Immun. 64:1011.
50. Seatter, S. C., L. Clair, T. Bennett, M. P. Bubrick, and M. A. West. 1995. Independent signal transduction pathways for IL-1 and TNF in LPS-tolerant macrophages. J. Surg. Res. 58:651.
51. Seatter, S. C., M. H. Li, M. P. Bubrick, and M. A. West. 1995. Endotoxin pretreatment of human monocytes alters subsequent endotoxin-triggered release of inflammatory mediators. Shock 3:252.
52. Means, T. K., B. W. Jones, A. B. Schromm, B. A. Shurtleff, J. A. Smith, J. Keane, D. T. Golenbock, S. N. Vogel, and M. J. Fenton. 2001. Differential effects of a Toll-like receptor antagonist on Mycobacterium tuberculosis-induced macrophage responses. J. Immunol. 166:4074.
53. Fernando, L. P., A. N. Fernando, M. Ferlito, P. V. Halushka, and J. A. Cook. 2000. Suppression of Cox-2 and TNF-α mRNA in endotoxin tolerance: effect of cycloheximide, actinomycin D, and okadaic acid. Shock 14:128.
54. Yoza, B. K., J. D. Wells, and C. E. McCall. 1998. Interleukin-1β expression after inhibition of protein phosphatases in endotoxin-tolerant cells. Clin. Diagn. Lab. Immunol. 5:281.
55. Favre, B., P. Turowski, and B. A. Hemmings. 1997. Differential inhibition and posttranslational modification of protein phosphatase 1 and 2A in MCF7 cells treated with calyculin-A, okadaic acid, and tautomycin. J. Biol. Chem. 272:13856.
56. Abraham, D., K. Podar, M. Pacher, M. Kubicek, N. Welzel, B. A. Hemmings, S. M. Dilworth, H. Mischak, W. Kolch, and M. Baccarini. 2000. Raf-1-associated protein phosphatase 2A as a posifive regulator of kinase activation. J. Biol. Chem. 275:22300.
57. Parameswaran, N., P. Nambi, C. S. Hall, D. P. Brooks, and W. S. Spielman. 2000. Adrenomedullin decreases extracellular signal-regulated kinase activity through an increase in protein phosphatase-2A activity in mesangial cells. Eur. J. Pharmacol. 388:133.
58. Zhou, B., Z. X. Wang, Y. Zhao, D. L. Brautigan, and Z. Y. Zhang. 2002. The specificity of extracellular signal-regulated kinase 2 dephosphorylation by protein phosphatases. J. Biol. Chem. 277:31818.
59. Xiao, Y. Q., K. Malcolm, G. S. Worthen, S. Gardai, W. P. Schiemann, V. A. Fadok, D. L. Bratton, and P. M. Henson. 2002. Cross-talk between ERK and p38 MAPK mediates selective suppression of pro-inflammatory cytokines by transforming growth factor-β. J. Biol. Chem. 277:14884.
60. Song, G. Y., C. S. Chung, I. H. Chaudry, and A. Ayala. 2001. MAPK p38 antagonism as a novel method of inhibiting lymphoid immune suppression in polymicrobial sepsis. Am. J. Physiol. Cell. Physiol. 281:C662.
61. Faas, M. M., H. Moes, J. W. Fijen, A. C. Muller Kobold, J. E. Tulleken, and J. G. Zijlstra. 2002. Monocyte intracellular cytokine production during human endotoxaemia with or without a second in vitro LPS challenge: effect of RWJ-67657, a p38 MAP-kinase inhibitor, on LPS-hyporesponsiveness. Clin. Exp. Immunol. 127:337.
62. Thomas, J. A., J. L. Allen, M. Tsen, T. Dubnicoff, J. Danao, X. C. Liao, Z. Cao, and S. A. Wasserman. 1999. Impaired cytokine signaling in mice lacking the IL-1 receptor-associated kinase. J. Immunol. 163:978.
63. Liu, H., P. Sidropoulos, G. Song, J. Pagliari, M. J. Birrer, B. Stein, J. Anrather, and R. M. Pope. 2000. TNF-α gene expression in macrophages: regulation by NF-κB is independent of c-Jun or C/EBPβ. J. Immunol. 164:4277.
64. Matsuguchi, T., T. Musikacharoen, T. R. Johnson, A. S. Kraft, and Y. Yoshikai. 2001. A novel mitogen-activated protein kinase phosphatase is an important negative regulator of lipopolysaccharide-mediated c-Jun N-terminal kinase activation in mouse macrophage cell lines. Mol. Cell. Biol. 21:6999.