Potentiation of caspase-1 activation by the P2X7 receptor is dependent on TLR signals and requires NF-κB-driven protein synthesis

Journal of Immunology

Volumn 175, Issue 11, 2005, Pages 7611-7622

  Kahlenberg, J Michelle ^a   Lundberg, Kathleen C ^a   Kertesy, Sylvia B ^a   Qu, Yan ^a   Dubyak, George R ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BAY 117085; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CYCLOHEXIMIDE; CYTOKINE; GENE PRODUCT; I KAPPA B KINASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; ION CHANNEL; IONOPHORE; LIPOPOLYSACCHARIDE; NIGERICIN; POTASSIUM ION; PROTEASOME INHIBITOR; PURINE P2X7 RECEPTOR; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; GENE CONTROL; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS REGULATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION;

EID: 28244459680     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.11.7611     Document Type: Article

References (62)

1. Dinarello, C. A. 1996. Biologic basis for interleukin-1 in disease. Blood 87: 2095-2147.
2. Le Feuvre, R. A., D. Brough, Y. Iwakura, K. Takeda, and N. J. Rothwell. 2002. Priming of macrophages with lipopolysaccharide potentiates P2X7-mediated cell death via a caspase-1-dependent mechanism, independently of cytokine production. J. Biol. Chem. 277: 3210-3218.
3. Rowe, S. J., L. Allen, V. C. Ridger, P. G. Hellewell, and M. K. Whyte. 2002. Caspase-1-deficient mice have delayed neutrophil apoptosis and a prolonged inflammatory response to lipopolysaccharide-induced acute lung injury. J. Immunol. 169: 6401-6407.
4. Yamamoto, M., K. Yaginuma, H. Tsutsui, J. Sagara, X. Guan, E. Seki, K. Yasuda, S. Akira, K. Nakanishi, T. Noda, and S. Taniguchi. 2004. ASC is essential for LPS-induced activation of procaspase-1 independently of TLR-associated signal adaptor molecules. Genes Cells 9: 1055-1067.
5. Mariathasan, S., K. Newton, D. M. Monack, D. Vucic, D. M. French, W. P. Lee, M. Roose-Girma, S. Erickson, and V. M. Dixit. 2004. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430: 213-218.
6. Martinon, F., K. Burns, and J. Tschopp. 2002. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-β. Mol. Cell 10: 417-426.
7. Poyet, J.-L., S. M. Srinivasula, M. Tnani, M. Razmara, T. Fernandes-Alnemri, and E. S. Alnemri. 2001. Identification of Ipaf, a human caspase-1-activating protein related to Apaf-1. J. Biol. Chem. 276: 28309-28313.
8. Srinivasula, S. M., J.-L. Poyet, M. Razmara, P. Datta, Z. Zhang, and E. S. Alnemri. 2002. The PYRIN-CARD protein ASC is an activating adaptor for caspase-1. J. Biol. Chem. 277: 21119-21122.
9. Stehlik, C., S. H. Lee, A. Dorfleutner, A. Stassinopoulos, J. Sagara, and J. C. Reed. 2003. Apoptosis-associated speck-like protein containing a caspase recruitment domain is a regulator of procaspase-1 activation. J. Immunol. 171: 6154-6163.
10. Grenier, J. M., L. Wang, G. A. Manji, W. J. Huang, A. Al-Garawi, R. Kelly, A. Carlson, S. Merriam, J. M. Lora, M. Briskin, et al. 2002. Functional screening of five PYPAF family members identifies PYPAF5 as a novel regulator of NF-κB and caspase-1. FEBS Lett. 530: 73-78.
11. Agostini, L., F. Martinon, K. Burns, M. F. McDermott, P. N. Hawkins, and J. Tschopp. 2004. NALP3 forms an IL-1β-processing inflammasome with increased activity in Muckle-wells autoinflammatory disorder. Immunity 20: 319-325.
12. Yamin, T. T., J. M. Ayala, and D. K. Miller. 1996. Activation of the native 45-kDa precursor form of interleukin-1-converting enzyme. J. Biol. Chem. 271: 13273-13282.
13. Perregaux, D., and C. A. Gabel. 1994. Interleukin-1β maturation and release in response to ATP and nigericin: evidence that potassium depletion mediated by these agents is a necessary and common feature of their activity. J. Biol. Chem. 269: 15195-15203.
14. Perregaux, D. G., R. E. Laliberte, and C. A. Gabel. 1996. Human monocyte interleukin-1β posttranslational processing: evidence of a volume-regulated response. J. Biol. Chem. 271: 29830-29838.
15. Perregaux, D. G., and C. A. Gabel. 1998. Human monocyte stimulus-coupled IL-1β posttranslational processing: modulation via monovalent cations. Am. J. Physiol. 275: C1538-C1547.
16. Cheneval, D., P. Ramage, T. Kastelic, T. Szelestenyi, H. Niggli, R. Hemmig, M. Bachmann, and A. MacKenzie. 1998. Increased mature interleukin-1β (IL-1β) secretion from THP-1 cells induced by nigericin is a result of activation of p45 IL-1β-converting enzyme processing. J. Biol. Chem. 273: 17846-17851.
17. 7 nucleotide receptor in monocytes. macrophages, and HEK293 fibroblasts. Am. J. Physiol. 285: C286-C299.
18. Walev, I., K. Reske, M. Palmer, A. Valeva, and S. Bhakdi. 1995. Potassium-inhibited processing of IL-1β in human monocytes. EMBO J. 14: 1607-1614.
19. MacKenzie, A., H. L. Wilson, E. Kiss-Toth, S. K. Dower, R. A. North, and A. Surprenant. 2001. Rapid secretion of interleukin-1β by microvesicle shedding. Immunity 15: 825-835.
20. + release. Am. J. Physiol. 286: C1100-C1108.
21. Schumann, R. R., C. Belka, D. Reuter, N. Lamping, C. J. Kirschning, J. R. Weber, and D. Pfeil. 1998. Lipopolysaccharide activates caspase-1 (interleukin-1-converting enzyme) in cultured monocytic and endothelial cells. Blood 91: 577-584.
22. Grahames, C. B., A. D. Michel, I. P. Chessell, and P. P. Humphrey. 1999. Pharmacological characterization of ATP- and LPS-induced IL-1β release in human monocytes. Br. J. Pharmacol. 127: 1915-1921.
23. Perregaux, D. G., P. McNiff, R. Laliberte, M. Conklyn, and C. A. Gabel. 2000. ATP acts as an agonist to promote stimulus-induced secretion of TL-1β and IL-18 in human blood. J. Immunol. 165: 4615-4623.
24. Martinon, F., L. Agostini, E. Meylan, and J. Tschopp. 2004. Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome. Curr. Biol. 14: 1929-1934.
25. Martin, M. U., and H. Wesche. 2002. Summary and comparison of the signaling mechanisms of the Toll/interleukin-1 receptor family. Biochim. Biophys. Acta 1592: 265-280.
26. Humphreys, B. D., J. Rice, S. B. Kertesy, and G. R. Dubyak. 2000. Stress-activated protein kinase/JNK activation and apoptotic induction by the macrophage P2X7 nucleotide receptor. J. Biol. Chem. 275: 26792-26798.
27. Pai, R. K., M. E. Pennini, A. A. Tobian, D. H. Canaday, W. H. Boom, and C. V. Harding. 2004. Prolonged Toll-like receptor signaling by Mycobacterium tuberculosis and its 19-kilodalton lipoprotein inhibits γ interferon-induced regulation of selected genes in macrophages. Infect. Immun. 12: 6603-6614.
28. Laliberte, R. E., J. Eggler, and C. A. Gabel. 1999. ATP treatment of human monocytes promotes caspase-1 maturation and externalization. J. Biol. Chem. 274: 36944-36951.
29. Perregaux, D., J. Barberia, A. J. Lanzetti, K. F. Geoghegan, T. J. Carty, and C. A. Gabel. 1992. IL-1β maturation: evidence that mature cytokine formation can be induced specifically by nigerian. J. Immunol. 149: 1294-1303.
30. Noss, E. H., R. K. Pai, T. J. Sellati, J. D. Radolf, J. Belisle, D. T. Golenbock, W. H. Boom, and C. V. Harding. 2001. Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J. Immunol. 167: 910-918.
31. Gould, M. P., J. A. Greene, V. Bhoj, J. L. DeVecchio, and F. P. Heinzel. 2004. Distinct modulatory effects of LPS and CpG on IL-18-dependent IFN-γ synthesis. J. Immunol. 172: 1754-1762.
32. Suzuki, N., S. Suzuki, and W. C. Yeh. 2002. IRAK-4 as the central TIR signaling mediator in innate immunity. Trends Immunol. 23: 503-506.
33. Guha, M., and N. Mackman. 2002. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J. Biol. Chem. 277: 32124-32132.
34. lck, MAP kinases, and transcription factors AP-1 and NF-κB. J. Biol. Chem. 278: 1549-1560.
35. 7R)-induced pore formation in human THP-1 cells. J. Pharmacol. Exp. Ther. 308: 1053-1061.
36. 7 receptor-mediated ERK1/2 phosphorylation in human astrocytoma cells. Am. J. Physiol. 284: C571-C581.
37. 7 receptors stimulate AKT phosphorylation in astrocytes. Br. J. Pharmacol. 141: 1106-1117.
38. Mehta, V. B., J. Hart, and M. D. Wewers. 2001. ATP-stimulated release of interleukin (IL)-1β and IL-18 requires priming by lipopolysaccharide and is independent of caspase-1 cleavage. J. Biol. Chem. 276: 3820-3826.
39. Beigi, R. D., and G. R. Dubyak. 2000. Endotoxin activation of macrophages does not induce ATP release and autocrine stimulation of P2 nucleotide receptors. J. Immunol. 165: 7189-7198.
40. Hentze, H., X. Y. Lin, M. S. Choi, and A. G. Porter. 2003. Critical role for cathepsin B in mediating caspase-1-dependent interleukin-18 maturation and caspase-1-independent necrosis triggered by the microbial toxin nigerian. Cell Death Differ. 10: 956-968.
41. Kahlenberg, J. M., and G. R. Dubyak. 2004. Differing caspase-1 activation states in monocyte versus macrophage models of IL-1β processing and release. J. Leukocyte Biol. 76: 676-684.
42. Silverman, N., and T. Maniatis. 2001. NF-κB signaling pathways in mammalian and insect innate immunity. Genes Dev. 15: 2321-2342.
43. 12,14-prostaglandin J2 inhibits Bay 11-7085-induced sustained extracellular signal-regulated kinase phosphorylation and apoptosis in human articular chondrocytes and synovial fibroblasts. J. Biol. Chem. 279: 22399-22403.
44. Horák, S. 2003. The role of ubiquitin in down-regulation and intracellular sorting of membrane proteins: insights from yeast. Biochim. Biophys. Acta 1614: 139-155.
45. Lee, J. Y., J. Ye, Z. Gao, H. S. Youn, W. H. Lee, L. Zhao, N. Sizemore, and D. H. Hwang. 2003. Reciprocal modulation of Toll-like receptor-4 signaling pathways involving MyD88 and phosphatidylinositol 3-kinase/AKT by saturated and polyunsaturated fatty acids. J. Biol. Chem. 278: 37041-37051.
46. Argast, G. M., N. Fausto, and J. S. Campbell. 2005. Inhibition of RIP2/RIck/ CARDIAK activity by pyridinyl imidazole inhibitors of p38 MAPK. Mol. Cell Biochem. 268: 129-140.
47. Kobayashi, K., N. Inohara, L. D. Hernandez, J. E. Galan, G. Nunez, C. A. Janeway, R. Medzhitov, and R. A. Flavell. 2002. RICK/Rip2/CARDIAK mediates signalling for receptors of the innate and adaptive immune systems. Nature 416: 194-199.
48. Chae, J. J., H. D. Komarow, J. Cheng, G. Wood, N. Raben, P. P. Liu, and D. L. Kastner. 2003. Targeted disruption of pyrin, the FMF protein, causes heightened sensitivity to endotoxin and a defect in macrophage apoptosis. Mol. Cell 11: 591-604.
49. Shiohara, M., S. Taniguchi, J. Masumoto, K. Yasui, K. Koike, A. Komiyama, and J. Sagara. 2002. ASC, which is composed of a PYD and a CARD, is up-regulated by inflammation and apoptosis in human neutrophils. Biochem. Biophys. Res. Commun. 293: 1314-1318.
50. Dowds, T. A., J. Masumoto, F. F. Chen, Y. Ogura, N. Inohara, and G. Nunez. 2003. Regulation of cryopyrin/Pypaf1 signaling by pyrin, the familial Mediterranean fever gene product. Biochem. Biophys. Res. Commun. 302: 575-580.
51. Humke, E. W., S. K. Shriver, M. A. Starovasnik, W. J. Fairbrother, and V. M. Dixit. 2000. ICEBERG: a novel inhibitor of interleukin-1β generation. Cell 103: 99-111.
52. Lee, S. H., C. Stehlik, and J. C. Reed. 2001. COP, a caspase recruitment domain-containing protein and inhibitor of caspase-1 activation processing. J. Biol. Chem. 276: 34495-34500.
53. Razmara, M., S. M. Srinivasula, L. Wang, J.-L. Poyet, B. J. Geddes, P. S. DiStefano, J. Bertin, and E. S. Alnemri. 2002. CARD-8 protein, a new CARD family member that regulates caspase-1 activation and apoptosis. J. Biol. Chem. 277: 13952-13958.
54. Campos, S. P., Y. Wang, and H. Baumann. 1996. Insulin modulates STAT3 protein activation and gene transcription in hepatic cells. J. Biol. Chem. 271: 24418-24424.
55. Wang, S., M. Miura, Y. K. Jung, H. Zhu, E. Li, and J. Yuan. 1998. Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE. Cell 92: 501-509.
56. Lin, X. Y., M. S. Choi, and A. G. Porter. 2000. Expression analysis of the human caspase-1 subfamily reveals specific regulation of the CASP5 gene by lipopolysaccharide and interferon-γ. J. Biol. Chem. 275: 39920-39926.
57. Van de Craen, M., P. Vandenabeele, W. Declercq, I. Van den Brande, G. Van Loo, F. Molemans, P. Schotte, W. Van Criekinge, R. Beyaert, and W. Fiers. 1997. Characterization of seven murine caspase family members. FEBS Lett. 403: 61-69.
58. Schauvliege, R., J. Vanrobaeys, P. Schotte, and R. Beyaert. 2002. Caspase-11 gene expression in response to lipopolysaccharide and interferon-γ requires nuclear factor-κB and signal transducer and activator of transcription (STAT)1. J. Biol. Chem. 277: 41624-41630.
59. Kobori, M., Z. Yang, D. Gong, V. Heissmeyer, H. Zhu, Y. K. Jung, M. A. Gakidis, A. Rao, T. Sekine, F. Ikegami, et al. 2004. Wedelolactone suppresses LPS-induced caspase-11 expression by directly inhibiting the IKK complex. Cell Death Differ. 11: 123-130.
60. Hur, J., S. Y. Kim, H. Kim, S. Cha, M. S. Lee, and K. Suk. 2001. Induction of caspase-11 by inflammatory stimuli in rat astrocytes: lipopolysaccharide induction through p38 mitogen-activated protein kinase pathway. FEBS Lett. 507: 157-162.
61. O'Connor, W., Jr., J. A. Harton, X. Zhu, M. W. Linhoff, and J. P. Ting. 2003. Cutting edge: CIAS1/cryopyrin/PYPAF1/NALP3/CATERPILLER 1.1 is an inducible inflammatory mediator with NF-κB suppressive properties. J. Immunol. 171: 6329-6333.
62. Han, S.-J., H.-M. Ko, J.-H. Choi, K. H. Seo, H.-S. Lee, E.-K. Choi, I.-W. Choi, H.-K. Lee, and S.-Y. Im. 2002. Molecular mechanisms for lipopolysaccharide-induced biphasic activation of nuclear factor-κB (NF-κB). J. Biol. Chem. 277: 44715-44721.