Acidosis drives damage-associated molecular pattern (DAMP)-induced interleukin-1 secretion via a caspase-1-independent pathway

Journal of Biological Chemistry

Volumn 288, Issue 42, 2013, Pages 30485-30494

  Edye, Michelle E ^a   Lopez Castejon, Gloria ^a   Allan, Stuart M ^a   Brough, David ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE-1; HOST RESPONSE; INTERLEUKIN-1; MOLECULAR PATTERNS; MULTIPLE PATHWAYS; PROINFLAMMATORY CYTOKINES;

BIOCHEMISTRY;

BIOLOGY;

CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LACTIC ACID; LIPOPOLYSACCHARIDE; PEPSTATIN;

ACIDOSIS; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; GLIA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ACIDOSIS; CASPASE; GLIA; INFLAMMATION; INNATE IMMUNITY; INTERLEUKIN; STROKE;

ACIDOSIS, LACTIC; ANIMALS; CARRIER PROTEINS; CASPASE 1; CATHEPSIN D; CELL LINE, TUMOR; HUMANS; HYDROGEN-ION CONCENTRATION; INFLAMMASOMES; INTERLEUKIN-1BETA; LACTIC ACID; LIPOPOLYSACCHARIDES; MICE; MICE, KNOCKOUT; NEUROGLIA; PEPSTATINS; PROTEASE INHIBITORS; SIGNAL TRANSDUCTION;

EID: 84886928516     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.478941     Document Type: Article

References (33)

1. Reardon, S. (2011) A world of chronic disease. Science 333, 558-559
2. Angell, S. Y., Danel, I., and DeCock, K. M. (2012) Global health. Global indicators and targets for noncommunicable diseases. Science 337, 1456-1457
3. Rock, K. L., Latz, E., Ontiveros, F., and Kono, H. (2010) The sterile inflammatory response. Annu. Rev. Immunol. 28, 321-342
4. Dinarello, C. A. (2010) Anti-inflammatory agents: present and future. Cell 140, 935-950
5. Dinarello, C. A. (2011) Blocking interleukin-1 in acute and chronic autoinflammatory diseases. J. Int. Med. 269, 16-28
6. Allan, S. M., Tyrrell, P. J., and Rothwell, N. J. (2005) Interleukin-1 and neuronal injury. Nat. Rev. Immunol. 5, 629-640
7. Luheshi, N. M., Rothwell, N. J., and Brough, D. (2009) Dual functionality of interleukin-1 family cytokines: implications for anti-interleukin-1 therapy. Br. J. Pharmacol. 157, 1318-1329
8. Strowig, T., Henao-Mejia, J., Elinav, E., and Flavell, R. (2012) Inflammasomes in health and disease. Nature 481, 278-286
9. Schroder, K., and Tschopp, J. (2010) The inflammasomes. Cell 140, 821-832
10. Chen, G. Y., and Nuñez, G. (2010) Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 10, 826-837
11. Iyer, S. S., Pulskens, W. P., Sadler, J. J., Butter, L. M., Teske, G. J., Ulland, T. K., Eisenbarth, S. C., Florquin, S., Flavell, R. A., Leemans, J. C., and Sutterwala, F. S. (2009) Necrotic cells trigger a sterile inflammatory response through the Nlrp3 inflammasome. Proc. Natl. Acad. Sci. U.S.A. 106, 20388-20393
12. Nemoto, E. M., and Frinak, S. (1981) Brain tissue pH after global brain ischemia and barbiturate loading in rats. Stroke 12, 77-82
13. Takenouchi, T., Iwamaru, Y., Sugama, S., Tsukimoto, M., Fujita, M., Sekigawa, A., Sekiyama, K., Sato, M., Kojima, S., Conti, B., Hashimoto, M., and Kitani, H. (2011) The activation of P2X7 receptor induces cathepsin D-dependent production of a 20-kDa form of IL-1β under acidic extracellular pH in LPS-primed microglial cells. J. Neurochem. 117, 712-723
14. Fantuzzi, G., Ku, G., Harding, M. W., Livingston, D. J., Sipe, J. D., Kuida, K., Flavell, R. A., and Dinarello, C. A. (1997) Response to local inflammation of IL-1β-converting enzyme- deficient mice. J. Immunol. 158, 1818-1824
15. Stehlik, C. (2009) Multiple interleukin-1βa-converting enzymes contribute to inflammatory arthritis. Arthritis Rheum. 60, 3524-3530
16. Joosten, L. A., Netea, M. G., Fantuzzi, G., Koenders, M. I., Helsen, M. M., Sparrer, H., Pham, C. T., van der Meer, J. W., Dinarello, C. A., and van den Berg, W. B. (2009) Inflammatory arthritis in caspase 1 gene-deficient mice: contribution of proteinase 3 to caspase 1-independent production of bioactive interleukin-1β. Arthritis Rheum 60, 3651-3662
17. Rajamäki, K., Nordström, T., Nurmi, K., Åkerman, K. E., Kovanen, P. T., Öörni, K., and Eklund, K. K. (2013) Extracellular acidosis is a novel danger signal alerting innate immunity via the NLRP3 inflammasome. J. Biol. Chem. 288, 13410-13419
18. Savage, C. D., Lopez-Castejon, G., Denes, A., and Brough, D. (2012) NLRP3-inflammasome activating DAMPs stimulate an inflammatory response in glia in the absence of priming which contributes to brain inflammation after injury. Front. Immunol. 3, 288
19. Sun, P. Z., Cheung, J. S., Wang, E., and Lo, E. H. (2011) Association between pH-weighted endogenous amide proton chemical exchange saturation transfer MRI and tissue lactic acidosis during acute ischemic stroke. J. Cereb. Blood Flow Metab. 31, 1743-1750
20. Luheshi, N. M., Kovács, K. J., Lopez-Castejon, G., Brough, D., and Denes, A. (2011) Interleukin-1 expression precedes IL-1 after ischemic brain injury and is localised to areas of focal neuronal loss and penumbral tissues. J. Neuroinflammation 8, 186
21. Greenhalgh, A. D., Brough, D., Robinson, E. M., Girard, S., Rothwell, N. J., and Allan, S. M. (2012) Interleukin-1 receptor antagonist is beneficial after subarachnoid haemorrhage in rat by blocking haem-driven inflammatory pathology. Dis. Model. Mech. 5, 823-833
22. Mariathasan, S., Weiss, D. S., Newton, K., McBride, J., O'Rourke, K., Roose-Girma, M., Lee, W. P., Weinrauch, Y., Monack, D. M., and Dixit, V. M. (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440, 228-232
23. Martinon, F., Pétrilli, V., Mayor, A., Tardivel, A., and Tschopp, J. (2006) Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440, 237-241
24. Guerne, P. A., Terkeltaub, R., Zuraw, B., and Lotz, M. (1989) Inflammatory microcrystals stimulate interleukin-6 production and secretion by human monocytes and synoviocytes. Arthritis Rheum. 32, 1443-1452
25. Bouchard, L., de Médicis, R., Lussier, A., Naccache, P. H., and Poubelle, P. E. (2002) Inflammatory microcrystals alter the functional phenotype of human osteoblast-like cells in vitro: synergism with IL-1 to overexpress cyclooxygenase-2. J. Immunol. 168, 5310-5317
26. Emsley, H. C., Smith, C. J., Georgiou, R. F., Vail, A., Hopkins, S. J., Rothwell, N. J., and Tyrrell, P. J. (2005) A randomised phase II study of interleukin-1 receptor antagonist in acute stroke patients. J. Neurol. Neurosurg. Psychiatry 76, 1366-1372
27. Xiong, Z. G., Zhu, X. M., Chu, X. P., Minami, M., Hey, J., Wei, W. L., MacDonald, J. F., Wemmie, J. A., Price, M. P., Welsh, M. J., and Simon, R. P. (2004) Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 118, 687-698
28. Gao, J., Duan, B., Wang, D. G., Deng, X. H., Zhang, G. Y., Xu, L., and Xu, T. L. (2005) Coupling between NMDA receptor and acid-sensing ion channel contributes to ischemic neuronal death. Neuron 48, 635-646
29. Hazuda, D. J., Strickler, J., Simon, P., and Young, P. R. (1991) Structurefunction mapping of interleukin 1 precursors. Cleavage leads to a conformational change in the mature protein. J. Biol. Chem. 266, 7081-7086
30. Afonina, I. S., Tynan, G. A., Logue, S. E., Cullen, S. P., Bots, M., Lüthi, A. U., Reeves, E. P., McElvaney, N. G., Medema, J. P., Lavelle, E. C., and Martin, S. J. (2011) Granzyme B-dependent proteolysis acts as a switch to enhance the proinflammatory activity of IL-1β. Molecular cell 44, 265-278
31. Zheng, Y., Humphry, M., Maguire, J. J., Bennett, M. R., and Clarke, M. C. (2013) Intracellular interleukin-1 receptor 2 binding prevents cleavage and activity of interleukin-1β, controlling necrosis-induced sterile inflammation. Immunity 38, 285-295
32. Gross, O., Yazdi, A. S., Thomas, C. J., Masin, M., Heinz, L. X., Guarda, G., Quadroni, M., Drexler, S. K., and Tschopp, J. (2012) Inflammasome activators induce interleukin-1 secretion via distinct pathways with differential requirement for the protease function of caspase-1. Immunity 36, 388-400
33. Boutin, H., LeFeuvre, R. A., Horai, R., Asano, M., Iwakura, Y., and Rothwell, N. J. (2001) Role of IL-1α and IL-1β in ischemic brain damage. J. Neurosci. 21, 5528-5534