Caspase-1-dependent processing of pro-interlukin-1β is cytosolic and precedes cell death

Journal of Cell Science

Volumn 120, Issue 5, 2007, Pages 772-781

  Brough, David ^a   Rothwell, Nancy J ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Caspase 1; Cathepsin D; Interlukin 1; Membrane fluidity; Pyroptosis

Indexed keywords

ADENOSINE TRIPHOSPHATE; CATHEPSIN D; CHOLESTEROL; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LACTATE DEHYDROGENASE; PURINE P2X7 RECEPTOR;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL MEMBRANE TRANSPORT; COW; CYTOSOL; MALE; MEMBRANE FLUIDITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN TRANSPORT;

ADENOSINE TRIPHOSPHATE; ANIMALS; CASPASE 1; CELL DEATH; CELL LINE; CELLS, CULTURED; CYTOSOL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-1BETA; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, PURINERGIC P2; TIME FACTORS;

EID: 34047179487     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03377     Document Type: Article

References (53)

1. Allan, S. M. and Rothwell, N. J. (2003). Inflammation in central nervous system injury. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 1669-1677.
2. Andrei, C., Dazzi, C., Lotti, L., Torrisi, M. R., Chimini, G. and Rubartelli, A. (1999). The secretory route of the leaderless protein interleukin 1beta involves exocytosis of endolysosome-related vesicles. Mol. Biol. Cell 10, 1463-1475.
3. Andrei, C., Margiocco, P., Poggi, A., Lotti, L. V., Torrisi, M. R. and Rubartelli, A. (2004). Phospholipases C and A2 control lysosome-mediated IL-1 beta secretion: Implications for inflammatory processes. Proc. Natl. Acad. Sci. USA 101, 9745-9750.
4. Baetz, K., Isaaz, S. and Griffiths, G. M. (1995). Loss of cytotoxic T lymphocyte function in Chediak-Higashi syndrome arises from a secretory defect that prevents lytic granule exocytosis. J. Immunol. 154, 6122-6131.
5. Brennan, M. A. and Cookson, B. T. (2000). Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol. Microbiol. 38, 31-40.
6. Brough, D., Le Feuvre, R. A., Iwakura, Y. and Rothwell, N. J. (2002). Purinergic (P2X7) receptor activation of microglia induces cell death via an interleukin-1-independent mechanism. Mol. Cell. Neurosci. 19, 272-280.
7. Brought, D., Le Feuvre, R. A., Wheeler, R. D., Solovyova, N., Hilfiker, S., Rothwell, N. J. and Verkhratsky, A. (2003). Ca2+ stores and Ca2+ entry differentially contribute to the release of IL-1 beta and IL-1 alpha from murine macrophages. J. Immunol. 170, 3029-3036.
8. Charras, G. T., Yarrow, J. C., Horton, M. A., Mahadevan, L. and Mitchison, T. J. (2005). Non-equilibration of hydrostatic pressure in blebbing cells. Nature 435, 365-369.
9. Chauvet, N., Palin, K., Verrier, D., Poole, S., Dantzer, R. and Lestage, J. (2001). Rat microglial cells secrete predominantly the precursor of interleukin-1beta in response to lipopolysaccharide. Eur. J. Neurosci. 14, 609-617.
10. Coleman, M. L., Sahai, E. A., Yeo, M., Bosch, M., Dewar A. and Olson, M. F., (2001). Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat. Cell Biol. 3, 339-345.
11. Dinarello, C. A. (2005). Blocking IL-1 in systemic inflammation. J. Exp. Med. 201, 1355-1359.
12. Ferrari, D., Chiozzi, P., Falzoni, S., Hanau, S. and Di Virgilio, F. (1997). Purinergic modulation of interleukin-1 beta release from microglial cells stimulated with bacterial endotoxin. J. Exp. Med. 185, 579-582.
13. Fink, S. L. and Cookson, B. T. (2005). Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect. Immun. 73, 1907-1916.
14. Franchi, L., Amer, A., Body-Malapel, M., Kanneganti, T. D., Ozoren, N., Jagirdar, R., Inohara, N., Vandenabeele, P., Bertin, J., Coyle, A. et al. (2006). Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat. Immunol. 7, 576-582.
15. Griffin, B. A., Adams, S. R. and Tsien, R. Y. (1998). Specific covalent labeling of recombinant protein molecules inside live cells. Science 281, 269-272.
16. Gudipaty, L., Munetz, J., Verhoef, P. A. and Dubyak, G. R. (2003). Essential role for Ca2+ in regulation of IL-1beta secretion by P2X7 nucleotide receptor in monocytes, macrophages, and HEK-293 cells. Am. J. Physiol. Cell Physiol. 285, C286-C299.
17. Hamon, Y., Luciani, M. F., Becq, F., Verrier, B., Rubartelli, A. and Chimini, G. (1997). Interleukin-1beta secretion is impaired by inhibitors of the Atp binding cassette transporter, ABC1. Blood 90, 2911-2915.
18. Hersh, D., Monack, D. M., Smith, M. R., Ghori, N., Falkow, S. and Zychlinsky, A. (1999). The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc. Natl. Acad. Sci. USA 96, 2396-2401.
19. Hilbi, H., Chen, Y., Thirumalai, K. and Zychlinsky, A. (1997). The interleukin 1beta-converting enzyme, caspase 1, is activated during Shigella flexneri-induced apoptosis in human monocyte-derived macrophages. Infect. Immun. 65, 5165-5170.
20. Hogquist, K. A., Unanue, E. R. and Chaplin, D. D. (1991). Release of IL-1 from mononuclear phagocytes. J. Immunol. 147, 2181-2186.
21. Huynh, C., Roth, D., Ward, D. M., Kaplan, J. and Andrews, N. W. (2004). Defective lysosomal exocytosis and plasma membrane repair in Chediak-Higashi/beige cells. Proc. Natl. Acad. Sci. USA 101, 16795-16800.
22. Johnston, J. B., Barrett, J. W., Nazarian, S. H., Goodwin, M., Ricuttio, D., Wang, G. and McFadden, G. (2005). A poxvirus-encoded pyrin domain protein interacts with ASC-1 to inhibit host inflammatory and apoptotic responses to infection. Immunity 23, 587-598.
23. Kay, J. G., Murray, R. Z., Pagan, J. K. and Stow, J. L. (2006). Cytokine secretion via cholesterol-rich lipid raft-associated SNAREs at the phagocytic cup. J. Biol. Chem. 281, 11949-11954.
24. Lara-Tejero, M., Sutterwala, E. S., Ogura, Y., Grant, E. P., Berlin, J., Coyle, A. J., Flavell, R. A. and Galan, J. E. (2006). Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J. Exp. Med. 203, 1407-1412.
25. Le Feuvre, R. A., Brough, D., Iwakura, Y., Takeda, K. and Rothwell, N. J. (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.
26. Lenne, P. F., Wawrezinieck, L., Conchonaud, F., Wurtz, O., Boned, A., Guo, X. J., Rigneault, H., He, H. T. and Marguet, D. (2006). Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J. 25, 3245-3256.
27. Lorenz, H., Hailey, D. W. and Lippincott-Schwartz, J. (2006). Fluorescence protease protection of GFP chimeras to reveal protein topology and subcellular localization. Nat. Methods 3, 205-210.
28. MacKenzie, A., Wilson, H. L., Kiss-Toth, E., Dower, S. K., North, R. A. and Surprenant, A. (2001). Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity 15, 825-835.
29. Mandinova, A., Soldi, R., Graziani, I., Bagala, C., Bellum, S., Landriscina, M., Tarantini, F., Prudovsky, I. and Maciag, T. (2003). S100A13 mediates the copper-dependent stress-induced release of IL-1alpha from both human U937 and murine NIH 3T3 cells. J. Cell Sci. 116, 2687-2696.
30. 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.
31. Martinon, F., Burns, K. and Tschopp, J. (2002). The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol. Cell 10, 417-426.
32. Martinon, F., Agostini, L., Meylan, E. and Tschopp, J. (2004). Identification of bacterial muramyl dipeptide as activator of the NALP3/ cryopyrin inflammasome. Curr. Biol. 14, 1929-1934.
33. Masumoto, J., Taniguchi, S. and Sagara, J. (2001). Pyrin N-terminal homology domain- and caspase recruitment domain-dependent oligomerization of ASC. Biochem. Biophys. Res. Commun. 280, 652-655.
34. Matsushima, K., Taguchi, M., Kovacs, E. J., Young, H. A. and Oppenheim, J. J. (1986). Intracellular localization of human monocyte associated interleukin 1 (IL 1) activity and release of biologically active IL 1 from monocytes by trypsin and plasmin. J. Immunol. 136, 2883-2891.
35. Moriya, M., Taniguchi S., Wu P., Liepinsh, E., Otting, G. and Sagara, J. (2005). Role of charged and hydrophobic residues in the oligomerization of the PYRIN domain of ASC. Biochemistry 44, 575-583.
36. Munro, S. (2003). Lipid rafts: elusive or illusive? Cell 115, 377-388.
37. Nickel, W. (2005). Unconventional secretory routes: direct protein export across the plasma membrane of mammalian cells. Traffic 6, 607-614.
38. Nusbaum, P., Laine, C., Seveau, S., Lesavre, P. and Halbwachs-Mecarelli, L. (2004). Early membrane events in polymorphonuclear cell (PMN) apoptosis: membrane blebbing and vesicle release, CD43 and CD16 down-regulation and phosphatidylserine externalization. Biochem. Soc. Trans. 32, 477-479.
39. Perregaux, D., and Gabel, C. A. (1994). Interleukin-1 beta 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.
40. Perregaux, D. G., Laliberte, R. E. and Gabel, C. A. (1996). Human monocyte interleukin-1beta posttranslational processing. Evidence of a volume-regulated response. J. Biol. Chem. 271, 29830-29838.
41. Raupach, B., Peuschel, S. K., Monack, D. M. and Zychlinsky, A. (2006). Caspase-1-mediated activation of interleukin-1beta (IL-1beta) and IL-18 contributes to innate immune defenses against Salmonella enterica serovar Typhimurium infection. Infect. Immun. 74, 4922-4926.
42. Rubartelli, A., Cozzolino, F., Talio, M. and Sitia, R. (1990). A novel secretory pathway for interleukin-1 beta, a protein lacking a signal sequence. EMBO J. 9, 1503-1510.
43. Schroeder, G. N. and Hilbi, H. (2007). Cholesterol is required to trigger caspase-1 activation and macrophage apoptosis after phagosomal escape of Shigella. Cell. Microbiol. 9, 265-278.
44. Shikama, Y., Mami, U., Miyashita, T. and Yamada, M. (2001). Comprehensive studies on subcellular localizations and cell death-inducing activities of eight GFP-tagged apoptosis-related caspases. Exp. Cell Res. 264, 315-325.
45. Singer, I. I., Scott, S., Chin, J., Bayne, E. K., Limjuco, G., Weidner, J., Miller, D. K., Chapman, K. and Kostura, M. J. (1995). The interleukin-1 beta-converting enzyme (ICE) is localized on the external cell surface membranes and in the cytoplasmic ground substance of human monocytes by immuno-electron microscopy. J. Exp. Med. 182, 1447-1459.
46. Solle, M., Labasi, J., Perregaux, D. G., Stam, E., Petrushova, N., Koller, B. H., Griffiths, R. J. and Gabel, C. A. (2001). Altered cytokine production in mice lacking P2X(7) receptors. J. Biol. Chem. 276, 125-132.
47. Srinivasula, S. M., Poyet, J. L., Razimara, M., Datta, P., Zhang, Z. and Alnemri, E. S. (2002). The PYRIN-CARD protein ASC is an activating adaptor for caspase-1. J. Biol. Chem. 277, 21119-21122.
48. Sutterwala, F. S., Ogura, Y., Szczepanik, M., Lara-Tejero, M., Lichtenberger, G. S., Grant, E. P., Bertin, J., Coyle, A. J., Galan, J. E., Askenase, P. W. et al. (2006). Critical role for NALP3/CIAS1/ Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24, 317-327.
49. Tchernev, V. T., Mansfield, T. A., Giot, L., Kumar, A. M., Nandabalan, K., Li, Y., Mishra, V. S., Detter, J. C., Rothberg, J. M., Wallace, M. R. et al. (2002). The Chediak-Higashi protein interacts with SNARE complex and signal transduction proteins. Mol. Med. 8, 56-64.
50. Thirumalai, K., Kim, K. S. and Zychlinsky, A. (1997). IpaB, a Shigella flexneri invasin, colocalizes with interleukin-1 beta-converting enzyme in the cytoplasm of macrophages. Infect. Immun. 65, 787-793.
51. Thornberry, N. A., Bull, H. G., Calaycay, J. R., Chapman, K. T., Howard, A. D., Kostura, M. J., Miller, D. K., Molineaux, S. M., Weidner, J. R., Attains, J. et al. (1992). A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356, 768-774.
52. Verhoef, P. A., Estacion, M., Schilling, W. and Dubyak, G. R. (2003). P2X7 receptor-dependent blebbing and the activation of Rbo-effector kinases, caspases, and IL-1 beta release. J. Immunol. 170, 5728-5738.
53. Yu, J. W., Wu, J., Zhang, Z., Datta, P., Ibrahimi, I., Taniguchi, S., Sagara, J., Fernandes-Alnemri, T. and Alnemri E. S. (2006). Cryopyrin and pyrin activate caspase-1, but not NF-kappaB, via ASC oligomerization. Cell Death Differ 13, 236-249.