Inflammasome Activators Induce Interleukin-1α Secretion via Distinct Pathways with Differential Requirement for the Protease Function of Caspase-1

Immunity

Volumn 36, Issue 3, 2012, Pages 388-400

  Groß, Olaf ^a,b   Yazdi, Amir S ^a,c   Thomas, Christina J ^a,b   Masin, Mark ^a   Heinz, Leonhard X ^a   Guarda, Greta ^a   Quadroni, Manfredo ^a   Drexler, Stefan K ^a   Tschopp, Jurg ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CATION CHANNEL; INFLAMMASOME; INTERLEUKIN 1; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM TRANSPORT; CELL DIVISION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVITY; ENZYME MECHANISM; MOUSE; NONHUMAN; PERITONITIS; PRIORITY JOURNAL; PROTEIN FUNCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS REGULATORY PROTEINS; CALCIUM CHANNELS; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; CASPASE 1; CELL DEATH; FEMALE; HUMANS; INFLAMMASOMES; INTERLEUKIN-1ALPHA; INTERLEUKIN-1BETA; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; NUCLEAR PROTEINS; PERITONITIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, INTERLEUKIN-1; SIGNAL TRANSDUCTION;

EID: 84858761335     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2012.01.018     Document Type: Article

References (45)

1. Beech D.J., Muraki K., Flemming R. Non-selective cationic channels of smooth muscle and the mammalian homologues of Drosophila TRP. J. Physiol. 2004, 559:685-706.
2. Carruth L.M., Demczuk S., Mizel S.B. Involvement of a calpain-like protease in the processing of the murine interleukin 1 alpha precursor. J. Biol. Chem. 1991, 266:12162-12167.
3. Chen C.J., Kono H., Golenbock D., Reed G., Akira S., Rock K.L. Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat. Med. 2007, 13:851-856.
4. Clapham D.E. TRP channels as cellular sensors. Nature 2003, 426:517-524.
5. Cox D., Tseng C.C., Bjekic G., Greenberg S. A requirement for phosphatidylinositol 3-kinase in pseudopod extension. J. Biol. Chem. 1999, 274:1240-1247.
6. Davidson H.W. Wortmannin causes mistargeting of procathepsin D. evidence for the involvement of a phosphatidylinositol 3-kinase in vesicular transport to lysosomes. J. Cell Biol. 1995, 130:797-805.
7. Di Paolo N.C., Miao E.A., Iwakura Y., Murali-Krishna K., Aderem A., Flavell R.A., Papayannopoulou T., Shayakhmetov D.M. Virus binding to a plasma membrane receptor triggers interleukin-1 alpha-mediated proinflammatory macrophage response in vivo. Immunity 2009, 31:110-121.
8. Dinarello C.A. Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 2009, 27:519-550.
9. Dostert C., Pétrilli V., Van Bruggen R., Steele C., Mossman B.T., Tschopp J. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 2008, 320:674-677.
10. Duewell P., Kono H., Rayner K.J., Sirois C.M., Vladimer G., Bauernfeind F.G., Abela G.S., Franchi L., Nuñez G., Schnurr M., et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 2010, 464:1357-1361.
11. Fernandes-Alnemri T., Wu J., Yu J.W., Datta P., Miller B., Jankowski W., Rosenberg S., Zhang J., Alnemri E.S. The pyroptosome: A supramolecular assembly of ASC dimers mediating inflammatory cell death via caspase-1 activation. Cell Death Differ. 2007, 14:1590-1604.
12. Franchi L., Kanneganti T.D., Dubyak G.R., Núñez G. Differential requirement of P2X7 receptor and intracellular K+ for caspase-1 activation induced by intracellular and extracellular bacteria. J. Biol. Chem. 2007, 282:18810-18818.
13. Fuhlbrigge R.C., Sheehan K.C., Schreiber R.D., Chaplin D.D., Unanue E.R. Monoclonal antibodies to murine IL-1 alpha. Production, characterization, and inhibition of membrane-associated IL-1 activity. J. Immunol. 1988, 141:2643-2650.
14. Gilbert R.J., Pothoulakis C., LaMont J.T., Yakubovich M. Clostridium difficile toxin B activates calcium influx required for actin disassembly during cytotoxicity. Am. J. Physiol. 1995, 268:G487-G495.
15. Gross O. Measuring the inflammasome. Methods Mol. Biol. 2012, 844:199-222.
16. Gross O., Poeck H., Bscheider M., Dostert C., Hannesschläger N., Endres S., Hartmann G., Tardivel A., Schweighoffer E., Tybulewicz V., et al. Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence. Nature 2009, 459:433-436.
17. Gross O., Thomas C.J., Guarda G., Tschopp J. The inflammasome: An integrated view. Immunol. Rev. 2011, 243:136-151.
18. Guarda G., Braun M., Staehli F., Tardivel A., Mattmann C., Förster I., Farlik M., Decker T., Du Pasquier R.A., Romero P., Tschopp J. Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 2011, 34:213-223.
19. Hornung V., Bauernfeind F., Halle A., Samstad E.O., Kono H., Rock K.L., Fitzgerald K.A., Latz E. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 2008, 9:847-856.
20. Howard A.D., Kostura M.J., Thornberry N., Ding G.J., Limjuco G., Weidner J., Salley J.P., Hogquist K.A., Chaplin D.D., Mumford R.A., et al. IL-1-converting enzyme requires aspartic acid residues for processing of the IL-1 beta precursor at two distinct sites and does not cleave 31-kDa IL-1 alpha. J. Immunol. 1991, 147:2964-2969.
21. Joosten L.A., Van De Veerdonk F.L., Vonk A.G., Boerman O.C., Keuter M., Fantuzzi G., Verschueren I., Van Der Poll T., Dinarello C.A., Kullberg B.J., et al. Differential susceptibility to lethal endotoxaemia in mice deficient in IL-1α, IL-1β or IL-1 receptor type I. APMIS 2010, 118:1000-1007.
22. Kamari Y., Shaish A., Shemesh S., Vax E., Grosskopf I., Dotan S., White M., Voronov E., Dinarello C.A., Apte R.N., Harats D. Reduced atherosclerosis and inflammatory cytokines in apolipoprotein-E-deficient mice lacking bone marrow-derived interleukin-1α. Biochem. Biophys. Res. Commun. 2011, 405:197-203.
23. Kavita U., Mizel S.B. Differential sensitivity of interleukin-1 alpha and -beta precursor proteins to cleavage by calpain, a calcium-dependent protease. J. Biol. Chem. 1995, 270:27758-27765.
24. Keller M., Rüegg A., Werner S., Beer H.D. Active caspase-1 is a regulator of unconventional protein secretion. Cell 2008, 132:818-831.
25. Kobayashi Y., Yamamoto K., Saido T., Kawasaki H., Oppenheim J.J., Matsushima K. Identification of calcium-activated neutral protease as a processing enzyme of human interleukin 1 alpha. Proc. Natl. Acad. Sci. USA 1990, 87:5548-5552.
26. Le Moal M.A., Stoeck M., Cavaillon J.M., MacDonald H.O., Truffa-Bachi P. A sensitive, IL-2-independent, assay for IL-1. J. Immunol. Methods 1988, 107:23-30.
27. Levine S., Saltzman A. Peritoneal toxicity of water: A model of chronic peritonitis caused by osmotic dysequilibrium in rats. J. Appl. Toxicol. 2001, 21:303-306.
28. Link T.M., Park U., Vonakis B.M., Raben D.M., Soloski M.J., Caterina M.J. TRPV2 has a pivotal role in macrophage particle binding and phagocytosis. Nat. Immunol. 2010, 11:232-239.
29. Mandrup-Poulsen T., Pickersgill L., Donath M.Y. Blockade of interleukin 1 in type 1 diabetes mellitus. Nat Rev Endocrinol 2010, 6:158-166.
30. Martinon F., Pétrilli V., Mayor A., Tardivel A., Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006, 440:237-241.
31. Monet M., Gkika D., Lehen'kyi V., Pourtier A., Vanden Abeele F., Bidaux G., Juvin V., Rassendren F., Humez S., Prevarsakaya N. Lysophospholipids stimulate prostate cancer cell migration via TRPV2 channel activation. Biochim. Biophys. Acta 2009, 1793:528-539.
32. Mosley B., Urdal D.L., Prickett K.S., Larsen A., Cosman D., Conlon P.J., Gillis S., Dower S.K. The interleukin-1 receptor binds the human interleukin-1 alpha precursor but not the interleukin-1 beta precursor. J. Biol. Chem. 1987, 262:2941-2944.
33. Ng J., Hirota S.A., Gross O., Li Y., Ulke-Lemee A., Potentier M.S., Schenck L.P., Vilaysane A., Seamone M.E., Feng H., et al. Clostridium difficile toxin-induced inflammation and intestinal injury are mediated by the inflammasome. Gastroenterology 2010, 139:542-552. 552, e1-e3.
34. Pétrilli V., Papin S., Dostert C., Mayor A., Martinon F., Tschopp J. Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ. 2007, 14:1583-1589.
35. Poyet J.L., Srinivasula S.M., Tnani M., Razmara M., Fernandes-Alnemri T., Alnemri E.S. Identification of Ipaf, a human caspase-1-activating protein related to Apaf-1. J. Biol. Chem. 2001, 276:28309-28313.
36. Schorn C., Frey B., Lauber K., Janko C., Strysio M., Keppeler H., Gaipl U.S., Voll R.E., Springer E., Munoz L.E., et al. Sodium overload and water influx activate the NALP3 inflammasome. J. Biol. Chem. 2011, 286:35-41.
37. Schroder K., Tschopp J. The inflammasomes. Cell 2010, 140:821-832.
38. Shao W., Yeretssian G., Doiron K., Hussain S.N., Saleh M. The caspase-1 digestome identifies the glycolysis pathway as a target during infection and septic shock. J. Biol. Chem. 2007, 282:36321-36329.
39. Sims J.E., Smith D.E. The IL-1 family: Regulators of immunity. Nat. Rev. Immunol. 2010, 10:89-102.
40. So A., De Meulemeester M., Pikhlak A., Yücel A.E., Richard D., Murphy V., Arulmani U., Sallstig P., Schlesinger N. Canakinumab for the treatment of acute flares in difficult-to-treat gouty arthritis: Results of a multicenter, phase II, dose-ranging study. Arthritis Rheum. 2010, 62:3064-3076.
41. Strange K., Emma F., Jackson P.S. Cellular and molecular physiology of volume-sensitive anion channels. Am. J. Physiol. 1996, 270:C711-C730.
42. Ting J.P., Willingham S.B., Bergstralh D.T. NLRs at the intersection of cell death and immunity. Nat. Rev. Immunol. 2008, 8:372-379.
43. Vonk A.G., Netea M.G., van Krieken J.H., Iwakura Y., van der Meer J.W., Kullberg B.J. Endogenous interleukin (IL)-1 alpha and IL-1 beta are crucial for host defense against disseminated candidiasis. J. Infect. Dis. 2006, 193:1419-1426.
44. Wewers M.D., Pope H.A., Miller D.K. Processing proIL-1 beta decreases detection by a proIL-1 beta specific ELISA but increases detection by a conventional ELISA. J. Immunol. Methods 1993, 165:269-278.
45. Yazdi A.S., Guarda G., Riteau N., Drexler S.K., Tardivel A., Couillin I., Tschopp J. Nanoparticles activate the NLR pyrin domain containing 3 (Nlrp3) inflammasome and cause pulmonary inflammation through release of IL-1α and IL-1β. Proc. Natl. Acad. Sci. USA 2010, 107:19449-19454.