Nonclassical IL-1β secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages

Journal of Immunology

Volumn 179, Issue 3, 2007, Pages 1913-1925

  Qu, Yan ^a   Franchi, Luigi ^b   Nunez, Gabriel ^b   Dubyak, George R ^a  

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

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PURINERGIC P2X7 RECEPTOR; ADENOSINE TRIPHOSPHATE; CATHEPSIN B; MULTIPROTEIN COMPLEX; PURINE P2 RECEPTOR; PURINE P2X7 RECEPTOR;

ANIMAL CELL; ARTICLE; BONE MARROW; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CYTOKINE RELEASE; ENDOSOME; ENZYME ACTIVATION; EXOCYTOSIS; EXOSOME; EXTRACELLULAR CALCIUM; KNOCKOUT MOUSE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; BIOLOGICAL MODEL; C57BL MOUSE; CELL CULTURE; COMPARATIVE STUDY; ENZYMOLOGY; GENETICS; IMMUNOLOGY; INFLAMMATION; LYSOSOME; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; SECRETION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CASPASE 1; CATHEPSIN B; CELLS, CULTURED; ENDOSOMES; ENZYME ACTIVATION; EXOCYTOSIS; INFLAMMATION; INTERLEUKIN-1BETA; LYSOSOMES; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, IMMUNOLOGICAL; MULTIPROTEIN COMPLEXES; RECEPTORS, PURINERGIC P2; SIGNAL TRANSDUCTION;

EID: 34548614009     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.3.1913     Document Type: Article

References (73)

1. Dinarello, C. A. 1996. Biologic basis for interleukin-1 in disease. Blood 87: 2095-2147.
2. Miller, D. K., J. M. Ayala, L. A. Egger, S. M. Raju, T. T. Yamin, G. J. Ding, E. P. Gaffney, A. D. Howard, O. C. Palyha, A. M. Rolando, et al. 1993. Purification and characterization of active human interleukin-1β-converting enzyme from THP.1 monocytic cells. J. Biol. Chem. 268: 18062-18069.
3. Li, P., H. Allen, S. Banerjee, S. Franklin, L. Herzog, C. Johnston, J. McDowell, M. Paskind, L. Rodman, J. Salfeld, et al. 1995. Mice deficient in IL-1β-converting enzyme are defective in production of mature IL-1β and resistant to endotoxic shock. Cell 80: 401-411.
4. 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.
5. Ogura, Y., F. S. Sutterwala, and R. A. Flavell. 2006. The inflammasome: first line of the immune response to cell stress. Cell 126: 659-662.
6. 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.
7. Tschopp, J., F. Martinon, and K. Burns. 2003. NALPs: a novel protein family involved in inflammation. Nat. Rev. Mol. Cell Biol. 4: 95-104.
8. Inohara, N., C. McDonald, and G. Nunez. 2005. NOD-LRR proteins: role in host-microbial interactions and inflammatory disease. Annu. Rev. Biochem. 74: 355-383.
9. 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.
10. 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.
11. Mariathasan, S., D. S. Weiss, K. Newton, J. McBride, K. O'Rourke, M. Roose-Girma, W. P. Lee, Y. Weinrauch, D. M. Monack, and V. M. Dixit. 2006. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440: 228-232.
12. Amer, A., L. Franchi, T. D. Kanneganti, M. Body-Malapel, N. Ozoren, G. Brady, S. Meshinchi, R. Jagirdar, A. Gewirtz, S. Akira, and G. Nunez. 2006. Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J. Biol. Chem. 281: 35217-35223.
13. Franchi, L., A. Amer, M. Body-Malapel, T. D. Kanneganti, N. Ozoren, R. Jagirdar, N. Inohara, P. Vandenabeele, J. Bertin, A. Coyle, et al. 2006. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1β in Salmonella-infected macrophages. Nat. Immunol. 7: 576-582.
14. Miao, E. A., C. M. Alpuche-Aranda, M. Dors, A. E. Clark, M. W. Bader, S. I. Miller, and A. Aderem. 2006. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1β via Ipaf. Nat. Immunol. 7: 569-575.
15. Kanneganti, T. D., N. Ozoren, M. Body-Malapel, A. Amer, J. H. Park, L. Franchi, J. Whitfield, W. Barchet, M. Colonna, P. Vandenabeele, et al. 2006. Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3. Nature 440: 233-236.
16. Kanneganti, T. D., M. Body-Malapel, A. Amer, J. H. Park, J. Whitfield, L. Franchi, Z. F. Taraporewala, D. Miller, J. T. Patton, N. Inohara, and G. Nunez. 2006. Critical role for cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA. J. Biol. Chem. 281: 36560-36568.
17. Martinon, F., V. Petrilli, A. Mayor, A. Tardivel, and J. Tschopp. 2006. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440: 237-241.
18. Sutterwala, F. S., Y. Ogura, M. Szczepanik, M. Lara-Tejero, G. S. Lichtenberger, E. P. Grant, J. Bertin, A. J. Coyle, J. E. Galan, P. W. Askenase, and R. A. Flavell. 2006. Critical role for NALP3/CIAS1/cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24: 317-327.
19. 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.
20. Ferrari, D., P. Chiozzi, S. Falzoni, M. Dal Susino, L. Melchiorri, O. R. Baricordi, and F. Di Virgilio. 1997. Extracellular ATP triggers IL-1β release by activating the purinergic P2Z receptor of human macrophages. J. Immunol. 159: 1451-1458.
21. 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.
22. Solle, M., J. Labasi, D. G. Perregaux, E. Stam, N. Petrushova, B. H. Koller, R. J. Griffiths, and C. A. Gabel. 2001. Altered cytokine production in mice lacking P2X(7) receptors. J. Biol. Chem. 276: 125-132.
23. 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 nigericin. J. Immunol. 149: 1294-1303.
24. 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.
25. 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.
26. Verhoef, P. A., S. B. Kertesy, M. Estacion, W. P. Schilling, and G. R. Dubyak. 2004. Maitotoxin induces biphasic interleukin-1β secretion and membrane blebbing in murine macrophages. Mol. Pharmacol. 66: 909-920.
27. Wewers, M. D. 2004. IL-1β: an endosomal exit. Proc. Natl. Acad. Sci. USA 101: 10241-10242.
28. Rubartelli, A., F. Cozzolino, M. Talio, and R. Sitia. 1990. A novel secretory pathway for interleukin-1β, a protein lacking a signal sequence. EMBO J. 9: 1503-1510.
29. Rubartelli, A., and R. Sitia. 1991. Interleukin 1β and thioredoxin are secreted through a novel pathway of secretion. Biochem. Soc. Trans. 19: 255-259.
30. Kahlenberg, J. M., K. C. Lundberg, S. B. Kertesy, Y. Qu, and G. R. Dubyak. 2005. Potentiation of caspase-1 activation by the P2X7 receptor is dependent on TLR signals and requires NF-κB-driven protein synthesis. J. Immunol. 175: 7611-7622.
31. 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.
32. Verhoef, P. A., S. B. Kertesy, K. Lundberg, J. M. Kahlenberg, and G. R. Dubyak. 2005. Inhibitory effects of chloride on the activation of caspase-1, IL-1β secretion, and cytolysis by the P2X7 receptor. J. Immunol. 175: 7623-7634.
33. Andrei, C., C. Dazzi, L. Lotti, M. R. Torrisi, G. Chimini, and A. Rubartelli. 1999. The secretory route of the leaderless protein interleukin 1β involves exocytosis of endolysosome-related vesicles. Mol. Biol. Cell 10: 1463-1475.
34. Andrei, C., P. Margiocco, A. Poggi, L. V. Lotti, M. R. Torrisi, and A. Rubartelli. 2004. Phospholipases C and A2 control lysosome-mediated IL-1β secretion: implications for inflammatory processes. Proc. Natl. Acad. Sci. USA 101: 9745-9750.
35. Carta, S., S. Tassi, C. Semino, G. Fossati, P. Mascagni, C. A. Dinarello, and A. Rubartelli. 2006. Histone deacetylase inhibitors prevent exocytosis of interleukin-1β-containing secretory lysosomes: role of microtubules. Blood 108: 1618-1626.
36. 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.
37. Bianco, F., E. Pravettoni, A. Colombo, U. Schenk, T. Moller, M. Matteoli, and C. Verderio. 2005. Astrocyte-derived ATP induces vesicle shedding and IL-1β release from microglia. J. Immunol. 174: 7268-7277.
38. Pizzirani, C., D. Ferrari, P. Chiozzi, E. Adinolfi, D. Sandona, E. Savaglio, and F. Di Virgilio. 2007. Stimulation of P2 receptors causes release of IL-1β-loaded microvesicles from human dendritic cells. Blood 109: 3856-3864.
39. Brough, D., and N. J. Rothwell. 2007. Caspase-1-dependent processing of pro-interleukin-1β is cytosolic and precedes cell death. J. Cell Sci. 120: 772-781.
40. Davies, J. Q., and S. Gordon. 2005. Isolation and culture of murine macrophages. Methods Mol. Biol. 290: 91-103.
41. 2+ in regulation of IL-1β secretion by P2X7 nucleotide receptor in monocytes, macrophages, and HEK-293 cells. Am. J. Physiol. 285: C286-C299.
42. Linebaugh, B. E., M. Sameni, N. A. Day, B. F. Sloane, and D. Keppler. 1999. Exocytosis of active cathepsin B enzyme activity at pH 7.0, inhibition and molecular mass. Eur. J. Biochem. 264: 100-109.
43. Verhoef, P. A., M. Estacion, W. Schilling, and G. R. Dubyak. 2003. P2X7 receptor-dependent blebbing and the activation of Rho-effector kinases, caspases, and IL-1β release. J. Immunol. 170: 5728-5738.
44. Andrews, N. W. 2000. Regulated secretion of conventional lysosomes. Trends Cell Biol. 10: 316-321.
45. 2+-regulated exocytic vesicles in fibroblasts and epithelial cells. J. Cell Biol. 137: 93-104.
46. 2+-regulated exocytosis of lysosomes. Cell 106: 157-169.
47. 2+ signaling in macrophages. J. Biol. Chem. 281: 35147-35155.
48. Da Cruz, C. M., A. L. Ventura, J. Schachter, H. M. Costa-Junior, H. A. da Silva Souza, F. R. Gomes, R. Coutinho-Silva, D. M. Ojcius, and P. M. Persechini. 2006. Activation of ERK1/2 by extracellular nucleotides in macrophages is mediated by multiple P2 receptors independently of P2X7-associated pore or channel formation. Br. J. Pharmacol. 147: 324-334.
49. Labasi, J. M., N. Petrushova, C. Donovan, S. McCurdy, P. Lira, M. M. Payette, W. Brissette, J. R. Wicks, L. Audoly, and C. A. Gabel. 2002. Absence of the P2X7 receptor alters leukocyte function and attenuates an inflammatory response. J. Immunol. 168: 6436-6445.
50. 2+ entry differentially contribute to the release of IL-1β and IL-1α from murine macrophages. J. Immunol. 170: 3029-3036.
51. + release. Am. J. Physiol. 286: C1100-C1108.
52. 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.
53. Pelegrin, P., and A. Surprenant. 2006. Pannexin-1 mediates large pore formation and interleukin-1β release by the ATP-gated P2X7 receptor. EMBO J. 25: 5071-5082.
54. Pelegrin, P., and A. Surprenant. 2007. Pannexin-1 couples to maitotoxin- and nigericin-induced interleukin-1β release through a dye uptake-independent pathway. J. Biol. Chem. 282: 2386-2394.
55. Walev, I., J. Klein, M. Husmann, A. Valeva, S. Strauch, H. Wirtz, O. Weichel, and S. Bhakdi. 2000. Potassium regulates IL-1β processing via calcium-independent phospholipase A2. J. Immunol. 164: 5120-5124.
56. Thery, C., L. Zitvogel, and S. Amigorena. 2002. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2: 569-579.
57. Fevrier, B., and G. Raposo. 2004. Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr. Opin. Cell Biol. 16: 415-421.
58. Hamon, Y., M. F. Luciani, F. Becq, B. Verrier, A. Rubartelli, and G. Chimini. 1997. Interleukin-1β secretion is impaired by inhibitors of the Atp binding cassette transporter, ABC1. Blood 90: 2911-2915.
59. Chessell, I. P., J. P. Hatcher, C. Bountra, A. D. Michel, J. P. Hughes, P. Green, J. Egerton, M. Murfin, J. Richardson, W. L. Peck, et al. 2005. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 114: 386-396.
60. Breese, N. M., A. C. George, L. E. Pauers, and C. L. Stucky. 2005. Peripheral inflammation selectively increases TRPV1 function in IB4-positive sensory neurons from adult mouse. Pain 115: 37-49.
61. Brack, A., H. L. Rittner, H. Machelska, K. Leder, S. A. Mousa, M. Schafer, and C. Stein. 2004. Control of inflammatory pain by chemokine-mediated recruitment of opioid-containing polymorphonuclear cells. Pain 112: 229-238.
62. Blott, E. J., and G. M. Griffiths. 2002. Secretory lysosomes. Nat. Rev. Mol. Cell Biol. 3: 122-131.
63. Quah, B. J., and H. C. O'Neill. 2005. The immunogenicity of dendritic cell-derived exosomes. Blood Cells Mol. Dis. 35: 94-110.
64. Van Niel, G., I. Porto-Carreiro, S. Simoes, and G. Raposo. 2006. Exosomes: a common pathway for a specialized function. J. Biochem. 140: 13-21.
65. Gurcel, L., L. Abrami, S. Girardin, J. Tschopp, and F. G. van der Goot. 2006. Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell 126: 1135-1145.
66. Mackenzie, A. B., M. T. Young, E. Adinolfi, and A. Surprenant. 2005. Pseudo-apoptosis induced by brief activation of ATP-gated P2X7 receptors. J. Biol. Chem. 280: 33968-33976.
67. Wilson, H. L., S. A. Wilson, A. Surprenant, and R. A. North. 2002. Epithelial membrane proteins induce membrane blebbing and interact with the P2X7 receptor C terminus. J. Biol. Chem. 277: 34017-34023.
68. Pfeiffer, Z. A., M. Aga, U. Prabhu, J. J. Watters, D. J. Hall, and P. J. Bertics. 2004. The nucleotide receptor P2X7 mediates actin reorganization and membrane blebbing in RAW 264.7 macrophages via p38 MAP kinase and Rho. J. Leukocyte Biol. 75: 1173-1182.
69. Panupinthu, N., L. Zhao, F. Possmayer, H. Z. Ke, S. M. Sims, and S. J. Dixon. 2007. P2X7 nucleotide receptors mediate blebbing in osteoblasts through a pathway involving lysophosphatidic acid. J. Biol. Chem. 282: 3403-3412.
70. Chiozzi, P., J. M. Sanz, D. Ferrari, S. Falzoni, A. Aleotti, G. N. Buell, G. Collo, and F. Di Virgilio. 1997. Spontaneous cell fusion in macrophage cultures expressing high levels of the P2Z/P2X7 receptor. J. Cell Biol. 138: 697-706.
71. Lemaire, I., S. Falzoni, N. Leduc, B. Zhang, P. Pellegatti, E. Adinolfi, P. Chiozzi, and F. Di Virgilio. 2006. Involvement of the purinergic P2X7 receptor in the formation of multinucleated giant cells. J. Immunol. 177: 7257-7265.
72. Kusner, D. J., and J. Adams. 2000. ATP-induced killing of virulent Mycobacterium tuberculosis within human macrophages requires phospholipase D. J. Immunol. 164: 379-388.
73. Kanneganti, T. D., M. Lamkanfi, Y. G. Kim, G. Chen, J. H. Park, L. Franchi, P. Vandenabeele, and G. Nunez. 2007. Pannexin-1-mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of Toll-like receptor signaling. Immunity 26: 433-443.