Transient P2X 7 receptor activation triggers macrophage death independent of toll-like receptors 2 and 4, caspase-1, and pannexin-1 proteins

Journal of Biological Chemistry

Volumn 287, Issue 13, 2012, Pages 10650-10663

  Hanley, Peter J ^a   Kronlage, Moritz ^a   Kirschning, Carsten ^b   Del Rey, Adriana ^c   Di Virgilio, Francesco ^d   Leipziger, Jens ^e   Chessell, Iain P ^f   Sargin, Sarah ^a   Filippov, Mikhail A ^g   Lindemann, Otto ^a   Mohr, Simon ^a   Königs, Volker ^a   Schillers, Hermann ^a   Bähler, Martin ^a   Schwab, Albrecht ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF DUISBURG ESSEN   (Germany)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d UNIVERSITY OF FERRARA   (Italy)

^e AARHUS UNIVERSITY   (Denmark)

^f MEDIMMUNE   (United States)

^g UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE-3; EXTRACELLULAR ATP; IMMUNE CELLS; ION CHANNEL; LARGE PORES; LIVE-CELL IMAGING; RECEPTOR ACTIVATION; TLR SIGNALING; TOLL-LIKE RECEPTORS; TOLL-LIKE RECEPTORS 2;

CELL DEATH; INTERFERONS; MAMMALS;

MACROPHAGES;

ADENOSINE TRIPHOSPHATE; CALCIUM ION; CASPASE 3; CASPASE 7; CELL PROTEIN; INTERLEUKIN 1BETA CONVERTING ENZYME; PANNEXIN 1; PURINERGIC P2X7 RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; CALCIUM; GAP JUNCTION PROTEIN; NERVE PROTEIN; PANX1 PROTEIN, MOUSE; TLR2 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM TRANSPORT; CASPASE 1 GENE; CELL DEATH; CELLULAR IMMUNITY; CONTROLLED STUDY; ENZYME ACTIVITY; GENE; INNATE IMMUNITY; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; P2X7 RECEPTOR GENE; PANNEXIN 1 GENE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN FUNCTION; RECEPTOR BLOCKING; TOLL LIKE RECEPTOR 2 GENE; TOLL LIKE RECEPTOR 4 GENE; ANIMAL; CELL CULTURE; DRUG EFFECT; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PERITONEUM MACROPHAGE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CASPASE 1; CELL DEATH; CELLS, CULTURED; CONNEXINS; MACROPHAGES, PERITONEAL; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; RECEPTORS, PURINERGIC P2X7; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

EID: 84858971504     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.332676     Document Type: Article

References (41)

1. North, R. A., and Surprenant, A. (2000) Pharmacology of cloned P2X receptors. Annu. Rev. Pharmacol. Toxicol. 40, 563-580 (Pubitemid 30340693)
2. Khakh, B. S., and North, R. A. (2006) P2X receptors as cell-surface ATP sensors in health and disease. Nature 442, 527-532 (Pubitemid 44167906)
3. North, R. A. (2002) Molecular physiology of P2X receptors. Physiol. Rev. 82, 1013-1067
4. 4- promotes cation fluxes in the J774 mouse macrophage cell line. J. Biol. Chem. 262, 3118-3122
5. Chessell, I. P., Simon, J., Hibell, A. D., Michel, A. D., Barnard, E. A., and Humphrey, P. P. (1998) Cloning and functional characterization of the mouse P2X7 receptor. FEBS Lett. 439, 26-30 (Pubitemid 28537856)
6. Pelegrin, P., and Surprenant, A. (2006) Pannexin-1 mediates large pore formation and interleukin-1β release by the ATP-gated P2X7 receptor. EMBO J. 25, 5071-5082 (Pubitemid 44658525)
7. 7 receptor-Pannexin-1 complex: pharmacology and signaling. Am. J. Physiol. Cell Physiol 295, C752-C760
8. 7 receptor. Neuropharmacology 36, 1277-1283
9. 7). Science 272, 735-738
10. 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 P2X7 receptors. J. Biol. Chem. 276, 125-132 (Pubitemid 32050297)
11. Perregaux, D., and Gabel, C. A. (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
12. Grahames, C. B., Michel, A. D., Chessell, I. P., and Humphrey, P. P.(1999) Pharmacological characterization of ATP- and LPS-induced IL-1β release in human monocytes. Br. J. Pharmacol. 127, 1915-1921 (Pubitemid 29392888)
13. Sanz, J. M., and Di Virgilio, F. (2000) Kinetics and mechanism of ATP-dependent IL-1β release from microglial cells. J. Immunol. 164, 4893- 4898
14. Mehta, V. B., Hart, J., and Wewers, M. D. (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
15. 7-mediated cell death via a caspase-1-dependent mechanism, independently of cytokine production. J. Biol. Chem. 277, 3210-3218
16. 2+ entry differentially contribute to the release of IL-1β and IL-1α from murine macrophages. J. Immunol. 170, 3029-3036
17. 7 nucleotide receptor in monocytes, macrophages, and HEK-293 cells. Am. J. Physiol. Cell Physiol. 285, C286-CC299
18. + release. Am. J. Physiol. Cell Physiol. 286, C1100-C1108
19. 7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J. Immunol. 179, 1913-1925
20. 7 receptor differentially couples to distinct release pathways for IL-1β in mouse macrophage. J. Immunol. 180, 7147-7157
21. Yegutkin, G. G. (2008) Nucleotide- and nucleoside-converting ectoenzymes: important modulators of purinergic signaling cascade. Biochim Biophys Acta 1783, 673-694
22. 2+ signals across the inner ear. Proc. Natl. Acad. Sci. U.S.A. 105, 18770-18775
23. Li, P., Allen, H., Banerjee, S., Franklin, S., Herzog, L., Johnston, C., McDowell, J., Paskind, M., Rodman, L., Salfeld, J., et al. (1995) Mice deficient in IL-1β-converting enzyme are defective in production of mature IL-1βand resistant to endotoxic shock. Cell 80, 401-411
24. 7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 114, 386-396
25. Hanley, P. J., Xu, Y., Kronlage, M., Grobe, K., Schön, P., Song, J., Sorokin, L., Schwab, A., and Bähler, M. (2010) Motorized RhoGAP myosin IXb (Myo9b) controls cell shape and motility. Proc. Natl. Acad. Sci. U.S.A. 107, 12145-12150
26. Kronlage, M., Song, J., Sorokin, L., Isfort, K., Schwerdtle, T., Leipziger, J., Robaye, B., Conley, P. B., Kim, H. C., Sargin, S., Schön, P., Schwab, A., and Hanley, P. J. (2010) Autocrine purinergic receptor signaling is essential for macrophage chemotaxis. Sci. Signal 3: ra55
27. Huang, Y. J., Maruyama, Y., Dvoryanchikov, G., Pereira, E., Chaudhari, N., and Roper, S. D. (2007) The role of pannexin-1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc. Natl. Acad. Sci. U.S.A. 104, 6436-6441 (Pubitemid 47186112)
28. Cen, H., Mao, F., Aronchik, I., Fuentes, R. J., and Firestone, G. L. (2008) DEVD-NucView488: a novel class of enzyme substrates for real-time detection of caspase-3 activity in live cells. FASEB J. 22, 2243-2252 (Pubitemid 351948643)
29. Taylor, R. C., Cullen, S. P., and Martin, S. J. (2008) Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell Biol. 9, 231-241 (Pubitemid 351301823)
30. del Rey, A., Renigunta, V., Dalpke, A. H., Leipziger, J., Matos, J. E., Robaye, B., Zuzarte, M., Kavelaars, A., and Hanley, P. J. (2006) Knock-out mice reveal the contributions of P2Y and P2X receptors to nucleotide-induced Ca2+ signaling in macrophages. J. Biol. Chem. 281, 35147-35155 (Pubitemid 46036554)
31. Nicke, A., Kuan, Y. H., Masin, M., Rettinger, J., Marquez-Klaka, B., Bender, O., Górecki, D. C., Murrell-Lagnado, R. D., and Soto, F. (2009) A functional P2X7 splice variant with an alternative transmembrane domain 1 escapes gene inactivation in P2X7 knock-out mice. J. Biol. Chem. 284, 25813-25822
32. Orrenius, S., Zhivotovsky, B., and Nicotera, P. (2003) Regulation of cell death: the calcium-apoptosis link. Nat. Rev. Mol. Cell Biol. 4, 552-565 (Pubitemid 36773407)
33. Locovei, S., Scemes, E., Qiu, F., Spray, D. C., and Dahl, G. (2007) Pannexin- 1 is part of the pore-forming unit of the P2X7 receptor death complex. FEBS Lett. 581, 483-488 (Pubitemid 46149626)
34. Pelegrin, P., and Surprenant, A. (2007) Pannexin-1 couples to maitotoxin-and nigericin-induced interleukin-1β release through a dye uptake-independent pathway. J. Biol. Chem. 282, 2386-2394 (Pubitemid 47076789)
35. MacVicar, B. A., and Thompson, R. J. (2010) Nonjunction functions of pannexin-1 channels. Trends Neurosci. 33, 93-102
36. Pelegrin, P., and Surprenant, A. (2009) Dynamics of macrophage polarization reveal new mechanism to inhibit IL-1β release through pyrophosphate. EMBO J. 28, 2114-2127
37. Bauernfeind, F., Bartok, E., Rieger, A., Franchi, L., Núñez, G., and Hornung, V. (2011) Cutting edge: reactive oxygen species inhibitors block priming, but not activation of the NLRP3 inflammasome. J. Immunol. 187, 613-617
38. Davis, B. K., Wen, H., and Ting, J. P. (2011) The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu. Rev. Immunol. 29, 707-735
39. Pétrilli, V., Dostert, C., Muruve, D. A., and Tschopp, J. (2007) The inflammasome: a danger-sensing complex triggering innate immunity. Curr. Opin Immunol. 19, 615-622 (Pubitemid 350236810)
40. Riedl, S. J., and Salvesen, G. S. (2007) The apoptosome: signaling platform of cell death. Nat. Rev. Mol. Cell Biol. 8, 405-413 (Pubitemid 46643237)
41. 7 receptor- operated single-channel currents. Biophys. J. 93, 846-858