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

Journal of Neurochemistry

Volumn 117, Issue 4, 2011, Pages 712-723

  Takenouchi, Takato ^a,b   Iwamaru, Yoshifumi ^c   Sugama, Shuei ^b,d   Tsukimoto, Mitsutoshi ^e   Fujita, Masayo ^b   Sekigawa, Akio ^b   Sekiyama, Kazunari ^b   Sato, Mitsuru ^a   Kojima, Shuji ^e   Conti, Bruno ^f   Hashimoto, Makoto ^b   Kitani, Hiroshi ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^c NATIONAL INSTITUTE OF ANIMAL HEALTH   (Japan)

^d NIPPON MEDICAL SCHOOL   (Japan)

^e TOKYO UNIVERSITY OF SCIENCE   (Japan)

^f SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

cathepsin D; IL 1 ; microglia; P2X7 receptor

Indexed keywords

CALCIUM ION; CATHEPSIN D; INTERLEUKIN 1BETA; PURINERGIC P2X7 RECEPTOR;

ANIMAL CELL; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOLYSIS; EXTRACELLULAR CALCIUM; MICROGLIA; MOLECULAR WEIGHT; MOUSE; NEWBORN; NONHUMAN; NUCLEAR PORE; PH; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; ANIMALS; BLOTTING, WESTERN; CASPASE 1; CATHEPSIN D; CELL LINE; EXOCYTOSIS; EXTRACELLULAR SPACE; HYDROGEN-ION CONCENTRATION; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; LYSOSOMES; MICE; MICE, INBRED C57BL; MICROGLIA; NERVE TISSUE PROTEINS; PEPSTATINS; RECEPTORS, PURINERGIC P2X7;

EID: 79955013413     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07240.x     Document Type: Article

References (40)

1. Andrei C., Dazzi C., Lotti L., Torrisi M. R., Chimini G., and, Rubartelli A., (1999) The secretory route of the leaderless protein interleukin 1β involves exocytosis of endolysosome-related vesicles. Mol. Biol. Cell 10, 1463-1475. (Pubitemid 29230902)
2. Andrei C., Margiocco P., Poggi A., Lotti L. V., Torrisi M. R., and, Rubartelli A., (2004) Phospholipases C and A2 control lysosome-mediated IL-1β secretion: implications for inflammatory processes. Proc. Natl Acad. Sci. USA 101, 9745-9750. (Pubitemid 38869307)
3. Arend W. P., Malyak M., Guthridge C. J., and, Gabay C., (1998) Interleukin-1 receptor antagonist: role in biology. Annu. Rev. Immunol. 16, 27-55. (Pubitemid 28183358)
4. Brough D., and, Rothwell N. J., (2007) Caspase-1-dependent processing of pro-interleukin-1β is cytosolic and precedes cell death. J. Cell Sci. 120, 772-781. (Pubitemid 46523479)
5. Chen C. S., Chen W. N., Zhou M., Arttamangkul S., and, Haugland R. P., (2000) Probing the cathepsin D using a BODIPY FL-pepstatin A: applications in fluorescence polarization and microscopy. J. Biochem. Biophys. Methods 42, 137-151. (Pubitemid 30100551)
6. Dinarello C. A., (1996) Biologic basis for interleukin-1 in disease. Blood 87, 2095-2147. (Pubitemid 26086851)
7. Dinarello C. A., (2002) The IL-1 family and inflammatory diseases. Clin. Exp. Rheumatol. 20, S1-S13. (Pubitemid 35174747)
8. Dinarello C. A., (2009) Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 27, 519-550.
9. Edlow D. W., and, Sheldon W. H., (1971) The pH of inflammatory exudates. Proc. Soc. Exp. Biol. Med. 137, 1328-1332.
10. Ferrari D., Pizzirani C., Adinolfi E., Lemoli R. M., Curti A., Idzko M., Panther E., and, Di Virgilio F., (2006) The P2X7 receptor: a key player in IL-1 processing and release. J. Immunol. 176, 3877-3883. (Pubitemid 44264361)
11. Franke H., Gunther A., Grosche J., Schmidt R., Rossner S., Reinhardt R., Faber-Zuschratter H., Schneider D., and, Illes P., (2004) P2X7 receptor expression after ischemia in the cerebral cortex of rats. J. Neuropathol. Exp. Neurol. 63, 686-699. (Pubitemid 38891085)
12. 2+ in regulation of IL-1β secretion by P2X7 nucleotide receptor in monocytes, macrophages, and HEK-293 cells. Am. J. Physiol. Cell Physiol. 285, C286-C299. (Pubitemid 36917843)
13. Gulnik S. V., Suvorov L. I., Majer P., Collins J., Kane B. P., Johnson D. G., and, Erickson J. W., (1997) Design of sensitive fluorogenic substrates for human cathepsin D. FEBS Lett. 413, 379-384. (Pubitemid 27353303)
14. Halle A., Hornung V., Petzold G. C., Stewart C. R., Monks B. G., Reinheckel T., Fitzgerald K. A., Latz E., Moore K. J., and, Golenbock D. T., (2008) The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat. Immunol. 9, 857-865.
15. Hanisch U. K., (2002) Microglia as a source and target of cytokines. Glia 40, 140-155.
16. Hazuda D. J., Strickler J., Simon P., and, Young P. R., (1991) Structure-function mapping of interleukin 1 precursors. Cleavage leads to a conformational change in the mature protein. J. Biol. Chem. 266, 7081-7086. (Pubitemid 21906334)
17. + release. Am. J. Physiol. Cell Physiol. 286, C1100-C1108. (Pubitemid 38506925)
18. Liu X., Ma W., Surprenant A., and, Jiang L. H., (2009) Identification of the amino acid residues in the extracellular domain of rat P2X(7) receptor involved in functional inhibition by acidic pH. Br. J. Pharmacol. 156, 135-142.
19. Lopez-Castejon G., Theaker J., Pelegrin P., Clifton A. D., Braddock M., and, Surprenant A., (2010) P2X(7) receptor-mediated release of cathepsins from macrophages is a cytokine-independent mechanism potentially involved in joint diseases. J. Immunol. 185, 2611-2619.
20. MacKenzie A., Wilson H. L., Kiss-Toth E., Dower S. K., North R. A., and, Surprenant A., (2001) Rapid secretion of interleukin-1β by microvesicle shedding. Immunity 15, 825-835. (Pubitemid 34008509)
21. North R. A., (2002) Molecular physiology of P2X receptors. Physiol. Rev. 82, 1013-1067.
22. 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)
23. Pelegrin P., Barroso-Gutierrez C., and, Surprenant A., (2008) P2X7 receptor differentially couples to distinct release pathways for IL-1β in mouse macrophage. J. Immunol. 180, 7147-7157.
24. 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.
25. Perregaux D., Barberia J., Lanzetti A. J., Geoghegan K. F., Carty T. J., and, Gabel C. A., (1992) IL-1β maturation: evidence that mature cytokine formation can be induced specifically by nigericin. J. Immunol. 149, 1294-1303.
26. Qu Y., Franchi L., Nunez G., and, Dubyak G. R., (2007) Nonclassical IL-1β secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J. Immunol. 179, 1913-1925.
27. Sastradipura D. F., Nakanishi H., Tsukuba T., Nishishita K., Sakai H., Kato Y., Gotow T., Uchiyama Y., and, Yamamoto K., (1998) Identification of cellular compartments involved in processing of cathepsin E in primary cultures of rat microglia. J. Neurochem. 70, 2045-2056. (Pubitemid 28207829)
28. Simmen H. P., and, Blaser J., (1993) Analysis of pH and pO2 in abscesses, peritoneal fluid, and drainage fluid in the presence or absence of bacterial infection during and after abdominal surgery. Am. J. Surg. 166, 24-27. (Pubitemid 23281416)
29. Suzumura A., Mezitis S. G., Gonatas N. K., and, Silberberg D. H., (1987) MHC antigen expression on bulk isolated macrophage-microglia from newborn mouse brain: induction of Ia antigen expression by gamma-interferon. J. Neuroimmunol. 15, 263-278. (Pubitemid 17108036)
30. 2+ influx and pore formation induced by the activation of P2X7 nucleotide receptors in mouse microglial cell line. Biochim. Biophys. Acta 1726, 177-186. (Pubitemid 41572257)
31. 2+ influx, pore formation and p44/42 MAP kinase phosphorylation mediated by P2X7 receptor activation in mouse microglial cells. J. Neurochem. 102, 1518-1532. (Pubitemid 47256191)
32. Takenouchi T., Iwamaru Y., Sugama S., Sato M., Hashimoto M., and, Kitani H., (2008) Lysophospholipids and ATP mutually suppress maturation and release of IL-1β in mouse microglial cells using a Rho-dependent pathway. J. Immunol. 180, 7827-7839.
33. Takenouchi T., Sugama S., Iwamaru Y., Hashimoto M., and, Kitani H., (2009a) Modulation of the ATP-lnduced release and processing of IL-1β in microglial cells. Crit. Rev. Immunol. 29, 335-345.
34. Takenouchi T., Nakai M., Iwamaru Y., et al. (2009b) The activation of P2X7 receptor impairs lysosomal functions and stimulates the release of autophagolysosomes in microglial cells. J. Immunol. 182, 2051-2062.
35. Tombaugh G. C., and, Sapolsky R. M., (1993) Evolving concepts about the role of acidosis in ischemic neuropathology. J. Neurochem. 61, 793-803. (Pubitemid 23241214)
36. Verhoef P. A., Kertesy S. B., Lundberg K., Kahlenberg J. M., and, Dubyak G. R., (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. (Pubitemid 41713462)
37. Virginio C., Church D., North R. A., and, Surprenant A., (1997) Effects of divalent cations, protons and calmidazolium at the rat P2X7 receptor. Neuropharmacology 36, 1285-1294. (Pubitemid 27465616)
38. Wewers M. D., (2004) IL-1β: an endosomal exit. Proc. Natl Acad. Sci. USA 101, 10241-10242.
39. Yao C., Li X., Murdiastuti K., Kosugi-Tanaka C., Akamatsu T., Kanamori N., and, Hosoi K., (2005) Lipopolysaccharide-induced elevation and secretion of interleukin-1β in the submandibular gland of male mice. Immunology 116, 213-222. (Pubitemid 41368663)
40. Yao C., Karabasil M. R., Purwanti N., Li X., Akamatsu T., Kanamori N., and, Hosoi K., (2006) Tissue kallikrein mK13 is a candidate processing enzyme for the precursor of interleukin-1β in the submandibular gland of mice. J. Biol. Chem. 281, 7968-7976. (Pubitemid 43847414)