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Mediators of Inflammation
Volume 2013 (2013), Article ID 271813, 18 pages
http://dx.doi.org/10.1155/2013/271813
Research Article

P2X7 Receptor Activation Induces Reactive Oxygen Species Formation and Cell Death in Murine EOC13 Microglia

1School of Biological Sciences, University of Wollongong, Wollongong, NSW 2522, Australia
2Illawarra Health and Medical Research Institute, Wollongong, NSW 2522, Australia

Received 14 September 2012; Revised 16 November 2012; Accepted 4 December 2012

Academic Editor: Sung-Jen Wei

Copyright © 2013 Rachael Bartlett et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Nimmerjahn, F. Kirchhoff, and F. Helmchen, “Neuroscience: resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo,” Science, vol. 308, no. 5726, pp. 1314–1318, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. K. Helmut, U. K. Hanisch, M. Noda, and A. Verkhratsky, “Physiology of microglia,” Physiological Reviews, vol. 91, no. 2, pp. 461–553, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. U. K. Hanisch and H. Kettenmann, “Microglia: active sensor and versatile effector cells in the normal and pathologic brain,” Nature Neuroscience, vol. 10, no. 11, pp. 1387–1394, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. R. M. Ransohoff and V. H. Perry, “Microglial physiology: unique stimuli, specialized responses,” Annual Review of Immunology, vol. 27, pp. 119–145, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. M. L. Block and J. S. Hong, “Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism,” Progress in Neurobiology, vol. 76, no. 2, pp. 77–98, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Monif, G. Burnstock, and D. A. Williams, “Microglia: proliferation and activation driven by the P2X7 receptor,” International Journal of Biochemistry and Cell Biology, vol. 42, no. 11, pp. 1753–1756, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. M. F. Jarvis and B. S. Khakh, “ATP-gated P2X cation-channels,” Neuropharmacology, vol. 56, no. 1, pp. 208–215, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. J. S. Wiley, R. Sluyter, B. J. Gu, L. Stokes, and S. J. Fuller, “The human P2X7 receptor and its role in innate immunity,” Tissue Antigens, vol. 78, no. 5, pp. 321–332, 2011.
  9. S. Duan and J. T. Neary, “P2X7 receptors: properties and relevance to CNS function,” GLIA, vol. 54, no. 7, pp. 738–746, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Hewinson and A. B. MacKenzie, “P2X7 receptor-mediated reactive oxygen and nitrogen species formation: from receptor to generators,” Biochemical Society Transactions, vol. 35, no. 5, pp. 1168–1170, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Adinolfi, C. Pizzirani, M. Idzko et al., “P2X7 receptor: death or life?” Purinergic Signalling, vol. 1, no. 3, pp. 219–227, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. F. di Virgilio, D. Ferrari, and E. Adinolfi, “P2X7: a growth-promoting receptor—implications for cancer,” Purinergic Signalling, vol. 5, no. 2, pp. 251–256, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. W. S. Walker, J. Gatewood, E. Olivas, D. Askew, and C. E. G. Havenith, “Mouse microglial cell lines differing in constitutive and interferon-γ-inducible antigen-presenting activities for naive and memory CD4+ and CD8+ T cells,” Journal of Neuroimmunology, vol. 63, no. 2, pp. 163–174, 1995. View at Publisher · View at Google Scholar · View at Scopus
  14. P. Constantinescu, B. Wang, K. Kovacevic et al., “P2X7 receptor activation induces cell death and microparticle release in murine erythroleukemia cells,” Biochimica et Biophysica Acta, vol. 1798, no. 9, pp. 1797–1804, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. R. A. North, “Molecular physiology of P2X receptors,” Physiological Reviews, vol. 82, no. 4, pp. 1013–1067, 2002. View at Scopus
  16. P. W. Marks and F. R. Maxfield, “Preparation of solutions with free calcium concentration in the nanomolar range using 1,2-bis(o-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid,” Analytical Biochemistry, vol. 193, no. 1, pp. 61–71, 1991. View at Scopus
  17. R. Coutinho-Silva, D. M. Ojcius, D. C. Górecki et al., “Multiple P2X and P2Y receptor subtypes in mouse J774, spleen and peritoneal macrophages,” Biochemical Pharmacology, vol. 69, no. 4, pp. 641–655, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. A. W. Farrell, S. Gadeock, A. Pupovac et al., “P2X7 receptor activation induces cell death and CD23 shedding in human RPMI 8226 multiple myeloma cells,” Biochimica et Biophysica Acta, vol. 1800, no. 11, pp. 1173–1182, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. D. W. Nelson, R. J. Gregg, M. E. Kort et al., “Structure-activity relationship studies on a series of novel, substituted 1-benzyl-5-phenyltetrazole P2X7 antagonists,” Journal of Medicinal Chemistry, vol. 49, no. 12, pp. 3659–3666, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. A. D. Michel, L. J. Chambers, W. C. Clay, J. P. Condreay, D. S. Walter, and I. P. Chessell, “Direct labelling of the human P2X7 receptor and identification of positive and negative cooperativity of binding,” British Journal of Pharmacology, vol. 151, no. 1, pp. 84–95, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Stokes, L. H. Jiang, L. Alcaraz et al., “Characterization of a selective and potent antagonist of human P2X7 receptors, AZ11645373,” British Journal of Pharmacology, vol. 149, no. 7, pp. 880–887, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. N. D'Ambrosi, P. Finocchi, S. Apolloni et al., “The proinflammatory action of microglial P2 receptors is enhanced in SOD1 models for amyotrophic lateral sclerosis,” Journal of Immunology, vol. 183, no. 7, pp. 4648–4656, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Díaz-Hernández, M. Díez-Zaera, J. Sánchez-Nogueiro et al., “Altered P2X7-receptor level and function in mouse models of Huntington's disease and therapeutic efficacy of antagonist administration,” FASEB Journal, vol. 23, no. 6, pp. 1893–1906, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. Y. K. Soo, H. M. Ju, G. L. Hwan, U. K. Seung, and B. L. Yong, “ATP released from β-amyloid-stimulated microglia induces reactive oxygen species production in an autocrine fashion,” Experimental and Molecular Medicine, vol. 39, no. 6, pp. 820–827, 2007. View at Scopus
  25. L. K. Parvathenani, S. Tertyshnikova, C. R. Greco, S. B. Roberts, B. Robertson, and R. Posmantur, “P2X7 mediates superoxide production in primary microglia and is up-regulated in a transgenic mouse model of Alzheimer's disease,” Journal of Biological Chemistry, vol. 278, no. 15, pp. 13309–13317, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. B. C. Suh, J. S. Kim, U. Namgung, H. Ha, and K. T. Kim, “P2X7 nucleotide receptor mediation of membrane pore formation and superoxide generation in human promyelocytes and neutrophils,” Journal of Immunology, vol. 166, no. 11, pp. 6754–6763, 2001. View at Scopus
  27. U. Fontanils, M. Seil, S. Pochet et al., “Stimulation by P2X7 receptors of calcium-dependent production of reactive oxygen species (ROS) in rat submandibular glands,” Biochimica et Biophysica Acta, vol. 1800, no. 11, pp. 1183–1191, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. F. Martinon, A. Mayor, and J. Tschopp, “The inflammasomes: guardians of the body,” Annual Review of Immunology, vol. 27, pp. 229–265, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Qu and G. R. Dubyak, “P2X7 receptors regulate multiple types of membrane trafficking responses and non-classical secretion pathways,” Purinergic Signalling, vol. 5, no. 2, pp. 163–173, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Noguchi, K. Ishii, H. Fukutomi et al., “Requirement of reactive oxygen species-dependent activation of ASK1-p38 MAPK pathway for extracellular ATP-induced apoptosis in macrophage,” Journal of Biological Chemistry, vol. 283, no. 12, pp. 7657–7665, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. I. P. Chessell, J. Simon, A. D. Hibell, A. D. Michel, E. A. Barnard, and P. P. A. Humphrey, “Cloning and functional characterisation of the mouse P2X7 receptor,” FEBS Letters, vol. 439, no. 1-2, pp. 26–30, 1998. View at Publisher · View at Google Scholar · View at Scopus
  32. D. Ferrari, P. Chiozzi, S. Falzoni et al., “ATP-mediated cytotoxicity in microglial cells,” Neuropharmacology, vol. 36, no. 9, pp. 1295–1301, 1997. View at Publisher · View at Google Scholar · View at Scopus
  33. D. Ferrari, M. Villalba, P. Chiozzi, S. Falzoni, P. Ricciardi-Castagnoli, and F. di Virgilio, “Mouse microglial cells express a plasma membrane pore gated by extracellular ATP,” Journal of Immunology, vol. 156, no. 4, pp. 1531–1539, 1996. View at Scopus
  34. I. P. Chessell, A. D. Michel, and P. P. A. Humphrey, “Properties of the pore-forming P2X7 purinoceptor in mouse NTW8 microglial cells,” British Journal of Pharmacology, vol. 121, no. 7, pp. 1429–1437, 1997. View at Publisher · View at Google Scholar · View at Scopus
  35. F. P. Gendron, M. Chalimoniuk, J. Strosznajder et al., “P2X7 nucleotide receptor activation enhances IFNγ-induced type II nitric oxide synthase activity in BV-2 microglial cells,” Journal of Neurochemistry, vol. 87, no. 2, pp. 344–352, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. S. D. Skaper, L. Facci, A. A. Culbert et al., “P2X7 receptors on microglial cells mediate injury to cortical neurons in vitro,” GLIA, vol. 54, no. 3, pp. 234–242, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. Y. Yiangou, P. Facer, P. Durrenberger et al., “COX-2, CB2 and P2X7-immunoreactivities are increased in activated microglial cells/macrophages of multiple sclerosis and amyotrophic lateral sclerosis spinal cord,” BMC Neurology, vol. 6, article 12, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. X. Chen, Z. Zhong, Z. Xu, L. Chen, and Y. Wang, “2′,7′-Dichlorodihydrofluorescein as a fluorescent probe for reactive oxygen species measurement: forty years of application and controversy,” Free Radical Research, vol. 44, no. 6, pp. 587–604, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Seil, U. Fontanils, I. G. Etxebarria et al., “Pharmacological evidence for the stimulation of NADPH oxidase by P2X7 receptors in mouse submandibular glands,” Purinergic Signalling, vol. 4, no. 4, pp. 347–355, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. B. Wang and R. Sluyter, “P2X7 receptor activation induces reactive oxygen species formation in erythroid cells,” Purinergic Signalling. In press. View at Publisher · View at Google Scholar
  41. D. Ferrari, M. Los, M. K. A. Bauer, P. Vandenabeele, S. Wesselborg, and K. Schulze-Osthoff, “P2Z purinoreceptor ligation induces activation of caspases with distinct roles in apoptotic and necrotic alterations of cell death,” FEBS Letters, vol. 447, no. 1, pp. 71–75, 1999. View at Publisher · View at Google Scholar · View at Scopus
  42. D. Brough, R. A. Le Feuvre, Y. Iwakura, and N. J. Rothwell, “Purinergic (P2X7) receptor activation of microglia induces cell death via an interleukin-1-independent mechanism,” Molecular and Cellular Neuroscience, vol. 19, no. 2, pp. 272–280, 2002. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Monif, C. A. Reid, K. L. Powell, M. L. Smart, and D. A. Williams, “The P2X7 receptor drives microglial activation and proliferation: a trophic role for P2X7R pore,” Journal of Neuroscience, vol. 29, no. 12, pp. 3781–3791, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. F. di Virgilio, S. Ceruti, P. Bramanti, and M. P. Abbracchio, “Purinergic signalling in inflammation of the central nervous system,” Trends in Neurosciences, vol. 32, no. 2, pp. 79–87, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. S. F. Moore and A. B. MacKenzie, “NADPH oxidase NOX2 mediates rapid cellular oxidation following ATP stimulation of endotoxin-primed macrophages,” Journal of Immunology, vol. 183, no. 5, pp. 3302–3308, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Qanungo, M. Wang, and A. L. Nieminen, “N-acetyl-L-cysteine enhances apoptosis through inhibition of nuclear factor-κB in hypoxic murine embryonic fibroblasts,” Journal of Biological Chemistry, vol. 279, no. 48, pp. 50455–50464, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. X. Liu, W. Ma, A. Surprenant, and L. H. Jiang, “Identification of the amino acid residues in the extracellular domain of rat P2X7 receptor involved in functional inhibition by acidic pH,” British Journal of Pharmacology, vol. 156, no. 1, pp. 135–142, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. Z. A. Pfeiffer, A. N. Guerra, L. M. Hill et al., “Nucleotide receptor signaling in murine macrophages is linked to reactive oxygen species generation,” Free Radical Biology and Medicine, vol. 42, no. 10, pp. 1506–1516, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. P. Pelegrin, C. Barroso-Gutierrez, and A. Surprenant, “P2X7 receptor differentially couples to distinct release pathways for IL-1β in mouse macrophage,” Journal of Immunology, vol. 180, no. 11, pp. 7147–7157, 2008. View at Scopus
  50. P. Chiozzi, J. M. Sanz, D. Ferrari et al., “Spontaneous cell fusion in macrophage cultures expressing high levels of the P2Z/P2X7 receptor,” Journal of Cell Biology, vol. 138, no. 3, pp. 697–706, 1997. View at Publisher · View at Google Scholar · View at Scopus
  51. T. H. Steinberg, “P2-mediated responses in osteoclasts and osteoclast-like cells,” Drug Development Research, vol. 53, no. 2-3, pp. 126–129, 2001. View at Publisher · View at Google Scholar · View at Scopus
  52. I. Lemaire, S. Falzoni, B. Zhang, P. Pellegatti, and F. di Virgilio, “The P2X7 receptor and pannexin-1 are both required for the promotion of multinucleated macrophages by the inflammatory cytokine GM-CSF,” Journal of Immunology, vol. 187, no. 7, pp. 3878–3887, 2011.
  53. P. Chiozzi, M. Murgia, S. Falzoni, D. Ferrari, and F. di Virgilio, “Role of the purinergic P2Z receptor in spontaneous cell death in J774 macrophage cultures,” Biochemical and Biophysical Research Communications, vol. 218, no. 1, pp. 176–181, 1996. View at Publisher · View at Google Scholar · View at Scopus
  54. D. L. Donnelly-Roberts, M. T. Namovic, P. Han, and M. F. Jarvis, “Mammalian P2X7 receptor pharmacology: comparison of recombinant mouse, rat and human P2X7 receptors,” British Journal of Pharmacology, vol. 157, no. 7, pp. 1203–1214, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. A. D. Michel, S. W. Ng, S. Roman, W. C. Clay, D. K. Dean, and D. S. Walter, “Mechanism of action of species-selective P2X7 receptor antagonists,” British Journal of Pharmacology, vol. 156, no. 8, pp. 1312–1325, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. B. S. Khakh and R. A. North, “P2X receptors as cell-surface ATP sensors in health and disease,” Nature, vol. 442, no. 7102, pp. 527–532, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. H. Franke and P. Illes, “Involvement of P2 receptors in the growth and survival of neurons in the CNS,” Pharmacology and Therapeutics, vol. 109, no. 3, pp. 297–324, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. I. Hide, M. Tanaka, A. Inoue et al., “Extracellular ATP triggers tumor necrosis factor-α release from rat microglia,” Journal of Neurochemistry, vol. 75, no. 3, pp. 965–972, 2000. View at Publisher · View at Google Scholar · View at Scopus
  59. H. Franke, A. Günther, J. Grosche et al., “P2X7 receptor expression after ischemia in the cerebral cortex of rats,” Journal of Neuropathology and Experimental Neurology, vol. 63, no. 7, pp. 686–699, 2004.
  60. T. Takenouchi, Y. Iwamaru, M. Imamura et al., “Prion infection correlates with hypersensitivity of P2X7 nucleotide receptor in a mouse microglial cell line,” FEBS Letters, vol. 581, no. 16, pp. 3019–3026, 2007. View at Publisher · View at Google Scholar · View at Scopus