Oxidative stress induced by P2X7 receptor stimulation in murine macrophages is mediated by c-Src/Pyk2 and ERK1/2

Biochimica et Biophysica Acta - General Subjects

Volumn 1830, Issue 10, 2013, Pages 4650-4659

  Martel Gallegos, Guadalupe ^a   Casas Pruneda, Griselda ^a   Ortega Ortega, Filiberta ^a   Sánchez Armass, Sergio ^a   Olivares Reyes, Jesús Alberto ^b   Diebold, Becky ^c   Pérez Cornejo, Patricia ^a   Arreola, Jorge ^a  

^a UNIVERSIDAD AUTÓNOMA DE SAN LUIS POTOSÍ   (Mexico)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium; Macrophage; Mitogen activated protein kinase; Oxidative stress; Purinergic receptor

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; CALMODULIN; ENZYME ANTIBODY; FOCAL ADHESION KINASE 2; FOCAL ADHESION KINASE 2 ANTIBODY; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 1 ANTIBODY; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 3 ANTIBODY; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN INHIBITOR; PROTEIN KINASE P60; PROTEIN P47; PROTEIN P67; PURINERGIC P2X7 RECEPTOR; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INACTIVATION; INTRACELLULAR SIGNALING; MACROPHAGE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

2′,3′-O-(4-BENZOYL-BENZOYL) ATP; 2′,7′-DICHLORODIHYDROFLUORESCEIN DIACETATE; 2′,7′-DICHLOROFLUORESCEIN; 2-(1-(3 DIMETHYLAMINOPROPYL)-5-METHOXYINDOL-3-YL)-3-(1H-INDOL-3-YL)MALEIMIDE; 2-(2-AMINO-3-METHOXYPHENYL)-4H-1-BENZOPYRAN-4-ONE; 4-[5-(4-FLUOROPHENYL)-2-[4-(METHYLSULFONYL)PHENYL]-1H-IMIDAZOL-4-YL]PYRIDINE; 4-AMINO-5-(4-CHLOROPHENYL)-7-(DIMETHYLETHYL) PYRAZOLO[3,4-D]PYRIMIDINE; 8-AMINO-5-CHLORO-7-PHENYLPYRIDO [3,4-D]PYRIDAZINE-1,4(2H,3H) DIONE; BZ-ATP; C-JUN N-TERMINAL KINASE; CALCIUM; DCF; DCFH(2)DA; DIMETHLYSULFOXIDE; DIPHENYLENEIODONIUM; DMSO; DPI; EGFR; EPIDERMAL GROWTH FACTOR RECEPTOR; ERK1/2; EXTRACELLULAR REGULATED KINASES 1 AND 2; FURA-2 AM; FURA-2-ACETOXYMETHYLESTER; GÖ6983; HANKS'S BALANCED SALT SOLUTION; HBSS; IL-1Β; INTERLEUKIN-1Β; JNK; L-012; LIPOPOLYSACCHARIDE; LPS; MACROPHAGE; MAPKS; MITOGEN-ACTIVATED PROTEIN KINASE; MITOGEN-ACTIVATED PROTEIN KINASES; N-METHYL-N-[2-[[[2-[(2,3-DIHYDRO-2- OXO-1H-INDOL-5-YL)AMINO]-5-(TRIFLUOROMETHYL)-4-PYRIMIDINYL]AMINO]METHYL]PHENYL]METHANESULFONAMIDE; OXIDATIVE STRESS; P2X7 RECEPTOR CHANNELS; P2X7R; PD98059; PF431396; PHORBOL MYRISTATE ACETATE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE D; PI3K; PLD; PMA; PP2; PURINERGIC RECEPTOR; REACTIVE OXYGEN SPECIES; ROS; SALINE SOLUTION; SB203580; SB239063; SS; TNFΑ; TRANS-4-[4-(4-FLUOROPHENYL)-5-(2-METHOXY-4-PYRIMIDINYL)-1H-IMIDAZOL-1-YL]CYCLOHEXANOL; TUMOR NECROSIS FACTOR Α; WB; WESTERN BLOT;

ANIMALS; CALCIUM; CELL LINE; FOCAL ADHESION KINASE 2; HUMANS; ION TRANSPORT; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MICE; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS PP60(C-SRC); RECEPTORS, PURINERGIC P2X7;

MURINAE;

EID: 84879489036     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.05.023     Document Type: Article

References (74)

1. J.L. Gordon Extracellular ATP: effects, sources and fate Biochem. J. 233 1986 309 319 (Pubitemid 16169477)
2. M.P. Abbracchio, and G. Burnstock Purinergic signalling: pathophysiological roles Jpn. J. Pharmacol. 78 1998 113 145 (Pubitemid 28508403)
3. M.J. Bours, E.L. Swennen, F. Di Virgilio, B.N. Cronstein, and P.C. Dagnelie Adenosine 5′-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation Pharmacol. Ther. 112 2006 358 404 (Pubitemid 44486409)
4. S. Gordon Development and distribution of mononuclear phagocytes: relevance to inflammation J.I.G.a.R. Snyderman, Inflammation: Basic Principles and Clinical Correlates 1999 Lippincott Williams and Wilkins Philadelphia 35 48
5. F. Di Virgilio, P. Chiozzi, D. Ferrari, S. Falzoni, J.M. Sanz, A. Morelli, M. Torboli, G. Bolognesi, and O.R. Baricordi Nucleotide receptors: an emerging family of regulatory molecules in blood cells Blood 97 2001 587 600 (Pubitemid 32113390)
6. B.D. Humphreys, and G.R. Dubyak Induction of the P2z/P2X7 nucleotide receptor and associated phospholipase D activity by lipopolysaccharide and IFN-gamma in the human THP-1 monocytic cell line J. Immunol. 157 1996 5627 5637 (Pubitemid 126448986)
7. D. Ferrari, C. Pizzinari, and E. Adinolfi The P2X7 receptor: a key player in IL-1 processing and release J. Immunol. 176 2006 3877 3883 (Pubitemid 44264361)
8. Y. Hu, P.L. Fisette, L.C. Denlinger, A.G. Guadarrama, J.A. Sommer, R.A. Proctor, and P.J. Bertics Purinergic receptor modulation of lipopolysaccharide signaling and inducible nitric-oxide synthase expression in RAW 264.7 macrophages J. Biol. Chem. 273 1998 27170 27175 (Pubitemid 28500425)
9. Z.A. Pfeiffer, M. Aga, and U. Prabhu The nucleotide receptor P2X7 mediates actin reorganization and membrane blebbing in RAW 264.7 macrophages via p38 MAP kinase and Rho J. Leukoc. Biol. 75 2004 1173 1182 (Pubitemid 38720662)
10. J. Hewinson, and A.B. Mackenzie P2X(7) receptor-mediated reactive oxygen and nitrogen species formation: from receptor to generators Biochem. Soc. Trans. 35 2007 1168 1170 (Pubitemid 350206453)
11. A.N. Guerra, M.L. Gavala, H.S. Chung, and P.J. Bertics Nucleotide receptor signalling and the generation of reactive oxygen species Purinergic Signal 3 2007 39 51
12. L.Y. Lenertz, M.L. Gavala, L.M. Hill, and P.J. Bertics Cell signaling via the P2X(7) nucleotide receptor: linkage to ROS production, gene transcription, and receptor trafficking Purinergic Signal 5 2009 175 187
13. Z.A. Pfeiffer, A.N. Guerra, and L.M. Hill Nucleotide receptor signaling in murine macrophages is linked to reactive oxygen species generation Free Radic. Biol. Med. 42 2007 1506 1516 (Pubitemid 46590610)
14. K. Noguchi, K. Ishii, H. Fukutomi, I. Naguro, A. Matsuzawa, K. Takeda, and H. Ichijo Requirement of reactive oxygen species-dependent activation of ASK1-p38 MAPK pathway for extracellular ATP-induced apoptosis in macrophage J. Biol. Chem. 283 2008 7657 7665
15. C.M. Cruz, A. Rinna, H.J. Forman, A.L. Ventura, P.M. Persechini, and D.M. Ojcius ATP activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages J. Biol. Chem. 282 2007 2871 2879 (Pubitemid 47084344)
16. D. Ferrari, S. Wesselborg, M.K. Bauer, and K. Schulze-Osthoff Extracellular ATP activates transcription factor NF-kappaB through the P2Z purinoreceptor by selectively targeting NF-kappaB p65 J. Cell Biol. 139 1997 1635 1643 (Pubitemid 28079229)
17. C.M. da Cruz, 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 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 2006 324 334 (Pubitemid 43214690)
18. D. Ferrari, M. Idzko, S. Dichmann, D. Purlis, C. Virchow, J. Norgauer, P. Chiozzi, F. Di Virgilio, and W. Luttmann P2 purinergic receptors of human eosinophils: characterization and coupling to oxygen radical production FEBS Lett. 486 2000 217 224
19. 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 J. Biol. Chem. 278 2003 13309 13317 (Pubitemid 36800102)
20. H. Harada, M. Tsukimoto, A. Ikari, K. Takagi, and Y. Suketa P2X(7) receptor-induced generation of reactive oxygen species in rat mesangial cells Drug Dev. Res. 59 2003 112 117 (Pubitemid 36682448)
21. M. Seil, U. Fontanils, I. Gorrono Etxebarria, S. Pochet, M. Garcia-Marcos, A. Marino, and J.P. Dehaye Pharmacological evidence for the stimulation of NADPH oxidase by P2X(7) receptors in mouse submandibular glands Purinergic Signal 4 2008 347 355
22. J.K. Murphy, F.R. Livingston, E. Gozal, M. Torres, and H.J. Forman Stimulation of the rat alveolar macrophage respiratory burst by extracellular adenine nucleotides Am. J. Respir. Cell Mol. Biol. 9 1993 505 510 (Pubitemid 2007510)
23. L.P. Faust, J. El Benna, B.M. Babior, and S.J. Chanock The phosphorylation targets of p47 phox a subunit of the respiratory burst oxidase. Functions of the individual target serines as evaluated by site-directed mutagenesis J. Clin. Invest. 96 1995 1499 1505
24. K. Bedard, and K.H. Krause The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology Physiol. Rev. 87 2007 245 313 (Pubitemid 46209993)
25. S.F. Moore, and A.B. MacKenzie NADPH oxidase NOX2 mediates rapid cellular oxidation following ATP stimulation of endotoxin-primed macrophages J. Immunol. 183 2009 3302 3308
26. P. Pelegrin, and A. Surprenant Pannexin-1 mediates large pore formation and interleukin-1 beta release by the ATP-gated P2X7 receptor EMBO J. 25 2006 5071 5082 (Pubitemid 44658525)
27. R. Coutinho-Silva, D.M. Ojcius, D.C. Górecki, P.M. Persechini, R.C. Bisaggio, A.N. Mendes, J. Marks, G. Burnstock, and P.M. Dunn Multiple P2X and P2Y receptor subtypes in mouse J774, spleen and peritoneal macrophages Biochem. Pharmacol. 69 2005 641 655
28. R.A. North Molecular physiology of P2X receptors Physiol. Rev. 82 2002 1013 1067
29. G. Cheng, B.A. Diebold, Y. Hughes, and J.D. Lambeth Nox1-dependent reactive oxygen generation is regulated by Rac1 J. Biol. Chem. 281 2006 17718 17726 (Pubitemid 44035570)
30. G. Casas-Pruneda, J.P. Reyes, G. Pérez-Flores, P. Pérez-Cornejo, and J. Arreola Functional interactions between P2X4 and P2X7 receptors from mouse salivary epithelia J. Physiol. 587 2009 2887 2901
31. M. Murgia, S. Hanau, P. Pizzo, M. Rippa, and F. Di Virgilio Oxidized ATP. An irreversible inhibitor of the macrophage purinergic P2Z receptor J. Biol. Chem. 268 1993 8199 8203 (Pubitemid 23120407)
32. D.W. Nelson, R.J. Gregg, M.E. Kort, A. Perez-Medrano, E.A. Voight, Y. Wang, G. Grayson, M.T. Namovic, D.L. Donnelly-Roberts, W. Niforatos, P. Honore, M.F. Jarvis, C.R. Faltynek, and W.A. Carroll Structure-activity relationship studies on a series of novel, substituted 1-benzyl-5-phenyltetrazole P2X7 antagonists J. Med. Chem. 49 2006 3659 3666 (Pubitemid 43902471)
33. J. Hewinson, S.F. Moore, C. Glover, A.G. Watts, and A.B. MacKenzie A key role for redox signaling in rapid P2X7 receptor-induced IL-1 beta processing in human monocytes J. Immunol. 180 2008 8410 8420
34. M. Gschwendt, S. Dieterich, J. Rennecke, W. Kittstein, H.J. Mueller, and F.J. Johannes Inhibition of protein kinase C mu by various inhibitors. Differentiation from protein kinase C isoenzymes FEBS Lett. 392 1996 77 80 (Pubitemid 26276722)
35. D. Toullec, P. Pianetti, H. Coste, P. Bellevergue, T. Grand-Perret, M. Ajakane, V. Baudet, P. Boissin, E. Boursier, F. Loriolle, L. Duhamel, D. Charon, and J. Kirilovsky The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C J. Biol. Chem. 266 1991 15771 15781 (Pubitemid 21907725)
36. D.A. Fruman, R.E. Meyers, and L.C. Cantley Phosphoinositide kinases Annu. Rev. Biochem. 67 1998 481 507 (Pubitemid 28411136)
37. D.C. Underwood, R.R. Osborn, C.J. Kotzer, J.L. Adamas, J.C. Lee, E.F. Webb, D.C. Carpenter, S. Bochnowicz, H.C. Thomas, D.W. Hay, and D.E. Griswold SB 239063, a potent p38 MAP kinase inhibitor, reduces inflammatory cytokine production, airways eosinophil infiltration, and persistence J. Pharmacol. Exp. Ther. 293 2000 281 288 (Pubitemid 30180950)
38. S.P. Davies, H. Reddy, M. Caivano, and P. Cohen Specificity and mechanism of action of some commonly used protein kinase inhibitors Biochem. J. 351 2000 95 105
39. D.R. Alessi, A. Cuenda, P. Cohen, D.T. Dudley, and A.R. Saltiel PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo J. Biol. Chem. 270 1995 27489 27494
40. J.V. Duncia, J.B. Santella, C.A. Higley, W.J. Pitts, J. Wityak, W.E. Frietze, F.W. Rankin, J.H. Sun, R.A. Earl, A.C. Tabaka, C.A. Teleha, K.F. Blom, M.F. Favata, E.J. Manos, A.J. Daulerio, D.A. Stradley, K. Horiuchi, R.A. Copeland, P.A. Scherle, J.M. Trzaskos, R.L. Magolda, G.L. Trainor, R.R. Wexler, F.W. Hobbs, and R.E. Olson MEK inhibitors: the chemistry and biological activity of U0126, its analogs, and cyclization products Bioorg. Med. Chem. Lett. 8 1998 2839 2844 (Pubitemid 28483178)
41. J.H. Hanke, J.P. Gardner, R.L. Dow, P.S. Changelian, W.H. Brissette, E.J. Weringer, B.A. Pollok, and P.A. Connelly Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation J. Biol. Chem. 271 1996 695 701
42. L. Buckbinder, D.T. Crawford, H. Qi, H.Z. Ke, L.M. Olson, K.R. Long, P.C. Bonnette, A.P. Baumann, J.E. Hambor, W.A. 3rd Grasser, L.C. Pan, T.A. Owen, M.J. Luzzio, C.A. Hulford, D.F. Gebhard, V.M. Paralkar, H.A. Simmons, J.C. Kath, W.G. Roberts, S.L. Smock, A. Guzman-Perez, T.A. Brown, and M. Li Proline-rich tyrosine kinase 2 regulates osteoprogenitor cells and bone formation, and offers an anabolic treatment approach for osteoporosis Proc. Natl. Acad. Sci. U.S.A. 104 2007 10619 10624 (Pubitemid 47185714)
43. K.W. Tse, M. Dang-Lawson, R.L. Lee, D. Vong, A. Bulic, L. Buckbinder, and M.R. Gold B cell receptor-induced phosphorylation of Pyk2 and focal adhesion kinase involves integrins and the Rap GTPases and is required for B cell spreading J. Biol. Chem. 284 2009 22865 22877
44. V. Ralevic, and G. Burnstock Receptors for purines and pyrimidines Pharmacol. Rev. 50 1998 413 492 (Pubitemid 28477681)
45. C. Virginio, D. Church, R.A. North, and A. Surprenant Effects of divalent cations, protons and calmidazolium at the rat P2X7 receptor Neuropharmacology 36 1997 1285 1294 (Pubitemid 27465616)
46. S.I. Gharbi, M.J. Zvelebil, S.J. Shuttleworth, T. Hancox, N. Saghir, J.F. Timms, and M.D. Waterfield Exploring the specificity of the PI3K family inhibitor LY294002 Biochem. J. 404 2007 15 21 (Pubitemid 46788080)
47. S. Lev, H. Moreno, R. Martinez, P. Canoll, E. Peles, J.M. Musacchio, G.D. Plowman, B. Rudy, and J. Schlessinger Protein tyrosine kinase PYK2 involved in Ca(2 +)-induced regulation of ion channel and MAP kinase functions Nature 376 1995 737 745
48. D.E. Clapham Calcium signaling Cell 131 2007 1047 1058 (Pubitemid 350258556)
49. P.J. Cullen, and P.J. Lockyer Integration of calcium and Ras signalling Nat. Rev. Mol. Cell Biol. 3 2002 339 348 (Pubitemid 34619268)
50. W.N. Hait, L. Glazer, C. Kaiser, J. Cross, and K.A. Kennedy Pharmacological properties of fluphenazine-mustard, an irreversible calmodulin antagonist Mol. Pharmacol. 32 1987 404 409 (Pubitemid 18007296)
51. J. El-Benna, J. Han, J.W. Park, E. Schmid, R.J. Ulevitch, and B.M. Babior Activation of p38 in stimulated human neutrophils: phosphorylation of the oxidase component p47phox by p38 and ERK but not by JNK Arch. Biochem. Biophys. 334 1996 395 400 (Pubitemid 26347324)
52. J. Emily, J. Swindle, A. Hunt, and J.W. Coleman A comparison of reactive oxygen species generation by rat peritoneal macrophages and mast cells using the highly sensitive real-time chemiluminescent probe pholasin: inhibition of antigen-induced mast cell degranulation by macrophage-derived hydrogen peroxide J. Immunol. 169 2002 5866 5873 (Pubitemid 35291691)
53. C. Guo, M. Masin, O.S. Qureshi, and R.D. Murell-Lagnado Evidence for functional P2X4/P2X7 heteromeric receptors Mol. Pharmacol. 72 2007 1447 1456 (Pubitemid 350146082)
54. S. Murasawa, Y. Mori, Y. Nozawa, H. Masaki, K. Maruyama, Y. Tustsumi, Y. Moriguchi, Y. Shibasaki, Y. Tanaka, T. Iwasaka, M. Inada, and H. Matsubara Role of calcium-sensitive tyrosine kinase PYK2/CAKβ/RAFTK in angiotensin II-induced Ras/ERK signaling Hypertension 32 1998 668 675 (Pubitemid 28480542)
55. D.J. Espiritu, A.A. Bernardo, R.B. Robey, and J.A. Arruda A central role for Pyk2-Src interaction in coupling diverse stimuli to increased epithelial NBC activity Am. J. Physiol. Renal Physiol. 283 2002 F663 F670
56. F.P. Gendron, J.T. Neary, P.M. Theiss, G.Y. Sun, F.A. Gonzalez, and G.A. Weisman Mechanisms of P2X7 receptor-mediated ERK1/2 phosphorylation in human astrocytoma cells Am. J. Physiol. Renal Physiol. 284 2003 C571 C581
57. J.A. Bartos, J.D. Ulrich, H. Li, M.A. Beazely, Y. Chen, J.F. Macdonald, and J.W. Hell Postsynaptic clustering and activation of Pyk2 by PSD-95 J. Neurosci. 30 2010 449 463
58. I. Dikic, G. Tokiwa, S. Lev, S.A. Courtneidge, and J. Schlessinger A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation Nature 383 1996 547 550 (Pubitemid 26346184)
59. B.H. Shah, and K.J. Catt Calcium-independent activation of extracellularly regulated kinases 1 and 2 by angiotensin II in hepatic C9 cells: roles of protein kinase C delta, Src/proline-rich tyrosine kinase 2, and epidermal growth receptor trans-activation Mol. Pharmacol. 61 2002 343 351 (Pubitemid 34112809)
60. P.M. Dang, A. Stensballe, T. Boussetta, H. Raad, C. Dewas, Y. Kroviarski, G. Hayem, O.N. Jensen, M.A. Gougerot-Pocidalo, and J. El-Benna A specific p47phox-serine phosphorylated by convergent MAPKs mediates neutrophil NADPH oxidase priming at inflammatory sites J. Clin. Invest. 116 2006 2033 2043 (Pubitemid 44033327)
61. C. Dewas, M.A. Gougerot-Pocidalo, and J. El-Benna The mitogen-activated protein kinase extracellular signal-regulated kinase 1/2 pathway is involved in formyl-methionyl-leucyl-phenylalanine-Induced p47phox phosphorylation in human neutrophils J. Immunol. 165 2000 5238 5244
62. A. Fontayne, P.M. Dang, M.A. Gougerot-Pocidalo, and J. El-Benna Phosphorylation of p47phox sites by PKC alpha, beta II, delta, and zeta: effect on binding to p22phox and on NADPH oxidase activation Biochemistry 41 2002 7743 7750 (Pubitemid 34627801)
63. L. Stefano, O.G. Rössler, D. Griesemer, M. Hoth, and G. Thiel P2X(7) receptor stimulation upregulates Egr-1 biosynthesis involving a cytosolic Ca(2 +) rise, transactivation of the EGF receptor and phosphorylation of ERK and Elk-1 J. Cell. Physiol. 213 2007 36 44 (Pubitemid 47378790)
64. C.E. Gargett, E.J. Cornish, and J.S. Wiley Phospholipase D activation by P2Z-purinoceptor agonists in human lymphocytes is dependent on bivalent cation influx Biochem. J. 313 1996 529 535
65. C. El-Moatassim, and G.R. Dubyak A novel pathway for the activation of phospholipase D by P2z purinergic receptors in BAC1.2F5 macrophages J. Biol. Chem. 267 1992 23664 23673 (Pubitemid 23088170)
66. R.M. Touyz, and E.L. Schiffrin Ang II-stimulated superoxide production is mediated via phospholipase D in human vascular smooth muscle cells Hypertension 34 1999 976 982 (Pubitemid 29501333)
67. M. El Ouaaliti, M.M. Seil, and J.P. Dehaye Activation of calcium-insensitive phospholipase A(2) (iPLA(2)) by P2X(7) receptors in murine peritoneal macrophages Prostaglandins Other Lipid Mediat. 99 2012 116 123
68. G. Martel-Gallegos, M.T. Rosales-Saavedra, J.P. Reyes, G. Casas-Pruneda, C. Toro-Castillo, P. Pérez-Cornejo, and J. Arreola Human neutrophils do not express purinergic P2X7 receptors Purinergic Signal 3 2010 297 306
69. A. Utomo, X. Cullere, M. Glogauer, W. Swat, and T.N. Mayadas Vav proteins in neutrophils are required for FcgammaR-mediated signaling to Rac GTPases and nicotinamide adenine dinucleotide phosphate oxidase component p40(phox) J. Immunol. 177 2006 6388 6397 (Pubitemid 44628857)
70. J.K. Ryu, J.G. McLarnon, and J.G. Block of purinergic P2X(7) receptor is neuroprotective in an animal model of Alzheimer's disease Neuroreport 19 2008 1715 1719
71. M. Díaz-Hernandez, A. del Puerto, J.I. Díaz-Hernandez, M. Diez-Zaera, J.J. Lucas, J.J. Garrido, and M.T. Miras-Portugal Inhibition of the ATP-gated P2X7 receptor promotes axonal growth and branching in cultured hippocampal neurons J. Cell Sci. 121 2008 3717 3728
72. M.P. Kuehnel, V. Rybin, P.K. Anand, E. Anes, and G. Griffiths Lipids regulate P2X7-receptor-dependent actin assembly by phagosomes via ADP translocation and ATP synthesis in the phagosome lumen J. Cell Sci. 122 2009 499 504
73. I.P. Fairbairn, C.B. Stober, D.S. Kumararatne, and D.A. Lammas ATP-mediated killing of intracellular mycobacteria by macrophages is a P2X7-dependent process inducing bacterial death by phagosome-lysosome fusion J. Immunol. 167 2001 3300 3307 (Pubitemid 32852571)
74. R. Coutinho-Silva, G. Correa, A.A. Sater, and D.M. Ojcius The P2X7 receptor and intracellular pathogens: a continuing struggle Purinergic Signal 5 2009 197 204