P2X7 receptor activation induces reactive oxygen species formation in erythroid cells

Purinergic Signalling

Volumn 9, Issue 1, 2013, Pages 101-112

  Wang, Bin ^a,b,c   Sluyter, Ronald ^a,b  

^a UNIVERSITY OF WOLLONGONG   (Australia)

^b ILLAWARRA HEALTH AND MEDICAL RESEARCH INSTITUTE   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Apoptosis; Extracellular ATP; P2X7; Reactive oxygen species; Red blood cell

Indexed keywords

3 [[5 (2, 3 DICHLOROPHENYL) 1H TETRAZOL 1 YL] METHYL] PYRIDINE; 4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL) IMIDAZOLE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL) IMIDAZOLE; ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATE; CALCIUM ION; CASPASE; CASPASE INHIBITOR; DIPHENYLIODONIUM SALT; MAGNESIUM ION; MITOGEN ACTIVATED PROTEIN KINASE P38; PURINERGIC P2X7 RECEPTOR; REACTIVE OXYGEN METABOLITE; SCAVENGER; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ERYTHROID CELL; ERYTHROLEUKEMIA CELL; FLOW CYTOMETRY; NONHUMAN; RECEPTOR DOWN REGULATION;

EID: 84873745869     PISSN: 15739538     EISSN: 15739546     Source Type: Journal    
DOI: 10.1007/s11302-012-9335-2     Document Type: Article

References (61)

1. Kaczmarek-Hájek K, Lörinczi E, Hausmann R, Nicke A (2012) Molecular and functional properties of P2X receptors-recent progress and persisting challenges. Purinergic Signal 8: 375-417.
2. Wiley JS, Sluyter R, Gu BJ, Stokes L, Fuller SJ (2011) The human P2X7 receptor and its role in innate immunity. Tissue Antigens 78: 321-332.
3. Lenertz L, Gavala M, Zhu Y, Bertics P (2011) Transcriptional control mechanisms associated with the nucleotide receptor P2X7, a critical regulator of immunologic, osteogenic, and neurologic functions. Immunol Res 50: 22-38.
4. Sluyter R, Stokes L (2011) Significance of P2X7 receptor variants to human health and disease. Recent Pat DNA Gene Seq 5: 41-54.
5. 7 receptor-mediated reactive oxygen and nitrogen species formation: from receptor to generators. Biochem Soc Trans 35: 1168-1170.
6. Ferrari D, Wesselborg S, Bauer MK, Schulze-Osthoff K (1997) Extracellular ATP activates transcription factor NF-kappaB through the P2Z purinoreceptor by selectively targeting NF-kappaB p65. J Cell Biol 139: 1635-1643.
7. Cruz CM, Rinna A, Forman HJ, Ventura ALM, Persechini PM, Ojcius DM (2007) ATP activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages. J Biol Chem 282: 2871-2879.
8. Hewinson J, Moore SF, Glover C, Watts AG, MacKenzie AB (2008) A key role for redox signaling in rapid P2X7 receptor-induced IL-1β processing in human monocytes. J Immunol 180: 8410-8420.
9. Corrêa G, Marques da Silva C, de Abreu Moreira-Souza AC, Vommaro RC, Coutinho-Silva R (2010) Activation of the P2X7 receptor triggers the elimination of Toxoplasma gondii tachyzoites from infected macrophages. Microbes Infect 12: 497-504.
10. Noguchi T, Ishii K, Fukutomi H, Naguro I, Matsuzawa A, Takeda K, Ichijo H (2008) Requirement of reactive oxygen species-dependent activation of ASK1-p38 MAPK pathway for extracellular ATP-induced apoptosis in macrophage. J Biol Chem 283: 7657-7665.
11. Moore SF, MacKenzie AB (2009) NADPH oxidase NOX2 mediates rapid cellular oxidation following ATP stimulation of endotoxin-primed macrophages. J Immunol 183: 3302-3308.
12. Kawano A, Tsukimoto M, Mori D, Noguchi T, Harada H, Takenouchi T, Kitani H, Kojima S (2012) Regulation of P2X7-dependent inflammatory functions by P2X4 receptor in mouse macrophages. Biochem Biophys Res Commun 420: 102-107.
13. Sluyter R, Shemon AN, Barden JA, Wiley JS (2004) Extracellular ATP increases cation fluxes in human erythrocytes by activation of the P2X7 receptor. J Biol Chem 279: 44749-44755.
14. 13 receptors is a negative feedback pathway for ATP release from human red blood cells. Circ Res 96: 189-196.
15. Parker JC, Snow RL (1972) Influence of external ATP on permeability and metabolism of dog red blood cells. Am J Physiol 223: 888-893.
16. Sluyter R, Shemon AN, Hughes WE, Stevenson RO, Georgiou JG, Eslick GD, Taylor RM, Wiley JS (2007) Canine erythrocytes express the P2X7 receptor: greatly increased function compared with human erythrocytes. Am J Physiol Regul Integr Comp Physiol 293: R2090-R2098.
17. Stevenson RO, Taylor RM, Wiley JS, Sluyter R (2009) The P2X7 receptor mediates the uptake of organic cations in canine erythrocytes and mononuclear leukocytes: comparison to equivalent human cell types. Purinergic Signal 5: 385-394.
18. Skals M, Jorgensenb NR, Leipzigera J, Praetoriusa HA (2009) α-Hemolysin from Escherichia coli uses endogenous amplification through P2X receptor activation to induce hemolysis. Proc Natl Acad Sci USA 106: 4030-4035.
19. Skals M, Leipziger J, Praetorius H (2011) Haemolysis induced by α-toxin from Staphylococcus aureus requires P2X receptor activation. Pflugers Arch 462: 669-679.
20. Sluyter R, Shemon AN, Wiley JS (2007) P2X7 receptor activation causes phosphatidylserine exposure in human erythrocytes. Biochem Biophys Res Commun 355: 169-173.
21. Jiang H, Zhu AG, Mamczur M, Falck JR, Lerea KM, McGiff JC (2007) Stimulation of rat erythrocyte P2X7 receptor induces the release of epoxyeicosatrienoic acids. Br J Pharmacol 151: 1033-1040.
22. Chahwala SB, Cantley LC (1984) Extracellular ATP induces ion fluxes and inhibits growth of Friend erythroleukemia cells. J Biol Chem 259: 13717-13722.
23. Constantinescu P, Wang B, Kovacevic K, Jalilian I, Bosman GJCGM, Wiley JS, Sluyter R (2010) P2X7 receptor activation induces cell death and microparticle release in murine erythroleukemia cells. Biochim Biophys Acta 1798: 1797-1804.
24. Marks PW, Maxfield FR (1991) Preparation of solutions with free calcium concentration in the nanomolar range using 1, 2-bis(o-aminophenoxy)ethane-N, N, N′, N′-tetraacetic acid. Anal Biochem 193: 61-71.
25. Donnelly-Roberts DL, Namovic MT, Han P, Jarvis MF (2009) Mammalian P2X7 receptor pharmacology: comparison of recombinant mouse, rat and human P2X7 receptors. Br J Pharmacol 157: 1203-1214.
26. Bianchi BR, Lynch KJ, Touma E, Niforatos W, Burgard EC, Alexander KM, Park HS, Yu H, Metzger R, Kowaluk EC, Jarvis MF, van Biesen T (1999) Pharmacological characterization of recombinant human and rat P2X7 receptor subtypes. Eur J Pharmacol 376: 127-138.
27. 5 receptor. Mol Pharmacol 63: 1407-1416.
28. Acuña-Castillo C, Coddou C, Bull P, Brito J, Huidobro-Toro JP (2007) Differential role of extracellular histidines in copper, zinc, magnesium and proton modulation of the P2X7 purinergic receptor. J Neurochem 101: 17-26.
29. Yan Z, Khadra A, Sherman A, Stojilkovic S (2011) Calcium-dependent block of P2X7 receptor channel function is allosteric. J Gen Physiol 138: 437-452.
30. Fontanils U, Seil M, Pochet S, El Ouaaliti M, Garcia-Marcos M, Dehaye JP, Marino A (2010) Stimulation by P2X7 receptors of calcium-dependent production of reactive oxygen species (ROS) in rat submandibular glands. Biochim Biophys Acta 1800: 1183-1191.
31. Seil M, Fontanils U, Etxebarria I, Pochet S, Garcia-Marcos M, Marino A, Dehaye J-P (2008) Pharmacological evidence for the stimulation of NADPH oxidase by P2X7 receptors in mouse submandibular glands. Purinergic Signal 4: 347-355.
32. Martinon F, Mayor A, Tschopp J (2009) The inflammasomes: guardians of the body. Annu Rev Immunol 27: 229-265.
33. Donnelly-Roberts DL, Namovic MT, Faltynek CR, Jarvis MF (2004) Mitogen-activated protein kinase and caspase signaling pathways are required for P2X7 receptor (P2X7R)-induced pore formation in human THP-1 cells. J Pharmacol Exp Ther 308: 1053-1061.
34. Faria RX, Defarias FP, Alves LA (2005) Are second messengers crucial for opening the pore associated with P2X7 receptor? Am J Physiol Cell Physiol 288: C260-C271.
35. Lenertz L, Gavala M, Hill L, Bertics P (2009) Cell signaling via the P2X7 nucleotide receptor: linkage to ROS production, gene transcription, and receptor trafficking. Purinergic Signal 5: 175-187.
36. Harada H, Tsukimoto M, Ikari A, Takagi K, Suketa Y (2003) P2X7 receptor-induced generation of reactive oxygen species in rat mesangial cells. Drug Dev Res 59: 112-117.
37. Koopman WJ, Nijtmans LG, Dieteren CE, Roestenberg P, Valsecchi F, Smeitink JA, Willems PH (2010) Mammalian mitochondrial complex I: biogenesis, regulation, and reactive oxygen species generation. Antioxid Redox Signal 12: 1431-1470.
38. Li Y, Trush M (1998) Diphenyleneiodonium, an NAD(P)H oxidase inhibitor, also potently inhibits mitochondrial reactive oxygen species production. Biochem Biophys Res Commun 253: 295-299.
39. Valko M, Leibfritz DMJ, Cronin MTD, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39: 44-84.
40. Hamanaka RB, Chandel NS (2010) Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes. Trends Biochem Sci 35: 505-513.
41. Ghaffari S (2008) Oxidative stress in the regulation of normal and neoplastic hematopoiesis. Antioxid Redox Signal 10: 1923-1940.
42. Dana M, Prus E, Fibach E (2012) Thalassemic DNA-containing red blood cells are under oxidative stress. Anemia 2012: 943974.
43. 7 receptors. Am J Physiol Cell Physiol 289: C1295-C1302.
44. Courageot M-P, Lepine S, Hours M, Giraud F, Sulpice J-C (2004) Involvement of sodium in ealry phophatidylserine exposure and phosolipid scrambling induced by P2X7 purinoceptor activation in thymocytes. J Biol Chem 279: 21815-21823.
45. Garcia-Marcos M, Fontanils U, Aguirre A, Pochet S, Dehaye JP, Marino A (2005) Role of sodium in mitochondrial membrane depolarization induced by P2X7 receptor activation in submandibular glands. FEBS Lett 579: 5407-5413.
46. 7 receptor. Neuropharmacology 36: 1285-1294.
47. Cankurtaran-Sayar S, Sayar K, Ugur M (2009) P2X7 receptor activates multiple selective dye-permeation pathways in RAW 264. 7 and human embryonic kidney 293 cells. Mol Pharmacol 76: 1323-1332.
48. Yamaguchi T, Hashiguchi K, Katsuki S, Iwamoto W, Tsuruhara S, Terada S (2008) Activation of the intrinsic and extrinsic pathways in high pressure-induced apoptosis of murine erythroleukemia cells. Cell Mol Biol Lett 13: 49-57.
49. Take J, Yamaguchi T, Mine N, Terada S (2001) Caspase activation in high-pressure-induced apoptosis of murine erythroleukemia cells. Jpn J Physiol 51: 193-199.
50. Labasi JM, Petrushova N, Donovan C, McCurdy S, Lira P, Payette MM, Brissette W, Wicks JR, Audoly L, Gabel CA (2002) Absence of the P2X7 receptor alters leukocyte function and attenuates an inflammatory response. J Immunol 168: 6436-6445.
51. Chessell IP, Hatcher JP, Bountra C, Michel AD, Hughes JP, Green P, Egerton J, Murfin M, Richardson J, Peck WL, Grahames CBA, Casula MA, Yiangou Y, Birch R, Anand P, Buell GN (2005) Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 114: 386-396.
52. Ke HZ, Qi H, Weidema AF, Zhang Q, Panupinthu N, Crawford DT, Grasser WA, Paralkar VM, Li M, Audoly LP, Gabel CA, Jee WSS, Dixon SJ, Sims SM, Thompson DD (2003) Deletion of the P2X7 nucleotide receptor reveals its regulatory roles in bone formation and resorption. Mol Endocrinol 17: 1356-1367.
53. Frascoli M, Marcandalli J, Schenk U, Grassi F (2012) Purinergic P2X7 receptor drives T cell lineage choice and shapes peripheral γδ cells. J Immunol 189: 174-180.
54. Testa U (2004) Apoptotic mechanisms in the control of erythropoiesis. Leukemia 18: 1176-1199.
55. Nagata S (2007) Autoimmune diseases caused by defects in clearing dead cells and nuclei expelled from erythroid precursors. Immunol Rev 220: 237-250.
56. Martins I, Tesniere A, Kepp O, Michaud M, Schlemmer F, Senovilla L, Seror C, Metivier D, Perfettini JL, Zitvogel L, Kroemer G (2009) Chemotherapy induces ATP release from tumor cells. Cell Cycle 8: 3723-3728.
57. Groopman JE, Itri LM (1999) Chemotherapy-induced anemia in adults: incidence and treatment. J Natl Cancer Inst 91: 1616-1634.
58. 7 receptor. Br J Pharmacol 142: 1015-1019.
59. Shemon AN, Sluyter R, Stokes L, Manley PW, Wiley JS (2008) Inhibiton of the human P2X7 receptor by a novel protein tyrosine kinase antagonist. Biochem Biophys Res Commun 365: 515-520.
60. 7 receptor stimulated phospholipase D activity in chronic lymphocytic leukaemia B-lymphocytes. Immunol Cell Biol 85: 68-72.
61. Michel AD, Thompson KM, Simon J, Boyfield I, Fonfria E, Humphrey PPA (2006) Species and response dependent differences in the effects of MAPK inhibitors on P2X7 receptor function. Br J Pharmacol 149: 948-957.