P2X7 receptors mediate resistance to toxin-induced cell lysis

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 5, 2014, Pages 915-922

  Schoenauer, Roman ^a   Atanassoff, Alexander P ^a   Wolfmeier, Heidi ^a   Pelegrin, Pablo ^b   Babiychuk, Eduard B ^a   Draeger, Annette ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b HOSPITAL UNIVERSITARIO VIRGEN DE LA ARRIXACA   (Spain)

Author keywords

Annexin; Blebbing; Calcium; Lysis; P2X7; Plasmalemma

Indexed keywords

ANNEXIN; BLEBBING; CALCIUM; LYSIS; P2X7; PLASMALEMMA;

BACTERIAL PROTEINS; BASE SEQUENCE; BLOTTING, WESTERN; CELL LINE; DNA PRIMERS; HUMANS; POLYMERASE CHAIN REACTION; RECEPTORS, PURINERGIC P2X7; STREPTOLYSINS;

EID: 84894373879     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.01.024     Document Type: Article

References (70)

1. Morgan B.P., Luzio J.P., Campbell A.K. Intracellular Ca2+ and cell injury: a paradoxical role of Ca2+ in complement membrane attack. Cell Calcium 1986, 7:399-411.
2. 2+ and proteolysis in lethal oxidative injury in endothelial cells. Am. J. Physiol. 1991, 261:C889-C896.
3. Parker M.W., Feil S.C. Pore-forming protein toxins: from structure to function. Prog. Biophys. Mol. Biol. 2005, 88:91-142.
4. Gonzalez M.R., Bischofberger M., Pernot L., van der Goot F.G., Freche B. Bacterial pore-forming toxins: the (w)hole story?. Cell. Mol. Life Sci. 2008, 65:493-507.
5. McNeil P.L., Steinhardt R.A. Plasma membrane disruption: repair, prevention, adaptation. Annu. Rev. Cell Dev. Biol. 2003, 19:697-731.
6. Eddleman C.S., Ballinger M.L., Smyers M.E., Godell C.M., Fishman H.M., Bittner G.D. Repair of plasmalemmal lesions by vesicles. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:4745-4750.
7. McNeil P.L., Kirchhausen T. An emergency response team for membrane repair. Nat. Rev. Mol. Cell Biol. 2005, 6:499-505.
8. Babiychuk E.B., Monastyrskaya K., Potez S., Draeger A. Intracellular Ca(2+) operates a switch between repair and lysis of streptolysin O-perforated cells. Cell Death Differ. 2009, 16:1126-1134.
9. Gerke V., Moss S.E. Annexins and membrane dynamics. Biochim. Biophys. Acta 1997, 1357:129-154.
10. Gerke V., Moss S.E. Annexins: from structure to function. Physiol. Rev. 2002, 82:331-371.
11. Monastyrskaya K., Babiychuk E.B., Hostettler A., Rescher U., Draeger A. Annexins as intracellular calcium sensors. Cell Calcium 2007, 41:207-219.
12. Bouter A., Gounou C., Berat R., Tan S., Gallois B., Granier T., d'Estaintot B.L., Poschl E., Brachvogel B., Brisson A.R. Annexin-A5 assembled into two-dimensional arrays promotes cell membrane repair. Nat. Commun. 2011, 2:270.
13. Draeger A., Monastyrskaya K., Babiychuk E.B. Plasma membrane repair and cellular damage control: the annexin survival kit. Biochem. Pharmacol. 2011, 81:703-712.
14. 2+ is mediated by the activation of a non-lysosomal proteolytic system. FEBS Lett. 1986, 209:139-144.
15. Babiychuk E.B., Monastyrskaya K., Potez S., Draeger A. Blebbing confers resistance against cell lysis. Cell Death Differ. 2011, 18:80-89.
16. Virginio C., MacKenzie A., Rassendren F.A., North R.A., Surprenant A. Pore dilation of neuronal P2X receptor channels. Nat. Neurosci. 1999, 2:315-321.
17. Kawate T., Michel J.C., Birdsong W.T., Gouaux E. Crystal structure of the ATP-gated P2X(4) ion channel in the closed state. Nature 2009, 460:592-598.
18. Gu B.J., Rathsam C., Stokes L., McGeachie A.B., Wiley J.S. Extracellular ATP dissociates nonmuscle myosin from P2X(7) complex: this dissociation regulates P2X(7) pore formation. Am. J. Physiol. Cell Physiol. 2009, 297:C430-C439.
19. Kim M., Jiang L.H., Wilson H.L., North R.A., Surprenant A. Proteomic and functional evidence for a P2X7 receptor signalling complex. EMBO J. 2001, 20:6347-6358.
20. North R.A. Molecular physiology of P2X receptors. Physiol. Rev. 2002, 82:1013-1067.
21. Virginio C., MacKenzie A., North R.A., Surprenant A. Kinetics of cell lysis, dye uptake and permeability changes in cells expressing the rat P2X7 receptor. J. Physiol. 1999, 519(Pt 2):335-346.
22. Pelegrin P., Surprenant A. The P2X(7) receptor-pannexin connection to dye uptake and IL-1beta release. Purinergic Signal 2009, 5:129-137.
23. Cheewatrakoolpong B., Gilchrest H., Anthes J.C., Greenfeder S. Identification and characterization of splice variants of the human P2X7 ATP channel. Biochem. Biophys. Res. Commun. 2005, 332:17-27.
24. Solle M., Labasi J., Perregaux D.G., Stam E., Petrushova N., Koller B.H., Griffiths R.J., Gabel C.A. Altered cytokine production in mice lacking P2X(7) receptors. J. Biol. Chem. 2001, 276:125-132.
25. Ferrari D., Pizzirani C., Adinolfi E., Lemoli R.M., Curti A., Idzko M., Panther E., Di Virgilio F. The P2X7 receptor: a key player in IL-1 processing and release. J. Immunol. 2006, 176:3877-3883.
26. Perregaux D.G., McNiff P., Laliberte R., Conklyn M., Gabel C.A. ATP acts as an agonist to promote stimulus-induced secretion of IL-1 beta and IL-18 in human blood. J. Immunol. 2000, 165:4615-4623.
27. Piccini A., Carta S., Tassi S., Lasiglie D., Fossati G., Rubartelli A. ATP is released by monocytes stimulated with pathogen-sensing receptor ligands and induces IL-1beta and IL-18 secretion in an autocrine way. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:8067-8072.
28. Wilson H.L., Wilson S.A., Surprenant A., North R.A. Epithelial membrane proteins induce membrane blebbing and interact with the P2X7 receptor C terminus. J. Biol. Chem. 2002, 277:34017-34023.
29. Verhoef P.A., Estacion M., Schilling W., Dubyak G.R. P2X7 receptor-dependent blebbing and the activation of Rho-effector kinases, caspases, and IL-1 beta release. J. Immunol. 2003, 170:5728-5738.
30. MacKenzie A., Wilson H.L., Kiss-Toth E., Dower S.K., North R.A., Surprenant A. Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity 2001, 15:825-835.
31. Qu Y., Franchi L., Nunez G., Dubyak G.R. Nonclassical IL-1 beta secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J. Immunol. 2007, 179:1913-1925.
32. Chiozzi P., Sanz J.M., Ferrari D., Falzoni S., Aleotti A., Buell G.N., Collo G., Di Virgilio F. Spontaneous cell fusion in macrophage cultures expressing high levels of the P2Z/P2X7 receptor. J. Cell Biol. 1997, 138:697-706.
33. Baricordi O.R., Melchiorri L., Adinolfi E., Falzoni S., Chiozzi P., Buell G., Di Virgilio F. Increased proliferation rate of lymphoid cells transfected with the P2X(7) ATP receptor. J. Biol. Chem. 1999, 274:33206-33208.
34. Ferrari D., Chiozzi P., Falzoni S., Dal Susino M., Collo G., Buell G., Di Virgilio F. ATP-mediated cytotoxicity in microglial cells. Neuropharmacology 1997, 36:1295-1301.
35. Gu B.J., Saunders B.M., Jursik C., Wiley J.S. The P2X7-nonmuscle myosin membrane complex regulates phagocytosis of nonopsonized particles and bacteria by a pathway attenuated by extracellular ATP. Blood 2010, 115:1621-1631.
36. Wiley J.S., Gu B.J. A new role for the P2X7 receptor: a scavenger receptor for bacteria and apoptotic cells in the absence of serum and extracellular ATP. Purinergic Signal 2012, 8:579-586.
37. Surprenant A., Rassendren F., Kawashima E., North R.A., Buell G. The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 1996, 272:735-738.
38. Humphreys B.D., Virginio C., Surprenant A., Rice J., Dubyak G.R. Isoquinolines as antagonists of the P2X7 nucleotide receptor: high selectivity for the human versus rat receptor homologues. Mol. Pharmacol. 1998, 54:22-32.
39. Hollins F., Kaur D., Yang W., Cruse G., Saunders R., Sutcliffe A., Berger P., Ito A., Brightling C.E., Bradding P. Human airway smooth muscle promotes human lung mast cell survival, proliferation, and constitutive activation: cooperative roles for CADM1, stem cell factor, and IL-6. J. Immunol. 2008, 181:2772-2780.
40. Al-Nasiry S., Geusens N., Hanssens M., Luyten C., Pijnenborg R. The use of Alamar Blue assay for quantitative analysis of viability, migration and invasion of choriocarcinoma cells. Hum. Reprod. 2007, 22:1304-1309.
41. Rescher U., Zobiack N., Gerke V. Intact Ca(2+)-binding sites are required for targeting of annexin 1 to endosomal membranes in living HeLa cells. J. Cell Sci. 2000, 113(Pt 22):3931-3938.
42. Draeger A., Wray S., Babiychuk E.B. Domain architecture of the smooth-muscle plasma membrane: regulation by annexins. Biochem. J. 2005, 387:309-314.
43. Ballerini P., Rathbone M.P., Di Iorio P., Renzetti A., Giuliani P., D'Alimonte I., Trubiani O., Caciagli F., Ciccarelli R. Rat astroglial P2Z (P2X7) receptors regulate intracellular calcium and purine release. Neuroreport 1996, 7:2533-2537.
44. Morelli A., Chiozzi P., Chiesa A., Ferrari D., Sanz J.M., Falzoni S., Pinton P., Rizzuto R., Olson M.F., Di Virgilio F. Extracellular ATP causes ROCK I-dependent bleb formation in P2X7-transfected HEK293 cells. Mol. Biol. Cell 2003, 14:2655-2664.
45. Young M.T., Pelegrin P., Surprenant A. Amino acid residues in the P2X7 receptor that mediate differential sensitivity to ATP and BzATP. Mol. Pharmacol. 2007, 71:92-100.
46. Charras G., Paluch E. Blebs lead the way: how to migrate without lamellipodia. Nat. Rev. Mol. Cell Biol. 2008, 9:730-736.
47. 2+ content of the endoplasmic reticulum, activates NFATc1, and protects from apoptosis. J. Biol. Chem. 2009, 284:10120-10128.
48. Straight A.F., Cheung A., Limouze J., Chen I., Westwood N.J., Sellers J.R., Mitchison T.J. Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 2003, 299:1743-1747.
49. Donnelly-Roberts D.L., Jarvis M.F. Discovery of P2X7 receptor-selective antagonists offers new insights into P2X7 receptor function and indicates a role in chronic pain states. Br. J. Pharmacol. 2007, 151:571-579.
50. Schulman E.S., Glaum M.C., Post T., Wang Y., Raible D.G., Mohanty J., Butterfield J.H., Pelleg A. ATP modulates anti-IgE-induced release of histamine from human lung mast cells. Am. J. Respir. Cell Mol. Biol. 1999, 20:530-537.
51. Sanz J.M., Di Virgilio F. Kinetics and mechanism of ATP-dependent IL-1 beta release from microglial cells. J. Immunol. 2000, 164:4893-4898.
52. Al-Shukaili A., Al-Kaabi J., Hassan B. A comparative study of interleukin-1beta production and p2x7 expression after ATP stimulation by peripheral blood mononuclear cells isolated from rheumatoid arthritis patients and normal healthy controls. Inflammation 2008, 31:84-90.
53. Wiley J.S., Sluyter R., Gu B.J., Stokes L., Fuller S.J. The human P2X7 receptor and its role in innate immunity. Tissue Antigens 2011, 78:321-332.
54. Labasi J.M., Petrushova N., Donovan C., McCurdy S., Lira P., Payette M.M., Brissette W., Wicks J.R., Audoly L., Gabel C.A. Absence of the P2X7 receptor alters leukocyte function and attenuates an inflammatory response. J. Immunol. 2002, 168:6436-6445.
55. Schwiebert E.M. ABC transporter-facilitated ATP conductive transport. Am. J. Physiol. 1999, 276:C1-C8.
56. 2+ response mediated by P2U and P2Y purinoceptors in human macrophages: signalling from dying cells to macrophages. Immunology 1999, 98:220-227.
57. Beigi R., Kobatake E., Aizawa M., Dubyak G.R. Detection of local ATP release from activated platelets using cell surface-attached firefly luciferase. Am. J. Physiol. 1999, 276:C267-C278.
58. Wilhelm K., Ganesan J., Muller T., Durr C., Grimm M., Beilhack A., Krempl C.D., Sorichter S., Gerlach U.V., Juttner E., Zerweck A., Gartner F., Pellegatti P., Di Virgilio F., Ferrari D., Kambham N., Fisch P., Finke J., Idzko M., Zeiser R. Graft-versus-host disease is enhanced by extracellular ATP activating P2X7R. Nat. Med. 2010, 16:1434-1438.
59. Coutinho-Silva R., Stahl L., Raymond M.N., Jungas T., Verbeke P., Burnstock G., Darville T., Ojcius D.M. Inhibition of chlamydial infectious activity due to P2X7R-dependent phospholipase D activation. Immunity 2003, 19:403-412.
60. Lees M.P., Fuller S.J., McLeod R., Boulter N.R., Miller C.M., Zakrzewski A.M., Mui E.J., Witola W.H., Coyne J.J., Hargrave A.C., Jamieson S.E., Blackwell J.M., Wiley J.S., Smith N.C. P2X7 receptor-mediated killing of an intracellular parasite, Toxoplasma gondii, by human and murine macrophages. J. Immunol. 2010, 184:7040-7046.
61. 2+-dependent endocytosis. J. Cell Biol. 2008, 180:905-914.
62. Piccin A., Murphy W.G., Smith O.P. Circulating microparticles: pathophysiology and clinical implications. Blood Rev. 2007, 21:157-171.
63. Qu Y., Dubyak G.R. P2X7 receptors regulate multiple types of membrane trafficking responses and non-classical secretion pathways. Purinergic Signal 2009, 5:163-173.
64. Segundo C., Medina F., Rodriguez C., Martinez-Palencia R., Leyva-Cobian F., Brieva J.A. Surface molecule loss and bleb formation by human germinal center B cells undergoing apoptosis: role of apoptotic blebs in monocyte chemotaxis. Blood 1999, 94:1012-1020.
65. Charras G.T. A short history of blebbing. J. Microsc. 2008, 231:466-478.
66. Fackler O.T., Grosse R. Cell motility through plasma membrane blebbing. J. Cell Biol. 2008, 181:879-884.
67. McNeil A.K., Rescher U., Gerke V., McNeil P.L. Requirement for annexin A1 in plasma membrane repair. J. Biol. Chem. 2006, 281:35202-35207.
68. Raynal P., Pollard H.B. Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins. Biochim. Biophys. Acta 1994, 1197:63-93.
69. Rosengarth A., Luecke H. A calcium-driven conformational switch of the N-terminal and core domains of annexin A1. J. Mol. Biol. 2003, 326:1317-1325.
70. Collo G., Neidhart S., Kawashima E., Kosco-Vilbois M., North R.A., Buell G. Tissue distribution of the P2X7 receptor. Neuropharmacology 1997, 36:1277-1283.