P2X7 on mouse T cells: One channel, many functions

Frontiers in Immunology

Volumn 6, Issue MAY, 2015, Pages

  Rissiek, Björn ^a   Haag, Friedrich ^a   Boyer, Olivier ^b,c,d   Koch Nolte, Friedrich ^a   Adriouch, Sahil ^b,c  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b INSERM   (France)

^c UNIVERSITY OF ROUEN   (France)

^d ROUEN UNIVERSITY HOSPITAL   (France)

Author keywords

ATP; P2RX7; P2X7; Purinergic signaling; T cells

Indexed keywords

ADENOSINE TRIPHOSPHATE; CD27 ANTIGEN; CD38 ANTIGEN; CD39 ANTIGEN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; L SELECTIN; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE; PANNEXIN 1; PEPTIDES AND PROTEINS; PURINERGIC P2X7 RECEPTOR; UNCLASSIFIED DRUG;

AUTOCRINE EFFECT; CELL DEATH; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL MEMBRANE; GENETIC VARIABILITY; HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; INFLAMMATION; NONHUMAN; PROTEIN EXPRESSION; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TRANS SPLICING;

EID: 84934291898     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00204     Document Type: Review

References (80)

1. Bartlett R, Stokes L, Sluyter R. The P2X7 receptor channel: recent developments and the use of P2X7 antagonists in models of disease. Pharmacol Rev (2014) 66:638-75. doi:10.1124/pr.113.008003
2. Seman M, Adriouch S, Scheuplein F, Krebs C, Freese D, Glowacki G, et al. NAD-induced T cell death: ADP-ribosylation of cell surface proteins by ART2 activates the cytolytic P2X7 purinoceptor. Immunity (2003) 19:571-82. doi:10.1016/S1074-7613(03)00266-8
3. Adriouch S, Bannas P, Schwarz N, Fliegert R, Guse AH, Seman M, et al. ADP-ribosylation at R125 gates the P2X7 ion channel by presenting a covalent ligand to its nucleotide binding site. FASEB J (2007) 22:861-9. doi:10.1096/fj.07-9294com
4. Scheuplein F, Schwarz N, Adriouch S, Krebs C, Bannas P, Rissiek B, et al. NAD+ and ATP released from injured cells induce P2X7-dependent shedding of CD62L and externalization of phosphatidylserine by murine T cells. J Immunol (2009) 182:2898-908. doi:10.4049/jimmunol.0801711
5. Hubert S, Rissiek B, Klages K, Huehn J, Sparwasser T, Haag F, et al. Extracellular NAD+ shapes the Foxp3+ regulatory T cell compartment through the ART2-P2X7 pathway. J Exp Med (2010) 207:2561-8. doi:10.1084/jem.20091154
6. Rissiek B, Danquah W, Haag F, Koch-Nolte F. Technical advance: a new cell preparation strategy that greatly improves the yield of vital and functional Tregs and NKT cells. J Leukoc Biol (2014) 95:543-9. doi:10.1189/jlb.0713407
7. Haag F, Koch-Nolte F, Kühl M, Lorenzen S, Thiele HG. Premature stop codons inactivate the RT6 genes of the human and chimpanzee species. J Mol Biol (1994) 243:537-46. doi:10.1006/jmbi.1994.1680
8. Schwarz N, Fliegert R, Adriouch S, Seman M, Guse AH, Haag F, et al. Activation of the P2X7 ion channel by soluble and covalently bound ligands. Purinergic Signal (2009) 5:139-49. doi:10.1007/s11302-009-9135-5
9. Lévesque SA, Kukulski F, Enjyoji K, Robson SC, Sévigny J. NTPDase1 governs P2X7-dependent functions in murine macrophages. Eur J Immunol (2010) 40:1473-85. doi:10.1002/eji.200939741
10. Kuhny M, Hochdörfer T, Ayata CK, Idzko M, Huber M. CD39 is a negative regulator of P2X7-mediated inflammatory cell death in mast cells. Cell Commun Signal (2014) 12:40. doi:10.1186/s12964-014-0040-3
11. Krebs C, Adriouch S, Braasch F, Koestner W, Leiter EH, Seman M, et al. CD38 controls ADP-ribosyltransferase-2-catalyzed ADP-ribosylation of T cell surface proteins. J Immunol (2005) 174:3298-305. doi:10.4049/jimmunol.174.6.3298
12. Deaglio S, Dwyer KM, Gao W, Friedman D, Usheva A, Erat A, et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med (2007) 204:1257-65. doi:10.1084/jem.20062512
13. Magnone M, Bauer I, Poggi A, Mannino E, Sturla L, Brini M, et al. NAD+ levels control Ca2+ store replenishment and mitogen-induced increase of cytosolic Ca2+ by Cyclic ADP-ribose-dependent TRPM2 channel gating in human T lymphocytes. J Biol Chem (2012) 287:21067-81. doi:10.1074/jbc. M111.324269
14. Di Virgilio F, Boeynaems J-M, Robson SC. Extracellular nucleotides as negative modulators of immunity. Curr Opin Pharmacol (2009) 9:507-13. doi:10.1016/j.coph.2009.06.021
15. Haag F, Adriouch S, Braß A, Jung C, Möller S, Scheuplein F, et al. Extracellular NAD and ATP: partners in immune cell modulation. Purinergic Signal (2007) 3:71-81. doi:10.1007/s11302-006-9038-7
16. Aymeric L, Apetoh L, Ghiringhelli F, Tesniere A, Martins I, Kroemer G, et al. Tumor cell death and ATP release prime dendritic cells and efficient anticancer immunity. Cancer Res (2010) 70:855-8. doi:10.1158/0008-5472.CAN-09-3566
17. Garg AD, Krysko DV, Verfaillie T, Kaczmarek A, Ferreira GB, Marysael T, et al. A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death. EMBO J (2012) 31:1062-79. doi:10.1038/emboj.2011.497
18. Adriouch S, Hubert S, Pechberty S, Koch-Nolte F, Haag F, Seman M. NAD+ released during inflammation participates in T cell homeostasis by inducing ART2-mediated death of naive T cells in vivo. J Immunol (2007) 179:186-94. doi:10.4049/jimmunol.179.1.186
19. Taylor SRJ, Gonzalez-Begne M, Dewhurst S, Chimini G, Higgins CF, Melvin JE, et al. Sequential shrinkage and swelling underlie P2X7-stimulated lymphocyte phosphatidylserine exposure and death. J Immunol (2008) 180:300-8. doi:10.4049/jimmunol.180.1.300
20. Adriouch S, Ohlrogge W, Haag F, Koch-Nolte F, Seman M. Rapid induction of naive T cell apoptosis by ecto-nicotinamide adenine dinucleotide: requirement for mono(ADP-ribosyl)transferase 2 and a downstream effector. J Immunol (2001) 167:196-203. doi:10.4049/jimmunol.167.1.196
21. Courageot M-P, Lépine S, Hours M, Giraud F, Sulpice J-C. Involvement of sodium in early phosphatidylserine exposure and phospholipid scrambling induced by P2X7 purinoceptor activation in thymocytes. J Biol Chem (2004) 279:21815-23. doi:10.1074/jbc. M401426200
22. Bratton DL, Fadok VA, Richter DA, Kailey JM, Guthrie LA, Henson PM. Appearance of phosphatidylserine on apoptotic cells requires calcium-mediated nonspecific flip-flop and is enhanced by loss of the aminophospholipid translocase. J Biol Chem (1997) 272:26159-65. doi:10.1074/jbc.272.42.26159
23. Bevers EM, Williamson PL. Phospholipid scramblase: an update. FEBS Lett (2010) 584:2724-30. doi:10.1016/j.febslet.2010.03.020
24. Mackenzie AB, Young MT, Adinolfi E, Surprenant A. Pseudoapoptosis induced by brief activation of ATP-gated P2X7 receptors. J Biol Chem (2005) 280:33968-76. doi:10.1074/jbc. M502705200
25. Becker D, Woltersdorf R, Boldt W, Schmitz S, Braam U, Schmalzing G, et al. The P2X7 carboxyl tail is a regulatory module of P2X7 receptor channel activity. J Biol Chem (2008) 283:25725-34. doi:10.1074/jbc. M803855200
26. Shoji KF, Sáez PJ, Harcha PA, Aguila HL, Sáez JC. Pannexin1 channels act downstream of P2X 7 receptors in ATP-induced murine T-cell death. Channels (Austin) (2014) 8:142-56. doi:10.4161/chan.28122
27. Ousingsawat J, Wanitchakool P, Kmit A, Romao AM, Jantarajit W, Schreiber R, et al. Anoctamin 6 mediates effects essential for innate immunity downstream of P2X7 receptors in macrophages. Nat Commun (2015) 6:6245. doi:10.1038/ncomms7245
28. Gu B, Bendall LJ, Wiley JS. Adenosine triphosphate-induced shedding of CD23 and L-selectin (CD62L) from lymphocytes is mediated by the same receptor but different metalloproteases. Blood (1998) 92:946-51.
29. Moon H, Na H-Y, Chong KH, Kim TJ. P2X7 receptor-dependent ATP-induced shedding of CD27 in mouse lymphocytes. Immunol Lett (2006) 102:98-105. doi:10.1016/j.imlet.2005.08.004
30. Garbers C, Janner N, Chalaris A, Moss ML, Floss DM, Meyer D, et al. Species specificity of ADAM10 and ADAM17 proteins in interleukin-6 (IL-6) trans-signaling and novel role of ADAM10 in inducible IL-6 receptor shedding. J Biol Chem (2011) 286:14804-11. doi:10.1074/jbc. M111.229393
31. Le Stunff H, Auger R, Kanellopoulos J, Raymond M-N. The Pro-451 to Leu polymorphism within the C-terminal tail of P2X7 receptor impairs cell death but not phospholipase D activation in murine thymocytes. J Biol Chem (2004) 279:16918-26. doi:10.1074/jbc. M313064200
32. Young MT, Pelegrín P, Surprenant A. Identification of Thr283 as a key determinant of P2X7 receptor function. Br J Pharmacol (2006) 149:261-8. doi:10.1038/sj.bjp.0706880
33. Sorge RE, Trang T, Dorfman R, Smith SB, Beggs S, Ritchie J, et al. Genetically determined P2X7 receptor pore formation regulates variability in chronic pain sensitivity. Nat Med (2012) 18:595-9. doi:10.1038/nm.2710
34. Syberg S, Petersen S, Beck Jensen J-E, Gartland A, Teilmann J, Chessell I, et al. Genetic background strongly influences the bone phenotype of P2X7 receptor knockout mice. J Osteoporos (2012) 2012:391097. doi:10.1155/2012/391097
35. Sluyter R, Stokes L. Significance of P2X7 receptor variants to human health and disease. Recent Pat DNA Gene Seq (2011) 5:41-54. doi:10.2174/187221511794839219
36. Adriouch S, Dox C, Welge V, Seman M, Koch-Nolte F, Haag F. Cutting edge: a natural P451L mutation in the cytoplasmic domain impairs the function of the mouse P2X7 receptor. J Immunol (2002) 169:4108-12. doi:10.4049/jimmunol.169.8.4108
37. Nicke A, Kuan Y-H, Masin M, Rettinger J, Marquez-Klaka B, Bender O, et al. A functional P2X7 splice variant with an alternative transmembrane domain 1 escapes gene inactivation in P2X7 knock-out mice. J Biol Chem (2009) 284:25813-22. doi:10.1074/jbc. M109.033134
38. Schwarz N, Drouot L, Nicke A, Fliegert R, Boyer O, Guse AH, et al. Alternative splicing of the N-terminal cytosolic and transmembrane domains of P2X7 controls gating of the ion channel by ADP-ribosylation. PLoS One (2012) 7:e41269. doi:10.1371/journal.pone.0041269
39. Xu XJ, Boumechache M, Robinson LE, Marschall V, Górecki DC, Masin M, et al. Splice-variants of the P2X7 receptor reveal differential agonist-dependence and functional coupling with pannexin-1. J Cell Sci (2012) 125(Pt 16):3776-89. doi:10.1242/jcs.099374
40. Hong S, Schwarz N, Braß A, Seman M, Haag F, Koch-Nolte F, et al. Differential regulation of P2X7 receptor activation by extracellular nicotinamide adenine dinucleotide and ecto-ADP-ribosyltransferases in murine macrophages and T cells. J Immunol (2009) 183:578-92. doi:10.4049/jimmunol.0900120
41. Solle M, Labasi J, Perregaux DG, Stam E, Petrushova N, Koller BH, et al. Altered cytokine production in mice lacking P2X(7) receptors. J Biol Chem (2001) 276:125-32. doi:10.1074/jbc. M006781200
42. Ke HZ, Qi H, Weidema AF, Zhang Q, Panupinthu N, Crawford DT, et al. Deletion of the P2X7 nucleotide receptor reveals its regulatory roles in bone formation and resorption. Mol Endocrinol (2003) 17:1356-67. doi:10.1210/me.2003-0021
43. Chessell IP, Hatcher JP, Bountra C, Michel AD, Hughes JP, Green P, et al. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain (2005) 114:386-96. doi:10.1016/j.pain.2005.01.002
44. Sim JA, Young MT, Sung H-Y, North RA, Surprenant A. Reanalysis of P2X7 receptor expression in rodent brain. J Neurosci (2004) 24:6307-14. doi:10.1523/JNEUROSCI.1469-04.2004
45. Taylor SRJ, Gonzalez-Begne M, Sojka DK, Richardson JC, Sheardown SA, Harrison SM, et al. Lymphocytes from P2X7-deficient mice exhibit enhanced P2X7 responses. J Leukoc Biol (2009) 85:978-86. doi:10.1189/jlb.0408251
46. Sharp AJ, Polak PE, Simonini V, Lin SX, Richardson JC, Bongarzone ER, et al. P2x7 deficiency suppresses development of experimental autoimmune encephalomyelitis. J Neuroinflammation (2008) 5:33. doi:10.1186/1742-2094-5-33
47. Chen L, Brosnan CF. Exacerbation of experimental autoimmune encephalomyelitis in P2X7R-/-mice: evidence for loss of apoptotic activity in lymphocytes. J Immun (2006) 176:3115-26. doi:10.4049/jimmunol.176.5.3115
48. Freedman BD, Liu QH, Gaulton G, Kotlikoff MI, Hescheler J, Fleischmann BK. ATP-evoked Ca2+ transients and currents in murine thymocytes: possible role for P2X receptors in death by neglect. Eur J Immunol (1999) 29:1635-46. doi:10.1002/(SICI)1521-4141(199905)29:05<1635::AID-IMMU1635>3.3.CO;2-2
49. Frascoli M, Marcandalli J, Schenk U, Grassi F. Purinergic P2X7 receptor drives T cell lineage choice and shapes peripheral γδ cells. J Immunol (2012) 189:174-80. doi:10.4049/jimmunol.1101582
50. Haag F, Freese D, Scheublein F, Ohlrogge W, Adriouch S, Seman M, et al. T cells of different developmental stages differ in sensitivity to apoptosis induced by extracellular NAD. Dev Immunol (2002) 9:197-202. doi:10.1080/10446670310001593514
51. Kahl S, Nissen M, Girisch R, Duffy T, Leiter EH, Haag F, et al. Metalloprotease-mediated shedding of enzymatically active mouse ecto-ADP-ribosyltransferase ART2.2 upon T cell activation. J Immunol (2000) 165:4463-9. doi:10.4049/jimmunol.165.8.4463
52. Aswad F, Dennert G. P2X7 receptor expression levels determine lethal effects of a purine based danger signal in T lymphocytes. Cell Immunol (2006) 243:58-65. doi:10.1016/j.cellimm.2006.12.003
53. Rissiek B, Haag F, Boyer O, Koch-Nolte F, Adriouch S. ADP-ribosylation of P2X7: a matter of life and death for regulatory T cells and natural killer T cells. Curr Top Microbiol Immunol (2014) 384:107-26. doi:10.1007/82_2014_420
54. Aswad F, Kawamura H, Dennert G. High sensitivity of CD4+CD25+ regulatory T cells to extracellular metabolites nicotinamide adenine dinucleotide and ATP: a role for P2X7 receptors. J Immunol (2005) 175:3075-83. doi:10.4049/jimmunol.175.5.3075
55. Kawamura H, Aswad F, Minagawa M, Govindarajan S, Dennert G. P2X7 receptors regulate NKT cells in autoimmune hepatitis. J Immunol (2006) 176:2152-60. doi:10.4049/jimmunol.176.4.2152
56. Koch-Nolte F, Reyelt J, Schössow B, Schwarz N, Scheuplein F, Rothenburg S, et al. Single domain antibodies from llama effectively and specifically block T cell ecto-ADP-ribosyltransferase ART2.2 in vivo. FASEB J (2007) 21:3490-8. doi:10.1096/fj.07-8661com
57. Bao L, Locovei S, Dahl G. Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett (2004) 572:65-8. doi:10.1016/j.febslet.2004.07.009
58. Bruzzone S, Guida L, Zocchi E, Franco L, De Flora A. Connexin 43 hemi channels mediate Ca2+-regulated transmembrane NAD+ fluxes in intact cells. FASEB J (2001) 15:10-2. doi:10.1096/fj.00-0566fje
59. Scheuplein F, Rissiek B, Driver JP, Chen Y-G, Koch-Nolte F, Serreze DV. A recombinant heavy chain antibody approach blocks ART2 mediated deletion of an iNKT cell population that upon activation inhibits autoimmune diabetes. J Autoimmun (2010) 34:145-54. doi:10.1016/j.jaut.2009.08.012
60. Takeda K, Hayakawa Y, Van Kaer L, Matsuda H, Yagita H, Okumura K. Critical contribution of liver natural killer T cells to a murine model of hepatitis. Proc Natl Acad Sci U S A (2000) 97:5498-503. doi:10.1073/pnas.040566697
61. Hofman P, Cherfils-Vicini J, Bazin M, Ilie M, Juhel T, Hebuterne X, et al. Genetic and pharmacological inactivation of the purinergic P2RX7 receptor dampens inflammation but increases tumor incidence in a mouse model of colitis-associated cancer. Cancer Res (2015) 75:835-45. doi:10.1158/0008-5472.CAN-14-1778
62. Ghiringhelli F, Apetoh L, Tesniere A, Aymeric L, Ma Y, Ortiz C, et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat Med (2009) 15:1170-8. doi:10.1038/nm.2028
63. Adinolfi E, Capece M, Franceschini A, Falzoni S, Giuliani AL, Rotondo A, et al. Accelerated tumor progression in mice lacking the ATP receptor P2X7. Cancer Res (2015) 75:635-44. doi:10.1158/0008-5472.CAN-14-1259
64. Heiss K, Jänner N, Mähnss B, Schumacher V, Koch-Nolte F, Haag F, et al. High sensitivity of intestinal CD8+ T cells to nucleotides indicates P2X7 as a regulator for intestinal T cell responses. J Immunol (2008) 181:3861-9. doi:10.4049/jimmunol.181.6.3861
65. Iwata M, Hirakiyama A, Eshima Y, Kagechika H, Kato C, Song S-Y. Retinoic acid imprints gut-homing specificity on T cells. Immunity (2004) 21:527-38. doi:10.1016/j.immuni.2004.08.011
66. Coombes JL, Siddiqui KRR, Arancibia-Cárcamo CV, Hall J, Sun C-M, Belkaid Y, et al. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med (2007) 204:1757-64. doi:10.1084/jem.20070590
67. Proietti M, Cornacchione V, Rezzonico Jost T, Romagnani A, Faliti CE, Perruzza L, et al. ATP-gated ionotropic P2X7 receptor controls follicular T helper cell numbers in Peyer's patches to promote host-microbiota mutualism. Immunity (2014) 41:789-801. doi:10.1016/j.immuni.2014.10.010
68. Praetorius HA, Leipziger J. ATP release from non-excitable cells. Purinergic Signal (2009) 5:433-46. doi:10.1007/s11302-009-9146-2
69. Loomis WH, Namiki S, Ostrom RS, Insel PA, Junger WG. Hypertonic stress increases T cell interleukin-2 expression through a mechanism that involves ATP release, P2 receptor, and p38 MAPK activation. J Biol Chem (2003) 278:4590-6. doi:10.1074/jbc. M207868200
70. Woehrle T, Yip L, Manohar M, Sumi Y, Yao Y, Chen Y, et al. Hypertonic stress regulates T cell function via pannexin-1 hemichannels and P2X receptors. J Leukoc Biol (2010) 88:1181-9. doi:10.1189/jlb.0410211
71. Schenk U, Westendorf AM, Radaelli E, Casati A, Ferro M, Fumagalli M, et al. Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci Signal (2008) 1:ra6-6. doi:10.1126/scisignal.1160583
72. Yip L, Woehrle T, Corriden R, Hirsh M, Chen Y, Inoue Y, et al. Autocrine regulation of T-cell activation by ATP release and P2X7 receptors. FASEB J (2009) 23:1685-93. doi:10.1096/fj.08-126458
73. Sarukhan A, Garcia C, Lanoue A, Boehmer von H. Allelic inclusion of T cell receptor alpha genes poses an autoimmune hazard due to low-level expression of autospecific receptors. Immunity (1998) 8:563-70. doi:10.1016/S1074-7613(00)80561-0
74. Woehrle T, Yip L, Elkhal A, Sumi Y, Chen Y, Yao Y, et al. Pannexin-1 hemichannel-mediated ATP release together with P2X1 and P2X4 receptors regulate T-cell activation at the immune synapse. Blood (2010) 116:3475-84. doi:10.1182/blood-2010-04-277707
75. Rissiek B, Koch-Nolte F, Magnus T. Nanobodies as modulators of inflammation: potential applications for acute brain injury. Front Cell Neurosci (2014) 8:344. doi:10.3389/fncel.2014.00344
76. Adinolfi E, Pizzirani C, Idzko M, Panther E, Norgauer J, Virgilio F, et al. P2X7 receptor: death or life? Purinergic Signal (2005) 1:219-27. doi:10.1007/s11302-005-6322-x
77. Trabanelli S, Ocadlíková D, Gulinelli S, Curti A, Salvestrini V, Vieira RP, et al. Extracellular ATP exerts opposite effects on activated and regulatory CD4+ T cells via purinergic P2 receptor activation. J Immunol (2012) 189:1303-10. doi:10.4049/jimmunol.1103800
78. Baricordi OR, Ferrari D, Melchiorri L, Chiozzi P, Hanau S, Chiari E, et al. An ATP-activated channel is involved in mitogenic stimulation of human T lymphocytes. Blood (1996) 87:682-90.
79. Burnstock G, Boeynaems J-M. Purinergic signalling and immune cells. Purinergic Signal (2014) 10:529-64. doi:10.1007/s11302-014-9427-2
80. Junger WG. Immune cell regulation by autocrine purinergic signalling. Nat Rev Immunol (2011) 11:201-12. doi:10.1038/nri2938