Adenine dinucleotide second messengers and T-lymphocyte calcium signaling

Frontiers in Immunology

Volumn 4, Issue AUG, 2013, Pages

  Ernst, Insa M A ^a   Fliegert, Ralf ^a   Guse, Andreas H ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Adenosine diphosphoribose; Calcium entry; Calcium release; Calcium signaling; Cyclic ADP ribose; Nicotinic acid adenine dinucleotide phosphate; T lymphocyte; TRPM2 cation channels

Indexed keywords

ADENINE DINUCLEOTIDE; ADENOSINE DIPHOSPHATE RIBOSE; BZ194; CALCIUM CHANNEL; CD3 ANTIGEN; CD38 ANTIGEN; CONCANAVALIN A; CXCL2 CHEMOKINE; CYCLIC ADENOSINE DIPHOSPHATE RIBOSE; DINUCLEOTIDE; GLYCOSIDASE; INOSITOL 1, 4, 5 TRISPHOSPHATE RECEPTOR; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NICOTINIC ACID ADENINE DINUCLEOTIDE PHOSPHATE; POLY ADENOSINE DIPHOSPHATE RIBOSE GLYCOHYDROLASE; PROTEIN KINASE FYN; PURINE ANTAGONIST; RYANODINE RECEPTOR; STROMAL INTERACTION MOLECULE 1; T LYMPHOCYTE RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL M2; TRANSIENT RECEPTOR POTENTIAL CHANNEL ML1; TWO PORE CALCIUM CHANNEL PROTEIN 1; TWO PORE CALCIUM CHANNEL PROTEIN 2; UNCLASSIFIED DRUG;

APOPTOSIS; CALCIUM SIGNALING; HUMAN; IMMUNE RESPONSE; NONHUMAN; OXIDATIVE STRESS; REVIEW; SECOND MESSENGER; T LYMPHOCYTE; UPREGULATION;

EID: 84883696782     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00259     Document Type: Review

References (89)

1. De Flora A, Guida L, Franco L, Zocchi E. The CD38/cyclic ADP-ribose system: a topological paradox. Int J Biochem Cell Biol (1997) 29:1149-66. doi:10.1016/S1357-2725(97)00062-9
2. Zhao YJ, Lam CM, Lee HC. The membrane-bound enzyme CD38 exists in two opposing orientations. Sci Signal (2012) 5:ra67. doi:10.1126/scisignal.2002700
3. Pollak N, Niere M, Ziegler M. NAD kinase levels control the NADPH concentration in human cells. J Biol Chem (2007) 282:33562-71. doi:10.1074/jbc.M704442200
4. Malavasi F, Funaro A, Alessio M, DeMonte LB, Ausiello CM, Dianzani U, et al. CD38: a multi-lineage cell activation molecule with a split personality. Int J Clin Lab Res (1992) 22:73-80. doi:10.1007/BF02591400
5. Deterre P, Berthelier V, Bauvois B, Dalloul A, Schuber F, Lund F. CD38 in T- and B-cell functions. Chem Immunol (2000) 75:146-68. doi:10.1159/000058767
6. Ho HN, Hultin LE, Mitsuyasu RT, Matud JL, Hausner MA, Bockstoce D, et al. Circulating HIV-specific CD8+ cytotoxic T cells express CD38 and HLA-DR antigens. J Immunol (1993) 150:3070-9.
7. Coetzee LM, Tay SS, Lawrie D, Janossy G, Glencross DK. From research tool to routine test: CD38 monitoring in HIV patients. Cytometry B Clin Cytom (2009) 76:375-84. doi:10.1002/cyto.b.20478
8. Mikoshiba K. IP3 receptor/Ca2+ channel: from discovery to new signaling concepts. J Neurochem (2007) 102:1426-46. doi:10.1111/j.1471-4159.2007.04825.x
9. Putney JW. Capacitative calcium entry: from concept to molecules. Immunol Rev (2009) 231:10-22. doi:10.1111/j.1600-065X.2009.00810.x
10. Gasser A, Bruhn S, Guse AH. Second messenger function of nicotinic acid adenine dinucleotide phosphate revealed by an improved enzymatic cycling assay. J Biol Chem (2006) 281:16906-13. doi:10.1074/jbc.M601347200
11. Gasser A, Glassmeier G, Fliegert R, Langhorst MF, Meinke S, Hein D, et al. Activation of T cell calcium influx by the second messenger ADP-ribose. J Biol Chem (2006) 281:2489-96. doi:10.1074/jbc.M506525200
12. Guse AH, Goldwich A, Weber K, Mayr GW. Non-radioactive, isomer-specific inositol phosphate mass determinations: high-performance liquid chromatography-micro-metal-dye detection strongly improves speed and sensitivity of analyses from cells and micro-enzyme assays. J Chromatogr B Biomed Appl (1995) 672:189-98. doi:10.1016/0378-4347(95)00219-9
13. Guse AH, Roth E, Emmrich F. D-myo-inositol 1,3,4,5-tetrakisphosphate releases Ca2+ from crude microsomes and enriched vesicular plasma membranes, but not from intracellular stores of permeabilized T-lymphocytes and monocytes. Biochem J (1992) 288(Pt 2):489-95.
14. Guse AH, da Silva CP, Berg I, Skapenko AL, Weber K, Heyer P, et al. Regulation of calcium signalling in T lymphocytes by the second messenger cyclic ADP-ribose. Nature (1999) 398:70-3. doi:10.1038/18024
15. Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel S-H, Tanasa B, et al. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature (2006) 441:179-85. doi:10.1038/nature04702
16. Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan PG. Orai1 is an essential pore subunit of the CRAC channel. Nature (2006) 443:230-3. doi:10.1038/nature05122
17. Vig M, Peinelt C, Beck A, Koomoa DL, Rabah D, Koblan-Huberson M, et al. CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science (2006) 312:1220-3. doi:10.1126/science.1127883
18. Berg I, Potter BVL, Mayr GW, Guse AH. Nicotinic acid adenine dinucleotide phosphate (Naadp+) is an essential regulator of T-lymphocyte Ca2+-signaling. J Cell Biol (2000) 150:581-8. doi:10.1083/jcb.150.3.581
19. Guse AH, Lee HC. NAADP: a universal Ca2+ trigger. Sci Signal (2008) 1:re10. doi:10.1126/scisignal.144re10
20. Aarhus R, Graeff RM, Dickey DM, Walseth TF, Lee HC. ADP-ribosyl cyclase and CD38 catalyze the synthesis of a calcium-mobilizing metabolite from NADP. J Biol Chem (1995) 270:30327-33. doi:10.1074/jbc.270.51.30327
21. Moreschi I, Bruzzone S, Melone L, De Flora A, Zocchi E. NAADP+ synthesis from cADPRP and nicotinic acid by ADP-ribosyl cyclases. Biochem Biophys Res Commun (2006) 345:573-80. doi:10.1016/j.bbrc.2006.04.096
22. Billington RA, Bellomo EA, Floriddia EM, Erriquez J, Distasi C, Genazzani AA. A transport mechanism for NAADP in a rat basophilic cell line. FASEB J (2006) 20:521-3.
23. Schmid F, Bruhn S, Weber K, Mittrücker H-W, Guse AH. CD38: a NAADP degrading enzyme. FEBS Lett (2011) 585:3544-8. doi:10.1016/j.febslet.2011.10.017
24. Soares S, Thompson M, White T, Isbell A, Yamasaki M, Prakash Y, et al. NAADP as a second messenger: neither CD38 nor base-exchange reaction are necessary for in vivo generation of NAADP in myometrial cells. Am J Physiol Cell Physiol (2007) 292:C227-39. doi:10.1152/ajpcell.00638.2005
25. Graeff R. Acidic residues at the active sites of CD38 and ADP-ribosyl cyclase determine nicotinic acid adenine dinucleotide phosphate (NAADP) synthesis and hydrolysis activities. J Biol Chem (2006) 281:28951-7. doi:10.1074/jbc.M604370200
26. Churamani D, Hooper R, Rahman T, Brailoiu E, Patel S. The N-terminal region of two-pore channel 1 regulates trafficking and activation by NAADP. Biochem J (2013) 453(1):147-51. doi:10.1042/BJ20130474
27. Wang X, Zhang X, Dong X-P, Samie M, Li X, Cheng X, et al. TPC proteins are phosphoinositide- activated sodium-selective ion channels in endosomes and lysosomes. Cell (2012) 151:372-83. doi:10.1016/j.cell.2012.08.036
28. Cang C, Zhou Y, Navarro B, Seo Y-J, Aranda K, Shi L, et al. mTOR regulates lysosomal ATP-sensitive two-pore Na(+) channels to adapt to metabolic state. Cell (2013) 152:778-90. doi:10.1016/j.cell.2013.01.023
29. Guse AH. Linking NAADP to ion channel activity: a unifying hypothesis. Sci Signal (2012) 5:e18. doi:10.1126/scisignal.2002890
30. Hohenegger M, Suko J, Gscheidlinger R, Drobny H, Zidar A. Nicotinic acid-adenine dinucleotide phosphate activates the skeletal muscle ryanodine receptor. Biochem J (2002) 367:423-31. doi:10.1042/BJ20020584
31. Gerasimenko JV, Maruyama Y, Yano K, Dolman NJ, Tepikin AV, Petersen OH, et al. NAADP mobilizes Ca2+ from a thapsigargin-sensitive store in the nuclear envelope by activating ryanodine receptors. J Cell Biol (2003) 163:271-82. doi:10.1083/jcb.200306134
32. Gerasimenko JV, Sherwood M, Tepikin AV, Petersen OH, Gerasimenko OV. NAADP, cADPR and IP3 all release Ca2+ from the endoplasmic reticulum and an acidic store in the secretory granule area. J Cell Sci (2006) 119:226-38. doi:10.1242/jcs.02721
33. Lee HC, Aarhus R. Functional visualization of the separate but interacting calcium stores sensitive to NAADP and cyclic ADP-ribose. J Cell Sci (2000) 113(Pt 24):4413-20.
34. Kinnear NP, Boittin F-X, Thomas JM, Galione A, Evans AM. Lysosome-sarcoplasmic reticulum junctions. A trigger zone for calcium signaling by nicotinic acid adenine dinucleotide phosphate and endothelin-1. J Biol Chem (2004) 279:54319-26. doi:10.1074/jbc.M406132200
35. Cancela JM, Churchill GC, Galione A. Coordination of agonist-induced Ca2+-signalling patterns by NAADP in pancreatic acinar cells. Nature (1999) 398:74-6. doi:10.1038/18032
36. Dammermann W, Guse AH. Functional ryanodine receptor expression is required for NAADP-mediated local Ca2+ signaling in T-lymphocytes. J Biol Chem (2005) 280:21394-9. doi:10.1074/jbc.M413085200
37. Steen M, Kirchberger T, Guse AH. NAADP mobilizes calcium from the endoplasmic reticular Ca(2+) store in T-lymphocytes. J Biol Chem (2007) 282:18864-71. doi:10.1074/jbc.M610925200
38. Langhorst MF, Schwarzmann N, Guse AH. Ca2+ release via ryanodine receptors and Ca2+ entry: major mechanisms in NAADP-mediated Ca2+ signaling in T-lymphocytes. Cell Signal (2004) 16:1283-9. doi:10.1016/j.cellsig.2004.03.013
39. Dammermann W, Zhang B, Nebel M, Cordiglieri C, Odoardi F, Kirchberger T, et al. NAADP-mediated Ca2+ signaling via type 1 ryanodine receptor in T cells revealed by a synthetic NAADP antagonist. Proc Natl Acad Sci U S A (2009) 106:10678-83. doi:10.1073/pnas.0809997106
40. Cordiglieri C, Odoardi F, Zhang B, Nebel M, Kawakami N, Klinkert WEF, et al. Nicotinic acid adenine dinucleotide phosphate-mediated calcium signalling in effector T cells regulates autoimmunity of the central nervous system. Brain J Neurol (2010) 133:1930-43. doi:10.1093/brain/awq135
41. Davis LC, Morgan AJ, Chen JL, Snead CM, Bloor-Young D, Shenderov E, et al. NAADP activates two-pore channels on T cell cytolytic granules to stimulate exocytosis and killing. Curr Biol (2012) 22:2331-7. doi:10.1016/j.cub.2012.10.035
42. Calcraft PJ, Ruas M, Pan Z, Cheng X, Arredouani A, Hao X, et al. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature (2009) 459:596-600. doi:10.1038/nature08030
43. Brailoiu E, Churamani D, Cai X, Schrlau MG, Brailoiu GC, Gao X, et al. Essential requirement for two-pore channel 1 in NAADP-mediated calcium signaling. J Cell Biol (2009) 186:201-9. doi:10.1083/jcb.200904073
44. Zong X, Schieder M, Cuny H, Fenske S, Gruner C, Rötzer K, et al. The two-pore channel TPCN2 mediates NAADP-dependent Ca(2+)-release from lysosomal stores. PflÜgers Arch (2009) 458:891-9. doi:10.1007/s00424-009-0690-y
45. Beck A, Kolisek M, Bagley LA, Fleig A, Penner R. Nicotinic acid adenine dinucleotide phosphate and cyclic ADP-ribose regulate TRPM2 channels in T lymphocytes. FASEB J (2006) 20:962-4. doi:10.1096/fj.05-5538fje
46. Lange I, Penner R, Fleig A, Beck A. Synergistic regulation of endogenous TRPM2 channels by adenine dinucleotides in primary human neutrophils. Cell Calcium (2008) 44:604-15. doi:10.1016/j.ceca.2008.05.001
47. Kirchberger T, Moreau C, Wagner GK, Fliegert R, Siebrands CC, Nebel M, et al. 8-Bromo-cyclic inosine diphosphoribose: towards a selective cyclic ADP-ribose agonist. Biochem J (2009) 422:139-49. doi:10.1042/BJ20082308
48. Tóth B, Csanády L. Identification of direct and indirect effectors of the transient receptor potential melastatin 2 (TRPM2) cation channel. J Biol Chem (2010) 285:30091-102. doi:10.1074/jbc.M109.066464
49. Zhang F, Jin S, Yi F, Li P-L. TRP-ML1 functions as a lysosomal NAADP-sensitive Ca2+ release channel in coronary arterial myocytes. J Cell Mol Med (2009) 13:3174-85. doi:10.1111/j.1582-4934.2008.00486.x
50. Walseth TF, Lin-Moshier Y, Jain P, Ruas M, Parrington J, Galione A, et al. Photoaffinity labeling of high affinity nicotinic acid adenine dinucleotide phosphate (NAADP)-binding proteins in sea urchin egg. J Biol Chem (2012) 287:2308-15. doi:10.1074/jbc.M111.306563
51. Lin-Moshier Y, Walseth TF, Churamani D, Davidson SM, Slama JT, Hooper R, et al. Photoaffinity labeling of nicotinic acid adenine dinucleotide phosphate (NAADP) targets in mammalian cells. J Biol Chem (2012) 287:2296-307. doi:10.1074/jbc.M111.305813
52. Clapper DL, Walseth TF, Dargie PJ, Lee HC. Pyridine nucleotide metabolites stimulate calcium release from sea urchin egg microsomes desensitized to inositol trisphosphate. J Biol Chem (1987) 262:9561-8.
53. Lee HC, Walseth TF, Bratt GT, Hayes RN, Clapper DL. Structural determination of a cyclic metabolite of NAD+ with intracellular Ca2+-mobilizing activity. J Biol Chem (1989) 264:1608-15.
54. Guse AH, da Silva CP, Emmrich F, Ashamu GA, Potter BV, Mayr GW. Characterization of cyclic adenosine diphosphate-ribose-induced Ca2+ release in T lymphocyte cell lines. J Immunol (1995) 1950(155):3353-9.
55. da Silva CP, Potter BV, Mayr GW, Guse AH. Quantification of intracellular levels of cyclic ADP-ribose by high-performance liquid chromatography. J Chromatogr B Biomed Sci Appl (1998) 707:43-50. doi:10.1016/S0378-4347(97)00622-1
56. Schwarzmann N, Kunerth S, Weber K, Mayr GW, Guse AH. Knock-down of the type 3 ryanodine receptor impairs sustained Ca2+ signaling via the T cell receptor/CD3 complex. J Biol Chem (2002) 277:50636-42. doi:10.1074/jbc.M209061200
57. Guse AH, Tsygankov AY, Weber K, Mayr GW. Transient tyrosine phosphorylation of human ryanodine receptor upon T cell stimulation. J Biol Chem (2001) 276:34722-7. doi:10.1074/jbc.M100715200
58. Kunerth S, Langhorst MF, Schwarzmann N, Gu X, Huang L, Yang Z, et al. Amplification and propagation of pacemaker Ca2+ signals by cyclic ADP-ribose and the type 3 ryanodine receptor in T cells. J Cell Sci (2004) 117:2141-9. doi:10.1242/jcs.01063
59. Guse AH, Berg I, da Silva CP, Potter BV, Mayr GW. Ca2+ entry induced by cyclic ADP-ribose in intact T-lymphocytes. J Biol Chem (1997) 272:8546-50. doi:10.1074/jbc.272.13.8546
60. Guse AH. Structure-activity relationship of cyclic ADP-ribose, an update. J Chin Pharm Sci (2013) 22:127-36. doi:10.5246/jcps.2013.02.017
61. Zocchi E, Guida L, Franco L, Silvestro L, Guerrini M, Benatti U, et al. Free ADP-ribose in human erythrocytes: pathways of intra-erythrocytic conversion and non-enzymic binding to membrane proteins. Biochem J (1993) 295(Pt 1):121-30.
62. Kun E, Chang AC, Sharma ML, Ferro AM, Nitecki D. Covalent modification of proteins by metabolites of NAD+. Proc Natl Acad Sci U S A (1976) 73:3131-5. doi:10.1073/pnas.73.9.3131
63. Jacobson EL, Cervantes-Laurean D, Jacobson MK. ADP-ribose in glycation and glycoxidation reactions. Adv Exp Med Biol (1997) 419:371-9. doi:10.1007/978-1-4419-8632-0_49
64. Canales J, Pinto RM, Costas MJ, Hernández MT, Miró A, Bernet D, et al. Rat liver nucleoside diphosphosugar or diphosphoalcohol pyrophosphatases different from nucleotide pyrophosphatase or phosphodiesterase I: substrate specificities of Mg(2+)-and/or Mn(2+)-dependent hydrolases acting on ADP-ribose. Biochim Biophys Acta (1995) 1246:167-77. doi:10.1016/0167-4838(94)00191-I
65. Yang H, Slupska MM, Wei YF, Tai JH, Luther WM, Xia YR, et al. Cloning and characterization of a new member of the Nudix hydrolases from human and mouse. J Biol Chem (2000) 275:8844-53. doi:10.1074/jbc.275.12.8844
66. Bernet D, Pinto RM, Costas MJ, Canales J, Cameselle JC. Rat liver mitochondrial ADP-ribose pyrophosphatase in the matrix space with low Km for free ADP-ribose. Biochem J (1994) 299(Pt 3):679-82.
67. Perraud A-L, Shen B, Dunn CA, Rippe K, Smith MK, Bessman MJ, et al. NUDT9, a member of the Nudix hydrolase family, is an evolutionarily conserved mitochondrial ADP-ribose pyrophosphatase. J Biol Chem (2003) 278:1794-801. doi:10.1074/jbc.M205601200
68. Perraud AL, Fleig A, Dunn CA, Bagley LA, Launay P, Schmitz C, et al. ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature (2001) 411:595-9. doi:10.1038/35079100
69. Sano Y, Inamura K, Miyake A, Mochizuki S, Yokoi H, Matsushime H, et al. Immunocyte Ca2+ influx system mediated by LTRPC2. Science (2001) 293:1327-30. doi:10.1126/science.1062473
70. Bastide B, Snoeckx K, Mounier Y. ADP-ribose stimulates the calcium release channel RyR1 in skeletal muscle of rat. Biochem Biophys Res Commun (2002) 296:1267-71. doi:10.1016/S0006-291X(02)02073-9
71. Yu P, Wang Q, Zhang L-H, Lee H-C, Zhang L, Yue J. A cell permeable NPE caged ADP-ribose for studying TRPM2. PLoS ONE (2012) 7:e51028. doi:10.1371/journal.pone.0051028
72. Gasser A, Guse AH. Determination of intracellular concentrations of the TRPM2 agonist ADP-ribose by reversed-phase HPLC. J Chromatogr B Analyt Technol Biomed Life Sci (2005) 821:181-7. doi:10.1016/j.jchromb.2005.05.002
73. Gelman L, Deterre P, Gouy H, Boumsell L, Debré P, Bismuth G. The lymphocyte surface antigen CD38 acts as a nicotinamide adenine dinucleotide glycohydrolase in human T lymphocytes. Eur J Immunol (1993) 23:3361-4. doi:10.1002/eji.1830231245
74. Howard M, Grimaldi JC, Bazan JF, Lund FE, Santos-Argumedo L, Parkhouse RM, et al. Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science (1993) 262:1056-9. doi:10.1126/science.8235624
75. Kim UH, Han MK, Park BH, Kim HR, An NH. Function of NAD glycohydrolase in ADP-ribose uptake from NAD by human erythrocytes. Biochim Biophys Acta (1993) 1178:121-6. doi:10.1016/0167-4889(93)90001-6
76. Albeniz I, Demir O, Nurten R, Bermek E. NAD glycohydrolase activities and ADP-ribose uptake in erythrocytes from normal subjects and cancer patients. Biosci Rep (2004) 24:41-53. doi:10.1023/B:BIRE.0000037755.42767.a4
77. Ferrero E, Saccucci F, Malavasi F. The making of a leukocyte receptor: origin, genes and regulation of human CD38 and related molecules. Chem Immunol (2000) 75:1-19. doi:10.1159/000058763
78. Fonfria E, Marshall ICB, Benham CD, Boyfield I, Brown JD, Hill K, et al. TRPM2 channel opening in response to oxidative stress is dependent on activation of poly(ADP-ribose) polymerase. Br J Pharmacol (2004) 143:186-92. doi:10.1038/sj.bjp.0705914
79. Bonicalzi M-E, Haince J-F, Droit A, Poirier GG. Regulation of poly(ADP-ribose) metabolism by poly(ADP-ribose) glycohydrolase: where and when? Cell Mol Life Sci (2005) 62:739-50. doi:10.1007/s00018-004-4505-1
80. Buelow B, Song Y, Scharenberg AM. The Poly(ADP-ribose) polymerase PARP-1 is required for oxidative stress-induced TRPM2 activation in lymphocytes. J Biol Chem (2008) 283:24571-83. doi:10.1074/jbc.M802673200
81. Hara Y, Wakamori M, Ishii M, Maeno E, Nishida M, Yoshida T, et al. LTRPC2 Ca2+-permeable channel activated by changes in redox status confers susceptibility to cell death. Mol Cell (2002) 9:163-73. doi:10.1016/S1097-2765(01)00438-5
82. Miller BA. The role of TRP channels in oxidative stress-induced cell death. J Membr Biol (2006) 209:31-41. doi:10.1007/s00232-005-0839-3
83. Melzer N, Hicking G, Göbel K, Wiendl H. TRPM2 cation channels modulate T cell effector functions and contribute to autoimmune CNS inflammation. PLoS ONE (2012) 7:e47617. doi:10.1371/journal.pone.0047617
84. Olabisi OA, Soto-Nieves N, Nieves E, Yang TTC, Yang X, Yu RYL, et al. Regulation of transcription factor NFAT by ADP-ribosylation. Mol Cell Biol (2008) 28:2860-71. doi:10.1128/MCB.01746-07
85. Valdor R, Schreiber V, Saenz L, Martínez T, Muñ7oz-Suano A, Dominguez-Villar M, et al. Regulation of NFAT by poly(ADP-ribose) polymerase activity in T cells. Mol Immunol (2008) 45:1863-71. doi:10.1016/j.molimm.2007.10.044
86. Wang R, Green DR. Metabolic checkpoints in activated T cells. Nat Immunol (2012) 13:907-15. doi:10.1038/ni.2386
87. Yamamoto S, Shimizu S, Kiyonaka S, Takahashi N, Wajima T, Hara Y, et al. TRPM2-mediated Ca2+influx induces chemokine production in monocytes that aggravates inflammatory neutrophil infiltration. Nat Med (2008) 14:738-47. doi:10.1038/nm1758
88. Hardaker L, Bahra P, de Billy BC, Freeman M, Kupfer N, Wyss D, et al. The ion channel transient receptor potential melastatin-2 does not play a role in inflammatory mouse models of chronic obstructive pulmonary diseases. Respir Res (2012) 13:30. doi:10.1186/1465-9921-13-30
89. Sumoza-Toledo A, Fleig A, Penner R. TRPM2 channels are not required for acute airway inflammation in OVA-induced severe allergic asthma in mice. J Inflamm (Lond) (2013) 10:19. doi:10.1186/1476-9255-10-19