Purinergic receptors modulate MAP kinases and transcription factors that control microglial inflammatory gene expression

Neurochemistry International

Volumn 49, Issue 2, 2006, Pages 204-214

  Potucek, Yvonne D ^a   Crain, Jessica M ^a   Watters, Jyoti J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Cyclic AMP response element binding protein (CREB); Interleukin 12 (IL 12); P2X7; Priming; Tumor necrosis factor alpha (TNF )

Indexed keywords

HYDROGEN PEROXIDE; INTERLEUKIN 12; MITOGEN ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BRAIN INJURY; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; INFLAMMATION; MICROGLIA; NEUROPROTECTION; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; ANIMALS; BRAIN DAMAGE, CHRONIC; CYTOPROTECTION; ENCEPHALITIS; GENE EXPRESSION REGULATION; GLIOSIS; HUMANS; MAP KINASE SIGNALING SYSTEM; MICROGLIA; RECEPTORS, PURINERGIC; TRANSCRIPTION FACTORS;

EID: 33745001458     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2006.04.005     Document Type: Article

References (117)

1. Abbott K.L., Loss II J.R., Robida A.M., and Murphy T.J. Evidence that Galpha(q)-coupled receptor-induced interleukin-6 mRNA in vascular smooth muscle cells involves the nuclear factor of activated T cells. Mol. Pharmacol. 58 (2000) 946-953
2. Abbracchio M.P., and Burnstock G. Purinoceptors: are there families of P2X and P2Y purinoceptors?. Pharmacol. Ther. 64 (1994) 445-475
3. Abbracchio M.P., and Burnstock G. Purinergic signalling: pathophysiological roles. Jpn. J. Pharmacol. 78 (1998) 113-145
4. Abe S., Nakamura H., Inoue S., Takeda H., Saito H., Kato S., Mukaida N., Matsushima K., and Tomoike H. Interleukin-8 gene repression by clarithromycin is mediated by the activator protein-1 binding site in human bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 22 (2000) 51-60
5. Adinolfi E., Kim M., Young M.T., Di Virgilio F., and Surprenant A. Tyrosine phosphorylation of HSP90 within the P2X7 receptor complex negatively regulates P2X7 receptors. J. Biol. Chem. 278 (2003) 37344-37351
6. Aga M., Watters J.J., Pfeiffer Z.A., Wiepz G.J., Sommer J.A., and Bertics P.J. Evidence for nucleotide receptor modulation of cross talk between MAP kinase and NF-{kappa}B signaling pathways in murine RAW 264.7 macrophages. Am. J. Physiol. Cell Physiol. 286 (2004) C923-C930
7. Aga M., Johnson C.J., Hart A.P., Guadarrama A.G., Suresh M., Svaren J., Bertics P.J., and Darien B.J. Modulation of monocyte signaling and pore formation in response to agonists of the nucleotide receptor P2X(7). J. Leukoc. Biol. 72 (2002) 222-232
8. Albert J.L., Boyle J.P., Roberts J.A., Challiss R.A., Gubby S.E., and Boarder M.R. Regulation of brain capillary endothelial cells by P2Y receptors coupled to Ca2+, phospholipase C and mitogen-activated protein kinase. Br. J. Pharmacol. 122 (1997) 935-941
9. Alzola E., Perez-Etxebarria A., Kabre E., Fogarty D.J., Metioui M., Chaib N., Macarulla J.M., Matute C., Dehaye J.-P., and Marino A. Activation by P2X7 agonists of two phospholipases A2 (PLA2) in ductal cells of rat submandibular gland. Coupling of the calcium-independent PLA2 with kallikrein secretion. J. Biol. Chem. 273 (1998) 30208-30217
10. Baeuerle P.A., and Henkel T. Function and activation of NF-kappa B in the immune system. Ann. Rev. Immunol. 12 (1994) 141-179
11. Baker A.E., Brautigam V.M., and Watters J.J. Estrogen modulates microglial inflammatory mediator production via interactions with estrogen receptor {beta}. Endocrinology 145 (2004) 5021-5032
12. Baldwin Jr. A.S. The NF-kappa B and I kappa B proteins: new discoveries and insights. Ann. Rev. Immunol. 14 (1996) 649-683
13. Beigi R., Kobatake E., Aizawa M., and Dubyak G.R. Detection of local ATP release from activated platelets using cell surface-attached firefly luciferase. Am. J. Physiol. 276 (1999) C267-C278
14. Beigi R.D., Kertesy S.B., Aquilina G., and Dubyak G.R. Oxidized ATP (oATP) attenuates proinflammatory signaling via P2 receptor-independent mechanisms. Br. J. Pharmacol. 140 (2003) 507-519
15. Berenbaum F., Humbert L., Bereziat G., and Thirion S. Concomitant recruitment of ERK1/2 and p38 MAPK signalling pathway is required for activation of cytoplasmic phospholipase A2 via ATP in articular chondrocytes. J. Biol. Chem. 278 (2003) 13680-13687
16. Bianchi B.R., Lynch K.J., Touma E., Niforatos W., Burgard E.C., Alexander K.M., Park H.S., Yu H., Metzger R., and Kowaluk E. Pharmacological characterization of recombinant human and rat P2X receptor subtypes. Eur. J. Pharmacol. 376 (1999) 127-138
17. Blanchard D.K., Hoffman S.L., and Djeu J.Y. Inhibition of extracellular ATP-mediated lysis of human macrophages by calmodulin antagonists. J. Cell Biochem. 57 (1995) 452-464
18. Bodin P., and Burnstock G. Purinergic signalling: ATP release. Neurochem. Res. 26 (2001) 959-969
19. Boucsein C., Zacharias R., Farber K., Pavlovic S., Hanisch U.K., and Kettenmann H. Purinergic receptors on microglial cells: functional expression in acute brain slices and modulation of microglial activation in vitro. Eur. J. Neurosci. 17 (2003) 2267-2276
20. Braun N., Lenz C., Gillardon F., Zimmermann M., and Zimmermann H. Focal cerebral ischemia enhances glial expression of ecto-5′-nucleotidase. Brain Res. 766 (1997) 213-226
21. Braun N., Zhu Y., Krieglstein J., Culmsee C., and Zimmermann H. Upregulation of the enzyme chain hydrolyzing extracellular ATP after transient forebrain ischemia in the rat. J. Neurosci. 18 (1998) 4891-4900
22. Brautigam V.M., Frasier C., Nikodemova M., and Watters J.J. Purinergic receptor modulation of BV-2 microglial cell activity: potential involvement of p38 MAP kinase and CREB. J. Neuroimmunol. 166 (2005) 113
23. Bshesh K., Zhao B., Spight D., Biaggioni I., Feokistov I., Denenberg A., Wong H.R., and Shanley T.P. The A2A receptor mediates an endogenous regulatory pathway of cytokine expression in THP-1 cells. J. Leukoc. Biol. 72 (2002) 1027-1036
24. Budagian V., Bulanova E., Brovko L., Orinska Z., Fayad R., Paus R., and Bulfone-Paus S. Signaling through P2X7 receptor in human T cells involves p56lck, MAP kinases, and transcription factors AP-1 and NF-kappa B. J. Biol. Chem. 278 (2003) 1549-1560
25. Burnstock G., and Knight G.E. Cellular Distribution and Functions of P2 Receptor Subtypes in Different Systems International Review of Cytology vol. 240 (2004), Academic Press pp. 31-304
26. Cantiello H.F. Nucleotide transport through the cystic fibrosis transmembrane conductance regulator. Biosci. Rep. 17 (1997) 147-171
27. Chen B.C., and Lin W.W. PKC- and ERK-dependent activation of I kappa B kinase by lipopolysaccharide in macrophages: enhancement by P2Y receptor-mediated CaMK activation. Br. J. Pharmacol. 134 (2001) 1055-1065
28. Chen L., He H.-Y., Li H.-M., Zheng J., Heng W.-J., You J.-F., and Fang W.-G. ERK1/2 and p38 pathways are required for P2Y receptor-mediated prostate cancer invasion. Cancer Lett. 215 (2004) 239
29. Chessell I.P., Michel A.D., and Humphrey P.P. Properties of the pore-forming P2X7 purinoceptor in mouse NTW8 microglial cells. Br. J. Pharmacol. 121 (1997) 1429-1437
30. Chessell I.P., Simon J., Hibell A.D., Michel A.D., Barnard E.A., and Humphrey P.P.A. Cloning and functional characterisation of the mouse P2X7 receptor. FEBS Lett. 439 (1998) 26-30
31. Chiozzi P., Sanz J.M., Ferrari D., Falzoni S., Aleotti A., Buell G.N., Collo G., and Virgilio F.D. Spontaneous cell fusion in macrophage cultures expressing high levels of the P2Z/P2X7 receptor. J. Cell Biol. 138 (1997) 697-706
32. Chorna N.E., Santiago-Perez L.I., Erb L., Seye C.I., Neary J.T., Sun G.Y., Weisman G.A., and Gonzalez F.A. P2Y receptors activate neuroprotective mechanisms in astrocytic cells. J. Neurochem. 91 (2004) 119-132
33. Cotrina M.L., Lin J.H., and Nedergaard M. Cytoskeletal assembly and ATP release regulate astrocytic calcium signaling. J. Neurosci. 18 (1998) 8794-8804
34. Cotrina M.L., Lin J.H., Lopez-Garcia J.C., Naus C.C., and Nedergaard M. ATP-mediated glia signaling. J. Neurosci. 20 (2000) 2835-2844
35. Cotrina M.L., Lin J.H., Alves-Rodrigues A., Liu S., Li J., Azmi-Ghadimi H., Kang J., Naus C.C., and Nedergaard M. Connexins regulate calcium signaling by controlling ATP release. Proc. Natl. Acad. Sci. USA 95 (1998) 15735-15740
36. Delgado M., and Ganea D. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit nuclear factor-kappa B-dependent gene activation at multiple levels in the human monocytic cell line THP-1. J. Biol. Chem. 276 (2001) 369-380
37. Denlinger L.C., Fisette P.L., Sommer J.A., Watters J.J., Prabhu U., Dubyak G.R., Proctor R.A., and Bertics P.J. Cutting edge: the nucleotide receptor P2X7 contains multiple protein- and lipid-interaction motifs including a potential binding site for bacterial lipopolysaccharide. J. Immunol. 167 (2001) 1871-1876
38. Di Virgilio F., Sanz J.M., Chiozzi P., and Falzoni S. The P2Z/P2X7 receptor of microglial cells: a novel immunomodulatory receptor. Prog. Brain Res. 120 (1999) 355-368
39. Dixon C.J., White P.J., Hall J.F., Kingston S., and Boarder M.R. Regulation of human hepatocytes by P2Y receptors: control of glycogen phosphorylase, Ca2+, and mitogen-activated protein kinases. J. Pharmacol. Exp. Ther. 313 (2005) 1305-1313
40. Dubyak G.R., and el-Moatassim C. Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides. Am J. Physiol. 265 (1993) C577-C606
41. Dunant Y., and Israel M. Neurotransmitter release at rapid synapses. Biochimie 82 (2000) 289-302
42. Edwards J., Sprung R., Sprague R., and Spence D. Chemiluminescence detection of ATP release from red blood cells upon passage through microbore tubing. Analyst 126 (2001) 1257-1260
43. el-Moatassim C., and Dubyak G.R. A novel pathway for the activation of phospholipase D by P2z purinergic receptors in BAC1.2F5 macrophages. J. Biol. Chem. 267 (1992) 23664-23673
44. Evans R., Lewis C., Buell G., Valera S., North R., and Surprenant A. Pharmacological characterization of heterologously expressed ATP-gated cation channels (P2x purinoceptors). Mol. Pharmacol. 48 (1995) 178-183
45. Feng C., Mery A.G., Beller E.M., Favot C., and Boyce J.A. Adenine nucleotides inhibit cytokine generation by human mast cells through a Gs-coupled receptor. J. Immunol. 173 (2004) 7539-7547
46. Ferrari D., Villalba M., Chiozzi P., Falzoni S., Ricciardi-Castagnoli P., and Di Virgilio F. Mouse microglial cells express a plasma membrane pore gated by extracellular ATP. J. Immunol. 156 (1996) 1531-1539
47. Ferrari D., Wesselborg S., Bauer M.K., and Schulze-Osthoff K. Extracellular ATP activates transcription factor NF-kappaB through the P2Z purinoreceptor by selectively targeting NF-kappaB p65. J. Cell Biol. 139 (1997) 1635-1643
48. Ferrari D., Chiozzi P., Falzoni S., Hanau S., and Di Virgilio F. Purinergic modulation of interleukin-1 beta release from microglial cells stimulated with bacterial endotoxin. J. Exp. Med. 185 (1997) 579-582
49. Ferrari D., Chiozzi P., Falzoni S., Dal Susino M., Melchiorri L., Baricordi O.R., and Di Virgilio F. Extracellular ATP triggers IL-1 beta release by activating the purinergic P2Z receptor of human macrophages. J. Immunol. 159 (1997) 1451-1458
50. Ferrari D., Chiozzi P., Falzoni S., Dal Susino M., Collo G., Buell G., and Di Virgilio F. ATP-mediated cytotoxicity in microglial cells. Neuropharmacology 36 (1997) 1295-1301
51. Ferrari D., Stroh C., and Schulze-Osthoff K. P2X7/P2Z purinoreceptor-mediated activation of transcription factor NFAT in microglial cells. J. Biol. Chem. 274 (1999) 13205-13210
52. Ferrari D., Los M., Bauer M.K., Vandenabeele P., Wesselborg S., and Schulze-Osthoff K. P2Z purinoreceptor ligation induces activation of caspases with distinct roles in apoptotic and necrotic alterations of cell death. FEBS Lett. 447 (1999) 71-75
53. Foletta V.C., Segal D.H., and Cohen D.R. Transcriptional regulation in the immune system: all roads lead to AP-1. J. Leukoc. Biol. 63 (1998) 139-152
54. Guthrie P.B., Knappenberger J., Segal M., Bennett M.V., Charles A.C., and Kater S.B. ATP released from astrocytes mediates glial calcium waves. J. Neurosci. 19 (1999) 520-528
55. Henkel T., Machleidt T., Alkalay I., Kronke M., Ben-Neriah Y., and Baeuerle P.A. Rapid proteolysis of I kappa B-alpha is necessary for activation of transcription factor NF-kappa B. Nature 365 (1993) 182-185
56. Hess J., Angel P., and Schorpp-Kistner M. AP-1 subunits: quarrel and harmony among siblings. J. Cell Sci. 117 (2004) 5965-5973
57. Hide I., Tanaka M., Inoue A., Nakajima K., Kohsaka S., Inoue K., and Nakata Y. Extracellular ATP triggers tumor necrosis factor-alpha release from rat microglia. J. Neurochem. 75 (2000) 965-972
58. Honda S., and Kohsaka S. Regulation of microglial cell function by ATP. Nihon Shinkei Seishin Yakurigaku Zasshi 21 (2001) 89-93
59. Honda S., Sasaki Y., Ohsawa K., Imai Y., Nakamura Y., Inoue K., and Kohsaka S. Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J. Neurosci. 21 (2001) 1975-1982
60. Hu Y., Fisette P.L., Denlinger L.C., Guadarrama A.G., Sommer J.A., Proctor R.A., and Bertics P.J. Purinergic receptor modulation of lipopolysaccharide signaling and inducible nitric-oxide synthase expression in RAW 264.7 macrophages. J. Biol. Chem. 273 (1998) 27170-27175
61. Humphreys B.D., Rice J., Kertesy S.B., and Dubyak G.R. Stress-activated protein kinase/JNK activation and apoptotic induction by the macrophage P2X7 nucleotide receptor. J. Biol. Chem. 275 (2000) 26792-26798
62. Huot J., Houle F., Rousseau S., Deschesnes R.G., Shah G.M., and Landry J. SAPK2/p38-dependent F-actin reorganization regulates early membrane blebbing during stress-induced apoptosis. J. Cell Biol. 143 (1998) 1361-1373
63. Huwiler A., van Rossum G., Wartmann M., and Pfeilschifter J. Stimulation by extracellular ATP and UTP of the stress-activated protein kinase cascade in rat renal mesangial cells. Br. J. Pharmacol. 120 (1997) 807-812
64. Igarashi H., Yokofujita J., Murakami K., Okada A., and Kuroda M. Microglial ecto-Ca2+-ATPase activity in a rat model of focal homologous blood clot embolic cerebral ischemia: an enzyme histochemical study. Brain Res. Bull. 60 (2003) 93-104
65. Im S.H., and Rao A. Activation and deactivation of gene expression by Ca2+/calcineurin-NFAT-mediated signaling. Mol. Cell 18 (2004) 1-9
66. Inoue K. Microglial activation by purines and pyrimidines. Glia 40 (2002) 156-163
67. Inoue K., Nakajima K., Morimoto T., Kikuchi Y., Koizumi S., Illes P., and Kohsaka S. ATP stimulation of Ca2+-dependent plasminogen release from cultured microglia. Br. J. Pharmacol. 123 (1998) 1304-1310
68. Inoue K., Tsuda M., and Koizumi S. ATP- and adenosine-mediated signaling in the central nervous system: chronic pain and microglia: involvement of the ATP receptor P2X4. J. Pharmacol. Sci. 94 (2004) 112-114
69. John G.R., Simpson J.E., Woodroofe M.N., Lee S.C., and Brosnan C.F. Extracellular nucleotides differentially regulate interleukin-1beta signaling in primary human astrocytes: implications for inflammatory gene expression. J. Neurosci. 21 (2001) 4134-4142
70. Karin M., Liu Z., and Zandi E. AP-1 function and regulation. Curr. Opin. Cell Biol. 9 (1997) 240-246
71. Kasai Y., Ohta T., Nakazato Y., and Ito S. Release of dopamine and ATP from PC12 cells treated with dexamethasone, reserpine and bafilomycin A1. J. Vet. Med. Sci. 63 (2001) 367-372
72. Kim M., Spelta V., Sim J., North R.A., and Surprenant A. Differential assembly of rat purinergic P2X7 receptor in immune cells of the brain and periphery. J. Biol. Chem. 276 (2001) 23262-23267
73. Kohsaka S., Nakajima K., Hamanoue M., Koizumi S., and Inoue K. Microglia-derived plasminogen has neurotrophic effects on the CNS neurons in vitro. Neuropathol. Appl. Neurobiol. 20 (1994) 190
74. Kugelgen I.V., and Wetter A. Molecular pharmacology of P2Y-receptors. Naunyn-Schmiedeberg's Arch. Pharmacol. 362 (2000) 310-323
75. la Sala A., Ferrari D., Di Virgilio F., Idzko M., Norgauer J., and Girolomoni G. Alerting and tuning the immune response by extracellular nucleotides. J. Leukoc. Biol. 73 (2003) 339-343
76. Lee Y.J., Park S.H., and Han H.J. ATP stimulates Na+-glucose cotransporter activity via cAMP and p38 MAPK in renal proximal tubule cells. Am. J. Physiol. Cell Physiol. 289 (2005) C1268-C1276
77. Liang Q., Bueno O.F., Wilkins B.J., Kuan C.Y., Xia Y., and Molkentin J.D. c-Jun N-terminal kinases (JNK) antagonize cardiac growth through cross-talk with calcineurin-NFAT signaling. Embo. J. 22 (2003) 5079-5089
78. Liu J.S., John G.R., Sikora A., Lee S.C., and Brosnan C.F. Modulation of interleukin-1beta and tumor necrosis factor alpha signaling by P2 purinergic receptors in human fetal astrocytes. J. Neurosci. 20 (2000) 5292-5299
79. Lonze B.E., and Ginty D.D. Function and regulation of CREB family transcription factors in the nervous system. Neuron 35 (2002) 605-623
80. Lutz P.L., and Kabler S. Release of adenosine and ATP in the brain of the freshwater turtle (Trachemys scripta) during long-term anoxia. Brain Res. 769 (1997) 281-286
81. MacKenzie A., Wilson H.L., Kiss-Toth E., Dower S.K., North R.A., and Surprenant A. Rapid secretion of interleukin-1[beta] by microvesicle shedding. Immunity 15 (2001) 825
82. Marteau F., Communi D., Boeynaems J.-M., and Suarez Gonzalez N. Involvement of multiple P2Y receptors and signaling pathways in the action of adenine nucleotides diphosphates on human monocyte-derived dendritic cells. J. Leukoc. Biol. 76 (2004) 796-803
83. Matsuka Y., Neubert J.K., Maidment N.T., and Spigelman I. Concurrent release of ATP and substance P within guinea pig trigeminal ganglia in vivo. Brain Res. 915 (2001) 248-255
84. Mayr B., and Montminy M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2 (2001) 599-609
85. Molliver D.C., Cook S.P., Carlsten J.A., Wright D.E., and McCleskey E.W. ATP and UTP excite sensory neurons and induce CREB phosphorylation through the metabotropic receptor, P2Y2. Eur. J. Neurosci. 16 (2002) 1850-1860
86. Morigiwa K., Quan M., Murakami M., Yamashita M., and Fukuda Y. P2 Purinoceptor expression and functional changes of hypoxia-activated cultured rat retinal microglia. Neurosci. Lett. 282 (2000) 153-156
87. Muscella A., Giovanna M., Greco E.S., Storelli C., and Marsigliante S. Activation of P2Y2 receptor induces c-FOS protein through a pathway involving mitogen-activated protein kinases and phosphoinositide 3-kinases in HeLa cells. J. Cell. Physiol. 195 (2003) 234-240
88. Neary J.T., Kang Y., Willoughby K.A., and Ellis E.F. Activation of extracellular signal-regulated kinase by stretch-induced injury in astrocytes involves extracellular ATP and P2 purinergic receptors. J. Neurosci. 23 (2003) 2348-2356
89. Newman E.A. Propagation of intercellular calcium waves in retinal astrocytes and Muller cells. J. Neurosci. 21 (2001) 2215-2223
90. North R.A. Molecular physiology of P2X receptors. Physiol. Rev. 82 (2002) 1013-1067
91. North R.A., and Surprenant A. Pharmacology of cloned P2X receptors. Ann. Rev. Pharmacol. Toxicol. 40 (2000) 563-580
92. Ogata T., Chuai M., Morino T., Yamamoto H., Nakamura Y., and Schubert P. Adenosine triphosphate inhibits cytokine release from lipopolysaccharide-activated microglia via P2y receptors. Brain Res. 981 (2003) 174
93. Olearczyk J.J., Stephenson A.H., Lonigro A.J., and Sprague R.S. Receptor-mediated activation of the heterotrimeric G-protein Gs results in ATP release from erythrocytes. Med. Sci. Monitor. 7 (2001) 669-674
94. Ollivier V., Parry G.C.N., Cobb R.R., Prost D.D., and Mackman N. Elevated cyclic AMP inhibits NF-kappa B-mediated transcription in human monocytic cells and endothelial cells. J. Biol. Chem. 271 (1996) 20828-20835
95. Perez R.L., Ritzenthaler J.D., and Roman J. Transcriptional regulation of the interleukin-1beta promoter via fibrinogen engagement of the CD18 integrin receptor. Am. J. Respir. Cell Mol. Biol. 20 (1999) 1059-1066
96. Pfeiffer Z.A. A Role for Mitogen-activated Protein Kinases in Modulation of the Macrophage Cytoskeleton and Inflammatory Responses by the Nucleotide Receptor P2X7 in Biomolecular Chemistry (2003), University of Wisconsin, Madison p. 254
97. Pfeiffer Z.A., Aga M., Prabhu U., Watters J.J., Hall D.J., and Bertics P.J. 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
98. Poelchen W., Sieler D., Wirkner K., and Illes P. Co-transmitter function of ATP in central catecholaminergic neurons of the rat. Neuroscience 102 (2001) 593-602
99. Ralevic V., and Burnstock G. Receptors for purines and pyrimidines. Pharmacol. Rev. 50 (1998) 413-492
100. Rao A., Luo C., and Hogan P.G. Transcription factors of the NFAT family: regulation and function. Ann. Rev. Immunol. 15 (1997) 707-747
101. Sanna B., Bueno O.F., Dai Y.S., Wilkins B.J., and Molkentin J.D. Direct and indirect interactions between calcineurin-NFAT and MEK1-extracellular signal-regulated kinase 1/2 signaling pathways regulate cardiac gene expression and cellular growth. Mol. Cell Biol. 25 (2005) 865-878
102. Santiago-Pérez L.I., Flores R.V., Santos-Berríos C., Chorna N.E., Krugh B., Garrad R.C., Erb L., Weisman G.A., and González F.A. P2Y2 nucleotide receptor signaling in human monocytic cells: activation, desensitization and coupling to mitogen-activated protein kinases. J. Cell. Physiol. 187 (2001) 196-208
103. Sanz J.M., and Di Virgilio F. Kinetics and mechanism of ATP-dependent IL-1 beta release from microglial cells. J. Immunol. 164 (2000) 4893-4898
104. Shiga H., Tojima T., and Ito E. Ca2+ signaling regulated by an ATP-dependent autocrine mechanism in astrocytes. Neuroreport 12 (2001) 2619-2622
105. Shigemoto-Mogami Y., Koizumi S., Tsuda M., Ohsawa K., Kohsaka S., and Inoue K. Mechanisms underlying extracellular ATP-evoked interleukin-6 release in mouse microglial cell line, MG-5. J. Neurochem. 78 (2001) 1339-1349
106. Sikora A., Liu J., Brosnan C., Buell G., Chessel I., and Bloom B.R. Cutting edge: purinergic signaling regulates radical-mediated bacterial killing mechanisms in macrophages through a P2X7-independent mechanism. J. Immunol. 163 (1999) 558-561
107. Surprenant A., Rassendren F., Kawashima E., North R.A., and Buell G. The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 272 (1996) 735-738
108. Takenouchi T., Ogihara K., Sato M., and Kitani H. Inhibitory effects of U73122 and U73343 on Ca2+ influx and pore formation induced by the activation of P2X7 nucleotide receptors in mouse microglial cell line. Biochim. Biophys. Acta (BBA): Gen. Sub. 1726 (2005) 177
109. Thevananther S., Sun H., Li D., Arjunan V., Awad S.S., Wyllie S., Zimmerman T.L., Goss J.A., and Karpen S.J. Extracellular ATP activates c-jun N-terminal kinase signaling and cell cycle progression in hepatocytes. Hepatology 39 (2004) 393-402
110. van Der Weyden L., Adams D.J., and Morris B.J. Capacity for purinergic control of renin promoter via P2Y(11) receptor and cAMP pathways. Hypertension 36 (2000) 1093-1098
111. Visentin S., Renzi M., Frank C., Greco A., and Levi G. Two different ionotropic receptors are activated by ATP in rat microglia. J. Physiol. 519 (1999) 723-736
112. Wang X., Franciosi S., Bae J.H., Kim S.U., and McLarnon J.G. Expression of P2y and P2x receptors in cultured human microglia. Proc. Western Pharmacol. Soc. 42 (1999) 79-81
113. Wang X., Kim S.U., van Breemen C., and McLarnon J.G. Activation of purinergic P2X receptors inhibits P2Y-mediated Ca2+ influx in human microglia. Cell Calcium 27 (2000) 205-212
114. Wang Z., Haydon P.G., and Yeung E.S. Direct observation of calcium-independent intercellular ATP signaling in astrocytes. Anal. Chem. 72 (2000) 2001-2007
115. Watters J.J., Sommer J.A., Pfeiffer Z.A., Prabhu U., Guerra A.N., and Bertics P.J. A differential role for the mitogen-activated protein kinases in lipopolysaccharide signaling: the MEK/ERK pathway is not essential for nitric oxide and interleukin 1beta production. J. Biol. Chem. 277 (2002) 9077-9087
116. Watters J.J., Sommer J.A., Fisette P.L., Pfeiffer Z.A., Aga M., Prabhu U., Guerra A., Denlinger L.C., and Bertics P.J. The P2X7 nucleotide receptor: modulation of LPS-induced macrophage signaling and mediator production. Drug Dev. Res. 53 (2001) 91-104
117. Wu C.C., Hsu S.C., Shih H.M., and Lai M.Z. Nuclear factor of activated T cells c is a target of p38 mitogen-activated protein kinase in T cells. Mol. Cell Biol. 23 (2003) 6442-6454