Purinergic receptor modulation of BV-2 microglial cell activity: Potential involvement of p38 MAP kinase and CREB

Journal of Neuroimmunology

Volumn 166, Issue 1-2, 2005, Pages 113-125

  Brautigam, Vielska M ^a   Frasier, Chuenchanok ^a,b   Nikodemova, Maria ^b   Watters, Jyoti J ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

ATP; Cyclooxygenase 2; Inflammation; Nitric oxide; Phosphorylation; Signal transduction

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLOOXYGENASE 2; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; PURINE RECEPTOR; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; CELL ACTIVITY; CONTROLLED STUDY; CORRELATION ANALYSIS; EXPOSURE; HUMAN; HUMAN CELL; INHIBITION KINETICS; MICROGLIA; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STIMULATION; TIME;

ADENINE NUCLEOTIDES; ADENOSINE TRIPHOSPHATE; ANIMALS; CELL LINE; CELL SURVIVAL; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; CYCLOOXYGENASE INHIBITORS; ENZYME INHIBITORS; IMIDAZOLES; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; MICE; MICROGLIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; PYRIDINES; RECEPTORS, PURINERGIC; RECEPTORS, PURINERGIC P2; TIME FACTORS;

EID: 23144441198     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2005.05.012     Document Type: Article

References (80)

1. L. Acarin, H. Peluffo, B. Gonzalez, and B. Castellano Expression of inducible nitric oxide synthase and cyclooxygenase-2 after excitotoxic damage to the immature rat brain J. Neurosci. Res. 68 2002 745 754
2. M. Aga, C.J. Johnson, A.P. Hart, A.G. Guadarrama, M. Suresh, J. Svaren, P.J. Bertics, and B.J. Darien Modulation of monocyte signaling and pore formation in response to agonists of the nucleotide receptor P2X(7) J. Leukoc. Biol. 72 2002 222 232
3. M. Aga, J.J. Watters, Z.A. Pfeiffer, G.J. Wiepz, J.A. Sommer, and P.J. Bertics 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
4. A.E. Baker, V.M. Brautigam, and J.J. Watters Estrogen modulates microglial inflammatory mediator production via interactions with estrogen receptor {beta} Endocrinology 145 2004 5021 5032
5. N.R. Bhat, D.L. Feinstein, Q. Shen, and A.N. Bhat p38 MAPK-mediated transcriptional activation of inducible nitric-oxide synthase in glial cells. Roles of nuclear factors, nuclear factor kappa B, cAMP response element-binding protein, CCAAT/enhancer-binding protein-beta, and activating transcription factor-2 J. Biol. Chem. 277 2002 29584 29592
6. B.R. Bianchi, K.J. Lynch, E. Touma, W. Niforatos, E.C. Burgard, K.M. Alexander, H.S. Park, H. Yu, R. Metzger, and E. Kowaluk Pharmacological characterization of recombinant human and rat P2X receptor subtypes Eur. J. Pharmacol. 376 1999 127 138
7. R.E. Birch, and S.H. Polmar Pharmacological modification of immunoregulatory T lymphocytes: I. Effect of adenosine, H1 and H2 histamine agonists upon T lymphocyte regulation of B lymphocyte differentiation in vitro Clin. Exp. Immunol. 48 1982 218 230
8. E. Blasi, R. Barluzzi, V. Bocchini, R. Mazzolla, and F. Bistoni Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus J. Neuroimmunol. 27 1990 229 237
9. C. Boucsein, R. Zacharias, K. Farber, S. Pavlovic, U.K. Hanisch, and H. Kettenmann 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
10. R. Brambilla, and M.P. Abbracchio Modulation of cyclooxygenase-2 and brain reactive astrogliosis by purinergic P2 receptors Ann. N.Y. Acad. Sci. 939 2001 54 62
11. R. Brambilla, G. Burnstock, A. Bonazzi, S. Ceruti, F. Cattabeni, and M.P. Abbracchio Cyclo-oxygenase-2 mediates P2Y receptor-induced reactive astrogliosis Br. J. Pharmacol. 126 1999 563 567
12. K. Bshesh, B. Zhao, D. Spight, I. Biaggioni, I. Feokistov, A. Denenberg, H.R. Wong, and T.P. Shanley The A2A receptor mediates an endogenous regulatory pathway of cytokine expression in THP-1 cells J. Leukoc. Biol. 72 2002 1027 1036
13. J.A. Calvert, A.E. Atterbury-Thomas, C. Leon, I.D. Forsythe, C. Gachet, and R.J. Evans Evidence for P2Y1, P2Y2, P2Y6 and atypical UTP-sensitive receptors coupled to rises in intracellular calcium in mouse cultured superior cervical ganglion neurons and glia Br. J. Pharmacol. 143 2004 525 532
14. C.C. Chen, and J.K. Wang p38 but not p44/42 mitogen-activated protein kinase is required for nitric oxide synthase induction mediated by lipopolysaccharide in RAW 264.7 macrophages (published erratum appears in Mol Pharmacol 1999 Jun;55(6):1108) Mol. Pharmacol. 55 1999 481 488
15. C. Chen, Y.H. Chen, and W.W. Lin Involvement of p38 mitogen-activated protein kinase in lipopolysaccharide-induced iNOS and COX-2 expression in J774 macrophages Immunology 97 1999 124 129
16. I.P. Chessell, J. Simon, A.D. Hibell, A.D. Michel, E.A. Barnard, and P.P.A. Humphrey Cloning and functional characterisation of the mouse P2X7 receptor FEBS Lett. 439 1998 26 30
17. M. Chhatriwala, R.G. Ravi, R.I. Patel, J.L. Boyer, K.A. Jacobson, and T.K. Harden Induction of novel agonist selectivity for the ADP-activated P2Y1 receptor versus the ADP-activated P2Y12 and P2Y13 receptors by conformational constraint of an ADP analog J. Pharmacol. Exp. Ther. 311 2004 1038 1043
18. D. Communi, M. Parmentier, and J.-M. Boeynaems Cloning, functional expression and tissue distribution of the human P2Y6 receptor Biochem. Biophys. Res. Commun. 222 1996 303 308
19. D. Communi, B. Robaye, and J.M. Boeynaems Pharmacological characterization of the human P2Y11 receptor Br. J. Pharmacol. 128 1999 1199 1206
20. M.L. Cotrina, J.H. Lin, A. Alves-Rodrigues, S. Liu, J. Li, H. Azmi-Ghadimi, J. Kang, C.C. Naus, and M. Nedergaard Connexins regulate calcium signaling by controlling ATP release Proc. Natl. Acad. Sci. U. S. A. 95 1998 15735 15740
21. M.L. Cotrina, J.H. Lin, and M. Nedergaard Cytoskeletal assembly and ATP release regulate astrocytic calcium signaling J. Neurosci. 18 1998 8794 8804
22. M.L. Cotrina, J.H. Lin, J.C. Lopez-Garcia, C.C. Naus, and M. Nedergaard ATP-mediated glia signaling J. Neurosci. 20 2000 2835 2844
23. M. Delgado, and D. Ganea 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
24. G.R. Dubyak, and C. el-Moatassim Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides Am. J. Physiol. 265 1993 C577 C606
25. S.J. Ennion, A.D. Powell, and E.P. Seward Identification of the P2Y12 receptor in nucleotide inhibition of exocytosis from bovine chromaffin cells Mol. Pharmacol. 66 2004 601 611
26. R. Evans, C. Lewis, G. Buell, S. Valera, R. North, and A. Surprenant Pharmacological characterization of heterologously expressed ATP-gated cation channels (P2x purinoceptors) Mol. Pharmacol. 48 1995 178 183
27. D. Ferrari, P. Chiozzi, S. Falzoni, M. Dal Susino, G. Collo, G. Buell, and F. Di Virgilio ATP-mediated cytotoxicity in microglial cells Neuropharmacology 36 1997 1295 1301
28. D. Ferrari, P. Chiozzi, S. Falzoni, S. Hanau, and F. Di Virgilio Purinergic modulation of interleukin-1 beta release from microglial cells stimulated with bacterial endotoxin J. Exp. Med. 185 1997 579 582
29. D. Ferrari, S. Wesselborg, M.K. Bauer, and K. Schulze-Osthoff Extracellular ATP activates transcription factor NF-kappaB through the P2Z purinoreceptor by selectively targeting NF-kappaB p65 J. Cell Biol. 139 1997 1635 1643
30. D. Ferrari, C. Stroh, and K. Schulze-Osthoff P2X7/P2Z purinoreceptor-mediated activation of transcription factor NFAT in microglial cells J. Biol. Chem. 274 1999 13205 13210
31. M. Frodin, and S. Gammeltoft Role and regulation of 90 kDa ribosomal S6 kinase (RSK) in signal transduction Mol. Cell. Endocrinol. 151 1999 65 77
32. E.M. Frohman, B. Vayuvegula, S. Gupta, and S. van den Noort Norepinephrine inhibits gamma-interferon-induced major histocompatibility class II (Ia) antigen expression on cultured astrocytes via beta-2-adrenergic signal transduction mechanisms Proc. Natl. Acad. Sci. U. S. A. 85 1988 1292 1296
33. E.M. Frohman, B. Vayuvegula, S. van den Noort, and S. Gupta Norepinephrine inhibits gamma-interferon-induced MHC class II (Ia) antigen expression on cultured brain astrocytes J. Neuroimmunol. 17 1988 89 101
34. E. Galea, and D.L. Feinstein Regulation of the expression of the inflammatory nitric oxide synthase (NOS2) by cyclic AMP FASEB J. 13 1999 2125 2137
35. F.-P. Gendron, M. Chalimoniuk, J. Strosznajder, S. Shen, F.A. Gonzalez, G.A. Weisman, and G.Y. Sun P2X7 nucleotide receptor activation enhances IFNgamma-induced type II nitric oxide synthase activity in BV-2 microglial cells J. Neurochem. 87 2003 344 352
36. P. Ghersa, R. Hooft van Huijsduijnen, J. Whelan, Y. Cambet, R. Pescini, and J.F. DeLamarter Inhibition of E-selectin gene transcription through a cAMP-dependent protein kinase pathway J. Biol. Chem. 269 1994 29129 29137
37. S.S. Greenberg, X. Zhao, J.F. Wang, L. Hua, and J. Ouyang cAMP and purinergic P2y receptors upregulate and enhance inducible NO synthase mRNA and protein in vivo Am. J. Physiol. 273 1997 L967 L979
38. P.B. Guthrie, J. Knappenberger, M. Segal, M.V. Bennett, A.C. Charles, and S.B. Kater ATP released from astrocytes mediates glial calcium waves J. Neurosci. 19 1999 520 528
39. I. Hide, M. Tanaka, A. Inoue, K. Nakajima, S. Kohsaka, K. Inoue, and Y. Nakata Extracellular ATP triggers tumor necrosis factor-alpha release from rat microglia J. Neurochem. 75 2000 965 972
40. S. Honda, Y. Sasaki, K. Ohsawa, Y. Imai, Y. Nakamura, K. Inoue, and S. Kohsaka Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors J. Neurosci. 21 2001 1975 1982
41. C. Iadecola, F. Zhang, R. Casey, M. Nagayama, and M.E. Ross Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene J. Neurosci. 17 1997 9157 9164
42. C. Iadecola, K. Niwa, S. Nogawa, X. Zhao, M. Nagayama, E. Araki, S. Morham, and M.E. Ross Reduced susceptibility to ischemic brain injury and N-methyl-D-aspartate-mediated neurotoxicity in cyclooxygenase-2-deficient mice Proc. Natl. Acad. Sci. U. S. A. 98 2001 1294 1299
43. K. Inoue The functions of ATP receptors in the hippocampus Pharmacol. Res. 38 1998 323 331
44. K. Inoue Microglial activation by purines and pyrimidines Glia 40 2002 156 163
45. K. Inoue, K. Nakajima, T. Morimoto, Y. Kikuchi, S. Koizumi, P. Illes, and S. Kohsaka ATP stimulation of Ca2+-dependent plasminogen release from cultured microglia Br. J. Pharmacol. 123 1998 1304 1310
46. B.S. Khakh, G. Burnstock, C. Kennedy, B.F. King, R.A. North, P. Seguela, M. Voigt, P.P.A. Humphrey, and International Union of Pharmacology XXIV. Current status of the nomenclature and properties of P2X receptors and their subunits Pharmacol. Rev. 53 2001 107 118
47. P.J. Knudsen, C.A. Dinarello, and T.B. Strom Prostaglandins posttranscriptionally inhibit monocyte expression of interleukin 1 activity by increasing intracellular cyclic adenosine monophosphate J. Immunol. 137 1986 3189 3194
48. I.v. Kugelgen, and A. Wetter Molecular pharmacology of P2Y-receptors Naunyn-Schmiedeberg's Arch. Pharmacol. 362 2000 310 323
49. S.L. Kunkel, M. Spengler, M.A. May, R. Spengler, J. Larrick, and D. Remick Prostaglandin E2 regulates macrophage-derived tumor necrosis factor gene expression J. Biol. Chem. 263 1988 5380 5384
50. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
51. L. Lecanu, C. Verrecchia, I. Margaill, R.G. Boulu, and M. Plotkine iNOS contribution to the NMDA-induced excitotoxic lesion in the rat striatum Br. J. Pharmacol. 125 1998 584 590
52. B.E. Lonze, and D.D. Ginty Function and regulation of CREB family transcription factors in the nervous system Neuron 35 2002 605 623
53. J.A. Mitchell, K.L. Kohlhaas, T. Matsumoto, J.S. Pollock, U. Forstermann, T.D. Warner, H.H. Schmidt, and F. Murad Induction of NADPH-dependent diaphorase and nitric oxide synthase activity in aortic smooth muscle and cultured macrophages Mol. Pharmacol. 41 1992 1163 1168
54. D.C. Molliver, S.P. Cook, J.A. Carlsten, D.E. Wright, and E.W. McCleskey ATP and UTP excite sensory neurons and induce CREB phosphorylation through the metabotropic receptor, P2Y2 Eur. J. Neurosci. 16 2002 1850 1860
55. K. Morigiwa, Y. Fukuda, and M. Yamashita Neurotransmitter ATP and cytokine release Nippon Yakurigaku Zasshi-Folia Pharmacologica Japonica 115 2000 185 192
56. K. Nakajima, and S. Kohsaka Microglia: neuroprotective and neurotrophic cells in the central nervous system Curr. Drug Targets. Cardiovasc. Haematol. Disord. 4 2004 65 84
57. J.T. Neary, Q. Zhu, Y. Kang, and P.K. Dash Extracellular ATP induces formation of AP-1 complexes in astrocytes via P2 purinoceptors NeuroReport 7 1996 2893 2896
58. E.A. Newman Propagation of intercellular calcium waves in retinal astrocytes and Muller cells J. Neurosci. 21 2001 2215 2223
59. R.A. Nicholas, W.C. Watt, E.R. Lazarowski, Q. Li, and K. Harden Uridine nucleotide selectivity of three phospholipase C-activating P2 receptors: identification of a UDP-selective, a UTP-selective, and an ATP- and UTP-specific receptor Mol. Pharmacol. 50 1996 224 229
60. S. Nogawa, F. Zhang, M.E. Ross, and C. Iadecola Cyclo-oxygenase-2 gene expression in neurons contributes to ischemic brain damage J. Neurosci. 17 1997 2746 2755
61. R.A. North Molecular physiology of P2X receptors Physiol. Rev. 82 2002 1013 1067
62. R.A. North, and A. Surprenant Pharmacology of cloned P2X receptors Annu. Rev. Pharmacol. Toxicol. 40 2000 563 580
63. Y. Ohtani, M. Minami, and M. Satoh Expression of inducible nitric oxide synthase mRNA and production of nitric oxide are induced by adenosine triphosphate in cultured rat microglia Neurosci. Lett. 293 2000 72 74
64. V. Ollivier, G.C.N. Parry, R.R. Cobb, D.d. Prost, and N. Mackman Elevated cyclic AMP inhibits NF-kappa B-mediated transcription in human monocytic cells and endothelial cells J. Biol. Chem. 271 1996 20828 20835
65. S.Y. Park, H. Lee, J. Hur, S.Y. Kim, H. Kim, J.H. Park, S. Cha, S.S. Kang, G.J. Cho, W.S. Choi, and K. Suk Hypoxia induces nitric oxide production in mouse microglia via p38 mitogen-activated protein kinase pathway Brain Res.Mol. Brain Res. 107 2002 9 16
66. S. Parmentier-Batteur, G.A. Bohme, D. Lerouet, L. Zhou-Ding, V. Beray, I. Margaill, and M. Plotkine Antisense oligodeoxynucleotide to inducible nitric oxide synthase protects against transient focal cerebral ischemia-induced brain injury J. Cereb. Blood Flow Metab. 21 2001 15 21
67. V. Ralevic, and G. Burnstock Receptors for purines and pyrimidines Pharmacol. Rev. 50 1998 413 492
68. J.M. Sanz, and F. Di Virgilio Kinetics and mechanism of ATP-dependent IL-1 beta release from microglial cells J. Immunol. 164 2000 4893 4898
69. H. Shiga, T. Tojima, and E. Ito Ca2+ signaling regulated by an ATP-dependent autocrine mechanism in astrocytes NeuroReport 12 2001 2619 2622
70. G. Stoll, S. Jander, and M. Schroeter Cytokines in CNS disorders: neurotoxicity versus neuroprotection J. Neural Transm., Suppl. 59 2000 81 89
71. W.J. Streit Microglial response to brain injury: a brief synopsis Toxicol. Pathol. 28 2000 28 30
72. L. van Der Weyden, D.J. Adams, and B.J. Morris Capacity for purinergic control of renin promoter via P2Y(11) receptor and cAMP pathways Hypertension 36 2000 1093 1098
73. K. Van Kolen, and H. Slegers P2Y12 receptor stimulation inhibits beta-adrenergic receptor-induced differentiation by reversing the cyclic AMP-dependent inhibition of protein kinase B J. Neurochem. 89 2004 442 453
74. I. von Kugelgen, and A. Wetter Molecular pharmacology of P2Y-receptors Naunyn-Schmiedeberg's Arch. Pharmacol. 362 2000 310 323
75. S.C. Wagstaff, W.B. Bowler, J.A. Gallagher, and R.A. Hipskind Extracellular ATP activates multiple signalling pathways and potentiates growth factor-induced c-fos gene expression in MCF-7 breast cancer cells Carcinogenesis 21 2000 2175 2181
76. J.J. Watters, J.A. Sommer, P.L. Fisette, Z.A. Pfeiffer, M. Aga, U. Prabhu, A. Guerra, L.C. Denlinger, and P.J. Bertics The P2X7 nucleotide receptor: modulation of LPS-induced macrophage signaling and mediator production Drug Dev. Res. 53 2001 91 104
77. J.J. Watters, J.A. Sommer, Z.A. Pfeiffer, U. Prabhu, A.N. Guerra, and P.J. Bertics 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
78. B.D. Welch, N.G. Carlson, H. Shi, L. Myatt, and B.K. Kishore P2Y2 receptor-stimulated release of prostaglandin E2 by rat inner medullary collecting duct preparations Am. J. Physiol., Renal Fluid Electrolyte Physiol. 285 2003 F711 F721
79. S.A. Willis, and P.D. Nisen Inhibition of lipopolysaccharide-induced IL-1 beta transcription by cyclic adenosine monophosphate in human astrocytic cells J. Immunol. 154 1995 1399 1406
80. J. Xu, M. Chalimoniuk, Y. Shu, A. Simonyi, A.Y. Sun, F.A. Gonzalez, G.A. Weisman, W.G. Wood, and G.Y. Sun Prostaglandin E2 production in astrocytes: regulation by cytokines, extracellular ATP, and oxidative agents Prostaglandins, Leukot. Essent. Fat. Acids 69 2003 437 448