The P2X7-Egr pathway regulates nucleotide-dependent inflammatory gene expression in microglia

GLIA

Volumn 59, Issue 1, 2011, Pages 1-13

  Friedle, S A ^a   Brautigam, V M ^b   Nikodemova, M ^b   Wright, M L ^b   Watters, J J ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Adenine nucleotides; Cytokine; Gene transcription

Indexed keywords

3' O (4 BENZOYLBENZOYL)ADENOSINE TRIPHOSPHATE; EARLY GROWTH RESPONSE FACTOR 1; EARLY GROWTH RESPONSE FACTOR 2; EARLY GROWTH RESPONSE FACTOR 3; INDUCIBLE NITRIC OXIDE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; PURINERGIC P2X7 RECEPTOR;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CYTOKINE RELEASE; GENE EXPRESSION; GENE INDUCTION; GENETIC TRANSCRIPTION; MICROGLIA; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA INTERFERENCE;

ADENOSINE TRIPHOSPHATE; ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CELL LINE; CELLS, CULTURED; EARLY GROWTH RESPONSE TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; INFLAMMATION; LIPOPOLYSACCHARIDES; MICE; MICROGLIA; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NITRIC OXIDE SYNTHASE TYPE II; NUCLEOTIDES; RECEPTORS, PURINERGIC P2X7; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 78349284376     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21071     Document Type: Article

References (66)

1. Aga M, Johnson CJ, Hart AP, Guadarrama AG, Suresh M, Svaren J, Bertics PJ, Darien BJ. 2002. Modulation of monocyte signaling and pore formation in response to agonists of the nucleotide receptor P2X(7). J Leuk Biol 72: 222-232.
2. Aga M, Watters JJ, Pfeiffer ZA, Wiepz GJ, Sommer JA, Bertics PJ. 2004. 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: C923-C930.
3. Aloisi F, De Simone R, Columba-Cabezas S, Levi G. 1999. Opposite effects of interferon-gamma and prostaglandin E2 on tumor necrosis factor and interleukin-10 production in microglia: A regulatory loop controlling microglia pro- and anti-inflammatory activities. J Neurosci Res 56: 571-580.
4. Baker AE, Brautigam VM, Watters JJ. 2004. Estrogen modulates microglial inflammatory mediator production via interactions with estrogen receptor {beta}. Endocrinology 145: 5021-5032.
5. Beigi RD, Kertesy SB, Aquilina G, Dubyak GR. 2003. Oxidized ATP (oATP) attenuates proinflammatory signaling via P2 receptor-independent mechanisms. Br J Pharmacol 140: 507-519.
6. Bhat NR, Zhang P, Lee JC, Hogan EL. 1998. Extracellular signal-regulated kinase and p38 subgroups of mitogen-activated protein kinases regulate inducible nitric oxide synthase and tumor necrosis factor-alpha gene expression in endotoxin-stimulated primary glial cultures. J Neurosci 18: 1633-1641.
7. Bianchi BR, Lynch KJ, Touma E, Niforatos W, Burgard EC, Alexander KM, Park HS, Yu H, Metzger R, Kowaluk E. 1999. Pharmacological characterization of recombinant human and rat P2X receptor subtypes. Eur J Pharmacol 376: 127-138.
8. Boucsein C, Zacharias R, Farber K, Pavlovic S, Hanisch UK, Kettenmann H. 2003. Purinergic receptors on microglial cells: Functional expression in acute brain slices and modulation of microglial activation in vitro. Eur J Neurosci 17: 2267-2276.
9. Brautigam VM, Frasier C, Nikodemova M, Watters JJ. 2005. Purinergic receptor modulation of BV-2 microglial cell activity: Potential involvement of p38 MAP kinase and CREB. J Neuroimmunol 166: 113.
10. Burnstock G, Knight GE. 2004. Cellular distribution and functions of P2 receptor subtypes in different systems. International Review of Cytology 240: 31-304.
11. Chessell IP, Hatcher JP, Bountra C, Michel AD, Hughes JP, Green P, Egerton J, Murfin M, Richardson J, Peck WL, Grahames CBA, Casula MA, Yiangou Y, Birch R, Anand P, Buell GN. 2005. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 114: 386.
12. Chiueh CC. 1999. Neuroprotective properties of nitric oxide. Ann N Y Acad Sci 890: 301-311.
13. Ciesielski-Treska J, Ulrich G, Chasserot-Golaz S, Zwiller J, Revel M-O, Aunis D, Bader M-F. 2001. Mechanisms underlying neuronal death induced by chromogranin A-activated microglia. J Biol Chem 276: 13113-13120.
14. Decker EL, Nehmann N, Kampen E, Eibel H, Zipfel PF, Skerka C. 2003. Early growth response proteins (EGR) and nuclear factors of activated T cells (NFAT) form heterodimers and regulate proinflammatory cytokine gene expression. Nucl Acids Res 31: 911-921.
15. Ferrari D, Stroh C, Schulze-Osthoff K. 1999. P2X7/P2Z purinoreceptor-mediated activation of transcription factor NFAT in microglial cells. J Biol Chem 274: 13205-13210.
16. Ferrari D, Villalba M, Chiozzi P, Falzoni S, Ricciardi-Castagnoli P, Di Virgilio F. 1996. Mouse microglial cells express a plasma membrane pore gated by extracellular ATP. J Immunol 156: 1531-1539.
17. Ferrari D, Wesselborg S, Bauer MK, Schulze-Osthoff K. 1997. Extracellular ATP activates transcription factor NF-kappaB through the P2Z purinoreceptor by selectively targeting NF-kappaB p 65. J Cell Biol 139: 1635-1643.
18. Gerasimovskaya EV, Ahmad S, White CW, Jones PL, Carpenter TC, Stenmark KR. 2002. Extracellular ATP is an autocrine/paracrine regulator of hypoxia-induced adventitial fibroblast growth. signaling through extracellular signal-regulated kinase-1/2 and the Egr-1 transcription factor. J Biol Chem 277: 44638-44650.
19. Gu BJ, Wiley JS. 2006. Rapid ATP-induced release of matrix metalloproteinase 9 is mediated by the P2X7 receptor. Blood 107: 4946-4953.
20. Harada H, Lama VN, Badri LN, Ohtsuka T, Petrovic-Djergovic D, Liao H, Yoshikawa Y, Iwanaga K, Lau CL, Pinsky DJ. 2007. Early growth response gene-1 promotes airway allograft rejection. Am J Physiol Lung Cell Mol Physiol 293: L124-L130.
21. Hide I, Tanaka M, Inoue A, Nakajima K, Kohsaka S, Inoue K, Nakata Y. 2000. Extracellular ATP triggers tumor necrosis factor-alpha release from rat microglia. J Neurochem 75: 965-972.
22. Hipskind RA, Baccarini M, Nordheim A. 1994. Transient activation of RAF-1, MEK, and ERK2 coincides kinetically with ternary complex factor phosphorylation and immediate-early gene promoter activity in vivo. Mol Cell Biol 14: 6219-6231.
23. Hoffmann E, Ashouri J, Wolter S, Doerrie A, Dittrich-Breiholz O, Schneider H, Wagner EF, Troppmair J, Mackman N, Kracht M. 2008. Transcriptional regulation of EGR-1 by the interleukin-1-JNK-MKK7-c-Jun pathway. J Biol Chem 283: 12120-12128.
24. Hur J, Lee P, Kim MJ, Kim Y, Cho Y-W. 2010. Ischemia-activated microglia induces neuronal injury via activation of gp91phox NADPH oxidase. Biochem Biophys Res Commun 391: 1526-1530.
25. Inoue K, Nakajima K, Morimoto T, Kikuchi Y, Koizumi S, Illes P, Kohsaka S. 1998. ATP stimulation of Ca2+-dependent plasminogen release from cultured microglia. Br J Pharmacol 123: 1304-1310.
26. Kataoka A, Tozaki-Saitoh H, Koga Y, Tsuda M, Inoue K. 2009. Activation of P2X7 receptors induces CCL3 production in microglial cells through transcription factor NFAT. J Neurochem 108: 115-125.
27. Kim CG, Choi BH, Son SW, Yi SJ, Shin SY, Lee YH. 2007. Tamoxifen-induced activation of p21Waf1/Cip1 gene transcription is mediated by early growth response-1 protein through the JNK, p 38 MAP kinase/Elk-1 cascades in MDA-MB-361 breast carcinoma cells. Cell Signal 19: 1290-1300.
28. Lim CP, Jain N, Cao X. 1998. Stress-induced immediate-early gene, egr-1, involves activation of p38/JNK1. Oncogene 16: 2915-2926.
29. Liu C, Adamson E, Mercola D. 1996a. Transcription factor EGR-1 suppresses the growth and transformation of human HT-1080 fibrosarcoma cells by induction of transforming growth factor beta 1. Proc Natl Acad Sci USA 93: 11831-11836.
30. Liu C, Calogero A, Ragona G, Adamson E, Mercola D. 1996b. EGR-1, the reluctant suppression factor: EGR-1 is known to function in the regulation of growth, differentiation, and also has significant tumor suppressor activity and a mechanism involving the induction of TGF-beta1 is postulated to account for this suppressor activity. Crit Rev Oncog 7: 101-125.
31. Lo LW, Cheng JJ, Chiu JJ, Wung BS, Liu YC, Wang DL. 2001. Endothelial exposure to hypoxia induces Egr-1 expression involving PKCalpha-mediated Ras/Raf-1/ERK1/2 pathway. J Cell Physiol 188: 304-312.
32. McCubrey JA, May WS, Duronio V, Mufson A. 2000. Serine/threonine phosphorylation in cytokine signal transduction. Leukemia 14: 9-21.
33. Mechta-Grigoriou F, Garel S, Charnay P. 2000. Nab proteins mediate a negative feedback loop controlling Krox-20 activity in the developing hindbrain. Development 127: 119-128.
34. Mitchell JA, Kohlhaas KL, Matsumoto T, Pollock JS, Forstermann U, Warner TD, Schmidt HH, Murad F. 1992. Induction of NADPH-dependent diaphorase and nitric oxide synthase activity in aortic smooth muscle and cultured macrophages. Mol Pharmacol 41: 1163-1168.
35. Morganti-Kossmann MC, Satgunaseelan L, Bye N, Kossmann T. 2007. Modulation of immune response by head injury. Injury 38: 1392-1400.
36. Morigiwa K, Quan M, Murakami M, Yamashita M, Fukuda Y. 2000. P2 Purinoceptor expression and functional changes of hypoxia-activated cultured rat retinal microglia. Neurosci Lett 282: 153-156.
37. Nagarajan R, Svaren J, Le N, Araki T, Watson M, Milbrandt J. 2001. EGR2 mutations in inherited neuropathies dominant-negatively inhibit myelin gene expression. Neuron 30: 355-368.
38. Nikodemova M, Duncan ID, Watters JJ. 2006. Minocycline exerts inhibitory effects on multiple mitogen-activated protein kinases and IkappaB alpha degradation in a stimulus-specific manner in microglia. J Neurochem 96: 314-323.
39. North RA. 2002. Molecular physiology of P2X receptors. Physiol Rev 82: 1013-1067.
40. Ogata T, Chuai M, Morino T, Yamamoto H, Nakamura Y, Schubert P. 2003. Adenosine triphosphate inhibits cytokine release from lipopolysaccharide-activated microglia via P2y receptors. Brain Res 981: 174.
41. Park JA, Koh JY. 1999. Induction of an immediate early gene egr-1 by zinc through extracellular signal-regulated kinase activation in cortical culture: Its role in zinc-induced neuronal death. J Neurochem 73: 450-456.
42. Pawlinski R, Pedersen B, Kehrle B, Aird WC, Frank RD, Guha M, Mackman N. 2003. Regulation of tissue factor and inflammatory mediators by Egr-1 in a mouse endotoxemia model. Blood 101: 3940-3947.
43. Perregaux DG, McNiff P, Laliberte R, Conklyn M, Gabel CA. 2000. ATP acts as an agonist to promote stimulus-induced secretion of IL-1{beta} and IL-18 in human blood. J Immunol 165: 4615-4623.
44. Potucek YD, Crain JM, Watters JJ. 2006. Purinergic receptors modulate MAP kinases and transcription factors that control microglial inflammatory gene expression. Neurochem Int 49: 204-214.
45. Prince JM, Ming MJ, Levy RM, Liu S, Pinsky DJ, Vodovotz Y, Billiar TR. 2007. Early growth response 1 mediates the systemic and hepatic inflammatory response initiated by hemorrhagic shock. Shock 27: 157-164.
46. Rampe D, Wang L, Ringheim GE. 2004. P2X7 receptor modulation of β-amyloid- and LPS-induced cytokine secretion from human macrophages and microglia. J Neuroimmunol 147: 56.
47. Righi M, Mori L, De Libero G, Sironi M, Biondi A, Mantovani A, Donini SD, Ricciardi-Castagnoli P. 1989. Monokine production by microglial cell clones. Eur J Immunol 19: 1443-1448.
48. Rolli-Derkinderen M, Gaestel M. 2000. p38/SAPK2-dependent gene expression in Jurkat T cells. Biol Chem 381: 193-198.
49. Schaefer A, Kósa F, Bittorf T, Magócsi M, Rosche A, Ramirez-Chávez Y, Marotzki S, Marquardt H. 2004. Opposite effects of inhibitors of mitogen-activated protein kinase pathways on the egr-1 and β-globin expression in erythropoietin-responsive murine erythroleukemia cells. Cellular Signalling 16: 223.
50. Seo DR, Kim SY, Kim KY, Lee HG, Moon JH, Lee JS, Lee SH, Kim SU, Lee YB. 2008. Cross talk between P2 purinergic receptors modulates extracellular ATP-mediated interleukin-10 production in rat microglial cells. Exp Mol Med 40: 19-26.
51. Shi L, Kishore R, McMullen MR, Nagy LE. 2002. Lipopolysaccharide stimulation of ERK1/2 increases TNF-alpha production via Egr-1. Am J Physiol Cell Physiol 282: C1205-C1211.
52. Shigemoto-Mogami Y, Koizumi S, Tsuda M, Ohsawa K, Kohsaka S, Inoue K. 2001. Mechanisms underlying extracellular ATP-evoked interleukin-6 release in mouse microglial cell line, MG-5. J Neurochem 78: 1339-1349.
53. Shin SY, Lee JH, Min B, Lee YH. 2006. The translation inhibitor anisomycin induces Elk-1-mediated transcriptional activation of egr-1 through multiple mitogen-activated protein kinase pathways. Exp Mol Med 38: 677-685.
54. Stefano L, Rossler OG, Griesemer D, Hoth M, Thiel G. 2007. P2X(7) receptor stimulation upregulates Egr-1 biosynthesis involving a cytosolic Ca(2+) rise, transactivation of the EGF receptor and phosphorylation of ERK, Elk-1. J Cell Physiol 213: 36-44.
55. Stoll G, Jander S, Schroeter M. 2000. Cytokines in CNS disorders: Neurotoxicity versus neuroprotection. J Neural Trans Suppl 59: 81-89.
56. Trang T, Beggs S, Wan X, Salter MW. 2009. P2X4-receptor-mediated synthesis and release of brain-derived neurotrophic factor in microglia is dependent on calcium and p38-mitogen-activated protein kinase activation. J Neurosci 29: 3518-3528.
57. Tsai EY, Falvo JV, Tsytsykova AV, Barczak AK, Reimold AM, Glimcher LH, Fenton MJ, Gordon DC, Dunn IF, Goldfeld AE. 2000. A lipopolysaccharide-specific enhancer complex involving Ets, Elk-1, Sp1, and CREB binding protein and p300 is recruited to the tumor necrosis factor alpha promoter in vivo. Mol Cell Biol 20: 6084-6094.
58. Ulmann L, Hatcher JP, Hughes JP, Chaumont S, Green PJ, Conquet F, Buell GN, Reeve AJ, Chessell IP, Rassendren F. 2008. Up-regulation of P2X4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J Neurosci 28: 11263-11268.
59. Watters JJ, Sommer JA, Fisette PL, Pfeiffer ZA, Aga M, Prabhu U, Guerra A, Denlinger LC, Bertics PJ. 2001. The P2X7 nucleotide receptor: Modulation of LPS-induced macrophage signaling and mediator production. Drug Dev Res 53: 91-104.
60. Watters JJ, Sommer JA, Pfeiffer ZA, Prabhu U, Guerra AN, Bertics PJ. 2002. 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: 9077-9087.
61. Wei W, Ryu JK, Choi HB, McLarnon JG. 2008. Expression and function of the P2X7 receptor in rat C6 glioma cells. Cancer Lett 260: 79.
62. Williams LM, Lali F, Willetts K, Balague C, Godessart N, Brennan F, Feldmann M, Foxwell BMJ. 2008. Rac mediates TNF-induced cytokine production via modulation of NF-κB. Mol Immunol 45: 2446.
63. Worden B, Yang XP, Lee TL, Bagain L, Yeh NT, Cohen JG, Van Waes C, Chen Z. 2005. Hepatocyte growth factor/scatter factor differentially regulates expression of proangiogenic factors through Egr-1 in head and neck squamous cell carcinoma. Cancer Res 65: 7071-7080.
64. Wu Q, Combs C, Cannady SB, Geldmacher DS, Herrup K. 2000. Beta-amyloid activated microglia induce cell cycling and cell death in cultured cortical neurons. Neurobiol Aging 21: 797-806.
65. Yao J, Mackman N, Edgington TS, Fan ST. 1997. Lipopolysaccharide induction of the tumor necrosis factor-alpha promoter in human monocytic cells. Regulation by Egr-1, c-Jun, and NF-kappaB transcription factors. J Biol Chem 272: 17795-17801.
66. Yoon S, Seger R, Choi EJ, Yoo YS. 2004. SB203580 induces prolonged B-Raf activation and promotes neuronal differentiation upon EGF treatment of PC12 cells. Biochemistry (Mosc) 69: 799-805.