ATP-P2X 7 receptor signaling controls basal and TNFα-stimulated glial cell proliferation

GLIA

Volumn 60, Issue 4, 2012, Pages 661-673

  Zou, Jian ^a   Vetreno, Ryan P ^a   Crews, Fulton T ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Cytokines; Microglia; Neuroinflammation; Progenitor; Purinergic signaling

Indexed keywords

1 [N,O BIS(5 ISOQUINOLINESULFONYL) N METHYLTYROSYL] 4 PHENYLPIPERAZINE; ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE P2X7 RECEPTOR; APYRASE; AQUAPORIN 4; BROXURIDINE; MESSENGER RNA; PROTEIN KINASE C; PURINERGIC P2X7 RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; 3' O (4 BENZOYL)BENZOYLADENOSINE 5' TRIPHOSPHATE; 3'-O-(4-BENZOYL)BENZOYLADENOSINE 5'-TRIPHOSPHATE; ACTIN BINDING PROTEIN; ADENOSINE TRIPHOSPHATASE; AIF1 PROTEIN, RAT; AQP4 PROTEIN, RAT; CALCIUM BINDING PROTEIN; DRUG DERIVATIVE; ENZYME INHIBITOR; IVERMECTIN; PURINERGIC P2X RECEPTOR AGONIST; PURINERGIC P2X RECEPTOR ANTAGONIST; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; ATTENUATION; BRAIN SLICE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENTORHINAL CORTEX; GLIA CELL; HIPPOCAMPUS; HYDROLYSIS; IMMUNOREACTIVITY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; ANIMAL; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; GENE INACTIVATION; GLIA; IN VITRO STUDY; METABOLISM; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TIME;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; ANIMALS, NEWBORN; AQUAPORIN 4; BROMODEOXYURIDINE; CALCIUM-BINDING PROTEINS; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENTORHINAL CORTEX; ENZYME INHIBITORS; GENE KNOCKOUT TECHNIQUES; HIPPOCAMPUS; IVERMECTIN; MICROFILAMENT PROTEINS; NEUROGLIA; ORGAN CULTURE TECHNIQUES; PURINERGIC P2X RECEPTOR AGONISTS; PURINERGIC P2X RECEPTOR ANTAGONISTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC P2X7; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84856722373     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22302     Document Type: Article

References (75)

1. Alexander JJ, Jacob A, Cunningham P, Hensley L, Quigg RJ. 2008. TNF is a key mediator of septic encephalopathy acting through its receptor, TNF receptor-1. Neurochem Int 52: 447-456.
2. Arnett HA, Mason J, Marino M, Suzuki K, Matsushima GK, Ting JP. 2001. TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat Neurosci 4: 1116-1122.
3. Baricordi OR, Melchiorri L, Adinolfi E, Falzoni S, Chiozzi P, Buell G, Di Virgilio F. 1999. Increased proliferation rate of lymphoid cells transfected with the P2X(7) ATP receptor. J Biol Chem 274: 33206-33208.
4. Bianco F, Ceruti S, Colombo A, Fumagalli M, Ferrari D, Pizzirani C, Matteoli M, Di Virgilio F, Abbracchio MP, Verderio C. 2006. A role for P2X7 in microglial proliferation. J Neurochem 99: 745-758.
5. Cacci E, Claasen JH, Kokaia Z. 2005. Microglia-derived tumor necrosis factor-alpha exaggerates death of newborn hippocampal progenitor cells in vitro. J Neurosci Res 80: 789-797.
6. Cavazzin C, Ferrari D, Facchetti F, Russignan A, Vescovi AL, La Porta CA, Gritti A. 2006. Unique expression and localization of aquaporin-4 and aquaporin-9 in murine and human neural stem cells and in their glial progeny. Glia 53: 167-181.
7. Choi HB, Ryu JK, Kim SU, McLarnon JG. 2007. Modulation of the purinergic P2X7 receptor attenuates lipopolysaccharide-mediated microglial activation and neuronal damage in inflamed brain. J Neurosci 27: 4957-4968.
8. Crews F, Nixon K, Kim D, Joseph J, Shukitt-Hale B, Qin L, Zou J. 2006. BHT blocks NF-kappaB activation and ethanol-induced brain damage. Alcohol Clin Exp Res 30: 1938-1949.
9. Dheen ST, Kaur C, Ling EA. 2007. Microglial activation and its implications in the brain diseases. Curr Med Chem 14: 1189-1197.
10. Di Virgilio F, Chiozzi P, Ferrari D, Falzoni S, Sanz JM, Morelli A, Torboli M, Bolognesi G, Baricordi OR. 2001. Nucleotide receptors: An emerging family of regulatory molecules in blood cells. Blood 97: 587-600.
11. Diaz-Hernandez M, Diez-Zaera M, Sanchez-Nogueiro J, Gomez-Villafuertes R, Canals JM, Alberch J, Miras-Portugal MT, Lucas JJ. 2009. Altered P2X7-receptor level and function in mouse models of Huntington's disease and therapeutic efficacy of antagonist administration. Faseb J 23: 1893-1906.
12. Donnelly-Roberts DL, Namovic MT, Faltynek CR, Jarvis MF. 2004. Mitogen-activated protein kinase and caspase signaling pathways are required for P2X7 receptor (P2X7R)-induced pore formation in human THP-1 cells. J Pharmacol Exp Ther 308: 1053-1061.
13. Donnelly-Roberts DL, Namovic MT, Han P, Jarvis MF. 2009. Mammalian P2X7 receptor pharmacology: Comparison of recombinant mouse, rat and human P2X7 receptors. Br J Pharmacol 157: 1203-1214.
14. Eng LF, Ghirnikar RS. 1994. GFAP and astrogliosis. Brain Pathol 4: 229-237.
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, Chiozzi P, Falzoni S, Dal Susino M, Collo G, Buell G, Di Virgilio F. 1997. ATP-mediated cytotoxicity in microglial cells. Neuropharmacology 36: 1295-1301.
17. Fields RD, Burnstock G. 2006. Purinergic signalling in neuron-glia interactions. Nat Rev Neurosci 7: 423-436.
18. Gargett CE, Wiley JS. 1997. The isoquinoline derivative KN-62 a potent antagonist of the P2Z-receptor of human lymphocytes. Br J Pharmacol 120: 1483-1490.
19. Griffin WS. 2006. Inflammation and neurodegenerative diseases. Am J Clin Nutr 83: 470S-474S.
20. Gudipaty L, Munetz J, Verhoef PA, Dubyak GR. 2003. Essential role for Ca2+ in regulation of IL-1beta secretion by P2X7 nucleotide receptor in monocytes, macrophages, and HEK-293 cells. Am J Physiol Cell Physiol 285: C286-C299.
21. Hibell AD, Thompson KM, Xing M, Humphrey PP, Michel AD. 2001. Complexities of measuring antagonist potency at P2X(7) receptor orthologs. J Pharmacol Exp Ther 296: 947-957.
22. 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.
23. Humphreys BD, Virginio C, Surprenant A, Rice J, Dubyak GR. 1998. Isoquinolines as antagonists of the P2X7 nucleotide receptor: High selectivity for the human versus rat receptor homologues. Mol Pharmacol 54: 22-32.
24. Inoue K, Tsuda M. 2009. Microglia and neuropathic pain. Glia 57: 1469-1479.
25. Iosif RE, Ekdahl CT, Ahlenius H, Pronk CJ, Bonde S, Kokaia Z, Jacobsen SE, Lindvall O. 2006. Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J Neurosci 26: 9703-9712.
26. Jung JS, Bhat RV, Preston GM, Guggino WB, Baraban JM, Agre P. 1994. Molecular characterization of an aquaporin cDNA from brain: Candidate osmoreceptor and regulator of water balance. Proc Natl Acad Sci USA 91: 13052-13056.
27. Katakowski M, Chen J, Zhang ZG, Santra M, Wang Y, Chopp M. 2007. Stroke-induced subventricular zone proliferation is promoted by tumor necrosis factor-alpha-converting enzyme protease activity. JCereb Blood Flow Metab 27: 669-678.
28. Klassen HJ, Imfeld KL, Kirov, II, Tai L, Gage FH, Young MJ, Berman MA. 2003. Expression of cytokines by multipotent neural progenitor cells. Cytokine 22: 101-106.
29. Kleindienst A, Fazzina G, Amorini AM, Dunbar JG, Glisson R, Marmarou A. 2006. Modulation of AQP4 expression by the protein kinase C activator, phorbol myristate acetate, decreases ischemia-induced brain edema. Acta neurochirurgica Suppl 96: 393-397.
30. Kong H, Sha LL, Fan Y, Xiao M, Ding JH, Wu J, Hu G. 2009. Requirement of AQP4 for antidepressive efficiency of fluoxetine: implication in adult hippocampal neurogenesis. Neuropsychopharmacology 34: 1263-1276.
31. Kong H, Fan Y, Xie J, Ding J, Sha L, Shi X, Sun X, Hu G. 2008. AQP4 knockout impairs proliferation, migration and neuronal differentiation of adult neural stem cells. J Cell Sci 121: 4029-4036.
32. Kuppers E, Gleiser C, Brito V, Wachter B, Pauly T, Hirt B, Grissmer S. 2008. AQP4 expression in striatal primary cultures is regulated by dopamine-Implications for proliferation of astrocytes. Eur J Neurosci 28: 2173-2182.
33. La Porta CA, Gena P, Gritti A, Fascio U, Svelto M, Calamita G. 2006. Adult murine CNS stem cells express aquaporin channels. Biol Cell 98: 89-94.
34. Lambrecht G. 2000. Agonists and antagonists acting at P2X receptors: selectivity profiles and functional implications. Naunyn Schmiedebergs Arch Pharmacol 362: 340-350.
35. Lee M, Lee SJ, Choi HJ, Jung YW, Frokiaer J, Nielsen S, Kwon TH. 2008. Regulation of AQP4 protein expression in rat brain astrocytes: Role of P2X7 receptor activation. Brain Res 1195: 1-11.
36. Lister MF, Sharkey J, Sawatzky DA, Hodgkiss JP, Davidson DJ, Rossi AG, Finlayson K. 2007. The role of the purinergic P2X7 receptor in inflammation. J Inflamm (Lond) 4: 5.
37. Mander PK, Jekabsone A, Brown GC. 2006. Microglia proliferation is regulated by hydrogen peroxide from NADPH oxidase. J Immunol 176: 1046-1052.
38. McCoy MK, Tansey MG. 2008. TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. J Neuroinflammation 5: 45.
39. McLarnon JG, Ryu JK, Walker DG, Choi HB. 2006. Upregulated expression of purinergic P2X(7) receptor in Alzheimer disease and amyloid-beta peptide-treated microglia and in peptide-injected rat hippocampus. J Neuropathol Exp Neurol 65: 1090-1097.
40. Michel AD, Clay WC, Ng SW, Roman S, Thompson K, Condreay JP, Hall M, Holbrook J, Livermore D, Senger S. 2008. Identification of regions of the P2X(7) receptor that contribute to human and rat species differences in antagonist effects. Br J Pharmacol 155: 738-751.
41. Monif M, Reid CA, Powell KL, Smart ML, Williams DA. 2009. The P2X7 receptor drives microglial activation and proliferation: A trophic role for P2X7R pore. J Neurosci 29: 3781-3791.
42. Monje ML, Toda H, Palmer TD. 2003. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302: 1760-1765.
43. Namba T, Mochizuki H, Onodera M, Namiki H, Seki T. 2007. Postnatal neurogenesis in hippocampal slice cultures: Early in vitro labeling of neural precursor cells leads to efficient neuronal production. J Neurosci Res 85: 1704-1712.
44. Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP. 1997. Specialized membrane domains for water transport in glial cells: High-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 17: 171-180.
45. Nixon K, Crews FT. 2002. Binge ethanol exposure decreases neurogenesis in adult rat hippocampus. J Neurochem 83: 1087-1093.
46. Noraberg J, Poulsen FR, Blaabjerg M, Kristensen BW, Bonde C, Montero M, Meyer M, Gramsbergen JB, Zimmer J. 2005. Organotypic hippocampal slice cultures for studies of brain damage, neuroprotection and neurorepair. Curr Drug Targets CNS Neurol Disord 4: 435-452.
47. Parvathenani LK, Tertyshnikova S, Greco CR, Roberts SB, Robertson B, Posmantur R. 2003. P2X7 mediates superoxide production in primary microglia and is up-regulated in a transgenic mouse model of Alzheimer's disease. J Biol Chem 278: 13309-13317.
48. Peng J, He F, Zhang C, Deng X, Yin F. 2011. Protein kinase C-alpha signals P115RhoGEF phosphorylation and RhoA activation in TNF-alpha-induced mouse brain microvascular endothelial cell barrier dysfunction. J Neuroinflammation 8: 28.
49. Peng W, Cotrina ML, Han X, Yu H, Bekar L, Blum L, Takano T, Tian GF, Goldman SA, Nedergaard M. 2009. Systemic administration of an antagonist of the ATP-sensitive receptor P2X7 improves recovery after spinal cord injury. Proc Natl Acad Sci USA 106: 12489-12493.
50. Ralevic V, Burnstock G. 1998. Receptors for purines and pyrimidines. Pharmacol Rev 50: 413-492.
51. Raouf R, Chabot-Dore AJ, Ase AR, Blais D, Seguela P. 2007. Differential regulation of microglial P2X4 and P2X7 ATP receptors following LPS-induced activation. Neuropharmacology 53: 496-504.
52. Robel S, Berninger B, Gotz M. 2011. The stem cell potential of glia: lessons from reactive gliosis. Nat Rev Neurosci 12: 88-104.
53. Rojo LE, Fernandez JA, Maccioni AA, Jimenez JM, Maccioni RB. 2008. Neuroinflammation: implications for the pathogenesis and molecular diagnosis of Alzheimer's disease. Arch Med Res 39: 1-16.
54. Saadoun S, Papadopoulos MC, Watanabe H, Yan D, Manley GT, Verkman AS. 2005. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J Cell Sci 118: 5691-5698.
55. Scholz J, Woolf CJ. 2007. The neuropathic pain triad: Neurons, immune cells and glia. Nat Neurosci 10: 1361-1368.
56. St Hillaire C, Vargas D, Pardo CA, Gincel D, Mann J, Rothstein JD, McArthur JC, Conant K. 2005. Aquaporin 4 is increased in association with human immunodeficiency virus dementia: implications for disease pathogenesis. J Neurovirol 11: 535-543.
57. Stoppini L, Buchs PA, Muller D. 1991. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37: 173-182.
58. Surprenant A, Rassendren F, Kawashima E, North RA, Buell G. 1996. The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 272: 735-738.
59. Tansey MG, Goldberg MS. 2010. Neuroinflammation in Parkinson's disease: Its role in neuronal death and implications for therapeutic intervention. Neurobiol Dis 37: 510-518.
60. Thrane AS, Rappold PM, Fujita T, Torres A, Bekar LK, Takano T, Peng W, Wang F, Thrane VR, Enger R, Haj-Yasein NN, Skare O, Holen T, Klungland A, Ottersen OP, Nedergaard M, Nagelhus EA. 2011. Critical role of aquaporin-4 (AQP4) in astrocytic Ca2+ signaling events elicited by cerebral edema. Proc Natl Acad Sci USA 108: 846-851.
61. Tomas-Camardiel M, Venero JL, de Pablos RM, Rite I, Machado A, Cano J. 2004. In vivo expression of aquaporin-4 by reactive microglia. J Neurochem 91: 891-899.
62. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415: 1030-1034.
63. Virginio C, MacKenzie A, Rassendren FA, North RA, Surprenant A. 1999. Pore dilation of neuronal P2X receptor channels. Nat Neurosci 2: 315-321.
64. Wajant H. 2003. Death receptors. Essays in biochemistry 39: 53-71.
65. Widera D, Mikenberg I, Elvers M, Kaltschmidt C, Kaltschmidt B. 2006. Tumor necrosis factor alpha triggers proliferation of adult neural stem cells via IKK/NF-kappaB signaling. BMC Neurosci 7: 64.
66. Witting A, Walter L, Wacker J, Moller T, Stella N. 2004. P2X7 receptors control 2-arachidonoylglycerol production by microglial cells. Proc Natl Acad Sci USA 101: 3214-3219.
67. Wu JP, Kuo JS, Liu YL, Tzeng SF. 2000. Tumor necrosis factor-alpha modulates the proliferation of neural progenitors in the subventricular/ventricular zone of adult rat brain. Neurosci Lett 292: 203-206.
68. Xiang Z, Burnstock G. 2005. Expression of P2X receptors on rat microglial cells during early development. Glia 52: 119-126.
69. Xie LL, Sun XL, Fan Y, Kong H, Ding JH, Hu G. 2009. Aquaporin 4 knockout resists negative regulation of neural cell proliferation by cocaine in mouse hippocampus. Int J Neuropsychopharmacol: 1-8.
70. Yu L, Miao H, Hou Y, Zhang B, Guo L. 2006. Neuroprotective effect of A20 on TNF-induced postischemic apoptosis. Neurochem Res 31: 21-32.
71. Yu Y, Ugawa S, Ueda T, Ishida Y, Inoue K, Kyaw Nyunt A, Umemura A, Mase M, Yamada K, Shimada S. 2008. Cellular localization of P2X7 receptor mRNA in the rat brain. Brain Res 1194: 45-55.
72. Zhou X, Yang W, Li J. 2006. Ca2+- and protein kinase C-dependent signaling pathway for nuclear factor-kappaB activation, inducible nitric-oxide synthase expression, and tumor necrosis factor-alpha production in lipopolysaccharide-stimulated rat peritoneal macrophages. J Biol Chem 281: 31337-31347.
73. Zou J, Crews F. 2006. CREB and NF-kappaB transcription factors regulate sensitivity to excitotoxic and oxidative stress induced neuronal cell death. Cell Mol Neurobiol 26: 385-405.
74. Zou J, Crews F. 2010. Induction of innate immune gene expression cascades in brain slice cultures by ethanol: Key role of NF-kappaB and proinflammatory cytokines. Alcoholism Clin Exp Res 34: 777-789.
75. Zou JY, Crews FT. 2005. TNF alpha potentiates glutamate neurotoxicity by inhibiting glutamate uptake in organotypic brain slice cultures: Neuroprotection by NF kappa B inhibition. Brain Res 1034: 11-24.