P2X7-dependent, but differentially regulated release of IL-6, CCL2, and TNF-α in cultured mouse microglia

GLIA

Volumn 62, Issue 4, 2014, Pages 592-607

  Shieh, Chu Hsin ^a,b   Heinrich, Annette ^b   Serchov, Tsvetan ^b   van Calker, Dietrich ^b   Biber, Knut ^b,c  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Antagonists; Neuroinflammation; Neuroprotection; Purine receptors

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 6; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y1 RECEPTOR; PURINERGIC P2Y12 RECEPTOR; PURINERGIC P2Y13 RECEPTOR; PURINERGIC P2Y2 RECEPTOR; PURINERGIC P2Y6 RECEPTOR; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID; SURAMIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; EXTRACELLULAR CALCIUM; GENE EXPRESSION; MICROGLIAL CELL CULTURE; MOUSE; NONHUMAN; PRIMARY CELL CULTURE; PRIORITY JOURNAL; RECEPTOR BLOCKING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ANTAGONISTS; NEUROINFLAMMATION; NEUROPROTECTION; PURINE RECEPTORS;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANIMALS, NEWBORN; BRAIN; CALCIUM; CELL DIFFERENTIATION; CELLS, CULTURED; CHEMOKINE CCL2; CONNEXINS; DOSE-RESPONSE RELATIONSHIP, DRUG; INTERLEUKIN-6; MICE; MICE, INBRED C57BL; MICROGLIA; NERVE TISSUE PROTEINS; PURINERGIC P2X RECEPTOR AGONISTS; PURINERGIC P2X RECEPTOR ANTAGONISTS; RECEPTORS, PURINERGIC P2X4; RECEPTORS, PURINERGIC P2X7; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84893739709     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22628     Document Type: Article

References (65)

1. Adinolfi E, Cirillo M, Woltersdorf R, Falzoni S, Chiozzi P, Pellegatti P, Callegari MG, Sandona D, Markwardt F, Schmalzing G, di Virgillio F. 2010. Trophic activity of a naturally occurring truncated isoform of the P2X7 receptor. FASEB J 24:3393-3404.
2. Aguzzi A, Barres BA, Bennett ML. 2013. Microglia: scapegoat, saboteur, or something else? Science 339:156-161.
3. Ajami B, Bennett JL, Krieger C, Tetzlaff W, Rossi FM. 2007. Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 10:1538-1543.
4. Alam MS, Kurtz CC, Wilson JM, Burnette BR, Wiznerowicz EB, Ross WG, Rieger JM, Figler RA, Linden J, Crowe SE, di Virgillio F. 2009. A2A adenosine receptor (AR) activation inhibits pro-inflammatory cytokine production by human CD4+ helper T cells and regulates Helicobacter-induced gastritis and bacterial persistence. Mucosal Immunol 2:232-242.
5. Barrera NP, Henderson RM, Murrell-Lagnado RD, Edwardson JM. 2007. The stoichiometry of P2X2/6 receptor heteromers depends on relative subunit expression levels. Biophys J 93:505-512.
6. Bernardino L, Balosso S, Ravizza T, Marchi N, Ku G, Randle JC, Malva JO, Vezzani A. 2008. Inflammatory events in hippocampal slice cultures prime neuronal susceptibility to excitotoxic injury: A crucial role of P2X7 receptor-mediated IL-1beta release. J Neurochem 106:271-280.
7. Bernier LP, Ase AR, Chevallier S, Blais D, Zhao Q, Boue-Grabot E, Logothetis D, Seguela P. 2008. Phosphoinositides regulate P2X4 ATP-gated channels through direct interactions. J Neurosci 28:12938-12945.
8. 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.
9. Bianco F, Fumagalli M, Pravettoni E, D'Ambrosi N, Volonte C, Matteoli M, Abbracchio MP, Verderio C. 2005. Pathophysiological roles of extracellular nucleotides in glial cells: Differential expression of purinergic receptors in resting and activated microglia. Brain Res Brain Res Rev 48:144-156.
10. Biber K, Pinto-Duarte A, Wittendorp MC, Dolga AM, Fernandes CC, Von Frijtag Drabbe Kunzel J, Keijser JN, de Vries R, Ijzerman AP, Ribeiro JA, Eisel U, Sebastião AM, Boddeke HW. 2008. Interleukin-6 upregulates neuronal adenosine A1 receptors: implications for neuromodulation and neuroprotection. Neuropsychopharmacology 33:2237-2250.
11. Brambilla R, Ashbaugh JJ, Magliozzi R, Dellarole A, Karmally S, Szymkowski DE, Bethea JR. 2011. Inhibition of soluble tumour necrosis factor is therapeutic in experimental autoimmune encephalomyelitis and promotes axon preservation and remyelination. Brain 134:2736-2754.
12. Buenestado A, Grassin Delyle S, Arnould I, Besnard F, Naline E, Blouquit-Laye S, Chapelier A, Bellamy JF, Devillier P. 2010. The role of adenosine receptors in regulating production of tumour necrosis factor-alpha and chemokines by human lung macrophages. Br J Pharmacol 159:1304-1311.
13. Carrasquero LM, Delicado EG, Bustillo D, Gutiérrez-Martín Y, Artalejo AR, Miras-Portugal MT. 2009. P2X7 and P2Y13 purinergic receptors mediate intracellular calcium responses to BzATP in rat cerebellar astrocytes. J Neurochem 110:879-889.
14. Chertoff M, Di Paolo N, Schoeneberg A, Depino A, Ferrari C, Wurst W, Pfizenmaier K, Eisel U, Pitossi F. 2011. Neuroprotective and neurodegenerative effects of the chronic expression of tumor necrosis factor alpha in the nigrostriatal dopaminergic circuit of adult mice. Exp Neurol 227:237-251.
15. Communi D, Robaye B, Boeynaems JM. 1999. Pharmacological characterization of the human P2Y11 receptor. Br J Pharmacol 128:1199-1206.
16. Compan V, Ulmann L, Stelmashenko O, Chemin J, Chaumont S, Rassendren F. 2012. P2X2 and P2X5 subunits define a new heteromeric receptor with P2X7-like properties. J Neurosci 32:4284-4296.
17. Dash PK, Moore AN. 1995. Enhanced processing of APP induced by IL-1 beta can be reduced by indomethacin and nordihydroguaiaretic acid. Biochem Biophys Res Commun 208:542-548.
18. Di Virgilio F. 2007. Liaisons dangereuses: P2X(7) and the inflammasome. Trends Pharmacol Sci 28:465-472.
19. Dinter A, Berger EG. 1998. Golgi-disturbing agents. Histochem Cell Biol 109:571-590.
20. 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.
21. Faria R, Ferreira L, Bezerra R, Frutuoso V, Alves L. 2012. Action of natural products on p2 receptors: A reinvented era for drug discovery. Molecules 17:13009-13025.
22. Ferrari D, Chiozzi P, Falzoni S, Hanau S, Di Virgilio F. 1997. Purinergic modulation of interleukin-1 beta release from microglial cells stimulated with bacterial endotoxin. J Exp Med 185:579-582.
23. Fotheringham JA, Mayne MB, Grant JA, Geiger JD. 2004. Activation of adenosine receptors inhibits tumor necrosis factor-alpha release by decreasing TNF-alpha mRNA stability and p38 activity. Eur J Pharmacol 497:87-95.
24. Friedle SA, Brautigam VM, Nikodemova M, Wright ML, Watters JJ. 2011. The P2X7-Egr pathway regulates nucleotide-dependent inflammatory gene expression in microglia. Glia 59:1-13.
25. Friedle SA, Curet MA, Watters JJ. 2010. Recent patents on novel P2X(7) receptor antagonists and their potential for reducing central nervous system inflammation. Recent Pat CNS Drug Discov 5:35-45.
26. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, Samokhvalov IM, Merad M. 2010. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330:841-845.
27. Ginhoux F, Lim S, Hoeffel G, Low D, Huber T. 2013. Origin and differentiation of microglia. Front Cell Neurosci 7:45.
28. Goldgaber D, Harris HW, Hla T, Maciag T, Donnelly RJ, Jacobsen JS, Vitek MP, Gajdusek DC. 1989. Interleukin 1 regulates synthesis of amyloid beta-protein precursor mRNA in human endothelial cells. Proc Natl Acad Sci USA 86:7606-7610.
29. Guo C, Masin M, Qureshi OS, Murrell-Lagnado RD. 2007. Evidence for functional P2X4/P2X7 heteromeric receptors. Mol Pharmacol 72:1447-1456.
30. Hellwig S, Heinrich A, Biber K. 2013. The brain's best friend: microglial neurotoxicity revisited. Front Cell Neurosci 7:71.
31. 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.
32. Inoue K. 2006. The function of microglia through purinergic receptors: Neuropathic pain and cytokine release. Pharmacol Ther 109:210-226.
33. 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.
34. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. 2011. Physiology of microglia. Physiol Rev 91:461-553.
35. Kierdorf K, Erny D, Goldmann T, Sander V, Schulz C, Perdiguero EG, Wieghofer P, Heinrich A, Riemke P, Holscher C, Müller DN, Luckow B, Brocker T, Debowski K, Fritz G, Opdenakker G, Diefenbach A, Biber K, Heikenwalder M, Geissmann F, Rosenbauer F, Prinz M. 2013. Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat Neurosci 16:273-280.
36. Kim B, Jeong HK, Kim JH, Lee SY, Jou I, Joe EH. 2011. Uridine 5′-diphosphate induces chemokine expression in microglia and astrocytes through activation of the P2Y6 receptor. J Immunol 186:3701-3709.
37. Kim JE, Ryu HJ, Kang TC. 2011. P2X7 receptor activation ameliorates CA3 neuronal damage via a tumor necrosis factor-alpha-mediated pathway in the rat hippocampus following status epilepticus. J Neuroinflammation 8:62.
38. Lambert C, Ase AR, Seguela P, Antel JP. 2010. Distinct migratory and cytokine responses of human microglia and macrophages to ATP. Brain Behav Immun 24:1241-1248.
39. Lambertsen KL, Clausen BH, Babcock AA, Gregersen R, Fenger C, Nielsen HH, Haugaard LS, Wirenfeldt M, Nielsen M, Dagnaes-Hansen F, Johansen FF, Keating A, Finsen B. 2009. Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J Neurosci 29:1319-1330.
40. Lee HG, Won SM, Gwag BJ, Lee YB. 2011. Microglial P2X(7) receptor expression is accompanied by neuronal damage in the cerebral cortex of the APPswe/PS1dE9 mouse model of Alzheimer's disease. Exp Mol Med 43:7-14.
41. Lewis C, Neidhart S, Holy C, North RA, Buell G, Surprenant A. 1995. Coexpression of P2X2 and P2X3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature 377:432-435.
42. Matute C, Torre I, Perez-Cerda F, Perez-Samartin A, Alberdi E, Etxebarria E, Arranz AM, Ravid R, Rodriguez-Antiguedad A, Sanchez-Gomez M, Domercq M. 2007. P2X(7) receptor blockade prevents ATP excitotoxicity in oligodendrocytes and ameliorates experimental autoimmune encephalomyelitis. J Neurosci 27:9525-9533.
43. McIlvain HB, Ma L, Ludwig B, Manners MT, Martone RL, Dunlop J, Kaftan EJ, Kennedy JD, Whiteside GT. 2010. Purinergic receptor-mediated morphological changes in microglia are transient and independent from inflammatory cytokine release. Eur J Pharmacol 643:202-210.
44. Mingam R, De Smedt V, Amedee T, Bluthe RM, Kelley KW, Dantzer R, Laye S. 2008. In vitro and in vivo evidence for a role of the P2X7 receptor in the release of IL-1 beta in the murine brain. Brain Behav Immun 22:234-244.
45. Miyamoto A, Wake H, Moorhouse AJ, Nabekura J. 2013. Microglia and synapse interactions: Fine tuning neural circuits and candidate molecules. Front Cell Neurosci 7:70.
46. 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.
47. North RA. 2002. Molecular physiology of P2X receptors. Physiol Rev 82:1013-1067.
48. 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 981:174-183.
49. Pelegrin P, Barroso-Gutierrez C, Surprenant A. 2008. P2X7 receptor differentially couples to distinct release pathways for IL-1beta in mouse macrophage. J Immunol 180:7147-7157.
50. Pelegrin P, Surprenant A. 2006. Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J 25:5071-5082.
51. Pelegrin P, Surprenant A. 2009. The P2X(7) receptor-pannexin connection to dye uptake and IL-1beta release. Purinergic Signal 5:129-137.
52. Pettigrew LC, Kindy MS, Scheff S, Springer JE, Kryscio RJ, Li Y, Grass DS. 2008. Focal cerebral ischemia in the TNFalpha-transgenic rat. J Neuroinflammation 5:47.
53. Rampe D, Wang L, Ringheim GE. 2004. P2X7 receptor modulation of beta-amyloid- and LPS-induced cytokine secretion from human macrophages and microglia. J Neuroimmunol 147:56-61.
54. Sharp AJ, Polak PE, Simonini V, Lin SX, Richardson JC, Bongarzone ER, Feinstein DL. 2008. P2x7 deficiency suppresses development of experimental autoimmune encephalomyelitis. J Neuroinflammation 5:33.
55. 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.
56. Shiratori M, Tozaki-Saitoh H, Yoshitake M, Tsuda M, Inoue K. 2010. P2X7 receptor activation induces CXCL2 production in microglia through NFAT and PKC/MAPK pathways. J Neurochem 114:810-819.
57. Sierra A, Abiega O, Shahraz A, Neumann H. 2013. Janus-faced microglia: beneficial and detrimental consequences of microglial phagocytosis. Front Cell Neurosci 7:6.
58. Skaper SD, Facci L, Culbert AA, Evans NA, Chessell I, Davis JB, Richardson JC. 2006. P2X(7) receptors on microglial cells mediate injury to cortical neurons in vitro. Glia 54:234-242.
59. Sun WC, Moore JN, Hurley DJ, Vandenplas ML, Linden J, Cao Z, Murray TF. 2008. Adenosine A2A receptor agonists inhibit lipopolysaccharide-induced production of tumor necrosis factor-alpha by equine monocytes. Vet Immunol Immunopathol 121:91-100.
60. 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.
61. Suzuki T, Hide I, Ido K, Kohsaka S, Inoue K, Nakata Y. 2004. Production and release of neuroprotective tumor necrosis factor by P2X7 receptor-activated microglia. J Neurosci 24:1-7.
62. Trautmann A. 2009. Extracellular ATP in the immune system: more than just a "danger signal". Sci Signal 2:pe6.
63. Visentin S, Nuccio CD, Bellenchi GC. 2006. Different patterns of Ca(2)(+) signals are induced by low compared to high concentrations of P2Y agonists in microglia. Purinergic Signal 2:605-617.
64. Yamamoto M, Kiyota T, Horiba M, Buescher JL, Walsh SM, Gendelman HE, Ikezu T. 2007. Interferon-gamma and tumor necrosis factor-alpha regulate amyloid-beta plaque deposition and beta-secretase expression in Swedish mutant APP transgenic mice. Am J Pathol 170:680-692.
65. Yanagisawa D, Kitamura Y, Takata K, Hide I, Nakata Y, Taniguchi T. 2008. Possible involvement of P2X7 receptor activation in microglial neuroprotection against focal cerebral ischemia in rats. Biol Pharm Bull 31:1121-1130.