Mechanism of microglia neuroprotection: Involvement of P2X7, TNFα, and valproic acid

GLIA

Volumn 64, Issue 1, 2016, Pages 76-89

  Masuch, Annette ^a   Shieh, Chu Hsin ^a   van Rooijen, Nico ^b   van Calker, Dietrich ^a   Biber, Knut ^a,c  

^a UNIVERSITY OF FREIBURG   (Germany)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

ATP; Cytokine; Excitotoxicity; Glia; Hippocampus; NMDA; OHSC; Purine receptor

Indexed keywords

ADENOSINE TRIPHOSPHATE; N METHYL DEXTRO ASPARTIC ACID; PURINERGIC P2X7 RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; VALPROIC ACID; MESSENGER RNA; N METHYLASPARTIC ACID; NEUROPROTECTIVE AGENT; TUMOR NECROSIS FACTOR;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; DRUG MECHANISM; EXCITOTOXICITY; FLUORESCENCE MICROSCOPY; IMMUNOFLUORESCENCE TEST; MICROGLIA; MOUSE; NERVE CELL; NEUROPROTECTION; NEUROTOXICITY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SLICE CULTURE; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; DRUG EFFECTS; GENETICS; HIPPOCAMPUS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TISSUE CULTURE TECHNIQUE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELLS, CULTURED; HIPPOCAMPUS; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; N-METHYLASPARTATE; NEURONS; NEUROPROTECTIVE AGENTS; RECEPTORS, PURINERGIC P2X7; RNA, MESSENGER; TISSUE CULTURE TECHNIQUES; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION; VALPROIC ACID;

EID: 84954287873     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22904     Document Type: Article

References (63)

1. Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H. 2009. Purinergic signalling in the nervous system: an overview. Trends Neurosci 32:19-29.
2. Algattas H, Huang JH. 2014. Traumatic Brain Injury pathophysiology and treatments: Early, intermediate, and late phases post-injury. Int J Mol Sci 15:309-341.
3. Anderson CM, Nedergaard M. 2006. Emerging challenges of assigning P2X7 receptor function and immunoreactivity in neurons. Trends Neurosci 29:257-262.
4. Bartlett R, Stokes L, Sluyter R. 2014. The P2X7 receptor channel: Recent developments and the use of P2X7 antagonists in models of disease. Pharmacol Rev 66:638-675.
5. Bernardino L, Xapelli S, Silva AP, Jakobsen B, Poulsen FR, Oliveira CR, Vezzani A, Malva JO, Zimmer J. 2005. Modulator effects of interleukin-1beta and tumor necrosis factor-alpha on AMPA-induced excitotoxicity in mouse organotypic hippocampal slice cultures. J Neurosci 25:6734-6744.
6. 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.
7. Biber K, Owens T, Boddeke E. 2014. What is microglia neurotoxicity (Not)? Glia 62:841-854.
8. Biber K, Pinto-Duarte A, Wittendorp MC, Dolga AM, Fernandes CC, Von Frijtag Drabbe Künzel J, Keijser JN, de Vries R, Ijzerman AP, Ribeiro JA, Eisel U Sebastião AM, Boddeke HWGM. 2008. Interleukin-6 upregulates neuronal adenosine A1 receptors: Implications for neuromodulation and neuroprotection. Neuropsychopharmacology 33:2237-2250.
9. Boscia F, Annunziato L, Taglialatela M. 2006. Retigabine and flupirtine exert neuroprotective actions in organotypic hippocampal cultures. Neuropharmacology 51:283-294.
10. Bours MJL, Dagnelie PC, Giuliani AL, Wesselius A, Di Virgilio F. 2011. P2 receptors and extracellular ATP: A novel homeostatic pathway in inflammation. Front Biosci Sch Ed 3:1443-1456.
11. Burnstock G. 2012. Purinergic signalling: Its unpopular beginning, its acceptance and its exciting future. BioEssays News Rev Mol Cell Dev Biol 34:218-225.
12. Chen S, Wu H, Klebe D, Hong Y, Zhang J. 2014. Valproic acid: A new candidate of therapeutic application for the acute central nervous system injuries. Neurochem Res 39:1621-1633.
13. Chiu C-T, Wang Z, Hunsberger JG, Chuang D-M. 2013. Therapeutic potential of mood stabilizers lithium and valproic acid: Beyond bipolar disorder. Pharmacol Rev 65:105-142.
14. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
15. Chu T, Zhou H, Lu L, Kong X, Wang T, Pan B, Feng S. 2015. Valproic acid-mediated neuroprotection and neurogenesis after spinal cord injury: From mechanism to clinical potential. Regen Med 10:193-209.
16. Coddou C, Yan Z, Obsil T, Huidobro-Toro JP, Stojilkovic SS. 2011. Activation and regulation of purinergic P2X receptor channels. Pharmacol Rev 63:641-683.
17. Cronberg T, Jensen K, Rytter A, Wieloch T. 2005. Selective sparing of hippocampal CA3 cells following in vitro ischemia is due to selective inhibition by acidosis. Eur J Neurosci 22:310-316.
18. Dale N, Frenguelli BG. 2009. Release of adenosine and ATP during ischemia and epilepsy. Curr Neuropharmacol 7:160-179.
19. Detich N, Bovenzi V, Szyf M. 2003. Valproate induces replication-independent active DNA demethylation. J Biol Chem 278:27586-27592.
20. Dong E, Chen Y, Gavin DP, Grayson DR Guidotti A. 2010. Valproate induces DNA demethylation in nuclear extracts from adult mouse brain. Epigenetics 5:730-735.
21. Figiel I. 2008. Pro-inflammatory cytokine TNF-alpha as a neuroprotective agent in the brain. Acta Neurobiol Exp (Warsz) 68:526-534.
22. Franke H, Grummich B, Härtig W, Grosche J, Regenthal R, Edwards RH, Illes P Krügel U. 2006. Changes in purinergic signaling after cerebral injury-Involvement of glutamatergic mechanisms? Int J Dev Neurosci 24:123-132.
23. Fujikawa DG. 2005. Prolonged seizures and cellular injury: Understanding the connection. Epilepsy Behav EB 7 Suppl 3:S3-11.
24. De Haas AH, Boddeke HWGM Biber K. 2008. Region-specific expression of immunoregulatory proteins on microglia in the healthy CNS. Glia 56:888-894.
25. De Haas AH, van Weering HRJ, de Jong EK, Boddeke HWGM, Biber KPH. 2007. Neuronal chemokines: Versatile messengers in central nervous system cell interaction. Mol Neurobiol 36:137-151.
26. Hailer NP, Jarhult JD, Nitsch R. 1996. Resting microglial cells in vitro: Analysis of morphology and adhesion molecule expression in organotypic hippocampal slice cultures. Glia 18:319-331.
27. Harry GJ, Kraft AD. 2008. Neuroinflammation and microglia: Considerations and approaches for neurotoxicity assessment. Expert Opin Drug Metab Toxicol 4:1265-1277.
28. Hellwig S, Heinrich A, Biber K. 2013. The brain's best friend: Microglial neurotoxicity revisited. Front Cell Neurosci 7:71-
29. 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.
30. Inoue K. 2008. Purinergic systems in microglia. Cell Mol Life Sci CMLS 65:3074-3080.
31. De Jong EK, de Haas AH, Brouwer N, van Weering HRJ, Hensens M, Bechmann I, Pratley P, Wesseling E, Boddeke HWGM Biber K. 2008. Expression of CXCL4 in microglia in vitro and in vivo and its possible signaling through CXCR3. J Neurochem 105:1726-1736.
32. Kettenmann H, Hanisch U-K, Noda M, Verkhratsky A. 2011. Physiology of microglia. Physiol Rev 91:461-553.
33. Khakh BS, Burnstock G. 2009. The double life of ATP. Sci Am 301:84-90, 92.
34. Kim J-E, Ryu HJ, Kang T-C. 2011. P2X7 receptor activation ameliorates CA3 neuronal damage via a tumor necrosis factor-α-mediated pathway in the rat hippocampus following status epilepticus. J Neuroinflammation 8:62-
35. Kreutz S, Koch M, Böttger C, Ghadban C, Korf H-W, Dehghani F. 2009. 2-Arachidonoylglycerol elicits neuroprotective effects on excitotoxically lesioned dentate gyrus granule cells via abnormal-cannabidiol-sensitive receptors on microglial cells. Glia 57:286-294.
36. Lambertsen KL, Clausen BH, Babcock AA, Gregersen R, Fenger C, Nielsen HH, Haugaard LS, Wirenfeldt M, Nielsen M, Dagnaes-Hansen F, Bluethmann H, Faergeman NJ, Meldgaard M, Deierborg T, Finsen B. 2009. Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J Neurosci 29:1319-1330.
37. Lambertucci C, Dal Ben D, Buccioni M, Marucci G, Thomas A, Volpini R. 2015. Medicinal chemistry of P2X receptors: Agonists and orthosteric antagonists. Curr Med Chem 22:915-928.
38. Lu W-H, Wang C-Y, Chen P-S, Wang J-W, Chuang D-M, Yang C-S, Tzeng S-F. 2013. Valproic acid attenuates microgliosis in injured spinal cord and purinergic P2X4 receptor expression in activated microglia. J Neurosci Res 91:694-705.
39. Marín-García P, Sánchez-Nogueiro J, Gómez-Villafuertes R, León D, Miras-Portugal MT. 2008. Synaptic terminals from mice midbrain exhibit functional P2X7 receptor. Neuroscience 151:361-373.
40. Masin M, Young C, Lim K, Barnes SJ, Xu XJ, Marschall V, Brutkowski W, Mooney ER, Gorecki DC, Murrell-Lagnado R. 2012. Expression, assembly and function of novel C-terminal truncated variants of the mouse P2X7 receptor: Re-evaluation of P2X7 knockouts. Br J Pharmacol 165:978-993.
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. Orr AG, Orr AL, Li X-J, Gross RE, Traynelis SF. 2009. Adenosine A(2A) receptor mediates microglial process retraction. Nat Neurosci 12:872-878.
43. Ou J-N, Torrisani J, Unterberger A, Provençal N, Shikimi K, Karimi M, Ekström TJ, Szyf M. 2007. Histone deacetylase inhibitor Trichostatin A induces global and gene-specific DNA demethylation in human cancer cell lines. Biochem Pharmacol 73:1297-1307.
44. Parsons MP, Raymond LA. 2014. Extrasynaptic NMDA receptor involvement in central nervous system disorders. Neuron 82:279-293.
45. Pocock JM, Kettenmann H. 2007. Neurotransmitter receptors on microglia. Trends Neurosci 30:527-535.
46. Rodrigues RJ, Tomé AR, Cunha RA. 2015. ATP as a multi-target danger signal in the brain. Front Neurosci 9:148-
47. Van Rooijen N, Sanders A. 1994. Liposome mediated depletion of macrophages: Mechanism of action, preparation of liposomes and applications. J Immunol Methods 174:83-93.
48. Sánchez-Nogueiro J, Marín-García P, Bustillo D, Olivos-Oré LA, Miras-Portugal MT, Artalejo AR. 2014. Subcellular distribution and early signalling events of P2X7 receptors from mouse cerebellar granule neurons. Eur J Pharmacol 744:190-202.
49. Sánchez-Nogueiro J, Marín-García P, Miras-Portugal MT. 2005. Characterization of a functional P2X(7)-like receptor in cerebellar granule neurons from P2X(7) knockout mice. FEBS Lett 579:3783-3788.
50. Schübeler D. 2015. Function and information content of DNA methylation. Nature 517:321-326.
51. Shieh C-H, Heinrich A, Serchov T, van Calker D, Biber K. 2014. P2X7-dependent, but differentially regulated release of IL-6, CCL2, and TNF-α in cultured mouse microglia. Glia 62:592-607.
52. Solle M, Labasi J, Perregaux DG, Stam E, Petrushova N, Koller BH, Griffiths RJ, Gabel CA. 2001. Altered cytokine production in mice lacking P2X(7) receptors. J Biol Chem 276:125-132.
53. Sperlágh B, Illes P. 2007. Purinergic modulation of microglial cell activation. Purinergic Signal 3:117-127.
54. Sperlágh B, Illes P. 2014. P2X7 receptor: An emerging target in central nervous system diseases. Trends Pharmacol Sci 35:537-547.
55. Stoppini L, Buchs PA, Muller D. 1991. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182.
56. Streit WJ. 2002. Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 40:133-139.
57. 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.
58. 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.
59. Tremblay M-È, Stevens B, Sierra A, Wake H, Bessis A, Nimmerjahn A. 2011. The role of microglia in the healthy brain. J Neurosci 31:16064-16069.
60. Vinet J, Weering HRJ, van Heinrich A, Kälin RE, Wegner A, Brouwer N, Heppner FL, Rooijen N van Boddeke HWGM Biber K. 2012. Neuroprotective function for ramified microglia in hippocampal excitotoxicity. J Neuroinflammation 9:27-
61. Van Weering HRJ, Boddeke HWGM Vinet J, Brouwer N, de Haas AH, van Rooijen N, Thomsen AR Biber KPH. 2011. CXCL10/CXCR3 signaling in glia cells differentially affects NMDA-induced cell death in CA and DG neurons of the mouse hippocampus. Hippocampus 21:220-232.
62. Zhou L, Luo L, Qi X, Li X, Gorodeski GI. 2009. Regulation of P2X(7) gene transcription. Purinergic Signal 5:409-426.
63. Zhu W-G, Otterson GA. 2003. The interaction of histone deacetylase inhibitors and DNA methyltransferase inhibitors in the treatment of human cancer cells. Curr Med Chem Anti-Cancer Agents 3:187-199.