P2X7 receptors at adult neural progenitor cells of the mouse subventricular zone

Neuropharmacology

Volumn 73, Issue , 2013, Pages 122-137

  Messemer, Nanette ^a   Kunert, Christin ^a   Grohmann, Marcus ^a   Sobottka, Helga ^a   Nieber, Karen ^a   Zimmermann, Herbert ^b   Franke, Heike ^a   Nörenberg, Wolfgang ^a   Straub, Isabelle ^a   Schaefer, Michael ^a   Riedel, Thomas ^a   Illes, Peter ^a   Rubini, Patrizia ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

Adult neural progenitor cells; Brain subventricular zone; Extracellular ATP; P2X7 receptors

Indexed keywords

3 [[5 (2,3 DICHLOROPHENYL) 1H TETRAZOL 1 YL]METHYL]PYRIDINE; ADENOSINE TRIPHOSPHATE; BRILLIANT BLUE; CALCIUM ION; CASPASE 3; MAGNESIUM ION; MESSENGER RNA; PURINERGIC P2X7 RECEPTOR; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID;

ADULT ANIMAL; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN SLICE; CALCIUM CELL LEVEL; CALCIUM CURRENT; CELL POLARITY; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; IMMUNOCYTOCHEMISTRY; MEMBRANE CURRENT; MOUSE; NEURAL STEM CELL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEADY STATE; SUBVENTRICULAR ZONE;

2-MESATP; 2-METHYLTHIO ATP; 2′(3′)-O-(4-BENZOYLBENZOYL)ADENOSINE-5′-TRIPHOSPHATE; 2′,3′-O-(2,4,6-TRINITROPHENYL) ADENOSINE 5′-TRIPHOSPHATE; 3-(4,5-DIMETHYLTHIOAZOL-2-YL)-2,5-DIPHENYLTETRAZOLIUMBROMID; 5-(3-BROMOPHENYL)-1,3-DIHYDRO-2H-BENZOFURO[3,2-E]-1,4-DIAZEPIN-2-ONE; 5-BDBD; ADULT NEURAL PROGENITOR CELLS; BBG; BRAIN SUBVENTRICULAR ZONE; BRILLIANT BLUE G; BZ-ATP; CENTRAL NERVOUS SYSTEM; CNS; CONCENTRATION OF AGONIST PRODUCING 50% OF E(MAX); DIVALENT CATION CONCENTRATION; E(MAX); EC(50); EGF; EPIDERMAL GROWTH FACTOR; EXTRACELLULAR ATP; FGF-2; FIBROBLAST GROWTH FACTOR-2; GAPDH; GFAP; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYCERALDEHYDE 3-PHOSPHATE DEHYDROGENASE; INTRACELLULAR CA(2+) CONCENTRATION; MAXIMAL EFFECT; MSI1; MTT; MUSASHI1; NEURAL PROGENITOR CELL; NPC; P2X7 RECEPTORS; PPADS; PYRIDOXALPHOSPHATE-6-AZOPHENYL-2′,4′-DISULFONIC ACID; SUBVENTRICULAR ZONE; SVZ; TNP-ATP; WILD-TYPE; WT; X(2) CONCENTRATION; [CA(2+)](I); Α,Β-MEATP; Α,Β-METHYLENE ATP;

ADENOSINE TRIPHOSPHATE; ANIMALS; BENZOXAZOLES; CALCIUM; CASPASE 3; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; LATERAL VENTRICLES; MEMBRANE POTENTIALS; MICE; MICE, KNOCKOUT; PRIMARY CELL CULTURE; PURINERGIC P2X RECEPTOR AGONISTS; PURINERGIC P2X RECEPTOR ANTAGONISTS; PYRIDINES; PYRIDOXAL PHOSPHATE; QUINOLINIUM COMPOUNDS; RECEPTORS, PURINERGIC P2X7; ROSANILINE DYES; STEM CELLS; TETRAZOLES;

EID: 84885167670     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.05.017     Document Type: Article

References (63)

1. Abbracchio, M.P., Burnstock, G., 1994. Purinoceptors: are there families of P2X and P2Y purinoceptors? Pharmacol. Ther. 64, 445-475.
2. Abbracchio, M.P., Burnstock, G., Boeynaems, J.M., Barnard, E.A., Boyer, J.L., Kennedy, C., Knight, G.E., Fumagalli, M., Gachet, C., Jacobson, K.A., Weisman, G.A., 2006. International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol. Rev. 58, 281-341.
3. Anderson, C.M., Nedergaard, M., 2006. Emerging challenges of assigning P2X7 receptor function and immunoreactivity in neurons. Trends Neurosci. 29, 257-262.
4. Antonio, L.S., Stewart, A.P., Xu, X.J., Varanda, W.A., Murrell-Lagnado, R.D., Edwardson, J.M., 2011. P2X4 receptors interact with both P2X2 and P2X7 receptors in the form of homotrimers. Br. J. Pharmacol. 163, 1069-1077.
5. Brass, D., Grably, M.R., Bronstein-Sitton, N., Gohar, O., Meir, A., 2012. Using antibodies against P2Y and P2X receptors in purinergic signaling research. Purinergic Signal 8 (Suppl. 1), 61-79.
6. Braun, N., Sevigny, J., Mishra, S.K., Robson, S.C., Barth, S.W., Gerstberger, R., Hammer, K., Zimmermann, H., 2003. Expression of the ecto-ATPase NTPDase2 in the germinal zones of the developing and adult rat brain. Eur. J. Neurosci. 17, 1355-1364.
7. Burnstock, G., Krügel, U., Abbracchio, M.P., Illes, P., 2011. Purinergic signalling: from normal behaviour to pathological brain function. Prog. Neurobiol. 95, 229-274.
8. Delarasse, C., Gonnord, P., Galante, M., Auger, R., Daniel, H., Motta, I., Kanellopoulos, J.M., 2009. Neural progenitor cell death is induced by extracellular ATP via ligation of P2X7 receptor. J. Neurochem. 109, 846-857.
9. Delarasse, C., Auger, R., Gonnord, P., Fontaine, B., Kanellopoulos, J.M., 2011. The purinergic receptor P2X7 triggers alpha-secretase-dependent processing of the amyloid precursor protein. J. Biol. Chem. 286, 2596-2606.
10. Doetsch, F., 2003. The glial identity of neural stem cells. Nat. Neurosci. 6, 1127-1134.
11. Engel, T., Gomez-Villafuertes, R., Tanaka, K., Mesuret, G., Sanz-Rodriguez, A., Garcia-Huerta, P., Miras-Portugal, M.T., Henshall, D.C., Diaz-Hernandez, M., 2012a. Seizure suppression and neuroprotection by targeting the purinergic P2X7 receptor during status epilepticus in mice. FASEB J. 26, 1616-1628.
12. Engel, T., Jimenez-Pacheco, A., Miras-Portugal, M.T., Diaz-Hernandez, M., Henshall, D.C., 2012b. P2X7 receptor in epilepsy; role in pathophysiology and potential targeting for seizure control. Int. J. Physiol. Pathophysiol. Pharmacol. 4, 174-187.
13. 1-deficient mice. Nat. Med. 5, 1199-1202.
14. Ferrari, D., Pizzirani, C., Adinolfi, E., Lemoli, R.M., Curti, A., Idzko, M., Panther, E., Di Virgilio, F., 2006. The P2X7 receptor: a key player in IL-1 processing and release. J. Immunol. 176, 3877-3883.
15. Filippov, V., Kronenberg, G., Pivneva, T., Reuter, K., Steiner, B., Wang, L.P., Yamaguchi, M., Kettenmann, H., Kempermann, G., 2003. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol. Cell Neurosci. 23, 373-382.
16. 2+ by P2X and P2Y receptor-subtypes in cultured cortical astroglia of the rat. Neuroscience 160, 767-783.
17. Franke, H., Verkhratsky, A., Burnstock, G., Illes, P., 2012. Pathophysiology of astroglial purinergic signalling. Purinergic Signal 8, 629-657.
18. Genzen, J.R., Platel, J.C., Rubio, M.E., Bordey, A., 2009. Ependymal cells along the lateral ventricle express functional P2X7 receptors. Purinergic Signal 5, 299-307.
19. Gerevich, Z., Zádori, Z., Müller, C., Wirkner, K., Schröder, W., Rubini, P., Illes, P., 2007. Metabotropic P2Y receptors inhibit P2X3 receptor-channels via G protein-dependent facilitation of their desensitization. Br. J. Pharmacol. 151, 226-236.
20. Götz, M., Huttner, W.B., 2005. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777-788.
21. Grimm, I., Messemer, N., Stanke, M., Gachet, C., Zimmermann, H., 2009. Coordinate pathways for nucleotide and EGF signaling in cultured adult neural progenitor cells. J. Cell Sci. 122, 2524-2533.
22. 2+-induced epileptiform activity in rat hippocampal slices. Epilepsy Res. Suppl. 8, 147-155.
23. Hogg, R.C., Chipperfield, H., Whyte, K.A., Stafford, M.R., Hansen, M.A., Cool, S.M., Nurcombe, V., Adams, D.J., 2004. Functional maturation of isolated neural progenitor cells from the adult rat hippocampus. Eur. J. Neurosci. 19, 2410-2420.
24. Hüttmann, K., Sadgrove, M., Wallraff, A., Hinterkeuser, S., Kirchhoff, F., Steinhauser, C., Gray, W.P., 2003. Seizures preferentially stimulate proliferation of radial glia-like astrocytes in the adult dentate gyrus: functional and immunocytochemical analysis. Eur. J. Neurosci. 18, 2769-2778.
25. Illes, P., Verkhratsky, A., Burnstock, G., Franke, H., 2012. P2X receptors and their roles in astroglia in the central and peripheral nervous system. Neuroscientist 18, 422-438.
26. Jarvis, M.F., Khakh, B.S., 2009. ATP-gated P2X cation-channels. Neuropharmacology 56, 208-215.
27. Jiang, L.H., 2009. Inhibition of P2X7 receptors by divalent cations: old action and new insight. Eur. Biophys. J. 38, 339-346.
28. Khakh, B.S., North, R.A., 2006. P2X receptors as cell-surface ATP sensors in health and disease. Nature 442, 527-532.
29. Khakh, B.S., Bao, X.R., Labarca, C., Lester, H.A., 1999a. Neuronal P2X transmittergated cation channels change their ion selectivity in seconds. Nat. Neurosci. 2, 322-330.
30. Khakh, B.S., Proctor, W.R., Dunwiddie, T.V., Labarca, C., Lester, H.A., 1999b. Allosteric control of gating and kinetics at P2X4 receptor channels. J. Neurosci. 19, 7289-7299.
31. Klaft, Z.J., Schulz, S.B., Maslarova, A., Gabriel, S., Heinemann, U., Gerevich, Z., 2012. Extracellular ATP differentially affects epileptiform activity via purinergic P2X7 and adenosine A1 receptors in naive and chronic epileptic rats. Epilepsia 53, 1978-1986.
32. Kriegstein, A., Alvarez-Buylla, A., 2009. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 32, 149-184.
33. Kunze, A., Grass, S., Witte, O.W., Yamaguchi, M., Kempermann, G., Redecker, C., 2006. Proliferative response of distinct hippocampal progenitor cell populations after cortical infarcts in the adult brain. Neurobiol. Dis. 21, 324-332.
34. Lacar, B., Young, S.Z., Platel, J.C., Bordey, A., 2010. Imaging and recording sub-ventricular zone progenitor cells inlive tissueofpostnatal mice. Front Neurosci. 4.
35. Leichsenring, A., Riedel, T., Qin, Y., Rubini, P., Illes, P., 2013. Anoxic depolarization of hippocampal astrocytes: possible modulation by P2X7 receptors. Neurochem. Int. 62, 15-22.
36. Lin, J.H., Takano, T., Arcuino, G., Wang, X., Hu, F., Darzynkiewicz, Z., Nunes, M., Goldman, S.A., Nedergaard, M., 2007. Purinergic signaling regulates neural progenitor cell expansion and neurogenesis. Dev. Biol. 302, 356-366.
37. Liu, R.H., Morassutti, D.J., Whittemore, S.R., Sosnowski, J.S., Magnuson, D.S., 1999. Electrophysiological properties of mitogen-expanded adult rat spinal cord and subventricular zone neural precursor cells. Exp. Neurol. 158, 143-154.
38. Liu, X., Hashimoto-Torii, K., Torii, M., Haydar, T.F., Rakic, P., 2008. The role of ATP signaling in the migration of intermediate neuronal progenitors to the neocortical subventricular zone. Proc. Natl. Acad. Sci. U. S. A 105, 11802-11807.
39. Mishra, S.K., Braun, N., Shukla, V., Fullgrabe, M., Schomerus, C., Korf, H.W., Gachet, C., Ikehara, Y., Sevigny, J., Robson, S.C., Zimmermann, H., 2006. Extracellular nucleotide signaling in adult neural stem cells: synergism with growth factor-mediated cellular proliferation. Development 133, 675-684.
40. Nörenberg, W., Schunk, J., Fischer, W., Sobottka, H., Riedel, T., Oliveira, J.F., Franke, H., Illes, P., 2010. Electrophysiological classification of P2X7 receptors in rat cultured neocortical astroglia. Br. J. Pharmacol. 160, 1941-1952.
41. Nörenberg, W., Hempel, C., Urban, N., Sobottka, H., Illes, P., Schaefer, M., 2011. Clemastine potentiates the human P2X7 receptor by sensitizing it to lower ATP concentrations. J. Biol. Chem. 286, 11067-11081.
42. Oliveira, J.F., Riedel, T., Leichsenring, A., Heine, C., Franke, H., Krügel, U., Nörenberg, W., Illes, P., 2011. Rodent cortical astroglia express in situ functional P2X7 receptors sensing pathologically high ATP concentrations. Cereb. Cortex 21, 806-820.
43. Pelegrin, P., Surprenant, A., 2006. Pannexin-1 mediates large pore formation and interleukin-1β release by the ATP-gated P2X7 receptor. EMBO J. 25, 5071-5082.
44. Roger, S., Pelegrin, P., Surprenant, A., 2008. Facilitation of P2X7 receptor currents and membrane blebbing via constitutive and dynamic calmodulin binding. J. Neurosci. 28, 6393-6401.
45. 2+ by adenine and uracil nucleotides in human midbrain-derived neuronal progenitor cells. Cell Calcium 45, 485-498.
46. Schuchmann, S., Schmitz, D., Rivera, C., Vanhatalo, S., Salmen, B., Mackie, K., Sipila, S.T., Voipio, J., Kaila, K., 2006. Experimental febrile seizures are precipitated by a hyperthermia-induced respiratory alkalosis. Nat. Med. 12, 817-823.
47. Shukla, V., Zimmermann, H., Wang, L., Kettenmann, H., Raab, S., Hammer, K., Sevigny, J., Robson, S.C., Braun, N., 2005. Functional expression of the ecto-ATPase NTPDase2 and of nucleotide receptors by neuronal progenitor cells in the adult murine hippocampus. J. Neurosci. Res. 80, 600-610.
48. Sim, J.A., Young, M.T., Sung, H.Y., North, R.A., Surprenant, A., 2004. Reanalysis of P2X7 receptor expression in rodent brain. J. Neurosci. 24, 6307-6314.
49. Solle, M., Labasi, J., Perregaux, D.G., Stam, E., Petrushova, N., Koller, B.H., Griffiths, R.J., Gabel, C.A., 2001. Altered cytokine production in mice lacking P2X7 receptors. J. Biol. Chem. 276, 125-132.
50. Sperlágh, B., Vizi, E.S., Wirkner, K., Illes, P., 2006. P2X7 receptors in the nervous system. Prog. Neurobiol. 78, 327-346.
51. Stoop, R., Surprenant, A., North, R.A., 1997. Different sensitivities to pH of ATP-induced currents at four cloned P2X receptors. J. Neurophysiol. 78, 1837-1840.
52. Suh, H., Deng, W., Gage, F.H., 2009. Signaling in adult neurogenesis. Annu. Rev. Cell Dev. Biol. 25, 253-275.
53. Suyama, S., Sunabori, T., Kanki, H., Sawamoto, K., Gachet, C., Koizumi, S., Okano, H., 2012. Purinergic signaling promotes proliferation of adult mouse subventricular zone cells. J. Neurosci. 32, 9238-9247.
54. Tsuda, M., Toyomitsu, E., Komatsu, T., Masuda, T., Kunifusa, E., Nasu-Tada, K., Koizumi, S., Yamamoto, K., Ando, J., Inoue, K., 2008. Fibronectin/integrin system is involved in P2X4 receptor upregulation in the spinal cord and neuropathic pain after nerve injury. Glia 56, 579-585.
55. Virginio, C., MacKenzie, A., North, R.A., Surprenant, A., 1999. Kinetics of cell lysis, dye uptake and permeability changes in cells expressing the rat P2X7 receptor. J. Physiol. 519 (2), 335-346.
56. Wang, D.D., Krueger, D.D., Bordey, A., 2003. Biophysical properties and ionic signature of neuronal progenitors of the postnatal subventricular zone in situ. J. Neurophysiol. 90, 2291-2302.
57. Yan, Z., Khadra, A., Li, S., Tomic, M., Sherman, A., Stojilkovic, S.S., 2010. Experimental characterization and mathematical modeling of P2X7 receptor channel gating. J. Neurosci. 30, 14213-14224.
58. Yan, Z., Khadra, A., Sherman, A., Stojilkovic, S.S., 2011. Calcium-dependent block of P2X7 receptor channel function is allosteric. J. Gen. Physiol. 138, 437-452.
59. v channels regulate electrical properties and proliferation of adult neural precursor cells. Mol. Cell. Neurosci. 37, 284-297.
60. Yu, T.S., Zhang, G., Liebl, D.J., Kernie, S.G., 2008. Traumatic brain injury-induced hippocampal neurogenesis requires activation of early nestin-expressing progenitors. J. Neurosci. 28, 12901-12912.
61. Yuahasi, K.K., Demasi, M.A., Tamajusuku, A.S., Lenz, G., Sogayar, M.C., Fornazari, M., Lameu, C., Nascimento, I.C., Glaser, T., Schwindt, T.T., Negraes, P.D., Ulrich, H., 2012. Regulation of neurogenesis and gliogenesis of retinoic acid-induced P19 embryonal carcinoma cells by P2X2 and P2X7 receptors studied by RNA interference. Int. J. Dev. Neurosci 30, 91-97.
62. Zhao, C., Deng, W., Gage, F.H., 2008. Mechanisms and functional implications of adult neurogenesis. Cell 132, 645-660.
63. Zimmermann, H., 2011. Purinergic signaling in neural development. Semin. Cell Dev. Biol. 22, 194-204.