Purinergic trophic signalling in glial cells: Functional effects and modulation of cell proliferation, differentiation, and death

Purinergic Signalling

Volumn 8, Issue 3, 2012, Pages 539-557

  Lecca, Davide ^a   Ceruti, Stefania ^a   Fumagalli, Marta ^a   Abbracchio, Maria P ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

Astrocytes; Microglial cells; M ller cells; Myelination; Oligodendrocytes; Reactive gliosis

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CYCLOOXYGENASE 1; GLIAL FIBRILLARY ACIDIC PROTEIN; PURINE; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y2 RECEPTOR; PURINERGIC P2Y4 RECEPTOR; PURINERGIC RECEPTOR; PYRIMIDINE; URIDINE DIPHOSPHATE; URIDINE TRIPHOSPHATE;

ARTICLE; ASTROCYTE; ASTROCYTOSIS; CALCIUM SIGNALING; CELL COMMUNICATION; CELL DEATH; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CELL SURVIVAL; CHEMOTAXIS; EPENDYMA CELL; GLIA CELL; GLIOSIS; HUMAN; IMMUNOSURVEILLANCE; MICROGLIA; MUELLER CELL; NERVE CELL; NERVE FUNCTION; OLIGODENDROGLIA; PERICYTE; PHAGOCYTOSIS; POLYDENDROCYTE; RETINA NERVE CELL; SATELLITE CELL; SCHWANN CELL; SIGNAL TRANSDUCTION; TISSUE REPAIR;

ANIMALS; ASTROCYTES; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; MICROGLIA; NEUROGLIA; OLIGODENDROGLIA; RECEPTORS, PURINERGIC; RETINA; SCHWANN CELLS; SIGNAL TRANSDUCTION;

EID: 84861532077     PISSN: 15739538     EISSN: 15739546     Source Type: Journal    
DOI: 10.1007/s11302-012-9310-y     Document Type: Article

References (148)

1. Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H (2009) Purinergic signalling in the nervous system: an overview. Trends Neurosci 32(1): 19-29.
2. Coco S, Calegari F, Pravettoni E, Pozzi D, Taverna E, Rosa P, Matteoli M, Verderio C (2003) Storage and release of ATP from astrocytes in culture. J Biol Chem 278(2): 1354-1362.
3. Verkhratsky A, Krishtal OA, Burnstock G (2009) Purinoceptors on neuroglia. Mol Neurobiol 39(3): 190-208.
4. Marpegan L, Swanstrom AE, Chung K, Simon T, Haydon PG, Khan SK, Liu AC, Herzog ED, Beaule C (2011) Circadian regulation of ATP release in astrocytes. J Neurosci 31(23): 8342-8350.
5. Fumagalli M, Brambilla R, D'Ambrosi N, Volontè C, Matteoli M, Verderio C, Abbracchio MP (2003) Nucleotide-mediated calcium signaling in rat cortical astrocytes: role of P2X and P2Y receptors. Glia 43(3): 218-230.
6. Abbracchio MP, Verderio C (2006) Pathophysiological roles of P2 receptors in glial cells. Novartis Found Symp 276: 91-103.
7. Buffo A, Rolando C, Ceruti S (2010) Astrocytes in the damaged brain: molecular and cellular insights into their reactive response and healing potential. Biochem Pharmacol 79(2): 77-89.
8. Abbracchio MP, Saffrey MJ, Hopker V, Burnstock G (1994) Modulation of astroglial cell proliferation by analogues of adenosine and ATP in primary cultures of rat striatum. Neuroscience 59(1): 67-76.
9. Abbracchio MP, Ceruti S, Langfelder R, Cattabeni F, Saffrey MJ, Burnstock G (1995) Effects of ATP analogues and basic fibroblast growth factor on astroglial cell differentiation in primary cultures of rat striatum. Int J Dev Neurosci 13(7): 685-693.
10. Brambilla R, Burnstock G, Bonazzi A, Ceruti S, Cattabeni F, Abbracchio MP (1999) Cyclo-oxygenase-2 mediates P2Y receptor-induced reactive astrogliosis. Br J Pharmacol 126(3): 563-567.
11. Brambilla R, Ceruti S, Malorni W, Cattabeni F, Abbracchio MP (2000) A novel gliotic P2 receptor mediating cyclooxygenase-2 induction in rat and human astrocytes. J Auton Nerv Syst 81(1-3): 3-9.
12. Neary JT, Kang Y, Shi YF, Tran MD, Wanner IB (2006) P2 receptor signalling, proliferation of astrocytes, and expression of molecules involved in cell-cell interactions. Novartis Found Symp 276: 131-143.
13. Franke H, Sauer C, Rudolph C, Krugel U, Hengstler JG, Illes P (2009) P2 receptor-mediated stimulation of the PI3-K/Akt-pathway in vivo. Glia 57(10): 1031-1045.
14. Kuboyama K, Harada H, Tozaki-Saitoh H, Tsuda M, Ushijima K, Inoue K (2011) Astrocytic P2Y(1) receptor is involved in the regulation of cytokine/chemokine transcription and cerebral damage in a rat model of cerebral ischemia. J Cereb Blood Flow Metab 31: 1930-1941.
15. Weisman GA, Wang M, Kong Q, Chorna NE, Neary JT, Sun GY, Gonzalez FA, Seye CI, Erb L (2005) Molecular determinants of P2Y2 nucleotide receptor function: implications for proliferative and inflammatory pathways in astrocytes. Mol Neurobiol 31(1-3): 169-183.
16. Abbracchio MP, Ceruti S (2006) Roles of P2 receptors in glial cells: focus on astrocytes. Purinergic Signal 2(4): 595-604.
17. Peterson TS, Camden JM, Wang Y, Seye CI, Wood WG, Sun GY, Erb L, Petris MJ, Weisman GA (2010) P2Y2 nucleotide receptor-mediated responses in brain cells. Mol Neurobiol 41(2-3): 356-366.
18. Tran MD (2011) P2 receptor stimulation induces amyloid precursor protein production and secretion in rat cortical astrocytes. Neurosci Lett 492(3): 155-159.
19. Fumagalli M, Lecca D, Abbracchio MP (2011) Role of purinergic signalling in neuro-immune cells and adult neural progenitors. Front Biosci 17: 2326-2341.
20. Simard M, Arcuino G, Takano T, Liu QS, Nedergaard M (2003) Signaling at the gliovascular interface. J Neurosci 23(27): 9254-9262.
21. Lecca D, Ceruti S (2008) Uracil nucleotides: from metabolic intermediates to neuroprotection and neuroinflammation. Biochem Pharmacol 75(10): 1869-1881.
22. Bjelobaba I, Parabucki A, Lavrnja I, Stojkov D, Dacic S, Pekovic S, Rakic L, Stojiljkovic M, Nedeljkovic N (2011) Dynamic changes in the expression pattern of ecto-5′-nucleotidase in the rat model of cortical stab injury. J Neurosci Res 89(6): 862-873.
23. Ciccarelli R, D'Alimonte I, Ballerini P, D'Auro M, Nargi E, Buccella S, Di Iorio P, Bruno V, Nicoletti F, Caciagli F (2007) Molecular signalling mediating the protective effect of A1 adenosine and mGlu3 metabotropic glutamate receptor activation against apoptosis by oxygen/glucose deprivation in cultured astrocytes. Mol Pharmacol 71(5): 1369-1380.
24. Hindley S, Herman MA, Rathbone MP (1994) Stimulation of reactive astrogliosis in vivo by extracellular adenosine diphosphate or an adenosine A2 receptor agonist. J Neurosci Res 38(4): 399-406.
25. Brambilla R, Cottini L, Fumagalli M, Ceruti S, Abbracchio MP (2003) Blockade of A2A adenosine receptors prevents basic fibroblast growth factor-induced reactive astrogliosis in rat striatal primary astrocytes. Glia 43(2): 190-194.
26. Trincavelli ML, Marroni M, Tuscano D, Ceruti S, Mazzola A, Mitro N, Abbracchio MP, Martini C (2004) Regulation of A2B adenosine receptor functioning by tumour necrosis factor a in human astroglial cells. J Neurochem 91(5): 1180-1190.
27. Abbracchio MP, Ceruti S, Brambilla R, Barbieri D, Camurri A, Franceschi C, Giammarioli A, Jacobson KA, Cattabeni F, Malorni W (1998) Adenosine A3 receptors and viability of astrocytes. Drug Dev Res 45: 379-386.
28. Von Lubitz DK, Simpson KL, Lin RC (2001) Right thing at a wrong time? Adenosine A3 receptors and cerebroprotection in stroke. Ann N Y Acad Sci 939: 85-96.
29. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97(6): 703-716.
30. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci U S A 96(20): 11619-11624.
31. Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A (2008) Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3(3): 265-278.
32. Jessen KR, Mirsky R (2008) Negative regulation of myelination: relevance for development, injury, and demyelinating disease. Glia 56(14): 1552-1565.
33. Emery B (2010) Regulation of oligodendrocyte differentiation and myelination. Science 330(6005): 779-782.
34. Nave KA (2010) Myelination and support of axonal integrity by glia. Nature 468(7321): 244-252.
35. Fields RD (2008) White matter in learning, cognition and psychiatric disorders. Trends Neurosci 31(7): 361-370.
36. Lee PR, Fields RD (2009) Regulation of myelin genes implicated in psychiatric disorders by functional activity in axons. Front Neuroanat 3: 4.
37. Fields RD, Stevens B (2000) ATP: an extracellular signaling molecule between neurons and glia. Trends Neurosci 23(12): 625-633.
38. Stevens B, Fields RD (2000) Response of Schwann cells to action potentials in development. Science 287(5461): 2267-2271.
39. Ansselin AD, Davey DF, Allen DG (1997) Extracellular ATP increases intracellular calcium in cultured adult Schwann cells. Neuroscience 76(3): 947-955.
40. Lyons SA, Morell P, McCarthy KD (1995) Schwann cell ATP-mediated calcium increases in vitro and in situ are dependent on contact with neurons. Glia 13(1): 27-38.
41. Mayer C, Quasthoff S, Grafe P (1998) Differences in the sensitivity to purinergic stimulation of myelinating and non-myelinating Schwann cells in peripheral human and rat nerve. Glia 23(4): 374-382.
42. Grafe P, Mayer C, Takigawa T, Kamleiter M, Sanchez-Brandelik R (1999) Confocal calcium imaging reveals an ionotropic P2 nucleotide receptor in the paranodal membrane of rat Schwann cells. J Physiol 515(Pt 2): 377-383.
43. Rousse I, Robitaille R (2006) Calcium signaling in Schwann cells at synaptic and extra-synaptic sites: active glial modulation of neuronal activity. Glia 54(7): 691-699.
44. Stevens B, Ishibashi T, Chen JF, Fields RD (2004) Adenosine: an activity-dependent axonal signal regulating MAP kinase and proliferation in developing Schwann cells. Neuron Glia Biol 1(1): 23-34.
45. Wachtler J, Mayer C, Grafe P (1998) Activity-dependent intracellular Ca2+ transients in unmyelinated nerve fibres of the isolated adult rat vagus nerve. Pflugers Arch 435(5): 678-686.
46. Verderio C, Bianco F, Blanchard MP, Bergami M, Canossa M, Scarfone E, Matteoli M (2006) Cross talk between vestibular neurons and Schwann cells mediates BDNF release and neuronal regeneration. Brain Cell Biol 35(2-3): 187-201.
47. Zimmermann H, Braun N, Kegel B, Heine P (1998) New insights into molecular structure and function of ectonucleotidases in the nervous system. Neurochem Int 32(5-6): 421-425.
48. Richardson WD, Kessaris N, Pringle N (2006) Oligodendrocyte wars. Nat Rev Neurosci 7(1): 11-18.
49. de Castro F, Bribian A (2005) The molecular orchestra of the migration of oligodendrocyte precursors during development. Brain Res Brain Res Rev 49(2): 227-241.
50. Stevens B, Porta S, Haak LL, Gallo V, Fields RD (2002) Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36(5): 855-868.
51. Othman T, Yan H, Rivkees SA (2003) Oligodendrocytes express functional A1 adenosine receptors that stimulate cellular migration. Glia 44(2): 166-172.
52. Takeda M, Nelson DJ, Soliven B (1995) Calcium signaling in cultured rat oligodendrocytes. Glia 14(3): 225-236.
53. Agresti C, Meomartini ME, Amadio S, Ambrosini E, Serafini B, Franchini L, Volonte C, Aloisi F, Visentin S (2005) Metabotropic P2 receptor activation regulates oligodendrocyte progenitor migration and development. Glia 50(2): 132-144.
54. Fumagalli M, Daniele S, Lecca D, Lee PR, Parravicini C, Fields RD, Rosa P, Antonucci F, Verderio C, Trincavelli ML, Bramanti P, Martini C, Abbracchio MP (2011) Phenotypic changes, signaling pathway, and functional correlates of GPR17-expressing neural precursor cells during oligodendrocyte differentiation. J Biol Chem 286(12): 10593-10604.
55. Ishibashi T, Dakin KA, Stevens B, Lee PR, Kozlov SV, Stewart CL, Fields RD (2006) Astrocytes promote myelination in response to electrical impulses. Neuron 49(6): 823-832.
56. Stankoff B, Aigrot MS, Noel F, Wattilliaux A, Zalc B, Lubetzki C (2002) Ciliary neurotrophic factor (CNTF) enhances myelin formation: a novel role for CNTF and CNTF-related molecules. J Neurosci 22(21): 9221-9227.
57. Amadio S, Tramini G, Martorana A, Viscomi MT, Sancesario G, Bernardi G, Volonte C (2006) Oligodendrocytes express P2Y12 metabotropic receptor in adult rat brain. Neuroscience 141(3): 1171-1180.
58. Amadio S, Montilli C, Magliozzi R, Bernardi G, Reynolds R, Volonte C (2010) P2Y12 receptor protein in cortical gray matter lesions in multiple sclerosis. Cereb Cortex 20(6): 1263-1273.
59. Ciana P, Fumagalli M, Trincavelli ML, Verderio C, Rosa P, Lecca D, Ferrario S, Parravicini C, Capra V, Gelosa P, Guerrini U, Belcredito S, Cimino M, Sironi L, Tremoli E, Rovati GE, Martini C, Abbracchio MP (2006) The orphan receptor GPR17 identified as a new dual uracil nucleotides/cysteinyl-leukotrienes receptor. EMBO J 25(19): 4615-4627.
60. Benned-Jensen T, Rosenkilde MM (2010) Distinct expression and ligand-binding profiles of two constitutively active GPR17 splice variants. Br J Pharmacol 159(5): 1092-1105.
61. Lecca D, Trincavelli ML, Gelosa P, Sironi L, Ciana P, Fumagalli M, Villa G, Verderio C, Grumelli C, Guerrini U, Tremoli E, Rosa P, Cuboni S, Martini C, Buffo A, Cimino M, Abbracchio MP (2008) The recently identified P2Y-like receptor GPR17 is a sensor of brain damage and a new target for brain repair. PLoS One 3(10): e3579.
62. Chen Y, Wu H, Wang S, Koito H, Li J, Ye F, Hoang J, Escobar SS, Gow A, Arnett HA, Trapp BD, Karandikar NJ, Hsieh J, Lu QR (2009) The oligodendrocyte-specific G protein-coupled receptor GPR17 is a cell-intrinsic timer of myelination. Nat Neurosci 12(11): 1398-1406.
63. Ceruti S, Viganò F, Boda E, Ferrario S, Magni G, Boccazzi M, Rosa P, Buffo A, Abbracchio MP (2011) Expression of the new P2Y-like receptor GPR17 during oligodendrocyte precursor cell maturation regulates sensitivity to ATP-induced death. Glia 59(3): 363-378.
64. Pugliese AM, Trincavelli ML, Lecca D, Coppi E, Fumagalli M, Ferrario S, Failli P, Daniele S, Martini C, Pedata F, Abbracchio MP (2009) Functional characterization of two isoforms of the P2Y-like receptor GPR17: [35S]GTPgammaS binding and electrophysiological studies in 1321N1 cells. Am J Physiol Cell Physiol 297(4): C1028-C1040.
65. Ceruti S, Villa G, Genovese T, Mazzon E, Longhi R, Rosa P, Bramanti P, Cuzzocrea S, Abbracchio MP (2009) The P2Y-like receptor GPR17 as a sensor of damage and a new potential target in spinal cord injury. Brain 132(Pt 8): 2206-2218.
66. Boda E, Viganò F, Rosa P, Fumagalli M, Labat-gest V, Tempia F, Abbracchio MP, Dimou L, Buffo A (2011) The GPR17 receptor in NG2 expressing cells: focus on in vivo cell maturation and participation in acute trauma and chronic damage. Glia 59: 1958-1973.
67. 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(35): 9525-9533.
68. Domercq M, Perez-Samartin A, Aparicio D, Alberdi E, Pampliega O, Matute C (2010) P2X7 receptors mediate ischemic damage to oligodendrocytes. Glia 58(6): 730-740.
69. Nishiyama A, Chang A, Trapp BD (1999) NG2+ glial cells: a novel glial cell population in the adult brain. J Neuropathol Exp Neurol 58(11): 1113-1124.
70. Windrem MS, Nunes MC, Rashbaum WK, Schwartz TH, Goodman RA, McKhann G 2nd, Roy NS, Goldman SA (2004) Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dysmyelinated brain. Nat Med 10(1): 93-97.
71. Nishiyama A, Komitova M, Suzuki R, Zhu X (2009) Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 10(1): 9-22.
72. Butt AM, Duncan A, Hornby MF, Kirvell SL, Hunter A, Levine JM, Berry M (1999) Cells expressing the NG2 antigen contact nodes of Ranvier in adult CNS white matter. Glia 26(1): 84-91.
73. Ong WY, Levine JM (1999) A light and electron microscopic study of NG2 chondroitin sulfate proteoglycan-positive oligodendrocyte precursor cells in the normal and kainate-lesioned rat hippocampus. Neuroscience 92(1): 83-95.
74. Nishiyama A, Watanabe M, Yang Z, Bu J (2002) Identity, distribution, and development of polydendrocytes: NG2-expressing glial cells. J Neurocytol 31(6-7): 437-455.
75. Butt AM, Kiff J, Hubbard P, Berry M (2002) Synantocytes: new functions for novel NG2 expressing glia. J Neurocytol 31(6-7): 551-565.
76. Butt AM, Hamilton N, Hubbard P, Pugh M, Ibrahim M (2005) Synantocytes: the fifth element. J Anat 207(6): 695-706.
77. Hamilton N, Vayro S, Wigley R, Butt AM (2010) Axons and astrocytes release ATP and glutamate to evoke calcium signals in NG2-glia. Glia 58(1): 66-79.
78. Belachew S, Gallo V (2004) Synaptic and extrasynaptic neurotransmitter receptors in glial precursors' quest for identity. Glia 48(3): 185-196.
79. Nishiyama A (2007) Polydendrocytes: NG2 cells with many roles in development and repair of the CNS. Neuroscientist 13(1): 62-76.
80. Ciceri P, Rabuffetti M, Monopoli A, Nicosia S (2001) Production of leukotrienes in a model of focal cerebral ischaemia in the rat. Br J Pharmacol 133(8): 1323-1329.
81. Melani A, Turchi D, Vannucchi MG, Cipriani S, Gianfriddo M, Pedata F (2005) ATP extracellular concentrations are increased in the rat striatum during in vivo ischemia. Neurochem Int 47(6): 442-448.
82. 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(3): 579-582.
83. 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): 1-7.
84. Lai AY, Todd KG (2008) Differential regulation of trophic and proinflammatory microglial effectors is dependent on severity of neuronal injury. Glia 56(3): 259-270.
85. Sperlagh B, Illes P (2007) Purinergic modulation of microglial cell activation. Purinergic Signal 3(1-2): 117-127.
86. Wang X, Arcuino G, Takano T, Lin J, Peng WG, Wan P, Li P, Xu Q, Liu QS, Goldman SA, Nedergaard M (2004) P2X7 receptor inhibition improves recovery after spinal cord injury. Nat Med 10(8): 821-827.
87. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8(6): 752-758.
88. Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10(11): 1387-1394.
89. Honda S, Sasaki Y, Ohsawa K, Imai Y, Nakamura Y, Inoue K, Kohsaka S (2001) Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J Neurosci 21(6): 1975-1982.
90. Haynes SE, Hollopeter G, Yang G, Kurpius D, Dailey ME, Gan WB, Julius D (2006) The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci 9(12): 1512-1519.
91. Rouach N, Calvo CF, Glowinski J, Giaume C (2002) Brain macrophages inhibit gap junctional communication and downregulate connexin 43 expression in cultured astrocytes. Eur J Neurosci 15(2): 403-407.
92. 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(2-3): 202-210.
93. Di Virgilio F (2000) Dr. Jekyll/Mr. Hyde: the dual role of extracellular ATP. J Auton Nerv Syst 81(1-3): 59-63.
94. Sanz JM, Chiozzi P, Ferrari D, Colaianna M, Idzko M, Falzoni S, Fellin R, Trabace L, Di Virgilio F (2009) Activation of microglia by amyloid {beta} requires P2X7 receptor expression. J Immunol 182(7): 4378-4385.
95. Koizumi S, Shigemoto-Mogami Y, Nasu-Tada K, Shinozaki Y, Ohsawa K, Tsuda M, Joshi BV, Jacobson KA, Kohsaka S, Inoue K (2007) UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 446(7139): 1091-1095.
96. Gyoneva S, Orr AG, Traynelis SF (2009) Differential regulation of microglial motility by ATP/ADP and adenosine. Parkinsonism Relat Disord 15(Suppl 3): S195-S199.
97. Monif M, Burnstock G, Williams DA (2010) Microglia: proliferation and activation driven by the P2X7 receptor. Int J Biochem Cell Biol 42(11): 1753-1756.
98. Di Virgilio F, Sanz JM, Chiozzi P, Falzoni S (1999) The P2Z/P2X7 receptor of microglial cells: a novel immunomodulatory receptor. Prog Brain Res 120: 355-368.
99. Tessier PA, Naccache PH, Clark-Lewis I, Gladue RP, Neote KS, McColl SR (1997) Chemokine networks in vivo: involvement of C-X-C and C-C chemokines in neutrophil extravasation in vivo in response to TNF-alpha. J Immunol 159(7): 3595-3602.
100. 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(3): 810-819.
101. Franke H, Gunther A, Grosche J, Schmidt R, Rossner S, Reinhardt R, Faber-Zuschratter H, Schneider D, Illes P (2004) P2X7 receptor expression after ischemia in the cerebral cortex of rats. J Neuropathol Exp Neurol 63(7): 686-699.
102. Yiangou Y, Facer P, Durrenberger P, Chessell IP, Naylor A, Bountra C, Banati RR, Anand P (2006) COX-2, CB2 and P2X7-immunoreactivities are increased in activated microglial cells/macrophages of multiple sclerosis and amyotrophic lateral sclerosis spinal cord. BMC Neurol 6: 12.
103. Adinolfi E, Melchiorri L, Falzoni S, Chiozzi P, Morelli A, Tieghi A, Cuneo A, Castoldi G, Di Virgilio F, Baricordi OR (2002) P2X7 receptor expression in evolutive and indolent forms of chronic B lymphocytic leukemia. Blood 99(2): 706-708.
104. 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(3): 745-758.
105. 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(12): 3781-3791.
106. Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P, Skatchkov SN, Osborne NN, Reichenbach A (2006) Muller cells in the healthy and diseased retina. Prog Retin Eye Res 25(4): 397-424.
107. Bringmann A, Wiedemann P (2009) Involvement of Muller glial cells in epiretinal membrane formation. Graefes Arch Clin Exp Ophthalmol 247(7): 865-883.
108. Wurm A, Pannicke T, Iandiev I, Francke M, Hollborn M, Wiedemann P, Reichenbach A, Osborne NN, Bringmann A (2011) Purinergic signaling involved in Muller cell function in the mammalian retina. Prog Retin Eye Res 30(5): 324-342.
109. Pannicke T, Fischer W, Biedermann B, Schadlich H, Grosche J, Faude F, Wiedemann P, Allgaier C, Illes P, Burnstock G, Reichenbach A (2000) P2X7 receptors in Muller glial cells from the human retina. J Neurosci 20(16): 5965-5972.
110. Innocenti B, Pfeiffer S, Zrenner E, Kohler K, Guenther E (2004) ATP-induced non-neuronal cell permeabilization in the rat inner retina. J Neurosci 24(39): 8577-8583.
111. Uckermann O, Wolf A, Kutzera F, Kalisch F, Beck-Sickinger AG, Wiedemann P, Reichenbach A, Bringmann A (2006) Glutamate release by neurons evokes a purinergic inhibitory mechanism of osmotic glial cell swelling in the rat retina: activation by neuropeptide Y. J Neurosci Res 83(4): 538-550.
112. Wurm A, Pannicke T, Iandiev I, Buhner E, Pietsch UC, Reichenbach A, Wiedemann P, Uhlmann S, Bringmann A (2006) Changes in membrane conductance play a pathogenic role in osmotic glial cell swelling in detached retinas. Am J Pathol 169(6): 1990-1998.
113. Wurm A, Pannicke T, Wiedemann P, Reichenbach A, Bringmann A (2008) Glial cell-derived glutamate mediates autocrine cell volume regulation in the retina: activation by VEGF. J Neurochem 104(2): 386-399.
114. Newman EA, Zahs KR (1998) Modulation of neuronal activity by glial cells in the retina. J Neurosci 18(11): 4022-4028.
115. Newman EA (2005) Calcium increases in retinal glial cells evoked by light-induced neuronal activity. J Neurosci 25(23): 5502-5510.
116. Newman EA, Zahs KR (1997) Calcium waves in retinal glial cells. Science 275(5301): 844-847.
117. Guidry C (2005) The role of Muller cells in fibrocontractive retinal disorders. Prog Retin Eye Res 24(1): 75-86.
118. Bringmann A, Pannicke T, Moll V, Milenkovic I, Faude F, Enzmann V, Wolf S, Reichenbach A (2001) Upregulation of P2X(7) receptor currents in Muller glial cells during proliferative vitreoretinopathy. Invest Ophthalmol Vis Sci 42(3): 860-867.
119. Uhlmann S, Bringmann A, Uckermann O, Pannicke T, Weick M, Ulbricht E, Goczalik I, Reichenbach A, Wiedemann P, Francke M (2003) Early glial cell reactivity in experimental retinal detachment: effect of suramin. Invest Ophthalmol Vis Sci 44(9): 4114-4122.
120. Bull ND, Martin KR (2011) Concise review: toward stem cell-based therapies for retinal neurodegenerative diseases. Stem Cells 29(8): 1170-1175.
121. Lawrence JM, Singhal S, Bhatia B, Keegan DJ, Reh TA, Luthert PJ, Khaw PT, Limb GA (2007) MIO-M1 cells and similar Müller glial cell lines derived from adult human retina exhibit neural stem cell characteristics. Stem Cells 25(8): 2033-2043.
122. Del Debbio CB, Balasubramanian S, Parameswaran S, Chaudhuri A, Qiu F, Ahmad I (2010) Notch and Wnt signaling mediated rod photoreceptor regeneration by Müller cells in adult mammalian retina. PLoS One 5(8): e12425.
123. Dublin P, Hanani M (2007) Satellite glial cells in sensory ganglia: their possible contribution to inflammatory pain. Brain Behav Immun 21(5): 592-598.
124. Jasmin L, Vit JP, Bhargava A, Ohara PT (2010) Can satellite glial cells be therapeutic targets for pain control? Neuron Glia Biol 6(1): 63-71.
125. Villa G, Fumagalli M, Verderio C, Abbracchio MP, Ceruti S (2010) Expression and contribution of satellite glial cells purinoceptors to pain transmission in sensory ganglia: an update. Neuron Glia Biol 6(1): 31-42.
126. Ceruti S, Fumagalli M, Villa G, Verderio C, Abbracchio MP (2008) Purinoceptor-mediated calcium signaling in primary neuron-glia trigeminal cultures. Cell Calcium 43(6): 576-590.
127. Kushnir R, Cherkas PS, Hanani M (2011) Peripheral inflammation upregulates P2X receptor expression in satellite glial cells of mouse trigeminal ganglia: a calcium imaging study. Neuropharmacology 61(4): 739-746.
128. Ceruti S, Villa G, Fumagalli M, Colombo L, Magni G, Zanardelli M, Fabbretti E, Verderio C, van den Maagdenberg AM, Nistri A, Abbracchio MP (2011) Calcitonin gene-related peptide-mediated enhancement of purinergic neuron/glia communication by the algogenic factor bradykinin in mouse trigeminal ganglia from wild-type and R192Q Cav2. 1 Knock-in mice: implications for basic mechanisms of migraine pain. J Neurosci 31(10): 3638-3649.
129. Sevc J, Daxnerova Z, Hanova V, Koval J (2011) Novel observations on the origin of ependymal cells in the ventricular zone of the rat spinal cord. Acta Histochem 113(2): 156-162.
130. Mothe AJ, Tator CH (2005) Proliferation, migration, and differentiation of endogenous ependymal region stem/progenitor cells following minimal spinal cord injury in the adult rat. Neuroscience 131(1): 177-187.
131. Meletis K, Barnabe-Heider F, Carlen M, Evergren E, Tomilin N, Shupliakov O, Frisen J (2008) Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol 6(7): e182.
132. 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.
133. 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 U S A 106(30): 12489-12493.
134. Armulik A, Genove G, Mae M, Nisancioglu MH, Wallgard E, Niaudet C, He L, Norlin J, Lindblom P, Strittmatter K, Johansson BR, Betsholtz C (2010) Pericytes regulate the blood-brain barrier. Nature 468(7323): 557-561.
135. Krueger M, Bechmann I (2010) CNS pericytes: concepts, misconceptions, and a way out. Glia 58(1): 1-10.
136. Dore-Duffy P (2008) Pericytes: pluripotent cells of the blood brain barrier. Curr Pharm Des 14(16): 1581-1593.
137. Ceruti S, Colombo L, Magni G, Viganò F, Boccazzi M, Deli MA, Sperlagh B, Abbracchio MP, Kittel A (2011) Oxygen-glucose deprivation increases the enzymatic activity and the microvescicle-mediated release of ectonucleotidases in the cells composing the blood-brain barrier. Neurochem Int 59(2): 259-271.
138. Kittel A, Sperlagh B, Pelletier J, Sevigny J, Kirley TL (2007) Transient changes in the localization and activity of ecto-nucleotidases in rat hippocampus following lipopolysaccharide treatment. Int J Dev Neurosci 25(5): 275-282.
139. Gulbransen BD, Sharkey KA (2009) Purinergic neuron-to-glia signaling in the enteric nervous system. Gastroenterology 136(4): 1349-1358.
140. Burnstock G (2008) The journey to establish purinergic signalling in the gut. Neurogastroenterol Motil 20(Suppl 1): 8-19.
141. Hanani M, Francke M, Hartig W, Grosche J, Reichenbach A, Pannicke T (2000) Patch-clamp study of neurons and glial cells in isolated myenteric ganglia. Am J Physiol Gastrointest Liver Physiol 278(4): G644-G651.
142. Ruhl A (2005) Glial cells in the gut. Neurogastroenterol Motil 17(6): 777-790.
143. Vanderwinden JM, Timmermans JP, Schiffmann SN (2003) Glial cells, but not interstitial cells, express P2X7, an ionotropic purinergic receptor, in rat gastrointestinal musculature. Cell Tissue Res 312(2): 149-154.
144. Kimball BC, Mulholland MW (1996) Enteric glia exhibit P2U receptors that increase cytosolic calcium by a phospholipase C-dependent mechanism. J Neurochem 66(2): 604-612.
145. Sarosi GA, Barnhart DC, Turner DJ, Mulholland MW (1998) Capacitative Ca2+ entry in enteric glia induced by thapsigargin and extracellular ATP. Am J Physiol 275(3 Pt 1): G550-G555.
146. Zhang W, Segura BJ, Lin TR, Hu Y, Mulholland MW (2003) Intercellular calcium waves in cultured enteric glia from neonatal guinea pig. Glia 42(3): 252-262.
147. Gulbransen BD, Bains JS, Sharkey KA (2010) Enteric glia are targets of the sympathetic innervation of the myenteric plexus in the guinea pig distal colon. J Neurosci 30(19): 6801-6809.
148. Braun N, Sevigny J, Robson SC, Hammer K, Hanani M, Zimmermann H (2004) Association of the ecto-ATPase NTPDase2 with glial cells of the peripheral nervous system. Glia 45(2): 124-132.