Nonvesicular Release of ATP from Rat Retinal Glial (Müller) Cells is Differentially Mediated in Response to Osmotic Stress and Glutamate

Neurochemical Research

Volumn 40, Issue 4, 2015, Pages 651-660

  Voigt, Juliane ^a   Grosche, Antje ^b   Vogler, Stefanie ^a   Pannicke, Thomas ^a   Hollborn, Margrit ^a   Kohen, Leon ^c   Wiedemann, Peter ^a   Reichenbach, Andreas ^a   Bringmann, Andreas ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c HELIOS Klinikum Aue   (Germany)

Author keywords

ATP; Cell swelling; Glia; Glutamate; Osmotic stress; Retina

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANNEXIN; GAP JUNCTION PROTEIN; GLUTAMIC ACID; MESSENGER RNA;

ANIMAL; FEMALE; GENETICS; LONG EVANS RAT; MACROGLIA; MALE; METABOLISM; OSMOTIC PRESSURE; RAT; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANNEXINS; CONNEXINS; EPENDYMOGLIAL CELLS; FEMALE; GLUTAMIC ACID; MALE; OSMOTIC PRESSURE; RATS; RATS, LONG-EVANS; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84940003370     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-014-1511-z     Document Type: Article

References (36)

1. Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H (2009) Purinergic signalling in the nervous system: an overview. Trends Neurosci 32:19–29
2. Bao L, Locovei S, Dahl G (2004) Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett 572:65–68
3. Barbe MT, Monyer H, Bruzzone R (2006) Cell–cell communication beyond connexins: the pannexin channels. Physiology (Bethesda) 21:103–114
4. Boeynaems JM, Communi D, Gonzalez NS, Robaye B (2005) Overview of the P2 receptors. Semin Thromb Hemost 31:139–149
5. Braunstein GM, Roman RM, Clancy JP, Kudlow BA, Taylor AL, Shylonsky VG, Jovov B, Peter K, Jilling T, Ismailov II, Benos DJ, Schwiebert LM, Fitz JG, Schwiebert EM (2001) Cystic fibrosis transmembrane conductance regulator facilitates ATP release by stimulating a separate ATP release channel for autocrine control of cell volume regulation. J Biol Chem 276:6621–6630
6. Bringmann A, Uckermann O, Pannicke T, Iandiev I, Reichenbach A, Wiedemann P (2005) Neuronal versus glial cell swelling in the ischaemic retina. Acta Ophthalmol Scand 83:528–538
7. Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P, Skatchkov SN, Osborne NN, Reichenbach A (2006) Müller cells in the healthy and diseased retina. Prog Retin Eye Res 25:397–424
8. Bruzzone R, Barbe MT, Jakob NJ, Monyer H (2005) Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes. J Neurochem 92:1033–1043
9. Dmitriev AV, Govardovskii VI, Schwahn HN, Steinberg RH (1999) Light-induced changes of extracellular ions and volume in the isolated chick retina-pigment epithelium preparation. Vis Neurosci 16:1157–1167
10. Dvoriantchikova G, Ivanov D, Panchin Y, Shestopalov VI (2006) Expression of pannexin family of proteins in the retina. FEBS Lett 580:2178–2182
11. Felmy F, Pannicke T, Richt JA, Reichenbach A, Guenther E (2001) Electrophysiological properties of rat retinal Müller (glial) cells in postnatally developing and in pathologically altered retinae. Glia 34:190–199
12. Housley GD, Bringmann A, Reichenbach A (2009) Purinergic signaling in special senses. Trends Neurosci 32:128–141
13. Krügel K, Wurm A, Linnertz R, Pannicke T, Wiedemann P, Reichenbach A, Bringmann A (2010) Erythropoietin inhibits osmotic swelling of retinal glial cells by Janus kinase and extracellular signal-regulated kinases1/2-mediated release of vascular endothelial growth factor. Neuroscience 165:1147–1158
14. 2+ channels is required for vesicular release of glutamate from retinal glial cells implicated in cell volume regulation. Neuroscience 188:23–34
15. Liu GJ, Kalous A, Werry EL, Bennett MR (2006) Purine release from spinal cord microglia after elevation of calcium by glutamate. Mol Pharmacol 70:851–859
16. Manley GT, Fujimura M, Ma T, Noshita N, Filiz F, Bollen AW, Chan P, Verkman AS (2000) Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat Med 6:159–163
17. Metea MR, Newman EA (2006) Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J Neurosci 26:2862–2870
18. Newman EA (2001) Propagation of intercellular calcium waves in retinal astrocytes and Müller cells. J Neurosci 21:2215–2223
19. Newman EA, Zahs KR (1997) Calcium waves in retinal glial cells. Science 275:844–847
20. Newman EA, Zahs KR (1998) Modulation of neuronal activity by glial cells in the retina. J Neurosci 18:4022–4028
21. Pannicke T, Iandiev I, Uckermann O, Biedermann B, Kutzera F, Wiedemann P, Wolburg H, Reichenbach A, Bringmann A (2004) A potassium channel-linked mechanism of glial cell swelling in the postischemic retina. Mol Cell Neurosci 26:493–502
22. Pearson RA, Dale N, Llaudet E, Mobbs P (2005) ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation. Neuron 46:731–744
23. Reigada D, Mitchell CH (2005) Release of ATP from retinal pigment epithelial cells involves both CFTR and vesicular transport. Am J Physiol 288:C132–C140
24. Reigada D, Lu W, Zhang M, Mitchell CH (2008) Elevated pressure triggers a physiological release of ATP from the retina: possible role for pannexin hemichannels. Neuroscience 157:396–404
25. Resta V, Novelli E, Vozzi G, Scarpa C, Caleo M, Ahluwalia A, Solini A, Santini E, Parisi V, Di Virgilio F, Galli-Resta L (2007) Acute retinal ganglion cell injury caused by intraocular pressure spikes is mediated by endogenous extracellular ATP. Eur J Neurosci 25:2741–2754
26. Skatchkov SN, Eaton MJ, Shuba YM, Kucheryavykh YV, Derst C, Veh RW, Wurm A, Iandiev I, Pannicke T, Bringmann A, Reichenbach A (2006) Tandem-pore domain potassium channels are functionally expressed in retinal (Müller) glial cells. Glia 53:266–276
27. Slezak M, Grosche A, Niemiec A, Tanimoto N, Pannicke T, Münch TA, Crocker B, Isope P, Härtig W, Beck SC, Huber G, Ferracci G, Perraut M, Reber M, Miehe M, Demais V, Lévêque C, Metzger D, Szklarczyk K, Przewlocki R, Seeliger MW, Sage-Ciocca D, Hirrlinger J, Reichenbach A, Reibel S, Pfrieger FW (2012) Relevance of exocytotic glutamate release from retinal glia. Neuron 74:504–516
28. Stout CE, Costantin JL, Naus CCG, Charles AC (2002) Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 277:10482–10488
29. Uckermann O, Vargová L, Ulbricht E, Klaus C, Weick M, Rillich K, Wiedemann P, Reichenbach A, Syková E, Bringmann A (2004) Glutamate-evoked alterations of glial and neuronal cell morphology in the guinea-pig retina. J Neurosci 24:10149–10158
30. Uckermann O, Wolf A, Kutzera F, Kalisch F, Beck-Sickinger A, 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 83:538–550
31. Vogler S, Grosche A, Pannicke T, Ulbricht E, Wiedemann P, Reichenbach A, Bringmann A (2013) Hypoosmotic and glutamate-induced swelling of bipolar cells in the rat retina: comparison with swelling of Müller glial cells. J Neurochem 126:372–381
32. 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 104:386–399
33. Zahs KR, Kofuji P, Meier C, Dermietzel R (2003) Connexin immunoreactivity in glial cells of the rat retina. J Comp Neurol 455:531–546
34. 2+ and kills retinal ganglion cells. Invest Ophthalmol Vis Sci 46:2183–2191
35. 7 receptor stimulation. J Neurochem 98:566–575
36. Zhang X, Li A, Ge J, Reigada D, Laties AM, Mitchell CH (2007) Acute increase of intraocular pressure releases ATP into the anterior chamber. Exp Eye Res 85:637–643