DCPIB, the proposed selective blocker of volume-regulated anion channels, inhibits several glutamate transport pathways in glial cellss

Molecular Pharmacology

Volumn 83, Issue 1, 2013, Pages 22-32

  Bowens, Nicole H ^a   Dohare, Preeti ^a   Kuo, Yu Hung ^b   Mongin, Alexander A ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (2 BUTYL 6,7 DICHLORO 2 CYCLOPENTYL INDAN 1 ON 5 YL)OXOBUTYRIC ACID; ANION CHANNEL; ASPARTIC ACID; BUTYRIC ACID DERIVATIVE; CARBON 14; CYSTINE; EXCITATORY AMINO ACID TRANSPORTER; GAP JUNCTION PROTEIN; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; SMALL INTERFERING RNA; TRITIUM; UNCLASSIFIED DRUG; VOLUME REGULATED ANION CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PERMEABILIZATION; GENE SILENCING; GLIA CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN TRANSPORT; RAT; SYNAPTOSOME;

ADENOSINE TRIPHOSPHATE; AMINO ACID TRANSPORT SYSTEM Y+; AMINO ACID TRANSPORT SYSTEMS; ANIMALS; ASTROCYTES; BIOLOGICAL TRANSPORT; CELLS, CULTURED; CEREBRAL CORTEX; CONNEXINS; CYCLOPENTANES; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; GLUTAMIC ACID; INDANS; MICROGLIA; PERMEABILITY; PRIMARY CELL CULTURE; RATS; RECEPTORS, PURINERGIC P2X7; SYNAPTOSOMES;

EID: 84871539801     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.112.080457     Document Type: Article

References (60)

1. Abdullaev IF, Rudkouskaya A, Schools GP, Kimelberg HK, and Mongin AA (2006) Pharmacological comparison of swelling-activated excitatory amino acid release and Cl- currents in cultured rat astrocytes. J Physiol 572:677-689.
2. Akita T, Fedorovich SV, and Okada Y (2011) Ca2+ nanodomain-mediated component of swelling-induced volume-sensitive outwardly rectifying anion current triggered by autocrine action of ATP in mouse astrocytes. Cell Physiol Biochem 28:1181-1190.
3. Bannai S (1986) Exchange of cystine and glutamate across plasma membrane of human fibroblasts. J Biol Chem 261:2256-2263.
4. Bargiotas P, Krenz A, Hormuzdi SG, Ridder DA, Herb A, Barakat W, Penuela S, von Engelhardt J, Monyer H, and Schwaninger M (2011) Pannexins in ischemia-induced neurodegeneration. Proc Natl Acad Sci USA 108:20772-20777.
5. Benfenati V, Caprini M, Nicchia GP, Rossi A, Dovizio M, Cervetto C, Nobile M, and Ferroni S (2009) Carbenoxolone inhibits volume-regulated anion conductance in cultured rat cortical astroglia. Channels (Austin) 3:323-336.
6. Best L, Yates AP, Decher N, Steinmeyer K, and Nilius B (2004) Inhibition of glucose-induced electrical activity in rat pancreatic beta-cells by DCPIB, a selective inhibitor of volume-sensitive anion currents. Eur J Pharmacol 489:13-19. (Pubitemid 38520066)
7. Choi DW (1992) Excitotoxic cell death. J Neurobiol 23:1261-1276.
8. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1-105.
9. Decher N, Lang HJ, Nilius B, Brüggemann A, Busch AE, and Steinmeyer K (2001) DCPIB is a novel selective blocker of I(Cl,swell) and prevents swelling-induced shortening of guinea-pig atrial action potential duration. Br J Pharmacol 134:1467-1479. (Pubitemid 33131898)
10. Duan S, Anderson CM, Keung EC, Chen Y, Chen Y, and Swanson RA (2003) P2X7 receptor-mediated release of excitatory amino acids from astrocytes. J Neurosci 23:1320-1328. (Pubitemid 36258910)
11. Feustel PJ, Jin Y, and Kimelberg HK (2004) Volume-regulated anion channels are the predominant contributors to release of excitatory amino acids in the ischemic cortical penumbra. Stroke 35:1164-1168. (Pubitemid 38543537)
12. Fisher SK, Heacock AM, Keep RF, and Foster DJ (2010) Receptor regulation of osmolyte homeostasis in neural cells. J Physiol 588:3355-3364.
13. Fogal B, Li J, Lobner D, McCullough LD, and Hewett SJ (2007) System x(c)- activity and astrocytes are necessary for interleukin-1 beta-mediated hypoxic neuronal injury. J Neurosci 27:10094-10105. (Pubitemid 47450471)
14. Hajós F (1975) An improved method for the preparation of synaptosomal fractions in high purity. Brain Res 93:485-489.
15. Harrigan TJ, Abdullaev IF, Jourd'heuil D, and Mongin AA (2008) Activation of microglia with zymosan promotes excitatory amino acid release via volume-regulated anion channels: the role of NADPH oxidases. J Neurochem 106:2449-2462.
16. Heacock AM, Dodd MS, and Fisher SK (2006) Regulation of volume-sensitive osmolyte efflux from human SH-SY5Y neuroblastoma cells following activation of lysophospholipid receptors. J Pharmacol Exp Ther 317:685-693.
17. Hoffmann EK, Lambert IH, and Pedersen SF (2009) Physiology of cell volume regulation in vertebrates. Physiol Rev 89:193-277.
18. Hyzinski-García MC, Vincent MY, Haskew-Layton RE, Dohare P, Keller RW, Jr, and Mongin AA (2011) Hypo-osmotic swelling modifies glutamate-glutamine cycle in the cerebral cortex and in astrocyte cultures. J Neurochem 118:140-152.
19. Iglesias R, Dahl G, Qiu F, Spray DC, and Scemes E (2009) Pannexin 1: the molecular substrate of astrocyte "hemichannels". J Neurosci 29:7092-7097.
20. Jackman NA, Uliasz TF, Hewett JA, and Hewett SJ (2010) Regulation of system x(c) (-)activity and expression in astrocytes by interleukin-1β: implications for hypoxic neuronal injury. Glia 58:1806-1815.
21. Kimelberg HK (2005) Astrocytic swelling in cerebral ischemia as a possible cause of injury and target for therapy. Glia 50:389-397.
22. Kimelberg HK, Feustel PJ, Jin Y, Paquette J, Boulos A, Keller RW, Jr, and Tranmer BI (2000) Acute treatment with tamoxifen reduces ischemic damage following middle cerebral artery occlusion. Neuroreport 11:2675-2679.
23. Kimelberg HK, Jin Y, Charniga C, and Feustel PJ (2003) Neuroprotective activity of tamoxifen in permanent focal ischemia. J Neurosurg 99:138-142. (Pubitemid 36753888)
24. Lang F, Busch GL, Ritter M, Völkl H, Waldegger S, Gulbins E, and Häussinger D (1998) Functional significance of cell volume regulatory mechanisms. Physiol Rev 78:247-306. (Pubitemid 28070981)
25. Lee S, Yoon BE, Berglund K, Oh SJ, Park H, Shin HS, Augustine GJ, and Lee CJ (2010) Channel-mediated tonic GABA release from glia. Science 330:790-796.
26. Liu HT, Akita T, Shimizu T, Sabirov RZ, and Okada Y (2009) Bradykinin-induced astrocyte-neuron signalling: glutamate release is mediated by ROS-activated volume-sensitive outwardly rectifying anion channels. J Physiol 587:2197-2209.
27. Melendez RI, Vuthiganon J, and Kalivas PW (2005) Regulation of extracellular glutamate in the prefrontal cortex: focus on the cystine glutamate exchanger and group I metabotropic glutamate receptors. J Pharmacol Exp Ther 314:139-147. (Pubitemid 41065025)
28. Min XJ, Li H, Hou SC, He W, Liu J, Hu B, and Wang J (2011) Dysfunction of volume-sensitive chloride channels contributes to cisplatin resistance in human lung adenocarcinoma cells. Exp Biol Med (Maywood) 236:483-491.
29. Mongin AA (2007) Disruption of ionic and cell volume homeostasis in cerebral ischemia: The perfect storm. Pathophysiology 14:183-193.
30. Mongin AA and Kimelberg HK (2002) ATP potently modulates anion channel-mediated excitatory amino acid release from cultured astrocytes. Am J Physiol Cell Physiol 283:C569-C578. (Pubitemid 34787540)
31. Mongin AA and Kimelberg HK (2003) Is autocrine ATP release required for activation of volume-sensitive chloride channels? J Neurophysiol 90 :2791-2792, author reply 2792-2793.
32. Mongin AA and Kimelberg HK (2005) Astrocytic swelling in neuropathology, in Neuroglia (Kettenmann H and Ransom BR eds) pp 550-562, Oxford University Press, Oxford, New York.
33. Mongin AA and Orlov SN (2001) Mechanisms of cell volume regulation and possible nature of the cell volume sensor. Pathophysiology 8 :77-88. (Pubitemid 33108983)
34. Musil LS and Goodenough DA (1991) Biochemical analysis of connexin43 intracellular transport, phosphorylation, and assembly into gap junctional plaques. J Cell Biol 115:1357-1374. (Pubitemid 21909980)
35. Nakajima K, Tohyama Y, Kohsaka S, and Kurihara T (2001) Ability of rat microglia to uptake extracellular glutamate. Neurosci Lett 307:171-174. (Pubitemid 32595656)
36. Nilius B, Eggermont J, Voets T, Buyse G, Manolopoulos V, and Droogmans G (1997) Properties of volume-regulated anion channels in mammalian cells. Prog Biophys Mol Biol 68:69-119. (Pubitemid 28066409)
37. Okada Y (1997) Volume expansion-sensing outward-rectifier Cl- channel: fresh start to the molecular identity and volume sensor. Am J Physiol 273:C755-C789.
38. Okada Y (2006) Cell volume-sensitive chloride channels: phenotypic properties and molecular identity. Contrib Nephrol 152:9-24.
39. Orellana JA, Sáez PJ, Shoji KF, Schalper KA, Palacios-Prado N, Velarde V, Giaume C, Bennett MV, and Sáez JC (2009) Modulation of brain hemichannels and gap junction channels by pro-inflammatory agents and their possible role in neurodegeneration. Antioxid Redox Signal 11:369-399.
40. Park H, Oh SJ, Han KS, Woo DH, Park H, Mannaioni G, Traynelis SF, and Lee CJ (2009) Bestrophin-1 encodes for the Ca2+-activated anion channel in hippocampal astrocytes. J Neurosci 29:13063-13073.
41. Patel SA, Warren BA, Rhoderick JF, and Bridges RJ (2004) Differentiation of substrate and non-substrate inhibitors of transport system xc(-): an obligate exchanger of L-glutamate and L-cystine. Neuropharmacology 46:273-284. (Pubitemid 37532835)
42. Pedersen SF, Prenen J, Droogmans G, Hoffmann EK, and Nilius B (1998) Separate swelling- and Ca2+-activated anion currents in Ehrlich ascites tumor cells. J Membr Biol 163:97-110. (Pubitemid 28255126)
43. Pelegrin P and Surprenant A (2006) Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J 25:5071-5082. (Pubitemid 44658525)
44. Reimer RJ and Edwards RH (2004) Organic anion transport is the primary function of the SLC17/type I phosphate transporter family. Pflugers Arch 447:629-635. (Pubitemid 38241447)
45. Rosenberg D, Kartvelishvily E, Shleper M, Klinker CM, Bowser MT, and Wolosker H (2010) Neuronal release of D-serine: a physiological pathway controlling extracellular D-serine concentration. FASEB J 24:2951-2961.
46. Rossi DJ, Oshima T, and Attwell D (2000) Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403:316-321. (Pubitemid 30062388)
47. Rothstein JD, Dykes-Hoberg M, and Pardo CA et al. (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16:675-686. (Pubitemid 26103145)
48. Rudkouskaya A, Sim V, Shah AA, Feustel PJ, Jourd'heuil D, and Mongin AA (2010) Long-lasting inhibition of presynaptic metabolism and neurotransmitter release by protein S-nitrosylation. Free Radic Biol Med 49:757-769.
49. 2 receptor-mediated autocrine role of somatodendritic release of AVP in rat vasopressin neurons under hypo-osmotic conditions. Sci Signal 4:ra5.
50. Seki Y, Feustel PJ, Keller RW, Jr, Tranmer BI, and Kimelberg HK (1999) Inhibition of ischemia-induced glutamate release in rat striatum by dihydrokinate and an anion channel blocker. Stroke 30:433-440. (Pubitemid 29071814)
51. Silverman W, Locovei S, and Dahl G (2008) Probenecid, a gout remedy, inhibits pannexin 1 channels. Am J Physiol Cell Physiol 295:C761-C767.
52. Strange K, Emma F, and Jackson PS (1996) Cellular and molecular physiology of volume-sensitive anion channels. Am J Physiol 270:C711-C730.
53. Swanson RA, Liu J, Miller JW, Rothstein JD, Farrell K, Stein BA, and Longuemare MC (1997) Neuronal regulation of glutamate transporter subtype expression in astrocytes. J Neurosci 17:932-940. (Pubitemid 27043952)
54. Szatkowski M, Barbour B, and Attwell D (1990) Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature 348:443-446. (Pubitemid 120015084)
55. Takeuchi H, Jin S, Wang J, Zhang G, Kawanokuchi J, Kuno R, Sonobe Y, Mizuno T, and Suzumura A (2006) Tumor necrosis factor-alpha induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J Biol Chem 281:21362-21368. (Pubitemid 44115475)
56. Thompson RJ, Zhou N, and MacVicar BA (2006) Ischemia opens neuronal gap junction hemichannels. Science 312:924-927. (Pubitemid 43727327)
57. Verkman AS and Galietta LJ (2009) Chloride channels as drug targets. Nat Rev Drug Discov 8:153-171.
58. Ye ZC, Oberheim N, Kettenmann H, and Ransom BR (2009) Pharmacological "crossinhibition" of connexin hemichannels and swelling activated anion channels. Glia 57:258-269.
59. Ye ZC, Wyeth MS, Baltan-Tekkok S, and Ransom BR (2003) Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J Neurosci 23:3588-3596. (Pubitemid 36958466)
60. Zhang Y, Zhang H, Feustel PJ, and Kimelberg HK (2008) DCPIB, a specific inhibitor of volume regulated anion channels (VRACs), reduces infarct size in MCAo and the release of glutamate in the ischemic cortical penumbra. Exp Neurol 210:514-520.