Functional hemichannels in astrocytes: A novel mechanism of glutamate release

Journal of Neuroscience

Volumn 23, Issue 9, 2003, Pages 3588-3596

  Ye, Zu Cheng ^a   Wyeth, Megan S ^a   Baltan Tekkok, Selva ^a   Ransom, Bruce R ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Astrocyte; Divalent cation; Gap junction; Glutamate; Glutamate release; Glutamate transport; Hemichannel

Indexed keywords

18ALPHA GLYCYRRHETINIC ACID; ASPARTIC ACID; BARIUM ION; CALCIUM ION; CARBENOXOLONE; DIVALENT CATION; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; FLUFENAMIC ACID; GLUTAMIC ACID; HEPTANOL; ION CHANNEL; LANTHANUM; LUCIFER YELLOW; MAGNESIUM ION; OCTANOL; PURINE P2X RECEPTOR; STRONTIUM; THAPSIGARGIN; 18ALPHA-GLYCYRRHETINIC ACID; ADENOSINE TRIPHOSPHATE; CALCIUM; CHELATING AGENT; CONNEXIN 43; DRUG DERIVATIVE; FLUORESCENT DYE; GLUTAMATE TRANSPORTER; GLYCYRRHETINIC ACID;

ANIMAL CELL; ARTICLE; ASTROCYTE; CALCIUM MOBILIZATION; CELL COMMUNICATION; CENTRAL NERVOUS SYSTEM; CHANNEL GATING; CONTROLLED STUDY; GAP JUNCTION; HEMICHANNEL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; ANIMAL; CELL CULTURE; CELL JUNCTION; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; IMMUNOHISTOCHEMISTRY; METABOLISM; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ADENOSINE TRIPHOSPHATE; AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; ASPARTIC ACID; ASTROCYTES; BIOLOGICAL TRANSPORT; CALCIUM; CARBENOXOLONE; CATIONS, DIVALENT; CELLS, CULTURED; CHELATING AGENTS; CONNEXIN 43; FLUFENAMIC ACID; FLUORESCENT DYES; GAP JUNCTIONS; GLUTAMIC ACID; GLYCYRRHETINIC ACID; HEPTANOL; IMMUNOHISTOCHEMISTRY; LANTHANUM; OCTANOLS; RATS;

EID: 0037531231     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-09-03588.2003     Document Type: Article

References (63)

1. Armstrong CM, Cota G (1991) Calcium ion as a cofactor in Na channel gating. Proc Natl Acad Sci USA 88:6528-6531.
2. Armstrong CM, Lopez-Barneo J (1987) External calcium ions are required for potassium channel gating in squid neurons. Science 236:712-714.
3. 2+? A critical test employing a heterologous expression system. Proc Natl Acad Sci USA 87:7579-7582.
4. Ballerini P, Rathbone MP, Di Iorio P, Renzetti A, Giuliani P, D'Alimonte I, Trubiani O, Caciagli F, Ciccarelli R (1996) Rat astroglial P2Z (P2X7) receptors regulate intracellular calcium and purine release. NeuroReport 7:2533-2537.
5. Baltan-Tekkok S, Goldberg MP (2001) AMPA/kainate receptor activation mediates hypoxic oligodendrocyte death and axonal injury in cerebral white matter. J Neurosci 21:4237-4248.
6. Bezzi P, Volterra A (2001) A neuron-glia signaling network in the active brain. Curr Opin Neurobiol 11:387-394.
7. Bezzi P, Carmignoto G, Pasti L, Vesce S, Rossi D, Rizzini BL, Pozzan T, Volterra A (1998) Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391:281-285.
8. 0 during anoxia in CNS white matter. NeuroReport 9:1997-2000.
9. + fluxes in intact cells. FASEB J 15:10-12.
10. Butt AM, Ransom BR (1993) Morphology of astrocytes and oligodendrocytes during development in the intact rat optic nerve. J Comp Neurol 338:141-158.
11. Campbell DT, Hille B (1976) Kinetic and pharmacological properties of the sodium channel of frog skeletal muscle. J Gen Physiol 67:309-323.
12. Ceelen PW, Lockridge A, Newman EA (2001) Electrical coupling between glial cells in the rat retina. Glia 35:1-13.
13. Choi DW (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623-634.
14. Contreras JE, Sanchez HA, Eugenin EA, Speidel D, Theis M, Willecke K, Bukauskas FF, Bennett MV, Saez JC (2002) Metabolic inhibition induces opening of unapposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture. Proc Natl Acad Sci USA 99:495-500.
15. Cotrina ML, Kang J, Lin JH, Bueno E, Hansen TW, He L, Liu Y, Nedergaard M (1998) Astrocytic gap junctions remain open during ischemic conditions. J Neurosci 18:2520-2537.
16. Dermietzel R, Hertberg EL, Kessler JA, Spray DC (1991) Gap junctions between cultured astrocytes: immunocytochemical, molecular, and electrophysiological analysis. J Neurosci 11:1421-1432.
17. DeVries SH, Schwartz EA (1992) Hemi-gap-junction channels in solitary horizontal cells of the catfish retina. J Physiol (Lond) 445:201-230.
18. Dubyak GR, el-Moatassim C (1993) Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides. Am J Physiol 265:C577-606.
19. Eskandari S, Zampighi GA, Leung DW, Wright EM, Loo DD (2002) Inhibition of gap junction hemichannels by chloride channel blockers. J Membr Biol 185:93-102.
20. Fern R, Waxman SG, Ransom BR (1995) Endogenous GABA attenuates CNS white matter dysfunction following anoxia. J Neurosci 15:699-708.
21. Frantseva MV, Kokarovtseva L, Perez Velazquez JL (2002a) Ischemia-induced brain damage depends on specific gap-junctional coupling. J Cereb Blood Flow Metab 22:453-462.
22. Frantseva MV, Kokarovtseva L, Naus CG, Carlen PL, MacFabe D, Perez Velazquez JL (2002b) Specific gap junctions enhance the neuronal vulnerability to brain traumatic injury. J Neurosci 22:644-653.
23. Giaume C, Fromaget C, el Aoumari A, Cordier J, Glowinski J, Gros D (1991) Gap junctions in cultured astrocytes: single-channel currents and characterization of channel-forming protein. Neuron 6:133-143.
24. Gutnick MJ, Connors BW, Ransom BR (1981) Dye-coupling between glial cells in the guinea pig neocortical slice. Brain Res 213:486-492.
25. Harks EG, de Roos AD, Peters PH, de Haan LH, Brouwer A, Ypey DL, van Zoelen EJ, Theuvenet AP (2001) Fenamates: a novel class of reversible gap junction blockers. J Pharmacol Exp Ther 298:1033-1041.
26. Harris AL (2001) Emerging issues of connexin channels: biophysics fills the gap. Q Rev Biophys 34:325-472.
27. Hille B (1992) Modifiers of gating. In: Ionic channels of excitable membranes, Ed 2, pp 445-471. Sunderland, MA: Sinauer.
28. Hofer A, Dermietzel R (1998) Visualization and functional blocking of gap junction hemichannels (connexons) with antibodies against external loop domains in astrocytes. Glia 24:141-154.
29. Imanaga I, Kameyama M, Irisawa H (1987) Cell-to-cell diffusion of fluorescent dyes in paired ventricular cells. Am J Physiol 252:H223-232.
30. Jeremic A, Jeftinija K, Stevanovic J, Glavaski A, Jeftinija S (2001) ATP stimulates calcium-dependent glutamate release from cultured astrocytes. J Neurochem 77:664-675.
31. John SA, Kondo R, Wang SY, Goldhaber JI, Weiss JN (1999) Connexin-43 hemichannels opened by metabolic inhibition. J Biol Chem 274:236-240.
32. Kamermans M, Fahrenfort I, Schultz K, Janssen-Bienhold U, Sjoerdsma T, Weiler R (2001) Hemichannel-mediated inhibition in the outer retina. Science 292:1178-1180.
33. Kimelberg HK, Goderie SK, Higman S, Pang S, Waniewski RA (1990) Swelling-induced release of glutamate, aspartate, and taurine from astrocyte cultures. J Neurosci 10:1583-1591.
34. + medium causes inhibition of glutamate and aspartate uptake and increases their release. J Cereb Blood Flow Metab 15:409-416.
35. Levi G, Patrizio M (1992) Astrocyte heterogeneity: endogenous amino acid levels and release evoked by non-N-methyl-D-aspartate receptor agonists and by potassium-induced swelling in type-1 and type-2 astrocytes. J Neurochem 58:1943-1952.
36. +-dependent glutamate transport. J Neurosci 19:RC16(1-9).
37. Lin JH, Weigel H, Cotrina ML, Liu S, Bueno E, Hansen AJ, Hansen TW, Goldman S, Nedergaard M (1998) Gap-junction-mediated propagation and amplification of cell injury. Nat Neurosci 1:494-500.
38. Liu TF, Li HY, Atkinson MM, Johnson RG (1995) Intracellular lucifer yellow leakage from Novikoff cells in the presence of ATP or low extracellular Ca: evidence for hemi-gap junction channels. Methods Find Exp Clin Pharmacol 17:23-28.
39. 2+. Methods Find Exp Clin Pharmacol 18:493-497.
40. Marks PW, Maxfield FR (1991) Preparation of solutions with free calcium concentration in the nanomolar range using 1,2-bis(o-aminophenoxy) ethane-N,N,N′, N′-tetraacetic acid. Anal Biochem 193:61-71.
41. Nicholls D, Attwell D (1990) The release and uptake of excitatory amino acids. Trends Pharmacol Sci 11:462-468.
42. Olney JW (1969) Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate. Science 164:719-721.
43. Ottersen OP (1989) Quantitative electron microscopic immunocytochemistry of neuroactive amino acids. Anat Embryol (Berl) 180:1-15.
44. Parpura V, Haydon PG (2000) Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. Proc Natl Acad Sci USA 97:8629-8634.
45. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369:744-747.
46. Pfahnl A, Dahl G (1999) Gating of cx46 gap junction hemichannels by calcium and voltage. Pflügers Arch 437:345-353.
47. Plotkin LI, Bellido T (2001) Bisphosphonate-induced, hemichannel-mediated, anti-apoptosis through the Src/ERK pathway: a gap junction-independent action of connexin43. Cell Commun Adhes 8:377-382.
48. Quist AP, Rhee SK, Lin H, Lal R (2000) Physiological role of gap-junctional hemichannels. Extracellular calcium-dependent isosmotic volume regulation. J Cell Biol 148:1063-1074.
49. Ransom BR (1995) Gap junctions. In: Neuroglia (Kettenmann H, Ransom BR, eds), pp 299-318. New York: Oxford UP.
50. Ransom BR, Waxman SG, Fern R (1998) Molecular pathophysiology of white matter anoxic/ischemic injury. In: Stroke: pathophysiology, diagnosis, and management, Ed 3 (Barnett HJM, Bennett JPM, Stein M, Yatsu FM, eds), pp 85-100. New York: Churchill Livingstone.
51. + concentration in astrocytes. Glia 20:299-307.
52. Rozental R, Srinivas M, Spray DC (2001) How to close a gap junction channel. Efficacies and potencies of uncoupling agents. Methods Mol Biol 154:447-476.
53. Sontheimer H, Ransom BR, Cornell-Bell AH, Black JA, Waxman SG (1991) Na(+)-current expression in rat hippocampal astrocytes in vitro: alterations during development. J Neurophysiol 65:3-19.
54. Spray DC, Harris AL, Bennett MV (1981) Gap junctional conductance is a simple and sensitive function of intracellular pH. Science 211:712-715.
55. Spray DC, Stern JH, Harris AL, Bennett MV (1982) Gap junctional conductance: comparison of sensitivities to H and Ca ions. Proc Natl Acad Sci USA 79:441-445.
56. Spray DC, White RL, de Carvalho AC, Harris AL, Bennett MV (1984) Gating of gap junction channels. Biophys J 45:219-230.
57. Stout CE, Costantin JL, Naus CC, Charles AC (2002) Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 277:10482-10488.
58. Szatkowski M, Barbour B, Attwell D (1990) Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature 348:443-446.
59. Virginio C, MacKenzie A, Rassendren FA, North RA, Surprenant A (1999) Pore dilation of neuronal P2X receptor channels. Nat Neurosci 2:315-321.
60. Wolff JR, Stuke K, Missler M, Tytko H, Schwarz P, Rohlmann A, Chao TI (1998) Autocellular coupling by gap junctions in cultured astrocytes: a new view on cellular autoregulation during process formation. Glia 24:121-140.
61. Ye ZC, Rothstein JD, Sontheimer H (1999) Compromised glutamate transport in human glioma cells: reduction-mislocalization of sodium-dependent glutamate transporters and enhanced activity of cystine-glutamate exchange. J Neurosci 19:10767-10777.
62. Ye ZC, Ransom BR, Sontheimer H (2001) (1R, 3S)-1-aminocyclopentane-1,3-dicarboxylic acid (RS-ACPD) reduces intracellular glutamate levels in astrocytes. J Neurochem 79:756-766.
63. Zerangue N, Kavanaugh MP (1996) Flux coupling in a neuronal glutamate transporter. Nature 383:634-637.