Taurine release by astrocytes modulates osmosensitive glycine receptor tone and excitability in the adult supraoptic nucleus

Journal of Neuroscience

Volumn 32, Issue 36, 2012, Pages 12518-12527

  Choe, Katrina Y ^a   Olson, James E ^b   Bourque, Charles W ^a  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b WRIGHT STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANION CHANNEL; GLYCINE RECEPTOR; TAURINE; UNCLASSIFIED DRUG; VOLTAGE REGULATED ANION CHANNEL;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CHLORIDE CONDUCTANCE; CONTROLLED STUDY; DEPOLARIZATION; ELECTROPHORESIS; ELECTROPHYSIOLOGY; GLIA CELL; GLIOTRANSMISSION; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE EXCITABILITY; NEUROTRANSMISSION; NONHUMAN; OSMOLALITY; PRIORITY JOURNAL; RAT; SPIKE; SUPRAOPTIC NUCLEUS; WESTERN BLOTTING;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELLS, CULTURED; MALE; MICE; ORGAN CULTURE TECHNIQUES; OSMOLAR CONCENTRATION; RATS; RATS, LONG-EVANS; RECEPTORS, GLYCINE; SUPRAOPTIC NUCLEUS; TAURINE;

EID: 84865725046     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1380-12.2012     Document Type: Article

References (59)

1. Adler R (1983) Taurine uptake by chick embryo retinal neurons and glial cells in purified culture. J Neurosci Res 10:369-379.
2. Becquet D, Girardet C, Guillaumond F, François-Bellan AM, Bosler O (2008) Ultrastructural plasticity in the rat suprachiasmatic nucleus. Possible involvement in clock entrainment. Glia 56:294-305.
3. Benesova J, Hock M, Butenko O, Prajerova I, Anderova M, Chvatal A (2009) Quantification of astrocyte volume changes during ischemia in situ reveals two populations of astrocytes in the cortex of GFAP/EGFP mice. J Neurosci Res 87:96-111.
4. Bourque CW (2008) Central mechanisms of osmosensation and systemic osmoregulation. Nat Rev Neurosci 9:519-531.
5. Chattipakorn SC, McMahon LL (2003) Strychnine-sensitive glycine receptors depress hyperexcitability in rat dentate gyrus. J Neurophysiol 89:1339-1342.
6. Chvátal A, Anderová M, Hock M, Prajerová I, Neprasová H, Chvátal V, Kirchhoff F, Syková E (2007) Three-dimensional confocal morphometry reveals structural changes in astrocyte morphology in situ. J Neurosci Res 85:260-271.
7. Decavel C, Hatton GI (1995) Taurine immunoreactivity in the rat supraoptic nucleus: prominent localization in glial cells. J Comp Neurol 354:13-26.
8. Decher N, Lang HJ, Nilius B, Bruggemann A, Busch AE, Steinmeyer K (2001) DCPIB is a novel selective blocker of I(Cl,swell) and prevents swellinginduced shortening of guinea-pig atrial action potential duration. Br J Pharmacol 134:1467-1479.
9. Deleuze C, Duvoid A, Hussy N (1998) Properties and glial origin of osmotic-dependent release of taurine from the rat supraoptic nucleus. J Physiol 507:463-471.
10. Deleuze C, Alonso G, Lefevre IA, Duvoid-Guillou A, Hussy N (2005) Extrasynaptic localization of glycine receptors in the rat supraoptic nucleus: further evidence for their involvement in glia-to-neuron communication. Neuroscience 133:175-183.
11. Dzhala V, Valeeva G, Glykys J, Khazipov R, Staley K (2012) Traumatic alterations in GABA signaling disrupt hippocampal network activity in the developing brain. J Neurosci 32:4017-4031.
12. Flint AC, Liu X, Kriegstein AR (1998) Nonsynaptic glycine receptor activation during early neocortical development. Neuron 20:43-53.
13. Ghamari-Langroudi M, Bourque CW (2001) Ionic basis of the caesium-induced depolarisation in rat supraoptic nucleus neurones. J Physiol 536:797-808.
14. Ghavanini AA, Mathers DA, Kim HS, Puil E (2006) Distinctive glycinergic currents with fast and slow kinetics in thalamus. J Neurophysiol 95:3438-3448.
15. Gutnick MJ, Heinemann U, Lux HD (1979) Stimulus induced and seizure related changes in extracellular potassium concentration in cat thalamus (VPL). Electroencephalogr Clin Neurophysiol 47:329-344.
16. Haam J, Popescu IR, Morton LA, Halmos KC, Teruyama R, Ueta Y, Tasker JG (2012) GABA is excitatory in adult vasopressinergic neuroendocrine cells. J Neurosci 32:572-582.
17. Haber M, Zhou L, Murai KK (2006) Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. J Neurosci 26:8881-8891.
18. He D, Luo X, Wei W, Xie M, Wang W, Yu Z (2012) DCPIB, a specific inhibitor of volume-regulated anion channels (VRACs), inhibits astrocyte proliferation and cell cycle progression via G1/S arrest. J Mol Neurosci 46:249-257.
19. Hirrlinger J, Hulsmann S, Kirchhoff F (2004) Astroglial processes show spontaneous motility at active synaptic terminals in situ. Eur J Neurosci 20:2235-2239.
20. Hussy N, Deleuze C, Pantaloni A, Desarménien MG, Moos F (1997) Agonist action of taurine on glycine receptors in rat supraoptic magnocellular neurones: possible role in osmoregulation. J Physiol 502:609-621.
21. Hussy N, Deleuze C, Desarménien MG, Moos FC (2000) Osmotic regulation of neuronal activity: a new role for taurine and glial cells in a hypothalamic neuroendocrine structure. Prog Neurobiol 62:113-134.
22. Huxtable RJ (1989) Taurine in the central nervous system and the mammalian actions of taurine. Prog Neurobiol 32:471-533.
23. Huxtable RJ, Laird HE 2nd, Lippincott SE (1979) The transport of taurine in the heart and the rapid depletion of tissue taurine content by guanidinoethyl sulfonate. J Pharmacol Exp Ther 211:465-471.
24. Jones TA, Hawrylak N, Greenough WT (1996) Rapid laminar-dependent changes in GFAP immunoreactive astrocytes in the visual cortex of rats reared in a complex environment. Psychoneuroendocrinology 21:189-201.
25. Karnani MM, Venner A, Jensen LT, Fugger L, Burdakov D (2011) Direct and indirect control of orexin/hypocretin neurons by glycine receptors. J Physiol 589:639-651.
26. Kim JS, Kim WB, Kim YB, Lee Y, Kim YS, Shen FY, Lee SW, Park D, Choi HJ, Hur J, Park JJ, Han HC, Colwell CS, Cho YW, Kim YI (2011) Chronic hyperosmotic stress converts GABAergic inhibition into excitation in vasopressin and oxytocin neurons in the rat. J Neurosci 31:13312-13322.
27. Kuhse J, Betz H, Kirsch J (1995) The inhibitory glycine receptor: architecture, synaptic localization and molecular pathology of a postsynaptic ionchannel complex. Curr Opin Neurobiol 5:318-323.
28. Leng G, Blackburn RE, Dyball RE, Russell JA (1989) Role of anterior peri-third ventricular structures in the regulation of supraoptic neuronal activity and neurohypophysial hormone secretion in the rat. J Neuroendocrinol 1:35-46.
29. Lerma J, Herranz AS, Herreras O, Abraira V, Martíndel Rio R (1986) In vivo determination of extracellular concentration of amino acids in the rat hippocampus. A method based on brain dialysis and computerized analysis. Brain Res 384:145-155.
30. Lynch JW (2004) Molecular structure and function of the glycine receptor chloride channel. Physiol Rev 84:1051-1095.
31. Miyata S, Nakashima T, Kiyohara T (1994) Structural dynamics of neural plasticity in the supraoptic nucleus of the rat hypothalamus during dehydration and rehydration. Brain Res Bull 34:169-175.
32. Morán J, Maar TE, Pasantes-Morales H (1994) Impaired cell volume regulation in taurine deficient cultured astrocytes. Neurochem Res 19:415-420.
33. Mori M, Gähwiler BH, Gerber U (2002) Beta-alanine and taurine as endogenous agonists at glycine receptors in rat hippocampus in vitro. J Physiol 539:191-200.
34. Nilsson P, Hillered L, Pontén U, Ungerstedt U (1990) Changes in cortical extracellular levels of energy-related metabolites and amino acids following concussive brain injury in rats. J Cereb Blood Flow Metab 10:631-637.
35. Okabe A, Kilb W, Shimizu-Okabe C, Hanganu IL, Fukuda A, Luhmann HJ (2004) Homogenous glycine receptor expression in cortical plate neurons and Cajal-Retzius cells of neonatal rat cerebral cortex. Neuroscience 123:715-724.
36. Oliet SH, Bourque CW (1993a) Steady-state osmotic modulation of cationic conductance in neurons of rat supraoptic nucleus. Am J Physiol 265:R1475-R1479.
37. Oliet SH, Bourque CW (1993b) Mechanosensitive channels transduce osmosensitivity in supraoptic neurons. Nature 364:341-343.
38. Oliet SH, Piet R, Poulain DA (2001) Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292:923-926.
39. Olson JE, Li GZ (2000) Osmotic sensitivity of taurine release from hippocampal neuronal and glial cells. Adv Exp Med Biol 483:213-218.
40. Pasantes-Morales H, Schousboe A (1989) Release of taurine from astrocytes during potassium-evoked swelling. Glia 2:45-50.
41. Pasantes-Morales H, Arzate ME, Quesada O, Huxtable RJ (1987) Higher susceptibility of taurine-deficient rats to seizures induced by 4-aminopyridine. Neuropharmacology 26:1721-1725.
42. Pasantes-Morales H, Alavez S, Sánchez Olea R, Morán J (1993) Contribution of organic and inorganic osmolytes to volume regulation in rat brain cells in culture. Neurochem Res 18:445-452.
43. Pasantes-Morales H, Franco R, Torres-Marquez ME, Hernández-Fonseca K, Ortega A (2000) Amino acid osmolytes in regulatory volume decrease and isovolumetric regulation in brain cells: contribution and mechanisms. Cell Physiol Biochem 10:361-370.
44. Paulsen RE, Contestabile A, Villani L, Fonnum F (1987) An in vivo model for studying function of brain tissue temporarily devoid of glial cell metabolism: the use of fluorocitrate. J Neurochem 48:1377-1385.
45. Poulain DA, Wakerley JB (1982) Electrophysiology of hypothalamic magnocellular neurones secreting oxytocin and vasopressin. Neuroscience 7:773-808.
46. Randle JC, Renaud LP (1987) Actions of gamma-aminobutyric acid on rat supraoptic nucleus neurosecretory neurones in vitro. J Physiol 387:629-647.
47. Rhodes CH, Morrell JI, Pfaff DW (1981) Immunohistochemical analysis of magnocellular elements in rat hypothalamus: distribution and numbers of cells containing neurophysin, oxytocin, and vasopressin. J Comp Neurol 198:45-64.
48. Sergeeva OA, Chepkova AN, Haas HL (2002) Guanidinoethyl sulphonate is a glycine receptor antagonist in striatum. Br J Pharmacol 137:855-860.
49. Shibanoki S, Kogure M, Sugahara M, Ishikawa K (1993) Effect of systemic administration of N-methyl-D-aspartic acid on extracellular taurine level measured by microdialysis in the hippocampal CA1 field and striatum of rats. J Neurochem 61:1698-1704.
50. Theodosis DT, Poulain DA (1984) Evidence for structural plasticity in the supraoptic nucleus of the rat hypothalamus in relation to gestation and lactation. Neuroscience 11:183-193.
51. Trudel E, Bourque CW (2010) Central clock excites vasopressin neurons by waking osmosensory afferents during late sleep. Nat Neurosci 13:467-474.
52. Tweedle CD, Hatton GI (1976) Ultrastructural comparisons of neurons of supraoptic and circularis nuclei in normal and dehydrated rats. Brain Res Bull 1:103-121.
53. Voisin DL, Bourque CW (2002) Integration of sodium and osmosensory signals in vasopressin neurons. Trends Neurosci 25:199-205.
54. Wang F, Xiao C, Ye JH (2005) Taurine activates excitatory non-synaptic glycine receptors on dopamine neurones in ventral tegmental area of young rats. J Physiol 565:503-516.
55. Whitehead KJ, Manning JP, Smith CG, Bowery NG (2001) Determination of the extracellular concentration of glycine in the rat spinal cord dorsal horn by quantitative microdialysis. Brain Res 910:192-194.
56. Zhang LH, Gong N, Fei D, Xu L, Xu TL (2008) Glycine uptake regulates hippocampal network activity via glycine receptor-mediated tonic inhibition. Neuropsychopharmacology 33:701-711.
57. Zhang Y, Zhang H, Feustel PJ, 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.
58. Zhang Z, Bourque CW (2003) Osmometry in osmosensory neurons. Nat Neurosci 6:1021-1022.
59. Zhang Z, Kindrat AN, Sharif-Naeini R, Bourque CW (2007) Actin filaments mediate mechanical gating during osmosensory transduction in rat supraoptic nucleus neurons. J Neurosci 27:4008-4013.