The transmembrane sodium gradient influences ambient GABA concentration by altering the equilibrium of GABA transporters

Journal of Neurophysiology

Volumn 96, Issue 5, 2006, Pages 2425-2436

  Wu, Yuanming ^a   Wang, Wengang ^a   Richerson, George B ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (4,4 DIPHENYL 3 BUTENYL)NIPECOTIC ACID; 3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; BICUCULLINE; CALCIUM ION; CARRIER PROTEIN; PROTEIN GABA TRANSPORTER; PROTEIN GAT1; PROTEIN GAT3; RINGER SOLUTION; SODIUM CHANNEL; SODIUM ION; TETRODOTOXIN; UNCLASSIFIED DRUG; VERATRIDINE;

4 AMINOBUTYRIC ACID RELEASE; AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CYTOSOL; DRUG INHIBITION; EVOKED RESPONSE; EXTRACELLULAR SPACE; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIAL; NERVE CELL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; SODIUM CURRENT; TISSUE CULTURE;

ANIMALS; ANIMALS, NEWBORN; CALCIUM CHANNEL BLOCKERS; CALCIUM SIGNALING; CELLS, CULTURED; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIALS; EXTRACELLULAR SPACE; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; NEUROGLIA; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SODIUM; SODIUM CHANNELS; SYNAPSES; VERATRIDINE;

EID: 33751206507     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00545.2006     Document Type: Article

References (50)

1. A receptors. J Physiol 497: 753-759, 1996.
2. A receptors suggest differential targeting of receptor subtypes. J Neurosci 19: 2960-2973, 1999.
3. Brickley SG, Revilla V, Cull-Candy SG, Wisden W, and Farrant M. Adaptive regulation of neuronal excitability by a voltage- independent potassium conductance. Nature 409: 88-92, 2001.
4. Cavelier P, Hamann M, Rossi D, Mobbs P, and Attwell D. Tonic excitation and inhibition of neurons: ambient transmitter sources and computational consequences. Prog Biophys Mol Biol 87: 3-16, 2005.
5. Cherubini E, Gaiarsa JL, and Ben-Ari Y. GABA: an excitatory transmitter in early postnatal life. Trends Neurosci 14: 515-519, 1991.
6. Chiu CS, Brickley S, Jensen K, Southwell A, Mckinney S, Cull-Candy S, Mody I, and Lester HA. GABA transporter deficiency causes tremor, ataxia, nervousness, and increased GABA-induced tonic conductance in cerebellum. J Neurosci 25: 3234-3245, 2005.
7. Conti F, Minelli A, and Melone M. GABA transporters in the mammalian cerebral cortex: localization, development and pathological implications. Brain Res Brain Res Rev 45: 196-212, 2004.
8. Frahm C, Engel D, and Draguhn A. Efficacy of background GABA uptake in rat hippocampal slices. Neuroreport 12: 1593-1596, 2001.
9. Gaspary HL, Wang W, and Richerson GB. Carrier-mediated GABA release activates GABA receptors on hippocampal neurons. J Neurophysiol 80: 270-281, 1998.
10. Hamann M, Rossi DJ, and Attwell D. Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 33: 625-633, 2002.
11. Hell JW, Edelmann L, Hartinger J, and Jahn R. Functional reconstitution of the γ-aminobutyric acid transporter from synaptic vesicles using artificial ion gradients. Biochemistry 30: 11795-11800, 1991.
12. Isaacson JS, Solis JM, and Nicoll RA. Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 10: 165-175, 1993.
13. B receptors in the hippocampus. J Neurophysiol 90: 2690-2701, 2003.
14. A conductances in rat neocortex. J Neurophysiol 94: 2073-2085, 2005.
15. Kimelberg HK, Goderie SK, Higman S, Pang S, and Waniewski RA. Swelling-induced release of glutamate, aspartate, and taurine from astrocyte cultures. J Neurosci 10: 1583-1591, 1990.
16. Kinney GA. GAT-3 transporters regulate inhibition in the neocortex. J Neurophysiol 94: 4533-4537, 2005.
17. Kinney GA and Spain WJ. Synaptically evoked GABA transporter currents in neocortical glia. J Neurophysiol 88: 2899-2908, 2002.
18. Kirmse K and Kirischuk S. Ambient GABA constrains the strength of GABAergic synapses at Cajal-Retzius cells in the developing visual cortex. J Neurosci 26: 4216-4227, 2006.
19. Lerma J, Herranz AS, Herreras O, Abraira V, and Martin dR. 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, 1986.
20. Llano I, Gonzalez J, Caputo C, Lai FA, Blayney LM, Tan YP, and Marty A. Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients. Nat Neurosci 3: 1256-1265, 2000.
21. Minelli A, Brecha NC, Karschin C, DeBiasi S, and Conti F. GAT-1, a high-affinity GABA plasma membrane transporter, is localized to neurons and astroglia in the cerebral cortex. J Neurosci 15: 7734-7746, 1995.
22. A receptors responsible for tonic and phasic conductances. Neurochem Res 26: 907-913, 2001.
23. Nusser Z and Mody I. Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J Neurophysiol 87: 2624-2628, 2002.
24. Onizuka S, Kasaba T, Hamakawa T, Ibusuki S, and Takasaki M. Lidocaine increases intracellular sodium concentration through voltage-dependent sodium channels in an identified lymnaea neuron. Anesthesiology 101: 110-120, 2004.
25. Overstreet LS and Westbrook GL. Paradoxical reduction of synaptic inhibition by vigabatrin. J Neurophysiol 86: 596-603, 2001.
26. Phillis JW, Song D, and O'Regan MH. Effects of hyperosmolarity and ion substitutions on amino acid efflux from the ischemic rat cerebral cortex. Brain Res 828: 1-11, 1999.
27. Rae J, Cooper K, Gates P, and Watsky M. Low access resistance perforated patch recordings using amphotericin B. J Neurosci Methods 37: 15-26, 1991.
28. Ribak CE, Tong WM, and Brecha NC. GABA plasma membrane transporters, GAT-1 and GAT-3, display different distributions in the rat hippocampus. J Comp Neurol 367: 595-606, 1996.
29. Richerson GB and Wu Y. The dynamic equilibrium of neurotransmitter transporters: not just for reuptake anymore. J Neurophysiol 90: 1363-1374, 2003.
30. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397: 251-255, 1999.
31. Rose CR and Ransom BR. Regulation of intracellular sodium in cultured rat hippocampal neurones. J Physiol 499: 573-587, 1997.
32. A receptors and glomerular geometry. Neuron 20: 783-795, 1998.
33. Rossi DJ, Hamann M, and Attwell D. Multiple modes of GABAergic inhibition of rat cerebellar granule cells. J Physiol 548: 97-110, 2003.
34. Semyanov A, Walker MC, and Kullmann DM. GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat Neurosci 6: 484-490, 2003.
35. A receptors: modulating gain and maintaining the tone. Trends Neurosci 27: 262-269, 2004.
36. 2+-free solution. Biophys J 84: 2099-2111, 2003.
37. Soltesz I and Nusser Z. Neurobiology - background inhibition to the fore. Nature 409: 24-27, 2001.
38. +-current expression in rat hippocampal astrocytes in vitro: alterations during development. J Neurophysiol 65: 3-19, 1991.
39. A receptors. Proc Natl Acad Sci USA 100: 14439-14444, 2003.
40. A conductances in hippocampal neurons. J Neurosci 22: RC223, 2002.
41. +, veratridine or electrical stimulation from rat cortical slices. J Neurochem 32: 1565-1573, 1979.
42. Tossman U, Jonsson G, and Ungerstedt U. Regional distribution and extracellular levels of amino acids in rat central nervous system. Acta Physiol Scand 127: 533-545, 1986.
43. Vautrin J, Maric D, Sukhareva M, Schaffner AE, and Barker JL. Surface-accessible GABA supports tonic and quantal synaptic transmission. Synapse 37: 38-55, 2000.
44. Vitellaro-Zuccarello L, Calvaresi N, and De BS. Expression of GABA transporters, GAT-1 and GAT-3, in the cerebral cortex and thalamus of the rat during postnatal development. Cell Tissue Res 313: 245-257, 2003.
45. A receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur J Neurosci 9: 533-548, 1997.
46. --dependent mechanism. Glia 37: 8-18, 2002.
47. Wu Y, Wang W, and Richerson GB. GABA transaminase inhibition induces spontaneous and enhances depolarization-evoked GABA efflux via reversal of the GABA transporter. J Neurosci 21: 2630-2639, 2001.
48. Wu Y, Wang W, and Richerson GB. Tonic inhibition in hippocampal cultures is due to GABA release via two distinct nonvesicular mechanisms. Soc Neurosci Abstr 31, 2005.
49. Wu Y, Wang W, and Richerson GB. Vigabatrin induces tonic inhibition via GABA transporter reversal without increasing vesicular GABA release. J Neurophysiol 89: 2021-2034, 2003.
50. Ye ZC, Wyeth MS, Baltan-Tekkok S, and Ransom BR. Functional hemichannels in astrocytes: A novel mechanism of glutamate release. J Neurosci 23: 3588-3596, 2003.