GAT-1 acts to limit a tonic GABAA current in rat CA3 pyramidal neurons at birth

European Journal of Neuroscience

Volumn 25, Issue 3, 2007, Pages 717-722

  Sipilä, Sampsa T ^a   Voipio, Juha ^a   Kaila, Kai ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Development; GABA uptake; Hippocampus; Interstitial GABA; Neuronal excitability

Indexed keywords

1 [2 (BENZHYDRYLIDENEAMINOOXY)ETHYL] 1,2,5,6 TETRAHYDRO 3 PYRIDINECARBOXYLIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID CARRIER; 4 AMINOBUTYRIC ACID TRANSPORTER 1; TETRODOTOXIN; UNCLASSIFIED DRUG; ZOLPIDEM;

4 AMINOBUTYRIC ACID UPTAKE; ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NETWORK; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

ACTION POTENTIALS; ANESTHETICS, LOCAL; ANIMALS; ANIMALS, NEWBORN; GABA ANTAGONISTS; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; HIPPOCAMPUS; NIPECOTIC ACIDS; ORGAN CULTURE TECHNIQUES; OXIMES; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; RATS; RATS, WISTAR; RECEPTORS, GABA-A; SYNAPSES; TETRODOTOXIN;

EID: 33847037479     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05342.x     Document Type: Article

References (38)

1. Bai, D., Zhu, G., Pennefather, P., Jackson, M.F., MacDonald, J.F. & Orser, B.A. (2001) Distinct functional and pharmacological properties of tonic and quantal inhibitory postsynaptic currents mediated by gamma-aminobutyric acid (A) receptors in hippocampal neurons. Mol. Pharmacol., 59, 814-824.
2. Barry, P.H. (1994) JPCalc, a software package for calculating liquid junction potential corrections in patch-clamp, intracellular, epithelial and bilayer measurements and for correcting junction potential measurements. J. Neurosci. Meth., 51, 107-116.
3. Ben-Ari, Y. (2001) Developing networks play a similar melody. Trends Neurosci., 24, 353-360.
4. Ben-Ari, Y., Cherubini, E., Corradetti, R. & Gaiarsa, J.L. (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J. Physiol. (Lond.), 416, 303-325.
5. Brunig, I., Scotti, E., Sidler, C. & Fritschy, J.M. (2002) Intact sorting, targeting, and clustering of gamma-aminobutyric acid A receptor subtypes in hippocampal neurons in vitro. J. Comp. Neurol., 443, 43-55.
6. Cammack, J.N., Rakhilin, S.V. & Schwartz, E.A. (1994) A GABA transporter operates asymmetrically and with variable stoichiometry. Neuron, 13, 949-960.
7. Caraiscos, V.B., Elliott, E.M., You-Ten, K.E., Cheng, V.Y., Belelli, D., Newell, J.G., Jackson, M.F., Lambert, J.J., Rosahl, T.W., Wafford, K.A., MacDonald, J.F. & Orser, B.A. (2004) Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by alpha5 subunit-containing gamma-aminobutyric acid type A receptors. Proc. Natl Acad. Sci. USA, 101, 3662-3667.
8. Chiu, C.S., Jensen, K., Sokolova, I., Wang, D., Li, M., Deshpande, P., Davidson, N., Mody, I., Quick, M.W., Quake, S.R. & Lester, H.A. (2002) Number, density, and surface/cytoplasmic distribution of GABA transporters at presynaptic structures of knock-in mice carrying GABA transporter subtype 1-green fluorescent protein fusions. J. Neurosci., 22, 10251-10266.
9. Coyle, J.T. & Enna, S.J. (1976) Neurochemical aspects of the ontogenesis of GABAnergic neurons in the rat brain. Brain Res., 111, 119-133.
10. 2+- and SNARE-independent release of GABA and glutamate prior to synapse formation. Neuron, 36, 1051-1061.
11. Draguhn, A. & Heinemann, U. (1996) Different mechanisms regulate IPSC kinetics in early postnatal and juvenile hippocampal granule cells. J. Neurophysiol., 76, 3983-3993.
12. Farrant, M. & Nusser, Z. (2005) Variations on an inhibitory theme: phasic and tonic activation of GABA (A) receptors. Nat. Rev. Neurosci., 6, 215-229.
13. Frahm, C. & Draguhn, A. (2001) GAD and GABA transporter (GAT-1) mRNA expression in the developing rat hippocampus. Dev. Brain Res., 132, 1-13.
14. Frahm, C., Engel, D. & Draguhn, A. (2001) Efficacy of background GABA uptake in rat hippocampal slices. Neuroreport, 12, 1593-1596.
15. Gordon-Weeks, P.R., Lockerbie, R.O. & Pearce, B.R. (1984) Uptake and release of [3H]GABA by growth cones isolated from neonatal rat brain. Neurosci. Lett., 52, 205-210.
16. Guastella, J., Nelson, N., Nelson, H., Czyzyk, L., Keynan, S., Miedel, M.C., Davidson, N., Lester, H.A. & Kanner, B.I. (1990) Cloning and expression of a rat brain GABA transporter. Science, 249, 1303-1306.
17. Kaila, K., Voipio, J., Paalasmaa, P., Pasternack, M. & Deisz, R.A. (1993) The role of bicarbonate in GABAA receptor-mediated IPSPs of rat neocortical neurones. J. Physiol. (Lond.), 464, 273-289.
18. A receptors. Prog. Neurobiol., 67, 113-159.
19. Laurie, D.J., Wisden, W. & Seeburg, P.H. (1992) The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J. Neurosci., 12, 4151-4172.
20. Minelli, A., Brecha, N.C., Karschin, C., DeBiasi, S. & Conti, F. (1995) GAT-1, a high-affinity GABA plasma membrane transporter, is localized to neurons and astroglia in the cerebral cortex. J. Neurosci., 15, 7734-7746.
21. Owens, D.F. & Kriegstein, A.R. (2002) Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci., 3, 715-727.
22. A receptor-mediated signaling during early neocortical development. J. Neurophysiol., 82, 570-583.
23. Richerson, G.B. & Wu, Y. (2003) Dynamic equilibrium of neurotransmitter transporters: not just for reuptake anymore. J. Neurophysiol., 90, 1363-1374.
24. - cotransporter KCC2 and carbonic anhydrase CAVII. J. Physiol. (Lond.), 562, 27-36.
25. Safiulina, V.F., Fattorini, G., Conti, F. & Cherubini, E. (2006) GABAergic signaling at mossy fiber synapses in neonatal rat hippocampus. J. Neurosci., 26, 597-608.
26. Semyanov, A., Walker, M.C. & Kullmann, D.M. (2003) GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat. Neurosci., 6, 484-490.
27. Sipilä, S.T., Huttu, K., Soltesz, I., Voipio, J. & Kaila, K. (2005) Depolarizing GABA acts on intrinsically bursting pyramidal neurons to drive giant depolarizing potentials in the immature hippocampus. J. Neurosci., 25, 5280-5289.
28. Sipilä, S., Huttu, K., Voipio, J. & Kaila, K. (2004) GABA uptake via GABA transporter-1 modulates GABAergic transmission in the immature hippocampus. J. Neurosci., 24, 5877-5880.
29. + current. Eur. J. Neurosci., 23, 2330-2338.
30. Sipilä, S.T., Schuchmann, S., Voipio, J., Yamada, J. & Kaila, K. (2006a) The cation-chloride cotransporter NKCC1 promotes sharp waves in the neonatal rat hippocampus. J. Physiol. (Lond.), 573, 765-773.
31. Stell, B.M., Brickley, S.G., Tang, C.Y., Farrant, M. & Mody, I. (2003) Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by delta subunit-containing GABAA receptors. Proc. Natl Acad. Sci. USA, 100, 14439-14444.
32. Stell, B.M. & Mody, I. (2002) Receptors with different affinities mediate phasic and tonic GABAA conductances in hippocampal neurons. J. Neurosci., 22, 223RC.
33. Stuart, G.J., Dodt, H.U. & Sakmann, B. (1993) Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pflugers Arch., 423, 511-518.
34. Tyzio, R., Ivanov, A., Bernard, C., Holmes, G.L., Ben-Ari, Y. & Khazipov, R. (2003) Membrane potential of CA3 hippocampal pyramidal cells during postnatal development. J. Neurophysiol., 90, 2964-2972.
35. Tyzio, R., Represa, A., Jorquera, I., Ben-Ari, Y., Gozlan, H. & Aniksztejn, L. (1999) The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite. J. Neurosci., 19, 10372-10382.
36. - channels are randomly activated by continuous GABA secretion in cultured embryonic rat hippocampal neurons. Neurosci. Lett., 155, 199-203.
37. Walker, C.R. & Peacock, J.H. (1981) Development of GABAergic function of dissociated hippocampal cultures from fetal mice. Brain Res., 254, 541-555.
38. Yan, X.X., Cariaga, W.A. & Ribak, C.E. (1997) Immunoreactivity for GABA plasma membrane transporter, GAT-1, in the developing rat cerebral cortex: transient presence in the somata of neocortical and hippocampal neurons. Brain Res. Dev. Brain Res., 99, 1-19.