GABA reverse transport by the neuronal cotransporter GAT1: Influence of internal chloride depletion

American Journal of Physiology - Cell Physiology

Volumn 301, Issue 5, 2011, Pages

  Bertram, Simone ^a   Cherubino, Francesca ^a,b   Bossi, Elena ^a   Castagna, Michela ^c   Peres, Antonio ^a  

^a University of Ininfria   (Italy)

^b IRCCS   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

aminobutyric acid; KCC2; Xenopus oocytes

Indexed keywords

4 AMINOBUTYRIC ACID; CHLORIDE ION; NEURONAL COTRANSPORTER GAT1; NEUROTRANSMITTER TRANSPORTER; POTASSIUM CHLORIDE COTRANSPORTER; POTASSIUM CHLORIDE COTRANSPORTER KCC2; POTASSIUM ION; SODIUM ION; UNCLASSIFIED DRUG;

AMINO ACID TRANSPORT; ANIMAL CELL; ARTICLE; CELL LEVEL; CELLULAR PARAMETERS; CHLORIDE CELL LEVEL; CHLORIDE DEPLETION; CONTROLLED STUDY; CYTOPLASM; DEPLETION; FEMALE; GAMMA AMINOBUTYRIC ACID REVERSE TRANSPORT; INWARD TRANSPORT CURRENT; NONHUMAN; OOCYTE; OUTWARD TRANSPORT CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SODIUM CELL LEVEL; XENOPUS LAEVIS;

ANIMALS; CHLORIDES; FEMALE; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GAMMA-AMINOBUTYRIC ACID; MEMBRANE POTENTIALS; NEURONS; OOCYTES; RATS; SODIUM; SYMPORTERS; XENOPUS LAEVIS;

EID: 80054909921     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00120.2011     Document Type: Article

References (47)

1. Barish ME. A transient calcium-dependent chloride current in the immature Xenopus oocyte. J Physiol 342: 309-325, 1983.
2. Ben-Ari Y. Excitatory action of GABA during development: the nature of the nurture. Nat Rev Neurosci 3: 728-739, 2002.
3. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416: 303-325, 1989.
4. Ben-Yona A, Bendahan A, Kanner BI. A glutamine residue conserved in the neurotransmitter:sodium:symporters is essential for the interaction of chloride with the GABA transporter GAT-1. J Biol Chem 286: 2826-2833, 2011.
5. Betté S, Castagna M, Bossi E, Peres A, Sacchi VF. The SLC6/NSS family members KAAT1 and CAATCH1 have a weak chloride dependence. Channels 2: 358-362, 2008.
6. Bossi E, Fabbrini MS, Ceriotti A. Exogenous protein expression in Xenopus laevis oocyte, basic procedure. In: In Vitro Transcription and Translation Protocols, edited by Grandi G. Totowa, NJ: Humana, 2007, p. 107-131.
7. Cammack JN, Rakhilin SV, Schwartz EA. A GABA transporter operates asymmetrically and with variable stoichiometry. Neuron 13: 949-960, 1994.
8. +/glucose cotransport. Biophys J 90: 3546-3554, 2006.
9. Cherubini E, Gaiarsa JL, Ben-Ari Y. GABA: an excitatory transmitter in early postnatal life. Trends Neurosci 14: 515-519, 1991.
10. Christoffersen GRJ, Skibsted LH. Calcium ion activity in physiological salt solutions: influence of anions infstituted for chloride. Comp Biochem Physiol 52A: 317-322, 1975.
11. - transporters cause a decrease of GABAergic inhibition in human peritumoral epileptic cortex. Epilepsia. In press.
12. --dependent transporters. Proc Natl Acad Sci USA 104: 12761-12766, 2007.
13. - effects on the function of the GABA cotransporter rGAT1 preserve the mutual relation between transient and transport currents. Cell Mol Life Sci 60: 550-556, 2003.
14. -) cotransport function. Database reconstruction with an alternating access model. J Gen Physiol 114: 459-475, 1999.
15. Hodgkin AL, Horowicz P. The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J Physiol 148: 127-160, 1959.
16. + on pHi. J Physiol 475: 45-57, 1994.
17. Khoshbouei H, Wang H, Lechleiter JD, Javitch JA, Galli A. Amphetamine-induced dopamine efflux. A voltage-sensitive and intracellular Na-dependent mechanism. J Biol Chem 278: 12070-12077, 2003.
18. Kottra G, Frey I, Daniel H. Inhibition of intracellular dipeptide hydrolysis uncovers large outward transport currents of the peptide transporter PEPT1 in Xenopus oocytes. Pflügers Arch 457: 809-820, 2009.
19. Kusano K, Miledi R, Stinnakre J. Cholinergic and catecholaminergic receptors in the Xenopus oocyte membrane. J Physiol 328: 143-170, 1982.
20. +-coupled cotransporters GAT1 and SGLT1. J Biol Chem 275: 37414-37422, 2000.
21. LoTurco J, Owen D, Heath M, Davis M, Kriegstein A. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15: 1287-1298, 1995.
22. -) cotransport function. Kinetic studies in giant Xenopus oocyte membrane patches. J Gen Physiol 114: 445-457, 1999.
23. -) cotransport function. Steady state studies in giant Xenopus oocyte membrane patches. J Gen Physiol 114: 429-444, 1999.
24. Mager S, Kleinberger-Doron N, Keshet GI, Davidson N, Kanner BI, Lester HA. Ion binding and permeation at the GABA transporter GAT1. J Neurosci 16: 5405-5414, 1996.
25. Mari SA, Soragna A, Castagna M, Santacroce M, Perego C, Bossi E, Peres A, Sacchi VF. Role of the conserved glutamine 291 in the rat gamma-aminobutyric acid transporter rGAT-1. Cell Mol Life Sci 63: 100-111, 2006.
26. Nelson N, Sacher A, Nelson H. The significance of molecular slips in transport systems. Nat Rev Mol Cell Biol 3: 876-881, 2002.
27. Pacheco-Alvarez D, San-Cristobal P, Meade P, Moreno E, Vazquez N, Muñoz E, Diaz A, Juárez ME, Giménez I, Gamba G. The Na:Cl Cotransporter is activated and phosphorylated at the amino-terminal domain upon intracellular chloride depletion. J Biol Chem 281: 28755-28763, 2006.
28. Ponce-Coira J, San-Cristobal P, Kahle KT, Vazquez N, Pacheco-Alvarez D, de los Heros P, Juárez P, Muñoz E, Michel G, Bobadilla NA, Gimenez I, Lifton RP, Hebert SC, Gamba G. Regulation of NKCC2 by a chloride-sensing mechanism involving the WNK3 and SPAK kinases. Proc Natl Acad Sci USA 105: 8458-8463, 2008.
29. Quick MW. Infstrates regulate gamma-aminobutyric acid transporters in a syntaxin 1A-dependent manner. Proc Natl Acad Sci USA 99: 5686-5691, 2002.
30. Quick MW, Corey JL, Davidson N, Lester HA. Second messengers, trafficking-related proteins, and amino acid residues that contribute to the functional regulation of the rat brain GABA transporter GAT1. J Neurosci 17: 2967-2979, 1997.
31. Richerson GB, Wu Y. Dynamic equilibrium of neurotransmitter transporters: not just for reuptake anymore. J Neurophys 90: 1363-1374, 2003.
32. Richerson GB, Wu Y. Role of the GABA transporter in epilepsy. In: Recent Advances in Epilepsy Research, edited by Binder DK and Scharfman HE. New York: Kluwer Academic/Plenum, 2004, p. 76-91.
33. - cotransporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397: 251-255, 1999.
34. Rossi DJ, Oshima T, Attwell D. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403: 316-321, 2000.
35. Sehy JV, Ackerman JJH, Neil JJ. Apparent diffusion of water, ions and small molecules in the Xenopus oocyte is consistent with Brownian displacement. Magn Reson Med 48: 42-51, 2002.
36. Seidel S, Singer EA, Just H, Farhan H, Scholze P, Kudlacek O, Holy M, Koppatz K, Krivanek P, Freissmuth M, Sitte HH. Amphetamines take two to tango: an oligomer-based counter-transport model of neurotransmitter transport explores the amphetamine action. Mol Pharmacol 67: 140-151, 2005.
37. Soragna A, Bossi E, Giovannardi S, Pisani R, Peres A. Relations between infstrate affinities and charge equilibration rates in the GABA cotransporter rGAT1. J Physiol 562: 333-345, 2005.
38. Wagner S, Castel M, Gainer H, Yarom Y. GABA in the mammalian suprachiasmatic nucleus and its role in diurnal rhytmicity. Nature 387: 554-555, 1997.
39. Wagner S, Sagiv N, Yarom Y. GABA-induced current and circadian regulation of chloride in neurones of the rat suprachiasmatic nucleus. J Physiol 537: 853-869, 2001.
40. Woo NS, Lu J, England R, McClellan R, Dufour S, Mount DB, Deutch AY, Lovinger DM, Delpire E. Hyperexcitability and epilepsy associated with disruption of the mouse neuronal specific K-Cl cotransporter gene. Hippocampus 12: 258-268, 2002.
41. Wu Y, Wang W, Díez-Sampedro A, Richerson GB. Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1. Neuron 56: 851-865, 2007.
42. Wu Y, Wang W, Richerson GB. The transmembrane sodium gradient influences ambient GABA concentration by altering the equilibrium of GABA transporters. J Neurophysiol 96: 2425-2436, 2006.
43. --dependent neurotransmitter transporters. Nature 437: 215-223, 2005.
44. 2+ from intracellular stores in response to ionomycin in oocytes of the frog Xenopus laevis. J Physiol 458: 307-318, 1992.
45. 2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 6: 333-344, 1991.
46. +-coupled sugar transporters (SGLT1). J Physiol 542: 71-87, 2002.
47. Zomot E, Bendahan A, Quick M, Zhao Y, Javitch JA, Kanner BI. Mechanism of chloride interaction with neurotransmitter:sodium symporters. Nature 449: 726-731, 2007.