Modulation of GABAergic transmission by activity via postsynaptic Ca 2+-dependent regulation of KCC2 function

Neuron

Volumn 48, Issue 5, 2005, Pages 773-786

  Fiumelli, Hubert ^a   Cancedda, Laura ^a   Poo, Mu Ming ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; CALCIUM ION; COTRANSPORTER; POTASSIUM CHLORINE COTRANSPORTER KCC2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CALCIUM TRANSPORT; CELL MATURATION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYO; GABAERGIC TRANSMISSION; GENE OVEREXPRESSION; HIPPOCAMPUS; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT;

ACTION POTENTIALS; ANIMALS; CALCIUM; CELL AGING; CELLS, CULTURED; CHLORIDE CHANNELS; ELECTRIC CONDUCTIVITY; EMBRYO; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; INTRACELLULAR MEMBRANES; NEURONS; OSMOLAR CONCENTRATION; PROTEIN KINASE C; RATS; SYMPORTERS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 28744450567     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2005.10.025     Document Type: Article

References (38)

1. N.C. Adragna, M.D. Fulvio, and P.K. Lauf Regulation of K-Cl cotransport: from function to genes J. Membr. Biol. 201 2004 109 137
2. C.D. Aizenman, P.B. Manis, and D.J. Linden Polarity of long-term synaptic gain change is related to postsynaptic spike firing at a cerebellar inhibitory synapse Neuron 21 1998 827 835
3. Y. Ben-Ari Excitatory actions of GABA during development: the nature of the nurture Nat. Rev. Neurosci. 3 2002 728 739
4. Y. Ben-Ari, K. Krnjevic, R.J. Reiffenstein, and W. Reinhardt Inhibitory conductance changes and action of gamma-aminobutyrate in rat hippocampus Neuroscience 6 1981 2445 2463
5. I. Chudotvorova, A. Ivanov, S. Rama, C.A. Hubner, C. Pellegrino, Y. Ben-Ari, and I. Medina Early expression of KCC2 in rat hippocampal cultures augments expression of functional GABA synapses J. Physiol. 566 2005 671 679
6. I. Cohen, V. Navarro, S. Clemenceau, M. Baulac, and R. Miles On the origin of interictal activity in human temporal lobe epilepsy in vitro Science 298 2002 1418 1421
7. J.L. Gaiarsa, O. Caillard, and Y. Ben-Ari Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance Trends Neurosci. 25 2002 564 570
8. K. Ganguly, A.F. Schinder, S.T. Wong, and M. Poo GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition Cell 105 2001 521 532
9. D.W. Hochman, S.C. Baraban, J.W. Owens, and P.A. Schwartzkroin Dissociation of synchronization and excitability in furosemide blockade of epileptiform activity Science 270 1995 99 102
10. K. Hong, M. Nishiyama, J. Henley, M. Tessier-Lavigne, and M. Poo Calcium signalling in the guidance of nerve growth by netrin-1 Nature 403 2000 93 98
11. M. Kano, U. Rexhausen, J. Dreessen, and A. Konnerth Synaptic excitation produces a long-lasting rebound potentiation of inhibitory synaptic signals in cerebellar Purkinje cells Nature 356 1992 601 604
12. W. Kelsch, S. Hormuzdi, E. Straube, A. Lewen, H. Monyer, and U. Misgeld Insulin-like growth factor 1 and a cytosolic tyrosine kinase activate chloride outward transport during maturation of hippocampal neurons J. Neurosci. 21 2001 8339 8347
13. A. Kyrozis, and D.B. Reichling Perforated-patch recording with gramicidin avoids artifactual changes in intracellular chloride concentration J. Neurosci. Methods 57 1995 27 35
14. H. Lee, C.X. Chen, Y.J. Liu, E. Aizenman, and K. Kandler KCC2 expression in immature rat cortical neurons is sufficient to switch the polarity of GABA responses Eur. J. Neurosci. 21 2005 2593 2599
15. X. Leinekugel, I. Medina, I. Khalilov, Y. Ben-Ari, and R. Khazipov Ca2+ oscillations mediated by the synergistic excitatory actions of GABA(A) and NMDA receptors in the neonatal hippocampus Neuron 18 1997 243 255
16. D.S. Ling, and L.S. Benardo Activity-dependent depression of monosynaptic fast IPSCs in hippocampus: contributions from reductions in chloride driving force and conductance Brain Res. 670 1995 142 146
17. P. Lipton Ischemic cell death in brain neurons Physiol. Rev. 79 1999 1431 1568
18. M. McCarren, and B.E. Alger Use-dependent depression of IPSPs in rat hippocampal pyramidal cells in vitro J. Neurophysiol. 53 1985 557 571
19. H.A. McLean, O. Caillard, Y. Ben-Ari, and J.L. Gaiarsa Bidirectional plasticity expressed by GABAergic synapses in the neonatal rat hippocampus J. Physiol. 496 1996 471 477
20. J. Nabekura, T. Ueno, A. Okabe, A. Furuta, T. Iwaki, C. Shimizu-Okabe, A. Fukuda, and N. Akaike Reduction of KCC2 expression and GABAA receptor-mediated excitation after in vivo axonal injury J. Neurosci. 22 2002 4412 4417
21. D.F. Owens, L.H. Boyce, M.B. Davis, and A.R. Kriegstein Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging J. Neurosci. 16 1996 6414 6423
22. J.A. Payne, T.J. Stevenson, and L.F. Donaldson Molecular characterization of a putative K-Cl cotransporter in rat brain. A neuronal-specific isoform J. Biol. Chem. 271 1996 16245 16252
23. J.A. Payne, C. Rivera, J. Voipio, and K. Kaila Cation-chloride co-transporters in neuronal communication, development and trauma Trends Neurosci. 26 2003 199 206
24. M.D. Plotkin, E.Y. Snyder, S.C. Hebert, and E. Delpire Expression of the Na-K-2Cl cotransporter is developmentally regulated in postnatal rat brains: a possible mechanism underlying GABA's excitatory role in immature brain J. Neurobiol. 33 1997 781 795
25. C. Rivera, J. Voipio, J.A. Payne, E. Ruusuvuori, H. Lahtinen, K. Lamsa, U. Pirvola, M. Saarma, and K. Kaila The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation Nature 397 1999 251 255
26. C. Rivera, H. Li, J. Thomas-Crusells, H. Lahtinen, T. Viitanen, A. Nanobashvili, Z. Kokaia, M.S. Airaksinen, J. Voipio, K. Kaila, and M. Saarma BDNF-induced TrkB activation down-regulates the K+-Cl- cotransporter KCC2 and impairs neuronal Cl- extrusion J. Cell Biol. 159 2002 747 752
27. C. Rivera, J. Voipio, J. Thomas-Crusells, H. Li, Z. Emri, S. Sipila, J.A. Payne, L. Minichiello, M. Saarma, and K. Kaila Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2 J. Neurosci. 24 2004 4683 4691
28. A. Stelzer, G. Simon, G. Kovacs, and R. Rai Synaptic disinhibition during maintenance of long-term potentiation in the CA1 hippocampal subfield Proc. Natl. Acad. Sci. USA 91 1994 3058 3062
29. K. Strange, T.D. Singer, R. Morrison, and E. Delpire Dependence of KCC2 K-Cl cotransporter activity on a conserved carboxy terminus tyrosine residue Am. J. Physiol. Cell Physiol. 279 2000 C860 C867
30. M. Taketo, H. Matsuda, and T. Yoshioka Calcium-independent inhibition of GABA(A) current by caffeine in hippocampal slices Brain Res. 1016 2004 229 239
31. S.M. Thompson, and B.H. Gahwiler Activity-dependent disinhibition. II. Effects of extracellular potassium, furosemide, and membrane potential on ECl- in hippocampal CA3 neurons J. Neurophysiol. 61 1989 512 523
32. H. Toyoda, K. Ohno, J. Yamada, M. Ikeda, A. Okabe, K. Sato, K. Hashimoto, and A. Fukuda Induction of NMDA and GABAA receptor-mediated Ca2+ oscillations with KCC2 mRNA downregulation in injured facial motoneurons J. Neurophysiol. 89 2003 1353 1362
33. A.N. Van Den Pol, K. Obrietan, and G. Chen Excitatory actions of GABA after neuronal trauma J. Neurosci. 16 1996 4283 4292
34. J. Wan, and M. Poo Activity-induced potentiation of developing neuromuscular synapses Science 285 1999 1725 1728
35. J. Wang, S. Liu, U. Haditsch, W. Tu, K. Cochrane, G. Ahmadian, L. Tran, J. Paw, Y. Wang, and I. Mansuy Interaction of calcineurin and type-A GABA receptor gamma 2 subunits produces long-term depression at CA1 inhibitory synapses J. Neurosci. 23 2003 826 836
36. N.S. Woo, J. Lu, R. England, R. McClellan, S. Dufour, D.B. Mount, A.Y. Deutch, D.M. Lovinger, and E. Delpire Hyperexcitability and epilepsy associated with disruption of the mouse neuronal-specific K-Cl cotransporter gene Hippocampus 12 2002 258 268
37. M.A. Woodin, K. Ganguly, and M.M. Poo Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl- transporter activity Neuron 39 2003 807 820
38. R. Zucchi, and S. Ronca-Testoni The sarcoplasmic reticulum Ca2+ channel/ryanodine receptor: modulation by endogenous effectors, drugs and disease states Pharmacol. Rev. 49 1997 1 51