Two developmental switches in GABAergic signalling: The K+-Cl- cotransporter KCC2 and carbonic anhydrase CAVII

Journal of Physiology

Volumn 562, Issue 1, 2005, Pages 27-36

  Rivera, Claudio ^a   Voipio, Juha ^b   Kaila, Kai ^b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICONVULSIVE AGENT; BICARBONATE; BRAIN DERIVED NEUROTROPHIC FACTOR; CARBONATE DEHYDRATASE; CHLORIDE ION; COTRANSPORTER; ISOENZYME; POTASSIUM CHLORIDE COTRANSPORTER KCC2; POTASSIUM ION; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CARBONATE DEHYDRATASE VII; POTASSIUM CHLORIDE COTRANSPORTER 2;

ANION TRANSPORT; ARTICLE; CELL KINETICS; CHLORIDE TRANSPORT; ENZYME ACTIVATION; ENZYME INACTIVATION; EPILEPTIC DISCHARGE; GABAERGIC TRANSMISSION; HIPPOCAMPUS; HOMEOSTASIS; HYPERPOLARIZATION; LIFESPAN; NERVE CELL DIFFERENTIATION; NERVE CELL INHIBITION; NERVE CELL LESION; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NONHUMAN; PATHOPHYSIOLOGY; PERINATAL PERIOD; POSTSYNAPTIC MEMBRANE; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SPIKE WAVE; BRAIN DAMAGE; BRAIN TISSUE; CELL MATURATION; CYTOSOL; DOWN REGULATION; EPILEPSY; EPILEPTOGENESIS; EVOKED RESPONSE; GABAERGIC SYSTEM; HUMAN; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NEUROPHYSIOLOGY; POSTSYNAPTIC NEURON; PROTEIN FUNCTION; QUALITATIVE ANALYSIS; UPREGULATION;

ANIMALS; CARBONIC ANHYDRASES; GAMMA-AMINOBUTYRIC ACID; HOMEOSTASIS; HUMANS; ISOENZYMES; NEURONAL PLASTICITY; SIGNAL TRANSDUCTION; SYMPORTERS; UP-REGULATION;

EID: 13444252908     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2004.077495     Document Type: Article

References (93)

1. - co-transporter KCC2. Development 130, 1267-1280.
2. Alvarez-Leefmans FJ & Russell JM (ed.) (1990). Chloride Channels and Carriers in Nerve, Muscle and Glial Cells. Plenum Press, New York.
3. Avishai-Eliner S, Brunson KL, Sandman CA & Baram TZ (2002). Stressed-out, or in (utero)? Trends Neurosci 25, 518-524.
4. + evoked by GABA, THIP and baclofen in the guinea-pig hippocampal slice. Exp Brain Res 84, 591-598.
5. Bartho P, Payne JA, Freund TF & Acsady L (2004). Differential distribution of the KCl cotransporter KCC2 in thalamic relay and reticular nuclei. Eur J Neurosci 20, 965-975.
6. Ben-Ari Y (2001). Developing networks play a similar melody. Trends Neurosci 24, 353-360.
7. Ben-Ari Y (2002). Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3, 728-739.
8. Ben-Ari Y, Cherubini E, Corradetti R & Gaiarsa JL (1989). Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416, 303-325.
9. Binder DK, Croll SD, Gall CM & Scharfman HE (2001). BDNF and epilepsy: too much of a good thing? Trends Neurosci 24, 47-53 (review).
10. Buhl EH, Otis TS & Mody I (1996). Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model. Science 271, 369-373.
11. Clancy B, Darlington RB & Finlay BL (2001). Translating developmental time across mammalian species. Neuroscience 105 7-17.
12. Cohen I, Navarro V, Clemenceau S, Baulac M & Miles R (2002). On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298, 1418-1421.
13. Cohen I, Navarro V, Le Duigou C & Miles R (2003). Mesial temporal lobe epilepsy: a pathological replay of developmental mechanisms? Biol Cell 95, 329-333 (review).
14. DeFazio RA, Keros S, Quick MW & Hablitz JJ (2000). Potassium-coupled chloride cotransport controls intracellular chloride in rat neocortical pyramidal neurons. J Neurosci 20, 8069-8076.
15. Deisz RA & Lux HD (1982). The role of intracellular chloride in hyperpolarizing post-synaptic inhibition of crayfish stretch receptor neurones. J Physiol 326, 123-138.
16. Delpire E & Mount DB (2002). Human and murine phenotypes associated with defects in cation-chloride cotransport. Annu Rev Physiol 64, 803-843 (review).
17. Earnhardt JN, Qian M, Tu C, Lakkis MM, Bergenhem NC, Laipis PJ, Tashian RE & Silverman DN (1998). The catalytic properties of murine carbonic anhydrase VII. Biochemistry 37, 10837-10845.
18. Erecinska M, Cherian S & Silver IA (2004). Energy metabolism in mammalian brain during development. Prog Neurobiol 73, 397-445.
19. Feller MB (1999). Spontaneous correlated activity in developing neural circuits. Neuron 22, 653-656 (review).
20. Freund TF & Buzsaki G (1996). Interneurons of the hippocampus. Hippocampus 6, 347-470.
21. Ganguly K, Schinder AF, Wong ST & Poo M (2001). GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105, 521-532.
22. Garaschuk O, Linn J, Eilers J & Konnerth A (2000). Large-scale oscillatory calcium waves in the immature cortex. Nat Neurosci 3, 452-459.
23. A receptor-mediated inhibition in rat substantia nigra. J Neurosci 23, 8237-8246.
24. Gulledge AT & Stuart GJ (2003). Excitatory actions of GABA in the cortex. Neuron 37, 299-309.
25. Gulyas AI, Sik A, Payne JA, Kaila K & Freund TF (2001). The KCl cotransporter, KCC2, is highly expressed in the vicinity of excitatory synapses in the rat hippocampus. Eur J Neurosci 13 2205-2217.
26. - cotransporter. J Biol Chem 274, 10661-10667.
27. Huang EJ & Reichardt LF (2001). Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24, 677-736 (review).
28. Huang EJ & Reichardt LF (2003). Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72, 609-642.
29. Hubner CA, Stein V, Hermans-Borgmeyer I, Meyer T, Ballanyi K & Jentsch TJ (2001). Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 30, 515-524.
30. - homeostasis contributes to differential GABAergic actions between developing rat visual cortex and dorsal lateral geniculate nucleus. Brain Res 984, 149-159.
31. - accumulation and depletion in cultured rat midbrain neurons. J Neurosci 19, 4695-4704.
32. A receptor channel function in the nervous system. Prog Neurobiol 42, 489-537 (review).
33. + transient. J Neuroscience 17, 7662-7672.
34. Kaila K, Pasternack M, Saarikoski J & Voipio J (1989). Influence of GABA-gated bicarbonate conductance on potential, current and intracellular chloride in crayfish muscle fibres. J Physiol 416 161-181.
35. Kaila K & Ransom B (ed.) (1998). pH and Brain Function. Wiley-Liss, New York.
36. Kaila K, Saarikoski J & Voipio J (1990). Mechanism of action of GABA on intracellular pH and on surface pH in crayfish muscle fibres. J Physiol 427, 241-260.
37. Kaila K & Voipio J (1987). Postsynaptic fall in intracellular pH induced by GABA-activated bicarbonate conductance. Nature 330 163-165.
38. A receptor-mediated IPSPs of rat neocortical neurones. J Physiol 464, 273-289.
39. - cotransport in rat central neurons. J Neurophysiol 84, 281-288.
40. Kandler K (2004). Activity-dependent organization of inhibitory circuits: lessons from the auditory system. Cur Opin Neurobiol 14, 96-104.
41. Kelsch W, Hormuzdi S, Straube E, Lewen A, Monyer H & Misgeld U (2001). Insulin-like growth factor 1 and a cytosolic tyrosine kinase activate chloride outward transport during maturation of hippocampal neurons. J Neurosci 21, 8339-8347.
42. Khazipov R, Khalilov I, Tyzio R, Morozova E, Ben-Ari Y & Holmes GL (2004). Developmental changes in GABAergic actions and seizure susceptibility in the rat hippocampus. Fur J Neurosci 19, 590-600.
43. Kovalchuk Y, Holthoff K & Konnerth A (2004). Neurotrophin action on a rapid timescale. Curr Opin Neurobiol 14,. 558-563.
44. Lahtinen H, Ludwig A, Karhunen T, Panula P, Kaila K & Rivera C (2004). Fast dendritic retraction and intrasomatic accumulation of KCC2 protein following neuronal trauma. The 3rd INMED/TINS Symposium, The Multiple Facets of GABAergic Neurotransmission, La Ciotat, France, 15-18 September, 2004.
45. Lahtinen H, Rivera C & Kaila K (2002). An excitotoxic insult leads to fast changes in the transcription of the neuronal K-Cl cotransporter, KCC2, in hippocampal slice cultures. FENS Abstr 1 A013.7
46. Lakkis MM, O'Shea KS & Tashian RE (1997). Differential expression of the carbonic anhydrase genes for CA VII (Car7) and CA-RP VIII (Car8) in mouse brain. J Histochem Cytochem 45, 657-662.
47. Leinekugel X, Khazipov R, Cannon R, Hirase H, Ben-Ari Y & Buzsaki G (2002). Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296, 2049-2052.
48. Li H, Tornberg J, Kaila K, Airaksinen MS & Rivera C (2002). Patterns of cation-chloride cotransporter expression during embryonic rodent CNS development. Eur J Neurosci 16, 2358-2370.
49. Lu J, Karadsheh M & Delpire E (1999). Developmental regulation of the neuronal-specific isoform of K-Cl cotransporter KCC2 in postnatal rat brains. J Neurobiol 39, 558-568.
50. Ludwig A, Li H, Saarma M, Kaila K & Rivera C (2003). Developmental upregulation of KCC2 in the absence of GABAergic and glutamatergic transmission. Eur J Neurosci 18, 3199-3206.
51. Luhmann HJ & Prince DA (1991). Postnatal maturation of the GABAergic system in rat neocortex. J Neurophysiol 65, 247-263.
52. Masereel B, Rolin S, Abbate F, Scozzafava A & Supuran CT (2002). Carbonic anhydrase inhibitors: anticonvulsant sulfonamides incorporating valproyl and other lipophilic moieties. J Med Chem 45, 312-320.
53. Mercado A, Mount DB & Gamba G (2004). Electroneutral cation-chloridc cotransporters in the central nervous system. Neurochem Res 29, 17-25.
54. Minichiello L, Casagranda F, Tatche RS, Stucky CL, Postigo A, Lewin GR, Davies AM & Klein R (1998). Point mutation in trkB causes loss of NT4-dependent neurons without major effects on diverse BDNF responses. Neuron 21, 335-345.
55. Misgeld U, Deisz RA, Dodt HU & Lux HD (1986). The role of chloride transport in postsynaptic inhibition of hippocampal neurons. Science 232, 1413-1415.
56. Mueller AL, Taube JS & Schwartzkroin PA (1984). Development of hyperpolarizing inhibitory postsynaptic potentials and hyperpolarizing response to gamma-aminobutyric acid in rabbit hippocampus studied in vitro. J Neurosci 4, 860-867.
57. A receptor-mediated excitation after in vivo axonal injury. J Neurosci 22, 4412-4417.
58. Owens DF & Kriegstein AR (2002). Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3, 715-727.
59. Pasternack M, Voipio J & Kaila K (1993). Intracellular carbonic anhydrase activity and its role in GABA-induced acidosis in isolated rat hippocampal pyramidal neurones. Acta Physiol Scand 148, 229-231
60. Pastorekova S, Parkkila S, Pastorek J & Supuran CT (2004). Carbonic anhydrases: current state of the art, therapeutic applications and future prospects. J Enzyme Inhib Med Chem 19, 199-229.
61. o regulation. Am J Physiol 273, C1516-C1525.
62. Payne JA, Rivera C, Voipio J & Kaila K (2003). Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 26, 199-206 (review).
63. Payne JA, Stevenson TJ & Donaldson LF (1996). Molecular characterization of a putative K-Cl cotransporter in rat brain. A neuronal-specific isoform. J Biol Chem 271, 16245-16252.
64. Penn AA & Shatz CJ (1999). Brain waves and brain wiring: the role of endogenous and sensory-driven neural activity in development. Pediatr Res 45, 447-458 (review).
65. Race JE, Makhlouf FN, Logue PJ, Wilson FH, Dunham PB & Holtzman EJ (1999). Molecular cloning and functional characterization of KCC3, a new K-Cl cotransporter. Am J Physiol 277, C1210-C1219.
66. - extrusion. J Cell Biol 159, 747-752.
67. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397, 251-255.
68. Rivera C, Voipio J, Thomas-Crusells J, Li H, Emri Z, Sipila S, Payne JA, Minichiello L, Saarma M & Kaila K (2004). Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J Neurosci 24, 4683-4691.
69. Ruusuvuori E, Li H, Huttu K, Palva JM, Smirnov S, Rivera C, Kaila K & Voipio J (2004). Carbonic anhydrase isoform VII acts as a molecular switch in the development of synchronous gamma-frequency firing of hippocampal CA1 pyramidal cells. J Neurosci 24, 2699-2707.
70. Scozzafava A, Mastrolorenzo A & Supuran CT (2004). Modulation of carbonic anhydrase activity and its applications in therapy. Expert Opin Ther Patents 14, 667-702.
71. Sernagor E, Young C & Eglen SJ (2003). Developmental modulation of retinal wave dynamics: shedding light on the GABA saga. J Neurosci 23, 7621-7629.
72. i in newborn rat cortex. Neuroreport 13, 2433-2437.
73. Smirnov S, Paalasmaa P, Uusisaari M, Voipio J & Kaila K (1999). Pharmacological isolation of the synaptic and nonsynaptic components of the GABA-mediated biphasic response in rat CA1 hippocampal pyramidal cells. J Neurosci 19, 9252-9260.
74. - transport. J Physiol 519, 693-712.
75. Stein V, Hermans-Borgmeyer I, Jentsch TJ & Hubner CA (2004). Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J Comp Neurol 468, 57-64..
76. Sun MK & Alkon DL (2002). Carbonic anhydrase gating of attention: memory therapy and enhancement. Trends Pharmacol Sci 23, 83-89.
77. A receptor-mediated currents in dorsal root ganglion neurons isolated from Na-K-2Cl cotransporter null mice. J Neurosci 20, 7531-7538.
78. Supuran CT, Scozzafava A & Casini A (2003). Carbonic anhydrase inhibitors. Med Res Rev 23, 146-189.
79. Thompson SM, Deisz RA & Prince DA (1988a). Relative contributions of passive equilibrium and active transport to the distribution of chloride in mammalian cortical neurons. J Neurophysiol 60, 105-124.
80. Thompson SM, Deisz RA & Prince DA (1988b). Outward chloride/cation co-transport in mammalian cortical neurons. Neurosci Lett 89, 49-54.
81. - in hippocampal CA3 neurons. J Neurophysiol 61, 512-523.
82. Titz S, Hans M, Kelsch W, Lewen A, Swandulla D & Misgeld U (2003). Hyperpolarizing inhibition develops without trophic support by GABA in cultured rat midbrain neurons. J Physiol 550, 719-730.
83. 2+ oscillations with KCC2 mRNA downregulation in injured facial motoneurons. J Neurophysiol 89, 1353-1362.
84. +-mediated volume transmission in the hippocampus. Progr Brain Res 125, 323-332.
85. Voipio J, Pasternack M, Rydqvist B & Kaila K (1991). Effect of gamma-aminobutyric acid (GABA) on intracellular pH in the crayfish stretch-receptor neurone. J Exp Biol 156, 349-361.
86. Wang C, Shimizu-Okabe C, Watanabe K, Okabe A, Matsuzaki H, Ogawa T, Mori N, Fukuda A & Sato K (2002). Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain. Brain Res Dev Brain Res 139, 59-66.
87. Wardle RA & Poo MM (2003). Brain-derived neurotrophic factor modulation of GABAergic synapses by postsynaptic regulation of chloride transport. J Neurosci 23, 8722-8732.
88. - cotransporter KCC2: thermodynamics and kinetics of alternate transport modes. Am J Physiol Cell Physiol 287, C919-C931.
89. Williams JR, Sharp JW, Kumari VG, Wilson M & Payne JA (1999). The neuron-specific K-Cl cotransporter, KCC2. Antibody development and initial characterization of the protein. J Biol Chem 274, 12656-12664.
90. Wyllie E (1997). The Treatment of Epilepsy: Principles and Practice. Williams & Wilkin, Baltimore.
91. - uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J Physiol 557, 829-841.
92. Zhang LI & Poo M-M (2001). Electrical activity and development of neural circuits. Nature Neurosci 4(Suppl.), 1207-1214 (review).
93. Zhang L, Spigelman I & Carlen PL (1991). Development of GABA-mediated, chloride-dependent inhibition in CA1 pyramidal neurones of immature rat hippocampal slices. J Physiol 444, 25-49.