Carbonic Anhydrase Isoform VII Acts As A Molecular Switch in the Development of Synchronous Gamma-Frequency Firing of Hippocampal CA1 Pyramidal Cells

Journal of Neuroscience

Volumn 24, Issue 11, 2004, Pages 2699-2707

  Ruusuvuori, Eva ^a   Li, Hong ^a,b   Huttu, Kristiina ^a   Palva, J Matias ^a   Smirnov, Sergei ^a   Rivera, Claudio ^a,b   Kaila, Kai ^a   Voipio, Juha ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Carbonic anhydrase; Epilepsy; Excitatory GABA; Gamma oscillations; GDP; Hippocampus; Potassium; Synchrony

Indexed keywords

CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE VII; ISOENZYME; POTASSIUM ION; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL PH; CONTROLLED STUDY; ENZYME ACTIVITY; EPILEPTOGENESIS; EXCITATION; EXTRACELLULAR SPACE; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MICROELECTRODE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; NUCLEOTIDE SEQUENCE; OSCILLATION; POTASSIUM CELL LEVEL; PRIORITY JOURNAL; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; RAT; UPREGULATION;

ACTION POTENTIALS; AGE FACTORS; ANIMALS; BICARBONATES; BIOLOGICAL CLOCKS; CARBONIC ANHYDRASES; ELECTRIC STIMULATION; ELECTROENCEPHALOGRAPHY; EXTRACELLULAR SPACE; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; ISOENZYMES; POTASSIUM; PYRAMIDAL CELLS; RATS; RATS, WISTAR;

EID: 1642412500     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5176-03.2004     Document Type: Article

References (67)

1. Agnati LF, Tinner B, Staines WA, Vaananen K, Fuxe K (1995) On the cellular localization and distribution of carbonic anhydrase II immunoreactivity in the rat brain. Brain Res 676:10-24.
2. Alvarez-Leefmans FJ, Gamino FJ, Reuss L (1992) Cell volume changes upon sodium pump inhibition in Helix aspersa neurons. J Physiol (Lond) 458:603-619.
3. Ben-Ari Y (2001) Developing networks playa similar melody. Trends Neurosci 24:353-360.
4. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurons. J Physiol (Lond) 416:303-325.
5. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
6. Bracci E, Vreugdenhil M, Hack SP, Jefferys JG (1999) On the synchronizing mechanisms of tetanically induced hippocampal oscillations. J Neurosci 19:8104-8113.
7. A receptor-mediated depolarizing postsynaptic potentials in hippocampal CA1 pyramidal cells of the rat. Eur J Neurosci 10:2880-2886.
8. Casini A, Antel J, Abbate F, Scozzafava A, David S, Waldeck H, Schäfer S, Supuran CT (2003) Carbonic anhydrase inhibitors: SAR and X-ray crystallographic study for the interaction of sugar sulfamates/sulfamides with isozymes I, II and IV. Bioorg Med Chem Lett 13:841-845.
9. Chabot C, Bernard J, Normandin M, Ohayon M, Baudry M, Massicotte G (1996) Developmental changes in depolarization-mediated AMPA receptor modifications and potassium-induced long-term potentiation. Brain Res Dev Brain Res 93:70-75.
10. Cobb SR, Manuel NA, Morton RA, Gill CH, Collingridge GL, Davies CH (1999) Regulation of depolarizing GABA(A) receptor-mediated synaptic potentials by synaptic activation of GABA(B) autoreceptors in the rat hippocampus. Neuropharmacology 38:1723-1732.
11. Collingridge GL (1992) The mechanism of induction of NMDA receptor-dependent long-term potentiation in the hippocampus. Exp Physiol 77:771-797.
12. Dietzel I, Heinemann U, Hofmeier G, Lux HG (1980) Transient changes in the size of the extracellular space in the sensorimotor cortex of cats in relation to stimulus-induced changes in potassium concentration. Exp Brain Res 40:432-439.
13. Draguhn A, Traub RD, Schmitz D, Jefferys JG (1998) Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394:189-192.
14. Fisahn A (1999) An investigation into cortical gamma frequency oscillations in vitro. PhD thesis, University of Oxford.
15. Fisahn A, Pike FG, Buhl EH, Paulsen O (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394:186-189.
16. Ghandour MS, Langley OK, Vincendon G, Gombos G, Filippi D, Limozin N, Dalmasso D, Laurent G (1980) Immunochemical and immunohistochemical study of carbonic anhydrase II in adult rat cerebellum: a marker for oligodendrocytes. Neuroscience 5:559-571.
17. Ghandour MS, Parkkila AK, Parkkila S, Waheed A, Sly WS (2000) Mitochondrial carbonic anhydrase in the nervous system: expression in neuronal and glial cells. J Neurochem 75:2212-2220.
18. 2+ induced epileptiform activity in rat hippocampal and entorhinal cortex slices during adolescence. Brain Res Dev Brain Res 87:145-152.
19. Gray CM (1999) The temporal correlation hypothesis of visual feature integration: still alive and well. Neuron 24:31-25.
20. A receptor-mediated responses in pyramidal cells of rat hippocampus. J Neurophysiol 69:1541-1555.
21. Harris KM, Teyler TJ (1984) Developmental onset of long-term potentiation in area CA1 of the rat hippocampus. J Physiol (Lond) 346:27-48.
22. + transient. J Neurosci 17:7662-7672.
23. A receptor-mediated oscillations. J Neurosci 20:6820-6829.
24. Lakis 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.
25. LeBeau FE, Towers SK, Traub RD, Whittington MA, Buhl EH (2002) Fast network oscillations induced by potassium transients in the rat hippocampus in vitro. J Physiol (Lond) 542:167-179.
26. 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.
27. Linden DJ (1999) The return of the spike: postsynaptic action potentials and the induction of LTP and LTD. Neuron 22:661-666.
28. Maren TH (1977) Use of inhibitors in physiological studies of carbonic anhydrase. Am J Physiol (Lond) 232:F291-F297.
29. McCormick DA, Contreras D (2001) On the cellular and network bases of epileptic seizures. Annu Rev Physiol 63:815-846.
30. Nicholson C (1993) Ion-selective microelectrodes and diffusional measurements as tools to explore the brain cell microenvironment. J Neurosci Methods 48:199-213.
31. Nógrádi A, Jonsson N, Walker R, Caddy K, Carter N, Kelly C (1997) Carbonic anhydrase II and carbonic anhydrase-related protein in the cerebellar cortex of normal and lurcher mice. Brain Res Dev Brain Res 98:91-101.
32. Parkkila S, Parkkila AK, Rajaniemi H, Shah GN, Grubb JH, Waheed A, Sly WS (2001) Expression of membrane-associated carbonic anhydrase XIV on neurons and axons in mouse and human brain. Proc Natl Acad Sci USA 98:1918-1923.
33. 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.
34. Perez Velazquez JL (2003) Bicarbonate-dependent depolarizing potentials in pyramidal cells and interneurons during epileptiform activity. Eur J Neurosci 18:1337-1342.
35. Perreault P, Avoli M (1988) A depolarizing inhibitory postsynaptic potential activated by synaptically released gamma-aminobutyric acid under physiological conditions in rat hippocampal pyramidal cells. Can J Physiol Pharmacol 66:1100-1102.
36. Rausche G, Sarvey JM, Heinemann U (1989) Slow synaptic inhibition in relation to frequency habituation in dentate granule cells of rat hippocampal slices. Exp Brain Res 78:233-242.
37. Ridderstråle Y, Wistrand PJ (1998) Carbonic anhydrase isoforms in the mammalian nervous system. In: pH and brain function (Kaila K, Ransom B, eds), pp 21-43. New York: Wiley-Liss.
38. - co-transpoter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397:251-255.
39. - extrusion. J Cell Biol 159:747-752.
40. Saarikoski J, Kaila K (1992) Simultaneous measurement of intracellular and extracellular carbonic anhydrase activity in intact muscle fibres. Pflügers Arch 421:357-363.
41. Santhakumar V, Voipio J, Kaila K, Soltesz I (2003) Post-traumatic hyperexcitability is not caused by impaired buffering of extracellular potassium. J Neurosci 23:5865-5876.
42. Schmitz D, Schuchmann S, Fisahn A, Draguhn A, Buhl EH, Petrasch-Parwez E, Dermietzel R, Heinemann U, Traub RD (2001) Axo-axonal coupling: a novel mechanism for ultrafast neuronal communication. Neuron 31:831-840.
43. Schuchmann S, Meierkord H, Stenkamp K, Breustedt J, Windmuller O, Heinemann U, Buchheim K (2002) Synaptic and nonsynaptic ictogenesis occurs at different temperatures in submerged and interface rat brain slices. J Neurophysiol 87:2929-2935.
44. Singer W (1999) Neuronal synchrony: a versatile code for the definition of relations? Neuron 24:49-65, 111-125.
45. 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.
46. A receptors. Science 269:977-981.
47. Stenkamp K, Palva JM, Uusisaari M, Schuchmann S, Schmitz D, Heinemann U, Kaila K (2001) Enhanced temporal stability of cholinergic hippocampal gamma oscillations following respiratory alkalosis in vitro. J Neurophysiol 85:2063-2069.
48. Supuran CT, Scozzafava A, Casini A (2003) Carbonic anhydrase inhibitors. Med Res Rev 23:146-189.
49. Svichar N, Chesler M (2003) Surface carbonic anhydrase activity on astrocytes and neurons facilitates lactate transport. Glia 41:415-419.
50. Swann JW, Brady RJ, Martin DL (1989) Postnatal development of GABA-mediated synaptic inhibition in rat hippocampus. Neuroscience 28:551-561.
51. Swann JW, Smith KL, Brady RJ (1993) Localized excitatory synaptic interactions mediate the sustained depolarization of electrographic seizures in developing hippocampus. J Neurosci 13:4680-4689.
52. Thomas JA, Buchsbaum RN, Zimniak A, Racker E (1979) Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ. Biochemistry 18:2210-2218.
53. Tong CK, Brion LP, Suarez C, Chesler M (2000) Interstitial carbonic anhydrase (CA) activity in brain is attributable to membrane-bound CA type IV. J Neurosci 20:8247-8253.
54. Traub RD, Whittington MA, Colling SB, Buzsáki G, Jefferys JG (1996a) Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J Physiol (Lond) 493:471-484.
55. Traub RD, Whittington MA, Stanford IM, Jefferys JG (1996b) A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383:621-624.
56. Traub RD, Spruston N, Soltesz I, Konnerth A, Whittington MA, Jefferys GR (1998) Gamma-frequency oscillations: a neuronal population phenomenon, regulated by synaptic and intrinsic cellular processes, and inducing synaptic plasticity. Prog Neurobiol 55:563-575.
57. Uusisaari M, Smirnov S, Voipio J, Kaila K (2000) Spontaneous epileptiform activity mediated by GABA(A) receptors and gap junctions in the rat hippocampal slice following long-term exposure to GABA(B) antagonists. Neuropharmacology 43:563-572.
58. 2 movements in brain tissue. In: pH and brain function (Kaila K, Ransom B, eds), pp 45-66. New York: Wiley-Liss.
59. Voipio J, Ballanyi K (1997) Interstitial PCO2 and pH, and their role as chemostimulants in the isolated respiratory network of neonatal rats. J Physiol (Lond) 499:527-542.
60. +-mediated volume transmission in the hippocampus. Prog Brain Res 125:329-338.
61. Voipio J, Pasternack M, MacLeod KT (1994) Ion-sensitive microelectrodes: microelectrode techniques. In: The Plymouth workshop handbook (Ogden D, ed), pp 275-316. Cambridge, UK: The Company of Biologist.
62. CO2. J Physiol (Lond) 540:951-970.
63. Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612-615.
64. Whittington MA, Stanford IM, Colling SB, Jefferys JG, Traub RD (1997a) Spatiotemporal patterns of gamma frequency oscillations tetanically induced in the rat hippocampal slice. J Physiol (Lond) 502:591-607.
65. Whittington MA, Traub RD, Faulkner HJ, Stanford IM, Jefferys JG (1997b) Recurrent excitatory postsynaptic potentials induced by synchronized fast cortical oscillations. Proc Natl Acad Sci USA 94:12198-12203.
66. Whittington MA, Doheny HC, Traub RD, LeBeau FE, Buhl EH (2001) Differential expression of synaptic and nonsynaptic mechanisms underlying stimulus-induced gamma oscillations in vitro. J Neurosci 21:1727-1738.
67. Wyllie E (1997) The treatment of epilepsy: principles and practice. Baltimore: Williams and Wilkins.