Anomalous levels of Cl- transporters cause a decrease of GABAergic inhibition in human peritumoral epileptic cortex

Epilepsia

Volumn 52, Issue 9, 2011, Pages 1635-1644

  Conti, Luca ^a   Palma, Eleonora ^a,b   Roseti, Cristina ^a,b   Lauro, Clotilde ^a   Cipriani, Raffaela ^a   De Groot, Marjolein ^c,d   Aronica, Eleonora ^c   Limatola, Cristina ^a,e  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b IRCCS SAN RAFFAELE PISANA   (Italy)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^e IRCCS NEUROMED   (Italy)

Author keywords

Brain tumor; Chloride homeostasis; Epilepsy; GABAA

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BUMETANIDE; COTRANSPORTER; KCC2 PROTEIN; N,N,N',N' TETRAKIS(2 PYRIDYLMETHYL)ETHYLENEDIAMINE; NKCC1 PROTEIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DEPOLARIZATION; EPILEPSY; EPILEPTOGENESIS; EVOKED CORTICAL RESPONSE; FEMALE; GABAERGIC SYSTEM; GLIOBLASTOMA; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; MICROELECTRODE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; VOLTAGE CLAMP; XENOPUS;

ADULT; AGED; ANIMALS; BIOPHYSICS; BRAIN NEOPLASMS; CEREBRAL CORTEX; ELECTRIC STIMULATION; EPILEPSY; FEMALE; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HUMANS; MALE; MEMBRANE POTENTIALS; MICROINJECTIONS; MIDDLE AGED; OOCYTES; PATCH-CLAMP TECHNIQUES; RECEPTORS, GABA-A; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SYMPORTERS; XENOPUS; YOUNG ADULT;

EID: 80052545981     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2011.03111.x     Document Type: Article

References (45)

1. Akaike N, Inomata N, Tokutomi N,. (1987) Contribution of chloride shifts to the fade of gamma-aminobutyric acid-gated currents in frog dorsal root ganglion cells. J Physiol 391: 219-234. (Pubitemid 17161438)
2. - -cotransporter, in epilepsy-associated malformations of cortical development. Neuroscience 145: 185-196. (Pubitemid 46227715)
3. Asiedu M, Ossipov MH, Kaila K, Price TJ,. (2010) Acetazolamide and midazolam act synergistically to inhibit neuropathic pain. Pain 148: 302-308.
4. Ben-Ari Y,. (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3: 728-739. (Pubitemid 135706678)
5. Ben-Ari Y, Gaiarsa JL, Tyzio R, Khazipov R,. (2007) GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87: 1215-1284. (Pubitemid 350041471)
6. Blaesse P, Airaksinen MS, Rivera C, Kaila K,. (2009) Cation-chloride cotransporters and neuronal function. Neuron 61: 820-838.
7. Bormann J, Hamill OP, Sakmann B,. (1987) Mechanism of anion permeation through channels gated by glycine and gamma-aminobutyric acid in mouse cultured spinal neurones. J Physiol 385: 243-286. (Pubitemid 17048935)
8. 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. (Pubitemid 35346141)
9. Dzhala VI, Talos DM, Sdrulla DA, Brumback AC, Mathews GC, Benke TA, Delpire E, Jensen FE, Staley KJ,. (2005) NKCC1 transporter facilitates seizures in the developing brain. Nat Med 11: 1205-1213. (Pubitemid 43093668)
10. Dzhala VI, Kuchibhotla KV, Glykys JC, Kahle KT, Swiercz WB, Feng G, Kuner T, Augustine GJ, Bacskai BJ, Staley KJ,. (2010) Progressive NKCC1-dependent neuronal chloride accumulation during neonatal seizures. J Neurosci 30: 11745-11761.
11. Ernest NJ, Weaver AK, Van Duyn LB, Sontheimer HW,. (2005) Relative contribution of chloride channels and transporters to regulatory volume decrease in human glioma cells. Am J Physiol Cell Physiol 288: C1451-C1460. (Pubitemid 40991082)
12. Eusebi F, Palma E, Amici M, Miledi R,. (2009) Microtransplantation of ligand-gated receptor-channels from fresh or frozen nervous tissue into Xenopus oocytes: a potent tool for expanding functional information. Prog Neurobiol 88: 32-40.
13. A receptor function in human temporal cortical neurons. J Neurophysiol 75: 1458-1471.
14. Grassi F,. (1992) Cl(-)-mediated interaction between GABA and glycine currents in cultured rat hippocampal neurons. Brain Res 594: 115-123.
15. Gulyás AI, Sík 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. (Pubitemid 32664304)
16. Habela CW, Ernest NJ, Swindall AF, Sontheimer H,. (2009) Chloride accumulation drives volume dynamics underlying cell proliferation and migration. J Neurophysiol 101: 750-757.
17. Hauser WA, Annegers JF, Kurland LT,. (1993) Incidence of epilepsy and unprovoked seizures in Rochester, Minnesota: 1935-1984. Epilepsia 34: 453-468. (Pubitemid 23184580)
18. Hershfinkel M, Kandler K, Knoch ME, Dagan-Rabin M, Aras MA, Abramovitch-Dahan C, Sekler I, Aizenman E,. (2009) Intracellular zinc inhibits KCC2 transporter activity. Nat Neurosci 12: 725-727.
19. Huberfeld G, Wittner L, Clemenceau S, Baulac M, Kaila K, Miles R, Rivera C,. (2007) Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy. J Neurosci 27: 9866-9873. (Pubitemid 47404011)
20. Janigro D,. (2006) Inhibitory GABA current rundown in epileptic brain: use-dependent and pathology-specific mechanisms. Epilepsy Curr 6: 138-139.
21. A receptor channel function in the nervous system. Prog Neurobiol 42: 489-537.
22. Kaila K, Voipio J,. (1987) Postsynaptic fall in intracellular pH induced by GABA-activated bicarbonate conductance. Nature 330: 163-165. (Pubitemid 17158543)
23. Kaila K, Voipio J, Paalasmaa P, Pasternack M, Deisz RA,. (1993) The role of bicarbonate in GABAA receptor-mediated IPSPs of rat neocortical neurones. J Physiol 464: 273-289. (Pubitemid 23169315)
24. Khirug S, Huttu K, Ludwig A, Smirnov S, Voipio J, Rivera C, Kaila K, Khiroug L,. (2005) Distinct properties of functional KCC2 expression in immature mouse hippocampal neurons in culture and in acute slices. Eur J Neurosci 21: 899-904. (Pubitemid 40461043)
25. Kusano K, Miledi R, Stinnakre J,. (1982) Cholinergic and catecholaminergic receptors in the Xenopus oocyte membrane. J Physiol 328: 143-170. (Pubitemid 12090159)
26. Labrakakis C, Patt S, Hartmann J, Kettenmann H,. (1998) Functional GABA(A) receptors on human glioma cells. Eur J Neurosci 10: 231-238.
27. Miledi R,. (1982) A calcium-dependent transient outward current in Xenopus laevis oocytes. Proc R Soc Lond B Biol Sci 215: 491-497. (Pubitemid 12026327)
28. Miledi R, Parker I,. (1984) Chloride current induced by injection of calcium into Xenopus oocytes. J Physiol 357: 173-183. (Pubitemid 15175338)
29. Miledi R, Eusebi F, Martínez-Torres A, Palma E, Trettel F,. (2002) Expression of functional neurotransmitter receptors in Xenopus oocytes after injection of human brain membranes. Proc Natl Acad Sci USA 99: 13238-13242.
30. Miledi R, Palma E, Eusebi F,. (2006) Microtransplantation of neurotransmitter receptors from cells to Xenopus oocyte membranes: new procedure for ion channel studies. Methods Mol Biol 322: 347-355.
31. Muñoz A, Méndez P, DeFelipe J, Alvarez-Leefmans FJ,. (2007) Cation-chloride cotransporters and GABA-ergic innervation in the human epileptic hippocampus. Epilepsia 48: 663-673. (Pubitemid 46587625)
32. Palma E, Trettel F, Fucile S, Renzi M, Miledi R, Eusebi F,. (2003) Microtransplantation of membranes from cultured cells to Xenopus oocytes: a method to study neurotransmitter receptors embedded in native lipids. Proc Natl Acad Sci USA 100: 2896-2900. (Pubitemid 36297595)
33. Palma E, Ragozzino DA, Di Angelantonio S, Spinelli G, Trettel F, Martinez-Torres A, Torchia G, Arcella A, Di Gennaro G, Quarato PP, Esposito V, Cantore G, Miledi R, Eusebi F,. (2004) Phosphatase inhibitors remove the run-down of gamma-aminobutyric acid type A receptors in the human epileptic brain. Proc Natl Acad Sci USA 101: 10183-10188. (Pubitemid 38891216)
34. A receptors from the human epileptic hippocampal subiculum microtransplanted to Xenopus oocytes. Proc Natl Acad Sci USA 102: 2514-2518. (Pubitemid 40279408)
35. Palma E, Amici M, Sobrero F, Spinelli G, Di Angelantonio S, Ragozzino D, Mascia A, Scoppetta C, Esposito V, Miledi R, Eusebi F,. (2006) Anomalous levels of Cl- transporters in the hippocampal subiculum from temporal lobe epilepsy patients make GABA excitatory. Proc Natl Acad Sci USA 103: 8465-8468. (Pubitemid 43838478)
36. 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. (Pubitemid 23179952)
37. Payne JA, Rivera C, Voipio J, Kaila K,. (2003) Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 26: 199-206. (Pubitemid 36412002)
38. Ragozzino D, Palma E, Di Angelantonio S, Amici M, Mascia A, Arcella A, Giangaspero F, Cantore G, Di Gennaro G, Manfredi M, Esposito V, Quarato PP, Miledi R, Eusebi F,. (2005) Rundown of GABA type A receptors is a dysfunction associated with human drug-resistant mesial temporal lobe epilepsy. Proc Natl Acad Sci USA 102: 15219-15223. (Pubitemid 41513362)
39. Rivera C, Voipio J, Payne JA, Ruusuvuori E, Lahtinen H, Lamsa K, Pirvola U, Saarma M, Kaila K,. (1999) The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397: 251-255.
40. Shamji MF, Fric-Shamji EC, Benoit BG,. (2009) Brain tumors and epilepsy: pathophysiology of peritumoral changes. Neurosurg Rev 32: 275-284.
41. Sontheimer H,. (2008) An unexpected role for ion channels in brain tumor metastasis. Exp Biol Med 233: 779-791.
42. Spitzer NC,. (2010) How GABA generates depolarization. J Physiol 588: 757-758.
43. A reversal potential contribute to epileptogenesis? Epilepsy Curr 8: 107-110.
44. Synowitz M, Ahmann P, Matyash M, Kuhn SA, Hofmann B, Zimmer C,. (2001) GABA (A)-receptor expression in glioma cells is triggered by contact with neuronal cells. Eur J Neurosci 14: 1294-1302. (Pubitemid 35463736)
45. Van Breemen MS, Wilms EB, Vecht CJ,. (2007) Epilepsy in patients with brain tumours: epidemiology, mechanisms, and management. Lancet Neurol 6: 421-430. (Pubitemid 46551867)