The extracellular space and epileptic activity in the adult brain: Explaining the antiepileptic effects of furosemide and bumetanide

Epilepsia

Volumn 53, Issue SUPPL. 1, 2012, Pages 18-25

  Hochman, Daryl W ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Astrocytes; Bumetanide; Epilepsy; Extracellular space; Furosemide; Intrinsic optical signal; KCC2; NKCC1

Indexed keywords

BUMETANIDE; FUROSEMIDE; GLUCONIC ACID; POTASSIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER;

ADULT; ANTICONVULSANT ACTIVITY; ARTICLE; BRAIN SLICE; CELL SWELLING; CORTICAL SYNCHRONIZATION; DRUG EFFECT; DRUG MECHANISM; DRUG POTENCY; EPILEPTIC DISCHARGE; EXTRACELLULAR SPACE; HIPPOCAMPUS; HUMAN; INTRACTABLE EPILEPSY; NONHUMAN; OSMOLARITY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL;

ANIMALS; ANTICONVULSANTS; BRAIN; BUMETANIDE; DIURETICS; EPILEPSY; EXTRACELLULAR SPACE; FUROSEMIDE; HUMANS; NEUROIMAGING; OSMOLAR CONCENTRATION; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SYMPORTERS;

EID: 84861349570     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2012.03471.x     Document Type: Article

References (46)

1. Ahmad S, Clarke L, Hewett AJ, Richens A,. (1976) Controlled trial of frusemide as an antiepileptic drug in focal epilepsy. Br J Clin Pharmacol 3: 621-625.
2. Andrew RD,. (1991) Seizure and acute osmotic change: clinical and neurophysiological aspects. J Neurol Sci 101: 7-18.
3. Andrew RD, MacVicar BA,. (1994) Imaging cell volume changes and neuronal excitation in the hippocampal slice. Neuroscience 62: 371-383.
4. Baran H, Lassmann H, Sperk G, Seitelberger F, Hornykiewicz O,. (1987) Effect of mannitol treatment on brain neurotransmitter markers in kainic acid-induced epilepsy. Neuroscience 21: 679-684.
5. Blaesse P, Airaksinen MS, Rivera C, Kaila K,. (2009) Cation-chloride cotransporters and neuronal function. Neuron 61: 820-838.
6. Cala PM,. (1990) Principles of cell volume regulation: ion flux pathways and the roles of anions. In, Alvarez-Leefmans FJ, Russell JM, (Eds) Chloride channels and carriers in nerve, muscle and glial cells. Plenum, New York, pp. 331-353.
7. Chen KC, Nicholson C,. (2000) Spatial buffering of potassium ions in brain extracellular space. Biophys J 78: 2776-2797.
8. Dudek FE, Obenaus A, Tasker JG,. (1990) Osmolality-induced changes in extracellular volume alter epileptiform bursts independent of chemical synapses in the rat: importance of non-synaptic mechanisms in hippocampal epileptogenesis. Neurosci Lett 120: 267-270.
9. Dudek FE, Yasumura T, Rash JE,. (1998) 'Non-synaptic' mechanisms in seizures and epileptogenesis. Cell Biol Int 22: 793-805.
10. 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.
11. Emmi A, Wenzel HJ, Schwartzkroin PA, Taglialatela M, Castaldo P, Bianchi L, Nerbonne J, Robertson GA, Janigro D,. (2000) Do glia have heart? Expression and functional role for ether-a-go-go currents in hippocampal astrocytes J Neurosci 20: 3915-3925.
12. Geck P, Pfeiffer B,. (1985) Na+- K + 2Cl- cotransport in animal cellsâ€"its role in volume regulation. Ann NY Acad Sci 456: 167-183.
13. Gutschmidt KU, Stenkamp K, Buchheim K, Heinemann U, Meierkord H,. (1999) Anticonvulsant actions of furosemide in vitro. Neuroscience 91: 1471-1481.
14. Haglund MM, Hochman DW,. (2005) Furosemide and mannitol suppression of epileptic activity in the human brain. J Neurophysiol 94: 907-918.
15. Haglund MM, Hochman DW,. (2009) Evidence that bumetanide suppresses epileptiform activity in adult primate cortex independent of effects on GABA-A signaling. American Epilepsy Society Meeting abstract. 3.035.
16. Hasannejad H, Takeda M, Taki K, Shin HJ, Babu E, Jutabha P, Khamdang S, Aleboyeh M, Onozato ML, Tojo A, Enomoto A, Anzai N, Narikawa S, Huang XL, Niwa T, Endou H,. (2004) Interactions of human organic anion transporters with diuretics. J Pharmacol Exp Ther 308: 1021-1029.
17. Hochman DW,. (2009) Changes in the extracellular space as a modulator of excitability and epileptogenicity. In, Schwartzkroin PA, (Ed.) Basic epilepsy research, Vol 2. Academic Press, Oxford, pp. 946-953.
18. Hochman DW, Schwartzkroin PA,. (2000) Chloride-cotransport blockade desynchronizes neuronal discharge in the "epileptic" hippocampal slice. J Neurophysiol 83: 406-417.
19. Hochman DW, Baraban SC, Owens JW, Schwartzkroin PA,. (1995) Dissociation of synchronization and excitability in furosemide blockade of epileptiform activity. Science 270: 99-102.
20. Hochman DW, D'Ambrosio R, Janigro D, Schwartzkroin PA,. (1999) Extracellular chloride and the maintenance of spontaneous epileptiform activity in rat hippocampal slices. J Neurophysiol 81: 49-59.
21. Holthoff K, Witte OW,. (1996) Intrinsic optical signals in rat neocortical slices measured with near-infrared dark-field microscopy reveal changes in extracellular space. J Neurosci 16: 2740-2749.
22. 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.
23. Jarolimek W, Brunner H, Lewen A, Misgeld U,. (1996) Role of chloride-homeostasis in the inhibitory control of neuronal network oscillators. J Neurophysiol 75: 2654-2657.
24. Jefferys JG,. (1995) Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol Rev 75: 689-723.
25. Kimelberg HK, Frangakis MV,. (1985) Furosemide- and bumetanide-sensitive ion transport and volume control in primary astrocyte cultures from rat brain. Brain Res 361: 125-134.
26. Kusuhara H, Sekine T, Utsunomiya-Tate N, Tsuda M, Kojima R, Cha SH, Sugiyama Y, Kanai Y, Endou H,. (1999) Molecular cloning and characterization of a new multispecific organic anion transporter from rat brain. J Biol Chem 274: 13675-13680.
27. Lebovitz RM,. (1996) Quantitative examination of dynamic interneuronal coupling via single-spike extracellular potassium ion transients. J Theor Biol 180: 11-25.
28. MacVicar BA, Hochman D,. (1991) Imaging of synaptically evoked intrinsic optical signals in hippocampal slices. J Neurosci 11: 1458-1469.
29. + uptake via NKCC1 and swelling of astrocytes. Glia 37: 114-123.
30. Margineanu DG, Klitgaard H,. (2006) Differential effects of cation-chloride co-transport-blocking diuretics in a rat hippocampal slice model of epilepsy. Epilepsy Res 69: 93-99.
31. Ostby I, Oyehaug L, Einevoll GT, Nagelhus EA, Plahte E, Zeuthen T, Lloyd CM, Ottersen OP, Omholt SW,. (2009) Astrocytic mechanisms explaining neural-activity-induced shrinkage of extraneuronal space. PLoS Comput Biol 5: e1000272.
32. Payne JA,. (1997) Functional characterization of the neuronal-specific K-Cl cotransporter: implications for [K+]o regulation. Am J Physiol 273 (5 Pt 1): C1516-C1525.
33. Ransom BR, Yamate CL, Connors BW,. (1985) Activity-dependent shrinkage of extracellular space in rat optic nerve: a developmental study. J Neurosci 5: 531-535.
34. Reed DJ, Woodbury DM,. (1964) The effect of hypertonic urea solution on electroshock seizure threshold and electrolyte distribution in rats. J Pharmacol 146: 154-159.
35. Reid KH, Guo SZ, Iyer VG,. (2000) Agents which block potassium-chloride cotransport prevent sound-triggered seizures in post-ischemic audiogenic seizure-prone rats. Brain Res 864: 134-137.
36. Roper SN, Obenaus A, Dudek FE,. (1992) Osmolality and nonsynaptic epileptiform bursts in rat CA1 and dentate gyrus. Ann Neurol 31: 81-85.
37. Russel JM,. (2000) Sodium-potassium-chloride cotransport. Physiol Rev 80: 211-276.
38. Schwartzkroin PA, Baraban SC, Hochman DW,. (1998) Osmolarity, ionic flux, and changes in brain excitability. Epilepsy Res 31: 275-285.
39. Simard M, Nedergaard M,. (2004) The neurobiology of glia in context of water and ion homeostasis. Neuroscience 129: 877-896.
40. Sontheimer H,. (1994) Voltage-dependent ion channels in glial cells. Glia 11: 156-172.
41. Tata NV, Venkataramanan R, Sahota SK,. (1993) Bumetanide. In, Brittain HG, (Ed.) Analytical profiles of drug substances and excipients. 22, Academic Press, San Diego, CA, pp. 107-144.
42. Thompson SM, Deisz RA, Prince DA,. (1988) Relative contributions of passive equilibrium and active transport to the distribution of chloride in mammalian cortical neurons. J Neurophysiol 60: 105-124.
43. Traynelis SF, Dingledine R,. (1989) Role of extracellular space in hyperosmotic suppression of potassium-induced electrographic seizures. J Neurophysiol 61: 927-938.
44. Viitanen T, Ruusuvuori E, Kaila K, Voipio J,. (2010) The K+-Cl- cotransporter KCC2 promotes GABAergic excitation in the mature rat hippocampus. J Physiol 588: 1527-1540.
45. Walz W, Hinks EC,. (1985) Carrier-mediated KCl accumulation accompanied by water movements is involved in the control of physiological K+ levels by astrocytes. Brain Res 343: 44-51.
46. Wenzel J, Lammert G, Meyer U, Krug M,. (1991) The influence of long-term potentiation on the spatial relationship between astrocyte processes and potentiated synapses in the dentate gyrus neuropil of rat brain. Brain Res 560: 122-131.