Bumetanide enhances phenobarbital efficacy in a neonatal seizure model

Annals of Neurology

Volumn 63, Issue 2, 2008, Pages 222-235

  Dzhala, Volodymyr I ^a,b   Brumback, Audrey C ^b   Staley, Kevin J ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUMETANIDE; CHLORIDE; MAGNESIUM; PHENOBARBITAL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICONVULSANT ACTIVITY; ARTICLE; BRAIN; CHLORIDE TRANSPORT; CONTROLLED STUDY; DISEASE DURATION; DRUG EFFICACY; HIPPOCAMPUS; IN VITRO STUDY; MALE; MORBIDITY; NEUROBLAST; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; RECURRENT DISEASE; SEIZURE; THERAPY EFFECT; TREATMENT FAILURE;

ANIMALS; ANTICONVULSANTS; BUMETANIDE; CHLORIDE CHANNELS; CHLORIDES; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; EPILEPSY, BENIGN NEONATAL; HIPPOCAMPUS; ION TRANSPORT; MAGNESIUM DEFICIENCY; MALE; MEMBRANE POTENTIALS; MODELS, BIOLOGICAL; NEURAL INHIBITION; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; PHENOBARBITAL; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SEIZURES; SODIUM POTASSIUM CHLORIDE SYMPORTER INHIBITORS; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS;

EID: 40449086100     PISSN: 03645134     EISSN: None     Source Type: Journal    
DOI: 10.1002/ana.21229     Document Type: Article

References (81)

1. Kaila K. Ionic basis of GABAA receptor channel function in the nervous system. Prog Neurobiol 1994;42:489-537.
2. Staley KJ, Mody I. Shunting of excitatory input to dentate gyrus granule cells by a depolarizing GABAA receptor-mediated postsynaptic conductance. J Neurophysiol 1992;68: 197-212.
3. Schwartzkroin PA, Prince DA. Penicillin-induced epileptiform activity in the hippocampal in vitro preparation. Ann Neurol 1977;1:463-469.
4. Schwartzkroin PA. Cellular electrophysiology of human epilepsy. Epilepsy Res 1994;17:185-192.
5. Yuste R, Katz LC. Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 1991;6:333-344.
6. Lin MH, Takahashi MP, Takahashi Y, et al. Intracellular calcium increase induced by GABA in visual cortex of fetal and neonatal rats and its disappearance with development. Neurosci Res 1994;20:85-94.
7. Leinekugel X, Tseeb V, Ben Ari Y, et al. Synaptic GABAA activation induces Ca2+ rise in pyramidal cells and interneurons from rat neonatal hippocampal slices. J Physiol 1995;487(pt 2): 319-329.
8. LoTurco JJ, Owens DF, Heath MJ, et al. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 1995;15:1287-1298.
9. Ganguly K, Schinder AF, Wong ST, et al. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 2001;105: 521-532.
10. Ben Ari Y. Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 2002;3:728-739.
11. Cossart R, Bernard C, Ben-Ari Y. Multiple facets of GABAergic neurons and synapses: multiple fates of GABA signalling in epilepsies. Trends Neurosci 2005;28:108-115.
12. Khalilov I, Khazipov R, Esclapez M, et al. Bicuculline induces ictal seizures in the intact hippocampus recorded in vitro. Eur J Pharmacol 1997;319:R5-R6.
13. Khalilov I, Le Van QM, Gozlan H, et al. Epileptogenic actions of GABA and fast oscillations in the developing hippocampus. Neuron 2005;48:787-796.
14. Mueller AL, Taube JS, Schwartzkroin PA. Development of hyperpolarizing inhibitory postsynaptic potentials and hyperpolarizing response to gamma-aminobutyric acid in rabbit hippocampus studied in vitro. J Neurosci 1984;4:860-867.
15. Chen G, Trombley PQ, van den Pol AN. Excitatory actions of GABA in developing rat hypothalamic neurones. J Physiol 1996;494(pt 2):451-464.
16. Khalilov I, Dzhala V, Ben Ari Y, et al. Dual role of GABA in the neonatal rat hippocampus. Dev Neurosci 1999;21: 310-319.
17. Psarropoulou C, Descombes S. Differential bicuculline-induced epileptogenesis in rat neonatal, juvenile and adult CA3 pyramidal neurons in vitro. Brain Res Dev Brain Res 1999;117: 117-120.
18. Wells JE, Porter JT, Agmon A. GABAergic inhibition suppresses paroxysmal network activity in the neonatal rodent hippocampus and neocortex. J Neurosci 2000;20:8822-8830.
19. Dzhala VI, Staley KJ. Excitatory actions of endogenously released GABA contribute to initiation of ictal epileptiform activity in the developing hippocampus. J Neurosci 2003;23: 1840-1846.
20. Khazipov R, Khalilov I, Tyzio R, et al, Developmental changes in GABAergic actions and seizure susceptibility in the rat hippocampus. Eur J Neurosci 2004;19:590-600.
21. Quilichini PP, Diabira D, Chiron C, et al. Effects of antiepileptic drugs on refractory seizures in the intact immature corticohippocampal formation in vitro. Epilepsia 2003;44:1365-1374.
22. Isaev D, Isaeva E, Khazipov R, et al. Shunting and hyperpolarizing GABAergic inhibition in the high-potassium model of ictogenesis in the developing rat hippocampus. Hippocampus 2007;17:210-219.
23. Twyman RE, Rogers CJ, Macdonald RL. Differential regulation of gamma-aminobutyric acid receptor channels by diazepam and phenobarbital. Ann Neurol 1989;25:213-220.
24. Carmo KB, Barr P. Drug treatment of neonatal seizures by neonatologists and paediatric neurologists. J Paediatr Child Health 2005;41:313-316.
25. Connell J, Oozeer R, de Vries L, et al. Clinical and EEG response to anticonvulsants in neonatal seizures. Arch Dis Child 1989;64:459-464.
26. Painter MJ, Scher MS, Stein AD, et al. Phenobarbital compared with phenytoin for the treatment of neonatal seizures. N Engl J Med 1999;341:485-489.
27. Scher MS, Alvin J, Gaus L, et al. Uncoupling of EEG-clinical neonatal seizures after antiepileptic drug use. Pediatr Neurol 2003;28:277-280.
28. Boylan GB, Rennie JM, Chorley G, et al. Second-line anticonvulsant treatment of neonatal seizures: a video-EEG monitoring study. Neurology 2004;62:486-488.
29. Sankar R, Painter MJ. Neonatal seizures: after all these years we still love what doesn't work. Neurology 2005;64:776-777.
30. Dzhala VI, Tabs DM, Sdrulla DA, et al. NKCC1 transporter facilitates seizures in the developing brain. Nat Med 2005;11: 1205-1213.
31. Isenring P, Jacoby SC, Payne JA, et al. Comparison of Na-K-Cl cotransporters. NKCC1, NKCC2, and the HEK cell Na-L-Cl cotransporter. J Biol Chem 1998;273:11295-11301.
32. Hannaert P, Alvarez-Guerra M, Pirot D, et al. Rat NKCC2/NKCC1 cotransporter selectivity for loop diuretic drugs. Naunyn Schmiedebergs Arch Pharmacol 2002;365:193-199.
33. Yamada J, Okabe A, Toyoda H, et al. Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J Physiol 2004;557: 829-841.
34. Sipila ST, Schuchmann S, Voipio J, et al. The cation-chloride cotransporter NKCC1 promotes sharp waves in the neonatal rat hippocampus. J Physiol 2006;573:765-773.
35. Sullivan JE, Witte MK, Yamashita TS, et al. Pharmacokinetics of bumetanide in critically ill infants. Clin Pharmacol Ther 1996;60:405-413.
36. Lopez-Sambias AM, Adams JA, Goldberg RN, et al. The pharmacokinetics of bumetanide in the newborn infanr. Biol Neonate 1997;72:265-272.
37. Khalilov I, Esclapez M, Medina I, et al. A novel in vitro preparation: the intact hippocampal formation. Neuron 1997; 19:743-749.
38. Mody I, Lambert JD, Heinemann U. Low extracellular magnesium induces epileptiform activity and spreading depression in rat hippocampal slices. J Neurophysiol 1987;57:869-888.
39. Ben Ari Y, Cherubini E, Corradetti R, et al. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 1989;416:303-325.
40. Leinekugel X, Khazipov R, Cannon R, et al. Correlated bursts of activity in the neonatal hippocampus in vivo. Science 2002; 296:2049-2052.
41. Sipila ST, Schuchmann S, Voipio J, et al. The cation-chloride cotransporter NKCC1 promotes sharp waves in the neonatal rat hippocampus. J Physiol 2006;573:765-773.
42. Kyrozis A, Reichling DB. Perforated-patch recording with gramicidin avoids artifactual changes in intracellular chloride concentration. J Neurosci Methods 1995;57:27-35.
43. Ebihara S, Shirato K, Harata N, et al. Gramicidin-perforared patch recording: GABA response in mammalian neurones with intact intracellular chloride. J Physiol 1995;484(pt 1): 77-86.
44. Tyzio R, Cossart R, Khalilov I, et al. Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 2006;314:1788-1792.
45. Gillen CM, Brill S, Payne JA, et al. Molecular cloning and functional expression of the K-Cl cotransporter from rabbit, rat, and human. A new member of the cation-chloride cotransporter family. J Biol Chem 1996;271:16237-16244.
46. Russell JM. Sodium-potassium-chloride cotransport. Physiol Rev 2000;80:211-276.
47. Khalilov I, Dzhala V, Medina I, et al. Maturation of kainate-induced epileptiform activities in interconnected intact neonatal limbic structures in vitro. Eur J Neurosci 1999;11: 3468-3480.
48. Luhmann HJ, Dzhala VI, Ben Ari Y. Generation and propagation of 4-AP-induced epileptiform activity in neonatal intact limbic structures in vitro. Eur J Neurosci 2000;12: 2757-2768.
49. Quilichini PP, Diabira D, Chiron C, et al. Persistent epileptiform activity induced by low Mg2+ in intact immature brain structures. Eur J Neurosci 2002;16:850-860.
50. Moser J, Kilb W, Werhahn KJ, et al. Early developmental alterations of low-Mg2+-induced epileptiform activity in the intact corticohippocampal formation of the newborn mouse in vitro. Brain Res 2006;1077:170-177.
51. Macdonald RL, Rogers CJ, Twyman RE. Barbiturate regulation of kinetic properties of the GABAA receptor channel of mouse spinal neurones in culture. J Physiol 1989;417:483-500.
52. Staley K. Enhancement of the excitatory actions of GABA by barbiturates and benzodiazepines. Neurosci Lett 1992;146: 105-107.
53. Kwan P, Sills GJ, Brodie MJ. The mechanisms of action of commonly used antiepileptic drugs. Pharmacol Ther 2001;90: 21-34.
54. Hill DR, Bowery NG. 3H-baclofen and 3H-GABA bind to bicuculline- insensitive GABA B sites in rat brain. Nature 1981; 290:149-152.
55. Khalilov I, Holmes GL, Ben-Ari Y. In vitro formation of a secondary epileptogenic mirror focus by interhippocampal propagation of seizures. Nat Neurosci 2003;6:1079-1085.
56. Jensen MS, Yaari Y. The relationship between interictal and ictal paroxysms in an in vitro model of focal hippocampal epilepsy. Ann Neurol 1988;24:591-598.
57. Traynelis SF, Dingledine R. Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J Neurophysiol 1988;59:259-276.
58. Talos DM, Fishman RE, Park H, et al. Developmental regulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. I. Rodent cerebral white matter and cortex. J Comp Neurol 2006;497:42-60.
59. Payne JA, Rivera C, Voipio J, et al. Cation-chloride cotransporters in neuronal communication, development and trauma. Trends Neurosci 2003;26:199-206.
60. Delpire E. Cation-chloride cotransporters in neuronal communication. News Physiol Sci 2000;15:309-312.
61. Gamba G. Molecular physiology and pathophysiology of electroneutral cation-chloride cotransporters. Physiol Rev 2005;85: 423-493.
62. Isenring P, Forbush B. Ion transport and ligand binding by the Na-K-Cl cotransporter, structure-function studies. Comp Biochem Physiol A Mol Integr Physiol 2001;130:487-497.
63. Tyzio R, Ivanov A, Bernard C, et al. Membrane potential of CA3 hippocampal pyramidal cells during postnatal development. J Neurophysiol 2003;90:2964-2972.
64. Ben Ari Y, Khazipov R, Leinekugel X, er al. GABAA, NMDA and AMPA receptors: a developmentally regulated 'menage a trois.' Trends Neurosci 1997;20:523-529.
65. Cohen I, Miles R. Contributions of intrinsic and synaptic activities to the generation of neuronal discharges in in vitro hippocampus. J Physiol 2000;524(pt 2):485-502.
66. Hochman DW, Baraban SC, Owens JW, et al. Dissociation of synchronization and excitability in furosemide blockade of epileptiform activity. Science 1995;270:99-102.
67. Gutschmidt KU, Stenkamp K, Buchheim K, et al. Anticonvulsant actions of furosemide in vitro. Neuroscience 1999;91: 1471-1481.
68. Hochman DW, Schwartzkroin PA. Chloride-cotransport blockade desynchronizes neuronal discharge in the "epileptic" hippocampal slice. J Neurophysiol 2000;83:406-417.
69. Reid KH, Guo SZ, Iyer VG. Agents which block potassium-chloride cotransport prevent sound-triggered seizures in post-ischemic audiogenic seizure-prone rats. Brain Res 2000;864: 134-137.
70. Hesdorffer DC, Stables JP, Hauser WA, et al. Are certain diuretics also anticonvulsants? Ann Neurol 2001;50: 458-462.
71. Margineanu DG, Klitgaard H. Differential effects of cation-chloride co-transport-blocking diuretics in a rat hippocampal slice model of epilepsy. Epilepsy Res 2006;69:93-99.
72. Haglund MM, Hochman DW. Furosemide and mannitol suppression of epilepric activity in the human brain. J Neurophysiol 2005;94:907-918.
73. Isaev D, Isaeva E, Khazipov R, et al. Anticonvulsant action of GABA in the high potassium-low magnesium model of ictogenesis in the neonatal rat hippocampus in vivo and in vitro. J Neurophysiol 2005;94:2987-2992.
74. Bittigau P, Sifringer M, Genz K, et al. Antiepileptic drugs and apoptotic neurodegeneration in the developing brain. Proc Natl Acad Sci U S A 2002;99:15089-15094.
75. Bittigau P, Sifringer M, Ikonomidou C. Antiepileptic drugs and apoptosis in the developing brain. Ann N Y Acad Sci 2003;993: 103-114.
76. Farwell JR, Lee YJ, Hirtz DG, et al. Phenobarbital for febrile seizures - effects on intelligence and on seizure recurrence. N Engl J Med 1990;322:364-369.
77. Reinisch JM, Sanders SA, Mortensen EL, et al. In utero exposure to phenobarbital and intelligence deficits in adult men. JAMA 1995;274:1518-1525.
78. Ge S, Goh ELK, Sailor KA, et al. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 2006;439:589-593.
79. Holmes GL, Ben Ari Y. Seizures in the developing brain: perhaps not so benign after all. Neuron 1998;21:1231-1234.
80. Cohen I, Navarro V, Clemenceau S, et al. On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 2002;298:1418-1421.
81. Palma E, Amici M, Sobrero F, et al. Anomalous levels of Cl-transporters in the hippocampal subiculum from temporal lobe epilepsy patients make GABA excitatory. Proc Natl Acad Sci U S A 2006;103:8465-8468.