NKCC1 transporter facilitates seizures in the developing brain (original) (raw)

References

  1. Ronen, G.M., Penney, S. & Andrews, W. The epidemiology of clinical neonatal seizures in Newfoundland: a population-based study. J. Pediatr. 134, 71–75 (1999).
    Article CAS Google Scholar
  2. Painter, M.J., Bergman, I. & Crumrine, P. Neonatal seizures. Pediatr. Clin. North Am. 33, 91–109 (1986).
    Article CAS Google Scholar
  3. Scher, M.S. et al. Electrographic seizures in preterm and full-term neonates: clinical correlates, associated brain lesions, and risk for neurologic sequelae. Pediatrics 91, 128–134 (1993).
    CAS PubMed Google Scholar
  4. Brunquell, P.J., Glennon, C.M., DiMario, F.J. Jr., Lerer, T. & Eisenfeld, L. Prediction of outcome based on clinical seizure type in newborn infants. J. Pediatr. 140, 707–712 (2002).
    Article Google Scholar
  5. Jensen, F.E., Holmes, G.L., Lombroso, C.T., Blume, H.K. & Firkusny, I.R. Age-dependent changes in long-term seizure susceptibility and behavior after hypoxia in rats. Epilepsia 33, 971–980 (1992).
    Article CAS Google Scholar
  6. Baram, T.Z. Long-term neuroplasticity and functional consequences of single versus recurrent early-life seizures. Ann. Neurol. 54, 701–705 (2003).
    Article Google Scholar
  7. Holmes, G.L. Effects of early seizures on later behavior and epileptogenicity. Ment. Retard. Dev. Disabil. Res. Rev. 10, 101–105 (2004).
    Article Google Scholar
  8. Swann, J.W. The impact of seizures on developing hippocampal networks. Prog. Brain Res. 147, 347–354 (2005).
    Article Google Scholar
  9. Sanchez, R.M., Dai, W., Levada, R.E., Lippman, J.J. & Jensen, F.E. AMPA/kainate receptor-mediated downregulation of GABAergic synaptic transmission by calcineurin after seizures in the developing rat brain. J. Neurosci. 25, 3442–3451 (2005).
    Article CAS Google Scholar
  10. Connell, J., Oozeer, R., de Vries, L., Dubowitz, L.M. & Dubowitz, V. Clinical and EEG response to anticonvulsants in neonatal seizures. Arch. Dis. Child. 64, 459–464 (1989).
    Article CAS Google Scholar
  11. Painter, M.J. et al. Phenobarbital compared with phenytoin for the treatment of neonatal seizures. N. Engl. J. Med. 341, 485–489 (1999).
    Article CAS Google Scholar
  12. Owens, D.F. & Kriegstein, A.R. Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci. 3, 715–727 (2002).
    Article CAS Google Scholar
  13. Ben Ari, Y. Excitatory actions of gaba during development: the nature of the nurture. Nat. Rev. Neurosci. 3, 728–739 (2002).
    Article CAS Google Scholar
  14. Dzhala, V.I. & Staley, K.J. Excitatory actions of endogenously released GABA contribute to initiation of ictal epileptiform activity in the developing hippocampus. J. Neurosci. 23, 1840–1846 (2003).
    Article CAS Google Scholar
  15. Khazipov, R. et al. Developmental changes in GABAergic actions and seizure susceptibility in the rat hippocampus. Eur. J. Neurosci. 19, 590–600 (2004).
    Article Google Scholar
  16. Stein, V., Hermans-Borgmeyer, I., Jentsch, T.J. & Hubner, C.A. Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J. Comp. Neurol. 468, 57–64 (2004).
    Article CAS Google Scholar
  17. Scher, M.S., Alvin, J., Gaus, L., Minnigh, B. & Painter, M.J. Uncoupling of EEG-clinical neonatal seizures after antiepileptic drug use. Pediatr. Neurol. 28, 277–280 (2003).
    Article Google Scholar
  18. Staley, K., Smith, R., Schaack, J., Wilcox, C. & Jentsch, T.J. Alteration of GABAA receptor function following gene transfer of the CLC-2 chloride channel. Neuron 17, 543–551 (1996).
    Article CAS Google Scholar
  19. Delpire, E. Cation-chloride cotransporters in neuronal communication. News Physiol. Sci. 15, 309–312 (2000).
    CAS PubMed Google Scholar
  20. Payne, J.A., Rivera, C., Voipio, J. & Kaila, K. Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci. 26, 199–206 (2003).
    Article CAS Google Scholar
  21. Yamada, J. et al. Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J. Physiol. (Lond.) 557, 829–841 (2004).
    Article CAS Google Scholar
  22. Isenring, P., Jacoby, S.C., Payne, J.A. & Forbush, B. III. Comparison of Na-K-Cl cotransporters. NKCC1, NKCC2, and the HEK cell Na-L-Cl cotransporter. J. Biol. Chem. 273, 11295–11301 (1998).
    Article CAS Google Scholar
  23. Hannaert, P., Alvarez-Guerra, M., Pirot, D., Nazaret, C. & Garay, R.P. Rat NKCC2/NKCC1 cotransporter selectivity for loop diuretic drugs. Naunyn Schmiedebergs Arch. Pharmacol. 365, 193–199 (2002).
    Article CAS Google Scholar
  24. Plotkin, M.D., Snyder, E.Y., Hebert, S.C. & Delpire, E. Expression of the Na-K-2Cl cotransporter is developmentally regulated in postnatal rat brains: a possible mechanism underlying GABA's excitatory role in immature brain. J. Neurobiol. 33, 781–795 (1997).
    Article CAS Google Scholar
  25. Wang, C. et al. Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain. Brain Res. Dev. Brain Res. 139, 59–66 (2002).
    Article CAS Google Scholar
  26. Clayton, G.H., Owens, G.C., Wolff, J.S. & Smith, R.L. Ontogeny of cation-Cl– cotransporter expression in rat neocortex. Brain Res. Dev. Brain Res. 109, 281–292 (1998).
    Article CAS Google Scholar
  27. Rivera, C. et al. The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397, 251–255 (1999).
    Article CAS Google Scholar
  28. Sullivan, J.E., Witte, M.K., Yamashita, T.S., Myers, C.M. & Blumer, J.L. Pharmacokinetics of bumetanide in critically ill infants. Clin. Pharmacol. Ther. 60, 405–413 (1996).
    Article CAS Google Scholar
  29. Lopez-Samblas, A.M., Adams, J.A., Goldberg, R.N. & Modi, M.W. The pharmacokinetics of bumetanide in the newborn infant. Biol. Neonate 72, 265–272 (1997).
    Article CAS Google Scholar
  30. Lu, J., Karadsheh, M. & Delpire, E. Developmental regulation of the neuronal-specific isoform of K-Cl cotransporter KCC2 in postnatal rat brains. J. Neurobiol. 39, 558–568 (1999).
    Article CAS Google Scholar
  31. Sankar, R. & Painter, M.J. Neonatal seizures: after all these years we still love what doesn't work. Neurology 64, 776–777 (2005).
    Article Google Scholar
  32. Twyman, R.E., Rogers, C.J. & Macdonald, R.L. Differential regulation of gamma-aminobutyric acid receptor channels by diazepam and phenobarbital. Ann. Neurol. 25, 213–220 (1989).
    Article CAS Google Scholar
  33. Staley, K. Enhancement of the excitatory actions of GABA by barbiturates and benzodiazepines. Neurosci. Lett. 146, 105–107 (1992).
    Article CAS Google Scholar
  34. Dzhala, V.I. & Staley, K.J. Transition from interictal to ictal activity in limbic networks in vitro. J. Neurosci. 23, 7873–7880 (2003).
    Article CAS Google Scholar
  35. Dzhala, V.I. & Staley, K.J. Mechanisms of fast ripples in the hippocampus. J. Neurosci. 24, 8896–8906 (2004).
    Article CAS Google Scholar
  36. Ben Ari, Y., Cherubini, E., Corradetti, R. & Gaiarsa, J.L. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J. Physiol. (Lond.) 416, 303–325 (1989).
    Article CAS Google Scholar
  37. Khalilov, I., Dzhala, V., Ben Ari, Y. & Khazipov, R. Dual role of GABA in the neonatal rat hippocampus. Dev. Neurosci. 21, 310–319 (1999).
    Article CAS Google Scholar
  38. Leinekugel, X. et al. Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296, 2049–2052 (2002).
    Article CAS Google Scholar
  39. Delpire, E., Lu, J., England, R., Dull, C. & Thorne, T. Deafness and imbalance associated with inactivation of the secretory Na-K-2Cl co-transporter. Nat. Genet. 22, 192–195 (1999).
    Article CAS Google Scholar
  40. Sung, K.W., Kirby, M., McDonald, M.P., Lovinger, D.M. & Delpire, E. Abnormal GABAA receptor-mediated currents in dorsal root ganglion neurons isolated from Na-K-2Cl cotransporter null mice. J. Neurosci. 20, 7531–7538 (2000).
    Article CAS Google Scholar
  41. Kanaka, C. et al. The differential expression patterns of messenger RNAs encoding K-Cl cotransporters (KCC1,2) and Na-K-2Cl cotransporter (NKCC1) in the rat nervous system. Neuroscience 104, 933–946 (2001).
    Article CAS Google Scholar
  42. Owens, D.F., Boyce, L.H., Davis, M.B. & Kriegstein, A.R. Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J. Neurosci. 16, 6414–6423 (1996).
    Article CAS Google Scholar
  43. Staley, K.J. & Mody, I. Shunting of excitatory input to dentate gyrus granule cells by a depolarizing GABAA receptor-mediated postsynaptic conductance. J. Neurophysiol. 68, 197–212 (1992).
    Article CAS Google Scholar
  44. Jin, X., Huguenard, J.R. & Prince, D.A. Impaired Cl− extrusion in layer V pyramidal neurons of chronically injured epileptogenic neocortex. J. Neurophysiol. 93, 2117–2126 (2005).
    Article CAS Google Scholar
  45. Hochman, D.W., Baraban, S.C., Owens, J.W. & Schwartzkroin, P.A. Dissociation of synchronization and excitability in furosemide blockade of epileptiform activity. Science 270, 99–102 (1995).
    Article CAS Google Scholar
  46. Stringer, J.L. & Pan, E. Effect of seizures and diuretics on the osmolality of the cerebrospinal fluid. Brain Res. 745, 328–330 (1997).
    Article CAS Google Scholar
  47. Haglund, M.M. & Hochman, D.W. Furosemide and mannitol suppression of epileptic activity in the human brain. J. Neurophysiol. 94, 907–918 (2005).
    Article CAS Google Scholar
  48. Hesdorffer, D.C., Stables, J.P., Hauser, W.A., Annegers, J.F. & Cascino, G. Are certain diuretics also anticonvulsants? Ann. Neurol. 50, 458–462 (2001).
    Article CAS Google Scholar
  49. Cohen, I., Navarro, V., Clemenceau, S., Baulac, M. & Miles, R. On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298, 1418–1421 (2002).
    Article CAS Google Scholar
  50. Ulfig, N., Nickel, J. & Bohl, J. Monoclonal antibodies SMI 311 and SMI 312 as tools to investigate the maturation of nerve cells and axonal patterns in human fetal brain. Cell Tissue Res. 291, 433–443 (1998).
    Article CAS Google Scholar

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