Differential expression patterns of chloride transporters, Na+-K+-2Cl--cotransporter and K+-Cl--cotransporter, in epilepsy-associated malformations of cortical development

Neuroscience

Volumn 145, Issue 1, 2007, Pages 185-196

  Aronica, E ^a   Boer, K ^a   Redeker, S ^a   Spliet, W G M ^b   van Rijen, P C ^b   Troost, D ^a   Gorter, J A ^c,d  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d STICHTING EPILEPSIE INSTELLINGEN NEDERLAND SEIN   (Netherlands)

Author keywords

cation chloride cotransporter; epilepsy; focal cortical dysplasia; ganglioglioma; hemimegalencephaly; immunocytochemistry

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; COTRANSPORTER; POTASSIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; ALEXANDER DISEASE; ARTICLE; BRAIN MALFORMATION; CELLULAR DISTRIBUTION; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CORTICAL DYSPLASIA; DEVELOPMENTAL DISORDER; FEMALE; GLIOMA; HUMAN; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; INTRACTABLE EPILEPSY; MALE; NEUROPIL; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TISSUE DISTRIBUTION;

ADOLESCENT; ADULT; CEREBRAL CORTEX; CEREBRAL HEMORRHAGE; CHILD; CHILD, PRESCHOOL; EPILEPSY; FEMALE; GANGLIOGLIOMA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMUNOHISTOCHEMISTRY; INFANT; MALE; NERVE TISSUE PROTEINS; POSTMORTEM CHANGES; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SYMPORTERS;

EID: 33846871704     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.11.041     Document Type: Article

References (52)

1. Aronica E., Gorter J.A., Jansen G.H., van Veelen C.W., van Rijen P.C., Ramkema M., and Troost D. Expression and cell distribution of group I and group II metabotropic glutamate receptor subtypes in Taylor-type focal cortical dysplasia. Epilepsia 44 (2003) 785-795
2. Aronica E., Leenstra S., Jansen G.H., van Veelen C.W., Yankaya B., and Troost D. Expression of brain-derived neurotrophic factor and tyrosine kinase B receptor proteins in glioneuronal tumors from patients with intractable epilepsy: colocalization with N-methyl-D-aspartic acid receptor. Acta Neuropathol (Berl) 101 (2001) 383-392
3. Avoli M., Louvel J., Mattia D., Olivier A., Esposito V., Pumain R., and D'Antuono M. Epileptiform synchronization in the human dysplastic cortex. Epileptic Disord 5 (2003) 45-50
4. Avoli M., Louvel J., Pumain R., and Kohling R. Cellular and molecular mechanisms of epilepsy in the human brain. Prog Neurobiol 77 (2005) 166-200
5. Barkovich A.J., Kuzniecky R.I., Jackson G.D., Guerrini R., and Dobyns W.B. A developmental and genetic classification for malformations of cortical development. Neurology 65 (2005) 1873-1887
6. Ben-Ari Y. Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3 (2002) 728-739
7. Binder D.K., and Steinhauser C. Functional changes in astroglial cells in epilepsy. Glia 54 (2006) 358-368
8. Blumcke I., and Wiestler O.D. Gangliogliomas: an intriguing tumor entity associated with focal epilepsies. J Neuropathol Exp Neurol 61 (2002) 575-584
9. Boonyapisit K., Najm I., Klem G., Ying Z., Burrier C., LaPresto E., Nair D., Bingaman W., Prayson R., and Luders H. Epileptogenicity of focal malformations due to abnormal cortical development: direct electrocorticographic-histopathologic correlations. Epilepsia 44 (2003) 69-76
10. Cepeda C., Andre V.M., Flores-Hernandez J., Nguyen O.K., Wu N., Klapstein G.J., Nguyen S., Koh S., Vinters H.V., Levine M.S., and Mathern G.W. Pediatric cortical dysplasia: correlations between neuroimaging, electrophysiology and location of cytomegalic neurons and balloon cells and glutamate/GABA synaptic circuits. Dev Neurosci 27 (2005) 59-76
11. Cepeda C., Andre V.M., Vinters H.V., Levine M.S., and Mathern G.W. Are cytomegalic neurons and balloon cells generators of epileptic activity in pediatric cortical dysplasia?. Epilepsia 46 (2005) 82-88
12. Cepeda C., Andre V.M., Levine M.S., Salamon N., Miyata H., Vinters H.V., and Mathern G.W. Epileptogenesis in pediatric cortical dysplasia: The dysmature cerebral developmental hypothesis. Epilepsy Behav 9 (2006) 219-235
13. Chen H., and Sun D. The role of Na-K-Cl co-transporter in cerebral ischemia. Neurol Res 27 (2005) 280-286
14. Clayton G.H., Owens G.C., Wolff J.S., and Smith R.L. Ontogeny of cation-Cl- cotransporter expression in rat neocortex. Brain Res Dev Brain Res 109 (1998) 281-292
15. Crino P.B. Molecular pathogenesis of focal cortical dysplasia and hemimegalencephaly. J Child Neurol 20 (2005) 330-336
16. Crino P.B., Miyata H., and Vinters H.V. Neurodevelopmental disorders as a cause of seizures: neuropathologic, genetic, and mechanistic considerations. Brain Pathol 12 (2002) 212-233
17. D'Antuono M., Louvel J., Kohling R., Mattia D., Bernasconi A., Olivier A., Turak B., Devaux A., Pumain R., and Avoli M. GABAA receptor-dependent synchronization leads to ictogenesis in the human dysplastic cortex. Brain 127 (2004) 1626-1640
18. Dzhala V.I., Talos D.M., Sdrulla D.A., Brumback A.C., Mathews G.C., Benke T.A., Delpire E., Jensen F.E., and Staley K.J. NKCC1 transporter facilitates seizures in the developing brain. Nat Med 11 (2005) 1205-1213
19. Engel J.J. Outcome with respect to epileptic seizures. In: Engel J.J. (Ed). Surgical treatment of the epilepsies (1993), Raven Press, New York 609-621
20. Englund C., Folkerth R.D., Born D., Lacy J.M., and Hevner R.F. Aberrant neuronal-glial differentiation in Taylor-type focal cortical dysplasia (type IIA/B). Acta Neuropathol 109 (2005) 519-533
21. Farrell M.A., and Vinters H.V. General neuropathology of epilepsy. In: Engel J., and Pedley T.A. (Eds). Epilepsy: A comprehensive textbook (1997), Lippincott-Raven, Philadelphia 157-174
22. Flores-Sarnat L., Sarnat H.B., Davila-Gutierrez G., and Alvarez A. Hemimegalencephaly: part 2. Neuropathology suggests a disorder of cellular lineage. J Child Neurol 18 (2003) 776-785
23. Gulyas A.I., Sik A., Payne J.A., Kaila K., and Freund T.F. The KCl cotransporter, KCC2, is highly expressed in the vicinity of excitatory synapses in the rat hippocampus. Eur J Neurosci 13 (2001) 2205-2217
24. - extrusion in layer V pyramidal neurons of chronically injured epileptogenic neocortex. J Neurophysiol 93 (2005) 2117-2126
25. Kanaka C., Ohno K., Okabe A., Kuriyama K., Itoh T., Fukuda A., and Sato K. 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 (2001) 933-946
26. Kleihues P., and Cavanee W.K. World Health Organization classification of tumours. Pathology and genetics of tumours of the nervous system (2000), IARC Press, Lyon
27. Lenart B., Kintner D.B., Shull G.E., and Sun D. Na-K-Cl cotransporter-mediated intracellular Na+ accumulation affects Ca2+ signaling in astrocytes in an in vitro ischemic model. J Neurosci 24 (2004) 9585-9597
28. Levada R., Talos D.M., Folkert R.D., Staley K.J., and Jensen E. Developmental expression of the chloride transporters KCC2 and NKCC1 in rat and human cortex. Epilepsia 46 13 (2005) IW23
29. Li H., Tornberg J., Kaila K., Airaksinen M.S., and Rivera C. Patterns of cation-chloride cotransporter expression during embryonic rodent CNS development. Eur J Neurosci 16 (2002) 2358-2370
30. Ludwig A., Li H., Saarma M., Kaila K., and Rivera C. Developmental up-regulation of KCC2 in the absence of GABAergic and glutamatergic transmission. Eur J Neurosci 18 (2003) 3199-3206
31. Majores M., Schick V., Engels G., Fassunke J., Elger C.E., Schramm J., Blumcke I., and Becker A.J. Mutational and immunohistochemical analysis of ezrin-, radixin-, moesin (ERM) molecules in epilepsy-associated glioneuronal lesions. Acta Neuropathol 110 (2005) 537-546
32. Mattia D., Olivier A., and Avoli M. Seizure-like discharges recorded in human dysplastic neocortex maintained in vitro. Neurology 45 (1995) 1391-1395
33. Mikawa S., Wang C., Shu F., Wang T., Fukuda A., and Sato K. Developmental changes in KCC1, KCC2 and NKCC1 mRNAs in the rat cerebellum. Brain Res Dev Brain Res 136 (2002) 93-100
34. Moore-Hoon M.L., and Turner R.J. Molecular and topological characterization of the rat parotid Na+-K+-2Cl- cotransporter1. Biochim Biophys Acta 1373 (1998) 261-269
35. Najm I., Ying Z., Babb T., Crino P.B., Macdonald R., Mathern G.W., and Spreafico R. Mechanisms of epileptogenicity in cortical dysplasias. Neurology 62 (2004) S9-S13
36. Okabe A., Ohno K., Toyoda H., Yokokura M., Sato K., and Fukuda A. Amygdala kindling induces upregulation of mRNA for NKCC1, a Na(+), K(+)-2Cl(-) cotransporter, in the rat piriform cortex. Neurosci Res 44 (2002) 225-229
37. Owens D.F., and Kriegstein A.R. Is there more to GABA than synaptic inhibition?. Nat Rev Neurosci 3 (2002) 715-727
38. - transporters in the hippocampal subiculum from temporal lobe epilepsy patients make GABA excitatory. [erratum appears in Proc Natl Acad Sci U S A 2006;103(31):11814]. Proc Natl Acad Sci U S A 103 (2006) 8465-8468
39. Palmini A., Gambardella A., Andermann F., Dubeau F., da Costa J.C., Olivier A., Tampieri D., Gloor P., Quesney F., Andermann E., et al. Intrinsic epileptogenicity of human dysplastic cortex as suggested by corticography and surgical results. Ann Neurol 37 (1995) 476-487
40. Palmini A., Najm I., Avanzini G., Babb T., Guerrini R., Foldvary-Schaefer N., Jackson G., Luders H.O., Prayson R., Spreafico R., and Vinters H.V. Terminology and classification of the cortical dysplasias. Neurology 62 (2004) S2-S8
41. Payne J.A., Rivera C., Voipio J., and Kaila K. Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 26 (2003) 199-206
42. Prayson R.A., Kotagal P., Wyllie E., and Bingaman W. Linear epidermal nevus and nevus sebaceus syndromes: a clinicopathologic study of 3 patients. Arch Pathol Lab Med 123 (1999) 301-305
43. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397 (1999) 251-255
44. Rosenow F., Luders H.O., Dinner D.S., Prayson R.A., Mascha E., Wolgamuth B.R., Comair Y.G., and Bennett G. Histopathological correlates of epileptogenicity as expressed by electrocorticographic spiking and seizure frequency. Epilepsia 39 (1998) 850-856
45. Salamon N., Andres M., Chute D.J., Nguyen S.T., Chang J.W., Huynh M.N., Chandra P.S., Andre V.M., Cepeda C., Levine M.S., Leite J.P., Neder L., Vinters H.V., and Mathern G.W. Contralateral hemimicrencephaly and clinical-pathological correlations in children with hemimegalencephaly. Brain 129 (2006) 352-365
46. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., Fujimoto E.K., Goeke N.M., Olson B.J., and Klenk D.C. Measurement of protein using bicinchoninic acid. [published erratum appears in Anal Biochem 1987;163(1):279]. Anal Biochem 150 (1985) 76-85
47. Staley K.J. Wrong-way chloride transport: is it a treatable cause of some intractable seizures?. Epilepsy Curr 6 (2006) 124-127
48. Thom M. Recent advances in the neuropathology of focal lesions in epilepsy. Expert Rev Neurother 4 (2004) 973-984
49. van Veelen C.W., Debets R.M., van Huffelen A.C., van Emde Boas W., Binnie C.D., Storm van Leeuwen W., Velis D.N., and van Dieren A. Combined use of subdural and intracerebral electrodes in preoperative evaluation of epilepsy. Neurosurgery 26 (1990) 93-101
50. Williams J.R., Sharp J.W., Kumari V.G., Wilson M., and Payne J.A. The neuron-specific K-Cl cotransporter, KCC2. Antibody development and initial characterization of the protein. J Biol Chem 274 (1999) 12656-12664
51. Yamada J., Okabe A., Toyoda H., Kilb W., Luhmann H.J., and Fukuda A. Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J Physiol 557 (2004) 829-841
52. Yan Y., Dempsey R.J., and Sun D. Expression of Na(+)-K(+)-Cl(-) cotransporter in rat brain during development and its localization in mature astrocytes. Brain Res 911 (2001) 43-55