Sex-specific KCC2 expression and GABAA receptor function in rat substantia nigra

Experimental Neurology

Volumn 183, Issue 2, 2003, Pages 628-637

  Galanopoulou, Aristea S ^a   Kyrozis, Andreas ^a   Claudio, Olga I ^a   Stanton, Patric K ^a   Moshé, Solomon L ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Calcium; Epilepsy; GABAA receptors; KCC2; Muscimol; Nifedipine; Potassium chloride cotransporter; Substantia nigra pars reticulata

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CALCIUM CHANNEL L TYPE; CALCIUM ION; COTRANSPORTER; FURA 2; GRAMICIDIN; MESSENGER RNA; MUSCIMOL; NIFEDIPINE; POTASSIUM CHLORIDE COTRANSPORTER; UNCLASSIFIED DRUG;

AGE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CALCIUM CELL LEVEL; CONTROLLED STUDY; CORRELATION ANALYSIS; DEPOLARIZATION; DOWN REGULATION; FEMALE; GENE EXPRESSION; HYPERPOLARIZATION; IN SITU HYBRIDIZATION; MALE; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PATCH CLAMP; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SEX DIFFERENCE; SUBSTANTIA NIGRA;

EID: 0141783825     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4886(03)00213-9     Document Type: Article

References (59)

1. Akaike N. Glycine responses in rat CNS neurons studied with gramicidin perforated patch recording. Jpn. J. Physiol. 44:1994;S113-S118.
2. Arnt J., Scheel-Kruger J. Behavioral differences induced by muscimol selectively injected into pars compacta and pars reticulata of Substantia nigra. Naunyn. Schmiedebergs Arch Pharmacol. 310:1979;43-51.
3. Barbin G., Pollard H., Gaiarsa J.L., Ben-Ari Y. Involvement of GABAA receptors in the outgrowth of cultured hippocampal neurons. Neurosci. Lett. 152:1993;150-154.
4. Ben-Ari Y. Excitatory actions of gaba during development the nature of the nurture . Nat. Rev. Neurosci. 3:2002;728-739.
5. Ben-Ari Y., Cherubini E., Corradetti R., Gaiarsa J.L. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J. Physiol. 416:1989;303-325.
6. Bonnet U., Bingmann D. GABAA-responses of CA3 neurones contribution of bicarbonate and of Cl(-)-extrusion mechanisms . Neuroreport. 6:1995;700-704.
7. Canonaco M., Tavolaro R., Facciolo R.M., Carelli A., Cagnin M., Cristaldi M. Sexual dimorphism of GABAA receptor levels in subcortical brain regions of a woodland rodent (Apodemus sylvaticus). Brain Res. Bull. 40:1996;187-194.
8. Cherubini E., Rovira C., Gaiarsa J.L., Corradetti R., Ben Ari Y. GABA mediated excitation in immature rat CA3 hippocampal neurons. Int. J. Dev. Neurosci. 8:1990;481-490.
9. 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. 109:1998;281-292.
10. Collingridge G.L., Davies J. The influence of striatal stimulation and putative neurotransmitters on identified neurones in the rat substantia nigra. Brain Res. 212:1981;345-359.
11. De Sarro G., Meldrum B.S., Reavill C. Anticonvulsant action of 2-amino-7-phosphonoheptanoic acid in the substantia nigra. Eur. J. Pharmacol. 106:1984;175-179.
12. Delpire E. Cation-Chloride Cotransporters in Neuronal Communication. News Physiol. Sci. 15:2000;309-312.
13. DiChiara G., Olianas M., Del Fiacco M., Spano P.F., Tagliamonte A. Intranigral kainic acid is evidence that nigral non-dopaminergic neurones control posture. Nature. 268:1977;743-745.
14. Facciolo R.M., Alo R., Tavolaro R., Canonaco M., Franzoni M.F. Dimorphic features of the different alpha-containing GABA-A receptor subtypes in the cortico-basal ganglia system of two distantly related mammals (hedgehog and rat). Exp. Brain Res. 130:2000;309-319.
15. Flugge G., Wuttke W., Fuchs E. Postnatal development of transmitter systems sexual differentiation of the GABAergic system and effects of muscimol . Int. J. Dev. Neurosci. 4:1986;319-326.
16. Furuta I., Yamada H., Sakuragi N., Fujimoto S. A sensitive, nonradioactive method for the detection of a low level of apoptosis in rat ovary and human placenta. Technical note. Gynecol. Obstet. Invest. 48:1999;259-262.
17. Galanopoulou A.S., Moshe S.L. Gonadal hormones regulate KCC2 expression in rat substantia nigra reticulata. Epilepsia. 43:(Suppl. 7):2002;144.
18. Gale K. Mechanisms of seizure control mediated by gamma-aminobutyric acid role of the substantia nigra . Fed. Proc. 44:1985;2414-2424.
19. Ganguly K., Schinder A.F., Wong S.T., Poo M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell. 105:2001;521-532.
20. Garant D.S., Gale K. Lesions of substantia nigra protect against experimentally induced seizures. Brain Res. 273:1983;156-161.
21. Gonzalez-Hernandez T., Rodriguez M. Compartmental organization and chemical profile of dopaminergic and GABAergic neurons in the substantia nigra of the rat. J. Comp. Neurol. 421:2000;107-135.
22. Grynkiewicz G., Poenie M., Tsien R.Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260:1985;3440-3450.
23. Hubner C.A., Stein V., Hermans-Borgmeyer I., Meyer T., Ballanyi K., Jentsch T.J. Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron. 30:2001;515-524.
24. Iadarola M.J., Gale K. Substantia nigra, site of anticonvulsant activity mediated by gamma-aminobutyric acid. Science. 218:1982;1237-1240.
25. Ikeda Y., Nishiyama N., Saito H., Katsuki H. Furosemide-sensitive calcium rise induced by GABAA-receptor stimulation in cultures of embryonic rat striatal neurons. Jpn. J. Pharmacol. 74:1997;165-169.
26. Kang J., Nedergaard M. Calcium imaging of identified astrocytes in hippocampal slices. Yuste R., Lanni F., Konnerth A. Imaging neurons a laboratory manual . 2000;42.1-42.11 Cold Spring Harbor Laboratory Press, New York.
27. Karadsheh M.F., Delpire E. Neuronal restrictive silencing element is found in the KCC2 gene molecular basis for KCC2-specific expression in neurons . J. Neurophysiol. 85:2001;995-997.
28. Kyrozis A., Reichling D.B. Perforated-patch recording with gramicidin avoids artifactual changes in intracellular chloride concentration. J Neurosci. Methods. 57:1995;27-35.
29. Manev H., Pericic D. Sex difference in the turnover of GABA in the rat substantia nigra. J. Neural. Transm. 70:1987;321-328.
30. McNamara J.O., Galloway M.T., Rigsbee L.C., Shin C. Evidence implicating substantia nigra in regulation of kindled seizure threshold. J. Neurosci. 4:1984;2410-2417.
31. Mikawa S., Wang C., Shu F., Wang T., Fukuda A., Sato K. Developmental changes in KCC1, KCC2 and NKCC1 mRNAs in the rat cerebellum. Brain Res. Dev. Brain Res. 136:2002;93-100.
32. Mitchell C.K., Redburn D.A. GABA and GABA-A receptors are maximally expressed in association with cone synaptogenesis in neonatal rabbit retina. Brain Res. Dev. Brain Res. 95:1996;63-71.
33. Moshé S.L., Sperber E.F. Substantia-nigra mediated control of generalized seizures. Gloor G., Kostopoulos R., Naquet M., Avoli M. Generalized epilepsy cellular, molecular and pharmacological approaches . 1990;355-367 Birkhauser Inc, Boston.
34. Murphy T.H., Worley P.F., Baraban J.M. L-type voltage-sensitive calcium channels mediate synaptic activation of immediate early genes. Neuron. 7:1991;625-635.
35. Myers V.B., Haydon D.A. Ion transfer across lipid membranes in the presence of gramicidin A. II. The ion selectivity. Biochim. Biophys. Acta. 274:1972;313-322.
36. Neri T.M., Carnevali L., Orlandini G., Gatti R., Scandroglio R., Savi M., Allegri L. Fluorescent in situ hybridisation on tissue sections a quantitative approach with confocal laser scanning microscopy . Eur. J. Histochem. 44:2000;193-198.
37. Obata K. Excitatory and trophic action of GABA and related substances in newborn mice and organotypic cerebellar culture. Dev. Neurosci. 19:1997;117-119.
38. 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. 16:1996;6414-6423.
39. Owens D.F., Kriegstein A.R. Is there more to GABA than synaptic inhibition. Nat. Rev. Neurosci. 3:2002;715-727.
40. Parent A., Hazrati L.N. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res. Brain Res. Rev. 20:1995;91-127.
41. Payne J.A. Functional characterization of the neuronal-specific K-Cl cotransporter implications for [K+]o regulation . Am. J. Physiol. 273:1997;C1516-1525.
42. Payne J.A., Stevenson T.J., Donaldson L.F. Molecular characterization of a putative K-Cl cotransporter in rat brain. A neuronal-specific isoform. J. Biol. Chem. 271:1996;16245-16252.
43. Ravizza T., Galanopoulou A.S., Veliskova J., Moshe S.L. Sex differences in androgen and estrogen receptor expression in rat substantia nigra during development an immunohistochemical study . Neuroscience. 115:2002;685-696.
44. Reichling D.B., Kyrozis A., Wang J., MacDermott A.B. Mechanisms of GABA and glycine depolarization-induced calcium transients in rat dorsal horn neurons. J. Physiol. 476:1994;411-421.
45. Rice M.E. Use of ascorbate in the preparation and maintenance of brain slices. Methods. 18:1999;144-149.
46. Richards C.D., Shiroyama T., Kitai S.T. Electrophysiological and immunocytochemical characterization of GABA and dopamine neurons in the substantia nigra of the rat. Neuroscience. 80:1997;545-557.
47. Rick C.E., Lacey M.G. Rat substantia nigra pars reticulata neurones are tonically inhibited via GABAA, but not GABAB, receptors in vitro. Brain Res. 659:1994;133-137.
48. Rivera C., Voipio J., Payne J.A., Ruusuvuori E., Lahtinen H., Lamsa K., Pirvola U., Saarma M., Kaila K. The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature. 397:1999;251-255.
49. Robbins E., Baldino F. Jr., Roberts-Lewis J.M., Meyer S.L., Grega D., Lewis M.E. Quantitative non-radioactive in situ hybridization of preproenkephalin mRNA with digoxigenin-labeled cRNA probes. Anat. Rec. 231:1991;559-562.
50. Rochelle P.A., Ferguson D.M., Johnson A.M., De Leon R. Quantitation of Cryptosporidium parvum infection in cell culture using a colorimetric in situ hybridization assay. J. Eukaryot. Microbiol. 48:2001;565-574.
51. Russell J.M. Sodium-potassium-chloride cotransport. Physiol. Rev. 80:2000;211-276.
52. Schaeren-Wiemers N., Gerfin-Moser A. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells in situ hybridization using digoxigenin-labelled cRNA probes . Histochemistry. 100:1993;431-440.
53. Sperber E.F., Wurpel J.N., Zhao D.Y., Moshe S.L. Evidence for the involvement of nigral GABAA receptors in seizures of adult rats. Brain Res. 480:1989;378-382.
54. Staley K.J., Soldo B.L., Proctor W.R. Ionic mechanisms of neuronal excitation by inhibitory GABAA receptors. Science. 269:1995;977-981.
55. Takahashi A., Camacho P., Lechleiter J.D., Herman B. Measurement of intracellular calcium. Physiol. Rev. 79:1999;1089-1125.
56. Veliskova J., Kubova H., Friedman L.K., Wu R., Sperber E.F., Zukin R.S., Moshe S.L. The expression of GABA(A) receptor subunits in the substantia nigra is developmentally regulated and region-specific. Ital. J. Neurol. Sci. 19:1998;205-210.
57. Veliskova J., Moshe S.L. Sexual dimorphism and developmental regulation of substantia nigra function. Ann. Neurol. 50:2001;596-601.
58. Wang C., Shimizu-Okabe C., Watanabe K., Okabe A., Matsuzaki H., Ogawa T., Mori N., Fukuda A., Sato K. Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain. Brain Res. Dev. Brain Res. 139:2002;59-66.
59. Woo N.S., Lu J., England R., McClellan R., Dufour S., Mount D.B., Deutch A.Y., Lovinger D.M., Delpire E. Hyperexcitability and epilepsy associated with disruption of the mouse neuronal-specific K-Cl cotransporter gene. Hippocampus. 12:2002;258-268.