Expression of plasma membrane GABA transporters but not of the vesicular GABA transporter in dentate granule cells after kainic acid seizures

Hippocampus

Volumn 13, Issue 7, 2003, Pages 806-815

  Sperk, Günther ^a   Schwarzer, Christoph ^a   Heilman, Jutta ^a   Furtinger, Sabine ^a   Reimer, Richard J ^b   Edwards, Robert H ^b   Nelson, Nathan ^c  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

Epilepsy; GABA transaminase; Kainic acid; Mossy fibers; Plasticity

Indexed keywords

4 AMINOBUTYRATE AMINOTRANSFERASE; 4 AMINOBUTYRIC ACID; AMINO ACID TRANSPORTER; GLUTAMATE DECARBOXYLASE; KAINIC ACID; MESSENGER RNA;

4 AMINOBUTYRIC ACID RELEASE; AMINO ACID BRAIN LEVEL; ANIMAL CELL; ARTICLE; CELL MEMBRANE TRANSPORT; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOPLASM VESICLE; DENTATE GYRUS; EPILEPTIC STATE; GENE EXPRESSION; GRANULE CELL; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; MALE; NERVE CELL STIMULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; SEIZURE;

ANIMALS; CARRIER PROTEINS; CELL MEMBRANE; DENTATE GYRUS; DISEASE MODELS, ANIMAL; EPILEPSY; EPILEPSY, TEMPORAL LOBE; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; ISOENZYMES; KAINIC ACID; MALE; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MOSSY FIBERS, HIPPOCAMPAL; NEURONS; ORGANIC ANION TRANSPORTERS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; UP-REGULATION;

EID: 0242624593     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/hipo.10133     Document Type: Article

References (52)

1. Attwell D, Barbour B, Szatkowski M. 1993. Nonvesicular release of neurotransmitter. Neuron 11:401-407.
2. Bellocchio EE, Reimer RJ, Fremeau RT Jr, Edwards RH. 2000. Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289:957-960.
3. Bowery NG. 1990. GABA transporter protein cloned from rat brain. Trends Pharmacol Sci 11:435-437.
4. Cao Y, Wilcox KS, Martin CE, Rachinsky TL, Eberwine J, Dichter MA. 1996. Presence of mRNA for glutamic acid decarboxylase in both excitatory and inhibitory neurons. Proc Natl Acad Sci U S A 93:9844-9849.
5. Chaudhry FA, Reimer RJ, Bellocchio EE, Danbolt NC, Osen KK, Edwards RH, Storm-Mathisen J. 1998. The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci 18:9733-9750.
6. Clark JA, Deutch AY, Gallipoli PZ, Amara SG. 1992. Functional expression and CNS distribution of a beta-alanine-sensitive neuronal GABA transporter. Neuron 9:337-348.
7. During MJ, Spencer DD. 1993. Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 341:1607-1610.
8. During MJ, Ryder KM, Spencer DD. 1995. Hippocampal GABA transporter function in temporal-lobe epilepsy. Nature 376:174-177.
9. Durkin MM, Smith KE, Borden LA, Weinshank RL, Branchek TA, Gustafson EL. 1995. Localization of messenger RNAs encoding three GABA transporters in rat brain: an in situ hybridization study. Brain Res Mol Brain Res 33:7-21.
10. Erlander MG, Tillakaratne NJ, Feldblum S, Patel N, Tobin AJ. 1991. Two genes encode distinct glutamate decarboxylases. Neuron 7:91-100.
11. Esclapez M, Houser CR. 1999. Up-regulation of GAD65 and GAD67 in remaining hippocampal GABA neurons in a model of temporal lobe epilepsy. J Comp Neurol 412:488-505.
12. Featherstone DE, Rushton EM, Hilderbrand-Chae M, Phillips AM, Jackson FR, Broadie K. 2000. Presynaptic glutamic acid decarboxylase is required for induction of the postsynaptic receptor field at a glutamatergic synapse. Neuron 27:71-84.
13. Frahm C, Engel D, Piechotta A, Heinemann U, Draguhn A. 2000. Presence of gamma-aminobutyric acid transporter mRNA in interneurons and principal cells of rat hippocampus. Neurosci Lett 288:175-178.
14. Freund T, Buzsaki G. 1996. Interneurons of the hippocampus. Hippocampus 6:347-470.
15. Fykse EM, Iversen EG, Fonnum F. 1992. Inhibition of L-glutamate uptake into synaptic vesicles. Neurosci Lett 135:125-128.
16. Guastella J, Nelson N, Nelson H, Czyzyk L, Keynan S, Miedel MC, Davidson N, Lester HA, Kanner BI. 1990. Cloning and expression of a rat brain GABA transporter. Science 249:1303-1306.
17. Gutierrez R. 2000. Seizures induce simultaneous GABAergic and glutamatergic transmission in the dentate gyrus-CA3 system. J Neurophysiol 84:3088-3090.
18. Gutierrez R, Heinemann U. 2001. Kindling induces transient fast inhibition in the dentate gyrus - CA3 projection. Eur J Neurosci 13:1371-1379.
19. Hirao T, Morimoto K, Yamamoto Y, Watanabe T, Sato H, Sato K, Sato S, Yamada N, Tanaka K, Suwaki H. 1998. Time-dependent and regional expression of GABA transporter mRNAs following amygdalakindled seizures in rats. Brain Res Mol Brain Res 54:49-55.
20. Houser CR, Esclapez M. 1994. Localization of mRNAs encoding two forms of glutamic acid decarboxylase in the rat hippocampal formation. Hippocampus 4:530-545.
21. Julien JF, Legay F, Dumas S, Tappaz M, Mallet J. 1987. Molecular cloning, expression and in situ hybridization of rat brain glutamic acid decarboxylase messenger RNA. Neurosci Lett 73:173-180.
22. Jursky F, Nelson N. 1996. Developmental expression of GABA transporters GAT1 and GAT4 suggests involvement in brain maturation. J Neurochem 67:857-867.
23. Kontani Y, Sakata SF, Matsuda K, Ohyama T, Sano K, Tamaki N. 1999. The mature size of rat 4-aminobutyrate aminotransferase is different in liver and brain. Eur J Biochem 264:218-222.
24. Lamas M, Gomez-Lira G, Gutierrez R. 2001. Vesicular GABA transporter mRNA expression in the dentate gyrus and in mossy fiber synaptosomes. Brain Res Mol Brain Res 93:209-214.
25. Lehmann H, Ebert U, Loscher W. 1996. Immunocytochemical localization of GABA immunoreactivity in dentate granule cells of normal and kindled rats. Neurosci Lett 212:41-44.
26. Liu QR, Mandiyan S, Nelson H, Nelson N. 1992. A family of genes encoding neurotransmitter transporters. Proc Natl Acad Sci U S A 89:6639-6643.
27. Marksteiner J, Wahler R, Bellmann R, Ortler M, Krause JE, Sperk G. 1992. Limbic seizures cause pronounced changes in the expression of neurokinin B in the hippocampus of the rat. Neuroscience 49:383-395.
28. Mathern GW, Mendoza D, Lozada A, Pretorius JK, Dehnes Y, Danbolt NC, Nelson N, Leite JP, Chimelli L, Born DE, Sakamoto AC, Assirati JA, Fried I, Peacock WJ, Ojemann GA, Adelson PD. 1999. Hippocampal GABA and glutamate transporter immunoreactivity in patients with temporal lobe epilepsy. Neurology 52:453-472.
29. McGinty JF, Henriksen SJ, Goldstein A, Terenius L, Bloom FE. 1983. Dynorphin is contained within hippocampal mossy fibers: immunochemical alterations after kainic acid administration and colchicine-induced neurotoxicity. Proc Natl Acad Sci U S A 80:589-593.
30. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM. 1997. Identification and characterization of the vesicular GABA transporter. Nature 389:870-876.
31. Orozco-Suarez S, Brunson K, Feria-Velasco A, Ribak CE. 2000. Increased expression of gamma-aminobutyric acid transporter-1 in the forebrain of infant rats with corticotropin-releasing hormone-induced seizures but not in those with hyperthermia-induced seizures. Epilepsy Res 4:141-157.
32. Palmiter RD, Cole TB, Quaife CJ, Findley SD. 1996. ZnT-3, a putative transporter of zinc into synaptic vesicles. Proc Natl Acad Sci U S A 93:14934-14939.
33. Patrylo PR, Spencer DD, Williamson A. 2001. GABA uptake and heterotransport are impaired in the dentate gyrus of epileptic rats and humans with temporal lobe sclerosis. J Neurophysiol 85:1533-1542.
34. Ribak CE, Tong WM, Brecha NC. 1996. GABA plasma membrane transporters, GAT-1 and GAT-3, display different distributions in the rat hippocampus. J Comp Neurol 367:595-606.
35. Sandler R, Smith AD. 1991. Coexistence of GABA and glutamate in mossy fiber terminals of the primate hippocampus: an ultrastructural study. J Comp Neurol 303:177-192.
36. Schwarzer C, Sperk G. 1995. Hippocampal granule cells express glutamic acid decarboxylase-67 after limbic seizures in the rat. Neuroscience 69:705-709.
37. Schwarzer C, Marksteiner J, Kroesen S, Kohl C, Sperk G, Winkler H. 1997a. Secretoneurin: a marker in rat hippocampal pathways. J Comp Neurol 377:29-40.
38. A receptor subunits in the rat hippocampus II: altered distribution in kainic acid-induced temporal lobe epilepsy. Neuroscience 80:1001-1017.
39. Sloviter RS, Nilaver G. 1987. Immunocytochemical localization of GABA-, cholecystokinin-, vasoactive intestinal polypeptide-, and somatostatin-like immunoreactivity in the area dentata and hippocampus of the rat. J Comp Neurol 256:42-60.
40. Sloviter RS, Dichter MA, Rachinsky TL, Dean E, Goodman JH, Sollas AL, Martin DL. 1996. Basal expression and induction of glutamate decarboxylase and GABA in excitatory granule cells of the rat and monkey hippocampal dentate gyrus. J Comp Neurol 373:593-618.
41. A receptor subunits in the rat hippocampus I: immunocytochemical distribution of 13 subunits. Neuroscience 80:987-1000.
42. Sperk G, Lassmann H, Baran H, Kish SJ, Seitelberger F, Hornykiewicz O. 1983. Kainic acid induced seizures: neurochemical and histopathological changes. Neuroscience 10:1301-1315.
43. Sperk G, Marksteiner J, Gruber B, Bellmann R, Mahata M, Ortler M. 1992. Functional changes in neuropeptide Y- and somatostatin-containing neurons induced by limbic seizures in the rat. Neuroscience 50:831-846.
44. Sternberger L. 1979. Immunohistochemistry. 2nd ed. New York: John Wiley & Sons.
45. Storm-Mathisen J, Leknes AK, Bore AT, Vaaland JL, Edminson P, Haug FM, Ottersen OP. 1983. First visualization of glutamate and GABA in neurones by immunocytochemistry. Nature 301:517-520.
46. Szabo G, Kartarova Z, Hoertnagl B, Somogyi R, Sperk G. 2000. Differential regulation of adult and embryonic glutamate decarboxylases in rat dentate granule cells after kainate-induced limbic seizures. Neuroscience 100:287-295.
47. Takamori S, Rhee JS, Rosenmund C, Jahn R. 2000. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407:189-194.
48. Ueda Y, Willmore LJ. 2000. Hippocampal gamma-aminobutyric acid transporter alterations following focal epileptogenesis induced in rat amygdala. Brain Res Bull 52:357-361.
49. Walker MC, Ruiz A, Kullmann DM. 2001. Monosynaptic GABAergic signaling from dentate to CA3 with a pharmacological and physiological profile typical of mossy fiber synapses. Neuron 29:703-715.
50. Weiler R, Marksteiner J, Bellmann R, Wohlfarter T, Schober M, Fischer-Colbrie R, Sperk G, Winkler H. 1990. Chromogranins in rat brain: characterization, topographical distribution and regulation of synthesis. Brain Res 532:87-94.
51. Williamson A, Telfeian AR, Spencer DD. 1995. Prolonged GABA responses in dentate granule cells in slices isolated from patients with temporal lobe sclerosis. J Neurophysiol 74:378-387.
52. Wu Y, Wang W, Richerson GB. 2001. GABA transaminase inhibition induces spontaneous and enhances depolarization-evoked GABA efflux via reversal of the GABA transporter. J Neurosci 21:2630-2639.