Developmental expression of glutamate transporters and glutamate dehydrogenase in astrocytes of the postnatal rat hippocampus

Hippocampus

Volumn 14, Issue 8, 2004, Pages 975-985

  Kugler, Peter ^a   Schleyer, Verena ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

GDH activity; GLAST; GLT1; Immunocytochemistry; In situ hybridization

Indexed keywords

GLUTAMATE DEHYDROGENASE; GLUTAMATE TRANSPORTER;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; GLIA CELL; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAT; STATISTICAL ANALYSIS; STATISTICAL SIGNIFICANCE;

AGING; AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELL DIFFERENTIATION; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUTAMATE DEHYDROGENASE; GLUTAMATE PLASMA MEMBRANE TRANSPORT PROTEINS; GLUTAMIC ACID; HIPPOCAMPUS; MALE; RATS; RATS, WISTAR; RNA, MESSENGER; SYMPORTERS; SYNAPSES; SYNAPTIC TRANSMISSION; UP-REGULATION;

EID: 11344253878     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/hipo.20015     Document Type: Article

References (57)

1. Amaral DG, Dent JA. 1981. Development of the mossy fibers of the dentate gyrus. I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 195:51-86.
2. Asau E, Kugler P. 1995. Qualitative and quantitative detection of alkaline phosphatase coupled to an oligonucleotide probe for somatostatin mRNA after in situ hybridization using unfixed rat brain tissue. Histochem Cell Biol 103:463-471.
3. Bar-Peled O, Ben-Hur H, Biegon A, Groner Y, Dewhurst S, Furuta A, Rothstein JD. 1997. Distribution of glutamate transporter subtypes during human brain development. J Neurochem. 69:2571-2580.
4. Berger UV, Hediger MA. 1998. Comparative analysis of glutamate transporter expression in rat brain using differential double in situ hybridization. Anat Embryol 198:13-30.
5. Bignami A, Eng LF, Dahl D, Uyeda CT. 1972. Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res 43:429-435.
6. Brooks-Kayal AR, Munir M, Jin H, Robinson MB. 1998. The glutamate transporter, GLT-1, is expressed in cultured hippocampal neurons. Neurochem Int 33:95-100.
7. Burnette WN. 1981. Western blotting: electrophoretic transfer of proteins from sodium dodecyl sulfate polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radionated protein A. Anal Biochem 112:195-203.
8. Butcher RG. 1978. The measurement in tissue sections of the two formazans derived from nitroblue tetrazolium in dehydrogenase reactions. Histochem J 10:739-744.
9. Chaudhry FA, Lehre KP, van Lookeren Campagne M, Ottersen OP, Danbolt NC, Storm-Mathisen J. 1995. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15:711-720.
10. Christensen H, Fonnum F. 1992. The ontogeny of the uptake systems for glutamate, GABA, and glycine in synaptic vesicles isolated from rat brain. Neurochem Res 17:457-462.
11. Danbolt NC. 2001. Glutamate uptake. Prog Neurobiol 65:1-105.
12. Diabira D, Hennou S, Chevassus-au-Louis N, Ben-Ari Y, Gozlan H. 1999. Late embryonic expression of AMPA receptor function in the CA1 region of the intact hippocampus in vitro. Eur J Neurosci 11: 4015-4023.
13. Friedman HV, Bresler T, Garner CC, Ziv NE. 2000. Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27:57-69.
14. Frotscher M, Kugler P, Misgeld U, Zilles K. 1988. Neurotransmission in the hippocampus. Adv Anat Embryol Cell Biol 111:1-103.
15. Furuta A, Rothstein JD, Martin LJ. 1997. Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J Neurosci 17:8363-8375.
16. Gaarskjaer FB. 1986. The organization and development of the hippocampal mossy fiber system. Brain Res Rev 11:335-357.
17. Gasparini S, Saviane C, Voronin LL, Cherubini E. 2000. Silent synapses in the developing hippocampus: lack of functional AMPA receptors or low probability of glutamate release? Proc Natl Acad Sci USA 97: 9741-9746.
18. Groc L, Gustafsson B, Hanse E. 2002. Spontaneous unitary synaptic activity in CA1 pyramidal neurons during early postnatal development: constant contribution of AMPA and NMDA receptors. J Neurosci 22:5552-5562.
19. Hein C, Horvath E, Kugler P. 2001. Glutamate transporter expression in astrocytes of the rat dentate gyrus following lesion of the entorhinal cortex. Eur J Neurosci 13:1839-1848.
20. Hsia AY, Malenka RC, Nicoll RA. 1998. Development of excitatory circuitry in the hippocampus. J Neurophysiol 79:2013-2024.
21. Kugler P. 1988. Quantitative enzyme histochemistry in the brain. Histochemistry 90:99-107.
22. Kugler P. 1990. Microphotometric determination of enzymes in brain sections. III. Glutamate dehydrogenase. Histochemistry 93:537-540.
23. Kugler P. 1993. Enzymes involved in glutamatergic and GABAergic neurotransmission. Int Rev Cytol 147:285-336.
24. Kugler P, Beyer A. 2003. Expression of glutamate transporters in human and rat retina and rat optic nerve. Histochem Cell Biol 120:199-212.
25. Kugler P, Schmitt A. 1999. The glutamate transporter EAAC1 is expressed in neurons and glial cells in the rat nervous system. Glia 27: 129-142.
26. Kugler P, Schmitt A. 2003. Complementary neuronal and glial expression of two high-affinity glutamate transporter GLT1/EAAT2 forms in rat cerebral cortex. Histochem Cell Biol 119:425-435.
27. Kugler P, Vogel S, Gehm M. 1988. Quantitative succinate dehydrogenase histochemistry in the hippocampus of aged rats. Histochemistry 88: 299-307.
28. Kugler P, Weeger T, Horvath E. 1995. Glutamate dehydrogenase in astrocytes of the rat dentate gyrus following lesion of the entorhinal cortex. Neuroscience 64:173-182.
29. Lehre KP, Levy LM, Ottersen OP, Storm-Mathisen J, Danbolt NC. 1995. Differential expression of two glial glutamate transporters in the rat brain quantitative and immunocytochemical observations. J Neurosci 15:1835-1853.
30. Loy R. 1980. Development of afferent lamination in Ammon's horn of the rat. Anat Embryol 159:257-275.
31. Lüthi A, Schwyzer L, Mateos JM, Gähwiler BH, McKinney RA. 2001. NMDA receptor activation limits the number of synaptic connections during hippocampal development. Nat Neurosci 4:1102-1107.
32. Martin LJ, Brambrink AM, Lehmann C, Portera-Cailliau C, Koehler R, Rothstein J, Traystman RJ. 1997. Hypoxia-ischemia causes abnormalities in glutamate transporters and death of astroglia and neurons in newborn striatum. Ann Neurol 42:335-348.
33. Matthias K, Kirchhoff F, Seifert G, Hüttmann K, Matyash M, Kettemann H, Steinhäuser C. 2003. Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J Neurosci 23:1750-1758.
34. Mattson MP, Lee RE, Adams ME, Guthrie PB, Kater SB. 1988. Interactions between entorhinal axons and target hippocampal neurons: a role for glutamate in the development of hippocampal circuitry. Neuron 1:865-876.
35. Mayor HD, Hampton JC, Rosario B. 1961. A simple method for removing the resin from epoxy-embedded tissue. J Biophys Biochem Cytol 9:909-910.
36. Mennerick S, Dhond RP, Benz A, Xu W, Rothstein JD, Danbolt NC, Isenberg KE, Zorumski CF. 1998. Neuronal expression of the glutamate transporter GLT-1 in hippocampal microcultures. J Neurosci 18:4490-4499.
37. Minelli A, Edwards RH, Manzoni T, Conti F. 2003. Postnatal development of the glutamate vesicular transporter VGLUT1 in rat cerebral cortex. Brain Res Dev Brain Res 16:309-314.
38. Northington FJ, Traystman RJ, Koehler RC, Martin LJ. 1999. GLT1, glial glutamate transporter, is transiently expressed in neurons and develops astrocyte specificity only after midgestation in the ovine fetal brain. J Neurobiol 39:515-26.
39. Plachez C, Danbolt NC, Recasens M. 2000. Transient expression of the glial glutamate transporters GLAST and GLT in hippocampal neurons in primary culture. J Neurosci Res 59:587-593.
40. Renger JJ, Egles C, Liu G. 2001. A developmental switch in neurotransmitter flux enhances synaptic efficacy by affecting AMPA receptor activation. Neuron 29:469-484.
41. Rothe F, Schmidt W, Wolf G. 1983. Postnatal changes in the activity of glutamate dehydrogenase and aspartate aminotransferase in the rat nervous system with special reference to the glutamate transmitter metabolism. Brain Res 313:67-74.
42. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning. A laboratory manual. 2nd ed. Cold Spring Harbor, NY. CSH Cold Spring Harbor Laboratory Press.
43. Schmitt A, Kugler P. 1999. Cellular and regional expression of glutamate dehydrogenase in the rat nervous system: non-radioactive in situ hybridization and comparative immunocytochemistry. Neuroscience 92: 293-308.
44. Schmitt A, Asan E, Püschel B, Jöns T, Kugler P. 1996. Expression of the glutamate transporter GLT1 in neural cells of the rat central nervous system: non-radioactive in situ hybridization and comparative immunocytochemistry. Neuroscience 71:989-1004.
45. Schmitt A, Asan E, Püschel B, Kugler P. 1997. Cellular and regional distribution of the glutamate transporter GLAST in the CNS of rats: nonradioactive in situ hybridization and comparative immunocytochemistry. J Neurosci 17:1-10.
46. Schmitt A, Asan E, Lesch KP, Kugler P. 2002. A splice variant of glutamate transporter GLT1/EAAT2 expressed in neurons: cloning and localization in rat nervous system. Neuroscience 109:45-61.
47. Shibata T, Watanabe M, Tanaka K, Wada K, Inoue Y. 1996. Dynamic changes in expression of glutamate transporter mRNAs in developing brain. NeuroReport 7:705-709.
48. Stanfield BB, Cowan WM. 1988. The development of the hippocampal region. In: Peters A, Jones EG, editors. Cerebral cortex. Vol VII. Development and maturation of cerebral cortex. New York: Plenum. p 91-122.
49. Sternberger LA, Hardy PH, Cuculis J, Meyer HG. 1990. The unlabelled antibody method of immunohistochemistry: preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-anti-horseradish peroxidase) and its use in identification of spirochaetes. J Histochem Cytochem 18:315-333.
50. Storm-Mathisen J, Ottersen OP. 1984. Neurotransmitters in the hippocampal formation. In: Reinoso-Suárez F, Ajmone-Marsan C, editors. Cortical integration. New York: Raven. p 105-130.
51. Sutherland ML, Delaney TA, Noebels JL. 1996. Glutamate transporter mRNA expression in proliferative zones of the developing and adult murine CNS. J Neurosci 16:2191-21207.
52. Tamamaki N. 1999. Development of afferent fiber lamination in the infrapyramidal blade of the rat dentate gyrus. J Comp Neurol 4111: 257-266.
53. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, Iwama H, Nishikawa T, Ichihara N, Kikuchi T, Okuyama S, Kawashima N, Hori S, Takimoto M, Wada K. 1997. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276:1699-1702.
54. Torp R, Danbolt NC, Babaie E, Bjørås M, Seeberg E, Storm-Mathisen J, Ottersen OP. 1994. Differential expression of two glial glutamate transporters in the rat brain: an in situ hybridization study. Eur J Neurosci 6:936-942.
55. Ullensvang K, Lehre KP, Storm-Mathisen J, Danbolt NC. 1997. Differential developmental expression of the two rat brain glutamate transporter proteins GLAST and GLT. Eur J Neurosci 9:1646-1655.
56. Voutsinos-Porche B, Bonvento G, Tanaka K, Steiner P, Welker E, Chatton JY, Magistretti PJ, Pellerin L. 2003. Glial glutamate transporters mediate a functional metabolic crosstalk between neurons and astrocytes in the mouse developing cortex. Neuron 37:275-286.
57. Yamada K, Watanabe M, Shibata T, Nagashima M, Tanaka K, Inoue Y. 1998. Glutamate transporter GLT-1 is transiently localized on growing axons of the mouse spinal cord before establishing astrocytic expression. J Neurosci 18:5706-5713.