GluR- and TrkB-mediated maturation of GABAA receptor function during the period of eye opening

European Journal of Neuroscience

Volumn 21, Issue 2, 2005, Pages 431-440

  Henneberger, Christian ^a   Jüttner, René ^a,b   Schmidt, Sonja A ^a   Walter, Jan ^a   Meier, Jochen C ^a   Rothe, Thomas ^a,c   Grantyn, Rosemarie ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

Activity dependent; BDNF; GABA; IPSC; Kinetic; NMDA; Synapse development; Visual system

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; GLUTAMATE RECEPTOR; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN TYROSINE KINASE; RECEPTOR SUBUNIT; UNCLASSIFIED DRUG; ZOLPIDEM;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; GABAERGIC SYSTEM; INHIBITORY POSTSYNAPTIC POTENTIAL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR INTRINSIC ACTIVITY; SIGNAL TRANSDUCTION; SUPERIOR COLLICULUS; SYNAPTOGENESIS; VISUAL SYSTEM;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BLOTTING, NORTHERN; BRAIN-DERIVED NEUROTROPHIC FACTOR; DIZOCILPINE MALEATE; EMBRYO; EYE; GABA AGONISTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, KNOCKOUT; N-METHYLASPARTATE; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; PYRIDINES; RATS; RATS, WISTAR; RECEPTOR, TRKB; RECEPTORS, GABA-A; RECEPTORS, GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SUPERIOR COLLICULUS; SYNAPSES; SYNAPTIC TRANSMISSION; VALINE;

EID: 13444256338     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.03869.x     Document Type: Article

References (65)

1. Aamodt, S.M., Shi, J., Colonnese, M.T., Veras, W. & Constantine-Paton, M. (2000) Chronic NMDA exposure accelerates development of GABAergic inhibition in the superior colliculus. J. Neurophysiol., 83, 1580-1591.
2. A receptor subunit messenger RNAs show differential expression during cortical development in the rat brain. Neuroscience, 51, 583-591.
3. Bao, S., Chen, L., Qiao, X. & Thompson, R.F. (1999) Transgenic brain-derived neurotrophic factor modulates a developing cerebellar inhibitory synapse. Learn. Mem., 6, 276-283.
4. Ben-Ari, Y. (2001) Developing networks play a similar melody. Trends Neurosci., 24, 353-360.
5. Blanchi, M.T. & Macdonald, R.L. (2002) Slow phases of GABA (A) receptor desensitization: structural determinants and possible relevance for synaptic function. J. Physiol. (Lond.), 544, 3-18.
6. Boller, M. & Schmidt, M. (2001) Postnatal maturation of GABA (A) and GABA (C) receptor function in the mammalian superior colliculus. Eur. J. Neurosci., 14, 1185-1193.
7. Bosman, L.W., Rosahl, T.W. & Brussaard, A.B. (2002) Neonatal development of the rat visual cortex: synaptic function of GABAA receptor alpha subunits. J. Physiol. (Lond.), 545, 169-181.
8. Bozzi, Y., Pizzorusso, T., Cremisi, R, Rossi, P.M., Barsacchi, G. & Maffei, L. (1995) Monocular deprivation decreases the expression of messenger RNA for brain-derived neurotrophic factor in the rat visual cortex. Neuroscience, 69, 1133-1144.
9. Brünig, I., Penschuck, S., Berninger, B., Benson, J. & Fritschy, J.M. (2001) BDNF reduces miniature inhibitory postsynaptic currents by rapid downregulation of GABA (A) receptor surface expression. Eur. J. Neurosci., 13, 1320-1328.
10. Castrén, E., Zafra, F., Thoenen, H. & Lindholm, D. (1992) Light regulates expression of brain-derived neurotrophic factor mRNA in rat visual cortex. Proc. Natl. Acad. Sci. USA, 89, 9444-9448.
11. Chen, L., Yang, C. & Mower, G.D. (2001) Developmental changes in the expression of GABA (A) receptor subunits (alpha (1), alpha (2), alpha (3) in the cat visual cortex and the effects of dark rearing. Mol. Brain Res., 88, 135-143.
12. Cheng, Q. & Yeh, H.H. (2003) Brain-derived neurotrophic factor attenuates mouse cerebellar granule cell GABA (A) receptor-mediated responses via postsynaptic mechanisms. J. Physiol. (Lond.), 548, 711-721.
13. Contestabile, A. (2000) Roles of NMDA receptor activity and nitric oxide production in brain development. Brain Res. Rev., 32, 476-509.
14. Cork, R.J., Calhoun, T., Perrone, M. & Mize, R.R. (2000) Postnatal development of nitric oxide synthase expression in the mouse superior colliculus. J. Comp. Neurol., 427, 581-592.
15. Cull-Candy, S., Brickley, S. & Farrant, M. (2001) NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol., 11, 327-335.
16. Dunning, D.D., Hoover, C.L., Soltesz, I., Smith, M.A. & O'Dowd, D.K. (1999) GABA (A) receptor-mediated miniature postsynaptic currents and alpha-subunit expression in developing cortical neurons. J. Neurophysiol., 82, 3286-3297.
17. Facchinetti, F., Ciani, E., Dall'Olio, R., Virgili, M., Contestabile, A. & Fonnum, F. (1993) Structural, neurochemical and behavioural consequences of neonatal blockade of NMDA receptor through chronic treatment with CGP 39551 or MK-801. Dev. Brain Res., 74, 219-224.
18. A-receptor subtypes during postnatal development: an immunohistochemical study. J. Neurosci., 14, 5302-5324.
19. Frost, D.O., Ma, Y.T., Hsieh, T., Forbes, M.E. & Johnson, J.E. (2001) Developmental changes in BDNF protein levels in the hamster retina and superior colliculus. J. Neurobiol., 49, 173-187.
20. A receptor α1 subunit mRNA in the rat brain. J. Neurobiol., 21, 1169-1179.
21. A receptor gating kinetics on the α-subunit isoform: implications for structure-function relations and synaptic transmission. J. Physiol. (Lond.), 489, 529-543.
22. Grantyn, R., Jüttner, R. & Meier, J. (2004) Development and use-dependent modification of synaptic connections in the visual layers of the rodent superior colliculus. In Hall, W. C. & Moschovakis, A. (eds) The Superior Colliculus. CRC Press, Boca Raton, pp. 173-210.
23. A receptor subunits. Mol. Brain Res., 28, 338-342.
24. Heinen, K., Bosman, L.W., Spijker, S., Van Pelt, J., Smit, A.B., Voorn, P., Baker, R.E. & Brussaard, A.B. (2004) GABAA receptor maturation in relation to eye opening in the rat visual cortex. Neuroscience, 124, 161-171.
25. Henneberger, C., Jüttner, R., Rothe, T. & Grantyn, R. (2002) Postsynaptic action of BDNF on GABAergic synaptic transmission in the superficial layers of the mouse superior colliculus. J. Neurophysiol., 88, 595-603.
26. Hestrin, S. (1992) Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature, 357, 686-689.
27. Hutcheon, B., Fritschy, J.M. & Poulter, M.O. (2004) Organization of GABA receptor alpha-subunit clustering in the developing rat neocortex and hippocampus. Eur. J. Neurosci., 19, 2475-2487.
28. Hutcheon, B., Morley, P. & Poulter, M.O. (2000) Developmental change in GABAA receptor desensitization kinetics and its role in synapse function in rat cortical neurons. J. Physiol. (Lond.), 522, 3-17.
29. Jack, J.J.B., Noble, D. & Tsien, R.W. (1975) Electric Current Flow in Excitable Cells. Oxford University Press, London.
30. Jefferis, G.S., Komiyama, T. & Luo, L. (2004) Neuroscience. Calcium and CREST for healthy dendrites. Science, 303, 179-181.
31. Jones, M.V. & Westbrook, G.L. (1997) Shaping of IPSCs by endogenous calcineurin activity. J. Neurosci., 17, 7626-7633.
32. Jovanovic, J.N., Thomas, P., Kittler, J.T., Smart, T.G. & Moss, S.J. (2004) Brain-derived neurotrophic factor modulates fast synaptic inhibition by regulating GABA (A) receptor phosphorylation, activity, and cell-surface stability. J. Neurosci., 24, 522-530.
33. Jüttner, R., Meier, J. & Grantyn, R. (2001) Slow IPSC kinetics, low levels of alpha1 subunit expression and paired-pulse depression are distinct properties of neonatal inhibitory GABAergic synaptic connections in the mouse superior colliculus. Eur. J. Neurosci., 13, 2088-2098.
34. Kraszewski, K. & Grantyn, R. (1992) Development of GABAergic connections in vitro: Increasing efficacy of synaptic transmission is not accompanied by changes in miniature currents. J. Neurobiol., 23, 766-781.
35. A receptor function by protein kinase C phosphorylation. Neuron, 12, 1081-1095.
36. A receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J. Neurosci., 12, 4151-4172.
37. Matthews, D.B., Devaud, L.L., Fritschy, J.M., Sieghart, W. & Morrow, A.L. (1998) Differential regulation of GABA (A) receptor gene expression by ethanol in the rat hippocampus versus cerebral cortex. J. Neurochem., 70, 1160-1166.
38. Meier, J., Akyeli, J., Kirischuk, S. & Grantyn, R. (2003) GABA (A) receptor activity and PKC control inhibitory synaptogenesis in CNS tissue slices. Mol. Cell. Neurosci., 23, 600-613.
39. Meier, J. & Grantyn, R. (2004) Preferential accumulation of GABA (A) receptor γ2L, not γ2S cytoplasmic loops at spinal cord inhibitory synapses. J. Physiol. (Lond.), 559, 355-365.
40. Meier, J., Jüttner, R., Kirischuk, S. & Grantyn, R. (2002) Synaptic anchoring of glycine receptors in developing collicular neurons under control of metabotropic glutamate receptor activity. Mol. Cell Neurosci., 21, 324-340.
41. Memo, M., Bovolin, P., Costa, E. & Grayson, D.R. (1991) Regulation of γ-aminobutyric acidA receptor subunit expression by activation of N-methyl-D-aspartate-selective glutamate receptors. Mol. Pharmacol., 39, 599-603.
42. Mishina, M., Takai, T., Imoto, K., Noda, M., Takanishi, T., Numa, S., Methfessel, C. & Sakmann, B. (1986) Molecular distinction between fetal and adult forms of muscle acetylcholine receptor. Nature, 321, 406-411.
43. Mizoguchi, Y., Ishibashi, H. & Nabekura, J. (2003) The action of BDNF on GABAA currents changes from potentiating to suppressing during maturation of rat hippocampal CA1 pyramidal neurons. J. Physiol. (Lond.), 548, 703-709.
44. Mower, G.D. & Guo, Y. (2001) Comparison of the expression of two forms of glutamic acid decarboxylase (GAD67 and GAD65) in the visual cortex of normal and dark-reared cats. Brain Res. Dev. Brain Res., 126, 65-74.
45. O'Leary, D.D. & Terashima, T. (1988) Cortical axons branch to multiple subcortical targets by interstitial axon budding: implications for target recognition and 'waiting periods'. Neuron, 1, 901-910.
46. Okada, M., Van Onodera, K., Renterghem, C., Sieghart, W. & Takahashi, T. (2000) Functional correlation of GABA (A) receptor alpha subunits expression with the properties of IPSCs in the developing thalamus. J. Neurosci., 20, 2202-2208.
47. A receptor regulates inhibitory synaptic strength. J. Neurophysiol., 92, 1718-1727.
48. Pollock, O.S., Vernon, E., Forbes, M.E., Yan, Q., Ma, Y.T., Hsieh, T., Robichon, R., Frost, D.O. & Johnson, J.E. (2001) Effects of early visual experience and diurnal rhythms on BDNF mRNA and protein levels in the visual system, hippocampus, and cerebellum. J. Neurosci., 21, 3923-3931.
49. Poulter, M.O., Barker, J.L., O'Carroll, A.M., Lolait, S.J. & Mahan, L.C. (1993) Co-existent expression of GABAA receptor beta 2, beta 3 and gamma 2 subunit messenger RNAs during embryogenesis and early postnatal development of the rat central nervous system. Neuroscience, 53, 1019-1033.
50. Rivera, C., Voipio, J., Thomas-Crusells, J., Li, H., Emri, Z., Sipila, S., Payne, J.A., Minichiello, L., Saarma, M. & Kaila, K. (2004) Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J. Neurosci., 24, 4683-4691.
51. Roberts, A.A. & Kellogg, C.K. (2000) Synchronous postnatal increase in alpha1 and gamma2L GABA (A) receptor mRNAs and high affinity zolpidem binding across three regions of rat brain. Brain Res. Dev. Brain Res., 119, 21-32.
52. Schoepp, D.D., Jane, D.E. & Monn, J.A. (1999) Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology, 38, 1431-1476.
53. 3 subunits in embryonic rat neurons. Eur. J. Neurosci., 10, 334-349.
54. Shi, J., Aamodt, S.M. & Constantine-Paton, M. (1997) Temporal correlations between functional and molecular changes in NMDA receptors and GABA neurotransmission in the superior colliculus. J. Neurosci., 17, 6264-6276.
55. Shi, J., Townsend, M. & Constantine-Paton, M. (2000) Activity-dependent induction of tonic calcineurin activity mediates a rapid developmental downregulation of NMDA receptor currents. Neuron, 28, 103-114.
56. Takahashi, T., Momiyama, A., Hirai, K., Hishinuma, F. & Akagi, H. (1992) Functional correlation of fetal and adult forms of glycine receptors with developmental changes in inhibitory synaptic receptor channels. Neuron, 9, 1155-1161.
57. Thong, I.G. & Dreher, B. (1986) The development of the corticotectal pathway in the albino rat. Brain Res., 390, 227-238.
58. Tropea, D., Capsoni, S., Tongiorgi, E., Giannotta, S., Cattaneo, A. & Domenici, L. (2001) Mismatch between BDNF mRNA and protein expression in the developing visual cortex: the role of visual experience. Eur. J. Biochem., 13, 709-721.
59. Verdoorn, T.A. (1994) Formation of heteromeric γ-aminobutyric acid type A receptors containing two different a subunits. Mol. Pharmacol., 45, 475-480.
60. Vicini, S., Ferguson, C., Prybylowski, K., Kralic, J., Morrow, A.L. & Homanics, G.E. (2001) GABA (A) receptor alphal subunit deletion prevents developmental changes of inhibitory synaptic currents in cerebellar neurons. J. Neurosci., 21, 3009-3016.
61. Wang, X.H., Zhu, W.J., Corsi, L., Ikonomovic, S., Paljug, W.R., Vicini, S. & Grayson, D.R. (1998) Chronic dizocilpine (MK-801) reversibly delays GABA (A) receptor maturation in cerebellar granule neurons in vitro. J. Neurochem., 71, 693-704.
62. Warton, S.S. & McCart, R. (1989) Synaptogenesis in the stratum griseum superficiale of the rat superior colliculus. Synapse, 3, 136-148.
63. Warton, S.S., Perouansky, M. & Grantyn, R. (1990) Development of GABAergic synaptic connections in vivo and in cultures from the rat superior colliculus. Dev. Brain Res., 52, 95-111.
64. Zheng, T.M., Zhu, W.J., Puia, G., Vicini, S., Grayson, D.R., Costa, E. & Caruncho, H.J. (1994) Changes in gamma-aminobutyrate type A receptor subunit mRNAs, translation product expression, and receptor function during neuronal maturation in vitro. Proc. Natl. Acad. Sci. USA, 91, 10952-10956.
65. Zhu, W.J., Vicini, S., Harris, B.T. & Grayson, D.R. (1995) NMDA-mediated modulation of gamma-aminobutyric acid type A receptor function in cerebellar granule neurons. J. Neurosci., 15, 7692-7701.