Brain-derived neurotrophic factor upregulates and maintains AMPA receptor currents in neocortical GABAergic neurons

Molecular and Cellular Neuroscience

Volumn 24, Issue 2, 2003, Pages 340-356

  Nagano, T ^a   Yanagawa, Y ^b   Obata, K ^b   Narisawa Saito, M ^a   Namba, H ^a   Otsu, Y ^a   Takei, N ^a   Nawa, H ^a  

^a NIIGATA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; AMPA RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EVALUATION; EXCITATORY POSTSYNAPTIC POTENTIAL; FREQUENCY ANALYSIS; IMMUNOHISTOCHEMISTRY; MOUSE; NEOCORTEX; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; RODENT;

EID: 0142188661     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1044-7431(03)00172-6     Document Type: Article

References (66)

1. Akaneya Y., Tsumoto T., Kinoshita S., Hatanaka H. Brain-derived neurotrophic factor enhances long-term potentiation in rat visual cortex. J. Neurosci. 17:1997;6707-6716.
2. Blum R., Kafitz K.W., Konnerth A. Neurotrophin-evoked depolarization requires the sodium channel Na(V) 1.9. Nature. 419:2002;687-693.
3. Brunig I., Penschuck S., Berninger B., Benson J., Fritschy J.M. BDNF reduces miniature inhibitory postsynaptic currents by rapid downregulation of GABA(A) receptor surface expression. Eur. J. Neurosci. 13:2001;1320-1328.
4. Castren E., Zafra F., Thoenen H., Lindholm D. Light regulates expression of brain-derived neurotrophic factor mRNA in rat visual cortex. Proc. Natl. Acad. Sci. USA. 89:1992;9444-9448.
5. Croll S.D., Wiegand S.J., Anderson K.D., Lindsay R.M., Nawa H. Regulation of neuropeptides in adult rat forebrain by the neurotrophins BDNF and NG. Eur. J. Neurosci. 6:1994;1343-1353.
6. Du J., Feng L., Yang F., Lu B. Activity- and Ca(2+)-dependent modulation of surface expression of brain-derived neurotrophic factor receptors in hippocampal neurons. J. Cell Biol. 150:2000;1423-1434.
7. Esclapez M., Hirsch J.C., Khazipov R., Ben-Ari Y., Bernard C. Operative GABAergic inhibition in hippocampal CA1 pyramidal neurons in experimental epilepsy. Proc. Natl. Acad. Sci. USA. 94:1997;12151-12156.
8. Fitzsimonds R.M., Song H.J., Poo M.M. Prppagation of activity-dependent synaptic depression in simple neural networks. Nature. 388:1997;439-448.
9. Figurov A., Pozzo-Miller L.D., Olafsson P., Wang T., Lu B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature. 381:1996;706-709.
10. Franklin, K.B.J., Paxinos, G., 1996. The Mouse Brain in Stereotaxic Coordinates. Academic Press, San Diego.
11. Frerking M., Malenka R.C., Nicoll R.A. Brain-derived neurotrophic factor (BDNF) modulates inhibitory, but not excitatory, transmission in the CA1 region of the hippocampus. J. Neurophysiol. 80:1998;3383-3386.
12. Geiger J.R., Melcher T., Koh D.S., Sakmann B., Seeburg P.H., Jonas P., Monyer H. Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron. 15:1995;193-204.
13. Griesbeck O., Canossa M., Campana G., Gartner A., Hoener M.C., Nawa H., Kolbeck R., Thoenen H. Are there differences between the secretion characteristics of NGF and BDNF? Implications for the modulatory role of neurotrophins in activity-dependent neuronal plasticity. Microsc. Res. Tech. 45:1999;262-275.
14. Hartmann M., Heumann R., Lessmann V. Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J. 20:2001;5887-5897.
15. Hayashi Y., Shi S.H., Esteban J.A., Piccini A., Poncer J.C., Malinow R. Driving AMPA receptors into synapses by LTP and CaMKII requirement for GluR1 and PDZ domain interaction . Science. 287:2000;2262-2267.
16. Hendry S.H.C., Jones E.G., DeFelipe J., Schmechel D., Brandon C., Emson P.C. Neuropeptide-Containing neurons of cerebral cortex are also GABAergic. Proc. Natl. Acad. Sci. USA. 81:1984;6526-6530.
17. Hensch T.K., Fagiolini M., Mataga N., Stryker M.P., Baekkeskov S., Kash S.F. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science. 282:1998;1504-1508.
18. Huang Z.J., Kirkwood A., Pizzorusso T., Porciatti V., Morales B., Bear M.F., Maffei L., Tonegawa S. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell. 98:1999;739-755.
19. Itami C., Mizuno K., Kohno T., Nakamura S. Brain-derived neurotrophic factor requirement for activity-dependent maturation of glutamatergic synapse in developing mouse somatosensory cortex. Brain Res. 857:2000;141-150.
20. Iwakura Y., Nagano T., Kawamura M., Horikawa H., Ibaraki K., Takei N., Nawa H. N-Methyl-D-aspartate-induced alpha-amino-3-hydroxy-5-methyl-4- isoxazoleproprionic acid (AMPA) receptor down-regulation involves interaction of the carboxyl terminus of GluR2/3 with Pick1 ligand-binding studies using Sindbis vectors carrying AMPA receptor decoys . J. Biol. Chem. 276:2001;40025-40032.
21. Jourdi H., Xiong H., Narisawa-Saito M., Nawa H. The up-regulation of postsynaptic density proteins by neurotrophic factors in cultured neocortical neurons. Soc. Neurosci. Abst. 25:1999;1012.
22. Jovanovic J.N., Czernik A.J., Fienberg A.A., Greengard P., Sihra T.S. Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nat. Neurosci. 3:2000;323-329.
23. Kafitz K.W., Rose C.R., Thoenen H., Konnerth A. Neurotrophin-evoked rapid excitation through TrkB receptors. Nature. 401:1999;918-921.
24. Kang H., Schuman E.M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science. 267:1995;1658-1662.
25. Kawaguchi Y. Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J. Neurophysiol. 69:1993;416-431.
26. D28K- immunoreactive neurons in layer V of rat frontal cortex. J. Neurophysiol. 70:1993;387-396.
27. Kohara K., Kitamura A., Morishima M., Tsumoto T. Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science. 291:2001;2419-2423.
28. Kojima M., Takei N., Numakawa T., Ishikawa Y., Suzuki S., Matsumoto T., Katoh-Semba R., Nawa H., Hatanaka H. Biological characterization and optical imaging of brain-derived neurotrophic factor-green fluorescent protein suggest an activity-dependent local release of brain-derived neurotrophic factor in neurites of cultured hippocampal neurons. J. Neurosci Res. 64:2001;1-10.
29. Kondo M., Sumino R., Okado H. Combinations of AMPA receptor subunit expression in individual cortical neurons correlate with expression of specific calcium-binding proteins. J. Neurosci. 17:1997;1570-1581.
30. Korte M., Griesbeck O., Gravel C., Carroll P., Staiger V., Thoenen H., Bonhoeffer T. Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice. Proc. Natl. Acad. Sci. USA. 93:1996;12547-12552.
31. Lessmann V., Gottmann K., Heumann R. BDNF and NT-4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones. Neuroreport. 6:1994;21-25.
32. Li Y.X., Zhang Y., Lester H.A., Schuman E.M., Davidson N. Enhancement of neurotransmitter release induced by brain-derived neurotrophic factor in cultured hippocampal neurons. J. Neurosci. 18:1998;10231-10240.
33. Li Y.X., Xu Y., Ju D., Lester H.A., Davidson N., Schuman E.M. Expression of a dominant negative TrkB receptor, T1, reveals a requirement for presynaptic signaling in BDNF-induced synaptic potentiation in cultured hippocampal neurons. Proc. Natl. Acad. Sci. USA. 95:1998;10884-10889.
34. Marty S., Berninger B., Carroll P., Thoenen H. GABAergic stimulation regulates the phenotype of hippocampal interneurons through the regulation of brain-derived neurotrophic factor. Neuron. 16:1996;565-570.
35. Marty S., Carroll P., Cellerino A., Castren E., Staiger V., Thoenen H., Lindholm D. Brain-derived neurotrophic factor promotes the differentiation of various hippocampal nonpyramidal neurons, including Cajal-Retzius cells, in organotypic slice cultures. J. Neurosci. 16:1996;675-687.
36. Marty S., Wehrle R., Sotelo C. Neuronal activity and brain-derived neurotrophic factor regulate the density of inhibitory synapses in organotypic slice cultures of postnatal hippocampus. J. Neurosci. 20:2000;8087-8095.
37. Mayer M.L., Westbrook G.L., Guthrie P.B. Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature. 309:1984;261-263.
38. McAllister A.K., Katz L.C., Lo D.C. Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron. 18:1997;767-778.
39. McLean-Bolton M., Pittman A.J., Lo D.C. Brain-derived neurotrophic factor differentially regulates excitatory and inhibitory synaptic transmission in hippocampal cultures. J. Neurosci. 20:2000;3221-3232.
40. Mizuno K., Carnahan J., Nawa H. Brain-derived neurotrophic factor promotes differentiation of striatal GABAergic neurons. Dev. Biol. 165:1994;243-256.
41. Nagano T., Iwakura Y., Ushiki T., Nawa H. Development of neurites, dendritic filopodia and synaptic spines in hippocampal low-density culture. Uyemura K., Kawamura K., Yazaki T. Neural Development. 1999;386-393 Springer-Verlag, Berlin.
42. Narisawa-Saito M., Carnahan J., Araki K., Yamaguchi T., Nawa H. Brain-derived neurotrophic factor regulates the expression of AMPA receptor proteins in neocortical neurons. Neuroscience. 88:1999;1009-1014.
43. Narisawa-Saito M., Silva A.J., Yamaguchi T., Hayashi T., Yamamoto T., Nawa H. Growth factor-mediated Fyn signaling regulates AMPA receptor expression in rodent neocortical neurons. Proc. Natl. Acad. Sci. USA. 96:1999;2461-2466.
44. Narisawa-Saito M., Iwakura Y., Kawamura M., Araki K., Kozaki S., Takei N., Nawa H. Brain-derived neurotrophic factor regulates surface expression of alpha-amino-3-hydroxy-5-methyl-4-isoxazoleproprionic acid receptors by enhancing the N-ethyl-maleimide-sensitive factor/GluR2 interaction in developing neocortical neurons. J. Biol. Chem. 277:2002;40901-40910.
45. Nawa H., Bessho Y., Carnahan J., Nakanishi S., Mizuno K. Regulation of neuropeptide expression in cultured cerebral cortical neurons by brain-derived neurotrophic factor. J. Neurochem. 60:1993;772-775.
46. Nawa H., Carnahan J., Gall C. BDNF protein measured by a novel enzyme immunoassay in normal brain and after seizure partial disagreement with mRNA levels . Eur. J. Neurosci. 7:1995;1527-1535.
47. Nawa H., Takei N. BDNF as an anterophin; a novel neurotrophic relationship between brain neurons. Trends Neurosci. 24:2001;683-684. discussion 684-685.
48. Nayak A., Zastrow D.J., Lickteig R., Zahniser N.R., Browning M.D. Maintenance of late-phase LTP is accompanied by PKA-dependent increase in AMPA receptor synthesis. Nature. 394:1998;680-683.
49. Olofsdotter K., Lindvall O., Asztely F. Increased synaptic inhibition in dentate gyrus of mice with reduced levels of endogenous brain-derived neurotrophic factor. Neuroscience. 101:2000;531-539.
50. Patterson S.L., Abel T., Deuel T.A., Martin K.C., Rose J.C., Kandel E.R. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron. 16:1996;1137-1145.
51. Poo M.M. Neurotrophins as synaptic modulators. Nat. Rev. Neurosci. 2:2001;24-32.
52. Rutherford L.C., DeWan A., Lauer H.M., Turrigiano G.G. Brain-derived neurotrophic factor mediates the activity-dependent regulation of inhibition in neocortical cultures. J. Neurosci. 17:1997;4527-4535.
53. Rutherford L.C., Nelson S.B., Turrigiano G.G. BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses. Neuron. 21:1998;521-530.
54. Schinder A.F., Berninger B., Poo M. Postsynaptic target specificity of neurotrophin-induced presynaptic potentiation. Neuron. 25:2000;151-163.
55. Sherwood N.T., Lo D.C. Long-term enhancement of central synaptic transmission by chronic brain-derived neurotrophic factor treatment. J. Neurosci. 19:1999;7025-7036.
56. Shi S., Hayashi Y., Esteban J.A., Malinow R. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell. 105:2001;331-343.
57. Takei N., Numakawa T., Kozaki S., Sakai N., Endo Y., Takahashi M., Hatanaka H. Brain-derived neurotrophic factor induces rapid and transient release of glutamate through the non-exocytotic pathway from cortical neurons. J. Biol. Chem. 273:1998;27620-27624.
58. Tanaka T., Saito H., Matsuki N. Inhibition of GABAA synaptic responses by brain-derived neurotrophic factor (BDNF) in rat hippocampus. J. Neurosci. 17:1997;2959-2966.
59. Taniguchi N., Takada N., Kimura F., Tsumoto T. Actions of brain-derived neurotrophic factor on evoked and spontaneous EPSCs dissociate with maturation of neurones cultured from rat visual cortex. J. Physiol. 527:2000;579-592.
60. Thoenen H. Neurotrophins and neuronal plasticity. Science. 270:1995;593-598.
61. Tomasulo R.A., Ramirez J.J., Steward O. Synaptic inhibition regulates associative interactions between afferents during the induction of long-term potentiation and depression. Proc. Natl. Acad. Sci. USA. 90:1993;11578-11582.
62. Trussell L.O., Thio L.L., Zorumski C.F., Fischbach G.D. Rapid desensitization of glutamate receptors in vertebrate central neurons. Proc. Natl. Acad. Sci. USA. 85:1988;4562-4566.
63. Turrigiano G.G., Leslie K.R., Desai N.S., Rutherford L.C., Nelson S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature. 391:1998;892-896.
64. Tyler W.J., Pozzo-Miller L.D. BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses. J. Neurosci. 21:2001;4249-4258.
65. Velazquez J.L., Carlen P.L. Synchronization of GABAergic interneuronal networks during seizure-like activity in the rat horizontal hippocampal slice. Eur. J. Neurosci. 11:1999;4110-4118.
66. Yanagawa Y., Kaneko K., Kanbara N., Totsuka M., Yagi T., Obata K. Development of mouse expressing GFP in GABAergic neurons. Neurosci. Res. Suppl. 25:2001;S77.