Neurotrophin-3 potentiates excitatory GABAergic synaptic transmission in cultured developing hypothalamic neurones of the rat

Journal of Physiology

Volumn 518, Issue 1, 1999, Pages 81-95

  Gao, Xiao Bing ^a   Van Den Pol, A N ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; CADMIUM; CALCIUM CHANNEL; K 252A; NEUROTROPHIN 3; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; GRAMICIDIN;

4 AMINOBUTYRIC ACID RELEASE; ACTION POTENTIAL; ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CALCIUM TRANSPORT; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; DEPOLARIZATION; DOSE RESPONSE; EMBRYO; ENZYME INDUCTION; EXTRACELLULAR CALCIUM; HYPERPOLARIZATION; ION CURRENT; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; SYNAPSE; SYNAPTIC TRANSMISSION; ACTION POTENTIAL AMPLITUDE; ANIMAL TISSUE; CELL DIFFERENTIATION; CELL GROWTH; CELL MEMBRANE DEPOLARIZATION; CENTRAL NERVOUS SYSTEM; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GABAERGIC TRANSMISSION; HYPOTHALAMUS NUCLEUS; PERIPHERAL NERVOUS SYSTEM; POSITIVE FEEDBACK; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RAT; WHOLE CELL PATCH CLAMP;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; CALCIUM; CARBAZOLES; CELLS, CULTURED; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GAMMA-AMINOBUTYRIC ACID; HYPOTHALAMUS; MEMBRANE POTENTIALS; NEURONS; NEUROTROPHIN 3; PATCH-CLAMP TECHNIQUES; PROTEIN-TYROSINE KINASES; RATS; SYNAPSES; SYNAPTIC TRANSMISSION; TETRODOTOXIN;

EID: 0033166263     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1469-7793.1999.0081r.x     Document Type: Article

References (62)

1. + current in vertebrate sympathetic neurones. Nature 296, 746-749.
2. AVILA, M. A., VARELA-NIETO, I., ROMERO, G., MATO, J. M., GIRALDEZ, F., VAN DE WATER, T. R. & REPRESA, J. (1993). Brain-derived neurotrophic factor and neurotrophin-3 support the survival and neuritogenesis response of developing cochleovestibular ganglion neurons. Developmental Biology 159, 266-275.
3. BARBACID, M. (1993). Nerve growth factor: a tale of two receptors. Ontogene 8, 2033-2042.
4. A receptors in the outgrowth of cultured hippocampal neurons. Neuroscience Letters 152, 150-152.
5. BELOUSOV, A. & VAN DEN POL, A. N. (1997). Local synaptic release of glutamate from neurons of the rat hypothalamic arcuate nucleus. Journal of Physiology 499, 747-761.
6. BEN-ARI, Y., CHERUBINI, E., CORRADETTI, R. & GAIARSA, J. L. (1989). Giant synaptic potentials in immature rat CA3 hippocampal neurons. Journal of Physiology 416, 303-325.
7. A, NMDA and AMPA receptors: a developmentally regulated 'ménage à trois'. Trends in Neurosciences 20, 523-529.
8. BERG-VON DER EMDE, K., DEES, W. L., HINEY, J. K., HILL, D. F., DISSEN, G. A., COSTA, M. E., MOHOLT-SIEBERT, M. & OJEDA, S. R. (1995). Neurotrophins and the neuroendocrine brain: different neurotrophins sustain anatomically and functionally segregated subsets of hypothalamic dopaminergic neurons. Journal of Neuroscience. 15, 4223-4237.
9. BERNINGER, B., GARCIA, D. E., INAGAKI, N., HAHNEL, C. & LINDHOLM, D. (1993). BDNF and NT-3 induce intracellular Ca elevation in hippocampal neurons. NeuroReport 4, 1303-1306.
10. CHAO, M. V. (1992). Neurotrophin receptors: a window into neuronal differentiation. Neuron 9, 583-593.
11. CHEN, G., TROMBLEY, P. Q. & VAN DEN POL, A. N. (1995). GABA receptors precede glutamate receptors in hypothalamic development; differential regulation by astrocytes. Journal of Neurophysiology 74, 1473-1484.
12. CHEN, G., TROMBLEY, P. Q. & VAN DEN POL, A. N. (1996). Excitatory actions of GABA in developing rat hypothalamic neurones. Journal of Physiology 494, 451-464.
13. CHEN, G. & VAN DEN POL, A. N. (1997). Adenosine modulation of calcium currents and presynaptic inhibition of GABA release in suprachiasmatic and arcuate nucleus neurons. Journal of Neurophysiology 77, 3035-3047.
14. CLEMENTS, J. D. & BEKKERS, J. M. (1997). Detection of spontaneous synaptic events with an optimally scaled template. Biophysical Journal 73, 220-229.
15. COLLAZO, D., TAKAHASHI, H. & MCKAY, R. D. G. (1992). Cellular targets and trophic functions of neurotrophin-3 in the developing rat hippocampus. Neuron 9, 643-656.
16. ERNFORS, P., IBANEZ, C. F., EBENDAL, T., OLSON, L. & PERSSON, H. (1990). Molecular cloning and neurotrophic activities of a protein with structural similarities to nerve growth factor: developmental and topographical expression in the brain. Proceedings of the National Academy of Sciences of the USA 87, 5454-5458.
17. ERNFORS, P., LEE, K.-F., KUCERA, J. & JAENISCH, R. (1994). Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell 7, 503-512.
18. ESCANDÓN, E., SOPPET, D., ROSENTHAL, A., MENDOZA-RAMÍREZ, J.-L., SZÖNYI, É., BURTON, L. E., HENDERSON, C. E., PARADA, L. F. & NIKOLICS, K. (1994). Regulation of neurotrophin receptor expression during embryonic and postnatal development. Journal of Neuroscience 14, 2054-2068.
19. FARINAS, I., JONES, K. R., BACKUS, C., WANG, X.-Y. & REICHARDT, L. F. (1994). Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature 369, 658-661.
20. FOX, A. P., NOWYCKY, M. C. & TSIEN, R. W. (1987). Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurons. Journal of Physiology 394, 149-172.
21. GAO, X.-B., CHEN, G. & VAN DEN POL, A. N. (1998). GABA-dependent firing of glutamate-evoked action potentials at AMPA/kainate receptors in developing hypothalamic neurons. Journal of Neurophysiology 79, 716-726.
22. GHOSH, A. & GREENBERG, M. E. (1995). Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis. Neuron 15, 89-103.
23. GREENGARD, P., VALTORTA, F., CZERNIK, A. J. & BENFENATI, F. (1993). Synaptic vesicle phosphorylation and regulation of synaptic function. Science 259, 780-785.
24. HENDERKON, C. K., CAMU, W., METTLINO, C., GOUIN, A., POULSON, K., KARIHALOO, M., RULLAMAS, J., EVANS, T., MCMAHON, S. B., ARMANINI, M. P., BERKEMEIER, L. R., PHILLIPS, H. S. & ROSENTHAL, A. (1993). Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363, 266-270.
25. HOHN, A., LEIBROCK, J., BAILEY, K. & BARDE, Y.-A. (1990). Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family'. Nature 344, 339-341.
26. HOLM, N. R., CHRISTOPHERSEN, P., OLESEN, S. P. & GAMMELTOFT, S. (1997). Activation of calcium-dependent potassium channels in rat brain neurons by neurotrophin-3 and nerve growth factor. Proceedings of the National Academy of Sciences of the USA 94, 1002-1006.
27. IP, N. Y., LI, Y., YANCOPOULOS, G. D. & LINDSAY, R. M. (1993). Cultured hippocampal neurons show response to BDNF, NT-3, and NT-4, but not NGF. Journal of Neuroscience 13, 3394-3405.
28. JARVIS, C. R., XIONG, Z. G., PLANT, J. R., CHURCHILL, D., LU, W. Y., MACVICAR, B. A. & MACDONALD, J. F. (1997). Neurotrophin modulation of NMDA receptors in cultured murine and isolated rat neurons. Journal of Neurophysiology 78, 2363-2371.
29. JOVANOVIC, J. N., BENFENATI, F., SIOW, Y. L., SIHRA, T. S., SASGHERA, J. S., PELECH, S. L., GREENGARD, P. & CZERNIK, A. J. (1996). Neurotrophins stimulate phosphorylation of synapsin I by MAP kinase and regulate synapsin I-actin interactions. Proceedings of the National Academy of Sciences of the USA 93, 3679-3683.
30. JUNO, A. B. & BENNETT, J. P. JR (1994). Development of striatal dopaminergic function. III: Pre- and postnatal development of striatal and cortical mRNAs for the neurotrophin receptors TrkBTK+ and TrkC and their regulation by synaptic dopamine. Developmental Brain Research 94, 133-143.
31. KANG, H. & SCHUMAN, E. M. (1995). Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267, 1658-1662.
32. KAPLAN, D. R. & STEPHENS, R. M. (1994). Neurotrophin signal transduction by the Trk receptor. Journal of Neurobiology 25, 1404-1417.
33. KIM, H. G., WANG, T., OLAFSSON, P. & LU, B. (1994). Neurotrophin-3 potentiates neuronal activity and inhibits γ-aminobutyratergic synaptic transmission in cortical neurons. Proceedings of the National Academy of Sciences of the USA 91, 12341-12345.
34. KNÜSEL, B. & HEFTI, F. (1992). K-252 compounds: modulators of neurotrophin signal transduction. Journal of Neurochemistry 59, 1987-1996.
35. LAMBALLE, F., SMEYNE, R. J. & BARBACID, M. (1994). Developmental expression of TrkC, the neurotrophin-3 receptor, in the mammalian nervous system. Journal of Neuroscience 14, 14-28.
36. LAMBALLE, F., TAPLEY, P. & BAUBACID, M. (1993). TrkC encodes multiple neurotrophin-3 receptors with distinct biological properties and substrate specificities. EMBO Journal 12, 3083-3094.
37. 2+ oscillations mediated by the synergistic excitatory actions of GABA-A and NMDA receptors in the neonatal hippocampus. Neuron 18, 243-255.
38. LEVINE, E. S., DREYFUS, C. F., BLACK, I. B. & PLUMMER, M. R. (1995). Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proceedings of the National Academy of Sciences of the USA 92, 8074-8077.
39. LINDHOLM, D., CASTREN, E., BERZAGHI, M., BLOCHL, A. & THOENEN, H. (1994). Activity-dependent and hormonal regulation of neurotrophin mRNA levels in the brain - implications for neuronal plasticity. Journal of Neurobiology 25, 1362-1372.
40. LINDHOLM, D., CASTREN, E., TSOULFAS, P., KOLBECK, R., BERZAGHI, M. DA P., LEINGARTNER, A., HEISENBERG, C. P., TESAROLLO, L., PARADA, L. F. & THOENEN, H. (1993). Neurotrophin-3 induced by tri-iodothyronine in cerebellar granule cells promotes Purkinje cell differentiation. Journal of Cell Biology 122, 443-450.
41. LIOU, J. C., YANG, R. S. & FU, W. M. (1997). Regulation of quantal secretion by neurotrophic factors at developing motoneurons in Xenopus cell cultures. Journal of Physiology 503, 129-139.
42. LOHOF, A. M., IP, N. Y. & POO, M. M. (1993). Potentiation of developing neuromuscular synapses by the neurotrophin NT-3 and BDNF. Nature 363, 350-353.
43. LOTURCO, J. J., OWENS, D. F., HEATH, M. J. S., DAVIS, M. B. E. & KRIEGSTEIN, A. R. (1995). GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15, 1287-1298.
44. MEIER, E., DREJER, J. & SCHOUSBOE, A. (1984). GABA induces functionally active low-affinity GABA receptors on cultured cerebellar granule cells. Journal of Neurochemistry 43, 1737-1744.
45. MICHLER, A. (1990). Involvement of GABA receptors in the regulation of neurite growth in cultured embryonic chick tectum. International Journal of Developmental Neuroscience 8, 463-472.
46. MINTZ, I. M., SABATINI, B. L. & REGEHR, W. G. (1995). Calcium control of transmitter release at a cerebellar synapse. Neuron 15, 675-688.
47. OBRIETAN, K. & VAN DEN POL, A. N. (1996). Growth cone calcium rise by GABA. Journal of Comparative Neurology 372, 167-175.
48. 2+ elevating to depressing. Journal of Neuroscience 15, 5065-5077.
49. OWENS, D. F., BOYCE, L. H., DAVIS, M. B. E. & KRIEGSTEIN, A. R. (1996). Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. Journal of Neuroscience 16, 6414-6423.
50. REYNOLDS, J. D. & BRIEN, J. F. (1992). Ontogeny of glutamate and y-aminobutyric acid in the hippocampus of the guinea pig. Journal of Developmental Physiology 18, 243-252.
51. RODRIOUEZ-TEBAR, A., DECHANT, G., GOTZ, R. & BARDE, Y. A. (1992). Binding of neurotrophin-3 to its neuronal receptors and interactions with nerve growth factor and brain-derived neurotrophic factor. EMBO Journal 11, 917-922.
52. ROMANO, C., NICHOLS, R. A. & GREENGARD, P. (1987). Synapsin I in PC12 cells. II. Evidence for regulation by NGF of phosphorylation on a novel site. Journal of Neuroscience 7, 1300-1306.
53. 2+ oscillations in cultured hippocampal neurons. Brain Research 778, 318-328.
54. SCHNELL, L., SCHNEIDER, R., KOLBECK, R., BARDE, Y.-A. & SCHWAB, M. E. (1994). Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367, 170-173.
55. SMITH, M. A., MAKINO, S., ALTEMUS, M., MICHELSON, D., HONG, S. K., KVKTNANSKY, R. & POST, R. M. (1995). Stress and antidepressants differentially regulate neurotrophin 3 mRNA expression in the locus coeruleus. Proccedings of the National Academy of Sciences of the USA 92, 8788-8792.
56. STORM, J. F. (1987). Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. Journal of Physiology 385, 733-759.
57. A synaptic responses by brain-derived neurotrophic factors (BDNF) in the rat hippocampus. Journal of Neuroscience 17, 2959-2966.
58. VAN DEN POL, A. N. & TROMBLEY, P. Q. (1993). Glutamate neurons in hypothalamus regulate excitatory transmission. Journal of Neuroscience 13, 2829-2836.
59. VAN DES POL, A. N., OBRIETAN, K. & CHEN, G. (1996). Excitatory actions of GABA after neuronal trauma. Journal of Neuroscience 16, 4283-4292.
60. WANG, X.-H. & POO, M.-M. (1997). Potentiation of developing synapses by postsynaptic release of neurotrophin-4. Neuron 19, 825-835.
61. 2+ channels in supporting hippocampal synaptic transmission. Science 264, 107-111.
62. WU, L. G. & SAGGAU, P. (1994). Pharmacological identification of two types of presynaptic voltage-dependent calcium channels at CA3-CA1 synapses of the hippocampus. Journal of Neuroscience 14, 5613-5622.