BDNF up-regulates evoked GABAergic transmission in developing hippocampus by potentiating presynaptic N- and P/Q-type Ca2+ channels signalling

European Journal of Neuroscience

Volumn 16, Issue 12, 2002, Pages 2297-2310

  Baldelli, P ^a   Novara, M ^a   Carabelli, V ^a   Hernandez Guijo J M ^a   Carbone, Emilio ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

Inhibitory synaptic transmission; IPSCs; Neurotrophins; Paired pulse depression; Presynaptic Ca2+ channels; TrkB receptors

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CALCIUM CHANNEL; CALCIUM CHANNEL N TYPE; CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; NEUROTROPHIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CELL MEMBRANE DEPOLARIZATION; CHANNEL GATING; CONTROLLED STUDY; EVOKED RESPONSE; FEMALE; GABAERGIC TRANSMISSION; HIPPOCAMPUS; MEMBRANE CURRENT; MINIATURE ENDPLATE POTENTIAL; NONHUMAN; PRESYNAPTIC NERVE; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; UPREGULATION;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; CALCIUM CHANNELS, N-TYPE; CALCIUM CHANNELS, P-TYPE; CALCIUM CHANNELS, Q-TYPE; CELL DIFFERENTIATION; CELLS, CULTURED; FEMALE; FETUS; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; NEURAL INHIBITION; POTASSIUM CHLORIDE; PREGNANCY; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKB; RECEPTORS, GABA-A; SYNAPTIC TRANSMISSION; UP-REGULATION;

EID: 0036920981     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02313.x     Document Type: Article

References (64)

1. 2+ channel synthesis in developing hippocampal neurons. Eur. J. Neurosci., 12, 4017-4032.
2. 2+ channels in rat embryo motoneurons by BDNF. Eur. J. Neurosci., 11, 1127-1133.
3. Balkowiec, A. & Katz, D.M. (2000) Activity-dependent release of endogenous brain-derived neurotrophic factor from primary sensory neurons detected by ELISA in situ. J. Neurosci., 20, 7417-7423.
4. Berninger, B., Marty, S., Zafra, F., da Penha Berzaghi, M., Thoenen, H. & Lindholm, D. (1995) GABAergic stimulation switches from enhancing to repressing BDNF expression in rat hippocampal neurons during maturation in vitro. Development, 121, 2327-2335.
5. Betz, W.J., Bewick, G.S. & Ridge, R.M. (1992) Intracellular movements of fluorescently labeled synaptic vesicles in frog motor nerve terminals during nerve stimulation. Neuron, 9, 805-813.
6. Bolton, M.M., Pittman, A.J. & Lo, D.C. (2000) Brain-derived neurotrophic factor differentially regulates excitatory and inhibitory synaptic transmission in hippocampal cultures. J. Neurosci., 20, 3221-3232.
7. 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.
8. 2+ channels in hippocampal mossy fiber synaptic transmission and long-term potentiation. Neuron, 12, 261-269.
9. Cellerino, A., Maffei, L. & Domenici, L. (1996) The distribution of brain-derived neurotrophic factor and its receptor trkB in parvalbumin-containing neurons of the rat visual cortex. Eur. J. Neurosci., 8, 1190-1197.
10. Cherubini, E., Gaiarsa, J.L. & Ben-Ari, Y. (1991) GABA: An excitatory transmitter in early postnatal life. Trends Neurosci., 14, 515-519.
11. Collin, C., Vicario-Abejon, C., Rubio, M.E., Wenthold, R.J., McKay, R.D. & Segal, M. (2001) Neurotrophins act at presynaptic terminals to activate synapses among cultured hippocampal neurons. Eur. J. Neurosci., 13, 1273-1282.
12. Davies, P., Anderton, B., Kirsch, J., Konnerth, A., Nitsch, R. & Sheetz, M. (1998) First one in, last one out: The role of GABAergic transmission in generation and degeneration. Prog. Neurobiol., 55, 651-658.
13. B receptor-mediated inhibition of GABA release in area CA1 of the rat hippocampus. J. Neurophysiol., 74, 43-53.
14. 2+ channels in mammalian central neurons. Trends Neurosci., 18, 89-98.
15. 2+-entry, and spontaneous transmitter release. Neuron, 29, 197-208.
16. Erickson, J.T., Conover, J.C., Borday, V., Champagnat, J., Barbacid, M., Yancopoulos, G. & Katz, D.M. (1996) Mice lacking brain-derived neurotrophic factor exhibit visceral sensory neuron losses distinct from mice lacking NT4 and display a severe developmental deficit in control of breathing. J. Neurosci., 16, 5361-5371.
17. Ernfors, P., Lee, K.F. & Jaenisch, R. (1994) Target derived and putative local actions of neurotrophins in the peripheral nervous system. Progr. Brain Res., 103, 43-54.
18. Fedulova, S.A., Vasilyev, D.V., Isaeva, E.V., Romanyuk, S.G. & Veselovsky, N.S. (1999) Possibility of multiquantal transmission at single inhibitory synapse in cultured rat hippocampal neurons. Neuroscience, 92, 1217-1230.
19. Figurov, A., Pozzo-Miller, L.D., Olafsson, P., Wang, T. & Lu, B. (1996) Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature, 381, 706-709.
20. Frerking, M., Malenka, R.C. & Nicoll, R.A. (1998) Brain-derived neurotrophic factor (BDNF) modulates inhibitory, but not excitatory, transmission in the CA1 region of the hippocampus. J. Neurophysiol., 80, 3383-3386.
21. Ganguly, K., Schinder, A.F., Wong, S.T. & Poo, M. (2001) GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell, 105, 521-532.
22. Ghosh, A., Carnahan, J. & Greenberg, M.E. (1994) Requirement for BDNF in activity-dependent survival of cortical neurons. Science, 263, 1618-1623.
23. 2+ channel types triggering GABA release onto medial preoptic neurons from rat. J. Physiol. (Lond.), 507, 77-91.
24. Halegoua, S., Armstrong, R.C. & Kremer, N.E. (1991) Dissecting the mode of action of a neuronal growth factor. Curr. Topics Microbiol. Immunol., 165, 119-170.
25. Hamill, O.P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F.J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pfluegers Arch., 391, 85-100.
26. Iwasaki, S., Momiyama, A., Uchitel, O.D. & Takahashi, T. (2000) Developmental changes in calcium channel types mediating central synaptic transmission. J. Neurosci., 20, 59-65.
27. 2+ channels in GABAergic synaptic transmission in cultured hippocampal neurons. J. Neurophysiol., 81, 1225-1230.
28. Jensen, K., Lambert, J.D. & Jensen, M.S. (1999b) Activity-dependent depression of GABAergic IPSCs in cultured hippocampal neurons. J. Neurophysiol., 82, 42-49.
29. Jones, K.R., Farinas, I., Backus, C. & Reichardt, L.F. (1994) Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell, 76, 989-999.
30. Jovanovic, J.N., Benfenati, F., Siow, Y.L., Sihra, T.S., Sanghera, 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. Proc. Natl. Acad. Sci. USA, 93, 3679-3683.
31. Kang, H. & Schuman, E.M. (1995) Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science, 267, 1658-1662.
32. A receptors on cultured hippocampal cells correlate only partially with functional synapses. Eur. J. Neurosci., 11, 1256-1264.
33. Katz, B. & Miledi, R. (1967) A study of synaptic transmission in the absence of nerve impulses. J. Physiol. (Lond.), 192, 407-436.
34. Kim, H.G., Wang, T., Olafsson, P. & Lu, B. (1994) Neurotrophin 3 potentiates neuronal activity and inhibits gamma-aminobutyratergic synaptic transmission in cortical neurons. Proc. Natl. Acad. Sci. USA, 91, 12341-12345.
35. Lambert, N.A. & Wilson, W.A. (1994) Temporally distinct mechanism of use-dependent depression at the inhibitory synapses in the rat hippocampus in vitro. J. Neurophysiol., 72, 121-130.
36. Lessmann, V., Gottmann, K. & Heumann, R. (1994) BDNF and NT-4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones. Neuroreport, 6, 21-25.
37. 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. Proc. Natl. Acad. Sci. USA, 92, 8074-8077.
38. Lewin, G.R. & Barde, Y.A. (1996) Physiology of the neurotrophins. Annu. Rev. Neurosci., 19, 289-317.
39. Lindholm, D., Dechant, G., Heisenberg, C.P. & Thoenen, H. (1993) Brain-derived neurotrophic factor is a survival factor for cultured rat cerebellar granule neurons and protects them against glutamate-induced neurotoxicity. Eur. J. Neurosci., 5, 1455-1464.
40. Lindsay, R.M., Wiegand, S.J., Altar, C.A. & DiStefano, P.S. (1994) Neurotrophic factors: From molecule to man. Trends Neurosci., 17, 182-190.
41. Liu, G. & Tsien, R.W. (1995) Synaptic transmission at single visualized hippocampal boutons. Neuropharmacology, 34, 1407-1421.
42. Llano, I., Gonzalez, J., Caputo, C., Lai, F.A., Blayney, L.M., Tan, Y.P. & Marty, A. (2000) Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients. Nature Neurosci., 3 (12), 1256-1265.
43. Magnelli, V., Baldelli, P. & Carbone, E. (1998) Antagonist-resistant calcium currents in rat embryo motoneurons. Eur. J. Neurosci., 10, 1810-1825.
44. Marty, S., Berzaghi, M.P. & Berninger, B. (1997) Neurotrophins and activity-dependent plasticity of cortical interneurons. Trends Neurosci., 20, 198-202.
45. Mintz, I.M., Sabatini, B.L. & Regehr, W.G. (1995) Calcium control of transmitter release at a cerebellar synapse. Neuron, 15, 675-688.
46. Patterson, S.L., Abel, T., Deuel, T.A., Martin, K.C., Rose, J.C. & Kandel, E.R. (1996) Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron, 16, 1137-1145.
47. Pfrieger, F.W., Veselovski, N.S., Gottmann, K. & Lux, H.D. (1992) Pharmacological characterization of calcium currents and synaptic transmission between thalamic neurons in vitro. J. Neurosci., 12, 4347-4357.
48. 2+ channels in human neuroblastoma IMR32 cells. Pfluegers Arch., 422, 75-83.
49. Poncer, J.C., McKinney, R.A., Gahwiler, B.H. & Thompson, S.M. (1997) Either N- or P-type calcium channels mediate GABA release at distinct hippocampal inhibitory synapses. Neuron, 18, 463-472.
50. Regehr, W.G. & Stevens, C.F. (2001) Physiology of synaptic transmission and short-term plasticity. In Cowan, W.M., Sudhof, T.C. & Stevens, C.F., (Eds) Synapse. The John Hopkins University Press, Baltimore, pp. 135-176.
51. 2+ channel subtypes on presynaptic terminals of excitatory synapses in hippocampal cultures. J. Neurosci., 17, 2738-2745.
52. Reuter, H. (1996) Diversity and function of presynaptic calcium channels in the brain. Curr. Op. Neurobiol., 6, 331-337.
53. Rosenmund, C. & Stevens, C.F. (1996) Definition of the ready releasable pool of vesicle at hippocampal synapses. Neuron, 16, 1197-1207.
54. Schinder, A.F. & Poo, M. (2000) The neurotrophins hypothesis for synaptic plasticity. Trends Neurosci., 23, 639-645.
55. Scholz, K.P. & Miller, R.J. (1995) Developmental changes in presynaptic calcium channels coupled to glutamate release in cultured rat hippocampal neurons. J. Neurosci., 15, 4612-4617.
56. Sherwood, N.T. & Lo, D.C. (1999) Long-term enhancement of central synaptic transmission by chronic brain-derived neurotrophic factor treatment. J. Neurosci., 19, 7025-7036.
57. Stevens, C.F. & Tsujimoto, T. (1995) Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill a pool. Proc. Natl. Acad. Sci. USA, 92, 846-849.
58. Suen, P.C., Wu, K., Levine, E.S., Mount, H.T., Xu, J.L., Lin, S.Y. & Black, I.B. (1997) Brain-derived neurotrophic factor rapidly enhances phosphorylation of the postsynaptic N-methyl-D-aspartate receptor subunit 1. Proc. Natl. Acad. Sci. USA, 94, 8191-8195.
59. Takahashi, T. & Momiyama, A. (1993) Different types of calcium channels mediate central synaptic transmission. Nature, 366, 156-158.
60. A synaptic responses by brain-derived neurotrophic factor (BDNF) in rat hippocampus. J. Neurosci., 17, 2959-2966.
61. Vicario-Abejon, C., Collin, C., McKay, R.D. & Segal, M. (1998) Neurotrophins induce formation of functional excitatory and inhibitory synapses between cultured hippocampal neurons. J. Neurosci., 18, 7256-7271.
62. 2+-induced exocytosis from single chromaffin cells. FEBS Lett., 336, 48-52.
63. 2+ channels in supporting hippocampal synaptic transmission. Science, 264, 107-111.
64. Wu, L.G. & Saggau, P. (1994) Pharmacological identification of two types of presynaptic voltage-dependent calcium channels at CA3-CA1 synapses of the hippocampus. J. Neurosci., 14, 5613-5622.