Brain-derived neurotrophic factor acutely inhibits AMPA-mediated currents in developing sensory relay neurons

Journal of Neuroscience

Volumn 20, Issue 5, 2000, Pages 1904-1911

  Balkowiec, Agnieszka ^a   Kunze, Diana L ^a   Katz, David M ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AMPA; BDNF; Glutamate; Nucleus tractus solitarius; Sensory neurons; Synaptic plasticity; Synaptic transmission

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; GLUTAMIC ACID; K 252A; NERVE GROWTH FACTOR; NEUROTROPHIN 4; PROTEIN TYROSINE KINASE INHIBITOR;

ANIMAL CELL; ARTICLE; BRAIN STEM; CONTROLLED STUDY; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; SENSORY GANGLION; SENSORY NERVE CELL; SOLITARY TRACT NUCLEUS; SYNAPTIC TRANSMISSION;

EID: 0034161295     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-05-01904.2000     Document Type: Article

References (71)

1. Ambalavanar R, Ludlow CL, Wenthold RJ, Tanaka Y, Damirjian M, Petralia RS (1998) Glutamate receptor subunits in the nucleus of the tractus solitarius and other regions of the medulla oblongata in the cat. J Comp Neurol 402:75-92.
2. Andresen MC, Yang M (1990) Non-NMDA receptors mediate sensory afferent synaptic transmission in medial nucleus tractus solitarius. Am J Physiol 259:H1307-H1311.
3. Apfel SC, Wright DE, Wiideman AM, Dormia C, Snider WD, Kessler JA (1996) Nerve growth factor regulates the expression of brain-derived neurotrophic factor mRNA in the peripheral nervous system. Mol Cell Neurosci 7:134-142.
4. Balkowiec A, Katz DM (1998) Brain-derived neurotrophic factor is required for normal development of the central respiratory rhythm in mice. J Physiol (Lond) 510:527-533.
5. Barbacid M (1994) The Trk family of neurotrophin receptors. J Neurobiol 25:1386-1403.
6. Barria A, Muller D, Derkach V, Griffith LC, Soderling TR (1997) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276:2042-2045.
7. Berg MM, Sternberg DW, Parada LF, Chao MV (1992) K-252a inhibits nerve growth factor-induced trk proto-oncogene tyrosine phosphorylation and kinase activity. J Biol Chem 267:13-16.
8. Bianchi AL, Denavit-Saubié M, Champagnat J (1995) Central control of breathing in mammals: neuronal circuitry, membrane properties, and neurotransmitters. Physiol Rev 75:1-45.
9. Botsford SA, Dean C, Hopp FA, Seagard JL (1999) Presence of glutamate receptor subtypes on barosensitive neurons in the nucleus tractus solitarius of the dog. Neurosci Lett 261:113-117.
10. Bozzi Y, Pizzorusso T, Cremisi F, Rossi FM, 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.
11. Brady R, Zaidi SIA, Mayer C, Katz DM (1999) BDNF is a targetderived survival factor for arterial baroreceptor and chemoafferent primary sensory neurons. J Neurosci 19:2131-2142.
12. Carroll RC, Nicoll RA, Malenka RC (1998) Effects of PKA and PKC on miniature excitatory postsynaptic currents in CA1 pyramidal cells. J Neurophysiol 80:2797-2800.
13. Carvalho AL, Kameyama K, Huganir RL (1999) Characterization of phosphorylation sites on the glutamate receptor 4 subunit of the AMPA receptors. J Neurosci 19:4748-4754.
14. 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.
15. Chao MV (1992) Neurotrophin receptors: a window into neuronal differentiation. Neuron 9:583-593.
16. Choi DW (1992) Excitotoxic cell death. J Neurobiol 23:1261-1276.
17. Denavit-Saubié M, Kalia M, Pierrefiche O, Schweitzer P, Foutz AS, Champagnat J (1994) Maturation of brain stem neurons involved in respiratory rhythmogenesis: biochemical, bioelectrical and morphological properties. Biol Neonate 65:171-175.
18. Drewe JA, Childs GV, Kunze DL (1988) Synaptic transmission between dissociated adult mammalian neurons and attached synaptic boutons. Science 241:1810-1813.
19. Figurov A, Pozzo-Miller LD, 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. Fritzsch B, Pirvola U, Ylikoski J (1999) Making and breaking the innervation of the ear: neurotrophic support during ear development and its clinical implications. Cell Tissue Res 295:369-382.
21. Gonzalez M, Collins WF (1997) Modulation of motoneuron excitability by brain-derived neurotrophic factor. J Neurophysiol 77:502-506.
22. Hallbook F, Fritzsch B (1997) Distribution of BDNFand trkB mRNA in the otic region of 3.5 and 4.5 day chick embryos as revealed with a combination of in situ hybridization and tract tracing. Int J Dev Biol 41:725-732.
23. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85-100.
24. Hayashi Y, Ishida A, Katagiri H, Mishina M, Fujisawa H, Manabe T, Takahashi T (1997) Calcium- and calmodulin-dependent phosphorylation of AMPA type glutamate receptor subunits by endogenous protein kinases in the post-synaptic density. Brain Res Mol Brain Res 46:338-342.
25. Ip NY, Ibanez CF, Nye SH, McClain J, Jones PF, Gies DR, Belluscio L, Le Beau MM, Espinosa R, Squinto SP, Persson H, Yancopoulos GD (1992) Mammalian neurotrophin-4: structure, chromosomal localization, tissue distribution, and receptor specificity. Proc Natl Acad Sci USA 89:3060-3064.
26. Kafitz KW, Rose CR, Thoenen H, Konnerth A (1999) Neurotrophinevoked rapid excitation through TrkB receptors. Nature 401:918-921.
27. Kalia M, Schweitzer P, Champagnat J, Denavit-Saubié M (1993) Two distinct phases characterize maturation of neurons in the nucleus of the tractus solarius during early development: morphological and electrophysiological evidence. J Comp Neurol 327:37-47.
28. Kang H, Schuman EM (1995a) Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267:1658-1662.
29. Kang HJ, Schuman EM (1995b) Neurotrophin-induced modulation of synaptic transmission in the adult hippocampus. J Physiol (Paris) 89:11-22.
30. Kerr BJ, Bradbury EJ, Bennett DLH, Trivedi PM, Dassan P, French J, Shelton DB, McMahon SB, Thompson SWN (1999) Brain-derived neurotrophic factor modulates nociceptive sensory inputs and NMDA-evoked responses in the rat spinal cord. J Neurosci 19:5138-5148.
31. Klein R, Lamballe F, Bryant S, Barbacid M (1992) The trkB tyrosine protein kinase is a receptor for neurotrophin-4. Neuron 8:947-956.
32. Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T (1995) Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci USA 92:8856-8860.
33. Lessmann V, Heumann R (1998) Modulation of unitary glutamatergic synapses by neurotrophin-4/5 or brain-derived neurotrophic factor in hippocampal microcultures: presynaptic enhancement depends on preestablished paired-pulse facilitation. Neuroscience 86:399-413.
34. Lessmann V, Gottmann K, Heumann R (1994) BDNF and NT-4/5 enhance glutamatcrgic synaptic transmission in cultured hippocampal neurones. NeuroReport 6:21-25.
35. Levine ES, Dreyfus CF, Black IB, Plummer MR (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.
36. Levine ES, Dreyfus CF, Black IB, Plummer MR (1996) Selective role for trkB neurotrophin receptors in rapid modulation of hippocampal synaptic transmission. Brain Res Mol Brain Res 38:300-303.
37. Levine ES, Crozier RA, Black IB, Plummer MR (1998) Brain-derived neurotrophic factor modulates hippocampal synaptic transmission by increasing N-methyl-D-aspartic acid receptor activity. Proc Natl Acad Sci USA 95:10235-10239.
38. Liao D, Zhang X, O'Brien R, Ehlers MD, Huganir RL (1999) Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nat Neurosci 2:37-43.
39. Lin S-Y, Wu K, Levine ES, Mount HTJ, Suen P-C, Black IB (1998) BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities. Brain Res Mol Brain Res 55:20-27.
40. 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.
41. Lissin DV, Carroll RC, Nicoll RA, Malenka RC, von Zastrow M (1999) Rapid, activation-induced redistribution of ionotropic glutamate receptors in cultured hippocampal neurons. J Neurosci 19:1263-1272.
42. Lohof AM, Ip NY, Poo M-M (1993) Potentiation of developing neuromuscular synapses by the neuratrophins NT-3 and BDNF. Nature 363:350-353.
43. Mammen AL, Kameyama K, Roche KW, Huganir RL (1997) Phosphorylation of the α-amino-3-hydroxy-5-methylisoxazole4-propionic acid receptor GluR1 subunit by calcium/calmodulin-dependent kinase II. J Biol Chem 272:32528-32533.
44. McAllister AK, Katz LC, Lo DC (1997) Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron 18:767-778.
45. Mendelowitz D, Yang M, Andresen MC, Kunze DL (1992) Localization and retention in vitro of fluorescently labeled aortic haroreccptor terminals on neurons from the nucleus tractus solitarius. Brain Res 581:339-343.
46. Michael GJ, Averill S, Nitkunan A, Rattray M, Bennett DL, Yan Q, Priestley JV (1997) Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in TrkA-expressing dorsal root ganglion cells and in their central terminations within the spinal cord. J Neurosci 17:8476-8490.
47. Miller AJ, McKoon M, Pinneau M, Silverstein R (1983) Postnatal synaptic development of the nucleus tractus solitarius (NTS) of the rat. Brain Res Dev Brain Res 8:205-213.
48. Murase K, Ryu PD, Randic M (1989) Excitatory and inhibitory amino acids and peptide-induced responses in acutely isolated rat spinal dorsal horn neurons. Neurosci Lett 103:56-63.
49. Nyc SH, Squinto SP, Glass DJ, Stitt TN, Hantzopoulos P, Macchi MJ, Lindsay NS, Ip NY, Yancopoulos GD (1992) K-252a and staurosporine selectively block autophosphorylation of neurotrophin receptors and neurotrophin-mediated responses. Mol Biol Cell 3:677-686.
50. O'Brien RJ, Kamboj S, Ehlers MD, Rosen KR, Fischbach GD, Huganir RL (1998) Activity-dependent modulation of synaptic AMPA receptor accumulation. Neuron 21:1067-1078.
51. Ozawa S, Kamiya H, Tsuzuki K (1998) Glutamate receptors in the mammalian central nervous system. Prog Neurobiol 54:581-618.
52. Patterson SL, Abel T, Deuel TAS, Martin KC, Rose JC Kandel ER (1996) Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16:1137-1145.
53. Rae J, Cooper K, Gates P, Watsky M (1991) Low access resistance perforated patch recordings using amphotericin B. J Neurosci Methods 37:15-26.
54. Ross AH, McKinnon CA, Daou M-C, Ratliff K, Wolf DE (1995) Differential biological effects of K252 kinase inhibitors are related to membrane solubility but not to permeability. J Neurochem 65:2748-2756.
55. Rutherford LC, DeWan A, Lauer HM, Turrigiano GG (1997) Brain-derived neurotrophic factor mediates the activity-dependent regulation of inhibition in neocortical cultures. J Neurosci 17:4527-4535.
56. Rutherford LC, Nelson SB, Turrigiano GG (1998) BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses. Neuron 21:521-530.
57. Scharfman HE (1997) Hyperexcitability in combined entorhinal/hippocampal slices of adult rat after exposure to brain-derived neurotrophic factor. J Neurophysiol 78:1082-1095.
58. Schecterson LC, Bothwell M (1992) Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons. Neuron 9:449-463.
59. Shimohama S, Tamura Y, Akaike A, Tsukahara T, Ohara O, Watanabe S, Kimura J (1993) Brain-derived neurotrophic factor pretreatment exerts a partially protective effect against glutamate-induced neurotoxicity in cultured rat cortical neurons. Neurosci Lett 164:55-58.
60. Smith BN, Dou P, Barber WD, Dudek FE (1998) Vagally evoked synaptic currents in the immature rat nucleus tractus solitarii in an intact in vitro preparation. J Physiol (Lond) 512:149-162.
61. Song D-K, Choe B, Bae JH, Park WK, Han IS, Ho W-K, Earm YE (1998) Brain-derived neurotrophic factor rapidly potentiates synaptic transmission through NMDA, but suppresses it through non-NMDA receptors in rat hippocampal neuron. Brain Res 799:176-179.
62. Suen P-C, Wu K, Levine ES, Mount HTJ, Xu J-L, Lin S-Y, Black IB (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.
63. Thoenen H (1995) Neurotrophins and neuronal plasticity. Science 270:593-598.
64. Tonra JR (1999) Classical and novel directions in neurotrophin transport and research: anterograde transport of brain-derived neurotrophic factor by sensory neurons. Microsc Res Tech 45:225-232.
65. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:892-896.
66. Wetmore C, Olson L (1995) Neuronal and nonneuronal expression of neurotrophins and their receptors in sensory and sympathetic ganglia suggest new intercellular trophic interactions. J Comp Neurol 353:143-159.
67. Yan Q, Radeke MJ, Matheson CR, Talvenheimo J, Welcher AA, Feinstein SC (1997) Immunocytochemical localization of TrkB in the central nervous system of the adult rat. J Comp Neurol 378:135-157.
68. Zhang J, Mifflin SW (1998) Differential roles for NMDA and non-NMDA receptor subtypes in baroreceptor afferent integration in the nucleus of the solitary tract of the rat. J Physiol (Lond) 511:733-745.
69. Zhou X-F, Chic ET, Rush RA (1998) Distribution of brain-derived neurotrophic factor in cranial and spinal ganglia. Exp Neurol 149:237-242.
70. Zhou X-F, Rush RA (1996) Endogenous brain-derived neurotrophic factor is anterogradely transported in primary sensory neurons. Neuroscience 74:945-951.
71. Zhou Z, Champagnat J, Poon C-S (1997) Phasic and long-term depression in brainstem nucleus tractus solitarius neurons: differing roles of AMPA receptor desensitization. J Neurosci 17:5349-5356.