From modulator to mediator: Rapid effects of BDNF on ion channels

BioEssays

Volumn 26, Issue 11, 2004, Pages 1185-1194

  Rose, Christine R ^a   Blum, Robert ^a   Kafitz, Karl W ^a   Kovalchuk, Yury ^a   Konnerth, Arthur ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CALCIUM ION; NERVE GROWTH FACTOR; NEUROTROPHIN 3; POTASSIUM CHANNEL; SODIUM CHANNEL;

CHANNEL GATING; HUMAN; LONG TERM POTENTIATION; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; HUMANS; ION CHANNEL GATING; ION CHANNELS; PHOSPHOTYROSINE; RECEPTOR, TRKB; SIGNAL TRANSDUCTION;

EID: 8844266876     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.20118     Document Type: Review

References (87)

1. Bibel M, Barde YA. 2000. Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev 14:2919-2937.
2. Thoenen H. 2000. Neurotrophins and activity-dependent plasticity. Prog Brain Res 128:183-191.
3. Murer MG, Van Q, Raisman-Vozari R. 2001. Brain-derived neurotrophic factor in the control human brain, and in Alzheimer's disease and Parkinson's disease. Prog Neurobiol 63:71-124.
4. Lessmann V, Gottmann K, Malcangio M. 2003. Neurotrophin secretion: current facts and future prospects. Prog Neurobiol 69:341-374.
5. Barde YA, Edgar D, Thoenen H. 1982. Purification of a new neurotrophic factor from mammalian brain. EMBO J 1:549-553.
6. McAllister AK, Katz LC, Lo DC. 1999. Neurotrophins and synaptic plasticity. Annu Rev Neurosci 22:295-318.
7. Goodman LJ, Valverde J, Lim F, Geschwind MD, Federoff HJ, et al. 1996. Regulated release and polarized localization of brain-derived neurotrophic factor in hippocampal neurons. Mol Cell Neurosci 7:222-238.
8. Canossa M, Gärtner A, Campana G, Inagaki N, Thoenen H. 2001. Regulated secretion of neurotrophins by metabotropic glutamate group 1 (mGluR1) and Trk receptor activation is mediated via phospholipase C signalling pathways. EMBO J 20:1640-1650.
9. Hartmann M, Heumann R, Lessmann V. 2001. Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J 20:5887-5897.
10. Kohara K, Kitamura A, Morishima M, Tsumoto T. 2001. Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science 291:2419-2423.
11. Gärtner A, Staiger V. 2002. Neurotrophin secretion from hippocampal neurons evoked by long-term-potentiation-inducing electrical stimulation patterns. Proc Natl Acad Sci USA 99:6386-6391.
12. Lu B. 2003. Pro-region of neurotrophins. Role in synaptic modulation. Neuron 39:735-738.
13. Poo M-M. 2001. Neurotrophins as synaptic modulators. Nature Neurosci Rev 2:1-9.
14. Patapoutian A, Reichardt LF. 2001. Trk receptors: mediators of neurotrophin action. Curr Opin Neurobiol 11:272-280.
15. Dechant G, Barde YA. 2002. The neurotrophin receptor p75(NTR): novel functions and implications for diseases of the nervous system. Nat Neurosci 5:1131-1136.
16. Chao MV. 2003. Neurotrophins and their receptors: A convergence point for many signalling pathways. Nat Rev Neurosci 4:299-309.
17. Huang EJ, Reichardt LF. 2003. TRK Receptors: Roles in Neuronal Signal Transduction. Annu Rev Biochem 27:27.
18. Barbacid M. 1995. Neurotrophic factors and their receptors. Curr Opin Cell Biol 7:148-155.
19. Klesse LJ, Parada LF. 1999. Trks: signal transduction and intracellular pathways. Microscopy Research and Technique 45:210-216.
20. Schlessinger J. 2000. Cell signaling by receptor tyrosine kinases. Cell 103:211-225.
21. Lohof AM, Ip NY, Poo MM. 1993. Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363:350-353.
22. Lessmann V, Gottmann K, Heumann R. 1994. BDNF and NT-4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones. Neuroreport 6:21-25.
23. Kang H, Schuman EM. 1995. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267:1658-1662.
24. Schuman EM. 1999. Neurotrophin regulation of synaptic transmission. Curr Opin Neurobiol 9:105-109.
25. Berninger B, Poo M. 1996. Fast actions of neurotrophic factors. Curr Opin Neurobiol 6:324-330.
26. Lessmann V. 1998. Neurotrophin-dependent modulation of glutamatergic synaptic transmission in the mammalian CNS. Gen Pharmacol 31:667-674.
27. Schinder AF, Berninger B, Poo M. 2000. Postsynaptic target specificity of neurotrophin-induced presynaptic potentiation. Neuron 25:151-163.
28. Tyler WJ, Perrett SP, Pozzo-Miller LD. 2002. The role of neurotrophins in neurotransmitter release. Neuroscientist 8:524-531.
29. Berninger B, Poo M-m. 1999. Exciting neurotrophins. Nature 401:862-863.
30. Manabe T. 2002. Does BDNF have pre- or postsynaptic targets? Science 295:1651-1653.
31. Kafitz KW, Rose CR, Thoenen H, Konnerth A. 1999. Neurotrophin-evoked rapid excitation through TrkB receptors. Nature 401:918-921.
32. Blum R, Kafitz KW, Konnerth A. 2002. Neurotrophin-evoked depolarization requires the sodium channel Na(V)1.9. Nature 419:687-693.
33. Rose CR, Blum R, Pichler B, Lepier A, Kafitz KW, et al. 2003. Truncated TrkB-T1 mediates neurotrophin-evoked calcium signalling in glia. Natur 426:74-78.
34. Baxter GT, Radeke MJ, Kuo RC, Makrides V, Hinkle B, et al. 1997. Signal transduction mediated by the truncated trkB receptor isoforms, trkB.T1 and trkB.T2. J Neurosci 17:2683-2690.
35. Haapasalo A, Saarelainen T, Moshnyakov M, Arumae U, Kiema TR, et al. 1999. Expression of the naturally occurring truncated trkB neurotrophin receptor induces outgrowth of filopodia and processes in neuroblastoma cells. Oncogene 18:1285-1296.
36. Kaplan DR, Miller FD. 2000. Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 10:381-391.
37. Widmer HR, Kaplan DR, Rabin SJ, Beck KD, Hefti F, et al. 1993. Rapid phosphorylation of phospholipase C gamma 1 by brain-derived neurotrophic factor and neurotrophin-3 in cultures of embryonic rat cortical neurons. J Neurochem 60:2111-2123.
38. Yamada M, Numakawa T, Koshimizu H, Tanabe K, Wada K, et al. 2002. Distinct usages of phospholipase C gamma and She in intracellular signaling stimulated by neurotrophins. Brain Res 955:183-190.
39. Minichiello L, Calella AM, Medina DL, Bonhoeffer T, Klein R, et al. 2002. Mechanism of TrkB-mediated hippocampal long-term potentiation. Neuron 36:121-137.
40. Tanaka T, Saito H, Matsuki N. 1997. Inhibition of GABAA synaptic responses by brain-derived neurotrophic factor (BDNF) in rat hippocampus. J Neurosci 17:2959-2966.
41. Li HS, Xu XZ, Montell C. 1999. Activation of a TRPC3-dependent cation current through the neurotrophin BDNF. Neuron 24:261-273.
42. Mizoguchi Y, Monji A, Nabekura J. 2002. Brain-derived neurotrophic factor induces long-lasting Ca2+-activated K+ currents in rat visual cortex neurons. Eur J Neurosci 16:1417-24.
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 548:703-709.
44. Kovalchuk Y, Hanse E, Kafitz KW, Konnerth A. 2002. Postsynaptic induction of BDNF-mediated long-term potentiation. Science 295:1729-1734.
45. 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.
46. Un SY, Wu K, Levine ES, Mount HT, Suen PC, et al. 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.
47. 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.
48. Mizuno M, Yamada K, He J, Nakajima A, Nabeshima T. 2003. Involvement of BDNF Receptor TrkB in Spatial Memory Formation. Learn Mem 10:108-115.
49. Jarvis CR, Xiong ZG, Plant JR, Churchill D, Lu WY, et al. 1997. Neurotrophin modulation of NMDA receptors in cultured murine and isolated rat neurons. J Neurophysiol 78:2363-2371.
50. Song DK, Choe B, Bae JH, Park WK, Han IS, et al. 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.
51. Balkowiec A, Kunze D, Katz D. 2000. Brain-derived neurotrophic factor acutely inhibits AMPA-mediated currents in developing sensory relay neurons. J Neurosci 20:1904-1911.
52. Narisawa-Saito M, Iwakura Y, Kawamura M, Araki K, Kozaki S, et al. 2002. Brain-derived neurotrophic factor regulates surface expression of alpha- amino-3-hydroxy-5-methyl-4-isoxazoleproprionic acid receptors by enhancing the N-ethylmaleimide-sensitive factor/GluR2 interaction in developing neocortical neurons. J Biol Chem 277:40901-40910.
53. Itami C, Kimura F, Kohno T, Matsuoka M, Ichikawa M, et al. 2003. Brain-derived neurotrophic factor-dependent unmasking of "silent" synapses in the developing mouse barrel cortex. Proc Natl Acad Sci USA 100:13069-13074.
54. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL. 1989. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416:303-325.
55. Garaschuk O, Hanse E, Konnerth A. 1998. Developmental profile and synaptic origin of early network oscillations in the CA1 region of rat neonatal hippocampus. J Physiol 507:219-236.
56. Brunig I, Penschuck S, Berninger B, Benson J, Fritschy JM. 2001. BDNF reduces miniature inhibitory postsynaptic currents by rapid down-regulation of GABA(A) receptor surface expression. Eur J Neurosci 13:1320-1328.
57. Cheng Q, Yeh HH. 2003. Brain-derived neurotrophic factor attenuates mouse cerebellar granule cell GABAA receptor-mediated responses via postsynaptic mechanisms. J Physiol 14:14.
58. Garaschuk O, Linn J, Eilers J, Konnerth A. 2000. Large-scale oscillatory calcium waves in the immature cortex. Nature Neuroscience 3:452-459.
59. Boxall AR. 2000. GABAergic mIPSCs in rat cerebellar Purkinje cells are modulated by TrkB and mGluR1-mediated stimulation of Src. J Physiol 524:677-684.
60. Wardle RA, Poo MM. 2003. Brain-derived neurotrophic factor modulation of GABAergic synapses by postsynaptic regulation of chloride transport. J Neurosci 23:8722-8732.
61. Jonas EA, Kaczmarek LK. 1996. Regulation of potassium channels by protein kinases. Curr Opin Neurobiol 6:318-323.
62. Catterall WA. 2000. Structure and regulation of voltage-gated Ca2+ channels. Annu Rev Cell Dev Biol 16:521-555.
63. Cantrell AR, Catterall WA. 2001. Neuromodulation of Na+ channels: an unexpected form of cellular plasticity. Nature Rev Neurosci 2:397-407.
64. Tucker K, Fadool DA. 2002. Neurotrophin modulation of voltage-gated potassium channels in rat through TrkB receptors is time and sensory experience dependent. J Physiol 542:413-429.
65. Rogalski SL, Appleyard SM, Pattillo A, Terman GW, Chavkin C. 2000. TrkB activation by brain-derived neurotrophic factor inhibits the G protein-gated inward rectifier Kir3 by tyrosine phosphorylation of the channel. J Biol Chem 275:25082-25088.
66. Ippolito DL, Temkin PA, Rogalski SL, Chavkin C. 2002. N-terminal tyrosine residues within the potassium channel Kir3 modulate GTPase activity of Gai. J Biol Chem 277:32692-32696.
67. Berninger B, Garcia DE, Inagaki N, Hahnel C, Lindholm D. 1993. BDNF and NT-3 induce intracellular Ca2+ elevation in hippocampal neurones. Neuroreport 4:1303-1306.
68. Matsumoto T, Numakawa T, Adachi N, Yokomaku D, Yamagishi S, et al. 2001. Brain-derived neurotrophic factor enhances depolarization-evoked glutamate release in cultured cortical neurons. J Neurochem 79:522-530.
69. Numakawa T, Matsumoto T, Adachi N, Yokomaku D, Kojima M, et al. 2001. Brain-derived neurotrophic factor triggers a rapid glutamate release through increase of intracellular Ca(2+) and Na(+) in cultured cerebellar neurons. J Neurosci Res 66:96-108.
70. Weiger TM, Hermann A, Levitan IB. 2002. Modulation of calcium-activated potassium channels. J Comp Physiol A 188:79-87.
71. Holm NR, Christophersen P, Diesen SP, Gammeltoft S. 1997. Activation of calcium-dependent potassium channels in mouse brain neurons by neurotrophin-3 and nerve growth factor. Proc Natl Acad Sci USA 94:1002-1006.
72. Chuang H, Prescott ED, Kong H, Shields S, Jordt SE, et al. 2001. Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411:957-962.
73. Kafitz KW, Lepier A, Thoenen H, Konnerth A. 2001. Saxitoxin-sensitivity of neurotrophin-induced rapid excitation and neurite growth. Pflügers Arch 441:R125.
74. Catterall WA. 2000. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26:13-25.
75. Dib-Hajj S, Black JA, Cummins TR, Waxman SG. 2002. NaN/Nav1.9: a sodium channel with unique properties. Trends Neurosci 25:253-259.
76. Jeong SY, Goto J, Hashida H, Suzuki T, Ogata K, et al. 2000. Identification of a novel human voltage-gated sodium channel alpha subunit gene, SCN12A. Biochem Biophys Res Commun 267:262-270.
77. Cummins TR, Dib-Hajj SD, Black JA, Akopian AN, Wood JN, et al. 1999. A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons. J Neurosci 19:RC43.
78. Herzog RI, Cummins TR, Waxman SG. 2001. Persistent TTX-resistant Na+ current affects resting potential and response to depolarization in simulated spinal sensory neurons. J Neurophysiol 86:1351-1364.
79. Baker MD, Chandra SY, Ding Y, Waxman SG, Wood JN. 2003. GTP-induced tetrodotoxin-resistant Na+ current regulates excitability in mouse and rat small diameter sensory neurones. J Physiol 548:373-382.
80. Okuse K, Malik-Hall M, Baker MD, Poon WY, Kong H, et al. 2002. Annexin II light chain regulates sensory neuron-specific sodium channel expression. Nature 417:653-656.
81. Barde YA. 2002. Neurobiology: Neurotrophin channels excitement. Nature 419:683-684.
82. Delmas P, Coste B. 2003. Na+ channel Nav1.9: in search of a gating mechanism. Trends Neurosci 26:55-57.
83. Bonhoeffer T. 1996. Neurotrophins and activity-dependent development of the neocortex. Curr Opin Neurobiol 6:119-126.
84. Mellstrom B, Naranjo JR. 2001. Mechanisms of Ca(2+)-dependent transcription. Curr Opin Neurobiol 11:312-319.
85. West AE, Chen WG, Dalva MB, Dolmetsch RE, Kornhauser JM, et al. 2001. Calcium regulation of neuronal gene expression. Proc Natl Acad Sci USA 98:11024-11031.
86. Farnsworth C, Freshnaey N, Rosen L, Ghosh A, Greenberg ME, et al. 1995. Calcium activation of Ras mediated by neuronal exchange factor Ras-GRF. Nature 376:524-527.
87. Cullen P, Lockyer P. 2002. Integration of calicum and Ras signalling. Nat Rev Mol Cell Biol 3:339-348.