Brain-derived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo

Journal of Neuroscience

Volumn 22, Issue 17, 2002, Pages 7453-7461

  Messaoudi, Elhoucine ^a   Ying, Shui Wang ^a,c   Kanhema, Tambudzai ^a   Croll, Susan D ^b   Bramham, Clive R ^a  

^a UNIVERSITY OF BERGEN   (Norway)

^b REGENERON PHARMACEUTICALS INC   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Activity regulated cytoskeleton associated protein (Arc); Brain derived neurotrophic factor (BDNF); Dentate gyrus; Gene expression; Hippocampus; Long term potentiation (LTP); Neurotrophin; Synaptic plasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DACTINOMYCIN; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; GENE ACTIVITY; GRANULE CELL; IMMEDIATE EARLY GENE; LONG TERM POTENTIATION; NONHUMAN; PERFORANT NERVE TRACT; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SYNAPSE; SYNAPTIC TRANSMISSION; TISSUE DISTRIBUTION;

EID: 0036759627     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-17-07453.2002     Document Type: Article

References (70)

1. Aakalu G, Smith WB, Nguyen N, Jiang C, Schuman EM (2001) Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 30:489-502.
2. Abraham WC, Mason SE (1988) Effects of the NMDA receptor/channel antagonists CPP and MK801 on hippocampal field potentials and long-term potentiation in anesthetized rats. Brain Res 462:40-46.
3. Abraham WC, Gustafsson B, Wigstrom H (1987) Long-term potentiation involves enhanced synaptic excitation relative to synaptic inhibition in guinea-pig hippocampus. J Physiol (Lond) 394:367-380.
4. Aoki C, Wu K, Elste A, Len G, Lin S, McAuliffe G, Black IB (2000) Localization of brain-derived neurotrophic factor and TrkB receptors to postsynaptic densities of adult rat cerebral cortex. J Neurosci Res 59:454-463.
5. Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM, Sweatt JD (1998) The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1:602-609.
6. Bibel M, Barde YA (2000) Neurotrophins: Key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev 14:2919-2937.
7. Biffo S, Offenhauser N, Carter BD, Barde YA (1995) Selective binding and internalisation by truncated receptors restrict the availability of BDNF during development. Development 121:2461-2470.
8. Binder DK, Croll SD, Gall CM, Scharfman HE (2001) BDNF and epilepsy: Too much of a good thing? Trends Neurosci 24:47-53.
9. Bliss TV, Collingridge GL (1993) A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361:31-39.
10. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:331-356.
11. Bramham CR, Milgram NW, Srebro B (1991) Activation of AP5-sensitive NMDA receptors is not required to induce LTP of synaptic transmission in the lateral perforant path. Eur J Neurosci 3:1300-1308.
12. Bramham CR, Southard T, Sarvey JM, Herkenham M, Brady LS (1996) Unilateral LTP triggers bilateral increases in hippocampal neurotrophin and trk receptor mRNA expression in behaving rats: Evidence for interhemispheric communication. J Comp Neurol 368:371-382.
13. Bramham CR, Messaoudi E, Bårdsen K (2002) Neurotophins and synaptic plasticity in the adult hippocampus. In: Site-selective Neurotoxicity (Lester DS, Slikker W, Lazarovici P, eds), pp 61-77. London: Taylar and Francis.
14. Chen G, Kolbeck R, Barde YA, Bonhoeffer T, Kossel A (1999 Relative contribution of endogenous neurotrophins in hippocampal long-term potentiation. J Neurosci 19:7983-7990.
15. Chowdhury S, Lyford GL, Steward O, Wallace C, Lanahan A, Worley P (1998) Arc, a neuronal immediate early gene, interacts with the association domain of CaMKII. Soc Neurosci Abstr 24:2021.
16. Croll SD, Chesnutt CR, Rudge JS, Acheson A, Ryan TE, Siuciak JA, DiStefano PS, Wiegand SJ, Lindsay RM (1998) Co-infusion with a TrkB-Fc receptor body carrier enhances BDNF distribution in the adult rat brain. Exp Neurol 152:1-15.
17. Crozier RA, Black IB, Plummer MR (1999) Blockade of NR2B-containing NMDA receptors prevents BDNF enhancement of glutamatergic transmission in hippocampal neurons. Learn Mem 6:257-266.
18. Davis S, Vanhoutte P, Pages C, Caboche J, Laroche S (2000) The MAPK/ERK cascade targets both Elk-1 and cAMP response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. J Neurosci 20:4563-4572.
19. Drake CT, Milner TA, Patterson SL (1999) Ultrastructural localization of full-length trkB immunoreactivity in rat hippocampus suggests multiple roles in modulating activity-dependent synaptic plasticity. J Neurosci 19:8009-8026.
20. Errington ML, Lynch MA, Bliss TV (1987) Long-term potentiation in the dentate gyrus: Induction and increased glutamate release are blocked by D(-)aminophosphonovalerate. Neuroscience 20:279-284.
21. Figurov A, Po Omillerzz 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.
22. French PJ, O'Connor V, Jones MW, Davis S, Errington ML, Voss K, Truchet B, Wotjak C, Stean T, Doyere V, Maroun M, Laroche S, Bliss TV (2001) Subfield-specific immediate early gene expression associated with hippocampal long-term potentiation in vivo. Eur J Neurosci 13:968-976.
23. Frerking M, Malenka RC, Nicoll RA (1998) Brain-derived neurotrophic factor (BDNF) modulates inhibitory, but not excitatory, transmission in the CA1 region of the hippocampus. J Neurophysiol 80:3383-3386.
24. Frey U, Schollmeier K, Reymann KG, Seidenbecher T (1995) Asymptotic hippocampal long-term potentiation in rats does not preclude additional potentiation at later phases. Neuroscience 67:799-807.
25. Frey U, Frey S, Schollmeier F, Krug M (1996) Influence of actinomycin D, a RNA synthesis inhibitor, on long-term potentiation in rat hippocampal neurons in vivo and in vitro. J Physiol (Lond) 490:703-711.
26. Gooney M, Lynch MA (2001) Long-term potentiation in the dentate gyrus of the rat hippocampus is accompanied by brain-derived neurotrophic factor-induced activation of TrkB. J Neurochem 77:1198-1207.
27. Gottschalk W, Pozzo-Miller LD, Figurov A, Lu B (1998) Presynaptic modulation of synaptic transmission and plasticity by brain-derived neurotrophic factor in the developing hippocampus. J Neurosci 18:6830-6839.
28. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, McGaugh JL, Worley PF, Barnes CA (2000) Inhibition of activity-dependent are protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 20:3993-4001.
29. Hartmann M, Heumann R, Lessmann V (2001) Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J 20:5887-5897.
30. 2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 21:869-883.
31. Jovanovic JN, Czernik AJ, Fienberg AA, Greengard P, Sihra TS (2000) Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nat Neurosci 3:323-329.
32. Kafitz KW, Rose CR, Thoenen H, Konnerth A (1999) Neurotrophin-evoked rapid excitation through TrkB receptors. Nature 401:918-921.
33. Kang H, Schuman EM (1995) Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267:1658-1662.
34. Kang H, Schuman EM (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273:1402-1406.
35. Kang HJ, Jia LZ, Suh K-Y, Tang L, Schuman EM (1996) Determinants of BDNF-induced hippocampal synaptic plasticity: Role of the Trk B receptor and the kinetics of neurotrophin delivery. Learn Mem 3:188-196.
36. Kang H, Welcher AA, Shelton D, Schuman EM (1997) Neurotrophins and time: Different roles for TrkB signaling in hippocampal long-term potentiation. Neuron 19:653-664.
37. Kanhema T, Ying SW, Nairn AC, Bramham CR (2001) BDNF-induced long-term potentiation in the dentate gyrus in vivo is associated with phosphorylation of elongation factor-2. Soc Neurosci Abstr 27:920.17.
38. Korte M, Kang H, Bonhoeffer T, Schuman EM (1998) A role for BDNF in the late-phase of hippocampal long-term potentiation. Neuropharmacology 37:553-559.
39. Kossel AH, Cambridge SB, Wagner U, Bonhoeffer T (2001) A caged Ab reveals an immediate/instructive effect of BDNF during hippocampal synaptic potentiation. Proc Natl Acad Sci USA 98:14702-14707.
40. Krug M, Lossner B, Ott T (1984) Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res Bull 13:39-42.
41. 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 pre-established paired-pulse facilitation. Neuroscience 86:399-413.
42. Lessmann V, Gottmann K, Heumann R (1994) BDNF and NT-4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones. NeuroReport 6:21-25.
43. 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.
44. Li YX, Xu Y, Ju D, Lester HA, Davidson N, Schuman EM (1998) 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 95:10884-10889.
45. Link W, Konietzko U, Kauselmann G, Krug M, Schwanke B, Frey U, Kuhl D (1995) Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc Natl Acad Sci USA 92:5734-5738.
46. Lu YM, Mansuy IM, Kandel ER, Roder J (2000) Calcineurin-mediated LTD of GABAergic inhibition underlies the increased excitability of CA1 neurons associated with LTP. Neuron 26:197-205.
47. Lyford GL, Yamagata K, Kaufmann WE, Barnes CA, Sanders LK, Copeland NG, Gilbert DJ, Jenkins NA, Lanahan AA, Worley PF (1995) Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14:433-445.
48. Matthies H, Frey U, Reymann K, Krug M, Jork R, Schroeder H (1990) Different mechanisms and multiple stages of LTP. Adv Exp Med Biol 268:359-368.
49. Messaoudi E, Bardsen K, Srebro B, Bramham CR (1998) Acute intrahippocampal infusion of BDNF induces lasting potentiation of synaptic transmission in the rat dentate gyrus. J Neurophysiol 79:496-499.
50. Minichiello L, Korte M, Wolfer D, Kuhn R, Unsicker K, Cestari V, Rossi AC, Lipp HP, Bonhoeffer T, Klein R (1999) Essential role for TrkB receptors in hippocampus-mediated learning. Neuron 24:401-414.
51. Morse JK, Wiegand SJ, Anderson K, You Y, Cai N, Carnahan J, Miller J, DiStefano PS, Altar CA, Lindsay RM (1993) Brain-derived neurotrophic factor (BDNF) prevents the degeneration of medial septal cholinergic neurons following fimbria transection. J Neurosci 13:4146-4156.
52. Nguyen PV, Kandel ER (1996) A macromolecular synthesis-dependent late phase of long-term potentiation requiring cAMP in the medial perforant pathway of rat hippocampal slices. J Neurosci 16:3189-3198.
53. Patterson SL, Abel T, Deuel TA, 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.
54. Patterson SL, Pittenger C, Morozov A, Martin KC, Scanlin H, Drake C, Kandel ER (2001) Some forms of cAMP-mediated long-lasting potentiation are associated with release of BDNF and nuclear translocation of phospho-MAP kinase. Neuron 32:123-140.
55. 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.
56. Rosenblum K, Futter M, Voss K, Eernt M, Skehel PA, French PJ, Obosi L, Jones MW, Bliss TVP (2002) The role of extracellular regulated kinases I/II in late-phase long-term potentiation. J Neurosci 22:5432-5441.
57. Schinder AF, Poo MM (2000) The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci 23:639-645.
58. Schuman EM (1999) Neurotrophin regulation of synaptic transmission. Curr Opin Neurobiol 9:105-109.
59. Song HJ, Poo MM (1999) Signal transduction underlying growth cone guidance by diffusible factors. Curr Opin Neurobiol 9:355-363.
60. Steward O, Schuman EM (2001) Protein synthesis at synaptic sites on dendrites. Annu Rev Neurosci 24:299-325.
61. Takei N, Kawamura M, Hara K, Yonezawa K, Nawa H (2001) Brain-derived neurotrophic factor enhances neuronal translation by activating multiple initiation processes: Comparison with the effects of insulin. J Biol Chem 276:42818-42825.
62. Tang SJ, Reis G, Kang H, Gingras AC, Sonenberg N, Schuman EM (2002) A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc Natl Acad Sci USA 99:467-472.
63. Thoenen H (1995) Neurotrophins and neuronal plasticity. Science 270:593-598.
64. Valentine G, Chakravarty S, Sarvey J, Bramham C, Herkenham M (2000) Fragile X (fmr1) mRNA expression is differentially regulated in two adult models of activity-dependent gene expression. Brain Res Mol Brain Res 75:337-341.
65. Villarreal DM, Do V, Haddad E, Derrick BE (2002) NMDA receptor antagonists sustain LTP and spatial memory: Active processes mediate LTP decay. Nat Neurosci 5:48-52.
66. Watson RE, Wiegand SJ, Clogh RW, Hoffman GE (1986) Use of cryo-protectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 7:155-159.
67. Williams JM, Mason-Parker SE, Abraham WC, Tate WP (1998) Biphasic changes in the levels of N-methyl-D-aspartate receptor-2 subunits correlate with the induction and persistence of long-term potentiation. Brain Res Mol Brain Res 60:21-27.
68. Xu B, Gottschalk W, Chow A, Wilson RI, Schnell E, Zang K, Wang D, Nicoll RA, Lu B, Reichardt LF (2000) The role of brain-derived neurotrophic factor receptors in the mature hippocampus: Modulation of long-term potentiation through a presynaptic mechanism involving TrkB. J Neurosci 20:6888-6897.
69. Yin Y, Edelman GM, Vanderklish PW (2002) The brain-derived neurotrophic factor enhances synthesis of Arc in synaptoneurosomes. Proc Natl Acad Sci USA 99:2368-2373.
70. Ying SW, Futter M, Rosenblum K, Webber MJ, Hunt SP, Bliss TV, Bramham CR (2002) Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: Requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. J Neurosci 22:1532-1540.