The Brain-derived Neurotrophic Factor Enhances Synthesis of Arc in Synaptoneurosomes

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2002 Feb 14

PMID 11842217

Citations 112

Authors

Yong Yin

Gerald M Edelman

Peter W Vanderklish

Affiliations

Soon will be listed here.

Abstract

Protein synthesis in neurons is essential for the consolidation of memory and for the stabilization of activity-dependent forms of synaptic plasticity such as long-term potentiation (LTP). Activity-dependent translation of dendritically localized mRNAs has been proposed to be a critical source of new proteins necessary for synaptic change. mRNA for the activity-regulated cytoskeletal protein, Arc, is transcribed during LTP and learning, and disruption of its translation gives rise to deficits in both. We have found that selective translation of Arc in a synaptoneurosomal preparation is induced by the brain-derived neurotrophic factor, a neurotrophin that is released during high-frequency stimulation patterns used to elicit LTP. This effect involves signaling through the TrkB receptor and is blocked by the N-methyl-d-aspartate-type glutamate receptor antagonist, MK801. The results suggest there is a synergy between neurotrophic and ionotropic mechanisms that may influence the specificity and duration of changes in synaptic efficacy at glutamatergic synapses.

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References

Gooney M, Lynch M . Long-term potentiation in the dentate gyrus of the rat hippocampus is accompanied by brain-derived neurotrophic factor-induced activation of TrkB. J Neurochem. 2001; 77(5):1198-207. DOI: 10.1046/j.1471-4159.2001.00334.x. View

Lessmann V . Neurotrophin-dependent modulation of glutamatergic synaptic transmission in the mammalian CNS. Gen Pharmacol. 1998; 31(5):667-74. DOI: 10.1016/s0306-3623(98)00190-6. View

Pinkstaff J, Chappell S, Mauro V, Edelman G, Krushel L . Internal initiation of translation of five dendritically localized neuronal mRNAs. Proc Natl Acad Sci U S A. 2001; 98(5):2770-5. PMC: 30214. DOI: 10.1073/pnas.051623398. View

Levine E, Kolb J . Brain-derived neurotrophic factor increases activity of NR2B-containing N-methyl-D-aspartate receptors in excised patches from hippocampal neurons. J Neurosci Res. 2000; 62(3):357-62. DOI: 10.1002/1097-4547(20001101)62:3<357::AID-JNR5>3.0.CO;2-6. View

Lyford G, Yamagata K, Kaufmann W, Barnes C, Sanders L, Copeland N . Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron. 1995; 14(2):433-45. DOI: 10.1016/0896-6273(95)90299-6. View

Kang H, Schuman E . Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science. 1995; 267(5204):1658-62. DOI: 10.1126/science.7886457. View

Wu L, Wells D, Tay J, Mendis D, Abbott M, Barnitt A . CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of alpha-CaMKII mRNA at synapses. Neuron. 1998; 21(5):1129-39. DOI: 10.1016/s0896-6273(00)80630-3. View

Aakalu G, Smith W, Nguyen N, Jiang C, Schuman E . Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron. 2001; 30(2):489-502. DOI: 10.1016/s0896-6273(01)00295-1. View

Galabru J, Hovanessian A . Autophosphorylation of the protein kinase dependent on double-stranded RNA. J Biol Chem. 1987; 262(32):15538-44. View

10.

Guillin O, Diaz J, Carroll P, Griffon N, Schwartz J, Sokoloff P . BDNF controls dopamine D3 receptor expression and triggers behavioural sensitization. Nature. 2001; 411(6833):86-9. DOI: 10.1038/35075076. View

11.

Lin S, Wu K, Levine E, Mount H, Suen P, Black I . BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities. Brain Res Mol Brain Res. 1998; 55(1):20-7. DOI: 10.1016/s0169-328x(97)00349-5. View

12.

Causing C, Gloster A, Aloyz R, Bamji S, Chang E, Fawcett J . Synaptic innervation density is regulated by neuron-derived BDNF. Neuron. 1997; 18(2):257-67. DOI: 10.1016/s0896-6273(00)80266-4. View

13.

Ghosh A, Carnahan J, Greenberg M . Requirement for BDNF in activity-dependent survival of cortical neurons. Science. 1994; 263(5153):1618-23. DOI: 10.1126/science.7907431. View

14.

Loeb J, Fischbach G . Neurotrophic factors increase neuregulin expression in embryonic ventral spinal cord neurons. J Neurosci. 1997; 17(4):1416-24. PMC: 6793741. View

15.

Kohara K, Kitamura A, Morishima M, Tsumoto T . Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science. 2001; 291(5512):2419-23. DOI: 10.1126/science.1057415. View

16.

Isackson P, Huntsman M, Murray K, Gall C . BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distinct from NGF. Neuron. 1991; 6(6):937-48. DOI: 10.1016/0896-6273(91)90234-q. View

17.

Steward O, Schuman E . Protein synthesis at synaptic sites on dendrites. Annu Rev Neurosci. 2001; 24:299-325. DOI: 10.1146/annurev.neuro.24.1.299. View

18.

Weiler I, Greenough W . Potassium ion stimulation triggers protein translation in synaptoneurosomal polyribosomes. Mol Cell Neurosci. 2009; 2(4):305-14. DOI: 10.1016/1044-7431(91)90060-2. View

19.

Tartaglia N, Du J, Tyler W, Neale E, Lu B . Protein synthesis-dependent and -independent regulation of hippocampal synapses by brain-derived neurotrophic factor. J Biol Chem. 2001; 276(40):37585-93. DOI: 10.1074/jbc.M101683200. View

20.

Scheetz A, Nairn A, Constantine-Paton M . NMDA receptor-mediated control of protein synthesis at developing synapses. Nat Neurosci. 2000; 3(3):211-6. DOI: 10.1038/72915. View