Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Synapse- and Stimulus-Specific Local Translation During Long-Term Neuronal Plasticity
Dan Ohtan Wang,1
Sang Mok Kim,1,2
Yali Zhao,1
Hongik Hwang,1
Satoru K. Miura,3
Wayne S. Sossin,6
Kelsey C. Martin1,3,4,5,*
Abstract:
Long-term memory and synaptic plasticity require changes ingene expression and yet can occur in a synapse-specific manner.Messenger RNA localization and regulated translation at synapsesare thus critical for establishing synapse specificity. Usinglive-cell microscopy of photoconvertible fluorescent proteintranslational reporters, we directly visualized local translationat synapses during long-term facilitation of Aplysia sensory-motorsynapses. Translation of the reporter required multiple applicationsof serotonin, was spatially restricted to stimulated synapses,was transcript- and stimulus-specific, and occurred during long-termfacilitation but not during long-term depression of sensory-motorsynapses. Translational regulation only occurred in the presenceof a chemical synapse and required calcium signaling in thepostsynaptic motor neuron. Thus, highly regulated local translationoccurs at synapses during long-term plasticity and requirestrans-synaptic signals.
1 Department of Psychiatry and Biobehavioral Sciences, University of California–Los Angeles (UCLA), BSRB 390B, 615 Charles E. Young Drive South, Los Angeles, CA 90095–1737, USA. 2 Interdepartmental Program in Neurosciences, UCLA, BSRB 390B, 615 Charles E. Young Drive South, Los Angeles, CA 90095–1737, USA. 3 Department of Biological Chemistry, UCLA, BSRB 310, 615 Charles E. Young Drive South, Los Angeles, CA 90095–1737, USA. 4 Semel Institute for Neuroscience and Human Behavior, UCLA, BSRB 390B, 615 Charles E. Young Drive South, Los Angeles, CA 90095–1737, USA. 5 Brain Research Institute, UCLA, BSRB 390B, 615 Charles E. Young Drive South, Los Angeles, CA 90095–1737, USA. 6 Montreal Neurological Institute, McGill University, 3801 University Street, Montreal, Quebec H3A-2B4, Canada.
* To whom correspondence should be addressed. E-mail: kcmartin{at}mednet.ucla.edu
The editors suggest the following Related Resources on Science sites:
In Science Magazine
PERSPECTIVES
Martin Korte (19 June 2009) Science324 (5934), 1527.
[DOI: 10.1126/science.1176484] |Summary »|Full Text »|PDF »
In Science Signaling
EDITORS' CHOICE
Stella M. Hurtley (23 June 2009) Sci. Signal.2 (76), ec208.
[DOI: 10.1126/scisignal.276ec208] |Abstract »
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
A strategy to capture and characterize the synaptic transcriptome.
S. V. Puthanveettil, I. Antonov, S. Kalachikov, P. Rajasethupathy, Y.-B. Choi, A. B. Kohn, M. Citarella, F. Yu, K. A. Karl, M. Kinet, et al. (2013)
PNAS
110, 7464-7469
|Abstract »|Full Text »|PDF »
MAPK Establishes a Molecular Context That Defines Effective Training Patterns for Long-Term Memory Formation.
G. T. Philips, X. Ye, A. M. Kopec, and T. J. Carew (2013)
J. Neurosci.
33, 7565-7573
|Abstract »|Full Text »|PDF »
Imaging Translation in Single Cells Using Fluorescent Microscopy.
J. A. Chao, Y. J. Yoon, and R. H. Singer (2012)
Cold Spring Harb Perspect Biol
4, a012310
|Abstract »|Full Text »|PDF »
Regulation of Neuronal Excitability by Interaction of Fragile X Mental Retardation Protein with Slack Potassium Channels.
Y. Zhang, M. R. Brown, C. Hyland, Y. Chen, J. Kronengold, M. R. Fleming, A. B. Kohn, L. L. Moroz, and L. K. Kaczmarek (2012)
J. Neurosci.
32, 15318-15327
|Abstract »|Full Text »|PDF »
Serotonin-Induced Cleavage of the Atypical Protein Kinase C Apl III in Aplysia.
J. K. Bougie, D. Cai, M. Hastings, C. A. Farah, S. Chen, X. Fan, P. K. McCamphill, D. L. Glanzman, and W. S. Sossin (2012)
J. Neurosci.
32, 14630-14640
|Abstract »|Full Text »|PDF »
Localization of molecular correlates of memory consolidation to buccal ganglia mechanoafferent neurons after learning that food is inedible in Aplysia.
D. Levitan, R. Saada-Madar, A. Teplinsky, and A. J. Susswein (2012)
Learn. Mem.
19, 503-512
|Abstract »|Full Text »|PDF »
Principles and roles of mRNA localization in animal development.
Relationship of Axonal Voltage-gated Sodium Channel 1.8 (NaV1.8) mRNA Accumulation to Sciatic Nerve Injury-induced Painful Neuropathy in Rats.
S. Ruangsri, A. Lin, Y. Mulpuri, K. Lee, I. Spigelman, and I. Nishimura (2011)
J. Biol. Chem.
286, 39836-39847
|Abstract »|Full Text »|PDF »
Tonic Dopamine Induces Persistent Changes in the Transient Potassium Current through Translational Regulation.
E. W. Rodgers, W.-D. C. Krenz, and D. J. Baro (2011)
J. Neurosci.
31, 13046-13056
|Abstract »|Full Text »|PDF »
The Ataxin-2 protein is required for microRNA function and synapse-specific long-term olfactory habituation.
C. McCann, E. E. Holohan, S. Das, A. Dervan, A. Larkin, J. A. Lee, V. Rodrigues, R. Parker, and M. Ramaswami (2011)
PNAS
108, E655-E662
|Abstract »|Full Text »|PDF »
microRNA-Seq reveals cocaine-regulated expression of striatal microRNAs.
J. E. Eipper-Mains, D. D. Kiraly, D. Palakodeti, R. E. Mains, B. A. Eipper, and B. R. Graveley (2011)
RNA
17, 1529-1543
|Abstract »|Full Text »|PDF »
Rapid increase in clusters of synaptophysin at onset of homosynaptic potentiation in Aplysia.
Whereas short-term facilitation is presynaptic, intermediate-term facilitation involves both presynaptic and postsynaptic protein kinases and protein synthesis.