Axon TRAP reveals learning-associated alterations in cortical axonal mRNAs in the lateral amygdala
Local translation can support memory consolidation by supplying new proteins to synapses undergoing plasticity. Translation in adult forebrain dendrites is an established mechanism of synaptic plasticity and is regulated by learning, yet there is no evidence for learning-regulated protein synthesis...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2019-12-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/51607 |
| _version_ | 1811236915469352960 |
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| author | Linnaea E Ostroff Emanuela Santini Robert Sears Zachary Deane Rahul N Kanadia Joseph E LeDoux Tenzin Lhakhang Aristotelis Tsirigos Adriana Heguy Eric Klann |
| author_facet | Linnaea E Ostroff Emanuela Santini Robert Sears Zachary Deane Rahul N Kanadia Joseph E LeDoux Tenzin Lhakhang Aristotelis Tsirigos Adriana Heguy Eric Klann |
| author_sort | Linnaea E Ostroff |
| collection | DOAJ |
| description | Local translation can support memory consolidation by supplying new proteins to synapses undergoing plasticity. Translation in adult forebrain dendrites is an established mechanism of synaptic plasticity and is regulated by learning, yet there is no evidence for learning-regulated protein synthesis in adult forebrain axons, which have traditionally been believed to be incapable of translation. Here, we show that axons in the adult rat amygdala contain translation machinery, and use translating ribosome affinity purification (TRAP) with RNASeq to identify mRNAs in cortical axons projecting to the amygdala, over 1200 of which were regulated during consolidation of associative memory. Mitochondrial and translation-related genes were upregulated, whereas synaptic, cytoskeletal, and myelin-related genes were downregulated; the opposite effects were observed in the cortex. Our results demonstrate that axonal translation occurs in the adult forebrain and is altered after learning, supporting the likelihood that local translation is more a rule than an exception in neuronal processes. |
| first_indexed | 2024-04-12T12:16:19Z |
| format | Article |
| id | doaj.art-0842f325d6e44b5a8e50779761297646 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T12:16:19Z |
| publishDate | 2019-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-0842f325d6e44b5a8e507797612976462022-12-22T03:33:24ZengeLife Sciences Publications LtdeLife2050-084X2019-12-01810.7554/eLife.51607Axon TRAP reveals learning-associated alterations in cortical axonal mRNAs in the lateral amygdalaLinnaea E Ostroff0https://orcid.org/0000-0002-3348-342XEmanuela Santini1Robert Sears2Zachary Deane3Rahul N Kanadia4Joseph E LeDoux5Tenzin Lhakhang6Aristotelis Tsirigos7Adriana Heguy8Eric Klann9https://orcid.org/0000-0001-7379-6802Department of Physiology and Neurobiology, University of Connecticut, Storrs, United StatesDepartment of Neuroscience, Karolinska Institutet, Solna, SwedenCenter for Neural Science, New York University, New York, United States; Emotional Brain Institute, Nathan Kline Institute for Psychiatry Research, Orangeburg, United States; Department of Child and Adolescent Psychiatry, New York University School of Medicine, New York, United StatesDepartment of Physiology and Neurobiology, University of Connecticut, Storrs, United StatesDepartment of Physiology and Neurobiology, University of Connecticut, Storrs, United StatesCenter for Neural Science, New York University, New York, United States; Emotional Brain Institute, Nathan Kline Institute for Psychiatry Research, Orangeburg, United StatesApplied Bioinformatics Laboratories, New York University School of Medicine, New York, United StatesApplied Bioinformatics Laboratories, New York University School of Medicine, New York, United States; Department of Pathology, New York University School of Medicine, New York, United StatesDepartment of Pathology, New York University School of Medicine, New York, United States; Genome Technology Center, New York University School of Medicine, New York, United StatesCenter for Neural Science, New York University, New York, United StatesLocal translation can support memory consolidation by supplying new proteins to synapses undergoing plasticity. Translation in adult forebrain dendrites is an established mechanism of synaptic plasticity and is regulated by learning, yet there is no evidence for learning-regulated protein synthesis in adult forebrain axons, which have traditionally been believed to be incapable of translation. Here, we show that axons in the adult rat amygdala contain translation machinery, and use translating ribosome affinity purification (TRAP) with RNASeq to identify mRNAs in cortical axons projecting to the amygdala, over 1200 of which were regulated during consolidation of associative memory. Mitochondrial and translation-related genes were upregulated, whereas synaptic, cytoskeletal, and myelin-related genes were downregulated; the opposite effects were observed in the cortex. Our results demonstrate that axonal translation occurs in the adult forebrain and is altered after learning, supporting the likelihood that local translation is more a rule than an exception in neuronal processes.https://elifesciences.org/articles/51607local translationamygdalatranslatomeaxonal translationmemory consolidation |
| spellingShingle | Linnaea E Ostroff Emanuela Santini Robert Sears Zachary Deane Rahul N Kanadia Joseph E LeDoux Tenzin Lhakhang Aristotelis Tsirigos Adriana Heguy Eric Klann Axon TRAP reveals learning-associated alterations in cortical axonal mRNAs in the lateral amygdala eLife local translation amygdala translatome axonal translation memory consolidation |
| title | Axon TRAP reveals learning-associated alterations in cortical axonal mRNAs in the lateral amygdala |
| title_full | Axon TRAP reveals learning-associated alterations in cortical axonal mRNAs in the lateral amygdala |
| title_fullStr | Axon TRAP reveals learning-associated alterations in cortical axonal mRNAs in the lateral amygdala |
| title_full_unstemmed | Axon TRAP reveals learning-associated alterations in cortical axonal mRNAs in the lateral amygdala |
| title_short | Axon TRAP reveals learning-associated alterations in cortical axonal mRNAs in the lateral amygdala |
| title_sort | axon trap reveals learning associated alterations in cortical axonal mrnas in the lateral amygdala |
| topic | local translation amygdala translatome axonal translation memory consolidation |
| url | https://elifesciences.org/articles/51607 |
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