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Subcellular and regional localization of mRNA translation in midbrain dopamine neurons

Benjamin D. Hobson, Linghao Kong, Maria Florencia Angelo, Ori J. Lieberman, Eugene V. Mosharov, Etienne Herzog, David Sulzer, Peter A. Sims
doi: https://doi.org/10.1101/2021.07.30.454065
Benjamin D. Hobson
1Department of Systems Biology, Columbia University Irving Medical Center, New York, NY 10032
2Medical Scientist Training Program, Columbia University Irving Medical Center, New York, NY 10032
6Department of Psychiatry, Columbia University Irving Medical Center, New York, NY 10032
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Linghao Kong
1Department of Systems Biology, Columbia University Irving Medical Center, New York, NY 10032
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Maria Florencia Angelo
3Interdisciplinary Institute for Neuroscience, Université de Bordeaux, Bordeaux, France
4Interdisciplinary Institute for Neuroscience, CNRS UMR 5297, Bordeaux, France
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Ori J. Lieberman
2Medical Scientist Training Program, Columbia University Irving Medical Center, New York, NY 10032
6Department of Psychiatry, Columbia University Irving Medical Center, New York, NY 10032
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Eugene V. Mosharov
6Department of Psychiatry, Columbia University Irving Medical Center, New York, NY 10032
8Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY 10032
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Etienne Herzog
3Interdisciplinary Institute for Neuroscience, Université de Bordeaux, Bordeaux, France
4Interdisciplinary Institute for Neuroscience, CNRS UMR 5297, Bordeaux, France
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  • For correspondence: pas2182@cumc.columbia.edu ds43@cumc.columbia.edu etienne.herzog@u-bordeaux.fr
David Sulzer
5Department of Neurology, Columbia University Irving Medical Center, New York, NY 10032
6Department of Psychiatry, Columbia University Irving Medical Center, New York, NY 10032
7Department of Pharmacology, Columbia University Irving Medical Center, New York, NY 10032
8Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY 10032
11Aligning Science Across Parkinson’s (ASAP) Collaborative Research Network, Chevy Chase, MD
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  • For correspondence: pas2182@cumc.columbia.edu ds43@cumc.columbia.edu etienne.herzog@u-bordeaux.fr
Peter A. Sims
1Department of Systems Biology, Columbia University Irving Medical Center, New York, NY 10032
9Department of Biochemistry & Molecular Biophysics, Columbia University Irving Medical Center, New York, NY 10032
10Sulzberger Columbia Genome Center, Columbia University Irving Medical Center, New York, NY 10032
11Aligning Science Across Parkinson’s (ASAP) Collaborative Research Network, Chevy Chase, MD
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  • For correspondence: pas2182@cumc.columbia.edu ds43@cumc.columbia.edu etienne.herzog@u-bordeaux.fr
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Abstract

Local translation within excitatory and inhibitory neurons is involved in neuronal development and synaptic plasticity. Despite the extensive dendritic and axonal arborizations of central monoaminergic neurons, the subcellular localization of protein synthesis is not well-characterized in these populations. Here, we investigated mRNA localization and translation in midbrain dopaminergic (mDA) neurons, cells with enormous axonal and dendritic projections, both of which exhibit stimulation-evoked dopamine (DA) release. Using highly-sensitive ribosome-bound RNA-sequencing and imaging approaches in mDA axons, we found no evidence for axonal mRNA localization or translation. In contrast, mDA neuronal dendritic projections into the substantia nigra reticulata (SNr) contain ribosomes and mRNAs encoding the major components of DA synthesis, release, and reuptake machinery. Surprisingly, we also observed dendritic localization of mRNAs encoding synaptic vesicle-related proteins, including those involved in vesicular exocytic fusion. Our results are consistent with a role for local translation in the regulation of DA release from dendrites, but not from axons. Our translatome data further defined a molecular signature of the sparse mDA neurons resident in the SNr, including enrichment of Atp2a3/SERCA3, an ER calcium pump previously undescribed in mDA neurons.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵12 Co-Senior Author

  • https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE180913

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted August 01, 2021.
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Subcellular and regional localization of mRNA translation in midbrain dopamine neurons
Benjamin D. Hobson, Linghao Kong, Maria Florencia Angelo, Ori J. Lieberman, Eugene V. Mosharov, Etienne Herzog, David Sulzer, Peter A. Sims
bioRxiv 2021.07.30.454065; doi: https://doi.org/10.1101/2021.07.30.454065
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Subcellular and regional localization of mRNA translation in midbrain dopamine neurons
Benjamin D. Hobson, Linghao Kong, Maria Florencia Angelo, Ori J. Lieberman, Eugene V. Mosharov, Etienne Herzog, David Sulzer, Peter A. Sims
bioRxiv 2021.07.30.454065; doi: https://doi.org/10.1101/2021.07.30.454065

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