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Articles, Neurobiology of Disease

Mapping the Subcellular Distribution of α-Synuclein in Neurons using Genetically Encoded Probes for Correlated Light and Electron Microscopy: Implications for Parkinson's Disease Pathogenesis

Daniela Boassa, Monica L. Berlanga, Mary Ann Yang, Masako Terada, Junru Hu, Eric A. Bushong, Minju Hwang, Eliezer Masliah, Julia M. George and Mark H. Ellisman
Journal of Neuroscience 6 February 2013, 33 (6) 2605-2615; https://doi.org/10.1523/JNEUROSCI.2898-12.2013
Daniela Boassa
1National Center for Microscopy and Imaging Research and Center for Research on Biological Systems and
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Monica L. Berlanga
1National Center for Microscopy and Imaging Research and Center for Research on Biological Systems and
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Mary Ann Yang
3Department of Cell and Developmental Biology, University of Illinois, Urbana, Illinois 61801
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Masako Terada
1National Center for Microscopy and Imaging Research and Center for Research on Biological Systems and
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Junru Hu
1National Center for Microscopy and Imaging Research and Center for Research on Biological Systems and
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Eric A. Bushong
1National Center for Microscopy and Imaging Research and Center for Research on Biological Systems and
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Minju Hwang
1National Center for Microscopy and Imaging Research and Center for Research on Biological Systems and
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Eliezer Masliah
2Department of Neurosciences, University of California, San Diego, La Jolla, California 92093, and
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Julia M. George
3Department of Cell and Developmental Biology, University of Illinois, Urbana, Illinois 61801
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Mark H. Ellisman
1National Center for Microscopy and Imaging Research and Center for Research on Biological Systems and
2Department of Neurosciences, University of California, San Diego, La Jolla, California 92093, and
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Abstract

Modifications to the gene encoding human α-synuclein have been linked to the development of Parkinson's disease. The highly conserved structure of α-synuclein suggests a functional interaction with membranes, and several lines of evidence point to a role in vesicle-related processes within nerve terminals. Using recombinant fusions of human α-synuclein, including new genetic tags developed for correlated light microscopy and electron microscopy (the tetracysteine-biarsenical labeling system or the new fluorescent protein for electron microscopy, MiniSOG), we determined the distribution of α-synuclein when overexpressed in primary neurons at supramolecular and cellular scales in three dimensions (3D). We observed specific association of α-synuclein with a large and otherwise poorly characterized membranous organelle system of the presynaptic terminal, as well as with smaller vesicular structures within these boutons. Furthermore, α-synuclein was localized to multiple elements of the protein degradation pathway, including multivesicular bodies in the axons and lysosomes within neuronal cell bodies. Examination of synapses in brains of transgenic mice overexpressing human α-synuclein revealed alterations of the presynaptic endomembrane systems similar to our findings in cell culture. Three-dimensional electron tomographic analysis of enlarged presynaptic terminals in several brain areas revealed that these terminals were filled with membrane-bounded organelles, including tubulovesicular structures similar to what we observed in vitro. We propose that α-synuclein overexpression is associated with hypertrophy of membrane systems of the presynaptic terminal previously shown to have a role in vesicle recycling. Our data support the conclusion that α-synuclein is involved in processes associated with the sorting, channeling, packaging, and transport of synaptic material destined for degradation.

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The Journal of Neuroscience: 33 (6)
Journal of Neuroscience
Vol. 33, Issue 6
6 Feb 2013
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Mapping the Subcellular Distribution of α-Synuclein in Neurons using Genetically Encoded Probes for Correlated Light and Electron Microscopy: Implications for Parkinson's Disease Pathogenesis
Daniela Boassa, Monica L. Berlanga, Mary Ann Yang, Masako Terada, Junru Hu, Eric A. Bushong, Minju Hwang, Eliezer Masliah, Julia M. George, Mark H. Ellisman
Journal of Neuroscience 6 February 2013, 33 (6) 2605-2615; DOI: 10.1523/JNEUROSCI.2898-12.2013

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Mapping the Subcellular Distribution of α-Synuclein in Neurons using Genetically Encoded Probes for Correlated Light and Electron Microscopy: Implications for Parkinson's Disease Pathogenesis
Daniela Boassa, Monica L. Berlanga, Mary Ann Yang, Masako Terada, Junru Hu, Eric A. Bushong, Minju Hwang, Eliezer Masliah, Julia M. George, Mark H. Ellisman
Journal of Neuroscience 6 February 2013, 33 (6) 2605-2615; DOI: 10.1523/JNEUROSCI.2898-12.2013
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