Stimulation of synaptoneurosome glutamate release by monomeric and fibrillated α-synuclein
Abstract
The α-synuclein protein exists in vivo in a variety of covalently modified and aggregated forms associated with Parkinson's disease (PD) pathology. However, the specific proteoform structures involved with neuropathological disease mechanisms are not clearly defined. Since α-synuclein plays a role in presynaptic neurotransmitter release, an in vitro enzyme-based assay was developed to measure glutamate release from mouse forebrain synaptoneurosomes (SNs) enriched in synaptic endings. Glutamate measurements utilizing SNs from various mouse genotypes (WT, over-expressers, knock-outs) suggested a concentration dependence of α-synuclein on calcium/depolarization-dependent presynaptic glutamate release from forebrain terminals. In vitro reconstitution experiments with recombinant human α-synuclein proteoforms including monomers and aggregated forms (fibrils, oligomers) produced further evidence of this functional impact. Notably, brief exogenous applications of fibrillated forms of α-synuclein enhanced SN glutamate release but monomeric forms did not, suggesting preferential membrane penetration and toxicity by the aggregated forms. However, when applied to brain tissue sections just prior to homogenization, both monomeric and fibrillated forms stimulated glutamate release. Immuno-gold and transmission electron microscopy (TEM) detected exogenous fibrillated α-synuclein associated with numerous SN membranous structures including synaptic terminals. Western blots and immuno-gold TEM were consistent with SN internalization of α-synuclein. Additional studies revealed no evidence of gross disruption of SNmore »
- Authors:
-
- Univ. of California, Los Angeles, CA (United States)
- Publication Date:
- Research Org.:
- Univ. of California, Los Angeles, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); UCSD
- OSTI Identifier:
- 1533184
- Report Number(s):
- JNR-2016-May-6760
Journal ID: ISSN 0360-4012
- Grant/Contract Number:
- FC02-02ER63421; P30 DK063491
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Neuroscience Research
- Additional Journal Information:
- Journal Volume: 95; Journal Issue: 9; Journal ID: ISSN 0360-4012
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; neurosciences & neurology; α-synuclein; electron microscopy; fibrillated; fluorescence; glutamate oxidase; synaptoneurosome; excitotoxicity
Citation Formats
Sarafian, Theodore A., Littlejohn, Kaitlyn, Yuan, Sarah, Fernandez, Charlene, Cilluffo, Marianne, Koo, Bon-Kyung, Whitelegge, Julian P., and Watson, Joseph B. Stimulation of synaptoneurosome glutamate release by monomeric and fibrillated α-synuclein. United States: N. p., 2017.
Web. doi:10.1002/jnr.24024.
Sarafian, Theodore A., Littlejohn, Kaitlyn, Yuan, Sarah, Fernandez, Charlene, Cilluffo, Marianne, Koo, Bon-Kyung, Whitelegge, Julian P., & Watson, Joseph B. Stimulation of synaptoneurosome glutamate release by monomeric and fibrillated α-synuclein. United States. https://doi.org/10.1002/jnr.24024
Sarafian, Theodore A., Littlejohn, Kaitlyn, Yuan, Sarah, Fernandez, Charlene, Cilluffo, Marianne, Koo, Bon-Kyung, Whitelegge, Julian P., and Watson, Joseph B. Tue .
"Stimulation of synaptoneurosome glutamate release by monomeric and fibrillated α-synuclein". United States. https://doi.org/10.1002/jnr.24024. https://www.osti.gov/servlets/purl/1533184.
@article{osti_1533184,
title = {Stimulation of synaptoneurosome glutamate release by monomeric and fibrillated α-synuclein},
author = {Sarafian, Theodore A. and Littlejohn, Kaitlyn and Yuan, Sarah and Fernandez, Charlene and Cilluffo, Marianne and Koo, Bon-Kyung and Whitelegge, Julian P. and Watson, Joseph B.},
abstractNote = {The α-synuclein protein exists in vivo in a variety of covalently modified and aggregated forms associated with Parkinson's disease (PD) pathology. However, the specific proteoform structures involved with neuropathological disease mechanisms are not clearly defined. Since α-synuclein plays a role in presynaptic neurotransmitter release, an in vitro enzyme-based assay was developed to measure glutamate release from mouse forebrain synaptoneurosomes (SNs) enriched in synaptic endings. Glutamate measurements utilizing SNs from various mouse genotypes (WT, over-expressers, knock-outs) suggested a concentration dependence of α-synuclein on calcium/depolarization-dependent presynaptic glutamate release from forebrain terminals. In vitro reconstitution experiments with recombinant human α-synuclein proteoforms including monomers and aggregated forms (fibrils, oligomers) produced further evidence of this functional impact. Notably, brief exogenous applications of fibrillated forms of α-synuclein enhanced SN glutamate release but monomeric forms did not, suggesting preferential membrane penetration and toxicity by the aggregated forms. However, when applied to brain tissue sections just prior to homogenization, both monomeric and fibrillated forms stimulated glutamate release. Immuno-gold and transmission electron microscopy (TEM) detected exogenous fibrillated α-synuclein associated with numerous SN membranous structures including synaptic terminals. Western blots and immuno-gold TEM were consistent with SN internalization of α-synuclein. Additional studies revealed no evidence of gross disruption of SN membrane integrity or glutamate transporter function by exogenous α-synuclein. Finally, overall excitotoxicity, due to enhanced glutamate release in the face of either overexpressed monomeric α-synuclein or extrasynaptic exposure to fibrillated α-synuclein, should be considered as a potential neuropathological pathway during the progression of PD and other synucleinopathies.},
doi = {10.1002/jnr.24024},
journal = {Journal of Neuroscience Research},
number = 9,
volume = 95,
place = {United States},
year = {Tue Jan 24 00:00:00 EST 2017},
month = {Tue Jan 24 00:00:00 EST 2017}
}
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