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}
}
Web of Science
Works referenced in this record:
Initiation and elongation in fibrillation of ALS-linked superoxide dismutase
journal, November 2008
- Chattopadhyay, M.; Durazo, A.; Sohn, S. H.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 48
From Macroscopic Measurements to Microscopic Mechanisms of Protein Aggregation
journal, August 2012
- Cohen, Samuel I. A.; Vendruscolo, Michele; Dobson, Christopher M.
- Journal of Molecular Biology, Vol. 421, Issue 2-3
The Parkinson's disease protein -synuclein disrupts cellular Rab homeostasis
journal, December 2007
- Gitler, A. D.; Bevis, B. J.; Shorter, J.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 1
Targeted Amino-Terminal Acetylation of Recombinant Proteins in E. coli
journal, December 2010
- Johnson, Matthew; Coulton, Arthur T.; Geeves, Michael A.
- PLoS ONE, Vol. 5, Issue 12
αB Crystallin Is Apically Secreted within Exosomes by Polarized Human Retinal Pigment Epithelium and Provides Neuroprotection to Adjacent Cells
journal, October 2010
- Sreekumar, Parameswaran G.; Kannan, Ram; Kitamura, Mizuki
- PLoS ONE, Vol. 5, Issue 10
Cytosolic Proteins Regulate α-Synuclein Dissociation from Presynaptic Membranes
journal, August 2006
- Wislet-Gendebien, Sabine; D'Souza, Cheryl; Kawarai, Toshitaka
- Journal of Biological Chemistry, Vol. 281, Issue 43
Different Species of -Synuclein Oligomers Induce Calcium Influx and Seeding
journal, August 2007
- Danzer, K. M.; Haasen, D.; Karow, A. R.
- Journal of Neuroscience, Vol. 27, Issue 34
α-Synuclein produces a long-lasting increase in neurotransmitter release
journal, October 2004
- Liu, Shumin; Ninan, Ipe; Antonova, Irina
- The EMBO Journal, Vol. 23, Issue 22
Direct Observation of the Interconversion of Normal and Toxic Forms of α-Synuclein
journal, May 2012
- Cremades, Nunilo; Cohen, Samuel I. A.; Deas, Emma
- Cell, Vol. 149, Issue 5
The genetics and neuropathology of Parkinson’s disease
journal, July 2012
- Houlden, Henry; Singleton, Andrew B.
- Acta Neuropathologica, Vol. 124, Issue 3
Progressive Aggregation of Alpha-Synuclein and Selective Degeneration of Lewy Inclusion-Bearing Neurons in a Mouse Model of Parkinsonism
journal, March 2015
- Osterberg, Valerie R.; Spinelli, Kateri J.; Weston, Leah J.
- Cell Reports, Vol. 10, Issue 8
Role of α-synuclein penetration into the membrane in the mechanisms of oligomer pore formation: α-syn membrane penetration
journal, February 2012
- Tsigelny, Igor F.; Sharikov, Yuriy; Wrasidlo, Wolfgang
- FEBS Journal, Vol. 279, Issue 6
Optical Reporters for the Conformation of -Synuclein Reveal a Specific Interaction with Mitochondria
journal, November 2008
- Nakamura, K.; Nemani, V. M.; Wallender, E. K.
- Journal of Neuroscience, Vol. 28, Issue 47
-Synuclein Promotes SNARE-Complex Assembly in Vivo and in Vitro
journal, August 2010
- Burre, J.; Sharma, M.; Tsetsenis, T.
- Science, Vol. 329, Issue 5999
Structural characterization of toxic oligomers that are kinetically trapped during α-synuclein fibril formation
journal, April 2015
- Chen, Serene W.; Drakulic, Srdja; Deas, Emma
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 16
A soluble -synuclein construct forms a dynamic tetramer
journal, October 2011
- Wang, W.; Perovic, I.; Chittuluru, J.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 43
Astrocyte Calcium Signal and Gliotransmission in Human Brain Tissue
journal, May 2012
- Navarrete, M.; Perea, G.; Maglio, L.
- Cerebral Cortex, Vol. 23, Issue 5
High Stability and Cooperative Unfolding of α-Synuclein Oligomers
journal, September 2014
- Paslawski, Wojciech; Andreasen, Maria; Nielsen, Søren Bang
- Biochemistry, Vol. 53, Issue 39
Impairment of Mitochondria in Adult Mouse Brain Overexpressing Predominantly Full-Length, N-Terminally Acetylated Human α-Synuclein
journal, May 2013
- Sarafian, Theodore A.; Ryan, Christopher M.; Souda, Puneet
- PLoS ONE, Vol. 8, Issue 5
Towards a Pharmacophore for Amyloid
journal, June 2011
- Landau, Meytal; Sawaya, Michael R.; Faull, Kym F.
- PLoS Biology, Vol. 9, Issue 6
Evidence for α-synuclein prions causing multiple system atrophy in humans with parkinsonism
journal, August 2015
- Prusiner, Stanley B.; Woerman, Amanda L.; Mordes, Daniel A.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 38
Molecular Underpinnings of Synaptic Vesicle Pool Heterogeneity: Molecularly Distinct Synaptic Vesicle Pools
journal, March 2015
- Crawford, Devon C.; Kavalali, Ege T.
- Traffic, Vol. 16, Issue 4
Role of α-Synuclein Carboxy-Terminus on Fibril Formation in Vitro †
journal, July 2003
- Murray, Ian V. J.; Giasson, Benoit I.; Quinn, Shawn M.
- Biochemistry, Vol. 42, Issue 28
α-Synuclein strains cause distinct synucleinopathies after local and systemic administration
journal, June 2015
- Peelaerts, W.; Bousset, L.; Van der Perren, A.
- Nature, Vol. 522, Issue 7556
Membrane Curvature Induction and Tubulation Are Common Features of Synucleins and Apolipoproteins
journal, August 2010
- Varkey, Jobin; Isas, Jose Mario; Mizuno, Naoko
- Journal of Biological Chemistry, Vol. 285, Issue 42
Exogenous α-Synuclein Fibrils Induce Lewy Body Pathology Leading to Synaptic Dysfunction and Neuron Death
journal, October 2011
- Volpicelli-Daley, Laura A.; Luk, Kelvin C.; Patel, Tapan P.
- Neuron, Vol. 72, Issue 1
Differential neuropathological alterations in transgenic mice expressing ?-synuclein from the platelet-derived growth factor and Thy-1 promoters
journal, May 2002
- Rockenstein, Edward; Mallory, Margaret; Hashimoto, Makoto
- Journal of Neuroscience Research, Vol. 68, Issue 5
Role of α-synuclein in synaptic glutamate release
journal, October 2007
- Gureviciene, Irina; Gurevicius, Kestutis; Tanila, Heikki
- Neurobiology of Disease, Vol. 28, Issue 1
Characterization of Semisynthetic and Naturally N α -Acetylated α-Synuclein in Vitro and in Intact Cells : IMPLICATIONS FOR AGGREGATION AND CELLULAR PROPERTIES OF α-SYNUCLEIN
journal, June 2012
- Fauvet, Bruno; Fares, Mohamed-Bilal; Samuel, Filsy
- Journal of Biological Chemistry, Vol. 287, Issue 34
GM1 Specifically Interacts with α-Synuclein and Inhibits Fibrillation †
journal, February 2007
- Martinez, Zak; Zhu, Min; Han, Shubo
- Biochemistry, Vol. 46, Issue 7
Parkinson's Disease
journal, September 2003
- Dauer, William; Przedborski, Serge
- Neuron, Vol. 39, Issue 6
Striatal Synaptosomes from Hdh140Q/140Q Knock-in Mice have Altered Protein Levels, Novel Sites of Methionine Oxidation, and Excess Glutamate Release after Stimulation
journal, January 2013
- Valencia, Antonio; Sapp, Ellen; Kimm, Jeffrey S.
- Journal of Huntington's Disease, Vol. 2, Issue 4
α-Synuclein Can Inhibit SNARE-Mediated Vesicle Fusion through Direct Interactions with Lipid Bilayers
journal, March 2013
- DeWitt, David C.; Rhoades, Elizabeth
- Biochemistry, Vol. 52, Issue 14
Native α-synuclein induces clustering of synaptic-vesicle mimics via binding to phospholipids and synaptobrevin-2/VAMP2
journal, April 2013
- Diao, Jiajie; Burré, Jacqueline; Vivona, Sandro
- eLife, Vol. 2
Olfactory deficits in mice overexpressing human wildtype -synuclein
journal, July 2008
- Fleming, Sheila M.; Tetreault, Nicole A.; Mulligan, Caitlin K.
- European Journal of Neuroscience, Vol. 28, Issue 2
Extracellular α-synuclein alters synaptic transmission in brain neurons by perforating the neuronal plasma membrane
journal, February 2015
- Pacheco, Carla R.; Morales, Camila N.; Ramírez, Alejandra E.
- Journal of Neurochemistry, Vol. 132, Issue 6
The Role of Stable α-Synuclein Oligomers in the Molecular Events Underlying Amyloid Formation
journal, February 2014
- Lorenzen, Nikolai; Nielsen, Søren Bang; Buell, Alexander K.
- Journal of the American Chemical Society, Vol. 136, Issue 10
Exogenous -Synuclein Decreases Raft Partitioning of Cav2.2 Channels Inducing Dopamine Release
journal, August 2014
- Ronzitti, G.; Bucci, G.; Emanuele, M.
- Journal of Neuroscience, Vol. 34, Issue 32
Inclusion formation and neuronal cell death through neuron-to-neuron transmission of -synuclein
journal, July 2009
- Desplats, P.; Lee, H. -J.; Bae, E. -J.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 31
Presynaptic Alpha-Synuclein Aggregation in a Mouse Model of Parkinson's Disease
journal, February 2014
- Spinelli, K. J.; Taylor, J. K.; Osterberg, V. R.
- Journal of Neuroscience, Vol. 34, Issue 6
Isolation and characterization of synaptoneurosomes from single rat hippocampal slices
journal, December 1997
- Johnson, Michael W.; Chotiner, Jennifer K.; Watson, Joseph B.
- Journal of Neuroscience Methods, Vol. 77, Issue 2
Systematic Mutagenesis of -Synuclein Reveals Distinct Sequence Requirements for Physiological and Pathological Activities
journal, October 2012
- Burre, J.; Sharma, M.; Sudhof, T. C.
- Journal of Neuroscience, Vol. 32, Issue 43
Structural Organization of α-Synuclein Fibrils Studied by Site-directed Spin Labeling
journal, June 2003
- Der-Sarkissian, Ani; Jao, Christine C.; Chen, Jeannie
- Journal of Biological Chemistry, Vol. 278, Issue 39
Modeling Lewy pathology propagation in Parkinson's disease
journal, January 2014
- Luk, Kelvin C.; Lee, Virginia M. -Y.
- Parkinsonism & Related Disorders, Vol. 20
Fibril growth and seeding capacity play key roles in α-synuclein-mediated apoptotic cell death
journal, July 2015
- Mahul-Mellier, A-L; Vercruysse, F.; Maco, B.
- Cell Death & Differentiation, Vol. 22, Issue 12
Synaptoneurosome micromethod for fractionation of mouse and human brain, and primary neuronal cultures
journal, November 2012
- Chang, Julia W.; Arnold, Monica M.; Rozenbaum, Anna
- Journal of Neuroscience Methods, Vol. 211, Issue 2
Seeking a Mechanism for the Toxicity of Oligomeric α-Synuclein
journal, March 2015
- Roberts, Hazel; Brown, David
- Biomolecules, Vol. 5, Issue 2
Parkinson's Disease: Genetics and Pathogenesis
journal, February 2011
- Shulman, Joshua M.; De Jager, Philip L.; Feany, Mel B.
- Annual Review of Pathology: Mechanisms of Disease, Vol. 6, Issue 1
A further update on the role of excitotoxicity in the pathogenesis of Parkinson’s disease
journal, January 2014
- Ambrosi, Giulia; Cerri, Silvia; Blandini, Fabio
- Journal of Neural Transmission, Vol. 121, Issue 8
Large -synuclein oligomers inhibit neuronal SNARE-mediated vesicle docking
journal, February 2013
- Choi, B. -K.; Choi, M. -G.; Kim, J. -Y.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 10
Alterations in corticostriatal synaptic plasticity in mice overexpressing human α-synuclein
journal, March 2009
- Watson, J. B.; Hatami, A.; David, H.
- Neuroscience, Vol. 159, Issue 2
Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation
journal, April 2008
- Li, Jia-Yi; Englund, Elisabet; Holton, Janice L.
- Nature Medicine, Vol. 14, Issue 5
Lewy body–like pathology in long-term embryonic nigral transplants in Parkinson's disease
journal, April 2008
- Kordower, Jeffrey H.; Chu, Yaping; Hauser, Robert A.
- Nature Medicine, Vol. 14, Issue 5
Soluble, Prefibrillar α-Synuclein Oligomers Promote Complex I-dependent, Ca 2+ -induced Mitochondrial Dysfunction
journal, June 2014
- Luth, Eric S.; Stavrovskaya, Irina G.; Bartels, Tim
- Journal of Biological Chemistry, Vol. 289, Issue 31
Function of the asparagine 74 residue of the inhibitory γ-subunit of retinal rod cGMP-phophodiesterase (PDE) in vivo
journal, October 2011
- Tsang, Stephen H.; Woodruff, Michael L.; Hsu, Chun Wei
- Cellular Signalling, Vol. 23, Issue 10
Definition of a Molecular Pathway Mediating -Synuclein Neurotoxicity
journal, April 2015
- Burre, J.; Sharma, M.; Sudhof, T. C.
- Journal of Neuroscience, Vol. 35, Issue 13
Membrane interactions and fibrillization of α-synuclein play an essential role in membrane disruption
journal, October 2014
- Chaudhary, Himanshu; Stefanovic, Anja N. D.; Subramaniam, Vinod
- FEBS Letters, Vol. 588, Issue 23
Increased Expression of α-Synuclein Reduces Neurotransmitter Release by Inhibiting Synaptic Vesicle Reclustering after Endocytosis
journal, January 2010
- Nemani, Venu M.; Lu, Wei; Berge, Victoria
- Neuron, Vol. 65, Issue 1
C-Terminal Turn Stability Determines Assembly Differences between Aβ40 and Aβ42
journal, January 2013
- Roychaudhuri, Robin; Yang, Mingfeng; Deshpande, Atul
- Journal of Molecular Biology, Vol. 425, Issue 2
Structure, function and toxicity of alpha-synuclein: the Bermuda triangle in synucleinopathies
journal, September 2015
- Villar-Piqué, Anna; Lopes da Fonseca, Tomás; Outeiro, Tiago Fleming
- Journal of Neurochemistry, Vol. 139
α‐synuclein assemblies sequester neuronal α3‐Na + /K + ‐ ATP ase and impair Na + gradient
journal, August 2015
- Shrivastava, Amulya Nidhi; Redeker, Virginie; Fritz, Nicolas
- The EMBO Journal, Vol. 34, Issue 19
ANS Binding Reveals Common Features of Cytotoxic Amyloid Species
journal, June 2010
- Bolognesi, Benedetta; Kumita, Janet R.; Barros, Teresa P.
- ACS Chemical Biology, Vol. 5, Issue 8
α-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation
journal, August 2011
- Bartels, Tim; Choi, Joanna G.; Selkoe, Dennis J.
- Nature, Vol. 477, Issue 7362
One-pot total chemical synthesis of human α-synuclein
journal, January 2013
- Fauvet, Bruno; Butterfield, Sara M.; Fuks, Jonas
- Chemical Communications, Vol. 49, Issue 81
Excitatory amino acid transporters: Roles in glutamatergic neurotransmission
journal, July 2014
- Divito, Christopher B.; Underhill, Suzanne M.
- Neurochemistry International, Vol. 73
The effect of guanidine on transmitter release in the ciliary ganglion of the chick.
journal, May 1978
- Banks, F. W.
- The Journal of Physiology, Vol. 278, Issue 1
Permeabilizing cells: Some methods and applications for the study of intracellular processes
book, January 1990
- Schulz, Irene
- Methods in Enzymology
KTKEGV repeat motifs are key mediators of normal α-synuclein tetramerization: Their mutation causes excess monomers and neurotoxicity
journal, July 2015
- Dettmer, Ulf; Newman, Andrew J.; von Saucken, Victoria E.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 31
Direct Observation of Amyloid Fibril Growth Monitored by Thioflavin T Fluorescence
journal, March 2003
- Ban, Tadato; Hamada, Daizo; Hasegawa, Kazuhiro
- Journal of Biological Chemistry, Vol. 278, Issue 19
Synaptic Vesicle Depletion Correlates with Attenuated Synaptic Responses to Prolonged Repetitive Stimulation in Mice Lacking α-Synuclein
journal, October 2002
- Cabin, Deborah E.; Shimazu, Kazuhiro; Murphy, Diane
- The Journal of Neuroscience, Vol. 22, Issue 20
-Synuclein Overexpression in PC12 and Chromaffin Cells Impairs Catecholamine Release by Interfering with a Late Step in Exocytosis
journal, November 2006
- Larsen, K. E.; Schmitz, Y.; Troyer, M. D.
- Journal of Neuroscience, Vol. 26, Issue 46
The Function of α-Synuclein
journal, September 2013
- Bendor, Jacob T.; Logan, Todd P.; Edwards, Robert H.
- Neuron, Vol. 79, Issue 6
dl- threo -β-Benzyloxyaspartate, A Potent Blocker of Excitatory Amino Acid Transporters
journal, February 1998
- Shimamoto, Keiko; Lebrun, Bruno; Yasuda-Kamatani, Yoshimi
- Molecular Pharmacology, Vol. 53, Issue 2
Pitfalls associated with the use of Thioflavin-T to monitor anti-fibrillogenic activity
journal, July 2014
- Coelho-Cerqueira, Eduardo; Pinheiro, Anderson S.; Follmer, Cristian
- Bioorganic & Medicinal Chemistry Letters, Vol. 24, Issue 14
Works referencing / citing this record:
Enhanced mitochondrial inhibition by 3,4‐dihydroxyphenyl‐acetaldehyde (DOPAL)‐oligomerized α‐synuclein
journal, August 2019
- Sarafian, Theodore A.; Yacoub, Amneh; Kunz, Anastasia
- Journal of Neuroscience Research
α-Synuclein and astrocytes: tracing the pathways from homeostasis to neurodegeneration in Lewy body disease
journal, February 2019
- Sorrentino, Zachary A.; Giasson, Benoit I.; Chakrabarty, Paramita
- Acta Neuropathologica, Vol. 138, Issue 1