The Potential Role of Astrocytes in Parkinson’s Disease (PD)
Abstract
:1. Introduction
2. The Physiological Role of Astrocytes
3. Neuron-Astrocyte Interactions in the Brain
4. The Role of Astrocytes in Parkinson’s Disease
4.1. Excitotoxicity and Parkinson’s Disease
4.2. Astrocytes and Parkinson’s Disease
4.2.1. EAAT1 and EAAT2 Dysfunction in Astrocytes and Parkinson’s Disease
4.2.2. AQP4 Dysfunction in Astrocytes and Parkinson’s Disease
4.2.3. EAAT2-AQP4 Interactions in Astrocytes and Parkinson’s Disease
4.2.4. Genetic Studies in Astrocytes and Parkinson’s Disease
5. Conclusions
Funding
Conflicts of Interest
Abbreviations
PD | Parkinson’s disease |
SNpc | Substantia Nigra pars compacta |
EAATs | Excitatory amino acid transporters) |
AQP4 | Aquaporin-4 |
DA | dopaminergic neurons |
ND | Neurodegenerative diseases |
BBB | Blood–brain barrier |
GLAST | glutamate aspartate transporter |
GLT1 | Glutamate transporter 1 |
SN | Substantia nigra |
GPe | Globus pallidus external |
GPi | Globus pallidus internal |
MPTP | 1-methyl-4-phenyl 1,2,3,6-tetrahydropyridine |
6-OHDA | 6-hydroxydopamine |
NMO-IgG | Neuromyelitis Optica immunoglobulin G |
HEK-293 | Human embryonic kidney cells |
References
- Dossi, E.; Vasile, F.; Rouach, N. Human astrocytes in the diseased brain. Brain Res. Bull. 2018, 136, 139–156. [Google Scholar] [CrossRef]
- Rose, C.F.; Verkhratsky, A.; Parpura, V. Astrocyte glutamine synthetase: Pivotal in health and disease. Biochem. Soc. Trans. 2013, 41, 1518–1524. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Tan, F.; Xu, P.; Qu, S. Recent Advance in the Relationship between Excitatory Amino Acid Transporters and Parkinson’s Disease. Neural Plast. 2016, 2016, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Prydz, A.; Stahl, K.; Puchades, M.; Davarpaneh, N.; Nadeem, M.; Ottersen, O.P.; Gundersen, V.; Amiry-Moghaddam, M. Subcellular expression of aquaporin-4 in substantia nigra of normal and MPTP-treated mice. Neuroscience 2017, 359, 258–266. [Google Scholar] [CrossRef] [PubMed]
- Booth, H.D.E.; Hirst, W.D.; Wade-Martins, R. The Role of Astrocyte Dysfunction in Parkinson’s Disease Pathogenesis. Trends Neurosci. 2017, 40, 358–370. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maiti, P.; Manna, J.; Dunbar, G.L. Current understanding of the molecular mechanisms in Parkinson’s disease: Targets for potential treatments. Transl. Neurodegener. 2017, 1–35. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lanciotti, A.; Brignone, M.S.; Bertini, E.; Petrucci, T.C.; Aloisi, F.; Ambrosini, E. Astrocytes: Emerging stars in leukodystrophy pathogenesis. Transl. Neurosci. 2013, 4, 144–164. [Google Scholar] [CrossRef] [Green Version]
- Stavale, L.M.; Soares, E.S.; Mendonça, M.C.P.; Irazusta, S.P.; da Cruz Höfling, M.A. Temporal relationship between aquaporin-4 and glial fibrillary acidic protein in cerebellum of neonate and adult rats administered a BBB disrupting spider venom. Toxicon 2013, 66, 37–46. [Google Scholar] [CrossRef] [Green Version]
- Yang, J.; Lunde, L.K.; Nuntagij, P.; Oguchi, T.; Camassa, L.M.A. Loss of Astrocyte Polarization in the Tg-ArcSwe Mouse Model of Alzheimer’s Disease. J. Alzheimers Dis. 2011, 27, 711–722. [Google Scholar] [CrossRef] [Green Version]
- Hinson, S.R.; Roemer, S.F.; Lucchinetti, C.F.; Fryer, J.P.; Kryzer, T.J.; Chamberlain, J.L.; Howe, C.L.; Pittock, S.J.; Lennon, V.A. Aquaporin-4–binding autoantibodies in patients with neuromyelitis optica impair glutamate transport by down-regulating EAAT2. J. Exp. Med. 2008, 205, 2473–2481. [Google Scholar] [CrossRef]
- Colangelo, A.M.; Alberghina, L.; Papa, M. Astrogliosis as a therapeutic target for neurodegenerative diseases. Neurosci. Lett. 2014, 565, 59–64. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ricci, G.; Volpi, L.; Pasquali, L.; Petrozzi, L.; Siciliano, G. Astrocyte-neuron interactions in neurological disorders. J. Biol. Phys. 2009, 35, 317–336. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guillamón-Vivancos, T.; Gómez-Pinedo, U.; Matías-Guiu, J. Astrocytes in neurodegenerative diseases (I): Function and molecular description. Neurología 2015, 30, 119–129. [Google Scholar] [CrossRef] [PubMed]
- Liu, B.; Teschemacher, A.G.; Kasparov, S. Astroglia as a cellular target for neuroprotection and treatment of neuro-psychiatric disorders. Glia 2017, 65, 1205–1226. [Google Scholar] [CrossRef] [Green Version]
- Nagelhus, E.A.; Amiry-Moghaddam, M.; Bergersen, L.H.; Bjaalie, J.G.; Eriksson, J.; Gundersen, V.; Leergaard, T.B.; Morth, P.; Storm-Mathisen, J.; Torp, R.; et al. The glia doctrine: Addressing the role of glial cells in healthy brain ageing. Mech. Ageing Dev. 2013, 134, 449–459. [Google Scholar] [CrossRef]
- Vargova, L.; Sykova, E. Astrocytes and extracellular matrix in extrasynaptic volume transmission. Phil. Trans. R. Soc. B 2013, 369, 20130608. [Google Scholar] [CrossRef] [Green Version]
- Dutta, S.; Gowda, D.V.; Gupta, N.V.; Vaghela, R. Astrocytes: Emerging role in immunomodulation and therapeutics an inclusive review. Int. J. ChemTech Res. 2017, 10, 148–159. [Google Scholar]
- Bellot-Saez, A.; Kékesi, O.; Morley, J.W.; Buskila, Y. Astrocytic modulation of neuronal excitability through K+spatial buffering. Neurosci. Biobehav. Rev. 2017, 77, 87–97. [Google Scholar] [CrossRef]
- Gentile, M.T.; D’Amato, L.C. Introductory Chapter: The Importance of Astrocytes in the Research of CNS Diseases. Astrocyte Physiol. Pathol. 2018, 3–8. [Google Scholar] [CrossRef] [Green Version]
- Roberts, R.C.; Roche, J.K.; McCullumsmith, R.E. Localization of excitatory amino acid transporters EAAT1 and EAAT2 in human postmortem cortex: A light and electron microscopic study. Neuroscience 2014, 277, 522–540. [Google Scholar] [CrossRef] [Green Version]
- Assefa, B.T.; Gebre, A.K.; Altaye, B.M. Reactive Astrocytes as Drug Target in Alzheimer’s Disease. Biomed. Res. Int. 2018, 2018, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Karki, P.; Webb, A.; Smith, K.; Johnson, J.; Lee, K.; Son, D.-S.; Aschner, M.; Lee, E. Yin Yang 1 Is a Repressor of Glutamate Transporter EAAT2, and It Mediates Manganese-Induced Decrease of EAAT2 Expression in Astrocytes. Mol. Cell Biol. 2014, 34, 1280–1289. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Binder, D.K. Unaltered glutamate transporter-1 protein levels in aquaporin-4 knockout mice. ASN Neuro. 2017, 9, 1–11. [Google Scholar]
- Robinson, M.B.; Jackson, J.G. Astroglial glutamate transporters coordinate excitatory signaling and brain energetics. Neurochem. Int. 2016, 98, 56–71. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chung, E.K.Y.; Chen, L.W.; Chan, Y.S.; Yung, K.K.L. Downregulation of glial glutamate transporters after dopamine denervation in the striatum of 6-hydroxydopamine-lesioned rats. J. Comp. Neurol. 2008, 511, 421–437. [Google Scholar] [CrossRef] [PubMed]
- Kim, K.; Lee, S.-G.; Kegelman, T.P.; Su, Z.-Z.; Das, S.K.; Dash, R.; Dasgupta, S.; Barral, P.M.; Hedvat, M.; Diaz, P.; et al. Role of Excitatory Amino Acid Transporter-2 (EAAT2) and Glutamate in Neurodegeneration: Opportunities for Developing Novel Therapeutics. J. Cell Physiol. 2011, 226, 2484–2493. [Google Scholar] [CrossRef] [Green Version]
- Gundersen, G.A. Roles of Aquaporin-4 in Brain Fluid Dynamics. Ph.D. Thesis, University of Oslo, Oslo, Norway, 2013. [Google Scholar]
- Centelles, J.J. Glutamate transporters: The regulatory proteins for excitatory/excitotoxic glutamate in brain. J. Transl. Sci. 2016, 2, 92–99. [Google Scholar] [CrossRef]
- Seifert, G.; Henneberger, C.; Steinhäuser, C. Diversity of astrocyte potassium channels: An update. Brain Res. Bull. 2018, 136, 26–36. [Google Scholar] [CrossRef]
- Wang, R.; Zhao, X.; Xu, J.; Wen, Y.; Li, A.; Lu, M.; Zhou, J. Astrocytic JWA deletion exacerbates dopaminergic neurodegeneration by decreasing glutamate transporters in mice. Cell Death Dis. 2018, 9, 1–15. [Google Scholar] [CrossRef]
- Wang, Q.; Liu, Y.; Zhou, J. Neuroinflammation in Parkinson’s disease and its potential as therapeutic target. Transl. Neurodegener. 2015, 4, 1–9. [Google Scholar] [CrossRef] [Green Version]
- Domenico, A. Investigating Glial Contributions During Parkinson’s, Disease Pathogenesis Using Patient-Specific iPSC-Derived Cells By. Available online: http://manteniment.csuc.cat/ (accessed on 10 April 2019).
- George, J.L.; Mok, S.; Moses, D.; Wilkins, S.; Bush, A.I.; Cherny, R.A.; Finkelstein, D.I. Targeting the Progression of Parkinson’s Disease. Curr. Neuropharmacol. 2009, 7, 9–36. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sidoryk-Wegrzynowicz, M.; Wegrzynowicz, M.; Lee, E.; Bowman, A.B.; Aschner, M. Role of Astrocytes in Brain Function and Disease. Toxicol. Pathol. 2011, 39, 115–123. [Google Scholar] [CrossRef] [PubMed]
- Karkia, P.; Smitha, K.; Johnson, J., Jr.; Aschner, M.; Lee, E. Genetic dys-regulation of astrocytic glutamate transporter EAAT2 and its implications in neurological disorders and manganese toxicity. NIH Public Access 2016, 40, 380–388. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Blandini, F. The role of the subthalamic nucleus in the pathophysiology of Parkinson’s disease. Funct. Neurol. 2001, 16, 99–106. [Google Scholar]
- Barreto, E.G.; Gonzalez, J.; Capani, F.; Morales, L. Role of Astrocytes in Neurodegenerative Diseases. Neurodegener. Dis. Process. Prev. Prot. Monit. 2011. [Google Scholar] [CrossRef] [Green Version]
- Allen, C.F.; Shaw, P.J.; Ferraiuolo, L. Can astrocytes be a target for precision medicine? Adv. Exp. Med. Biol. 2017, 1007, 111–128. [Google Scholar]
- Fiorentino, A.; Sharp, S.I.; McQuillin, A. Association of rare variation in the glutamate receptor gene SLC1A2 with susceptibility to bipolar disorder and schizophrenia. Eur. J. Hum. Genet. 2015, 23, 1200–1206. [Google Scholar] [CrossRef] [Green Version]
- Rajput, A.H.; Sitte, H.H.; Rajput, A.; Fenton, M.E.; Pifl, C.; Hornykiewicz, O. Globus pallidus dopamine and Parkinson motor subtypes: Clinical and brain biochemical correlation. Neurology 2008, 70, 1403–1410. [Google Scholar] [CrossRef]
- Joe, E.; Choi, D.; An, J.; Eun, J.; Jou, I.; Park, S. Astrocytes, Microglia, and Parkinson’s Disease. Exp. Neurobiol. 2018, 27, 77–87. [Google Scholar] [CrossRef]
- Cabezas, R.; Ávila, M.; Gonzalez, J.; El-Bachá, R.S.; Báez, E.; García-Segura, L.M.; Coronel, J.C.J.; Capani, F.; Cardona-Gomez, G.P.; Barreto, G.E. Astrocytic modulation of blood brain barrier: Perspectives on Parkinson’s disease. Front. Cell Neurosci. 2014, 8, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Huang, D.; Wang, Z.; Tong, J.; Wang, M.; Wang, J.; Xu, J.; Bai, X.; Li, H.; Huang, Y.; Wu, Y. Long-term Changes in the Nigrostriatal Pathway in the MPTP Mouse Model of Parkinson’s Disease. Neuroscience 2018, 369, 303–313. [Google Scholar] [CrossRef] [PubMed]
- Gloria, E. Meredith DJR. MPTP Mouse Models of Parkinson’s Disease: An Update. J. Park. Dis. 2012, 1, 19–33. [Google Scholar]
- Bruinsma, I. Astrocytes in Parkinson’s Disease. Master Thesis, Utrecht university, Utrecht, The Netherlands, 20 December 2009. [Google Scholar]
- Nielsen, S.; Nagelhus, E.A.; Amiry-Moghaddam, M.; Bourque, C.; Agre, P.; Ottersen, O.P. Specialized membrane domains for water transport in glial cells: High-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J. Neurosci. 1997, 17, 171–180. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Beschorner, R.; Simon, P.; Schauer, N.; Mittelbronn, M.; Schluesener, H.J.; Trautmann, K. Reactive astrocytes and activated microglial cells express EAAT1, but not EAAT2, reflecting a neuroprotective potential following ischaemia. Histopathology 2007, 1, 897–910. [Google Scholar] [CrossRef]
- Holmseth, S.; Dehnes, Y.; Huang, Y.H.; Follin-Arbelet, V.V.; Grutle, N.J.; Mylonakou, M.N.; Plachez, C.; Zhou, Y.; Furness, D.N.; Bergles, D.E.; et al. The Density of EAAC1 (EAAT3) Glutamate Transporters Expressed by Neurons in the Mammalian CNS. J. Neurosci. 2012, 32, 6000–6013. [Google Scholar] [CrossRef] [Green Version]
- Velasco, M.; Quintero, J.R.; Castillo, M.C.; Rojas, M.; Bautista, J.; Martinez, M.S.; Salazar, J.; Mendoza, R.; Bermúdez, V. Excitotoxicity: An Organized Crime at The Cellular Level. J. Neurol. Neurosci. 2017, 8, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Lan, Y.L.; Zou, S.; Chen, J.J.; Zhao, J.; Li, S. The Neuroprotective Effect of the Association of Aquaporin-4/Glutamate Transporter-1 against Alzheimer’s Disease. Neural Plast. 2016, 2016, 8. [Google Scholar] [CrossRef] [Green Version]
- Thumburu, K.K.; Dhiman, R.K.; Vasishta, R.K.; Chakraborti, A.; Butterworth, R.F.; Beauchesne, E.; Desjardins, P.; Goyal, S.; Sharma, N.; Duseja, A. Expression of astrocytic genes coding for proteins implicated in neural excitation and brain edema is altered after acute liver failure. J. Neurochem. 2014, 128, 617–627. [Google Scholar] [CrossRef] [Green Version]
- Szu, J.I.; Binder, D.K. The Role of Astrocytic Aquaporin-4 in Synaptic Plasticity and Learning and Memory. Front. Integr. Neurosci. 2016, 10, 1–16. [Google Scholar] [CrossRef] [Green Version]
- Hoddevik, E.H.; Khan, F.H.; Rahmani, S.; Ottersen, O.P.; Boldt, H.B.; Amiry-Moghaddam, M. Factors determining the density of AQP4 water channel molecules at the brain–blood interface. Brain Struct. Funct. 2017, 222, 1753–1766. [Google Scholar] [CrossRef] [Green Version]
- Ayers-Ringler, J.R.; Jia, Y.-F.; Qiu, Y.-Y.; Choi, D.-S. Role of astrocytic glutamate transporter in alcohol use disorder. World J. Psychiatry 2016, 6, 31. [Google Scholar] [CrossRef] [PubMed]
- Foglio, E.; Luigi Fabrizio, R. Aquaporins and Neurodegenerative Diseases. Curr. Neuropharmacol. 2010, 8, 112–121. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, N.; Lu, X.Q.; Yan, H.T.; Su, R.B.; Wang, J.F.; Liu, Y.; Hu, G.; Li, J. Aquaporin 4 deficiency modulates morphine pharmacological actions. Neurosci. Lett. 2008, 448, 221–225. [Google Scholar] [CrossRef] [PubMed]
- Zeng, X.N.; Sun, X.L.; Gao, L.; Fan, Y.; Ding, J.H.; Hu, G. Aquaporin-4 deficiency down-regulates glutamate uptake and GLT-1 expression in astrocytes. Mol. Cell Neurosci. 2007, 34, 34–39. [Google Scholar] [CrossRef]
- Yang, J.; Li, M.X.; Luo, Y.; Chen, T.; Liu, J.; Fang, P.; Jiang, B.; Hu, Z.-L.; Jin, Y.; Chen, J.-G.; et al. Chronic ceftriaxone treatment rescues hippocampal memory deficit in AQP4 knockout mice via activation of GLT-1. Neuropharmacology 2013, 75, 213–222. [Google Scholar] [CrossRef]
- Mogoanta, L.; Ciurea, M.; Pirici, I.; Margaritescu, C.; Simionescu, C.; Ion, D.A.; Pirici, D. Different dynamics of aquaporin 4 and glutamate transporter-1 distribution in the perineuronal and perivascular compartments during ischemic stroke. Brain Pathol. 2014, 24, 475–493. [Google Scholar] [CrossRef]
- Lee, M.R.; Ruby, C.L.; Hinton, D.J.; Choi, S.; Adams, C.A.; Young Kang, N.; Choi, D.-S. Striatal adenosine signaling regulates EAAT2 and astrocytic AQP4 expression and alcohol drinking in mice. Neuropsychopharmacology 2013, 38, 437–445. [Google Scholar] [CrossRef] [Green Version]
- Gundersen, G.A.; Vindedal, G.F.; Skare, O.; Nagelhus, E.A. Evidence that pericytes regulate aquaporin-4 polarization in mouse cortical astrocytes. Brain Struct. Funct. 2014, 219, 2181–2186. [Google Scholar] [CrossRef] [Green Version]
- Wu, X.; Zhang, J.T.; Li, D.; Zhou, J.; Yang, J.; Zheng, H.L.; Chen, J.-G.; Wang, F. Aquaporin-4 deficiency facilitates fear memory extinction in the hippocampus through excessive activation of extrasynaptic GluN2B-containing NMDA receptors. Neuropharmacology 2017, 112, 124–134. [Google Scholar] [CrossRef]
- Karki, P.; Webb, A.; Smith, K.; Lee, K.; Son, D.S.; Aschner, M.; Lee, E. CAMP response element-binding protein (CREB) and nuclear factor κB mediate the tamoxifen-induced up-regulation of glutamate transporter 1 (GLT-1) in rat astrocytes. J. Biol. Chem. 2013, 288, 28975–28986. [Google Scholar] [CrossRef] [Green Version]
- Lee, E.S.Y.; Sidoryk, M.; Jiang, H.; Yin, Z.; Aschner, M. Estrogen and tamoxifen reverse manganese-induced glutamate transporter impairment in astrocytes. J. Neurochem. 2009, 110, 530–544. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Karki, P.; Kim, C.; Smith, K.; Son, D.S.; Aschner, M.; Lee, E. Transcriptional regulation of the astrocytic excitatory amino acid transporter 1 (EAAT1) via NF-κB and Yin Yang 1 (YY1). J. Biol. Chem. 2015, 290, 23725–23737. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jain, S.; Singleton, A.B. Genetics and Genomics of Parkinson’s Disease. Essent. Genom. Pers. Med. 2010, 700–711. [Google Scholar] [CrossRef]
- Sleiman, P.M.A.; Healy, D.G.; Muqit, M.M.K.; Yang, Y.X.; Brug, M.V.D.; Holton, J.L.; Revesz, T.; Quinn, N.P.; Bhatia, K.; Diss, J.K.J.; et al. Characterisation of a novel NR4A2 mutation in Parkinson’s disease brain. Neurosci Lett. 2016, 457, 75–79. [Google Scholar] [CrossRef] [Green Version]
- Hernandez, D.G.; Reed, X.; Singleton, A.B. HHS Public Access. J. Neurochem. 2016, 139, 59–74. [Google Scholar] [CrossRef]
- Inamdar, N.N.; Arulmozhi, D.K.; Tandon, A.; Bodhankar, S.L. Parkinson’s Disease: Genetics and Beyond. Curr. Neuropharmacol. 2007, 5, 99–113. [Google Scholar] [CrossRef]
- Williams, E.T.; Chen, X.; Moore, D.J.; Rapids, G. VPS35, the Retromer Complex and Parkinson’s Disease. J. Parkinsons Dis. 2017, 7, 219–233. [Google Scholar] [CrossRef] [Green Version]
- Joseph, S.; Schulz, J.B.; Stegmüller, J. Mechanistic Contributions of FBXO7 to Parkinson Disease. J. Neurochem. 2018, 144, 118–127. [Google Scholar] [CrossRef] [Green Version]
- Velayati, A.; Yu, W.H.; Sidransky, E. The Role of Glucocerebrosidase Mutations in Parkinson Disease and Lewy Body Disorders. Curr. Neurol. Neurosci. Rep. 2012, 10, 190–198. [Google Scholar] [CrossRef] [Green Version]
- Sun, L.; Shen, R.; Agnihotri, S.K.; Chen, Y.; Huang, Z.; Büeler, H. Lack of PINK1 alters glia innate immune responses and enhances inflammation-induced, nitric oxide-mediated neuron death. Sci. Rep. 2018, 8, 1–16. [Google Scholar] [CrossRef] [Green Version]
Gene Loci | Chromosomes | Proteins | Forms of PD and Age Onset | References |
---|---|---|---|---|
PARK1 | 4q21 | α-Synuclein (SNCA) | Autosomal dominant, early onset | [5,6,33,69] |
PARK2 | 6q25-27 | Parkin | Autosomal recessive, early onset | [5,6,33,69] |
PARK3 | Unknown | 2p13 | Autosomal dominant, | [6,33,69] |
PARK4 | 4q21 | SNCA | Autosomal dominant, early onset | [6,33,66,69] |
PARK5 | 4p14 | UCH-L1 | Autosomal dominant, idiopathic | [5,6,33,69] |
PARK 6 | p35–p36 | PINK1 | Autosomal recessive, early onset | [5,6,33,69] |
PARK7 | 1p36 | DJ-1 | Autosomal recessive, early onset | [5,6,33,69] |
PARK 8 | 12q12 | LRRK2 | Autosomal dominant, idiopathic | [5,6,33,66,69] |
PARK 9 | 1p36 | ATP13A2 | Kufor-Rakeb Syndrome, early onset | [6,69] |
NR4A2 | 2q22-23 | NURR1 | Autosomal dominant, late onset | [67,69] |
VPS35 | 16q11.2 | D620N | Autosomal dominant, late onset | [5,66,69,70] |
FBXO7 | 22q12.3 | F-Box Protein 7 | Autosomal-recessive, early onset | [5,66,71] |
GBA | 1q21-22 | Glucocerebrosidase | Autosomal-recessive, late onset | [5,6,66,72] |
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Hindeya Gebreyesus, H.; Gebrehiwot Gebremichael, T. The Potential Role of Astrocytes in Parkinson’s Disease (PD). Med. Sci. 2020, 8, 7. https://doi.org/10.3390/medsci8010007
Hindeya Gebreyesus H, Gebrehiwot Gebremichael T. The Potential Role of Astrocytes in Parkinson’s Disease (PD). Medical Sciences. 2020; 8(1):7. https://doi.org/10.3390/medsci8010007
Chicago/Turabian StyleHindeya Gebreyesus, Hiluf, and Teklu Gebrehiwot Gebremichael. 2020. "The Potential Role of Astrocytes in Parkinson’s Disease (PD)" Medical Sciences 8, no. 1: 7. https://doi.org/10.3390/medsci8010007
APA StyleHindeya Gebreyesus, H., & Gebrehiwot Gebremichael, T. (2020). The Potential Role of Astrocytes in Parkinson’s Disease (PD). Medical Sciences, 8(1), 7. https://doi.org/10.3390/medsci8010007