Alpha-synuclein transfers from neurons to oligodendrocytes

GLIA

Volumn 62, Issue 3, 2014, Pages 387-398

  Reyes, Juan F ^a   Rey, Nolwen L ^a   Bousset, Luc ^b   Melki, Ronald ^b   Brundin, Patrik ^a,c   Angot, Elodie ^a  

^a LUND UNIVERSITY   (Sweden)

^b LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^c VAN ANDEL RESEARCH INSTITUTE   (United States)

Author keywords

Glial cytoplasmic inclusion; Multiple system atrophy; Prion like transfer

Indexed keywords

ALPHA SYNUCLEIN; DYNAMIN; 2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; GALACTOSYLCERAMIDASE; HYDRAZONE DERIVATIVE; N'-(3,4-DIHYDROXYBENZYLIDENE)-3-HYDROXY-2-NAPHTHAHYDRAZIDE; NERVE PROTEIN; OLIG2 PROTEIN, RAT; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLP1 PROTEIN, MOUSE; PROTEOLIPID PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL INCLUSION; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN TRANSPORT; RAT; ADENOVIRIDAE; ANIMAL; ANIMAL EMBRYO; BRAIN; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DOSE RESPONSE; GENETIC TRANSDUCTION; GENETICS; HUMAN; METABOLISM; NERVE CELL; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

2',3'-CYCLIC-NUCLEOTIDE PHOSPHODIESTERASES; ADENOVIRIDAE; ALPHA-SYNUCLEIN; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; FEMALE; GALACTOSYLCERAMIDASE; HUMANS; HYDRAZONES; MALE; MICE; MICE, INBRED C57BL; MYELIN PROTEOLIPID PROTEIN; NERVE TISSUE PROTEINS; NEURONS; OLIGODENDROGLIA; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; TRANSDUCTION, GENETIC;

EID: 84892538035     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22611     Document Type: Article

References (39)

1. Ahn KJ, Paik SR, Chung KC, Kim J. 2006. Amino acid sequence motifs and mechanistic features of the membrane translocation of alpha-synuclein. J Neurochem 97:265-279.
2. Angot E, Steiner JA, Hansen C, Li JY, Brundin P. 2010. Are synucleinopathies prion-like disorders? Lancet Neurol 9:1128-1138.
3. Angot E, Steiner JA, Lema Tome CM, Ekstrom P, Mattsson B, Bjorklund A, Brundin P. 2012. Alpha-synuclein cell-to-cell transfer and seeding in grafted dopaminergic neurons in vivo. PLoS One 7:e39465.
4. Bendor JT, Logan TP, Edwards RH. 2013. The function of alpha-synuclein. Neuron 79:1044-1066.
5. Bousset L, Pieri L, Ruiz-Arlandis G, Gath J, Jensen PH, Habenstein B, Madiona K, Olieric V, Bockmann A, Meier BH, Melki R. 2013. Structural and functional characterization of two alpha-synuclein strains. Nat Commun 4:2575.
6. Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E. 2003. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 24:197-211.
7. Campbell BC, McLean CA, Culvenor JG, Gai WP, Blumbergs PC, Jakala P, Beyreuther K, Masters CL, Li QX. 2001. The solubility of alpha-synuclein in multiple system atrophy differs from that of dementia with Lewy bodies and Parkinson's disease. J Neurochem 76:87-96.
8. Danzer KM, Krebs SK, Wolff M, Birk G, Hengerer B. 2009. Seeding induced by alpha-synuclein oligomers provides evidence for spreading of alpha-synuclein pathology. J Neurochem 111:192-203.
9. Decressac M, Mattsson B, Lundblad M, Weikop P, Bjorklund A. 2012. Progressive neurodegenerative and behavioural changes induced by AAV-mediated overexpression of alpha-synuclein in midbrain dopamine neurons. Neurobiol Dis 45:939-953.
10. Frost B, Diamond MI. 2010. Prion-like mechanisms in neurodegenerative diseases. Nat Rev Neurosci 11:155-159.
11. Gai WP, Power JH, Blumbergs PC, Culvenor JG, Jensen PH. 1999. Alpha-synuclein immunoisolation of glial inclusions from multiple system atrophy brain tissue reveals multiprotein components. J Neurochem 73:2093-2100.
12. Ghee M, Melki R, Michot N, Mallet J. 2005. PA700, the regulatory complex of the 26S proteasome, interferes with alpha-synuclein assembly. FEBS J 272:4023-4033.
13. Goedert M, Clavaguera F, Tolnay M. 2010. The propagation of prion-like protein inclusions in neurodegenerative diseases. Trends Neurosci 33:317-325.
14. Hansen C, Angot E, Bergström AL, Steiner JA, Pieri L, Paul G, Outeiro TF, Melki R, Kallunki P, Fog K, Li JY, Brundin P. 2011. Alpha-synuclein propagates from mouse brain to grafted dopaminergic neurons and seeds aggregation in cultured human cells. J Clin Invest 121:715-725.
15. Kisos H, Pukass K, Ben-Hur T, Richter-Landsberg C, Sharon R. 2012. Increased neuronal alpha-synuclein pathology associates with its accumulation in oligodendrocytes in mice modeling alpha-synucleinopathies. PLoS One 7:e46817.
16. Konno M, Hasegawa T, Baba T, Miura E, Sugeno N, Kikuchi A, Fiesel FC, Sasaki T, Aoki M, Itoyama Y, Takeda A. 2012. Suppression of dynamin GTPase decreases alpha-synuclein uptake by neuronal and oligodendroglial cells: A potent therapeutic target for synucleinopathy. Mol Neurodegener 7:38.
17. Lee HJ, Suk JE, Bae EJ, Lee JH, Paik SR, Lee SJ. 2008. Assembly-dependent endocytosis and clearance of extracellular alpha-synuclein. Int J Biochem Cell Biol 40:1835-1849.
18. Luk KC, Kehm V, Carroll J, Zhang B, O'Brien P, Trojanowski JQ, Lee VM. 2012a. Pathological alpha-synuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice. Science 338:949-953.
19. Luk KC, Kehm VM, Zhang B, O'Brien P, Trojanowski JQ, Lee VM. 2012b. Intracerebral inoculation of pathological alpha-synuclein initiates a rapidly progressive neurodegenerative alpha-synucleinopathy in mice. J Exp Med 209:975-986.
20. Luk KC, Song C, O'Brien P, Stieber A, Branch JR, Brunden KR, Trojanowski JQ, Lee VM. 2009. Exogenous alpha-synuclein fibrils seed the formation of Lewy body-like intracellular inclusions in cultured cells. Proc Natl Acad Sci USA 106:20051-20056.
21. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T. 2006. Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10:839-850.
22. Masuda-Suzukake M, Nonaka T, Hosokawa M, Oikawa T, Arai T, Akiyama H, Mann DM, Hasegawa M. 2013. Prion-like spreading of pathological alpha-synuclein in brain. Brain 136(Pt 4):1128-1138.
23. Miller DW, Johnson JM, Solano SM, Hollingsworth ZR, Standaert DG, Young AB. 2005. Absence of alpha-synuclein mRNA expression in normal and multiple system atrophy oligodendroglia. J Neural Transm 112:1613-1624.
24. Moser M, Colello RJ, Pott U, Oesch B. 1995. Developmental expression of the prion protein gene in glial cells. Neuron 14:509-517.
25. Mougenot AL, Nicot S, Bencsik A, Morignat E, Verchere J, Lakhdar L, Legastelois S, Baron T. 2012. Prion-like acceleration of a synucleinopathy in a transgenic mouse model. Neurobiol Aging 33:2225-2228.
26. Nave KA, Trapp BD. 2008. Axon-glial signaling and the glial support of axon function. Annu Rev Neurosci 31:535-561.
27. Nonaka T, Watanabe ST, Iwatsubo T, Hasegawa M. 2010. Seeded aggregation and toxicity of {alpha}-synuclein and tau: Cellular models of neurodegenerative diseases. J Biol Chem 285:34885-34898.
28. Pieri L, Madiona K, Bousset L, Melki R. 2012. Fibrillar alpha-synuclein and huntingtin exon 1 assemblies are toxic to the cells. Biophys J 102:2894-2905.
29. Pomozi V, Le Saux O, Brampton C, Apana A, Ilias A, Szeri F, Martin L, Monostory K, Paku S, Sarkadi B, Váradi A. 2013. ABCC6 is a basolateral plasma membrane protein. Circ Res 112:e148-e151.
30. Rey NL, Petit GH, Bousset L, Melki R, Brundin P. 2013. Transfer of human alpha-synuclein from the olfactory bulb to interconnected brain regions in mice. Acta Neuropathol 126:555-573.
31. Rockenstein E, Ubhi K, Inglis C, Mante M, Patrick C, Adame A, Masliah E. 2012. Neuronal to oligodendroglial alpha-synuclein redistribution in a double transgenic model of multiple system atrophy. Neuroreport 23:259-264.
32. Sung JY, Kim J, Paik SR, Park JH, Ahn YS, Chung KC. 2001. Induction of neuronal cell death by Rab5A-dependent endocytosis of alpha-synuclein. The Journal of biological chemistry 276:27441-27448.
33. Tong J, Wong H, Guttman M, Ang LC, Forno LS, Shimadzu M, Rajput AH, Muenter MD, Kish SJ, Hornykiewicz O, Furukawa Y. 2010. Brain alpha-synuclein accumulation in multiple system atrophy, Parkinson's disease and progressive supranuclear palsy: A comparative investigation. Brain 133(Pt 1):172-188.
34. Ubhi K, Low P, Masliah E. 2011. Multiple system atrophy: A clinical and neuropathological perspective. Trends Neurosci 34:581-590.
35. van Meeteren ME, Koetsier MA, Dijkstra CD, van Tol EA. 2005. Markers for OLN-93 oligodendroglia differentiation. Brain Res Dev Brain Res 156:78-86.
36. Volpicelli-Daley LA, Luk KC, Patel TP, Tanik SA, Riddle DM, Stieber A, Meaney DF, Trojanowski JQ, Lee VM. 2011. Exogenous alpha-synuclein fibrils induce Lewy body pathology leading to synaptic dysfunction and neuron death. Neuron 72:57-71.
37. Waxman EA, Giasson BI. 2009. Molecular mechanisms of alpha-synuclein neurodegeneration. Biochim Biophys Acta 1792:616-624.
38. Waxman EA, Giasson BI. 2010. A novel, high-efficiency cellular model of fibrillar alpha-synuclein inclusions and the examination of mutations that inhibit amyloid formation. J Neurochem 113:374-388.
39. Yakunin E, Loeb V, Kisos H, Biala Y, Yehuda S, Yaari Y, Selkoe DJ, Sharon R. 2012. Alpha-synuclein neuropathology is controlled by nuclear hormone receptors and enhanced by docosahexaenoic acid in a mouse model for Parkinson's disease. Brain Pathol 22:280-294.