α-Synuclein impairs oligodendrocyte progenitor maturation in multiple system atrophy

Neurobiology of Aging

Volumn 35, Issue 10, 2014, Pages 2357-2368

  May, Verena E L ^a   Ettle, Benjamin ^a   Poehler, Anne Maria ^a   Nuber, Silke ^b   Ubhi, Kiren ^b   Rockenstein, Edward ^b   Winner, Beate ^c   Wegner, Michael ^a   Masliah, Eliezer ^b   Winkler, Jürgen ^a,b  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY HOSPITAL ERLANGEN   (Germany)

Author keywords

Alpha synuclein; CG4; Differentiation; Maturation; Multiple system atrophy; Myelin basic protein; Oligodendrocyte precursors; Oligodendrogenesis; Platelet derived growth factor receptor alpha; Transgenic

Indexed keywords

ALPHA SYNUCLEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; MYELIN BASIC PROTEIN; NEUROTROPHIC FACTOR; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; TRANSCRIPTION FACTOR HES 5;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPSY; BRAIN CORTEX; CATALYSIS; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; CORPUS CALLOSUM; CORPUS STRIATUM; DOWN REGULATION; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; OLIGODENDROGLIA; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SHY DRAGER SYNDROME; STEM CELL; WESTERN BLOTTING; AGING; ANIMAL; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; DISEASE MODEL; METABOLISM; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE; VERY ELDERLY;

AGED; AGED, 80 AND OVER; AGING; ALPHA-SYNUCLEIN; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CEREBRAL CORTEX; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE, TRANSGENIC; MIDDLE AGED; MULTIPLE SYSTEM ATROPHY; OLIGODENDROGLIA; STEM CELLS;

EID: 84903816220     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.02.028     Document Type: Article

References (58)

1. Ahmed Z., Asi Y.T., Lees A.J., Revesz T., Holton J.L. Identification and quantification of oligodendrocyte precursor cells in multiple system atrophy, progressive supranuclear palsy and Parkinson's disease. Brain Pathol. 2012, 23:263-273. 10.1111/j.1750-3639.2012.00637.x.
2. Ahmed Z., Asi Y.T., Sailer A., Lees A.J., Houlden H., Revesz T., Holton J.L. The neuropathology, pathophysiology and genetics of multiple system atrophy. Neuropathol. Appl. Neurobiol. 2012, 38:4-24.
3. Arnett H.A., Fancy S.P., Alberta J.A., Zhao C., Plant S.R., Kaing S., Raine C.S., Rowitch D.H., Franklin R.J., Stiles C.D. bHLH transcription factor Olig1 is required to repair demyelinated lesions in the CNS. Science 2004, 306:2111-2115.
4. Dawson M.R., Levine J.M., Reynolds R. NG2-expressing cells in the central nervous system: are they oligodendroglial progenitors?. J.Neurosci. Res. 2000, 61:471-479.
5. Dickson D.W., Liu W., Hardy J., Farrer M., Mehta N., Uitti R., Mark M., Zimmerman T., Golbe L., Sage J., Sima A., D'Amato C., Albin R., Gilman S., Yen S.H. Widespread alterations of alpha-synuclein in multiple system atrophy. Am. J. Pathol. 1999, 155:1241-1251.
6. Du Y., Fischer T.Z., Clinton-Luke P., Lercher L.D., Dreyfus C.F. Distinct effects of p75 in mediating actions of neurotrophins on basal forebrain oligodendrocytes. Mol. Cell Neurosci. 2006, 31:366-375.
7. Du Y., Fischer T.Z., Lee L.N., Lercher L.D., Dreyfus C.F. Regionally specific effects of BDNF on oligodendrocytes. Dev. Neurosci. 2003, 25:116-126.
8. Du Y., Lercher L.D., Zhou R., Dreyfus C.F. Mitogen-activated protein kinase pathway mediates effects of brain-derived neurotrophic factor on differentiation of basal forebrain oligodendrocytes. J.Neurosci. Res. 2006, 84:1692-1702.
9. Emery B. Regulation of oligodendrocyte differentiation and myelination. Science 2010, 330:779-782.
10. Emery B., Agalliu D., Cahoy J.D., Watkins T.A., Dugas J.C., Mulinyawe S.B., Ibrahim A., Ligon K.L., Rowitch D.H., Barres B.A. Myelin gene regulatory factor is a critical transcriptional regulator required for CNS myelination. Cell 2009, 138:172-185.
11. Fancy S.P., Baranzini S.E., Zhao C., Yuk D.I., Irvine K.A., Kaing S., Sanai N., Franklin R.J., Rowitch D.H. Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes dev. 2009, 23:1571-1585.
12. Fancy S.P., Chan J.R., Baranzini S.E., Franklin R.J., Rowitch D.H. Myelin regeneration: a recapitulation of development?. Annu. Rev. Neurosci. 2011, 34:21-43.
13. Franklin K.B., Paxinos G. The Mouse Brain in Stereotaxic Coordinates 2008, Elsevier. third ed.
14. Gundersen H.J., Bendtsen T.F., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenberg B., Sorensen F.B., Vesterby A., West M.J. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 1988, 96:379-394.
15. Hansen C., Angot E., Bergstrom A.L., Steiner J.A., Pieri L., Paul G., Outeiro T.F., Melki R., Kallunki P., Fog K., Li J.Y., Brundin P. alpha-Synuclein propagates from mouse brain to grafted dopaminergic neurons and seeds aggregation in cultured human cells. J.Clin. Invest 2011, 121:715-725.
16. Hayes J.D., Pulford D.J. The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit. Rev. Biochem. Mol. Biol. 1995, 30:445-600.
17. John G.R., Shankar S.L., Shafit-Zagardo B., Massimi A., Lee S.C., Raine C.S., Brosnan C.F. Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nat. Med. 2002, 8:1115-1121.
18. Jones R. Glia: oligodendrocyte transporters feed axons. Nat. Rev. Neurosci. 2012, 13:601.
19. Kahle P.J., Neumann M., Ozmen L., Muller V., Jacobsen H., Spooren W., Fuss B., Mallon B., Macklin W.B., Fujiwara H., Hasegawa M., Iwatsubo T., Kretzschmar H.A., Haass C. Hyperphosphorylation and insolubility of alpha-synuclein in transgenic mouse oligodendrocytes. EMBO Rep. 2002, 3:583-588.
20. Kisos H., Pukass K., Ben-Hur T., Richter-Landsberg C., Sharon R. Increased neuronal alpha-synuclein pathology associates with its accumulation in oligodendrocytes in mice modeling alpha-synucleinopathies. PLoS One 2012, 7:e46817.
21. Klucken J., Poehler A.M., Ebrahimi-Fakhari D., Schneider J., Nuber S., Rockenstein E., Schlotzer-Schrehardt U., Hyman B.T., McLean P.J., Masliah E., Winkler J. Alpha-synuclein aggregation involves a bafilomycin A 1-sensitive autophagy pathway. Autophagy 2012, 8:754-766.
22. Kohl Z., Winner B., Ubhi K., Rockenstein E., Mante M., Munch M., Barlow C., Carter T., Masliah E., Winkler J. Fluoxetine rescues impaired hippocampal neurogenesis in a transgenic A53T synuclein mouse model. Eur. J. Neurosci. 2012, 35:10-19.
23. Kordower J.H., Dodiya H.B., Kordower A.M., Terpstra B., Paumier K., Madhavan L., Sortwell C., Steece-Collier K., Collier T.J. Transfer of host-derived alpha synuclein to grafted dopaminergic neurons in rat. Neurobiol. Dis. 2011, 43:552-557.
24. Kuhlmann T., Miron V., Cui Q., Wegner C., Antel J., Bruck W. Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 2008, 131(Pt 7):1749-1758.
25. Lang E.M., Schlegel N., Reiners K., Hofmann G.O., Sendtner M., Asan E. Single-dose application of CNTF and BDNF improves remyelination of regenerating nerve fibers after C7 ventral root avulsion and replantation. J.Neurotrauma 2008, 25:384-400.
26. Lee H.J., Suk J.E., Bae E.J., Lee S.J. Clearance and deposition of extracellular alpha-synuclein aggregates in microglia. Biochem. Biophys. Res. Commun. 2008, 372:423-428.
27. Lee S.J., Desplats P., Sigurdson C., Tsigelny I., Masliah E. Cell-to-cell transmission of non-prion protein aggregates. Nat. Rev. Neurol. 2010, 6:702-706.
28. Liu A., Li J., Marin-Husstege M., Kageyama R., Fan Y., Gelinas C., Casaccia-Bonnefil P. Amolecular insight of Hes5-dependent inhibition of myelin gene expression: old partners and new players. EMBO J. 2006, 25:4833-4842.
29. Marxreiter F., Regensburger M., Winkler J. Adult neurogenesis in Parkinson's disease. Cell. Mol. Life Sci. 2012, 10.1007/s00018-012-1062-x.
30. McTigue D.M., Horner P.J., Stokes B.T., Gage F.H. Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J.Neurosci. 1998, 18:5354-5365.
31. Miller R.H. Regulation of oligodendrocyte development in the vertebrate CNS. Prog. Neurobiol. 2002, 67:451-467.
32. Nemani V.M., Lu W., Berge V., Nakamura K., Onoa B., Lee M.K., Chaudhry F.A., Nicoll R.A., Edwards R.H. Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron 2010, 65:66-79.
33. Nicolay D.J., Doucette J.R., Nazarali A.J. Transcriptional control of oligodendrogenesis. Glia 2007, 55:1287-1299.
34. Ozawa T., Okuizumi K., Ikeuchi T., Wakabayashi K., Takahashi H., Tsuji S. Analysis of the expression level of alpha-synuclein mRNA using postmortem brain samples from pathologically confirmed cases of multiple system atrophy. Acta Neuropathol. 2001, 102:188-190.
35. Ozawa T., Paviour D., Quinn N.P., Josephs K.A., Sangha H., Kilford L., Healy D.G., Wood N.W., Lees A.J., Holton J.L., Revesz T. The spectrum of pathological involvement of the striatonigral and olivopontocerebellar systems in multiple system atrophy: clinicopathological correlations. Brain 2004, 127(Pt 12):2657-2671.
36. Papp M.I., Kahn J.E., Lantos P.L. Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J.Neurol. Sci. 1989, 94:79-100.
37. Papp M.I., Lantos P.L. The distribution of oligodendroglial inclusions in multiple system atrophy and its relevance to clinical symptomatology. Brain 1994, 117(Pt 2):235-243.
38. Patel J.R., Klein R.S. Mediators of oligodendrocyte differentiation during remyelination. FEBS lett. 2011, 585:3730-3737.
39. Richardson W.D., Young K.M., Tripathi R.B., McKenzie I. NG2-glia as multipotent neural stem cells: fact or fantasy?. Neuron 2011, 70:661-673.
40. Rivers L.E., Young K.M., Rizzi M., Jamen F., Psachoulia K., Wade A., Kessaris N., Richardson W.D. PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat. Neurosci. 2008, 11:1392-1401.
41. Shults C.W., Rockenstein E., Crews L., Adame A., Mante M., Larrea G., Hashimoto M., Song D., Iwatsubo T., Tsuboi K., Masliah E. Neurological and neurodegenerative alterations in a transgenic mouse model expressing human alpha-synuclein under oligodendrocyte promoter: implications for multiple system atrophy. J.Neurosci. 2005, 25:10689-10699.
42. Simon C., Gotz M., Dimou L. Progenitors in the adult cerebral cortex: cell cycle properties and regulation by physiological stimuli and injury. Glia 2011, 59:869-881.
43. Stefanova N., Reindl M., Neumann M., Haass C., Poewe W., Kahle P.J., Wenning G.K. Oxidative stress in transgenic mice with oligodendroglial alpha-synuclein overexpression replicates the characteristic neuropathology of multiple system atrophy. Am. J. Pathol. 2005, 166:869-876.
44. Tamura Y., Kataoka Y., Cui Y., Takamori Y., Watanabe Y., Yamada H. Intracellular translocation of glutathione S-transferase pi during oligodendrocyte differentiation in adult rat cerebral cortex invivo. Neuroscience 2007, 148:535-540.
45. Tansey F.A., Cammer W. Api form of glutathione-S-transferase is a myelin- and oligodendrocyte-associated enzyme in mouse brain. J.Neurochem. 1991, 57:95-102.
46. Tofaris G.K., Spillantini M.G. Physiological and pathological properties of alpha-synuclein. Cell. Mol. Life Sci. 2007, 64:2194-2201.
47. Trotter J., Karram K., Nishiyama A. NG2 cells: properties, progeny and origin. Brain Res. Rev. 2010, 10.1016/j.brainresrev.2009.12.006.
48. Ubhi K., Inglis C., Mante M., Patrick C., Adame A., Spencer B., Rockenstein E., May V., Winkler J., Masliah E. Fluoxetine ameliorates behavioral and neuropathological deficits in a transgenic model mouse of alpha-synucleinopathy. Exp. Neurol. 2012, 234:405-416.
49. Ubhi K., Rockenstein E., Mante M., Inglis C., Adame A., Patrick C., Whitney K., Masliah E. Neurodegeneration in a transgenic mouse model of multiple system atrophy is associated with altered expression of oligodendroglial-derived neurotrophic factors. J.Neurosci. 2010, 30:6236-6246.
50. Wakabayashi K., Takahashi H. Cellular pathology in multiple system atrophy. Neuropathology 2006, 26:338-345.
51. Wang S., Sdrulla A.D., diSibio G., Bush G., Nofziger D., Hicks C., Weinmaster G., Barres B.A. Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 1998, 21:63-75.
52. Wegner M. Amatter of identity: transcriptional control in oligodendrocytes. J.Mol. Neurosci. 2008, 35:3-12.
53. Wenning G.K., Colosimo C. Diagnostic criteria for multiple system atrophy and progressive supranuclear palsy. Rev. Neurol. (Paris) 2010, 166:829-833.
54. Winner B., Kohl Z., Gage F.H. Neurodegenerative disease and adult neurogenesis. Eur. J. Neurosci. 2011, 33:1139-1151.
55. Winner B., Regensburger M., Schreglmann S., Boyer L., Prots I., Rockenstein E., Mante M., Zhao C., Winkler J., Masliah E., Gage F.H. Role of alpha-synuclein in adult neurogenesis and neuronal maturation in the dentate gyrus. J.Neurosci. 2012, 32:16906-16916.
56. Xiao J., Wong A.W., Willingham M.M., van den Buuse M., Kilpatrick T.J., Murray S.S. Brain-derived neurotrophic factor promotes central nervous system myelination via a direct effect upon oligodendrocytes. Neuro-Signals 2010, 18:186-202.
57. Yazawa I., Giasson B.I., Sasaki R., Zhang B., Joyce S., Uryu K., Trojanowski J.Q., Lee V.M. Mouse model of multiple system atrophy alpha-synuclein expression in oligodendrocytes causes glial and neuronal degeneration. Neuron 2005, 45:847-859.
58. Ye F., Chen Y., Hoang T., Montgomery R.L., Zhao X.H., Bu H., Hu T., Taketo M.M., van Es J.H., Clevers H., Hsieh J., Bassel-Duby R., Olson E.N., Lu Q.R. HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat. Neurosci. 2009, 12:829-838.