|
|
|
Oligodendrocytes in neurodegenerative diseases |
Yingjun LIU, Jiawei ZHOU( ) |
| Institute of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China |
|
|
|
|
Abstract Oligodendrocyte is a highly specialized glial cell type in the vertebrate central nervous system, which guarantees the long-distance transmission of action potential by producing myelin sheath wrapping adjacent axons. Disrupted myelin and oligodendrocytes are hallmarks of some devastating neurological diseases, such as multiple sclerosis, although their contribution to neurodegeneration in a given disease is still controversial. However, accumulating evidence from clinical studies and genetic animal models implicates oligodendrocyte dysfunction as one of major events in the processes of initiation and progression of neurodegeneration. In this article, we will review recent progress in understanding non-traditional function of oligodendrocytes in neuronal support and protection independent of myelin sheath and its possible contribution to neurodegeneration. Oligodendrocytes play a pivotal role in neurodegenerative diseases among which special emphasis is given to multiple system atrophy and Alzheimer’s disease in this review.
|
| Keywords
Glia
oligodendrocyte
neurodegenerative disease
myelin sheath
multiple sclerosis
multiple system atrophy
Alzheimer’s disease
Parkinson’s disease
|
|
Corresponding Author(s):
ZHOU Jiawei,Email:jwzhou@ion.ac.cn
|
|
Issue Date: 01 April 2013
|
|
| 1 |
Anderson T J, Schneider A, Barrie J A, Klugmann M, McCulloch M C, Kirkham D, Kyriakides E, Nave K A, Griffiths I R (1998). Late-onset neurodegeneration in mice with increased dosage of the proteolipid protein gene. J Comp Neurol , 394(4): 506-519
doi: 10.1002/(SICI)1096-9861(19980518)394:4<506::AID-CNE8>3.0.CO;2-5 pmid:9590558
|
| 2 |
Arima K, Uéda K, Sunohara N, Arakawa K, Hirai S, Nakamura M, Tonozuka-Uehara H, Kawai M (1998). NACP/alpha-synuclein immunoreactivity in fibrillary components of neuronal and oligodendroglial cytoplasmic inclusions in the pontine nuclei in multiple system atrophy. Acta Neuropathol , 96(5): 439-444
doi: 10.1007/s004010050917 pmid:9829806
|
| 3 |
Bartzokis G (2004). Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer’s disease. Neurobiol Aging , 25(1): 5-18, author reply 49-62
doi: 10.1016/j.neurobiolaging.2003.03.001 pmid:14675724
|
| 4 |
Benrud-Larson L M, Sandroni P, Schrag A, Low P A (2005). Depressive symptoms and life satisfaction in patients with multiple system atrophy. Mov Disord , 20(8): 951-957
doi: 10.1002/mds.20450 pmid:15782421
|
| 5 |
Breteler M M, Claus J J, van Duijn C M, Launer L J, Hofman A (1992). Epidemiology of Alzheimer’s disease. Epidemiol Rev , 14: 59-82
pmid:1289117
|
| 6 |
Buch T, Heppner F L, Tertilt C, Heinen T J, Kremer M, Wunderlich F T, Jung S, Waisman A (2005). A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat Methods , 2(6): 419-426
doi: 10.1038/nmeth762 pmid:15908920
|
| 7 |
Desai M K, Guercio B J, Narrow W C, Bowers W J (2011). An Alzheimer’s disease-relevant presenilin-1 mutation augments amyloid-beta-induced oligodendrocyte dysfunction. Glia , 59(4): 627-640
doi: 10.1002/glia.21131 pmid:21294162
|
| 8 |
Desai M K, Mastrangelo M A, Ryan D A, Sudol K L, Narrow W C, Bowers W J (2010). Early oligodendrocyte/myelin pathology in Alzheimer’s disease mice constitutes a novel therapeutic target. Am J Pathol , 177(3): 1422-1435
doi: 10.2353/ajpath.2010.100087 pmid:20696774
|
| 9 |
Desai M K, Sudol K L, Janelsins M C, Mastrangelo M A, Frazer M E, Bowers W J (2009). Triple-transgenic Alzheimer’s disease mice exhibit region-specific abnormalities in brain myelination patterns prior to appearance of amyloid and tau pathology. Glia , 57(1): 54-65
doi: 10.1002/glia.20734 pmid:18661556
|
| 10 |
Dickson D W, Lin W, Liu W K, Yen S H (1999). Multiple system atrophy: a sporadic synucleinopathy. Brain Pathol , 9(4): 721-732
doi: 10.1111/j.1750-3639.1999.tb00553.x pmid:10517510
|
| 11 |
Edgar J M, McLaughlin M, Barrie J A, McCulloch M C, Garbern J, Griffiths I R (2004). Age-related axonal and myelin changes in the rumpshaker mutation of the Plp gene. Acta Neuropathol , 107(4): 331-335
doi: 10.1007/s00401-003-0808-9 pmid:14745569
|
| 12 |
Feigenbaum V, Gélot A, Casanova P, Daumas-Duport C, Aubourg P, Dubois-Dalcq M (2000). Apoptosis in the central nervous system of cerebral adrenoleukodystrophy patients. Neurobiol Dis , 7(6 6 Pt B): 600-612
doi: 10.1006/nbdi.2000.0315 pmid:11114259
|
| 13 |
Fellner L, Jellinger K A, Wenning G K, Stefanova N (2011). Glial dysfunction in the pathogenesis of α-synucleinopathies: emerging concepts. Acta Neuropathol , 121(6): 675-693
doi: 10.1007/s00401-011-0833-z pmid:21562886
|
| 14 |
Fünfschilling U, Supplie L M, Mahad D, Boretius S, Saab A S, Edgar J, Brinkmann B G, Kassmann C M, Tzvetanova I D, M?bius W, Diaz F, Meijer D, Suter U, Hamprecht B, Sereda M W, Moraes C T, Frahm J, Goebbels S, Nave K A (2012). Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature , 485(7399): 517-521
pmid:22622581
|
| 15 |
Garcia-Ladona F J, Huss Y, Frey P, Ghandour M S (1997). Oligodendrocytes express different isoforms of beta-amyloid precursor protein in chemically defined cell culture conditions: in situ hybridization and immunocytochemical detection. J Neurosci Res , 50(1): 50-61
doi: 10.1002/(SICI)1097-4547(19971001)50:1<50::AID-JNR6>3.0.CO;2-K pmid:9379493
|
| 16 |
Ghosh A, Manrique-Hoyos N, Voigt A, Schulz J B, Kreutzfeldt M, Merkler D, Simons M (2011). Targeted ablation of oligodendrocytes triggers axonal damage. PLoS ONE , 6(7): e22735
doi: 10.1371/journal.pone.0022735 pmid:21818378
|
| 17 |
Griffiths I, Klugmann M, Anderson T, Yool D, Thomson C, Schwab M H, Schneider A, Zimmermann F, McCulloch M, Nadon N, Nave K A (1998). Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science , 280(5369): 1610-1613
doi: 10.1126/science.280.5369.1610 pmid:9616125
|
| 18 |
Harrington E P, Zhao C, Fancy S P, Kaing S, Franklin R J, Rowitch D H (2010). Oligodendrocyte PTEN is required for myelin and axonal integrity, not remyelination. Ann Neurol , 68(5): 703-716
doi: 10.1002/ana.22090 pmid:20853437
|
| 19 |
Heneka M T, Rodríguez J J, Verkhratsky A (2010). Neuroglia in neurodegeneration. Brain Res Brain Res Rev , 63(1-2): 189-211
doi: 10.1016/j.brainresrev.2009.11.004 pmid:19944719
|
| 20 |
Higuchi M, Zhang B, Forman M S, Yoshiyama Y, Trojanowski J Q, Lee V M (2005). Axonal degeneration induced by targeted expression of mutant human tau in oligodendrocytes of transgenic mice that model glial tauopathies. J Neurosci , 25(41): 9434-9443
doi: 10.1523/JNEUROSCI.2691-05.2005 pmid:16221853
|
| 21 |
Jantaratnotai N, Ryu J K, Kim S U, McLarnon J G (2003). Amyloid beta peptide-induced corpus callosum damage and glial activation in vivo. Neuroreport , 14(11): 1429-1433
doi: 10.1097/00001756-200308060-00005 pmid:12960758
|
| 22 |
Kahle P J (2008). alpha-Synucleinopathy models and human neuropathology: similarities and differences. Acta Neuropathol , 115(1): 87-95
doi: 10.1007/s00401-007-0302-x pmid:17932682
|
| 23 |
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 (2002). Hyperphosphorylation and insolubility of alpha-synuclein in transgenic mouse oligodendrocytes. EMBO Rep , 3(6): 583-588
doi: 10.1093/embo-reports/kvf109 pmid:12034752
|
| 24 |
Kassmann C M, Lappe-Siefke C, Baes M, Brügger B, Mildner A, Werner H B, Natt O, Michaelis T, Prinz M, Frahm J, Nave K A (2007). Axonal loss and neuroinflammation caused by peroxisome-deficient oligodendrocytes. Nat Genet , 39(8): 969-976
doi: 10.1038/ng2070 pmid:17643102
|
| 25 |
Kato S, Nakamura H (1990). Cytoplasmic argyrophilic inclusions in neurons of pontine nuclei in patients with olivopontocerebellar atrophy: immunohistochemical and ultrastructural studies. Acta Neuropathol , 79(6): 584-594
doi: 10.1007/BF00294235 pmid:2163181
|
| 26 |
Kato S, Nakamura H, Hirano A, Ito H, Llena J F, Yen S H (1991). Argyrophilic ubiquitinated cytoplasmic inclusions of Leu-7-positive glial cells in olivopontocerebellar atrophy (multiple system atrophy). Acta Neuropathol , 82(6): 488-493
doi: 10.1007/BF00293383 pmid:1723828
|
| 27 |
Kohama S G, Rosene D L, Sherman L S (2011). Age-related changes in human and non-human primate white matter: from myelination disturbances to cognitive decline. Age, 34(5): 1093-1110
|
| 28 |
Lappe-Siefke C, Goebbels S, Gravel M, Nicksch E, Lee J, Braun PE, Griffiths IR, Nave KA(2003). Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet , 33(3): 366-374
|
| 29 |
Lasiene J, Matsui A, Sawa Y, Wong F, Horner P J (2009). Age-related myelin dynamics revealed by increased oligodendrogenesis and short internodes. Aging Cell , 8(2): 201-213
doi: 10.1111/j.1474-9726.2009.00462.x pmid:19338498
|
| 30 |
Lee J T, Xu J, Lee J M, Ku G, Han X, Yang D I, Chen S, Hsu C Y (2004). Amyloid-beta peptide induces oligodendrocyte death by activating the neutral sphingomyelinase-ceramide pathway. J Cell Biol , 164(1): 123-131
doi: 10.1083/jcb.200307017 pmid:14709545
|
| 31 |
Lee Y, Morrison B M, Li Y, Lengacher S, Farah M H, Hoffman P N, Liu Y, Tsingalia A, Jin L, Zhang P W, Pellerin L, Magistretti P J, Rothstein J D (2012). Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature , 487(7408): 443-448
doi: 10.1038/nature11314 pmid:22801498
|
| 32 |
Locatelli G, W?rtge S, Buch T, Ingold B, Frommer F, Sobottka B, Krüger M, Karram K, Bühlmann C, Bechmann I, Heppner F L, Waisman A, Becher B (2012). Primary oligodendrocyte death does not elicit anti-CNS immunity. Nat Neurosci , 15(4): 543-550
doi: 10.1038/nn.3062 pmid:22366759
|
| 33 |
Mena M A, García de Yébenes J (2008). Glial cells as players in parkinsonism: the “good,” the “bad,” and the “mysterious” glia. Neuroscientist , 14(6): 544-560
doi: 10.1177/1073858408322839 pmid:19029058
|
| 34 |
Mitew S, Kirkcaldie M T, Halliday G M, Shepherd C E, Vickers J C, Dickson T C (2010). Focal demyelination in Alzheimer’s disease and transgenic mouse models. Acta Neuropathol , 119(5): 567-577
doi: 10.1007/s00401-010-0657-2 pmid:20198482
|
| 35 |
Nave K A (2010a). Myelination and support of axonal integrity by glia. Nature , 468(7321): 244-252
doi: 10.1038/nature09614 pmid:21068833
|
| 36 |
Nave K A (2010b). Myelination and the trophic support of long axons. Nat Rev Neurosci , 11(4): 275-283
doi: 10.1038/nrn2797 pmid:20216548
|
| 37 |
Nave K A, Trapp B D (2008). Axon-glial signaling and the glial support of axon function. Annu Rev Neurosci , 31(1): 535-561
doi: 10.1146/annurev.neuro.30.051606.094309 pmid:18558866
|
| 38 |
Oluich L J, Stratton J A, Xing Y L, Ng S W, Cate H S, Sah P, Windels F, Kilpatrick T J, Merson T D (2012). Targeted ablation of oligodendrocytes induces axonal pathology independent of overt demyelination. J Neurosci , 32(24): 8317-8330
doi: 10.1523/JNEUROSCI.1053-12.2012 pmid:22699912
|
| 39 |
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 (2004). The spectrum of pathological involvement of the striatonigral and olivopontocerebellar systems in multiple system atrophy: clinicopathological correlations. Brain , 127(Pt 12): 2657-2671
doi: 10.1093/brain/awh303 pmid:15509623
|
| 40 |
Papp M I, Kahn J E, Lantos P L (1989). Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J Neurol Sci , 94(1-3): 79-100
doi: 10.1016/0022-510X(89)90219-0 pmid:2559165
|
| 41 |
Papp M I, Lantos P L (1992). Accumulation of tubular structures in oligodendroglial and neuronal cells as the basic alteration in multiple system atrophy. J Neurol Sci , 107(2): 172-182
doi: 10.1016/0022-510X(92)90286-T pmid:1314292
|
| 42 |
Pfeiffer R F (2007). Multiple system atrophy. Handb Clin Neurol , 84: 305-326
doi: 10.1016/S0072-9752(07)84046-2 pmid:18808955
|
| 43 |
Pohl H B, Porcheri C, Mueggler T, Bachmann L C, Martino G, Riethmacher D, Franklin R J, Rudin M, Suter U (2011). Genetically induced adult oligodendrocyte cell death is associated with poor myelin clearance, reduced remyelination, and axonal damage. J Neurosci , 31(3): 1069-1080
doi: 10.1523/JNEUROSCI.5035-10.2011 pmid:21248132
|
| 44 |
Roher A E, Weiss N, Kokjohn T A, Kuo Y M, Kalback W, Anthony J, Watson D, Luehrs D C, Sue L, Walker D, Emmerling M, Goux W, Beach T (2002). Increased A beta peptides and reduced cholesterol and myelin proteins characterize white matter degeneration in Alzheimer’s disease. Biochemistry , 41(37): 11080-11090
doi: 10.1021/bi026173d pmid:12220172
|
| 45 |
Rowe W B, Blalock E M, Chen K C, Kadish I, Wang D, Barrett J E, Thibault O, Porter N M, Rose G M, Landfield P W (2007). Hippocampal expression analyses reveal selective association of immediate-early, neuroenergetic, and myelinogenic pathways with cognitive impairment in aged rats. J Neurosci , 27(12): 3098-3110
doi: 10.1523/JNEUROSCI.4163-06.2007 pmid:17376971
|
| 46 |
Schiffmann R, van der Knaap M S (2004). The latest on leukodystrophies. Curr Opin Neurol , 17(2): 187-192
doi: 10.1097/00019052-200404000-00017 pmid:15021247
|
| 47 |
Shin D, Shin J Y, McManus M T, Ptácek L J, Fu Y H (2009). Dicer ablation in oligodendrocytes provokes neuronal impairment in mice. Ann Neurol , 66(6): 843-857
doi: 10.1002/ana.21927 pmid:20035504
|
| 48 |
Shults C W, Rockenstein E, Crews L, Adame A, Mante M, Larrea G, Hashimoto M, Song D, Iwatsubo T, Tsuboi K, Masliah E (2005). Neurological and neurodegenerative alterations in a transgenic mouse model expressing human alpha-synuclein under oligodendrocyte promoter: implications for multiple system atrophy. J Neurosci , 25(46): 10689-10699
doi: 10.1523/JNEUROSCI.3527-05.2005 pmid:16291942
|
| 49 |
Singh S, Swarnkar S, Goswami P, Nath C (2011). Astrocytes and microglia: responses to neuropathological conditions. Int J Neurosci , 121(11): 589-597
doi: 10.3109/00207454.2011.598981 pmid:21827229
|
| 50 |
Sloane J A, Hinman J D, Lubonia M, Hollander W, Abraham C R (2003). Age-dependent myelin degeneration and proteolysis of oligodendrocyte proteins is associated with the activation of calpain-1 in the rhesus monkey. J Neurochem , 84(1): 157-168
doi: 10.1046/j.1471-4159.2003.01541.x pmid:12485412
|
| 51 |
Soma H, Yabe I, Takei A, Fujiki N, Yanagihara T, Sasaki H (2006). Heredity in multiple system atrophy. J Neurol Sci , 240(1-2): 107-110
doi: 10.1016/j.jns.2005.09.003 pmid:16307759
|
| 52 |
Spillantini M G, Crowther R A, Jakes R, Cairns N J, Lantos P L, Goedert M (1998). Filamentous alpha-synuclein inclusions link multiple system atrophy with Parkinson’s disease and dementia with Lewy bodies. Neurosci Lett , 251(3): 205-208
doi: 10.1016/S0304-3940(98)00504-7 pmid:9726379
|
| 53 |
Stefanova N, Bücke P, Duerr S, Wenning G K (2009). Multiple system atrophy: an update. Lancet Neurol , 8(12): 1172-1178
doi: 10.1016/S1474-4422(09)70288-1 pmid:19909915
|
| 54 |
Stefanova N, Reindl M, Neumann M, Kahle P J, Poewe W, Wenning G K (2007). Microglial activation mediates neurodegeneration related to oligodendroglial alpha-synucleinopathy: implications for multiple system atrophy. Mov Disord , 22(15): 2196-2203
doi: 10.1002/mds.21671 pmid:17853477
|
| 55 |
Stemberger S, Poewe W, Wenning G K, Stefanova N (2010). Targeted overexpression of human alpha-synuclein in oligodendroglia induces lesions linked to MSA-like progressive autonomic failure. Exp Neurol , 224(2): 459-464
doi: 10.1016/j.expneurol.2010.05.008 pmid:20493840
|
| 56 |
Tanaka J, Okuma Y, Tomobe K, Nomura Y (2005). The age-related degeneration of oligodendrocytes in the hippocampus of the senescence-accelerated mouse (SAM) P8: a quantitative immunohistochemical study. Biol Pharm Bull , 28(4): 615-618
doi: 10.1248/bpb.28.615 pmid:15802797
|
| 57 |
Trapp B D, Nave K A (2008). Multiple sclerosis: an immune or neurodegenerative disorder? Annu Rev Neurosci , 31(1): 247-269
doi: 10.1146/annurev.neuro.30.051606.094313 pmid:18558855
|
| 58 |
Tu P H, Galvin J E, Baba M, Giasson B, Tomita T, Leight S, Nakajo S, Iwatsubo T, Trojanowski J Q, Lee V M (1998). Glial cytoplasmic inclusions in white matter oligodendrocytes of multiple system atrophy brains contain insoluble alpha-synuclein. Ann Neurol , 44(3): 415-422
doi: 10.1002/ana.410440324 pmid:9749615
|
| 59 |
Ubhi K, Low P, Masliah E (2011). Multiple system atrophy: a clinical and neuropathological perspective. Trends Neurosci , 34(11): 581-590
doi: 10.1016/j.tins.2011.08.003 pmid:21962754
|
| 60 |
Ubhi K, Rockenstein E, Mante M, Inglis C, Adame A, Patrick C, Whitney K, Masliah E (2010). Neurodegeneration in a transgenic mouse model of multiple system atrophy is associated with altered expression of oligodendroglial-derived neurotrophic factors. J Neurosci , 30(18): 6236-6246
doi: 10.1523/JNEUROSCI.0567-10.2010 pmid:20445049
|
| 61 |
Valenza M, Cattaneo E (2011). Emerging roles for cholesterol in Huntington’s disease. Trends Neurosci , 34(9): 474-486
doi: 10.1016/j.tins.2011.06.005 pmid:21774998
|
| 62 |
Valenza M, Leoni V, Karasinska J M, Petricca L, Fan J, Carroll J, Pouladi M A, Fossale E, Nguyen H P, Riess O, MacDonald M, Wellington C, DiDonato S, Hayden M, Cattaneo E (2010). Cholesterol defect is marked across multiple rodent models of Huntington’s disease and is manifest in astrocytes. J Neurosci , 30(32): 10844-10850
doi: 10.1523/JNEUROSCI.0917-10.2010 pmid:20702713
|
| 63 |
Wakabayashi K, Yoshimoto M, Tsuji S, Takahashi H (1998). Alpha-synuclein immunoreactivity in glial cytoplasmic inclusions in multiple system atrophy. Neurosci Lett , 249(2-3): 180-182
doi: 10.1016/S0304-3940(98)00407-8 pmid:9682846
|
| 64 |
Wenning G K, Stefanova N, Jellinger K A, Poewe W, Schlossmacher M G (2008). Multiple system atrophy: a primary oligodendrogliopathy. Ann Neurol , 64(3): 239-246
doi: 10.1002/ana.21465 pmid:18825660
|
| 65 |
Yazawa I, Giasson B I, Sasaki R, Zhang B, Joyce S, Uryu K, Trojanowski J Q, Lee V M (2005). Mouse model of multiple system atrophy alpha-synuclein expression in oligodendrocytes causes glial and neuronal degeneration. Neuron , 45(6): 847-859
doi: 10.1016/j.neuron.2005.01.032 pmid:15797547
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
