Oligodendrocyte regeneration: Its significance in myelin replacement and neuroprotection in multiple sclerosis

Neuropharmacology

Volumn 110, Issue , 2016, Pages 633-643

  Chamberlain, Kelly A ^a   Nanescu, Sonia E ^a   Psachoulia, Konstantina ^a   Huang, Jeffrey K ^a  

^a GEORGETOWN UNIVERSITY   (United States)

Author keywords

Inflammation; Multiple sclerosis; Myelin; Oligodendrocyte precursor cells; Oligodendrocytes; Regeneration; Remyelination

Indexed keywords

BENZATROPINE; CYTOKINE; FRIZZLED PROTEIN; LIGAND; NITROGEN DERIVATIVE; REACTIVE OXYGEN METABOLITE; SEMAPHORIN; SEMAPHORIN 3A; SEMAPHORIN 3F; THYMIDINE PHOSPHORYLASE; VASCULOTROPIN A; WNT PROTEIN;

ADULT; ALZHEIMER DISEASE; APOPTOSIS; ASTROCYTE; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL REGENERATION; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; CORPUS CALLOSUM; DISEASE COURSE; ENVIRONMENTAL FACTOR; HUMAN; HUMAN CELL; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MICROGLIA; MULTIPLE SCLEROSIS; MYELIN SHEATH; NERVE CONDUCTION; NERVOUS SYSTEM INFLAMMATION; NEURAL STEM CELL; NEUROPROTECTION; OLIGODENDROCYTE PROGENITOR; OLIGODENDROGLIA; PARKINSON DISEASE; PRIORITY JOURNAL; REGENERATIVE MEDICINE; REMYELINIZATION; REVIEW; SCHIZOPHRENIA; T LYMPHOCYTE; WOUND HEALING; ANIMAL; DISEASE MODEL; NERVE REGENERATION; PHYSIOLOGY;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; MULTIPLE SCLEROSIS; MYELIN SHEATH; NERVE REGENERATION; NEUROPROTECTION; OLIGODENDROGLIA;

EID: 84964681309     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.10.010     Document Type: Review

References (206)

1. Agoston, G., Wu, J., Izenwasser, S., George, C., Katz, J., Kline, R., Newman, A., Novel N-substituted 3r-[Bis(4′-fluorophenyl)methoxy]tropane analogues: selective ligands for the dopamine transporter. J. Med. Chem. 40 (1997), 4329–4339.
2. Argaw, A.T., Asp, L., Zhang, J., Navrazhina, K., Pham, T., Mariani, J.N., Mahase, S., Dutta, D.J., Seto, J., Kramer, E.G., Ferrara, N., Sofroniew, M.V., John, G.R., Astrocyte-derived VEGF-A drives blood-brain barrier disruption in CNS inflammatory disease. J. Clin. Invest. 122 (2012), 2454–2468, 10.1172/JCI60842.
3. Arnett, H., Mason, J., Marino, M., Suzuki, K., Matsushima, G.K., Ting, J.P., TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat. Neurosci. 4 (2001), 1116–1122, 10.1038/nn738.
4. Azim, K., Butt, A.M., GSK3β negatively regulates oligodendrocyte differentiation and myelination in vivo. Glia 59 (2011), 540–553, 10.1002/glia.21122.
5. Azim, K., Rivera, A., Raineteau, O., Butt, A.M., GSK3β regulates oligodendrogenesis in the dorsal microdomain of the subventricular zone via Wnt-β-catenin signaling. Glia 62 (2014), 778–789, 10.1002/glia.22641.
6. Back, S.A., Tuohy, T.M.F., Chen, H., Wallingford, N., Craig, A., Struve, J., Luo, N.L., Banine, F., Liu, Y., Chang, A., Trapp, B.D., Bebo, B.F., Rao, M.S., Sherman, L.S., Hyaluronan accumulates in demyelinated lesions and inhibits oligodendrocyte progenitor maturation. Nat. Med. 11 (2005), 966–972, 10.1038/nm1279.
7. Ballanger, F., Nguyen, J.M., Khammari, a., Dréno, B., Evolution of clinical and molecular responses to bexarotene treatment in cutaneous T-cell lymphoma. Dermatology 220 (2010), 370–375, 10.1159/000305354.
8. Bannerman, P., Hahn, A., Soulika, A., Gallo, V., Pleasure, D., Astrogliosis in EAE spinal cord: derivation from radial glia, and relationships to oligodendroglia. Glia 55 (2007), 57–64, 10.1002/glia.
9. Baxter, A.G., The origin and application of experimental autoimmune encephalomyelitis. Nat. Rev. Immunol. 7 (2007), 904–912, 10.1038/nri2190.
10. Behrens, J., Jerchow, B.A, Würtele, M., Grimm, J., Asbrand, C., Wirtz, R., Kühl, M., Wedlich, D., Birchmeier, W., Functional interaction of an axin homolog, conductin, with beta-catenin, APC, and GSK3beta. Science 280 (1998), 596–599, 10.1126/science.280.5363.596.
11. Bhatt, A., Fan, L., Pang, Y., Strategies for myelin regeneration: lessons learned from development. Neural Regen. Res. 9 (2014), 1347–1350.
12. Bieber, A.J., Kerr, S., Rodriguez, M., Efficient central nervous system remyelination requires T cells. Ann. Neurol. 53 (2003), 680–684, 10.1002/ana.10578.
13. Bitsch, A., Schuchardt, J., Bunkowski, S., Kuhlmann, T., Brück, W., Acute axonal injury in multiple sclerosis. Correlation with demyelination and inflammation. Brain 123:Pt 6 (2000), 1174–1183, 10.1093/brain/123.6.1174.
14. Bjartmar, C., Kidd, G., Mörk, S., Rudick, R., Trapp, B.D., Neurological disability correlates with spinal cord axonal loss and reduced N-acetyl aspartate in chronic multiple sclerosis patients. Ann. Neurol. 48 (2000), 893–901, 10.1002/1531-8249(200012)48 6<893::AID-ANA10>3.0.CO;2-B.
15. Bjartmar, C., Wujek, J.R., Trapp, B.D., Axonal loss in the pathology of MS: consequences for understanding the progressive phase of the disease. J. Neurol. Sci. 206 (2003), 165–171, 10.1016/S0022-510X(02)00069-2.
16. Blakemore, W., Franklin, R., Blakemore and Franklin_Curr Top Microbio_2008.pdf. Adv. Mult. Scler. Exp. Demyelinat. Dis. Curr. Top. Microbiol. Immunol. 318 (2008), 193–212.
17. Boyd, A., Zhang, H., Williams, A., Insufficient OPC migration into demyelinated lesions is a cause of poor remyelination in MS and mouse models. Acta Neuropathol. 125 (2013), 841–859, 10.1007/s00401-013-1112-y.
18. Brambilla, R., Morton, P.D., Ashbaugh, J.J., Karmally, S., Lambertsen, K.L., Bethea, J.R., Astrocytes play a key role in EAE pathophysiology by orchestrating in the CNS the inflammatory response of resident and peripheral immune cells and by suppressing remyelination. Glia 62 (2014), 452–467, 10.1002/glia.22616.
19. Brambilla, R., Persaud, T., Hu, X., Karmally, S., Shestopalov, V.I., Dvoriantchikova, G., Ivanov, D., Nathanson, L., Barnum, S.R., Bethea, J.R., Transgenic inhibition of astroglial NF-kappa B improves functional outcome in experimental autoimmune encephalomyelitis by suppressing chronic central nervous system inflammation. J. Immunol. 182 (2009), 2628–2640, 10.4049/jimmunol.0802954.
20. Brinkmann, B.G., Agarwal, A., Sereda, M.W., Garratt, A.N., Müller, T., Wende, H., Stassart, R.M., Nawaz, S., Humml, C., Velanac, V., Radyushkin, K., Goebbels, S., Fischer, T.M., Franklin, R.J., Lai, C., Ehrenreich, H., Birchmeier, C., Schwab, M.H., Nave, K.A., Neuregulin-1/ErbB signaling serves distinct functions in myelination of the peripheral and central nervous system. Neuron 59 (2008), 581–595, 10.1016/j.neuron.2008.06.028.
21. Brosnan, C.F., John, G.R., Revisiting notch in remyelination of multiple sclerosis lesions. J. Clin. Invest. 119 (2009), 10–13, 10.1172/JCI37786.progressive.
22. Byravan, S., Foster, L.M., Phan, T., Verity, A.N., Campagnoni, A.T., Murine oligodendroglial cells express nerve growth factor. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 8812–8816, 10.1073/pnas.91.19.8812.
23. Campbell, G.R., Ohno, N., Turnbull, D.M., Mahad, D.J., Mitochondrial changes within axons in multiple sclerosis: an update. Curr. Opin. Neurol. 25 (2012), 221–230, 10.1097/WCO.0b013e3283533a25.
24. Campbell, G.R., Worrall, J.T., Mahad, D.J., The central role of mitochondria in axonal degeneration in multiple sclerosis. Mult. Scler. J. 20 (2014), 1806–1813, 10.1177/1352458514544537.
25. Carrithers, M.D., Update on disease-modifying treatments for multiple sclerosis. Clin. Ther. 36 (2014), 1938–1945.
26. Chang, A., Tourtellotte, W.W., Rudick, R., Trapp, B.D., Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N. Engl. J. Med. 346 (2002), 165–173, 10.1056/NEJMoa010994.
27. Chapouly, C., Tadesse Argaw, a., Horng, S., Castro, K., Zhang, J., Asp, L., Loo, H., Laitman, B.M., Mariani, J.N., Straus Farber, R., Zaslavsky, E., Nudelman, G., Raine, C.S., John, G.R., Astrocytic TYMP and VEGFA drive blood-brain barrier opening in inflammatory central nervous system lesions. Brain, 2015, 1548–1567, 10.1093/brain/awv077.
28. Charil, A., Zijdenbos, A.P., Taylor, J., Boelman, C., Worsley, K.J., Evans, A.C., Dagher, A., Statistical mapping analysis of lesion location and neurological disability in multiple sclerosis: application to 452 patient data sets. Neuroimage 19 (2003), 532–544, 10.1016/S1053-8119(03)00117-4.
29. Charles, P., Hernandez, M.P., Stankoff, B., Aigrot, M.S., Colin, C., Rougon, G., Zalc, B., Lubetzki, C., Negative regulation of central nervous system myelination by polysialylated-neural cell adhesion molecule. Proc. Natl. Acad. Sci. U. S. A. 97 (2000), 7585–7590, 10.1073/pnas.100076197.
30. Charles, P., Reynolds, R., Seilhean, D., Rougon, G., Aigrot, M.S., Niezgoda, A., Zalc, B., Lubetzki, C., Re-expression of PSA-NCAM by demyelinated axons: an inhibitor of remyelination in multiple sclerosis?. Brain 125 (2002), 1972–1979, 10.1093/brain/awf216.
31. Ciccarelli, O., Barkhof, F., Bodini, B., Stefano, N. De, Golay, X., Nicolay, K., Pelletier, D., Pouwels, P.J.W., Smith, S.A, Wheeler-Kingshott, C.A.M., Stankoff, B., Yousry, T., Miller, D.H., Pathogenesis of multiple sclerosis: insights from molecular and metabolic imaging. Lancet Neurol. 13 (2014), 807–822, 10.1016/S1474-4422(14)70101-2.
32. Colton, C.A., Heterogeneity of microglial activation in the innate immune response in the brain. J. Neuroimmune Pharmacol. 4 (2009), 399–418.
33. Coman, I., Aigrot, M.S., Seilhean, D., Reynolds, R., Girault, J.A., Zalc, B., Lubetzki, C., Nodal, paranodal and juxtaparanodal axonal proteins during demyelination and remyelination in multiple sclerosis. Brain 129 (2006), 3186–3195, 10.1093/brain/awl144.
34. Compston, A., Coles, A., Multiple sclerosis. Lancet 372 (2008), 1502–1517, 10.1016/S0140-6736(08)61620-7.
35. Copelman, C.A., Diemel, L.T., Gveric, D., Gregson, N.A., Louise Cuzner, M., Myelin phagocytosis and remyelination of macrophage-enriched central nervous system aggregate cultures. J. Neurosci. Res. 66 (2001), 1173–1178, 10.1002/jnr.10026.
36. Craner, M., Hains, B.C., Lo, A.C., Black, J.A, Waxman, S.G., Co-localization of sodium channel Nav1.6 and the sodium-calcium exchanger at sites of axonal injury in the spinal cord in EAE. Brain 127 (2004), 294–303, 10.1093/brain/awh032.
37. D'Souza, B., Miyamoto, A., Weinmaster, G., The many facets of notch ligands. Oncogene 27 (2008), 5148–5167, 10.1038/onc.2008.229.
38. Dai, X., Lercher, L.D., Clinton, P.M., Du, Y., Livingston, D.L., Vieira, C., Yang, L., Shen, M.M., Dreyfus, C.F., The trophic role of oligodendrocytes in the basal forebrain. J. Neurosci. 23 (2003), 5846–5853.
39. Dai, Z., Sun, S., Wang, C., Huang, H., Hu, X., Zhang, Z., Lu, Q.R., Qiu, M., Stage-specific regulation of oligodendrocyte development by Wnt/β-catenin signaling. J. Neurosci. 34 (2014), 8467–8473, 10.1523/JNEUROSCI.0311-14.2014.
40. Dawson, M.R.L., Polito, A., Levine, J.M., Reynolds, R., NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol. Cell. Neurosci. 24 (2003), 476–488, 10.1016/S1044-7431(03)00210-0.
41. Denic, a, Johnson, A., Bieber, A., The relevance of animal models in multiple sclerosis research. Pathophysiology 18 (2011), 1–16, 10.1016/j.pathophys.2010.04.004.The.
42. Denney, L., Kok, W.L., Cole, S.L., Sanderson, S., McMichael, A.J., Ho, L.-P., Activation of invariant NKT cells in early phase of experimental autoimmune encephalomyelitis results in differentiation of Ly6Chi inflammatory monocyte to M2 macrophages and improved outcome. J. Immunol. 189 (2012), 551–557, 10.4049/jimmunol.1103608.
43. Deshmukh, V., Tardif, V., Lyssiotis, C., Green, C., Kerman, B., Kim, H.J., Padmanabhan, K., Swoboda, J.G., Ahmad, I., Kondo, T., Gage, F.H., Theofilopoulos, a N., Lawson, B.R., Schultz, P.G., Lairson, L.L., A regenerative approach to the treatment of multiple sclerosis. Nature 502 (2013), 327–332, 10.1038/nature12647.
44. Dougherty, K.D., Dreyfus, C.F., Black, I.B., Brain-derived neurotrophic factor in astrocytes, oligodendrocytes, and microglia/macrophages after spinal cord injury. Neurobiol. Dis. 7 (2000), 574–585, 10.1006/nbdi.2000.0318.
45. Dutta, R., Trapp, B.D., Mechanisms of neuronal dysfunction and degeneration in multiple sclerosis. Prog. Neurobiol. 93 (2011), 1–12, 10.1016/j.pneurobio.2010.09.005.
46. Dziedzic, T., Metz, I., Dallenga, T., König, F.B., Müller, S., Stadelmann, C., Brück, W., Wallerian degeneration: a major component of early axonal pathology in multiple sclerosis. Brain Pathol. 20 (2010), 976–985, 10.1111/j.1750-3639.2010.00401.x.
47. Edgar, J.M., McCulloch, M.C., Montague, P., Brown, A.M., Thilemann, S., Pratola, L., Gruenenfelder, F.I., Griffiths, I.R., Nave, K.-A., Demyelination and axonal preservation in a transgenic mouse model of Pelizaeus-Merzbacher disease. EMBO Mol. Med. 2 (2010), 42–50, 10.1002/emmm.200900057.
48. Edgar, J.M., McLaughlin, M., Werner, H.B., McCulloch, M.C., Barrie, J.A., Brown, A., Faichney, A.B., Snaidero, N., Nave, K.-A., Griffiths, I.R., Early ultrastructural defects of axons and axon-glia junctions in mice lacking expression of Cnp1. Glia 57 (2009), 1815–1824, 10.1002/glia.20893.
49. England, J.D., Gamboni, F., Levinson, S.R., Finger, T.E., Changed distribution of sodium channels along demyelinated axons. Proc. Natl. Acad. Sci. U. S. A. 87 (1990), 6777–6780, 10.1073/pnas.87.17.6777.
50. Eshleman, a J., Henningsen, R.A., Neve, K.A., Janowsky, A, Release of dopamine via the human transporter. Mol. Pharmacol. 45 (1994), 312–316.
51. Fancy, S.P.J., Baranzini, S.E., Zhao, C., Yuk, D.I., Irvine, K.A., Kaing, S., Sanai, N., Franklin, R.J.M., Rowitch, D.H., Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev. 23 (2009), 1571–1585, 10.1101/gad.1806309.
52. Fancy, S.P.J., Chan, J.R., Baranzini, S.E., Franklin, R.J.M., Rowitch, D.H., Myelin regeneration: a recapitulation of development?. Annu. Rev. Neurosci. 34 (2011), 21–43, 10.1146/annurev-neuro-061010-113629.
53. Fancy, S.P.J., Harrington, E.P., Baranzini, S.E., Silbereis, J.C., Shiow, L.R., Yuen, T.J., Huang, E.J., Lomvardas, S., Rowitch, D.H., Parallel states of pathological Wnt signaling in neonatal brain injury and colon cancer. Nat. Neurosci. 17 (2014), 506–512, 10.1038/nn.3676.
54. Fancy, S.P.J., Harrington, E.P., Yuen, T.J., Silbereis, J.C., Zhao, C., Baranzini, S.E., Bruce, C.C., Otero, J.J., Huang, E.J., Nusse, R., Franklin, R.J.M., Rowitch, D.H., Axin2 as regulatory and therapeutic target in newborn brain injury and remyelination. Nat. Neurosci. 14 (2011), 1009–1016, 10.1038/nn.2855.
55. Fancy, S.P.J., Kotter, M.R., Harrington, E.P., Huang, J.K., Zhao, C., Rowitch, D.H., Franklin, R.J.M., Overcoming remyelination failure in multiple sclerosis and other myelin disorders. Exp. Neurol. 225 (2010), 18–23, 10.1016/j.expneurol.2009.12.020.
56. Ferguson, B., Matyszak, M.K., Esiri, M.M., Perry, V.H., Axonal damage in acute multiple sclerosis lesions. Brain 120:3 (1997), 393–399, 10.1093/brain/120.3.393.
57. Fischer, M.T., Sharma, R., Lim, J.L., Haider, L., Frischer, J.M., Drexhage, J., Mahad, D., Bradl, M., van Horssen, J., Lassmann, H., NADPH oxidase expression in active multiple sclerosis lesions in relation to oxidative tissue damage and mitochondrial injury. Brain 135 (2012), 886–899, 10.1093/brain/aws012.
58. Fisher, E., Rudick, R.A., Simon, J.H., Cutter, G., Baier, M., Lee, J.-C., Miller, D., Weinstock-Guttman, B., Mass, M.K., Dougherty, D.S., Simonian, N. a, Eight-year follow-up study of brain atrophy in patients with MS. Neurology 59 (2002), 1412–1420, 10.1212/01.WNL.0000036271.49066.06.
59. Frankenhaeuser, B., Saltatory conduction in myelinated nerve fibres. J. Physiol. 118 (1952), 107–112.
60. Franklin, R.J.M., Why does remyelination fail in multiple sclerosis?. Nat. Rev. Neurosci. 3 (2002), 705–714, 10.1038/nrn917.
61. Franklin, R.J.M., ffrench-Constant, C., Remyelination in the CNS: from biology to therapy. Nat. Rev. Neurosci. 9 (2008), 839–855, 10.1038/nrn2480.
62. Fu, H., Cai, J., Clevers, H., Fast, E., Gray, S., Greenberg, R., Jain, M.K., Ma, Q., Qiu, M., Rowitch, D.H., Taylor, C.M., Stiles, C.D., A genome-wide screen for spatially restricted expression patterns identifies transcription factors that regulate glial development. J. Neurosci. 29 (2009), 11399–11408, 10.1523/JNEUROSCI.0160-09.2009.
63. Fünfschilling, U., Supplie, L.M., Mahad, D., Boretius, S., Saab, A.S., Edgar, J., Brinkmann, B.G., Kassmann, C.M., Tzvetanova, I.D., Möbius, W., Diaz, F., Meijer, D., Suter, U., Hamprecht, B., Sereda, M.W., Moraes, C.T., Frahm, J., Goebbels, S., Nave, K.-A., Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485 (2012), 517–521, 10.1038/nature11007.
64. Gadea, A., Aguirre, A., Haydar, T.F., Gallo, V., Endothelin-1 regulates oligodendrocyte development. J. Neurosci. 29 (2009), 10047–10062, 10.1523/jneurosci.0822-09.2009.
65. Gadea, A., Schinelli, S., Gallo, V., Endothelin-1 regulates astrocyte proliferation and reactive gliosis via a JNK/c-Jun signaling pathway. J. Neurosci. 28 (2008), 2394–2408, 10.1523/jneurosci.5652-07.2008.
66. Genoud, S., Lappe-Siefke, C., Goebbels, S., Radtke, F., Aguet, M., Scherer, S.S., Suter, U., Nave, K.A., Mantei, N., Notch1 control of oligodendrocyte differentiation in the spinal cord. J. Cell Biol. 158 (2002), 709–718, 10.1083/jcb.200202002.
67. Giraudon, P., Vincent, P., Vuaillat, C., Verlaeten, O., Cartier, L., Marie-Cardine, A., Mutin, M., Bensussan, A., Belin, M.-F., Boumsell, L., Semaphorin CD100 from activated T lymphocytes induces process extension collapse in oligodendrocytes and death of immature neural cells. J. Immunol. 172 (2004), 1246–1255.
68. Givogri, M.I., Costa, R.M., Schonmann, V., Silva, A.J., Campagnoni, A.T., Bongarzone, E.R., Central nervous system myelination in mice with deficient expression of Notch1 receptor. J. Neurosci. Res. 67 (2002), 309–320, 10.1002/jnr.10128.
69. Goldschmidt, T., Antel, J., König, F.B., Brück, W., Kuhlmann, T., Remyelination capacity of the MS brain decreases with disease chronicity. Neurology 72 (2009), 1914–1921, 10.1212/WNL.0b013e3181a8260a.
70. Gonzalez, D., Dees, W., Hiney, J., Ojeda, S., Saneto, R., Expression of beta-nerve growth factor in cultured cells derived from the hypothalamus and cerebral cortex. Brain Res. 511 (1990), 249–258.
71. Gray, E., Rice, C., Nightingale, H., Ginty, M., Hares, K., Kemp, K., Cohen, N., Love, S., Scolding, N., Wilkins, A., Accumulation of cortical hyperphosphorylated neurofilaments as a marker of neurodegeneration in multiple sclerosis. Mult. Scler. J. 19 (2012), 153–161, 10.1177/1352458512451661.
72. Griffiths, I., Klugmann, M., Anderson, T., Yool, D., Thomson, C., Schwab, M., Schneider, A., Zimmerman, F., McCulloch, M., Nadon, N., Nave, K.-A., Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280:80 (1998), 1610–1613, 10.1126/science.280.5369.1610.
73. Guo, F., Lang, J., Sohn, J., Hammond, E., Chang, M., Pleasure, D., Canonical Wnt signaling in the oligodendroglial lineage-puzzles remain. Glia 63 (2015), 1671–1693, 10.1002/glia.22813.
74. Haines, J., Inglese, M., Casaccia, P., Axonal damage in multiple sclerosis. Mt. Sinai J. Med. 78 (2011), 231–243, 10.1002/MSJ.
75. Haines, J.D., Inglese, M., Casaccia, P., Axonal damage in multiple sclerosis. Mt. Sinai J. Med. 76 (2009), 173–181, 10.1002/MSJ.
76. Hammond, T.R., Gadea, A., Dupree, J., Kerninon, C., Nait-oumesmar, B., Aguirre, A., Astrocyte-derived endothelin-1 inhibits remyelination through notch activation. Neuron 81 (2014), 588–602.
77. Hartline, D.K., Colman, D.R., Rapid conduction and the evolution of giant axons and myelinated fibers. Curr. Biol. 17 (2007), 29–35, 10.1016/j.cub.2006.11.042.
78. Hinks, G.L., Franklin, R.J., Distinctive patterns of PDGF-A, FGF-2, IGF-I, and TGF-beta1 gene expression during remyelination of experimentally-induced spinal cord demyelination. Mol. Cell. Neurosci. 14 (1999), 153–168, 10.1006/mcne.1999.0771.
79. Horner, P.M.T., et al. Defining the NG2-expressing cell of the adult CNS. J. Neurocytol. 31 (2002), 469–480.
80. Huang, J.K., Franklin, R.J.M., Regenerative medicine in multiple sclerosis: identifying pharmacological targets of adult neural stem cell differentiation. Neurochem. Int. 59 (2011), 329–332, 10.1016/j.neuint.2011.01.017.
81. Huang, J.K., Jarjour, A. a, Nait Oumesmar, B., Kerninon, C., Williams, A., Krezel, W., Kagechika, H., Bauer, J., Zhao, C., Baron-Van Evercooren, A., Chambon, P., Ffrench-Constant, C., Franklin, R.J.M., Retinoid X receptor gamma signaling accelerates CNS remyelination. Nat. Neurosci. 14 (2011), 45–53, 10.1038/nn.2702.
82. Irvine, K.A., Blakemore, W.F., Remyelination protects axons from demyelination-associated axon degeneration. Brain 131 (2008), 1464–1477, 10.1093/brain/awn080.
83. Jeffery, N.D., Blakemore, W.F., Locomotor deficits induced by experimental spinal cord demyelination are abolished by spontaneous remyelination. Brain 120 (1997), 27–37, 10.1093/brain/120.1.27.
84. L – catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol. 22 (2002), 1172–1183, 10.1128/MCB.22.4.1172.
85. Ji, B., Li, M., Wu, W.T., Yick, L.W., Lee, X., Shao, Z., Wang, J., So, K.F., McCoy, J.M., Blake Pepinsky, R., Mi, S., Relton, J.K., LINGO-1 antagonist promotes functional recovery and axonal sprouting after spinal cord injury. Mol. Cell. Neurosci. 33 (2006), 311–320, 10.1016/j.mcn.2006.08.003.
86. John, G., Shankar, S., Shafit-Zagardo, B., Massimi, A., Lee, S., Raine, C., Brosnan, C., Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nat. Med. 8 (2002), 1115–1121, 10.1038/nm.
87. Jongbloets, B.C., Pasterkamp, R.J., Semaphorin signalling during development. Development 141 (2014), 3292–3297, 10.1242/dev.105544.
88. Joshi, D.C., Zhang, C.-L., Lin, T.-M., Gusain, a., Harris, M.G., Tree, E., Yin, Y., Wu, C., Sheng, Z.-H., Dempsey, R.J., Fabry, Z., Chiu, S.Y., Deletion of mitochondrial anchoring protects dysmyelinating shiverer: implications for progressive MS. J. Neurosci. 35 (2015), 5293–5306, 10.1523/JNEUROSCI.3859-14.2015.
89. Katsumoto, a., Lu, H., Miranda, a. S., Ransohoff, R.M., Ontogeny and functions of central nervous system macrophages. J. Immunol. 193 (2014), 2615–2621, 10.4049/jimmunol.1400716.
90. Katzenschlager, R., Sampaio, C., Costa, J., Lees, A., Anticholinergics for symptomatic management of Parkinson's disease. Cochrane Database Syst. Rev., 2, 2003, 10.1002/14651858.CD003735.
91. Kim, J.Y., Sun, Q., Oglesbee, M., Yoon, S.O., The role of ErbB2 signaling in the onset of terminal differentiation of oligodendrocytes in vivo. J. Neurosci. 23 (2003), 5561–5571 doi:23/13/5561.
92. Kiryu-Seo, S., Ohno, N., Kidd, G.J., Komuro, H., Trapp, B.D., Demyelination increases axonal stationary mitochondrial size and the speed of axonal mitochondrial transport. J. Neurosci. 30 (2010), 6658–6666, 10.1523/JNEUROSCI.5265-09.2010.
93. Klaver, R., Popescu, V., Voorn, P., Graaf, Y.G., Valk, P., Van Der Vries, H.E., De Schenk, G.J., Geurts, J.J.G., Neuronal and axonal loss in normal-appearing gray matter and subpial lesions in multiple sclerosis. J. Neuropathol. Exp. Neurol. 74 (2015), 453–458.
94. Kornek, B., Storch, M.K., Weissert, R., Wallstroem, E., Stefferl, a, Olsson, T., Linington, C., Schmidbauer, M., Lassmann, H., Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative quantitative study of axonal injury in active, inactive, and remyelinated lesions. Am. J. Pathol. 157 (2000), 267–276, 10.1016/S0002-9440(10)64537-3.
95. Kotter, M.R., Li, W.-W., Zhao, C., Franklin, R.J.M., Myelin impairs CNS remyelination by inhibiting oligodendrocyte precursor cell differentiation. J. Neurosci. 26 (2006), 328–332, 10.1523/JNEUROSCI.2615-05.2006.
96. Kotter, M.R., Zhao, C., Van Rooijen, N., Franklin, R.J.M., Macrophage-depletion induced impairment of experimental CNS remyelination is associated with a reduced oligodendrocyte progenitor cell response and altered growth factor expression. Neurobiol. Dis. 18 (2005), 166–175, 10.1016/j.nbd.2004.09.019.
97. Kuhlmann, T., Miron, V., Cuo, Q., Wegner, C., Antel, J., Brück, W., Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 131 (2008), 1749–1758, 10.1093/brain/awn096.
98. Lang, A., Lees, A., Management of Parkinson's disease: an evidence based review. Mov. Disord. 17 (2002), S1–S6, 10.1002/mds.5555.
99. Lang, J., Maeda, Y., Bannerman, P., Xu, J., Horiuchi, M., Pleasure, D., Guo, F., Adenomatous polyposis coli regulates oligodendroglial development. J. Neurosci. 33 (2013), 3113–3130, 10.1523/JNEUROSCI.3467-12.2013.
100. Langmead, C.J., Watson, J., Reavill, C., Muscarinic acetylcholine receptors as CNS drug targets. Pharmacol. Ther. 117 (2008), 232–243, 10.1016/j.pharmthera.2007.09.009.
101. Lappe-Siefke, C., Goebbels, S., Gravel, M., Nicksch, E., Lee, J., Braun, P.E., Griffiths, I.R., Nave, K.-A., Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat. Genet. 33 (2003), 366–374, 10.1038/ng1095.
102. Lassmann, H., Mechanisms of white matter damage in multiple sclerosis. Glia 62 (2014), 1816–1830, 10.1002/glia.22597.
103. Le, P.N., Mcdermott, J.D., Jimeno, A., Pharmacology & therapeutics targeting the Wnt pathway in human cancers: therapeutic targeting with a focus on OMP-54F28. Pharmacol. Ther. 146C (2014), 1–11.
104. Lee, H.K., Chaboub, L.S., Fancy, S.P.J., Deneen, B., Lee, H.K., Chaboub, L.S., Zhu, W., Zollinger, D., Rasband, M.N., Fancy, S.P.J., Daam2-PIP5K is a regulatory pathway for wnt signaling and therapeutic target for remyelination in the CNS. Neuron 85 (2015), 1227–1243.
105. Lee, X., Shao, Z., Sheng, G., Pepinsky, B., Mi, S., LINGO-1 regulates oligodendrocyte differentiation by inhibiting ErbB2 translocation and activation in lipid rafts. Mol. Cell. Neurosci. 60 (2014), 36–42, 10.1016/j.mcn.2014.02.006.
106. Lee, X., Yang, Z., Shao, Z., Rosenberg, S.S., Levesque, M., Pepinsky, R.B., Qiu, M., Miller, R.H., Chan, J.R., Mi, S., NGF regulates the expression of axonal LINGO-1 to inhibit oligodendrocyte differentiation and myelination. J. Neurosci. 27 (2007), 220–225, 10.1523/JNEUROSCI.4175-06.2007.
107. 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., Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487 (2012), 443–448, 10.1038/nature11314.
108. Lees, A., Alternatives to levodopa in the initial treatment of early Parkinson's disease. Drugs Aging 22 (2005), 731–740.
109. Li, H., He, Y., Richardson, W.D., Casaccia, P., Two-tier transcriptional control of oligodendrocyte differentiation. Curr. Opin. Neurobiol. 19 (2009), 479–485, 10.1016/j.conb.2009.08.004.
110. Lucchinetti, C., Brück, W., Parisi, J., Scheithauer, B., Rodriguez, M., Lassmann, H., A quantitative analysis of oligodendrocytes in multiple sclerosis lesions. A study of 113 cases. Brain 122 (1999), 2279–2295, 10.1093/brain/122.12.2279.
111. Mahad, D., Ziabreva, I., Lassmann, H., Turnbull, D., Mitochondrial defects in acute multiple sclerosis lesions. Brain 131 (2008), 1722–1735, 10.1093/brain/awn105.
112. Mahad, D.H., Trapp, B.D., Lassmann, H., Series Progressive Multiple Sclerosis 1 Pathological Mechanisms in Progressive Multiple Sclerosis C. 2015, 183–193.
113. Mahad, D.J., Ziabreva, I., Campbell, G., Lax, N., White, K., Hanson, P.S., Lassmann, H., Turnbull, D.M., Mitochondrial changes within axons in multiple sclerosis. Brain 132 (2009), 1161–1174, 10.1093/brain/awp046.
114. Makinodan, M., Rosen, K.M., Ito, S., Corfas, G., A critical period for social experience – dependent oligodendrocyte maturation and myelination period for social experience. Science 337:80 (2012), 1357–1360.
115. Mantovani, A., Biswas, S.K., Galdiero, M.R., Sica, A., Locati, M., Macrophage plasticity and polarization in tissue repair and remodelling. J. Pathol. 229 (2013), 176–185.
116. Mark, M., Ghyselinck, N.B., Chambon, P., Function of retinoic acid receptors during embryonic development. Nucl. Recept. Signal, 7, 2009, e002, 10.1621/nrs.07002.
117. Mason, J.L., Suzuki, K., Chaplin, D.D., Matsushima, G.K., Interleukin-1beta promotes repair of the CNS. J. Neurosci. 21 (2001), 7046–7052 doi:21/18/7046.
118. Mayo, L., Trauger, S. a, Blain, M., Nadeau, M., Patel, B., Alvarez, J.I., Mascanfroni, I.D., Yeste, A., Kivisäkk, P., Kallas, K., Ellezam, B., Bakshi, R., Prat, A., Antel, J.P., Weiner, H.L., Quintana, F.J., Regulation of astrocyte activation by glycolipids drives chronic CNS inflammation. Nat. Med., 20, 2014, 10.1038/nm.3681.
119. McKearney, J., Stimulant actions of histamine H1 antagonists on operant behavior in the squirrel monkey. Psychopharmacol. (Berl.) 77 (1982), 156–158.
120. Mei, F., Fancy, S.P.J., Shen, Y.-A. A., Niu, J., Zhao, C., Presley, B., Miao, E., Lee, S., Mayoral, S.R., Redmond, S. a, Etxeberria, A., Xiao, L., Franklin, R.J.M., Green, A., Hauser, S.L., Chan, J.R., Micropillar arrays as a high-throughput screening platform for therapeutics in multiple sclerosis. Nat. Med. 20 (2014), 954–960, 10.1038/nm.3618.
121. Mews, I., Bergmann, M., Bunkowski, S., Gullotta, F., Brück, W., Oligodendrocyte and axon pathology in clinically silent multiple sclerosis lesions. Mult. Scler. 4 (1998), 55–62, 10.1191/135245898678919582.
122. Mi, S., Hu, B., Hahm, K., Luo, Y., Kam Hui, E.S., Yuan, Q., Wong, W.M., Wang, L., Su, H., Chu, T.-H., Guo, J., Zhang, W., So, K.-F., Pepinsky, B., Shao, Z., Graff, C., Garber, E., Jung, V., Wu, E.X., Wu, W., LINGO-1 antagonist promotes spinal cord remyelination and axonal integrity in MOG-induced experimental autoimmune encephalomyelitis. Nat. Med. 13 (2007), 1228–1233, 10.1038/nm1664.
123. Mi, S., Miller, R.H., Lee, X., Scott, M.L., Shulag-Morskaya, S., Shao, Z., Chang, J., Thill, G., Levesque, M., Zhang, M., Hession, C., Sah, D., Trapp, B., He, Z., Jung, V., McCoy, J.M., Pepinsky, R.B., LINGO-1 negatively regulates myelination by oligodendrocytes. Nat. Neurosci. 8 (2005), 745–751, 10.1038/nn1460.
124. Mi, S., Miller, R.H., Tang, W., Lee, X., Hu, B., Wu, W., Zhang, Y., Shields, C.B., Zhang, Y., Miklasz, S., Shea, D., Mason, J., Franklin, R.J.M., Ji, B., Shao, Z., Chédotal, A., Bernard, F., Roulois, A., Xu, J., Jung, V., Pepinsky, B., Promotion of central nervous system remyelination by induced differentiation of oligodendrocyte precursor cells. Ann. Neurol. 65 (2009), 304–315, 10.1002/ana.21581.
125. Mikita, J., Dubourdieu-Cassagno, N., Deloire, M.S., Vekris, A., Biran, M., Raffard, G., Brochet, B., Canron, M.-H., Franconi, J.-M., Boiziau, C., Petry, K.G., Altered M1/M2 activation patterns of monocytes in severe relapsing experimental rat model of multiple sclerosis. Amelioration of clinical status by M2 activated monocyte administration. Mult. Scler. 17 (2011), 2–15, 10.1177/1352458510379243.
126. Milo, R., Kahana, E., Multiple sclerosis: geoepidemiology, genetics and the environment. Autoimmun. Rev., 9, 2010, 10.1016/j.autrev.2009.11.010.
127. Miron, V.E., Boyd, A., Zhao, J.-W., Yuen, T.J., Ruckh, J.M., Shadrach, J.L., van Wijngaarden, P., Wagers, A.J., Williams, A., Franklin, R.J.M., ffrench-Constant, C., M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat. Neurosci. 16 (2013), 1211–1218, 10.1038/nn.3469.
128. Mutsaers, S.E., Carroll, W.M., Focal accumulation of intra-axonal mitochondria in demyelination of the cat optic nerve. Acta Neuropathol. 96 (1998), 139–143.
129. Nave, K.-A., Myelination and the trophic support of long axons. Nat. Rev. Neurosci. 11 (2010), 275–283, 10.1038/nrn2797.
130. Nave, K.-A., Trapp, B.D., Axon-glial signaling and the glial support of axon function. Annu. Rev. Neurosci. 31 (2008), 535–561, 10.1146/annurev.neuro.30.051606.094309.
131. Nikić, I., Merkler, D., Sorbara, C., Brinkoetter, M., Kreutzfeldt, M., Bareyre, F.M., Brück, W., Bishop, D., Misgeld, T., Kerschensteiner, M., A reversible form of axon damage in experimental autoimmune encephalomyelitis and multiple sclerosis. Nat. Med. 17 (2011), 495–499, 10.1038/nm.2324.
132. Oluich, L.-J., Stratton, J.A.S., Xing, Y.L., Ng, S.W., Cate, H.S., Sah, P., Windels, F., Kilpatrick, T.J., Merson, T.D., Targeted ablation of oligodendrocytes induces axonal pathology independent of overt demyelination. J. Neurosci. 32 (2012), 8317–8330, 10.1523/JNEUROSCI.1053-12.2012.
133. Ortega, F., Gascón, S., Masserdotti, G., Deshpande, A., Simon, C., Fischer, J., Dimou, L., Chichung Lie, D., Schroeder, T., Berninger, B., Oligodendrogliogenic and neurogenic adult subependymal zone neural stem cells constitute distinct lineages and exhibit differential responsiveness to Wnt signalling. Nat. Cell Biol. 15 (2013), 602–613, 10.1038/ncb2736.
134. Ousman, S.S., David, S., Lysophosphatidylcholine induces rapid recruitment and activation of macrophages in the adult mouse spinal cord. Glia 30 (2000), 92–104.
135. Pachner, A.R., Experimental models of multiple sclerosis. Curr. Opin. Neurol. 24 (2011), 291–299, 10.1097/WCO.0b013e328346c226.
136. Park, S.K., Miller, R., Krane, I., Vartanian, T., The ErbB2 gene is required for the development of terminally differentiated spinal cord oligodendrocytes. J. Cell Biol. 154 (2001), 1245–1258, 10.1083/jcb.200104025.
137. Patrikios, P., Stadelmann, C., Kutzelnigg, A., Rauschka, H., Schmidbauer, M., Laursen, H., Sorensen, P.S., Brück, W., Lucchinetti, C., Lassmann, H., Remyelination is extensive in a subset of multiple sclerosis patients. Brain 129 (2006), 3165–3172, 10.1093/brain/awl217.
138. Pedraza, L., Huang, J.K., Colman, D.R., Organizing principles of the axoglial apparatus. Neuron 30 (2001), 335–344.
139. Petzold, A., Gveric, D., Groves, M., Schmierer, K., Grant, D., Chapman, M., Keir, G., Cuzner, L., Thompson, E.J., Phosphorylation and compactness of neurofilaments in multiple sclerosis: Indicators of axonal pathology. Exp. Neurol. 213 (2008), 326–335, 10.1016/j.expneurol.2008.06.008.
140. Piaton, G., Aigrot, M.S., Williams, A., Moyon, S., Tepavcevic, V., Moutkine, I., Gras, J., Matho, K.S., Schmitt, A., Soellner, H., Huber, A.B., Ravassard, P., Lubetzki, C., Class 3 semaphorins influence oligodendrocyte precursor recruitment and remyelination in adult central nervous system. Brain 134 (2011), 1156–1167, 10.1093/brain/awr022.
141. Podbielska, M., Banik, N.L., Kurowska, E., Hogan, E.L., Myelin recovery in multiple sclerosis: the challenge of remyelination. Brain Sci. 3 (2013), 1282–1324, 10.3390/brainsci3031282.
142. Pringle, N.P., Mudhar, H.S., Collarini, E.J., Richardson, W.D., PDGF receptors in the rat CNS: during late neurogenesis, PDGF alpha-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage. Development 115 (1992), 535–551.
143. Qi, X., Lewin, A.S., Sun, L., Hauswirth, W.W., Guy, J., Mitochondrial protein nitration primes neurodegeneration in experimental autoimmune encephalomyelitis. J. Biol. Chem. 281 (2006), 31950–31962, 10.1074/jbc.M603717200.
144. Ransohoff, R.M., Animal models of multiple sclerosis: the good, the bad and the bottom line. Nat. Neurosci. 15 (2012), 1074–1077, 10.1038/nn.3168.
145. + channels get anchored...with a little help. J. Cell Biol. 183 (2008), 975–977, 10.1083/jcb.200811086.
146. Rasband, M.N., Clustered K+ channel complexes in axons. Neurosci. Lett. 486 (2010), 101–106, 10.1016/j.neulet.2010.08.081.
147. Rastinejad, F., Retinoid X receptor and its partners in the nuclear receptor family. Curr. Opin. Struct. Biol. 11 (2001), 33–38, 10.1016/S0959-440X(00)00165-2.
148. Rice, C.M., Disease modification in multiple sclerosis: an update. Pract. Neurol. 14 (2014), 6–13, 10.1136/practneurol-2013-000601.
149. Robinson, S., Miller, R., Contact with central nervous system myelin inhibits oligodendrocyte progenitor maturation. Dev. Biol. 216 (1999), 359–368.
150. Rodriguez, J.P., Coulter, M., Miotke, J., Meyer, R.L., Takemaru, K.-I., Levine, J.M., Abrogation of b-catenin signaling in oligodendrocyte precursor cells reduces glial Scarring and promotes axon regeneration after CNS injury. J. Neurosci. 34 (2014), 10285–10297, 10.1523/JNEUROSCI.4915-13.2014.
151. Rodriguez, M., Effectors of demyelination and remyelination in the CNS: Implications for multiple sclerosis. Brain Pathol. 17 (2007), 219–229, 10.1111/j.1750-3639.2007.00065.x.
152. Ruckh, J., Zhao, J., Shadrach, J., van Wijngaarden, P., Rao, T., Wagers, A., Franklin, R., Rejuvenation of regeneration in the aging central nervous system. Cell Stem Cell 10 (2012), 96–103, 10.1016/j.biotechadv.2011.08.021.Secreted.
153. Rudick, R.A., Fisher, E., Lee, J.C., Simon, J., Jacobs, L., Use of the brain parenchymal fraction to measure whole brain atrophy in relapsing-remitting MS. Multiple Sclerosis Collaborative Research Group. Neurology 53 (1999), 1698–1704, 10.1212/WNL.53.8.1698.
154. Rudick, R.A., Mi, S., Sandrock, A.W., LINGO-1 antagonists as therapy for multiple sclerosis: in vitro and in vivo evidence. Expert Opin. Biol. Ther. 8 (2008), 1561–1570, 10.1517/14712598.8.10.1561.
155. Saab, A.S., Tzvetanova, I.D., Nave, K.A., The role of myelin and oligodendrocytes in axonal energy metabolism. Curr. Opin. Neurobiol. 23 (2013), 1065–1072, 10.1016/j.conb.2013.09.008.
156. Sailer, M., Fischl, B., Salat, D., Tempelmann, C., Schönfeld, M.A., Busa, E., Bodammer, N., Heinze, H.J., Dale, A., Focal thinning of the cerebral cortex in multiple sclerosis. Brain 126 (2003), 1734–1744, 10.1093/brain/awg175.
157. Saxena, S., Caroni, P., Mechanisms of axon degeneration: from development to disease. Prog. Neurobiol. 83 (2007), 174–191, 10.1016/j.pneurobio.2007.07.007.
158. Scherer, S.S., Arroyo, E.J., Recent progress on the molecular organization of myelinated axons. J. Peripher. Nerv. Syst. 7 (2002), 1–12.
159. Schirmer, L., Antel, J.P., Brück, W., Stadelmann, C., Axonal loss and neurofilament phosphorylation changes accompany lesion development and clinical progression in multiple sclerosis. Brain Pathol. 21 (2011), 428–440, 10.1111/j.1750-3639.2010.00466.x.
160. Seifert, T., Bauer, J., Weissert, R., Fazekas, F., Storch, M.K., Notch1 and its ligand Jagged1 are present in remyelination in a T-cell- and antibody-mediated model of inflammatory demyelination. Acta Neuropathol. 113 (2007), 195–203, 10.1007/s00401-006-0170-9.
161. Shechter, R., Schwartz, M., Harnessing monocyte-derived macrophages to control central nervous system pathologies: no longer if’ but how. J. Pathol. 229 (2013), 332–346, 10.1002/path.4106.
162. Shimizu, T., Kagawa, T., Wada, T., Muroyama, Y., Takada, S., Ikenaka, K., Wnt signaling controls the timing of oligodendrocyte development in the spinal cord. Dev. Biol. 282 (2005), 397–410, 10.1016/j.ydbio.2005.03.020.
163. Sim, F.J., Zhao, C., Penderis, J., Franklin, R.J.M., The age-related decrease in CNS remyelination efficiency is attributable to an impairment of both oligodendrocyte progenitor recruitment and differentiation. J. Neurosci. 22 (2002), 2451–2459, 10.1097/00041327-200306000-00025.
164. Smith, E.S., Jonason, A., Reilly, C., Veeraraghavan, J., Fisher, T., Doherty, M., Klimatcheva, E., Mallow, C., Cornelius, C., Leonard, J.E., Marchi, N., Janigro, D., Tadesse, A., Pham, T., Seils, J., Bussler, H., Torno, S., Kirk, R., Howell, A., Evans, E.E., Paris, M., Bowers, W.J., John, G., Zauderer, M., SEMA4D compromises blood-brain barrier, activates microglia, and inhibits remyelination in neurodegenerative disease. Neurobiol. Dis. 73 (2015), 254–268.
165. Smith, K., Blakemore, W., McDonald, W., Central remyelination restores secure conduction. Nature 280 (1979), 395–396.
166. Sofroniew, M.V., Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 32 (2009), 638–647, 10.1016/j.tins.2009.08.002.
167. Sosa, R.A., Murphey, C., Ji, N., Cardona, A.E., Forsthuber, T.G., The kinetics of myelin antigen uptake by myeloid cells in the central nervous system during experimental autoimmune encephalomyelitis. J. Immunol. 191 (2013), 5848–5857, 10.4049/jimmunol.1300771.
168. Spassky, N., de Castro, F., Le Bras, B., Heydon, K., Quéraud-LeSaux, F., Bloch-Gallego, E., Chédotal, A., Zalc, B., Thomas, J.-L., Directional guidance of oligodendroglial migration by class 3 semaphorins and netrin-1. J. Neurosci. 22 (2002), 5992–6004 doi:20026573.
169. Sriram, S., Steiner, I., Experimental allergic encephalomyelitis: a misleading model of multiple sclerosis. Ann. Neurol. 58 (2005), 939–945, 10.1002/ana.20743.
170. Stidworthy, M.F., Genoud, S., Li, W.W., Leone, D.P., Mantei, N., Suter, U., Franklin, R.J.M., Notch1 and jagged1 are expressed after CNS demyelination, but are not a major rate-determining factor during remyelination. Brain 127 (2004), 1928–1941, 10.1093/brain/awh217.
171. Stolt, C.C., Rehberg, S., Ader, M., Lommes, P., Riethmacher, D., Schachner, M., Bartsch, U., Wegner, M., Terminal Differentiation of Myelin-forming Oligodendrocytes Depends on the Transcription Factor Sox10 Service Terminal Differentiation of Myelin-forming Oligodendrocytes Depends on the Transcription Factor Sox10. 2002, 165–170, 10.1101/gad.215802.
172. Sugimoto, Y., Taniguchi, M., Yagi, T., Akagi, Y., Nojyo, Y., Tamamaki, N., Guidance of glial precursor cell migration by secreted cues in the developing optic nerve. Development 128 (2001), 3321–3330.
173. Sussman, C.R., Vartanian, T., Miller, R.H., The ErbB4 neuregulin receptor mediates suppression of oligodendrocyte maturation. J. Neurosci. 25 (2005), 5757–5762, 10.1523/JNEUROSCI.4748-04.2005.
174. Syed, Y.A., Hand, E., Möbius, W., Zhao, C., Hofer, M., Nave, K.A., Kotter, M.R., Inhibition of CNS remyelination by the presence of semaphorin 3A. J. Neurosci. 31 (2011), 3719–3728, 10.1523/JNEUROSCI.4930-10.2011.
175. Tanaka, T., Yoshida, S., Mechanisms of remyelination: recent insight from experimental models. Biomol. Concepts 5 (2014), 289–298, 10.1515/bmc-2014-0015.
176. Tawk, M., Makoukji, J., Belle, M., Fonte, C., Trousson, A., Hawkins, T., Li, H., Ghandour, S., Schumacher, M., Massaad, C., Wnt/beta-catenin signaling is an essential and direct driver of myelin gene expression and myelinogenesis. J. Neurosci. 31 (2011), 3729–3742, 10.1523/JNEUROSCI.4270-10.2011.
177. Traka, M., Arasi, K., Avila, R.L., Podojil, J.R., Christakos, A., Miller, S.D., Soliven, B., Popko, B., A genetic mouse model of adult-onset, pervasive central nervous system demyelination with robust remyelination. Brain 133 (2010), 3017–3029, 10.1093/brain/awq247.
178. Trapp, B.D., Nave, K.-A., Multiple sclerosis: an immune or neurodegenerative disorder?. Annu. Rev. Neurosci. 31 (2008), 247–269, 10.1146/annurev.neuro.30.051606.094313.
179. Trapp, B.D., Peterson, J., Ransohoff, R.M., Rudick, R., Mörk, S., Bö, L., Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med. 338 (1998), 278–285, 10.1056/NEJM199801293380502.
180. Trapp, B.D., Stys, P.K., Virtual hypoxia and chronic necrosis of demyelinated axons in multiple sclerosis. Lancet Neurol. 8 (2009), 280–291, 10.1016/S1474-4422(09)70043-2.
181. Tran, J.Q., Rana, J., Barkhof, F., Melamed, I., Gevorkyan, H., Wattjes, M.P., de Jong, R., Brosofsky, K., Ray, S., Xu, L., Zhao, J., Parr, E., Cadavid, D., Randomized phase I trials of the safety/tolerability of anti-LINGO-1 monoclonal antibody BIIB033. Neurol. Neuroimmunol. Neuroinflamm., 1, 2014, e18.
182. Van Wijngaarden, P., Franklin, R.J.M., Ageing stem and progenitor cells: implications for rejuvenation of the central nervous system. Development 140 (2013), 2562–2575, 10.1242/dev.092262.
183. Vela, J.M., Molina-Holgado, E., Arévalo-Martín, A., Almazán, G., Guaza, C., Interleukin-1 regulates proliferation and differentiation of oligodendrocyte progenitor cells. Mol. Cell. Neurosci. 20 (2002), 489–502, 10.1006/mcne.2002.1127.
184. 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 21 (1998), 63–75, 10.1016/S0896-6273(00)80515-2.
185. Waxman, S.G., Axonal conduction and injury in multiple sclerosis: the role of sodium channels. Nat. Rev. Neurosci. 7 (2006), 932–941, 10.1038/nrn2023.
186. Wegner, C., Esiri, M.M., Chance, S.A, Palace, J., Matthews, P., Neocortical neuronal, synaptic, and glial loss in multiple sclerosis. Neurology 67 (2006), 960–967, 10.1212/01.wnl.0000237551.26858.39.
187. Wilkins, A., Chandran, S., Compston, A., Words, K.E.Y., A Role for Oligodendrocyte-derived IGF-1 in Trophic Support, vol. 57, 2001, 48–57, 10.1002/glia.1094.
188. Wilkins, A., Compston, A., Trophic factors attenuate nitric oxide mediated neuronal and axonal injury in vitro: roles and interactions of mitogen-activated protein kinase signalling pathways. J. Neurochem. 92 (2005), 1487–1496, 10.1111/j.1471-4159.2004.02981.x.
189. Williams, A., Piaton, G., Aigrot, M.S., Belhadi, A., Théaudin, M., Petermann, F., Thomas, J.L., Zalc, B., Lubetzki, C., Semaphorin 3A and 3F: key players in myelin repair in multiple sclerosis?. Brain 130 (2007), 2554–2565, 10.1093/brain/awm202.
190. Williamson, T.L., Cleveland, D.W., Slowing of axonal transport is a very early event in the toxicity of ALS-linked SOD1 mutants to motor neurons. Nat. Neurosci. 2 (1999), 50–56, 10.1038/4553.
191. Witte, M.E., Bø, L., Rodenburg, R.J., Belien, J.A., Musters, R., Hazes, T., Wintjes, L.T., Smeitink, J.A., Geurts, J.J.G., Vries, H.E. De, Valk, P. Van Der, Enhanced Number and Activity of Mitochondria in Multiple Sclerosis Lesions. 2009, 10.1002/path.
192. Witte, M.E., Geurts, J.J.G., de Vries, H.E., van der Valk, P., van Horssen, J., Mitochondrial dysfunction: a potential link between neuroinflammation and neurodegeneration?. Mitochondrion 10 (2010), 411–418, 10.1016/j.mito.2010.05.014.
193. Witte, M.E., Mahad, D.J., Lassmann, H., van Horssen, J., Mitochondrial dysfunction contributes to neurodegeneration in multiple sclerosis. Trends Mol. Med. 20 (2014), 179–187, 10.1016/j.molmed.2013.11.007.
194. Wolswijk, G., Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. J. Neurosci. 18 (1998), 601–609.
195. Wolswijk, G., Balesar, R., Changes in the expression and localization of the paranodal protein Caspr on axons in chronic multiple sclerosis. Brain 126 (2003), 1638–1649, 10.1093/brain/awg151.
196. Wood, E.T., Ronen, I., Techawiboonwong, a., Jones, C.K., Barker, P.B., Calabresi, P., Harrison, D., Reich, D.S., Investigating axonal damage in multiple sclerosis by diffusion tensor spectroscopy. J. Neurosci. 32 (2012), 6665–6669, 10.1523/jneurosci.0044-12.2012.
197. Wu, E., Raine, C.S., Multiple sclerosis interactions between oligodendrocytes and hypertrophic astrocytes and their occurence in other, nondemyelinating conditions. Lab. Investig., 67, 1992, 88.
198. Wujek, J.R., Bjartmar, C., Richer, E., Ransohoff, R.M., Yu, M., Tuohy, V.K., Trapp, B.D., Axon loss in the spinal cord determines permanent neurological disability in an animal model of multiple sclerosis. J. Neuropathol. Exp. Neurol. 61 (2002), 23–32.
199. Xie, C., Li, Z., Zhang, G.X., Guan, Y., Wnt signaling in remyelination in multiple sclerosis: friend or foe?. Mol. Neurobiol. 49 (2014), 1117–1125, 10.1007/s12035-013-8584-6.
200. Ye, F., Chen, Y., Hoang, T., Montgomery, R.L., Zhao, X., 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. 12 (2009), 829–838, 10.1038/nn.2333.
201. Yin, W., Hu, B., Knockdown of Lingo1b protein promotes myelination and oligodendrocyte differentiation in zebrafish. Exp. Neurol. 251 (2014), 72–83, 10.1016/j.expneurol.2013.11.012.
202. Yuen, T.J., Johnson, K.R., Miron, V.E., Zhao, C., Quandt, J., Harrisingh, M.C., Swire, M., Williams, A., McFarland, H.F., Franklin, R.J.M., Ffrench-Constant, C., Identification of endothelin 2 as an inflammatory factor that promotes central nervous system remyelination. Brain 136 (2013), 1035–1047, 10.1093/brain/awt024.
203. Zambonin, J.L., Zhao, C., Ohno, N., Campbell, G.R., Engeham, S., Ziabreva, I., Schwarz, N., Lee, S.E., Frischer, J.M., Turnbull, D.M., Trapp, B.D., Lassmann, H., Franklin, R.J.M., Mahad, D.J., Increased mitochondrial content in remyelinated axons: implications for multiple sclerosis. Brain 134 (2011), 1901–1913, 10.1093/brain/awr110.
204. Zhang, Y., Argaw, A.T., Gurfein, B.T., Zameer, A., Snyder, B.J., Ge, C., Lu, Q.R., Rowitch, D.H., Raine, C.S., Brosnan, C.F., John, G.R., Notch1 signaling plays a role in regulating precursor differentiation during CNS remyelination. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 19162–19167, 10.1073/pnas.0902834106.
205. Zhang, Y., Chen, K., Sloan, S.A., Bennett, M.L., Scholze, A.R., Keeffe, S.O., Phatnani, H.P., Guarnieri, P., Caneda, C., Ruderisch, N., Deng, S., Liddelow, S.A., Zhang, C., Daneman, R., Maniatis, T., Barres, B.A., Wu, J.Q., An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J. Neurosci. 34 (2014), 1–19, 10.1523/jneurosci.1860-14.2014.
206. Zhang, Y., Ping, Y., Pepinsky, B., Huang, G., Shields, L.B.E., Shields, C.B., Mi, S., Inhibition of LINGO-1 promotes functional recovery after experimental spinal cord demyelination. Exp. Neurol. 266 (2015), 68–73.