Mechanisms of remyelination: Recent insight from experimental models

Biomolecular Concepts

Volumn 5, Issue 4, 2014, Pages 289-298

  Tanaka, Tatsuhide ^a   Yoshida, Shigetaka ^a  

^a ASAHIKAWA MEDICAL COLLEGE   (Japan)

Author keywords

Cuprizone; demyelination; lysolecithin; oligodendrocyte; remyelination

Indexed keywords

ANIMALIA; VERTEBRATA;

ANIMAL; BIOLOGICAL MODEL; CELL DIFFERENTIATION; CYTOLOGY; DEMYELINATING DISEASE; GLIA; HUMAN; METABOLISM; MULTIPLE SCLEROSIS; MYELIN SHEATH; NERVE REGENERATION; OLIGODENDROGLIA; PATHOPHYSIOLOGY; PHYSIOLOGY; THEORETICAL MODEL;

ANIMALS; CELL DIFFERENTIATION; DEMYELINATING DISEASES; HUMANS; MODELS, BIOLOGICAL; MODELS, THEORETICAL; MULTIPLE SCLEROSIS; MYELIN SHEATH; NERVE REGENERATION; NEUROGLIA; OLIGODENDROGLIA;

EID: 84928794684     PISSN: 18685021     EISSN: 1868503X     Source Type: Journal    
DOI: 10.1515/bmc-2014-0015     Document Type: Review

References (119)

1. Taveggia C, Feltri ML, Wrabetz L. Signals to promote myelin formation and repair. Nat Rev Neurol 2010; 6: 276-87.
2. Wipfler P, Harrer A, Pilz G, Oppermann K, Trinka E, Kraus J. Recent developments in approved and oral multiple sclerosis treatment and an update on future treatment options. Drug Discov Today 2011; 16: 8-21.
3. Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG. Multiple sclerosis. N Engl J Med 2000; 343: 938-52.
4. Dutta R, Trapp BD. Mechanisms of neuronal dysfunction and degeneration in multiple sclerosis. Prog Neurobiol 2011; 93: 1-12.
5. Franklin RJ. Why does remyelination fail in multiple sclerosis? Nat Rev Neurosci 2002; 3: 705-14.
6. Kuhlmann T, Miron V, Cui Q, Wegner C, Antel J, Brück W. Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 2008; 131: 1749-58.
7. Dubois-Dalcq M, Ffrench-Constant C, Franklin RJ. Enhancing central nervous system remyelination in multiple sclerosis. Neuron 2005; 48: 9-12.
8. Miller RH, Mi S. Dissecting demyelination. Nat Neurosci 2007; 10: 1351-4.
9. Jolanda Münzel E, Williams A. Promoting remyelination in multiple sclerosis-recent advances. Drugs 2013; 73: 2017-29.
10. Goldenberg MM. Multiple sclerosis review. P T. 2012; 37: 175-84.
11. Lucchinetti CF, Brück W, Rodriguez M, Lassmann H. Distinct patterns of multiple sclerosis pathology indicates heterogeneity on pathogenesis. Brain Pathol 1996; 6: 259-74.
12. Lucchinetti C, Brück W, Parisi J, Scheithauer B, Rodriguez M, Lassmann H. Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann Neurol 2000; 47: 707-17.
13. Patrikios P, Stadelmann C, Kutzelnigg A, Rauschka H, Schmidbauer M, Laursen H, Sorensen PS, Brück W, Lucchinetti C, Lassmann H. Remyelination is extensive in a subset of multiple sclerosis patients. Brain 2006; 129: 3165-72.
14. Goldschmidt T, Antel J, König FB, Brück W, Kuhlmann T. Remyelination capacity of the MS brain decreases with disease chronicity. Neurology 2009; 72: 1914-21.
15. Brück W, Kuhlmann T, Stadelmann C. Remyelination in multiple sclerosis. J Neurol Sci 2003; 206: 181-5.
16. Piraino PS, Yednock TA, Messersmith EK, Pleiss MA, Freedman SB, Hammond RR, Karlik SJ. Spontaneous remyelination following prolonged inhibition of alpha4 integrin in chronic EAE. J Neuroimmunol 2005; 167: 53-63.
17. Gudi V, Gingele S, Skripuletz T, Stangel M. Glial response during cuprizone-induced de-and remyelination in the CNS: lessons learned. Front Cell Neurosci 2014; 8: 73.
18. Baxter AG. The origin and application of experimental autoimmune encephalomyelitis. Nat Rev Immunol 2007; 7: 904-12.
19. Patel JR, Klein RS. Mediators of oligodendrocyte differentiation during remyelination. FEBS Lett 2011; 585: 3730-7.
20. Fancy SP, Harrington EP, Yuen TJ, Silbereis JC, Zhao C, Baranzini SE, Bruce CC, Otero JJ, Huang EJ, Nusse R, Franklin RJ, Rowitch DH. Axin2 as regulatory and therapeutic target in newborn brain injury and remyelination. Nat Neurosci 2011; 14: 1009-16.
21. Denic A, Johnson AJ, Bieber AJ, Warrington AE, Rodriguez M, Pirko I. The relevance of animal models in multiple sclerosis research. Pathophysiology 2011; 18: 21-9.
22. Morris-Downes MM, Smith PA, Rundle JL, Piddlesden SJ, Baker D, Pham-Dinh D, Heijmans N, Amor S. Pathological and regulatory effects of anti-myelin antibodies in experimental allergic encephalomyelitis in mice. J Neuroimmunol 2002; 125: 114-24.
23. Bettelli E, Korn T, Oukka M, Kuchroo VK. Induction and effector functions of T(H)17 cells. Nature 2008; 453: 1051-7.
24. Ascherio A, Munger KL. Environmental risk factors for multiple sclerosis. Part I: the role of infection. Ann Neurol 2007; 61: 288-99.
25. Dal Canto MC, Kim BS, Miller SD, Melvold RW. Theiler's Murine Encephalomyelitis Virus (TMEV)-Induced Demyelination: A Model for Human Multiple Sclerosis. Methods 1996; 10: 453-61.
26. Sibley WA, Bamford CR, Clark K. Clinical viral infections and multiple sclerosis. Lancet 1985; 1: 1313-5.
27. Sarchielli P, Trequattrini A, Usai F, Murasecco D, Gallai V. Role of viruses in the etiopathogenesis of multiple sclerosis. Acta Neurol (Napoli) 1993; 15: 363-81.
28. Kipp M, Clarner T, Dang J, Copray S, Beyer C. The cuprizone animal model: new insights into an old story. Acta Neuropathol 2009; 118: 723-36.
29. Torkildsen O, Brunborg LA, Myhr KM, Bo L. The cuprizone model for demyelination. Acta Neurol Scand Suppl 2008; 188: 72-6.
30. Matsushima GK, Morell P. The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol 2001; 11: 107-16.
31. Tanaka T, Murakami K, Bando Y, Yoshida S. Minocycline reduces remyelination by suppressing ciliary neurotrophicfactor expression after cuprizone-induced demyelination. J Neurochem 2013; 127: 259-70.
32. Rawji KS, Yong VW. The benefits and detriments of macrophages/microglia in models of multiple sclerosis. Clin Dev Immunol 2013; 2013: 948-76.
33. Bieber AJ, Kerr S, Rodriguez M. Efficient central nervous system remyelination requires T cells. Ann Neurol 2003; 53: 680-4.
34. Imai M, Watanabe M, Suyama K, Osada T, Sakai D, Kawada H, Matsumae M, Mochida J. Delayed accumulation of activated macrophages and inhibition of remyelination after spinal cord injury in an adult rodent model. J Neurosurg Spine 2008; 8: 58-66.
35. Lau LW, Keough MB, Haylock-Jacobs S, Cua R, Döring A, Sloka S, Stirling DP, Rivest S, Yong VW. Chondroitin sulfate proteoglycans in demyelinated lesions impair remyelination. Ann Neurol 2012; 72: 419-32.
36. Wolswijk G. Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. J Neurosci 1998; 18: 601-9.
37. Franklin RJ, Ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 2008; 9: 839-55.
38. Williams A, Piaton G, Lubetzki C. Astrocytes-friends or foes in multiple sclerosis? Glia 2007; 55: 1300-12.
39. Nair A, Frederick TJ, Miller SD. Astrocytes in multiple sclerosis: a product of their environment. Cell Mol Life Sci 2008; 65: 2702-20.
40. David S, Kroner A. Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci 2011; 12: 388-99.
41. Sobel RA. The extracellular matrix in multiple sclerosis: an update. Braz J Med Biol Res 2001; 34: 603-9.
42. Wahl S, Barth H, Ciossek T, Aktories K, Mueller BK. Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase. J Cell Biol 2000; 149: 263-70.
43. Bitsch A, Kuhlmann T, Da Costa C, Bunkowski S, Polak T, Brück W. Tumour necrosis factor alpha mRNA expression in early multiple sclerosis lesions: correlation with demyelinating activity and oligodendrocyte pathology. Glia 2000; 29: 366-75.
44. Moore CS, Abdullah SL, Brown A, Arulpragasam A, Crocker SJ. How factors secreted from astrocytes impact myelin repair. J Neurosci Res 2011; 89: 13-21.
45. Napoli I, Neumann H. Protective effects of microglia in multiple sclerosis. Exp Neurol 2010; 225: 24-8.
46. Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol 2010; 6: 193-201.
47. Miron VE, Boyd A, Zhao JW, Yuen TJ, Ruckh JM, Shadrach JL, van Wijngaarden P, Wagers AJ, Williams A, Franklin RJ, ffrench-Constant C. M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat Neurosci 2013; 16: 1211-8.
48. Shijie J, Takeuchi H, Yawata I, Harada Y, Sonobe Y, Doi Y, Liang J, Hua L, Yasuoka S, Zhou Y, Noda M, Kawanokuchi J, Mizuno T, Suzumura A. Blockade of glutamate release from microglia attenuates experimental autoimmune encephalomyelitis in mice. Tohoku J Exp Med 2009; 217: 87-92.
49. van Horssen J, Witte ME, Schreibelt G, de Vries HE. Radical changes in multiple sclerosis pathogenesis. Biochim Biophys Acta 2011; 1812: 141-50.
50. Piccio L, Buonsanti C, Mariani M, Cella M, Gilfillan S, Cross AH, Colonna M, Panina-Bordignon P. Blockade of TREM-2 exacerbates experimental autoimmune encephalomyelitis. Eur J Immunol 2007; 37: 1290-301.
51. Takahashi K, Prinz M, Stagi M, Chechneva O, Neumann H. TREM2-transduced myeloid precursors mediate nervous tissue debris clearance and facilitate recovery in an animal model of multiple sclerosis. PLoS Med 2007; 4: e124.
52. Voss EV, Škuljec J, Gudi V, Skripuletz T, Pul R, Trebst C, Stangel M. Characterisation of microglia during de-and remyelination: can they create a repair promoting environment? Neurobiol Dis 2012; 45: 519-28.
53. Olah M, Amor S, Brouwer N, Vinet J, Eggen B, Biber K, Boddeke HW. Identification of a microglia phenotype supportive of remyelination. Glia 2012; 60: 306-21.
54. Skripuletz T, Hackstette D, Bauer K, Gudi V, Pul R, Voss E, Berger K, Kipp M, Baumgärtner W, Stangel M. Astrocytes regulate myelin clearance through recruitment of microglia during cuprizone-induced demyelination. Brain 2013; 136: 147-67.
55. Rosenberg SS, Ng BK, Chan JR. The quest for remyelination: a new role for neurotrophins and their receptors. Brain Pathol 2006; 16: 288-94.
56. Althaus HH, Klöppner S, Klopfleisch S, Schmitz M. Oligodendroglial cells and neurotrophins: a polyphonic cantata in major and minor. J Mol Neurosci 2008; 35: 65-79.
57. Roth GA, Spada V, Hamill K, Bornstein MB. Insulin-like growth factor I increases myelination and inhibits demyelination in cultured organotypic nerve tissue. Brain Res Dev Brain Res 1995; 88: 102-8.
58. Mason JL, Ye P, Suzuki K, D'Ercole AJ, Matsushima GK. Insulinlike growth factor-1 inhibits mature oligodendrocyte apoptosis during primary demyelination. J Neurosci 2000; 20: 5703-8.
59. Goddard DR, Berry M, Kirvell SL, Butt AM. Fibroblast growth factor-2 inhibits myelin production by oligodendrocytes in vivo. Mol Cell Neurosci 2001; 18: 557-69.
60. Rottlaender A, Villwock H, Addicks K, Kuerten S. Neuroprotective role of fibroblast growth factor-2 in experimental autoimmune encephalomyelitis. Immunology 2011; 133: 370-8.
61. Furusho M, Dupree JL, Nave KA, Bansal R. Fibroblast growth factor receptor signaling in oligodendrocytes regulates myelin sheath thickness. J Neurosci 2012; 32: 6631-41.
62. Sarchielli P, Di Filippo M, Ercolani MV, Chiasserini D, Mattioni A, Bonucci M, Tenaglia S, Eusebi P, Calabresi P. Fibroblast growth factor-2 levels are elevated in the cerebrospinal fluid of multiple sclerosis patients. Neurosci Lett 2008; 435: 223-8.
63. Hart IK, Richardson WD, Heldin CH, Westermark B, Raff MC. PDGF receptors on cells of the oligodendrocyte-type-2 astrocyte (O-2A) cell lineage. Development 1989; 105: 595-603.
64. Woodruff RH, Fruttiger M, Richardson WD, Franklin RJ. Plateletderived growth factor regulates oligodendrocyte progenitor numbers in adult CNS and their response following CNS demyelination. Mol Cell Neurosci 2004; 25: 252-62.
65. Vana AC, Flint NC, Harwood NE, Le TQ, Fruttiger M, Armstrong RC. Platelet-derived growth factor promotes repair of chronically demyelinated white matter. J Neuropathol Exp Neurol 2007; 66: 975-88.
66. Allamargot C, Pouplard-Barthelaix A, Fressinaud C. A single intracerebral microinjection of platelet-derived growth factor (PDGF) accelerates the rate of remyelination in vivo. Brain Res 2001; 918: 28-39.
67. Albrecht PJ, Enterline JC, Cromer J, Levison SW. CNTF-activated astrocytes release a soluble trophic activity for oligodendrocyte progenitors. Neurochem Res 2007; 32: 263-71.
68. Nash B, Thomson CE, Linington C, Arthur AT, McClure JD, McBride MW, Barnett SC. Functional duality of astrocytes in myelination. J Neurosci 2011; 31: 13028-38.
69. McTigue DM, Horner PJ, Stokes BT, Gage FH. 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: 5354-65.
70. He L, Lu QR. Coordinated control of oligodendrocyte development by extrinsicand intrinsic signaling cues. Neurosci Bull 2013; 29: 129-43.
71. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006; 127: 469-80.
72. van Amerongen R, Nusse R. Towards an integrated view of Wnt signaling in development. Development 2009; 136: 3205-14.
73. Fancy SP, Baranzini SE, Zhao C, Yuk DI, Irvine KA, Kaing S, Sanai N, Franklin RJ, Rowitch DH. Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev 2009; 23: 1571-85.
74. Han MH, Hwang SI, Roy DB, Lundgren DH, Price JV, Ousman SS, Fernald GH, Gerlitz B, Robinson WH, Baranzini SE, Grinnell BW, Raine CS, Sobel RA, Han DK, Steinman L. Proteomic analysis of active multiple sclerosis lesions reveals therapeutic targets. Nature 2008; 451: 1076-81.
75. 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 2011; 31: 3729-42.
76. Fu H, Kesari S, Cai J. Tcf7l2 is tightly controlled during myelin formation. Cell Mol Neurobiol 2012; 32: 345-52.
77. Xie C, Li Z, Zhang GX, Guan Y. Wnt Signaling in Remyelination in Multiple Sclerosis: Friend or Foe? Mol Neurobiol 2014; 49: 1117-25.
78. Gaiano N, Fishell G. The role of notch in promoting glial and neural stem cell fates. Annu Rev Neurosci 2002; 25: 471-90.
79. Wang S, Sdrulla AD, diSibio G, Bush G, Nofziger D, Hicks C, Weinmaster G, Barres BA. Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 1998; 21: 63-75.
80. Genoud S, Lappe-Siefke C, Goebbels S, Radtke F, Aguet M, Scherer SS, Suter U, Nave KA, Mantei N. Notch1 control of oligodendrocyte differentiation in the spinal cord. J Cell Biol 2002; 158: 709-18.
81. Zhang Y, Argaw AT, Gurfein BT, Zameer A, Snyder BJ, Ge C, Lu QR, Rowitch DH, Raine CS, Brosnan CF, John GR. Notch1 signaling plays a role in regulating precursor differentiation during CNS remyelination. Proc Natl Acad Sci USA 2009; 106: 19162-7.
82. Hu QD, Ang BT, Karsak M, Hu WP, Cui XY, Duka T, Takeda Y, Chia W, Sankar N, Ng YK, Ling EA, Maciag T, Small D, Trifonova R, Kopan R, Okano H, Nakafuku M, Chiba S, Hirai H, Aster JC, Schachner M, Pallen CJ, Watanabe K, Xiao ZC. F3/contactin acts as a functional ligand for Notch during oligodendrocyte maturation. Cell 2003; 115: 163-75.
83. Grinspan JB, Edell E, Carpio DF, Beesley JS, Lavy L, Pleasure D, Golden JA. Stage-specific effects of bone morphogenetic proteins on the oligodendrocyte lineage. J Neurobiol 2000; 43: 1-17.
84. Sabo JK, Aumann TD, Merlo D, Kilpatrick TJ, Cate HS. Remyelination is altered by bone morphogenic protein signaling in demyelinated lesions. J Neurosci 2011; 31: 4504-10.
85. Weng Q, Chen Y, Wang H, Xu X, Yang B, He Q, Shou W, Chen Y, Higashi Y, van den Berghe V, Seuntjens E, Kernie SG, Bukshpun P, Sherr EH, Huylebroeck D, Lu QR. Dual-mode modulation of Smad signaling by Smad-interacting protein Sip1 is required for myelination in the central nervous system. Neuron 2012; 3: 713-28.
86. Nery S, Wichterle H, Fishell G. Sonic hedgehog contributes to oligodendrocyte specification in the mammalian forebrain. Development 2001; 128: 527-40.
87. Tekki-Kessaris N, Woodruff R, Hall AC, Gaffield W, Kimura S, Stiles CD, Rowitch DH, Richardson WD. Hedgehog-dependent oligodendrocyte lineage specification in the telencephalon. Development 2001; 128: 2545-54.
88. Wang Y, Imitola J, Rasmussen S, O'Connor KC, Khoury SJ. Paradoxical dysregulation of the neural stem cell pathway sonic hedgehog-Gli1 in autoimmune encephalomyelitis and multiple sclerosis. Ann Neurol 2008; 64: 417-27.
89. Ortega JA, Radonji NV, Zecevic N. Sonic hedgehog promotes generation and maintenance of human forebrain Olig2 progenitors. Front Cell Neurosci 2013; 7: 254.
90. Seifert T, Bauer J, Weissert R, Fazekas F, Storch MK. Differential expression of sonic hedgehog immunoreactivity during lesion evolution in autoimmune encephalomyelitis. J Neuropathol Exp Neurol 2005; 64: 404-11.
91. Fancy SP, Zhao C, Franklin RJ. Increased expression of Nkx2.2 and Olig2 identifies reactive oligodendrocyte progenitor cells responding to demyelination in the adult CNS. Mol Cell Neurosci 2004; 27: 247-54.
92. Mi S, Lee X, Shao Z, Thill G, Ji B, Relton J, Levesque M, Allaire N, Perrin S, Sands B, Crowell T, Cate RL, McCoy JM, Pepinsky RB. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat Neurosci 2004; 7: 221-8.
93. Mi S, Miller RH, Lee X, Scott ML, Shulag-Morskaya S, Shao Z, Chang J, Thill G, Levesque M, Zhang M, Hession C, Sah D, Trapp B, He Z, Jung V, McCoy JM, Pepinsky RB. LINGO-1 negatively regulates myelination by oligodendrocytes. Nat Neurosci 2005; 8: 745-51.
94. Mi S, Miller RH, Tang W, Lee X, Hu B, Wu W, Zhang Y, Shields CB, Zhang Y, Miklasz S, Shea D, Mason J, Franklin RJ, 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 2009; 65: 304-15.
95. Arnett HA, Fancy SP, Alberta JA, Zhao C, Plant SR, Kaing S, Raine CS, Rowitch DH, Franklin RJ, Stiles CD. bHLH transcription factor Olig1 is required to repair demyelinated lesions in the CNS. Science 2004; 306: 2111-5.
96. Ligon KL, Fancy SP, Franklin RJ, Rowitch DH. Olig gene function in CNS development and disease. Glia 2006; 54: 1-10.
97. Islam MS, Tatsumi K, Okuda H, Shiosaka S, Wanaka A. Olig2-expressing progenitor cells preferentially differentiate into oligodendrocytes in cuprizone-induced demyelinated lesions. Neurochem Int 2009; 54: 192-8.
98. Lu QR, Sun T, Zhu Z, Ma N, Garcia M, Stiles CD, Rowitch DH. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 2002; 109: 75-86.
99. Stolt CC, Lommes P, Friedrich RP, Wegner M. Transcription factors Sox8 and Sox10 perform non-equivalent roles during oligodendrocyte development despite functional redundancy. Development 2004; 131: 2349-58.
100. Wegner M, Stolt CC. From stem cells to neurons and glia: a Soxist's view of neural development. Trends Neurosci 2005; 28: 583-8.
101. Li H, Lu Y, Smith HK, Richardson WD. Olig1 and Sox10 interact synergistically to drive myelin basic protein transcription in oligodendrocytes. J Neurosci 2007; 27: 14375-82.
102. Watanabe M, Hadzic T, Nishiyama A. Transient upregulation of Nkx2.2 expression in oligodendrocyte lineage cells during remyelination. Glia 2004; 46: 311-22.
103. Nakatani H, Martin E, Hassani H, Clavairoly A, Maire CL, Viadieu A, Kerninon C, Delmasure A, Frah M, Weber M, Nakafuku M, Zalc B, Thomas JL, Guillemot F, Nait-Oumesmar B, Parras C. Ascl1/Mash1 promotes brain oligodendrogenesis during myelination and remyelination. J Neurosci 2013; 33: 9752-68.
104. Wang SZ, Dulin J, Wu H, Hurlock E, Lee SE, Jansson K, Lu QR. An oligodendrocyte-specific zinc-finger transcription regulator cooperates with Olig2 to promote oligodendrocyte differentiation. Development 2006; 133: 3389-98.
105. Soundarapandian MM, Selvaraj V, Lo UG, Golub MS, Feldman DH, Pleasure DE, Deng W. Zfp488 promotes oligodendrocyte differentiation of neural progenitor cells in adult mice after demyelination. Sci Rep 2011; 1: 2.
106. Shen S, Li J, Casaccia-Bonnefil P. Histone modifications affect timing of oligodendrocyte progenitor differentiation in the developing rat brain. J Cell Biol 2005; 169: 577-89.
107. Shen S, Sandoval J, Swiss VA, Li J, Dupree J, Franklin RJ, Casaccia-Bonnefil P. Age-dependent epigenetic control of differentiation inhibitors is critical for remyelination efficiency. Nat Neurosci 2008; 11: 1024-34.
108. Ye F, Chen Y, Hoang T, Montgomery RL, Zhao XH, Bu H, Hu T, Taketo MM, van Es JH, Clevers H, Hsieh J, Bassel-Duby R, Olson EN, Lu QR. HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat Neurosci 2009; 12: 829-38.
109. Stefani G, Slack FJ. Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol 2008; 9: 219-30.
110. Dugas JC, Cuellar TL, Scholze A, Ason B, Ibrahim A, Emery B, Zamanian JL, Foo LC, McManus MT, Barres BA. Dicer1 and miR-219 are required for normal oligodendrocyte differentiation and myelination. Neuron 2010; 65: 597-611.
111. Li JS, Yao ZX. MicroRNAs: novel regulators of oligodendrocyte differentiation and potential therapeutic targets in demyelination-related diseases. Mol Neurobiol 2012; 45: 200-12.
112. Kondo T, Raff M. Basic helix-loop-helix proteins and the timing of oligodendrocyte differentiation. Development 2000; 127: 2989-98.
113. Samanta J, Kessler JA. Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development 2004; 131: 4131-42.
114. Marin-Husstege M, He Y, Li J, Kondo T, Sablitzky F, Casaccia-Bonnefil P. Multiple roles of Id4 in developmental myelination: predicted outcomes and unexpected findings. Glia 2006; 54: 285-96.
115. Ohtsuka T, Ishibashi M, Gradwohl G, Nakanishi S, Guillemot F, Kageyama R. Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. EMBO J 1999; 18: 2196-207.
116. Ogata T, Ueno T, Hoshikawa S, Ito J, Okazaki R, Hayakawa K, Morioka K, Yamamoto S, Nakamura K, Tanaka S, Akai M. Hes1 functions downstream of growth factors to maintain oligodendrocyte lineage cells in the early progenitor stage. Neuroscience 2011; 176: 132-41.
117. Jurynczyk M, Jurewicz A, Bielecki B, Raine CS, Selmaj K. Inhibition of Notch signaling enhances tissue repair in an animal model of multiple sclerosis. J Neuroimmunol 2005; 170: 3-10.
118. Morita S, Tatsumi K, Makinodan M, Okuda H, Kishimoto T, Wanaka A. Geissoschizine methyl ether, an alkaloid from the Uncaria hook, improves remyelination after cuprizone-induced demyelination in medial prefrontal cortex of adult mice. Neurochem Res 2014; 39: 59-67.
119. Crawford AH, Chambers C, Franklin RJ. Remyelination: the true regeneration of the central nervous system. J Comp Pathol 2013; 149: 242-54.