Multiple sclerosis - remyelination failure as a cause of disease progression

Histology and Histopathology

Volumn 27, Issue 3, 2012, Pages 277-287

  Hagemeier, Karin ^a   Brück, Wolfgang ^b   Kuhlmann, Tanja ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

Multiple sclerosis; Oligodendrocytes; Remyelination

Indexed keywords

ANTIINFLAMMATORY AGENT; IMMUNOSUPPRESSIVE AGENT; NEUROPROTECTIVE AGENT;

ANIMAL; DISEASE COURSE; DISEASE MODEL; DRUG EFFECT; HUMAN; METABOLISM; MULTIPLE SCLEROSIS; MYELIN SHEATH; MYELINATED NERVE; NERVE FIBER; PATHOLOGY; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; AXONS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HUMANS; IMMUNOSUPPRESSIVE AGENTS; MULTIPLE SCLEROSIS; MYELIN SHEATH; NERVE FIBERS, MYELINATED; NEUROPROTECTIVE AGENTS; RISK FACTORS; SIGNAL TRANSDUCTION;

RODENTIA;

EID: 84857769209     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (136)

1. Albert M., Antel J., Bruck W. and Stadelmann C. (2007). Extensive cortical remyelination in patients with chronic multiple sclerosis. Brain Pathol. 17, 129-138.
2. Artavanis-Tsakonas S., Rand M.D. and Lake R.J. (1999). Notch signaling: cell fate control and signal integration in development. Science 284, 770-776.
3. Bachelin C., Zujovic V., Buchet D., Mallet J. and Baron-Van Evercooren A. (2010). Ectopic expression of polysialylated neural cell adhesion molecule in adult macaque Schwann cells promotes their migration and remyelination potential in the central nervous system. Brain 133, 406-420.
4. Baer A.S., Syed Y.A., Kang S.U., Mitteregger D., Vig R., Ffrench- Constant C., Franklin R.J., Altmann F., Lubec G. and Kotter M.R. (2009). Myelin-mediated inhibition of oligodendrocyte precursor differentiation can be overcome by pharmacological modulation of Fyn-RhoA and protein kinase C signalling. Brain 132, 465-481.
5. Bauer N.G., Richter-Landsberg C. and Ffrench-Constant C. (2009). Role of the oligodendroglial cytoskeleton in differentiation and myelination. Glia 57, 1691-1705.
6. Baumann N. and Pham-Dinh D. (2001). Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol. Rev. 81, 871-927.
7. Bebo B.F.J., Zelinka-Vincent E., Adamus G., Amundson D., Vandenbark A.A. and Offner H. (1998). Gonadal hormones influence the immune response to PLP 139-151 and the clinical course of relapsing experimental autoimmune encephalomyelitis. J. Neuroimmunol. 84, 122-130.
8. Blakemore W.F. and Franklin R.J. (2008). Remyelination in experimental models of toxin-induced demyelination. Curr. Top. Microbiol. Immunol. 318, 193-212.
9. Bramow S., Frischer J.M., Lassmann H., Koch-Henriksen N., Lucchinetti C.F., Sorensen P.S. and Laursen H. (2010). Demyelination versus remyelination in progressive multiple sclerosis. Brain 133, 2983-2998.
10. Cai J., Qi Y., Hu X., Tan M., Liu Z., Zhang J., Li Q., Sander M. and Qiu M. (2005). Generation of oligodendrocyte precursor cells from mouse dorsal spinal cord independent of Nkx6 regulation and Shh signaling. Neuron 45, 41-53.
11. Caruso A., Di Giorgi Gerevini V., Castiglione M., Marinelli F., Tomassini V., Pozzilli C., Caricasole A., Bruno V., Caciagli F., Moretti A., Nicoletti F. and Melchiorri D. (2004). Testosterone amplifies excitotoxic damage of cultured oligodendrocytes. J. Neurochem. 88, 1179-1185.
12. Cerghet M., Skoff R.P., Bessert D., Zhang Z., Mullins C. and Ghandour M.S. (2006). Proliferation and death of oligodendrocytes and myelin proteins are differentially regulated in male and female rodents. J. Neurosci. 26, 1439-1447.
13. Chang A., Tourtellotte W.W., Rudick R. and Trapp B.D. (2002). Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N. Engl. J. Med. 346, 165-173.
14. Charles P., Hernandez M.P., Stankoff B., Aigrot M.S., Colin C., Rougon G., Zalc B. and Lubetzki C. (2000). Negative regulation of central nervous system myelination by polysialylated-neural cell adhesion molecule. Proc. Natl. Acad. Sci. USA 97, 7585-7590.
15. Charles P., Reynolds R., Seilhean D., Rougon G., Aigrot M.S., Niezgoda A., Zalc B. and Lubetzki C. (2002). Re-expression of PSANCAM by demyelinated axons: an inhibitor of remyelination in multiple sclerosis? Brain 125, 1972-1979.
16. D'Souza B., Miyamoto A. and Weinmaster G. (2008). The many facets of Notch ligands. Oncogene 27, 5148-5167.
17. Dalal M., Kim S. and Voskuhl R.R. (1997). Testosterone therapy ameliorates experimental autoimmune encephalomyelitis and induces a T helper 2 bias in the autoantigen-specific T lymphocyte response. J. Immunol. 159, 3-6.
18. Dawson M.R., Polito A., Levine J.M. and Reynolds R. (2003). NG2- expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol. Cell. Neurosci. 24, 476-488.
19. Debouverie M., Pittion-Vouyovitch S., Louis S. and Guillemin F. (2008). Natural history of multiple sclerosis in a population-based cohort. Eur. J. Neurol. 15, 916-921.
20. Decker L., Picard-Riera N., Lachapelle F. and Baron-Van Evercooren A. (2002). Growth factor treatment promotes mobilization of young but not aged adult subventricular zone precursors in response to demyelination. J. Neurosci. Res. 69, 763-771.
21. Dimou L., Simon C., Kirchhoff F., Takebayashi H. and Gotz M. (2008). Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J. Neurosci. 28, 10434-10442.
22. Doherty P., Cohen J. and Walsh F.S. (1990). Neurite outgrowth in response to transfected N-CAM changes during development and is modulated by polysialic acid. Neuron 5, 209-219.
23. Duncan I. D., Brower A., Kondo Y., Curlee J.F.J. and Schultz R.D. (2009). Extensive remyelination of the CNS leads to functional recovery. Proc. Natl. Acad. Sci. USA 106, 6832-6836.
24. Emery B., Agalliu D., Cahoy J.D., Watkins T. A., Dugas J.C., Mulinyawe S.B., Ibrahim A., Ligon K.L., Rowitch D.H. and Barres B.A. (2009). Myelin gene regulatory factor is a critical transcriptional regulator required for CNS myelination. Cell 138, 172-185.
25. Esiri M.M. and Morris C.S. (1991). Immunocytochemical study of macrophages and microglial cells and extracellular matrix components in human CNS disease. 2. Non-neoplastic diseases. J. Neurol. Sci. 101, 59-72.
26. Fancy S.P., Baranzini S.E., Zhao C., Yuk D.I., Irvine K.A., Kaing S., Sanai N., Franklin R.J. and Rowitch D.H. (2009). Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev. 23, 1571-1585.
27. Fannon A.M. and Colman D.R. (1996). A model for central synaptic junctional complex formation based on the differential adhesive specificities of the cadherins. Neuron 17, 423-434.
28. Ffrench-Constant C. (1994). Pathogenesis of multiple sclerosis. Lancet 343, 271-275.
29. Fogarty M., Richardson W.D. and Kessaris N. (2005). A subset of oligodendrocytes generated from radial glia in the dorsal spinal cord. Development 132, 1951-1959.
30. Franceschini I., Vitry S., Padilla F., Casanova P., Tham T.N., Fukuda M., Rougon G., Durbec P. and Dubois-Dalcq M. (2004). Migrating and myelinating potential of neural precursors engineered to overexpress PSA-NCAM. Mol. Cell. Neurosci. 27, 151-162.
31. Franklin R.J. (2002). Why does remyelination fail in multiple sclerosis? Nat. Rev. Neurosci. 3, 705-714.
32. Fu H., Qi Y., Tan M., Cai J., Takebayashi H., Nakafuku M., Richardson W. and Qiu M. (2002). Dual origin of spinal oligodendrocyte progenitors and evidence for the cooperative role of Olig2 and Nkx2.2 in the control of oligodendrocyte differentiation. Development 129, 681-693.
33. Fukuda H., Sano N., Muto S. and Horikoshi M. (2006). Simple histone acetylation plays a complex role in the regulation of gene expression. Brief Funct. Genomic Proteomic 5, 190-208.
34. Gerstner B., Sifringer M., Dzietko M., Schuller A., Lee J., Simons S., Obladen M., Volpe J.J., Rosenberg P.A. and Felderhoff-Mueser U. (2007). Estradiol attenuates hyperoxia-induced cell death in the developing white matter. Ann. Neurol. 61, 562-573.
35. Gilson J. and Blakemore W.F. (1993). Failure of remyelination in areas of demyelination produced in the spinal cord of old rats. Neuropathol. Appl. Neurobiol. 19, 173-181.
36. Girault J.A. and Peles E. (2002). Development of nodes of Ranvier. Curr. Opin. Neurobiol. 12, 476-485.
37. Goldschmidt T., Antel J., Konig F.B., Bruck W. and Kuhlmann T. (2009). Remyelination capacity of the MS brain decreases with disease chronicity. Neurology 72, 1914-1921.
38. Gregg C., Shikar V., Larsen P., Mak G., Chojnacki A., Yong V.W. and Weiss S. (2007). White matter plasticity and enhanced remyelination in the maternal CNS. J. Neurosci. 27, 1812-1823.
39. Gutowski N.J., Newcombe J. and Cuzner M.L. (1999). Tenascin-R and C in multiple sclerosis lesions: relevance to extracellular matrix remodelling. Neuropathol. Appl. Neurobiol. 25, 207-214.
40. Haberland M., Montgomery R.L. and Olson E.N. (2009). The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 10, 32-42.
41. Harsan L.A., Steibel J., Zaremba A., Agin A., Sapin R., Poulet P., Guignard B., Parizel N., Grucker D., Boehm N., Miller R.H. and Ghandour M.S. (2008). Recovery from chronic demyelination by thyroid hormone therapy: myelinogenesis induction and assessment by diffusion tensor magnetic resonance imaging. J. Neurosci. 28, 14189-14201.
42. He Y., Dupree J., Wang J., Sandoval J., Li J., Liu H., Shi Y., Nave K.A. and Casaccia-Bonnefil P. (2007). The transcription factor Yin Yang 1 is essential for oligodendrocyte progenitor differentiation. Neuron 55, 217-230.
43. Horner P.J., Power A.E., Kempermann G., Kuhn H.G., Palmer T.D., Winkler J., Thal L.J. and Gage F.H. (2000). Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J. Neurosci. 20, 2218-2228.
44. Hu Q.D., Ang B.T., Karsak M., Hu W. P., Cui X. Y., Duka T., Takeda Y., Chia W., Sankar N., Ng Y.K., Ling E.A., Maciag T., Small D., Trifonova R., Kopan R., Okano H., Nakafuku M., Chiba S., Hirai H., Aster J. C., Schachner M., Pallen C.J., Watanabe K. and Xiao Z.C. (2003). F3/contactin acts as a functional ligand for Notch during oligodendrocyte maturation. Cell 115, 163-175.
45. Ibanez C., Shields S.A., El-Etr M., Baulieu E.E., Schumacher M. and Franklin R.J. (2004). Systemic progesterone administration results in a partial reversal of the age-associated decline in CNS remyelination following toxin-induced demyelination in male rats. Neuropathol. Appl. Neurobiol. 30, 80-89.
46. Irvine K.A. and Blakemore W.F. (2006). Age increases axon loss associated with primary demyelination in cuprizone-induced demyelination in C57BL/6 mice. J. Neuroimmunol. 175, 69-76.
47. Ishibashi T., Dakin K.A., Stevens B., Lee P.R., Kozlov S. V., Stewart C.L. and Fields R.D. (2006). Astrocytes promote myelination in response to electrical impulses. Neuron 49,823-832.
48. Jarjour A.A. and Kennedy T.E. (2004). Oligodendrocyte precursors on the move: mechanisms directing migration. Neuroscientist 10,99-105.
49. Jarjour A.A., Manitt C., Moore S.W., Thompson K.M., Yuh S.J. and Kennedy T.E. (2003). Netrin-1 is a chemorepellent for oligodendrocyte precursor cells in the embryonic spinal cord. J Neurosci. 23,3735-3744.
50. John G.R., Shankar S.L., Shafit-Zagardo B., Massimi A., Lee S.C., Raine C.S. and Brosnan C.F. (2002). Multiple sclerosis: reexpression of a developmental pathway that restricts oligodendrocyte maturation. Nat. Med. 8,1115-1121.
51. Keirstead H.S., Ben-Hur T., Rogister B., O'Leary M.T., Dubois-Dalcq M. and Blakemore W.F. (1999). Polysialylated neural cell adhesion molecule-positive CNS precursors generate both oligodendrocytes and Schwann cells to remyelinate the CNS after transplantation. J Neurosci. 19,7529-7536.
52. Kessaris N., Fogarty M., Iannarelli P., Grist M., Wegner M. and Richardson W.D. (2006). Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat Neurosci. 9,173-179.
53. Kiss J.Z., Wang C., Olive S., Rougon G., Lang J., Baetens D., Harry D. and Pralong W.F. (1994). Activity-dependent mobilization of the adhesion molecule polysialic NCAM to the cell surface of neurons and endocrine cells. EMBO J. 13,5284-5292.
54. Kotter M.R., Zhao C., van Rooijen N. and Franklin R.J. (2005). 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, 166-175.
55. Kotter M.R., Li W.W., Zhao C. and Franklin R.J. (2006). Myelin impairs CNS remyelination by inhibiting oligodendrocyte precursor cell differentiation. J. Neurosci. 26,328-332.
56. Kuhlmann T., Wendling U., Nolte C., Zipp F., Maruschak B., Stadelmann C., Siebert H. and Bruck W. (2002). Differential regulation of myelin phagocytosis by macrophages/microglia, involvement of target myelin, Fc receptors and activation by intravenous immunoglobulins. J. Neurosci. Res. 67, 185-190.
57. Kuhlmann T., Remington L., Maruschak B., Owens T. and Bruck W. (2007). Nogo-A is a reliable oligodendroglial marker in adult human and mouse CNS and in demyelinated lesions. J. Neuropathol. Exp. Neurol. 66, 238-246.
58. Kuhlmann T., Miron V., Cui Q., Wegner C., Antel J. and Bruck W. (2008). Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 131, 1749-1758.
59. Kuhlmann T., Goldschmidt T., Antel J., Wegner C., Konig F., Metz I. and Bruck W. (2009). Gender differences in the histopathology of MS? J. Neurol. Sci. 286, 86-91.
60. Langseth A.J., Munji R.N., Choe Y., Huynh T., Pozniak C.D. and Pleasure S. J. (2010). Wnts influence the timing and efficiency of oligodendrocyte precursor cell generation in the telencephalon. J. Neurosci. 30, 13367-13372.
61. Lasiene J., Shupe L., Perlmutter S. and Horner P. (2008). No evidence for chronic demyelination in spared axons after spinal cord injury in a mouse. J. Neurosci. 28, 3887-3896.
62. Lau P., Verrier J.D., Nielsen J.A., Johnson K.R., Notterpek L. and Hudson L.D. (2008). Identification of dynamically regulated microRNA and mRNA networks in developing oligodendrocytes. J. Neurosci. 28, 11720-11730.
63. Lavdas A.A., Franceschini I., Dubois-Dalcq M. and Matsas R. (2006). Schwann cells genetically engineered to express PSA show enhanced migratory potential without impairment of their myelinating ability in vitro. Glia 53, 868-878.
64. Lee X., Yang Z., Shao Z., Rosenberg S. S., Levesque M., Pepinsky R.B., Qiu M., Miller R.H., Chan J R. and Mi S. (2007). NGF regulates the expression of axonal LINGO-1 to inhibit oligodendrocyte differentiation and myelination. J. Neurosci. 27, 220-225.
65. Lu Q.R., Sun T., Zhu Z., Ma N., Garcia M., Stiles C.D. and Rowitch D.H. (2002). Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109, 75-86.
66. Marin-Husstege M., Muggironi M., Liu A. and Casaccia-Bonnefil P. (2002). Histone deacetylase activity is necessary for oligodendrocyte lineage progression. J. Neurosci. 22, 10333-10345.
67. Marin-Husstege M., Muggironi M., Raban D., Skoff R.P. and Casaccia- Bonnefil P. (2004). Oligodendrocyte progenitor proliferation and maturation is differentially regulated by male and female sex steroid hormones. Dev. Neurosci. 26, 245-254.
68. Matsushima G.K. and Morell P. (2001). The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol. 11, 107-116.
69. McFarland H.F. and Martin R. (2007). Multiple sclerosis: a complicated picture of autoimmunity. Nat. Immunol. 8, 913-919.
70. Merkler D., Ernsting T., Kerschensteiner M., Bruck W. and Stadelmann C. (2006). A new focal EAE model of cortical demyelination: multiple sclerosis-like lesions with rapid resolution of inflammation and extensive remyelination. Brain 129, 1972-1983.
71. Mi S., Lee X., Shao Z., Thill G., Ji B., Relton J., Levesque M., Allaire N., Perrin S., Sands B., Crowell T., Cate R.L., McCoy J.M. and Pepinsky R.B. (2004). LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat. Neurosci. 7, 221-228.
72. 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. and Pepinsky R.B. (2005). LINGO-1 negatively regulates myelination by oligodendrocytes. Nat. Neurosci. 8, 745-751.
73. 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. and Wu W. (2007). LINGO-1 antagonist promotes spinal cord remyelination and axonal integrity in MOG-induced experimental autoimmune encephalomyelitis. Nat. Med. 13, 1228-1233.
74. Mi S., Sandrock A. and Miller R.H. (2008). LINGO-1 and its role in CNSrepair. Int. J. Biochem. Cell Biol. 40, 1971-1978.
75. Mi S., Miller R.H., Tang W., Lee X., Hu B., Wu W., Zhang Y., Shields C.B., Miklasz S., Shea D., Mason J., Franklin R.J., Ji B., Shao Z., Chedotal A., Bernard F., Roulois A., Xu J., Jung V. and Pepinsky B. (2009). Promotion of central nervous system remyelination by induced differentiation of oligodendrocyte precursor cells. Ann. Neurol. 65, 304-315.
76. Miller R.H. (1999). Contact with central nervous system myelin inhibits oligodendrocyte progenitor maturation. Dev. Biol. 216, 359-368.
77. Miller R.H. (2002). Regulation of oligodendrocyte development in the vertebrate CNS. Prog. Neurobiol. 67, 451-467.
78. Moon R.T., Bowerman B., Boutros M. and Perrimon N. (2002). The promise and perils of Wnt signaling through beta-catenin. Science 296, 1644-1646.
79. Nait-Oumesmar B., Decker L., Lachapelle F., Avellana-Adalid V., Bachelin C. and Van Evercooren A.B. (1999). Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur. J. Neurosci. 11, 4357-4366.
80. Nait-Oumesmar B., Picard-Riera N., Kerninon C., Decker L., Seilhean D., Hoglinger G.U., Hirsch E.C., Reynolds R. and Baron-Van Evercooren A. (2007). Activation of the subventricular zone in multiple sclerosis: evidence for early glial progenitors. Proc. Natl. Acad. Sci. USA 104, 4694-4699.
81. Nakahara J., Kanekura K., Nawa M., Aiso S. and Suzuki N. (2009). Abnormal expression of TIP30 and arrested nucleocytoplasmic transport within oligodendrocyte precursor cells in multiple sclerosis. J. Clin. Invest. 119, 169-181.
82. Nan X., Ng H.H., Johnson C.A., Laherty C.D., Turner B.M., Eisenman R.N. and Bird A. (1998). Transcriptional repression by the methyl- CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393, 386-389.
83. Nelson W.J. and Nusse R. (2004). Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303, 1483-1487.
84. Noll E. and Miller R.H. (1993). Oligodendrocyte precursors originate at the ventral ventricular zone dorsal to the ventral midline region in the embryonic rat spinal cord. Development 118, 563-573.
85. Noseworthy J.H., Lucchinetti C., Rodriguez M. and Weinshenker B.G. (2000). Multiple sclerosis. N. Engl. J. Med. 343, 938-952.
86. Patani R., Balaratnam M., Vora A. and Reynolds R. (2007). Remyelination can be extensive in multiple sclerosis despite a long disease course. Neuropathol. Appl. Neurobiol. 33, 277-287.
87. Patrikios P., Stadelmann C., Kutzelnigg A., Rauschka H., Schmidbauer M., Laursen H., Sorensen P.S., Bruck W., Lucchinetti C. and Lassmann H. (2006). Remyelination is extensive in a subset of multiple sclerosis patients. Brain 129, 3165-3172.
88. Pedre X., Mastronardi F., Bruck W., Lopez-Rodas G., Kuhlmann T. and Casaccia P. (2011). Changed histone acetylation patterns in normalappearing white matter and early multiple sclerosis lesions. J. Neurosci. 31, 3435-3445.
89. Pierfelice T., Alberi L. and Gaiano N. (2011). Notch in the vertebrate nervous system: an old dog with new tricks. Neuron 69, 840-855.
90. Pohl H.B., Porcheri C., Mueggler T., Bachmann L.C., Martino G., Riethmacher D., Franklin R.J., Rudin M. and Suter U. (2011). Genetically induced adult oligodendrocyte cell death is associated with poor myelin clearance, reduced remyelination, and axonal damage. J. Neurosci. 31, 1069-1080.
91. Popko B. (2008). Epigenetic control of myelin repair. Nat. Neurosci. 11, 987-988.
92. Pringle N.P., Guthrie S., Lumsden A. and Richardson W.D. (1998). Dorsal spinal cord neuroepithelium generates astrocytes but not oligodendrocytes. Neuron 20, 883-893.
93. Raine C.S. and Wu E. (1993). Multiple sclerosis: remyelination in acute lesions. J. Neuropathol. Exp. Neurol. 52, 199-204.
94. Rougon G. (1993). Structure, metabolism and cell biology of polysialic acids. Eur. J. Cell Biol. 61, 197-207.
95. Rowitch D.H. (2004). Glial specification in the vertebrate neural tube. Nat. Rev. Neurosci. 5, 409-419.
96. Satoh J., Tabunoki H., Yamamura T., Arima K. and Konno H. (2007). TROY and LINGO-1 expression in astrocytes and macrophages/microglia in multiple sclerosis lesions. Neuropathol. Appl. Neurobiol. 33, 99-107.
97. Schonrock L.M., Kuhlmann T., Adler S., Bitsch A. and Bruck W. (1998). Identification of glial cell proliferation in early multiple sclerosis lesions. Neuropathol. Appl. Neurobiol. 24, 320-330.
98. Seki T. and Arai Y. (1991). The persistent expression of a highly polysialylated NCAM in the dentate gyrus of the adult rat. Neurosci. Res. 12, 503-513.
99. Seki T. and Arai Y. (1993). Distribution and possible roles of the highly polysialylated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system. Neurosci. Res. 17, 265-290.
100. Shao Z., Browning J.L., Lee X., Scott M.L., Shulga-Morskaya S., Allaire N., Thill G., Levesque M., Sah D., McCoy J.M., Murray B., Jung V., Pepinsky R.B. and Mi S. (2005). TAJ/TROY, an orphan TNF receptor family member, binds Nogo-66 receptor 1 and regulates axonal regeneration. Neuron 45, 353-359.
101. Shen S., Li J. and Casaccia-Bonnefil P. (2005). Histone modifications affect timing of oligodendrocyte progenitor differentiation in the developing rat brain. J. Cell. Biol. 169, 577-589.
102. Shen S., Liu A., Li J., Wolubah C. and Casaccia-Bonnefil P. (2008a). Epigenetic memory loss in aging oligodendrocytes in the corpus callosum. Neurobiol Aging 29, 452-463.
103. Shen S., Sandoval J., Swiss V.A., Li J., Dupree J., Franklin R.J. and Casaccia-Bonnefil P. (2008b). Age-dependent epigenetic control of differentiation inhibitors is critical for remyelination efficiency. Nat. Neurosci. 11, 1024-1034.
104. Shields S., Gilson J., Blakemore W. and Franklin R. (2000). Remyelination occurs as extensively but more slowly in old rats compared to young rats following fliotoxin-induced CNS demyelination. Glia 29, 102.
105. Shimizu T., Kagawa T., Wada T., Muroyama Y., Takada S. and Ikenaka K. (2005). Wnt signaling controls the timing of oligodendrocyte development in the spinal cord. Dev. Biol. 282, 397-410.
106. Shin D., Shin J.Y., McManus M.T., Ptacek L.J. and Fu Y.H. (2009). Dicer ablation in oligodendrocytes provokes neuronal impairment in mice. Ann. Neurol. 66, 843-857.
107. Sim J.A., Skynner M.J. and Herbison A.E. (2001). Heterogeneity in the basic membrane properties of postnatal gonadotropin-releasing hormone neurons in the mouse. J. Neurosci. 21, 1067-1075.
108. Sim F.J., Zhao C., Penderis J. and Franklin R.J. (2002). The age-related decrease in CNS remyelination efficiency is attributable to an impairment of both oligodendrocyte progenitor recruitment and differentiation. J. Neurosci. 22, 2451-2459.
109. Smith P.M. and Jeffery N.D. (2006). Histological and ultrastructural analysis of white matter damage after naturally-occurring spinal cord injury. Brain Pathol. 16, 99-109.
110. Sobel R.A., Chen M., Maeda A. and Hinojoza J.R. (1995). Vitronectinand integrin vitronectin receptor localization in multiple sclerosis lesions. J. Neuropathol. Exp. Neurol. 54, 202-213.
111. Sobel R.A. and Mitchell M.E. (1989). Fibronectin in multiple sclerosis lesions. Am. J. Pathol. 135, 161-168.
112. Spassky N., de Castro F., Le Bras B., Heydon K., Queraud-LeSaux F., Bloch-Gallego E., Chedotal A., Zalc B. and Thomas J.L. (2002). Directional guidance of oligodendroglial migration by class 3 semaphorins and netrin-1. J. Neurosci. 22, 5992-6004.
113. Stidworthy M.F., Genoud S., Li W.W., Leone D.P., Mantei N., Suter U. and Franklin R.J. (2004). Notch1 and Jagged1 are expressed after CNS demyelination, but are not a major rate-determining factor during remyelination. Brain 127, 1928-1941.
114. Sugimoto Y., Taniguchi M., Yagi T., Akagi Y., Nojyo Y. and Tamamaki N. (2001). Guidance of glial precursor cell migration by secreted cues in the developing optic nerve. Development 128, 3321-3330.
115. Takahashi K., Prinz M., Stagi M., Chechneva O. and Neumann H. (2007). TREM2-transduced myeloid precursors mediate nervous tissue debris clearance and facilitate recovery in an animal model of multiple sclerosis. PLoS Med. 4, e124.
116. Theodosis D.T., Bonhomme R., Vitiello S., Rougon G. and Poulain D.A. (1999). Cell surface expression of polysialic acid on NCAM is a prerequisite for activity-dependent morphological neuronal and glial plasticity. J. Neurosci. 19, 10228-10236.
117. Vallstedt A., Klos J.M. and Ericson J. (2005). Multiple dorsoventral origins of oligodendrocyte generation in the spinal cord and hindbrain. Neuron 45, 55-67.
118. van de Wetering M., Sancho E., Verweij C., de Lau W., Oving I., Hurlstone A., van der Horn K., Batlle E., Coudreuse D., Haramis A. P., Tjon-Pon-Fong M., Moerer P., van den Born M., Soete G., Pals S., Eilers M., Medema R. and Clevers H. (2002). The betacatenin/ TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111, 241-250.
119. Wang C., Rougon G. and Kiss J.Z. (1994). Requirement of polysialic acid for the migration of the O-2A glial progenitor cell from neurohypophyseal explants. J. Neurosci. 14, 4446-4457.
120. Wang C., Pralong W. F., Schulz M.F., Rougon G., Aubry J.M., Pagliusi S., Robert A. and Kiss J.Z. (1996). Functional N-methyl-D-aspartate receptors in O-2A glial precursor cells: a critical role in regulating polysialic acid-neural cell adhesion molecule expression and cell migration. J. Cell Biol. 135, 1565-1581.
121. Weinshenker B.G. (1998). The natural history of multiple sclerosis: update 1998. Semin. Neurol. 18, 301-307.
122. Williams A., Piaton G., Aigrot M. S., Belhadi A., Theaudin M., Petermann F., Thomas J. L., Zalc B. and Lubetzki C. (2007). Semaphorin 3A and 3F: key players in myelin repair in multiple sclerosis? Brain 130, 2554-2565.
123. Wolswijk G. (1998). Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. J. Neurosci. 18, 601-609.
124. Wolswijk G. (2000). Oligodendrocyte survival, loss and birth in lesions of chronic-stage multiple sclerosis. Brain 123 (Pt 1), 105-115.
125. Wolswijk G. (2002). Oligodendrocyte precursor cells in the demyelinated multiple sclerosis spinal cord. Brain 125, 338-349.
126. Woodruff R.H. and Franklin R.J. (1999). The expression of myelin protein mRNAs during remyelination of lysolecithin-induced demyelination. Neuropathol. Appl. Neurobiol. 25, 226-235.
127. Woodruff R.H., Fruttiger M., Richardson W.D. and Franklin R.J. (2004). Platelet-derived growth factor regulates oligodendrocyte progenitor numbers in adult CNS and their response following CNS demyelination. Mol. Cell. Neurosci. 25, 252-262.
128. 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. and Lu Q.R. (2009). HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat. Neurosci. 12, 829-838.
129. Zamvil S.S. and Steinman L. (1990). The T lymphocyte in experimental allergic encephalomyelitis. Annu. Rev. Immunol. 8, 579-621.
130. Zhang H., Miller R.H. and Rutishauser U. (1992). Polysialic acid is required for optimal growth of axons on a neuronal substrate. J. Neurosci. 12, 3107-3114.
131. 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. and John G.R. (2009). Notch1 signaling plays a role in regulating precursor differentiation during CNS remyelination. Proc. Natl. Acad. Sci. USA 106, 19162-19167.
132. Zhao C., Li W.W. and Franklin R.J. (2006). Differences in the early inflammatory responses to toxin-induced demyelination are associated with the age-related decline in CNS remyelination. Neurobiol. Aging 27, 1298-1307.
133. Zhao X., He X., Han X., Yu Y., Ye F., Chen Y., Hoang T., Xu X., Mi Q.S., Xin M., Wang F., Appel B. and Lu Q.R. (2010). MicroRNAmediated control of oligodendrocyte differentiation. Neuron 65, 612-626.
134. Zhao X.H., Jin W.L. and Ju G. (2007). An in vitro study on the involvement of LINGO-1 and Rho GTPases in Nogo-A regulated differentiation of oligodendrocyte precursor cells. Mol. Cell. Neurosci. 36, 260-269.
135. Zhou Q. and Anderson D.J. (2002). The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109, 61-73.
136. Zhou Q., Wang S. and Anderson D.J. (2000). Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25, 331-343.