The Myelin Mutants as Models to Study Myelin Repair in the Leukodystrophies

Neurotherapeutics

Volumn 8, Issue 4, 2011, Pages 607-624

  Duncan, Ian D ^a   Kondo, Yoichi ^a   Zhang, Su Chun ^b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Cell transplantation; Leukodystrophies; Myelin mutants; Myelination; Oligodendrocyte progenitors

Indexed keywords

CEREBROSIDE SULFATASE; LYSOSOME ENZYME; MYELIN;

ADRENOLEUKODYSTROPHY; ALEXANDER DISEASE; CANAVAN DISEASE; CELL THERAPY; CELL TRANSPLANTATION; CEREBROTENDINOUS XANTHOMATOSIS; GLOBOID CELL LEUKODYSTROPHY; LEUKODYSTROPHY; NONHUMAN; PELIZAEUS MERZBACHER DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REFSUM DISEASE; REVIEW;

ANIMALS; CELL TRANSPLANTATION; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; HUMANS; MICE; MICE, TRANSGENIC; MUTATION; MYELIN SHEATH;

EID: 80955131264     PISSN: 19337213     EISSN: 18787479     Source Type: Journal    
DOI: 10.1007/s13311-011-0080-y     Document Type: Review

References (125)

1. Costello DJ, Eichler AF, Eichler FS. Leukodystrophies: classification, diagnosis, and treatment. Neurologist 2009; 15: 319-328.
2. Zhang SC, Duncan ID. Remyelination and restoration of axonal function by glial cell transplantation. Prog Brain Res 2000; 127: 515-533.
3. Franklin RJ, ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 2008; 9: 839-855.
4. Irvine KA, Blakemore WF. Remyelination protects axons from demyelination-associated axon degeneration. Brain 2008; 131: 1464-1477.
5. Huang JK, Franklin RJ. Regenerative medicine in multiple sclerosis: Identifying pharmacological targets of adult neural stem cell differentiation. Neurochem Int 2011; 59(3): 329-332.
6. Kondo Y, Wenger DA, Gallo V, Duncan ID. Galactocerebrosidase-deficient oligodendrocytes maintain stable central myelin by exogenous replacement of the missing enzyme in mice. Proc Natl Acad Sci U S A 2005; 102: 18670-18675.
7. Blakemore WF, Eames RA. Remyelination in the spinal cord of the cat following intraspinal injections of lysolecithin. J Neurol Sci 1977; 33: 31-43.
8. Blakemore WF. Ethidium bromide induced demyelination in the spinal cord of the cat. Neuropathol Appl Neurobiol 1982; 8: 365-375.
9. Blakemore WF, Patterson RC. Suppression of remyelination in the CNS by X-irradiation. Acta Neuropathologica 1978; 42: 105-113.
10. Mason JL, Toews A, Hostettler JD, et al. Oligodendrocytes and progenitors become progressively depleted within chronically demyelinated lesions. Am J Pathol 2004; 164: 1673-1682.
11. Griffiths IR. Myelin mutants: Model systems for the study of normal and abnormal myelination. BioEssays 1996; 18: 789-797.
12. Duncan ID. Inherited disorders of myelination of the central nervous system. In: Ransom BR, Kettenmann HR, eds. Neuroglial Cells. Cambridge: Oxford University Press, 1995: 990-1009.
13. Griffiths IR, Schneider A, Anderson JM, Nave KA. Transgenic and natural mouse models of proteolipid protein (PLP)-related dysmyelination and demyelination. Brain Pathol 1995; 5: 275-281.
14. Hodes ME, Woodward K, Spinner NB, et al. Additional copies of the proteolipid protein gene causing Pelizaeus-Merzbacher disease arise by separate integration into the X chromosome. Am J Hum Genet 2000; 67: 14-22.
15. Mimault C, Giraud G, Courtois V, et al. Proteolipoprotein gene analysis in 82 patients with sporadic Pelizaeus-Merzbacher disease: Duplications, the major cause of the disease, originate more frequently in male germ cells, but point mutations do not. Am J Hum Genet 1999; 65: 360-369.
16. Bradl M, Bauer J, Inomata T, et al. Transgenic Lewis rats overexpressing the proteolipid protein gene: myelin degeneration and its effect on T cell-mediated experimental autoimmune encephalomyelitis. Acta Neuropathol(Berl) 1999; 97: 595-606.
17. Mayer J, Larsen E, Duncan I. Characterization of the PLP-overexpressing transgenic rat, a model for the connatal form of Pelizaeus-Merzbacher disease. Neurobiol Dis 2010; 44(2): 231-238.
18. Jackson KF, Duncan ID. Cell kinetics and cell death in the optic nerve of the myelin deficient rat. J Neurocytol 1988; 17: 657-670.
19. Csiza CK, de Lahunta A. Myelin deficiency (md): a neurologic mutant in the Wistar rat. Am J Pathol 1979; 95: 215-224.
20. Wolf NI, Sistermans EA, Cundall M, et al. Three or more copies of the proteolipid protein gene PLP1 cause severe Pelizaeus-Merzbacher disease. Brain 2005; 128(Pt 4): 743-751.
21. Duncan ID, Hammang JP, Jackson KF, Wood PM, Bunge RP, Langford LA. Transplantation of oligodendrocytes and Schwann cells into the spinal cord of the myelin-deficient rat. J Neurocytol 1988; 17: 351-360.
22. Rosenbluth J, Liu Z, Guo D, Schiff R. Myelin formation by mouse glia in myelin-deficient rats treated with cyclosporine. J Neurocytol 1993; 22: 967-977.
23. Tontsch U, Archer DR, Dubois-Dalcq M, Duncan ID. Transplantation of an oligodendrocyte cell line leading to extensive myelination. Proc Natl Acad Sci U S A 1994; 91: 11616-11620.
24. Wenger D, Suzuki K, Suzuki Y, Suzuki K. Galactosylceramide lipidosis. Globoid cell leukodystrophy (Krabbe disease). In: Scriver C, Beaudet A, Sly W, et al, eds. The Metabolic and Molecular Bases of Inherited Disease, 8th ed. New York: McGraw-Hill, 2001: 3669-3694.
25. Hess B, Saftig P, Hartmann D, et al. Phenotype of arylsulfatase A-deficient mice: relationship to human metachromatic leukodystrophy. Proc Natl Acad Sci U S A 1996; 93: 93(25): 14821-14826.
26. Biffi A, Capotondo A, Fasano S, et al. Gene therapy of metachromatic leukodystrophy reverses neurological damage and deficits mice. J Clin Invest 2006; 116: 3070-3082.
27. Givogri MI, Bottai D, Zhu HL, et al. Multipotential neural precursors transplanted into the metachromatic leukodystrophy brain fail to generate oligodendrocytes but contribute to limit brain dysfunction. Dev Neurosci 2008; 30: 340-357.
28. Moser HW. Adrenoleukodystrophy: phenotype, genetics, pathogenesis and therapy. Brain 1997; 120: 1485-1508.
29. Dubois-Dalcq M, Feigenbaum V, Aubourg P. The neurobiology of X-linked adrenoleukodystrophy, a demyelinating peroxisomal disorder. Trends Neurosci 1999; 22: 4-12.
30. Powers JM. The pathology of peroxisomal disorders with pathogenetic considerations. J Neuropathol Exp Neurol 1995; 54: 710-719.
31. Ferrer I, Aubourg P, Pujol A. General aspects and neuropathology of X-linked adrenoleukodystrophy. Brain Pathol 2010; 20: 817-830.
32. Kassmann CM, Lappe-Siefke C, Baes M, et al. Axonal loss and neuroinflammation caused by peroxisome-deficient oligodendrocytes. Nat Genet 2007; 39: 969-976.
33. Hagemann TL, Connor JX, Messing A. Alexander disease-associated glial fibrillary acidic protein mutations in mice induce Rosenthal fiber formation and a white matter stress response. J Neurosci 2006; 26: 11162-11173.
34. Matalon R, Rady PL, Platt KA, et al. Knock-out mouse for Canavan disease: a model for gene transfer to the central nervous system. J Gene Med 2000; 2: 165-175.
35. Surendran S, Campbell GA, Tyring SK, Matalon R. Aspartoacylase gene knockout results in severe vacuolation in the white matter and gray matter of the spinal cord in the mouse. Neurobiol Dis 2005; 18: 385-389.
36. Kitada K, Akimitsu T, Shigematsu Y, et al. Accumulation of N-acetyl-L-aspartate in the brain of the tremor rat, a mutant exhibiting absence-like seizure and spongiform degeneration in the central nervous system. J Neurochem 2000; 74: 2512-2519.
37. Li FY, Cuddon PA, Song J, et al. Canine spongiform leukoencephalomyelopathy is associated with a missense mutation in cytochrome b. Neurobiol Dis 2006; 21: 35-42.
38. Oldfors A, Tulinius M. Mitochondrial encephalomyopathies. J Neuropathol Exp Neurol 2003; 62: 217-227.
39. Surendran S, Shihabuddin LS, Clarke J, et al. Mouse neural progenitor cells differentiate into oligodendrocytes in the brain of a knockout mouse model of Canavan disease. Dev Brain Res 2004; 153: 19-27.
40. van der Knaap M, Pronk J, Scheper G. Vanishing white matter disease. Lancet Neurol 2006; 5: 413-423.
41. Garbern JY, Yool DA, Moore GJ, et al. Patients lacking the major CNS myelin protein, proteolipid protein 1, develop length-dependent axonal degeneration in the absence of demyelination and inflammation. Brain 2002; 125: 551-561.
42. Trapp BD, Nave KA. Multiple sclerosis: an immune or neurodegenerative disorder? Annu Rev Neurosci 2008; 31: 247-269.
43. Simons R, Riordan JR. The myelin-deficient rat has a single base substitution in the third exon of the myelin proteolipid protein gene. J Neurochem 1990; 54: 1079-1081.
44. Lipsitz D, Goetz BD, Duncan ID. Apoptotic glial cell death and kinetics in the spinal cord of the myelin-deficient rat. J Neurosci Res 1998; 51: 497-507.
45. Duncan ID, Hammang JP, Trapp BD. Abnormal compact myelin in the myelin-deficient rat: Absence of proteolipid protein correlates with a defect in the intraperiod line. Proc Natl Acad Sci U S A 1987; 84: 6287-6291.
46. Learish RD, Brüstle O, Zhang SC, Duncan ID. Intraventricular transplantation of oligodendrocyte progenitors into a fetal myelin mutant results in widespread formation of myelin. Ann Neurol 1999; 46: 716-722.
47. Duncan ID, Nadon NL, Hoffman RL, Lunn KF, Csiza CK, Wells MR. Oligodendrocyte survival and function in the long-lived strain of the myelin deficient rat. J Neurocytol 1995; 24: 745-762.
48. Duncan ID, Griffiths IR. Shaking pups: A disorder of central myelination in the Spaniel dog. III. Quantitative aspects of glia and myelin in the spinal cord and optic nerve. Neuropathol Appl Neurobiol 1983; 9: 355-368.
49. Griffiths IR, Duncan ID, McCulloch M, Harvey MJA. Shaking pups: A disorder of central myelination in the Spaniel dog. I Clinical, genetic and light microscopical observations. J Neurol Sci 1981; 50: 423-433.
50. Nadon NL, Duncan ID, Hudson LD. A point mutation in the proteolipid protein gene of the "shaking pup" interrupts oligodendrocyte development. Development 1990; 110: 529-537.
51. Wu Y-C, Field AS, Duncan ID, Samsonov AA, Alexander AL. High b-value and diffusion tensor imaging in a canine model of dysmyelination and brain maturation. Neuroimage 2011; 58(3): 829-837.
52. Archer DR, Cuddon PA, Lipsitz D, Duncan ID. Myelination of the canine central nervous system by glial cell transplantation: a model for repair of human myelin disease. Nat Med 1997; 3: 54-59.
53. Mikoshiba K, Aruga J, Ikenaka K, Okano H, Martenson RE. Shiverer and allelic mutant mld mice. In: Myelin: Biology and Chemistry. Boca Raton: CRC Press, 1992: 723-744.
54. Lachapelle F, Gumpel M, Baulac M, Jacque C, Duc P, Baumann N. Transplantation of CNS fragments into the brain of shiverer mutant mice: extensive myelination by implanted oligodendrocytes. I. Immunohistochemical studies. Dev Neurosci 1983; 6: 325-334.
55. Windrem MS, Schanz SJ, Guo M, et al. Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2008; 2: 553-565.
56. O'Connor LT, Goetz BD, Kwiecien JM, Delaney KH, Fletch AL, Duncan ID. Insertion of a retrotransposon into the myelin basic gene causes CNS dysmyelination in the Long Evans shaker (les) rat. J Neurosci 1999; 19: 3404-3413.
57. Kwiecien JM, O'Connor LT, Goetz BD, Delaney KH, Fletch AL, Duncan ID. Morphological and morphometric studies of the dysmyelinating mutant, the Long Evans shaker rat. J Neurocytol 1998; 27: 581-591.
58. Zhang SC, Goetz BD, Carr' JL, Duncan ID. Reactive microglia in dysmyelination and demyelination. GLIA 2001; 34: 101-109.
59. Duncan ID, Lunn KF, Holmgren B, Urba-Holmgren R, Brignolo-Holmes L. The taiep rat: A myelin mutant with an associated oligodendrocyte microtubular defect. J Neurocytol 1992; 21: 870-884.
60. Song J, O'Connor LT, Yu W, Baas PW, Duncan ID. Microtubule alterations in cultured taiep rat oligodendrocytes lead to deficits in myelin membrane formation. J Neurocytol 1999; 28: 671-683.
61. O'Connor LT, Goetz BD, Couve E, Song J, Duncan ID. Intracellular distribution of myelin protein gene products is altered in oligodendrocytes of the taiep rat. Mol Cell Neurosci 2000; 16: 396-407.
62. Song J, Goetz BD, Baas PW, Duncan ID. Cytoskeletal reorganization during the formation of oligodendrocyte processes and branches. Mol Cell Neurosci 2001; 17: 624-636.
63. Song J, Carson JH, Barbarese E, Li FY, Duncan ID. RNA transport in oligodendrocytes from the taiep mutant rat. Mol Cell Neurosci 2003; 24: 926-938.
64. Li FY, Song J, Duncan ID. Mapping of taiep rat phenotype to rat Chromosome 9. Mamm Genome 2003; 14: 703-705.
65. Duchen LW, Eicher EM, Jacobs JM, Scaravilli F, Teixeira F. Hereditary leucodystrophy in the mouse: the new mutant twitcher. Brain 1980; 103: 695-710.
66. Sakai N, Inui K, Tatsumi N, et al. Molecular cloning and expression of cDNA for murine galactocerebrosidase and mutation analysis of the twitcher mouse, a model of Krabbe's disease. J Neurochem 1996; 66: 1118-1124.
67. Rafi MA, Rao HZ, Passini MA, et al. AAV-mediated expression of galactocerebrosidase in brain results in attenuated symptoms and extended life span in murine models of globoid cell leukodystrophy. Mol Ther 2005; 11: 734-744.
68. Kondo Y, Adams JM, Vanier MT, Duncan ID. Macrophages counteract demyelination in a mouse model of globoid cell leukodystrophy. J Neurosci 2011; 31: 3610-3624.
69. Taniike M, Suzuki K. Spacio-temporal progression of demyelination in twitcher mouse: With clinico-pathological correlation. Acta Neuropathol 1994; 88: 228-236.
70. Victoria T, Rafi MA, Wenger DA. Cloning of the canine GALC cDNA and identification of the mutation causing globoid cell leukodystrophy in West Highland White and Cairn terriers. Genomics 1996; 33: 457-462.
71. Capucchio MT, Prunotto M, Lotti D, et al. Krabbe's disease in two West Highland White terriers. Clin Neuropathol 2008; 27: 295-301.
72. Sigurdson CJ, Basaraba RJ, Mazzaferro EM, Gould DH. Globoid cell-like Leukodystrophy in a domestic longhaired cat. Vet Pathol 2002; 39: 494-496.
73. Baskin GB, Ratterree M, Davison BB, et al. Genetic galactocerebrosidase deficiency (globoid cell leukodystrophy, Krabbe disease) in Rhesus monkeys (macaca mulatta). Lab Anim Sci 1998; 48: 476-482.
74. Gumpel M, Lachapelle F, Baumann N, Björklund A, Stenevi U. Central nervous tissue transplantation into mouse brain: differentiation of myelin from transplanted oligodendrocytes. In: Neural Grafting in the Mammalian CNS: Elsevier Science Publishers, B. V., 1985: 151-158.
75. Gumpel M, Gout O. Myelination and remyelination in the central nervous system by transplanted oligodendrocytes using the shiverer model. Dev Neurosci 1989; 11: 132-139.
76. Gansmuller A, Lachapelle F, Baron-van Evercooren A, Hauw JJ, Baumann N, Gumpel M. Transplantations of newborn CNS fragments into the brain of shiverer mutant mice: extensive myelination by transplanted oligodendrocytes. II. Electron microscopic study. Dev Neurosci 1986; 8: 197-207.
77. Schiff R, Rosenbluth J, Dou WK, Liang WL, Moon D. Distribution and morphology of transgenic mouse oligodendroglial- lineage cells following transplantation into normal and myelin-deficient rat CNS. J Comp Neurol 2002; 446: 46-57.
78. Taylor RM, Lee JP, Palacino JJ, et al. Intrinsic resistance of neural stem cells to toxic metabolites may make them well suited for cell non-autonomous disorders: evidence from a mouse model of Krabbe leukodystrophy. J Neurochem 2006; 97: 1585-1599.
79. Eftekharpour E, Karimi-Abdolrezaee S, Wang J, El Beheiry H, Morshead C, Fehlings MG. Myelination of congenitally dysmyelinated spinal cord axons by adult neural precursor cells results in formation of nodes of Ranvier and improved axonal conduction. J Neurosci 2007; 27: 3416-3428.
80. Mothe AJ, Kulbatski I, Parr A, Mohareb M, Tator CH. Adult spinal cord stem/progenitor cells transplanted as neurospheres preferentially differentiate into oligodendrocytes in the adult rat spinal cord. Cell Transplant 2008; 17: 735-751.
81. Foote AK, Blakemore WF. Inflammation stimulates remyelination in areas of chronic demyelination. Brain 2005; 128: 528-539.
82. Mitome M, Low HP, van den Pol A, et al. Towards the reconstruction of central nervous system white matter using neural precursor cells. Brain 2001; 124: 2147-2161.
83. Buchet D, Garcia C, Deboux C, Nait-Oumesmar B, Baron-van Evercooren A. Human neural progenitors from different foetal forebrain regions remyelinate the adult mouse spinal cord. Brain 2011; 134: 1168-1183.
84. Zhang SC, Wagner D, Duncan ID. Acute death of grafted oligodendroglial progenitors. Soc for Neurosci 1999; 25: 215.
85. Milward EA, Zhang SC, Zhao M, et al. Enhanced proliferation and directed migration of oligodendroglial progenitors co-grafted with growth factor-secreting cells. GLIA 2000; 32: 264-270.
86. Bulte JWM, Douglas T, Witwer B, et al. Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat Biotechnol 2001; 19: 1141-1147.
87. Bulte JWM, Zhang SC, van Gelderen P, et al. Neurotransplantation of magnetically labeled oligodendrocyte progenitors: MR tracking of cell migration and myelination. Proc Natl Acad Sci 1999; 96(26): 15256-15261.
88. Sher F, van Dam G, Boddeke E, Copray S. Bioluminescence imaging of Olig2-neural stem cells reveals improved engraftment in a demyelination mouse model. Stem Cells 2009; 27: 1582-1591.
89. Utzschneider DA, Archer DR, Kocsis JD, Waxman SG, Duncan ID. Transplantation of glial cells enhances action potential conduction of amyelinated spinal cord axons in the myelin-deficient rat. Proc Natl Acad Sci U S A 1994; 91: 53-57.
90. Yandava BD, Billinghurst LL, Snyder EY. "Global" cell replacement is feasible via neural stem cell transplantation: Evidence from the dysmyelinated shiverer mouse brain. Proc Natl Acad Sci USA 1999; 96: 7029-7034.
91. Scaravilli F, Suzuki K. Enzyme replacement in grafted nerve of twitcher mouse. Nature 1983; 305: 713-715.
92. Scaravilli F, Jacobs JM. Improved myelination in nerve grafts from the leucodystrophic twitcher into trembler mice: Evidence for enzyme replacement. Brain Res 1982; 237: 163-172.
93. Luddi A, Volterrani M, Strazza M, et al. Retrovirus-mediated gene transfer and galactocerebrosidase uptake into twitcher glial cells results in appropriate localization and phenotype correction. Neurobiol Dis 2001; 8: 600-610.
94. Lee WC, Courtenay A, Troendle FJ, et al. Enzyme replacement therapy results in substantial improvements in early clinical phenotype in a mouse model of globoid cell leukodystrophy. FASEB J 2005; 19(11): 1549-1551.
95. Yuan X, Chittajallu R, Belachew S, Anderson S, McBain CJ, Gallo V. Expression of the green fluorescent protein in the oligodendrocyte lineage: a transgenic mouse for developmental and physiological studies. J Neurosci Res 2002; 70: 529-545.
96. Krivit W, Shapiro EG, Peters C, et al. Hematopoietic stem-cell transplantation in globoid-cell leukodystrophy. N Engl J Med 1998; 338: 1119-1126.
97. Escolar ML, Poe MD, Provenzale JM, et al. Transplantation of umbilical-cord blood in babies with infantile Krabbe's disease. New Engl J Med 2005; 352: 2069-2081.
98. Gentner B, Visigalli I, Hiramatsu H, et al. Identification of hematopoietic stem cell-specific miRNAs enables gene therapy of globoid cell leukodystrophy. Sci Transl Med 2010; 2(58): 58ra84.
99. Buchet D, Baron-van Evercooren A. In search of human oligodendroglia for myelin repair. Neurosci Lett 2009; 456: 112-119.
100. Duncan ID. Oligodendrocytes and stem cell transplantation: their potential in the treatment of leukoencephalopathies. J Inherit Metab Dis 2005; 28: 357-368.
101. Ben-Hur T, Goldman SA. Prospects of cell therapy for disorders of myelin. Ann N Y Acad Sci 2008; 1142: 218-249.
102. Duncan ID, Goldman S, Macklin WB, Rao M, Weiner LP, Reingold SC. Stem cell therapy in multiple sclerosis: promise and controversy. Mult Scler 2008; 14: 541-546.
103. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992; 255: 1707-1710.
104. Avellana-Adalid V, Nait-Oumesmar B, Lachapelle F, Baron-van Evercooren A. Expansion of rat oligodendrocyte progenitors into proliferative "oligospheres" that retain differentiation potential. J Neurosci Res 1996; 45: 558-570.
105. Zhang SC, Lipsitz D, Duncan ID. Self-renewing canine oligodendroglial progenitor expanded as oligospheres. J Neurosci Res 1998; 54: 181-190.
106. Zhang SC, Lundberg C, Lipsitz D, O'Connor LT, Duncan ID. Generation of oligodendroglial progenitors from neural stem cells. J Neurocytol 1998; 27: 475-489.
107. Hammang JP, Archer DR, Duncan ID. Myelination following transplantation of EGF-responsive neural stem cells into a myelin-deficient environment. Exp Neurol 1997; 147: 84-95.
108. Mothe AJ, Tator CH. Transplanted neural stem/progenitor cells generate myelinating oligodendrocytes and Schwann cells in spinal cord demyelination and dysmyelination. Exp Neurol 2008; 213: 176-190.
109. Brüstle O, Jones KN, Learish RD, et al. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science 1999; 285: 754-756.
110. Nistor GI, Totoiu MO, Haque N, Carpenter MK, Keirstead HS. Human embryonic stem cells differentiate into oligodendrocytes in high purity and myelinate after spinal cord transplantation. GLIA 2005; 49: 385-396.
111. Hu BY, Du ZW, Li XJ, Ayala M, Zhang SC. Human oligodendrocytes from embryonic stem cells: conserved SHH signaling networks and divergent FGF effects. Development 2009; 136: 1443-1452.
112. Koch P, Kokaia Z, Lindvall O, Brustle O. Emerging concepts in neural stem cell research: autologous repair and cell-based disease modelling. Lancet Neurol 2009; 8: 819-829.
113. Hu BY, Weick JP, Yu J, et al. Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proc Natl Acad Sci U S A 2010; 107: 4335-4340.
114. Zhao T, Zhang ZN, Rong Z, Xu Y. Immunogenicity of induced pluripotent stem cells. Nature 2011; 474: 212-215.
115. Windrem MS, Roy NS, Wang J, et al. Progenitor cells derived from the adult human subcortical white matter disperse and differentiate as oligodendrocytes within demyelinated lesions of the rat brain. J Neurosci Res 2002; 69: 966-975.
116. Zhang SC, Ge B, Duncan ID. Adult brain retains the potential to generate oligodendroglial progenitors with extensive myelination capacity. Proc Natl Acad Sci 1999; 96: 4089-4094.
117. Klugmann M, Schwab MH, Pühlhofer A, et al. Assembly of CNS myelin in the absence of proteolipid protein. Neuron 1997; 18: 59-70.
118. Boison D, Stoffel W. Disruption of the compacted myelin sheath of axons of the central nervous system in proteolipid protein-deficient mice. Proc Natl Acad Sci U S A 1994; 91: 11709-11713.
119. Windrem MS, Nunes MC, Rashbaum WK, et al. Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dysmyelinated brain. NatMed 2004; 10: 93-97.
120. Lee WC, Tsoi YK, Troendle FJ, et al. Single-dose intracerebroventricular administration of galactocerebrosidase improves survival in a mouse model of globoid cell leukodystrophy. Faseb J 2007; 21: 2520-2527.
121. Yeager A, Brennan S. Prolonged survival and remyelination after hematopoietic cell transplantation in the twitcher mouse. Science 1984; 225: 1052-1054.
122. Matzner U, Herbst E, Hedayati KK, et al. Enzyme replacement improves nervous system pathology and function in a mouse model for metachromatic leukodystrophy. Hum Mol Genet 2005; 14: 1139-1152.
123. Sevin C, Verot L, Benraiss A, et al. Partial cure of established disease in an animal model of metachromatic leukodystrophy after intracerebral adeno-associated virus-mediated gene transfer. Gene Ther 2007; 14: 405-414.
124. Matzner U, Hartmann D, Lullmann-Rauch R, et al. Bone marrow stem cell-based gene transfer in a mouse model for metachromatic leukodystrophy: effects on visceral and nervous system disease manifestations. Gene Ther 2002; 9: 53-63.
125. Lu JF, Lawler AM, Watkins PA, et al. A mouse model for X-linked adrenoleukodystrophy. Proc Natl Acad Sci U S A 1997; 94: 9366-9371.