Biotherapies in multiple sclerosis: A step toward remyelination and neuroprotection?

Revue Neurologique

Volumn 170, Issue 12, 2014, Pages 770-778

  Dubessy, A L ^a,b   Zujovic, V ^a,b   Papeix, C ^a,b   Stankoff, B ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b AP HP ^*  (France)

Author keywords

Lingo1; Multiple sclerosis; Nogo; Remyelination; Stem cells; Transplantation

Indexed keywords

ALEMTUZUMAB; DACLIZUMAB; HYALURONIC ACID; LINGO MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY; OCRELIZUMAB; PROTEIN NOGO; RITUXIMAB; UNCLASSIFIED DRUG; NEUROPROTECTIVE AGENT;

ARTICLE; BIOLOGICAL THERAPY; CELL THERAPY; DEMYELINATION; GRAY MATTER; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; MULTIPLE SCLEROSIS; NERVE CELL LESION; NERVE FIBER; NEUROPROTECTION; OLFACTORY ENSHEATHING CELL; OLIGODENDROGLIA; REMYELINIZATION; SCHWANN CELL; SIGNAL TRANSDUCTION; SOMATIC CELL; STEM CELL TRANSPLANTATION; WHITE MATTER; ANIMAL; DEMYELINATING DISEASES; MYELIN SHEATH; NERVE REGENERATION; PHYSIOLOGY; PROCEDURES;

ANIMALS; ANTIBODIES, MONOCLONAL; BIOLOGICAL THERAPY; DEMYELINATING DISEASES; HUMANS; MULTIPLE SCLEROSIS; MYELIN SHEATH; NERVE REGENERATION; NEUROPROTECTIVE AGENTS;

EID: 84920647269     PISSN: 00353787     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurol.2014.10.004     Document Type: Article

References (111)

1. Koch-Henriksen N, Sørensen PS. The changing demographic pattern of multiple sclerosis epidemiology. Lancet Neurol 2010;9(5):520-32.
2. Nave KA. Myelination and the trophic support of long axons. Nat Rev Neurosci 2010;11(4):275-83.
3. Fünfschilling U, Supplie LM, Mahad D, Boretius S, Saab AS, Edgar J, et al. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 2012;485(7399):517-21.
4. Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, Hoffman PN, et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 2012;487(7408):443-8.
5. Stadelmann C, Albert M, Wegner C, Brück W. Cortical pathology in multiple sclerosis. Curr Opin Neurol 2008;21(3):229-34.
6. Trapp BD, Nave KA. Multiple sclerosis: an immune or neurodegenerative disorder? Annu Rev Neurosci 2008;31:247-69.
7. Pirko I, Lucchinetti CF, Sriram S, Bakshi R. Gray matter involvement in multiple sclerosis. Neurology 2007;68(9):634-42.
8. Wiendl H, Gross CC. Modulation of IL-2Ra with daclizumab for treatment of multiple sclerosis. Nature Publishing Group 2013;9(7):394-404.
9. DJO MD, PPAC MD. Emerging injectable therapies for multiple sclerosis. Lancet Neurol 2013;12(11):1115-26.
10. Nave KA. Myelination and support of axonal integrity by glia. Nature 2010;468(7321):244-52.
11. Trapp BD, Ransohoff R, Rudick R. Axonal pathology in multiple sclerosis: relationship to neurologic disability. Curr Opin Neurol 1999;12(3):295-302.
12. Onuki M, Ayers MM, Bernard CC, Orian JM. Axonal degeneration is an early pathological feature in autoimmune-mediated demyelination in mice. Microsc Res Tech 2001;52(6):731-9.
13. Schwab ME, Caroni P. Oligodendrocytes and CNS myelin are nonpermissive substrates for neurite growth and fibroblast spreading in vitro. J Neurosci 1988;8(7): 2381-93.
14. Chen MS, Huber AB, van der Haar ME, Frank M, Schnell L, Spillmann AA, et al. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 2000;403(6768):434-9.
15. GrandPré T, Nakamura F, Vartanian T, Strittmatter SM. Identification of the Nogo inhibitor of axon regeneration as a reticulon protein. Nature 2000;403(6768):439-44.
16. Prinjha R, Moore SE, Vinson M, Blake S, Morrow R, Christie G, et al. Inhibitor of neurite outgrowth in humans. Nature 2000;403(6768):383-4.
17. Fournier AE, GrandPré T, Strittmatter SM. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 2001;409(6818):341-6.
18. Liu BP. Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor. Science 2002;297(5584):1190-3.
19. Oertle T, van der Haar ME, Bandtlow CE, Robeva A, Burfeind P, Buss A, et al. Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. J Neurosci 2003;23(13):5393-406.
20. Shao Z, Browning JL, Lee X, Scott ML, Shulga-Morskaya S, Allaire N, et al. TAJ/TROY, an orphan TNF receptor family member, binds Nogo-66 receptor 1 and regulates axonal regeneration. Neuron 2005;45(3):353-9.
21. Mi S, Lee X, Shao Z, Thill G, Ji B, Relton J, et al. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat Neurosci 2004;7(3):221-8.
22. Petratos S, Ozturk E, Azari MF, Kenny R, Young Lee J, Magee KA, et al. Limiting multiple sclerosis related axonopathy by blocking Nogo receptor and CRMP-2 phosphorylation. Brain 2012;135(6):1794-818.
23. Kempf A, Schwab ME. Nogo-A represses anatomical and synaptic plasticity in the central nervous system. Physiology (Bethesda) 2013;28(3):151-63.
24. McGee AW. Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor. Science 2005;309(5744):2222-6.
25. Delekate A, Zagrebelsky M, Kramer S, Schwab ME, Korte M. NogoA restricts synaptic plasticity in the adult hippocampus on a fast time scale. Proc Natl Acad Sci U S A 2011;108(6):2569-74.
26. Chong SYC, Rosenberg SS, Fancy SPJ, Shen YAA, Zhao C, Hahn AT, et al. Neurite outgrowth inhibitor Nogo-A establishes spatial segregation and extent of oligodendrocyte myelination. Proc Natl Acad Sci U S A 2012;109(4):1299-304.
27. Satoh JI, Onoue H, Arima K, Yamamura T. Nogo-A and nogo receptor expression in demyelinating lesions of multiple sclerosis. J Neuropathol Exp Neurol 2005;64(2):129-38.
28. Wang X, Baughman KW, Basso DM, Strittmatter SM. Delayed Nogo receptor therapy improves recovery from spinal cord contusion. Ann Neurol 2006;60(5): 540-9.
29. Karnezis T, Mandemakers W, McQualter JL, Zheng B, Ho PP, Jordan KA, et al. The neurite outgrowth inhibitor Nogo A is involved in autoimmune-mediated demyelination. Nat Neurosci 2004;7(7):736-44 [Internet]. Available from: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=15184901&retmode=ref&cmd= prlinks.
30. Zheng B, Ho C, Li S, Keirstead H, Steward O, Tessier-Lavigne M. Lack of enhanced spinal regeneration in Nogo-deficient mice. Neuron 2003;38(2):213-24.
31. Kim JE, Li S, GrandPré T, Qiu D, Strittmatter SM. Axon regeneration in young adult mice lacking Nogo-A/B. Neuron 2003;38(2):187-99.
32. Simonen M, Pedersen V, Weinmann O, Schnell L, Buss A, Ledermann B, et al. Systemic deletion of the myelin-associated outgrowth inhibitor Nogo-A improves regenerative and plastic responses after spinal cord injury. Neuron 2003;38(2):201-11.
33. Wang KC, Koprivica V, Kim JA, Sivasankaran R, Guo Y, Neve RL, et al. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 2002;417(6892):941-4.
34. Benson MD, Romero MI, Lush ME, Lu QR, Henkemeyer M, Parada LF. Ephrin-B3 is a myelin-based inhibitor of neurite outgrowth. Proc Natl Acad Sci U S A 2005;102(30): 10694-9.
35. Patrikios P, Stadelmann C, Kutzelnigg A, Rauschka H, Schmidbauer M, Laursen H, et al. Remyelination is extensive in a subset of multiple sclerosis patients. Brain 2006;129(Pt 12):3165-72.
36. Irvine KA, Blakemore WF. Remyelination protects axons from demyelination-associated axon degeneration. Brain 2008;131(Pt 6):1464-77.
37. Piaton G, Williams A, Seilhean D, Lubetzki C. Remyelination in multiple sclerosis. Prog Brain Res 2009;175:453-64.
38. Franklin RJM. Why does remyelination fail in multiple sclerosis? Nat Rev Neurosci 2002;3(9):705-14.
39. Piaton G, Aigrot MS, Williams A, Moyon S, Tepavcevic V, Moutkine I, et al. Class 3 semaphorins influence oligodendrocyte precursor recruitment and remyelination in adult central nervous system. Brain 2011;134(Pt 4): 1156-67.
40. Syed YA, Baer A, Hofer MP, Gonzá lez GA, Rundle J, Myrta S, et al. Inhibition of phosphodiesterase-4 promotes oligodendrocyte precursor cell differentiation and enhances CNS remyelination. EMBO Mol Med 2013;5(12):1918-34.
41. Back SA, Tuohy TMF, Chen H, Wallingford N, Craig A, Struve J, et al. Hyaluronan accumulates in demyelinated lesions and inhibits oligodendrocyte progenitor maturation. Nat Med 2005;11(9):966-72.
42. Bourikas D, Mir A, Walmsley AR. Molecular and cellular neuroscience. Mol Cell Neurosci 2010;45(4):363-9.
43. Jepson S, Vought B, Gross CH, Gan L, Austen D, Frantz JD, et al. LINGO-1, a transmembrane signaling protein, inhibits oligodendrocyte differentiation and myelination through intercellular self-interactions. J Biol Chem 2012;287(26):22184-95.
44. Zhao X-H, Jin W-L, Wu J, Mi S, Ju G. Inactivation of glycogen synthase kinase-3b and up-regulation of LINGO- 1 are involved in LINGO-1 antagonist regulated survival of cerebellar granular neurons. Cell Mol Neurobiol 2008;28(5):727-35.
45. Inoue H, Lin L, Lee X, Shao Z, Mendes S, Snodgrass-Belt P, et al. Inhibition of the leucine-rich repeat protein LINGO-1 enhances survival, structure, and function of dopaminergic neurons in Parkinson's disease models. Proc Natl Acad Sci U S A 2007;104(36):14430-5.
46. Ji B, Li M, Wu W-T, Yick L-W, Lee X, Shao Z, et al. LINGO-1 antagonist promotes functional recovery and axonal sprouting after spinal cord injury. Mol Cell Neurosci 2006;33(3):311-20.
47. Lv J, Xu R-X, Jiang X-D, Lu X, Ke Y-Q, Cai Y-Q, et al. Passive immunization with LINGO-1 polyclonal antiserum afforded neuroprotection and promoted functional recovery in a rat model of spinal cord injury. Neuroimmunomodulation 2010;17(4):270-8.
48. Fu QL, Hu B, Wu W, Pepinsky RB, Mi S, So KF. Blocking LINGO-1 function promotes retinal ganglion cell survival following ocular hypertension and optic nerve transection. Invest Ophthalmol Vis Sci 2008;49(3):975-85.
49. Mi S, Miller RH, Lee X, Scott ML, Shulag-Morskaya S, Shao Z, et al. LINGO-1 negatively regulates myelination by oligodendrocytes. Nat Neurosci 2005;8(6):745-51.
50. Mi S, Miller RH, Tang W, Lee X, Hu B, Wu W, et al. Promotion of central nervous system remyelination by induced differentiation of oligodendrocyte precursor cells. Ann Neurol 2009;65(3):304-15.
51. Mi S, Hu B, Hahm K, Luo Y, Kam Hui ES, Yuan Q, et al. LINGO-1 antagonist promotes spinal cord remyelination and axonal integrity in MOG-induced experimental autoimmune encephalomyelitis. Nat Med 2007;13(10):1228-33.
52. 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(6):325-34.
53. Groves AK, Barnett SC, Franklin RJ, Crang AJ, Mayer M, Blakemore WF, et al. Repair of demyelinated lesions by transplantation of purified O-2A progenitor cells. Nature 1993;362(6419):453-5.
54. Windrem MS, Schanz SJ, Guo M, Tian G-F, Washco V, Stanwood N, 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(6):553-65.
55. Rutkowski JL, Kirk CJ, Lerner MA, Tennekoon GI. Purification and expansion of human Schwann cells in vitro. Nat Med 1995;1(1):80-3.
56. Levi AD. Characterization of the technique involved in isolating Schwann cells from adult human peripheral nerve. J Neurosci Methods 1996;68(1):21-6.
57. Honmou O, Felts PA, Waxman SG, Kocsis JD. Restoration of normal conduction properties in demyelinated spinal cord axons in the adult rat by transplantation of exogenous Schwann cells. J Neurosci 1996;16(10):3199-208.
58. Duncan ID, Aguayo AJ, Bunge RP, Wood PM. Transplantation of rat Schwann cells grown in tissue culture into the mouse spinal cord. J Neurol Sci 1981;49(2):241-52.
59. Zujovic V, Doucerain C, Hidalgo A, Bachelin C, Lachapelle F, Weissert R, et al. Exogenous schwann cells migrate, remyelinate and promote clinical recovery in experimental auto-immune encephalomyelitis. PLoS ONE 2012;7(9):e42667.
60. Bachelin C, Lachapelle F, Girard C, Moissonnier P, Serguera-Lagache C, Mallet J, et al. Efficient myelin repair in the macaque spinal cord by autologous grafts of Schwann cells. Brain 2005;128(Pt 3):540-9.
61. Pluchino S, Furlan R, Martino G. Cell-based remyelinating therapies in multiple sclerosis: evidence from experimental studies. Curr Opin Neurol 2004;17(3):247-55.
62. Zujovic V, Bachelin C, Baron-Van Evercooren A. Remyelination of the central nervous system: a valuable contribution from the periphery. Neuroscientist 2007;13(4):383-91.
63. Grimpe B, Silver J. A novel DNA enzyme reduces glycosaminoglycan chains in the glial scar and allows microtransplanted dorsal root ganglia axons to regenerate beyond lesions in the spinal cord. J Neurosci 2004;24(6):1393-7.
64. Santos-Silva A, Fairless R, Frame MC, Montague P, Smith GM, Toft A, et al. FGF/heparin differentially regulatesSchwann cell and olfactory ensheathing cell interactions with astrocytes: a role in astrocytosis. J Neurosci 2007;27(27):7154-67.
65. Kaneko S, Iwanami A, Nakamura M, Kishino A, Kikuchi K, Shibata S, et al. A selective Sema3A inhibitor enhances regenerative responses and functional recovery of the injured spinal cord. Nat Med 2006;12(12):1380-9.
66. Bachelin C, Zujovic V, Buchet D, Mallet J, Baron-Van Evercooren A. 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 2010;133(Pt 2): 406-20.
67. Franklin RJ, Barnett SC. Olfactory ensheathing cells and CNS regeneration: the sweet smell of success? Neuron 2000;28(1):15-8.
68. Vincent AJ, West AK, Chuah MI. Morphological and functional plasticity of olfactory ensheathing cells. J Neurocytol 2005;34(1-2):65-80.
69. Lakatos A, Franklin RJ, Barnett SC. Olfactory ensheathing cells and Schwann cells differ in their in vitro interactions with astrocytes. Glia 2000;32(3):214-25.
70. Lakatos A, Barnett SC, Franklin RJM. Olfactory ensheathing cells induce less host astrocyte response and chondroitin sulphate proteoglycan expression than Schwann cells following transplantation into adult CNS white matter. Exp Neurol 2003;184(1):237-46.
71. Franklin RJ, Gilson JM, Franceschini IA, Barnett SC. Schwann cell-like myelination following transplantation of an olfactory bulb-ensheathing cell line into areas of demyelination in the adult CNS. Glia 1996;17(3):217-24.
72. Franklin RJM. Remyelination by transplanted olfactory ensheathing cells. Anat Rec B New Anat 2003;271(1):71-6.
73. Barnett SC, Alexander CL, Iwashita Y, Gilson JM, Crowther J, Clark L, et al. Identification of a human olfactory ensheathing cell that can effect transplant-mediated remyelination of demyelinated CNS axons. Brain 2000;123(Pt 8):1581-8.
74. Kato T, Honmou O, Uede T, Hashi K, Kocsis JD. Transplantation of human olfactory ensheathing cells elicits remyelination of demyelinated rat spinal cord. Glia 2000;30(3):209-18.
75. Smith PM, Lakatos A, Barnett SC, Jeffery ND, Franklin RJM. Cryopreserved cells isolated from the adult canine olfactory bulb are capable of extensive remyelination following transplantation into the adult rat CNS. Exp Neurol 2002;176(2):402-6.
76. Deng C, Gorrie C, Hayward I, Elston B, Venn M, Mackay-Sim A, et al. Survival and migration of human and rat olfactory ensheathing cells in intact and injured spinal cord. J Neurosci Res 2006;83(7):1201-12.
77. Radtke C, Aizer AA, Agulian SK, Lankford KL, Vogt PM, Kocsis JD. Transplantation of olfactory ensheathing cells enhances peripheral nerve regeneration after microsurgical nerve repair. Brain Res 2009;1254:10-7.
78. Jeffery ND, Lakatos A, Franklin RJM. Autologous olfactory glial cell transplantation is reliable and safe in naturally occurring canine spinal cord injury. J Neurotrauma 2005;22(11):1282-93.
79. Féron F, Perry C, Cochrane J, Licina P, Nowitzke A, Urquhart S, et al. Autologous olfactory ensheathing cell transplantation in human spinal cord injury. Brain 2005;128(Pt 12):2951-60.
80. Lima C, Pratas-Vital J, Escada P, Hasse-Ferreira A, Capucho C, Peduzzi JD. Olfactory mucosa autografts in human spinal cord injury: a pilot clinical study. J Spinal Cord Med 2006;29(3):191-203 [discussion 204-6].
81. Lima C, Escada P, Pratas-Vital J, Branco C, Arcangeli CA, Lazzeri G, et al. Olfactory mucosal autografts and rehabilitation for chronic traumatic spinal cord injury. Neurorehabil Neural Repair 2010;24(1):10-22.
82. Chhabra HS, Lima C, Sachdeva S, Mittal A, Nigam V, Chaturvedi D, et al. Autologous olfactory [corrected] mucosal transplant in chronic spinal cord injury: an Indian Pilot Study. Spinal Cord 2009;47(12):887-95.
83. Bianco JI, Perry C, Harkin DG, Mackay-Sim A, Féron F. Neurotrophin 3 promotes purification and proliferation of olfactory ensheathing cells from human nose. Glia 2004;45(2):111-23.
84. Féron F, Perry C, McGrath JJ, Mackay-Sim A. New techniques for biopsy and culture of human olfactory epithelial neurons. Arch Otolaryngol Head Neck Surg 1998;124(8):861-6.
85. Rubio M-P, Muñoz-Quiles C, Ramón-Cueto A. Adult olfactory bulbs from primates provide reliable ensheathing glia for cell therapy. Glia 2008;56(5): 539-51.
86. Kriegstein A, Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 2009;32:149-84.
87. Gage FH. Mammalian neural stem cells. Science 2000;287(5457):1433-8.
88. Temple S. Stem cell plasticity - building the brain of our dreams. Nat Rev Neurosci 2001;2(7):513-20.
89. 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(Pt 4):1168-83.
90. Zhang SC, Ge B, Duncan ID. Adult brain retains the potential to generate oligodendroglial progenitors with extensive myelination capacity. Proc Natl Acad Sci U S A 1999;96(7):4089-94.
91. Vitry S, Avellana-Adalid V, Lachapelle F, Baron-Van Evercooren A. Migration and multipotentiality of PSA-NCAM+ neural precursors transplanted in the developing brain. Mol Cell Neurosci 2001;17(6):983-1000.
92. Ben-Hur T, Einstein O, Mizrachi-Kol R, Ben-Menachem O, Reinhartz E, Karussis D, et al. Transplanted multipotential neural precursor cells migrate into the inflamed white matter in response to experimental autoimmune encephalomyelitis. Glia 2003;41(1):73-80.
93. Uchida N, Chen K, Dohse M, Hansen KD, Dean J, Buser JR, et al. Human neural stem cells induce functional myelination in mice with severe dysmyelination. Sci Transl Med 2012;4(155):155ra136.
94. Maire CL, Buchet D, Kerninon C, Deboux C, Baron-Van Evercooren A, Nait-Oumesmar B. Directing human neural stem/precursor cells into oligodendrocytes by overexpression of Olig2 transcription factor. J Neurosci Res 2009;87(15):3438-46.
95. Gupta N, Henry RG, Strober J, Kang SM, Lim DA, Bucci M, et al. Neural stem cell engraftment and myelination in the human brain. Sci Transl Med 2012;4(155):155ra137.
96. Amoh Y, Li L, Campillo R, Kawahara K, Katsuoka K, Penman S, et al. Implanted hair follicle stem cells form Schwann cells that support repair of severed peripheral nerves. Proc Natl Acad Sci U S A 2005;102(49):17734-8.
97. McKenzie IA, Biernaskie J, Toma JG, Midha R, Miller FD. Skin-derived precursors generate myelinating Schwann cells for the injured and dysmyelinated nervous system. J Neurosci 2006;26(24):6651-60.
98. Biernaskie J, Sparling JS, Liu J, Shannon CP, Plemel JR, Xie Y, et al. Skin-derived precursors generate myelinating Schwann cells that promote remyelination and functional recovery after contusion spinal cord injury. J Neurosci 2007;27(36):9545-59.
99. Hunt DPJ, Morris PN, Sterling J, Anderson JA, Joannides A, Jahoda C, et al. A highly enriched niche of precursor cellswith neuronal and glial potential within the hair follicle dermal papilla of adult skin. Stem Cells 2008;26(1):163-72.
100. Pluchino S, Quattrini A, Brambilla E, Gritti A, Salani G, Dina G, et al. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 2003;422(6933):688-94.
101. Pluchino S, Zanotti L, Rossi B, Brambilla E, Ottoboni L, Salani G, et al. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 2005;436(7048):266-71.
102. Atkins HL, Freedman MS. Hematopoietic stem cell therapy for multiple sclerosis: top 10 lessons learned. Neurotherapeutics 2013;10(1):68-76.
103. Karussis D, Petrou P, Vourka-Karussis U, Kassis I. Hematopoietic stem cell transplantation in multiple sclerosis. Expert Rev Neurother 2013;13(5):567-78.
104. Burman J, Iacobaeus E, Svenningsson A, Lycke J, Gunnarsson M, Nilsson P, et al. Autologous haematopoietic stem cell transplantation for aggressive multiple sclerosis: the Swedish experience. J Neurol Neurosurg Psychiatr 2014;85(10):1116-21.
105. Kassis I, Grigoriadis N, Gowda-Kurkalli B, Mizrachi-Kol R, Ben-Hur T, Slavin S, et al. Neuroprotection and immunomodulation with mesenchymal stem cells in chronic experimental autoimmune encephalomyelitis. Arch Neurol 2008;65(6):753-61.
106. Uccelli A, Laroni A, Freedman MS. Mesenchymal stem cells for the treatment of multiple sclerosis and other neurological diseases. Lancet Neurol 2011;10(7):649-56.
107. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126(4):663-76.
108. Wang S, Bates J, Li X, Schanz S, Chandler-Militello D, Levine C, et al. Human iPSC-derived oligodendrocyte progenitor cells can myelinate and rescue a mouse model of congenital hypomyelination. Cell Stem Cell 2013;12(2):252-64.
109. Wang A, Tang Z, Park IH, Zhu Y, Patel S, Daley GQ, et al. Induced pluripotent stem cells for neural tissue engineering. Biomaterials 2011;32(22):5023-32.
110. Yang N, Zuchero JB, Ahlenius H, Marro S, Ng YH, Vierbuchen T, et al. Generation of oligodendroglial cells by direct lineage conversion. Nat Biotechnol 2013;31(5): 434-9.
111. Najm FJ, Lager AM, Zaremba A, Wyatt K, Caprariello AV, Factor DC, et al. Transcription factor-mediated reprogramming of fibroblasts to expandable, myelinogenic oligodendrocyte progenitor cells. Nat Biotechnol 2013;31(5):426-33.