Strategies for protecting oligodendrocytes and enhancing remyelination in multiple sclerosis

Discovery Medicine

Volumn 16, Issue 86, 2013, Pages 53-63

  Rodgers, Jane M ^a   Robinson, Andrew P ^a   Miller, Stephen D ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMILORIDE; ATORVASTATIN; BETA CATENIN; BETA INTERFERON; BETA1A INTERFERON; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CASPASE; CASPASE INHIBITOR; FINGOLIMOD; FUMARIC ACID DIMETHYL ESTER; GAMMA SECRETASE INHIBITOR; GLATIRAMER; INTERFERON BETA SERINE; LINGO 1; MINOCYCLINE; MITOXANTRONE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY GNBAC1; MYELIN; NATALIZUMAB; NOTCH RECEPTOR; NOVATRONE; RECOMBINANT IMMUNOGLOBULIN M ANTIBODY; RETINOID X RECEPTOR GAMMA; TACROLIMUS; UNCLASSIFIED DRUG; UNINDEXED DRUG; WIN212 2; WIN55; WNT PROTEIN;

ARTICLE; CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM FUNCTION; CEREBROVASCULAR ACCIDENT; DEMYELINATING DISEASE; DEMYELINATION; DRUG EFFECT; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; IMMUNOMODULATION; MULTIPLE SCLEROSIS; MYELIN SHEATH; NEURAL STEM CELL; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PHASE 1 CLINICAL TRIAL; PHASE 2 CLINICAL TRIAL; PHYSIOLOGY; REGENERATION; REMYELINIZATION; STEM CELL TRANSPLANTATION;

EID: 84886261529     PISSN: 15396509     EISSN: 19447930     Source Type: Journal    
DOI: None     Document Type: Article

References (122)

1. Alberts AW. Discovery, biochemistry and biology of lovastatin. Am J Cardiol 62(15):10J-15J, 1988.
2. Arevalo-Martin A, Garcia-Ovejero D, Gomez O, Rubio-Araiz A, Navarro-Galve B, Guaza C, Molina-Holgado E, Molina-Holgado F. CB2 cannabinoid receptors as an emerging target for demyelinating diseases: from neuroimmune interactions to cell replacement strategies. Br J Pharmacol 153(2):216-225, 2008.
3. Asakura K, Miller DJ, Pease LR, Rodriguez M. Targeting of IgMkappa antibodies to oligodendrocytes promotes CNS remyelination. J Neurosci 18(19):7700-7708, 1998.
4. Ballanger F, Nguyen JM, Khammari A, Dreno B. Evolution of clinical and molecular responses to bexarotene treatment in cutaneous T-cell lymphoma. Dermatology 220(4):370-375, 2010.
5. Bieber AJ, Warrington A, Asakura K, Ciric B, Kaveri SV, Pease LR, Rodriguez M. Human antibodies accelerate the rate of remyelination following lysolecithin-induced demyelination in mice. Glia 37(3):241-249, 2002.
6. Blakemore WF, Chari DM, Gilson JM, Crang AJ. Modelling large areas of demyelination in the rat reveals the potential and possible limitations of transplanted glial cells for remyelination in the CNS. Glia 38(2):155-168, 2002.
7. Brundula V, Rewcastle NB, Metz LM, Bernard CC, Yong VW. Targeting leukocyte MMPs and transmigration: minocycline as a potential therapy for multiple sclerosis. Brain 125(Pt 6):1297-1308, 2002.
8. Chu K, Kim M, Chae SH, Jeong SW, Kang KS, Jung KH, Kim J, Kim YJ, Kang L, Kim SU, Yoon BW. Distribution and in situ proliferation patterns of intravenously injected immortalized human neural stem-like cells in rats with focal cerebral ischemia. Neurosci Res 50(4):459-465, 2004.
9. Compston A. The basis for treatment in multiple sclerosis. Acta Neurol Scand Suppl 183:41-47, 2006.
10. Connick P, Kolappan M, Crawley C, Webber DJ, Patani R, Michell AW, Du MQ, Luan SL, Altmann DR, Thompson AJ, Compston A, Scott MA, Miller DH, Chandran S. Autologous mesenchymal stem cells for the treatment of secondary progressive multiple sclerosis: an open-label phase 2a proof-of-concept study. Lancet Neurol 11(2):150-156, 2012.
11. Craighead MW, Tiwari P, Keynes RG, Waters CM. Human oligodendroglial cell line, MO3.13, can be protected from apoptosis using the general caspase inhibitor zVAD-FMK. J Neurosci Res 57(2):236-243, 1999.
12. Crockett DP, Burshteyn M, Garcia C, Muggironi M, Casaccia-Bonnefil P. Number of oligodendrocyte progenitors recruited to the lesioned spinal cord is modulated by the levels of the cell cycle regulatory protein p27Kip-1. Glia 49(2):301-308, 2005.
13. Croxford JL, Miller SD. Towards cannabis and cannabinoid treatment of multiple sclerosis. Drugs Today (Barc) 40(8):663-676, 2004.
14. Croxford JL, Pryce G, Jackson SJ, Ledent C, Giovannoni G, Pertwee RG, Yamamura T, Baker D. Cannabinoid-mediated neuroprotection, not immunosuppression, may be more relevant to multiple sclerosis. J Neuroimmunol 193(1-2):120-129, 2008.
15. Curtin F, Lang AB, Perron H, Laumonier M, Vidal V, Porchet HC, Hartung HP. GNbAC1, a humanized monoclonal antibody against the envelope protein of multiple sclerosis-associated endogenous retrovirus: a first-in-humans randomized clinical study. Clin Ther 34(12):2268-2278, 2012.
16. Czepiel M, Balasubramaniyan V, Schaafsma W, Stancic M, Mikkers H, Huisman C, Boddeke E, Copray S. Differentiation of induced pluripotent stem cells into functional oligodendrocytes. Glia 59(6):882-892, 2011.
17. Das A, Guyton MK, Butler JT, Ray SK, Banik NL. Activation of calpain and caspase pathways in demyelination and neurodegeneration in animal model of multiple sclerosis. CNS Neurol Disord Drug Targets 7(3):313-320, 2008.
18. Derwenskus J. Current disease-modifying treatment of multiple sclerosis. Mt Sinai J Med 78(2):161-175, 2011.
19. Dery MA, Rousseau G, Benderdour M, Beaumont E. Atorvastatin prevents early apoptosis after thoracic spinal cord contusion injury and promotes locomotion recovery. Neurosci Lett 453(1):73-76, 2009.
20. Diab A, Hussain RZ, Lovett-Racke AE, Chavis JA, Drew PD, Racke MK. Ligands for the peroxisome proliferator-activated receptor-gamma and the retinoid X receptor exert additive anti-inflammatory effects on experimental autoimmune encephalomyelitis. J Neuroimmunol 148(1-2):116-126, 2004.
21. Duncan ID, Goldman S, Macklin WB, Rao M, Weiner LP, Reingold SC. Stem cell therapy in multiple sclerosis: promise and controversy. Mult Scler 14(4):541-546, 2008.
22. Einstein O, Karussis D, Grigoriadis N, Mizrachi-Kol R, Reinhartz E, Abramsky O, Ben-Hur T. Intraventricular transplantation of neural precursor cell spheres attenuates acute experimental allergic encephalomyelitis. Mol Cell Neurosci 24(4):1074-1082, 2003.
23. 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 23(13):1571-1585, 2009.
24. 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 14(8):1009-1016, 2011.
25. Feigenson K, Reid M, See J, Crenshaw EB, 3rd, Grinspan JB. Wnt signaling is sufficient to perturb oligodendrocyte maturation. Mol Cell Neurosci 42(3):255-265, 2009.
26. Feldman DH, Horiuchi M, Keachie K, Mccauley E, Bannerman P, Itoh A, Itoh T, Pleasure D. Characterization of acid-sensing ion channel expression in oligodendrocyte-lineage cells. Glia 56(11):1238-1249, 2008.
27. Firouzi R, Rolland A, Michel M, Jouvin-Marche E, Hauw JJ, Malcus-Vocanson C, Lazarini F, Gebuhrer L, Seigneurin JM, Touraine JL, Sanhadji K, Marche PN, Perron H. Multiple sclerosis-associated retrovirus particles cause T lymphocyte-dependent death with brain hemorrhage in humanized SCID mice model. J Neurovirol 9(1):79-93, 2003.
28. Fleisher AS, Raman R, Siemers ER, Becerra L, Clark CM, Dean RA, Farlow MR, Galvin JE, Peskind ER, Quinn JF, Sherzai A, Sowell BB, Aisen PS, Thal LJ. Phase 2 safety trial targeting amyloid beta production with a gamma-secretase inhibitor in Alzheimer disease. Arch Neurol 65(8):1031-1038, 2008.
29. Foote AK, Blakemore WF. Inflammation stimulates remyelination in areas of chronic demyelination. Brain 128(Pt 3):528-539, 2005.
30. Franklin RJ. Why does remyelination fail in multiple sclerosis? Nat Rev Neurosci 3(9):705-714, 2002.
31. Franklin RJ, Ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 9 (11):839-855, 2010.
32. Franklin RJ, Ffrench-Constant C. Stem cell treatments and multiple sclerosis. BMJ 340:c1387, 2010.
33. Franklin RJ, Kotter MR. The biology of CNS remyelination: the key to therapeutic advances. J Neurol 255 Suppl 1:19-25, 2008.
34. Freedman MS, Bar-Or A, Atkins HL, Karussis D, Frassoni F, Lazarus H, Scolding N, Slavin S, Le Blanc K, Uccelli A. The therapeutic potential of mesenchymal stem cell transplantation as a treatment for multiple sclerosis: consensus report of the International MSCT Study Group. Mult Scler 16(4):503-510, 2010.
35. Friese MA, Craner MJ, Etzensperger R, Vergo S, Wemmie JA, Welsh MJ, Vincent A, Fugger L. Acid-sensing ion channel-1 contributes to axonal degeneration in autoimmune inflammation of the central nervous system. Nat Med 13(12):1483-1489, 2007.
36. Galiegue S, Mary S, Marchand J, Dussossoy D, Carriere D, Carayon P, Bouaboula M, Shire D, Le Fur G, Casellas P. Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. Eur J Biochem 232(1):54-61, 1995.
37. Garay L, Deniselle MC, Lima A, Roig P, De Nicola AF. Effects of progesterone in the spinal cord of a mouse model of multiple sclerosis. J Steroid Biochem Mol Biol 107(3-5):228-237, 2007.
38. Garay L, Tungler V, Deniselle MC, Lima A, Roig P, De Nicola AF. Progesterone attenuates demyelination and microglial reaction in the lysolecithin-injured spinal cord. Neuroscience 192:588-597, 2011.
39. Garay LI, Gonzalez Deniselle MC, Brocca ME, Lima A, Roig P, De Nicola AF. Progesterone down-regulates spinal cord inflammatory mediators and increases myelination in experimental autoimmune encephalomyelitis. Neuroscience 226:40-50, 2012.
40. Garcia PJ. Pleiotropic effects of statins: moving beyond cholesterol control. Curr Atheroscler Rep 7(1):34-39, 2005.
41. Gensert JM, Goldman JE. Endogenous progenitors remyelinate demyelinated axons in the adult CNS. Neuron 19(1):197-203, 1997.
42. Getts DR, Martin AJ, Mccarthy DP, Terry RL, Hunter ZN, Yap WT, Getts MT, Pleiss M, Luo X, King NJ, Shea LD, Miller SD. Microparticles bearing encephalitogenic peptides induce T-cell tolerance and ameliorate experimental autoimmune encephalomyelitis. Nat Biotechnol 31(6):565, 2013.
43. Getts DR, Turley DM, Smith CE, Harp CT, Mccarthy D, Feeney EM, Getts MT, Martin AJ, Luo X, Terry RL, King NJ, Miller SD. Tolerance induced by apoptotic antigen-coupled leukocytes is induced by PD-L1+ and IL-10-producing splenic macrophages and maintained by T regulatory cells. J Immunol 187(5):2405-2417, 2011.
44. Gold BG, Voda J, Yu X, Mckeon G, Bourdette DN. FK506 and a nonimmunosuppressant derivative reduce axonal and myelin damage in experimental autoimmune encephalomyelitis: neuroimmunophilin ligand-mediated neuroprotection in a model of multiple sclerosis. J Neurosci Res 77(3):367-377, 2004.
45. Gomez O, Arevalo-Martin A, Garcia-Ovejero D, Ortega-Gutierrez S, Cisneros JA, Almazan G, Sanchez-Rodriguez MA, Molina-Holgado F, Molina-Holgado E. The constitutive production of the endocannabinoid 2-arachidonoylglycerol participates in oligodendrocyte differentiation. Glia 58(16):1913-1927, 2010.
46. Gomez O, Sanchez-Rodriguez A, Le M, Sanchez-Caro C, Molina-Holgado F, Molina-Holgado E. Cannabinoid receptor agonists modulate oligodendrocyte differentiation by activating PI3K/Akt and the mammalian target of rapamycin (mTOR) pathways. Br J Pharmacol 163(7):1520-1532, 2011.
47. Hu BY, Du ZW, Zhang SC. Differentiation of human oligodendrocytes from pluripotent stem cells. Nat Protoc 4(11):1614-1622, 2009.
48. Huang JK, Franklin RJ. Current status of myelin replacement therapies in multiple sclerosis. Prog Brain Res 201:219-231, 2012.
49. Huang JK, Jarjour AA, Ffrench-Constant C, Franklin RJ. Retinoid X receptors as a potential avenue for regenerative medicine in multiple sclerosis. Expert Rev Neurother 11(4):467-468, 2011a.
50. Huang JK, Jarjour AA, Nait Oumesmar B, Kerninon C, Williams A, Krezel W, Kagechika H, Bauer J, Zhao C, Baron-Van Evercooren A, Chambon P, Ffrench-Constant C, Franklin RJ. Retinoid X receptor gamma signaling accelerates CNS remyelination. Nat Neurosci 14(1):45-53, 2011b.
51. John GR, Shankar SL, Shafit-Zagardo B, Massimi A, Lee SC, Raine CS, Brosnan CF. Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nat Med 8(10):1115-1121, 2002.
52. Jones SA, Jolson DM, Cuta KK, Mariash CN, Anderson GW. Triiodothyronine is a survival factor for developing oligodendrocytes. Mol Cell Endocrinol 199(1-2):49-60, 2003.
53. 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 170(1-2):3-10, 2005.
54. Jurynczyk M, Selmaj K. Notch: a new player in MS mechanisms. J Neuroimmunol 218(1-2):3-11, 2010.
55. Keirstead HS, Blakemore WF. Identification of post-mitotic oligodendrocytes incapable of remyelination within the demyelinated adult spinal cord. J Neuropathol Exp Neurol 56(11):1191-1201, 1997.
56. Kim HS, Suh YH. Minocycline and neurodegenerative diseases. Behav Brain Res 196(2):168-179, 2009.
57. Klein NC, Cunha BA. Tetracyclines. Med Clin North Am 79(4):789-801, 1995.
58. Kloppenburg M, Brinkman BM, De Rooij-Dijk HH, Miltenburg AM, Daha MR, Breedveld FC, Dijkmans BA, Verweij C. The tetracycline derivative minocycline differentially affects cytokine production by monocytes and T lymphocytes. Antimicrob Agents Chemother 40(4):934-940, 1996.
59. Kornek B, Storch MK, Weissert R, Wallstroem E, Stefferl A, Olsson T, Linington C, Schmidbauer M, Lassmann H. Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative quantitative study of axonal injury in active, inactive, and remyelinated lesions. Am J Pathol 157(1):267-276, 2000.
60. Kotter MR, Li WW, Zhao C, Franklin RJ. Myelin impairs CNS remyelination by inhibiting oligodendrocyte precursor cell differentiation. J Neurosci 26(1):328-332, 2006.
61. Kuhlmann T, Miron V, Cui Q, Wegner C, Antel J, Bruck W. Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 131(Pt 7):1749-1758, 2008.
62. Lajtha A, Toth J, Fujimoto K, Agrawal HC. Turnover of myelin proteins in mouse brain in vivo. Biochem J 164(2):323-329, 1977.
63. Lalive PH, Neuhaus O, Benkhoucha M, Burger D, Hohlfeld R, Zamvil SS, Weber MS. Glatiramer acetate in the treatment of multiple sclerosis: emerging concepts regarding its mechanism of action. CNS Drugs 25(5):401-414, 2011.
64. Liu J, Farmer JD, Jr., Lane WS, Friedman J, Weissman I, Schreiber SL. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66(4):807-815, 1991.
65. Liu Y, Jiang P, Deng W. OLIG gene targeting in human pluripotent stem cells for motor neuron and oligodendrocyte differentiation. Nat Protoc 6(5):640-655, 2011.
66. Luccarini I, Ballerini C, Biagioli T, Biamonte F, Bellucci A, Rosi MC, Grossi C, Massacesi L, Casamenti F. Combined treatment with atorvastatin and minocycline suppresses severity of EAE. Exp Neurol 211(1):214-226, 2008.
67. Lucchinetti C, Bruck W, Parisi J, Scheithauer B, Rodriguez M, Lassmann H. A quantitative analysis of oligodendrocytes in multiple sclerosis lesions. A study of 113 cases. Brain 122 ( Pt 12):2279-2295, 1999.
68. Lutterotti A, Yousef S, Sputtek A, Sturner KH, Stellmann JP, Breiden P, Reinhardt S, Schulze C, Bester M, Heesen C, Schippling S, Miller SD, Sospedra M, Martin R. Antigen-specific tolerance by autologous myelin Peptide-coupled cells: a phase 1 trial in multiple sclerosis. Sci Transl Med 5(188):188ra175, 2013.
69. Mahad D, Lassmann H, Turnbull D. Review: Mitochondria and disease progression in multiple sclerosis. Neuropathol Appl Neurobiol 34(6):577-589, 2008.
70. Maresz K, Pryce G, Ponomarev ED, Marsicano G, Croxford JL, Shriver LP, Ledent C, Cheng X, Carrier EJ, Mann MK, Giovannoni G, Pertwee RG, Yamamura T, Buckley NE, Hillard CJ, Lutz B, Baker D, Dittel BN. Direct suppression of CNS autoimmune inflammation via the cannabinoid receptor CB1 on neurons and CB2 on autoreactive T cells. Nat Med 13(4):492-497, 2007.
71. Mecha M, Torrao AS, Mestre L, Carrillo-Salinas FJ, Mechoulam R, Guaza C. Cannabidiol protects oligodendrocyte progenitor cells from inflammation-induced apoptosis by attenuating endoplasmic reticulum stress. Cell Death Dis 3:e331, 2012.
72. Metz LM, Li D, Traboulsee A, Myles ML, Duquette P, Godin J, Constantin M, Yong VW. Glatiramer acetate in combination with minocycline in patients with relapsing-remitting multiple sclerosis: results of a Canadian, multicenter, double-blind, placebo-controlled trial. Mult Scler 15(10):1183-1194, 2009.
73. Metz LM, Zhang Y, Yeung M, Patry DG, Bell RB, Stoian CA, Yong VW, Patten SB, Duquette P, Antel JP, Mitchell JR. Minocycline reduces gadolinium-enhancing magnetic resonance imaging lesions in multiple sclerosis. Ann Neurol 55(5):756, 2004.
74. 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 8(6):745-751, 2005.
75. Mi S, Miller RH, Tang W, Lee X, Hu B, Wu W, Zhang Y, Shields CB, Miklasz S, Shea D, Mason J, Franklin RJ, Ji B, Shao Z, Chedotal A, Bernard F, Roulois A, Xu J, Jung V, Pepinsky B. Promotion of central nervous system remyelination by induced differentiation of oligodendrocyte precursor cells. Ann Neurol 65(3):304-315, 2009.
76. Mi S, Sandrock A, Miller RH. LINGO-1 and its role in CNS repair. Int J Biochem Cell Biol 40(10):1971-1978, 2008.
77. Miller DJ, Njenga MK, Murray PD, Leibowitz J, Rodriguez M. A monoclonal natural autoantibody that promotes remyelination suppresses central nervous system inflammation and increases virus expression after Theiler's virus-induced demyelination. Int Immunol 8(1):131-141, 1996.
78. Miron VE, Kuhlmann T, Antel JP. Cells of the oligodendroglial lineage, myelination, and remyelination. Biochim Biophys Acta 1812(2):184-193, 2011.
79. Mokhtarian F, Safavi F, Sarafraz-Yazdi E. Immunization with a peptide of Semliki Forest virus promotes remyelination in experimental autoimmune encephalomyelitis. Brain Res 1488:92-103, 2012.
80. Molina-Holgado E, Vela JM, Arevalo-Martin A, Almazan G, Molina-Holgado F, Borrell J, Guaza C. Cannabinoids promote oligodendrocyte progenitor survival: involvement of cannabinoid receptors and phosphatidylinositol-3 kinase/Akt signaling. J Neurosci 22(22):9742-9753, 2002.
81. Munoz JR, Stoutenger BR, Robinson AP, Spees JL, Prockop DJ. Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc Natl Acad Sci U S A 102(50):18171-18176, 2005.
82. Najm FJ, Lager AM, Zaremba A, Wyatt K, Caprariello AV, Factor DC, Karl RT, Maeda T, Miller RH, Tesar PJ. Transcription factor-mediated reprogramming of fibroblasts to expandable, myelinogenic oligodendrocyte progenitor cells. Nat Biotechnol 31(5):426-433, 2013.
83. Najm FJ, Zaremba A, Caprariello AV, Nayak S, Freundt EC, Scacheri PC, Miller RH, Tesar PJ. Rapid and robust generation of functional oligodendrocyte progenitor cells from epiblast stem cells. Nat Methods 8(11):957-962, 2011.
84. Nottingham S, Knapp P, Springer J. FK506 treatment inhibits caspase-3 activation and promotes oligodendroglial survival following traumatic spinal cord injury. Exp Neurol 177(1):242-251, 2002.
85. Pannu R, Barbosa E, Singh AK, Singh I. Attenuation of acute inflammatory response by atorvastatin after spinal cord injury in rats. J Neurosci Res 79(3):340-350, 2005.
86. Paul F, Waiczies S, Wuerfel J, Bellmann-Strobl J, Dorr J, Waiczies H, Haertle M, Wernecke KD, Volk HD, Aktas O, Zipp F. Oral high-dose atorvastatin treatment in relapsing-remitting multiple sclerosis. PLoS One 3(4):e1928, 2008.
87. Perron H, Garson JA, Bedin F, Beseme F, Paranhos-Baccala G, Komurian-Pradel F, Mallet F, Tuke PW, Voisset C, Blond JL, Lalande B, Seigneurin JM, Mandrand B. Molecular identification of a novel retrovirus repeatedly isolated from patients with multiple sclerosis. The Collaborative Research Group on Multiple Sclerosis. Proc Natl Acad Sci U S A 94(14):7583-7588, 1997.
88. Pluchino S, Martino G. The therapeutic plasticity of neural stem/precursor cells in multiple sclerosis. J Neurol Sci 265(1-2):105-110, 2008.
89. Pluchino S, Quattrini A, Brambilla E, Gritti A, Salani G, Dina G, Galli R, Del Carro U, Amadio S, Bergami A, Furlan R, Comi G, Vescovi AL, Martino G. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422(6933):688-694, 2003.
90. Pohl HB, Porcheri C, Mueggler T, Bachmann LC, Martino G, Riethmacher D, Franklin RJ, Rudin M, Suter U. Genetically induced adult oligodendrocyte cell death is associated with poor myelin clearance, reduced remyelination, and axonal damage. J Neurosci 31(3):1069-1080, 2011.
91. Popovic N, Schubart A, Goetz BD, Zhang SC, Linington C, Duncan ID. Inhibition of autoimmune encephalomyelitis by a tetracycline. Ann Neurol 51(2):215-223, 2002.
92. Prineas JW, Barnard RO, Kwon EE, Sharer LR, Cho ES. Multiple sclerosis: remyelination of nascent lesions. Ann Neurol 33(2):137-151, 1993.
93. Prineas JW, Kwon EE, Cho ES, Sharer LR. Continual breakdown and regeneration of myelin in progressive multiple sclerosis plaques. Ann N Y Acad Sci 436:11-32, 1984.
94. Raine CS, Wu E. Multiple sclerosis: remyelination in acute lesions. J Neuropathol Exp Neurol 52(3):199-204, 1993.
95. Reynolds BA, Rietze RL. Neural stem cells and neurospheres-re-evaluating the relationship. Nat Methods 2(5):333-336, 2005.
96. Robinson AP, Foraker JE, Ylostalo J, Prockop DJ. Human stem/progenitor cells from bone marrow enhance glial differentiation of rat neural stem cells: a role for transforming growth factor beta and Notch signaling. Stem Cells Dev 20(2):289-300, 2011.
97. Rodriguez M, Miller DJ, Lennon VA. Immunoglobulins reactive with myelin basic protein promote CNS remyelination. Neurology 46(2):538-545, 1996.
98. Rudick RA, Mi S, Sandrock AW, Jr. LINGO-1 antagonists as therapy for multiple sclerosis: in vitro and in vivo evidence. Expert Opin Biol Ther 8(10):1561-1570, 2008.
99. Ruggieri M, Pica C, Lia A, Zimatore GB, Modesto M, Di Liddo E, Specchio LM, Livrea P, Trojano M, Avolio C. Combination treatment of Glatiramer Acetate and Minocycline affects phenotype expression of blood monocyte-derived dendritic cells in Multiple Sclerosis patients. J Neuroimmunol 197(2):140-146, 2008.
100. Safavi F, Feliberti JP, Raine CS, Mokhtarian F. Role of gammadelta T cells in antibody production and recovery from SFV demyelinating disease. J Neuroimmunol 235(1-2):18-26, 2011.
101. Setzu A, Lathia JD, Zhao C, Wells K, Rao MS, Ffrench-Constant C, Franklin RJ. Inflammation stimulates myelination by transplanted oligodendrocyte precursor cells. Glia 54(4):297-303, 2006.
102. Sim FJ, Zhao C, Penderis J, Franklin RJ. The age-related decrease in CNS remyelination efficiency is attributable to an impairment of both oligodendrocyte progenitor recruitment and differentiation. J Neurosci 22(7):2451-2459, 2002.
103. Solbrig MV, Fan Y, Hermanowicz N, Morgese MG, Giuffrida A. A synthetic cannabinoid agonist promotes oligodendrogliogenesis during viral encephalitis in rats. Exp Neurol 226(1):231-241, 2010.
104. Stidworthy MF, Genoud S, Li WW, Leone DP, Mantei N, Suter U, Franklin RJ. Notch1 and Jagged1 are expressed after CNS demyelination, but are not a major rate-determining factor during remyelination. Brain 127(Pt 9):1928-1941, 2004.
105. Uccelli A, Laroni A, Freedman MS. Mesenchymal stem cells for the treatment of multiple sclerosis and other neurological diseases. Lancet Neurol 10(7):649-656, 2011.
106. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol 8(9):726-736, 2008.
107. Van De Loosdrecht AA, Ossenkoppele GJ, Beelen RH, Broekhoven MG, Drager AM, Langenhuijsen MM. Apoptosis in tumor necrosis factor-alpha-dependent, monocyte-mediated leukemic cell death: a functional, morphologic, and flow-cytometric analysis. Exp Hematol 21(13):1628-1639, 1993.
108. Vergo S, Craner MJ, Etzensperger R, Attfield K, Friese MA, Newcombe J, Esiri M, Fugger L. Acid-sensing ion channel 1 is involved in both axonal injury and demyelination in multiple sclerosis and its animal model. Brain 134(Pt 2):571-584, 2011.
109. Vukusic S, Confavreux C. Pregnancy and multiple sclerosis: the children of PRIMS. Clin Neurol Neurosurg 108(3):266-270, 2006.
110. Wang S, Bates J, Li X, Schanz S, Chandler-Militello D, Levine C, Maherali N, Studer L, Hochedlinger K, Windrem M, Goldman SA. Human iPSC-derived oligodendrocyte progenitor cells can myelinate and rescue a mouse model of congenital hypomyelination. Cell Stem Cell 12(2):252-264, 2013.
111. Warrington AE, Asakura K, Bieber AJ, Ciric B, Van Keulen V, Kaveri SV, Kyle RA, Pease LR, Rodriguez M. Human monoclonal antibodies reactive to oligodendrocytes promote remyelination in a model of multiple sclerosis. Proc Natl Acad Sci U S A 97(12):6820-6825, 2000.
112. Warrington AE, Bieber AJ, Ciric B, Pease LR, Van Keulen V, Rodriguez M. A recombinant human IgM promotes myelin repair after a single, very low dose. J Neurosci Res 85(5):967-976, 2007.
113. Watzlawik J, Holicky E, Edberg DD, Marks DL, Warrington AE, Wright BR, Pagano RE, Rodriguez M. Human remyelination promoting antibody inhibits apoptotic signaling and differentiation through Lyn kinase in primary rat oligodendrocytes. Glia 58(15):1782-1793, 2010.
114. Watzlawik JO, Warrington AE, Rodriguez M. PDGF is required for remyelination-promoting IgM stimulation of oligodendrocyte progenitor cell proliferation. PLoS One 8(2):e55149, 2013.
115. Waubant E, Pelletier D, Mass M, Cohen JA, Kita M, Cross A, Bar-Or A, Vollmer T, Racke M, Stuve O, Schwid S, Goodman A, Kachuck N, Preiningerova J, Weinstock-Guttman B, Calabresi PA, Miller A, Mokhtarani M, Ikle D, Murphy S, et al. Randomized controlled trial of atorvastatin in clinically isolated syndrome: the STAyCIS study. Neurology 78(15):1171-1178, 2012.
116. Windrem MS, Roy NS, Wang J, Nunes M, Benraiss A, Goodman R, Mckhann GM, 2nd, Goldman SA. 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 69(6):966-975, 2002.
117. Windrem MS, Schanz SJ, Guo M, Tian GF, Washco V, Stanwood N, Rasband M, Roy NS, Nedergaard M, Havton LA, Wang S, Goldman SA. Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2(6):553-565, 2008.
118. Xu J, Drew PD. 9-Cis-retinoic acid suppresses inflammatory responses of microglia and astrocytes. J Neuroimmunol 171(1-2):135-144, 2006.
119. Yang N, Zuchero JB, Ahlenius H, Marro S, Ng YH, Vierbuchen T, Hawkins JS, Geissler R, Barres BA, Wernig M. Generation of oligodendroglial cells by direct lineage conversion. Nat Biotechnol 31(5):434-439, 2013.
120. 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 12(7):829-838, 2009.
121. Youssef S, Stuve O, Patarroyo JC, Ruiz PJ, Radosevich JL, Hur EM, Bravo M, Mitchell DJ, Sobel RA, Steinman L, Zamvil SS. The HMG-CoA reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease. Nature 420(6911):78-84, 2002.
122. Zajicek JP, Apostu VI. Role of cannabinoids in multiple sclerosis. CNS Drugs 25(3):187-201, 2011.