In Vitro and in vivo models of multiple sclerosis

CNS and Neurological Disorders - Drug Targets

Volumn 11, Issue 5, 2012, Pages 570-588

  van der Star, Baukje J ^a   Vogel, Daphne Y S ^a   Kipp, Markus ^a,b   Puentes, Fabiola ^c   Baker, David ^c   Amor, Sandra ^a,c  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Central nervous system; Cuprizone; Demyelination; Experimental autoimmune encephalomyelitis; Experimental models; In vitro; In vivo; Multiple sclerosis; Neurodegeneration

Indexed keywords

CD11B ANTIGEN; CHLORDANE; CUPRIZONE; ETHIDIUM BROMIDE; FC RECEPTOR; GAMMA INTERFERON; GLUCOSE TRANSPORTER 5; HLA DR ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LYSOPHOSPHATIDYLCHOLINE; LYSOZYME; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYELIN; NEUROTRANSMITTER;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL CULTURE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN SLICE; CALLITRICHINAE; CELL AGGREGATION; CELL DEATH; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; COMPUTER MODEL; CYTOKINE RELEASE; DEMYELINATION; ELECTROPHYSIOLOGY; ENDOTHELIUM CELL; EXPERIMENTAL MODEL; EXPERIMENTAL MOUSE; GRAY MATTER; GUINEA PIG; IN VITRO STUDY; IN VIVO STUDY; JAPANESE MACAQUE ENCEPHALOMYELITIS; KNOCKOUT MOUSE; MACACA; MEMBRANE PERMEABILITY; MICROGLIA; MICROVASCULATURE; MULTIPLE SCLEROSIS; MURINE ENCEPHALOMYELITIS VIRUS; MUTANT; NERVE CELL; NERVE DEGENERATION; NONHUMAN; OLIGODENDROGLIA; PARABIOTIC MOUSE; PATCH CLAMP; PROTEIN EXPRESSION; RAT; REMYELINIZATION; REVIEW; SEMLIKI FOREST ALPHAVIRUS; SYNAPSE; TRANSGENIC MOUSE;

EID: 84863916403     PISSN: 18715273     EISSN: 19963181     Source Type: Journal    
DOI: 10.2174/187152712801661284     Document Type: Review

References (162)

1. Amor, S.; Puentes, F.; Baker, D.; van der Valk, P. Inflammation in Neurodegenerative Diseases. Immunology, 2010, 129, 154-169.
2. Amor, S.; Smith, P.A.; Hart, B.; Baker, D. Biozzi mice: of mice and human neurological diseases. J. Neuroimmunol., 2005, 165, 1-10.
3. Kipp, M.; van der Star, B.J.; Vogel, D.Y.; Puentes, F.; Baker, D.; Amor, S. Experimental in vivo and in vitro Models of Multiple Sclerosis: EAE and beyond. Mult. Scler. Relat. Disord., 2012, 1, 15-28.
4. 't Hart, B.A.; Bauer, J.; Brok, H.P.; Amor, S. Non-human primate models of experimental autoimmune encephalomyelitis: Variations on a theme. J. Neuroimmunol., 2005, 168, 1-12.
5. Huizinga, R.; Heijmans, N.; Schubert, P.; Gschmeissner, S.;'t Hart, B.A.; Herrmann, H,.; Amor, S. Immunization with neurofilament light protein induces spastic paresis and axonal degeneration in Biozzi ABH mice. J. Neuropathol. Exp. Neurol., 2007, 66, 295-304.
6. Huizinga, R.; Gerritsen, W.; Heijmans, N.; Amor, S. Axonal loss and gray matter pathology as a direct result of autoimmunity to neurofilaments. Neurobiol. Dis., 2008, 32, 461-470.
7. Vesterinen, H.M.; Sena, E.S.; ffrench-Constant, C.; Williams, A.; Chandran, S.; Macleod, M.R. Improving the translational hit of experimental treatments in multiple sclerosis. Mult. Scler., 2010, 16, 1044-1055.
8. Baker, D.; Gerritsen, W.; Rundle, J.; Amor, S. Critical appraisal of animal models of multiple sclerosis. Mult. Scler., 2011, 17, 647-657.
9. Baker, D.; Amor, S. Publication guidelines for refereeing and reporting on animal use in experimental autoimmune encephalomyelitis. J. Neuroimmunol., 2012, 242, 78-83.
10. Amor, S.; Baker, D. Checklist for reporting and reviewing studies of experimental animal models of multiple sclerosis and related disorders. Mult. Scler. Relat. Disord., 2012, 1, 111-115.
11. Drexler, B.; Hentschke, H.; Antkowiak, B.; Grasshoff, C. Organotypic cultures as tools for testing neuroactive drugs-link between in-vitro and in-vivo experiments. Curr. Med. Chem., 2010, 17, 4538-4350.
12. Kilkenny, C.; Browne, W.J.; Cuthill, I.C.; Emerson, M.; Altman, D.G. Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. J. Pharmacol. Pharmacother., 2010 1, 94-99.
13. De Vries, G.H.; Boullerne, A.I. Glial cell lines: an overview. Neurochem. Res., 2010, 35, 1978-2000.
14. Zuiderwijk-Sick, E.A.; van der Putten, C.; Bsibsi, M.; Deuzing, I.P.; de Boer, W.; Persoon-Deen, C.; Kondova, I.; Boven, L.A.; van Noort, J.M.; 't Hart, B.A.; Amor, S.; Bajramovic, J.J. Differentiation of primary adult microglia alters their response to TLR8-mediated activation but not their capacity as APC. Glia, 2007, 55, 1589-600.
15. de Groot, C.J.; Hulshof, S.; Hoozemans, J.J.; Veerhuis, R. Establishment of microglial cell cultures derived from postmortem human adult brain tissue: immunophenotypical and functional characterization. Microsc. Res. Tech., 2001, 54, 34-39.
16. Gibbons, H.M.; Dragunow, M. Adult human brain cell culture for neuroscience research. Int. J. Biochem. Cell Biol., 2010, 42, 844-856.
17. von Bernhardi, R.; Tichauer, J.; Eugenín-von Bernhardi, L. Proliferating culture of aged microglia for the study of neurodegenerative diseases. J. Neurosci. Methods, 2011, 202, 65-69.
18. Ford, A.L.; Goodsall, A.L.; Hickey, W.F.; Sedgwick, J.D. Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4+ T cells compared. J. Immunol., 1995, 154, 4309-4321.
19. Hao, C.; Richardson, A.; Fedoroff, S. Macrophage-like cells originate from neuroepithelium in culture: characterization and properties of the macrophage-like cells. Int. J. Dev. Neurosci., 1991, 9, 1-14.
20. Ganter, S.; Northoff, H.; Mannel, D.; Gebicke-Harter, P.J. Growth control of cultured microglia. J. Neurosci. Res., 1992, 33, 218-230.
21. Olah, M.; Raj, D.; Brouwer, N.; De Haas, A.H.; Eggen, B.J.; Den Dunnen, W.F.; Biber, K.P.; Boddeke, H.W. An optimized protocol for the acute isolation of human microglia from autopsy brain samples. Glia, 2012, 60, 96-111.
22. McCarthy, K.D.; de Vellis, J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell. Biol., 1980, 85, 890-902.
23. Kim, S.; Steelman, A.J.; Koito, H.; Li, J. Astrocytes promote TNFmediated toxicity to oligodendrocyte precursors. J. Neurochem., 2011, 116, 53-66.
24. Giulian, D.; Baker, T.J. Characterization of ameboid microglia isolated from developing mammalian brain. J. Neurosci., 1986, 6, 2163-2178.
25. Olah, M.; Amor, S.; Brouwer, N.; Vinet, J.; Eggen, B.; Biber, K,; Boddeke, H.W. Identification of a microglia phenotype supportive of remyelination. Glia, 2012, 60, 306-321.
26. van Noort, J.M.; van den Elsen, P.J.; van Horssen, J.; Geurts, J.J.G.; van der Valk, P.; Amor, S. Preactive multiple sclerosis lesions offer novel clues for neuroprotective therapeutic strategies. CNS Neurol. Disord. Drug Targets, 2011, 10, 68-81.
27. van der Valk, P.; Amor, S. The early lesion(s) in multiple sclerosis. Curr. Opin. Neurol., 2009, 22, 207-213.
28. Fancy, S.P.; Chan, J.R.; Baranzini, S.E.; Franklin, R.J.; Rowitch, D.H. Myelin regeneration: a recapitulation of development? Annu. Rev. Neurosci., 2011, 34, 21-43.
29. Trotter, J. The development of myelin-forming glia: studies with primary cell cultures and immortalized cell lines. Perspect. Dev. Neurobiol., 1993, 1, 149-154.
30. Raff, M.C.; Williams, B.P.; Miller, R.H. The in vitro differentiation of a bipotential glial progenitor cell. EMBO J., 1984, 3, 1857-1864.
31. Chen, K.; Hughes, S.M.; Connor, B. Neural progenitor cells derived from the adult rat subventricular zone: characterization and transplantation. Cell Transplant., 2007, 16, 799-810.
32. 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, 2011, 59, 882-892.
33. Seki, Y.; Suzuki, S.O.; Masui, K.; Harada, S.; Nakamura, S.; Kanba, S.; Iwaki, T. A simple and high-yield method for preparation of rat microglial cultures utilizing Aclar plastic film. Neuropathology, 2011, 31, 215-222.
34. van der Valk, P.; De Groot, C.J. Staging of multiple sclerosis (MS) lesions: pathology of the time frame of MS. Neuropathol. Appl. Neurobiol., 2000, 26, 2-10.
35. Tracy, E.T.; Zhang, C.Y.; Gentry, T.; Shoulars, K.W.; Kurtzberg, J. Isolation and expansion of oligodendrocyte progenitor cells from cryopreserved human umbilical cord blood. Cytotherapy, 2011, 13, 722-729.
36. Hu, B.Y.; Du, Z.W.; Zhang, S.C. Differentiation of human oligodendrocytes from pluripotent stem cells. Nat. Protoc., 2009, 4, 1614-1622.
37. Sharp, J.; Hatch, M.; Nistor, G.; Keirstead, H. Derivation of oligodendrocyte progenitor cells from human embryonic stem cells. Methods Mol. Biol., 2011, 767, 399-409.
38. Buntinx, M.; Vanderlocht, J.; Hellings, N.; Vandenabeele, F.; Lambrichts, I.; Raus, J.; Ameloot, M.; Stinissen, P.; Steels, P. Characterization of three human oligodendroglial cell lines as a model to study oligodendrocyte injury: morphology and oligodendrocyte-specific gene expression. J. Neurocytol., 2003, 32, 25-38.
39. Sundberg, M.; Skottman, H.; Suuronen, R.; Narkilahti, S. Production and isolation of NG2+ oligodendrocyte precursors from human embryonic stem cells in defined serum-free medium. Stem Cell Res., 2010, 5, 91-103.
40. O'Meara, R.W.; Ryan, S.D.; Colognato, H.; Kothary, R. Derivation of enriched oligodendrocyte cultures and oligodendrocyte/neuron myelinating co-cultures from post-natal murine tissues. J. Vis. Exp., 2011, 21, pii: 3324.
41. de Vellis, J.; Cole, R. Preparation of mixed glial cultures from postnatal rat brain. Methods Mol. Biol. 2012, 814, 49-59.
42. Ruffini, F.; Arbour, N.; Blain, M.; Olivier, A.; Antel, J.P. Distinctive properties of human adult brain-derived myelin progenitor cells. Am. J. Pathol., 2004, 165, 2167-2175.
43. Louis, J.C.; Muir, D.; Varon, S. Autocrine inhibition of mitotic activity in cultured oligodendrocyte-type-2 astrocyte (O-2A) precursor cells. Glia, 1992, 6, 30-38.
44. Richter-Landsberg, C.; Heinrich, M. OLN-93: a new permanent oligodendroglia cell line derived from primary rat brain glial cultures. J. Neurosci. Res., 1996, 45, 161-73.
45. Jung, M.; Krämer, E.; Grzenkowski, M.; Tang, K.; Blakemore, W.; Aguzzi, A.; Khazaie, K.; Chlichlia, K.; von Blankenfeld, G.; Kettenmann, H.; Trotter, J. Lines of murine oligodendroglial precursor cells immortalized by an activated neu tyrosine kinase show distinct degrees of interaction with axons in vitro and in vivo. Eur. J. Neurosci., 1995, 7, 1245-1265.
46. Foster, L.M.; Phan, T.; Verity, A.N.; Bredesen, D.; Campagnoni, A.T. Generation and analysis of normal and shiverer temperaturesensitive immortalized cell lines exhibiting phenotypic characteristics of oligodendrocytes at several stages of differentiation. Dev. Neurosci., 1993, 15, 100-109.
47. Post, G.R.; Dawson, G. Characterization of a cell line derived from a human oligodendroglioma. Mol. Chem. Neuropathol., 1992, 16, 303-317.
48. McLaurin, J.; Trudel, G.C.; Shaw, I.T.; Antel, J.P.; Cashman, N.R. A human glial hybrid cell line differentially expressing genes subserving oligodendrocyte and astrocyte phenotype. J. Neurobiol., 1995, 26, 283-293.
49. De Groot, C.J.; Langeveld, C.H.; Jongenelen, C.A.; Montagne, L.; Van Der Valk, P.; Dijkstra, C.D. Establishment of human adult astrocyte cultures derived from postmortem multiple sclerosis and control brain and spinal cord regions: immunophenotypical and functional characterization. J. Neurosci. Res., 1997, 49, 342-354.
50. Sharif, A.; Prevot, V. Isolation and culture of human astrocytes. Methods. Mol. Biol., 2012, 814, 137-155.
51. Losciuto, S.; Dorban, G.; Gabel, S.; Gustin, A.; Hoenen, C.; Grandbarbe, L.; Heuschling, P.; Heurtaux, T. An efficient method to limit microglia-dependent effects in astroglial cultures. J Neurosci. Methods, 2012, 207(1), 59-71.
52. Bertrand, S.J.; Aksenova, M.V.; Aksenov, M.Y.; Mactutus, C.F.; Booze, R.M. Endogenous amyloidogenesis in long-term rat hippocampal cell cultures. BMC Neurosci., 2011, 12, 38-48.
53. Copray, S.; Balasubramaniyan, V.; Levenga, J.; de Bruijn, J.; Liem, R.; Boddeke, E. Olig2 overexpression induces the in vitro differentiation of neural stem cells into mature oligodendrocytes. Stem Cells, 2006, 24, 1001-1010.
54. Lorenz, L.; Dang, J.; Misiak, M.; Tameh Abolfazl, A.; Beyer, C.; Kipp, M. Combined 17beta-oestradiol and progesterone treatment prevents neuronal cell injury in cortical but not midbrain neurones or neuroblastoma cells. J. Neuroendocrinol., 2009, 21, 841-849.
55. Kitazawa, A.; Shimizu, N. Differentiation of mouse embryonic stem cells into neurons using conditioned medium of dorsal root ganglia. J. Biosci. Bioeng., 2005, 100, 94-99.
56. Salli, U.; Reddy, A.P.; Salli, N.; Lu, N.Z.; Kuo, H.C.; Pau, F.K.; Wolf, D.P.; Bethea, C.L. Serotonin neurons derived from rhesus monkey embryonic stem cells: similarities to CNS serotonin neurons. Exp. Neurol., 2004, 188, 351-364.
57. Brewer, G.J.; Espinosa, J.; McIlhaney, M.P.; Pencek, T.P.; Kesslak, J.P.; Cotman, C.; Viel, J.; McManus, D.C. Culture and regeneration of human neurons after brain surgery. J. Neurosci. Methods, 2001, 107, 15-23.
58. Cano-Abad, M.F.; Herrera-Peco, I.; Sola, R.G.; Pastor, J.; Garcia-Navarrete, E.; Moro, R.C.; Pizzo, P.; Ruiz-Nuno, A. New insights on culture and calcium signalling in neurons and astrocytes from epileptic patients. Int. J. Dev. Neurosci., 2011, 29, 121-129.
59. Agholme, L.; Lindström, T.; Kågedal, K.; Marcusson, J.; Hallbeck, M. An in vitro model for neuroscience: differentiation of SH-SY5Y cells into cells with morphological and biochemical characteristics of mature neurons. J. Alzheimers Dis., 2010, 20, 1069-1082.
60. Forsby, A.; Bal-Price, A.K.; Camins, A.; Coecke, S.; Fabre, N.; Gustafsson, H.; Honegger, P.; Kinsner-Ovaskainen, A.; Pallas, M.; Rimbau, V.; Rodriguez-Farre, E.; Sunol, C.; Vericat, J.A.; Zurich, M.G. Neuronal in vitro models for the estimation of acute systemic toxicity. Toxicol. In Vitro, 2009, 23, 1564-1569.
61. Zhang, Z.; Drzewiecki, G.J.; Hom, J.T.; May, P.C.; Hyslop, P.A. Human cortical neuronal (HCN) cell lines: a model for amyloid beta neurotoxicity. Neurosci. Lett., 1994, 177, 162-164.
62. Pleasure, S.J.; Page, C.; Lee, V.M. Pure, postmitotic, polarized human neurons derived from NTera 2 cells provide a system for expressing exogenous proteins in terminally differentiated neurons. J. Neurosci., 1992, 12, 1802-1815.
63. Kim, H.J.; Park, J.W.; Park, J.W.; Byun, J.H.; Vahidi, B.; Rhee, S.W.; Jeon, N.L. Integrated Microfluidics Platforms for Investigating Injury and Regeneration of CNS Axons. Ann. Biomed. Eng., 2012, in press.
64. Levi, G.; Meyer, H. Nouvelles recherches sur le tissu nerveux cultivé in vitro. Morphologie, croissance et relations réciproques des neurones. Arch. Biol., 1941, 52, 133-278.
65. Hild, W. Myelin formation in central nervous system tissue cultures. Verh. Anat. Ges., 1956, 53, 315-317.
66. Lossi, L.; Alasia, S.; Salio, C.; Merighi, A. Prog. Neurobiol., 2009, 88, 221-245.
67. Huang, J.H.; Zager, E.L.; Zhang, J.; Groff, R.F.; Pfister, B.J.; Cohen, A.S.; Grady, M.S.; Maloney-Wilensky, E.; Smith, D.H. Harvested human neurons engineered as live nervous tissue constructs: implications for transplantation. Laboratory investigation. J. Neurosurg., 2008, 108, 343-347.
68. Mi, S.; Miller, R.H.; Tang, W.; Lee, X.; Hu, B.; Wu, W.; Zhang, Y.; Shields, C.B.; Zhang, Y.; Miklasz, S.; Shea, D.; Mason, J.; Franklin, R.J.; 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., 2009, 65, 304-315.
69. Birgbauer, E.; Rao, T.S.; Webb, M. Lysolecithin induces demyelination in vitro in a cerebellar slice culture system. J. Neurosci. Res., 2004, 78, 157-166.
70. Verwer, R.W.; Hermens, W.T.; Dijkhuizen, P.; ter Brake, O.; Baker, R.E.; Salehi, A.; Sluiter, A.A.; Kok, M.J.; Muller, L.J.; Verhaagen, J.; Swaab, D.F. Cells in human postmortem brain tissue slices remain alive for several weeks in culture. FASEB J., 2002, 16, 54-60.
71. Bornstein, M.B.; Appel, S.H. Demyelination in cultures of rat cerebellum produced by experimental allergic encephalomyelitic serum. Trans. Am. Neurol. Assoc., 1959, 84, 165-166.
72. Aktas, O.; Smorodchenko, A.; Brocke, S.; Infante-Duarte, C.; Schulze Topphoff, U.; Vogt, J.; Prozorovski, T.; Meier, S.; Osmanova, V.; Pohl, E.; Bechmann, I.; Nitsch, R.; Zipp, F. Neuronal damage in autoimmune neuroinflammation mediated by the death ligand TRAIL. Neuron, 2005, 46, 421-432.
73. Dörr, J.; Roth, K.; Zurbuchen, U.; Deisz, R.; Bechmann, I.; Lehmann, T.N.; Meier, S.; Nitsch, R.; Zipp, F. Tumor-necrosisfactor-related apoptosis-inducing-ligand (TRAIL)-mediated death of neurons in living human brain tissue is inhibited by flupirtinemaleate. J. Neuroimmunol., 2005, 167, 204-209.
74. Defaux, A.; Zurich, M.G.; Honegger, P.; Monnet-Tschudi, F. Minocycline promotes remyelination in aggregating rat brain cell cultures after interferon-gamma plus lipopolysaccharide-induced demyelination. Neuroscience, 2011, 187, 84-92.
75. Vereyken, E.J.; Fluitsma, D.M.; Bolijn, M.J.; Dijkstra, C.D.; Teunissen, C.E. An in vitro model for de-and remyelination using lysophosphatidyl choline in rodent whole brain spheroid cultures. Glia, 2009, 57, 1326-1340.
76. Pulliam, L.; Stubblebine, M.; Hyun, W. Quantification of neurotoxicity and identification of cellular subsets in a threedimensional brain model. Cytometry, 1998, 32, 66-69.
77. Hayes, G.M.; Fox, R.M.; Cuzner, M.L.; Griffin, G.E. Human rotation-mediated fetal mixed brain cell aggregate culture: characterization and N-methyl-D-aspartate toxicity. Neurosci. Lett., 2000, 287, 146-150.
78. Devon, R.M. Comparison of oligodendrocytes grown in neocortex and spinal cord aggregate cultures. Brain Res., 1987, 429, 289-294.
79. Diemel, L.T.; Wolswijk, G.; Jackson, S.J.; Cuzner, M.L. Remyelination of cytokine-or antibody-demyelinated CNS aggregate cultures is inhibited by macrophage supplementation. Glia, 2004, 45, 278-286.
80. Jackson, S.J.; Baker, D.; Cuzner, M.L.; Diemel, L.T. Cannabinoidmediated neuroprotection following interferon-gamma treatment in a three-dimensional mouse brain aggregate cell culture. Eur. J. Neurosci., 2004, 20, 2267-2275.
81. Abbott, N.J.; Patabendige, A.A.; Dolman, D.E.; Yusof, S. R; Begley D.J. Structure and function of the blood-brain barrier. Neurobiol. Dis., 2010, 37, 13-25.
82. Garberg, P.; Ball, M.; Borg, N.; Cecchelli, R.; Fenart, L.; Hurst, R.D.; Lindmark, T.; Mabondzo, A.; Nilsson, J.E.; Raub, T.J.; Stanimirovic, D.; Terasaki, T.; Oberg, J.O.; Osterberg, T. In vitro models for the blood-brain barrier. Toxicol. In Vitro, 2005, 19, 299-334.
83. Wilhelm, I.; Fazakas, C.; Krizbai, I.A. In vitro models of the bloodbrain barrier. Acta Neurobiol. Exp. (Wars), 2011, 71, 113-128.
84. Cucullo, L.; Marchi, N.; Hossain, M.; Janigro, D. A dynamic in vitro BBB model for the study of immune cell trafficking into the central nervous system. J. Cereb. Blood Flow Metab., 2011, 31, 767-777.
85. Naik, P.; Cucullo, L. In vitro blood-brain barrier models: Current and perspective technologies. J. Pharm. Sci., 2012, 101, 1337-1354.
86. Baxter, A.G. The origin and application of experimental autoimmune encephalomyelitis. Nat. Rev. Immunol., 2007, 7, 904-912.
87. Kabat, E.A.; Wolf, A.; Bezer, A.E. Rapid production of acute disseminated encephalomyelitis in rhesus monkeys by injection of brain tissue with adjuvants. Science, 1946, 104, 362-363.
88. Libbey, J.E.; Fujinami, R.S. Experimental autoimmune encephalomyelitis as a testing paradigm for adjuvants and vaccines. Vaccine, 2011, 29, 3356-3362.
89. Lorentzen, J.C.; Issazadeh, S.; Storch, M.; Mustafa, M.I.; Lassman, H.; Linington, C.; Klareskog, L.; Olsson, T. Protracted, relapsing and demyelinating experimental autoimmune encephalomyelitis in DA rats immunized with syngeneic spinal cord and incomplete Freund's adjuvant. J. Neuroimmunol., 1995, 63, 193-205.
90. Hampton, D.W.; Anderson, J.; Pryce, G.; Irvine, K.A.; Giovannoni, G.; Fawcett, J.W.; Compston, A.; Franklin, R.J.; Baker, D.; Chandran, S. An experimental model of secondary progressive multiple sclerosis that shows regional variation in gliosis, remyelination, axonal and neuronal loss. J. Neuroimmunol., 2008, 201-202, 200-211.
91. Baker, D.; O'Neill, J.K.; Gschmeissner, S.E.; Wilcox, C.E.; Butter, C.; Turk, J.L. Induction of chronic relapsing experimental allergic encephalomyelitis in Biozzi mice. J. Neuroimmunol., 1990, 28, 261-270.
92. Mendel, I.; Kerlero de Rosbo, N.; Ben-Nun, A. A myelin oligodendrocyte glycoprotein peptide induces typical chronic experimental autoimmune encephalomyelitis in H-2b mice: fine specificity and T cell receptor V beta expression of encephalitogenic T cells. Eur. J. Immunol., 1995, 25, 1951-1959.
93. Amor, S.; Groome, N.; Linington, C.; Morris, M.M.; Dornmair, K.; Gardinier, M.V.; Matthieu, J.M.; Baker, D. Identification of epitopes of myelin oligodendrocyte glycoprotein for the induction of experimental allergic encephalomyelitis in SJL and Biozzi AB/H mice. J. Immunol., 1994, 153, 4349-4356.
94. Amor, S.; O'Neill, J.K.; Morris, M.M.; Smith, R.M.; Wraith, D.C.; Groome, N.; Travers, P.J.; Baker, D. Encephalitogenic epitopes of myelin basic protein, proteolipid protein, myelin oligodendrocyte glycoprotein for experimental allergic encephalomyelitis induction in Biozzi ABH (H-2Ag7) mice share an amino acid motif. J. Immunol., 1996, 156, 3000-3008.
95. Smith, P.A.; Heijmans, N.; Ouwerling, B.; Breij, E.C.; Evans, N.; van Noort, J.M.; Plomp, A.C.; Delarasse, C.; 't Hart, B.; Pham-Dinh, D.; Amor, S. Native myelin oligodendrocyte glycoprotein promotes severe chronic neurological disease and demyelination in Biozzi ABH mice. Eur. J. Immunol., 2005, 35, 1311-1319.
96. Ditamo, Y.; Degano, A.L.; Maccio, D.R.; Pistoresi-Palencia, M.C.; Roth, G.A. Age-related changes in the development of experimental autoimmune encephalomyelitis. Immunol. Cell. Biol., 2005, 83, 75-82.
97. Scheikl, T.; Pignolet, B.; Mars, L.T.; Liblau, R.S. Transgenic mouse models of multiple sclerosis. Cell Mol. Life Sci., 2010, 67, 4011-4034.
98. Swanborg, R.H. Experimental autoimmune encephalomyelitis in the rat: lessons in T-cell immunology and autoreactivity. Immunol. Rev., 2001, 184, 129-135.
99. Gambi, D.; Di Cesare, N.; Di Trapani, G.; Macchi, G.; Sbriccoli, A. Experimental allergic encephalomyelitis in guinea pig: variability of response to intradermal emulsion injection. Ital. J. Neurol. Sci., 1989, 10, 33-41.
100. Genain, C.P.; Hauser, S.L. Experimental allergic encephalomyelitis in the New World monkey Callithrix jacchus. Immunol. Rev., 2001, 183, 159-172.
101. Bajramovic, J.J.; Brok, H.P.; Ouwerling, B.; Jagessar, S.A.; van Straalen, L.; Kondova, I.; Bauer, J.; Amor, S.; t Hart, B.A.; Ben-Nun, A. Oligodendrocyte-specific protein is encephalitogenic in rhesus macaques and induces specific demyelination of the optic nerve. Eur. J. Immunol., 2008, 38, 1452-1464.
102. Thoua, N.M.; van Noort, J.M.; Baker, D.; Bose, A.; van Sechel, A.C.; van Stipdonk, M.J.; Travers, P.J.; Amor, S. Encephalitogenic and immunogenic potential of the stress protein alphaB-crystallin in Biozzi ABH (H-2A(g7) mice. J. Neuroimmunol., 2000, 104, 47-57.
103. Morris-Downes, M.M.; McCormack, K.; Baker, D.; Sivaprasad, D.; Natkunarajah, J.; Amor, S. Encephalitogenic and immunogenic potential of myelin-associated glycoprotein (MAG), oligodendrocyte-specific glycoprotein (OSP) and 2',3'-cyclic nucleotide 3'-phosphodiesterase (CNPase) in ABH and SJL mice. J. Neuroimmunol., 2002, 122, 20-33
104. Mackenzie-Graham, A.; Rinek, G.A.; Avedisian, A.; Gold, S.M.; Frew, A.J.; Aguilar, C.; Lin, D.R.; Umeda, E.; Voskuhl, R.R.; Alger, J.R. Cortical atrophy in experimental autoimmune encephalomyelitis: In vivo imaging. Neuroimage, 2011, 60, 95-104.
105. Pomeroy, I.M.; Jordan, E.K.; Frank, J.A.; Matthews, P.M.; Esiri, M.M. Diffuse cortical atrophy in a marmoset model of multiple sclerosis. Neurosci. Lett., 2008, 437, 121-124.
106. Mangiardi, M.; Crawford, D.K.; Xia, X., Du, S.; Simon-Freeman, R.; Voskuhl, R.R.; Tiwari-Woodruff, S.K. An animal model of cortical and callosal pathology in multiple sclerosis. Brain Pathol., 2011, 21, 263-278.
107. Virtanen, J.O.; Jacobson, S. Viruses and multiple sclerosis. CNS Neurol. Disord. Drug Targets, 2012, 11(5), [Epub ahead of print].
108. Atkins, G.J.; McQuaid, S., Morris-Downes, M.M.; Galbraith, S.E.; Amor, S.; Cosby, S.L.; Sheahan, B.J. Transient virus infection and multiple sclerosis. Rev. Med. Virol., 2000, 10, 291-303.
109. Smithburn, K.C.; Haddow, A.J.; Mahaffy, A.F. A neurotropic virus isolated from Aedes mosquitoes caught in the Semliki forest. Am. J. Trop. Med. Hyg., 1946, 26, 189-208.
110. Fazakerley, J.K.; Amor, S.; Webb, H.E. Reconstitution of Semliki forest virus infected mice, induces immune mediated pathological changes in the CNS. Clin. Exp. Immunol., 1983, 52, 115-120.
111. Amor, S.; Scallan, M.; Morris, M.M.; Dyson, H.; Fazakerley, J.K. Role of immune responses in protection and pathogenesis during SFV infection. J. Gen. Virol., 1996, 77, 281-291.
112. Amor, S.; Webb, H.E. The effect of cycloleucine on SFV A7(74) infection in mice. Brit. J. Exp. Path., 1987, 97 373-377.
113. Smith, J-P.; Morris, M.M.; Brennan, F.; Wallace, G.; Amor S. A role for alpha4-integrin in Semliki Forest virus infection. J. Neuroimmunol., 2000, 106, 60-68.
114. Theiler, M. Spontaneous Encephalomyelitis of Mice-a New Virus Disease. Science, 1934, 80, 122-128.
115. Tsunoda, I.; Fujinami, R.S. Neuropathogenesis of Theiler's murine encephalomyelitis virus infection, an animal model for multiple sclerosis. Neuroimmune Pharmacol., 2010, 5, 355-369.
116. Pringproa, K.; Rohn, K.; Kummerfeld, M.; Wewetzer, K.; Baumgartner, W. Theiler's murine encephalomyelitis virus preferentially infects immature stages of the murine oligodendrocyte precursor cell line BO-1 and blocks oligodendrocytic differentiation in vitro. Brain Res., 2010, 1327, 24-37.
117. Axthelm, M.K.; Bourdette, D.N.; Marracci, G.H.; Su, W.; Mullaney, E.T.; Manoharan, M.; Kohama, S.G.; Pollaro, J.; Witkowski, E.; Wang, P.; Rooney, W.D.; Sherman, L.S.; Wong, S.W. Japanese macaque encephalomyelitis: a spontaneous multiple sclerosis-like disease in a nonhuman primate. Ann. Neurol., 2011, 70, 362-373.
118. Woodruff, R.H.; Franklin, R.J. Demyelination and remyelination of the caudal cerebellar peduncle of adult rats following stereotaxic injections of lysolecithin, ethidium bromide, and complement/antigalactocerebroside: a comparative study. Glia, 1999, 25, 216-228.
119. Franklin, R. J,; Crang, A.J.; Blakemore, W.F. The reconstruction of an astrocytic environment in glia-deficient areas of white matter. J. Neurocytol., 1993, 22, 382-396.
120. Talbott, J.F.; Cao, Q.; Enzmann, G. U; Benton, R. L,; Achim, V.; Cheng, X.X.; Mills, M.D.; Rao, M.S.; Whittemore, S.R. Schwann cell-like differentiation by adult oligodendrocyte precursor cells following engraftment into the demyelinated spinal cord is BMPdependent. Glia, 2006, 54, 147-159.
121. Mothe, A.J.; Tator, C.H. Transplanted neural stem/progenitor cells generate myelinating oligodendrocytes and Schwann cells in spinal cord demyelination and dysmyelination. Exp. Neurol., 2008, 213, 176-190.
122. Rosenbluth, J.; Schiff, R.; Liang, W.L.; Dou, W. Antibodymediated CNS demyelination II. Focal spinal cord lesions induced by implantation of an IgM antisulfatide-secreting hybridoma. J. Neurocytol., 2003, 32, 265-276.
123. Rosenbluth, J.; Schiff, R. Spinal cord dysmyelination caused by an antiproteolipid protein IgM antibody: implications for the mechanism of central nervous system myelin formation. J. Neurosci. Res., 2009, 87, 956-963.
124. Felts, P.A.; Woolston, A.M.; Fernando, H.B.; Asquith, S.; Gregson, N.A.; Mizzi, O.J.; Smith, K.J. Inflammation and primary demyelination induced by the intraspinal injection of lipopolysaccharide. Brain, 2005, 128, 1649-1666.
125. Blakemore, W.F. Lesions in the cat spinal cord following local injections of 6-aminonicotinamide. Res. Vet. Sci., 1978, 24, 390-391.
126. Rojiani, A.M.; Prineas, J.W.; Cho, E.S. Electrolyte-induced demyelination in rats. 1. Role of the blood-brain barrier and edema. Acta Neuropathol., 1994, 88, 287-292.
127. Mastaglia, F.L.; Carroll, W.M.; Jennings, A.R. Spinal cord lesions induced by antigalactocerebroside serum. Clin. Exp. Neurol., 1989, 26, 33-44.
128. Kipp, M.; Clarner, T.; Dang, J.; Copray, S.; Beyer, C. The cuprizone animal model: new insights into an old story. Acta Neuropathol., 2009, 118, 723-736.
129. Gregson, N.A. Lysolipids and membrane damage: lysolecithin and its interaction with myelin. Biochem. Soc. Trans., 1989, 17, 280-283.
130. Quinn, M.T.; Parthasarathy, S.; Steinberg, D. Lysophosphatidylcholine: a chemotactic factor for human monocytes and its potential role in atherogenesis. Proc. Natl. Acad. Sci. USA, 1988, 85, 2805-2809.
131. Nagai, J.; Uchida, H.; Matsushita, Y.; Yano, R.; Ueda, M.; Niwa, M.; Aoki, J.; Chun, J.; Ueda, H. Autotaxin and lysophosphatidic acid1 receptor-mediated demyelination of dorsal root fibers by sciatic nerve injury and intrathecal lysophosphatidylcholine. Mol. Pain, 2010, 6, 78-88.
132. Kipp, M.; Gingele, S.; Pott, F.; Clarner, T.; van der Valk, P.; Denecke, B.; Gan, L.; Siffrin, V.; Zipp, F.; Dreher, W.; Baumgartner, W.; Pfeifenbring, S.; Godbout, R.; Amor, S.; Beyer, C. BLBP-expression in astrocytes during experimental demyelination and in human multiple sclerosis lesions. Brain Behav. Immun., 2011, 25, 1554-1568.
133. Carlton, W.W. Studies on the induction of hydrocephalus and spongy degeneration by cuprizone feeding and attempts to antidote the toxicity. Life Sci., 1967, 6, 11-19.
134. Suzuki, K.; Kikkawa, Y. Status spongiosus of CNS and hepatic changes induced by cuprizone biscyclohexanone oxalyldihydrazone. Am. J. Pathol., 1969, 54, 307-325.
135. Norkute, A.; Hieble, A.; Braun, A.; Johann, S.; Clarner, T.; Baumgartner, W.; Beyer, C.; Kipp, M. Cuprizone treatment induces demyelination and astrocytosis in the mouse hippocampus. J. Neurosci. Res., 2009, 87, 1343-1355.
136. Taylor, L.C.; Gilmore, W.; Matsushima, G.K. SJL mice exposed to cuprizone intoxication reveal strain and gender pattern differences in demyelination. Brain Pathol., 2009, 19, 467-479.
137. Acs, P.; Kipp, M.; Norkute, A.; Johann, S.; Clarner, T.; Braun, A.; Berente, Z.; Komoly, S.; Beyer, C. 17beta-estradiol and progesterone prevent cuprizone provoked demyelination of corpus callosum in male mice. Glia, 2009, 57, 807-814.
138. Groebe, A.; Clarner, T.; Baumgartner, W.; Dang, J.; Beyer, C.; Kipp, M. Cuprizone treatment induces distinct demyelination, astrocytosis, and microglia cell invasion or proliferation in the mouse cerebellum. Cerebellum, 2009, 8, 163-174.
139. Pott, F.; Gingele, S.; Clarner, T.; Dang, J.; Baumgartner, W.; Beyer, C.; Kipp, M. Cuprizone effect on myelination, astrogliosis and microglia attraction in the mouse basal ganglia. Brain Res., 2009, 1305, 137-149.
140. Clarner, T.; Parabucki, A.; Beyer, C.; Kipp, M. Corticosteroids impair remyelination in the corpus callosum of cuprizone-treated mice. J. Neuroendocrinol., 2011, 23, 601-611.
141. Harsan, L.A.; Steibel, J.; Zaremba, A.; Agin, A.; Sapin, R.; Poulet, P.; Guignard, B.; Parizel, N.; Grucker, D.; Boehm, N.; Miller, R.H.; Ghandour, MS. Recovery from chronic demyelination by thyroid hormone therapy: myelinogenesis induction and assessment by diffusion tensor magnetic resonance imaging. J. Neurosci., 2008, 28, 14189-14201.
142. Pasquini, L.A.; Calatayud, C.A.; Bertone, Una, A.L.; Millet, V.; Pasquini, J.M.; Soto, EF. The neurotoxic effect of cuprizone on oligodendrocytes depends on the presence of pro-inflammatory cytokines secreted by microglia. Neurochem. Res., 2007, 32, 279-292.
143. Cammer, W. The neurotoxicant, cuprizone, retards the differentiation of oligodendrocytes in vitro. J. Neurol. Sci., 1999, 168, 116-120.
144. Manrique-Hoyos, N.; Jurgens, T.; Gronborg, M.; Kreutzfeldt, M.; Schedensack, M.; Kuhlmann, T.; Schrick, C.; Bruck, W.; Urlaub, H.; Simons, M.; Merkler, D. Late motor decline after accomplished remyelination: impact for progressive multiple sclerosis. Ann. Neurol., 2012, 71, 227-244.
145. Benetti, F.; Ventura, M.; Salmini, B.; Ceola, S.; Carbonera, D.; Mammi, S.; Zitolo, A.; D'Angelo, P.; Urso, E.; Maffia, M.; Salvato, B.; Spisni, E. Cuprizone neurotoxicity, copper deficiency and neurodegeneration. Neurotoxicology, 2010, 31, 509-517.
146. Venturini, G. Enzymic activities and sodium, potassium and copper concentrations in mouse brain and liver after cuprizone treatment in vivo. J. Neurochem., 1973, 21, 1147-1151.
147. Emerson, M.R.; Biswas, S.; LeVine, S.M. Cuprizone and piperonyl butoxide, proposed inhibitors of T-cell function, attenuate experimental allergic encephalomyelitis in SJL mice. J. Neuroimmunol., 2011, 19, 205-213.
148. Liu, L.; Darnall, L.; Hu, T.; Choi, K.; Lane, T.E.; Ransohoff, R.M. Myelin repair is accelerated by inactivating CXCR2 on nonhematopoietic cells. J. Neurosci., 2010, 30, 9074-9083.
149. Xiao, L.; Guo, D.; Hu, C.; Shen, W.; Shan, L.; Li, C.; Liu, X.; Yang, W.; Zhang, W.; He C. Diosgenin promotes oligodendrocyte progenitor cell differentiation through estrogen receptor-mediated ERK1/2 activation to accelerate remyelination. Glia, 2012, 60(7), 1037-1052.
150. Delarasse, C.; Daubas, P.; Mars, LT.; Vizler, C.; Gaspera, BD.; Decker, L.; Bauer, J.; Litzenburger, T.; Iglesias, A.; Schubart, A.; Dimitri, D.; Dierich, A.; LeMeur, M.; Roussel, G.; Nussbaum, J-L.; Amor, S.; Liblau, R.; Dautigny, A.; Pham-Dinh, D. Myelin/oligodendrocyte glycoprotein (MOG)-deficient mice reveal lack of immune tolerance to mog in wild-type mice. J. Clin. Invest., 2003, 11, 544-555.
151. Jagessar, SA.; Smith, PA.; Blezer, E.; Delarasse, C.; Pham-Dinh, D.; Laman, J.D.; Bauer, J.; Amor, S.; 't Hart, B. Autoimmunity against myelin oligodendrocyte glycoprotein is dispensable for the initiation although essential for the progression of chronic encephalomyelitis in common marmosets. J. Neuropathol. Exp. Neurol., 2008, 6, 326-340.
152. Ellmerich, S.; Takacs, K.; Mycko, M.; Waldner, H.; Wahi, F.; Boyton, R.; Baker, D.; Amor, S.; Hafler, D.; Kuchroo, V.; Altmann, DM. Disease-related epitope spread in a humanized T cell receptor transgenic model of multiple sclerosis. Eur. J. Immunol., 2004, 34, 1839-1848.
153. Ellmerich, S.; Mycko, M.; Takacs, K.; Waldner, H.; Wahid, F.N.; Boyton, R.J.; King, R.H.; Smith, P.A.; Amor, S.; Herlihy, A.H.; Hewitt, R.E.; Jutton, M.; Price, D.A.; Hafler, D.A.; Kuchroo, V.K.; Altmann, D.M. High incidence of spontaneous disease in an HLADR15 and TCR transgenic multiple sclerosis model. J. Immunol., 2005, 174, 1938-1946.
154. Lyons, J.A.; San, M.; Happ, M.P.; Cross, A.H. B cells are critical to induction of experimental allergic encephalomyelitis by protein but not by a short encephalitogenic peptide. Eur. J. Immunol., 1999, 29, 3432-3439.
155. Kim, S.S.; Richman, D.P.; Zamvil, S.S.; Agius, M.A. Accelerated central nervous system autoimmunity in BAFF-receptordeficient mice. J. Neurol. Sci., 2011, 306, 9-15.
156. Krishnamoorthy, G.; Lassmann, H.; Wekerle, H.; Holz, A. Spontaneous opticospinal encephalomyelitis in a double-transgenic mouse model of autoimmune T cell/B cell cooperation. J. Clin. Invest., 2006, 116, 2385-2392.
157. Morris-Downes, M.M.; Smith, P.A.; Piddlesden, S.; Rundle, J.L.; Baker, D.; Pham-Dinh, D.; Heijmans, N.; Amor, S. Pathological and regulatory effects of anti-myelin antibodies in experimental allergic encephalomyelitis in mice. J. Neuroimmunol., 2002, 125, 114-124.
158. Barnett, M.H.; Prineas, J.W. Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann. Neurol., 2004, 55, 458-468.
159. Pohl, H.B.; Porcheri, C.; Mueggler, T.; Bachmann, L.C.; Martino, G.; Riethmacher, D.; Franklin, R.J.; Rudin, M.; Suter, U. Genetically induced adult oligodendrocyte cell death is associated with poor myelin clearance, reduced remyelination, and axonal damage. J. Neurosci., 2011, 31, 1069-1080.
160. Locatelli, G.; Wörtge, S.; Buch, T.; Ingold, B.; Frommer, F.; Sobottka, B.; Krüger, M.; Karram, K.; Bühlmann, C.; Bechmann, I.; Heppner, F.L.; Waisman, A.; Becher, B. Primary oligodendrocyte death does not elicit anti-CNS immunity. Nat. Neurosci., 2012, 15, 543-550.
161. Ajami, B.; Bennett, J.L.; Krieger, C.; McNagny, K.M.; Rossi, F.M. Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat. Neurosci., 2011, 14, 1142-1149.
162. Ruckh, J.M.; Zhao, J.W.; Shadrach, J.L.; van Wijngaarden, P.; Rao, T.N.; Wagers, A.J.; Franklin, R.J. Rejuvenation of regeneration in the aging central nervous system. Cell Stem Cell, 2012, 10, 96-103.