Modeling multiple sclerosis in laboratory animals

Seminars in Immunopathology

Volumn 31, Issue 4, 2009, Pages 479-495

  Schreiner, Bettina ^a   Heppner, Frank L ^b   Becher, Burkhard ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Animal models; Autoimmunity; CD8; CTL; Cytokines; EAE; Gene targeting; IL 12; IL 18; IL 23; Immunopathology; In vivo; Multiple sclerosis; Mus musculus; TH1; TH17; Transgenic

Indexed keywords

CUPRIZONE; CYTOKINE; LIPOPOLYSACCHARIDE; LYSOPHOSPHATIDYLCHOLINE;

ALLERGIC ENCEPHALOMYELITIS; BLOOD BRAIN BARRIER; BRAIN DISEASE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DEMYELINATION; EXPERIMENTAL ANIMAL; EXPERIMENTAL MODEL; EXPERIMENTAL MONKEY; EXPERIMENTAL MOUSE; EXPERIMENTAL RAT; GOLD STANDARD; HISTOPATHOLOGY; HUMAN; IMMUNIZATION; KNOCKOUT MOUSE; LEUKOCYTE MIGRATION; MULTIPLE SCLEROSIS; MURINE ENCEPHALOMYELITIS VIRUS; NONHUMAN; OVARY INFLAMMATION; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; TRANSGENIC MOUSE;

ANIMALS; AUTOIMMUNITY; CYTOKINES; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; MICE; MICE, TRANSGENIC; MULTIPLE SCLEROSIS; SPINAL CORD;

EID: 73449102477     PISSN: 18632297     EISSN: 18632300     Source Type: Journal    
DOI: 10.1007/s00281-009-0181-4     Document Type: Review

References (228)

1. PK Olitsky RH Yager 1949 Experimental disseminated encephalomyelitis in white mice J Exp Med 90 213 224 1:STN:280:DyaH1M%2FjvVyksA%3D%3D 18137295
2. AM Brown DE McFarlin 1981 Relapsing experimental allergic encephalomyelitis in the SJL/J mouse Lab Invest 45 278 284 1:STN:280: DyaL38%2FhtFOrtw%3D%3D 6792424
3. RB Fritz CH Chou DE McFarlin 1983 Induction of experimental allergic encephalomyelitis in PL/J and (SJL/J x PL/J)F1 mice by myelin basic protein and its peptides: localization of a second encephalitogenic determinant J Immunol 130 191 194 1:STN:280:DyaL3s%2FlvVSrtQ%3D%3D 6183347
4. JL Trotter HB Clark KG Collins CL Wegeschiede JD Scarpellini 1987 Myelin proteolipid protein induces demyelinating disease in mice J Neurol Sci 79 173 188 1:CAS:528:DyaL2sXltFeltL0%3D 2440996
5. DS Linthicum JA Frelinger 1982 Acute autoimmune encephalomyelitis in mice. II. Susceptibility is controlled by the combination of H-2 and histamine sensitization genes J Exp Med 156 31 40 1:STN:280:DyaL383hsFKrsA%3D%3D 6806429
6. SM Kerfoot, et al. 2004 TLR4 contributes to disease-inducing mechanisms resulting in central nervous system autoimmune disease J Immunol 173 7070 7077 1:CAS:528:DC%2BD2cXhtVShsbvM 15557205
7. T Kamradt PD Soloway DL Perkins ML Gefter 1991 Pertussis toxin prevents the induction of peripheral T cell anergy and enhances the T cell response to an encephalitogenic peptide of myelin basic protein J Immunol 147 3296 3302 1:CAS:528:DyaK38XlslWmsQ%3D%3D 1719074
8. H Waldner M Collins VK Kuchroo 2004 Activation of antigen-presenting cells by microbial products breaks self tolerance and induces autoimmune disease J Clin Invest 113 990 997 1:CAS:528:DC%2BD2cXivFCqs7c%3D 15057305
9. CL Shive H Hofstetter L Arredondo C Shaw TG Forsthuber 2000 The enhanced antigen-specific production of cytokines induced by pertussis toxin is due to clonal expansion of T cells and not to altered effector functions of long-term memory cells Eur J Immunol 30 2422 2431 1:CAS:528:DC%2BD3cXlvFemsrY%3D 10940934
10. DM Muller MP Pender JM Greer 2000 A neuropathological analysis of experimental autoimmune encephalomyelitis with predominant brain stem and cerebellar involvement and differences between active and passive induction Acta Neuropathol 100 174 182 1:STN:280:DC%2BD3M%2Fmt1artQ%3D%3D 10963365
11. S Abromson-Leeman, et al. 2004 T-cell properties determine disease site, clinical presentation, and cellular pathology of experimental autoimmune encephalomyelitis Am J Pathol 165 1519 1533 1:CAS:528:DC%2BD2cXhtVCgsLfF 15509523
12. C Teuscher, et al. 2004 Gender, age, and season at immunization uniquely influence the genetic control of susceptibility to histopathological lesions and clinical signs of experimental allergic encephalomyelitis: implications for the genetics of multiple sclerosis Am J Pathol 165 1593 1602 15509529
13. ME Smith NL Eller HF McFarland MK Racke CS Raine 1999 Age dependence of clinical and pathological manifestations of autoimmune demyelination. Implications for multiple sclerosis Am J Pathol 155 1147 1161 1:STN:280:DyaK1MvksFegsQ%3D%3D 10514398
14. PD Fillmore, et al. 2003 Genetic analysis of the influence of neuroantigen-complete Freund's adjuvant emulsion structures on the sexual dimorphism and susceptibility to experimental allergic encephalomyelitis Am J Pathol 163 1623 1632 1:CAS:528:DC%2BD3sXotlegtLs%3D 14507669
15. JA Maatta PT Nygardas AE Hinkkanen 2000 Enhancement of experimental autoimmune encephalomyelitis severity by ultrasound emulsification of antigen/adjuvant in distinct strains of mice Scand J Immunol 51 87 90 1:CAS:528:DC%2BD3cXhtFaku7o%3D 10632981
16. AR Oliver GM Lyon NH Ruddle 2003 Rat and human myelin oligodendrocyte glycoproteins induce experimental autoimmune encephalomyelitis by different mechanisms in C57BL/6 mice J Immunol 171 462 468 1:CAS:528:DC%2BD3sXks12jurk%3D 12817031
17. RA Sobel 2000 Genetic and epigenetic influence on EAE phenotypes induced with different encephalitogenic peptides J Neuroimmunol 108 45 52 1:CAS:528:DC%2BD3cXkvFSgsr0%3D 10900336
18. I Tsunoda LQ Kuang DJ Theil RS Fujinami 2000 Antibody association with a novel model for primary progressive multiple sclerosis: induction of relapsing-remitting and progressive forms of EAE in H2s mouse strains Brain Pathol 10 402 418 1:CAS:528:DC%2BD3cXltFSjtLY%3D 10885659
19. CB Pettinelli DE McFarlin 1981 Adoptive transfer of experimental allergic encephalomyelitis in SJL/J mice after in vitro activation of lymph node cells by myelin basic protein: requirement for Lyt 1+ 2- T lymphocytes J Immunol 127 1420 1423 1:STN:280:DyaL38%2FgvV2ntA%3D%3D 6168690
20. S Zamvil, et al. 1985 T-cell clones specific for myelin basic protein induce chronic relapsing paralysis and demyelination Nature 317 355 358 1:CAS:528:DyaL2MXlslKrt7o%3D 2413363
21. ES Huseby, et al. 2001 A pathogenic role for myelin-specific CD8(+) T cells in a model for multiple sclerosis J Exp Med 194 669 676 1:CAS:528:DC%2BD3MXms1KhsLk%3D 11535634
22. D Sun, et al. 2001 Myelin antigen-specific CD8+ T cells are encephalitogenic and produce severe disease in C57BL/6 mice J Immunol 166 7579 7587 1:CAS:528:DC%2BD3MXksVOmsLo%3D 11390514
23. CL Langrish, et al. 2005 IL-23 drives a pathogenic T cell population that induces autoimmune inflammation J Exp Med 201 233 240 1:CAS:528: DC%2BD2MXot12mtA%3D%3D 15657292
24. IM Stromnes LM Cerretti D Liggitt RA Harris JM Goverman 2008 Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells Nat Med 14 337 342 1:CAS:528:DC%2BD1cXivFOrtLo%3D 18278054
25. A Flugel, et al. 2001 Migratory activity and functional changes of green fluorescent effector cells before and during experimental autoimmune encephalomyelitis Immunity 14 547 560 1:CAS:528:DC%2BD3MXktVantL0%3D 11371357
26. EJ McMahon SL Bailey CV Castenada H Waldner SD Miller 2005 Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis Nat Med 11 335 339 1:CAS:528:DC%2BD2MXhvVSqsrs%3D 15735651
27. JJ Lafaille K Nagashima M Katsuki S Tonegawa 1994 High incidence of spontaneous autoimmune encephalomyelitis in immunodeficient anti-myelin basic protein T cell receptor transgenic mice Cell 78 399 408 1:CAS:528: DyaK2cXlsFGmt7s%3D 7520367
28. D Olivares-Villagomez Y Wang JJ Lafaille 1998 Regulatory CD4(+) T cells expressing endogenous T cell receptor chains protect myelin basic protein-specific transgenic mice from spontaneous autoimmune encephalomyelitis J Exp Med 188 1883 1894 1:CAS:528:DyaK1cXnsVKksrw%3D 9815266
29. LS Madsen, et al. 1999 A humanized model for multiple sclerosis using HLA-DR2 and a human T-cell receptor Nat Genet 23 343 347 1:CAS:528: DyaK1MXnt1Gns7Y%3D 10610182
30. S Ellmerich, et al. 2005 High incidence of spontaneous disease in an HLA-DR15 and TCR transgenic multiple sclerosis model J Immunol 174 1938 1946 1:CAS:528:DC%2BD2MXhtV2rs74%3D 15699121
31. JA Quandt, et al. 2004 Unique clinical and pathological features in HLA-DRB1*0401-restricted MBP 111-129-specific humanized TCR transgenic mice J Exp Med 200 223 234 1:CAS:528:DC%2BD2cXmtFSqs7o%3D 15263029
32. H Waldner MJ Whitters RA Sobel M Collins VK Kuchroo 2000 Fulminant spontaneous autoimmunity of the central nervous system in mice transgenic for the myelin proteolipid protein-specific T cell receptor Proc Natl Acad Sci U S A 97 3412 3417 1:CAS:528:DC%2BD3cXitlWqt74%3D 10737797
33. E Bettelli, et al. 2003 Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis J Exp Med 197 1073 1081 1:CAS:528:DC%2BD3sXjs1ygs70%3D 12732654
34. E Bettelli D Baeten A Jager RA Sobel VK Kuchroo 2006 Myelin oligodendrocyte glycoprotein-specific T and B cells cooperate to induce a Devic-like disease in mice J Clin Invest 116 2393 2402 1:CAS:528: DC%2BD28Xps1SgsLs%3D 16955141
35. G Krishnamoorthy H Lassmann H Wekerle A Holz 2006 Spontaneous opticospinal encephalomyelitis in a double-transgenic mouse model of autoimmune T cell/B cell cooperation J Clin Invest 116 2385 2392 1:CAS:528: DC%2BD28Xps1SgsLo%3D 16955140
36. MK Waldor, et al. 1985 Reversal of experimental allergic encephalomyelitis with monoclonal antibody to a T-cell subset marker Science 227 415 417 1:STN:280:DyaL2M%2FptVCnsQ%3D%3D 3155574
37. S Sriram L Steinman 1983 Anti I-A antibody suppresses active encephalomyelitis: treatment model for diseases linked to IR genes J Exp Med 158 1362 1367 1:STN:280:DyaL2c%2FgvFGltg%3D%3D 6194246
38. BA Jameson JM McDonnell JC Marini R Korngold 1994 A rationally designed CD4 analogue inhibits experimental allergic encephalomyelitis Nature 368 744 746 1:CAS:528:DyaK2cXjtFGnsLs%3D 8152486
39. A Seamons A Perchellet J Goverman 2003 Immune tolerance to myelin proteins Immunol Res 28 201 221 1:CAS:528:DC%2BD2cXltVaisw%3D%3D 14713715
40. SM Tompkins, et al. 2002 De novo central nervous system processing of myelin antigen is required for the initiation of experimental autoimmune encephalomyelitis J Immunol 168 4173 4183 1:CAS:528:DC%2BD38XivV2isbg%3D 11937578
41. WF Hickey H Kimura 1988 Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo Science 239 290 292 1:STN:280:DyaL1c%2FpvFGisw%3D%3D 3276004
42. M Greter, et al. 2005 Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis Nat Med 11 328 334 1:CAS:528: DC%2BD2MXhvVSqsr4%3D 15735653
43. B Becher I Bechmann M Greter 2006 Antigen presentation in autoimmunity and CNS inflammation: how T lymphocytes recognize the brain J Mol Med 84 532 543 1:CAS:528:DC%2BD28XmsFSmurw%3D 16773356
44. B Becher A Prat JP Antel 2000 Brain-immune connection: immuno-regulatory properties of CNS-resident cells Glia 29 293 304 1:STN:280: DC%2BD3c7hvFaisQ%3D%3D 10652440
45. FL Heppner, et al. 2005 Experimental autoimmune encephalomyelitis repressed by microglial paralysis Nat Med 11 146 152 1:CAS:528: DC%2BD2MXpvF2msg%3D%3D 15665833
46. B Becher BG Durell AV Miga WF Hickey RJ Noelle 2001 The clinical course of experimental autoimmune encephalomyelitis and inflammation is controlled by the expression of CD40 within the central nervous system J Exp Med 193 967 974 1:CAS:528:DC%2BD3MXivFOhtrk%3D 11304557
47. B Becher BG Durell RJ Noelle 2003 IL-23 produced by CNS-resident cells controls T cell encephalitogenicity during the effector phase of experimental autoimmune encephalomyelitis J Clin Invest 112 1186 1191 1:CAS:528: DC%2BD3sXotlWis7g%3D 14561703
48. M Prinz, et al. 2006 Innate immunity mediated by TLR9 modulates pathogenicity in an animal model of multiple sclerosis J Clin Invest 116 456 464 1:CAS:528:DC%2BD28Xht1Sqs7o%3D 16440059
49. J De Keyser E Zeinstra E Frohman 2003 Are astrocytes central players in the pathophysiology of multiple sclerosis? Arch Neurol 60 132 136 12533101
50. JL Ridet SK Malhotra A Privat FH Gage 1997 Reactive astrocytes: cellular and molecular cues to biological function Trends Neurosci 20 570 577 1:CAS:528:DyaK2sXnvFWnt7c%3D 9416670
51. A Volterra J Meldolesi 2005 Astrocytes, from brain glue to communication elements: the revolution continues Nat Rev Neurosci 6 626 640 1:CAS:528:DC%2BD2MXmvVGht7Y%3D 16025096
52. SL Bailey B Schreiner EJ McMahon SD Miller 2007 CNS myeloid DCs presenting endogenous myelin peptides 'preferentially' polarize CD4+ T(H)-17 cells in relapsing EAE Nat Immunol 8 172 180 1:CAS:528:DC%2BD2sXnt1KitQ%3D%3D 17206145
53. BL McRae CL Vanderlugt MC Dal Canto SD Miller 1995 Functional evidence for epitope spreading in the relapsing pathology of experimental autoimmune encephalomyelitis J Exp Med 182 75 85 1:CAS:528:DyaK2MXmsVCks7g%3D 7540658
54. CL Vanderlugt, et al. 2000 Pathologic role and temporal appearance of newly emerging autoepitopes in relapsing experimental autoimmune encephalomyelitis J Immunol 164 670 678 1:CAS:528:DC%2BD3cXlt1Cnsw%3D%3D 10623809
55. BH Waksman RD Adams 1956 A comparative study of experimental allergic neuritis in the rabbit, guinea pig, and mouse J Neuropathol Exp Neurol 15 293 334 1:CAS:528:DyaG28Xotl2nsA%3D%3D 13346395
56. BH Waksman 1960 The distribution of experimental auto-allergic lesions. Its relation to the distribution of small veins Am J Pathol 37 673 693 1:STN:280:DyaF3c7gt1ynsg%3D%3D 13782611
57. R Lebar JM Boutry C Vincent R Robineaux GA Voisin 1976 Studies on autoimmune encephalomyelitis in the guinea pig. II. An in vitro investigation on the nature, properties, and specificity of the serum-demyelinating factor J Immunol 116 1439 1446 1:STN:280:DyaE287pt1Chuw%3D%3D 58035
58. CP Genain, et al. 1995 Antibody facilitation of multiple sclerosis-like lesions in a nonhuman primate J Clin Invest 96 2966 2974 1:CAS:528: DyaK28XmtVemsg%3D%3D 8675668
59. HJ Schluesener RA Sobel C Linington HL Weiner 1987 A monoclonal antibody against a myelin oligodendrocyte glycoprotein induces relapses and demyelination in central nervous system autoimmune disease J Immunol 139 4016 4021 1:CAS:528:DyaL1cXlsVaitw%3D%3D 3500978
60. BA t Hart, et al. 2004 Modelling of multiple sclerosis: lessons learned in a non-human primate Lancet Neurol 3 588 597
61. CP Genain, et al. 1994 In healthy primates, circulating autoreactive T cells mediate autoimmune disease J Clin Invest 94 1339 1345 1:STN:280: DyaK2czmsFajtA%3D%3D 7521889
62. AG Baxter 2007 The origin and application of experimental autoimmune encephalomyelitis Nat Rev Immunol 7 904 912 1:CAS:528:DC%2BD2sXht1WgsL7J 17917672
63. W Bruck T Kuhlmann C Stadelmann 2003 Remyelination in multiple sclerosis J Neurol Sci 206 181 185 12559508
64. C Lucchinetti, et al. 2000 Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination Ann Neurol 47 707 717 1:STN:280:DC%2BD3czgvFektA%3D%3D 10852536
65. T Kuhlmann H Lassmann W Bruck 2008 Diagnosis of inflammatory demyelination in biopsy specimens: a practical approach Acta Neuropathol 115 275 287 18175128
66. SD Miller WJ Karpus 2007 Experimental autoimmune encephalomyelitis in the mouse Curr Protoc Immunol 15 15.1
67. CM Brodmerkel K Vaddi 2003 Transgenic animals in inflammatory disease models Curr Opin Biotechnol 14 652 658 1:CAS:528:DC%2BD3sXps1Oqtbs%3D 14662397
68. T Owens H Wekerle J Antel 2001 Genetic models for CNS inflammation Nat Med 7 161 166 1:CAS:528:DC%2BD3MXhtVygsr8%3D 11175845
69. L Morel 2004 Mouse models of human autoimmune diseases: essential tools that require the proper controls PLoS Biol 2 E241 15314657
70. EH Leiter 2002 Mice with targeted gene disruptions or gene insertions for diabetes research: problems, pitfalls, and potential solutions Diabetologia 45 296 308 1:CAS:528:DC%2BD38XitVejurY%3D 11914735
71. L Steinman 1997 Some misconceptions about understanding autoimmunity through experiments with knockouts J Exp Med 185 2039 2041 1:CAS:528: DyaK2sXktVemsb4%3D 9221283
72. Y Yu A Bradley 2001 Engineering chromosomal rearrangements in mice Nat Rev Genet 2 780 790 1:CAS:528:DC%2BD38Xmt1Wguro%3D 11584294
73. MK Thomas, et al. 2001 Development of diabetes mellitus in aging transgenic mice following suppression of pancreatic homeoprotein IDX-1 J Clin Invest 108 319 329 1:CAS:528:DC%2BD3MXlt1KltrY%3D 11457885
74. PG Hirrlinger A Scheller C Braun J Hirrlinger F Kirchhoff 2006 Temporal control of gene recombination in astrocytes by transgenic expression of the tamoxifen-inducible DNA recombinase variant CreERT2 Glia 54 11 20 16575885
75. F Tronche, et al. 1999 Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety Nat Genet 23 99 103 1:CAS:528:DyaK1MXlvFWht78%3D 10471508
76. G Krishnamoorthy A Holz H Wekerle 2007 Experimental models of spontaneous autoimmune disease in the central nervous system J Mol Med 85 1161 1173 1:CAS:528:DC%2BD2sXhtFyrurzE 17569024
77. T Buch, et al. 2005 A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration Nat Methods 2 419 426 1:CAS:528:DC%2BD2MXktlWhs74%3D 15908920
78. J Luo, et al. 2007 Glia-dependent TGF-beta signaling, acting independently of the TH17 pathway, is critical for initiation of murine autoimmune encephalomyelitis J Clin Invest 117 3306 3315 1:CAS:528: DC%2BD2sXht12isrjM 17965773
79. M Mohrs K Shinkai K Mohrs RM Locksley 2001 Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter Immunity 15 303 311 1:CAS:528: DC%2BD3MXmsF2itrg%3D 11520464
80. E Bettelli, et al. 2006 Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells Nature 441 235 238 1:CAS:528:DC%2BD28XksVGns7g%3D 16648838
81. JD Fontenot, et al. 2005 Regulatory T cell lineage specification by the forkhead transcription factor foxp3 Immunity 22 329 341 1:CAS:528: DC%2BD2MXjt1Ohsbk%3D 15780990
82. TR Mosmann H Cherwinski MW Bond MA Giedlin RL Coffman 1986 Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins J Immunol 136 2348 2357 1:CAS:528: DyaL28XhvVClsbk%3D 2419430
83. I Gutcher B Becher 2007 APC-derived cytokines and T cell polarization in autoimmune inflammation J Clin Invest 117 1119 1127 1:CAS:528: DC%2BD2sXlt1Omtr8%3D 17476341
84. M Comabella, et al. 1998 Elevated interleukin-12 in progressive multiple sclerosis correlates with disease activity and is normalized by pulse cyclophosphamide therapy J Clin Invest 102 671 678 1:CAS:528:DyaK1cXlsFartbs%3D 9710434
85. A O'Garra L Steinman K Gijbels 1997 CD4+ T-cell subsets in autoimmunity Curr Opin Immunol 9 872 883 9492992
86. DO Willenborg S Fordham CC Bernard WB Cowden IA Ramshaw 1996 IFN-gamma plays a critical down-regulatory role in the induction and effector phase of myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis J Immunol 157 3223 3227 1:CAS:528:DyaK28Xmtlahtbw%3D 8871615
87. B Becher BG Durell RJ Noelle 2002 Experimental autoimmune encephalitis and inflammation in the absence of interleukin-12 J Clin Invest 110 493 497 1:CAS:528:DC%2BD38XmsVSiurc%3D 12189243
88. I Gutcher E Urich K Wolter M Prinz B Becher 2006 Interleukin 18-independent engagement of interleukin 18 receptor-alpha is required for autoimmune inflammation Nat Immunol 7 946 953 1:CAS:528:DC%2BD28XotlCitbg%3D 16906165
89. K Frei, et al. 1997 Tumor necrosis factor alpha and lymphotoxin alpha are not required for induction of acute experimental autoimmune encephalomyelitis J Exp Med 185 2177 2182 1:CAS:528:DyaK2sXktVers7w%3D 9182689
90. B Gran, et al. 2002 IL-12p35-deficient mice are susceptible to experimental autoimmune encephalomyelitis: evidence for redundancy in the IL-12 system in the induction of central nervous system autoimmune demyelination J Immunol 169 7104 7110 1:CAS:528:DC%2BD38XpsFGjtr8%3D 12471147
91. DJ Cua, et al. 2003 Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain Nature 421 744 748 1:CAS:528:DC%2BD3sXhsV2rsbs%3D 12610626
92. T Korn E Bettelli M Oukka VK Kuchroo 2009 IL-17 and Th17 Cells Annu Rev Immunol 27 485 517 1:CAS:528:DC%2BD1MXlsFSltrY%3D 19132915
93. HH Hofstetter, et al. 2005 Therapeutic efficacy of IL-17 neutralization in murine experimental autoimmune encephalomyelitis Cell Immunol 237 123 130 1:CAS:528:DC%2BD28Xls1ahsg%3D%3D 16386239
94. Y Komiyama, et al. 2006 IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis J Immunol 177 566 573 1:CAS:528:DC%2BD28XlvV2ntbg%3D 16785554
95. S Haak, et al. 2009 IL-17A and IL-17F do not contribute vitally to autoimmune neuro-inflammation in mice J Clin Invest 119 61 69 1:CAS:528:DC%2BD1MXmtFChsw%3D%3D 19075395
96. K Kreymborg, et al. 2007 IL-22 is expressed by Th17 cells in an IL-23-dependent fashion, but not required for the development of autoimmune encephalomyelitis J Immunol 179 8098 8104 1:CAS:528:DC%2BD2sXhtlyitrbN 18056351
97. MJ McGeachy, et al. 2009 The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo Nat Immunol 10 314 324 1:CAS:528:DC%2BD1MXht1ehtLw%3D 19182808
98. G Gyülvészi S Haak B Becher 2009 Eur J Immunol 39 7 1864 1869 19544494
99. WF Hickey 2001 Basic principles of immunological surveillance of the normal central nervous system Glia 36 118 124 1:STN:280:DC%2BD3MrkvVylsA%3D%3D 11596120
100. I Bechmann I Galea VH Perry 2007 What is the blood-brain barrier (not)? Trends Immunol 28 5 11 1:CAS:528:DC%2BD2sXhsFCjtQ%3D%3D 17140851
101. GL Suidan JR McDole Y Chen I Pirko AJ Johnson 2008 Induction of blood brain barrier tight junction protein alterations by CD8 T cells PLoS ONE 3 e3037 18725947
102. SR Parathath S Parathath SE Tsirka 2006 Nitric oxide mediates neurodegeneration and breakdown of the blood-brain barrier in tPA-dependent excitotoxic injury in mice J Cell Sci 119 339 349 1:CAS:528:DC%2BD28Xhs1eitb8%3D 16410551
103. M Yepes, et al. 2003 Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein J Clin Invest 112 1533 1540 1:CAS:528:DC%2BD3sXptFWqtL8%3D 14617754
104. C Coisne W Mao B Engelhardt 2009 Cutting edge: natalizumab blocks adhesion but not initial contact of human T cells to the blood-brain barrier in vivo in an animal model of multiple sclerosis J Immunol 182 5909 5913 1:CAS:528:DC%2BD1MXltlygu7c%3D 19414741
105. A Doring M Wild D Vestweber U Deutsch B Engelhardt 2007 E- and P-selectin are not required for the development of experimental autoimmune encephalomyelitis in C57BL/6 and SJL mice J Immunol 179 8470 8479 18056394
106. SM Kerfoot P Kubes 2002 Overlapping roles of P-selectin and alpha 4 integrin to recruit leukocytes to the central nervous system in experimental autoimmune encephalomyelitis J Immunol 169 1000 1006 1:CAS:528: DC%2BD38XlsVWjsL8%3D 12097407
107. P Vajkoczy M Laschinger B Engelhardt 2001 Alpha4-integrin-VCAM-1 binding mediates G protein-independent capture of encephalitogenic T cell blasts to CNS white matter microvessels J Clin Invest 108 557 565 1:CAS:528: DC%2BD3MXmt1Sqtrg%3D 11518729
108. DC Bullard, et al. 2007 Intercellular adhesion molecule-1 expression is required on multiple cell types for the development of experimental autoimmune encephalomyelitis J Immunol 178 851 857 1:CAS:528:DC%2BD2sXhvVajtQ%3D%3D 17202346
109. R Cayrol, et al. 2008 Activated leukocyte cell adhesion molecule promotes leukocyte trafficking into the central nervous system Nat Immunol 9 137 145 1:CAS:528:DC%2BD1cXovV2mtA%3D%3D 18157132
110. CH Polman, et al. 2006 A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis N Engl J Med 354 899 910 1:CAS:528:DC%2BD28XitVertL4%3D 16510744
111. RA Rudick, et al. 2006 Natalizumab plus interferon beta-1a for relapsing multiple sclerosis N Engl J Med 354 911 923 1:CAS:528:DC%2BD28XitVertLw%3D 16510745
112. C Wu, et al. 2009 Endothelial basement membrane laminin alpha5 selectively inhibits T lymphocyte extravasation into the brain Nat Med 15 519 527 1:CAS:528:DC%2BD1MXltValt78%3D 19396173
113. C Alt M Laschinger B Engelhardt 2002 Functional expression of the lymphoid chemokines CCL19 (ELC) and CCL 21 (SLC) at the blood-brain barrier suggests their involvement in G-protein-dependent lymphocyte recruitment into the central nervous system during experimental autoimmune encephalomyelitis Eur J Immunol 32 2133 2144 1:CAS:528:DC%2BD38XmslSlt74%3D 12209625
114. H Toft-Hansen, et al. 2006 Metalloproteinases control brain inflammation induced by pertussis toxin in mice overexpressing the chemokine CCL2 in the central nervous system J Immunol 177 7242 7249 1:CAS:528:DC%2BD28XhtFGrtrnP 17082642
115. AA Babcock WA Kuziel S Rivest T Owens 2003 Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS J Neurosci 23 7922 7930 1:CAS:528:DC%2BD3sXmvFGhu78%3D 12944523
116. AR Glabinski M Tani VK Tuohy RJ Tuthill RM Ransohoff 1995 Central nervous system chemokine mRNA accumulation follows initial leukocyte entry at the onset of acute murine experimental autoimmune encephalomyelitis Brain Behav Immun 9 315 330 1:CAS:528:DyaK28Xps1yrtQ%3D%3D 8903849
117. S Agrawal, et al. 2006 Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis J Exp Med 203 1007 1019 1:CAS:528:DC%2BD28Xjsl2isLw%3D 16585265
118. DA Hafler, et al. 2007 Risk alleles for multiple sclerosis identified by a genome wide study N Engl J Med 357 851 862 1:CAS:528:DC%2BD2sXpvVyltrY%3D 17660530
119. L Steinman 1996 Multiple sclerosis: a coordinated immunological attack against myelin in the central nervous system Cell 85 299 302 1:CAS:528:DyaK28XivVyrs74%3D 8616884
120. SL Hauser, et al. 1986 Immunohistochemical analysis of the cellular infiltrate in multiple sclerosis lesions Ann Neurol 19 578 587 1:STN:280:DyaL283mslCgug%3D%3D 3524414
121. J Booss MM Esiri WW Tourtellotte DY Mason 1983 Immunohistological analysis of T lymphocyte subsets in the central nervous system in chronic progressive multiple sclerosis J Neurol Sci 62 219 232 1:STN:280: DyaL2c7jslOjtQ%3D%3D 6607973
122. MP Crawford, et al. 2004 High prevalence of autoreactive, neuroantigen-specific CD8+ T cells in multiple sclerosis revealed by novel flow cytometric assay Blood 103 4222 4231 1:CAS:528:DC%2BD2cXkvVyit7c%3D 14976054
123. H Jiang NS Braunstein B Yu R Winchester L Chess 2001 CD8+ T cells control the TH phenotype of MBP-reactive CD4+ T cells in EAE mice Proc Natl Acad Sci U S A 98 6301 6306 1:CAS:528:DC%2BD3MXktVWksb8%3D 11353822
124. H Babbe, et al. 2000 Clonal expansions of CD8(+) T cells dominate the T cell infiltrate in active multiple sclerosis lesions as shown by micromanipulation and single cell polymerase chain reaction J Exp Med 192 393 404 1:CAS:528:DC%2BD3cXlsFygt7g%3D 10934227
125. Q Ji J Goverman 2007 Experimental autoimmune encephalomyelitis mediated by CD8+ T cells Ann N Y Acad Sci 1103 157 166 1:CAS:528:DC%2BD2sXmt12rtbo%3D 17376824
126. ML Ford BD Evavold 2005 Specificity, magnitude, and kinetics of MOG-specific CD8+ T cell responses during experimental autoimmune encephalomyelitis Eur J Immunol 35 76 85 1:CAS:528:DC%2BD2MXnvFaqtw%3D%3D 15593305
127. N Najafian, et al. 2003 Regulatory functions of CD8+CD28- T cells in an autoimmune disease model J Clin Invest 112 1037 1048 1:CAS:528: DC%2BD3sXnvFGrsLk%3D 14523041
128. H Jiang, et al. 2003 Regulatory CD8+ T cells fine-tune the myelin basic protein-reactive T cell receptor V beta repertoire during experimental autoimmune encephalomyelitis Proc Natl Acad Sci U S A 100 8378 8383 1:CAS:528:DC%2BD3sXlsFGntL4%3D 12824465
129. H Jiang SI Zhang B Pernis 1992 Role of CD8+ T cells in murine experimental allergic encephalomyelitis Science 256 1213 1215 1:STN:280:DyaK383ntFamtw%3D%3D 1375398
130. I Medana MA Martinic H Wekerle H Neumann 2001 Transection of major histocompatibility complex class I-induced neurites by cytotoxic T lymphocytes Am J Pathol 159 809 815 1:CAS:528:DC%2BD3MXnt12ms7Y%3D 11549572
131. SB Su, et al. 2005 Essential role of the MyD88 pathway, but nonessential roles of TLRs 2, 4, and 9, in the adjuvant effect promoting Th1-mediated autoimmunity J Immunol 175 6303 6310 1:CAS:528:DC%2BD2MXhtF2jur7P 16272281
132. HC Yip, et al. 1999 Adjuvant-guided type-1 and type-2 immunity: infectious/noninfectious dichotomy defines the class of response J Immunol 162 3942 3949 1:CAS:528:DyaK1MXitFKjsb4%3D 10201913
133. M Brisebois SP Zehntner J Estrada T Owens S Fournier 2006 A pathogenic role for CD8+ T cells in a spontaneous model of demyelinating disease J Immunol 177 2403 2411 1:CAS:528:DC%2BD28Xns1Khu74%3D 16888002
134. CW Ip, et al. 2006 Immune cells contribute to myelin degeneration and axonopathic changes in mice overexpressing proteolipid protein in oligodendrocytes J Neurosci 26 8206 8216 1:CAS:528:DC%2BD28XosVehsrs%3D 16885234
135. A Cornet, et al. 2001 Enterocolitis induced by autoimmune targeting of enteric glial cells: a possible mechanism in Crohn's disease? Proc Natl Acad Sci U S A 98 13306 13311 1:CAS:528:DC%2BD3MXosFygtLw%3D 11687633
136. J Cabarrocas J Bauer E Piaggio R Liblau H Lassmann 2003 Effective and selective immune surveillance of the brain by MHC class I-restricted cytotoxic T lymphocytes Eur J Immunol 33 1174 1182 1:CAS:528:DC%2BD3sXjvFOqu7g%3D 12731042
137. A Perchellet I Stromnes JM Pang J Goverman 2004 CD8+ T cells maintain tolerance to myelin basic protein by 'epitope theft' Nat Immunol 5 606 614 1:CAS:528:DC%2BD2cXkt1Ont7k%3D 15146180
138. K Baur, et al. 2008 Antiviral CD8 T cells recognize Borna disease virus antigen transgenically expressed in either neurons or astrocytes J Virol 82 3099 3108 1:CAS:528:DC%2BD1cXjtVaru7w%3D 18184705
139. A Saxena, et al. 2008 Cutting edge: multiple sclerosis-like lesions induced by effector CD8 T cells recognizing a sequestered antigen on oligodendrocytes J Immunol 181 1617 1621 1:CAS:528:DC%2BD1cXos12gur0%3D 18641296
140. I Galea, et al. 2007 An antigen-specific pathway for CD8 T cells across the blood-brain barrier J Exp Med 204 2023 2030 1:CAS:528:DC%2BD2sXhtVWnurjM 17682068
141. SY Na, et al. 2008 Naive CD8 T-cells initiate spontaneous autoimmunity to a sequestered model antigen of the central nervous system Brain 131 2353 2365 18669487
142. LT Mars, et al. 2007 CD8 T cell responses to myelin oligodendrocyte glycoprotein-derived peptides in humanized HLA-A*0201-transgenic mice J Immunol 179 5090 5098 1:CAS:528:DC%2BD2sXhtFWitrvN 17911594
143. MA Friese, et al. 2008 Opposing effects of HLA class I molecules in tuning autoreactive CD8+ T cells in multiple sclerosis Nat Med 14 1227 1235 1:CAS:528:DC%2BD1cXhtlCjtL7K 18953350
144. C Munz JD Lunemann MT Getts SD Miller 2009 Antiviral immune responses: triggers of or triggered by autoimmunity? Nat Rev Immunol 9 246 258 19319143
145. CF Evans MS Horwitz MV Hobbs MB Oldstone 1996 Viral infection of transgenic mice expressing a viral protein in oligodendrocytes leads to chronic central nervous system autoimmune disease J Exp Med 184 2371 2384 1:CAS:528:DyaK2sXjsVSn 8976191
146. JK Olson JL Croxford MA Calenoff MC Dal Canto SD Miller 2001 A virus-induced molecular mimicry model of multiple sclerosis J Clin Invest 108 311 8 1:CAS:528:DC%2BD3MXlt1Kltrk%3D 11457884
147. EA Butz MJ Bevan 1998 Massive expansion of antigen-specific CD8+ T cells during an acute virus infection Immunity 8 167 175 1:CAS:528:DyaK1cXhsVCiu70%3D 9491998
148. K Murali-Krishna, et al. 1998 Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection Immunity 8 177 187 1:CAS:528:DyaK1cXhsVChsr4%3D 9491999
149. JL Croxford AM Ercolini M Degutes SD Miller 2006 Structural requirements for initiation of cross-reactivity and CNS autoimmunity with a PLP139-151 mimic peptide derived from murine hepatitis virus Eur J Immunol 36 2671 2680 1:CAS:528:DC%2BD28XhtFGqtrfJ 16981179
150. JS Haring LL Pewe S Perlman 2002 Bystander CD8 T cell-mediated demyelination after viral infection of the central nervous system J Immunol 169 1550 1555 1:CAS:528:DC%2BD38XlslWhtL0%3D 12133983
151. AA Dandekar D Anghelina S Perlman 2004 Bystander CD8 T-cell-mediated demyelination is interferon-gamma-dependent in a coronavirus model of multiple sclerosis Am J Pathol 164 363 369 1:CAS:528:DC%2BD2cXhsFGqs74%3D 14742242
152. AM Ercolini SD Miller 2009 The role of infections in autoimmune disease Clin Exp Immunol 155 1 15 1:CAS:528:DC%2BD1MXhsFCgtL4%3D 19076824
153. MC Dal Canto HL Lipton 1975 Primary demyelination in Theiler's virus infection. An ultrastructural study Lab Invest 33 626 637 1:STN:280: DyaE28%2FntlKgtA%3D%3D 1202282
154. HL Lipton 1975 Theiler's virus infection in mice: an unusual biphasic disease process leading to demyelination Infect Immun 11 1147 1155 1:STN:280:DyaE2M7jt1GrsA%3D%3D 164412
155. MC Dal Canto HL Lipton 1982 Ultrastructural immunohistochemical localization of virus in acute and chronic demyelinating Theiler's virus infection Am J Pathol 106 20 29 1:STN:280:DyaL387htFWiuw%3D%3D 6275708
156. HL Lipton G Twaddle ML Jelachich 1995 The predominant virus antigen burden is present in macrophages in Theiler's murine encephalomyelitis virus-induced demyelinating disease J Virol 69 2525 2533 1:CAS:528: DyaK2MXksVSmur4%3D 7884902
157. M Trottier P Kallio W Wang HL Lipton 2001 High numbers of viral RNA copies in the central nervous system of mice during persistent infection with Theiler's virus J Virol 75 7420 7428 1:CAS:528:DC%2BD3MXlsFKkur0%3D 11462014
158. C Aubert M Chamorro M Brahic 1987 Identification of Theiler's virus infected cells in the central nervous system of the mouse during demyelinating disease Microb Pathog 3 319 326 1:STN:280:DyaL1M%2FntValuw%3D%3D 2849023
159. M Rodriguez JL Leibowitz PW Lampert 1983 Persistent infection of oligodendrocytes in Theiler's virus-induced encephalomyelitis Ann Neurol 13 426 433 1:STN:280:DyaL3s7ns12msg%3D%3D 6340596
160. L Zheng MA Calenoff MC Dal Canto 2001 Astrocytes, not microglia, are the main cells responsible for viral persistence in Theiler's murine encephalomyelitis virus infection leading to demyelination J Neuroimmunol 118 256 267 1:CAS:528:DC%2BD3MXlslCntL0%3D 11498260
161. M Rodriguez 1985 Virus-induced demyelination in mice: "dying back" of oligodendrocytes Mayo Clin Proc 60 433 438 1:STN:280: DyaL2M3jvFWntQ%3D%3D 4040195
162. RP Roos R Wollmann 1984 DA strain of Theiler's murine encephalomyelitis virus induces demyelination in nude mice Ann Neurol 15 494 499 1:STN:280:DyaL2c3ivF2iuw%3D%3D 6732198
163. MH Kang EY So H Park BS Kim 2008 Replication of Theiler's virus requires NF-kappa B-activation: higher viral replication and spreading in astrocytes from susceptible mice Glia 56 942 953 18383344
164. JP Palma BS Kim 2004 The scope and activation mechanisms of chemokine gene expression in primary astrocytes following infection with Theiler's virus J Neuroimmunol 149 121 129 1:CAS:528:DC%2BD2cXitFChtLk%3D 15020072
165. JP Palma D Kwon NA Clipstone BS Kim 2003 Infection with Theiler's murine encephalomyelitis virus directly induces proinflammatory cytokines in primary astrocytes via NF-kappa B activation: potential role for the initiation of demyelinating disease J Virol 77 6322 6331 1:CAS:528:DC%2BD3sXktV2nsro%3D 12743289
166. EY So MH Kang BS Kim 2006 Induction of chemokine and cytokine genes in astrocytes following infection with Theiler's murine encephalomyelitis virus is mediated by the Toll-like receptor 3 Glia 53 858 867 16586493
167. EY So BS Kim 2009 Theiler's virus infection induces TLR3-dependent upregulation of TLR2 critical for proinflammatory cytokine production Glia 57 1216 1226 19191335
168. PA Carpentier BR Williams SD Miller 2007 Distinct roles of protein kinase R and toll-like receptor 3 in the activation of astrocytes by viral stimuli Glia 55 239 252 17091495
169. JL Croxford JK Olson SD Miller 2002 Epitope spreading and molecular mimicry as triggers of autoimmunity in the Theiler's virus-induced demyelinating disease model of multiple sclerosis Autoimmun Rev 1 251 260 1:CAS:528:DC%2BD38XoslKrt7s%3D 12848977
170. SD Miller, et al. 1997 Persistent infection with Theiler's virus leads to CNS autoimmunity via epitope spreading Nat Med 3 1133 1136 1:CAS:528: DyaK2sXmsF2is7Y%3D 9334726
171. CL Vanderlugt SD Miller 2002 Epitope spreading in immune-mediated diseases: implications for immunotherapy Nat Rev Immunol 2 85 95 1:CAS:528:DC%2BD38XitFSnu7w%3D 11910899
172. Y Katz-Levy, et al. 2000 Temporal development of autoreactive Th1 responses and endogenous presentation of self myelin epitopes by central nervous system-resident APCs in Theiler's virus-infected mice J Immunol 165 5304 5314 1:CAS:528:DC%2BD3cXnvVOntL8%3D 11046065
173. M Brahic JF Bureau T Michiels 2005 The genetics of the persistent infection and demyelinating disease caused by Theiler's virus Annu Rev Microbiol 59 279 298 1:CAS:528:DC%2BD2MXht1Shs7fK 16153171
174. HL Lipton R Melvold 1984 Genetic analysis of susceptibility to Theiler's virus-induced demyelinating disease in mice J Immunol 132 1821 1825 1:STN:280:DyaL2c7js12ktA%3D%3D 6699403
175. P Borrow P Tonks CJ Welsh AA Nash 1992 The role of CD8+T cells in the acute and chronic phases of Theiler's murine encephalomyelitis virus-induced disease in mice J Gen Virol 73 Pt 7 1861 1865 1629706
176. L Fiette C Aubert M Brahic CP Rossi 1993 Theiler's virus infection of beta 2-microglobulin-deficient mice J Virol 67 589 592 1:STN:280: DyaK3s7gtVynug%3D%3D 8416386
177. DR Ure M Rodriguez 2002 Preservation of neurologic function during inflammatory demyelination correlates with axon sparing in a mouse model of multiple sclerosis Neuroscience 111 399 411 1:CAS:528:DC%2BD38Xjt1WjsLo%3D 11983325
178. WS Begolka, et al. 2001 CD8-deficient SJL mice display enhanced susceptibility to Theiler's virus infection and increased demyelinating pathology J Neurovirol 7 409 420 1:STN:280:DC%2BD3MrjsVaqtg%3D%3D 11582513
179. CL Howe, et al. 2007 CD8+ T cells directed against a viral peptide contribute to loss of motor function by disrupting axonal transport in a viral model of fulminant demyelination J Neuroimmunol 188 13 21 1:CAS:528: DC%2BD2sXotlWqtLk%3D 17493690
180. CL Howe JD Adelson M Rodriguez 2007 Absence of perforin expression confers axonal protection despite demyelination Neurobiol Dis 25 354 359 1:CAS:528:DC%2BD2sXpvVKlug%3D%3D 17112732
181. RH Woodruff RJ Franklin 1999 Demyelination and remyelination of the caudal cerebellar peduncle of adult rats following stereotaxic injections of lysolecithin, ethidium bromide, and complement/anti-galactocerebroside: a comparative study Glia 25 216 228 1:STN:280:DyaK1M7ivFKnug%3D%3D 9932868
182. GK Matsushima P Morell 2001 The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system Brain Pathol 11 107 116 1:CAS:528:DC%2BD3MXktFOntA%3D%3D 11145196
183. LC Taylor W Gilmore GK Matsushima 2008 SJL mice exposed to cuprizone intoxication reveal strain and gender pattern differences in demyelination Brain Pathol 19 467 479 19016742
184. K Suzuki 1969 Giant hepatic mitochondria: production in mice fed with cuprizone Science 163 81 82 1:CAS:528:DyaF1MXksFCgtQ%3D%3D 5763494
185. WF Blakemore 1973 Remyelination of the superior cerebellar peduncle in the mouse following demyelination induced by feeding cuprizone J Neurol Sci 20 73 83 1:STN:280:DyaE2c%2FgvFWmsg%3D%3D 4744512
186. T Skripuletz, et al. 2008 Cortical demyelination is prominent in the murine cuprizone model and is strain-dependent Am J Pathol 172 1053 1061 18349131
187. K Hoffmann M Lindner I Groticke M Stangel W Loscher 2008 Epileptic seizures and hippocampal damage after cuprizone-induced demyelination in C57BL/6 mice Exp Neurol 210 308 321 1:CAS:528:DC%2BD1cXksVKku7s%3D 18096162
188. PN Koutsoudaki, et al. 2009 Demyelination of the hippocampus is prominent in the cuprizone model Neurosci Lett 451 83 88 1:CAS:528:DC%2BD1MXhtVejtLo%3D 19084049
189. KA Irvine WF Blakemore 2006 Age increases axon loss associated with primary demyelination in cuprizone-induced demyelination in C57BL/6 mice J Neuroimmunol 175 69 76 1:CAS:528:DC%2BD28XkvVOlsr8%3D 16626812
190. JL Mason C Langaman P Morell K Suzuki GK Matsushima 2001 Episodic demyelination and subsequent remyelination within the murine central nervous system: changes in axonal calibre Neuropathol Appl Neurobiol 27 50 58 1:STN:280:DC%2BD3MzisV2isw%3D%3D 11299002
191. KA Irvine WF Blakemore 2008 Remyelination protects axons from demyelination-associated axon degeneration Brain 131 1464 1477 1:STN:280:DC%2BD1czlsl2htA%3D%3D 18490361
192. H Jurevics, et al. 2001 Cerebroside synthesis as a measure of the rate of remyelination following cuprizone-induced demyelination in brain J Neurochem 77 1067 1076 1:CAS:528:DC%2BD3MXktVWit7o%3D 11359872
193. QZ Wu, et al. 2008 MRI identification of the rostral-caudal pattern of pathology within the corpus callosum in the cuprizone mouse model J Magn Reson Imaging 27 446 453 17968901
194. JL Mason, et al. 2000 Mature oligodendrocyte apoptosis precedes IGF-1 production and oligodendrocyte progenitor accumulation and differentiation during demyelination/remyelination J Neurosci Res 61 251 262 1:CAS:528:DC%2BD3cXlslCnt7g%3D 10900072
195. M Lindner, et al. 2008 Sequential myelin protein expression during remyelination reveals fast and efficient repair after central nervous system demyelination Neuropathol Appl Neurobiol 34 105 114 1:STN:280: DC%2BD1c%2FksV2qtg%3D%3D 17961136
196. A Kondo T Nakano K Suzuki 1987 Blood-brain barrier permeability to horseradish peroxidase in twitcher and cuprizone-intoxicated mice Brain Res 425 186 190 1:STN:280:DyaL1c7gvVyjsA%3D%3D 3427420
197. EJ McMahon K Suzuki GK Matsushima 2002 Peripheral macrophage recruitment in cuprizone-induced CNS demyelination despite an intact blood-brain barrier J Neuroimmunol 130 32 45 1:CAS:528:DC%2BD38XmvVWqsbc%3D 12225886
198. MM Hiremath, et al. 1998 Microglial/macrophage accumulation during cuprizone-induced demyelination in C57BL/6 mice J Neuroimmunol 92 38 49 1:CAS:528:DyaK1cXnvVWisrg%3D 9916878
199. LT Remington AA Babcock SP Zehntner T Owens 2007 Microglial recruitment, activation, and proliferation in response to primary demyelination Am J Pathol 170 1713 1724 17456776
200. HA Arnett, et al. 2001 TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination Nat Neurosci 4 1116 1122 1:CAS:528:DC%2BD3MXot1ajsrc%3D 11600888
201. MM Hiremath VS Chen K Suzuki JP Ting GK Matsushima 2008 MHC class II exacerbates demyelination in vivo independently of T cells J Neuroimmunol 203 23 32 1:CAS:528:DC%2BD1cXhtFylsL7M 18805594
202. HA Arnett Y Wang GK Matsushima K Suzuki JP Ting 2003 Functional genomic analysis of remyelination reveals importance of inflammation in oligodendrocyte regeneration J Neurosci 23 9824 9832 1:CAS:528:DC%2BD3sXovVKis7g%3D 14586011
203. MR Kotter A Setzu FJ Sim N Van Rooijen RJ Franklin 2001 Macrophage depletion impairs oligodendrocyte remyelination following lysolecithin-induced demyelination Glia 35 204 212 1:STN:280:DC%2BD3Mvks1CgtQ%3D%3D 11494411
204. P Mana D Linares S Fordham M Staykova D Willenborg 2006 Deleterious role of IFN gamma in a toxic model of central nervous system demyelination Am J Pathol 168 1464 1473 1:CAS:528:DC%2BD28XkvF2nsbc%3D 16651614
205. W Lin, et al. 2006 Interferon-gamma inhibits central nervous system remyelination through a process modulated by endoplasmic reticulum stress Brain 129 1306 1318 16504972
206. C Trebst, et al. 2007 Lack of interferon-beta leads to accelerated remyelination in a toxic model of central nervous system demyelination Acta Neuropathol 114 587 596 1:CAS:528:DC%2BD2sXhtlWktL7L 17940777
207. MP Marriott, et al. 2008 Leukemia inhibitory factor signaling modulates both central nervous system demyelination and myelin repair Glia 56 686 698 18293407
208. SR Plant HA Arnett JP Ting 2005 Astroglial-derived lymphotoxin-alpha exacerbates inflammation and demyelination, but not remyelination Glia 49 1 14 15382206
209. SR Plant, et al. 2007 Lymphotoxin beta receptor (Lt beta R): dual roles in demyelination and remyelination and successful therapeutic intervention using Lt beta R-Ig protein J Neurosci 27 7429 7437 1:CAS:528:DC%2BD2sXnvFyhur8%3D 17626203
210. JL Mason K Suzuki DD Chaplin GK Matsushima 2001 Interleukin-1 beta promotes repair of the CNS J Neurosci 21 18 7046 7052 1:CAS:528: DC%2BD3MXmvFWhtLY%3D 11549714
211. JL Mason S Xuan I Dragatsis A Efstratiadis JE Goldman 2003 Insulin-like growth factor (IGF) signaling through type 1 IGF receptor plays an important role in remyelination J Neurosci 23 20 7710 7718 1:CAS:528:DC%2BD3sXmvFaitrY%3D 12930811
212. D Linares M Taconis P Mana M Correcha S Fordham M Staykova DO Willenborg 2006 Neuronal nitric oxide synthase plays a key role in CNS demyelination J Neurosci 26 49 12672 12681 1:CAS:528:DC%2BD2sXps1A%3D 17151270
213. HA Arnett RP Hellendall GK Matsushima K Suzuki VE Laubach P Sherman JP Ting 2002 The protective role of nitric oxide in a neurotoxicant-induced demyelinating model J Immunol 168 1 427 433 1:CAS:528:DC%2BD38Xht1KisA%3D%3D 11751989
214. EJ McMahon DN Cook K Suzuki GK Matsushima 2001 Absence of macrophage-inflammatory protein-1alpha delays central nervous system demyelination in the presence of an intact blood-brain barrier J Immunol 167 5 2964 2971 1:CAS:528:DC%2BD3MXmtlSju70%3D 11509646
215. N Franco-Pons M Torrente MT Colomina E Vilella 2007 Behavioral deficits in the cuprizone-induced murine model of demyelination/remyelination Toxicol Lett 169 205 213 1:CAS:528:DC%2BD2sXjsVGgu78%3D 17317045
216. D Liebetanz D Merkler 2006 Effects of commissural de- and remyelination on motor skill behaviour in the cuprizone mouse model of multiple sclerosis Exp Neurol 202 217 224 1:CAS:528:DC%2BD28XpslSmt7Y%3D 16857191
217. PB Andersson VH Perry S Gordon 1992 The acute inflammatory response to lipopolysaccharide in CNS parenchyma differs from that in other body tissues Neuroscience 48 169 186 1:STN:280:DyaK383mtFyktA%3D%3D 1584421
218. MD Bell VH Perry 1995 Adhesion molecule expression on murine cerebral endothelium following the injection of a proinflammagen or during acute neuronal degeneration J Neurocytol 24 695 710 1:CAS:528:DyaK2MXovVans78%3D 7500124
219. PA Felts, et al. 2005 Inflammation and primary demyelination induced by the intraspinal injection of lipopolysaccharide Brain 128 1649 1666 15872019
220. C Marik PA Felts J Bauer H Lassmann KJ Smith 2007 Lesion genesis in a subset of patients with multiple sclerosis: a role for innate immunity? Brain 130 2800 2815 17956913
221. KA Ji, et al. 2007 Resident microglia die and infiltrated neutrophils and monocytes become major inflammatory cells in lipopolysaccharide-injected brain Glia 55 1577 1588 17823975
222. PB Andersson VH Perry S Gordon 1992 Intracerebral injection of proinflammatory cytokines or leukocyte chemotaxins induces minimal myelomonocytic cell recruitment to the parenchyma of the central nervous system J Exp Med 176 255 259 1:CAS:528:DyaK38Xks1yhsLk%3D 1613459
223. H Zhou BM Lapointe SR Clark L Zbytnuik P Kubes 2006 A requirement for microglial TLR4 in leukocyte recruitment into brain in response to lipopolysaccharide J Immunol 177 8103 8110 1:CAS:528:DC%2BD28Xht1WrsLjI 17114485
224. S Lehnardt, et al. 2002 The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS J Neurosci 22 2478 2486 1:CAS:528:DC%2BD38Xis1eqtLk%3D 11923412
225. J Li O Baud T Vartanian JJ Volpe PA Rosenberg 2005 Peroxynitrite generated by inducible nitric oxide synthase and NADPH oxidase mediates microglial toxicity to oligodendrocytes Proc Natl Acad Sci U S A 102 9936 9941 1:CAS:528:DC%2BD2MXmsFaqsr8%3D 15998743
226. Y Pang Z Cai PG Rhodes 2000 Effects of lipopolysaccharide on oligodendrocyte progenitor cells are mediated by astrocytes and microglia J Neurosci Res 62 510 520 1:CAS:528:DC%2BD3cXotVWiu74%3D 11070494
227. J Li, et al. 2008 Tumor necrosis factor alpha mediates lipopolysaccharide-induced microglial toxicity to developing oligodendrocytes when astrocytes are present J Neurosci 28 5321 5330 1:CAS:528: DC%2BD1cXmt1SltLs%3D 18480288
228. D Brockschnieder Y Pechmann E Sonnenberg-Riethmacher D Riethmacher 2006 An improved mouse line for Cre-induced cell ablation due to diphtheria toxin A, expressed from the Rosa26 locus Genesis 44 322 327 1:CAS:528: DC%2BD28XpsVegsbY%3D 16791847