The immune pathogenesis of multiple sclerosis

Journal of Neuroimmune Pharmacology

Volumn 8, Issue 4, 2013, Pages 857-866

  Weissert, Robert ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

EAE; MHC; Multiple sclerosis; T cell; Therapy

Indexed keywords

4 AMINOPYRIDINE; AUTOANTIGEN; AZATHIOPRINE; BETA1A INTERFERON; CORTICOSTEROID DERIVATIVE; CYCLOPHOSPHAMIDE; ECULIZUMAB; FINGOLIMOD; FUMARIC ACID DIMETHYL ESTER; GLATIRAMER; IMMUNOGLOBULIN; INTERFERON BETA SERINE; MITOXANTRONE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; MYELIN BASIC PROTEIN; NATALIZUMAB; RALENOVA; RITUXIMAB; TERIFLUNOMIDE; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ALLELE; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ASTROCYTE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DISEASE COURSE; GRAY MATTER; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; MICROGLIA; MULTIPLE SCLEROSIS; MYELOOPTIC NEUROPATHY; NATURAL KILLER CELL; NERVE CONDUCTION DISORDER; OLIGODENDROGLIA; PLASMAPHERESIS; PRIORITY JOURNAL; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; REVIEW; TISSUE INJURY; WHITE MATTER;

ANIMALS; AUTOIMMUNE DISEASES; HUMANS; IMMUNITY, INNATE; IMMUNOTHERAPY; MULTIPLE SCLEROSIS; T-LYMPHOCYTES;

EID: 84882276270     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-013-9467-3     Document Type: Review

References (75)

1. Arun T, Tomassini V, Sbardella E, de Ruiter MB, Matthews L, Leite MI, Gelineau-Morel R, Cavey A, Vergo S, Craner M, Fugger L, Rovira A, Jenkinson M, Palace J (2013) Targeting ASIC1 in primary progressive multiple sclerosis: evidence of neuroprotection with amiloride. Brain 136:106-115
2. Barcellos LF, Sawcer S, Ramsay PP, Baranzini SE, Thomson G, Briggs F, Cree BC, Begovich AB, Villoslada P, Montalban X, Uccelli A, Savettieri G, Lincoln RR, DeLoa C, Haines JL, Pericak-Vance MA, Compston A, Hauser SL, Oksenberg JR (2006) Heterogeneity at the HLA-DRB1 locus and risk for multiple sclerosis. Hum Mol Genet 15:2813-2824
3. Becher B, Prat A, Antel JP (2000) Brain-immune connection: immuno-regulatory properties of CNS-resident cells. Glia 29:293-304
4. Berer K, Mues M, Koutrolos M, Rasbi ZA, Boziki M, Johner C, Wekerle H, Krishnamoorthy G (2011) Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 479:538-541
5. Bloomgren G, Richman S, Hotermans C, Subramanyam M, Goelz S, Natarajan A, Lee S, Plavina T, Scanlon JV, Sandrock A, Bozic C (2012) Risk of natalizumab-associated progressive multifocal leukoencephalopathy. N Engl J Med 366:1870-1880
6. Breij EC, Brink BP, Veerhuis R, van den Berg C, Vloet R, Yan R, Dijkstra CD, van der Valk P, Bo L (2008) Homogeneity of active demyelinating lesions in established multiple sclerosis. Ann Neurol 63:16-25
7. Centonze D, Muzio L, Rossi S, Furlan R, Bernardi G, Martino G (2010) The link between inflammation, synaptic transmission and neurodegeneration in multiple sclerosis. Cell Death Differ 17:1083-1091
8. Cheng MH, Anderson MS (2012) Monogenic autoimmunity. Annu Rev Immunol 30:393-427
9. Compston A (1999) The genetic epidemiology of multiple sclerosis. Phil Trans Roy Soc Lond B Biol Sci 354:1623-1634
10. de Graaf KL, Weissert R, Kjellen P, Holmdahl R, Olsson T (1999) Allelic variations in rat MHC class II binding of myelin basic protein peptides correlate with encephalitogenicity. Int Immunol 11:1981-1988
11. de Graaf KL, Albert M, Weissert R (2012) Autoantigen conformation influences both B- and T-cell responses and encephalitogenicity. J Biol Chem 287:17206-17213
12. Delmotte P (1971) Gel isoelectric focusing of cerebrospinal fluid proteins: a potential diagnostic tool. Z Klin Chem Klin Biochem 9:334-336
13. Ebers GC (2008) Environmental factors and multiple sclerosis. Lancet Neurol 7:268-277
14. Fissolo N, Haag S, de Graaf KL, Drews O, Stevanovic S, Rammensee HG, Weissert R (2009) Naturally presented peptides on major histocompatibility complex I and II molecules eluted from central nervous system of multiple sclerosis patients. Mol Cell Proteomics 8:2090-2101
15. Forsthuber TG, Shive CL, Wienhold W, de Graaf K, Spack EG, Sublett R, Melms A, Kort J, Racke MK, Weissert R (2001) T cell epitopes of human myelin oligodendrocyte glycoprotein identified in HLA-DR4 (DRB10401) transgenic mice are encephalitogenic and are presented by human B cells. J Immunol 167:7119-7125
16. Garg SK, Banerjee R, Kipnis J (2008) Neuroprotective immunity: T cell-derived glutamate endows astrocytes with a neuroprotective phenotype. J Immunol 180:3866-3873
17. Gold R, Kappos L, Arnold DL, Bar-Or A, Giovannoni G, Selmaj K, Tornatore C, Sweetser MT, Yang M, Sheikh SI, Dawson KT, Investigators DS (2012) Placebo-controlled phase 3 study of oral BG-12 for relapsing multiple sclerosis. N Engl J Med 367:1098-1107
18. Grewal IS, Foellmer HG, Grewal KD, Wang H, Lee WP, Tumas D, Janeway CA Jr, Flavell RA (2001) CD62L is required on effector cells for local interactions in the CNS to cause myelin damage in experimental allergic encephalomyelitis. Immunity 14:291-302
19. Haring JS, Pewe LL, Perlman S (2002) Bystander CD8 T cell-mediated demyelination after viral infection of the central nervous system. J Immunol 169:1550-1555
20. Harkiolaki M, Holmes SL, Svendsen P, Gregersen JW, Jensen LT, McMahon R, Friese MA, van Boxel G, Etzensperger R, Tzartos JS, Kranc K, Sainsbury S, Harlos K, Mellins ED, Palace J, Esiri MM, van der Merwe PA, Jones EY, Fugger L (2009) T cell-mediated autoimmune disease due to low-affinity crossreactivity to common microbial peptides. Immunity 30:348-357
21. Hartung HP, Gonsette R, Konig N, Kwiecinski H, Guseo A, Morrissey SP, Krapf H, Zwingers T, Mitoxantrone in Multiple Sclerosis Study G (2002) Mitoxantrone in progressive multiple sclerosis: a placebo-controlled, double-blind, randomised, multicentre trial. Lancet 360:2018
22. Hauser SL, Waubant E, Arnold DL, Vollmer T, Antel J, Fox RJ, Bar-Or A, Panzara M, Sarkar N, Agarwal S, Langer-Gould A, Smith CH (2008) B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N Engl J Med 358:676-688
23. Hedstrom AK, Sundqvist E, Baarnhielm M, Nordin N, Hillert J, Kockum I, Olsson T, Alfredsson L (2011) Smoking and two human leukocyte antigen genes interact to increase the risk for multiple sclerosis. Brain 134:653-664
24. Hinson SR, Romero MF, Popescu BF, Lucchinetti CF, Fryer JP, Wolburg H, Fallier-Becker P, Noell S, Lennon VA (2012) Molecular outcomes of neuromyelitis optica (NMO)-IgG binding to aquaporin-4 in astrocytes. Proc Natl Acad Sci U S A 109:1245-1250
25. International Multiple Sclerosis Genetics C et al (2011) Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 476:214-219
26. Jacob A, Weinshenker BG, Violich I, McLinskey N, Krupp L, Fox RJ, Wingerchuk DM, Boggild M, Constantinescu CS, Miller A, De Angelis T, Matiello M, Cree BA (2008) Treatment of neuromyelitis optica with rituximab: retrospective analysis of 25 patients. Arch Neurol 65:1443-1448
27. Jacobs LD et al (1996) Intramuscular interferon beta-1a for disease progression in relapsing multiple sclerosis. The Multiple Sclerosis Collaborative Research Group (MSCRG). Ann Neurol 39:285-294
28. Ji Q, Perchellet A, Goverman JM (2010) Viral infection triggers central nervous system autoimmunity via activation of CD8+ T cells expressing dual TCRs. Nat Immunol 11:628-634
29. Johnson KP, Brooks BR, Cohen JA, Ford CC, Goldstein J, Lisak RP, Myers LW, Panitch HS, Rose JW, Schiffer RB (1995) Copolymer 1 reduces relapse rate and improves disability in relapsing-remitting multiple sclerosis: results of a phase III multicenter, double-blind placebo-controlled trial. The Copolymer 1 Multiple Sclerosis Study Group. Neurology 45:1268-1276
30. Kappos L, Radue EW, O'Connor P, Polman C, Hohlfeld R, Calabresi P, Selmaj K, Agoropoulou C, Leyk M, Zhang-Auberson L, Burtin P, Group FS (2010) A placebo-controlled trial of oral fingolimod in relapsing multiple sclerosis. N Engl J Med 362:387-401
31. Karman J, Chu HH, Co DO, Seroogy CM, Sandor M, Fabry Z (2006) Dendritic cells amplify T cell-mediated immune responses in the central nervous system. J Immunol 177:7750-7760
32. Keegan M, Konig F, McClelland R, Bruck W, Morales Y, Bitsch A, Panitch H, Lassmann H, Weinshenker B, Rodriguez M, Parisi J, Lucchinetti CF (2005) Relation between humoral pathological changes in multiple sclerosis and response to therapeutic plasma exchange. Lancet 366:579-582
33. Kleiter I, Hellwig K, Berthele A, Kumpfel T, Linker RA, Hartung HP, Paul F, Aktas O, Neuromyelitis Optica Study G (2012) Failure of natalizumab to prevent relapses in neuromyelitis optica. Arch Neurol 69:239-245
34. Kutzelnigg A, Lucchinetti CF, Stadelmann C, Bruck W, Rauschka H, Bergmann M, Schmidbauer M, Parisi JE, Lassmann H (2005) Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain 128:2705-2712
35. Lauterbach H, Zuniga EI, Truong P, Oldstone MB, McGavern DB (2006) Adoptive immunotherapy induces CNS dendritic cell recruitment and antigen presentation during clearance of a persistent viral infection. J Exp Med 203:1963-1975
36. Lennon VA, Wingerchuk DM, Kryzer TJ, Pittock SJ, Lucchinetti CF, Fujihara K, Nakashima I, Weinshenker BG (2004) A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 364:2106-2112
37. Lublin FD, Reingold SC (1996) Defining the clinical course of multiple sclerosis: results of an international survey. National Multiple Sclerosis Society (USA) Advisory Committee on Clinical Trials of New Agents in Multiple Sclerosis. Neurology 46:907-911
38. Lucchinetti CF, Popescu BF, Bunyan RF, Moll NM, Roemer SF, Lassmann H, Bruck W, Parisi JE, Scheithauer BW, Giannini C, Weigand SD, Mandrekar J, Ransohoff RM (2011) Inflammatory cortical demyelination in early multiple sclerosis. N Engl J Med 365:2188-2197
39. Martin R, Howell MD, Jaraquemada D, Flerlage M, Richert J, Brostoff S, Long EO, McFarlin DE, McFarland HF (1991) A myelin basic protein peptide is recognized by cytotoxic T cells in the context of four HLA-DR types associated with multiple sclerosis. J Exp Med 173:19-24
40. McElroy JP, Isobe N, Gourraud PA, Caillier SJ, Matsushita T, Kohriyama T, Miyamoto K, Nakatsuji Y, Miki T, Hauser SL, Oksenberg JR, Kira J (2011) SNP-based analysis of the HLA locus in Japanese multiple sclerosis patients. Genes Immun 12:523-530
41. Min JH, Kim BJ, Lee KH (2012) Development of extensive brain lesions following fingolimod (FTY720) treatment in a patient with neuromyelitis optica spectrum disorder. Mult Scler 18:113-115
42. Moreno B, Jukes JP, Vergara-Irigaray N, Errea O, Villoslada P, Perry VH, Newman TA (2011) Systemic inflammation induces axon injury during brain inflammation. Ann Neurol 70:932-942
43. Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308:1314-1318
44. O'Connor P, Wolinsky JS, Confavreux C, Comi G, Kappos L, Olsson TP, Benzerdjeb H, Truffinet P, Wang L, Miller A, Freedman MS, Group TT (2011) Randomized trial of oral teriflunomide for relapsing multiple sclerosis. N Engl J Med 365:1293-1303
45. Odoardi F, Sie C, Streyl K, Ulaganathan VK, Schlager C, Lodygin D, Heckelsmiller K, Nietfeld W, Ellwart J, Klinkert WE, Lottaz C, Nosov M, Brinkmann V, Spang R, Lehrach H, Vingron M, Wekerle H, Flugel-Koch C, Flugel A (2012) T cells become licensed in the lung to enter the central nervous system. Nature 488:675-679
46. Pesic MBI, Kyratsous NI, Heissmeyer V, Wekerle H, Kawakami N (2013) 2-photon imaging of phagocyte-mediated T cell activation in the CNS. J Clin Invest 123:1191-1201
47. Peterson JW, Bo L, Mork S, Chang A, Trapp BD (2001) Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol 50:389-400
48. Polman CH, O'Connor PW, Havrdova E, Hutchinson M, Kappos L, Miller DH, Phillips JT, Lublin FD, Giovannoni G, Wajgt A, Toal M, Lynn F, Panzara MA, Sandrock AW, Investigators A (2006) A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. N Engl J Med 354:899-910
49. Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L, Lublin FD, Montalban X, O'Connor P, Sandberg-Wollheim M, Thompson AJ, Waubant E, Weinshenker B, Wolinsky JS (2011) Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 69:292-302
50. Popescu BF, Lucchinetti CF (2012) Pathology of demyelinating diseases. Annu Rev Pathol 7:185-217
51. Probstel AK et al (2011) Antibodies to MOG are transient in childhood acute disseminated encephalomyelitis. Neurology 77:580-588
52. Ransohoff RM, Perry VH (2009) Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 27:119-145
53. Rongvaux A, Takizawa H, Strowig T, Willinger T, Eynon EE, Flavell RA, Manz MG (2013) Human hemato-lymphoid system mice: current use and future potential for medicine. Annu Rev Immunol 31:635-674
54. Sallusto F, Impellizzieri D, Basso C, Laroni A, Uccelli A, Lanzavecchia A, Engelhardt B (2012) T-cell trafficking in the central nervous system. Immunol Rev 248:216-227
55. Salzer J, Hallmans G, Nystrom M, Stenlund H, Wadell G, Sundstrom P (2012) Vitamin D as a protective factor in multiple sclerosis. Neurology 79:2140-2145
56. Serafini B, Rosicarelli B, Magliozzi R, Stigliano E, Aloisi F (2004) Detection of ectopic B-cell follicles with germinal centers in the meninges of patients with secondary progressive multiple sclerosis. Brain Pathol 14:164-174
57. Shimizu Y, Yokoyama K, Misu T, Takahashi T, Fujihara K, Kikuchi S, Itoyama Y, Iwata M (2008) Development of extensive brain lesions following interferon beta therapy in relapsing neuromyelitis optica and longitudinally extensive myelitis. J Neurol 255:305-307
58. Sholl-Franco A, Marques PM, Ferreira CM, de Araujo EG (2002) IL-4 increases GABAergic phenotype in rat retinal cell cultures: involvement of muscarinic receptors and protein kinase C. J Neuroimmunol 133:20-29
59. Sorensen PS, Bertolotto A, Edan G, Giovannoni G, Gold R, Havrdova E, Kappos L, Kieseier BC, Montalban X, Olsson T (2012) Risk stratification for progressive multifocal leukoencephalopathy in patients treated with natalizumab. Mult Scler 18:143-152
60. Storch MK, Bauer J, Linington C, Olsson T, Weissert R, Lassmann H (2006) Cortical demyelination can be modeled in specific rat models of autoimmune encephalomyelitis and is major histocompatability complex (MHC) haplotype-related. J Neuropathol Exp Neurol 65:1137-1142
61. 't Hart BA, Gran B, Weissert R (2011) EAE: imperfect but useful models of multiple sclerosis. Trends Mol Med 17:119-125
62. The IFNB Multiple Sclerosis Study Group (1993) Interferon beta-1b is effective in relapsing-remitting multiple sclerosis. I. Clinical results of a multicenter randomized, double-blind, placebo-controlled trial. Neurology 43:655-661
63. Tien-Hsiang Chen J, Easley K, Schneider C, Nakamura K, Kidd GJ, Chang A, Staugaitis SM, Fox RJ, Fisher E, Arnold DL, Trapp BD (2012) Clinically feasible MTR is sensitive to cortical demyelination in MS. Neurology 30:246-252
64. Trapp BD, Nave KA (2008) Multiple sclerosis: an immune or neurodegenerative disorder? Annu Rev Neurosci 31:247-269
65. Uze G, Schreiber G, Piehler J, Pellegrini S (2007) The receptor of the type I interferon family. Curr Top Microbiol Immunol 316:71-95
66. Weissert R (2011) Progressive multifocal leukoencephalopathy. J Neuroimmunol 231:73-77
67. Weissert R (2012) Experimental Autoimmune Encephalomyelitis. DOI 10.5772/29792: 1-19. In "Experimental Autoimmune Encephalomyelitis - Models, Disease Biology and Experimental Therapy", book edited by Robert Weissert, ISBN 978-953-51-0038-6
68. Weissert R, Svenningsson A, Lobell A, de Graaf KL, Andersson R, Olsson T (1998a) Molecular and genetic requirements for preferential recruitment of TCRBV8S2+ T cells in Lewis rat experimental autoimmune encephalomyelitis. J Immunol 160:681-690
69. Weissert R, Wallstrom E, Storch MK, Stefferl A, Lorentzen J, Lassmann H, Linington C, Olsson T (1998b) MHC haplotype-dependent regulation of MOG-induced EAE in rats. J Clin Invest 102:1265-1273
70. Weissert R, Kuhle J, de Graaf KL, Wienhold W, Herrmann MM, Muller C, Forsthuber TG, Wiesmuller KH, Melms A (2002) High immunogenicity of intracellular myelin oligodendrocyte glycoprotein epitopes. J Immunol 169:548-556
71. Weller RO, Engelhardt B, Phillips MJ (1996) Lymphocyte targeting of the central nervous system: a review of afferent and efferent CNS-immune pathways. Brain Pathol 6:275-288
72. WHO (2008) Atlas of multiple sclerosis resources in the world 2008, 1st edn. WHO Press, Geneva
73. Wingerchuk DM, Weinshenker BG (2005) Neuromyelitis optica. Curr Treat Options Neurol 7:173-182
74. Wingerchuk DM, Lennon VA, Pittock SJ, Lucchinetti CF, Weinshenker BG (2006) Revised diagnostic criteria for neuromyelitis optica. Neurology 66:1485-1489
75. Wucherpfennig KW, Strominger JL (1995) Molecular mimicry in T cell-mediated autoimmunity: viral peptides activate human T cell clones specific for myelin basic protein. Cell 80:695-705