Evidence for the role of B cells and immunoglobulins in the pathogenesis of multiple sclerosis

Neurology Research International

Volumn 2011, Issue , 2011, Pages

  Wootla, Bharath ^a   Denic, Aleksandar ^a   Keegan, B Mark ^a   Winters, Jeffrey L ^a   Astapenko, David ^b   Warrington, Arthur E ^a   Bieber, Allan J ^a   Rodriguez, Moses ^a,c  

^a MAYO CLINIC   (United States)

^b CHARLES UNIVERSITY   (Czech Republic)

^c MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84860275553     PISSN: 20901852     EISSN: 20901860     Source Type: Journal    
DOI: 10.1155/2011/780712     Document Type: Review

References (160)

1. C. Lucchinetti, W. Bruck, J. Parisi, B. Scheithauer, M. Rodriguez, and H. Lassmann, "Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination," Annals of Neurology, vol. 47, no. 6, pp. 707-717, 2000. (Pubitemid 30390191)
2. E.M. Frohman,M. K. Racke, and C. S. Raine, "Multiple sclerosis- the plaque and its pathogenesis," New England Journal of Medicine, vol. 354, no. 9, pp. 942-955, 2006.
3. H. Lassmann, W. Bruck, and C. Lucchinetti, "Heterogeneity of multiple sclerosis pathogenesis: implications for diagnosis and therapy," Trends in Molecular Medicine, vol. 7, no. 3, pp. 115-121, 2001. (Pubitemid 32201673)
4. H. Wekerle, "Immune pathogenesis of multiple sclerosis," Neurological Sciences, vol. 26, supplement 1, pp. S1-S2, 2005. (Pubitemid 40637349)
5. E. A. Kabat, D. H. Moore, and H. Landow, "An electrophoretic study of the protein components in cerebrospinal fluid and their relationship to the serum proteins," Journal of Clinical Investigation, vol. 21, pp. 571-577, 1942.
6. A. Denic, A. J. Johnson, A. J. Bieber, A. E. Warrington, M. Rodriguez, and I. Pirko, "The relevance of animal models in multiple sclerosis research," Pathophysiology, vol. 18, no. 1, pp. 21-29, 2011.
7. B. D. Jankoovic, I. M. Rakic, M. Janjic, J. Ivanus, and K. Mitrovic, "Effect of experimental allergic encephalomyelitis gamma-globulin upon the electrical activity of the brain," Experientia, vol. 22, pp. 459-460, 1966.
8. B. D. Jankoovic, I. M. Rakic, M. Janjic, K. Mitrovic, and J. Ivanus, "Immuno-neurophysiological studies of the experimental allergic encephalomyelitis following the injection of antibrain antibodies and myelin protein into the cerebral cavity," Path Europ, vol. 2, p. 87, 1966.
9. M. B.Oldstone and F. J. Dixon, "Immunohistochemical study ofallergic encephalomyelitis," American Journal of Pathology, vol. 52, no. 2, pp. 251-263, 1968.
10. S. H. Appel and M. B. Bornstein, "The Application of tissue culture to the study of experimental allergic encephalomyelitis. Ii. Serum factors responsible for demyelination," Journal of Experimental Medicine, vol. 119, pp. 303-312, 1964.
11. C. S. Raine, B. Cannella, S. L. Hauser, and C. P. Genain, "Demyelination in primate autoimmune encephalomyelitis and acute multiple sclerosis lesions: A case for antigen-specific antibody mediation," Annals of Neurology, vol. 46, no. 2, pp. 144-160, 1999. (Pubitemid 29382870)
12. M. Rodriguez, C. F. Lucchinetti, R. J. Clark, T. L. Yaksh, H. Markowitz, and V. A. Lennon, "Immunoglobulins and complement in demyelination induced in mice by Theiler's virus," Journal of Immunology, vol. 140, no. 3, pp. 800-806, 1988. (Pubitemid 18067266)
13. H. Goto, H.Matsuo, S. Nakane et al., "Plasmapheresis affects T helper type-1/T helper type-2 balance of circulating peripheral lymphocytes," Therapeutic Apheresis, vol. 5, no. 6, pp. 494-496, 2001. (Pubitemid 34037589)
14. C. Kambara, H. Matsuo, T. Fukudome, H. Goto, and N. Shibuya, "Miller Fisher syndrome and plasmapheresis," Therapeutic Apheresis, vol. 6, no. 6, pp. 450-453, 2002. (Pubitemid 35417156)
15. S. Shariatmadar, M. Nassiri, and V. Vincek, "Effect of plasma exchange on cytokines measured by multianalyte bead array in thrombotic thrombocytopenic purpura," American Journal of Hematology, vol. 79, no. 2, pp. 83-88, 2005. (Pubitemid 40770665)
16. G. De Luca, A. Lugaresi, C. Iarlori et al., "Prednisone and plasma exchange improve suppressor cell function in chronic inflammatory demyelinating polyneuropathy," Journal of Neuroimmunology, vol. 95, no. 1-2, pp. 190-194, 1999. (Pubitemid 29173037)
17. M. D. Griffin, W. H. Lutz, V. A. Phan, L. A. Bachman, D. J. McKean, and R. Kumar, "Potent inhibition of dendritic cell differentiation and maturation by vitamin D analogs," Biochemical and Biophysical Research Communications, vol. 270, no. 3, pp. 701-708, 2000. (Pubitemid 30444768)
18. M. Rodriguez, W. E. Karnes, J. D. Bartleson, and A. A. Pineda, "Plasmapheresis in acute episodes of fulminant CNS inflammatory demyelination," Neurology, vol. 43, no. 6, pp. 1100-1104, 1993. (Pubitemid 23177705)
19. B. G. Weinshenker, P. C. O'Brien, T. M. Petterson et al., "A randomized trial of plasma exchange in acute central nervous system inflammatory demyelinating disease," Annals of Neurology, vol. 46, no. 6, pp. 878-886, 1999.
20. M. Keegan, F. Konig, R. McClelland et al., "Relation between humoral pathological changes in multiple sclerosis and response to therapeutic plasma exchange," The Lancet, vol. 366, no. 9485, pp. 579-582, 2005. (Pubitemid 41140333)
21. M. Keegan, A. A. Pineda, R. L. McClelland, C. H. Darby, M. Rodriguez, and B. G. Weinshenker, "Plasma exchange for severe attacks of CNS demyelination: predictors of response," Neurology, vol. 58, no. 1, pp. 143-146, 2002.
22. A. Moldenhauer, J. Haas, C. Wascher et al., "Immunoadsorption patients with multiple sclerosis: an open-label pilot study," European Journal of Clinical Investigation, vol. 35, no. 8, pp. 523-530, 2005. (Pubitemid 41153207)
23. S. M. Magana, B. M. Keegan, B. G. Weinshenker et al., "Beneficial plasma exchange response in central nervous system inflammatory demyelination," Archives of Neurology, vol. 68, no. 7, pp. 870-878, 2011.
24. I. Cortese, V. Chaudhry, Y. T. So, F. Cantor, D. R. Cornblath, and A. Rae-Grant, "Evidence-based guideline update: plasmapheresis in neurologic disorders: report of the therapeutics and technology assessment subcommittee of the American Academy of Neurology," Neurology, vol. 76, no. 3, pp. 294-300, 2011.
25. J. H. Noseworthy, P. C. O'Brien, B. G.Weinshenker et al., "IV immunoglobulin does not reverse established weakness in MS," Neurology, vol. 55, no. 8, pp. 1135-1143, 2000.
26. J. L. Winters, D. Brown, E. Hazard, A. Chainani, and C. Andrzejewski Jr., "Cost-minimization analysis of the direct costs of TPE and IVIg in the treatment of Guillain-Barre syndrome," BMCHealth Services Research, vol. 11, article 101, 2011.
27. M. M. Esiri, "Multiple sclerosis: A quantitative and qualitative study of immunoglobulin-containing cells in the central nervous system," Neuropathology and Applied Neurobiology, vol. 6, no. 1, pp. 9-21, 1980. (Pubitemid 10001746)
28. S. Cepok, M. Jacobsen, S. Schock et al., "Patterns of cerebrospinal fluid pathology correlate with disease progression in multiple sclerosis," Brain, vol. 124, no. 11, pp. 2169-2176, 2001. (Pubitemid 33055362)
29. S. E. Baranzini, M. C. Jeong, C. Butunoi, R. S. Murray, C. C. Bernard, and J. R. Oksenberg, "B cell repertoire diversity and clonal expansion in multiple sclerosis brain lesions," Journal of Immunology, vol. 163, no. 9, pp. 5133-5144, 1999. (Pubitemid 29501283)
30. M. Colombo, M. Dono, P. Gazzola et al., "Accumulation of clonally related B lymphocytes in the cerebrospinal fluid of multiple sclerosis patients," Journal of Immunology, vol. 164, no. 5, pp. 2782-2789, 2000. (Pubitemid 30115513)
31. P. M. Knopf, C. J. Harling-Berg, H. F. Cserr et al., " Antigendependent intrathecal antibody synthesis in the normal rat brain: rissue entry and local retention of antigen-specific B cells," Journal of Immunology, vol. 161, no. 2, pp. 692-701, 1998. (Pubitemid 28323531)
32. A. Corcione, S. Casazza, E. Ferretti et al., "Recapitulation of B cell differentiation in the central nervous system of patients with multiple sclerosis," Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 30, pp. 11064-11069, 2004. (Pubitemid 38989584)
33. Y. Qin, P. Duquette, Y. Zhang, P. Talbot, R. Poole, and J. Antel, "Clonal expansion and somatic hypermutation of V(H) genes of B cells from cerebrospinal fluid in multiple sclerosis," Journal of Clinical Investigation, vol. 102, no. 5, pp. 1045-1050, 1998. (Pubitemid 28419250)
34. A. H. Cross and G. F. Wu, "Multiple sclerosis: oligoclonal bands still yield clues about multiple sclerosis," Nature Reviews Neurology, vol. 6, no. 11, pp. 588-589, 2010.
35. E. Paolino, E. Fainardi, P. Ruppi et al., "A prospective study on the predictive value of CSF oligoclonal bands and MRI in acute isolated neurological syndromes for subsequent progression to multiple sclerosis," Journal of Neurology Neurosurgery and Psychiatry, vol. 60, no. 5, pp. 572-575, 1996. (Pubitemid 26147901)
36. M. P. Amato and G. Ponziani, "A prospective study on the prognosis ofmultiple sclerosis," Neurological Sciences, vol. 21, no. 4, supplement 2, pp. S831-S838, 2000. (Pubitemid 33621534)
37. F.G. Joseph, C. L. Hirst, T. P. Pickersgill, Y. Ben-Shlomo,N. P. Robertson, and N. J. Scolding, "CSF oligoclonal band status informs prognosis in multiple sclerosis: A case control study of 100 patients," Journal of Neurology, Neurosurgery and Psychiatry, vol. 80, no. 3, pp. 292-296, 2009.
38. W. Bruck, K. Neubert, T. Berger, and J. R. Weber, "Clinical, radiological, immunological and pathological findings in inflammatory CNS demyelination-possible markers for an antibody-mediated process," Multiple Sclerosis, vol. 7, no. 3, pp. 173-177, 2001. (Pubitemid 32651817)
39. A. A. Belogurov Jr., I. N. Kurkova, A. Friboulet et al., "Recognition and degradation of myelin basic protein peptides by serum autoantibodies: novel biomarker for multiple sclerosis," Journal of Immunology, vol. 180, no. 2, pp. 1258-1267, 2008.
40. M. H. Barnett, J. D. Parratt, E. S. Cho, and J.W. Prineas, "Immunoglobulins and complement in postmortem multiple sclerosis tissue," Annals of Neurology, vol. 65, no. 1, pp. 32-46, 2009.
41. S. Avrameas, "Natural autoantibodies: from 'horror autotoxicus' to 'gnothi seauton'," Immunology Today, vol. 12, no. 5, pp. 154-159, 1991.
42. M. Rodriguez, V. A. Lennon, E. N. Benveniste, and J. E. Merrill, "Remyelination by oligodendrocytes stimulated by antiserum to spinal cord," Journal of Neuropathology and Experimental Neurology, vol. 46, no. 1, pp. 84-95, 1987. (Pubitemid 17232257)
43. A. E. Warrington, K. Asakura, A. J. Bieber et al., "Human monoclonal antibodies reactive to oligodendrocytes promote remyelination in a model of multiple sclerosis," Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 12, pp. 6820-6825, 2000. (Pubitemid 30412798)
44. A. E. Warrington, A. J. Bieber, V. Van Keulen, B. Ciric, L. R. Pease, and M. Rodriguez, "Neuron-binding human monoclonal antibodies support central nervous system neurite extension," Journal of Neuropathology and Experimental Neurology, vol. 63, no. 5, pp. 461-473, 2004. (Pubitemid 38669667)
45. D. H.Mattson, R. P. Roos, and B. G. Arnason, "Isoelectric focusing of IgG eluted from multiple sclerosis and subacute sclerosing panencephalitis brains," Nature, vol. 287, no. 5780, pp. 335-337, 1980. (Pubitemid 10001723)
46. D. H.Mattson, R. P. Roos, and B. G. Arnason, "Oligoclonal IgG in multiple sclerosis and subacute sclerosing panencephalitis brains," Journal of Neuroimmunology, vol. 2, no. 3-4, pp. 261-276, 1982. (Pubitemid 12042613)
47. C.C.Whitacre, D. H. Mattson, P. Y. Paterson,R. P.Roos, D. J. Peterson, and B. G. Arnason, "Cerebrospinal fluid and serum oligoclonal IgG bands in rabbits with experiment allergic encephalomyelitis," Neurochemical Research, vol. 6, pp. 87-96, 1981. (Pubitemid 11153514)
48. M. J. Walsh and W. W. Tourtellotte, "Temporal invariance and clonal uniformity of brain and cerebrospinal IgG, IgA, and IgM in multiple sclerosis," Journal of Experimental Medicine, vol. 163, no. 1, pp. 41-53, 1986. (Pubitemid 16189509)
49. R. Goswami, R. K. Marwaha, N. Gupta et al., "Prevalence of vitamin D deficiency and its relationship with thyroid autoimmunity in Asian Indians: A community-based survey," British Journal ofNutrition, vol. 102, no. 3, pp. 382-386, 2009.
50. W. B. Grant, H. S. Cross, C. F. Garland et al., "Estimated benefit of increased vitamin D status in reducing the economic burden of disease in western Europe," Progress in Biophysics and Molecular Biology, vol. 99, no. 2-3, pp. 104-113, 2009.
51. J. Kragt, B. van Amerongen, J. Killestein et al., "Higher levels of 25-hydroxyvitaminDare associated with a lower incidence of multiple sclerosis only in women," Multiple Sclerosis, vol. 15, no. 1, pp. 9-15, 2009.
52. K. L. Munger, L. I. Levin, B. W. Hollis, N. S. Howard, and A. Ascherio, "Serum 25-hydroxyvitamin D levels and risk of multiple sclerosis," Journal of the American Medical Association, vol. 296, no. 23, pp. 2832-2838, 2006. (Pubitemid 44969183)
53. S. M. Orton, A. P. Morris, B. M. Herrera et al., "Evidence for genetic regulation of vitamin D status in twins with multiple sclerosis," American Journal of Clinical Nutrition, vol. 88, no. 2, pp. 441-447, 2008.
54. A. Raghuwanshi, S. S. Joshi, and S. Christakos, "Vitamin D and multiple sclerosis," Journal of Cellular Biochemistry, vol. 105, no. 2, pp. 338-343, 2008.
55. J. Smolders, J. Damoiseaux, P. Menheere, J. W. Tervaert, and R. Hupperts, "Association study on two vitamin D receptor gene polymorphisms and vitamin D metabolites in multiple sclerosis," Annals of the New York Academy of Sciences, vol. 1173, pp. 515-520, 2009.
56. J. Smolders, J. Damoiseaux, P. Menheere, J. W. Tervaert, and R. Hupperts, "Fok-I vitamin D receptor gene polymorphism (rs10735810) and vitamin D metabolism in multiple sclerosis," Journal of Neuroimmunology, vol. 207, no. 1-2, pp. 117-121, 2009.
57. J. Smolders, P. Menheere, A. Kessels, J. Damoiseaux, and R. Hupperts, "Association of vitamin D metabolite levels with relapse rate and disability in multiple sclerosis," Multiple Sclerosis, vol. 14, no. 9, pp. 1220-1224, 2008.
58. J. Smolders, E. Peelen, M. Thewissen et al., "The relevance of vitamin D receptor gene polymorphisms for vitamin D research in multiple sclerosis," Autoimmunity Reviews, vol. 8, no. 7, pp. 621-626, 2009.
59. J. Smolders, M. Thewissen, E. Peelen et al., "Vitamin D status is positively correlated with regulatory T cell function in patients with multiple sclerosis," PLoS One, vol. 4, no. 8, Article ID e6635, 2009.
60. M. Soilu-Hanninen, M. Laaksonen, I. Laitinen, J. P. Eralinna, E. M. Lilius, and I.Mononen, "A longitudinal study of serum 25-hydroxyvitamin D and intact parathyroid hormone levels indicate the importance of vitamin D and calcium homeostasis regulation in multiple sclerosis," Journal of Neurology, Neurosurgery and Psychiatry, vol. 79, no. 2, pp. 152-157, 2008. (Pubitemid 351236545)
61. I. A. van der Mei, A. L. Ponsonby, T. Dwyer et al., "Vitamin D levels in people with multiple sclerosis and community controls in Tasmania, Australia," Journal of Neurology, vol. 254, no. 5, pp. 581-590, 2007. (Pubitemid 46781963)
62. T. A. Craig, S. Sommer, C. R. Sussman, J. P. Grande, and R. Kumar, "Expression and regulation of the vitamin D receptor in the zebrafish, Danio rerio," Journal of Bone and Mineral Research, vol. 23, no. 9, pp. 1486-1496, 2008.
63. M. Gross and R. Kumar, "Physiology and biochemistry of vitamin D-dependent calcium binding proteins," American Journal of Physiology, vol. 259, no. 2, pp. F195-F209, 1990. (Pubitemid 20257477)
64. K. G. Warren and I. Catz, "Autoantibodies to myelin basic protein within multiple sclerosis central nervous system tissue," Journal of the Neurological Sciences, vol. 115, no. 2, pp. 169-176, 1993. (Pubitemid 23102445)
65. C. P. Genain, B. Cannella, S. L. Hauser, and C. S. Raine, "Identification of autoantibodies associated with myelin damage in multiple sclerosis," Nature Medicine, vol. 5, no. 2, pp. 170-175, 1999. (Pubitemid 29068523)
66. K. C. O'Connor, H. Appel, L. Bregoli et al., "Antibodies from inflamed central nervous system tissue recognize myelin oligodendrocyte glycoprotein," Journal of Immunology, vol. 175, no. 3, pp. 1974-1982, 2005. (Pubitemid 41023105)
67. S. Schmidt, C. G. Haase, L. Bezman et al., "Serum autoantibody responses to myelin oligodendrocyte glycoprotein and myelin basic protein in X-linked adrenoleukodystrophy and multiple sclerosis," Journal of Neuroimmunology, vol. 119, no. 1, pp. 88-94, 2001. (Pubitemid 32781732)
68. A. Karni, R. Bakimer-Kleiner, O. Abramsky, and A. Ben-Nun, "Elevated levels of antibody to myelin oligodendrocyte glycoprotein is not specific for patients with multiple sclerosis," Archives of Neurology, vol. 56, no. 3, pp. 311-315, 1999. (Pubitemid 29120228)
69. V. Lampasona, D. Franciotta, R. Furlan et al., "Similar low frequency of anti-MOG IgG and IgM in MS patients and healthy subjects," Neurology, vol. 62, no. 11, pp. 2092-2094, 2004. (Pubitemid 38738228)
70. R. Arnon, E. Crisp, and R. Kelley, "Anti-ganglioside antibodies in multiple sclerosis," Journal of the Neurological Sciences, vol. 46, no. 2, pp. 179-186, 1980. (Pubitemid 10156204)
71. T. Endo, D. D. Scott, S. S. Stewart, S. K. Kundu, and D. M. Marcus, "Antibodies to glycosphingolipids in patients with multiple sclerosis and SLE," Journal of Immunology, vol. 132, pp. 1793-1797, 1984. (Pubitemid 14168138)
72. S. Saidi, T. Mahjoub, and W. Y. Almawi, "Lupus anticoagulants and anti-phospholipid antibodies as risk factors for a first episode of ischemic stroke," Journal of Thrombosis and Haemostasis, vol. 7, no. 7, pp. 1075-1080, 2009.
73. W. Lim, M. A. Crowther, and J. W. Eikelboom, "Management of antiphospholipid antibody syndrome: A systematic review," Journal of the AmericanMedical Association, vol. 295, no. 9, pp. 1050-1057, 2006.
74. M. S. Freedman, J. Laks, N. Dotan, R. T. Altstock, A. Dukler, and C. J. Sindic, "Anti-glucose-based glycan IgM antibodies predict relapse activity in multiple sclerosis after the first neurological event," Multiple Sclerosis, vol. 15, no. 4, pp. 422-430, 2009.
75. M. Schwarz, L. Spector, M. Gortler et al., "Serum anti-Glc(?1,4)Glc(?) antibodies as a biomarker for relapsingremitting multiple sclerosis," Journal of the Neurological Sciences, vol. 244, no. 1-2, pp. 59-68, 2006.
76. L. M. Villar, M. C. Sadaba, E. Roldan et al., "Intrathecal synthesis of oligoclonal IgM against myelin lipids predicts an aggressive disease course in MS," Journal of Clinical Investigation, vol. 115, no. 1, pp. 187-194, 2005. (Pubitemid 40385520)
77. S. R. Hinson, S. J. Pittock, C. F. Lucchinetti et al., "Pathogenic potential of IgG binding to water channel extracellular domain in neuromyelitis optica," Neurology, vol. 69, no. 24, pp. 2221-2231, 2007. (Pubitemid 350294677)
78. S. R. Hinson, S. F. Roemer, C. F. Lucchinetti et al., "Aquaporin-4-binding autoantibodies in patients with neuromyelitis optica impair glutamate transport by downregulating EAAT2," Journal of Experimental Medicine, vol. 205, no. 11, pp. 2473-2481, 2008.
79. V. A. Lennon, T. J. Kryzer, S. J. Pittock, A. S. Verkman, and S. R. Hinson, "IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel," Journal of Experimental Medicine, vol. 202, no. 4, pp. 473-477, 2005. (Pubitemid 41186945)
80. J. H. Noseworthy, P. C. O'Brien, T. M. Petterson et al., "A randomized trial of intravenous immunoglobulin in inflammatory demyelinating optic neuritis," Neurology, vol. 56, no. 11, pp. 1514-1522, 2001. (Pubitemid 32532263)
81. B. Weinstock-Guttman, M. Ramanathan, N. Lincoff et al., "Study of mitoxantrone for the treatment of recurrent neuromyelitis optica (Devic disease)," Archives of Neurology, vol. 63, no. 7, pp. 957-963, 2006. (Pubitemid 44036296)
82. A. Jacob, M.Matiello, B. G.Weinshenker et al., "Treatment of neuromyelitis optica with mycophenolate mofetil: retrospective analysis of 24 patients," Archives of Neurology, vol. 66, no. 9, pp. 1128-1133, 2009.
83. B. A. Cree, S. Lamb, K. Morgan, A. Chen, E. Waubant, and C. Genain, "An open label study of the effects of rituximab in neuromyelitis optica," Neurology, vol. 64, no. 7, pp. 1270-1272, 2005.
84. M. Rodriguez, "Have we finally identified an autoimmune demyelinating disease?" Annals of Neurology, vol. 66, no. 5, pp. 572-573, 2009.
85. R. E. Bailey, "Diagnosis and treatment of infectiousmononucleosis, " American Family Physician, vol. 49, no. 4, pp. 879-885, 1994.
86. H. B. Jenson, "Virologic diagnosis, viral monitoring, and treatment of Epstein-Barr virus infectious mononucleosis," Current Infectious Disease Reports, vol. 6, no. 3, pp. 200-207, 2004. (Pubitemid 38899191)
87. S. Cepok, D. Zhou, R. Srivastava et al., "Identification of Epstein-Barr virus proteins as putative targets of the immune response in multiple sclerosis," Journal of Clinical Investigation, vol. 115, no. 5, pp. 1352-1360, 2005. (Pubitemid 40629055)
88. A. E. Handel, A. J.Williamson, G. Disanto, L. Handunnetthi, G. Giovannoni, and S. V. Ramagopalan, "An updated metaanalysis of risk of multiple sclerosis following infectious mononucleosis," PLoS One, vol. 5, no. 9, Article ID e12496, pp. 1-5, 2010.
89. E. L. Thacker, F. Mirzaei, and A. Ascherio, "Infectious mononucleosis and risk for multiple sclerosis: A meta-analysis," Annals of Neurology, vol. 59, no. 3, pp. 499-503, 2006. (Pubitemid 43358070)
90. S. V. Ramagopalan, A. E. Handel, G. Giovannoni, S. Rutherford Siegel, G. C. Ebers, and G. Chaplin, "Relationship of UV exposure to prevalence of multiple sclerosis in England," Neurology, vol. 76, no. 16, pp. 1410-1414, 2011.
91. M. J. Goldacre, C. J. Wotton, V. Seagroatt, and D. Yeates, "Multiple sclerosis after infectious mononucleosis: record linkage study," Journal of Epidemiology and Community Health, vol. 58, no. 12, pp. 1032-1035, 2004. (Pubitemid 39564205)
92. T. R. Nielsen, K. Rostgaard, N. M. Nielsen et al., "Multiple sclerosis after infectious mononucleosis," Archives of Neurology, vol. 64, no. 1, pp. 72-75, 2007. (Pubitemid 46072426)
93. G. C. Ebers and A. D. Sadovnick, "The geographic distribution of multiple sclerosis: A review," Neuroepidemiology, vol. 12, no. 1, pp. 1-5, 1993. (Pubitemid 23186648)
94. C. M. Poser, J. Benedikz, and P. L. Hibberd, "The epidemiology of multiple sclerosis: The Iceland model. Onset-adjusted prevalence rate and other methodological considerations," Journal of the Neurological Sciences, vol. 111, no. 2, pp. 143-152, 1992.
95. L. N. Rosen, I. R. Livingstone, and N. E. Rosenthal, "Multiple sclerosis and latitude: A new perspective on an old association," Medical Hypotheses, vol. 36, no. 4, pp. 376-378, 1991.
96. M. T. Cantorna, "Vitamin D and autoimmunity: is vitamin D status an environmental factor affecting autoimmune disease prevalence?" Proceedings of the Society for Experimental Biology and Medicine, vol. 223, no. 3, pp. 230-233, 2000. (Pubitemid 30337776)
97. M. T. Cantorna, "Vitamin D and multiple sclerosis: an update," Nutrition Reviews, vol. 66, supplement 2, pp. S135-S138, 2008.
98. B. M. VanAmerongen, C. D. Dijkstra, P. Lips, and C. H. Polman, "Multiple sclerosis and vitamin D: an update," European Journal of Clinical Nutrition, vol. 58, no. 8, pp. 1095-1109, 2004. (Pubitemid 39172383)
99. M. R. Haussler, C. A. Haussler, L. Bartik et al., "Vitamin D receptor: molecular signaling and actions of nutritional ligands in disease prevention," Nutrition Reviews, vol. 66, supplement 2, pp. S98-S112, 2008.
100. J. A. Johnson and R. Kumar, "Renal and intestinal calcium transport: roles of vitamin D and vitamin D-dependent calcium binding proteins," Seminars in Nephrology, vol. 14, no. 2, pp. 119-128, 1994. (Pubitemid 24083803)
101. P. W. Jurutka, L. Bartik, G. K. Whitfield et al., "Vitamin D receptor: key roles in bone mineral pathophysiology, molecular mechanism of action, and novel nutritional ligands," Journal of Bone and Mineral Research, vol. 22, no. 2, pp. V2-V10, 2007. (Pubitemid 351304640)
102. P. W. Jurutka, G. K. Whitfield, J. C. Hsieh, P. D. Thompson, C. A. Haussler, and M. R. Haussler, "Molecular nature of the vitamin D receptor and its role in regulation of gene expression," Reviews in Endocrine and Metabolic Disorders, vol. 2, no. 2, pp. 203-216, 2001. (Pubitemid 33635523)
103. R. Kumar, "Metabolism of 1,25-dihydroxyvitamin D3," Physiological Reviews, vol. 64, no. 2, pp. 478-504, 1984.
104. T. D. Veenstra, K. Prufer, C. Koenigsberger, S. W. Brimijoin, J. P. Grande, and R. Kumar, "1,25-dihydroxyvitamin D3 receptors in the central nervous system of the rat embryo," Brain Research, vol. 804, no. 2, pp. 193-205, 1998. (Pubitemid 28496623)
105. X. Dong, W. Lutz, T. M. Schroeder et al., "Regulation of relB in dendritic cells by means of modulated association of vitamin D receptor and histone deacetylase 3 with the promoter," Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 44, pp. 16007-16012, 2005. (Pubitemid 41552858)
106. M. D. Griffin, X. Dong, and R. Kumar, "Vitamin D receptormediated suppression of RelB in antigen presenting cells: A paradigm for ligand-augmented negative transcriptional regulation," Archives of Biochemistry and Biophysics, vol. 460, no. 2, pp. 218-226, 2007. (Pubitemid 46589403)
107. M. D. Griffin and R. Kumar, "Effects of ?,25(OH)2D3 and its analogs on dendritic cell function," Journal of Cellular Biochemistry, vol. 88, no. 2, pp. 323-326, 2003. (Pubitemid 36119905)
108. M. D. Griffin and R. Kumar, "Multiple potential clinical benefits for 1?,25-dihydroxyvitamin D3 analogs in kidney transplant recipients," Journal of Steroid Biochemistry and Molecular Biology, vol. 97, no. 1-2, pp. 213-218, 2005. (Pubitemid 41546231)
109. M. D. Griffin, W. Lutz, V. A. Phan, L. A. Bachman, D. J. McKean, and R. Kumar, "Dendritic cell modulation by 1?,25 dihydroxyvitamin D3 and its analogs: A vitamin D receptor-dependent pathway that promotes a persistent state of immaturity in vitro and in vivo," Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 12, pp. 6800-6805, 2001. (Pubitemid 32538297)
110. M. D. Griffin, N. Xing, and R. Kumar, "Vitamin D and its analogs as regulators of immune activation and antigen presentation," Annual Review of Nutrition, vol. 23, pp. 117-145, 2003. (Pubitemid 37059719)
111. N. Xing, M. L. Maldonado, L. A. Bachman, D. J. McKean, R. Kumar, and M. D. Griffin, "Distinctive dendritic cell modulation by vitamin D3 and glucocorticoid pathways," Biochemical and Biophysical Research Communications, vol. 297, no. 3, pp. 645-652, 2002.
112. J. J. Cannell, M. Zasloff, C. F. Garland, R. Scragg, and E. Giovannucci, "On the epidemiology of influenza," Virology Journal, vol. 5, article 29, 2008.
113. W. B. Grant, "Latitude and multiple sclerosis prevalence: vitamin D reduces risk of Epstein-Barr virus infection," Multiple Sclerosis, vol. 16, no. 3, pp. 373-375, 2010.
114. A. Dal Bianco, M. Bradl, J. Frischer, A. Kutzelnigg, K. Jellinger, and H. Lassmann, "Multiple sclerosis and Alzheimer's disease," Annals of Neurology, vol. 63, no. 2, pp. 174-183, 2008. (Pubitemid 351355296)
115. R. B. Lindert, C. G. Haase, U. Brehm, C. Linington, H. Wekerle, and R. Hohlfeld, "Multiple sclerosis: B-and Tcell responses to the extracellular domain of the myelin oligodendrocyte glycoprotein," Brain, vol. 122, no. 11, pp. 2089-2100, 1999.
116. L. Y. Wang and R. S. Fujinami, "Enhancement of EAE and induction of autoantibodies to T-cell epitopes in mice infected with a recombinant vaccinia virus encoding myelin proteolipid protein," Journal of Neuroimmunology, vol. 75, no. 1-2, pp. 75-83, 1997. (Pubitemid 27170305)
117. K.W.Wucherpfennig, I. Catz, S.Hausmann, J. L. Strominger, L. Steinman, and K. G.Warren, "Recognition of the immunodominant myelin basic protein peptide by autoantibodies andHLA-DR2-restricted T cell clones frommultiple sclerosis patients. Identity of key contact residues in the B-cell and Tcell epitopes," Journal of Clinical Investigation, vol. 100, no. 5, pp. 1114-1122, 1997. (Pubitemid 27386295)
118. C. T. Harp, A. E. Lovett-Racke, M. K. Racke, E. M. Frohman, and N. L. Monson, "Impact of myelin-specific antigen presenting B cells on T cell activation in multiple sclerosis," Clinical Immunology, vol. 128, no. 3, pp. 382-391, 2008.
119. D. Bourdette and V. Yadav, "B-cell depletion with rituximab in relapsing-remitting multiple sclerosis," Current Neurology and Neuroscience Reports, vol. 8, pp. 417-418, 2008.
120. S. L.Hauser, E.Waubant, D. L. Arnold et al., "B-cell depletion with rituximab in relapsing-remitting multiple sclerosis," New England Journal of Medicine, vol. 358, no. 7, pp. 676-688, 2008. (Pubitemid 351240747)
121. A. H. Cross, J. L. Stark, J. Lauber, M. J. Ramsbottom, and J. A. Lyons, "Rituximab reduces B cells and T cells in cerebrospinal fluid of multiple sclerosis patients," Journal of Neuroimmunology, vol. 180, no. 1-2, pp. 63-70, 2006. (Pubitemid 44767709)
122. A. Bar-Or, L. Fawaz, B. Fan et al., "Abnormal B-cell cytokine responses a trigger of T-cell-mediated disease inMS?" Annals of Neurology, vol. 67, no. 4, pp. 452-461, 2010.
123. S. Fillatreau, C. H. Sweenie, M. J. McGeachy, D. Gray, and S. M. Anderton, "B cells regulate autoimmunity by provision of IL-10," Nature Immunology, vol. 3, no. 10, pp. 944-950, 2002. (Pubitemid 35154008)
124. M. Duddy, M. Niino, F. Adatia et al., "Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis," Journal of Immunology, vol. 178, no. 10, pp. 6092-6099, 2007. (Pubitemid 46717389)
125. G. B. Pier, J. B. Lyczak, and L. M. Wetzler, Immunology, Infection, and Immunity, ASM Press, Washington, DC, USA, 2004.
126. J. P. Chippaux, "Snakebite epidemiology in Benin (West Africa)," Toxicon, vol. 27, p. 37, 1988.
127. H. Uhlig and R. Dernick, "Monoclonal autoantibodies derived from multiple sclerosis patients and control persons and their reactivities with antigens of the central nervous system," Autoimmunity, vol. 5, no. 1-2, pp. 87-99, 1989. (Pubitemid 20376847)
128. J. V. Ravetch and S. Bolland, "IgG Fc receptors," Annual Review of Immunology, vol. 19, pp. 275-290, 2001. (Pubitemid 32368037)
129. M. K. Storch, S. Piddlesden,M.Haltia, M. Iivanainen, P.Morgan, and H. Lassmann, "Multiple sclerosis: in situ evidence for antibody-and complement-mediated demyelination," Annals of Neurology, vol. 43, no. 4, pp. 465-471, 1998. (Pubitemid 28231721)
130. S. J. Piddlesden,H. Lassmann, F. Zimprich, B. P.Morgan, and C. Linington, "The demyelinating potential of antibodies to myelin oligodendrocyte glycoprotein is related to their ability to fix complement," American Journal of Pathology, vol. 143, no. 2, pp. 555-564, 1993. (Pubitemid 24058211)
131. E. Okun, M. P. Mattson, and T. V. Arumugam, "Involvement of Fc receptors in disorders of the central nervous system," NeuroMolecular Medicine, vol. 12, no. 2, pp. 164-178, 2010.
132. J.Neumann, "Ueber das Vorkommen der sogneannten " Mastzellen" bei pathologischen Veraenderungen des Gehirns," Virchows Archiv fur Pathologische Anatomie und Physiologie und fur Klinische Medizin, vol. 122, pp. 378-381, 1890.
133. Y. Olsson, "Mast cells in plaques of multiple sclerosis," Acta Neurologica Scandinavica, vol. 50, pp. 611-618, 1974.
134. P. G. Kruger, L. Bo, K. M.Myhr et al., "Mast cells andmultiple sclerosis: A light and electron microscopic study of mast cells in multiple sclerosis emphasizing staining procedures," Acta Neurologica Scandinavica, vol. 81, no. 1, pp. 31-36, 1990. (Pubitemid 20067134)
135. V. H. Secor, W. E. Secor, C. A. Gutekunst, and M. A. Brown, "Mast cells are essential for early onset and severe disease in a murine model of multiple sclerosis," Journal of Experimental Medicine, vol. 191, no. 5, pp. 813-822, 2000.
136. E. Frick and H. Stickl, "Antibody-dependent lymphocyte cytotoxicity against basic protein of myelin in multiple sclerosis," Journal of the Neurological Sciences, vol. 46, no. 2, pp. 187-197, 1980. (Pubitemid 10156205)
137. E. Frick and H. Stickl, "Specificity of antibody-dependent lymphocyte cytotoxicity against cerebral tissue constituents in multiple sclerosis. Studies with basic protein of myelin, encephalitogenic peptide, cerebrosides and gangliosides," Acta Neurologica Scandinavica, vol. 65, no. 1, pp. 30-37, 1982. (Pubitemid 12178844)
138. J. E. Merrill, B.Wahlin, A. Siden, and P. Perlmann, "Elevated direct and IgMenhanced ADCC activity in multiple sclerosis patients," Journal of Immunology, vol. 128, no. 4, pp. 1728-1735, 1982. (Pubitemid 12193033)
139. N. A. Ponomarenko, O. M. Durova, I. I. Vorobiev et al., "Catalytic antibodies in clinical and experimental pathology: human and mouse models," Journal of Immunological Methods, vol. 269, no. 1-2, pp. 197-211, 2002.
140. N. A. Ponomarenko, O. M. Durova, I. I. Vorobiev et al.,
141. A. A. Belogurov, I. N. Kurkova, V. K.Misikov et al., "Substrate specificity of catalytic autoantibodies in neurodegenerative processes," Doklady Biochemistry and Biophysics, vol. 413, no. 1, pp. 61-64, 2007. (Pubitemid 46726056)
142. W. Lang, M. Rodriguez, V. A. Lennon, and P. W. Lampert, "Demyelination and remyelination in murine viral encephalomyelitis," Annals of the New York Academy of Sciences, vol. 436, pp. 98-102, 1984. (Pubitemid 15102034)
143. M. Rodriguez, "Immunoglobulins stimulate central nervous system remyelination: electron microscopic and morphometric analysis of proliferating cells," Laboratory Investigation, vol. 64, no. 3, pp. 358-370, 1991.
144. M. Rodriguez and V. A. Lennon, "Immunoglobulins promote remyelination in the central nervous system," Annals of Neurology, vol. 27, no. 1, pp. 12-17, 1990. (Pubitemid 20031353)
145. K. Asakura, D. J. Miller, L. R. Pease, and M. Rodriguez, "Targeting of IgM? antibodies to oligodendrocytes promotes CNS remyelination," Journal of Neuroscience, vol. 18, no. 19, pp. 7700-7708, 1998. (Pubitemid 28441011)
146. K. Asakura, D. J. Miller, K. Murray, R. Bansal, S. E. Pfeiffer, and M. Rodriguez, "Monoclonal autoantibody SCH94.03, which promotes central nervous system remyelination, recognizes an antigen on the surface of oligodendrocytes," Journal of Neuroscience Research, vol. 43, no. 3, pp. 273-281, 1996. (Pubitemid 26057424)
147. K. Asakura, D. J. Miller, R. J. Pogulis, L. R. Pease, and M. Rodriguez, "Oligodendrocyte-reactive O1, O4, and HNK-1 monoclonal antibodies are encoded by germline immunoglobulin genes," Molecular Brain Research, vol. 34, no. 2, pp. 283-293, 1995. (Pubitemid 26007084)
148. D. J. Miller and M. Rodriguez, "A monoclonal autoantibody that promotes central nervous system remyelination in a model ofmultiple sclerosis is a natural autoantibody encoded by germline immunoglobulin genes," Journal of Immunology, vol. 154, no. 5, pp. 2460-2469, 1995.
149. A. J. Bieber, A. Warrington, K. Asakura et al., "Human antibodies accelerate the rate of remyelination following lysolecithin-induced demyelination in mice," Glia, vol. 37, no. 3, pp. 241-249, 2002.
150. Y. Mitsunaga, B. Ciric, V. Van Keulen et al., "Direct evidence that a human antibody derived from patient serum can promote myelin repair in a mouse model of chronic-progressive demyelinating disease," The FASEB Journal, vol. 16, no. 10, pp. 1325-1327, 2002.
151. V. P. Van Keulen, B. Ciric, S. Radhakrishnan et al., " Immunomodulation using the recombinant monoclonal human B7-DC cross-linking antibody rHIgM12," Clinical and Experimental Immunology, vol. 143, no. 2, pp. 314-321, 2006.
152. N. A. Ponomarenko, O. M. Durova, I. I. Vorobiev et al., "Catalytic activity of autoantibodies toward myelin basic protein correlates with the scores on the multiple sclerosis expanded disability status scale," Immunology Letters, vol. 103, no. 1, pp. 45-50, 2006. (Pubitemid 43162945)
153. A. E. Warrington, A. J. Bieber, B. Ciric, L. R. Pease, V. Van Keulen, and M. Rodriguez, "A recombinant human IgM promotes myelin repair after a single, very low dose," Journal of Neuroscience Research, vol. 85, no. 5, pp. 967-976, 2007. (Pubitemid 46580338)
154. I. Pirko, B. Ciric, J. Gamez et al., "A human antibody that promotes remyelination enters the CNS and decreases lesion load as detected by T2-weighted spinal cord MRI in a virusinduced murine model of MS," The FASEB Journal, vol. 18, no. 13, pp. 1577-1579, 2004. (Pubitemid 39561638)
155. M. M. Paz Soldan, A. E. Warrington, A. J. Bieber et al., "Remyelination-promoting antibodies activate distinct Ca2+ influx pathways in astrocytes and oligodendrocytes: relationship to the mechanism of myelin repair,"Molecular and Cellular Neuroscience, vol. 22, no. 1, pp. 14-24, 2003. (Pubitemid 36269112)
156. C. L. Howe, A. J. Bieber, A. E. Warrington, L. R. Pease, and M. Rodriguez, "Antiapoptotic signaling by a remyelinationpromoting human antimyelin antibody," Neurobiology of Disease, vol. 15, no. 1, pp. 120-131, 2004. (Pubitemid 38134387)
157. J. Watzlawik, E. Holicky, D. D. Edberg et al., "Human remyelination promoting antibody inhibits apoptotic signaling and differentiation through Lyn kinase in primary rat oligodendrocytes," Glia, vol. 58, no. 15, pp. 1782-1793, 2010.
158. M. Vrethem, T. Skogh, G. Berlin, H. Holmgren, and J. Ernerudh, "Antibodies to peripheral nerve myelin may occur without clinical neuropathy in healthypersons," Journal of Neuroimmunology, vol. 32, no. 3, pp. 219-222, 1991.
159. M. R. Kotter, W. W. Li, C. Zhao, and R. J. Franklin, "Myelin impairs CNS remyelination by inhibiting oligodendrocyte precursor cell differentiation," Journal of Neuroscience, vol. 26, no. 1, pp. 328-332, 2006. (Pubitemid 43089546)
160. C. L. Howe, S. Mayoral, and M. Rodriguez, "Activated microglia stimulate transcriptional changes in primary oligodendrocytes via IL-1?," Neurobiology of Disease, vol. 23, no. 3, pp. 731-739, 2006. (Pubitemid 44234109)