Epstein-Barr virus and multiple sclerosis

Journal of Neurology, Neurosurgery and Psychiatry

Volumn 82, Issue 10, 2011, Pages 1142-1148

  Lucas, R M ^a   Hughes, A M ^a   Lay, M L J ^b   Ponsonby, A L ^c   Dwyer, D E ^b   Taylor, B V ^d   Pender, M P ^e  

^a The Australian National University   (Australia)

^b WESTMEAD HOSPITAL   (Australia)

^c MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF TASMANIA   (Australia)

^e UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CRYSTALLIN; EPSTEIN BARR VIRUS ANTIGEN; EPSTEIN BARR VIRUS ANTIGEN 1; HLA DR ANTIGEN; INTERLEUKIN 10;

AGE DISTRIBUTION; ANTIBODY TITER; CROSS REACTION; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; DISEASE COURSE; DOSE RESPONSE; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; GENETIC ASSOCIATION; GEOGRAPHIC DISTRIBUTION; HUMAN; MEDICAL HISTORY; MULTIPLE SCLEROSIS; PATHOGENESIS; PREVALENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECURRENT DISEASE; REVIEW; RISK FACTOR; SEROLOGY; TONSILLECTOMY; TONSILLITIS; VIRUS CELL INTERACTION; VIRUS LOAD; VIRUS REACTIVATION;

ALPHA-CRYSTALLIN B CHAIN; ANTIBODIES, VIRAL; AUTOANTIGENS; B-LYMPHOCYTES; CROSS-SECTIONAL STUDIES; DISEASE PROGRESSION; DNA, VIRAL; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; HERPESVIRUS 4, HUMAN; HUMANS; INFECTIOUS MONONUCLEOSIS; MOLECULAR MIMICRY; MULTIPLE SCLEROSIS; RISK FACTORS; T-LYMPHOCYTES;

EID: 80052640129     PISSN: 00223050     EISSN: 1468330X     Source Type: Journal    
DOI: 10.1136/jnnp-2011-300174     Document Type: Review

References (97)

1. Ascherio A, Munger K. Epidemiology of multiple sclerosis: from risk factors to prevention. Semin Neurol 2008;28:17-28. (Pubitemid 351273081)
2. Rolls AE, Giovannoni G, Constantinescu CS, et al. Multiple sclerosis, lymphoma and nasopharyngeal carcinoma: the central role of Epstein-Barr virus? Eur Neurol 2010;63:29-35.
3. Ascherio A, Munger KL. Epstein-Barr virus infection and multiple sclerosis: a review. J Neuroimmune Pharmacol 2010;5:271-7.
4. Milo R, Kahana E. Multiple sclerosis: geoepidemiology, genetics and the environment. Autoimmun Rev 2010;9:A387-94.
5. Ramagopalan SV, Hoang U, Seagroatt V, et al. Geography of hospital admissions for multiple sclerosis in England and comparison with the geography of hospital admissions for infectious mononucleosis: a descriptive study. J Neurol Neurosurg Psychiatry 2011;82:682-7.
6. Warner HB, Carp RI. Multiple sclerosis and Epstein-Barr virus. Lancet 1981;2:1290.
7. Hallee TJ, Evans AS, Niederman JC, et al. Infectious mononucleosis at the United States Military Academy. A prospective study of a single class over four years. Yale J Biol Med 1974;47:182-95.
8. Pordeus V, Barzilai O, Sherer Y, et al. A latitudinal gradient study of common anti-infectious agent antibody prevalence in Italy and Colombia. Isr Med Assoc J 2008;10:65-8. (Pubitemid 351649470)
9. Taylor BV, Lucas RM, Dear K, et al. Latitudinal variation in incidence and type of first central nervous system demyelinating events. Mult Scler 2010;16:398-405.
10. Ascherio A, Munger KL. Environmental risk factors for multiple sclerosis. Part II: noninfectious factors. Ann Neurol 2007;61:504-13. (Pubitemid 47068132)
11. Pancharoen C, Mekmullica J, Chinratanapisit S, et al. Seroprevalence of Epstein- Barr virus antibody among children in various age groups in Bangkok, Thailand. Asian Pac J Allergy Immunol 2001;19:135-7. (Pubitemid 33034811)
12. Morris MC, Edmunds WJ, Hesketh LM, et al. Sero-epidemiological patterns of Epstein-Barr and herpes simplex (HSV-1 and HSV-2) viruses in England and Wales. J Med Virol 2002;67:522-7. (Pubitemid 34747671)
13. Handel AE, Williamson AJ, Disanto G, et al. An updated meta-analysis of risk of multiple sclerosis following infectious mononucleosis. PLoS One 2010;5:e12496.
14. Zaadstra BM, Chorus AM, Van Buuren S, et al. Selective association of multiple sclerosis with infectious mononucleosis. Mult Scler 2008;14:307-13. (Pubitemid 351676425)
15. Ahlgren C, Toren K, Oden A, et al. A population-based case-control study on viral infections and vaccinations and subsequent multiple sclerosis risk. Eur J Epidemiol 2009;24:541-52.
16. Yamanaka N, Kataura A. Viral infections associated with recurrent tonsillitis. Acta Otolaryngol Suppl 1984;416:30-7. (Pubitemid 15117198)
17. Goldacre MJ, Wotton CJ, Seagroatt V, et al. Multiple sclerosis after infectious mononucleosis: record linkage study. J Epidemiol Community Health 2004;58:1032-5. (Pubitemid 39564205)
18. Nielsen TR, Rostgaard K, Nielsen NM, et al. Multiple sclerosis after infectious mononucleosis. Arch Neurol 2007;64:72-5. (Pubitemid 46072426)
19. Nielsen TR, Rostgaard K, Askling J, et al. Effects of infectious mononucleosis and HLA-DRB1*15 in multiple sclerosis. Mult Scler 2009;15:431-6.
20. Sumaya CV, Myers LW, Ellison GW. Epstein-Barr virus antibodies in multiple sclerosis. Arch Neurol 1980;37:94-6. (Pubitemid 10174389)
21. Munch M, Riisom K, Christensen T, et al. The significance of Epstein-Barr virus seropositivity in multiple sclerosis patients? Acta Neurol Scand 1998;97:171-4. (Pubitemid 28254913)
22. Wagner HJ, Hennig H, Jabs WJ, et al. Altered prevalence and reactivity of anti- Epstein-Barr virus antibodies in patients with multiple sclerosis. Viral Immunol 2000;13:497-502. (Pubitemid 32063561)
23. Ascherio A, Munch M. Epstein-Barr virus and multiple sclerosis. Epidemiology 2000;11:220-4. (Pubitemid 30112026)
24. Ascherio A, Munger KL. Environmental risk factors for multiple sclerosis. Part I: the role of infection. Ann Neurol 2007;61:288-99. (Pubitemid 46676728)
25. Gulley ML, Tang W. Laboratory assays for Epstein-Barr virus-related disease. J Mol Diagn 2008;10:279-92. (Pubitemid 352022708)
26. Klutts JS, Ford BA, Perez NR, et al. Evidence-based approach for interpretation of Epstein-Barr virus serological patterns. J Clin Microbiol 2009;47:3204-10.
27. Santiago O, Gutierrez J, Sorlozano A, et al. Relation between Epstein-Barr virus and multiple sclerosis: analytic study of scientific production. Eur J Clin Microbiol Infect Dis 2010;29:857-66.
28. Ascherio A, Munger KL, Lennette ET, et al. Epstein-Barr virus antibodies and risk of multiple sclerosis: a prospective study. JAMA 2001;286:3083-8. (Pubitemid 34016522)
29. Levin LI, Munger KL, Rubertone MV, et al. Temporal relationship between elevation of Epstein-Barr virus antibody titers and initial onset of neurological symptoms in multiple sclerosis. JAMA 2005;293:2496-500. (Pubitemid 40705731)
30. Lunemann JD, Jelcic I, Roberts S, et al. EBNA1-specific T cells from patients with multiple sclerosis cross react with myelin antigens and co-produce IFN-gamma and IL-2. J Exp Med 2008;205:1763-73.
31. Andersson M, Alvarez-Cermeno J, Bernardi G, et al. Cerebrospinal fluid in the diagnosis of multiple sclerosis: a consensus report. J Neurol Neurosurg Psychiatry 1994;57:897-902. (Pubitemid 24251050)
32. Christensen T. The role of EBV in MS pathogenesis. Int MS J 2006;13:52-7. (Pubitemid 43764528)
33. Franciotta D, Di Stefano AL, Jarius S, et al. Cerebrospinal BAFF and Epstein-Barr virus-specific oligoclonal bands in multiple sclerosis and other inflammatory demyelinating neurological diseases. J Neuroimmunol 2011;230:160-3.
34. Villegas E, Santiago O, Carrillo JA, et al. Low intrathecal immune response of anti- EBNA-1 antibodies and EBV DNA from multiple sclerosis patients. Diagn Microbiol Infect Dis 2011;70:85-90.
35. Bray PF, Luka J, Culp KW, et al. Antibodies against Epstein-Barr nuclear antigen (EBNA) in multiple sclerosis CSF, and two pentapeptide sequence identities between EBNA and myelin basic protein. Neurology 1992;42:1798-804.
36. Cepok S, Zhou D, Srivastava R, et al. Identification of Epstein-Barr virus proteins as putative targets of the immune response in multiple sclerosis. J Clin Invest 2005;115:1352-60. (Pubitemid 40629055)
37. Jaquiery E, Jilek S, Schluep M, et al. Intrathecal immune responses to EBV in early MS. Eur J Immunol 2010;40:878-87.
38. Rand KH, Houck H, Denslow ND, et al. Epstein-Barr virus nuclear antigen-1 (EBNA-1) associated oligoclonal bands in patients with multiple sclerosis. J Neurol Sci 2000;173:32-9. (Pubitemid 30081773)
39. DeLorenze GN, Munger KL, Lennette ET, et al. Epstein-Barr virus and multiple sclerosis: evidence of association from a prospective study with long-term follow-up. Arch Neurol 2006;63:839-44. (Pubitemid 43882291)
40. Sundstrom P, Juto P, Wadell G, et al. An altered immune response to Epstein-Barr virus in multiple sclerosis: a prospective study. Neurology 2004;62:2277-82. (Pubitemid 38787787)
41. Banwell B, Bar-Or A, Arnold DL, et al. Clinical, environmental, and genetic determinants of multiple sclerosis in children with acute demyelination: a prospective national cohort study. Lancet Neurol 2011;10:436-45.
42. Levin LI, Munger KL, O'Reilly EJ, et al. Primary infection with the Epstein-Barr virus and risk of multiple sclerosis. Ann Neurol 2010;67:824-30.
43. Lunemann JD, Tintore M, Messmer B, et al. Elevated Epstein-Barr virus-encoded nuclear antigen-1 immune responses predict conversion to multiple sclerosis. Ann Neurol 2010;67:159-69.
44. Villoslada P, Juste C, Tintore M, et al. The immune response against herpesvirus is more prominent in the early stages of MS. Neurology 2003;60:1944-8. (Pubitemid 36736010)
45. Nielsen TR, Pedersen M, Rostgaard K, et al. Correlations between Epstein-Barr virus antibody levels and risk factors for multiple sclerosis in healthy individuals. Mult Scler 2007;13:420-3. (Pubitemid 46706004)
46. Simon KC, Van der Mei IA, Munger KL, et al. Combined effects of smoking, anti- EBNA antibodies, and HLA-DRB1*1501 on multiple sclerosis risk. Neurology 2010;74:1365-71.
47. De Jager PL, Simon KC, Munger KL, et al. Integrating risk factors: HLA-DRB1*1501 and Epstein-Barr virus in multiple sclerosis. Neurology 2008;70:1113-18. (Pubitemid 351464768)
48. Van der Mei IA, Ponsonby AL, Taylor BV, et al. Human leukocyte antigen-DR15, low infant sibling exposure and multiple sclerosis: gene-environment interaction. Ann Neurol 2010;67:261-5.
49. Sundstrom P, Nystrom L, Jidell E, et al. EBNA-1 reactivity and HLA DRB1*1501 as statistically independent risk factors for multiple sclerosis: a case-control study. Mult Scler 2008;14:1120-2.
50. Sundstrom P, Nystrom M, Ruuth K, et al. Antibodies to specific EBNA-1 domains and HLA DRB1*1501 interact as risk factors for multiple sclerosis. J Neuroimmunol 2009;215:102-7.
51. James JA, Anderson J, Chabas D, et al. Pediatric-onset multiple sclerosis patients sera recognize unique regions of Epstein-Barr nuclear antigen 1. Mult Scler J 2009;15:1406.
52. Lunemann JD, Huppke P, Roberts S, et al. Broadened and elevated humoral immune response to EBNA1 in pediatric multiple sclerosis. Neurology 2008;71:1033-5.
53. Lunemann JD, Edwards N, Muraro PA, et al. Increased frequency and broadened specificity of latent EBV nuclear antigen-1-specific T cells in multiple sclerosis. Brain 2006;129:1493-506. (Pubitemid 43999382)
54. Lindsey JW, Hatfield LM, Crawford MP, et al. Quantitative PCR for Epstein-Barr virus DNA and RNA in multiple sclerosis. Mult Scler 2009;15:153-8.
55. Alvarez-Lafuente R, De Las Heras V, Bartolome M, et al. Human herpesvirus 6 and multiple sclerosis: a one-year follow-up study. Brain Pathol 2006;16:20-7.
56. Lucas RM, Ponsonby AL, Dear K, et al. Current and past Epstein-Barr virus infection in risk of initial CNS demyelination. Neurology 2011;77:371-9.
57. Wagner HJ, Munger KL, Ascherio A. Plasma viral load of Epstein-Barr virus and risk of multiple sclerosis. Eur J Neurol 2004;11:833-4. (Pubitemid 39665060)
58. Serafini B, Rosicarelli B, Franciotta D, et al. Dysregulated Epstein-Barr virus infection in the multiple sclerosis brain. J Exp Med 2007;204:2899-912. (Pubitemid 350179559)
59. Willis SN, Stadelmann C, Rodig SJ, et al. Epstein-Barr virus infection is not a characteristic feature of multiple sclerosis brain. Brain 2009;132:3318-28.
60. Peferoen LA, Lamers F, Lodder LN, et al. Epstein Barr virus is not a characteristic feature in the central nervous system in established multiple sclerosis. Brain 2010;133:-137.
61. Pender MP. Does Epstein-Barr virus infection in the brain drive the development of multiple sclerosis? Brain 2009;132:3196-8.
62. Mancuso R, Hernis A, Cavarretta R, et al. Detection of viral DNA sequences in the cerebrospinal fluid of patients with multiple sclerosis. J Med Virol 2010;82:1051-7.
63. Sargsyan SA, Shearer AJ, Ritchie AM, et al. Absence of Epstein-Barr virus in the brain and CSF of patients with multiple sclerosis. Neurology 2010;74:1127-35.
64. Casiraghi C, Dorovini-Zis K, Horwitz MS. Epstein-Barr virus infection of human brain microvessel endothelial cells: a novel role in multiple sclerosis. J Neuroimmunol 2011;230:173-7.
65. Brennan R, Burrows J, Bell M, et al. Strains of Epstein-Barr virus infecting multiple sclerosis patients. Mult Scler 2010;16:643-51.
66. Lindsey JW, Patel S, Zou J. Epstein-Barr virus genotypes in multiple sclerosis. Acta Neurol Scand 2008;117:141-4.
67. Hollsberg P, Hansen HJ, Haahr S. Altered CD8+ T cell responses to selected Epstein-Barr virus immunodominant epitopes in patients with multiple sclerosis. Clin Exp Immunol 2003;132:137-43. (Pubitemid 36418916)
68. Gronen F, Ruprecht K, Weissbrich B, et al. Frequency analysis of HLA-B7-restricted Epstein-Barr virus-specific cytotoxic T lymphocytes in patients with multiple sclerosis and healthy controls. J Neuroimmunol 2006;180:185-92. (Pubitemid 44692331)
69. Pender MP, Csurhes PA, Lenarczyk A, et al. Decreased T cell reactivity to Epstein- Barr virus infected lymphoblastoid cell lines in multiple sclerosis. J Neurol Neurosurg Psychiatry 2009;80:498-505.
70. Shi Y, Smith KD, Kurilla MG, et al. Cytotoxic CD8+ T cells recognize EBV antigen but poorly kill autologous EBV-infected B lymphoblasts: immunodominance is elicited by a peptide epitope that is presented at low levels in vitro. J Immunol 1997;159:1844-52. (Pubitemid 127484172)
71. Pudney VA, Leese AM, Rickinson AB, et al. CD8+ immunodominance among Epstein-Barr virus lytic cycle antigens directly reflects the efficiency of antigen presentation in lytically infected cells. J Exp Med 2005;201:349-60. (Pubitemid 40229410)
72. Tynan FE, Elhassen D, Purcell AW, et al. The immunogenicity of a viral cytotoxic T cell epitope is controlled by its MHC-bound conformation. J Exp Med 2005;202:1249-60. (Pubitemid 41586955)
73. Craig JC, Haire M, Merrett JD. T-cell-mediated suppression of Epstein-Barr virus-induced B lymphocyte activation in multiple sclerosis. Clin Immunol Immunopathol 1988;48:253-60.
74. Fraser KB, Haire M, Millar JH, et al. Increased tendency to spontaneous in-vitro lymphocyte transformation in clinically active multiple sclerosis. Lancet 1979;2:175-6.
75. Ponsonby AL, Van der Mei I, Dwyer T, et al. Exposure to infant siblings during early life and risk of multiple sclerosis. JAMA 2005;293:463-9.
76. Alotaibi S, Kennedy J, Tellier R, et al. Epstein-Barr virus in pediatric multiple sclerosis. JAMA 2004;291:1875-9. (Pubitemid 38509501)
77. Banwell B, Krupp L, Kennedy J, et al. Clinical features and viral serologies in children with multiple sclerosis: a multinational observational study. Lancet Neurol 2007;6:773-81. (Pubitemid 47238663)
78. Sibley WA, Bamford CR, Clark K. Clinical viral infections and multiple sclerosis. Lancet 1985;1:1313-15. (Pubitemid 15059152)
79. Correale J, Fiol M, Gilmore W. The risk of relapses in multiple sclerosis during systemic infections. Neurology 2006;67:652-9. (Pubitemid 44273613)
80. Tremlett H, Van der Mei IA, Pittas F, et al. Monthly ambient sunlight, infections and relapse rates in multiple sclerosis. Neuroepidemiology 2008;31:271-9.
81. Pender M. The essential role of Epstein-Barr virus in the pathogenesis of multiple sclerosis. Neuroscientist 2011;17:351-67.
82. Lucas RM, McMichael AJ. Association or causation: evaluating links between "environment and disease". Bull World Health Organ 2005;83:792-5. (Pubitemid 41474699)
83. Lang HL, Jacobsen H, Ikemizu S, et al. A functional and structural basis for TCR cross-reactivity in multiple sclerosis. Nat Immunol 2002;3:940-3. (Pubitemid 35154007)
84. Pender MP. Infection of autoreactive B lymphocytes with EBV, causing chronic autoimmune diseases. Trends Immunol 2003;24:584-8. (Pubitemid 37338526)
85. Van Sechel AC, Bajramovic JJ, Van Stipdonk MJ, et al. EBV-induced expression and HLA-DR-restricted presentation by human B cells of alpha B-crystallin, a candidate autoantigen in multiple sclerosis. J Immunol 1999;162:129-35. (Pubitemid 29018912)
86. Van Noort JM, Bajramovic JJ, Plomp AC, et al. Mistaken self, a novel model that links microbial infections with myelin-directed autoimmunity in multiple sclerosis. J Neuroimmunol 2000;105:46-57. (Pubitemid 30125428)
87. Hayes CE, Acheson DE. A unifying multiple sclerosis etiology linking virus infection, sunlight, and vitamin D, through viral interleukin-10. Med Hypotheses 2008;71:85-90.
88. Correale J, Farez M. Association between parasite infection and immune responses in multiple sclerosis. Ann Neurol 2007;61:97-108. (Pubitemid 46363837)
89. Amu S, Saunders SP, Kronenberg M, et al. Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J Allergy Clin Immunol 2010;125:1114-24 -8.
90. Lund FE, Randall TD. Effector and regulatory B cells: modulators of CD4(+) T cell immunity. Nat Rev Immunol 2010;10:236-47.
91. Holmoy T. Vitamin D status modulates the immune response to Epstein Barr virus: Synergistic effect of risk factors in multiple sclerosis. Med Hypotheses 2008;70:66-9. (Pubitemid 350167496)
92. Mowry EM, James JA, Krupp LB, et al. Vitamin D status and antibody levels to common viruses in pediatric-onset multiple sclerosis. Mult Scler 2011;17:666-71.
93. Ponsonby AL, Dwyer T, Van der Mei I, et al. Asthma onset prior to multiple sclerosis and the contribution of sibling exposure in early life. Clin Exp Immunol 2006;146:463-70. (Pubitemid 44722165)
94. Lunemann JD, Kamradt T, Martin R, et al. Epstein-Barr virus: environmental trigger of multiple sclerosis? J Virol 2007;81:6777-84. (Pubitemid 46986614)
95. Tai AK, O'Reilly EJ, Alroy KA, et al. Human endogenous retrovirus-K18 Env as a risk factor in multiple sclerosis. Mult Scler 2008;14:1175-80.
96. Wardemann H, Yurasov S, Schaefer A, et al. Predominant autoantibody production by early human B cell precursors. Science 2003;301:1374-7. (Pubitemid 37075812)
97. Hauser SL, Waubant E, Arnold DL, et al. B-cell depletion with rituximab in relapsingremitting multiple sclerosis. N Engl J Med 2008;358:676-88. (Pubitemid 351240747)