A complex role of herpes viruses in the disease process of multiple sclerosis

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Wuest, Simone C ^a   Mexhitaj, Ina ^a   Chai, Noo Ri ^a   Romm, Elena ^a   Scheffel, Joerg ^b   Xu, Biying ^c   Lane, Kelly ^c   Wu, Tianxia ^a   Bielekova, Bibiana ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; DACLIZUMAB; MYELIN; EPITOPE; IMMUNOGLOBULIN G; IMMUNOSUPPRESSIVE AGENT; MONOCLONAL ANTIBODY; VIRUS ANTIGEN;

ADULT; AGED; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; BRAIN HOMOGENATE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL LYSATE; CEREBROSPINAL FLUID; CHRONIC DRUG ADMINISTRATION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOMEGALOVIRUS; DENDRITIC CELL; DISEASE ACTIVITY; DRUG EFFICACY; DRUG MECHANISM; EPSTEIN BARR VIRUS; FEMALE; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 6; LYMPHOCYTE PROLIFERATION; MAJOR CLINICAL STUDY; MALE; MULTIPLE SCLEROSIS; NERVE CELL; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OLIGODENDROGLIA; TH1 CELL; VIRUS PATHOGENESIS; VIRUS REACTIVATION; YOUNG ADULT; CASE CONTROL STUDY; COMPLICATION; DRUG EFFECTS; HERPES VIRUS INFECTION; HERPESVIRIDAE; IMMUNOLOGY; IMMUNOPHENOTYPING; LYMPHOCYTE ACTIVATION; METABOLISM; MIDDLE AGED; PHENOTYPE; T LYMPHOCYTE SUBPOPULATION;

ADULT; AGED; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIGENS, VIRAL; AUTOANTIGENS; CASE-CONTROL STUDIES; EPITOPES, T-LYMPHOCYTE; FEMALE; HERPESVIRIDAE; HERPESVIRIDAE INFECTIONS; HUMANS; IMMUNOGLOBULIN G; IMMUNOPHENOTYPING; IMMUNOSUPPRESSIVE AGENTS; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; PHENOTYPE; T-LYMPHOCYTE SUBSETS; YOUNG ADULT;

EID: 84908420575     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0105434     Document Type: Article

References (51)

1. Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG (2000) Multiple sclerosis. N Engl J Med 343: 938-952.
2. Baxevanis CN, Reclos GJ, Servis C, Anastasopoulos E, Arsenis P, et al. (1989) Peptides of myelin basic protein stimulate T lymphocytes from patients with multiple sclerosis. J Neuroimmunol 22: 23-30. (Pubitemid 19064633)
3. Olsson T, Sun J, Hillert J, Hojeberg B, Ekre HP, et al. (1992) Increased numbers of T cells recognizing multiple myelin basic protein epitopes in multiple sclerosis. Eur J Immunol 22: 1083-1087.
4. Arbour N, Holz A, Sipe JC, Naniche D, Romine JS, et al. (2003) A new approach for evaluating antigen-specific T cell responses to myelin antigens during the course of multiple sclerosis. J Neuroimmunol 137: 197-209. (Pubitemid 36351582)
5. Utz PJ, Gensler TJ, Anderson P (2000) Death, autoantigen modifications, and tolerance. Arthritis Res 2: 101-114. (Pubitemid 32223707)
6. Hall JC, Casciola-Rosen L, Rosen A (2004) Altered structure of autoantigens during apoptosis. Rheum Dis Clin North Am 30: 455-471, vii. (Pubitemid 38916996)
7. Lincoln MR, Montpetit A, Cader MZ, Saarela J, Dyment DA, et al. (2005) A predominant role for the HLA class II region in the association of the MHC region with multiple sclerosis. Nat Genet 37: 1108-1112. (Pubitemid 41486664)
8. International Multiple Sclerosis Genetics C, Wellcome Trust Case Control C, Sawcer S, Hellenthal G, Pirinen M, et al. (2011) Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 476: 214-219.
9. Maimone D, Gregory S, Arnason BG, Reder AT (1991) Cytokine levels in the cerebrospinal fluid and serum of patients with multiple sclerosis. J Neuroimmunol 32: 67-74.
10. Tsukada N, Miyagi K, Matsuda M, Yanagisawa N, Yone K (1991) Tumor necrosis factor and interleukin-1 in the CSF and sera of patients with multiple sclerosis. J Neurol Sci 104: 230-234.
11. Edwards LJ, Sharrack B, Ismail A, Tench CR, Gran B, et al. (2013) Increased levels of interleukins 2 and 17 in the cerebrospinal fluid of patients with idiopathic intracranial hypertension. Am J Clin Exp Immunol 2: 234-244.
12. von Budingen HC, Kuo TC, Sirota M, van Belle CJ, Apeltsin L, et al. (2012) B cell exchange across the blood-brain barrier in multiple sclerosis. J Clin Invest 122: 4533-4543.
13. Becker KJ, Kalil AJ, Tanzi P, Zierath DK, Savos AV, et al. (2011) Autoimmune responses to the brain after stroke are associated with worse outcome. Stroke 42: 2763-2769.
14. Becker KJ (2012) Activation of immune responses to brain antigens after stroke. J Neurochem 123 Suppl 2: 148-155.
15. Han S, Lin YC, Wu T, Salgado AD, Mexhitaj I, et al. (2014) Comprehensive Immunophenotyping of Cerebrospinal Fluid Cells in Patients with Neuroimmunological Diseases. J Immunol.
16. Challoner PB, Smith KT, Parker JD, MacLeod DL, Coulter SN, et al. (1995) Plaque-associated expression of human herpesvirus 6 in multiple sclerosis. Proc Natl Acad Sci U S A 92: 7440-7444.
17. Soldan SS, Jacobson S (2001) Role of viruses in etiology and pathogenesis of multiple sclerosis. Adv Virus Res 56: 517-555. (Pubitemid 33804570)
18. Ascherio A, Munger KL (2007) Environmental risk factors for multiple sclerosis. Part I: the role of infection. Ann Neurol 61: 288-299. (Pubitemid 46676728)
19. Landis SC, Amara SG, Asadullah K, Austin CP, Blumenstein R, et al. (2012) A call for transparent reporting to optimize the predictive value of preclinical research. Nature 490: 187-191.
20. Jaeger LB, Dohgu S, Sultana R, Lynch JL, Owen JB, et al. (2009) Lipopolysaccharide alters the blood-brain barrier transport of amyloid beta protein: a mechanism for inflammation in the progression of Alzheimer's disease. Brain Behav Immun 23: 507-517.
21. Norton WT, Poduslo SE (1973) Myelination in rat brain: method of myelin isolation. J Neurochem 21: 749-757.
22. Bickham K, Munz C, Tsang ML, Larsson M, Fonteneau JF, et al. (2001) EBNA1-specific CD4+ T cells in healthy carriers of Epstein-Barr virus are primarily Th1 in function. J Clin Invest 107: 121-130. (Pubitemid 32047421)
23. Wuest SC, Edwan JH, Martin JF, Han S, Perry JS, et al. (2011) A role for interleukin-2 trans-presentation in dendritic cell-mediated T cell activation in humans, as revealed by daclizumab therapy. Nat Med 17: 604-609.
24. Elong Ngono A, Pettre S, Salou M, Bahbouhi B, Soulillou JP, et al. (2012) Frequency of circulating autoreactive T cells committed to myelin determinants in relapsing-remitting multiple sclerosis patients. Clin Immunol 144: 117-126.
25. Bielekova B, Howard T, Packer AN, Richert N, Blevins G, et al. (2009) Effect of anti-CD25 antibody daclizumab in the inhibition of inflammation and stabilization of disease progression in multiple sclerosis. Arch Neurol 66: 483-489.
26. Wynn D, Kaufman M, Montalban X, Vollmer T, Simon J, et al. (2010) Daclizumab in active relapsing multiple sclerosis (CHOICE study): a phase 2, randomised, double-blind, placebo-controlled, add-on trial with interferon beta. Lancet Neurol 9: 381-390.
27. Bielekova B, Richert N, Herman ML, Ohayon J, Waldmann TA, et al. (2011) Intrathecal effects of daclizumab treatment of multiple sclerosis. Neurology 77: 1877-1886.
28. Banwell B, Bar-Or A, Cheung R, Kennedy J, Krupp LB, et al. (2008) Abnormal T-cell reactivities in childhood inflammatory demyelinating disease and type 1 diabetes. Ann Neurol 63: 98-111. (Pubitemid 351240556)
29. Bielekova B, Sung MH, Kadom N, Simon R, McFarland H, et al. (2004) Expansion and functional relevance of high-avidity myelin-specific CD4+ T cells in multiple sclerosis. J Immunol 172: 3893-3904. (Pubitemid 38337977)
30. O'Connor KC, Chitnis T, Griffin DE, Piyasirisilp S, Bar-Or A, et al. (2003) Myelin basic protein-reactive autoantibodies in the serum and cerebrospinal fluid of multiple sclerosis patients are characterized by low-affinity interactions. J Neuroimmunol 136: 140-148. (Pubitemid 36298853)
31. Reindl M, Di Pauli F, Rostasy K, Berger T (2013) The spectrum of MOG autoantibody-associated demyelinating diseases. Nat Rev Neurol 9: 455-461.
32. Hummel M, Bonifacio E, Schmid S, Walter M, Knopff A, et al. (2004) Brief communication: early appearance of islet autoantibodies predicts childhood type 1 diabetes in offspring of diabetic parents. Ann Intern Med 140: 882-886.
33. Ziegler AG, Rewers M, Simell O, Simell T, Lempainen J, et al. (2013) Seroconversion to multiple islet autoantibodies and risk of progression to diabetes in children. JAMA 309: 2473-2479.
34. Srivastava R, Aslam M, Kalluri SR, Schirmer L, Buck D, et al. (2012) Potassium channel KIR4.1 as an immune target in multiple sclerosis. N Engl J Med 367: 115-123.
35. Derfuss T, Parikh K, Velhin S, Braun M, Mathey E, et al. (2009) Contactin-2/TAG-1-directed autoimmunity is identified in multiple sclerosis patients and mediates gray matter pathology in animals. Proc Natl Acad Sci U S A 106: 8302-8307.
36. Bielekova B, Goodwin B, Richert N, Cortese I, Kondo T, et al. (2000) Encephalitogenic potential of the myelin basic protein peptide (amino acids 83-99) in multiple sclerosis: results of a phase II clinical trial with an altered peptide ligand. Nat Med 6: 1167-1175.
37. Mahnke YD, Brodie TM, Sallusto F, Roederer M, Lugli E (2013) The who's who of T-cell differentiation: human memory T-cell subsets. Eur J Immunol 43: 2797-2809.
38. Bielekova B, Catalfamo M, Reichert-Scrivner S, Packer A, Cerna M, et al. (2006) Regulatory CD56(bright) natural killer cells mediate immunomodulatory effects of IL-2Ralpha-targeted therapy (daclizumab) in multiple sclerosis. Proc Natl Acad Sci U S A 103: 5941-5946.
39. Castellazzi M, Tamborino C, Cani A, Negri E, Baldi E, et al. (2010) Epstein-Barr virus-specific antibody response in cerebrospinal fluid and serum of patients with multiple sclerosis. Mult Scler 16: 883-887.
40. Villegas E, Santiago O, Carrillo JA, Sorlozano A, Guerrero M, et al. (2011) Low intrathecal immune response of anti-EBNA-1 antibodies and EBV DNA from multiple sclerosis patients. Diagn Microbiol Infect Dis.
41. Pohl D, Rostasy K, Jacobi C, Lange P, Nau R, et al. (2010) Intrathecal antibody production against Epstein-Barr and other neurotropic viruses in pediatric and adult onset multiple sclerosis. J Neurol 257: 212-216.
42. Lunemann JD, Munz C (2007) Epstein-Barr virus and multiple sclerosis. Curr Neurol Neurosci Rep 7: 253-258. (Pubitemid 46831520)
43. Buljevac D, van Doornum GJJ, Flach HZ, Groen J, Osterhaus ADME, et al. (2005) Epstein-Barr virus and disease activity in multiple sclerosis. Journal of Neurology, Neurosurgery & Psychiatry 76: 1377-1381. (Pubitemid 41360975)
44. Sawtell NM, Thompson RL (2004) Comparison of herpes simplex virus reactivation in ganglia in vivo and in explants demonstrates quantitative and qualitative differences. J Virol 78: 7784-7794. (Pubitemid 38915924)
45. Peferoen LA, Lamers F, Lodder LN, Gerritsen WH, Huitinga I, et al. (2010) Epstein Barr virus is not a characteristic feature in the central nervous system in established multiple sclerosis. Brain 133: e137.
46. Iwakiri D, Zhou L, Samanta M, Matsumoto M, Ebihara T, et al. (2009) Epstein-Barr virus (EBV)-encoded small RNA is released from EBV-infected cells and activates signaling from Toll-like receptor 3. J Exp Med 206: 2091-2099.
47. Derfuss T, Hohlfeld R, Meinl E (2005) Intrathecal antibody (IgG) production against human herpesvirus type 6 occurs in about 20% of multiple sclerosis patients and might be linked to a polyspecific B-cell response. J Neurol 252: 968-971. (Pubitemid 41186970)
48. Virtanen JO, Pietilainen-Nicklen J, Uotila L, Farkkila M, Vaheri A, et al. (2011) Intrathecal human herpesvirus 6 antibodies in multiple sclerosis and other demyelinating diseases presenting as oligoclonal bands in cerebrospinal fluid. J Neuroimmunol 237: 93-97.
49. Hufner K, Arbusow V, Himmelein S, Derfuss T, Sinicina I, et al. (2007) The prevalence of human herpesvirus 6 in human sensory ganglia and its co-occurrence with alpha-herpesviruses. J Neurovirol 13: 462-467. (Pubitemid 350104393)
50. Perry JS, Han S, Xu Q, Herman ML, Kennedy LB, et al. (2012) Inhibition of LTi Cell Development by CD25 Blockade Is Associated with Decreased Intrathecal Inflammation in Multiple Sclerosis. Sci Transl Med 4: 145ra106.
51. Seder RA, Darrah PA, Roederer M (2008) T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 8: 247-258. (Pubitemid 351432801)