Skip to main content

Advertisement

SpringerLink
Log in

Up-to-date knowledge about the association between multiple sclerosis and the reactivation of human endogenous retrovirus infections

  • Review
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Background

Although existing studies show that reactivation of the human endogenous retrovirus (HERVs) plays a leading role in multiple sclerosis (MS) progression, the practitioners are yet to establish effective approaches for managing MS without jeopardizing the patients’ immune systems.

Aim

To provide up-to-date knowledge on the specific roles played by the reactivation of the HERVs in the pathogenesis of MS.

Materials and methods

A systematic review of 70 peer-reviewed journals accessed via PubMed was conducted. The searches generated more than 600 sources that were evaluated based on three step in and exclusion criteria. The selected sources were critically analyzed vis-à-vis the paper’s hypothesis which posits that the HERVs reactivation does not directly cause the MS, but triggers a demyelination process by promoting the pathogenic effects of the retroviruses. The paper further documents the advancements in the therapeutic applications resulting from the immunohistological analysis and pathological studies aimed at minimizing the adverse consequences of the HERVs reactivation.

Results and discussions

Only three out of the 70 reviewed sources did not find provide evidence linking the reactivation of HERV and MS progression. On the other hand, overwhelming pieces of evidence confirm that the reactivations often drive the demyelinating plaques by initiating microglial inflammation. Pathological examinations reveal that the inflammatory monocytes (Ly6ChiCCR2 + CX3CR1lo) trigger the reactivation of the malignant T cells that are responsible for the progression of MS. These findings are promoting new discoveries as far as managing MS is concerned.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

CNS:

Central nervous system

DNA:

Deoxyribonucleic acid

EAE:

Experimental autoimmune encephalomyelitis

EBV:

Epstein Barr virus

ERVWE:

Endogenous retrovirus group W member 1, envelope

GEMs:

Genes and environment in multiple sclerosis

HERVs:

Human endogenous retrovirus

IFN-β:

Interferon-β

mAbs:

Monoclonal antibodies

MS:

Multiple sclerosis

MSRV:

Multiple sclerosis associated virus

PP:

Primary progressive

PR:

Primary relapsing

RCT:

Randomized controlled trials

RNA:

Ribonucleic acid

SP:

Secondary progressive

TLR4:

Toll-like receptor 4

References

  1. Laska MJ, Brudek T, Nissen KK, Christensen T, Møller-Larsen A, Petersen T, Nexø BA (2012) Expression of HERV-Fc1, a human endogenous retrovirus, is increased in patients with active multiple sclerosis. J Virol 86(7):3713–3722

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Fierz W (2017) Multiple sclerosis: an example of pathogenic viral interaction. Virol J 14:42. https://doi.org/10.1186/s12985-017-0719-3

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Magiorkinis G, Belshaw R, Katzourakis A (2013) “There and back again”: revisiting the pathophysiological roles of human endogenous retroviruses in the post-genomic era. Philos Trans R Soc B Biol Sci 368(1626):20120504. https://doi.org/10.1098/rstb.2012.0504

    Article  Google Scholar 

  4. Nath A, Küry P, Sciascia do Olival G, Dolei A, Karlsson H, Groc L et al (2015) International workshop on human endogenous retroviruses and diseases, HERVs & disease 2015. Mob DNA 6:20. https://doi.org/10.1186/s13100-015-0051-7

    Article  PubMed Central  PubMed  Google Scholar 

  5. Mameli G, Serra C, Astone V, Castellazzi M, Poddighe L, Fainardi E, Neri W, Granieri E, Dolei A (2008) Inhibition of multiple sclerosis—associated retrovirus as biomarker of interferon therapy. J Neurovirol 14(1):73–77. https://doi.org/10.1080/13550280701801107

    Article  PubMed  CAS  Google Scholar 

  6. D’Amico E, Patti F, Zanghì A, Zappia M (2016) A personalized approaches in progressive multiple sclerosis: the current status of disease modifying therapies (DMTs) and future perspectives. Int J Mol Sci 17(10):1725. https://doi.org/10.3390/ijms17101725

    Article  PubMed Central  CAS  Google Scholar 

  7. Sotgiu S, Mameli G, Serra C, Zarbo IR, Arru G, Dolei A (2010) Multiple sclerosis-associated retrovirus and progressive disability of multiple sclerosis. Mult Scler J 16(10):1248–1251. https://doi.org/10.1177/1352458510376956

    Article  CAS  Google Scholar 

  8. Van Munster CEP, Uitdehaag BMJ (2017) Outcome measures in clinical trials for multiple sclerosis. CNS Drugs 31(3):217–236. https://doi.org/10.1007/s40263-017-0412-5

    Article  PubMed  PubMed Central  Google Scholar 

  9. Morandi E, Tarlinton RE, Gran B (2015) Multiple sclerosis between genetics and infections: human endogenous retroviruses in monocytes and macrophages. Front Immunol 6:1–6

    Article  CAS  Google Scholar 

  10. Uzameckis D, Capenko S, Logina I, Murovska M, Blomberg J (2016) No definite evidence for human endogenous retroviral HERV-W and HERV-H RNAs in plasma of Latvian patients suffering from multiple sclerosis and other neurological diseases. Proc Latv Acad Sci 4:182–192

    Google Scholar 

  11. Van Horssen J, Van der Pol S, Nijland P, Amor S, Perron H (2016) Human endogenous retrovirus W in brain lesions: rationale for targeted therapy in multiple sclerosis. Mult Scler Relat Disord 8:11–18

    Article  PubMed  Google Scholar 

  12. Mameli G, Poddighe L, Astone V, Delogu G, Arru G, Sotgiu S, Dolei A (2009) Novel reliable real-time PCR for differential detection of MSRVenv and syncytin-1 in RNA and DNA from patients with multiple sclerosis. J Virol Methods 161(1):98–106. https://doi.org/10.1016/j.jviromet.2009.05.024

    Article  PubMed  CAS  Google Scholar 

  13. Tongyoo P, Avihingsanon Y, Prom-On S, Mutirangura A, Mhuantong W, Hirankarn N (2017) EnHERV: enrichment analysis of specific human endogenous retrovirus patterns and their neighboring genes. Belshaw R, ed. PLoS One 12(5):e0177119. https://doi.org/10.1371/journal.pone.0177119

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Nissen KK, Laska MJ, Hansen B, Pedersen FS, Nexø BA (2012) No additional copies of HERV-Fc1 in the germ line of multiple sclerosis patients. Virol J 9:188. https://doi.org/10.1186/1743-422X-9-188

    Article  PubMed  PubMed Central  Google Scholar 

  15. Olival GS, Faria TS, Nali LHS, de Oliveira A, Casseb J, Vidal J et al (2013) Genomic analysis of ERVWE2 locus in patients with multiple sclerosis: absence of genetic association but potential role of human endogenous retrovirus type W elements in molecular mimicry with myelin antigen. Front Microbiol 4:172. https://doi.org/10.3389/fmicb.2013.00172

    Article  PubMed  PubMed Central  Google Scholar 

  16. Miranda-Hernandez S, Baxter A (2015) The role of toll-like receptors in multiple sclerosis. Am J Clin Exp Immunol 2(1):75–93

    Google Scholar 

  17. Grandi N, Tramontano E (2017) Type W Human Endogenous Retrovirus (HERV-W) integrations and their mobilization by l1 machinery: contribution to the human transcriptome and impact on the host physiopathology. Viruses 9(7):162. https://doi.org/10.3390/v9070162

    Article  PubMed Central  Google Scholar 

  18. De la Hera B, Varadé J, García-Montojo M, Alcina A, Fedetz M, Alloza I et al (2014) Human endogenous retrovirus HERV-Fc1 association with multiple sclerosis susceptibility: a meta-analysis. PLoS One 9(3):e90182. https://doi.org/10.1371/journal.pone.0090182

    Article  PubMed  PubMed Central  Google Scholar 

  19. Møller-Larsen A, Brudek T, Petersen T, Petersen E, Aagaard M, Hansen D, Christensen T (2013) Flow cytometric assay detecting cytotoxicity against human endogenous retrovirus antigens expressed on cultured multiple sclerosis cells. Clin Exp Immunol 173(3):398–410. https://doi.org/10.1111/cei.12133

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Garcia-Montojo M, Dominguez-Mozo M, Arias-Leal A, Arias-Leal A, Garcia-Martinez Á, De las Heras V, Casanova I et al (2013) The DNA copy number of human endogenous retrovirus-w (msrv-type) is increased in multiple sclerosis patients and is influenced by gender and disease severity. PLoS One 8(1):e53623. https://doi.org/10.1371/journal.pone.0053623

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Krone B, Grange JM (2013) Is a hypothetical melanoma-like neuromelanin the underlying factor essential for the aetiopathogenesis and clinical manifestations of multiple sclerosis? BMC Neurol 13:91. https://doi.org/10.1186/1471-2377-13-91

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Mameli G, Madeddu G, Mei A, Uleri E, Poddighe L, Delogu L et al (2013) Activation of MSRV-type endogenous retroviruses during infectious mononucleosis and Epstein–Barr virus latency: the missing link with multiple sclerosis? Stewart JP, ed. PLoS One 8(11):e78474. https://doi.org/10.1371/journal.pone.0078474

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. De Meirleir KL, Khaiboullina SF, Frémont M, Rizvanov A, Palotás A, Lombardi V (2013) Plasmacytoid dendritic cells in the duodenum of individuals diagnosed with myalgic encephalomyelitis are uniquely immunoreactive to antibodies to human endogenous retroviral proteins. In Vivo (Athens, Greece) 27(2):177–187

    Google Scholar 

  24. Campos-Sánchez R, Cremona MA, Pini A, Chiaromonte F, Makova KD (2016) Integration and fixation preferences of human and mouse endogenous retroviruses uncovered with functional data analysis. Kosakovsky Pond SL, ed. PLoS Comput Biol 12(6):e1004956. https://doi.org/10.1371/journal.pcbi.1004956

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. García-Montojo M, de la Hera B, Varadé J et al (2014) HERV-W polymorphism in chromosome X is associated with multiple sclerosis risk and with differential expression of MSRV. Retrovirology 11:2. https://doi.org/10.1186/1742-4690-11-2

    Article  PubMed  PubMed Central  Google Scholar 

  26. Duperray A, Barbe D, Raguenez G, Weksler B, Romero I, Couraud P et al (2015) Inflammatory response of endothelial cells to a human endogenous retrovirus associated with multiple sclerosis is mediated by TLR4. Int Immunol 27(11):545–553. https://doi.org/10.1093/intimm/dxv025

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Derfuss T, Curtin F, Guebelin C (2015) A phase IIa randomised clinical study of GNbAC1, a humanised monoclonal antibody against the envelope protein of multiple sclerosis-associated endogenous retrovirus in multiple sclerosis patients. Mult Scler 21(7):885–893

    Article  PubMed  CAS  Google Scholar 

  28. Lyksborg M, Siebner HR, Sørensen PS, Blinkenberg M, Parker G, Dogonowski A et al (2014) Secondary progressive and relapsing remitting multiple sclerosis leads to motor-related decreased anatomical connectivity. PLoS One 9(4):e95540. https://doi.org/10.1371/journal.pone.0095540

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Mallucci G, Peruzzotti-Jametti L, Bernstock JD, Pluchino S (2015) The role of immune cells, glia and neurons in white and gray matter pathology in multiple sclerosis. Prog Neurobiol. https://doi.org/10.1016/j.pneurobio.2015.02.003

    Article  PubMed  PubMed Central  Google Scholar 

  30. Heffernan C, Sumer H, Guillemin GJ, Manuelpillai U, Verma PJ (2012) Design and screening of a glial cell-specific, cell penetrating peptide for therapeutic applications in multiple sclerosis. Nait-Oumesmar B, ed. PLoS One 7(9):e45501. https://doi.org/10.1371/journal.pone.0045501

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Rawji KS, Yong VW (2013) The benefits and detriments of macrophages/microglia in models of multiple sclerosis. Clin Dev Immunol 2013:948976. https://doi.org/10.1155/2013/948976

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Morandi E, Tanasescu R, Tarlinton R, Constantinescu C, Zhang W, Tench C, Gran B (2017) The association between human endogenous retroviruses and multiple sclerosis: a systematic review and meta-analysis. PLoS One 12(2):e0172415. https://doi.org/10.1371/journal.pone.0172415 (Accessed 20 Aug 2017)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Brütting C, Emmer A, Kornhuber ME, Staege MS (2017) Cooccurrences of putative endogenous retrovirus-associated diseases. Biomed Res Int 2017:7973165. https://doi.org/10.1155/2017/7973165

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Rahn AC, Backhus I, Fuest F (2016) Comprehension of confidence intervals—development and piloting of patient information materials for people with multiple sclerosis: qualitative study and pilot randomised controlled trial. BMC Med Inform Decis Mak 16:122. https://doi.org/10.1186/s12911-016-0362-8

    Article  PubMed  PubMed Central  Google Scholar 

  35. Katoh I, Kurata S (2013) Association of endogenous retroviruses and long terminal repeats with human disorders. Front Oncol 3:234. https://doi.org/10.3389/fonc.2013.00234

    Article  PubMed  PubMed Central  Google Scholar 

  36. Grandi N, Cadeddu M, Blomberg J, Tramontano E (2016) Contribution of type W human endogenous retroviruses to the human genome: characterization of HERV-W proviral insertions and processed pseudogenes. Retrovirology 13(1):67. https://doi.org/10.1186/s12977-016-0301-x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Balestrieri E, Pica F, Matteucci C, Zenobi R, Sorrentino R, Argaw-Denboba A et al (2015) Transcriptional activity of human endogenous retroviruses in human peripheral blood mononuclear cells. Biomed Res Int 2015:164529. https://doi.org/10.1155/2015/164529

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Rodgers JM, Miller S (2012) Cytokine control of inflammation and repair in the pathology of multiple sclerosis. Yale J Biol Med 85(4):447–468

    PubMed  PubMed Central  CAS  Google Scholar 

  39. Khalaj AJ, Yoon J, Nakai J, Winchester Z, Moore SM, Yoo T et al (2013) Estrogen receptor (ER) β expression in oligodendrocytes is required for attenuation of clinical disease by an ERβ ligand. Proc Natl Acad Sci USA 110(47):19125–19130. https://doi.org/10.1073/pnas.1311763110 (Accessed 20 Aug 2017)

    Article  PubMed  CAS  Google Scholar 

  40. Douvaras P, Wang J, Zimmer M, Hanchuk S, O’Bara M, Sadiq S et al (2014) Efficient generation of myelinating oligodendrocytes from primary progressive multiple sclerosis patients by induced pluripotent stem cells. Stem Cell Rep 3(2):250–259. https://doi.org/10.1016/j.stemcr.2014.06.012

    Article  CAS  Google Scholar 

  41. Romano CM (2013) Erratum: genomic analysis of ERVWE2 locus in patients with Multiple sclerosis: Absence of genetic association but potential role of Human Endogenous retrovirus type W elements in molecular mimicry with myelin antigen. Front Microbiol 4:345. https://doi.org/10.3389/fmicb.2013.00345

    Article  PubMed  PubMed Central  Google Scholar 

  42. Menezes SM, Decanine D, Brassat D, Khouri R, Schnitman S, Kruschewsky R et al (2014) CD80+ and CD86+ B cells as biomarkers and possible therapeutic targets in HTLV-1 associated myelopathy/tropical spastic paraparesis and multiple sclerosis. J Neuroinflamm 11:18. https://doi.org/10.1186/1742-2094-11-18

    Article  CAS  Google Scholar 

  43. Mameli G, Poddighe L, Mei A, Uleri E, Sotgiu S, Serra C et al (2012) Expression and activation by Epstein Barr virus of human endogenous retroviruses-W in blood cells and astrocytes: inference for multiple sclerosis. Villoslada P, ed. PLoS One 7(9):e44991. https://doi.org/10.1371/journal.pone.0044991

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Schmitt K, Richter C, Backes C, Meese E, Ruprecht K, Mayer J (2013) Comprehensive analysis of human endogenous retrovirus group HERV-W locus transcription in multiple sclerosis brain lesions by high-throughput amplicon sequencing. J Virol 87(24):13837–13852. https://doi.org/10.1128/JVI.02388-13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Maliniemi P, Vincendeau M, Mayer J, Frank O, Hahtola S, Karenko L et al (2013) Expression of human endogenous retrovirus-W including syncytin-1 in cutaneous t-cell lymphoma. Schindler M, ed. PLoS One 8(10):e76281. https://doi.org/10.1371/journal.pone.0076281

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Lossius A, Johansen JN, Torkildsen Ø, Vartdal F, Holmøy T (2012) Epstein–Barr virus in systemic lupus erythematosus, rheumatoid arthritis and multiple sclerosis—association and causation. Viruses 4(12):3701–3730. https://doi.org/10.3390/v4123701

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Cusick MF, Libbey JE, Fujinami RS (2013) Multiple sclerosis: autoimmunity and viruses. Curr Opin Rheumatol 25(4):496–501. https://doi.org/10.1097/BOR.0b013e328362004d

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Libbey JE, Cusick MF, Fujinami RS (2014) Role of pathogens in multiple sclerosis. Int Rev Immunol 33(4):266–283. https://doi.org/10.3109/08830185.2013.823422

    Article  PubMed  CAS  Google Scholar 

  49. Bello-Morales R, Crespillo AJ, García B, Dorado L, Martín B, Tabarés E et al (2014) Effect of cellular differentiation on HSV-1 infection of oligodendrocytic cells. Shukla D, ed. PLoS One 9(2):e89141. https://doi.org/10.1371/journal.pone.0089141

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Jones RB, Leal FE, Hasenkrug AM, Segurado A, Nixon D, Ostrowski M, Kallas E (2013) Human endogenous retrovirus K(HML-2) Gag and Env specific T-cell responses are not detected in HTLV-I-infected subjects using standard peptide screening methods. J Negat Results Biomed 12:3. https://doi.org/10.1186/1477-5751-12-3

    Article  PubMed  PubMed Central  Google Scholar 

  51. Buzdin AA, Prassolov V, Garazha AV (2017) Friends-enemies: endogenous retroviruses are major transcriptional regulators of human DNA. Front Chem 5:35. https://doi.org/10.3389/fchem.2017.00035

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Goris A, Pauwels I, Gustavsen MW et al (2015) Genetic variants are major determinants of CSF antibody levels in multiple sclerosis. Brain 138(3):632–643. https://doi.org/10.1093/brain/awu405

    Article  PubMed  PubMed Central  Google Scholar 

  53. Laska MJ, Nissen KK, Nexø BA (2013) Cellular mechanisms influencing the transcription of human endogenous retrovirus, HERV-Fc1. PLoS One 8(1):e53895. https://doi.org/10.1371/journal.pone.0053895

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Faucard R, Madeira A, Gehin N, Authier F, Panaite P, Lesage C et al (2016) Human endogenous retrovirus and neuroinflammation in chronic inflammatory demyelinating polyradiculoneuropathy. EBioMedicine 6:190–198. https://doi.org/10.1016/j.ebiom.2016.03.001

    Article  PubMed  PubMed Central  Google Scholar 

  55. Douville R, Nath A (2014) Human endogenous retroviruses and the nervous system. Handb Clin Neurol 123:465–485. https://doi.org/10.1016/B978-0-444-53488-0.00022-5

    Article  PubMed  PubMed Central  Google Scholar 

  56. O’Gorman C, Lucas R, Taylor B (2012) Environmental risk factors for multiple sclerosis: a review with a focus on molecular mechanisms. Int J Mol Sci 13(9):11718–11752. https://doi.org/10.3390/ijms130911718

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Nexø BA, Villesen P, Nissen KK, Lindegaard H, Rossing P, Petersen T et al (2016) Are human endogenous retroviruses triggers of autoimmune diseases? Unveiling associations of three diseases and viral loci. Immunol Res 64:55–63. https://doi.org/10.1007/s12026-015-8671-z

    Article  PubMed  CAS  Google Scholar 

  58. Marchione P, Morreale M, Giacomini P, Izzo C, Pontecorvo S, Altieri M, Francia A (2014) Ultrasonographic evaluation of cerebral arterial and venous haemodynamics in multiple sclerosis: a case–control study. PLoS One 9(10):e111486. https://doi.org/10.1371/journal.pone.0111486

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Shirani A, Okuda DT, Stüve O (2016) Therapeutic advances and future prospects in progressive forms of multiple sclerosis. Neurotherapeutics 13(1):58–69. https://doi.org/10.1007/s13311-015-0409-z

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Wuest SC, Mexhitaj I, Chai NR, Romm E, Scheffel J, Xu B et al (2014) Complex role of Herpes viruses in the disease process of multiple sclerosis. PLoS One 9(8):e105434. https://doi.org/10.1371/journal.pone.0105434

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Harris VK, Sadiq SA (2014) Biomarkers of therapeutic response in multiple sclerosis: current status. Mol Diagn Ther 18(6):605–617. https://doi.org/10.1007/s40291-0140117-0

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Miljković D, Spasojević I (2013) Multiple sclerosis: molecular mechanisms and therapeutic opportunities. Antioxid Redox Signal 19(18):2286–2334. https://doi.org/10.1089/ars.2012.5068

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Xia Z, White CC, Owen EK, Von Korff A, Clarkson S, McCabe C et al (2016) GEMS project: a platform to investigate multiple sclerosis risk. Ann Neurol 79(2):178–189. https://doi.org/10.1002/ana.24560

    Article  PubMed  Google Scholar 

  64. Rommer PS, Dudesek A, Stüve O, Zettl UK (2014) Monoclonal antibodies in treatment of multiple sclerosis. Clin Exp Immunol 175(3):373–384

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Wootla B, Watzlawik JO, Stavropoulos N (2016) Recent advances in monoclonal antibody therapies for multiple sclerosis. Expert Opin Biol Ther 16(6):827–839. https://doi.org/10.1517/14712598.2016.1158809

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Curtin F, Perron H, Kromminga A, Porchet H, Lang AB (2015) Preclinical and early clinical development of GNbAC1, a humanized IgG4 monoclonal antibody targeting endogenous retroviral MSRV-Env protein. mAbs 7(1):265–275. https://doi.org/10.4161/19420862.2014.985021

    Article  PubMed  CAS  Google Scholar 

  67. Najafi S, Ghane M, Yousefzadeh-Chabok S, Amiri M (2016) The high prevalence of the varicella zoster virus in patients with relapsing-remitting multiple sclerosis: a case-control study in the north of Iran. Jundishapur J Microbiol 9(3):e34158. https://doi.org/10.5812/jjm.34158

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Longbrake EE, Parks BJ, Cross AH (2013) Monoclonal antibodies as disease modifying therapy in multiple sclerosis. Curr Neurol Neurosci Rep 13(11):390. https://doi.org/10.1007/s11910-013-0390-z

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Arru G, Leoni S, Pugliatti M, Mei A, Serra C, Delogu LG, Mameli G (2014) Natalizumab inhibits the expression of human endogenous retroviruses of the W family in multiple sclerosis patients: a longitudinal cohort study. Mult Scler J 20(2):174–182. https://doi.org/10.1177/1352458513494957

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Laboratory Medicine and Pathobiochemistry, Molecular Diagnostics, University Hospital of the University of Marburg UKGM, Justus Liebig University, Feulgenstr. 12, 35392, Giessen, Germany

    Borros Arneth

Authors
  1. Borros Arneth
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Borros Arneth.

Ethics declarations

Conflicts of interest

Dr. Arneth reports no disclosures.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Arneth, B. Up-to-date knowledge about the association between multiple sclerosis and the reactivation of human endogenous retrovirus infections. J Neurol 265, 1733–1739 (2018). https://doi.org/10.1007/s00415-018-8783-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-018-8783-1

Keywords

Search

Navigation