Human endogenous retrovirus protein activates innate immunity and promotes Experimental Allergic Encephalomyelitis in mice

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Perron, Hervé ^a,b   Dougier Reynaud, Hei Lanne ^c,d,e   Lomparski, Christina ^c,d   Popa, Iuliana ^f   Firouzi, Reza ^b   Bertrand, Jean Baptiste ^a   Marusic, Suzana ^g   Portoukalian, Jacques ^b   Jouvin Marche, Evelyne ^c,d   Villiers, Christian L ^c,d   Touraine, Jean Louis ^b,h   Marche, Patrice N ^c,d  

^a GENEURO SA   (Switzerland)

^b UNIVERSITÉ LYON 1   (France)

^c UNIV GRENOBLE ALPES   (France)

^d INSTITUT ALBERT BONNIOT   (France)

^e ImmunAlp   (France)

^f UNIV PARIS SUD   (France)

^g Hooke Laboratories Inc   (United States)

^h HOSPICES CIVILS DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 12P70; INTERLEUKIN 4; INTERLEUKIN 6; MULTIPLE SCLEROSIS ASSOCIATED RETROVIRAL ENVELOPE PROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

ALLERGIC ENCEPHALITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; BRAIN DAMAGE; CELL ACTIVATION; CYTOKINE PRODUCTION; DENDRITIC CELL; FEMALE; HISTOLOGY; INNATE IMMUNITY; MOUSE; MULTIPLE SCLEROSIS; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PROTEIN TARGETING;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGENS, CD14; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENE EXPRESSION; GENE PRODUCTS, ENV; HUMANS; IMMUNITY, INNATE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPLE SCLEROSIS; MYELIN-OLIGODENDROCYTE GLYCOPROTEIN; PEPTIDE FRAGMENTS; PREGNANCY PROTEINS; RECOMBINANT PROTEINS; TOLL-LIKE RECEPTOR 4;

EID: 84891486502     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080128     Document Type: Article

References (52)

1. Costenbader KH, Gay S, Alarcon-Riquelme ME, Iaccarino L, Doria A (2012) Genes, epigenetic regulation and environmental factors: which is the most relevant in developing autoimmune diseases? Autoimmun Rev 11: 604-609.
2. Kuhlmann T, Miron V, Cui Q, Wegner C, Antel J, et al. (2008) Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 131: 1749-1758. (Pubitemid 351957453)
3. Romme Christensen J, Bornsen L, Khademi M, Olsson T, Jensen PE, et al. (2012) CSF inflammation and axonal damage are increased and correlate in progressive multiple sclerosis. Mult Scler.
4. 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.
5. Baker D, Gerritsen W, Rundle J, Amor S (2011) Critical appraisal of animal models of multiple sclerosis. Mult Scler 17: 647-657.
6. Constantinescu CS, Farooqi N, O'Brien K, Gran B (2011) Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis (MS). Br J Pharmacol 164: 1079-1106.
7. Mackay IR, Anderson WH (2010) What's in a name? Experimental encephalomyelitis: 'allergic' or 'autoimmune'. J Neuroimmunol 223: 1-4.
8. Staykova MA, Linares D, Fordham SA, Paridaen JT, Willenborg DO (2008) The innate immune response to adjuvants dictates the adaptive immune response to autoantigens. J Neuropathol Exp Neurol 67: 543-554. (Pubitemid 351787081)
9. Wexler AG, Frielle C, Berry G, Budgeon LR, Baccon J, et al. (2013) The innate immune adaptor MyD88 is dispensable for spontaneous autoimmune demyelination in a mouse model of multiple sclerosis. J Neuroimmunol 255: 60-69.
10. Deng C, Radu C, Diab A, Tsen MF, Hussain R, et al. (2003) IL-1 receptorassociated kinase 1 regulates susceptibility to organ-specific autoimmunity. J Immunol 170: 2833-2842. (Pubitemid 36302153)
11. Marta M, Meier UC, Lobell A (2009) Regulation of autoimmune encephalomyelitis by toll-like receptors. Autoimmun Rev 8: 506-509.
12. Perron H, Garson JA, Bedin F, Beseme F, Paranhos-Baccala G, et al. (1997) Molecular identification of a novel retrovirus repeatedly isolated from patients with multiple sclerosis. The Collaborative Research Group on Multiple Sclerosis. Proc Natl Acad Sci U S A 94: 7583-7588. (Pubitemid 27345359)
13. Perron H, Lalande B, Gratacap B, Laurent A, Genoulaz O, et al. (1991) Isolation of retrovirus from patients with multiple sclerosis. Lancet 337: 862-863.
14. Blond JL, Beseme F, Duret L, Bouton O, Bedin F, et al. (1999) Molecular characterization and placental expression of HERV-W, a new human endogenous retrovirus family. J Virol 73: 1175-1185. (Pubitemid 29036769)
15. Feschotte C, Gilbert C (2012) Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet 13: 283-296.
16. Mirsattari SM, Johnston JB, McKenna R, Del Bigio MR, Orr P, et al. (2001) Aboriginals with multiple sclerosis: HLA types and predominance of neuromyelitis optica. Neurology 56: 317-323. (Pubitemid 32144141)
17. Perron H, Hamdani N, Faucard R, Lajnef M, Jamain S, et al. (2013) Molecular characteristics of Human Endogenous Retrovirus type-W in schizophrenia and bipolar disorder. Transl Psychiatry 3: e224.
18. Garcia-Montojo M, Dominguez-Mozo M, Arias-Leal A, Garcia-Martinez A, De Las Heras V, 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: e53623.
19. Perron H, Lang A (2010) The human endogenous retrovirus link between genes and environment in multiple sclerosis and in multifactorial diseases associating neuroinflammation. Clin Rev Allergy Immunol 39: 51-61.
20. Cherifi S, Byl B, Deplano A, Nonhoff C, Denis O, et al. (2013) Comparative Epidemiology of Staphylococcus epidermidis Isolates from Patients with Catheter-Related Bacteremia and from Healthy Volunteers. J Clin Microbiol 51: 1541-1547.
21. D'Andrea MM, Arena F, Pallecchi L, Rossolini GM (2013) CTX-M-type betalactamases: A successful story of antibiotic resistance. Int J Med Microbiol.
22. Zawada M, Liwien I, Pernak M, Januszkiewicz-Lewandowska D, Nowicka-Kujawska K, et al. (2003) MSRV pol sequence copy number as a potential marker of multiple sclerosis. Pol J Pharmacol 55: 869-875. (Pubitemid 37540883)
23. Jaubert C, Danioux C, Oberto J, Cortez D, Bize A, et al. (2013) Genomics and genetics of Sulfolobus islandicus LAL14/1, a model hyperthermophilic archaeon. Open Biol 3: 130010.
24. Krupovic M, Gonnet M, Hania WB, Forterre P, Erauso G (2013) Insights into dynamics of mobile genetic elements in hyperthermophilic environments from five new Thermococcus plasmids. PLoS One 8: e49044.
25. Antony JM, van Marle G, Opii W, Butterfield DA, Mallet F, et al. (2004) Human endogenous retrovirus glycoprotein-mediated induction of redox reactants causes oligodendrocyte death and demyelination. Nat Neurosci 7: 1088-1095. (Pubitemid 41184449)
26. Perron H, Germi R, Bernard C, Garcia-Montojo M, Deluen C, et al. (2012) Human endogenous retrovirus type W envelope expression in blood and brain cells provides new insights into multiple sclerosis disease. Mult Scler 18: 1721-1736.
27. Garson J, Creange A, Dolei A, Ferrante P, Jouvin-Marche E, et al. (2005) MSRV, Syncytin and the role of endogenous retroviral proteins in demyelination. Mult Scler 11: 249-250. (Pubitemid 40403269)
28. Menard A, Amouri R, Michel M, Marcel F, Brouillet A, et al. (1997) Gliotoxicity, reverse transcriptase activity and retroviral RNA in monocyte/macrophage culture supernatants from patients with multiple sclerosis. FEBS Lett 413: 477-485. (Pubitemid 27371487)
29. Kremer D, Schichel T, Forster M, Tzekova N, Bernard C, et al. (2013) HERVW envelope protein inhibits oligodendroglial precursor cell differentiation. Ann Neurol Jul 8. doi: 10.1002/ana.23970.
30. Perron H, Jouvin-Marche E, Michel M, Ounanian-Paraz A, Camelo S, et al. (2001) Multiple sclerosis retrovirus particles and recombinant envelope trigger an abnormal immune response in vitro, by inducing polyclonal Vbeta16 Tlymphocyte activation. Virology 287: 321-332. (Pubitemid 32804018)
31. Rolland A, Jouvin-Marche E, Viret C, Faure M, Perron H, et al. (2006) The envelope protein of a human endogenous retrovirus-W family activates innate immunity through CD14/TLR4 and promotes Th1-like responses. J Immunol 176: 7636-7644. (Pubitemid 43849064)
32. Perron H, Lazarini F, Ruprecht K, Pechoux-Longin C, Seilhean D, et al. (2005) Human endogenous retrovirus (HERV)-W ENV and GAG proteins: physiological expression in human brain and pathophysiological modulation in multiple sclerosis lesions. J Neurovirol 11: 23-33. (Pubitemid 40458368)
33. Firouzi R, Rolland A, Michel M, Jouvin-Marche E, Hauw JJ, et al. (2003) Multiple sclerosis-associated retrovirus particles cause T lymphocyte-dependent death with brain hemorrhage in humanized SCID mice model. J Neurovirol 9: 79-93. (Pubitemid 36372548)
34. Gerondakis S, Grumont RJ, Banerjee A (2007) Regulating B-cell activation and survival in response to TLR signals. Immunol Cell Biol 85: 471-475. (Pubitemid 47367507)
35. Kaisho T, Akira S (2006) Toll-like receptor function and signaling. J Allergy Clin Immunol 117: 979-987; quiz 988.
36. Bsibsi M, Ravid R, Gveric D, van Noort JM (2002) Broad expression of Toll-like receptors in the human central nervous system. J Neuropathol Exp Neurol 61: 1013-1021. (Pubitemid 35278723)
37. Bowman CC, Rasley A, Tranguch SL, Marriott I (2003) Cultured astrocytes express toll-like receptors for bacterial products. Glia 43: 281-291. (Pubitemid 37047684)
38. Olson JK, Miller SD (2004) Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 173: 3916-3924. (Pubitemid 39280755)
39. Tang SC, Arumugam TV, Xu X, Cheng A, Mughal MR, et al. (2007) Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits. Proc Natl Acad Sci U S A 104: 13798-13803. (Pubitemid 350003400)
40. Janeway CA Jr, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20: 197-216. (Pubitemid 34293424)
41. Akira S, Hemmi H (2003) Recognition of pathogen-associated molecular patterns by TLR family. Immunol Lett 85: 85-95. (Pubitemid 36071561)
42. Burzyn D, Rassa JC, Kim D, Nepomnaschy I, Ross SR, et al. (2004) Toll-like receptor 4-dependent activation of dendritic cells by a retrovirus. J Virol 78: 576-584. (Pubitemid 38067579)
43. Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, et al. (2003) Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc Natl Acad Sci U S A 100: 8514-8519. (Pubitemid 36842576)
44. Lehnardt S, Lachance C, Patrizi S, Lefebvre S, Follett PL, et al. (2002) The tolllike receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J Neurosci 22: 2478-2486. (Pubitemid 37465796)
45. Wekerle H, Kojima K, Lannes-Vieira J, Lassmann H, Linington C (1994) Animal models. Ann Neurol 36 Suppl: S47-53. (Pubitemid 24220843)
46. Steinman L, Zamvil SS (2006) How to successfully apply animal studies in experimental allergic encephalomyelitis to research on multiple sclerosis. Ann Neurol 60: 12-21.
47. Gold R, Hartung HP, Toyka KV (2000) Animal models for autoimmune demyelinating disorders of the nervous system. Mol Med Today 6: 88-91. (Pubitemid 30070671)
48. Perron H, Suh M, Lalande B, Gratacap B, Laurent A, et al. (1993) Herpes simplex virus ICP0 and ICP4 immediate early proteins strongly enhance expression of a retrovirus harboured by a leptomeningeal cell line from a patient with multiple sclerosis. J Gen Virol 74 (Pt 1): 65-72. (Pubitemid 23053767)
49. Ruprecht K, Obojes K, Wengel V, Gronen F, Kim KS, et al. (2006) Regulation of human endogenous retrovirus W protein expression by herpes simplex virus type 1: implications for multiple sclerosis. J Neurovirol 12: 65-71.
50. Kremer D, Schichel T, Fö rster M, Bernard C, Van Horssen J, et al. (2012) The envelope protein of a human endogenous retrovirus type W is present in human chronic active MS lesions and inhibits oligodendroglial precursor cell differentiation via nitrosative stress. Mult Scler 18: 142-143.
51. Curtin F, Lang AB, Perron H, Laumonier M, Vidal V, et al. (2012) GNbAC1, a Humanized Monoclonal Antibody Against the Envelope Protein of Multiple Sclerosis-Associated Endogenous Retrovirus: A First-in-Humans Randomized Clinical Study. Clin Ther 34: 2268-2278.
52. Perron H, Bertrand JB, Faucard R, Bernard C, Firouzi R, et al. (2012) Novel humanized antibody therapy in Multiple Sclerosis targeting immunopathogenic protein from endogenous retroviral element while preserving host's immune system. Multiple Sclerosis journal 18, Supplement 4: 192.