Human endogenous retrovirus type W envelope protein inhibits oligodendroglial precursor cell differentiation

Annals of Neurology

Volumn 74, Issue 5, 2013, Pages 721-732

  Kremer, David ^a   Schichel, Tanja ^a   Förster, Moritz ^a   Tzekova, Nevena ^a   Bernard, Corinne ^b   Van Der Valk, Paul ^c   Van Horssen, Jack ^c   Hartung, Hans Peter ^a   Perron, Hervé ^b   Küry, Patrick ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b GENEURO SA   (Switzerland)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; MYELIN; MYELIN PROTEIN; N ACETYL S NITROSOPENICILLAMINE; N(G) NITRO DEXTRO ARGININE METHYL ESTER; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ARTICLE; BRAIN TISSUE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE RESPONSE; ENDOGENOUS RETROVIRUS; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN ENDOGENOUS RETROVIRUS TYPE W; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; MULTIPLE SCLEROSIS; NERVE CELL DIFFERENTIATION; NITROSATIVE STRESS; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REMYELINIZATION; VIRUS INHIBITION;

EID: 84890798859     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.23970     Document Type: Article

References (49)

1. Feschotte C, Gilbert C,. Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet 2012; 13: 283-296.
2. Perron H, Lang A,. The human endogenous retrovirus link between genes and environment in multiple sclerosis and in multifactorial diseases associating neuroinflammation. Clin Rev Allergy Immunol 2010; 39: 51-61.
3. Haahr S, Sommerlund M, Moller-Larsen A,. Multiple sclerosis as a retroviral disease? Epidemiological considerations in relation to HTLV-I epidemiology. Neuroepidemiology 1991; 10: 232-235.
4. Perron H, Geny C, Laurent A, et al. Leptomeningeal cell line from multiple sclerosis with reverse transcriptase activity and viral particles. Res Virol 1989; 140: 551-561.
5. Perron H, Lalande B, Gratacap B, et al. Isolation of retrovirus from patients with multiple sclerosis. Lancet 1991; 337: 862-863.
6. Ruprecht K, Gronen F, Sauter M, et al. Lack of immune responses against multiple sclerosis-associated retrovirus/human endogenous retrovirus W in patients with multiple sclerosis. J Neurovirol 2008; 14: 143-151.
7. Perron H, Garson JA, Bedin F, et al. 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 1997; 94: 7583-7588.
8. Perron H, Jouvin-Marche E, Michel M, et al. Multiple sclerosis retrovirus particles and recombinant envelope trigger an abnormal immune response in vitro, by inducing polyclonal Vbeta16 T-lymphocyte activation. Virology 2001; 287: 321-332.
9. Rolland A, Jouvin-Marche E, Viret C, et al. The envelope protein of a human endogenous retrovirus-W family activates innate immunity through CD14/TLR4 and promotes Th1-like responses. J Immunol 2006; 176: 7636-7644.
10. Mameli G, Poddighe L, Astone V, et al. 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 2009; 161: 98-106.
11. Perron H, Germi R, Bernard C, et al. Human endogenous retrovirus type W envelope expression in blood and brain cells provides new insights into multiple sclerosis disease. Mult Scler 2012; 18: 1721-1736.
12. Sotgiu S, Arru G, Mameli G, et al. Multiple sclerosis-associated retrovirus in early multiple sclerosis: a six-year follow-up of a Sardinian cohort. Mult Scler 2006; 12: 698-703.
13. Sotgiu S, Arru G, Soderstrom M, et al. Multiple sclerosis-associated retrovirus and optic neuritis. Mult Scler 2006; 12: 357-359.
14. Sotgiu S, Serra C, Mameli G, et al. Multiple sclerosis-associated retrovirus and MS prognosis: an observational study. Neurology 2002; 59: 1071-1073.
15. Kremer D, Heinen A, Jadasz J, et al. p57kip2 is dynamically regulated in experimental autoimmune encephalomyelitis and interferes with oligodendroglial maturation. Proc Natl Acad Sci U S A 2009; 106: 9087-9092.
16. Heinen A, Kremer D, Göttle P, et al. The cyclin-dependent kinase inhibitor p57kip2 is a negative regulator of Schwann cell differentiation and in vitro myelination. Proc Natl Acad Sci U S A 2008; 105: 8748-8753.
17. Heinen A, Tzekova N, Graffmann N, et al. Histone methyltransferase enhancer of zeste homolog 2 regulates Schwann cell differentiation. Glia 2012; 60: 1696-1708.
18. Chang A, Nishiyama A, Peterson J, et al. NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci 2000; 20: 6404-6412.
19. Lehnardt S, Massillon L, Follett P, et al. Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc Natl Acad Sci U S A 2003; 100: 8514-8519.
20. Taylor DL, Pirianov G, Holland S, et al. Attenuation of proliferation in oligodendrocyte precursor cells by activated microglia. J Neurosci Res 2010; 88: 1632-1644.
21. Takeda K, Akira S,. TLR signaling pathways. Semin Immunol 2004; 16: 3-9.
22. Eu JP, Liu L, Zeng M, et al. An apoptotic model for nitrosative stress. Biochemistry 2000; 39: 1040-1047.
23. Klatt P, Lamas S,. Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur J Biochem 2000; 267: 4928-4944.
24. Bolanos JP, Almeida A, Stewart V, et al. Nitric oxide-mediated mitochondrial damage in the brain: mechanisms and implications for neurodegenerative diseases. J Neurochem 1997; 68: 2227-2240.
25. Hamada Y, Hayakawa T, Hattori H, et al. Inhibitor of nitric oxide synthesis reduces hypoxic-ischemic brain damage in the neonatal rat. Pediatr Res 1994; 35: 10-14.
26. Iadecola C, Zhang F, Xu S, et al. Inducible nitric oxide synthase gene expression in brain following cerebral ischemia. J Cereb Blood Flow Metab 1995; 15: 378-384.
27. Khan F, Siddiqui AA,. Prevalence of anti-3-nitrotyrosine antibodies in the joint synovial fluid of patients with rheumatoid arthritis, osteoarthritis and systemic lupus erythematosus. Clin Chim Acta 2006; 370: 100-107.
28. Lau D, Baldus S,. Myeloperoxidase and its contributory role in inflammatory vascular disease. Pharmacol Ther 2006; 111: 16-26.
29. Murray J, Taylor SW, Zhang B, et al. Oxidative damage to mitochondrial complex I due to peroxynitrite: identification of reactive tyrosines by mass spectrometry. J Biol Chem 2003; 278: 37223-37230.
30. Chang A, Tourtellotte WW, Rudick R, et al. Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N Engl J Med 2002; 346: 165-173.
31. Kremer D, Aktas O, Hartung HP, et al. The complex world of oligodendroglial differentiation inhibitors. Ann Neurol 2011; 69: 602-618.
32. Kuhlmann T, Miron V, Cui Q, et al. Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 2008; 131: 1749-1758.
33. Komurian-Pradel F, Paranhos-Baccala G, Bedin F, et al. Molecular cloning and characterization of MSRV-related sequences associated with retrovirus-like particles. Virology 1999; 260: 1-9.
34. Noble M, Murray K, Stroobant P, et al. Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature 1988; 333: 560-562.
35. Shibata T, Motoi Y, Tanimura N, et al. Intracellular TLR4/MD-2 in macrophages senses Gram-negative bacteria and induces a unique set of LPS-dependent genes. Int Immunol 2011; 23: 503-510.
36. Dunzendorfer S, Lee HK, Soldau K, et al. Toll-like receptor 4 functions intracellularly in human coronary artery endothelial cells: roles of LBP and sCD14 in mediating LPS responses. FASEB J 2004; 18: 1117-1119.
37. Sotgiu S, Mameli G, Serra C, et al. Multiple sclerosis-associated retrovirus and progressive disability of multiple sclerosis. Mult Scler 2010; 16: 1248-1251.
38. Douville R, Liu J, Rothstein J, et al. Identification of active loci of a human endogenous retrovirus in neurons of patients with amyotrophic lateral sclerosis. Ann Neurol 2011; 69: 141-151.
39. Boje KM,. Inhibition of nitric oxide synthase attenuates blood-brain barrier disruption during experimental meningitis. Brain Res 1996; 720: 75-83.
40. Mayhan WG,. Nitric oxide donor-induced increase in permeability of the blood-brain barrier. Brain Res 2000; 866: 101-108.
41. Winkler F, Koedel U, Kastenbauer S, et al. Differential expression of nitric oxide synthases in bacterial meningitis: role of the inducible isoform for blood-brain barrier breakdown. J Infect Dis 2001; 183: 1749-1759.
42. Hooper DC, Bagasra O, Marini JC, et al. Prevention of experimental allergic encephalomyelitis by targeting nitric oxide and peroxynitrite: implications for the treatment of multiple sclerosis. Proc Natl Acad Sci U S A 1997; 94: 2528-2533.
43. Antony JM, van Marle G, Opii W, et al. Human endogenous retrovirus glycoprotein-mediated induction of redox reactants causes oligodendrocyte death and demyelination. Nat Neurosci 2004; 7: 1088-1095.
44. Blond JL, Beseme F, Duret L, et al. Molecular characterization and placental expression of HERV-W, a new human endogenous retrovirus family. J Virol 1999; 73: 1175-1185.
45. Mi S, Lee X, Li X, et al. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 2000; 403: 785-789.
46. Ruprecht K, Obojes K, Wengel V, et al. Regulation of human endogenous retrovirus W protein expression by herpes simplex virus type 1: implications for multiple sclerosis. J Neurovirol 2006; 12: 65-71.
47. Ruprecht K, Perron H,. Exposure to infant siblings during early life and risk of multiple sclerosis. JAMA 2005; 293: 2089-2090.
48. Roebke C, Wahl S, Laufer G, et al. An N-terminally truncated envelope protein encoded by a human endogenous retrovirus W locus on chromosome Xq22.3. Retrovirology 2010; 7: 69.
49. Curtin F, Lang AB, Perron H, et al. GNbAC1, a humanized monoclonal antibody against the envelope protein of multiple sclerosis-associated endogenous retrovirus: a first-in-humans randomized clinical study. Clin Ther 2012; 34: 2268-2278.