Interferon-triggered transcriptional cascades in the oligodendroglial lineage: A comparison of induction of MHC class II antigen between oligodendroglial progenitor cells and mature oligodendrocytes

Journal of Neuroimmunology

Volumn 212, Issue 1-2, 2009, Pages 53-64

  Itoh, Takayuki ^a,b   Horiuchi, Makoto ^a,b   Itoh, Aki ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SHRINERS HOSPITALS FOR CHILDREN NORTHERN CALIFORNIA   (United States)

Author keywords

CIITA; DNA methylation; Interferon; IRF; MHC; Oligodendroglial lineage

Indexed keywords

BETA INTERFERON; DNA; GAMMA INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANIMAL CELL; ARTICLE; CELL LINEAGE; CELL MATURATION; COMPARATIVE STUDY; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; GENETIC TRANSCRIPTION; NERVE CELL DIFFERENTIATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN INDUCTION; RAT; STEM CELL;

ANIMALS; ANTIGENS, CD80; CELL LINEAGE; CELLS, CULTURED; DNA METHYLATION; GENES, MHC CLASS II; INTERFERON REGULATORY FACTOR-1; INTERFERONS; MICE; MICE, INBRED C57BL; NUCLEAR PROTEINS; OLIGODENDROGLIA; STEM CELLS; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 67649866311     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2009.04.021     Document Type: Article

References (52)

1. Arnett H.A., Wang Y., Matsushima G.K., Suzuki K., and Ting J.P.-Y. Functional genomic analysis of remyelination reveals importance of inflammation in oligodendrocyte regeneration. J. Neurosci. 23 (2003) 9824-9832
2. Boss J.M., and Jensen P.E. Transcriptional regulation of the MHC class II antigen presentation pathway. Curr. Opin. Immunol. 15 (2003) 105-111
3. Calder V.L., Wolswijk G., and Noble M. The differentiation of O-2A progenitor cells into oligodendrocytes is associated with a loss of inducibility of Ia antigens. Eur. J. Immunol. 18 (1988) 1195-1201
4. Clerico M., Rivoiro C., Contessa G., Viglietti D., and Durelli L. The therapy of multiple sclerosis with immune-modulating or immunosuppressive drug. A critical evaluation based upon evidence based parameters and published systematic reviews. Clin. Neurol. Neurosurg. 110 (2008) 878-885
5. Cha Y., and Deisseroth A.B. Human interferon regulatory factor 2 gene. Intron-exon organization and functional analysis of 5′-flanking region. J. Biol. Chem. 269 (1994) 5279-5287
6. Chang T.T., Jabs C., Sobel R.A., Kuchroo V.K., and Sharpe A.H. Studies in B7-deficient mice reveal a critical role for B7 costimulation in both induction and effector phases of experimental autoimmune encephalomyelitis. J. Exp. Med. 190 (1999) 733-740
7. Croce M., De Ambrosis A., Corrias M.V., Pistoia V., Occhino M., Meazza R., Giron-Michel J., Azzarone B., Accolla R.S., and Ferrini S. Different levels of control prevent interferon-γ -inducible HLA-class II expression in human neuroblastoma cells. Oncogene 22 (2003) 7848-7857
8. Ettinger R.A., Moustakas A.K., and Lobaton S.D. Open reading frame sequencing and structure-based alignment of polypeptides encoded by RT1-Bb, RT1-Ba, RT1-Db, and RT1-Da alleles. Immunogenetics 56 (2004) 585-596
9. Giroux M., Schmidt M., and Descoteaux A. IFN-γ -induced MHC class II expression: transactivation of class II transactivator promoter IV by IFN regulatory factor-1 is regulated by protein kinase C-α. J. Immunol. 171 (2003) 4187-4194
10. Girvin A.M., Gordon K.B., Jane Welsh C., Clipstone N.A., and Miller S.D. Differential abilities of central nervous system resident endothelial cells and astrocytes to serve as inducible antigen-presenting cells. Blood 99 (2002) 3692-3701
11. Gobin S.J.P., Montagne L., Van Zutphen M., Van Der Valk P., Van Der Elsen P.J., and De Groot C.J.A. Upregulation of transcription factors controlling MHC expression in multiple sclerosis lesions. Glia 36 (2001) 68-77
12. Günther E., and Walter L. The major histocompatibility complex of the rat (Rattus norvegicus). Immunogenetics 53 (2001) 520-542
13. Harada H., Fujita T., Miyamoto M., Kimura Y., Maruyama M., Furia A., Miyata T., and Taniguchi T. Structurally similar but functionally distinct factors, IRF-1 and IRF-2, bind to the same regulatory elements of IFN and IFN-inducible gene. Cell 58 (1989) 729-739
14. + T cell-mediated skin disease in mice lacking IRF-2, the transcriptional attenuator of interferon-α /β signaling. Immunity 13 (2000) 643-655
15. Horiuchi M., Itoh A., Pleasure D., and Itoh T. MEK-ERK signaling is involved in interferon-γ -induced death of oligodendroglial progenitor cells. J. Biol. Chem. 281 (2006) 20095-20106
16. Hurt P., Walter L., Sudbrak R., Klages S., Müller I., Shiina T., Inoko H., Lehrach H., Günther E., Reinhardt R., and Himmelbauer H. The genomic sequence and comparative analysis of the rat major histocompatibility complex. Genome Res. 14 (2004) 631-639
17. Inaba K., Kitaura M., Kato T., Watanabe Y., Kawade Y., and Muramatsu S. Contrasting effects of α /β and γ -interferons on expression of macrophage Ia antigens. J. Exp. Med. 163 (1986) 1030-1035
18. Itoh T., Beesley J., Itoh A., Cohen A.S., Kavanaugh B., Coulter D.A., Grinspan J.B., and Pleasure D. AMPA glutamate receptor-mediated calcium signaling is transiently enhanced during development of oligodendrocytes. J. Neurochem. 81 (2002) 390-402
19. Itoh T., Itoh A., and Pleasure D. Bcl-2-related protein family gene expression during oligodendroglial differentiation. J. Neurochem. 85 (2003) 1500-1512
20. Kato T., Kitaura M., Inaba K., Watanabe Y., Kawade Y., and Muramatsu S. Suppression of macrophage Ia antigen expression by endogenous interferon-alpha/beta. J. Interf. Res. 9 (1989) 393-405
21. Lee S.C., and Raine C.S. Multiple sclerosis: oligodendrocytes in active lesions do not express class II major histocompatibility complex molecules. J. Neuroimmnol. 25 (1989) 261-266
22. Lee P.T., Holt P.G., and McWilliam A.S. Failure of MHC class II expression in neonatal alveolar macrophages: potential role of class II transactivator. Eur. J. Immunol. 31 (2001) 2347-2356
23. Leeuwenberg J.F., Van Damme J., Meager T., Jeunhomme T.M., and Buurman W.A. Effects of tumor necrosis factor on the interferon-gamma-induced major histocompatibility complex class II antigen expression by human endothelial cells. Eur. J. Immunol. 18 (1988) 1469-1472
24. Ling P.D., Warren M.K., and Vogel S.N. Antagonistic effect of interferon-beta on the interferon-gamma-induced expression of Ia antigen in murine macrophages. J. Immunol. 135 (1985) 1857-1863
25. Lu H.-T., Riley J.L., Babcock G.T., Huston M., Stark G.R., Boss J.M., and Ransohoff R.M. Interferon (IFN) β acts downstream of IFN-γ -induced class II transactivator messenger RNA accumulation to block major histocompatibility complex class II gene expression and requires the 48-kD DNA-binding protein, ISGF3-γ. J. Exp. Med. 182 (1995) 1517-1525
26. Massa P.T., Ozato K., and McFarlin D.E. Cell type-specific regulation of major histocompatibility complex (MHC) class I gene expression in astrocytes, oligodendrocytes, and neurons. Glia 8 (1993) 201-207
27. Masternak K., and Reith W. Promoter-specific functions of CIITA and the MHC class II enhanceosome in transcriptional activation. EMBO J. 21 (2002) 1379-1388
28. Matsuyama T., Kimura T., Kitagawa M., Pfeffer K., Kawakami T., Watanabe N., Kündig T.M., Amakawa R., Kishihara K., Wakeham A., Potter J., Furionger C.L., Narendran A., Suzuki H., Ohashi P.S., Paige C.J., Taniguchi T., and Mak T.W. Targeted disruption of IRF-1 or IRF-2 results in abnormal type I IFN gene induction and aberrant lymphocyte development. Cell 75 (1993) 83-97
29. Morris A.C., Spangler W.E., and Boss J.M. Methylation of class II trans-activator promoter IV: a novel mechanism of MHC class II gene control. J. Immunol. 164 (2000) 4143-4149
30. Morris A.C., Beresford G.W., Mooney M.R., and Boss J.M. Kinetics of a gamma interferon response: expression and assembly of CIITA promoter IV and inhibition by methylation. Mol. Cell. Biol. 22 (2002) 4781-4791
31. Muhlethaler-Mottet A., Otten L.A., Steimle V., and Mach B. Expression of MHC class II molecules in different cellular and functional compartments is controlled by differential usage of multiple promoters of the transactivator CIITA. EMBO J. 16 (1997) 2851-2860
32. Muhlethaler-Mottet A., Di Berardino W., Otten L.A., and Mach B. Activation of the MHC class II transactivator CIITA by interferon-γ requires cooperative interaction between Stat1 and USF-1. Immunity 8 (1998) 157-166
33. O'Keefe G.M., Nguyen V.T., Tang L.P., and Benveniste E.N. IFN-γ regulation of class II transactivator promoter IV in macrophages and microglia: involvement of the suppressors of cytokine signaling-1 protein. J. Immunol. 166 (2001) 2260-2269
34. Panitch H.S., Hirsch R.L., Haley A.S., and Johnson K.P. Exacerbations of multiple sclerosis in patients treated with gamma interferon. Lancet 1 (1987) 893-895
35. Park C., Li S., Cha E., and Schindler C. Immune response in Stat2 knockout mice. Immunity 13 (2000) 795-804
36. Pine R., Canova A., and Schindler C. Tyrosine phosphorylated p91 binds to a single element in the ISGF2/IRF1 promoter to mediate induction by IFNα and IFNγ, and is likely to autoregulate the p91 gene. EMBO J. 13 (1994) 158-167
37. Platanias L.C. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev., Immunol. 5 (2005) 375-386
38. Prinz M., Schmidt H., Mildner A., Knobeloch K.P., Hanisch U.K., Raasch J., Merkler D., Detje C., Gutcher I., Mages J., Lang R., Martin R., Gold R., Becher B., Brück W., and Kalinke U. Distinct and nonredundant in vivo functions of IFNAR on myeloid cells limit autoimmunity in the central nervous system. Immunity 28 (2008) 675-686
39. Ransohoff R.M., Devajyothi C., Estes M.L., Babcock G., Rudick R.A., Frohman E.M., and Barna B.P. Interferon-β specifically inhibits interferon-γ -induced class II major histocompatibility complex gene transcription in a human astrocytoma cell line. J. Neuroimmunol. 33 (1991) 103-112
40. Satoh J., Kim S.U., Kastrukoff L.F., and Takei F. Expression and induction of intercellular adhesion molecules (ICAMs) and major histocompatibility complex (MHC) antigens on cultured murine oligodendrocytes and astrocytes. J. Neurosci. Res. 29 (1991) 1-12
41. Satoh J., Paty D.W., and Kim S.U. Differential effects of beta and gamma interferons on expression of major histocompatibility complex antigens and intercellular adhesion molecule-1 in cultured fetal human astrocytes. Neurology 45 (1995) 367-373
42. Soos J.M., Ashley T.A., Morrow J., Patarroyo J.C., Szente B.E., and Zamvil S.S. Differential expression of B7 co-stimulatory molecules by astrocytes correlates with T cell activation and cytokine production. Int. Immunol. 11 (1999) 1169-1179
43. Steimle V., Siegrist C.-A., Mottet A., Lisowska-Grospierre B., and Mach B. Regulation of MHC class II expression by interferon-g mediated by the transactivator gene CIITA. Science 265 (1994) 106-109
44. Suzumura A., Silberberg D.H., and Lisak R.P. The expression of MHC antigens on oligodendrocytes: induction of polymorphic H-2 expression by lymphokines. J. Neuroimmunol. 11 (1986) 179-190
45. Taniguchi T., Ogasawara K., Takaoka A., and Tanaka N. IRF family of transcription factors as regulators of host defense. Annu. Rev. Immunol. 19 (2001) 623-655
46. Tepavcevic V., and Blakemore W.F. Glial grafting for demyelinating disease. Philos. Trans. R. Soc. Lond., B Biol. Sci. 360 (2005) 1775-1795
47. Turnley A.M., Miller J.F.A.P., and Bartlett P.F. Regulation of MHC molecules on MBP positive oligodendrocytes in mice by IFN-γ and TNF-α. Neurosci. Lett. 123 (1991) 45-48
48. van den Elsen P.J., Holling T.M., Kuipers H.F., and van der Stoep N. Transcriptional regulation of antigen presentation. Curr. Opin. Immunol. 16 (2004) 67-75
49. Vestberg M., Brunsberg U., Bergsteinsdottir K., Karlsson M., Gustafsson K., Wedekind D., Hedrich H., and Holmdahl R. Limited polymorphism in the first domain of the rat MHC class II RT1-D molecule. Immunogenetics 48 (1998) 344-349
50. Weinstock-Guttman B., Ransohoff R.M., Kinkel R.P., and Rudick R.A. The interferons: biological effects, mechanisms of action, and use in multiple sclerosis. Ann. Neurol. 37 (1995) 7-15
51. Wong G.H.W., Bartlett P.F., Clark-Lewis I., Battye F., and Schrader J.W. Inducible expression of H-2 and Ia antigens on brain cells. Nature 310 (1984) 688-691
52. Wright K.L., and Ting J.P.-Y. Epigenetic regulation of MHC-II and CIITA genes. Trends Immunol. 27 (2006) 405-412