Specificity and expression of CIITA, the master regulator of MHC class II genes

European Journal of Immunology

Volumn 34, Issue 6, 2004, Pages 1513-1525

  LeibundGut Landmann, Salomé ^a   Waldburger, Jean Marc ^a   Krawczyk, Michal ^a   Otten, Luc A ^b   Suter, Tobias ^c   Fontana, Adriano ^c   Acha Orbea, Hans ^b   Reith, Walter ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

Cell type specifity; Class II transactivator; Gene expression; MHC class II; Repression

Indexed keywords

ANTIINFLAMMATORY AGENT; FAS LIGAND; GAMMA INTERFERON; HISTONE DEACETYLASE INHIBITOR; HLA DP ANTIGEN; HLA DQ ANTIGEN; HLA DR ANTIGEN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; HYPOCHOLESTEROLEMIC AGENT; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NITRIC OXIDE SYNTHASE INHIBITOR; STAT1 PROTEIN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; HLA ANTIGEN CLASS 2; MHC CLASS II TRANSACTIVATOR PROTEIN; NUCLEAR PROTEIN;

ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ANTIINFLAMMATORY ACTIVITY; BACTERIAL IMMUNITY; CELLULAR IMMUNITY; DENDRITIC CELL; DOWN REGULATION; DRUG RECEPTOR BINDING; ENZYME INHIBITION; GENE ACTIVATION; GENE EXPRESSION; GENE FUNCTION; GENE REPRESSION; GENE SILENCING; GENE TARGETING; GENETIC CODE; GENETIC REGULATION; GENETIC TRANSCRIPTION; HUMAN; HUMORAL IMMUNITY; IMMUNOSTIMULATION; MACROPHAGE ACTIVATION; MELANOMA CELL; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROMOTER REGION; RHEUMATOID ARTHRITIS; SHORT SURVEY; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TUMOR IMMUNITY; VIRUS IMMUNITY; ANIMAL; BIOSYNTHESIS; GENE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MOUSE MUTANT; REVIEW; TRANSACTIVATION;

ANIMALS; ANTIGEN PRESENTATION; GENE EXPRESSION REGULATION; GENES, MHC CLASS II; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; MICE; MICE, KNOCKOUT; NUCLEAR PROTEINS; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

EID: 4544234467     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200424964     Document Type: Short Survey

References (114)

1. Starr, T. K., Jameson, S. C. and Hogquist, K. A., Positive and negative selection of T cells. Annu. Rev. Immunol. 2003. 21: 139-176.
2. Anderson, M. S., Venanzi, E. S., Klein, L., Chen, Z., Berzins, S. P., Turley, S. J., von Boehmer, H., Bronson, R., Dierich, A., Benoist, C. and Mathis, D., Projection of an immunological self shadow within the thymus by the AIRE protein. Science 2002. 298: 1395-1401.
3. Liston, A., Lesage, S., Wilson, J., Peltonen, L. and Goodnow, C. C., Aire regulates negative selection of organ-specific T cells. Nat. Immunol. 2003. 4: 350-354.
4. Reith, W. and Mach, B., The bare lymphocyte syndrome and the regulation of MHC expression. Annu. Rev. Immunol. 2001. 19: 331-373.
5. Ting, J. P. and Trowsdale, J., Genetic control of MHC class II expression. Cell 2002. 109 Suppl: S21-S33.
6. Steimle, V., Durand, B., Barras, E., Zufferey, M., Hadam, M. R., Mach, B. and Reith, W., A novel DNA binding regulatory factor is mutated in primary MHC class II deficiency (Bare Lymphocyte Syndrome). Genes Dev. 1995. 9: 1021-1032.
7. Masternak, K., Barras, E., Zufferey, M., Conrad, B., Corthals, G., Aebersold, R., Sanchez, J. C., Hochstrasser, D. F., Mach, B. and Reith, W., A gene encoding a novel RFX-associated transactivator is mutated in the majority of MHC class II deficiency patients. Nat. Genet. 1998. 20: 273-277.
8. Nagarajan, U. M., Louis-Plence, R, DeSandro, A., Nilsen, R., Bushey, A. and Boss, J. M., RFX-B is the gene responsible for the most common cause of the bare lymphocyte syndrome, an MHC class II immunodeficiency. Immunity 1999. 10: 153-162.
9. Durand, B., Sperisen, P., Emery, P., Barras, E., Zufferey, M., Mach, B. and Reith, W., RFXAP, a novel subunit of the RFX DNA binding complex is mutated in MHC class II deficiency. EMBO J. 1997. 16: 1045-1055.
10. Moreno, C. S., Beresford, G. W., Louis-Plence, P., Morris, A. C. and Boss, J. M., CREB regulates MHC class II expression in a CIITA-dependent manner. Immunity 1999. 10: 143-151.
11. Mantovani, R., The molecular biology of the CCAAT-binding factor NF-Y. Gene 1999. 239: 15-27.
12. Jabrane-Ferrat, N., Fontes, J. D., Boss, J. M. and Peterlin, B. M., Complex architecture of major histocompatibility complex class II promoters: reiterated motifs and conserved protein-protein interactions. Mol. Cell Biol. 1996. 16: 4683-4690.
13. Masternak, K., Muhlethaler-Mottet, A., Villard, J., Zufferey, M., Steimle, V. and Reith, W., CIITA is a transcriptional coactivator that is recruited to MHC class II promoters by multiple synergistic interactions with an enhanceosome complex. Genes Dev. 2000. 14: 1156-1166.
14. Steimle, V., Otten, L. A., Zufferey, M. and Mach, B., Complementation cloning of an MHC class II transactivator mutated in hereditary MHC class II deficiency. Cell 1993. 75: 135-146.
15. Boss, J. M. and Jensen, P. E., Transcriptional regulation of the MHC class II antigen presentation pathway. Curr. Opin. Immunol. 2003. 15: 105-111.
16. van den Eisen, P. J., Holling, T. M., Kuipers, H. F. and van der Stoep, N., Transcriptional regulation of antigen presentation. Curr. Opin. Immunol. 2004. 16: 67-75.
17. Westerheide, S. D., Louis-Plence, P., Ping, D., He, X. F. and Boss, J. M., HLA-DMA and HLA-DMB gene expression functions through the conserved S-X- Y region. J. Immunol. 1997. 158: 4812-4821.
18. Taxman, D. J., Cressman, D. E. and Ting, J. P., Identification of class II transcriptional activator- induced genes by representational difference analysis: discoordinate regulation of the DN alpha / DO beta heterodimer. J. Immunol. 2000. 165: 1410-1416.
19. Nagarajan, U. M., Lochamy, J., Chen, X., Beresford, G. W., Nilsen, R., Jensen, P. E. and Boss, J. M., Class II transactivator is required for maximal expression of HLA-DOB in B cells. J. Immunol. 2002. 168: 1780-1786.
20. Khalil, H., Deshaies, F., Bellemare-Pelletier, A., Brunet, A., Faubert, A., Azar, G. A. and Thibodeau, J., Class II transactivator-induced expression of HLA-DO(beta) in HeLa cells. Tissue Antigens 2002. 60: 372-382.
21. Martin, B. K., Chin, K. C., Olsen, J. C., Skinner, C. A., Dey, A., Ozato, K. and Ting, J. P., Induction of MHC class I expression by the MHC class II transactivator CIITA. Immunity 1997. 6: 591-600.
22. Gobin, S. J., Peijnenburg, A., Keijsers, V. and van den Elsen, P. J., Site alpha is crucial for two routes of IFN gamma-induced MHC class I transactivation: the ISRE-mediated route and a novel pathway involving CIITA. Immunity 1997. 6: 601-611.
23. Gourley, T., Roys, S., Lukacs, N. W., Kunkel, S. L., Flavell, R. A. and Chang, C. H., A novel role for the major histocompatibility complex class II transactivator CIITA in the repression of IL-4 production. Immunity 1999. 10: 377-386.
24. Gourley, T. S., Patel, D. R., Nickerson, K., Hong, S. C. and Chang, C. H., Aberrant expression of Fas ligand in mice deficient for the MHC class II transactivator. J. Immunol. 2002. 168: 4414-4419.
25. Sisk, T. J., Gourley, T., Roys, S. and Chang, C. H., MHC class II transactivator inhibits IL-4 gene transcription by competing with NF-AT to bind the coactivator CREB binding protein (CBP)/p300. J. Immunol. 2000. 165: 2511-2517.
26. Otten, L. A., Tacchini-Cottier, F., Lohoff, M., Annunziato, F., Cosmi, L., Scarpellino, L., Louis, J., Steimle, V., Reith, W. and Acha-Orbea, H., Deregulated MHC class II transactivator expression leads to a strong Th2 bias in CD4+ T lymphocytes. J. Immunol. 2003. 170: 1150-1157.
27. Gourley, T. S. and Chang, C. H., Cutting edge: the class II transactivator prevents activation-induced cell death by inhibiting Fas ligand gene expression. J. Immunol. 2001. 166: 2917-2921.
28. Zhu, X. S. and Ting, J. P., A 36-amino-acid region of CIITA is an effective inhibitor of CBP: novel mechanism of gamma interferon-mediated suppression of collagen alpha(2)(I) and other promoters. Mol. Cell Biol. 2001. 21: 7078-7088.
29. Sengupta, P. K., Fargo, J. and Smith, B. D., The RFX family interacts at the collagen (COL1A2) start site and represses transcription. J. Biol. Chem. 2002. 277: 24926-24937.
30. Saifuddin, M., Roebuck, K. A., Chang, C., Ting, J. R and Spear, G. T., Cutting edge: activation of HIV-1 transcription by the MHC class II transactivator. J. Immunol. 2000. 164: 3941-3945.
31. Saifuddin, M., Spear, G. T., Chang, C. and Roebuck, K. A., Expression of MHC class II in T cells is associated with increased HIV-1 expression. Clin. Exp. Immunol. 2000. 121: 324-331.
32. Lima, R. G., Van Weyenbergh, J., Saraiva, E. M., Barral-Netto, M., Galvao-Castro, B. and Bou-Habib, D. C., The replication of human immunodeficiency virus type 1 in macrophages is enhanced after phagocytosis of apoptotic cells. J. Infect. Dis. 2002. 185: 1561-1566.
33. Accolla, R. S., Mazza, S., De Lerma Barbaro, A., De Maria, A. and Tosi, G., The HLA class II transcriptional activator blocks the function of HIV-1 Tat and inhibits viral replication. Eur. J. Immunol. 2002. 32: 2783-2791.
34. Okamoto, H., Asamitsu, K., Nishimura, H., Kamatani, N. and Okamoto, T., Reciprocal modulation of transcriptional activities between HIV-1 Tat and MHC class II transactivator CIITA. Biochem. Biophys. Res. Commun. 2000. 279: 494-499.
35. Wong, A. W., Brickey, W. J., Taxman, D. J., van Deventer, H. W., Reed, W., Gao, J. X., Zheng, P., Liu, Y., Li, P., Blum, J. S. et al., CIITA-regulated plexin-A1 affects T-cell-dendritic cell interactions. Nat. Immunol. 2003. 4: 891-898.
36. Landmann, S., Muhlethaler-Mottet, A., Bernasconi, L., Suter, T., Waldburger, J. M., Masternak, K., Arrighi, J. F., Hauser, C., Fontana, A. and Reith, W., Maturation of dendritic cells is accompanied by rapid transcriptional silencing of class II transactivator (CIITA) expression. J. Exp. Med. 2001. 194: 379-392.
37. Nagarajan, U. M., Bushey, A. and Boss, J. M., Modulation of gene expression by the MHC class II transactivator. J. Immunol. 2002. 169: 5078-5088.
38. 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. 1997. 16: 2851-2860.
39. Barbieri, G., Deffrennes, V., Prod'homme, T., Vedrenne, J., Baton, F., Cortes, C., Fischer, A., Bono, M. R., Lisowska-Grospierre, B., Charron, D. and Alcaide-Loridan, C., Isoforms of the class II transactivator protein. Int. Immunol. 2002. 14: 839-848.
40. Waldburger, J. M., Suter, T., Fontana, A., Acha-Orbea, H. and Reith, W., Selective abrogation of major histocompatibility complex class II expression on extrahematopoietic cells in mice lacking promoter IV of the class II transactivator gene. J. Exp. Med. 2001. 194: 393-406.
41. Muhlethaler-Mottet, A., Di Berardino, W., Otten, L. A. and Mach, B., Activation of the MHC class II transactivator CIITA by interferon-gamma requires cooperative interaction between Stat1 and USF-1. Immunity 1998. 8: 157-166.
42. Piskurich, J. F., Wang, Y., Linhoff, M. W., White, L. C. and Ting, J. P., Identification of distinct regions of 5′ flanking DNA that mediate constitutive, IFN-gamma, STAT1, and TGF-beta-regulated expression of the class II transactivator gene. J. Immunol. 1998. 160: 233-240.
43. Piskurich, J. F., Linhoff, M. W., Wang, Y. and Ting, J. P., Two distinct gamma interferon-inducible promoters of the major histocompatibility complex class II transactivator gene are differentially regulated by STAT1, interferon regulatory factor 1, and transforming growth factor beta. Mol. Cell Biol. 1999. 19: 431-440.
44. Dong, Y., Rohn, W. M. and Benveniste, E. N., IFN-gamma regulation of the type IV class II transactivator promoter in astrocytes. J. Immunol. 1999. 162: 4731-4739.
45. Rohn, W., Tang, L. P., Dong, Y. and Benveniste, E. N., IL-1 beta inhibits IFN-gamma-induced class II MHC expression by suppressing transcription of the class II transactivator gene. J. Immunol. 1999. 162: 886-896.
46. O'Keefe, G. M., Nguyen, V. T., Ping Tang, L. L. and Benveniste, E. N., IFN-gamma regulation of class II transactivator promoter IV in macrophages and microglia: involvement of the suppressors of cytokine signaling-1 protein. J. Immunol. 2001. 166: 2260-2269.
47. Steimle, V., Siegrist, C.-A., Mottet, A., Lisowska-Grospierre, B. and Mach, B., Regulation of MHC class II expression by interferon-gamma mediated by the transactivator gene CIITA. Science 1994. 265: 106-109.
48. Nikcevich, K. M., Piskurich, J. F., Hellendall, R. P., Wang, Y. and Ting, J. P., Differential selectivity of CIITA promoter activation by IFN-gamma and IRF-1 in astrocytes and macrophages: CIITA promoter activation is not affected by TNF-alpha. J. Neuroimmunol. 1999. 99: 195-204.
49. Pai, R. K., Askew, D., Boom, W. H. and Harding, C. V., Regulation of class II MHC expression in APCs: roles of types I, III, and IV class II transactivator. J. Immunol. 2002. 169: 1326-1333.
50. Waldburger, J. M., Rossi, S., Hollander, G. A., Rodewald, H. R., Reith, W. and Acha-Orbea, H., Promoter IV of the class II transactivator gene is essential for positive selection of CD4+ T cells. Blood 2003. 101: 3550-3559.
51. Lennon, A. M., Ottone, C., Rigaud, G., Deaven, L. L., Longmire, J., Fellous, M., Bono, R. and Alcaide-Loridan, C., Isolation of a B-cell-specific promoter for the human class II transactivator. Immunogenetics 1997. 45: 266-273.
52. Ghosh, N., Piskurich, J. F., Wright, G., Hassani, K., Ting, J. P. and Wright, K. L., A novel element and a TEF-2-like element activate the major histocompatibility complex class II transactivator in B-lymphocytes. J. Biol. Chem. 1999. 274: 32342-32350.
53. van der Stoep, N., Quinten, E. and van den Elsen, P. J., Transcriptional regulation of the MHC class II trans-activator (CIITA) promoter III: identification of a novel regulatory region in the 5′-untranslated region and an important role for cAMP-responsive element binding protein 1 and activating transcription factor-1 in CIITA-promoter III transcriptional activation in B lymphocytes. J. Immunol. 2002. 169: 5061-5071.
54. Ko, H. S., Fu, S. M., Winchester, R. J., Yu, D. T. and Kunkel, H. G., la determinants on stimulated human T lymphocytes. Occurrence on mitogen- and antigen-activated T cells. J. Exp. Med. 1979. 150: 246-255.
55. Holling, T. M., van der Stoep, N., Quinten, E. and van den Elsen, P. J., Activated human T cells accomplish MHC class II expression through T cell-specific occupation of class II transactivator promoter III. J. Immunol. 2002. 168: 763-770.
56. Wong, A. W., Ghosh, N., McKinnon, K. P., Reed, W., Piskurich, J. F., Wright, K. L. and Ting, J. P., Regulation and specificity of MHC2TA promoter usage in human primary T lymphocytes and cell line. J. Immunol. 2002. 169: 3112-3119.
57. Chang, C. H., Hong, S. C., Hughes, C. C., Janeway, C. A. Jr. and Flavell, R. A., CIITA activates the expression of MHC class II genes in mouse T cells. Int. Immunol. 1995. 7: 1515-1518.
58. Deffrennes, V., Vedrenne, J., Stolzenberg, M. C., Piskurich, J., Barbieri, G., Ting, J. P., Charron, D. and Alcaide-Loridan, C., Constitutive expression of MHC class II genes in melanoma cell lines results from the transcription of class II transactivator abnormally initiated from its B cell-specific promoter. J. Immunol. 2001. 167: 98-106.
59. Goodwin, B. L., Xi, H., Tejiram, R., Eason, D. D., Ghosh, N., Wright, K. L., Nagarajan, U., Boss, J. M. and Blanck, G., Varying functions of specific major histocompatibility class II transactivator promoter III and IV elements in melanoma cell lines. Cell Growth Differ. 2001. 12: 327-335.
60. Suter, T., Malipiero, U., Otten, L., Ludewig, B., Muelethaler-Mottet, A., Mach, B., Reith, W. and Fontana, A., Dendritic cells and differential usage of the MHC class II transactivator promoters in the central nervous system in experimental autoimmune encephalitis. Eur. J. Immunol. 2000. 30: 794-802.
61. Asselin-Paturel, C., Boonstra, A., Dalod, M., Durand, I., Yessaad, N., Dezutter-Dambuyant, C., Vicari, A., O'Garra, A., Biron, C., Briere, F. and Trinchieri, G., Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat. Immunol. 2001. 2: 1144-1150.
62. Ardavin, C., Origin, precursors and differentiation of mouse dendritic cells. Nat. Rev. Immunol. 2003. 3: 582-590.
63. Silacci, P., Mottet, A., Steimle, V., Reith, W. and Mach, B., Developmental extinction of major histocompatibility complex class II gene expression in plasmocytes is mediated by silencing of the transactivator gene CIITA. J. Exp. Med. 1994. 180: 1329-1336.
64. Sartoris, S., Tosi, G., De Lerma, B., Cestari, T and Accolla, R. S., Active suppression of the class II transactivator-encoding AIR-1 locus is responsible for the lack of major histocompatibility complex class II gene expression observed during differentiation from B cells to plasma cells. Eur. J. Immunol. 1996. 26: 2456-2460.
65. Keller, A. D. and Maniatis, T., Identification and characterization of a novel repressor of beta-interferon gene expression. Genes Dev. 1991. 5: 868-879.
66. Kakkis, E., Riggs, K. J., Gillespie, W. and Calame, K., A transcriptional repressor of c-myc. Nature 1989. 339: 718-721.
67. Piskurich, J. F., Lin, K. I., Lin, Y., Wang, Y., Ting, J. P. and Calame, K., BLIMP-I mediates extinction of major histocompatibility class II transactivator expression in plasma cells. Nat. Immunol. 2000. 11: 526-532.
68. Ghosh, N., Gyory, I., Wright, G., Wood, J. and Wright, K. L., Positive regulatory domain I binding factor 1 silences class II transactivator expression in multiple myeloma cells. J. Biol. Chem. 2001. 276: 15264-15268.
69. Turner, C. A. Jr., Mack, D. H. and Davis, M. M., Blimp-1, a novel zinc finger-containing protein that can drive the maturation of B lymphocytes into immunoglobulin-secreting cells. Cell 1994. 77: 297-306.
70. Lee, Y. J., Han, Y., Lu, H. T., Nguyen, V., Qin, H., Howe, P. H., Hocevar, B. A., Boss, J. M., Ransohoff, R. M. and Benveniste, E. N., TGF-beta suppresses IFN-gamma induction of class II MHC gene expression by inhibiting class II transactivator messenger RNA expression. J. Immunol. 1997. 158: 2065-2075.
71. Nandan, D. and Reiner, N. E., TGF-beta attenuates the class II transactivator and reveals an accessory pathway of IFN-gamma action. J. Immunol. 1997. 158: 1095-1101.
72. O'Keefe, G. M., Nguyen, V. T. and Benveniste, E. N., Class II transactivator and class II MHC gene expression in microglia: modulation by the cytokines TGF-beta, IL-4, IL-13 and IL-10. Eur J. Immunol. 1999. 29: 1275-1285.
73. Panek, R. B., Lee, Y. J. and Benveniste, E. N., TGF-beta suppression of IFN-gamma-induced class II MHC gene expression does not involve inhibition of phosphorylation of JAK1, JAK2, or signal transducers and activators of transcription, or modification of IFN-gamma enhanced factor X expression. J. Immunol. 1995. 154: 610-619.
74. Dong, Y., Tang, L., Letterio, J. J. and Benveniste, E. N., The Smad3 protein is involved in TGF-beta inhibition of class II transactivator and class II MHC expression. J. Immunol. 2001. 167: 311-319.
75. Navarrete, S. A., Kehlen, A., Schutte, W., Langner, J. and Riemann, D., Regulation by transforming growth factor-beta 1 of class II mRNA and protein expression in fibroblast-like synoviocytes from patients with rheumatoid arthritis. Int. Immunol. 1998. 10: 601-607.
76. Endo, T. A., Masuhara, M., Yokouchi, M., Suzuki, R., Sakamoto, H., Mitsui, K., Matsumoto, A., Tanimura, S., Ohtsubo, M., Misawa, H. et al., A new protein containing an SH2 domain that inhibits JAK kinases. Nature 1997. 387: 921-924.
77. Yasukawa, H., Misawa, H., Sakamoto, H., Masuhara, M., Sasaki, A., Wakioka, T., Ohtsuka, S., Imaizumi, T., Matsuda, T., Ihle, J. N. and Yoshimura, A., The JAK-binding protein JAB inhibits Janus tyrosine kinase activity through binding in the activation loop. EMBO J. 1999. 18: 1309-1320.
78. Kielar, M. L., Sicher, S. C., Penfield, J. G., Jeyarajah, D. R. and Lu, C. Y., Nitric oxide inhibits INF-gamma-induced increaaes in CIITA mRNA abundance and activation of CIITA dependent genes - class II MHC, Ii and H-2 M. class II transactivator. Inflammation 2000. 24: 431-445.
79. Kwak, B., Mulhaupt, F., Myit, S. and Mach, F., Statins as a newly recognized type of immunomodulator. Nat. Med. 2000. 6: 1399-1402.
80. Youssef, S., Stuve, O., Patarroyo, J. C., Ruiz, P. J., Radosevich, J. L., Hur, E. M., Bravo, M., Mitchell, D. J., Sobel, R. A., Steinman, L. and Zamvil, S. S., The HMG-CoA reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease. Nature 2002. 420: 78-84.
81. Leung, B. P., Sattar, N., Crilly, A., Prach, M., McCarey, D. W., Payne, H., Madhok, R., Campbell, C., Gracie, J. A., Liew, F. Y. and McInnes, I. B., A novel anti-inflammatory role for simvastatin in inflammatory arthritis. J. Immunol. 2003. 170: 1524-1530.
82. Morris, A. C., Riley, J. L., Fleming, W. H. and Boss, J. M., MHC class II gene silencing in trophoblast cells is caused by inhibition of CIITA expression. Am. J. Reprod. Immunol. 1998. 40: 385-394.
83. Murphy, S. P. and Tomasi, T. B., Absence of MHC class II antigen expression in trophoblast cells results from a lack of class II transactivator (CIITA) gene expression. Mol. Reprod. Dev 1998. 51: 1-12.
84. 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. 2000. 164: 4143-4149.
85. van den Eisen, P. J., van der Stoep, N., Vietor, H. E., Wilson, L., van Zutphen, M. and Gobin, S. J., Lack of CIITA expression is central to the absence of antigen presentation functions of trophoblast cells and is caused by methylation of the IFN-gamma inducible promoter (PIV) of CIITA. Hum. Immunol. 2000. 61: 850-862.
86. 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. 2002. 22: 4781-4791.
87. Geirsson, A., Paliwal, I., Lynch, R. J., Bothwell, A. L. and Hammond, G. L., Class II transactivator promoter activity is suppressed through regulation by a trophoblast noncoding RNA. Transplantation 2003. 76: 387-394.
88. Foss, F. M., Immunologic mechanisms of antitumor activity. Semin. Oncol. 2002. 29: 5-11.
89. Garcia-Lora, A., Algarra, I., Collado, A. and Garrido, F., Tumour immunology, vaccination and escape strategies. Eur. J. Immunogenet. 2003. 30: 177-183.
90. Wang, R. F., Zeng, G., Johnston, S. F., Voo, K. and Ying, H., T cell-mediated immune responses in melanoma: implications for immunotherapy. Crit. Rev. Oncol. Hematol. 2002. 43: 1-11.
91. Toes, R. E., Schoenberger, S. P., van der Voort, E. I., Offringa, R. and Melief, C. J., CD40-CD40 Ligand interactions and their role in cytotoxic T lymphocyte priming and anti-tumor immunity. Semin. Immunol. 1998. 10: 443-448.
92. Ossendorp, F., Toes, R. E., Offringa, R., van der Burg, S. H. and Melief, C. J., Importance of CD4(+) T helper cell responses in tumor immunity. Immunol. Lett. 2000. 74: 75-79.
93. Drenou, B., Le Friec, G., Bernard, M., Pangault, C., Grosset, J. M., Lamy, T., Fauchet, R. and Amiot, L., Major histocompatibility complex abnormalities in non-Hodgkin lymphomas. Br. J. Haematol. 2002. 119: 417-424.
94. Momburg, F., Herrmann, B., Moldenhauer, G. and Moller, P., B-cell lymphomas of high-grade malignancy frequently lack HLA-DR, -DP and -DQ antigens and associated invariant chain. Int. J. Cancer 1987. 40: 598-603.
95. van den Eisen, P. J., Holling, T. M., van der Stoep, N. and Boss, J. M., DNA methylation and expression of major histocompatibility complex class I and class II transactivator genes in human developmental tumor cells and in T cell malignancies. Clin. Immunol. 2003. 109: 46-52.
96. Magner, W. J., Kazim, A. L., Stewart, C., Romano, M. A., Catalano, G., Grande, C., Keiser, N., Santaniello, F. and Tomasi, T. B., Activation of MHC class I, II, and CD40 gene expression by histone deacetylase inhibitors. J. Immunol. 2000. 165: 7017-7024.
97. 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-gamma-inducible HLA-class II expression in human neuroblastoma cells. Oncogene 2003. 22: 7848-7857.
98. Yazawa, T., Kamma, H., Fujiwara, M., Matsui, M., Horiguchi, H., Satoh, H., Fujimoto, M., Yokoyama, K. and Ogata, T., Lack of class II transactivator causes severe deficiency of HLA-DR expression in small cell lung cancer. J. Pathol. 1999. 187: 191-199.
99. Naves, R., Lennon, A. M., Barbieri, G., Reyes, L., Puga, G., Salas, L., Deffrennes, V., Rosemblatt, M., Fellous, M., Charron, D. et al., MHC class II-deficient tumor cell lines with a defective expression of the class II transactivator. Int. Immunol. 2002. 14: 481-491.
100. van der Stoep, N., Biesta, P., Quinten, E. and van den Elsen, P. J., Lack of IFN-gamma-mediated induction of the class II transactivator (CIITA) through promoter methylation is predominantly found in developmental tumor cell lines. Int. J. Cancer 2002. 97: 501-507.
101. Holling, T. M., Schooten, E., Langerak, A. W. and Van Den Elsen, P. J., Regulation of MHC class II expression in human T-cell malignancies. Blood 2004. 130: 1438-1444.
102. Murphy, S. P., Holtz, R., Lewandowski, N., Tomasi, T. B. and Fuji, H., DNA alkylating agents alleviate silencing of class II transactivator gene expression in L1210 lymphoma cells. J. Immunol. 2002. 169: 3085-3093.
103. Kanaseki, T., Ikeda, H., Takamura, Y., Toyota, M., Hirohashi, Y., Tokino, T., Himi, T. and Sato, N., Histone deacetylation, but not hypermethylation, modifies class II transactivator and MHC class II gene expression in squamous cell carcinomas. J. Immunol. 2003. 170: 4980-4985.
104. Miller, D. M., Cebulla, C. M. and Sedmak, D. D., Human cytomegalovirus inhibition of major histocompatibility complex transcription and interferon signal transduction. Curr. Top. Microbiol. Immunol. 2002. 269: 153-170.
105. Hegde, N. R., Chevalier, M. S. and Johnson, D. C., Viral inhibition of MHC class II antigen presentation. Trends Immunol. 2003. 24: 278-285.
106. Zhong, G., Fan, T. and Liu, L., Chlamydia inhibits interferon gamma-inducible major histocompatibility complex class II expression by degradation of upstream stimulatory factor 1. J. Exp. Med. 1999. 189: 1931-1938.
107. Wojciechowski, W., DeSanctis, J., Skamene, E. and Radzioch, D., Attenuation of MHC class II expression in macrophages infected with Mycobacterium bovis bacillus Calmette-Guerin involves class II transactivator and depends on the Nramp1 gene. J. Immunol. 1999. 163: 2688-2696.
108. Pai, R. K., Convery, M., Hamilton, T. A., Boom, W. H. and Harding, C. V., Inhibition of IFN-gamma-induced class II transactivator expression by a 19-kDa lipoprotein from Mycobacterium tuberculosis: a potential mechanism for immune evasion. J. Immunol. 2003. 171: 175-184.
109. Luder, C. G., Lang, C., Giraldo-Velasquez, M., Algner, M., Gerdes, J. and Gross, U., Toxoplasma gondii inhibits MHC class II expression in neural antigen-presenting cells by down-regulating the class II transactivator CIITA. J. Neuroimmunol. 2003. 134: 12-24.
110. Abendroth, A., Slobedman, B., Lee, E., Mellins, E., Wallace, M. and Arvin, A. M., Modulation of major histocompatibility class II protein expression by varicella-zoster virus. J. Virol. 2000. 74: 1900-1907.
111. Miller, D. M., Rahill, B. M., Boss, J. M., Lairmore, M. D., Durbin, J. E., Waldman, J. W. and Sedmak, D. D., Human cytomegalovirus inhibits major histocompatibility complex class II expression by disruption of the Jak/Stat pathway. J. Exp. Med. 1998. 187: 675-683.
112. Le Roy, E., Muhlethaler-Mottet, A., Davrinche, C., Mach, B. and Davignon, J. L., Escape of human cytomegalovirus from HLA-DR-restricted CD4(+) T-cell response is mediated by repression of gamma interferon-induced class II transactivator expression. J. Virol. 1999. 73: 6582-6589.
113. Gao, J., De, B. P., Han, Y., Choudhary, S., Ransohoff, R. and Banerjee, A. K., Human parainfluenza virus type 3 inhibits gamma interferon-induced major histocompatibility complex class II expression directly and by inducing alpha/beta interferon. J. Virol. 2001. 75: 1124-1131.
114. Kanazawa, S., Okamoto, T. and Peterlin, B. M., Tat competes with CIITA for the binding to P-TEFb and blocks the expression of MHC class II genes in HIV infection. Immunity 2000. 12: 61-70.