Epigenetic control of MHC-II: Interplay between CIITA and histone-modifying enzymes

Current Opinion in Immunology

Volumn 17, Issue 1, 2005, Pages 58-64

  Zika, Eleni ^a   Ting, Jenny P Y ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSACTIVATOR PROTEIN;

ACETYLATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; ENZYME MODIFICATION; EPIGENETICS; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE INTERACTION; GENE REPRESSION; HUMAN; METHYLATION; MOLECULAR DYNAMICS; NONHUMAN; PROMOTER REGION; PROTEIN ASSEMBLY; PROTEIN PHOSPHORYLATION; REVIEW; TRANSCRIPTION INITIATION; UBIQUITINATION;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIGENESIS, GENETIC; GENES, MHC CLASS II; HISTONES; HUMANS; NUCLEAR PROTEINS; PROMOTER REGIONS (GENETICS); TRANS-ACTIVATORS;

EID: 11844275242     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coi.2004.11.008     Document Type: Review

References (48)

1. B. Mach, V. Steimle, E. Martinez-Soria, and W. Reith Regulation of MHC class II genes: lessons from a disease Annu Rev Immunol 14 1996 301 331
2. J.M. Boss, and P.E. Jensen Trancriptional regulation of the MHC class II antigen presentation pathway Curr Opin Immunol 15 2003 105 111
3. J.P. Ting, and J. Trowsdale Genetic control of MHC class II expression Cell 109 2002 S21 S33
4. P.J. van den Elsen, T.M. Holling, N. van der Stoep, and J.M. Boss 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 109 2003 46 52
5. S.P. Murphy, J.C. Choi, and R. Holtz Regulation of major histocompatibility complex class II gene expression in trophoblast cells Reprod Biol Endocrinol 2 2004 52
6. J.A. Harton, and J.P. Ting Class II transactivator: mastering the art of major histocompatibility complex expression Mol Cell Biol 20 2000 6185 6194
7. S.N. Maity, and B. de Crombrugghe Role of the CCAAT-binding protein CBF/NF-Y in transcription Trends Biochem Sci 23 1998 174 178
8. R. Mantovani The molecular biology of the CCAAT-binding factor NF-Y Gene 239 1999 15 27
9. V. Steimle, B. Durand, E. Barras, M. Zufferey, M.R. Hadam, B. Mach, and W. Reith A novel DNA-binding regulatory factor is mutated in primary MHC class II deficiency (bare lymphocyte syndrome) Genes Dev 9 1995 1021 1032
10. U.M. Nagarajan, P. Louis-Plence, A. DeSandro, R. Nilsen, A. Bushey, and J.M. Boss RFX-B is the gene responsible for the most common cause of the bare lymphocyte syndrome, an MHC class II immunodeficiency Immunity 10 1999 153 162
11. K. Masternak, E. Barras, M. Zufferey, B. Conrad, G. Corthals, R. Aebersold, J.C. Sanchez, D.F. Hochstrasser, B. Mach, and W. Reith A gene encoding a novel RFX-associated transactivator is mutated in the majority of MHC class II deficiency patients Nat Genet 20 1998 273 277
12. C.S. Moreno, G.W. Beresford, P. Louis-Plence, A.C. Morris, and J.M. Boss CREB regulates MHC class II expression in a CIITA-dependent manner Immunity 10 1999 143 151
13. A. Muhlethaler-Mottet, M. Krawczyk, K. Masternak, C. Spilianakis, A. Kretsovali, J. Papamatheakis, and W. Reith The S box of MHC class II promoters is a key determinant for recruitment of the transcriptional coactivator CIITA J Biol Chem 279 2004 40529 40535 This paper suggests a critical role of the S-box in the recruitment of CIITA to the promoter that does not require binding of RFX to a putative duplicated binding site in the W box.
14. X.S. Zhu, M.W. Linhoff, G. Li, K.C. Chin, S.N. Maity, and J.P. Ting Transcriptional scaffold: CIITA interacts with NF-Y, RFX, and CREB to cause stereospecific regulation of the class II major histocompatibility complex promoter Mol Cell Biol 20 2000 6051 6061
15. K. Masternak, A. Muhlethaler-Mottet, J. Villard, M. Zufferey, V. Steimle, and W. Reith CIITA is a transcriptional coactivator that is recruited to MHC class II promoters by multiple synergistic interactions with an enhanceosome complex Genes Dev 14 2000 1156 1166
16. K. Masternak, N. Peyraud, M. Krawczyk, E. Barras, and W. Reith Chromatin remodeling and extragenic transcription at the MHC class II locus control region Nat Immunol 4 2003 132 137 The authors demonstrate that an upstream inverted S-X-Y module might function as a locus control region for MHC-II through the recruitment of CIITA and RFX. This association also correlates with increased histone acetylation and recruitment of the basal transcriptional machinery to the MHC-II promoter region.
17. A. Dorn, H.J. Fehling, W. Koch, M. Le Meur, P. Gerlinger, C. Benoist, and D. Mathis B-cell control region at the 5′ end of a major histocompatibility complex class II gene: sequences and factors Mol Cell Biol 8 1988 3975 3987
18. R. Mudhasani, and J.D. Fontes The class II transactivator requires brahma-related gene 1 to activate transcription of major histocompatibility complex class II genes Mol Cell Biol 22 2002 5019 5026
19. K.L. Wright, K.C. Chin, M. Linhoff, C. Skinner, J.A. Brown, J.M. Boss, G.R. Stark, and J.P. Ting CIITA stimulation of transcription factor binding to major histocompatibility complex class II and associated promoters in vivo Proc Natl Acad Sci USA 95 1998 6267 6272
20. A. Kretsovali, T. Agalioti, C. Spilianakis, E. Tzortzakaki, M. Merika, and J. Papamatheakis Involvement of CREB binding protein in expression of major histocompatibility complex class II genes via interaction with the class II transactivator Mol Cell Biol 18 1998 6777 6783
21. J.D. Fontes, S. Kanazawa, D. Jean, and B.M. Peterlin Interactions between the class II transactivator and CREB binding protein increase transcription of major histocompatibility complex class II genes Mol Cell Biol 19 1999 941 947
22. α2(I) and other promoters Mol Cell Biol 21 2001 7078 7088
23. C. Spilianakis, J. Papamatheakis, and A. Kretsovali Acetylation by PCAF enhances CIITA nuclear accumulation and transactivation of major histocompatibility complex class II genes Mol Cell Biol 20 2000 8489 8498
24. J.A. Harton, E. Zika, and J.P. Ting The histone acetyltransferase domains of CREB-binding protein (CBP) and p300/CBP-associated factor are not necessary for cooperativity with the class II transactivator J Biol Chem 276 2001 38715 38720
25. E. Tzortzakaki, C. Spilianakis, E. Zika, A. Kretsovali, and J. Papamatheakis Steroid receptor coactivator 1 links the steroid and interferon gamma response pathways Mol Endocrinol 17 2003 2509 2518 This paper demonstrates that CIITA interacts with SRC-1 providing a link between the IFN-γ and steroid-response pathways.
26. G.W. Beresford, and J.M. Boss CIITA coordinates multiple histone acetylation modifications at the HLA-DRA promoter Nat Immunol 2 2001 652 657
27. A. Raval, T.K. Howcroft, J.D. Weissman, S. Kirshner, X.S. Zhu, K. Yokoyama, J. Ting, and D.S. Singer Transcriptional coactivator, CIITA, is an acetyltransferase that bypasses a promoter requirement for TAF(II)250 Mol Cell 7 2001 105 115
28. A. Osborne, H. Zhang, W.M. Yang, E. Seto, and G. Blanck Histone deacetylase activity represses gamma interferon-inducible HLA-DR gene expression following the establishment of a DNase I-hypersensitive chromatin conformation Mol Cell Biol 21 2001 6495 6506
29. W.J. Magner, A.L. Kazim, C. Stewart, M.A. Romano, G. Catalano, C. Grande, N. Keiser, F. Santaniello, and T.B. Tomasi Activation of MHC class I, II, and CD40 gene expression by histone deacetylase inhibitors J Immunol 165 2000 7017 7024
30. T. Kanaseki, H. Ikeda, Y. Takamura, M. Toyota, Y. Hirohashi, T. Tokino, T. Himi, and N. Sato Histone deacetylation, but not hypermethylation, modifies class II transactivator and MHC class II gene expression in squamous cell carcinomas J Immunol 170 2003 4980 4985
31. A.N. Khan, W.J. Magner, and T.B. Tomasi An epigenetically altered tumor cell vaccine Cancer Immunol Immunother 53 2004 748 754
32. E. Zika, S.F. Greer, X.S. Zhu, and J.P. Ting Histone deacetylase 1/mSin3A disrupts gamma interferon-induced CIITA function and major histocompatibility complex class II enhanceosome formation Mol Cell Biol 23 2003 3091 3102 This paper demonstrates that CIITA can also interact with repressors, such as HDAC1, and can mediate MHC-II inhibition. This interaction results in the disruption of the MHC-II enhanceosome.
33. S.F. Greer, E. Zika, B. Conti, X.S. Zhu, and J.P. Ting Enhancement of CIITA transcriptional function by ubiquitin Nat Immunol 4 2003 1074 1082 The authors show that CIITA is ubiquitinated. This modification enhances its transactivation function, and therefore MHC-II expression, and can be regulated by HATs.
34. A. Moren, U. Hellman, Y. Inada, T. Imamura, C.H. Heldin, and A. Moustakas Differential ubiquitination defines the functional status of the tumor suppresor Smad4 J Biol Chem 278 2003 33571 33582
35. V. Bres, R.E. Kiernan, L.K. Linares, C. Chable-Bessia, O. Plechakova, C. Treand, S. Emiliani, J.M. Peloponese, K.T. Jeang, and O. Coux A non-proteolytic role for ubiquitin in Tat-mediated transactivation of the HIV-1 promoter Nat Cell Biol 5 2003 754 761
36. T.J. Sisk, T. Gourley, S. Roys, and C.H. Chang 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 165 2000 2511 2517
37. S. Nozell, Z. Ma, C. Wilson, R. Shah, and E.N. Benveniste Class II major histocompatibility complex transactivator (CIITA) inhibits matrix metallproteinase-9 gene expression J Biol Chem 279 2004 38577 38589 This paper demonstrates the direct role of CIITA in the inhibition of metallproteinase-9 gene expression.
38. Y. Xu, L. Wang, G. Buttice, P.K. Sengupta, and B.D. Smith Major histocompatibility class II transactivator (CIITA) mediates repression of collagen (COL1A2) transcription by interferon gamma J Biol Chem 279 2004 41319 41332 This paper demonstrates that CIITA represses the collagen promoter mainly through its N-terminal domain during IFN-γ treatment, further supporting the novel role of CIITA in transcription repression.
39. B.D. Strahl, S.D. Briggs, C.J. Brame, J.A. Caldwell, S.S. Koh, H. Ma, R.G. Cook, J. Shabanowitz, D.F. Hunt, and M.R. Stallcup Methylation of histone H4 at arginine 3 occurs in vivo and is mediated by the nuclear receptor coactivator PRMT1 Curr Biol 11 2001 996 1000
40. U.M. Bauer, S. Daujat, S.J. Nielsen, K. Nightingale, and T. Kouzarides Methylation at arginine 17 of histone H3 is linked to gene activation EMBO Rep 3 2002 39 44
41. H. Wang, Z.Q. Huang, L. Xia, Q. Feng, H. Erdjument-Bromage, B.D. Strahl, S.D. Briggs, C.D. Allis, J. Wong, and P. Tempst Methylation of histone H4 at arginine 3 facilitating transcriptional activation by nuclear hormone receptor Science 293 2001 853 857
42. W. Xu, H. Chen, K. Du, H. Asahara, M. Tini, B.M. Emerson, M. Montminy, and R.M. Evans A transcriptional switch mediated by cofactor methylation Science 294 2001 2507 2511
43. M. Chevillard-Briet, D. Trouche, and L. Vandel Control of CBP co-activating activity by arginine methylation EMBO J 21 2002 5457 5466
44. J.D. Fontes, B. Jiang, and B.M. Peterlin The class II trans-activator CIITA interacts with the TBP-associated factor TAFII32 Nucleic Acids Res 25 1997 2522 2528
45. S.K. Mahanta, T. Scholl, F.C. Yang, and J.L. Strominger Transactivation by CIITA, the type II bare lymphocyte syndrome-associated factor, requires participation of multiple regions of the TATA box binding protein Proc Natl Acad Sci USA 94 1997 6324 6329
46. J.D. Weissman, T.K. Howcroft, and D.S. Singer TAF(II)250-independent transcription can be conferred on a TAF(II)250-dependent basal promoter by upstream activators J Biol Chem 275 2000 10160 10167
47. S. Kanazawa, T. Okamoto, and B.M. Peterlin Tat competes with CIITA for the binding to P-TEFb and blocks the expression of MHC class II genes in HIV infection Immunity 12 2000 61 70
48. C. Spilianakis, A. Kretsovali, T. Agalioti, T. Makatounakis, D. Thanos, and J. Papamatheakis CIITA regulates transcription onset via Ser5-phosphorylation of RNA Pol II EMBO J 22 2003 5125 5136 The authors demonstrate the association of CIITA with kinases CDK7 and CDK9 during transcriptional activation. CIITA facilitates the phosphorylation of RNA polymerase II by CDK7, thereby enabling promoter clearance and elongation. Therefore, CIITA controls both transcription initiation and elongation.