A BAF-centred view of the immune system

Nature Reviews Immunology

Volumn 4, Issue 12, 2004, Pages 965-977

  Chi, Tian ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CD4 ANTIGEN; CD8 ANTIGEN; DNA; HISTONE; INOSITOL PHOSPHATE; INOSITOL PHOSPHATE KINASE 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NUCLEAR PROTEIN; SMALL INTERFERING RNA; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ADENOSINE DIPHOSPHATE RIBOSYLATION; CHROMATIN STRUCTURE; COMPLEX FORMATION; DNA METHYLATION; DNA TEMPLATE; EMBRYO; EMBRYO DEVELOPMENT; ENHANCER REGION; GENE REPRESSION; GENETIC TRANSCRIPTION; IMMUNE SYSTEM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; SIGNAL TRANSDUCTION; SILENCER ELEMENT; T LYMPHOCYTE;

ANIMALS; CHROMATIN; DNA-BINDING PROTEINS; HISTONES; HUMANS; IMMUNE SYSTEM; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 10244236502     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri1501     Document Type: Review

References (93)

1. Felsenfeld, G. & Groudine, M. Controlling the double helix. Nature 421, 448-453 (2003).
2. Komberg, R. D. & Lorch, Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98, 285-294 (1999).
3. Katsani, K. R., Mahmoudi, T. & Verrijzer, C. P. Selective gene regulation by SWI/SNF-related chromatin remodeling factors. Curr. Top. Microbiol. Immunol. 274, 113-141 (2003).
4. Cheung, R, Allis, C. D. & Sassone-Corsi, P. Signaling to chromatin through histone modifications. Cell 103, 263-271 (2000).
5. Kikyo, N., Wade, P. A., Guschin, D., Ge, H. & Wolffe, A. P. Active remodeling of somatic nuclei in egg cytoplasm by the nucleosomal ATPase ISWI. Science 289, 2360-2362 (2000).
6. Muller, C. & Leutz, A. Chromatin remodeling in development and differentiation. Curr. Opin. Genet. Dev, 11, 167-174 (2001).
7. Fisher, A. G. Cellular identity and lineage choice. Nature Rev. Immunol. 2, 977-982 (2002).
8. Agarwal, S., Viola, J. P. & Rao, A. Chromatin-based regulatory mechanisms governing cytokine gene transcription. J. Allergy Clin. Immunol. 103, 990-999 (1999).
9. Lohning, M., Richter, A. & Radbruch, A. Cytokine memory of T helper lymphocytes. Adv. Immunol. 80, 115-181 (2002).
10. Narlikar, G. J., Fan, H. Y. & Kingston, R. E. Cooperation between complexes that regulate chromatin structure and transcription, Cell 108, 475-487 (2002).
11. Fry, C. J. & Peterson, C. L. Chromatin remodeling enzymes: who's on first? Curr. Biol. 11, R185-R197 (2001).
12. Khavari, P. A., Peterson, C. L., Tamkun, J. W., Mendel, D. B. & Crabtree, G. R. BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription. Nature 366, 170-174 (1993).
13. Muchardt, C. & Yaniv, M. A human homologue of Saccharomyces cerevisae SNF2/SWI2 and Drosophila brm genes potentiates transcripttonal activation by the glucocorticoid receptor. EMBO J. 12, 4279-4290 (1993).
14. Wang, W. et al. Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J. 15, 5370-5382 (1996).
15. Strobeck, M. W. et al. Compensation of BRG-1 function by Brm: insight into the role of the core SWI-SNF subunits in retinoblastoma tumor suppressor signaling. J. Biol. Chem. 277, 4782-4789 (2002).
16. Bultman, S. et al. A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol. Cell 6, 1287-1295 (2000).
17. Chi, T. H. et al. Sequential roles of Brg, the ATPase subunit of BAF chromatin remodeling complexes, in thymocyte development. Immunity 19, 169-182 (2003). References 17 and 19 use T-cell development as a model system to carry out the first in-depth genetic analysis of BRG in animals.
18. Reyes, J. C. et al. Altered control of cellular proliferation in the absence of mammalian brahma (SNF2α). EMBO J. 17, 6979-6991 (1998).
19. Gebuhr, T. C. et al. The role of Brg1, a catalytic subunit of mammalian chromatin-remodeling complexes, in T cell development. J. Exp. Med. 198, 1937-1949 (2003).
20. Kadam, S. & Emerson, B. M. Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes. Mol. Cell 11, 377-389 (2003).
21. Nie, Z. et al. A specificity and targeting subunit of a human SWI/SNF family-related chromatin-remodeling complex. Mol. Cell. Biol. 20, 8879-8883 (2000).
22. Lemon, B., Inouye, C., King, D. S. & Tjian, R. Selectivity of chromatin-remodelling cofactors for ligand-activated transcription. Nature 414, 924-928 (2001).
23. Wang, W. et al. Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev. 10, 2117-2130 (1996).
24. Olave, I., Wang, W., Xue, Y., Kuo, A. & Crabtree, G. R. Identification of a polymorphic, neuron-specific chromatin remodeling complex. Genes Dev. 16, 2509-2517 (2002).
25. Xu, W. et al. A methylation-mediator complex in hormone signaling. Genes Dev. 18, 144-156 (2004).
26. Tong, J. K., Hassig, C. A., Schnitzler, G. R., Kingston, R. E. & Schreiber, S. L. Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature 395, 917-921 (1998).
27. Xue, Y. et al. NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase actvities. Mol. Cell 2, 851-861 (1998).
28. Zhang, Y., LeRoy, G., Seelig, H. P., Lane, W. S. & Reinberg, D. The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 95, 279-289 (1998).
29. Chi, T. H. et al. Reciprocal regulation of CD4/CD8 expression by SWI/SNF-like BAF complexes. Nature 418, 195-199 (2002). This paper shows that BAF57, a subunit dispensable for chromatin remodelling in vitro, has essential functions in vivo. It establishes BAF complexes as the key regulator of CD4 and CD8 expression.
30. Morshead, K. B., Ciccone, D. N., Taverna, S. D., Allis, C. D. & Oettinger, M. A. Antigen receptor loci poised for V(D)J rearrangement are broadly associated with BRG1 and flanked by peaks of histone H3 dimethylated at lysine 4. Proc. Natl Acad. Sci. USA 100, 11577-11582 (2003).
31. Kwon, J., Morshead, K. B., Guyon, J. R., Kingston, R. E. & Oettinger, M. A. Histone acetylation and hSWI/SNF remodeling act in concert to stimulate V(D)J cleavage of nucleosomal DNA. Mol. Cell 6, 1037-1048 (2000).
32. Patenge, N., Elkin, S. K. & Oettinger, M. A. ATP-dependent remodeling by SWI/SNF and ISWI proteins stimulates V(D)J cleavage of 5 S arrays. J. Biol. Chem. 279, 35360-35367 (2004).
33. Golding, A., Chandler, S., Ballestar, E., Wolffe, A. P. & Schlissel, M. S. Nucleosome structure completely inhibits in vitro cleavage by the V(D)J recombinase. EMBO J. 18, 3712-3723 (1999).
34. Spicuglia, S. et al. Promoter activation by enhancer-dependent and -independent loading of activator and coactivator complexes. Mol. Cell 10, 1479-1487 (2002).
35. Agalioti, T. et al. Ordered recruitment of chromatin modifying and general transcription factors to the IFN-β promoter. Cell 103, 667-678 (2000).
36. Lomvardas, S. & Thanos, D. Nucleosome sliding via TBP DNA binding In vivo. Cell 106, 685-696 (2001).
37. Lomvardas, S. & Thanos, D. Modifying gene expression programs by altering core promoter chromatin architecture. Cell 110, 261-271 (2002).
38. Agalioti, T., Chen, G. & Thanos, D. Deciphering the transcriptional histone acetylation code for a human gene. Cell 111, 381-392 (2002). References 35-38 set up a paradigm for dissecting the mechanisms of regulation of a natural promoter. They show the biological significance of the chromatin configuration of a promoter, how signalling pathways mobilize both BRG and HAT, and how these two enzymes cooperate to reconfigure the chromatin to allow gene induction.
39. Cui, K. et al. The chromatin-remodeling BAF complex mediates cellular antiviral activities by promoter priming. Mol. Cell. Biol. 24, 4476-4486 (2004). This paper shows that BAF complexes use a unique strategy to regulate an IFN-α-responsive promoter.
40. Huang, M. et al. Chromatin-remodelling factor BRG1 selectively activates a subset of interferon-α-inducible genes. Nature Cell Biol. 4, 774-781 (2002).
41. Liu, H., Kang, H., Liu, R., Chen, X. & Zhao, K. Maximal induction of a subset of interferon target genes requires the chromatin-remodeling activity of the BAF complex. Mol. Cell. Biol. 22, 6471-6479 (2002).
42. Zhao, K. et al. Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 95, 625-636 (1998). This is the first paper that links nuclear inositol signalling to chromatin remodelling. It indicates that BRG functions downstream of TCR signalling to decondense chromatin during T-cell activation.
43. Landsverk, H. B. et al. Reprogrammed gene expression in a somatic cell-free extract. EMBO Rep. 3, 384-389 (2002).
44. Hakelien, A. M., Landsverk, H. B., Robl, J. M., Skalhegg, B. S. & Collas, P. Reprogramming fibroblasts to express T-cell functions using cell extracts. Nature Biotechnol. 20, 460-466 (2002).
45. Goodbourn, S., Didcock, L. & Randall, R. E. Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J. Gen. Virol. 81, 2341-2364 (2000).
46. Munshi, N. et al. Acetylation of HMG I(Y) by CBP turns off IFN β expression by disrupting the enhanceosome. Mol. Cell 2, 457-467 (1998).
47. Gyory, I., Wu, J., Fejer, G., Seto, E. & Wright, K. L. PRDI-BF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing. Nature Immunol. 5, 299-308 (2004).
48. Wack, A., Coles, M., Norton, T., Hostert, A. & Kioussis, D. Early onset of CDS transgene expression inhibits the transition from DN3 to DP thymocytes. J. Immunol. 165, 1236-1242 (2000).
49. Bhattacharya, S. et al. Cooperation of Stat2 and p300/CBP in signalling induced by interteron-β. Nature 383, 344-347 (1996).
50. Ting, J. P. & Trowsdale, J. Genetic control of MHC class II expression. Cell 109, S21-S33 (2002).
51. Pattenden, S. G., Klose, R., Karaskov, E. & Bremner, R. Interferon-γ-induced chromatin remodeling at the CIITA locus is BRG1 dependent. EMBO J. 21, 1978-1986 (2002). This is the first paper that links BAF complexes to cytokine-mediated signalling.
52. Mudhasani, R. & Fortes, J. D. The class II transactivator requires brahma-related gene 1 to activate transcription of major histocompatibility complex class II genes. Mol. Cell. Biol. 22, 5019-5026 (2002).
53. Masternak, K. et al. CIITA is a transcriptional coactivator that is recruited to MHC class II promoters by multiple synergistic interactions with an enhanceosome complex. Genes Dev. 14, 1156-1166 (2000).
54. Kara, C. J. & Glimcher, L. H. Developmental and cytokine-mediated regulation of MHC class II gene promoter occupancy in vivo. J. Immunol. 150, 4934-4942 (1993).
55. Beresford, G. W. & Boss, J. M. CIITA coordinates multiple histone acetylation modifications at the HLA-DRA promoter. Nature Immunol. 2, 652-657 (2001).
56. Smale, S. T. The establishment and maintenance of lymphocyte identity through gene silencing. Nature Immunol. 4, 607-615 (2003).
57. Fisher, A. G. & Merkenschlager, M. Gene silencing, cell fate and nuclear organisation. Curr. Opin. Genet. Dev. 12, 193-197 (2002).
58. Ellmeier, W., Sawada, S. & Littman, D. R. The regulation of CD4 and CD8 coreceptor gene expression during T cell development. Annu. Rev. Immunol. 17, 523-554 (1999).
59. Zou, Y. R. et al. Epigenetic silencing of CD4 in T cells committed to the cytotoxic lineage. Nature Genet. 29, 332-336 (2001).
60. Taniuchi, I. et al. Differential requirements for Runx proteins in CD4 repression and epigenetic silencing during T lymphocyte development. Cell 111, 621-633 (2002). This paper shows that the CD4 silencer has two distinct functions at different stages of T-cell development.
61. Coisy, M. et al. Cyclin A repression in quiescent cells is associated with chromatin remodeling of its promoter and requires Brahma/SNF2α. Mol. Cell 15, 43-56 (2004).
62. Sif, S., Saurin, A. J., Imbalzano, A. N. & Kingston, R. E. Purification and characterization of mSinSA-containing Brg1 and hBrm chromatin remodeling complexes. Genes Dev. 15, 603-618 (2001).
63. Pal, S. et al. mSinSA/histone deacetylase 2- and PRMT5-containing Brg1 complex is involved in transcriptional repression of the Myc target gene cad. Mol. Cell. Biol. 23, 7475-7487 (2003).
64. Williams, C. J. et al. The chromatin remodeler Mi-2β is required for CD4 expression and T cell development. Immunity 20, 719-733 (2004).
65. Simone, C. et al. p38 pathway targets SWI-SNF chromatin-remodeling complex to muscle-specific loci. Nature Genet. 36, 738-743 (2004).
66. Bourachot, B., Yaniv, M. & Muchardt, C. Growth inhibition by the mammalian SWI-SNF subunit Brm is regulated by acetylation. EMBO J. 22, 6505-6515 (2003).
67. Steger, D. J., Haswell, E. S., Miller, A. L., Wente, S. R. & O'Shea, E. K. Regulation of chromatin remodeling by inositol polyphosphates. Science 299, 114-116 (2003).
68. Shen, X., Xiao, H., Ranallo, R., Wu, W. H. & Wu, C. Modulation of ATP-dependent chromatin-remodeling complexes by inositol polyphosphates. Science 299, 112-114 (2003).
69. Martelli, A. M., Manzoli, L. & Cocco, L. Nuclear inositides: facts and perspectives. Phamacol. Ther. 101, 47-64 (2004).
70. Cocco, L., Maraldi, N. M. & Manzoli, F. A. New frontiers of inositide-specific phospholipase C in nuclear signalling. Eur. J. Histochem. 48, 83-88 (2004).
71. Irvine, R. F. Nuclear lipid signaling. Sci STKE 2002, re13 (2002).
72. Rando, O. J., Zhao, K., Janmey, P. & Crabtree, G. R. Phosphatidylinositol-dependent actin filament binding by the SWI/SNF-like BAF chromatin remodeling complex. Proc. Natl Acad. Sci. USA 99, 2824-2829 (2002).
73. Gozani, O. et al. The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell 114, 99-111 (2003).
74. Festenstein, R. et al. Modulation of heterochromatin protein 1 dynamics in primary mammalian cells. Science 299, 719-721 (2003).
75. Sif, S., Stukenberg, P. T., Kirschner, M. W. & Kingston, R. E. Mitotic inactivation of a human SWI/SNF chromatin remodeling complex. Genes Dev. 12, 2842-2851 (1998).
76. Reyes, J. C., Muchardt, C. & Yaniv, M. Components of the human SWI/SNF complex are enriched in active chromatin and are associated with the nuclear matrix. J. Cell Biol. 137, 263-274 (1997).
77. Turelli, P. et al. Cytoplasmic recruitment of INU and PML on incoming HIV preintegration complexes: interference with early steps of viral replication. Mol. Cell 7, 1245-1254 (2001).
78. Craig, E., Zhang, Z. K., Davies, K. P. & Kalpana, G. V. A masked NES in INI1/hSNF5 mediates hCRM1-dependent nuclear export: implications for tumorigenesis. EMBO J. 21, 31-12 (2002).
79. Memedula, S. & Belmont, A. S. Sequential recruitment of HAT and SWI/SNF components to condensed chromatin by VP16. Curr. Biol. 13, 241-246 (2003).
80. Madakamutil, L. T. et al. CD8αα-mediated survival and differentiation of CD8 memory T cell precursors. Science 304, 590-593 (2004).
81. Kaech, S.M. et al. Selective expression of the interteukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nature Immunol. 4, 1191-1198 (2003).
82. Belandia, B., Orford, R. L., Hurst, H. C. & Parker, M. G. Targeting of SWI/SNF chromatin remodelling complexes to estrogen-responsive genes. EMBO J. 21, 4094-4103 (2002).
83. Hsiao, P. W., Fryer, C. J., Trotter, K. W., Wang, W. & Archer, T. K. BAF60a mediates critical interactions between nuclear receptors and the BRG1 chromatin-remodeling complex for transactivation. Mol. Cell. Biol. 23, 6210-6220 (2003).
84. Inoue, H. et al. Largest subunits of the human SWI/SNF chromatin-remodeling complex promote transcriptional activation by steroid hormone receptors. J. Biol. Chem. 277, 41674-41685 (2002).
85. Trotter, K. W. & Archer, T. K. Reconstitution of glucocorticoid receptor-dependent transcription in vivo. Mol. Cell. Biol. 24, 3347-3358 (2004).
86. Kalpana, G. V., Marmon, S., Wang, W., Crabtree, G. R. & Goff, S. P. Binding and stimulation of HIV-1 integrase by a human homolog of yeast transcription factor SNFS. Science 266, 2002-2006 (1994).
87. Strahl, B. D. & Allis, C. D. The language of covalent histone modifications. Nature 403, 41-45 (2000).
88. Kurdistani, S. K., Tavazoie, S. & Grunstein, M. Mapping global histone acetylation patterns to gene expression. Cell 117, 721-733 (2004).
89. Lusser, A. & Kadonaga, J. T. Chromatin remodeling by ATP-dependent molecular machines. Bioessays 25, 1192-1200 (2003).
90. Martens, J. A. & Winston, F. Recent advances in understanding Chromatin remodeling by Swi/Snf complexes. Curr. Opin. Genet. Dev. 13, 136-142 (2003).
91. Fan, H. Y., He, X., Kingston, R. E. & Nartikar, G. J. Distinct strategies to make nucleosomal DNA accessible. Mol. Cell 11, 1311-1322 (2003).
92. Stopka, T. & Skoultchi, A. I. The ISWI ATPase Snf2h is required for early mouse development. Proc. Natl Acad. Sci. USA 100, 14097-14102 (2003).
93. Lickert, H. et al. Baf60c is essential for function of BAF Chromatin remodelling complexes in heart development. Nature 432, 107-112 (2004).