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PMID: 11953317 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Interferon-gamma-induced chromatin remodeling at the CIITA locus is BRG1 dependent.

The EMBO journal ·Vol. 21 ·No. 8 ·2002-04-15 ·Pages 1978-86

Pattenden SG, Klose R, Karaskov E, Bremner R

Abstract

SWI/SNF regulates growth control, differentiation and tumor suppression, yet few direct targets of this chromatin-remodeling complex have been identified in mammalian cells. We report that SWI/SNF is required for interferon (IFN)-gamma induction of CIITA, the master regulator of major histocompatibility complex class II expression. Despite the presence of functional STAT1, IRF-1 and USF-1, activators implicated in CIITA expression, IFN-gamma did not induce CIITA in cells lacking BRG1 and hBRM, the ATPase subunits of SWI/SNF. Reconstitution with BRG1, but not an ATPase-deficient version of this protein (K798R), rescued CIITA induction, and enhanced the rate of induction of the IFN-gamma-responsive GBP-1 gene. Not ably, BRG1 inhibited the CIITA promoter in transient transfection assays, underscoring the importance of an appropriate chromosomal environment. Chromatin immunoprecipitation revealed that BRG1 interacts directly with the endogenous CIITA promoter in an IFN-gamma-inducible fashion, while in vivo DNase I footprinting and restriction enzyme accessibility assays showed that chromatin remodeling at this locus requires functional BRG1. These data provide the first link between a cytokine pathway and SWI/SNF, and suggest a novel role for this chromatin-remodeling complex in immune surveillance.

MeSH Terms
Cell Line, Transformed Chromatin/physiology DNA Helicases Gene Expression Regulation HeLa Cells Histocompatibility Antigens Class II/genetics Humans Interferon-gamma/pharmacology Nuclear Proteins/metabolism Promoter Regions, Genetic Trans-Activators/genetics Transcription Factors/metabolism Tumor Cells, Cultured
Chemicals
Chromatin Histocompatibility Antigens Class II MHC class II transactivator protein Nuclear Proteins SMARCA2 protein, human Trans-Activators Transcription Factors Interferon-gamma SMARCA4 protein, human DNA Helicases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Pattenden Samantha G
Molecular and Cellular Division, Toronto Western Research Institute, Department of Ophthalmology and Visual Science, University of Toronto, Toronto, Canada M5T 2S8.
Klose Robert
Karaskov Elizabeth
Bremner Rod
References (72)
72 references, click to expand
  1. 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 Jan 1;160(1):233-40 PMID: 9551976
  2. Chromatin remodelling by the glucocorticoid receptor requires the BRG1 complex.
    Nature. 1998 May 7;393(6680):88-91 PMID: 9590696
  3. A human RNA polymerase II complex containing factors that modify chromatin structure.
    Mol Cell Biol. 1998 Sep;18(9):5355-63 PMID: 9710619
  4. Mitotic inactivation of a human SWI/SNF chromatin remodeling complex.
    Genes Dev. 1998 Sep 15;12(18):2842-51 PMID: 9744861
  5. Alteration of nucleosome structure as a mechanism of transcriptional regulation.
    Annu Rev Biochem. 1998;67:545-79 PMID: 9759497
  6. Dissecting the regulatory circuitry of a eukaryotic genome.
    Cell. 1998 Nov 25;95(5):717-28 PMID: 9845373
  7. 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 Jan;19(1):431-40 PMID: 9858567
  8. Mice lacking the transcription factor CIITA--a second look.
    Int Immunol. 1998 Dec;10(12):1957-67 PMID: 9885917
  9. Human SWI-SNF component BRG1 represses transcription of the c-fos gene.
    Mol Cell Biol. 1999 Apr;19(4):2724-33 PMID: 10082538
  10. IFN-gamma regulation of the type IV class II transactivator promoter in astrocytes.
    J Immunol. 1999 Apr 15;162(8):4731-9 PMID: 10202014
  11. c-MYC interacts with INI1/hSNF5 and requires the SWI/SNF complex for transactivation function.
    Nat Genet. 1999 May;22(1):102-5 PMID: 10319872
  12. The mammalian SWI/SNF complex and the control of cell growth.
    Semin Cell Dev Biol. 1999 Apr;10(2):189-95 PMID: 10441072
  13. pRB is required for interferon-gamma-induction of the MHC class II abeta gene.
    Oncogene. 1999 Sep 2;18(35):4940-7 PMID: 10490828
  14. Recruitment of the SWI/SNF chromatin remodeling complex by transcriptional activators.
    Genes Dev. 1999 Sep 15;13(18):2369-74 PMID: 10500094
  15. Constitutional mutations of the hSNF5/INI1 gene predispose to a variety of cancers.
    Am J Hum Genet. 1999 Nov;65(5):1342-8 PMID: 10521299
  16. Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer.
    Nature. 1998 Jul 9;394(6689):203-6 PMID: 9671307
  17. Activation domain-mediated targeting of the SWI/SNF complex to promoters stimulates transcription from nucleosome arrays.
    Mol Cell. 1999 Oct;4(4):649-55 PMID: 10549297
  18. Spectrum of hSNF5/INI1 somatic mutations in human cancer and genotype-phenotype correlations.
    Hum Mol Genet. 1999 Dec;8(13):2359-68 PMID: 10556283
  19. Co-occupancy of the interferon regulatory element of the class II transactivator (CIITA) type IV promoter by interferon regulatory factors 1 and 2.
    Oncogene. 1999 Oct 21;18(43):5889-903 PMID: 10557076
  20. Cell-based vaccines for the stimulation of immunity to metastatic cancers.
    Immunol Rev. 1999 Aug;170:101-14 PMID: 10566145
  21. A C/EBP beta isoform recruits the SWI/SNF complex to activate myeloid genes.
    Mol Cell. 1999 Nov;4(5):735-43 PMID: 10619021
  22. The language of covalent histone modifications.
    Nature. 2000 Jan 6;403(6765):41-5 PMID: 10638745
  23. Mammalian SWI-SNF complexes contribute to activation of the hsp70 gene.
    Mol Cell Biol. 2000 Apr;20(8):2839-51 PMID: 10733587
  24. Whole-genome expression analysis of snf/swi mutants of Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3364-9 PMID: 10725359
  25. Exit from G1 and S phase of the cell cycle is regulated by repressor complexes containing HDAC-Rb-hSWI/SNF and Rb-hSWI/SNF.
    Cell. 2000 Mar 31;101(1):79-89 PMID: 10778858
  26. The role of STATs in transcriptional control and their impact on cellular function.
    Oncogene. 2000 May 15;19(21):2468-73 PMID: 10851045
  27. BRG-1 is required for RB-mediated cell cycle arrest.
    Proc Natl Acad Sci U S A. 2000 Jul 5;97(14):7748-53 PMID: 10884406
  28. BRG-1 is recruited to estrogen-responsive promoters and cooperates with factors involved in histone acetylation.
    Mol Cell Biol. 2000 Oct;20(20):7541-9 PMID: 11003650
  29. Functional selectivity of recombinant mammalian SWI/SNF subunits.
    Genes Dev. 2000 Oct 1;14(19):2441-51 PMID: 11018012
  30. HSNF5/INI1 gene mutations in lymphoid malignancy.
    Cancer Genet Cytogenet. 2000 Oct 1;122(1):37-42 PMID: 11104031
  31. Haploinsufficiency of Snf5 (integrase interactor 1) predisposes to malignant rhabdoid tumors in mice.
    Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13796-800 PMID: 11095756
  32. Ordered recruitment of chromatin modifying and general transcription factors to the IFN-beta promoter.
    Cell. 2000 Nov 10;103(4):667-78 PMID: 11106736
  33. INI1 mutations in meningiomas at a potential hotspot in exon 9.
    Br J Cancer. 2001 Jan;84(2):199-201 PMID: 11161377
  34. Mammalian SWI/SNF complexes promote MyoD-mediated muscle differentiation.
    Nat Genet. 2001 Feb;27(2):187-90 PMID: 11175787
  35. 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 Feb 15;166(4):2260-9 PMID: 11160280
  36. A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes.
    Mol Cell. 2000 Dec;6(6):1287-95 PMID: 11163203
  37. Purification and characterization of mSin3A-containing Brg1 and hBrm chromatin remodeling complexes.
    Genes Dev. 2001 Mar 1;15(5):603-18 PMID: 11238380
  38. The bare lymphocyte syndrome and the regulation of MHC expression.
    Annu Rev Immunol. 2001;19:331-73 PMID: 11244040
  39. Mechanisms for ATP-dependent chromatin remodelling.
    Curr Opin Genet Dev. 2001 Apr;11(2):148-54 PMID: 11250137
  40. The murine SNF5/INI1 chromatin remodeling factor is essential for embryonic development and tumor suppression.
    EMBO Rep. 2000 Dec;1(6):500-6 PMID: 11263494
  41. Chromatin remodeling enzymes: who's on first?
    Curr Biol. 2001 Mar 6;11(5):R185-97 PMID: 11267889
  42. Disruption of Ini1 leads to peri-implantation lethality and tumorigenesis in mice.
    Mol Cell Biol. 2001 May;21(10):3598-603 PMID: 11313485
  43. Impaired class II transactivator expression in mice lacking interferon regulatory factor-2.
    Oncogene. 2001 Jul 12;20(31):4219-27 PMID: 11464288
  44. Transcriptional activation domains of human heat shock factor 1 recruit human SWI/SNF.
    Mol Cell Biol. 2001 Sep;21(17):5826-37 PMID: 11486022
  45. The bromodomain: a regulator of ATP-dependent chromatin remodeling?
    Front Biosci. 2001 Aug 1;6:D1019-23 PMID: 11487477
  46. Regulation of CSF1 promoter by the SWI/SNF-like BAF complex.
    Cell. 2001 Aug 10;106(3):309-18 PMID: 11509180
  47. The chromatin remodelling factor Brg-1 interacts with beta-catenin to promote target gene activation.
    EMBO J. 2001 Sep 3;20(17):4935-43 PMID: 11532957
  48. ATP-driven chromatin remodeling activity and histone acetyltransferases act sequentially during transactivation by RAR/RXR In vitro.
    Mol Cell. 2000 Nov;6(5):1049-58 PMID: 11106744
  49. Complementation cloning of an MHC class II transactivator mutated in hereditary MHC class II deficiency (or bare lymphocyte syndrome).
    Cell. 1993 Oct 8;75(1):135-46 PMID: 8402893
  50. A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor.
    EMBO J. 1993 Nov;12(11):4279-90 PMID: 8223438
  51. BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription.
    Nature. 1993 Nov 11;366(6451):170-4 PMID: 8232556
  52. Evidence for retinoblastoma protein (RB) dependent and independent IFN-gamma responses: RB coordinately rescues IFN-gamma induction of MHC class II gene transcription in noninducible breast carcinoma cells.
    Oncogene. 1994 Apr;9(4):1015-9 PMID: 8134104
  53. Regulation of MHC class II expression by interferon-gamma mediated by the transactivator gene CIITA.
    Science. 1994 Jul 1;265(5168):106-9 PMID: 8016643
  54. The retinoblastoma protein and BRG1 form a complex and cooperate to induce cell cycle arrest.
    Cell. 1994 Oct 7;79(1):119-30 PMID: 7923370
  55. A role for retinoblastoma protein in potentiating transcriptional activation by the glucocorticoid receptor.
    Nature. 1995 Apr 6;374(6522):562-5 PMID: 7700385
  56. Direct transcriptional repression by pRB and its reversal by specific cyclins.
    Mol Cell Biol. 1995 Jun;15(6):3256-65 PMID: 7760821
  57. Molecular analysis of G1B and G3A IFN gamma mutants reveals that defects in CIITA or RFX result in defective class II MHC and Ii gene induction.
    Immunity. 1994 Nov;1(8):687-97 PMID: 7600294
  58. RNA polymerase II holoenzyme contains SWI/SNF regulators involved in chromatin remodeling.
    Cell. 1996 Jan 26;84(2):235-44 PMID: 8565069
  59. Mice lacking the MHC class II transactivator (CIITA) show tissue-specific impairment of MHC class II expression.
    Immunity. 1996 Feb;4(2):167-78 PMID: 8624807
  60. Stat1 alpha expression is involved in IFN-gamma induction of the class II transactivator and class II MHC genes.
    J Immunol. 1996 Aug 15;157(4):1559-68 PMID: 8759739
  61. Diversity and specialization of mammalian SWI/SNF complexes.
    Genes Dev. 1996 Sep 1;10(17):2117-30 PMID: 8804307
  62. Purification and biochemical heterogeneity of the mammalian SWI-SNF complex.
    EMBO J. 1996 Oct 1;15(19):5370-82 PMID: 8895581
  63. Two contact regions between Stat1 and CBP/p300 in interferon gamma signaling.
    Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15092-6 PMID: 8986769
  64. Nuclear integration of JAK/STAT and Ras/AP-1 signaling by CBP and p300.
    Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1074-9 PMID: 9037008
  65. IFN regulatory factor-1 plays a central role in the regulation of the expression of class I and II MHC genes in vivo.
    J Immunol. 1997 May 1;158(9):4260-9 PMID: 9126988
  66. Cellular responses to interferon-gamma.
    Annu Rev Immunol. 1997;15:749-95 PMID: 9143706
  67. 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 May 15;16(10):2851-60 PMID: 9184229
  68. RB and hbrm cooperate to repress the activation functions of E2F1.
    Proc Natl Acad Sci U S A. 1997 Oct 14;94(21):11268-73 PMID: 9326598
  69. The structure, regulation and function of the Janus kinases (JAKs) and the signal transducers and activators of transcription (STATs).
    Eur J Biochem. 1997 Sep 15;248(3):615-33 PMID: 9342212
  70. Transcriptional regulation of mammalian genes in vivo. A tale of two templates.
    J Biol Chem. 1997 Oct 31;272(44):27493-6 PMID: 9346875
  71. Factors associated with the mammalian RNA polymerase II holoenzyme.
    Nucleic Acids Res. 1998 Feb 1;26(3):847-53 PMID: 9443979
  72. Activation of the MHC class II transactivator CIITA by interferon-gamma requires cooperative interaction between Stat1 and USF-1.
    Immunity. 1998 Feb;8(2):157-66 PMID: 9491997
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
DOI
10.1093/emboj/21.8.1978
Published
2002-04-15
Pages
1978-86
Language
English
Region
England
NLM ID
8208664
PMCID
PMC125964
Subset
IM
External Links
PubMed source DOI: 10.1093/emboj/21.8.1978 PMC Full Text View journal details
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