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PMID: 12370291 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Gamma interferon triggers interaction between ICSBP (IRF-8) and TEL, recruiting the histone deacetylase HDAC3 to the interferon-responsive element.

Molecular and cellular biology ·Vol. 22 ·No. 21 ·2002-11-00 ·Pages 7439-48

Kuwata T, Gongora C, Kanno Y, Sakaguchi K, Tamura T, Kanno T, Basrur V, Martinez R, Appella E, Golub T, Ozato K

Abstract

ICSBP (IRF-8) is a transcription factor of the IRF family expressed only in the immune system. It is induced in macrophages by gamma interferon (IFN-gamma) and contributes to macrophage functions. By interacting with Ets family protein PU.1, ICSBP binds to the IRF/Ets composite element and stimulates transcription. ICSBP binds to another DNA element, the IFN-stimulated response element (ISRE), a common target of the IRF family. Limited knowledge as to how ICSBP and other IRF proteins regulate ISRE-dependent transcription in IFN-gamma-activated macrophages is available. By mass-spectrometric analysis of ISRE-bound proteins in macrophages, we identified TEL, another Ets member, as a factor recruited to the element in an IFN-gamma-dependent manner. In vitro analysis with recombinant proteins indicated that this recruitment is due to a direct interaction between ICSBP and TEL, which is enhanced by the presence of ISRE. Significantly, the interaction with TEL in turn resulted in the recruitment of the histone deacetytase HDAC3 to the ISRE, causing increased repression of IFN-gamma-mediated reporter activity through the ISRE. This repression may provide a negative-feedback mechanism operating after the initial transcriptional activation by IFN-gamma. By associating with two different Ets family proteins, ICSBP exerts a dual function in IFN-gamma-dependent gene regulation in an immune system-specific manner.

MeSH Terms
Animals Cell Line Cell Nucleus/metabolism DNA/metabolism DNA-Binding Proteins/chemistry,metabolism Gene Deletion Gene Expression Regulation Genes, Reporter Glutathione Transferase/metabolism Histone Deacetylases/metabolism Interferon Regulatory Factors Interferon-gamma/metabolism,physiology Interferons/metabolism Macrophages/immunology,metabolism Mass Spectrometry Mice Models, Biological Mutation Protein Binding Protein Structure, Tertiary Proto-Oncogene Proteins c-ets RNA, Messenger/metabolism Repressor Proteins/chemistry,metabolism Reverse Transcriptase Polymerase Chain Reaction
Chemicals
DNA-Binding Proteins ETS translocation variant 6 protein Interferon Regulatory Factors Proto-Oncogene Proteins c-ets RNA, Messenger Repressor Proteins interferon regulatory factor-8 Interferon-gamma DNA Interferons Glutathione Transferase Histone Deacetylases histone deacetylase 3
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Kuwata Takeshi
Laboratory of Molecular Growth Regulation, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, USA.
Gongora Celine
Kanno Yuka
Sakaguchi Kazuyasu
Tamura Tomohiko
Kanno Tomohiko
Basrur Venkatesha
Martinez Robert
Appella Ettore
Golub Todd
Ozato Keiko
References (61)
61 references, click to expand
  1. Vesicular stomatitis virus infection induces a nuclear DNA-binding factor specific for the interferon-stimulated response element.
    J Virol. 1995 Jul;69(7):4173-81 PMID: 7539506
  2. TEL is a sequence-specific transcriptional repressor.
    J Biol Chem. 1999 Oct 15;274(42):30132-8 PMID: 10514502
  3. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels.
    Anal Chem. 1996 Mar 1;68(5):850-8 PMID: 8779443
  4. The TEL gene and human leukemia.
    Biochim Biophys Acta. 1996 Aug 8;1288(1):M7-10 PMID: 8764840
  5. Pip, a lymphoid-restricted IRF, contains a regulatory domain that is important for autoinhibition and ternary complex formation with the Ets factor PU.1.
    Genes Dev. 1996 Sep 15;10(18):2335-47 PMID: 8824592
  6. Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene.
    Cell. 1996 Oct 18;87(2):307-17 PMID: 8861914
  7. Interferon regulatory factors and TFIIB cooperatively regulate interferon-responsive promoter activity in vivo and in vitro.
    Mol Cell Biol. 1996 Nov;16(11):6313-24 PMID: 8887661
  8. PU.1 can participate in an active enhancer complex without its transcriptional activation domain.
    Proc Natl Acad Sci U S A. 1997 Jan 7;94(1):127-32 PMID: 8990172
  9. A domain of TEL conserved in a subset of ETS proteins defines a specific oligomerization interface essential to the mitogenic properties of the TEL-PDGFR beta oncoprotein.
    EMBO J. 1997 Jan 2;16(1):69-82 PMID: 9009269
  10. The TEL gene products: nuclear phosphoproteins with DNA binding properties.
    Oncogene. 1997 Jan 23;14(3):349-57 PMID: 9018121
  11. Stimulation of macrophages by lipopolysaccharide alters the phosphorylation state, conformation, and function of PU.1 via activation of casein kinase II.
    J Immunol. 1997 Feb 15;158(4):1848-56 PMID: 9029125
  12. Phosphorylation events modulate the ability of interferon consensus sequence binding protein to interact with interferon regulatory factors and to bind DNA.
    J Biol Chem. 1997 Apr 11;272(15):9785-92 PMID: 9092512
  13. Cellular responses to interferon-gamma.
    Annu Rev Immunol. 1997;15:749-95 PMID: 9143706
  14. Interferon consensus sequence binding protein-deficient mice display impaired resistance to intracellular infection due to a primary defect in interleukin 12 p40 induction.
    J Exp Med. 1997 Nov 3;186(9):1523-34 PMID: 9348310
  15. A two-step mechanism for recruitment of Pip by PU.1.
    J Immunol. 1998 Jan 1;160(1):241-52 PMID: 9551977
  16. PU.1, interferon regulatory factor 1, and interferon consensus sequence-binding protein cooperate to increase gp91(phox) expression.
    J Biol Chem. 1998 May 29;273(22):13957-65 PMID: 9593745
  17. The growing family of interferon regulatory factors.
    Cytokine Growth Factor Rev. 1997 Dec;8(4):293-312 PMID: 9620643
  18. SAP30, a novel protein conserved between human and yeast, is a component of a histone deacetylase complex.
    Mol Cell. 1998 Jun;1(7):1021-31 PMID: 9651585
  19. The TEL/ETV6 gene is required specifically for hematopoiesis in the bone marrow.
    Genes Dev. 1998 Aug 1;12(15):2392-402 PMID: 9694803
  20. How cells respond to interferons.
    Annu Rev Biochem. 1998;67:227-64 PMID: 9759489
  21. Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex.
    Nature. 1998 Oct 29;395(6705):917-21 PMID: 9804427
  22. Assembly requirements of PU.1-Pip (IRF-4) activator complexes: inhibiting function in vivo using fused dimers.
    EMBO J. 1999 Feb 15;18(4):977-91 PMID: 10022840
  23. The histone acetylase PCAF is a phorbol-ester-inducible coactivator of the IRF family that confers enhanced interferon responsiveness.
    Mol Cell Biol. 1999 Mar;19(3):1810-20 PMID: 10022868
  24. Physical and functional interactions between the transcription factor PU.1 and the coactivator CBP.
    Oncogene. 1999 Feb 18;18(7):1495-501 PMID: 10050886
  25. Histone deacetylases, transcriptional control, and cancer.
    J Cell Physiol. 2000 Jul;184(1):1-16 PMID: 10825229
  26. An IFN-gamma-inducible transcription factor, IFN consensus sequence binding protein (ICSBP), stimulates IL-12 p40 expression in macrophages.
    J Immunol. 2000 Jul 1;165(1):271-9 PMID: 10861061
  27. The histone deacetylase-3 complex contains nuclear receptor corepressors.
    Proc Natl Acad Sci U S A. 2000 Jun 20;97(13):7202-7 PMID: 10860984
  28. Both corepressor proteins SMRT and N-CoR exist in large protein complexes containing HDAC3.
    EMBO J. 2000 Aug 15;19(16):4342-50 PMID: 10944117
  29. The leukemia-associated gene TEL encodes a transcription repressor which associates with SMRT and mSin3A.
    Biochem Biophys Res Commun. 1999 Nov 2;264(3):871-7 PMID: 10544023
  30. Protein-protein and DNA-protein interactions affect the activity of lymphoid-specific IFN regulatory factors.
    J Immunol. 1999 Dec 15;163(12):6468-78 PMID: 10586038
  31. Identification of gel-separated tumor marker proteins by mass spectrometry.
    Electrophoresis. 2000 Feb;21(3):679-86 PMID: 10726777
  32. PU.1 and interferon consensus sequence-binding protein regulate the myeloid expression of the human Toll-like receptor 4 gene.
    J Biol Chem. 2000 Mar 31;275(13):9773-81 PMID: 10734131
  33. IFN-gamma up-regulates IL-18 gene expression via IFN consensus sequence-binding protein and activator protein-1 elements in macrophages.
    J Immunol. 2000 Sep 15;165(6):3198-205 PMID: 10975835
  34. ICSBP directs bipotential myeloid progenitor cells to differentiate into mature macrophages.
    Immunity. 2000 Aug;13(2):155-65 PMID: 10981959
  35. Proteins of the ETS family with transcriptional repressor activity.
    Oncogene. 2000 Dec 18;19(55):6524-32 PMID: 11175368
  36. Ets target genes: past, present and future.
    Oncogene. 2000 Dec 18;19(55):6533-48 PMID: 11175369
  37. Stable histone deacetylase complexes distinguished by the presence of SANT domain proteins CoREST/kiaa0071 and Mta-L1.
    J Biol Chem. 2001 Mar 2;276(9):6817-24 PMID: 11102443
  38. IRF family of transcription factors as regulators of host defense.
    Annu Rev Immunol. 2001;19:623-55 PMID: 11244049
  39. Functional significance of histone deacetylase diversity.
    Curr Opin Genet Dev. 2001 Apr;11(2):162-6 PMID: 11250139
  40. PU.1 and multiple IFN regulatory factor proteins synergize to mediate transcriptional activation of the human IL-1 beta gene.
    J Immunol. 2001 Jun 1;166(11):6829-38 PMID: 11359842
  41. TEL contacts multiple co-repressors and specifically associates with histone deacetylase-3.
    Oncogene. 2001 Jun 21;20(28):3716-25 PMID: 11439334
  42. Negative regulation of cytokine signaling.
    J Leukoc Biol. 2001 Sep;70(3):348-56 PMID: 11527983
  43. SHP1 protein-tyrosine phosphatase inhibits gp91PHOX and p67PHOX expression by inhibiting interaction of PU.1, IRF1, interferon consensus sequence-binding protein, and CREB-binding protein with homologous Cis elements in the CYBB and NCF2 genes.
    J Biol Chem. 2001 Oct 12;276(41):37868-78 PMID: 11483597
  44. ICSBP/IRF-8: its regulatory roles in the development of myeloid cells.
    J Interferon Cytokine Res. 2002 Jan;22(1):145-52 PMID: 11846985
  45. IFN consensus sequence binding protein/IFN regulatory factor-8 guides bone marrow progenitor cells toward the macrophage lineage.
    J Immunol. 2002 Aug 1;169(3):1261-9 PMID: 12133947
  46. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei.
    Nucleic Acids Res. 1983 Mar 11;11(5):1475-89 PMID: 6828386
  47. Enhancer-like interferon responsive sequences of the human and murine (2'-5') oligoadenylate synthetase gene promoters.
    EMBO J. 1988 May;7(5):1411-9 PMID: 2457496
  48. Interactions of alpha- and gamma-interferon in the transcriptional regulation of the gene encoding a guanylate-binding protein.
    EMBO J. 1989 Jul;8(7):2009-14 PMID: 2507314
  49. The macrophage and B cell-specific transcription factor PU.1 is related to the ets oncogene.
    Cell. 1990 Apr 6;61(1):113-24 PMID: 2180582
  50. An interferon gamma-regulated protein that binds the interferon-inducible enhancer element of major histocompatibility complex class I genes.
    Proc Natl Acad Sci U S A. 1990 May;87(10):3743-7 PMID: 2111015
  51. Human interferon consensus sequence binding protein is a negative regulator of enhancer elements common to interferon-inducible genes.
    J Biol Chem. 1992 Dec 15;267(35):25589-96 PMID: 1460054
  52. Interferon consensus sequence-binding protein, a member of the interferon regulatory factor family, suppresses interferon-induced gene transcription.
    Mol Cell Biol. 1993 Jan;13(1):588-99 PMID: 7678054
  53. Fusion of PDGF receptor beta to a novel ets-like gene, tel, in chronic myelomonocytic leukemia with t(5;12) chromosomal translocation.
    Cell. 1994 Apr 22;77(2):307-16 PMID: 8168137
  54. Functional role of type I and type II interferons in antiviral defense.
    Science. 1994 Jun 24;264(5167):1918-21 PMID: 8009221
  55. Interferon regulatory factor 1 is required for mouse Gbp gene activation by gamma interferon.
    Mol Cell Biol. 1995 Feb;15(2):975-82 PMID: 7823961
  56. The human 2',5'-oligoadenylate synthetase family: interferon-induced proteins with unique enzymatic properties.
    J Interferon Cytokine Res. 1999 Apr;19(4):295-308 PMID: 10334380
  57. Regulation of IFN consensus sequence binding protein expression in murine macrophages.
    J Immunol. 1999 Jun 15;162(12):7417-25 PMID: 10358195
  58. Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation.
    Genes Dev. 1999 Aug 1;13(15):1924-35 PMID: 10444591
  59. Differential expression and distinct functions of IFN regulatory factor 4 and IFN consensus sequence binding protein in macrophages.
    J Immunol. 1999 Sep 1;163(5):2713-22 PMID: 10453013
  60. Both TEL and AML-1 contribute repression domains to the t(12;21) fusion protein.
    Mol Cell Biol. 1999 Oct;19(10):6566-74 PMID: 10490596
  61. The t(12;21) translocation converts AML-1B from an activator to a repressor of transcription.
    Mol Cell Biol. 1996 Apr;16(4):1349-55 PMID: 8657108
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
DOI
10.1128/MCB.22.21.7439-7448.2002
Published
2002-11-00
Pages
7439-48
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC135656
Subset
IM
External Links
PubMed source DOI: 10.1128/MCB.22.21.7439-7448.2002 PMC Full Text View journal details
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