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PMID: 20679482 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

The type I interferon signaling pathway is a target for glucocorticoid inhibition.

Molecular and cellular biology ·Vol. 30 ·No. 19 ·2010-10-00 ·Pages 4564-74

Flammer JR, Dobrovolna J, Kennedy MA, Chinenov Y, Glass CK, Ivashkiv LB, Rogatsky I

Abstract

Type I interferon (IFN) is essential for host defenses against viruses; however, dysregulated IFN signaling is causally linked to autoimmunity, particularly systemic lupus erythematosus. Autoimmune disease treatments rely on glucocorticoids (GCs), which act via the GC receptor (GR) to repress proinflammatory cytokine gene transcription. Conversely, cytokine signaling through cognate Jak/STAT pathways is reportedly unaffected or even stimulated by GR. Unexpectedly, we found that GR dramatically inhibited IFN-stimulated gene (ISG) expression in macrophages. The target of inhibition, the heterotrimeric STAT1-STAT2-IRF9 (ISGF3) transcription complex, utilized the GR cofactor GRIP1/TIF2 as a coactivator. Consequently, GRIP1 knockdown, genetic ablation, or depletion by GC-activated GR attenuated ISGF3 promoter occupancy, preinitiation complex assembly, and ISG expression. Furthermore, this regulatory loop was restricted to cell types such as macrophages expressing the GRIP1 protein at extremely low levels, and pharmacological disruption of the GR-GRIP1 interaction or transient introduction of GRIP1 restored RNA polymerase recruitment to target ISGs and the subsequent IFN response. Thus, type I IFN is a cytokine uniquely controlled by GR at the levels of not only production but also signaling through antagonism with the ISGF3 effector function, revealing a novel facet of the immunosuppressive properties of GCs.

MeSH Terms
3T3 Cells Adaptor Proteins, Signal Transducing/genetics,metabolism Animals Blotting, Western Cell Line Cells, Cultured Dexamethasone/pharmacology Fibroblasts/cytology,drug effects,metabolism Gene Expression/drug effects Glucocorticoids/pharmacology Interferon Type I/pharmacology Interferon-Stimulated Gene Factor 3, alpha Subunit/genetics,metabolism Macrophages/cytology,drug effects,metabolism Mice Mice, Inbred C57BL Nerve Tissue Proteins/genetics,metabolism Protein Binding/drug effects RNA Interference Reverse Transcriptase Polymerase Chain Reaction Signal Transduction/genetics Transcription, Genetic/drug effects
Chemicals
Adaptor Proteins, Signal Transducing Glucocorticoids Grip1 protein, mouse Interferon Type I Interferon-Stimulated Gene Factor 3, alpha Subunit Nerve Tissue Proteins Dexamethasone
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Flammer Jamie R
Graduate Program in Immunology and Microbial Pathogenesis, Weill Cornell Graduate School of Medical Sciences, 1300 York Avenue, New York, New York 10021, USA.
Dobrovolna Jana
Kennedy Megan A
Chinenov Yurii
Glass Christopher K
Ivashkiv Lionel B
Rogatsky Inez
References (61)
61 references, click to expand
  1. Selective phosphorylations of the SRC-3/AIB1 coactivator integrate genomic reponses to multiple cellular signaling pathways.
    Mol Cell. 2004 Sep 24;15(6):937-49 PMID: 15383283
  2. Glucocorticoids and interferon-alpha in the acquired immunodeficiency syndrome.
    J Clin Endocrinol Metab. 1996 Jul;81(7):2601-6 PMID: 8675584
  3. MUC1 oncoprotein stabilizes and activates estrogen receptor alpha.
    Mol Cell. 2006 Jan 20;21(2):295-305 PMID: 16427018
  4. Multiple signal input and output domains of the 160-kilodalton nuclear receptor coactivator proteins.
    Mol Cell Biol. 1999 Sep;19(9):6164-73 PMID: 10454563
  5. Immune interferon in the circulation of patients with autoimmune disease.
    N Engl J Med. 1979 Jul 5;301(1):5-8 PMID: 449915
  6. Localization of tumor necrosis factor alpha in synovial tissues and at the cartilage-pannus junction in patients with rheumatoid arthritis.
    Arthritis Rheum. 1991 Sep;34(9):1125-32 PMID: 1930331
  7. Ringing the interferon alarm: differential regulation of gene expression at the interface between innate and adaptive immunity.
    Curr Opin Immunol. 2003 Feb;15(1):52-8 PMID: 12495733
  8. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus.
    Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2610-5 PMID: 12604793
  9. STATs and gene regulation.
    Science. 1997 Sep 12;277(5332):1630-5 PMID: 9287210
  10. The function of TIF2/GRIP1 in mouse reproduction is distinct from those of SRC-1 and p/CIP.
    Mol Cell Biol. 2002 Aug;22(16):5923-37 PMID: 12138202
  11. Influence of in vivo immunosuppressive drugs on production of lymphokines.
    Transplantation. 1985 Feb;39(2):143-7 PMID: 3918367
  12. Toll-like receptors differentially regulate GPCR kinases and arrestins in primary macrophages.
    Mol Immunol. 2008 Apr;45(8):2312-22 PMID: 18180038
  13. DNA binding site sequence directs glucocorticoid receptor structure and activity.
    Science. 2009 Apr 17;324(5925):407-10 PMID: 19372434
  14. Allosteric regulation of estrogen receptor structure, function, and coactivator recruitment by different estrogen response elements.
    Mol Endocrinol. 2002 Mar;16(3):469-86 PMID: 11875105
  15. Glucocorticoid regulation of human eosinophil gene expression.
    J Steroid Biochem Mol Biol. 2003 Mar;84(4):441-52 PMID: 12732289
  16. Glucocorticoid receptor interacting protein-1 restores glucocorticoid responsiveness in steroid-resistant airway structural cells.
    Am J Respir Cell Mol Biol. 2010 Jan;42(1):9-15 PMID: 19805480
  17. A CBP integrator complex mediates transcriptional activation and AP-1 inhibition by nuclear receptors.
    Cell. 1996 May 3;85(3):403-14 PMID: 8616895
  18. Determinants of cell- and gene-specific transcriptional regulation by the glucocorticoid receptor.
    PLoS Genet. 2007 Jun;3(6):e94 PMID: 17559307
  19. Functional interaction of STAT3 transcription factor with the coactivator NcoA/SRC1a.
    J Biol Chem. 2002 Mar 8;277(10):8004-11 PMID: 11773079
  20. Promoter-dependent synergy between glucocorticoid receptor and Stat5 in the activation of beta-casein gene transcription.
    J Biol Chem. 1997 Aug 15;272(33):20954-60 PMID: 9252424
  21. Molecular determinants of crosstalk between nuclear receptors and toll-like receptors.
    Cell. 2005 Sep 9;122(5):707-21 PMID: 16143103
  22. Antiinflammatory effects of dexamethasone are partly dependent on induction of dual specificity phosphatase 1.
    J Exp Med. 2006 Aug 7;203(8):1883-9 PMID: 16880258
  23. Glucocorticoid signaling: a nongenomic mechanism for T-cell immunosuppression.
    Trends Mol Med. 2007 Apr;13(4):158-63 PMID: 17293163
  24. Stats: transcriptional control and biological impact.
    Nat Rev Mol Cell Biol. 2002 Sep;3(9):651-62 PMID: 12209125
  25. Structure and specificity of nuclear receptor-coactivator interactions.
    Genes Dev. 1998 Nov 1;12(21):3343-56 PMID: 9808622
  26. Cooperation among Stat1, glucocorticoid receptor, and PU.1 in transcriptional activation of the high-affinity Fc gamma receptor I in monocytes.
    J Immunol. 2000 Jun 1;164(11):5689-97 PMID: 10820245
  27. Allosteric effects of DNA on transcriptional regulators.
    Nature. 1998 Apr 30;392(6679):885-8 PMID: 9582068
  28. Factor recruitment and TIF2/GRIP1 corepressor activity at a collagenase-3 response element that mediates regulation by phorbol esters and hormones.
    EMBO J. 2001 Nov 1;20(21):6071-83 PMID: 11689447
  29. GRIP1-associated SET-domain methyltransferase in glucocorticoid receptor target gene expression.
    Proc Natl Acad Sci U S A. 2008 Dec 23;105(51):20185-90 PMID: 19074285
  30. Estradiol repression of tumor necrosis factor-alpha transcription requires estrogen receptor activation function-2 and is enhanced by coactivators.
    Proc Natl Acad Sci U S A. 1999 Dec 21;96(26):15161-6 PMID: 10611355
  31. Microarray analysis of gene expression in lupus.
    Arthritis Res Ther. 2003;5(6):279-87 PMID: 14680503
  32. Cooperation of Stat2 and p300/CBP in signalling induced by interferon-alpha.
    Nature. 1996 Sep 26;383(6598):344-7 PMID: 8848048
  33. DBA/1 mice expressing the human TNF-alpha transgene develop a severe, erosive arthritis: characterization of the cytokine cascade and cellular composition.
    J Immunol. 1997 Sep 15;159(6):2867-76 PMID: 9300710
  34. Glucocorticoids inhibit IRF3 phosphorylation in response to Toll-like receptor-3 and -4 by targeting TBK1 activation.
    J Biol Chem. 2008 May 23;283(21):14277-85 PMID: 18356163
  35. Minireview: latest perspectives on antiinflammatory actions of glucocorticoids.
    Mol Endocrinol. 2009 Mar;23(3):281-91 PMID: 19095768
  36. Destabilization of binding to cofactors and SCFMet30 is the rate-limiting regulatory step in degradation of polyubiquitinated Met4.
    Mol Cell. 2006 Dec 8;24(5):689-699 PMID: 17157252
  37. Nuclear hormone receptor coregulator GRIP1 suppresses, whereas SRC1A and p/CIP coactivate, by domain-specific binding of MyoD.
    J Biol Chem. 2005 Feb 4;280(5):3129-37 PMID: 15563453
  38. Crystal structure of the glucocorticoid receptor ligand binding domain reveals a novel mode of receptor dimerization and coactivator recognition.
    Cell. 2002 Jul 12;110(1):93-105 PMID: 12151000
  39. Interferon regulatory factor subcellular localization is determined by a bipartite nuclear localization signal in the DNA-binding domain and interaction with cytoplasmic retention factors.
    Proc Natl Acad Sci U S A. 2000 Jun 20;97(13):7278-83 PMID: 10860992
  40. Review of the in vivo functions of the p160 steroid receptor coactivator family.
    Mol Endocrinol. 2003 Sep;17(9):1681-92 PMID: 12805412
  41. The coactivator-associated arginine methyltransferase is necessary for muscle differentiation: CARM1 coactivates myocyte enhancer factor-2.
    J Biol Chem. 2002 Feb 8;277(6):4324-33 PMID: 11713257
  42. A pivotal role for the natural interferon alpha-producing cells (plasmacytoid dendritic cells) in the pathogenesis of lupus.
    J Exp Med. 2001 Dec 17;194(12):F59-63 PMID: 11748288
  43. The GRIP1:IRF3 interaction as a target for glucocorticoid receptor-mediated immunosuppression.
    EMBO J. 2006 Jan 11;25(1):108-17 PMID: 16362036
  44. Role of metazoan mediator proteins in interferon-responsive transcription.
    Mol Cell Biol. 2003 Jan;23(2):620-8 PMID: 12509459
  45. STAT3-dependent enhanceosome assembly and disassembly: synergy with GR for full transcriptional increase of the alpha 2-macroglobulin gene.
    Genes Dev. 2003 Oct 15;17(20):2564-77 PMID: 14522952
  46. Alternate surfaces of transcriptional coregulator GRIP1 function in different glucocorticoid receptor activation and repression contexts.
    Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):16701-6 PMID: 12481024
  47. Serum interferon levels in patients with systemic lupus erythematosus.
    Arthritis Rheum. 1982 Apr;25(4):401-6 PMID: 6176248
  48. Immediate mediators of the inflammatory response are poised for gene activation through RNA polymerase II stalling.
    Proc Natl Acad Sci U S A. 2009 Oct 27;106(43):18207-12 PMID: 19820169
  49. A novel mitogen-activated protein kinase phosphatase-1 and glucocorticoid receptor (GR) interacting protein-1-dependent combinatorial mechanism of gene transrepression by GR.
    Mol Endocrinol. 2009 Jan;23(1):86-99 PMID: 18945810
  50. Rapid estrogen-induced phosphorylation of the SRC-3 coactivator occurs in an extranuclear complex containing estrogen receptor.
    Mol Cell Biol. 2005 Sep;25(18):8273-84 PMID: 16135815
  51. Transcriptional activation by STAT6 requires the direct interaction with NCoA-1.
    J Biol Chem. 2001 Dec 7;276(49):45713-21 PMID: 11574547
  52. TPL-2 negatively regulates interferon-beta production in macrophages and myeloid dendritic cells.
    J Exp Med. 2009 Aug 31;206(9):1863-71 PMID: 19667062
  53. Functional interactions between Stat5 and the glucocorticoid receptor.
    Nature. 1996 Oct 24;383(6602):726-8 PMID: 8878484
  54. Inhibition of Th1 immune response by glucocorticoids: dexamethasone selectively inhibits IL-12-induced Stat4 phosphorylation in T lymphocytes.
    J Immunol. 2000 Feb 15;164(4):1768-74 PMID: 10657623
  55. Crosstalk between the interleukin-6 (IL-6)-JAK-STAT and the glucocorticoid-nuclear receptor pathway: synergistic activation of IL-6 response element by IL-6 and glucocorticoid.
    J Endocrinol. 1998 Nov;159(2):323-30 PMID: 9795374
  56. Activation of type I interferon system in systemic lupus erythematosus correlates with disease activity but not with antiretroviral antibodies.
    Lupus. 2000;9(9):664-71 PMID: 11199920
  57. Systemic lupus erythematosus: presence in human serum of an unusual acid-labile leukocyte interferon.
    Science. 1982 Apr 23;216(4544):429-31 PMID: 6176024
  58. Chaperoning of glucocorticoid receptors.
    Handb Exp Pharmacol. 2006;(172):111-38 PMID: 16610357
  59. The interferon antiviral response: from viral invasion to evasion.
    Curr Opin Infect Dis. 2002 Jun;15(3):259-67 PMID: 12015460
  60. Inhibition of IL-2-induced Jak-STAT signaling by glucocorticoids.
    Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9573-8 PMID: 10920190
  61. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood.
    J Exp Med. 2003 Mar 17;197(6):711-23 PMID: 12642603
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
1098-5549
Published
2010-10-00
Epub
2010-00-02
Pages
4564-74
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC2950533
Subset
IM
Grants
NIAID NIH HHS · R01 AI046712-11 · United States
NIAID NIH HHS · R01 AI046712 · United States
NIAID NIH HHS · R01 AI059636-04 · United States
NIAMS NIH HHS · T32 AR007517 · United States
NIAMS NIH HHS · R01 AR050401-06A2 · United States
NIAID NIH HHS · R01 AI046712-10 · United States
NIAID NIH HHS · R01 AI068820 · United States
NIAID NIH HHS · R01 AI059636-03 · United States
NIAID NIH HHS · R01 AI059636 · United States
NIAMS NIH HHS · T32 AR07517 · United States
NIAMS NIH HHS · R01 AR050401 · United States
NIAMS NIH HHS · R01 AR050401-05 · United States
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