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PMID: 11413190 Published · ppublish English Journal Article

Two waves of nuclear factor kappaB recruitment to target promoters.

The Journal of experimental medicine ·Vol. 193 ·No. 12 ·2001-06-18 ·Pages 1351-9

Saccani S, Pantano S, Natoli G

Abstract

Proinflammatory stimuli induce the rapid and transient translocation of nuclear factor (NF)-kappaB to the nucleus, where it activates transcription from several genes, including those encoding inflammatory cytokines and chemokines, adhesion molecules, and cytoprotective proteins. Using chromatin immunoprecipitation, we show that after an acute stimulation two distinct waves of NF-kappaB recruitment to target promoters occur: a fast recruitment to constitutively and immediately accessible (CIA) promoters and a late recruitment to promoters requiring stimulus-dependent modifications in chromatin structure to make NF-kappaB sites accessible (promoters with regulated and late accessibility [RLA]). Our results suggest that a mechanism of specificity in NF-kappaB-dependent transcriptional responses relies on the ability of individual stimuli to make RLA promoters accessible to NF-kappaB before its rapid extrusion from the nucleus.

MeSH Terms
Acetylation Animals Binding Sites Cell Line Cell Nucleus/metabolism Chromatin/metabolism DNA-Binding Proteins/genetics Histones/metabolism I-kappa B Proteins Kinetics Lipopolysaccharides/pharmacology Macrophages/drug effects,metabolism Mice NF-KappaB Inhibitor alpha NF-kappa B/metabolism Precipitin Tests Promoter Regions, Genetic Protein Transport
Chemicals
Chromatin DNA-Binding Proteins Histones I-kappa B Proteins Lipopolysaccharides NF-kappa B Nfkbia protein, mouse NF-KappaB Inhibitor alpha
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Saccani S
Institute for Research in Biomedicine, CH6501 Bellinzona, Switzerland.
Pantano S
Natoli G
References (47)
47 references, click to expand
  1. TNF regulates the in vivo occupancy of both distal and proximal regulatory regions of the MCP-1/JE gene.
    Immunity. 1996 May;4(5):455-69 PMID: 8630731
  2. Rapid and selective remodeling of a positioned nucleosome during the induction of IL-12 p40 transcription.
    Immunity. 1999 Dec;11(6):665-75 PMID: 10626889
  3. Role of unphosphorylated, newly synthesized I kappa B beta in persistent activation of NF-kappa B.
    Mol Cell Biol. 1996 Oct;16(10):5444-9 PMID: 8816457
  4. I kappa B epsilon, a novel member of the I kappa B family, controls RelA and cRel NF-kappa B activity.
    EMBO J. 1997 Mar 17;16(6):1413-26 PMID: 9135156
  5. Identification and characterization of an IkappaB kinase.
    Cell. 1997 Jul 25;90(2):373-83 PMID: 9244310
  6. A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB.
    Nature. 1997 Aug 7;388(6642):548-54 PMID: 9252186
  7. Histone acetylation in chromatin structure and transcription.
    Nature. 1997 Sep 25;389(6649):349-52 PMID: 9311776
  8. The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation.
    Cell. 1997 Oct 17;91(2):243-52 PMID: 9346241
  9. The language of covalent histone modifications.
    Nature. 2000 Jan 6;403(6765):41-5 PMID: 10638745
  10. The transcription factor NF-kappaB: control of oncogenesis and cancer therapy resistance.
    Biochim Biophys Acta. 2000 Mar 27;1470(2):M55-62 PMID: 10722927
  11. The IKK complex: an integrator of all signals that activate NF-kappaB?
    Trends Cell Biol. 2000 Apr;10(4):129-33 PMID: 10740266
  12. Acetylation and chromosomal functions.
    Curr Opin Cell Biol. 2000 Jun;12(3):326-33 PMID: 10801466
  13. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity.
    Annu Rev Immunol. 2000;18:621-63 PMID: 10837071
  14. Selective requirement for c-Rel during IL-12 P40 gene induction in macrophages.
    Proc Natl Acad Sci U S A. 2000 Nov 7;97(23):12705-10 PMID: 11058167
  15. Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of I kappa B alpha: a mechanism for NF-kappa B activation.
    Mol Cell Biol. 1993 Jun;13(6):3301-10 PMID: 8497253
  16. Rapid proteolysis of I kappa B-alpha is necessary for activation of transcription factor NF-kappa B.
    Nature. 1993 Sep 9;365(6442):182-5 PMID: 8371761
  17. I kappa B-beta regulates the persistent response in a biphasic activation of NF-kappa B.
    Cell. 1995 Feb 24;80(4):573-82 PMID: 7867065
  18. Inducible nuclear expression of newly synthesized I kappa B alpha negatively regulates DNA-binding and transcriptional activities of NF-kappa B.
    Mol Cell Biol. 1995 May;15(5):2689-96 PMID: 7739549
  19. Site-specific phosphorylation of IkappaBalpha by a novel ubiquitination-dependent protein kinase activity.
    Cell. 1996 Mar 22;84(6):853-62 PMID: 8601309
  20. What does 'chromatin remodeling' mean?
    Trends Biochem Sci. 2000 Nov;25(11):548-55 PMID: 11084367
  21. Ordered recruitment of chromatin modifying and general transcription factors to the IFN-beta promoter.
    Cell. 2000 Nov 10;103(4):667-78 PMID: 11106736
  22. Regulation of IL-6 and IL-8 expression in rheumatoid arthritis synovial fibroblasts: the dominant role for NF-kappa B but not C/EBP beta or c-Jun.
    J Immunol. 2000 Dec 15;165(12):7199-206 PMID: 11120852
  23. Nucleosome remodeling at the IL-12 p40 promoter is a TLR-dependent, Rel-independent event.
    Nat Immunol. 2001 Jan;2(1):51-7 PMID: 11135578
  24. I kappa B: a specific inhibitor of the NF-kappa B transcription factor.
    Science. 1988 Oct 28;242(4878):540-6 PMID: 3140380
  25. Purified human I kappa B can rapidly dissociate the complex of the NF-kappa B transcription factor with its cognate DNA.
    Cell. 1990 Apr 20;61(2):255-65 PMID: 2184941
  26. Characterization of an immediate-early gene induced in adherent monocytes that encodes I kappa B-like activity.
    Cell. 1991 Jun 28;65(7):1281-9 PMID: 1829648
  27. Rel-associated pp40: an inhibitor of the rel family of transcription factors.
    Science. 1991 Sep 13;253(5025):1268-71 PMID: 1891714
  28. The ankyrin repeat domains of the NF-kappa B precursor p105 and the protooncogene bcl-3 act as specific inhibitors of NF-kappa B DNA binding.
    Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2489-93 PMID: 1532257
  29. I kappa B interacts with the nuclear localization sequences of the subunits of NF-kappa B: a mechanism for cytoplasmic retention.
    Genes Dev. 1992 Oct;6(10):1899-913 PMID: 1340770
  30. Chromatin condensation: does histone H1 dephosphorylation play a role?
    Trends Biochem Sci. 1992 Mar;17(3):93-8 PMID: 1412698
  31. I kappa B/MAD-3 masks the nuclear localization signal of NF-kappa B p65 and requires the transactivation domain to inhibit NF-kappa B p65 DNA binding.
    Mol Biol Cell. 1992 Dec;3(12):1339-52 PMID: 1493333
  32. Nuclear uptake control of NF-kappa B by MAD-3, an I kappa B protein present in the nucleus.
    EMBO J. 1993 Jan;12(1):201-11 PMID: 7679069
  33. NF-kappa B and Rel: participants in a multiform transcriptional regulatory system.
    Int Rev Cytol. 1993;143:1-62 PMID: 8449662
  34. IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation.
    Science. 1997 Oct 31;278(5339):860-6 PMID: 9346484
  35. IkappaB kinase-beta: NF-kappaB activation and complex formation with IkappaB kinase-alpha and NIK.
    Science. 1997 Oct 31;278(5339):866-9 PMID: 9346485
  36. Tumor necrosis factor alpha and interleukin-1beta regulate the murine manganese superoxide dismutase gene through a complex intronic enhancer involving C/EBP-beta and NF-kappaB.
    Mol Cell Biol. 1997 Dec;17(12):6970-81 PMID: 9372929
  37. Prolonged glucocorticoid exposure dephosphorylates histone H1 and inactivates the MMTV promoter.
    EMBO J. 1998 Mar 2;17(5):1454-66 PMID: 9482742
  38. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses.
    Annu Rev Immunol. 1998;16:225-60 PMID: 9597130
  39. Recruitment of CBP/p300 by the IFN beta enhanceosome is required for synergistic activation of transcription.
    Mol Cell. 1998 Jan;1(2):277-87 PMID: 9659924
  40. Identification of the receptor component of the IkappaBalpha-ubiquitin ligase.
    Nature. 1998 Dec 10;396(6711):590-4 PMID: 9859996
  41. A ubiquitin ligase complex essential for the NF-kappaB, Wnt/Wingless, and Hedgehog signaling pathways.
    Genes Dev. 1999 Mar 1;13(5):505-10 PMID: 10072378
  42. A critical role for the RelA subunit of nuclear factor kappaB in regulation of multiple immune-response genes and in Fas-induced cell death.
    J Exp Med. 1999 Mar 15;189(6):999-1004 PMID: 10075983
  43. Activation of the human RANTES gene promoter in a macrophage cell line by lipopolysaccharide is dependent on stress-activated protein kinases and the IkappaB kinase cascade: implications for exacerbation of allergic inflammation by environmental pollutants.
    Clin Immunol. 1999 Mar;90(3):287-301 PMID: 10075858
  44. Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle- and developmentally regulated promoter.
    Cell. 1999 Apr 30;97(3):299-311 PMID: 10319811
  45. Mapping DNA interaction sites of chromosomal proteins using immunoprecipitation and polymerase chain reaction.
    Methods Enzymol. 1999;304:399-414 PMID: 10372373
  46. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome.
    Cell. 1999 Aug 6;98(3):285-94 PMID: 10458604
  47. The NF-kappa B and I kappa B proteins: new discoveries and insights.
    Annu Rev Immunol. 1996;14:649-83 PMID: 8717528
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
DOI
10.1084/jem.193.12.1351
Published
2001-06-18
Pages
1351-9
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2193297
Subset
IM
External Links
PubMed source DOI: 10.1084/jem.193.12.1351 PMC Full Text View journal details
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