Home LiteratureArticle Details
PMID: 8441422 Published · ppublish English Journal Article

The NFAT-1 DNA binding complex in activated T cells contains Fra-1 and JunB.

Molecular and cellular biology ·Vol. 13 ·No. 3 ·1993-03-00 ·Pages 1911-9

Boise LH, Petryniak B, Mao X, June CH, Wang CY, Lindsten T, Bravo R, Kovary K, Leiden JM, Thompson CB

Abstract

Activation of T cells induces transcription of the interleukin-2 (IL-2) gene. IL-2 expression is regulated through the binding of transcription factors to multiple sites within the IL-2 enhancer. One such cis-acting element within the IL-2 enhancer is the NFAT-1 (nuclear factor of activated T cells) binding site. NFAT-1 binding activity is absent in resting cells but is induced upon T-cell activation. The induction of NFAT-1 binding activity can be inhibited by cyclosporin A, potentially accounting for the ability of cyclosporin A to inhibit IL-2 production by T cells. We have previously reported that the NFAT-1 binding complex is composed of at least two proteins and that the 5' portion of the NFAT-1 sequence acts as a binding site for one or more proteins from the Ets family of transcription factors. We now report that the 3' portion of the NFAT-1 sequence contains a variant AP-1 binding site. NFAT-1 binding can be specifically inhibited by oligonucleotides containing a consensus AP-1 site. Moreover, mutation of the AP-1 site at the 3' end of the NFAT-1 sequence inhibits both NFAT-1 binding and the ability of the NFAT-1 binding site to activate expression from a reporter plasmid upon T-cell activation. Since AP-1 sites bind dimeric protein complexes composed of individual members of the Fos and Jun families of transcription factors, we used antibodies specific for individual Fos and Jun family members to determine whether they are present in the NFAT-1 binding complex. These experiments demonstrated that the NFAT-1 binding complex contains JunB and Fra-1 proteins. Northern (RNA) blot analyses demonstrate that both fra-1 and junB mRNAs are induced upon T-cell activation, although fra-1 mRNA is present even in quiescent T cells. Of interest, junB is not expressed in quiescent T cells, and it is induced with kinetics that are similar to those for the induction of IL-2 mRNA expression. Taken together, these results suggested that the JunB-Fra-1 heterodimer is the inducible nuclear component of the NFAT-1 binding activity and that JunB expression regulates the formation of the heterodimer. In addition, these data indicated that specific heterodimers of Fos and Jun family members may have selective roles in the induction of transcription during cellular activation.

Related Genes
MeSH Terms
Enhancer Elements, Genetic/genetics Interleukin-2/metabolism Lymphocyte Activation Macromolecular Substances Proto-Oncogene Proteins c-jun/metabolism Recombinant Proteins/biosynthesis T-Lymphocytes/metabolism Transcription, Genetic beta-Galactosidase/genetics
Chemicals
Interleukin-2 Macromolecular Substances Proto-Oncogene Proteins c-jun Recombinant Proteins beta-Galactosidase
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Boise L H
Howard Hughes Medical Institute, University of Michigan Medical Center, Ann Arbor 48109.
Petryniak B
Mao X
June C H
Wang C Y
Lindsten T
Bravo R
Kovary K
Leiden J M
Thompson C B
References (41)
41 references, click to expand
  1. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  2. A novel modulator domain of Ets transcription factors.
    Genes Dev. 1992 Jun;6(6):965-74 PMID: 1592263
  3. Expression of the c-myb proto-oncogene during cellular proliferation.
    Nature. 1986 Jan 30-Feb 5;319(6052):374-80 PMID: 3511387
  4. Regulation of human interleukin-2 gene: functional DNA sequences in the 5' flanking region for the gene expression in activated T lymphocytes.
    Cell. 1986 Aug 1;46(3):401-5 PMID: 3015413
  5. A 275 basepair fragment at the 5' end of the interleukin 2 gene enhances expression from a heterologous promoter in response to signals from the T cell antigen receptor.
    J Exp Med. 1987 Feb 1;165(2):395-407 PMID: 3102668
  6. Human proto-oncogene c-jun encodes a DNA binding protein with structural and functional properties of transcription factor AP-1.
    Science. 1987 Dec 4;238(4832):1386-92 PMID: 2825349
  7. A gene activated by growth factors is related to the oncogene v-jun.
    Proc Natl Acad Sci U S A. 1988 Mar;85(5):1487-91 PMID: 3422745
  8. Characterization of antigen receptor response elements within the interleukin-2 enhancer.
    Mol Cell Biol. 1988 Apr;8(4):1715-24 PMID: 3260003
  9. fra-1: a serum-inducible, cellular immediate-early gene that encodes a fos-related antigen.
    Mol Cell Biol. 1988 May;8(5):2063-9 PMID: 3133553
  10. HTLV-1 transactivator induces interleukin-2 receptor expression through an NF-kappa B-like factor.
    Nature. 1988 Jun 23;333(6175):776-8 PMID: 2838755
  11. Identification of a putative regulator of early T cell activation genes.
    Science. 1988 Jul 8;241(4862):202-5 PMID: 3260404
  12. Interaction of murine ets-1 with GGA-binding sites establishes the ETS domain as a new DNA-binding motif.
    Genes Dev. 1992 Jun;6(6):975-90 PMID: 1592264
  13. Existence of different Fos/Jun complexes during the G0-to-G1 transition and during exponential growth in mouse fibroblasts: differential role of Fos proteins.
    Mol Cell Biol. 1992 Nov;12(11):5015-23 PMID: 1406676
  14. Transcriptional activation of c-jun during the G0/G1 transition in mouse fibroblasts.
    Nature. 1988 Aug 11;334(6182):535-7 PMID: 3136397
  15. jun-D: a third member of the jun gene family.
    Proc Natl Acad Sci U S A. 1989 Mar;86(5):1500-3 PMID: 2493644
  16. Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway.
    Science. 1989 Apr 21;244(4902):339-43 PMID: 2540528
  17. Ubiquitous and lymphocyte-specific factors are involved in the induction of the mouse interleukin 2 gene in T lymphocytes.
    EMBO J. 1989 Feb;8(2):465-73 PMID: 2542017
  18. The product of a novel growth factor activated gene, fos B, interacts with JUN proteins enhancing their DNA binding activity.
    EMBO J. 1989 Mar;8(3):805-13 PMID: 2498083
  19. Evidence for the involvement of three distinct signals in the induction of IL-2 gene expression in human T lymphocytes.
    J Immunol. 1989 Jul 1;143(1):153-61 PMID: 2543699
  20. Characterization of junD: a new member of the jun proto-oncogene family.
    EMBO J. 1989 May;8(5):1433-9 PMID: 2504580
  21. A T-cell-specific transcriptional enhancer element 3' of C alpha in the human T-cell receptor alpha locus.
    Proc Natl Acad Sci U S A. 1989 Sep;86(17):6714-8 PMID: 2788889
  22. Cyclosporin A specifically inhibits function of nuclear proteins involved in T cell activation.
    Science. 1989 Dec 22;246(4937):1617-20 PMID: 2595372
  23. Isolation of human fos-related genes and their expression during monocyte-macrophage differentiation.
    Oncogene. 1990 Mar;5(3):249-55 PMID: 2107490
  24. The collagenase gene promoter contains a TPA and oncogene-responsive unit encompassing the PEA3 and AP-1 binding sites.
    EMBO J. 1990 Jul;9(7):2241-6 PMID: 2162765
  25. The c-ets proto-oncogenes encode transcription factors that cooperate with c-Fos and c-Jun for transcriptional activation.
    Nature. 1990 Jul 12;346(6280):191-3 PMID: 2114554
  26. Cyclosporin A suppresses the expression of the interleukin 2 gene by inhibiting the binding of lymphocyte-specific factors to the IL-2 enhancer.
    EMBO J. 1990 Aug;9(8):2529-36 PMID: 2369902
  27. Sequence-specific binding of human Ets-1 to the T cell receptor alpha gene enhancer.
    Science. 1990 Nov 9;250(4982):814-8 PMID: 2237431
  28. Single cell assay of a transcription factor reveals a threshold in transcription activated by signals emanating from the T-cell antigen receptor.
    Genes Dev. 1990 Oct;4(10):1823-34 PMID: 2123468
  29. Nuclear proto-oncogenes fos and jun.
    Annu Rev Cell Biol. 1990;6:539-57 PMID: 2125830
  30. Expression of different Jun and Fos proteins during the G0-to-G1 transition in mouse fibroblasts: in vitro and in vivo associations.
    Mol Cell Biol. 1991 May;11(5):2451-9 PMID: 1901942
  31. c-JUN, JUN B, and JUN D differ in their binding affinities to AP-1 and CRE consensus sequences: effect of FOS proteins.
    Oncogene. 1991 Apr;6(4):533-42 PMID: 1827665
  32. The jun and fos protein families are both required for cell cycle progression in fibroblasts.
    Mol Cell Biol. 1991 Sep;11(9):4466-72 PMID: 1908553
  33. Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A.
    Nature. 1991 Aug 29;352(6338):803-7 PMID: 1715516
  34. Characterization of a protein that regulates the DNA-binding activity of NF-AT, the nuclear factor of activated T cells.
    Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11431-4 PMID: 1722332
  35. A T cell nuclear factor resembling NF-AT binds to an NF-kappa B site and to the conserved lymphokine promoter sequence "cytokine-1".
    J Biol Chem. 1992 Jan 25;267(3):1864-71 PMID: 1730723
  36. Analysis of the AP-1 sites in the IL-2 promoter.
    J Immunol. 1992 Feb 15;148(4):1240-50 PMID: 1737937
  37. cis-acting sequences required for inducible interleukin-2 enhancer function bind a novel Ets-related protein, Elf-1.
    Mol Cell Biol. 1992 Mar;12(3):1043-53 PMID: 1545787
  38. Induction of junB expression, but not c-jun, by granulocyte colony-stimulating factor or macrophage colony-stimulating factor in the proliferative response of human myeloid leukemia cells.
    J Clin Invest. 1992 May;89(5):1657-61 PMID: 1373742
  39. Evolutionarily conserved Ets family members display distinct DNA binding specificities.
    J Exp Med. 1992 May 1;175(5):1391-9 PMID: 1569404
  40. Nuclear factor of activated T cells contains Fos and Jun.
    Nature. 1992 Apr 30;356(6372):801-4 PMID: 1533441
  41. Sequential expression of genes involved in human T lymphocyte growth and differentiation.
    J Exp Med. 1985 Jun 1;161(6):1593-8 PMID: 2989408
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1993-03-00
Pages
1911-9
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC359505
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com