Home LiteratureArticle Details
PMID: 9234715 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Multiple control elements mediate activation of the murine and human interleukin 12 p40 promoters: evidence of functional synergy between C/EBP and Rel proteins.

Molecular and cellular biology ·Vol. 17 ·No. 8 ·1997-08-00 ·Pages 4572-88

Plevy SE, Gemberling JH, Hsu S, Dorner AJ, Smale ST

Abstract

Interleukin 12 (IL-12) is a heterodimeric cytokine whose activity is critical for T-helper 1 responses. The gene for the IL-12 p40 subunit is expressed in macrophages following induction by bacterial products, and its expression is augmented by gamma interferon. In this study, we performed a functional analysis of the murine and human p40 promoters in the murine macrophage cell line RAW 264.7. Transcription from the murine p40 promoter was strongly induced by lipopolysaccharide and heat-killed Listeria monocytogenes (HKLM), but promoter activity was not enhanced by gamma interferon. Multiple cis-acting elements involved in activated transcription were identified through an extensive mutant analysis. The most critical element, whose activity is conserved in mice and humans, is located between positions -96 and -88 relative to the murine transcription start site. This element exhibits functional synergy with a previously described NF-kappaB half-site which interacts with Rel proteins. DNase I footprinting and electrophoretic mobility shift assays demonstrated that C/EBP proteins interact with the critical element, but in nuclear extracts, cooperative binding of C/EBP and Rel proteins to their respective sites was not observed. Interestingly, promoter activity was induced by HKLM in the presence of cycloheximide, consistent with induction by posttranslational mechanisms. The results suggest that C/EBP and Rel proteins play important roles in the activation of IL-12 p40 transcription by bacteria. However, many complex interactions will need to be clarified to fully understand p40 regulation.

MeSH Terms
Animals Base Sequence Binding Sites CCAAT-Enhancer-Binding Protein-beta CCAAT-Enhancer-Binding Proteins Cell Line Cycloheximide/pharmacology DNA Footprinting DNA-Binding Proteins/metabolism Humans Interferon-gamma/pharmacology Interleukin-12/genetics Lipopolysaccharides/pharmacology Listeria monocytogenes/immunology Macrophages Mice Molecular Sequence Data Mutation NF-kappa B/metabolism Nuclear Proteins/metabolism Promoter Regions, Genetic/genetics Protein Synthesis Inhibitors/pharmacology Proto-Oncogene Proteins/metabolism Proto-Oncogene Proteins c-rel Recombinant Fusion Proteins Recombinant Proteins Repressor Proteins/metabolism Transcription Factors/metabolism Transcriptional Activation/genetics
Chemicals
CCAAT-Enhancer-Binding Protein-beta CCAAT-Enhancer-Binding Proteins DNA-Binding Proteins Lipopolysaccharides NF-kappa B Nuclear Proteins Protein Synthesis Inhibitors Proto-Oncogene Proteins Proto-Oncogene Proteins c-rel Recombinant Fusion Proteins Recombinant Proteins Repressor Proteins Transcription Factors Interleukin-12 Interferon-gamma Cycloheximide
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Plevy S E
Howard Hughes Medical Institute and Department of Microbiology and Immunology, UCLA School of Medicine, Los Angeles, California 90095-1662, USA.
Gemberling J H
Hsu S
Dorner A J
Smale S T
References (66)
66 references, click to expand
  1. Restoration of HIV-specific cell-mediated immune responses by interleukin-12 in vitro.
    Science. 1993 Dec 10;262(5140):1721-4 PMID: 7903123
  2. The adjuvant effect of interleukin-12 in a vaccine against Leishmania major.
    Science. 1994 Jan 14;263(5144):235-7 PMID: 7904381
  3. Functional and physical associations between NF-kappa B and C/EBP family members: a Rel domain-bZIP interaction.
    Mol Cell Biol. 1993 Jul;13(7):3964-74 PMID: 8321203
  4. Impaired interleukin 12 production in human immunodeficiency virus-infected patients.
    J Exp Med. 1994 Apr 1;179(4):1361-6 PMID: 7908324
  5. Interleukin 12 at the site of disease in tuberculosis.
    J Clin Invest. 1994 Apr;93(4):1733-9 PMID: 7909320
  6. An NFIL-6 sequence near the transcriptional initiation site is necessary for the lipopolysaccharide induction of murine interleukin-1 beta.
    DNA Cell Biol. 1994 Jun;13(6):561-9 PMID: 8024700
  7. Parasite-induced IL-12 stimulates early IFN-gamma synthesis and resistance during acute infection with Toxoplasma gondii.
    J Immunol. 1994 Sep 15;153(6):2533-43 PMID: 7915739
  8. C/EBP beta regulation of the tumor necrosis factor alpha gene.
    J Clin Invest. 1994 Oct;94(4):1449-55 PMID: 7929820
  9. Constitutive nuclear NF-kappa B in cells of the monocyte lineage.
    Biochem J. 1994 Nov 15;304 ( Pt 1):87-94 PMID: 7998962
  10. Targeted disruption of the NF-IL6 gene discloses its essential role in bacteria killing and tumor cytotoxicity by macrophages.
    Cell. 1995 Jan 27;80(2):353-61 PMID: 7530603
  11. Interaction of the COOH-terminal transactivation domain of p65 NF-kappa B with TATA-binding protein, transcription factor IIB, and coactivators.
    J Biol Chem. 1995 Mar 31;270(13):7219-26 PMID: 7706261
  12. Cytokine patterns at the site of mycobacterial infection.
    Immunobiology. 1994 Oct;191(4-5):378-87 PMID: 7713551
  13. Lymphoproliferative disorder and imbalanced T-helper response in C/EBP beta-deficient mice.
    EMBO J. 1995 May 1;14(9):1932-41 PMID: 7744000
  14. Early responses of trans-activating factors to growth hormone in preadipocytes: differential regulation of CCAAT enhancer-binding protein-beta (C/EBP beta) and C/EBP delta.
    Mol Endocrinol. 1995 Jan;9(1):108-20 PMID: 7760844
  15. Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity.
    Annu Rev Immunol. 1995;13:251-76 PMID: 7612223
  16. Regulation of interleukin 12 p40 expression through an NF-kappa B half-site.
    Mol Cell Biol. 1995 Oct;15(10):5258-67 PMID: 7565674
  17. CCAAT/enhancer binding protein-alpha amino acid motifs with dual TBP and TFIIB binding ability co-operate to activate transcription in both yeast and mammalian cells.
    EMBO J. 1995 Sep 1;14(17):4318-28 PMID: 7556073
  18. IL-1 beta is required for IL-12 to induce production of IFN-gamma by NK cells. A role for IL-1 beta in the T cell-independent mechanism of resistance against intracellular pathogens.
    J Immunol. 1995 Nov 1;155(9):4347-54 PMID: 7594594
  19. The C/EBP family of transcription factors.
    Immunobiology. 1995 Jul;193(2-4):171-85 PMID: 8530141
  20. Differential utilization of IFN-gamma-responsive elements in two maturationally distinct macrophage cell lines.
    J Immunol. 1995 Nov 15;155(10):4933-8 PMID: 7594498
  21. The interleukin 12 p40 gene promoter is primed by interferon gamma in monocytic cells.
    J Exp Med. 1996 Jan 1;183(1):147-57 PMID: 8551218
  22. Regulation of murine macrophage IL-12 production. Activation of macrophages in vivo, restimulation in vitro, and modulation by other cytokines.
    J Immunol. 1996 Feb 1;156(3):1196-206 PMID: 8557998
  23. Regulation of bioactive IL-12 production in lipopolysaccharide-stimulated human monocytes is determined by the expression of the p35 subunit.
    J Immunol. 1996 Feb 1;156(3):1207-12 PMID: 8557999
  24. Progesterone inhibits inducible nitric oxide synthase gene expression and nitric oxide production in murine macrophages.
    J Leukoc Biol. 1996 Mar;59(3):442-50 PMID: 8604025
  25. Evidence for posttranscriptional regulation of C/EBPalpha and C/EBPbeta isoform expression during the lipopolysaccharide-mediated acute-phase response.
    Mol Cell Biol. 1996 May;16(5):2295-306 PMID: 8628296
  26. Molecular analysis of decreased interleukin-12 production in persons infected with human immunodeficiency virus.
    J Infect Dis. 1996 Jul;174(1):46-53 PMID: 8656012
  27. Neutralization of IL-12 decreases resistance to Listeria in SCID and C.B-17 mice. Reversal by IFN-gamma.
    J Immunol. 1994 Feb 15;152(4):1883-7 PMID: 7907107
  28. Differential regulation of interleukin-12 (IL-12), tumor necrosis factor alpha, and IL-1 beta production in human myeloid leukemia cell lines and peripheral blood mononuclear cells.
    Blood. 1994 Apr 1;83(7):1847-55 PMID: 7908232
  29. Analysis of interferon mRNA in human fibroblast cells induced to produce interferon.
    Proc Natl Acad Sci U S A. 1981 Dec;78(12):7426-30 PMID: 6174973
  30. 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
  31. Oligonucleotide that binds nuclear factor NF-kappa B acts as a lymphoid-specific and inducible enhancer element.
    Proc Natl Acad Sci U S A. 1988 Mar;85(5):1482-6 PMID: 3125549
  32. The "initiator" as a transcription control element.
    Cell. 1989 Apr 7;57(1):103-13 PMID: 2467742
  33. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties.
    Annu Rev Immunol. 1989;7:145-73 PMID: 2523712
  34. Activation of HIV gene expression during monocyte differentiation by induction of NF-kappa B.
    Nature. 1989 May 4;339(6219):70-3 PMID: 2654643
  35. Site-directed mutagenesis by overlap extension using the polymerase chain reaction.
    Gene. 1989 Apr 15;77(1):51-9 PMID: 2744487
  36. Scissors-grip model for DNA recognition by a family of leucine zipper proteins.
    Science. 1989 Nov 17;246(4932):911-6 PMID: 2683088
  37. Luciferase reporter gene vectors for analysis of promoters and enhancers.
    Biotechniques. 1988 May;6(5):454-8 PMID: 2908509
  38. Cloning of cDNA for natural killer cell stimulatory factor, a heterodimeric cytokine with multiple biologic effects on T and natural killer cells.
    J Immunol. 1991 May 1;146(9):3074-81 PMID: 1673147
  39. Superinduction of IL-2 gene transcription in the presence of cycloheximide.
    J Immunol. 1991 Jun 1;146(11):3857-63 PMID: 2033254
  40. Coexpression of two distinct genes is required to generate secreted bioactive cytotoxic lymphocyte maturation factor.
    Proc Natl Acad Sci U S A. 1991 May 15;88(10):4143-7 PMID: 1674604
  41. Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells.
    Genes Dev. 1991 Sep;5(9):1538-52 PMID: 1840554
  42. cAMP stimulates the C/EBP-related transcription factor rNFIL-6 to trans-locate to the nucleus and induce c-fos transcription.
    Genes Dev. 1991 Oct;5(10):1754-66 PMID: 1655570
  43. LyF-1, a transcriptional regulator that interacts with a novel class of promoters for lymphocyte-specific genes.
    Mol Cell Biol. 1991 Oct;11(10):5229-43 PMID: 1922043
  44. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA.
    Cell. 1991 Nov 1;67(3):569-79 PMID: 1934061
  45. Cloning and expression of murine IL-12.
    J Immunol. 1992 Jun 1;148(11):3433-40 PMID: 1350290
  46. The p50 subunit of NF-kappa B associates with the NF-IL6 transcription factor.
    Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):8145-9 PMID: 1518839
  47. A novel temporal expression pattern of three C/EBP family members in differentiating myelomonocytic cells.
    Blood. 1992 Oct 1;80(7):1725-35 PMID: 1391942
  48. Production of natural killer cell stimulatory factor (interleukin 12) by peripheral blood mononuclear cells.
    J Exp Med. 1992 Nov 1;176(5):1387-98 PMID: 1357073
  49. The two C/EBP isoforms, IL-6DBP/NF-IL6 and C/EBP delta/NF-IL6 beta, are induced by IL-6 to promote acute phase gene transcription via different mechanisms.
    Nucleic Acids Res. 1993 Jan 25;21(2):289-94 PMID: 7680115
  50. Cytokine patterns in the pathogenesis of human leishmaniasis.
    J Clin Invest. 1993 Apr;91(4):1390-5 PMID: 8473490
  51. Development of TH1 CD4+ T cells through IL-12 produced by Listeria-induced macrophages.
    Science. 1993 Apr 23;260(5107):547-9 PMID: 8097338
  52. Electroporation and DNA-dependent cell death in murine macrophages.
    Immunol Cell Biol. 1993 Apr;71 ( Pt 2):75-85 PMID: 8486399
  53. Tumor necrosis factor alpha promotes nuclear localization of cytokine-inducible CCAAT/enhancer binding protein isoforms in hepatocytes.
    J Biol Chem. 1996 Jul 26;271(30):17974-8 PMID: 8663327
  54. Differential roles for IL-12 in the maintenance of immune responses in infectious versus autoimmune disease.
    J Immunol. 1996 Oct 1;157(7):2745-8 PMID: 8816374
  55. Functional diversity of helper T lymphocytes.
    Nature. 1996 Oct 31;383(6603):787-93 PMID: 8893001
  56. Transactivation by NF-IL6/LAP is enhanced by phosphorylation of its activation domain.
    Nature. 1993 Aug 5;364(6437):544-7 PMID: 8336793
  57. The regulated expression of B lineage associated genes during B cell differentiation in bone marrow and fetal liver.
    J Exp Med. 1993 Sep 1;178(3):951-60 PMID: 8350062
  58. C/EBP, NF-kappa B, and c-Ets family members and transcriptional regulation of the cell-specific and inducible macrophage inflammatory protein 1 alpha immediate-early gene.
    Mol Cell Biol. 1993 Sep;13(9):5276-89 PMID: 8355682
  59. CCAAT/enhancer-binding protein mRNA is translated into multiple proteins with different transcription activation potentials.
    Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):8219-23 PMID: 8367486
  60. 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
  61. Distinct mechanisms for regulation of the interleukin-8 gene involve synergism and cooperativity between C/EBP and NF-kappa B.
    Mol Cell Biol. 1993 Nov;13(11):7191-8 PMID: 8413306
  62. Association between proto-oncoprotein Rel and TATA-binding protein mediates transcriptional activation by NF-kappa B.
    Nature. 1993 Sep 30;365(6445):412-9 PMID: 8413585
  63. Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon gamma and lipopolysaccharide.
    Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9730-4 PMID: 7692452
  64. Transcription factors NF-IL6 and NF-kappa B synergistically activate transcription of the inflammatory cytokines, interleukin 6 and interleukin 8.
    Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10193-7 PMID: 8234276
  65. The role of NF-kappa B and NF-IL6 transactivating factors in the synergistic activation of human serum amyloid A gene expression by interleukin-1 and interleukin-6.
    J Biol Chem. 1993 Dec 5;268(34):25624-31 PMID: 8244997
  66. Promoter analysis of an interferon-inducible gene associated with macrophage activation.
    J Immunol. 1994 Jan 1;152(1):153-62 PMID: 8254188
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1997-08-00
Pages
4572-88
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC232311
Subset
IM
Grants
NIDDK NIH HHS · K11 DK02358-08 · United States
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