Home LiteratureArticle Details
PMID: 9710616 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

GATA-Dependent expression of the interleukin-1 receptor-related T1 gene in mast cells.

Molecular and cellular biology ·Vol. 18 ·No. 9 ·1998-09-00 ·Pages 5320-31

Gächter T, Moritz DR, Gheyselinck J, Klemenz R

Abstract

The murine delayed-early serum-responsive gene T1 encodes glycoproteins of the interleukin-1 receptor family. Transcriptional initiation in fibroblasts is regulated by c-Fos and gives rise to a rare 5-kb mRNA and an abundant 2.7-kb mRNA. These transcripts are translated into a receptor-like membrane-anchored protein and a secreted protein consisting only of the ectodomain. In mast cells, T1 gene transcription is initiated 10.5 kb further upstream than in fibroblasts and gives rise predominantly to the 5-kb transcript under normal growth conditions. Here we demonstrate that calcium ionophore stimulation of mast cells resulted in an upregulation of T1 gene expression and a switch from the long to the short T1 transcript. This was paralleled by the disappearance of the receptor-type T1 protein on the mast cell surface and the secretion of large amounts of the truncated T1 protein. c-Fos and a T1 enhancer, which have previously been identified to be essential for T1 expression in fibroblasts, were not required for calcium ionophore-mediated T1 gene upregulation. Overexpression of the transcription factor GATA-1 in mast cells caused elevated T1 synthesis. Three GATA elements were identified in the minimal GATA-responsive mast cell promoter. Mutational analysis revealed that all three GATA elements are involved in T1 gene expression. Point mutations within the middle GATA element eliminated promoter activity completely, while mutations of the distal and proximal GATA binding sites reduced promoter strength by factors of 2 and 5, respectively. Exogenous expression of GATA-1 was not sufficient to activate the mast cell-specific promoter in NIH 3T3 fibroblasts.

MeSH Terms
3T3 Cells Animals Bone Marrow Cells/cytology Calcimycin/pharmacology Cell Division Cells, Cultured DNA-Binding Proteins/metabolism Dactinomycin/pharmacology Erythroid-Specific DNA-Binding Factors GATA1 Transcription Factor Gene Expression Regulation Interleukin-1 Receptor-Like 1 Protein Kinetics Mast Cells/cytology,drug effects,physiology Membrane Proteins Mice Mutagenesis, Site-Directed Nuclear Proteins/metabolism Point Mutation Promoter Regions, Genetic Protein Biosynthesis Proteins/chemistry Proto-Oncogene Proteins c-fos/metabolism Receptors, Interleukin Recombinant Proteins/biosynthesis Transcription Factors/metabolism Transcription, Genetic Transfection
Chemicals
DNA-Binding Proteins Erythroid-Specific DNA-Binding Factors GATA1 Transcription Factor Gata1 protein, mouse Il1rl1 protein, mouse Interleukin-1 Receptor-Like 1 Protein Membrane Proteins Nuclear Proteins Proteins Proto-Oncogene Proteins c-fos Receptors, Interleukin Recombinant Proteins Transcription Factors Dactinomycin Calcimycin
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Gächter T
Division of Cancer Research, Department of Pathology, University Hospital, CH-8091 Zürich, Switzerland.
Moritz D R
Gheyselinck J
Klemenz R
References (67)
67 references, click to expand
  1. Expression of ST2, an interleukin-1 receptor homologue, is induced by proinflammatory stimuli.
    Biochem Biophys Res Commun. 1997 Jun 27;235(3):474-8 PMID: 9207179
  2. Effects of the immunosuppressive drugs CsA and FK506 on intracellular signalling and gene regulation.
    Immunobiology. 1997 Dec;198(1-3):192-206 PMID: 9442391
  3. Effects of ras transformation on the induction of the IL-1 receptor related T1 gene in response to mitogens, anisomycin, IL-1 and TNFalpha.
    Oncogene. 1998 Feb 5;16(5):575-86 PMID: 9482103
  4. Fos and bone cell development: lessons from a nuclear oncogene.
    Trends Genet. 1995 Nov;11(11):436-41 PMID: 8578600
  5. Expression analysis of the soluble and membrane-associated forms of the interleukin-1 receptor-related T1 protein in primary mast cells and fibroblasts.
    Hybridoma. 1998 Apr;17(2):107-16 PMID: 9627050
  6. U1 snRNP inhibits pre-mRNA polyadenylation through a direct interaction between U1 70K and poly(A) polymerase.
    Mol Cell. 1998 Jan;1(2):255-64 PMID: 9659922
  7. The IL-1 receptor-related T1 antigen is expressed on immature and mature mast cells and on fetal blood mast cell progenitors.
    J Immunol. 1998 Nov 1;161(9):4866-74 PMID: 9794420
  8. T1 is a c-Fos- and FosB-responsive gene which is induced by growth factors through multiple signal transduction pathways.
    J Biol Chem. 1994 Mar 4;269(9):6866-73 PMID: 8120048
  9. Alternative promoter usage of the Fos-responsive gene Fit-1 generates mRNA isoforms coding for either secreted or membrane-bound proteins related to the IL-1 receptor.
    EMBO J. 1994 Mar 1;13(5):1176-88 PMID: 8131748
  10. Growth factor-mediated induction of the delayed early gene T1 depends on a 12-O-tetradecanoylphorbol 13-acetate-responsive element located 3.6 kb upstream of the transcription initiation site.
    Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3896-900 PMID: 8171009
  11. Mast cells: function and contents.
    Curr Opin Immunol. 1994 Feb;6(1):91-7 PMID: 8172685
  12. PU.1 and GATA: components of a mast cell-specific interleukin 4 intronic enhancer.
    Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7737-41 PMID: 8052653
  13. GATA-and SP1-binding sites are required for the full activity of the tissue-specific promoter of the tal-1 gene.
    Oncogene. 1994 Sep;9(9):2623-32 PMID: 8058326
  14. NF-ATp: a transcription factor required for the co-ordinate induction of several cytokine genes.
    Immunol Today. 1994 Jun;15(6):274-81 PMID: 8068174
  15. GATA transcription factors: key regulators of hematopoiesis.
    Exp Hematol. 1995 Feb;23(2):99-107 PMID: 7828675
  16. Analysis of single- and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange.
    Proc Natl Acad Sci U S A. 1977 Nov;74(11):4835-8 PMID: 73185
  17. Transformation of mammalian cells with genes from procaryotes and eucaryotes.
    Cell. 1979 Apr;16(4):777-85 PMID: 222468
  18. Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter.
    J Mol Appl Genet. 1982;1(4):327-41 PMID: 6286831
  19. FBJ murine osteosarcoma virus: identification and molecular cloning of biologically active proviral DNA.
    J Virol. 1982 Nov;44(2):674-82 PMID: 6292525
  20. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity.
    Anal Biochem. 1983 Jul 1;132(1):6-13 PMID: 6312838
  21. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum.
    Anal Biochem. 1984 Feb;137(1):266-7 PMID: 6329026
  22. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  23. Establishment of mouse cell lines which constitutively secrete large quantities of interleukin 2, 3, 4 or 5, using modified cDNA expression vectors.
    Eur J Immunol. 1988 Jan;18(1):97-104 PMID: 2831066
  24. Cloning of cDNA for the major DNA-binding protein of the erythroid lineage through expression in mammalian cells.
    Nature. 1989 Jun 8;339(6224):446-51 PMID: 2725678
  25. Site-directed mutagenesis by overlap extension using the polymerase chain reaction.
    Gene. 1989 Apr 15;77(1):51-9 PMID: 2744487
  26. Serum- and oncoprotein-mediated induction of a gene with sequence similarity to the gene encoding carcinoembryonic antigen.
    Proc Natl Acad Sci U S A. 1989 Aug;86(15):5708-12 PMID: 2527364
  27. A putative protein of a growth specific cDNA from BALB/c-3T3 cells is highly similar to the extracellular portion of mouse interleukin 1 receptor.
    FEBS Lett. 1989 Dec 4;258(2):301-4 PMID: 2532153
  28. Induction of a mitogen-responsive gene after expression of the Ha-ras oncogene in NIH 3T3 fibroblasts.
    Mol Cell Biol. 1989 Nov;9(11):5207-14 PMID: 2689874
  29. Necessity of IgE antibodies and mast cells for manifestation of resistance against larval Haemaphysalis longicornis ticks in mice.
    J Immunol. 1990 Jan 1;144(1):259-62 PMID: 2295794
  30. Regulation of interleukin 3 mRNA expression in mast cells occurs at the posttranscriptional level and is mediated by calcium ions.
    Proc Natl Acad Sci U S A. 1990 Jan;87(2):777-81 PMID: 2105489
  31. Expression of an erythroid transcription factor in megakaryocytic and mast cell lineages.
    Nature. 1990 Mar 29;344(6265):444-7 PMID: 2320112
  32. Transcriptional activation and DNA binding by the erythroid factor GF-1/NF-E1/Eryf 1.
    Genes Dev. 1990 Nov;4(11):1886-98 PMID: 2276623
  33. Anaphylaxis.
    N Engl J Med. 1991 Jun 20;324(25):1785-90 PMID: 1789822
  34. Molecular cloning of the murine ST2 gene. Characterization and chromosomal mapping.
    Biochim Biophys Acta. 1991 Aug 27;1090(1):1-8 PMID: 1832015
  35. Interferon-gamma inhibits serotonin release from mouse peritoneal mast cells.
    Eur J Immunol. 1991 Oct;21(10):2559-64 PMID: 1915558
  36. GATA-binding transcription factors in mast cells regulate the promoter of the mast cell carboxypeptidase A gene.
    J Biol Chem. 1991 Dec 5;266(34):22948-53 PMID: 1744088
  37. Cyclosporine and FK506 inhibition of murine mast cell cytokine production.
    J Pharmacol Exp Ther. 1992 Feb;260(2):680-8 PMID: 1371158
  38. GATA-binding transcription factors in hematopoietic cells.
    Blood. 1992 Aug 1;80(3):575-81 PMID: 1638017
  39. Growth factor-induced delayed early response genes.
    Mol Cell Biol. 1992 Sep;12(9):3919-29 PMID: 1508193
  40. Vaccinia and cowpox viruses encode a novel secreted interleukin-1-binding protein.
    Cell. 1992 Oct 2;71(1):145-52 PMID: 1339315
  41. A soluble receptor for interleukin-1 beta encoded by vaccinia virus: a novel mechanism of virus modulation of the host response to infection.
    Cell. 1992 Oct 2;71(1):153-67 PMID: 1394428
  42. New concepts about the mast cell.
    N Engl J Med. 1993 Jan 28;328(4):257-65 PMID: 8418407
  43. Enhancer-dependent transcription of the epsilon-globin promoter requires promoter-bound GATA-1 and enhancer-bound AP-1/NF-E2.
    Mol Cell Biol. 1993 Feb;13(2):911-7 PMID: 8423810
  44. Presence of a novel primary response gene ST2L, encoding a product highly similar to the interleukin 1 receptor type 1.
    FEBS Lett. 1993 Feb 22;318(1):83-7 PMID: 7916701
  45. T1, an immunoglobulin superfamily member, is expressed in H-ras-dependent epithelial tumours of mammary cells.
    Oncogene. 1993 Mar;8(3):609-17 PMID: 8437844
  46. Transcriptional regulation of the pyruvate kinase erythroid-specific promoter.
    J Biol Chem. 1993 Mar 15;268(8):5431-7 PMID: 8449904
  47. Secreted and membrane-bound isoforms of T1, an orphan receptor related to IL-1-binding proteins, are differently expressed in vivo.
    Dev Biol. 1995 Mar;168(1):86-97 PMID: 7883081
  48. Functional synergy and physical interactions of the erythroid transcription factor GATA-1 with the Krüppel family proteins Sp1 and EKLF.
    Mol Cell Biol. 1995 May;15(5):2437-47 PMID: 7739528
  49. Low affinity binding of interleukin-1 beta and intracellular signaling via NF-kappa B identify Fit-1 as a distant member of the interleukin-1 receptor family.
    J Biol Chem. 1995 Jul 28;270(30):17645-8 PMID: 7629057
  50. ST2/T1 protein functionally binds to two secreted proteins from Balb/c 3T3 and human umbilical vein endothelial cells but does not bind interleukin 1.
    J Biol Chem. 1995 Nov 17;270(46):27905-13 PMID: 7499265
  51. Genomic organization of the type I and type II IL-1 receptors.
    Cytokine. 1995 Aug;7(6):483-90 PMID: 8580363
  52. Transcription of the interleukin-1 receptor-related T1 gene is initiated at different promoters in mast cells and fibroblasts.
    J Biol Chem. 1996 Jan 5;271(1):124-9 PMID: 8550546
  53. Transgenic mice expressing the human high-affinity immunoglobulin (Ig) E receptor alpha chain respond to human IgE in mast cell degranulation and in allergic reactions.
    J Exp Med. 1996 Jan 1;183(1):49-56 PMID: 8551243
  54. The two faces of the mast cell.
    Nature. 1996 May 2;381(6577):21-2 PMID: 8609979
  55. Critical protective role of mast cells in a model of acute septic peritonitis.
    Nature. 1996 May 2;381(6577):75-7 PMID: 8609992
  56. Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through TNF-alpha.
    Nature. 1996 May 2;381(6577):77-80 PMID: 8609993
  57. Assignment of the human ST2 gene to chromosome 2 at q11.2.
    Hum Genet. 1996 May;97(5):561-3 PMID: 8655130
  58. T1/ST2 signaling establishes it as a member of an expanding interleukin-1 receptor family.
    J Biol Chem. 1996 Mar 8;271(10):5777-83 PMID: 8621445
  59. Cloning of a putative ligand for the T1/ST2 receptor.
    J Biol Chem. 1996 Mar 8;271(10):5784-9 PMID: 8621446
  60. The transcriptional control of hematopoiesis.
    Blood. 1996 May 15;87(10):4025-39 PMID: 8639758
  61. IL-1Rrp is a novel receptor-like molecule similar to the type I interleukin-1 receptor and its homologues T1/ST2 and IL-1R AcP.
    J Biol Chem. 1996 Feb 23;271(8):3967-70 PMID: 8626725
  62. Calcium-dependent immediate-early gene induction in lymphocytes is negatively regulated by p21Ha-ras.
    Mol Cell Biol. 1996 Nov;16(11):6582-92 PMID: 8887687
  63. The polyadenylation factor CstF-64 regulates alternative processing of IgM heavy chain pre-mRNA during B cell differentiation.
    Cell. 1996 Nov 29;87(5):941-52 PMID: 8945520
  64. Selective reporter expression in mast cells using a chymase promoter.
    J Biol Chem. 1997 Jan 31;272(5):2969-76 PMID: 9006944
  65. IgE enhances mouse mast cell Fc(epsilon)RI expression in vitro and in vivo: evidence for a novel amplification mechanism in IgE-dependent reactions.
    J Exp Med. 1997 Feb 17;185(4):663-72 PMID: 9034145
  66. Analysis of the genes encoding the mast cell function-associated antigen and its alternatively spliced transcripts.
    J Immunol. 1997 Apr 1;158(7):3235-43 PMID: 9120279
  67. The interleukin-1 receptor complex and interleukin-1 signal transduction.
    Eur Cytokine Netw. 1997 Mar;8(1):5-17 PMID: 9110143
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
DOI
10.1128/MCB.18.9.5320
Published
1998-09-00
Pages
5320-31
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC109117
Subset
IM
External Links
PubMed source DOI: 10.1128/MCB.18.9.5320 PMC Full Text View journal details
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: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2