Home LiteratureArticle Details
PMID: 7937976 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Transcriptional regulation of the human insulin gene is dependent on the homeodomain protein STF1/IPF1 acting through the CT boxes.

Petersen HV, Serup P, Leonard J, Michelsen BK, Madsen OD

Abstract

Insulin gene transcription is a unique feature of the pancreatic beta cells and is increased in response to glucose. The recent cloning of insulin promoter factor 1 (IPF1) and somatostatin transcription factor 1 (STF1) unexpectedly revealed that these are mouse and rat homologues of the same protein mediating transactivation through binding of CT box-like elements in rat insulin 1 and somatostatin promoter/enhancer regions, respectively. By using oligonucleotides representing each of the three CT boxes of the human insulin (HI) gene enhancer and nuclear extracts from the mouse islet tumor cell lines beta TC3 and alpha TC1, we have identified a beta-cell-specific binding activity as reported for IPF1, which has maximal affinity toward the CT2 box. However, in pluripotent, HI-transfected rat islet tumor cells, NHI-6F, this binding activity is present prior to induction of (human) insulin gene transcription. Its migration is identical to that of in vitro translated STF1 in electrophoretic mobility-shift assays; it is specifically recognized by anti-STF1 antibodies and has an apparent molecular mass of 46 kDa. Mutation of the CT2 box decreases transcriptional activity of a HI reporter plasmid by approximately 65% in beta TC3 cells and blocks the glucose response in isolated newborn rat islet cells. Furthermore, cotransfection with STF1 cDNA into the glucagon-producing alpha TC1 cells increases the activity of the HI enhancer 4- to 5-fold, suggesting that STF1/IPF1 can confer on alpha TC1 cells the ability to transcribe the HI gene. We conclude that STF1/IPF1 is a necessary but not sufficient key regulator of insulin gene activity, possibly also involved in glucose-regulated transcription.

MeSH Terms
Animals Base Sequence Cell Line Cell Nucleus/metabolism Enhancer Elements, Genetic Gene Expression Regulation Homeodomain Proteins/metabolism Humans Insulin/biosynthesis,genetics Insulinoma Mice Molecular Sequence Data Oligodeoxyribonucleotides Pancreatic Neoplasms Plasmids Rats Substrate Specificity Trans-Activators/biosynthesis,metabolism Transcription, Genetic Transcriptional Activation Transfection Tumor Cells, Cultured
Chemicals
Homeodomain Proteins Insulin Oligodeoxyribonucleotides Trans-Activators pancreatic and duodenal homeobox 1 protein
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Petersen H V
Hagedorn Research Institute, Gentofte, Denmark.
Serup P
Leonard J
Michelsen B K
Madsen O D
References (35)
35 references, click to expand
  1. Tissue-specific expression of transfected human insulin genes in pluripotent clonal rat insulinoma lines induced during passage in vivo.
    Proc Natl Acad Sci U S A. 1988 Sep;85(18):6652-6 PMID: 2842785
  2. Precursor cells of mouse endocrine pancreas coexpress insulin, glucagon and the neuronal proteins tyrosine hydroxylase and neuropeptide Y, but not pancreatic polypeptide.
    Development. 1993 Aug;118(4):1031-9 PMID: 7903631
  3. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence.
    Cell. 1989 Aug 11;58(3):537-44 PMID: 2503252
  4. A tissue-specific nuclear factor binds to multiple sites in the human insulin-gene enhancer.
    Biochem J. 1989 Nov 15;264(1):233-9 PMID: 2690822
  5. Glucagon gene regulatory region directs oncoprotein expression to neurons and pancreatic alpha cells.
    Neuron. 1988 Sep;1(7):605-13 PMID: 2483103
  6. Insulin gene enhancer binding protein Isl-1 is a member of a novel class of proteins containing both a homeo- and a Cys-His domain.
    Nature. 1990 Apr 26;344(6269):879-82 PMID: 1691825
  7. Positive and negative regulation of the human insulin gene by multiple trans-acting factors.
    J Biol Chem. 1990 May 15;265(14):8285-96 PMID: 2186040
  8. Regulation of insulin gene expression by glucose and calcium in transfected primary islet cultures.
    J Biol Chem. 1990 Dec 25;265(36):22063-6 PMID: 1979979
  9. Effect of 5'-flanking sequence deletions on expression of the human insulin gene in transgenic mice.
    Mol Endocrinol. 1990 May;4(5):669-77 PMID: 2274051
  10. Islet amyloid polypeptide and insulin expression are controlled differently in primary and transformed islet cells.
    Mol Endocrinol. 1991 Jan;5(1):143-8 PMID: 1850107
  11. Glucose induces insulin gene transcription in a murine pancreatic beta-cell line.
    J Biol Chem. 1991 Jun 15;266(17):11141-3 PMID: 1710218
  12. Distribution and characterization of helix-loop-helix enhancer-binding proteins from pancreatic beta cells and lymphocytes.
    Nucleic Acids Res. 1991 Jul 25;19(14):3893-9 PMID: 1861981
  13. Two proteins act as the IUF1 insulin gene enhancer binding factor.
    FEBS Lett. 1991 Sep 23;290(1-2):27-30 PMID: 1915886
  14. Novel insulin promoter- and enhancer-binding proteins that discriminate between pancreatic alpha- and beta-cells.
    Mol Endocrinol. 1991 Jul;5(7):897-904 PMID: 1944296
  15. Immature transformed rat islet beta-cells differentially express C-peptides derived from the genes coding for insulin I and II as well as a transfected human insulin gene.
    Mol Endocrinol. 1992 Feb;6(2):299-307 PMID: 1569972
  16. Control of insulin gene expression by glucose.
    Biochem J. 1992 Jul 15;285 ( Pt 2):563-8 PMID: 1322137
  17. Synergistic activation of the insulin gene by a LIM-homeo domain protein and a basic helix-loop-helix protein: building a functional insulin minienhancer complex.
    Genes Dev. 1992 Nov;6(11):2165-76 PMID: 1358758
  18. Cell-specific gene expression in the islets of Langerhans: E boxes and TAAT boxes.
    Biochem Soc Trans. 1993 Feb;21(1):154-9 PMID: 8449283
  19. Rapid isolation of functionally intact pancreatic islets from mice and rats by percollTM gradient centrifucation.
    Diabete Metab. 1980 Jun;6(2):87-9 PMID: 6250926
  20. 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
  21. Cell-specific expression controlled by the 5'-flanking region of insulin and chymotrypsin genes.
    Nature. 1983 Dec 8-14;306(5943):557-61 PMID: 6358900
  22. Structure and evolution of the insulin gene.
    Annu Rev Genet. 1985;19:463-84 PMID: 3909947
  23. Pancreatic expression of human insulin gene in transgenic mice.
    Proc Natl Acad Sci U S A. 1986 Apr;83(8):2511-5 PMID: 3517871
  24. Regulation of human insulin gene expression in transgenic mice.
    Nature. 1986 May 29-Jun 4;321(6069):525-8 PMID: 3520336
  25. Cloned cell lines from a transplantable islet cell tumor are heterogeneous and express cholecystokinin in addition to islet hormones.
    J Cell Biol. 1986 Nov;103(5):2025-34 PMID: 2877997
  26. Hybrid insulin genes reveal a developmental lineage for pancreatic endocrine cells and imply a relationship with neurons.
    Cell. 1988 Apr 22;53(2):295-308 PMID: 3282675
  27. A beta-cell-specific protein binds to the two major regulatory sequences of the insulin gene enhancer.
    Proc Natl Acad Sci U S A. 1988 Jun;85(12):4228-31 PMID: 3288987
  28. Glucose modulates the binding of an islet-specific factor to a conserved sequence within the rat I and the human insulin promoters.
    Proc Natl Acad Sci U S A. 1993 May 1;90(9):3865-9 PMID: 8483904
  29. Chronic exposure of HIT cells to high glucose concentrations paradoxically decreases insulin gene transcription and alters binding of insulin gene regulatory protein.
    J Clin Invest. 1993 Jul;92(1):514-9 PMID: 8326016
  30. Human insulin gene enhancer-binding proteins in pancreatic alpha and beta cell lines.
    FEBS Lett. 1993 Aug 23;329(1-2):139-43 PMID: 8354388
  31. The dissociation of tumor-induced weight loss from hypoglycemia in a transplantable pluripotent rat islet tumor results in the segregation of stable alpha- and beta-cell tumor phenotypes.
    Endocrinology. 1993 Nov;133(5):2022-30 PMID: 8404649
  32. The helix-loop-helix transcription factor USF (upstream stimulating factor) binds to a regulatory sequence of the human insulin gene enhancer.
    Biochem J. 1993 Oct 1;295 ( Pt 1):233-7 PMID: 8216223
  33. IPF1, a homeodomain-containing transactivator of the insulin gene.
    EMBO J. 1993 Nov;12(11):4251-9 PMID: 7901001
  34. Characterization of somatostatin transactivating factor-1, a novel homeobox factor that stimulates somatostatin expression in pancreatic islet cells.
    Mol Endocrinol. 1993 Oct;7(10):1275-83 PMID: 7505393
  35. Beta-cell lines derived from transgenic mice expressing a hybrid insulin gene-oncogene.
    Proc Natl Acad Sci U S A. 1988 Dec;85(23):9037-41 PMID: 2848253
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1994-10-25
Pages
10465-9
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC45041
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