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PMID: 10393106 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Goblet-cell-specific transcription of mouse intestinal trefoil factor gene results from collaboration of complex series of positive and negative regulatory elements.

The Biochemical journal ·Vol. 341 ( Pt 2) ·1999-07-15 ·Pages 461-72

Itoh H, Inoue N, Podolsky DK

Abstract

Intestinal trefoil factor (ITF) is expressed selectively in intestinal goblet cells. Previous studies of the rat ITF gene identified one cis-regulatory element, designated the goblet-cell-response element (GCRE), present in the proximal region of the promoter. To identify additional cis-regulatory elements responsible for goblet-cell-specific expression, a DNA fragment containing 6353 bp of the 5'-flanking region of the mouse ITF gene was cloned and its promoter activity was examined extensively. In human and murine intestinal-derived cell lines (LS174T and CMT-93), the luciferase activities of a 6.3-kb construct were 5- and 2-fold greater than the smaller 1.8-kb construct, respectively. In contrast, the activity in non-intestinal cell lines (HepG2 and HeLa) was 2-4-fold lower than the smaller construct. In the region downstream from the 1.8-kb position, strong luciferase activities in LS174T and HepG2 cells were observed using a 201-bp construct. Interestingly, increased activity was almost completely suppressed in cells transfected with a 391-bp construct. Detailed analyses of this region revealed the existence of a 11-bp positive regulatory element (-181 to -170; ACCTCTTCCTG) and a 9-bp negative regulatory element (-208 to -200; ATTGACAGA) in addition to the GCRE. All three elements were well conserved among human, rat and mouse ITF gene promoters. In addition, a mutant 1.8-kb construct in which the negative regulatory region was deleted yielded the same approximate luciferase activity as a 6.3-kb construct, suggesting binding of a goblet-cell-specific silencer inhibitor (SI) between -6.3 and -1.8 kb. The SI present in goblet cells may block the silencers' binding to the pre-initiation complex and allow increased transcriptional activity driven by specific and non-specific enhancers. High-level expression of the mouse ITF gene specifically in intestinal goblet cells may be achieved through the combined effects of these regulatory elements.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Gene Expression Regulation Goblet Cells/metabolism Growth Substances/genetics,metabolism Humans Mice Molecular Sequence Data Mucins Muscle Proteins Neuropeptides Peptides/genetics,metabolism Promoter Regions, Genetic Rats Transcription, Genetic Trefoil Factor-2 Trefoil Factor-3
Chemicals
Growth Substances Mucins Muscle Proteins Neuropeptides Peptides TFF3 protein, rat Trefoil Factor-2 Trefoil Factor-3
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Itoh H
Gastrointestinal Unit and Center for the Study of Inflammatory Bowel Disease, Department of Medicine, Massachusetts General Hospital and Harvard Medical School, 32 Fruit Street, Boston, MA 02114, USA.
Inoue N
Podolsky D K
References (47)
47 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. Identification of a goblet cell-specific enhancer element in the rat intestinal trefoil factor gene promoter bound by a goblet cell nuclear protein.
    J Biol Chem. 1998 Jan 30;273(5):3060-7 PMID: 9446622
  3. Cloning of cDNA sequences of hormone-regulated genes from the MCF-7 human breast cancer cell line.
    Nucleic Acids Res. 1982 Dec 20;10(24):7895-903 PMID: 6897676
  4. Identification of a protein-binding site that mediates transcriptional response of the c-fos gene to serum factors.
    Cell. 1986 Aug 15;46(4):567-74 PMID: 3524858
  5. Relationship between life expectancy, endogenous antioxidants and products of oxygen free radical reactions in the housefly, Musca domestica.
    Mech Ageing Dev. 1986 Sep;36(1):71-7 PMID: 3762235
  6. Structure of the human oestrogen-responsive gene pS2.
    Nucleic Acids Res. 1987 Feb 25;15(4):1401-14 PMID: 3822834
  7. The human and rodent intestinal fatty acid binding protein genes. A comparative analysis of their structure, expression, and linkage relationships.
    J Biol Chem. 1987 Nov 25;262(33):16060-71 PMID: 2824476
  8. Isolation of cDNA encoding transcription factor Sp1 and functional analysis of the DNA binding domain.
    Cell. 1987 Dec 24;51(6):1079-90 PMID: 3319186
  9. Distinct regions of Sp1 modulate DNA binding and transcriptional activation.
    Science. 1988 Dec 16;242(4885):1566-70 PMID: 3059495
  10. The 5' flanking region of the pS2 gene contains a complex enhancer region responsive to oestrogens, epidermal growth factor, a tumour promoter (TPA), the c-Ha-ras oncoprotein and the c-jun protein.
    EMBO J. 1989 Mar;8(3):823-9 PMID: 2498085
  11. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells.
    Nucleic Acids Res. 1989 Aug 11;17(15):6419 PMID: 2771659
  12. hSP, the domain-duplicated homolog of pS2 protein, is co-expressed with pS2 in stomach but not in breast carcinoma.
    EMBO J. 1990 Feb;9(2):407-14 PMID: 2303034
  13. Epidermal growth factor stimulation of stromelysin mRNA in rat fibroblasts requires induction of proto-oncogenes c-fos and c-jun and activation of protein kinase C.
    Mol Cell Biol. 1990 Aug;10(8):4284-93 PMID: 2115124
  14. Induction of pS2 and hSP genes as markers of mucosal ulceration of the digestive tract.
    Gastroenterology. 1991 Feb;100(2):375-9 PMID: 1985035
  15. Epidermal growth factor (EGF/URO) induces expression of regulatory peptides in damaged human gastrointestinal tissues.
    J Pathol. 1990 Dec;162(4):279-84 PMID: 2290113
  16. A GC-rich element confers epidermal growth factor responsiveness to transcription from the gastrin promoter.
    Mol Cell Biol. 1991 May;11(5):2686-96 PMID: 2017173
  17. Structure of the chromosomal gene and cDNAs coding for lactase-phlorizin hydrolase in humans with adult-type hypolactasia or persistence of lactase.
    Am J Hum Genet. 1991 May;48(5):889-902 PMID: 1902057
  18. Expression of the pNR-2/pS2 protein in diverse human epithelial tumours.
    Br J Cancer. 1991 Oct;64(4):677-82 PMID: 1911216
  19. Identification and characterization of rat intestinal trefoil factor: tissue- and cell-specific member of the trefoil protein family.
    Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11017-21 PMID: 1763017
  20. Sequence of the complete cDNA and the 5' structure of the human sucrase-isomaltase gene. Possible homology with a yeast glucoamylase.
    Biochem J. 1992 Aug 1;285 ( Pt 3):915-23 PMID: 1353958
  21. Trefoil peptide gene expression in gastrointestinal epithelial cells in inflammatory bowel disease.
    Gastroenterology. 1993 Jan;104(1):12-20 PMID: 8419234
  22. Identification of human intestinal trefoil factor. Goblet cell-specific expression of a peptide targeted for apical secretion.
    J Biol Chem. 1993 Mar 25;268(9):6694-702 PMID: 8454642
  23. The mouse one P-domain (pS2) and two P-domain (mSP) genes exhibit distinct patterns of expression.
    J Cell Biol. 1993 Jul;122(1):191-8 PMID: 8314841
  24. hP1.B, a human P-domain peptide homologous with rat intestinal trefoil factor, is expressed also in the ulcer-associated cell lineage and the uterus.
    Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):6961-5 PMID: 8346203
  25. Trefoil peptides: a newly recognized family of epithelial mucin-associated molecules.
    Am J Physiol. 1993 Aug;265(2 Pt 1):G205-13 PMID: 8368306
  26. The P-domain or trefoil motif: a role in renewal and pathology of mucous epithelia?
    Trends Biochem Sci. 1993 Jul;18(7):239-43 PMID: 8267796
  27. Spasmolytic polypeptide: a trefoil peptide secreted by rat gastric mucous cells.
    Gastroenterology. 1994 Feb;106(2):336-45 PMID: 8299900
  28. Trefoil peptides promote epithelial migration through a transforming growth factor beta-independent pathway.
    J Clin Invest. 1994 Jul;94(1):376-83 PMID: 8040278
  29. Molecular cloning of the rat intestinal trefoil factor gene. Characterization of an intestinal goblet cell-associated promoter.
    J Biol Chem. 1995 Apr 21;270(16):9353-61 PMID: 7721858
  30. Structure and expression of murine intestinal trefoil factor: high evolutionary conservation and postnatal expression.
    Biochem Biophys Res Commun. 1995 May 5;210(1):31-7 PMID: 7741746
  31. Experimental ulceration leads to sequential expression of spasmolytic polypeptide, intestinal trefoil factor, epidermal growth factor and transforming growth factor alpha mRNAs in rat stomach.
    J Pathol. 1995 Apr;175(4):405-14 PMID: 7790995
  32. Trefoil peptide protection of intestinal epithelial barrier function: cooperative interaction with mucin glycoprotein.
    Gastroenterology. 1995 Aug;109(2):516-23 PMID: 7615201
  33. Characterization of the genomic structure and the promoter region of the human intestinal trefoil factor.
    Biochem Biophys Res Commun. 1995 Sep 5;214(1):195-9 PMID: 7669039
  34. Molecular cloning of mouse intestinal trefoil factor and its expression during goblet cell changes.
    Biochem J. 1995 Oct 1;311 ( Pt 1):293-7 PMID: 7575467
  35. Oral trefoil peptides protect against ethanol- and indomethacin-induced gastric injury in rats.
    Gastroenterology. 1996 Feb;110(2):489-97 PMID: 8566596
  36. The trefoil peptide family.
    Annu Rev Physiol. 1996;58:253-73 PMID: 8815795
  37. The gene encoding mouse intestinal trefoil factor: structural organization, partial sequence analysis and mapping to murine chromosome 17q.
    Gene. 1996 Jun 1;171(2):249-53 PMID: 8666281
  38. Conserved expression of intestinal trefoil factor in the human colonic adenoma-carcinoma sequence.
    Lab Invest. 1996 Jul;75(1):25-32 PMID: 8683937
  39. Trefoil peptides.
    Baillieres Clin Gastroenterol. 1996 Mar;10(1):113-34 PMID: 8732304
  40. Impaired defense of intestinal mucosa in mice lacking intestinal trefoil factor.
    Science. 1996 Oct 11;274(5285):262-5 PMID: 8824194
  41. cDNA cloning of rat pS2 peptide and expression of trefoil peptides in acetic acid-induced colitis.
    Biochem J. 1996 Sep 15;318 ( Pt 3):939-44 PMID: 8836141
  42. Regulation of the plasminogen activator inhibitor type-2 gene in monocytes: localization of an upstream transcriptional silencer.
    Blood. 1996 Nov 15;88(10):3686-97 PMID: 8916932
  43. Human intestinal trefoil factor is expressed in human hypothalamus and pituitary: evidence for a novel neuropeptide.
    FASEB J. 1996 Nov;10(13):1518-23 PMID: 8940297
  44. Identification and characterization of the MUC2 (human intestinal mucin) gene 5'-flanking region: promoter activity in cultured cells.
    Biochem J. 1997 Jul 1;325 ( Pt 1):259-67 PMID: 9224654
  45. Trefoil peptide expression and secretion is regulated by neuropeptides and acetylcholine.
    Am J Physiol. 1997 Aug;273(2 Pt 1):G348-54 PMID: 9277413
  46. Intestinal trefoil factor (TFF 3) and pS2 (TFF 1), but not spasmolytic polypeptide (TFF 2) mRNAs are co-expressed in normal, hyperplastic, and neoplastic human breast epithelium.
    J Pathol. 1997 Sep;183(1):30-8 PMID: 9370944
  47. Pancreatic spasmolytic polypeptide (PSP): I. Preparation and initial chemical characterization of a new polypeptide from porcine pancreas.
    Regul Pept. 1982 Mar;3(3-4):207-19 PMID: 6896240
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
1999-07-15
Pages
461-72
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1220380
Subset
IM
Grants
NIDDK NIH HHS · DK43351 · United States
NIDDK NIH HHS · DK46906 · United States
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