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. 1991 Nov 15;280(Pt 1):157–162. doi: 10.1042/bj2800157

Transforming-growth-factor-beta activation elements in the distal promoter regions of the rat alpha 1 type I collagen gene.

J D Ritzenthaler 1, R H Goldstein 1, A Fine 1, A Lichtler 1, D W Rowe 1, B D Smith 1
PMCID: PMC1130614  PMID: 1741743

Abstract

We have located a cis-acting element (alpha 1-TAE) within the promoter sequences of the rat collagen alpha 1(I) gene (COL1A1) 1600 bases upstream of the transcription start site which mediates transcriptional activation by transforming growth factor beta (TGF-beta). The functional significance of this region was established by (1) deletion analysis of the alpha 1(I) promoter cloned upstream of the bacterial chloramphenicol acetyltransferase (CAT) gene and (2) by co-transfection of promoter constructs with double-stranded oligonucleotides. DNA-mobility-shift assays with radiolabelled alpha 1-TAE demonstrated increased nuclear binding activity after TGF-beta stimulation. Oligonucleotides encoding the alpha 1-TAE, additional upstream regions within the alpha 1(I) promoter, as well as consensus nuclear-factor-1 (NF-1) sequences, competed with the alpha 1-TAE sequence. The two collagen type I genes are stimulated by TGF-beta through different regions of their promoters.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bornstein P., McKay J., Morishima J. K., Devarayalu S., Gelinas R. E. Regulatory elements in the first intron contribute to transcriptional control of the human alpha 1(I) collagen gene. Proc Natl Acad Sci U S A. 1987 Dec;84(24):8869–8873. doi: 10.1073/pnas.84.24.8869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bornstein P., Sage H. Regulation of collagen gene expression. Prog Nucleic Acid Res Mol Biol. 1989;37:67–106. doi: 10.1016/s0079-6603(08)60695-9. [DOI] [PubMed] [Google Scholar]
  3. Chu M. L., de Wet W., Bernard M., Ramirez F. Fine structural analysis of the human pro-alpha 1 (I) collagen gene. Promoter structure, AluI repeats, and polymorphic transcripts. J Biol Chem. 1985 Feb 25;260(4):2315–2320. [PubMed] [Google Scholar]
  4. Dignam J. D., Martin P. L., Shastry B. S., Roeder R. G. Eukaryotic gene transcription with purified components. Methods Enzymol. 1983;101:582–598. doi: 10.1016/0076-6879(83)01039-3. [DOI] [PubMed] [Google Scholar]
  5. Fine A., Goldstein R. H. The effect of transforming growth factor-beta on cell proliferation and collagen formation by lung fibroblasts. J Biol Chem. 1987 Mar 15;262(8):3897–3902. [PubMed] [Google Scholar]
  6. Fine A., Poliks C. F., Donahue L. P., Smith B. D., Goldstein R. H. The differential effect of prostaglandin E2 on transforming growth factor-beta and insulin-induced collagen formation in lung fibroblasts. J Biol Chem. 1989 Oct 15;264(29):16988–16991. [PubMed] [Google Scholar]
  7. Fine A., Poliks C. F., Smith B. D., Goldstein R. H. The accumulation of type I collagen mRNAs in human embryonic lung fibroblasts stimulated by transforming growth factor-beta. Connect Tissue Res. 1990;24(3-4):237–247. doi: 10.3109/03008209009152152. [DOI] [PubMed] [Google Scholar]
  8. Gil G., Osborne T. F., Goldstein J. L., Brown M. S. Purification of a protein doublet that binds to six TGG-containing sequences in the promoter for hamster 3-hydroxy-3-methylglutaryl-coenzyme A reductase. J Biol Chem. 1988 Dec 15;263(35):19009–19019. [PubMed] [Google Scholar]
  9. Goldstein R. H., Fine A., Farnsworth L. J., Poliks C., Polgar P. Phorbol ester-induced inhibition of collagen accumulation by human lung fibroblasts. J Biol Chem. 1990 Aug 15;265(23):13623–13628. [PubMed] [Google Scholar]
  10. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gruppuso P. A., Mikumo R., Brautigan D. L., Braun L. Growth arrest induced by transforming growth factor beta 1 is accompanied by protein phosphatase activation in human keratinocytes. J Biol Chem. 1991 Feb 25;266(6):3444–3448. [PubMed] [Google Scholar]
  12. Hall C. V., Jacob P. E., Ringold G. M., Lee F. Expression and regulation of Escherichia coli lacZ gene fusions in mammalian cells. J Mol Appl Genet. 1983;2(1):101–109. [PubMed] [Google Scholar]
  13. Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol. 1967 Jun 14;26(2):365–369. doi: 10.1016/0022-2836(67)90307-5. [DOI] [PubMed] [Google Scholar]
  14. Ignotz R. A., Endo T., Massagué J. Regulation of fibronectin and type I collagen mRNA levels by transforming growth factor-beta. J Biol Chem. 1987 May 15;262(14):6443–6446. [PubMed] [Google Scholar]
  15. Jones K. A., Kadonaga J. T., Rosenfeld P. J., Kelly T. J., Tjian R. A cellular DNA-binding protein that activates eukaryotic transcription and DNA replication. Cell. 1987 Jan 16;48(1):79–89. doi: 10.1016/0092-8674(87)90358-8. [DOI] [PubMed] [Google Scholar]
  16. Kerr L. D., Miller D. B., Matrisian L. M. TGF-beta 1 inhibition of transin/stromelysin gene expression is mediated through a Fos binding sequence. Cell. 1990 Apr 20;61(2):267–278. doi: 10.1016/0092-8674(90)90807-q. [DOI] [PubMed] [Google Scholar]
  17. Kim S. J., Denhez F., Kim K. Y., Holt J. T., Sporn M. B., Roberts A. B. Activation of the second promoter of the transforming growth factor-beta 1 gene by transforming growth factor-beta 1 and phorbol ester occurs through the same target sequences. J Biol Chem. 1989 Nov 15;264(32):19373–19378. [PubMed] [Google Scholar]
  18. Laiho M., DeCaprio J. A., Ludlow J. W., Livingston D. M., Massagué J. Growth inhibition by TGF-beta linked to suppression of retinoblastoma protein phosphorylation. Cell. 1990 Jul 13;62(1):175–185. doi: 10.1016/0092-8674(90)90251-9. [DOI] [PubMed] [Google Scholar]
  19. Lichtler A., Stover M. L., Angilly J., Kream B., Rowe D. W. Isolation and characterization of the rat alpha 1(I) collagen promoter. Regulation by 1,25-dihydroxyvitamin D. J Biol Chem. 1989 Feb 25;264(6):3072–3077. [PubMed] [Google Scholar]
  20. Meisterernst M., Rogge L., Foeckler R., Karaghiosoff M., Winnacker E. L. Structural and functional organization of a porcine gene coding for nuclear factor I. Biochemistry. 1989 Oct 3;28(20):8191–8200. doi: 10.1021/bi00446a034. [DOI] [PubMed] [Google Scholar]
  21. Mitchell P. J., Tjian R. Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science. 1989 Jul 28;245(4916):371–378. doi: 10.1126/science.2667136. [DOI] [PubMed] [Google Scholar]
  22. Nowock J., Borgmeyer U., Püschel A. W., Rupp R. A., Sippel A. E. The TGGCA protein binds to the MMTV-LTR, the adenovirus origin of replication, and the BK virus enhancer. Nucleic Acids Res. 1985 Mar 25;13(6):2045–2061. doi: 10.1093/nar/13.6.2045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Osborn L., Kunkel S., Nabel G. J. Tumor necrosis factor alpha and interleukin 1 stimulate the human immunodeficiency virus enhancer by activation of the nuclear factor kappa B. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2336–2340. doi: 10.1073/pnas.86.7.2336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Paonessa G., Gounari F., Frank R., Cortese R. Purification of a NF1-like DNA-binding protein from rat liver and cloning of the corresponding cDNA. EMBO J. 1988 Oct;7(10):3115–3123. doi: 10.1002/j.1460-2075.1988.tb03178.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Penttinen R. P., Kobayashi S., Bornstein P. Transforming growth factor beta increases mRNA for matrix proteins both in the presence and in the absence of changes in mRNA stability. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1105–1108. doi: 10.1073/pnas.85.4.1105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Piña B., Brüggemeier U., Beato M. Nucleosome positioning modulates accessibility of regulatory proteins to the mouse mammary tumor virus promoter. Cell. 1990 Mar 9;60(5):719–731. doi: 10.1016/0092-8674(90)90087-u. [DOI] [PubMed] [Google Scholar]
  27. Raghow R., Postlethwaite A. E., Keski-Oja J., Moses H. L., Kang A. H. Transforming growth factor-beta increases steady state levels of type I procollagen and fibronectin messenger RNAs posttranscriptionally in cultured human dermal fibroblasts. J Clin Invest. 1987 Apr;79(4):1285–1288. doi: 10.1172/JCI112950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Raghow R., Thompson J. P. Molecular mechanisms of collagen gene expression. Mol Cell Biochem. 1989 Mar 16;86(1):5–18. doi: 10.1007/BF00231686. [DOI] [PubMed] [Google Scholar]
  29. Ravazzolo R., Karsenty G., de Crombrugghe B. A fibroblast-specific factor binds to an upstream negative control element in the promoter of the mouse alpha 1(I) collagen gene. J Biol Chem. 1991 Apr 25;266(12):7382–7387. [PubMed] [Google Scholar]
  30. Rippe R. A., Lorenzen S. I., Brenner D. A., Breindl M. Regulatory elements in the 5'-flanking region and the first intron contribute to transcriptional control of the mouse alpha 1 type I collagen gene. Mol Cell Biol. 1989 May;9(5):2224–2227. doi: 10.1128/mcb.9.5.2224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ristiniemi J., Oikarinen J. Histone H1 binds to the putative nuclear factor I recognition sequence in the mouse alpha 2(I) collagen promoter. J Biol Chem. 1989 Feb 5;264(4):2164–2174. [PubMed] [Google Scholar]
  32. Rossi P., Karsenty G., Roberts A. B., Roche N. S., Sporn M. B., de Crombrugghe B. A nuclear factor 1 binding site mediates the transcriptional activation of a type I collagen promoter by transforming growth factor-beta. Cell. 1988 Feb 12;52(3):405–414. doi: 10.1016/s0092-8674(88)80033-3. [DOI] [PubMed] [Google Scholar]
  33. Rossi P., de Crombrugghe B. Identification of a cell-specific transcriptional enhancer in the first intron of the mouse alpha 2 (type I) collagen gene. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5590–5594. doi: 10.1073/pnas.84.16.5590. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rossouw C. M., Vergeer W. P., du Plooy S. J., Bernard M. P., Ramirez F., de Wet W. J. DNA sequences in the first intron of the human pro-alpha 1(I) collagen gene enhance transcription. J Biol Chem. 1987 Nov 5;262(31):15151–15157. [PubMed] [Google Scholar]
  35. Santoro C., Mermod N., Andrews P. C., Tjian R. A family of human CCAAT-box-binding proteins active in transcription and DNA replication: cloning and expression of multiple cDNAs. Nature. 1988 Jul 21;334(6179):218–224. doi: 10.1038/334218a0. [DOI] [PubMed] [Google Scholar]
  36. Schmidt A., Rossi P., de Crombrugghe B. Transcriptional control of the mouse alpha 2(I) collagen gene: functional deletion analysis of the promoter and evidence for cell-specific expression. Mol Cell Biol. 1986 Feb;6(2):347–354. doi: 10.1128/mcb.6.2.347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Stuiver M. H., van der Vliet P. C. Adenovirus DNA-binding protein forms a multimeric protein complex with double-stranded DNA and enhances binding of nuclear factor I. J Virol. 1990 Jan;64(1):379–386. doi: 10.1128/jvi.64.1.379-386.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Zabel U., Baeuerle P. A. Purified human I kappa B can rapidly dissociate the complex of the NF-kappa B transcription factor with its cognate DNA. Cell. 1990 Apr 20;61(2):255–265. doi: 10.1016/0092-8674(90)90806-p. [DOI] [PubMed] [Google Scholar]

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