Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1991 Feb 11;19(3):485–491. doi: 10.1093/nar/19.3.485

The promoter of the chicken alpha 2(VI) collagen gene has features characteristic of house-keeping genes and of proto-oncogenes.

E Koller 1, A R Hayman 1, B Trueb 1
PMCID: PMC333637  PMID: 2011522

Abstract

The promoter of the chicken alpha 2(VI) collagen gene reveals several interesting features characteristic of house-keeping genes and growth control related genes. It does not possess a typical TATAA or CAAT box, but it contains several potential binding sites for transcription factors Sp1 and ETF. The 5' flanking region of the gene forms a typical 'CpG island' where the dinucleotide sequence CpG occurs with high frequency relative to the bulk genome. Consistent with the lack of a TATAA element, the gene contains multiple transcription initiation sites distributed over 75 bp of genomic DNA. A short DNA fragment (207 bp) encompassing all the transcription initiation sites and the entire CpG island shows strong promoter activity when linked to a heterologous reporter gene. The upstream region of the promoter harbours a long homopurine/homopyrimidine element (403 bp) which is sensitive to endonuclease S1. This element might have the ability to adopt an intramolecular hairpin triplex structure and could play a role in the organization of the chromatin at the alpha 2(VI) collagen locus. Our results demonstrate that the structure of the alpha 2(VI) collagen promoter is completely different from that of any other collagen promoter characterized so far.

Full text

PDF
485

Images in this article

488Image
on p.488
489Image
on p.489

Selected References

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

  1. Aumailley M., Mann K., von der Mark H., Timpl R. Cell attachment properties of collagen type VI and Arg-Gly-Asp dependent binding to its alpha 2(VI) and alpha 3(VI) chains. Exp Cell Res. 1989 Apr;181(2):463–474. doi: 10.1016/0014-4827(89)90103-1. [DOI] [PubMed] [Google Scholar]
  2. Bonaldo P., Russo V., Bucciotti F., Bressan G. M., Colombatti A. Alpha 1 chain of chick type VI collagen. The complete cDNA sequence reveals a hybrid molecule made of one short collagen and three von Willebrand factor type A-like domains. J Biol Chem. 1989 Apr 5;264(10):5575–5580. [PubMed] [Google Scholar]
  3. Bonaldo P., Russo V., Bucciotti F., Doliana R., Colombatti A. Structural and functional features of the alpha 3 chain indicate a bridging role for chicken collagen VI in connective tissues. Biochemistry. 1990 Feb 6;29(5):1245–1254. doi: 10.1021/bi00457a021. [DOI] [PubMed] [Google Scholar]
  4. Carter W. G. Transformation-dependent alterations is glycoproteins of extracellular matrix of human fibroblasts. Characterization of GP250 and the collagen-like GP140. J Biol Chem. 1982 Nov 25;257(22):13805–13815. [PubMed] [Google Scholar]
  5. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  6. Chu M. L., Pan T. C., Conway D., Kuo H. J., Glanville R. W., Timpl R., Mann K., Deutzmann R. Sequence analysis of alpha 1(VI) and alpha 2(VI) chains of human type VI collagen reveals internal triplication of globular domains similar to the A domains of von Willebrand factor and two alpha 2(VI) chain variants that differ in the carboxy terminus. EMBO J. 1989 Jul;8(7):1939–1946. doi: 10.1002/j.1460-2075.1989.tb03598.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Collier D. A., Wells R. D. Effect of length, supercoiling, and pH on intramolecular triplex formation. Multiple conformers at pur.pyr mirror repeats. J Biol Chem. 1990 Jun 25;265(18):10652–10658. [PubMed] [Google Scholar]
  8. Collis P., Antoniou M., Grosveld F. Definition of the minimal requirements within the human beta-globin gene and the dominant control region for high level expression. EMBO J. 1990 Jan;9(1):233–240. doi: 10.1002/j.1460-2075.1990.tb08100.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Farnham P. J., Abrams J. M., Schimke R. T. Opposite-strand RNAs from the 5' flanking region of the mouse dihydrofolate reductase gene. Proc Natl Acad Sci U S A. 1985 Jun;82(12):3978–3982. doi: 10.1073/pnas.82.12.3978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  11. Graham F. L., van der Eb A. J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973 Apr;52(2):456–467. doi: 10.1016/0042-6822(73)90341-3. [DOI] [PubMed] [Google Scholar]
  12. Hatamochi A., Aumailley M., Mauch C., Chu M. L., Timpl R., Krieg T. Regulation of collagen VI expression in fibroblasts. Effects of cell density, cell-matrix interactions, and chemical transformation. J Biol Chem. 1989 Feb 25;264(6):3494–3499. [PubMed] [Google Scholar]
  13. Hayman A. R., Köppel J., Winterhalter K. H., Trueb B. The triple-helical domain of alpha 2(VI) collagen is encoded by 19 short exons that are multiples of 9 base pairs. J Biol Chem. 1990 Jun 15;265(17):9864–9868. [PubMed] [Google Scholar]
  14. Hoffman E. K., Trusko S. P., Murphy M., George D. L. An S1 nuclease-sensitive homopurine/homopyrimidine domain in the c-Ki-ras promoter interacts with a nuclear factor. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2705–2709. doi: 10.1073/pnas.87.7.2705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Johnson A. C., Ishii S., Jinno Y., Pastan I., Merlino G. T. Epidermal growth factor receptor gene promoter. Deletion analysis and identification of nuclear protein binding sites. J Biol Chem. 1988 Apr 25;263(12):5693–5699. [PubMed] [Google Scholar]
  16. Kageyama R., Merlino G. T., Pastan I. Nuclear factor ETF specifically stimulates transcription from promoters without a TATA box. J Biol Chem. 1989 Sep 15;264(26):15508–15514. [PubMed] [Google Scholar]
  17. Karsenty G., de Crombrugghe B. Two different negative and one positive regulatory factors interact with a short promoter segment of the alpha 1 (I) collagen gene. J Biol Chem. 1990 Jun 15;265(17):9934–9942. [PubMed] [Google Scholar]
  18. Keene D. R., Engvall E., Glanville R. W. Ultrastructure of type VI collagen in human skin and cartilage suggests an anchoring function for this filamentous network. J Cell Biol. 1988 Nov;107(5):1995–2006. doi: 10.1083/jcb.107.5.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Koller E., Winterhalter K. H., Trueb B. The globular domains of type VI collagen are related to the collagen-binding domains of cartilage matrix protein and von Willebrand factor. EMBO J. 1989 Apr;8(4):1073–1077. doi: 10.1002/j.1460-2075.1989.tb03475.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Koller M., Schnyder B., Strehler E. E. Structural organization of the human CaMIII calmodulin gene. Biochim Biophys Acta. 1990 Oct 23;1087(2):180–189. doi: 10.1016/0167-4781(90)90203-e. [DOI] [PubMed] [Google Scholar]
  21. Mar J. H., Antin P. B., Cooper T. A., Ordahl C. P. Analysis of the upstream regions governing expression of the chicken cardiac troponin T gene in embryonic cardiac and skeletal muscle cells. J Cell Biol. 1988 Aug;107(2):573–585. doi: 10.1083/jcb.107.2.573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mavrothalassitis G. J., Watson D. K., Papas T. S. Molecular and functional characterization of the promoter of ETS2, the human c-ets-2 gene. Proc Natl Acad Sci U S A. 1990 Feb;87(3):1047–1051. doi: 10.1073/pnas.87.3.1047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mirkin S. M., Lyamichev V. I., Drushlyak K. N., Dobrynin V. N., Filippov S. A., Frank-Kamenetskii M. D. DNA H form requires a homopurine-homopyrimidine mirror repeat. Nature. 1987 Dec 3;330(6147):495–497. doi: 10.1038/330495a0. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Ramirez F., Di Liberto M. Complex and diversified regulatory programs control the expression of vertebrate collagen genes. FASEB J. 1990 Apr 1;4(6):1616–1623. doi: 10.1096/fasebj.4.6.2180769. [DOI] [PubMed] [Google Scholar]
  26. Rowe D. W., Moen R. C., Davidson J. M., Byers P. H., Bornstein P., Palmiter R. D. Correlation of procollagen mRNA levels in normal and transformed chick embryo fibroblasts with different rates of procollagen synthesis. Biochemistry. 1978 May 2;17(9):1581–1590. doi: 10.1021/bi00602a001. [DOI] [PubMed] [Google Scholar]
  27. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schreier T., Friis R. R., Winterhalter K. H., Trüeb B. Regulation of type VI collagen synthesis in transformed mesenchymal cells. Biochem J. 1988 Jul 15;253(2):381–386. doi: 10.1042/bj2530381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Selden R. F., Howie K. B., Rowe M. E., Goodman H. M., Moore D. D. Human growth hormone as a reporter gene in regulation studies employing transient gene expression. Mol Cell Biol. 1986 Sep;6(9):3173–3179. doi: 10.1128/mcb.6.9.3173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tewari D. S., Cook D. M., Taub R. Characterization of the promoter region and 3' end of the human insulin receptor gene. J Biol Chem. 1989 Sep 25;264(27):16238–16245. [PubMed] [Google Scholar]
  31. Trüeb B., Lewis J. B., Carter W. G. Translatable mRNA for GP140 (a subunit of type VI collagen) is absent in SV40 transformed fibroblasts. J Cell Biol. 1985 Feb;100(2):638–641. doi: 10.1083/jcb.100.2.638. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Trüeb B., Schaeren-Wiemers N., Schreier T., Winterhalter K. H. Molecular cloning of chicken type VI collagen. Primary structure of the subunit alpha 2(VI)-pepsin. J Biol Chem. 1989 Jan 5;264(1):136–140. [PubMed] [Google Scholar]
  33. Vuorio E., de Crombrugghe B. The family of collagen genes. Annu Rev Biochem. 1990;59:837–872. doi: 10.1146/annurev.bi.59.070190.004201. [DOI] [PubMed] [Google Scholar]
  34. Weaver R. F., Weissmann C. Mapping of RNA by a modification of the Berk-Sharp procedure: the 5' termini of 15 S beta-globin mRNA precursor and mature 10 s beta-globin mRNA have identical map coordinates. Nucleic Acids Res. 1979 Nov 10;7(5):1175–1193. doi: 10.1093/nar/7.5.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Weil D., Mattei M. G., Passage E., N'Guyen V. C., Pribula-Conway D., Mann K., Deutzmann R., Timpl R., Chu M. L. Cloning and chromosomal localization of human genes encoding the three chains of type VI collagen. Am J Hum Genet. 1988 Mar;42(3):435–445. [PMC free article] [PubMed] [Google Scholar]
  36. Weintraub H. A dominant role for DNA secondary structure in forming hypersensitive structures in chromatin. Cell. 1983 Apr;32(4):1191–1203. doi: 10.1016/0092-8674(83)90302-1. [DOI] [PubMed] [Google Scholar]
  37. Wells R. D., Collier D. A., Hanvey J. C., Shimizu M., Wohlrab F. The chemistry and biology of unusual DNA structures adopted by oligopurine.oligopyrimidine sequences. FASEB J. 1988 Nov;2(14):2939–2949. [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES