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. 1991 Feb 11;19(3):517–524. doi: 10.1093/nar/19.3.517

DNA protein interactions at the interferon-responsive promoter elements: potential for an H-DNA conformation.

C Roy 1, B Lebleu 1
PMCID: PMC333642  PMID: 1707163

Abstract

The regions of several genes (IFI-56K, HLA-A3, HLA-DR and 6-16) containing the (putative) ISRE (Interferon Stimulatable Response Element) were tested for their ability to be recognized by HeLa cells nuclear extract proteins. In a band shift assay, all probes yielded two B1 and B2 DNA-protein complexes of similar mobilities. Unexpectedly the titration of the B1 complex with a synthetic ISRE core (OL1), promoted the formation of B2. Both the probe and OL1 were recovered in B2. For each probe, the possibility of the part of the sequence involved in B1 complex to form a H-DNA structure with the part of the sequence involved in B2 exists. Such a structure was favored by the colinearity of the pairing regions and requires ATP. Although probes seemed to have a secondary structure, the formal existence of a H-DNA structure has not been demonstrated. Such a model could be extended to other interferon inducible gene promoters and may account for their binding properties and differential inducibility after 5' deletion or point mutations.

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Selected References

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

  1. Aguet M., Dembić Z., Merlin G. Molecular cloning and expression of the human interferon-gamma receptor. Cell. 1988 Oct 21;55(2):273–280. doi: 10.1016/0092-8674(88)90050-5. [DOI] [PubMed] [Google Scholar]
  2. Anderson P., Yip Y. K., Vilcek J. Specific binding of 125I-human interferon-gamma to high affinity receptors on human fibroblasts. J Biol Chem. 1982 Oct 10;257(19):11301–11304. [PubMed] [Google Scholar]
  3. Benech P., Vigneron M., Peretz D., Revel M., Chebath J. Interferon-responsive regulatory elements in the promoter of the human 2',5'-oligo(A) synthetase gene. Mol Cell Biol. 1987 Dec;7(12):4498–4504. doi: 10.1128/mcb.7.12.4498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bernués J., Beltrán R., Casasnovas J. M., Azorín F. Structural polymorphism of homopurine--homopyrimidine sequences: the secondary DNA structure adopted by a d(GA.CT)22 sequence in the presence of zinc ions. EMBO J. 1989 Jul;8(7):2087–2094. doi: 10.1002/j.1460-2075.1989.tb03617.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boles T. C., Hogan M. E. DNA structure equilibria in the human c-myc gene. Biochemistry. 1987 Jan 27;26(2):367–376. doi: 10.1021/bi00376a006. [DOI] [PubMed] [Google Scholar]
  6. Bradford M. M. 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;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  7. Broxmeyer H. E., Cooper S., Rubin B. Y., Taylor M. W. The synergistic influence of human interferon-gamma and interferon-alpha on suppression of hematopoietic progenitor cells is additive with the enhanced sensitivity of these cells to inhibition by interferons at low oxygen tension in vitro. J Immunol. 1985 Oct;135(4):2502–2506. [PubMed] [Google Scholar]
  8. Caddle M. S., Lussier R. H., Heintz N. H. Intramolecular DNA triplexes, bent DNA and DNA unwinding elements in the initiation region of an amplified dihydrofolate reductase replicon. J Mol Biol. 1990 Jan 5;211(1):19–33. doi: 10.1016/0022-2836(90)90008-A. [DOI] [PubMed] [Google Scholar]
  9. Cohen B., Peretz D., Vaiman D., Benech P., Chebath J. Enhancer-like interferon responsive sequences of the human and murine (2'-5') oligoadenylate synthetase gene promoters. EMBO J. 1988 May;7(5):1411–1419. doi: 10.1002/j.1460-2075.1988.tb02958.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cohen B., Vaiman D., Chebath J. Enhancer functions and in vitro protein binding of native and mutated interferon-responsive sequences. Nucleic Acids Res. 1989 Feb 25;17(4):1679–1695. doi: 10.1093/nar/17.4.1679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cooney M., Czernuszewicz G., Postel E. H., Flint S. J., Hogan M. E. Site-specific oligonucleotide binding represses transcription of the human c-myc gene in vitro. Science. 1988 Jul 22;241(4864):456–459. doi: 10.1126/science.3293213. [DOI] [PubMed] [Google Scholar]
  12. Czarniecki C. W., Fennie C. W., Powers D. B., Estell D. A. Synergistic antiviral and antiproliferative activities of Escherichia coli-derived human alpha, beta, and gamma interferons. J Virol. 1984 Feb;49(2):490–496. doi: 10.1128/jvi.49.2.490-496.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dale T. C., Imam A. M., Kerr I. M., Stark G. R. Rapid activation by interferon alpha of a latent DNA-binding protein present in the cytoplasm of untreated cells. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1203–1207. doi: 10.1073/pnas.86.4.1203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dale T. C., Rosen J. M., Guille M. J., Lewin A. R., Porter A. G., Kerr I. M., Stark G. R. Overlapping sites for constitutive and induced DNA binding factors involved in interferon-stimulated transcription. EMBO J. 1989 Mar;8(3):831–839. doi: 10.1002/j.1460-2075.1989.tb03444.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Davis T. L., Firulli A. B., Kinniburgh A. J. Ribonucleoprotein and protein factors bind to an H-DNA-forming c-myc DNA element: possible regulators of the c-myc gene. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9682–9686. doi: 10.1073/pnas.86.24.9682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dorn A., Bollekens J., Staub A., Benoist C., Mathis D. A multiplicity of CCAAT box-binding proteins. Cell. 1987 Sep 11;50(6):863–872. doi: 10.1016/0092-8674(87)90513-7. [DOI] [PubMed] [Google Scholar]
  18. François J. C., Saison-Behmoaras T., Barbier C., Chassignol M., Thuong N. T., Hélène C. Sequence-specific recognition and cleavage of duplex DNA via triple-helix formation by oligonucleotides covalently linked to a phenanthroline-copper chelate. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9702–9706. doi: 10.1073/pnas.86.24.9702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. François J. C., Saison-Behmoaras T., Hélène C. Sequence-specific recognition of the major groove of DNA by oligodeoxynucleotides via triple helix formation. Footprinting studies. Nucleic Acids Res. 1988 Dec 23;16(24):11431–11440. doi: 10.1093/nar/16.24.11431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Friedman R. L., Stark G. R. alpha-Interferon-induced transcription of HLA and metallothionein genes containing homologous upstream sequences. Nature. 1985 Apr 18;314(6012):637–639. doi: 10.1038/314637a0. [DOI] [PubMed] [Google Scholar]
  21. Fu X. Y., Kessler D. S., Veals S. A., Levy D. E., Darnell J. E., Jr ISGF3, the transcriptional activator induced by interferon alpha, consists of multiple interacting polypeptide chains. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8555–8559. doi: 10.1073/pnas.87.21.8555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gilmour D. S., Thomas G. H., Elgin S. C. Drosophila nuclear proteins bind to regions of alternating C and T residues in gene promoters. Science. 1989 Sep 29;245(4925):1487–1490. doi: 10.1126/science.2781290. [DOI] [PubMed] [Google Scholar]
  23. Goodbourn S., Burstein H., Maniatis T. The human beta-interferon gene enhancer is under negative control. Cell. 1986 May 23;45(4):601–610. doi: 10.1016/0092-8674(86)90292-8. [DOI] [PubMed] [Google Scholar]
  24. Griffin L. C., Dervan P. B. Recognition of thymine adenine.base pairs by guanine in a pyrimidine triple helix motif. Science. 1989 Sep 1;245(4921):967–971. doi: 10.1126/science.2549639. [DOI] [PubMed] [Google Scholar]
  25. Hanvey J. C., Shimizu M., Wells R. D. Intramolecular DNA triplexes in supercoiled plasmids. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6292–6296. doi: 10.1073/pnas.85.17.6292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hemmi S., Peghini P., Metzler M., Merlin G., Dembic Z., Aguet M. Cloning of murine interferon gamma receptor cDNA: expression in human cells mediates high-affinity binding but is not sufficient to confer sensitivity to murine interferon gamma. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9901–9905. doi: 10.1073/pnas.86.24.9901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Htun H., Dahlberg J. E. Topology and formation of triple-stranded H-DNA. Science. 1989 Mar 24;243(4898):1571–1576. doi: 10.1126/science.2648571. [DOI] [PubMed] [Google Scholar]
  29. Hug H., Costas M., Staeheli P., Aebi M., Weissmann C. Organization of the murine Mx gene and characterization of its interferon- and virus-inducible promoter. Mol Cell Biol. 1988 Aug;8(8):3065–3079. doi: 10.1128/mcb.8.8.3065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Johnson A. C., Jinno Y., Merlino G. T. Modulation of epidermal growth factor receptor proto-oncogene transcription by a promoter site sensitive to S1 nuclease. Mol Cell Biol. 1988 Oct;8(10):4174–4184. doi: 10.1128/mcb.8.10.4174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kelly J. M., Porter A. C., Chernajovsky Y., Gilbert C. S., Stark G. R., Kerr I. M. Characterization of a human gene inducible by alpha- and beta-interferons and its expression in mouse cells. EMBO J. 1986 Jul;5(7):1601–1606. doi: 10.1002/j.1460-2075.1986.tb04402.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kessler D. S., Levy D. E., Darnell J. E., Jr Two interferon-induced nuclear factors bind a single promoter element in interferon-stimulated genes. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8521–8525. doi: 10.1073/pnas.85.22.8521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kessler D. S., Veals S. A., Fu X. Y., Levy D. E. Interferon-alpha regulates nuclear translocation and DNA-binding affinity of ISGF3, a multimeric transcriptional activator. Genes Dev. 1990 Oct;4(10):1753–1765. doi: 10.1101/gad.4.10.1753. [DOI] [PubMed] [Google Scholar]
  34. Kinniburgh A. J. A cis-acting transcription element of the c-myc gene can assume an H-DNA conformation. Nucleic Acids Res. 1989 Oct 11;17(19):7771–7778. doi: 10.1093/nar/17.19.7771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kohwi Y., Kohwi-Shigematsu T. Magnesium ion-dependent triple-helix structure formed by homopurine-homopyrimidine sequences in supercoiled plasmid DNA. Proc Natl Acad Sci U S A. 1988 Jun;85(11):3781–3785. doi: 10.1073/pnas.85.11.3781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Korber B., Hood L., Stroynowski I. Regulation of murine class I genes by interferons is controlled by regions located both 5' and 3' to the transcription initiation site. Proc Natl Acad Sci U S A. 1987 May;84(10):3380–3384. doi: 10.1073/pnas.84.10.3380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kusari J., Sen G. C. Transcriptional analyses of interferon-inducible mRNAs. Mol Cell Biol. 1987 Jan;7(1):528–531. doi: 10.1128/mcb.7.1.528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Lengyel P. Biochemistry of interferons and their actions. Annu Rev Biochem. 1982;51:251–282. doi: 10.1146/annurev.bi.51.070182.001343. [DOI] [PubMed] [Google Scholar]
  39. Levy D. E., Kessler D. S., Pine R., Darnell J. E., Jr Cytoplasmic activation of ISGF3, the positive regulator of interferon-alpha-stimulated transcription, reconstituted in vitro. Genes Dev. 1989 Sep;3(9):1362–1371. doi: 10.1101/gad.3.9.1362. [DOI] [PubMed] [Google Scholar]
  40. Levy D. E., Kessler D. S., Pine R., Reich N., Darnell J. E., Jr Interferon-induced nuclear factors that bind a shared promoter element correlate with positive and negative transcriptional control. Genes Dev. 1988 Apr;2(4):383–393. doi: 10.1101/gad.2.4.383. [DOI] [PubMed] [Google Scholar]
  41. Levy D. E., Lew D. J., Decker T., Kessler D. S., Darnell J. E., Jr Synergistic interaction between interferon-alpha and interferon-gamma through induced synthesis of one subunit of the transcription factor ISGF3. EMBO J. 1990 Apr;9(4):1105–1111. doi: 10.1002/j.1460-2075.1990.tb08216.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Lew D. J., Decker T., Darnell J. E., Jr Alpha interferon and gamma interferon stimulate transcription of a single gene through different signal transduction pathways. Mol Cell Biol. 1989 Dec;9(12):5404–5411. doi: 10.1128/mcb.9.12.5404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Lichtsteiner S., Wuarin J., Schibler U. The interplay of DNA-binding proteins on the promoter of the mouse albumin gene. Cell. 1987 Dec 24;51(6):963–973. doi: 10.1016/0092-8674(87)90583-6. [DOI] [PubMed] [Google Scholar]
  44. Lyamichev V. I., Frank-Kamenetskii M. D., Soyfer V. N. Protection against UV-induced pyrimidine dimerization in DNA by triplex formation. Nature. 1990 Apr 5;344(6266):568–570. doi: 10.1038/344568a0. [DOI] [PubMed] [Google Scholar]
  45. Maher L. J., 3rd, Wold B., Dervan P. B. Inhibition of DNA binding proteins by oligonucleotide-directed triple helix formation. Science. 1989 Aug 18;245(4919):725–730. doi: 10.1126/science.2549631. [DOI] [PubMed] [Google Scholar]
  46. Melgar E., Goldthwait D. A. Deoxyribonucleic acid nucleases. II. The effects of metals on the mechanism of action of deoxyribonuclease I. J Biol Chem. 1968 Sep 10;243(17):4409–4416. [PubMed] [Google Scholar]
  47. Mogensen K. E., Bandu M. T. Kinetic evidence for an activation step following binding of human interferon alpha 2 to the membrane receptors of Daudi cells. Eur J Biochem. 1983 Aug 1;134(2):355–364. doi: 10.1111/j.1432-1033.1983.tb07575.x. [DOI] [PubMed] [Google Scholar]
  48. Moser H. E., Dervan P. B. Sequence-specific cleavage of double helical DNA by triple helix formation. Science. 1987 Oct 30;238(4827):645–650. doi: 10.1126/science.3118463. [DOI] [PubMed] [Google Scholar]
  49. Munro S., Maniatis T. Expression cloning of the murine interferon gamma receptor cDNA. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9248–9252. doi: 10.1073/pnas.86.23.9248. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Pestka S., Langer J. A., Zoon K. C., Samuel C. E. Interferons and their actions. Annu Rev Biochem. 1987;56:727–777. doi: 10.1146/annurev.bi.56.070187.003455. [DOI] [PubMed] [Google Scholar]
  51. Porter A. C., Chernajovsky Y., Dale T. C., Gilbert C. S., Stark G. R., Kerr I. M. Interferon response element of the human gene 6-16. EMBO J. 1988 Jan;7(1):85–92. doi: 10.1002/j.1460-2075.1988.tb02786.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Portugal J. Do Hoogsteen base pairs occur in DNA? Trends Biochem Sci. 1989 Apr;14(4):127–130. doi: 10.1016/0968-0004(89)90141-2. [DOI] [PubMed] [Google Scholar]
  53. Postel E. H., Mango S. E., Flint S. J. A nuclease-hypersensitive element of the human c-myc promoter interacts with a transcription initiation factor. Mol Cell Biol. 1989 Nov;9(11):5123–5133. doi: 10.1128/mcb.9.11.5123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Reid L. E., Brasnett A. H., Gilbert C. S., Porter A. C., Gewert D. R., Stark G. R., Kerr I. M. A single DNA response element can confer inducibility by both alpha- and gamma-interferons. Proc Natl Acad Sci U S A. 1989 Feb;86(3):840–844. doi: 10.1073/pnas.86.3.840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Roy C., Lebleu B. DNA-protein interactions at the interferon-responsive promoter: evidences for an involvement of phosphorylation. Nucleic Acids Res. 1990 Apr 25;18(8):2125–2131. doi: 10.1093/nar/18.8.2125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Roy C., Lebleu B. Interferon-induced early changes in nuclear protein interactions with the interferon consensus sequence. Biochem Biophys Res Commun. 1989 Aug 30;163(1):370–377. doi: 10.1016/0006-291x(89)92145-1. [DOI] [PubMed] [Google Scholar]
  57. Rutherford M. N., Hannigan G. E., Williams B. R. Interferon-induced binding of nuclear factors to promoter elements of the 2-5A synthetase gene. EMBO J. 1988 Mar;7(3):751–759. doi: 10.1002/j.1460-2075.1988.tb02872.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Samanta H., Engel D. A., Chao H. M., Thakur A., García-Blanco M. A., Lengyel P. Interferons as gene activators. Cloning of the 5' terminus and the control segment of an interferon activated gene. J Biol Chem. 1986 Sep 5;261(25):11849–11858. [PubMed] [Google Scholar]
  59. 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]
  60. Shea R. G., Ng P., Bischofberger N. Thermal denaturation profiles and gel mobility shift analysis of oligodeoxynucleotide triplexes. Nucleic Acids Res. 1990 Aug 25;18(16):4859–4866. doi: 10.1093/nar/18.16.4859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Shimizu M., Hanvey J. C., Wells R. D. Multiple non-B-DNA conformations of polypurine.polypyrimidine sequences in plasmids. Biochemistry. 1990 May 15;29(19):4704–4713. doi: 10.1021/bi00471a027. [DOI] [PubMed] [Google Scholar]
  62. Sklenár V., Feigon J. Formation of a stable triplex from a single DNA strand. Nature. 1990 Jun 28;345(6278):836–838. doi: 10.1038/345836a0. [DOI] [PubMed] [Google Scholar]
  63. Wathelet M. G., Clauss I. M., Nols C. B., Content J., Huez G. A. New inducers revealed by the promoter sequence analysis of two interferon-activated human genes. Eur J Biochem. 1987 Dec 1;169(2):313–321. doi: 10.1111/j.1432-1033.1987.tb13614.x. [DOI] [PubMed] [Google Scholar]
  64. Wu L. C., Morley B. J., Campbell R. D. Cell-specific expression of the human complement protein factor B gene: evidence for the role of two distinct 5'-flanking elements. Cell. 1987 Jan 30;48(2):331–342. doi: 10.1016/0092-8674(87)90436-3. [DOI] [PubMed] [Google Scholar]
  65. Zerial A., Hovanessian A. G., Stefanos S., Huygen K., Werner G. H., Falcoff E. Synergistic activities of type I (alpha, beta) and type II (gamma) murine interferons. Antiviral Res. 1982 Sep;2(4):227–239. doi: 10.1016/0166-3542(82)90045-6. [DOI] [PubMed] [Google Scholar]
  66. Zoon K. C., Arnheiter H. Studies of the interferon receptors. Pharmacol Ther. 1984;24(2):259–278. doi: 10.1016/0163-7258(84)90037-8. [DOI] [PubMed] [Google Scholar]
  67. de los Santos C., Rosen M., Patel D. NMR studies of DNA (R+)n.(Y-)n.(Y+)n triple helices in solution: imino and amino proton markers of T.A.T and C.G.C+ base-triple formation. Biochemistry. 1989 Sep 5;28(18):7282–7289. doi: 10.1021/bi00444a021. [DOI] [PubMed] [Google Scholar]

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