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. 1992 Feb 11;20(3):525–532. doi: 10.1093/nar/20.3.525

Transcriptional enhancer related DNA sequences: anomalous 1H NMR NOE crosspeaks.

M E Donlan 1, P Lu 1
PMCID: PMC310418  PMID: 1311077

Abstract

A dynamic heterogeneity which correlates with the function of the operator DNA in the lactose operon of E. coli. was previously observed (1) as a local minimum in the thymine imino proton T1 centered at a GTG/C-CAC sequence. Since this triplet occurs frequently in DNA regulatory regions, it was proposed that these sequences may be part of a structural element for specific protein interaction. We examine here three additional biologically significant 17 base pair duplexes containing GTG/CAC triplets: (1) a sequence from the mouse heavy chain immunoglobulin enhancer, (2) a sequence from the critical core of the Simian Virus 40 (SV40) enhancer, and (3) a sequence from pBR322 plasmid used as control for experiments with the SV40 DNA sequences. The 1H NMR resonance assignment for nearly all the nonexchangeable protons for both eukaryotic enhancer duplexes with the exception of the H5'/H5" protons was accomplished to use for structural analysis of these duplexes. The data presented show several NOE's associated with the GTG/CAC triplets which suggest structural variation from uniform B-DNA. In addition, anomalous broad crosspeaks for the fixed thymine methyl to its own H6 proton in combination with the imino proton kinetics associated with these triplets reinforces the original observation of a sequence dependent dynamic variation.

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Selected References

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  1. Aggarwal A. K., Rodgers D. W., Drottar M., Ptashne M., Harrison S. C. Recognition of a DNA operator by the repressor of phage 434: a view at high resolution. Science. 1988 Nov 11;242(4880):899–907. doi: 10.1126/science.3187531. [DOI] [PubMed] [Google Scholar]
  2. Arnott S., Hukins D. W. Optimised parameters for A-DNA and B-DNA. Biochem Biophys Res Commun. 1972 Jun 28;47(6):1504–1509. doi: 10.1016/0006-291X(72)90243-4. [DOI] [PubMed] [Google Scholar]
  3. Atchison M. L. Enhancers: mechanisms of action and cell specificity. Annu Rev Cell Biol. 1988;4:127–153. doi: 10.1146/annurev.cb.04.110188.001015. [DOI] [PubMed] [Google Scholar]
  4. Azorin F., Nordheim A., Rich A. Formation of Z-DNA in negatively supercoiled plasmids is sensitive to small changes in salt concentration within the physiological range. EMBO J. 1983;2(5):649–655. doi: 10.1002/j.1460-2075.1983.tb01479.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barber A. M., Zhurkin V. B. CAP binding sites reveal pyrimidine-purine pattern characteristic of DNA bending. J Biomol Struct Dyn. 1990 Oct;8(2):213–232. doi: 10.1080/07391102.1990.10507803. [DOI] [PubMed] [Google Scholar]
  6. Benoist C., Chambon P. In vivo sequence requirements of the SV40 early promotor region. Nature. 1981 Mar 26;290(5804):304–310. doi: 10.1038/290304a0. [DOI] [PubMed] [Google Scholar]
  7. Brennan R. G., Roderick S. L., Takeda Y., Matthews B. W. Protein-DNA conformational changes in the crystal structure of a lambda Cro-operator complex. Proc Natl Acad Sci U S A. 1990 Oct;87(20):8165–8169. doi: 10.1073/pnas.87.20.8165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brennan R. G., Roderick S. L., Takeda Y., Matthews B. W. Protein-DNA conformational changes in the crystal structure of a lambda Cro-operator complex. Proc Natl Acad Sci U S A. 1990 Oct;87(20):8165–8169. doi: 10.1073/pnas.87.20.8165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cheung S., Arndt K., Lu P. Correlation of lac operator DNA imino proton exchange kinetics with its function. Proc Natl Acad Sci U S A. 1984 Jun;81(12):3665–3669. doi: 10.1073/pnas.81.12.3665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Clark L., Nicholson J., Hay R. T. Enhancer binding protein (EBP1) makes base and backbone contacts over one complete turn of the DNA double helix. J Mol Biol. 1989 Apr 20;206(4):615–626. doi: 10.1016/0022-2836(89)90570-6. [DOI] [PubMed] [Google Scholar]
  11. DiGabriele A. D., Sanderson M. R., Steitz T. A. Crystal lattice packing is important in determining the bend of a DNA dodecamer containing an adenine tract. Proc Natl Acad Sci U S A. 1989 Mar;86(6):1816–1820. doi: 10.1073/pnas.86.6.1816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Doucet J., Benoit J. P., Cruse W. B., Prange T., Kennard O. Coexistence of A- and B-form DNA in a single crystal lattice. Nature. 1989 Jan 12;337(6203):190–192. doi: 10.1038/337190a0. [DOI] [PubMed] [Google Scholar]
  13. Drew H. R., Dickerson R. E. Structure of a B-DNA dodecamer. III. Geometry of hydration. J Mol Biol. 1981 Sep 25;151(3):535–556. doi: 10.1016/0022-2836(81)90009-7. [DOI] [PubMed] [Google Scholar]
  14. Drew H. R., McCall M. J., Calladine C. R. Recent studies of DNA in the crystal. Annu Rev Cell Biol. 1988;4:1–20. doi: 10.1146/annurev.cb.04.110188.000245. [DOI] [PubMed] [Google Scholar]
  15. Early T. A., Kearns D. R., Hillen W., Wells R. D. A 300- and 600-MHz proton nuclear magnetic resonance investigation of a 12 base pair deoxyribonucleic acid restriction fragment: relaxation behavior of the low-field resonances in water. Biochemistry. 1981 Jun 23;20(13):3756–3764. doi: 10.1021/bi00516a014. [DOI] [PubMed] [Google Scholar]
  16. Early T. A., Kearns D. R., Hillen W., Wells R. D. A 300-MHz proton nuclear magnetic resonance investigation of deoxyribonucleic acid restriction fragments: dynamic properties. Biochemistry. 1981 Jun 23;20(13):3764–3769. doi: 10.1021/bi00516a015. [DOI] [PubMed] [Google Scholar]
  17. Ephrussi A., Church G. M., Tonegawa S., Gilbert W. B lineage--specific interactions of an immunoglobulin enhancer with cellular factors in vivo. Science. 1985 Jan 11;227(4683):134–140. doi: 10.1126/science.3917574. [DOI] [PubMed] [Google Scholar]
  18. Gicquel-Sanzey B., Cossart P. Homologies between different procaryotic DNA-binding regulatory proteins and between their sites of action. EMBO J. 1982;1(5):591–595. doi: 10.1002/j.1460-2075.1982.tb01213.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gillies S. D., Morrison S. L., Oi V. T., Tonegawa S. A tissue-specific transcription enhancer element is located in the major intron of a rearranged immunoglobulin heavy chain gene. Cell. 1983 Jul;33(3):717–728. doi: 10.1016/0092-8674(83)90014-4. [DOI] [PubMed] [Google Scholar]
  20. Gruss P., Dhar R., Khoury G. Simian virus 40 tandem repeated sequences as an element of the early promoter. Proc Natl Acad Sci U S A. 1981 Feb;78(2):943–947. doi: 10.1073/pnas.78.2.943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Holak T. A., Borer P. N., Levy G. C., van Boom J. H., Wang A. H. 31P-NMR analysis of the B to Z transition in double-stranded (dC-dG)3 and (dC-dG)4 in high salt solution. Nucleic Acids Res. 1984 Jun 11;12(11):4625–4635. doi: 10.1093/nar/12.11.4625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Jain S., Sundaralingam M. Effect of crystal packing environment on conformation of the DNA duplex. Molecular structure of the A-DNA octamer d(G-T-G-T-A-C-A-C) in two crystal forms. J Biol Chem. 1989 Aug 5;264(22):12780–12784. [PubMed] [Google Scholar]
  23. Jordan S. R., Pabo C. O. Structure of the lambda complex at 2.5 A resolution: details of the repressor-operator interactions. Science. 1988 Nov 11;242(4880):893–899. doi: 10.1126/science.3187530. [DOI] [PubMed] [Google Scholar]
  24. Kennard O., Hunter W. N. Oligonucleotide structure: a decade of results from single crystal X-ray diffraction studies. Q Rev Biophys. 1989 Aug;22(3):327–379. doi: 10.1017/s0033583500002997. [DOI] [PubMed] [Google Scholar]
  25. Khoury A. M., Nick H. S., Lu P. In vivo interaction of Escherichia coli lac repressor N-terminal fragments with the lac operator. J Mol Biol. 1991 Jun 20;219(4):623–634. doi: 10.1016/0022-2836(91)90659-t. [DOI] [PubMed] [Google Scholar]
  26. Khoury G., Gruss P. Enhancer elements. Cell. 1983 Jun;33(2):313–314. doi: 10.1016/0092-8674(83)90410-5. [DOI] [PubMed] [Google Scholar]
  27. Kintanar A., Klevit R. E., Reid B. R. Two-dimensional NMR investigation of a bent DNA fragment: assignment of the proton resonances and preliminary structure analysis. Nucleic Acids Res. 1987 Jul 24;15(14):5845–5862. doi: 10.1093/nar/15.14.5845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Laimins L. A., Khoury G., Gorman C., Howard B., Gruss P. Host-specific activation of transcription by tandem repeats from simian virus 40 and Moloney murine sarcoma virus. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6453–6457. doi: 10.1073/pnas.79.21.6453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lee S. J., Akutsu H., Kyogoku Y., Kitano K., Tozuka Z., Ohta A., Ohtsuka E., Ikehara M. Dynamic behavior of the imino protons of the gamma OR3 17mer in H2O solution studied by high-resolution NMR. J Biochem. 1985 Dec;98(6):1463–1472. doi: 10.1093/oxfordjournals.jbchem.a135415. [DOI] [PubMed] [Google Scholar]
  30. Leroy J. L., Charretier E., Kochoyan M., Guéron M. Evidence from base-pair kinetics for two types of adenine tract structures in solution: their relation to DNA curvature. Biochemistry. 1988 Dec 13;27(25):8894–8898. doi: 10.1021/bi00425a004. [DOI] [PubMed] [Google Scholar]
  31. Leroy J. L., Kochoyan M., Huynh-Dinh T., Guéron M. Characterization of base-pair opening in deoxynucleotide duplexes using catalyzed exchange of the imino proton. J Mol Biol. 1988 Mar 20;200(2):223–238. doi: 10.1016/0022-2836(88)90236-7. [DOI] [PubMed] [Google Scholar]
  32. Lewin B. Commitment and activation at pol II promoters: a tail of protein-protein interactions. Cell. 1990 Jun 29;61(7):1161–1164. doi: 10.1016/0092-8674(90)90675-5. [DOI] [PubMed] [Google Scholar]
  33. Lu P., Cheung S., Arndt K. Possible molecular detent in the DNA structure at regulatory sequences. J Biomol Struct Dyn. 1983 Oct;1(2):509–521. doi: 10.1080/07391102.1983.10507458. [DOI] [PubMed] [Google Scholar]
  34. Lu P., Cheung S., Donlan M. A recurrent DNA sequence at sites of protein interaction. Adv Biophys. 1985;20:153–175. doi: 10.1016/0065-227x(85)90035-8. [DOI] [PubMed] [Google Scholar]
  35. Magasanik B. Priority claims policy and disenhancement. Nature. 1987 Jun 18;327(6123):561–562. doi: 10.1038/327561c0. [DOI] [PubMed] [Google Scholar]
  36. Maquat L. E., Thornton K., Reznikoff W. S. lac Promoter mutations located downstream from the transcription start site. J Mol Biol. 1980 May 25;139(3):537–549. doi: 10.1016/0022-2836(80)90145-x. [DOI] [PubMed] [Google Scholar]
  37. Martínez-Balbás A., Casasnovas J. M., Azorín F. Determination of the DNA conformation of the simian virus 40 (SV40) enhancer in SV40 minichromosomes. Eur J Biochem. 1990 Mar 10;188(2):269–273. doi: 10.1111/j.1432-1033.1990.tb15399.x. [DOI] [PubMed] [Google Scholar]
  38. McClure W. R. Mechanism and control of transcription initiation in prokaryotes. Annu Rev Biochem. 1985;54:171–204. doi: 10.1146/annurev.bi.54.070185.001131. [DOI] [PubMed] [Google Scholar]
  39. 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]
  40. Neuberger M. S. Expression and regulation of immunoglobulin heavy chain gene transfected into lymphoid cells. EMBO J. 1983;2(8):1373–1378. doi: 10.1002/j.1460-2075.1983.tb01594.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Nick H., Arndt K., Boschelli F., Jarema M. A., Lillis M., Sadler J., Caruthers M., Lu P. lac repressor-lac operator interaction: NMR observations. Proc Natl Acad Sci U S A. 1982 Jan;79(2):218–222. doi: 10.1073/pnas.79.2.218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Nordheim A., Lafer E. M., Peck L. J., Wang J. C., Stollar B. D., Rich A. Negatively supercoiled plasmids contain left-handed Z-DNA segments as detected by specific antibody binding. Cell. 1982 Dec;31(2 Pt 1):309–318. doi: 10.1016/0092-8674(82)90124-6. [DOI] [PubMed] [Google Scholar]
  43. Nordheim A., Rich A. Negatively supercoiled simian virus 40 DNA contains Z-DNA segments within transcriptional enhancer sequences. Nature. 1983 Jun 23;303(5919):674–679. doi: 10.1038/303674a0. [DOI] [PubMed] [Google Scholar]
  44. Nussinov R., Lennon G. G. Periodic structurally similar oligomers are found on one side of the axes of symmetry in the lac, trp, and gal operators. J Biomol Struct Dyn. 1984 Oct;2(2):387–395. doi: 10.1080/07391102.1984.10507574. [DOI] [PubMed] [Google Scholar]
  45. Otwinowski Z., Schevitz R. W., Zhang R. G., Lawson C. L., Joachimiak A., Marmorstein R. Q., Luisi B. F., Sigler P. B. Crystal structure of trp repressor/operator complex at atomic resolution. Nature. 1988 Sep 22;335(6188):321–329. doi: 10.1038/335321a0. [DOI] [PubMed] [Google Scholar]
  46. Pardi A., Tinoco I., Jr Kinetics for exchange of imino protons in deoxyribonucleic acid, ribonucleic acid, and hybrid oligonucleotide helices. Biochemistry. 1982 Sep 14;21(19):4686–4693. doi: 10.1021/bi00262a026. [DOI] [PubMed] [Google Scholar]
  47. Patel D. J., Shapiro L., Hare D. DNA and RNA: NMR studies of conformations and dynamics in solution. Q Rev Biophys. 1987 Aug;20(1-2):35–112. doi: 10.1017/s0033583500004224. [DOI] [PubMed] [Google Scholar]
  48. Ptashne M. How eukaryotic transcriptional activators work. Nature. 1988 Oct 20;335(6192):683–689. doi: 10.1038/335683a0. [DOI] [PubMed] [Google Scholar]
  49. Quadrifoglio F., Manzini G., Yathindra N. Short oligodeoxynucleotides with d(G-C)n sequence do not assume left-handed conformation in high salt conditions. J Mol Biol. 1984 May 25;175(3):419–423. doi: 10.1016/0022-2836(84)90358-9. [DOI] [PubMed] [Google Scholar]
  50. Reid D. G., Salisbury S. A., Williams D. H. A 1H nOe and CD study of the salt-concentration dependence of the structure of d(G-C). Nucleic Acids Res. 1983 Jun 11;11(11):3779–3793. doi: 10.1093/nar/11.11.3779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Schultz S. C., Shields G. C., Steitz T. A. Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees. Science. 1991 Aug 30;253(5023):1001–1007. doi: 10.1126/science.1653449. [DOI] [PubMed] [Google Scholar]
  52. Shakked Z., Guerstein-Guzikevich G., Eisenstein M., Frolow F., Rabinovich D. The conformation of the DNA double helix in the crystal is dependent on its environment. Nature. 1989 Nov 23;342(6248):456–460. doi: 10.1038/342456a0. [DOI] [PubMed] [Google Scholar]
  53. Timsit Y., Vilbois E., Moras D. Base-pairing shift in the major groove of (CA)n tracts by B-DNA crystal structures. Nature. 1991 Nov 14;354(6349):167–170. doi: 10.1038/354167a0. [DOI] [PubMed] [Google Scholar]
  54. Tran-Dinh S., Neumann J. M., Taboury J., Huynh-Dinh T., Renous S., Genissel B., Igolen J. DNA fragment conformations. 1H-NMR comparative studies of helix-coil transition and conformation of d(C-A-C-G-T-G) and d(G-T-G-C-A-C). Influence of helix formation on proton chemical shifts. Eur J Biochem. 1983 Jul 1;133(3):579–589. doi: 10.1111/j.1432-1033.1983.tb07502.x. [DOI] [PubMed] [Google Scholar]
  55. Tsao B. P., Wang X. F., Peterson C. L., Calame K. In vivo functional analysis of in vitro protein binding sites in the immunoglobulin heavy chain enhancer. Nucleic Acids Res. 1988 Apr 25;16(8):3239–3253. doi: 10.1093/nar/16.8.3239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Wang A. H., Quigley G. J., Kolpak F. J., Crawford J. L., van Boom J. H., van der Marel G., Rich A. Molecular structure of a left-handed double helical DNA fragment at atomic resolution. Nature. 1979 Dec 13;282(5740):680–686. doi: 10.1038/282680a0. [DOI] [PubMed] [Google Scholar]
  57. Weiher H., König M., Gruss P. Multiple point mutations affecting the simian virus 40 enhancer. Science. 1983 Feb 11;219(4585):626–631. doi: 10.1126/science.6297005. [DOI] [PubMed] [Google Scholar]
  58. Wolberger C., Dong Y. C., Ptashne M., Harrison S. C. Structure of a phage 434 Cro/DNA complex. Nature. 1988 Oct 27;335(6193):789–795. doi: 10.1038/335789a0. [DOI] [PubMed] [Google Scholar]
  59. Yanagi K., Privé G. G., Dickerson R. E. Analysis of local helix geometry in three B-DNA decamers and eight dodecamers. J Mol Biol. 1991 Jan 5;217(1):201–214. doi: 10.1016/0022-2836(91)90620-l. [DOI] [PubMed] [Google Scholar]
  60. de Villiers J., Olson L., Tyndall C., Schaffner W. Transcriptional 'enhancers' from SV40 and polyoma virus show a cell type preference. Nucleic Acids Res. 1982 Dec 20;10(24):7965–7976. doi: 10.1093/nar/10.24.7965. [DOI] [PMC free article] [PubMed] [Google Scholar]

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