Energetics of strand-displacement reactions in triple helices: A spectroscopic study

Journal of Molecular Biology

Volumn 291, Issue 5, 1999, Pages 1035-1054

  Mills, Martin ^a   Arimondo, Paola B ^a   Lacroix, Laurent ^a   Garestier, Thérèse ^a   Hélène, Claude ^a   Klump, Horst ^b   Mergny, Jean Louis ^a  

^a CNRS   (France)

^b NONE

Author keywords

DNA recognition; DNA structure; Purine motif; Triple helix; UV spectroscopy

Indexed keywords

OLIGODEOXYNUCLEOTIDE; PURINE; PYRIMIDINE;

ARTICLE; CONTROLLED STUDY; DNA DENATURATION; DNA FOOTPRINTING; DNA STRUCTURE; GENE EXPRESSION REGULATION; OLIGONUCLEOTIDE PROBE; PH; PRIORITY JOURNAL; TEMPERATURE SENSITIVITY; THERMODYNAMICS; TRIPLE HELIX; ULTRAVIOLET SPECTROSCOPY;

PHASEOLUS (ANGIOSPERM); VIGNA RADIATA VAR. RADIATA;

EID: 0033520344     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3014     Document Type: Article

References (99)

1. Aich P., Ritchie S., Bonham K., Lee J. S. Thermodynamic and kinetic studies of the formation of triple helices between purine-rich deoxyribo-oligonucleotides and the promoter region of the human c-src proto-oncogene. Nucl. Acids Res. 26:1998;4173-4177.
2. Alunni-Fabbroni M., Pirulli D., Manzini G., Xodo L. E. (A,G)-oligonucleotides form extraordinary stable triple helices with a critical R. Y sequence of the murine c-Ki-ras promoter and inhibit transcription in transfected NIH 3T3 cells. Biochemistry. 35:1996;16361-16369.
3. Arimondo P. B., Barcelo F., Sun J. S., Maurizot J. C., Garestier T., Hélène C. Triple helix formation by (G,A)-containing oligonucleotides: asymmetric sequence effect. Biochemistry. 37:1998;16627-16635.
4. Breslauer K. J., Franck R., Blöcker H., Marky L. A. Predicting DNA duplex stability from the base sequence. Proc. Natl Acad. Sci. USA. 83:1986;3746-3750.
5. Cantor C. R., Warshaw M. M. Oligonucleotide interactions. 3. Circular dichroism studies of the confomation of deoxynucleotides. Biopolymers. 9:1970;1059-1077.
6. Cassidy S. A., Strekowski L., Wilson W. D., Fox K. R. Effect of a triplex-binding ligand on parallel and antiparallel DNA triple helices using short unmodified and acridine-linked oligonucleotides. Biochemistry. 33:1994;15338-15347.
7. Cheng A.-J., Van Dyke M. W. Monovalent cation effects on intermolecular purine-purine-pyrimidine triple-helix formation. Nucl. Acids Res. 21:1993;5630-5635.
8. Cheng A. J., Van Dyke M. W. Oligodeoxyribonucleotide length and sequence effects on intramolecular and intermolecular G-quartet formation. Gene. 197:1997;253-260.
9. Clegg R. M., Murchie A. I. H., Zechel A., Carlberg C., Diekmann S., Lilley D. M. J. Fluorescence resonance energy transfer analysis of the structure of the four-way DNA junction. Biochemistry. 31:1992;4846-4856.
10. Clegg R. M., Murchie A. I. H., Zechel A., Lilley D. M. J. Observing the helical geometry of double-stranded DNA in solution by fluorescence resonance energy transfer. Proc. Natl Acad. Sci. USA. 90:1993;2994-2998.
11. Cooney M., Czernuszewicz G., Postel E. H., Flint S. J., Hogan M. E. Site specific oligonucleotide binding represses transcription of human c-myc gene in vitro. Science. 241:1988;456-459.
12. de los Santos C., Rosen M., Patel D. NMR study of DNA (R+)n (Y-)n (Y+)n triple helices in solution: imino and amino proton markers of TAT and CGC+ base-triple formation. Biochemistry. 28:1989;7282-7289.
13. Escudé C., Mohammadi S., Sun J. S., Nguyen C. H., Bisagni E., Liquier J., Taillandier E., Garestier T., Hélène C. Ligand-induced formation of Hoogsteen-paired parallel DNA. Chem. Biol. 3:1996;57-65.
14. Faucon B., Mergny J. L., Hélène C. Effect of third strand composition on triple helix formation: Purine versus pyrimidine oligodeoxynucleotides. Nucl. Acids Res. 24:1996;3181-3188.
15. Felsenfeld G., Davies D. R., Rich A. Formation of a three-stranded polynucleotide molecule. J. Am. Chem. Soc. 79:1957;2023.
16. François J. C., Saison-Behmoaras T., Thuong N. T., Hélène C. Inhibition of restriction endonuclease cleavage via triple helix fomation by homopyrimidine oligonucleotides. Biochemistry. 28:1989;9617-9619.
17. Freier S. M., Kierzek R., Jaeger J. A., Sugimoto N., Caruthers M. H., Neilson T., Turner D. H. Improved free-energy parameters for predictions of RNA duplex stability. Proc. Natl Acad. Sci. USA. 83:1986;9373-9377.
18. Gamper H. B. Jr, Kutyavin I. V., Rhinehart R. L., Lokhov S. G., Reed M. W., Meyer R. B. Modulation of Cm/T, G/A, and G/T triplex stability by conjugate groups in the presence and absence of KCl. Biochemistry. 36:1997;14816-14826.
19. Giovannangeli C., Montenay-Garestier T., Rougée M., Chassignol M., Thuong N. T., Hélène C. Single-stranded DNA as a target for triple-helix formation. J. Am. Chem. Soc. 113:1991;7775-7777.
20. Giovannangeli C., Montenay-Garestier T., Thuong N. T., Hélène C. Triple helix formation by oligodeoxynucleotides containing the three bases: T, C and G. Proc. Natl Acad. Sci. USA. 89:1992;8631-8635.
21. Gondeau C., Maurizot J. C., Durand M. Circular dichroism and UV melting studies on formation of an intramolecular triplex containing parallel T*A:T and G*G:C triplets: netropsin complexation with the triplex. Nucl. Acids Res. 26:1998;4996-5003.
22. Grigoriev M., Praseuth D., Robin P., Hemar A., Saison-Behmoaras T., Dautry-Varsat A., Thuong N. T., Hélène C., Harel-Bellan A. A triple helix-forming oligonucleotide-intercalator conjugate acts as a transcriptional repressor via inhibition of NF-kB binding to interleukin-2 receptor alpha-regulatory sequence. J. Biol. Chem. 267:1992;3389-3395.
23. Hampel K. J., Crosson P., Lee J. S. Polyamines favor DNA triplex formation at neutral pH. Biochemistry. 30:1991;4455-4459.
24. Hanvey J. C., Shimizu M., Wells R. D. Site-specific inhibition of EcoRI restriction/modification enzymes by a DNA triple helix. Nucl. Acids Res. 18:1990;157-161.
25. Haq I., Chowdhry B. Z., Chaires J. B. Singular value decomposition of 3-D DNA melting curves reveals complexity in the melting process. Eur. Biophys. J. 26:1997;419-426.
26. Havre P. A., Gunther E. J., Gasparro F. P., Glazer P. M. Targeted mutagenesis of DNA using triple helix-forming oligonucleotides linked to psoralen. Proc. Natl Acad. Sci. USA. 90:1993;7879-7883.
27. Hüsler P. L., Klump H. H. Prediction of pH-dependent properties of DNA triple-helices. Arch. Biochem. Biophys. 317:1995;46-56.
28. Ing N. H., Beekman J. M., Kessler D. J., Murphy M., Jayaraman K., Zendegui J. G., Hogan M. E., O'Malley B. W., Tsai M. J. In vivo transcription of a progesterone-responsive gene is specifically inhibited by a triplex-forming oligonucleotide. Nucl. Acids Res. 21:1993;2789-2796.
29. Jares-Erijman E. A., Jovin T. M. Determination of DNA helical handedness by fluorescence resonance energy transfer. J. Mol. Biol. 257:1996;597-617.
30. Kamiya M., Torigoe H., Shindo H., Sarai A. Temperature dependence and sequence specificity of DNA triplex formation: An analysis using isothermal titration calorimetry. J. Am. Chem. Soc. 118:1996;4532-4538.
31. Kandimalla E. R., Agrawal S. Single strand targeted triplex-formation. Destabilization of guanine quadruplex structures by foldback triplex-forming oligonucleotides. Nucl. Acids Res. 23:1995;1068-1074.
32. Klump H. H. Energetics of order/order transitions in nucleic acids. Can. J. Chem. 66:1988;804-811.
33. Kool E. T. Molecular recognition by circular oligonucleotides: increasing the selectivity of DNA binding. J. Am. Chem. Soc. 113:1991;6265-6266.
34. Latimer L. J. P., Payton N., Forsyth G., Lee J. S. The binding of analogues of coralyne and related heterocyclics to DNA triplexes. Biochem. Cell Biol. 73:1995;11-18.
35. Lavelle L., Fresco J. R. UV spectroscopic identification and thermodynamic analysis of protonated third strand deoxycytidine residues at neutrality in the triplex d(C+-T):[d(A-G)6.d(C-T)6]; evidence for a proton switch. Nucl. Acids Res. 23:1995;2692-2705.
36. Le Doan T., Perrouault L., Praseuth D., Habhoub N., Decout J.-L., Thuong N. T., Lhomme J., Hélène C. Sequence specific recognition, photocrosslinking and cleavage of the DNA double helix by an oligo α thymidylate covalently linked to an azidoproflavine derivative. Nucl. Acids Res. 15:1987;7749-7760.
37. Lee J. S., Woodsworth M. L., Latimer L. J. P., Morgan A. R. Polypyrimidine. polypurine synthetic DNAs containing 5-methyl cytosine form stable duplexes at neutral pH. Nucl. Acids Res. 12:1984;6603-6614.
38. Macaya R. F., Gilbert D. E., Malek S., Sinheimer J. S., Feigon J. Structure and stability of X. C. G mismatches in the third strand of intramolecular triplexes. Science. 254:1991;270-274.
39. Macaya R. F., Schultze P., Feigon J. Sugar conformation in intramolecular DNA triplexes determined by coupling constants obtained by automated simulation of P. Cosy cross peaks. J. Am. Chem. Soc. 114:1992;781-783.
40. Maher L. J. III, Wold B., Dervan P. B. Inhibition of DNA binding proteins by oligonucleotide-directed triple helix formation. Science. 245:1989;725-730.
41. Maher L. J. III, Dervan P. B., Wold B. Analysis of promoter-specific repression by triple-helical DNA complexes in a eukaryotic cell-free transcription system. Biochemistry. 31:1992;70-81.
42. Majumdar A., Khorlin A., Dyatkina N., Lin F. L. M., Powell J., Liu J., Feiz Z. Z., Khripine Y., Watanabe K. A., George J., Glazer P. M., Seidman M. M. Targeted gene knockout mediated by triple helix forming oligonucleotides. Nature Genet. 20:1998;212-214.
43. Manzini G., Xodo L. E., Gasparotto D., Quadrifoglio F., van der Marel G. A., van Boom J. H. Triple helix formation by oligopurine-oligopyrimidine DNA fragments. J. Mol. Biol. 213:1990;833-843.
44. Marky L. A., Breslauer K. J. Calculating thermodynamic data for transitions of any molecularity from equilibrium melting curves. Biopolymers. 26:1987;1601-1620.
45. Marky L. A., Kallenbach N. R., McDonough K. A., Seeman N. C., Breslauer K. J. The melting behavior of a DNA junction structure: a calorimetric and spectroscopic study. Biopolymers. 26:1987;1621-1634.
46. Mergny J. L. Fluorescence energy transfer as a probe for tetraplex formation: the i-motif. Biochemistry. 38:1999;1573-1581.
47. Mergny J. L., Lacroix L. Kinetics and Thermodynamics of i-DNA Formation: phosphodiester vs. modified oligodeoxynucleotides. Nucl. Acids Res. 26:1998;4897-4903.
48. Mergny J. L., Collier D., Rougée M., Montenay-Garestier T., Hélène C. Intercalation of ethidium bromide in a triple stranded oligonucleotide. Nucl. Acids Res. 19:1991;1521-1526.
49. Mergny J. L., Duval-Valentin G., Nguyen C. H., Perrouault L., Faucon B., Rougée M., Montenay-Garestier T., Bisagni E., Hélène C. Triple helix specific ligands. Science. 256:1992;1691-1694.
50. Mergny J. L., Garestier T., Rougee M., Lebedev A. V., Chassignol M., Thuong N. T., Hélène C. Fluorescence energy transfer between two triple helix-forming oligonucleotides bound to duplex DNA. Biochemistry. 33:1994;15321-15328.
51. Mergny J. L., Lacroix L., Han X., Leroy J. L., Hélène C. Intramolecular folding of pyrimidine oligodeoxynucleotides into an i-DNA motif. J. Am. Chem. Soc. 117:1995;8887-8898.
52. Mergny J. L., Phan A. T., Lacroix L. Following G-quartet formation by UV-spectroscopy. FEBS Letters. 435:1998;74-78.
53. Milligan J. F., Krawczyk S. H., Wadwani S., Matteucci M. D. An anti-parallel triple helix motif with oligodeoxynucleotides containing 2′-deoxyguanosine and 7-deaza-2′-deoxyxanthosine. Nucl. Acids Res. 21:1993;327-333.
54. Mills M., Klump H. H. Systematic mutation in the third strand of a Purine motif DNA triple helix: a story of a molecule which hides its tail. Nucleosides Nucleotides. 17:1998;1919-1936.
55. Mills M., Völker J., Klump H. H. Triple helical structures involving inosine: there is a penalty for promiscuity. Biochemistry. 35:1996;13338-13344.
56. Moser H. E., Dervan P. B. Sequence specific cleavage of double helical DNA by triple helix formation. Science. 238:1987;645-650.
57. Murchie A. I. H., Clegg R. M., Kitzing E., Duckett D. R., Diekmann S., Lilley D. M. J. Fluorescence energy transfert shows that the four way DNA junction is a right handed cross of antiparallel molecules. Nature. 341:1989;763-766.
58. Noonberg S. B., François J. C., Garestier T., Hélène C. Effect of competing self-structure on triplex formation with purine-rich oligodeoxynucleotides containing GA repeats. Nucl. Acids Res. 25:1995;1956-1963.
59. Olivas W. M., Maher L. J. III. Competitive triplex/quadruplex equilibria involving guanine-rich oligonucleotides. Biochemistry. 34:1995a;278-284.
60. Olivas W. M., Maher L. J. III. Overcoming potassium-mediated triplex inhibition. Nucl. Acids Res. 23:1995b;1936-1941.
61. Paes H. M., Fox K. R. Kinetic studies on the formation of intermolecular triple helices. Nucl. Acids Res. 25:1997;3269-3274.
62. Pascolo E., Toulmé J. J. Double hairpin complexes allow accommodation of all four base pairs in triple helices containing both DNA and RNA strands. J. Biol. Chem. 271:1996;24187-24192.
63. Peyret N., Seneviratne P. A., Allawi H. T., SantaLucia J. Nearest-neighbor thermodynamics and NMR of DNA sequences with internal A.A, C.C, G.G, and T.T mismatches. Biochemistry. 38:1999;3468-3477.
64. Pilch D. S., Brousseau R., Shafer R. H. Thermodynamics of triple helix formation: spectrophotometric studies on the d(A)10.2d(T)10 and d(C3T4C3).d(G3A4G3).d(C3T4C3) triple helices. Nucl. Acids Res. 18:1990;5743-5750.
65. Pilch D. S., Levenson C., Shafer R. H. Structure, stability, and thermodynamics of a short intermolecular purine-purine-pyrimidine triple helix. Biochemistry. 30:1991;6081-6087.
66. Plateau P., Guéron M. Exchangeable proton NMR without base-line distortion, using strong pulse sequences. J. Am. Chem. Soc. 104:1982;7310-7311.
67. Plum G. E. Thermodynamics of oligonucleotide triple helices. Biopolymers. 44:1998;241-256.
68. Plum G. E., Breslauer K. J. Thermodynamics of an intramolecular DNA triple helix: a calorimetric and spectroscopic study of the pH and salt dependence of thermally induced structural transitions. J. Mol. Biol. 248:1995;679-695.
69. Radhakrishnan I., de los Santos C., Patel D. J. Nuclear magnetic resonance structural studies of intramolecular purine-purine-pyrimidine DNA triplexes in solution. J. Mol. Biol. 221:1991a;1403-1418.
70. Radhakrishnan I., Gao X., de los Santos C., live D., Patel D. J. NMR structural studies of intramolecular (Y+)n.(R+)n(Y-)n DNA triplexes in solution: imino and amino proton and nitrogen markers of G. TA base triple formation. Biochemistry. 30:1991b;9022-9030.
71. Radhakrishnan I., Patel D. J., Gao X. Three-dimensional homonuclear NOESY-TOCSY of an intramolecular pyrimidine.purine.pyrimidne DNA triplex containing a central G. TA triple: non-exchangeable proton assignments and structural implications. Biochemistry. 31:1992;2514-2523.
72. Rajagopal P., Feigon J. Triple-strand formation in the homopurine homopyrimidine DNA oligonucleotides d(G-A)4 and d(T-C)4. Nature. 339:1989;637-640.
73. Rentzeperis D., Marky L. A. Ligand binding to the Hoogsteen-WC groove of TAT base triplets: Thermodynamic contribution of the thymine methyl groups. J. Am. Chem. Soc. 117:1995;5423-5424.
74. Roberts R. W., Crothers D. M. Kinetic discrimination in the folding of intramolecular triple helices. J. Mol. Biol. 260:1996a;135-146.
75. Roberts R. W., Crothers D. M. Prediction of the stability of DNA triplexes. Proc. Natl Acad. Sci. USA. 93:1996b;4320-4325.
76. Rougée M., Faucon B., Mergny J. L., Barcelo F., Giovannangeli C., Garestier T., Hélène C. Kinetics and thermodynamics of triple-helix formation: effects of ionic strength and mismatches. Biochemistry. 31:1992;9269-9278.
77. Roy C. Inhibition of gene transcription by purine rich triplex forming oligodeoxyribonucleotides. Nucl. Acids Res. 21:1993;2845-2852.
78. Sandor Z., Bredberg A. Repair of triple helix directed psoralen adducts in human cells. Nucl. Acids Res. 22:1994;2051-2056.
79. Scaria P. V., Shafer R. H. Binding of ethidium bromide to a DNA triple helix. J. Biol. Chem. 266:1991;5417-5423.
80. Scaria P. V., Shafer R. H. Calorimetric analysis of triple helices targeted to the d(G3A4G3). d(C3T4C3) duplex. Biochemistry. 35:1996;10985-10994.
81. Scaria P. V., Will S., Levenson C., Shafer R. H. Physicochemical studies of the d(G(3)T(4)G(3))*d(G(3)A(4)G(3)).d(C3T4C3) triple helix. J. Biol. Chem. 270:1995;7295-7303.
82. Shafer R. H. Stability and structure of model DNA triplexes and quadruplexes and their interactions with small ligands. Moldave K. Progress in Nucleic Acid Rese. 1998;55-94 Academic Press Inc, San Diego.
83. Sklénar V., Felgon J. Formation of a stable triplex from a single DNA strand. Nature. 345:1990;836-838.
84. Sun J. S., De Bizemont T., Duval-Valentin G., Montenay-Garestier T., Hélène C. Extension of the range of recognition sequences for triple helix formation by oligonucleotides containing guanines and thymines. C. R. Acad. Sci. Paris, série III. 313:1991;585-590.
85. Svinarchuk F., Bertrand J. R., Malvy C. A short purine oligonucleotide forms a highly stable triple helix with the promoter of the murine c-pim-1 proto-oncogene. Nucl. Acids Res. 22:1994;3742-3747.
86. Svinarchuk F., Paoletti J., Malvy C. An unusually stable purine(purine-pyrimidine) short triplex - The third strand stabilizes double-stranded DNA. J. Biol. Chem. 270:1995;14068-14071.
87. Tuschl T., Gohlke C., Jovin T. M., Westhof E., Eckstein F. Three-dimensional model for the hammerhead ribozyme based on fluorescence measurements. Science. 266:1994;785-789.
88. Vo T., Wang S. H., Kool E. T. Targeting pyrimidine single strands by triplex formation: structural optimization of binding. Nucl. Acids Res. 23:1995;2937-2944.
89. Völker J. S., Klump H. H. Electrostatic effects in DNA triple helices. Biochemistry. 33:1994;13502-13508.
90. Völker J., Botes D. P., Lindsey G. G., Klump H. H. Energetics of a stable intramolecular DNA triple helix formation. J. Mol. Biol. 230:1993;1278-1290.
91. Völker J., Osborne S. E., Glick G. D., Breslauer K. J. Thermodynamic properties of a conformationally constrained intramolecular DNA triple helix. Biochemistry. 36:1997;756-767.
92. Wang G., Levy D. D., Seidman M. M., Glazer P. M. Targeted mutagenesis in mammalian cells mediated by intracellular triple helix formation. Mol. Cell. Biol. 15:1995;1759-1768.
93. Wang G., Seidman M. M., Glazer P. M. Mutagenesis in mammalian cells induced by triple helix formation and transcription-coupled repair. Science. 271:1996;802-805.
94. Waring M. J. Stabilization of two-stranded ribohomopolymer helices and destabilization of a three-stranded helix by ethidium bromide. J. Phys. Chem. 143:1974;483-486.
95. Xodo L. E., Manzini G., Quadrifoglio F. Spectroscopic and calorimetric investigation on the DNA triplex formed by d(CTCTTCTTTC TTTTCTTTCTTCTC) and d(GAGAAGAAAGA) at acidic pH. Nucl. Acids Res. 18:1990;3557-3564.
96. Yang M., Millar D. P. Fluorescence resonance energy transfer as a probe of DNA structure and function. Methods Enzymol. 278:1997;417-444.
97. Yang M. S., Ghosh S. S., Millar D. P. Direct measurement of thermodynamic and kinetic parameters of DNA triple helix formation by fluorescence spectroscopy. Biochemistry. 33:1994;15329-15337.
98. Yang M., Ren L. Q., Huang M., Kong R. Y., Fong W. F. A DNA assay based on fluorescence resonance energy transfer and DNA triplex formation. Anal. Biochem. 259:1998;272-274.
99. Young S. L., Krawczyk S. H., Matteucci M. D., Toole J. J. Triple helix formation inhibits transcription elongation in vitro. Proc. Natl Acad. Sci. USA. 88:1991;10023-10026.