A Fluorescent Intercalator Displacement Assay for Establishing DNA Binding Selectivity and Affinity

Accounts of Chemical Research

Volumn 37, Issue 1, 2004, Pages 61-69

  Tse, Winston C ^a   Boger, Dale L ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONGOCIDINE; DNA; FLUORESCENT DYE; NYLON; OLIGODEOXYRIBONUCLEOTIDE; THIAZOLE DERIVATIVE;

ARTICLE; ASSAY; BINDING AFFINITY; BINDING COMPETITION; BINDING SITE; CHEMISTRY; COMPARATIVE STUDY; DNA BINDING; FLUORESCENT INTERCALATOR DISPLACEMENT ASSAY; METABOLISM; METHODOLOGY; NUCLEOTIDE SEQUENCE; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; SPECTROFLUOROMETRY; STOICHIOMETRY;

BASE SEQUENCE; BINDING, COMPETITIVE; DNA; FLUORESCENT DYES; NETROPSIN; NYLONS; OLIGODEOXYRIBONUCLEOTIDES; SPECTROMETRY, FLUORESCENCE; THIAZOLES;

EID: 1642576322     PISSN: 00014842     EISSN: None     Source Type: Journal    
DOI: 10.1021/ar030113y     Document Type: Article

References (68)

1. Browne, M. J.; Thurlbey, P. L. Genomes, Molecular Biology and Drug Discovery;, Academic: London, 1996.
2. Matteucci, M. D.; Wagner, R. W. In pursuit of antisense. Nature 1996, 384, 20-22.
3. Neidle, S.; Thurston, D. E. In New Targets for Cancer Chemotherapy; Kerr, D. J., Workman, P., Eds.; CRC: Boca Raton, FL, 1994.
4. Thurston, D. E. Nucleic acid targeting: therapeutic strategies for the 21st century. Br. J. Cancer 1999, 80 (Suppl. 1), 65-85.
5. Choo, Y.; Sanchez-Garcia, I.; Klug, A. In vivo repression by a site-specific DNA-binding protein designed against an oncogenic sequence. Nature 1994, 372, 642-645.
6. Neidle, S. Recent developments in triple-helix regulation of gene expression. Anticancer Drug Des. 1997, 12, 433-442.
7. Trauger, J. W.; Baird, E. E.; Dervan, P. B. Recognition of DNA by designed ligands at subnanomolar concentrations. Nature 1996, 382, 559-561.
8. Knudsen, H.; Nielsen, P. E. Antisense properties of duplex- and triplex-forming PNAs. Nucleic Acids Res. 1996, 24, 494-500.
9. Werstuck, G.; Green, M. R. Controlling gene expression in living cells through small molecule-RNA interactions. Science 1998, 282, 296-298.
10. Chiang, S. Y.; Azizkhan, J. C.; Beerman, T. A. A comparison of DNA-binding drugs as inhibitors of E2F1- and Sp1-DNA complexes and associated gene expression. Biochemistry 1998, 37, 3109-3115.
11. Gottesfeld, J. M.; Neely, L.; Trauger, J. W.; Baird, E. E.; Dervan, P. B. Regulation of gene expression by small molecules. Nature 1997, 387, 202-205.
12. Dervan, P. B. Design of sequence-specific DNA-binding molecules. Science 1986, 232, 464-471.
13. Taylor, J. S.; Schultz, P. G.; Dervan, P. B. DNA affinity cleaving. Sequence specific cleavage of DNA by distamycin-EDTA-iron-(II) and EDTA-distamycin-iron(II). Tetrahedron 1984, 40, 457-465.
14. Galas, D. J.; Schmitz, A. DNase footprinting: a simple method for the detection of protein-DNA binding specificity. Nucleic Acids Res. 1978, 5, 3157-3170.
15. Royer-Pokora, B.; Gordon, L. K.; Haseltine, W. A. Use of exonuclease III to determine the site of stable lesions in defined sequences of DNA: the cyclobutane pyrimidine dimer and cis and trans dichlorodiammine platinum II examples. Nucleic Acids Res. 1981, 9, 4595-4609.
16. Van Dyke, M. W.; Hertzberg, R. P.; Dervan, P. B. Map of distamycin, netropsin, and actinomycin binding sites on heterogeneous DNA: DNA cleavage-inhibition patterns with methidiumpropyl-EDTA-Fe(II). Proc. Natl. Acad. Sci. U.S.A. 1982, 79, 5470-5474.
17. Kuwabara, M. D.; Sigman, D. S. Footprinting DNA-protein complexes in situ following gel retardation assays using 1,10-phenanthroline-copper ion: Escherichia coli RNA polymeraselac promoter complexes. Biochemistry 1987, 26, 7234-7238.
18. Tullius, T. D.; Dombroski, B. A.; Churchill, M. E.; Kam, L. Hydroxyl radical footprinting: a high-resolution method for mapping protein-DNA contacts. Methods Enzymol. 1987, 155, 537-558.
19. Hayashibara, K. C.; Verdine, G. L. Template-directed interference footprinting of cytosine contacts in a protein-DNA complex: potent interference by 5-aza-2′-deoxycytidine. Biochemistry 1992, 31, 11265-11273.
20. Boger, D. L.; Johnson, D. S. CC-1065 and the duocarmycins: Understanding their biological function through mechanistic studies. Angew. Chem., Int. Ed. Engl. 1996, 35, 1438-1474.
21. Rajski, S. R.; Williams, R. M. DNA Cross-linking agents as antitumor drugs. Chem. Rev. 1998, 98, 2723-2796.
22. Tao, Z. F.; Saito, I.; Sugiyama, H. Highly cooperative DNA dialkylation by the homodimer of imidazole-pyrrole diamide-CPI conjugate with vinyl linker. J. Am. Chem. Soc. 2000, 122, 1602-1608.
23. Hardenbol, P.; Wang, J. C.; Van Dyke, M. W. Identification of preferred distamycin-DNA binding sites by the combinatorial method REPSA. Bioconjugate Chem. 1997, 8, 617-620.
24. Chaltin, P.; Borgions, F.; Van Aerschot, A.; Herdewijn, P. Comparison of library screening techniques used in the development of dsDNA ligands. Bioorg. Med. Chem. Lett. 2003, 13, 47-50.
25. Guelev, V. M.; Harting, M. T.; Lokey, R. S.; Iverson, B. L. Altered sequence specificity identified from a library of DNA-binding small molecules. Chem. Biol. 2000, 7, 1-8.
26. Hamy, F.; Albrecht, G.; Florsheimer, A.; Bailly, C. An ARE-selective DNA minor groove binder from a combinatorial approach. Biochem. Biophys. Res. Commun. 2000, 270, 393-399.
27. Larson, C. J.; Verdine, G. L. In Bioorganic Chemistry: Nucleic Acids; Hecht, S. M., Ed.; Oxford University: Oxford, 1996; pp 324-346.
28. Blackwell, T. K.; Kretzner, L.; Blackwood, E. M.; Eisenman, R. N.; Weintraub, H. Sequence-specific DNA binding by the c-Myc protein. Science 1990, 250, 1149-1151.
29. Blackwell, T. K.; Weintraub, H. Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection. Science 1990, 250, 1104-1110.
30. Thiesen, H. J.; Bach, C. Target Detection Assay (TDA): a versatile procedure to determine DNA binding sites as demonstrated on SP1 protein. Nucleic Acids Res. 1990, 18, 3203-3209.
31. Chodosh, L. A.; Carthew, R. W.; Sharp, P. A. A single polypeptide possesses the binding and transcription activities of the adenovirus major late transcription factor. Mol. Cell Biol. 1986, 6, 4723-4733.
32. Boger, D. L.; Fink, B. E.; Brunette, S. R.; Tse, W. C.; Hedrick, M. P. A simple, high-resolution method for establishing DNA binding affinity and sequence selectivity. J. Am. Chem. Soc. 2001, 123, 5878-5891.
33. Boger, D. L.; Fink, B. E.; Hedrick, M. P. Total synthesis of distamycin A and 2640 analogs: A solution-phase combinatorial approach to the discovery of new, bioactive DNA binding agents and development of a rapid, high-throughput screen for determining relative DNA binding affinity or DNA binding sequence selectivity. J. Am. Chem. Soc. 2000, 122, 6382-6394.
34. Lee, L. G.; Chen, C. H.; Chiu, L. A. Thiazole orange: a new dye for reticulocyte analysis. Cytometry 1986, 7, 508-517.
35. Nygren, J.; Svanvik, N.; Kubista, M. The interactions between the fluorescent dye thiazole orange and DNA. Biopolymers 1998, 46, 39-51.
36. LePecq, J. B.; Paoletti, C. A fluorescent complex between ethidium bromide and nucleic acids. Physical-chemical characterization. J. Mol. Biol. 1967, 27, 87-106. Reviews: Morgan, A. R.; Lee, J. S.; Pulleyblank, D. E.; Murray, N. L.; Evans, D. H. Ethidium fluorescence assays. Part I. Physiochemical studies. Nucleic Acids Res. 1979, 7, 547-569. Morgan, A. R.; Evans, D. H.; Lee, J. S.; Pulleyblank, D. E. Ethidium fluorescence assay. Part II. Ezymatic studies and DNA-protein interactions. Nucleic Acids Res. 1979, 7, 571-594.
37. LePecq, J. B.; Paoletti, C. A fluorescent complex between ethidium bromide and nucleic acids. Physical-chemical characterization. J. Mol. Biol. 1967, 27, 87-106. Reviews: Morgan, A. R.; Lee, J. S.; Pulleyblank, D. E.; Murray, N. L.; Evans, D. H. Ethidium fluorescence assays. Part I. Physiochemical studies. Nucleic Acids Res. 1979, 7, 547-569. Morgan, A. R.; Evans, D. H.; Lee, J. S.; Pulleyblank, D. E. Ethidium fluorescence assay. Part II. Ezymatic studies and DNA-protein interactions. Nucleic Acids Res. 1979, 7, 571-594.
38. LePecq, J. B.; Paoletti, C. A fluorescent complex between ethidium bromide and nucleic acids. Physical-chemical characterization. J. Mol. Biol. 1967, 27, 87-106. Reviews: Morgan, A. R.; Lee, J. S.; Pulleyblank, D. E.; Murray, N. L.; Evans, D. H. Ethidium fluorescence assays. Part I. Physiochemical studies. Nucleic Acids Res. 1979, 7, 547-569. Morgan, A. R.; Evans, D. H.; Lee, J. S.; Pulleyblank, D. E. Ethidium fluorescence assay. Part II. Ezymatic studies and DNA-protein interactions. Nucleic Acids Res. 1979, 7, 571-594.
39. For a complete list of references, see ref 32, footnote 9.
40. Ethidium possesses relatively little sequence preference, although it displays a slight bias toward binding GC-rich DNA tracts. Each hairpin is normalized to its own 100% fluorescence to ensure that any bias in ethidium binding does not affect assay results, and accurate results may be obtained with any sequence composition.
41. Boger, D. L.; Tse, W. C. Thiazole orange as the fluorescent intercalator in a high-resolution FID assay for determining DNA binding affinity and sequence selectivity of small molecules. Bioorg. Med. Chem. 2001, 9, 2511-2518.
42. Broude, N. E. Stem-loop oligonucleotides: a robust tool for molecular biology and biotechnology. Trends Biotechnol. 2002, 20, 249-256.
43. 260 at 90 °C/25 °C were determined to be 1.18, 1.13, 1.12, 1.12, 1.10, and 1.06 for the six combinations of 5-bp A/T sites contained in the 512 library: 5-bp AT, 4-bp AT/1 bp G/C, 3-bp AT/2-bp GC, 2-bp AT/3-bp GC, 1-bp AT/4-bp GC, and 5-bp GC, respectively.
44. Browne, K. A.; He, G. X.; Bruice, T. C. Microgonotropens and their interactions with DNA. 2. Quantitative evaluation of equilibrium constants for 1:1 and 2:1 binding of dien-microgonotropen-a, -b, and -c as well as distamycin and Hoechst-33258 to d(GGCGCAAATTTGGCGG)/d(CCGCCAAATTTGCGCC). J. Am. Chem. Soc. 1993, 115, 7072-7079.
45. Satz, A. L.; Bruice, T. C. Synthesis of fluorescent microgonotropens (FMGTs) and their interactions with dsDNA. Bioorg. Med. Chem. 2000, 8, 1871-1880.
46. Scatchard, G. Ann. N.Y. Acad. Sci. 1949, 51, 660.
47. Tse, W. C.; Ishii, T.; Boger, D. L. Comprehensive high-resolution analysis of hairpin polyamides utilizing a fluorescent intercalator displacement (FID) assay. Bioorg. Med. Chem. 2003, 11, 4479-4486.
48. Hawkins, C. A.; Pelaez de Clairac, R.; Dominey, R. N.; Baird, E. E.; White, S.; Dervan, P. B.; Wemmer, D. E. Controlling binding orientation in hairpin polyamide DNA complexes. J. Am. Chem. Soc. 2000, 122, 5235-5243.
49. Lacy, E. R.: Le, N. M.; Price, C. A.; Lee, M.; Wilson, W. D. Influence of a terminal formamido group on the sequence recognition of DNA by polyamides. J. Am. Chem. Soc. 2002, 124, 2153-2163.
50. Parks, M. E.; Baird, E. E.; Dervan, P. B. Optimization of the hairpin polyamide design for recognition of the minor groove of DNA. J. Am. Chem. Soc. 1996, 118, 6147-6152.
51. Boger, D. L.; Dechantsreiter, M. A.; Ishii, T.; Fink, B. E.; Hedrick, M. P. Assessment of solution-phase positional scanning libraries based on distamycin A for the discovery of new DNA binding agents. Bioorg. Med. Chem. 2000, 8, 2049-2057.
52. Dervan, P. B. Molecular recognition of DNA by small molecules. Bioorg. Med. Chem. 2001, 9, 2215-2235.
53. Woods, C. R.; Ishii, T.; Wu, B.; Bair, K. W.; Boger, D. L. Hairpin versus extended DNA binding of a substituted β-alanine linked polyamide. J. Am. Chem. Soc. 2002, 124, 2148-2152.
54. Woods, C. R.; Ishii, T.; Boger, D. L. Synthesis and DNA binding properties of iminodiacetic acid-linked polyamides: characterization of cooperative extended 2:1 side-by-side parallel binding. J. Am. Chem. Soc. 2002, 124, 10676-10682.
55. Wade, W. S.; Mrksich, M.; Dervan, P. B. Design of peptides that bind in the minor groove of DNA at 5′-(A,T)G(A,T)C(A,T)-3′ sequences by a dimeric side-by-side motif. J. Am. Chem. Soc. 1992, 114, 8783-8794.
56. Mrksich, M.; Wade, W. S.; Dwyer, T. J.; Geierstanger, B. H.; Wemmer, D. E.; Dervan, P. B. Antiparallel side-by-side dimeric motif for sequence-specific recognition in the minor groove of DNA by the designed peptide 1-methylimidazole-2-carboxamide netropsin. Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 7586-7590.
57. Wade, W. S.; Mrksich, M.; Dervan, P. B. Binding affinities of synthetic peptides, pyridine-2-carboxamidonetropsin and 1-methylimidazole-2-carboxamidonetropsin, that form 2:1 complexes in the minor groove of double-helical DNA. Biochemistry 1993, 32, 11385-11389.
58. Travis, A.; Amsterdam, A.; Belanger, C.; Grosschedl, R. LEF-1, a gene encoding a lymphoid-specific protein with an HMG domain, regulates T-cell receptor alpha enhancer function. Genes Dev. 1991, 5, 880-894.
59. Waterman, M. L.; Jones, K. A. Purification of TCF-1 alpha, a T-cell-specific transcription factor that activates the T-cell receptor C alpha gene enhancer in a context-dependent manner. New Biol. 1990, 2, 621-636.
60. Waterman, M. L.; Fischer, W. H.; Jones, K. A. A thymus-specific member of the HMG protein family regulates the human T cell receptor C alpha enhancer. Genes Dev. 1991, 5, 656-669.
61. van de Wetering, M.; Oosterwegel, M.; Dooijes, D.; Clevers, H. Identification and cloning of TCF-1, a T lymphocyte-specific transcription factor containing a sequence-specific HMG box. Embo J. 1991, 10, 123-132.
62. Grosschedl, R.; Giese, K.; Pagel, J. HMG domain proteins - Architectural elements in the assembly of nucleoprotein structures. Trends Genet. 1994, 10, 94-100.
63. Eastman, Q.; Grosschedl, R. Regulation of LEF-1/TCF transcription factors by Wnt and other signals. Curr. Opin. Cell. Biol. 1999, 11, 233-240.
64. Aoki, M.; Hecht, A.; Kruse, U.; Kemler, R.; Vogt, P. K. Nuclear endpoint of Wnt signaling: Neoplastic transformation induced by transactivating lymphoid-enhancing factor 1. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 139-144.
65. Giese, K.; Amsterdam, A.; Grosschedl, R. DNA-binding properties of the HMG domain of the lymphoid-specific transcriptional regulator LEF-1. Genes Dev. 1991, 5, 2567-2578.
66. Love, J. J.; Li, X. A.; Case, D. A.; Giese, K.; Grosschedl, R.; Wright, P. E. Structural basis for DNA bending by the architectural transcription factor LEF-1. Nature 1995, 376, 791-795.
67. Ham, Y. W.; Tse, W. C.; Boger, D. L. High-resolution assessment of protein DNA binding affinity and selectivity utilizing a fluorescent intercalator displacement (FID) assay. Bioorg. Med. Chem. Lett. 2003, 13, 3805-3807.
68. Yeung, B. K. S.; Tse, W. C.; Boger, D. L. Determination of binding affinities of triplex forming oligonucleotides using a fluorescent intercalator displacement (FID) assay, Bioorg. Med. Chem. Lett. 2003, 13, 3801-3804.