Simian virus 40 large T-antigen G-quadruplex DNA helicase inhibition by G-quadruplex DNA-interactive agents

Biochemistry

Volumn 47, Issue 7, 2008, Pages 1896-1909

  Tuesuwan, Bodin ^a   Kern, Jonathan T ^a,c   Thomas, Pei Wang ^a   Rodriguez, Mireya ^a   Li, Jing ^a   David, Wendi M ^b   Kerwin, Sean M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b Texas State University   (United States)

^c MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN-ANTIBODY REACTIONS; DNA; FLUORESCENCE SPECTROSCOPY; MOLECULAR INTERACTIONS; VIRUSES;

DUPLEX DNA HELICASE ACTIVITIES; INTRAMOLECULAR G-QUADRUPLEXES; PROTOTYPICAL REPLICATIVE HELICASE;

ENZYME INHIBITION;

ENZYME INHIBITOR; GENOMIC DNA; HELICASE; VIRUS DNA; VIRUS ENZYME; VIRUS LARGE T ANTIGEN;

ARTICLE; BINDING AFFINITY; COMPARATIVE STUDY; DNA CONFORMATION; DNA DENATURATION; DNA REPLICATION; DNA SEQUENCE; DNA STRUCTURE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SUBSTRATE; FLUORESCENCE SPECTROSCOPY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; SIMIAN VIRUS 40; SURFACE PLASMON RESONANCE; VIRUS GENOME; VIRUS REPLICATION;

ANTIGENS, POLYOMAVIRUS TRANSFORMING; BASE SEQUENCE; DNA; DNA HELICASES; DNA PRIMERS; SIMIAN VIRUS 40; SPECTROMETRY, FLUORESCENCE;

SIMIAN VIRUS 40;

EID: 39649090955     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701747d     Document Type: Article

References (79)

1. Kerwin, S. M. (2000) G-Quadruplex DNA as a target for drug design, Curr. Pharm. Des. 6, 441-471.
2. Kan, Z. Y., Yao, Y. A., Wang, P., Li, X. H., Hao, Y. H., and Tan, Z. (2006) Molecular crowding induces telomere G-quadruplex formation under salt-deficient conditions and enhances its competition with duplex formation, Angew. Chem., Int. Ed. 45, 1629-1632.
3. Phan, A. T., and Mergny, J. L. (2002) Human telomeric DNA: G-quadruplex, i-motif, and Watson-Crick double helix, Nucleic Acids Res. 30, 4618-4625
4. Li, W., Miyoshi, D., Nakano, S., and Sugimoto, N. (2003) Structural competition involving G-quadruplex DNA and its complement, Biochemistry 42, 11736-11744.
5. Davis, J. T. (2004) G-quartets 40 years later: From 5′-GMP to molecular biology and supramolecular chemistry, Angew. Chem., Int. Ed. 43, 668-698.
6. Huppert, J. L., and Balasubramanian, S. (2005) Prevalence of quadruplexes in the human genome, Nucleic Acids Res. 33, 2908-2916.
7. Todd, A. K., Johnston, M., and Neidle, S. (2005) Highly prevalent putative quadruplex sequence motifs in human DNA, Nucleic Acids Res. 33, 2901-2907.
8. Duquette, M. L., Huber, M. D., and Maizels, N. (2007) G-rich proto-oncogenes are targeted for genomic instability in B-cell lymphomas, Cancer Res. 67, 2586-2594.
9. Fry, M., and Leob, L. A. (1994) The fragile X syndrome d(CGG)-n nucleotide repeats form a stable tetrahelical structure, Proc. Natl. Acad. Sci. U.S.A. 91, 4950-4954.
10. Saha, T., and Usdin, K. (2001) Tetraplex formation by the progressive myoclonus epilepsy type-1 repeat: Implications of instability in the repeat expansion diseases, FEBS Lett. 491, 184-187.
11. Eddy, J., Maizels, N. (2006) Gene function correlates with potential for G4 DNA formation in the human genome, Nucleic Acids Res. 34, 3887-3896.
12. Rawal, P., Kummarasetti, V. B. R., Ravindran, J., Kumar, N., Halder, K., Sharma, R., Mukerji, M., Das, S. K., and Chowdhury, S. (2006) Genome-wide prediction of G4 DNA as regulatory motifs: Role in Escherichia coli global regulation, Genome Res. 644-655.
13. Duquette, M. L., Handa, P., Vincent, J. A., Taylor, A. F., and Maizels, N. (2004) Intracellular transcription of G-rich DNA induces formation of G-quadruplex DNA structures in vivo, Genes Dev. 18, 1618-1629.
14. Oganesian, L., and Bryan, T. M. (2007) Physiological relevance of telomeric G-quadruplex formation: A potential drug target, BioEssays 29, 155-165.
15. Wu, X., and Maizels, N. (2001) Substrate-specific inhibition of RecQ helicase, Nucleic Acids Res. 29, 1765-1771.
16. Sun, H., Bennett, R. J., and Maizels, N. (1999) The Saccharomyces cerevisiae Sgs1 helicase efficiently unwinds G-G paired DNAs, Nucleic Acids Res. 27, 1978-1984.
17. Sun, H., Karow, J. K., Hickson, I. D., and Maizels, N. (1998) The Bloom's syndrome helicase unwinds G4 DNA, J. Biol. Chem. 273, 27587-27592.
18. Fry, M., and Loeb, L. A. (1999) Human Werner syndrome DNA helicase unwinds tetrahelical structures of the fragile X syndrome repeat sequence d(CGG)n, J. Biol. Chem. 274, 12797-12802.
19. Huber, M. D., Duquette, M. L., Shiels, J. C., and Maizels, N. (2006) A conserved G4 DNA binding domain in RecQ family helicases, J. Mol. Biol. 358, 1071-1080.
20. Vaughn, J. P., Creacy, S. D., Routh, E. D., Joyner-Butt, C., Jenkins, G. S., Pauli, S, Nagamine, Y., and Akman, S. A. (2005) The DEXH protein product of DHX36 gene is the major source of tetramolecular quadruplex G4-DNA resolving activity in HeLa cell lysates, J. Biol. Chem. 280, 38117-38120.
21. Simmons, D. T. (2000) SV40 large T antigen functions in DNA replication and transformation, Adv. Virus Res. 55, 75-133.
22. Li, J. J., and Kelly, T. J. (1984) Siman virus 40 DNA replication in vitro, Proc. Natl. Acad. Sci. U.S.A. 81, 6973-6977.
23. Dziegielewska, B., Kowalski, D., and Beerman, T. A. (2004) SV40 DNA replication inhibition by the monofunctional DNA alkylator Et743, Biochemistry 43, 14228-14237.
24. Bullock, P. A. (1997) The initiation of Simian Virus 40 DNA replication in vitro, Crit. Rev. Biochem. Mol. Biol. 32, 503-568.
25. Baran, N., Pucshansky, L., Marco, Y., Benjamin, S., and Manor, H. (1997) The SV40 large T-antigen helicase can unwind four stranded DNA structures linked by G-quartets, Nucleic Acids Res. 25, 297-303.
26. Patel, P. K., Bhavesh, N. S., and Hosur, R. V. (2000) NMR observation of a novel C-tetrad in the structure of the SV40 repeat sequence GGGCGG, Biochem. Biophys. Res. Commun. 270, 967-971.
27. Dapic, V., Abdomerovic, V., Marrington, R., Peberdy, J., Rodger, A., Trent, J. O., and Bates, P. J. (2003) Biophysical and biological properties of quadruplex oligodeoxyribonucleotides, Nucleic Acids Res. 31, 2097-2107.
28. Xu, X., Hamhouyia, F., Thomas, S. D., Burke, T. J., Girvan, A. C., McGregor, W. G., Trent, J. O., Miller, D. M., and Bates, P. J. (2001) Inhibition of DNA replication and induction of S phase cell cycle arrest by G-rich oligonucleotides, J. Biol. Chem. 276, 43221-43230.
29. Hardin, C. C., Perry, A. G., and White, K. (2001) Thermodynamics and kinetic characterization of the dissociation and assembly of quadruplex nucleic acids, Biopolymers 56, 147-194.
30. Han, H. Y., Hurley, L. H., and Salazar, M. (1999) A DNA polymerase stop assay for G-quadruplex-interactive compounds, Nucleic Acids Res. 27, 537-542.
31. Fedoroff, O. Y., Salazar, M., Han, H. Y., Chemeris, V. V., Kerwin, S. M., and Hurley, L. H. (1998) NMR model of a telomerase-inhibiting compound bound to G-quadruplex DNA, Biochemistry 37, 12367-12374.
32. Kern, J. T., and Kerwin, S. M. (2002) The aggregation and G-quadruplex DNA selectivity of charged 3,4,9,10-perylenetetracarboxylic acid diimides, Bioorg. Med. Chem. Lett. 12, 3395-3398.
33. Tuntiwechapikul, W., and Salazar, M. (2001) Cleavage of telomeric G-quadruplex DNA with perylene-EDTA-Fe(II), Biochemistry 40, 13652-13658.
34. Rossetti, L., Franceschin, M., Schirripa, S., Bianco, A., Ortaggi, G., and Savino, M. (2005) Selective interactions of perylene derivatives having different side chains with inter- and intramolecular G-quadruplex DNA structures. A correlation with telomerase inhibition, Bioorg. Med Chem. Lett. 15, 413-420.
35. Tuntiwechapikul, W., Taka, T., Bethencourt, M., Makonkawkeyoon, L., and Lee, T. R. (2006) The influence of pH on the G-quadruplex binding selectivity of perylene derivatives, Bioorg. Med. Chem. Lett. 16, 4120-4126.
36. Samudrala, R., Zhang, X., Wadkins, R. M., and Mattern, D. L. (2007) Synthesis of a non-cationic, water-soluble perylenetetracarboxylic diimide and its interactions with G-quadruplex-forming DNA, Bioorg. Med. Chem. 15, 186-193.
37. Sissi, C., Lucatello, L., Krapcho, A. P., Maloney, D. J., Boxer, M. B., Camarasa, M. V., Pezzoni, G., Menta, E., and Palumbo, M. (2007) Tri-, tetra-, and heptacyclic perylene analogues as new potential antineoplastic agents based on DNA telomerase inhibition, Bioorg. Med. Chem. 15, 555-562.
38. Kern, J. T., Thomas, P. W., and Kerwin, S. M. (2002) The relationship between ligand aggregation and G-quadruplex DNA selectivity in a series of 3,4,9,10-perylenetetracarboxylic acid diimides, Biochemistry 41, 11379-11389.
39. David, W. M., Brodbelt, J., Kerwin, S. M., and Thomas, P. W. (2002) Investigation of quadruplex oligonucleotide-drug interactions by electrospray ionization-mass spectrometry, Anal. Chem. 74, 2029-2033.
40. Gupta, R., and Brosh, R. M., Jr. (2007) DNA repair helicases as targets for anti-cancer therapy, Curr. Med. Chem. 14, 503-517.
41. Huber, M. D., Lee, D. C., and Maizels, N. (2002) G4 DNA unwinding by Blm and Sgs1p: Substrate specificity and substrate-specific inhibition, Nucleic Acids Res. 30, 3954-3961.
42. Li, J. L., Harrison, R. J., Reszka, A. P., Brosh, R. M., Bohr, V. A., Neidle, S., and Hickson, I. D. (2001) Inhibition of the Bloom's and Werner's syndrome helicases by G-quadruplex interacting ligands, Biochemistry 40, 15194-15202.
43. Cocco, M. J., Hanakahi, L. A., Huber, M. D., and Maizels, N. (2003) Specific interactions of distamycin with G-quadruplex DNA, Nucleic Acids Res. 31, 2944-2951.
44. Han, H. Y., Bennett, R. J., and Hurley, L. H. (2000) Inhibition of unwinding of G-quadruplex structures by Sgs1 helicase in the presence of N,N′-bis[2-(1-piperidino)ethyl]-3,4,9,10-perylenetetracarboxylic diimide, a G-quadruplex-interactive ligand, Biochemistry 39, 9311-9316.
45. Stootman, F. H., Fisher, D. M., Rodger, A., and Aldrich-Wright, J. R. (2006) Improved curve fitting procedures to determine equilibrium binding constants, Analyst 131, 1145-1151.
46. Mazzitelli, C. L., Rodriguez, M., Kern, J. T., Kerwin, S. M., and Brodbelt, J. S. (2006) Evaluation of binding of perylene diimide and benzannulated perylene diimide ligands to DNA by electrospray ionization mass spectrometry, J. Am. Soc. Mass Spectrom. 17, 593-604.
47. Franceschin, M., Alvino, A., Casagrande, V., Mauriello, C., Pascucci, E., Savino, M., Ortaggi, G., and Bianco, A. (2007) Specific interactions with intra- and intermolecular G-quadruplex DNA structures by hydrosoluble coronene derivatives: A new class of telomerase inhibitors, Bioorg. Med. Chem. 15, 1848-1858.
48. Sadrai, M., Hadel, L., Sauers, R. R., Husain, S., Krogh-Jespersen, K., Westbrook, J. D., and Bird, G. R. (1992) Lasing action in a family of perylene derivatives: Singlet absorption and emission spectra, triplet absorption and oxygen quenching constants, and molecular mechanics and semiempirical molecular-orbital calculations, J. Phys. Chem. 96, 7988-7996.
49. Molecular mechanics calculations were carried out to confirm the prediction that the twisted chromophore of Tel18, particularly the (M)-enantiomer, could still effectively interact with the terminal G-tetrads of G-quadruplex DNA.
50. Langhals, H., and Kirner, S. (2000) Novel fluorescent dyes by the extension of the core of perylenetetracarboxylic bisimides, Eur. J. Org. Chem. 365-380.
51. This is not the case with appropriate intramolecular G-quadruplex helicase substrates with 3′-tails, which are not well-resolved from single-stranded DNA on nondenaturing PAGE (data not shown).
52. Immunochromatography-purified recombinant T-ag expressed in Sf9 insect cells was kindly provided by Prof. Daniel Simmons, University of Delaware, and was prepared according to: Simmons, D. T., Melendy, T., Usher, D., and Stillman, D. (1996) Simian virus 40 large T antigen binds to topoisomerase I, Virology 222, 365-374.
53. Kouzine, F., and Levens, D. (2007) Supercoil-driven DNA structures regulate genetic transactions, Front. Biosci. 12, 4409-4423
54. Scaria, V., Hariharan, M., Arora, A., Maiti, S., Kikin, O., D'Antonio, L., and Bagga, P. S. (2006) Quadfinder: Server for identification and analysis of quadruplex-forming motifs in nucleotide sequences, Nucleic Acids Res. 34, 683-685.
55. Kikin, O., D'Antonio, L., and Bagga, P. (2006) SQGRS Mapper: A web-based server for predicting G-quadruplexes in nucleotide sequences, Nucleic Acids Res. 34, 676-682.
56. Lednicky, J., and Folk, W. R. (1992) Two synthetic Sp1-binding sites functional substitute for the 21-base-pair repeat region to activate simian virus growth in CV-1 cells, J. Virol. 66, 6379-6390.
57. Han, H., Langley, D. R., Rangan, A., and Hurley, L. H. (2001) Selective interactions of cationic porphyrins with G-quadruplex structures, J. Am. Chem. Soc. 123, 8902-8913.
58. Chen, Q., Kuntz, I. D., and Shafer, R. H. (1996) Spectroscopic recognition of guanine dimeric hairpin quadruplexes by a carbocyanine dye, Proc. Natl. Acad. Sci. U.S.A. 93, 2635-2639.
59. Cheng, J.-Y., Lin, S.-H., and Chang, T.-C. (1998) Vibrational investigation of DODC cation for recognition of guanine dimeric hairpin quadruplex studied by satellite holes, J. Phys. Chem. B 102, 5542-5546.
60. Franceschin, M., Rossetti, L., D'Ambrosio, A., Schirripa, S., Bianco, A., Ortaggi, G., Savino, M., Schultes, C., and Neidle, S. (2006) Natural and synthetic G-quadruplex interactive berberine derivatives, Bioorg. Med. Chem. Lett. 16, 1707-1711.
61. Maiti, S., Chaudhury, N. K., and Chowdhury, S. (2003) Hoechst 33258 binds to G-quadruplex in the promoter region of human c-myc, Biochem. Biophys. Res. Commun. 310, 505-512.
62. Kerwin, S. M., Sun, D., Kern, J. T., Rangan, A., and Thomas, P. W. (2001) G-quadruplex DNA binding by a series of carbocyanine dyes, Bioorg. Med. Chem. Lett. 11, 2411-2414.
63. Brosh, R. M., Jr., Karow, J. K., White, E. J., Shaw, N. D., Hickson, I. D., and Bohr, V. A. (2000) Potent inhibition of Werner and Bloom helicases by DNA minor groove binding drugs, Nucleic Acids Res. 28, 2420-2430.
64. Pothukuchy, A., Mazzitelli, C. L., Rodriguez, M. L., Tuesuwan, B., Salazar, M., Brodbelt, J. S., and Kerwin, S. M. (2005) Duplex and quadruplex DNA binding and photocleavage by trioxatriangulenium ion, Biochemistry 44, 2163-2172.
65. Guo, Q., Lu, M., Marky, L. A., and Kallenbach, N. R. (1992) Interaction of the dye ethidium bromide with DNA containing guanine repeats, Biochemistry 31, 2451-2455.
66. Rosu, F., De Pauw, E., Guittat, L., Alberti, P., Lacroix, L., Mailliet, P., Riou, J.-F., and Mergny, J.-L. (2003) Selective interaction of ethidium derivatives with quadruplexes: An equilibrium dialysis and electrospray ionization mass spectrometry analysis, Biochemistry 42, 10361-10371.
67. Bachur, N. R., Yu, F., Johnson, R., Hickey, R., Wu, Y., and Malkas, L. (1992) Helicase inhibition by anthracycline anticancer agents, Mol. Pharmacol. 41, 993-998.
68. 4, Chem. Commun. 11, 1030-1031.
69. McGovern, S. L., Helfand, B. T., Feng, B., and Shoichet, B. K. (2003) A specific mechanism of nonspecific inhibition, J. Med. Chem. 46, 4265-4272.
70. Arthanari, H., Basu, S., Kawano, T. L., and Bolton, P. H. (1998) Fluorescent dyes specific for quadruplex DNA, Nucleic Acids Res. 26, 3724-3728.
71. Pasternack, R. F., Goldsmith, J. I., Szep, S., and Gibbs, E. J. (1998) A spectroscopic and thermodynamic study of porphyrin/DNA supramolecular assemblies, Biophys. J. 75, 1024-1031.
72. Raymond, E., Soria, J.-C., Izbicka, E., Boussin, F., Hurley, L., and Von Hoff, D. D. (2000) DNA G-quadruplexes, telomere-specific proteins, and telomere-associated enzymes as potential targets for new anticancer drugs, Invest. New Drugs 18, 123-137.
73. Neidle, S., and Parkinson, G. (2002) Telomere maintenance as a target for anticancer drug discovery, Nat. Rev. Drug Discov. 1, 383-393.
74. Shay, J. W., and Wright, W. E. (2006) Telomerase therapeutics for cancer: Challenges and new directions, Nat. Rev. Drug Discov. 5, 577-584.
75. Hurley, L. H. (2001) Secondary DNA-structures as molecular targets for cancer therapeutics, Biochem. Soc. Trans. 29, 692-696.
76. Sun, D., Guo, K., Rusche, J. J., and Hurley, L. H. (2005) Facilitation of a structural transition in the polypurine/polypyrimidine tract within the proximal promoter region of the human VEGF gene by the presence of potassium and G-quadruplex-interactive agents, Nucleic Acids Res. 33, 6070-6080.
77. Rankin, S., Reszka, A. P., Huppert, J., Zloh, M., Parkinson, G. N., Todd, A. K., Ladame, S., Balasubramanian, S., and Neidle, S. (2005) Putative DNA quadruplex formation within the human c-kit oncogene, J. Am. Chem. Soc. 127, 10584-10589.
78. Siddiqui-Jain, A., Grand, C. L., Bearss, D. J., and Hurley, L. H. (2002) Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription, Proc. Natl. Acad. Sci. U.S.A. 99, 11593-11598.
79. Phan, A. T., Modi, Y. S., and Patel, D. J. (2004) Propeller-type parallel-stranded G-quadruplexes in the human c-myc promoter, J. Am. Chem. Soc. 126, 8710-8716.