Spectroscopic, molecular modeling, and NMR-spectroscopic investigation of the binding mode of the natural alkaloids berberine and sanguinarine to human telomeric G-quadruplex DNA

ACS Chemical Biology

Volumn 7, Issue 6, 2012, Pages 1109-1119

  Bessi, Irene ^a,b   Bazzicalupi, Carla ^a   Richter, Christian ^b   Jonker, Hendrik R A ^b   Saxena, Krishna ^b   Sissi, Claudia ^c   Chioccioli, Matteo ^a   Bianco, Sara ^c   Bilia, Anna Rita ^a   Schwalbe, Harald ^b   Gratteri, Paola ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BERBERINE; GUANINE QUADRUPLEX; SANGUINARINE;

ANTINEOPLASTIC ACTIVITY; ARTICLE; DNA BINDING; DNA STRUCTURE; DRUG STRUCTURE; FLUORESCENCE; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; STOICHIOMETRY; TELOMERE;

BENZOPHENANTHRIDINES; BERBERINE; CIRCULAR DICHROISM; DNA; G-QUADRUPLEXES; HUMANS; ISOQUINOLINES; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; SPECTROMETRY, FLUORESCENCE;

EID: 84862587840     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb300096g     Document Type: Article

References (61)

1. Balasubramanian, S. and Neidle, S. (2009) G-quadruplex nucleic acids as therapeutic targets Curr. Opin. Chem. Biol. 13, 345-353
2. Ou, T. M., Lu, Y. J., Tan, J. H., Huang, Z. S., Wong, K. Y., and Gu, L. Q. (2008) G-quadruplexes: Targets in anticancer drug design ChemMedChem 3, 690-713
3. Neidle, S. (2010) Human telomeric G-quadruplex: The current status of telomeric G-quadruplexes as therapeutic targets in human cancer FEBS J. 277, 1118-1125
4. Lipps, H. J. and Rhodes, D. (2009) G-quadruplex structures: in vivo evidence and function Trends Cell Biol. 19, 414-422
5. De Cian, A., Lacroix, L., Douarre, C., Temime-Smaali, N., Trentesaux, C., Riou, J. F., and Mergny, J. L. (2008) Targeting telomeres and telomerase Biochimie 90, 131-155 (Pubitemid 350245369)
6. Arora, A., Kumar, N., Agarwal, T., and Maiti, S. (2010) Human telomeric G-quadruplex: targeting with small molecules (Retraction of vol 6, pg 627, 2008) FEBS J. 277, 1345
7. Efferth, T., Li, P. C. H., Konkimalla, V. S. B., and Kaina, B. (2007) From traditional Chinese medicine to rational cancer therapy Trends Mol. Med. 13, 353-361 (Pubitemid 47126989)
8. Franceschin, M., Rossetti, L., DAmbrosio, 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 (Pubitemid 43197550)
9. Arora, A., Balasubramanian, C., Kumar, N., Agrawal, S., Ojha, R. P., and Maiti, S. (2008) Binding of berberine to human telomeric quadruplex- spectroscopic, calorimetric and molecular modeling studies FEBS J. 275, 3971-3983 (Pubitemid 351990958)
10. Maiti, M. and Kumar, G. S. (2010) Polymorphic nucleic acid binding of bioactive isoquinoline alkaloids and their role in cancer. J Nucleic Acids 2010, DOI: 10.4061/2010/593408.
11. Bhadra, Kakali and Suresh, K. G. (2011) Interaction of berberine, palmatine, coralyne, and sanguinarine to quadruplex DNA: A comparative spectroscopic and calorimetric study Biochim. Biophys. Acta, Gen. Subj. 1810, 485-496
12. Liu, Y. Q., Zheng, B., Xu, X. J., and Yuan, G. (2010) Probing the binding affinity of small-molecule natural products to the G-quadruplex in C-myc oncogene by electrospray ionization mass spectrometry Rapid Commun. Mass Spectrom. 24, 3072-3075
13. Li, W., Zhang, M., Zhang, J. L., Li, H. Q., Zhang, X. C., Sun, Q., and Qiu, C. M. (2006) Interactions of daidzin with intramolecular G-quadruplex FEBS Lett. 580, 4905-4910 (Pubitemid 44308331)
14. Yang, S., Xiang, J., Yang, Q., Zhou, Q., Zhang, X., Li, Q., Tang, Y., and Xu, G. (2010) Distinct G-quadruplex structures of human telomeric DNA formed by the induction of sanguinarine and nitidine under salt-deficient condition Fitoterapia 81, 1026-1032
15. Bai, L. P., Hagihara, M., Jiang, Z. H., and Nakatani, K. (2008) Ligand binding to tandem G quadruplexes from human telomeric DNA ChemBioChem 9, 2583-2587
16. Petraccone, L., Garbett, N. C., Chaires, J. B., and Trent, J. O. (2010) An integrated molecular dynamics (MD) and experimental study of higher order human telomeric quadruplexes Biopolymers 93, 533-548
17. Hänsel, R., Löhr, F., Foldynova-Trantirkova, S., Bamberg, E., Trantirek, L., and Dötsch, V. (2011) The parallel G-quadruplex structure of vertebrate telomeric repeat sequences is not the preferred folding topology under physiological conditions Nucleic Acids Res. 39, 5768-5775
18. Dai, J. X., Carver, M., and Yang, D. Z. (2008) Polymorphism of human telomeric quadruplex structures Biochimie 90, 1172-1183
19. Phan, A. T. (2010) Human telomeric G-quadruplex: structures of DNA and RNA sequences FEBS J. 277, 1107-1117
20. Wang, Y. and Patel, D. J. (1993) Solution structure of the human telomeric repeat D[Ag(3)(T(2)Ag(3))3] G-tetraplex Structure 1, 263-282 (Pubitemid 2031126)
21. Dai, J. X., Punchihewa, C., Ambrus, A., Chen, D., Jones, R. A., and Yang, D. Z. (2007) Structure of the intramolecular human telomeric G-quadruplex in potassium solution: a novel adenine triple formation Nucleic Acids Res. 35, 2440-2450 (Pubitemid 47073725)
22. Dai, J. X., Carver, M., Punchihewa, C., Jones, R. A., and Yang, D. Z. (2007) Structure of the Hybrid-2 type intramolecular human telomeric G-quadruplex in K+ solution: insights into structure polymorphism of the human telomeric sequence Nucleic Acids Res. 35, 4927-4940 (Pubitemid 47394180)
23. Maiti, M., Nandi, R., and Chaudhuri, K. (1983) The effect of Ph on the absorption and fluorescence-spectra of sanguinarine Photochem. Photobiol. 38, 245-249
24. Jones, R. R., Harkrader, R. J., and Southard, G. L. (1986) The effect of pH on sanguinarine iminium ion form J. Nat. Prod. 49, 1109-1111 (Pubitemid 17041087)
25. Zhang, W. J., Ou, T. M., Lu, Y. J., Huang, Y. Y., Wu, W. B., Huang, Z. S., Zhou, J. L., Wong, K. Y., and Gu, L. Q. (2007) 9-Substituted berberine derivatives as G-quadruplex stabilizing ligands in telomeric DNA Bioorg. Med. Chem. 15, 5493-5501
26. Maiti, M. and Chaudhuri, K. (1981) Interaction of berberine chloride with naturally occurring deoxyribonucleic acids Indian J. Biochem. Biophys. 18, 245-250 (Pubitemid 12106786)
27. Tripathi, A. N., Chauhan, L., Thankachan, P. P., and Barthwal, R. (2007) Quantum chemical and nuclear magnetic resonance spectral studies on molecular properties and electronic structure of berberine and berberrubine Magn. Reson. Chem. 45, 647-655
28. Marek, R., Tousek, J., Dostal, J., Slavik, J., Dommisse, R., and Sklenar, V. (1999) H-1 and C-13 NMR study of quaternary benzo[ c ]phenanthridine alkaloids Magn. Reson. Chem. 37, 781-787
29. Dixon, I. M., Lopez, F., Esteve, J. P., Tejera, A. M., Blasco, M. A., Pratviel, G., and Meunier, B. (2005) Porphyrin derivatives for telomere binding and telomerase inhibition ChemBioChem 6, 123-132 (Pubitemid 40128645)
30. Buurma, N. J. and Haq, I. (2008) Calorimetric and spectroscopic studies of Hoechst 33258: Self-association and binding to non-cognate DNA J. Mol. Biol. 381, 607-621
31. Parkinson, G. N., Ghosh, R., and Neidle, S. (2007) Structural basis for binding of porphyrin to human telomeres Biochemistry 46, 2390-2397 (Pubitemid 46362413)
32. Parkinson, G. N., Cuenca, F., and Neidle, S. (2008) Topology conservation and loop flexibility in quadruplex-drug recognition: Crystal structures of inter- and intramolecular telomeric DNA quadruplex-drug complexes J. Mol. Biol. 381, 1145-1156
33. Campbell, N. H., Parkinson, G. N., Reszka, A. P., and Neidle, S. (2008) Structural basis of DNA quadruplex recognition by an acridine drug J. Am. Chem. Soc. 130, 6722
34. McGhee, J. D. and Von Hippel, P. H. (1974) Theoretical aspects of DNA-protein interactions: Co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice J. Mol. Biol. 86, 469-489
35. Hwang, T. L. and Shaka, A. J. (1995) Water suppression that works-Excitation sculpting using arbitrary wave-forms and pulsed-field gradients J. Magn. Reson. Ser. A 112, 275-279
36. Bax, A. and Davis, D. G. (1985) Practical aspects of two-dimensional transverse NOE spectroscopy J. Magn. Reson. 63, 207-213
37. Schleucher, J., Schwendinger, M., Sattler, M., Schmidt, P., Schedletzky, O., Glaser, S. J., Sorensen, O. W., and Griesinger, C. (1994) A general enhancement scheme in heteronuclear multidimensional NMR employing pulsed-field gradients J. Biomol. NMR 4, 301-306
38. Kay, L. E., Keifer, P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity J. Am. Chem. Soc. 114, 10663-10665
39. Palmer, A. G., Cavanagh, J., Wright, P. E., and Rance, M. (1991) Sensitivity improvement in proton-detected 2-dimensional heteronuclear correlation NMR-spectroscopy J. Magn. Reson. 93, 151-170
40. Sklenar, V. and Bax, A. (1987) Spin-Echo water suppression for the generation of pure-phase two-dimensional NMR-spectra J. Magn. Reson. 74, 469
41. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-Tailored Excitation for Single-Quantum NMR-Spectroscopy of Aqueous-Solutions J. Biomol. NMR 2, 661-666
42. 15N HSQC Experiments Optimized to Retain Full Sensitivity J. Magn. Reson. Ser. A 102, 241-245
43. Goddard, T. D. and Kneller, D. G. (2007) SPARKY 3, University of California, San Francisco.
44. Maestro v 8.5 (2007) Schrödinger, LLC, New York, NY.
45. Glide v. 4.5 (2007) Schrödinger, LLC, New York, NY.
46. Macromodel v. 9.6 (2008) Schrödinger, L.L.C., New York, NY.
47. Bayly, C. I., Cieplak, P., Cornell, W. D., and Kollman, P. A. (1993) A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges-the Resp model J. Phys. Chem. 97, 10269-10280
48. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Scalmani, G., Barone, V., Mennucci, B., Petersson, G. A., Nakatsuji, H., Caricato, M., Li, X., Hratchian, H. P., Izmaylov, A. F., Bloino, J., Zheng, G., Sonnenberg, J. L., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Vreven, T., Montgomery, Jr., J. A., Peralta, J. E., Ogliaro, F., Bearpark, M., Heyd, J. J., Brothers, E., Kudin, K. N., Staroverov, V. N., Kobayashi, R., Normand, J., Raghavachari, K., Rendell, A., Burant, J. C., Iyengar, S. S., Tomasi, J., Cossi, M., Rega, N., Millam, J. M., Klene, M., Knox, J. E., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C., Ochterski, J. W., Martin, R. L., Morokuma, K., Zakrzewski, V. G., Voth, G. A., Salvador, P., Dannenberg, J. J., Dapprich, S., Daniels, A. D., Farkas, Ö., Foresman, J. B., Ortiz, J. V., Cioslowski, J., and Fox, D. J. (2009) Gaussian 09, Revision A.01 ed., Gaussian, Inc., Wallingford, CT.
49. Case, D. A., Darden, T. A., Cheatham, T. E., III, Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Merz, K. M., Pearlman, D. A., Crowley, M., Walker, R. C., Zhang, W., Wang, B., Hayik, S., Roitberg, A., Seabra, G., Wong, K. F., Paesani, F., Wu, X., Brozell, S., Tsui, V., Gohlke, H., Yang, L., Tan, C., Mongan, J., Hornak, V., Cui, G., Beroza, P., Mathews, D. H., Schafmeister, C., Ross, W. S., and Kollman, P. A. (2006) AMBER 9, University of California, San Francisco, CA.
50. Duan, Y., Wu, C., Chowdhury, S., Lee, M. C., Xiong, G. M., Zhang, W., Yang, R., Cieplak, P., Luo, R., Lee, T., Caldwell, J., Wang, J. M., and Kollman, P. (2003) A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations J. Comput. Chem. 24, 1999-2012
51. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79, 926-935
52. Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., and Pedersen, L. G. (1995) A smooth particle mesh Ewald method J. Chem. Phys. 103, 8577-8593
53. Ryckaert, J. P., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical-integration of cartesian equations of motion of a system with constraints-molecular-dynamics of N-alkanes J. Comput. Phys. 23, 327-341
54. Berendsen, H. J. C., Postma, J. P. M, van Gunsteren, W. F., Dinola, A., and Haak, J. R. (1984) Molecular-dynamics with coupling to an external bath J. Chem. Phys. 81, 3684-3690
55. Dominguez, C., Boelens, R., and Bonvin, A. M. J. J. (2003) HADDOCK: A protein-protein docking approach based on biochemical or biophysical information J. Am. Chem. Soc. 125, 1731-1737 (Pubitemid 36232568)
56. van Dijk, M., van Dijk, A. D. J., Hsu, V., Boelens, R., and Bonvin, A. M. J. J. (2006) Information-driven protein-DNA docking using HADDOCK: it is a matter of flexibility Nucleic Acids Res. 34, 3317-3325
57. Schüttelkopf, A. W. and van Aalten, D. M. F. (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 1355-1363 (Pubitemid 41079731)
58. Linge, J. P., Williams, M. A., Spronk, C. A. E. M., Bonvin, A. M. J. J., and Nilges, M. (2003) Refinement of protein structures in explicit solvent Proteins: Struct., Funct., Bioinf, 50, 496-506 (Pubitemid 36158461)
59. Jorgensen, W. L. and Tirado-Rives, J. (1988) The OPLS force field for proteins. energy minimizations for crystals of cyclic peptides and crambin J. Am. Chem. Soc. 110, 1657-1666
60. Pranata, J., Wierschke, S. G., and Jorgensen, W. L. (1991) OPLS potential functions for nucleotide bases-relative association constants of hydrogen-bonded base-pairs in chloroform J. Am. Chem. Soc. 113, 2810-2819
61. Nozinovic, S., Fürtig, B., Jonker, H. R. A., Richter, C., and Schwalbe, H. (2010) High-resolution NMR structure of an RNA model system: the 14-mer cUUCGg tetraloop hairpin RNA Nucleic Acids Res. 38, 683-694