Targeting human telomeric DNA quadruplex with novel berberrubine derivatives: insights from spectroscopic and docking studies

References

• Artese, A., Costa, G., Distinto, S., Moraca, F., Ortuso, F., Parrotta, L., & Alcaro, S. (2013). Identification of new natural DNA G-quadruplex binders selected by a structure-Based virtual screening approach. European Journal of Medicinal Chemistry, 68, 139–149. doi:10.1016/j.ejmech.2013.07.022
   PubMed Web of Science ®Google Scholar
• Balasubramanian, S., Hurley, L. H., & Neidle, S. (2011). Targeting G-quadruplexes in gene promoters: A novel anticancer strategy? Nature Reviews Drug Discovery, 10, 261–275. doi:10.1038/nrd3428
   PubMed Web of Science ®Google Scholar
• Barone, V., & Cossi, M. (1998). Quantum calculation of molecular energies and energy gradients in solution by a conductor solvent model. Journal of Physical Chemistry A, 102, 1995–2001. doi:10.1021/jp9716997
   Web of Science ®Google Scholar
• Basu, P., & Suresh Kumar, G. (2015). Structural and thermodynamic basis of interaction of the putative anticancer agent chelerythrine with single, double and triple-stranded RNAs. RSC Advances, 5, 29953–29964. doi:10.1039/C5RA00660K
   Web of Science ®Google Scholar
• Basu, A., Jaisankar, P., & Suresh Kumar, G. (2012). Synthesis of novel 9-O-N-aryl/aryl–alkyl amino carbonyl methyl substituted berberine analogs and evaluation of DNA binding aspects. Bioorganic & Medicinal Chemistry, 20, 2498–2505. doi:10.1016/j.bmc.2012.03.006
   PubMedGoogle Scholar
• Bauernschmitt, R., & Ahlrichs, R. (1996). Treatment of electronic excitations within the adiabatic approximation of time dependent density functional theory. Chemical Physics Letters, 256, 454–464. doi:10.1016/0009-2614(96)00440-X
   Web of Science ®Google Scholar
• Becke, A. D. (1993). Density-functional thermochemistry. III. The role of exact exchange. Journal of Chemical Physics, 98, 5648–5652. doi:10.1063/1.464913
   Web of Science ®Google Scholar
• Bhowmik, D., Hossain, M., Buzzetti, F., D’Auria, R., Lombardi, P., & Suresh Kumar, G. (2012). Biophysical studies on the effect of the 13 position substitution of the anticancer alkaloid berberine on its DNA binding. The Journal of Physical Chemistry B, 116, 2314–2324. doi:10.1021/jp210072a
   PubMed Web of Science ®Google Scholar
• Bhowmik, D., Buzzetti, F., Fiorillo, G., Orzi, F., Syeda, T. M., Lombardi, P., & Suresh Kumar, G. (2014). Synthesis of new 13-diphenylalkyl analogues of berberine and elucida- tion of their base pair specificity and energetics of DNA binding. Medicinal Chemistry Communication, 5, 226–231. doi:10.1039/C3MD00254C
   Google Scholar
• Bhowmik, D., Fiorillo, G., Lombardi, P., & Suresh Kumar, G. (2015). Recognition of human telomeric G-quadruplex DNA by berberine analogs: Effect of substitution at the 9 and 13 positions of the isoquinoline moiety. Journal of Molecular Recognition, 28, 722–730. doi:10.1002/jmr.2486
   PubMed Web of Science ®Google Scholar
• Casida, M. E., Jamoroski, C., Casida, K. C., & Salahub, D. R. (1998). Molecular excitation energies to high-lying bound states from time-dependent density-functional response theory: Characterization and correction of the time-dependent local density approximation ionization threshold. Journal of Chemical Physics, 108, 4439–4449. doi:10.1063/1.475855
   Web of Science ®Google Scholar
• Cossi, M., & Barone, V. (2001). Time-dependent density functional theory for molecules in liquid solutions. Journal of Chemical Physics, 115, 4708–4717. doi:10.1063/1.1394921
   Web of Science ®Google Scholar
• Cossi, M., Rega, N., Scalmani, G., & Barone, V. (2003). Energies, structures, and electronic properties of molecules in solution with the CPCM solvation model. Journal of Computational Chemistry, 24, 669–681.10.1002/jcc.10189
   PubMed Web of Science ®Google Scholar
• Ferraroni, M., Bazzicalupi, C., Papi, F., Fiorillo, G., Guaman-Ortiz, L. M., Nocentini, A., … Gratteri, P. (2016). Solution and solid-state analysis of binding of 13-substituted berberine analogues to Human telomeric G-quadruplexes. Chemistry – An Asian Journal, 11, 1107–1115. doi:10.1002/asia.201600116
   PubMed Web of Science ®Google Scholar
• Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., & Petersson, G. A. (2009). Gaussian 09, revisions B. 01 and A. 02. Wallingford, CT: Gaussian.
   Google Scholar
• Haider, S. M., Parkinson, G. N., & Neidle, S. (2003). Structure of a G-quadruplex–ligand complex. Journal of Molecular Biology, 326, 117–125. doi:10.1016/S0022-2836(02)01354-2
   PubMed Web of Science ®Google Scholar
• Huang, C. Y. (1982). Determination of Binding Stoichiometry by the Continuous Variation Method: The Job Plot. Methods in Enzymology, 87, 509–525.
   PubMed Web of Science ®Google Scholar
• Izbicka, E., Wheelhouse, R. T., Raymond, E., Davidson, K. K., Lawrence, R. A., Sun, D., … Von Hoff, D. D. (1999). Effects of cationic porphyrins as G-quadruplex interactive agents in human tumor cells. Cancer Research, 59, 639–644.
   PubMed Web of Science ®Google Scholar
• Job, P. (1928). Formation and stability of inorganic complexes in solution. Annali di Chimica Applicata., 9, 113–203.
   Google Scholar
• Jokar, M., Safaralizadeh, M. H., Hadizadeh, F., Rahmani, F., & Kalani, M. R. (2017). Apta-nanosensor preparation and in vitro assay for rapid Diazinon detection using a computational molecular approach. Journal of Biomolecular Structure and Dynamics, 35, 343–353. doi:10.1080/07391102.2016.1140594
   PubMed Web of Science ®Google Scholar
• Kerwin, S. M., Sun, D., Kern, J. T., Rangan, A., & Thomas, P. W. (2001). G-quadruplex DNA binding by a series of carbocyanine dyes. Bioorganic & Medicinal Chemistry Letters, 11, 2411–2414. doi:10.1016/S0960-894X(01)00490-5
   PubMed Web of Science ®Google Scholar
• Kobayashi, Y., Yamashita, Y., Fujii, N., Takaboshi, K., Kawakami, T., Kawamura, M., … Nakano, H. (1995). Inhibitors of DNA topoisomerase I and II isolated from the Coptis rhizomes. Planta Medica, 61, 414–418. doi:10.1055/s-2006-958127
   PubMed Web of Science ®Google Scholar
• Lee, C., Yang, W., & Parr, R. G. (1998). Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Physical Review B, 37, 785–789. doi:10.1103/PhysRevB.37.785
   Web of Science ®Google Scholar
• Lim, K. W., Amrane, S., Bouaziz, S., Xu, W., Mu, Y., Patel, D. J., … Phan, A. T. (2009). Structure of the human telomere in K+ solution: A stable basket-type G-quadruplex with only two G-tetrad layers. Journal of the American Chemical Society, 131, 4301–4309. doi:10.1021/ja807503g
   PubMed Web of Science ®Google Scholar
• Liu, Y., Cheng, D., Ge, Min, & Lin, W. (2016). The truncated human telomeric sequence forms a hybrid-type intramolecular mixed parallel/antiparallel G-quadruplex structure in K+ solution. Chemical Biology & Drug Design, 88, 122–128. doi:10.1111/cbdd.12740
   PubMed Web of Science ®Google Scholar
• Maji, B., & Bhattacharya, S. (2014). Advances in the molecular design of potential anticancer agents via targeting of human telomeric DNA. Chemical Communications, 50, 6422–6438. doi:10.1039/C4CC00611A
   PubMed Web of Science ®Google Scholar
• Mikutis, G., Karakose, H., Jaiswal, R., LeGresley, A., Islam, T., Fernandez-Lahore, M., & Kuhnert, N. (2013). Phenolic promiscuity in the cell nucleus–epigallocatechingallate (EGCG) and theaflavin-3,3′-digallate from green and black tea bind to model cell nuclear structures, including histone proteins, double stranded DNA and telomeric quadruplex DNA. Food & Functions, 4, 328–337. doi:10.1039/c2fo30159h
   PubMed Web of Science ®Google Scholar
• Mitrasinovic, P. M. (2017). Structural insights into the binding of small ligand molecules to a G-quadruplex DNA located in the HIV-1 promoter. Journal of Biomolecular Structure and Dynamics. doi:10.1080/07391102.2017.1358670
   PubMed Web of Science ®Google Scholar
• Mohanty, J., Barooah, N., Dhamodharan, V., Harikrishna, S., Pradeepkumar, P. I., & Bhasikuttan, A. C. (2013). Thioflavin T as an efficient inducer and selective fluorescent sensor for the human telomeric G-quadruplex DNA. Journal of the American Chemical Society, 135, 367–376. doi:10.1021/ja309588h
   PubMed Web of Science ®Google Scholar
• Monchaud, D., Allain, C., & Teulade-Fichou, M. P. (2007). Thiazole orange: A useful probe for fluorescence sensing of G-quadruplex–ligand interactions. Nucleosides, Nucleotides, and Nucleic Acids, 26, 1585–1588. doi:10.1080/15257770701548212
   PubMed Web of Science ®Google Scholar
• Moyzis, R. K., Buckingham, J. M., Cram, L. S., Dani, M., Deaven, L. L., Jones, M. D., … Wu, J. R. (1988). A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proceedings of the National Academy of Sciences of the United States of America, 85, 6622–6626.10.1073/pnas.85.18.6622
   PubMed Web of Science ®Google Scholar
• O’Boyle, N. M., Tenderholt, A. L., & Langner, K. M. (2008). cclib: A library for package-independent computational chemistry algorithms. Journal of Computational Chemistry, 29, 839–845. doi:10.1002/jcc.20823
   PubMed Web of Science ®Google Scholar
• Padmapriya, K., & Barthwal, R. (2016). Binding of the alkaloid coralyne to parallel G-quadruplex DNA [d(TTGGGGT)]4 studied by multi-spectroscopic techniques. Biophysical Chemistry, 219, 49–58. doi:10.1016/j.bpc.2016.09.006
   PubMed Web of Science ®Google Scholar
• Park, K. D., Lee, J. H., Kim, S. H., Kang, T. H., Sun Moon, J., & Kim, S. U. (2006). Synthesis of 13-(substituted benzyl) berberine and berberrubine derivatives as antifungal agents. Bioorganic & Medicinal Chemistry Letters, 16, 3913–3916. doi:10.1016/j.bmcl.2006.05.033
   PubMed Web of Science ®Google Scholar
• Parr, R. G., & Yang, W. (1989). Density functional theory of atoms and molecules. New York, NY: Oxford University Press.
   Google Scholar
• Paul, P., & Suresh Kumar, G. (2012). Thionine interaction to DNA: Comparative spectroscopic studies on double stranded versus single stranded DNA. Journal of Fluorescence, 22, 71–80. doi:10.1007/s10895-011-0931-2
   PubMed Web of Science ®Google Scholar
• Pierpaoli, E., Arcamone, A. G., Buzzetti, F., Lombardi, P., Salvatore, C., & Provinciali, M. (2013). Antitumor effect of novel berberine derivatives in breast cancer cells. BioFactors, 39, 672–679. doi:10.1002/biof.1131
   PubMed Web of Science ®Google Scholar
• Radhika, R., Shankar, R., Vijayakumar, S., & Kolandaivel, P. (2017). Role of 6-Mercaptopurine in the potential therapeutic targets DNA base pairs and G-quadruplex DNA: Insights from quantum chemical and molecular dynamics simulations. Journal of Biomolecular Structure and Dynamics. doi:10.1080/07391102.2017.1323013
   PubMed Web of Science ®Google Scholar
• Read, M. A., Wood, A. A., Harrison, J. R., Gowan, S. M., Kelland, L. R., Dosanjh, H. S., & Neidle, S. (1999). Molecular modeling studies on G-quadruplex complexes of telomerase inhibitors: Structure-activity relationships. Journal of Medicinal Chemistry, 42, 4538–4546. doi:10.1021/jm990287e
   PubMed Web of Science ®Google Scholar
• Shi, S., Huang, H.-L., Gao, X., Yao, J.-L., Lv, C.-Y., Zhao, J., … Ji, L.-N. (2013). A comparative study of the interaction of two structurally analogous ruthenium complexes with human telomeric G-quadruplex DNA. Journal of Inorganic Biochemistry, 121, 19–27. doi:10.1016/j.jinorgbio.2012.12.011
   PubMed Web of Science ®Google Scholar
• Shirani, M. P., Rezaei, B., Khayamian, T., Dinari, M., Karami, K., Mehri-Lighvan, Z., … Alibolandi, M. (2017). Folate receptor-targeted multimodal fluorescence mesosilica nanoparticles for imaging, delivery palladium complex and in vitro G-quadruplex DNA interaction. Journal of Biomolecular Structure and Dynamics. doi:10.1080/07391102.2017.1411294
   Web of Science ®Google Scholar
• Singh, A., & Kukreti, S. (2017). A triple stranded G-quadruplex formation in the promoter region of human myosin β(Myh7). Journal of Biomolecular Structure and Dynamics. doi:10.1080/07391102.2017.1374211
   Web of Science ®Google Scholar
• Spinozzi, S., Colliva, C., Camborata, C., Roberti, M., Ianni, C., Neri, F., … Roda, A. (2014). Berberine and its metabolites: relationship between physicochemical properties and plasma levels after administration to human subjects. Journal of Natural Products, 77, 766–772. doi:10.1021/np400607k
   PubMed Web of Science ®Google Scholar
• Stratmann, R. E., Scuseria, G. E., & Frisch, M. J. (1998). An efficient implementation of time-dependent density-functional theory for the calculation of excitation energies of large molecules. Journal of Chemical Physics, 109, 8218–8224. doi:10.1063/1.477483
   Web of Science ®Google Scholar
• Sun, D., Thompson, B., Cathers, B. E., Salazar, M., Kerwin, S. M., Trent, J. O., … Hurley, L. H. (1997). Inhibition of human telomerase by a G-quadruplex interactive compound. Journal of Medicinal Chemistry, 40, 2113–2116. doi:10.1021/jm970199z
   PubMed Web of Science ®Google Scholar
• Tripathi, A. N., Chauhan, L., Thankachan, P. P., & Barthwal, R. (2007). Quantum chemical and nuclear magnetic resonance spectral studies on molecular properties and electronic structure of berberine and berberrubine. Magnetic Resonance in Chemistry, 45, 647–655. doi:10.1002/mrc.2019
   PubMed Web of Science ®Google Scholar
• Vieira, S., Castelli, S., Falconi, M., Takarada, J., Fiorillo, G., Buzzetti, F., … Desideri, A. (2015). Role of 13-(di)phenylalkyl berberine derivatives in the modulation of the activity of human topoisomerase IB. International Journal of Biological Macromolecules, 77, 68–75. doi:10.1016/j.ijbiomac.2015.02.051
   PubMed Web of Science ®Google Scholar
• Vivek Kumar, S., Muthusubramanian, S., & Perumal, S. (2015). A solvent- and catalyst-free domino reaction for the efficient synthesis of 3-arylthiazolidine-2-thiones under microwave irradiation. RSC Advances, 5, 90451–90456. doi:10.1039/C5RA19112B
   Google Scholar
• Wang, M., Mao, Z., Kang, T.-S., Wong, C.-Y., Mergny, J.-L., Leung, C.-H., & Ma, D.-L. (2016). Conjugating a groove-binding motif to an. Ir(III) complex for the enhancement of G-quadruplex probe behaviour. Chemical Science, 7, 2516–2523. doi:10.1039/c6sc00001k
   PubMed Web of Science ®Google Scholar
• Wen, L.-N., & Xie, M.-X. (2017). Spectroscopic investigation of the interaction between G-quadruplex of KRAS promoter sequence and three isoquinoline alkaloids. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, 171, 287–296. doi:10.1016/j.saa.2016.08.013
   PubMed Web of Science ®Google Scholar
• Wilson, W. D., & Paul, A. (2014). Kinetics and structures on the molecular path to the quadruplex form of the human telomere. Journal of Molecular Biology, 426, 1625–1628. doi:10.1016/j.jmb.2014.02.001
   PubMed Web of Science ®Google Scholar
• Xiong, Y.-X., Su, H.-F., Lv, P., Ma, Y., Wang, S.-K., Miao, H., … Huang, Z.-S. (2015). A newly identified berberine derivative induces cancer cell senescence by stabilizing endogenous G-quadruplexes and sparking a DNA damage response at the telomere region. Oncotarget, 6, 35625–35635. doi:10.18632/oncotarget.5521
   PubMedGoogle Scholar
• Zahler, A. M., Williamson, J. R., Cech, T. R., & Prescott, D. M. (1991). Inhibition of telomerase by G-quartet DNA structures. Nature, 350, 718–720. doi:10.1038/350718a0
   PubMed Web of Science ®Google Scholar
• Zeng, D.-Y., Kuang, G.-T., Wang, S.-K., Peng, W., Lin, S.-L., Zhang, Q., … Ou, T.-M. (2017). Discovery of novel 11-Triazole substituted enzofuro[3,2-b]quinolone derivatives as c-myc G-quadruplex specific stabilizers via click chemistry. Journal of Medicinal Chemistry, 60, 5407–5423. doi:10.1021/acs.jmedchem.7b00016
   PubMed Web of Science ®Google Scholar
• Zhang, Z., Dai, J., Veliath, E., Jones, R. A., & Yang, D. Z. (2010). Structure of a two-G-tetrad intramolecular G-quadruplex formed by a variant human telomeric sequence in K+ solution: Insights into the interconversion of human telomeric G-quadruplex structures. Nucleic Acids Research, 38, 1009–1021. doi:10.1093/nar/gkp1029
   PubMed Web of Science ®Google Scholar