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Research Articles

LNA-induced dynamic stability in a therapeutic aptamer: insights from molecular dynamics simulations

, , ORCID Icon & ORCID Icon
Pages 2221-2230 | Received 02 Sep 2021, Accepted 08 Jan 2022, Published online: 01 Feb 2022

References

  • Arora, A., & Maiti, S. (2009). Differential biophysical behavior of human telomeric RNA and DNA quadruplex. The Journal of Physical Chemistry B, 113(30), 10515–10520. https://doi.org/10.1021/jp810638n
  • Berendsen, H. J. C., Grigera, J. R., & Straatsma, T. P. (1987). The missing term in effective pair potentials. The Journal of Physical Chemistry, 91(24), 6269–6271. https://doi.org/10.1021/j100308a038
  • Burmeister, P. E., Lewis, S. D., Silva, R. F., Preiss, J. R., Horwitz, L. R., Pendergrast, P. S., McCauley, T. G., Kurz, J. C., Epstein, D. M., Wilson, C., & Keefe, A. D. (2005). Direct in vitro selection of a 2'-O-methyl aptamer to VEGF. Chemistry & Biology, 12(1), 25–33. https://doi.org/10.1016/j.chembiol.2004.10.017
  • Case, D. A., Belfon, K., Ben-Shalom, I. Y., Brozell, S. R., Cerutti, D. S., Cheatham, T. E., III, Cruzeiro, V. W. D., Darden, T. A., Duke, R. E., Giambasu, G., Gilson, M. K., Gohlke, H., Goetz, A. W., Harris, R., Izadi, S., Iz-Mailov, S. A., Kasavajhala, K., Kovalenko, A., Krasny, R., … Kollman, P. A. (2020). AMBER 2020. University of California.
  • Case, D. A., Cerutti, D. S., Cheatham, T. E., III., Darden, T. A., Duke, R. E., Giese, T. J., Gohlke, H., Goetz, A. W., Greene, D., Homeyer, N., Izadi, S., Kovalenko, A., Lee, T. S., LeGrand, S., Li, P., Lin, C., Liu, J., Luchko, T., Luo, R., … Kollman, P. A. (2017). AMBER 2017. University of California.
  • Chaubey, A. K., Dubey, K. D., & Ojha, R. P. (2012). Stability and free energy calculation of LNA modified quadruplex: A molecular dynamics study. Journal of Computer-Aided Molecular Design, 26(3), 289–299. https://doi.org/10.1007/s10822-012-9548-z
  • Chaubey, A. K., Dubey, K. D., & Ojha, R. P. (2015). MD simulation of LNA-modified human telomeric G-quadruplexes: A free energy calculation. Medicinal Chemistry Research, 24(2), 753–763. https://doi.org/10.1007/s00044-014-1182-y
  • Condon, D. E., Yildirim, I., Kennedy, S. D., Mort, B. C., Kierzek, R., & Turner, D. H. (2014). Optimization of an AMBER force field for the artificial nucleic acid, LNA, and benchmarking with NMR of L(CAAU). The Journal of Physical Chemistry B, 118(5), 1216–1228. https://doi.org/10.1021/jp408909t
  • Črnugelj, M., Šket, P., & Plavec, J. (2003). Small change in a G-rich sequence, a dramatic change in topology: New dimeric G-quadruplex folding motif with unique loop orientations. Journal of the American Chemical Society, 125(26), 7866–7871. https://doi.org/10.1021/ja0348694
  • Darfeuille, F., Hansen, J. B., Orum, H., Primo, C. D., & Toulmé, J. J. (2004). LNA/DNA chimeric oligomers mimic RNA aptamers targeted to the TAR RNA element of HIV-1. Nucleic Acids Research, 32(10), 3101–3107. https://doi.org/10.1093/nar/gkh636
  • Edwards, S. L., Poongavanam, V., Kanwar, J. R., Roy, K., Hillman, K. M., Prasad, N., Leth-Larsen, R., Petersen, M., Marušič, M., Plavec, J., Wengel, J., & Veedu, R. N. (2015). Targeting VEGF with LNA-stabilized G-rich oligonucleotide for efficient breast cancer inhibition. Chemical Communications (Cambridge, England), 51(46), 9499–9502. https://doi.org/10.1039/c5cc02756j
  • Ellington, A. D., & Szostak, J. W. (1990). In vitro selection of RNA molecules that bind specific ligands. Nature, 346(6287), 818–822. https://doi.org/10.1038/346818a0
  • Foloppe, N., Hartmann, B., Nilsson, L., & MacKerell, A. D. (2002). Intrinsic conformational energetics associated with the glycosyl torsion in DNA: A quantum mechanical study. Biophysical Journal, 82(3), 1554–1569. https://doi.org/10.1016/S0006-3495(02)75507-0
  • Gatto, B., Palumbo, M., & Sissi, C. (2009). Nucleic acid aptamers based on the G-quadruplex structure: Therapeutic and diagnostic potential. Current Medicinal Chemistry, 16(10), 1248–1265. https://doi.org/10.2174/092986709787846640
  • Haase, L., Karg, B., & Weisz, K. (2019). Manipulating DNA G-quadruplex structures by using guanosine analogues. Chembiochem: A European Journal of Chemical Biology, 20(8), 985–993. https://doi.org/10.1002/cbic.201800642
  • Hazel, P., Huppert, J., Balasubramanian, S., & Neidle, S. (2004). Loop-length-dependent folding of G-quadruplexes. Journal of the American Chemical Society, 126(50), 16405–16415. https://doi.org/10.1021/ja045154j
  • Joachimi, A., Benz, A., & Hartig, J. S. (2009). A comparison of DNA and RNA quadruplex structures and stabilities. Bioorganic & Medicinal Chemistry, 17(19), 6811–6815. https://doi.org/10.1016/j.bmc.2009.08.043
  • Joung, I. S., & Cheatham, T. E. III. (2008). Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations. The Journal of Physical Chemistry. B, 112(30), 9020–9041. https://doi.org/10.1021/jp8001614
  • Keck, P. J., Hauser, S. D., Krivi, G., Sanzo, K., Warren, T., Feder, J., & Connolly, D. T. (1989). Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science (New York, N.Y.), 246(4935), 1309–1312. https://doi.org/10.1126/science.2479987
  • Lane, A. N., Chaires, J. B., Gray, R. D., & Trent, J. O. (2008). Stability and kinetics of G-quadruplex structures. Nucleic Acids Research, 36(17), 5482–5515. https://doi.org/10.1093/nar/gkn517
  • Lebars, I., Richard, T., Di Primo, C., & Toulmé, J. J. (2007). LNA derivatives of a kissing aptamer targeted to the trans-activating responsive RNA element of HIV-1. Blood Cells, Molecules & Diseases, 38(3), 204–209. https://doi.org/10.1016/j.bcmd.2006.11.008
  • Leung, D. W., Cachianes, G., Kuang, W. J., Goeddel, D. V., & Ferrara, N. (1989). Vascular endothelial growth factor is a secreted angiogenic mitogen. Science (New York, N.Y.), 246(4935), 1306–1309. https://doi.org/10.1126/science.2479986
  • Liang, C., Li, F., Wang, L., Zhang, Z.-K., Wang, C., He, B., Li, J., Chen, Z., Shaikh, A. B., Liu, J., Wu, X., Peng, S., Dang, L., Guo, B., He, X., Au, D. W. T., Lu, C., Zhu, H., Zhang, B.-T., Lu, A., & Zhang, G. (2017). Tumor cell-targeted delivery of CRISPR/Cas9 by aptamer-functionalized lipopolymer for therapeutic genome editing of VEGFA in osteosarcoma. Biomaterials, 147, 68–85. https://doi.org/10.1016/j.biomaterials.2017.09.015
  • Li, Z., Lech, C. J., & Phan, A. T. (2014). Sugar-modified G-quadruplexes: effects of LNA-, 2' F-RNA–and 2' F-ANA-guanosine chemistries on G-quadruplex structure and stability. Nucleic acids research, 42(6), 4068–4079. https://doi.org/10.1093/nar/gkt1312
  • Liu, B., & Li, D. (2014). Structural transformation induced by locked nucleic acid or 2'–O-methyl nucleic acid site-specific modifications on thrombin binding aptamer. Chemistry Central Journal, 8(1), 1–6. https://doi.org/10.1186/1752-153X-8-19
  • Lu, X. J. (2020). DSSR-enabled innovative schematics of 3d nucleic acid structures with PyMOL. Nucleic Acids Research, 48(13), e74. https://doi.org/10.1093/nar/gkaa426
  • Marušič, M., Veedu, R. N., Wengel, J., & Plavec, J. (2013). G-rich VEGF aptamer with locked and unlocked nucleic acid modifications exhibits a unique G-quadruplex fold. Nucleic Acids Research, 41(20), 9524–9536. https://doi.org/10.1093/nar/gkt697
  • Moon, J., Han, J. H., Kim, D. Y., Jung, M.-J., & Kim, S. K. (2015). Effects of deficient of the Hoogsteen base-pairs on the G-quadruplex stabilization and binding mode of a cationic porphyrin. Biochemistry and Biophysics Reports, 2, 29–35. https://doi.org/10.1016/j.bbrep.2015.03.012
  • Ni, S., Zhuo, Z., Pan, Y., Yu, Y., Li, F., Liu, J., Wang, L., Wu, X., Li, D., Wan, Y., Zhang, L., Yang, Z., Zhang, B.-T., Lu, A., & Zhang, G. (2021). Recent progress in aptamer discoveries and modifications for therapeutic applications. ACS Applied Materials & Interfaces, 13(8), 9500–9519. https://doi.org/10.1021/acsami.0c05750
  • Nielsen, J. T., Arar, K., & Petersen, M. (2006). NMR solution structures of LNA (locked nucleic acid) modified quadruplexes. Nucleic Acids Research, 34(7), 2006–2014. https://doi.org/10.1093/nar/gkl144
  • Nielsen, J. T., Arar, K., & Petersen, M. (2009). Solution structure of a locked nucleic acid modified quadruplex: Introducing the V4 folding topology. Angewandte Chemie, 121(17), 3145–3149. https://doi.org/10.1002/ange.200806244
  • Nonaka, Y., Sode, K., & Ikebukuro, K. (2010). Screening and improvement of an anti-VEGF DNA aptamer. Molecules (Basel, Switzerland), 15(1), 215–225. https://doi.org/10.3390/molecules15010215
  • Nozari, A., & Berezovski, M. V. (2017). Aptamers for CD antigens: From cell profiling to activity modulation. Molecular Therapy-Nucleic Acids, 6, 29–44. https://doi.org/10.1016/j.omtn.2016.12.002
  • Olsen, C. M., Gmeiner, W. H., & Marky, L. A. (2006). Unfolding of G-quadruplexes: Energetic, and ion and water contributions of G-quartet stacking. The Journal of Physical Chemistry B, 110(13), 6962–6969. https://doi.org/10.1021/jp0574697
  • Olsen, C. M., Lee, H. T., & Marky, L. A. (2009). Unfolding thermodynamics of intramolecular G-quadruplexes: Base sequence contributions of the loops. The Journal of Physical Chemistry B, 113(9), 2587–2595. https://doi.org/10.1021/jp806853n
  • Pérez, A., Marchán, I., Svozil, D., Sponer, J., Cheatham, T. E., III, Laughton, C. A., & Orozco, M. (2007). Refinement of the AMBER force field for nucleic acids: Improving the description of alpha/gamma conformers. Biophysical Journal, 92(11), 3817–3829. https://doi.org/10.1529/biophysj.106.097782
  • Potty, A. S., Kourentzi, K., Fang, H., Jackson, G. W., Zhang, X., Legge, G. B., & Willson, R. C. (2009). Biophysical characterization of DNA aptamer interactions with vascular endothelial growth factor. Biopolymers, 91(2), 145–156. https://doi.org/10.1002/bip.21097
  • Pradhan, D., Hansen, L. H., Vester, B., & Petersen, M. (2011). Selection of G-quadruplex folding topology with LNA-modified human telomeric sequences in K + solution. Chemistry (Weinheim an Der Bergstrasse, Germany), 17(8), 2405–2413. https://doi.org/10.1002/chem.201001961
  • R Core Team, (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
  • Roe, D. R., & Cheatham, T. E. III, (2013). PTRAJ and CPPTRAJ: Software for processing and analysis of molecular dynamics trajectory data. Journal of Chemical Theory and Computation, 9(7), 3084–3095. https://doi.org/10.1021/ct400341p
  • Roxo, C., Kotkowiak, W., & Pasternak, A. (2019). G-quadruplex-forming aptamers—characteristics, applications, and perspectives. Molecules, 24(20), 3781. https://doi.org/10.3390/molecules24203781
  • Schmidt, K. S., Borkowski, S., Kurreck, J., Stephens, A. W., Bald, R., Hecht, M., Friebe, M., Dinkelborg, L., & Erdmann, V. A. (2004). Application of locked nucleic acids to improve aptamer in vivo stability and targeting function. Nucleic Acids Research, 32(19), 5757–5765. https://doi.org/10.1093/nar/gkh862
  • Šponer, J., Šponer, J. E., Mládek, A., Jurečka, P., Banáš, P., & Otyepka, M. (2013). Nature and magnitude of aromatic base stacking in DNA and RNA: Quantum chemistry, molecular mechanics, and experiment. Biopolymers, 99(12), 978–988. https://doi.org/10.1002/bip.22322
  • Stanciu, L. A., Wei, Q., Barui, A. K., & Mohammad, N. (2021). Recent advances in aptamer-based biosensors for global health applications. Annual Review of Biomedical Engineering, 23, 433–459. https://doi.org/10.1146/annurev-bioeng-082020-035644
  • Sun, H., Zhu, X., Lu, P. Y., Rosato, R. R., Tan, W., & Zu, Y. (2014). Oligonucleotide aptamers: new tools for targeted cancer therapy. Molecular Therapy-Nucleic Acids, 3, e182. https://doi.org/10.1038/mtna.2014.32
  • Tan, W., Donovan, M. J., & Jiang, J. (2013). Aptamers from cell-based selection for bioanalytical applications. Chemical Reviews, 113(4), 2842–2862. https://doi.org/10.1021/cr300468w
  • Tucker, B. A., Hudson, J. S., Ding, L., Lewis, E., Sheardy, R. D., Kharlampieva, E., & Graves, D. (2018). Stability of the Na + form of the human telomeric G-quadruplex: role of adenines in stabilizing G-quadruplex structure. ACS Omega, 3(1), 844–855. https://doi.org/10.1021/acsomega.7b01649
  • Tuerk, C., & Gold, L. (1990). Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science (New York, N.Y.), 249(4968), 505–510. https://doi.org/10.1126/science.2200121
  • Wang, H., Lam, C. H., Li, X., West, D. L., & Yang, X. (2018). Selection of pd1/pd-l1 x-aptamers. Biochimie, 145, 125–130.
  • Wei, L., & Cohen, A. (2019). Commentary: medication during pregnancy and negative impact on offspring. British Journal of Clinical Pharmacology, 85(7), 1393–1393. https://doi.org/10.1111/bcp.13931
  • Zgarbová, M., Sponer, J., Otyepka, M., Cheatham, T. E., III, Galindo-Murillo, R., & Jurecka, P. (2015). Refinement of the sugar-phosphate backbone torsion beta for AMBER force fields improves the description of Z- and B-DNA. Journal of Chemical Theory and Computation, 11(12), 5723–5736. https://doi.org/10.1021/acs.jctc.5b00716

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