187
Views
0
CrossRef citations to date
0
Altmetric
Research Articles

Ribonucleic acid (RNA) condensation by thermal cycling with metal cations: yield of nanoparticles and their applicability for transfection

, , , , , & show all
Pages 3959-3971 | Received 05 Jul 2019, Accepted 13 Sep 2019, Published online: 27 Sep 2019

References

  • Afonin, K. A., Viard, M., Koyfman, A. Y., Martins, A. N., Kasprzak, W. K., Panigaj, M., … Shapiro, B. A. (2014). Multifunctional RNA nanoparticles. Nano Letters, 14(10), 5662–5671. doi:10.1021/nl502385k
  • Albrecht, R., Fehse, S., Pant, K., Nowag, S., Stephan, H., Haag, R., & Tzschucke, C. C. (2016). Polyglycerol-based copper chelators for the transport and release of copper ions in biological environments. Macromolecular Bioscience, 16(3), 412–419. doi:10.1002/mabi.201500284
  • Arscott, P. G., Ma, S., Wenner, J. R., & Bloomfield, V. A. (1995). DNA condensation by cobalt hexaamine (III) in alcohol–water mixture. Biopolymers, 36(3), 345–364. doi:10.1002/bip.360360309
  • Auffinger, P., Grover, N., & Westhof, E. (2011). Metal ion binding to RNA. Metal Ions in Life Sciences, 9, 1–35. doi: 10.1039/978184973251200001
  • Barnaby, S. N., Sita, T. L., Petrosko, S. H., Stegh, A. H., & Mirkin, C. A. (2015). Therapeutic applications of spherical nucleic acids. Cancer Treatment and Research, 166, 23–50. doi:10.1007/978-3-319-16555-4_2
  • Baugh, C., Grate, D., & Wilson, C. (2000). 2.8 A crystal structure of the malachite green aptamer. Journal of Molecular Biology, 301(1), 117–128. doi:10.1006/jmbi.2000.3951
  • Bechara, C., & Sagan, S. (2013). Cell-penetrating peptides: 20 years later, where do we stand? FEBS Letters, 587(12), 1693–1702. doi:10.1016/j.febslet.2013.04.031
  • Breslow, R., & Huang, D.-L. (1991). Effects of metal ions, including Mg2+ and lanthanides, on the cleavage of ribonucleotides and RNA model compounds. Proceedings of the National Academy of Sciences of the United States of America, 88(10), 4080–4083. doi:10.1073/pnas.88.10.4080
  • Butzow, J. J., & Eichhorn, G. L. (1971). Interaction of metal ions with nucleic acids and related compounds. XVII. On the mechanism of degradation of polyribonucleotides and oligoribonucleotides by zinc(II) ions. Biochemistry, 10(11), 2019–2027. doi:10.1021/bi00787a009
  • Chahal, J. S., Khan, O. F., Cooper, C. L., McPartlan, J. S., Tsosie, J. K., Tilley, L. D., … Anderson, D. G. (2016). Dendrimer-RNA nanoparticles generate protective immunity against lethal Ebola, H1N1 influenza, and Toxoplasma gondii challenges with a single dose. Proceedings of the National Academy of Sciences of the United States of America, 113(29), E4133–E4142. doi:10.1073/pnas.1600299113
  • Chattoraj, D. K., Gosule, L. C., & Schellman, J. A. (1978). DNA condensation with polyamines: II. Electron-microscopic studies. Journal of Molecular Biology, 121(3), 327–337. doi:10.1016/0022-2836(78)90367-4
  • Conwell, C. C., & Hud, N. V. (2004). Evidence that both kinetic and thermodynamic factors govern DNA toroid dimensions: Effects of magnesium (II) on DNA condensation by hexammine cobalt (III). Biochemistry, 43(18), 5380–5387. doi:10.1021/bi049872u
  • Dallas, A., Vlassov, A. V., & Kazakov, S. A. (2004). Principles of nucleic acid cleavage by Metal ions. In M. A. Zenkova (Ed.), Nucleic acids and molecular biology (Vol. 13, pp. 61–88). Berlin: Springer-Verlag.
  • Danilevich, V. N. (2012). Rapid and efficient technique for the production of condensed DNA and RNA nanoparticles using thermal cycling. Doklady Biochemistry and Biophysics, 443(1), 71–75. doi:10.1134/S1607672912020044
  • Danilevich, V. N., Mulyukin, A. L., Machulin, A. V., Sorokin, V. V., & Kozlov, S. A. (2019). Structural variability of DNA-containing Mg-pyrophosphate microparticles: Optimized conditions to produce particles with desired size and morphology. Journal of Biomolecular Structure and Dynamics, 37, 918–930. doi:10.1080/07391102.2018.1442747
  • Danilevich, V. N., Sorokin, V. V., Moiseev, Y. P., & Sizova, S. V. (2018). Preparation and properties of nanoparticles - tRNA-bivalent metal cation complexes, and perspectives of their practical use. Doklady Biochemistry and Biophysics, 479(1), 118–122. doi:10.1134/S1607672918020187
  • Dao, B. N., Viard, M., Martins, A. N., Kasprzak, W. K., Shapiro, B. A., & Afonin, K. A. (2015). Triggering RNAi with multifunctional RNA nanoparticles and their delivery. DNA and RNA Nanotechnology, 2(1), 1–12. doi:10.1515/rnan-2015-0001
  • DeRouchey, J., Hoover, B., & Rau, D. C. (2013). A comparison of DNA compaction by arginine and lysine peptides: A physical basis for arginine rich protamines. Biochemistry, 52(17), 3000–3009. doi:10.1021/bi4001408
  • Ding, Y., Jiang, Z., Saha, K., Kim, C. S., Kim, S. T., Landis, R. F., & Rotello, V. M. (2014). Gold nanoparticles for nucleic acid delivery. Molecular Therapy, 22(6), 1075–1083. doi:10.1038/mt.2014.30
  • Duguid, J. G., & Bloomfield, V. A. (1995). Aggregation of melted DNA by divalent metal ion-mediated cross-linking. Biophysical Journal, 69(6), 2642–2648. doi:10.1016/S0006-3495(95)80134-7
  • Duguid, J. G., Bloomfield, V. A., Benevides, J., & Thomas, G. J. (1993). Raman spectroscopy of DNA-metal complexes. I. Interactions and conformational effects of the divalent cations: Mg, Ca, Sr, Ba, Mn, Co, Ni, Cu, Pd, and Cd. Biophysical Journal, 65(5), 1916–1928. doi:10.1016/S0006-3495(93)81263-3
  • Feng, L., Zhang, Y., Jiang, M., Mo, Y., Wan, R., Jia, Z., … Zhang, Q. (2015). Up-regulation of Gadd45α after exposure to metal nanoparticles: The role of hypoxia inducible factor 1α. Environmental Toxicology, 30(4), 490–499. doi:10.1002/tox.21926
  • Forconi, M., & Herschlag, D. (2009). Metal ion-based RNA cleavage as a structural probe. Methods Enzymology, 468, 91–106. doi:10.1016/S0076-6879(09)68005-8
  • Gavrilov, K., & Saltzman, W. M. (2012). Therapeutic siRNA: Principles, challenges, and strategies. The Yale Journal of Biology and Medicine, 85(2), 187–200.
  • Gross, D. S., & Simpkins, H. (1981). Evidence for two-site binding in the terbium (III)-nucleic acid interaction. The Journal of Biological Chemistry, 256(18), 9593–9598.
  • Guidotti, G., Brambilla, L., & Rossi, D. (2017). Cell-penetrating peptides: From basic research to clinics. Trends in Pharmacological Sciences, 38(4), 406–424. doi:10.1016/j.tips.2017.01.003
  • Hud, N. V. (Ed.). (2009). Nucleic acid–metal ion interactions (p. 448). Cambridge: Royal Society of Chemistry.
  • Irisawa, M., & Komiyama, M. (1995). Hydrolysis of DNA and RNA through cooperation of two metal ions: A novel mimic of phosphoesterases. The Journal of Biochemistry, 117(3), 465–466. doi:10.1093/oxfordjournals.jbchem.a124729
  • Jensen, S. A., Day, E. S., Ko, C. H., Hurley, L. A., Luciano, J. P., Kouri, F. M., … Stegh, A. H. (2013). Spherical nucleic acid nanoparticle conjugates as an RNAi-based therapy for glioblastoma. Science Translational Medicine, 5(209), 209ra152. doi:10.1126/scitranslmed.3006839
  • Jere, D., Jiang, H. L., Arote, R., Kim, Y. K., Choi, Y. J., Cho, M. H., … Cho, C. S. (2009). Degradable polyethyleneimines as DNA and small interfering RNA carriers. Expert Opinion on Drug Delivery, 6(8), 827–834. doi:10.1517/17425240903029183
  • Kaczmarek, J. C., Kowalski, P. S., & Anderson, D. G. (2017). Advances in the delivery of RNA therapeutics: From concept to clinical reality. Genome Medicine, 9(1), 60.doi:10.1186/s13073-017-0450-0
  • Khan, O. F., Zaia, E. W., Jhunjhunwala, S., Xue, W., Cai, W., Yun, D. S., … Anderson, D. G. (2015). Dendrimer-inspired nanomaterials for the in vivo delivery of siRNA to lung vasculature. Nano Letters, 15(5), 3008–3016. doi:10.1021/nl5048972
  • Kim, I. D., Lim, C. M., Kim, J. B., Nam, H. Y., Nam, K., Kim, S. W., … Lee, J. K. (2010). Neuroprotection by biodegradable PAMAM ester (e-PAM-R)-mediated HMGB1 siRNA delivery in primary cortical cultures and in the postischemic brain. Journal of Controlled Release, 142(3), 422–430. doi:10.1016/j.jconrel.2009.11.011
  • Kulkarni, J. A., Cullis, P. R., & van der Meel, R. (2018). Lipid nanoparticles enabling gene therapies: From concepts to clinical utility. Nucleic Acid Therapeutics, 28(3), 146–157. doi:10.1089/nat.2018.0721
  • Laufer, S. D., & Restle, T. (2008). Peptide-mediated cellular delivery of oligonucleotide-based therapeutics in vitro: Quantitative evaluation of overall efficacy employing easy to handle reporter systems. Current Pharmaceutical Design, 14(34), 3637–3655. doi:10.2174/138161208786898806
  • Lee, T. J., Haque, F., Shu, D., Yoo, J. Y., Li, H., Yokel, R. A., …Croce, C. M. (2015). RNA nanoparticle as a vector for targeted siRNA delivery into glioblastoma mouse model. Oncotarget, 6, 14766–14776. doi:10.18632/oncotarget.3632
  • Levina, A. S., Repkova, M. N., Ismagilov, Z. R., Shikina, N. V., Malygin, E. G., Mazurkova, N. A., … Zarytova, V. F. (2012). High-performance method for specific effect on nucleic acids in cells using TiO2∼DNA nanocomposites. Scientific Reports, 2(1), 756. doi:10.1038/srep00756
  • Levina, A. S., Repkova, M. N., Bessudnova, E. V., Filippova, E. I., Mazurkova, N. A., & Zarytova, V. F. (2016). High antiviral effect of TiO2·PL-DNA nanocomposites targeted to conservative regions of (-)RNA and (+)RNA of influenza A virus in cell culture. Beilstein Journal of Nanotechnology, 7, 1166–1173. doi:10.3762/bjnano.7.108
  • Li, H., Lee, T., Dziubla, T., Pi, F., Guo, S., Xu, J., … Guo, P. (2015). RNA as a stable polymer to build controllable and defined nanostructures for material and biomedical applications. Nano Today, 10(5), 631–655. doi:10.1016/j.nantod.2015.09.003
  • Luten, J., van Nostrum, C. F., de Smedt, S. C., & Hennink, W. E. (2008). Biodegradable polymers as non-viral carriers for plasmid DNA delivery. Journal of Controlled Release, 126(2), 97–110. doi:10.1016/j.jconrel.2007.10.028
  • Maryon, E., Molloy, S. A., Ivy, K., Yu, H., & Kaplan, J. H. (2013). Rate and regulation of copper transport by human copper transporter 1 (hCTR1). Journal of Biological Chemistry, 288(25), 18035–18046. doi:10.1074/jbc.M112.442426
  • Mendes, L. P., Pan, J., & Torchilin, V. P. (2017). Dendrimers as nanocarriers for nucleic acid and drug delivery in cancer therapy. Molecules, 22, 1401. doi:10.3390/molecules22091401
  • Morris, D. L. Jr. (2014). DNA-bound metal ions: Recent developments. Biomolecular Concepts, 5(5), 397–407. doi:10.1515/bmc-2014-0021
  • Morris, M. C., Gros, E., Aldrian-Herrada, G., Choob, M., Archdeacon, J., Heitz, F., & Divita, G. (2007). A non-covalent peptide-based carrier for in vivo delivery of DNA mimics. Nucleic Acids Research, 35(7), e49. doi:10.1093/nar/gkm053
  • Nikitenko, N. A., & Prassolov, V. S. (2013). Non-viral delivery and therapeutic application of small interfering RNAs. Acta Naturae, 5(3), 35–53. doi:10.32607/20758251-2013-5-3-35-53
  • Oblak, A., Pohar, J., & Jerala, R. (2015). MD-2 determinants of nickel and cobalt-mediated activation of human TLR4. PLoS One, 10(3), e0120583. doi:10.1371/journal.pone.0120583
  • Pandey, A. P., & Sawant, K. K. (2016). Polyethylenimine: A versatile, multifunctional non-viral vector for nucleic acid delivery. Materials Science and Engineering: C, 68, 904–918. doi:10.1016/j.msec.2016.07.066
  • Perevyazko, I. Y., Bauer, M., Pavlov, G. M., Hoeppener, S., Schubert, S., Fischer, D., & Schubert, U. S. (2012). Polyelectrolyte complexes of DNA and linear PEI: Formation, composition and properties. Langmuir, 28(46), 16167–16176. doi:10.1021/la303094b
  • Petris, M. J., Smith, K., Lee, J., & Thiele, D. J. (2003). Copper-stimulated endocytosis and degradation of the human copper transporter, hCtr1. Journal of Biological Chemistry, 278(11), 9639–9646. doi:10.1074/jbc.M209455200
  • Reif, R., Haque, F., & Guo, P. (2012). Fluorogenic RNA nanoparticles for monitoring RNA folding and degradation in real time in living cells. Nucleic Acid Therapeutics, 22(6), 428–437. doi:10.1089/nat.2012.0380
  • Rychahou, P., Haque, F., Shu, Y., Zaytseva, Y., Weiss, H. L., Lee, E. Y., … Evers, B. M. (2015). Delivery of RNA nanoparticles into colorectal cancer metastases following systemic administration. ACS Nano, 9(2), 1108–1116. doi:10.1021/acsnano.5b00067
  • Shopsowitz, K. E., Roh, Y. H., Deng, Z. J., Morton, S. W., & Hammond, P. T. (2014). Composite RNAi-microsponges form through self-assembly of the organic and inorganic products of transcription. Small, 10(8), 1623–1633.
  • Shu, Y., Pi, F., Sharma, A., Rajabi, M., Haque, F., Shu, D., … Guo, P. (2014). Stable RNA nanoparticles as potential new generation drugs for cancer therapy. Advanced Drug Delivery Reviews, 66, 74–89. doi:10.1016/j.addr.2013.11.006
  • Singh, M. S., & Peer, D. (2016). RNA nanomedicines: The next generation drugs? Current Opinion in Biotechnology, 39, 28–34. doi:10.1016/j.copbio.2015.12.011
  • Soltani, N., Manzoori, J. L., Amjadi, M., Lotfipour, F., & Jouyban, A. (2016). Development and validation of a spectrofluorimetric determination of calf thymus DNA using a terbium-danofloxacin probe. Pharmaceutical Sciences, 22(1), 2–8. doi:10.15171/PS.2016.02
  • Steinbach, J. M., Weller, C. E., Booth, C. J., & Saltzman, W. M. (2012). Polymer nanoparticles encapsulating siRNA for treatment of HSV-2 genital infection. Journal of Controlled Release, 162(1), 102–110. doi:10.1016/j.jconrel.2012.06.008
  • Stewart, K. M., Horton, K. L., & Kelley, S. O. (2008). Cell-penetrating peptides as delivery vehicles for biology and medicine. Organic & Biomolecular Chemistry, 6(13), 2242–2255. doi:10.1039/b719950c
  • Taratula, O., Garbuzenko, O. B., Kirkpatrick, P., Pandya, I., Savla, R., Pozharov, V. P., … Minko, T. (2009). Surface-engineered targeted PPI dendrimer for efficient intracellular and intratumoral siRNA delivery. Journal of Controlled Release, 140(3), 284–293. doi:10.1016/j.jconrel.2009.06.019
  • Treiber, C., Quadir, M. A., Voigt, P., Radowski, M., Xu, S., Munter, L.-M., … Multhaup, G. (2009). Cellular copper import by nanocarrier systems, intracellular availability, and effects on amyloid beta peptide secretion. Biochemistry, 48(20), 4273–4284. doi:10.1021/bi900290c
  • Tünnemann, G., Ter-Avetisyan, G., Martin, R. M., Stöckl, M., Herrmann, A., & Cardoso, M. C. (2008). Live-cell analysis of cell penetration ability and toxicity of oligo-arginine. Journal of Peptide Science, 14(4), 469–476. doi:10.1002/psc.968
  • Vijayanathan, V., Thomas, T., Antony, T., Shirahata, A., & Thomas, T. J. (2004). Formation of DNA nanoparticles in the presence of novel polyamine analogues: A laser light scattering and atomic force microscopic study. Nucleic Acids Research, 32(1), 127–134. doi:10.1093/nar/gkg936
  • Xue, H. Y., Guo, P., Wen, W. C., & Wong, H. L. (2015). Lipid-based nanocarriers for RNA delivery. Current Pharmaceutical Design, 21(22), 3140–3147. doi:10.2174/1381612821666150531164540

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.