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Review Articles

DNA nanotechnology in ionic liquids and deep eutectic solvents

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Pages 941-961 | Received 10 Oct 2022, Accepted 01 Jun 2023, Published online: 30 Jul 2023

References

  • Seeman NC. Nucleic acid junctions and lattices. J Theor Biol. 1982;99:237–247. doi: 10.1016/0022-5193(82)90002-9.
  • Bunney PE, Zink AN, Holm AA, et al. The RNA 3D motif atlas: computational methods for extraction, organization and evaluation of RNA motifs. Physiol Behav. 2017; 176:139–148. doi: 10.1016/j.physbeh.2017.03.040.
  • Neubacher S, Hennig S. RNA structure and cellular applications of fluorescent light-up aptamers. angew chem int ed. 2019;58:1266–1279. doi: 10.1002/anie.201806482.
  • Lindahl T, Jones IL, Fiona MH. Instability and decay of the primary structure of DNA. Nature. 1993;362:709–715. doi: 10.1038/362709a0.
  • Simmel FC, Yurke B, Singh HR. Principles and applications of nucleic acid strand displacement reactions. Chem Rev. 2019;119:6326–6369. doi: 10.1021/acs.chemrev.8b00580.
  • Tang MSL, Shiu SCC, Godonoga M, et al. An aptamer-enabled DNA nanobox for protein sensing. Nanomedicine. 2018;14:1161–1168. doi: 10.1016/j.nano.2018.01.018.
  • Ball P. Water is an active matrix of life for cell and molecular biology. Proc Natl Acad Sci U S A. 2017;114:13327–13335. doi: 10.1073/pnas.1703781114.
  • He C, Lozoya-Colinas A, Gállego I, et al. Solvent viscosity facilitates replication and ribozyme catalysis from an RNA duplex in a model prebiotic process. Nucleic Acids Res. 2019;47:6569–6577. doi: 10.1093/nar/gkz496.
  • Egorova KS, Posvyatenko AV, Larin SS, et al. Ionic liquids: prospects for nucleic acid handling and delivery. Nucleic Acids Res. 2021; 49:1201–1234. doi: 10.1093/nar/gkaa1280.
  • Gates KS. An overview of chemical processes that damage cellular dna: spontaneous hydrolysis, alkylation, and reactions with radicals. Chem Res Toxicol. 2009; 22:1747–1760. doi: 10.1021/tx900242k.
  • Han H, Hurley LH. G-quadruplex DNA: a potential target for anti-cancer drug design. Trends Pharmacol Sci. 2000;21:136–142. doi: 10.1016/s0165-6147(00)01457-7.
  • Shrestha P, Jonchhe S, Emura T, et al. Confined space facilitates G-quadruplex formation. Nat Nanotechnol. 2017;12(6):582–588.
  • Keller A, Linko V. Challenges and perspectives of DNA nanostructures in biomedicine. Angew Chem Int Ed Engl. 2020;59:15818–15833. doi: 10.1002/anie.201916390.
  • Dordick JS. Industrial Enzymes. Polaina J, MacCabe AP, editors. Vol. 11, Enzyme and Microbial Technology. Dordrecht: Springer Netherlands; 2007. p. 194–211.
  • Carrea G, Riva S. Medium engineering of enzyme reaction. Angew Chem Int Ed. 2000;39:2226–2254. doi: 10.1002/1521-3773(20000703)39:13<2226::AID-ANIE2226>3.0.CO;2-L.
  • Polaina J, MacCabe AP. Industrial enzymes: structure, function and applications. Dordrecht: Springer; 2007. p. 19–34.
  • Hayes R, Warr GG, Atkin R. Structure and nanostructure in ionic liquids. Chem Rev. 2015;115:6357–6426. doi: 10.1021/cr500411q.
  • Bedrov D, Piquemal JP, Borodin O, et al. Molecular dynamics simulations of ionic liquids and electrolytes using polarizable force fields. Chem Rev. 2019;119:7940–7995. doi: 10.1021/acs.chemrev.8b00763.
  • Wang B, Qin L, Mu T, et al. Are ionic liquids chemically stable? Chem Rev. 2017;117:7113–7131. doi: 10.1021/acs.chemrev.6b00594.
  • Liu H, Dong Y, Wu J, et al. Evaluation of interaction between imidazolium-based chloride ionic liquids and calf thymus DNA. Sci Total Environ. 2016; 566-567:1–7. doi: 10.1016/j.scitotenv.2016.05.087.
  • Nakano M, Tateishi-Karimata H, Tanaka S, et al. Local thermodynamics of the water molecules around single- and double-stranded DNA studied by grid inhomogeneous solvation theory. Chem Phys Lett. 2016;660:250–255. doi: 10.1016/j.cplett.2016.08.032.
  • Feng B, Sosa RP, Mårtensson AKF, et al. Hydrophobic catalysis and a potential biological role of DNA unstacking induced by environment effects. Proc Natl Acad Sci U S A. 2019;116:17169–17174. doi: 10.1073/pnas.1909122116.
  • Privalov PL, Crane-Robinson C. Forces maintaining the DNA double helix. Eur Biophys J. 2020;49:315–321. doi: 10.1007/s00249-020-01437-w.
  • Duboue E, Fogarty AC, Hynes JT, et al. Dynamical disorder in the DNA hydration Shell. J Am Chem Soc. 2016;138:7610–7620. doi: 10.1021/jacs.6b02715.
  • Miyoshi D, Nakamura K, Tateishi-Karimata H, et al. Hydration of watson crick base pairs and dehydration of hoogsteen base pairs inducing structural polymorphism under molecular crowding conditions. J Am Chem Soc. 2009;131:3522–3531. doi: 10.1021/ja805972a.
  • Nakano S, Miyoshi D, Sugimoto N. Effects of molecular crowding on the structures, interactions, and functions of nucleic acids. Chem Rev. 2014;114:2733–2758. doi: 10.1021/cr400113m.
  • Khimji I, Shin J, Liu J. DNA duplex stabilization in crowded polyanion solutions. Chem Commun (Camb). 2013;49:1306–1308. doi: 10.1039/c2cc38627e.
  • Carlon E, Orlandini E, Stella AL. Roles of stiffness and excluded volume in DNA denaturation. Phys Rev Lett. 2002;88:4. doi: 10.1103/PhysRevLett.88.198101.
  • Knowles DB, LaCroix AS, Deines NF, et al. Separation of preferential interaction and excluded volume effects on DNA duplex and hairpin stability. Proc Natl Acad Sci U S A. 2011;108:12699–12704. doi: 10.1073/pnas.1103382108.
  • Lei Q, Ren C, Su X, et al. Crowding-induced cooperativity in DNA surface hybridization. Sci Rep. 2015;5:9217. doi: 10.1038/srep09217.
  • Muhuri S, Mimura K, Miyoshi D, et al. Stabilization of three-way junctions of DNA under molecular crowding conditions. J Am Chem Soc. 2009;131:9268–9280. doi: 10.1021/ja900744e.
  • Yildirim A, Sharma M, Varner BM, et al. Conformational preferences of DNA in reduced dielectric environments. J Phys Chem B. 2014;118:10874–10881. doi: 10.1021/jp505727w.
  • Jaiswal AK, Srivastava R, Pandey P, et al. Microscopic picture of water-ethylene glycol interaction near a model DNA by computer simulation: concentration dependence, structure, and localized thermodynamics. PLoS One. 2018;13:e0206359. doi: 10.1371/journal.pone.0206359.
  • Zhang T, Shang C, Duan R, et al. Polar organic solvents accelerate the rate of DNA strand replacement reaction. Analyst. 2015;140:2023–2028. doi: 10.1039/c4an02302a.
  • Dave N, Liu J. Fast molecular beacon hybridization in organic solvents with improved target specificity. J Phys Chem B. 2010;114:15694–15699. doi: 10.1021/jp106754k.
  • Cui S, Yu J, Kühner F, et al. Double-stranded DNA dissociates into single strands when dragged into a poor solvent. J Am Chem Soc. 2007;129:14710–14716. doi: 10.1021/ja074776c.
  • Del Vecchio P, Esposito D, Ricchi L, et al. The effects of polyols on the thermal stability of calf thymus DNA. Int J Biol Macromol. 1999;24:361–369. doi: 10.1016/s0141-8130(99)00058-6.
  • Nakano S, Sugimoto N. The structural stability and catalytic activity of DNA and RNA oligonucleotides in the presence of organic solvents. Biophys Rev. 2016; 8:11–23. doi: 10.1007/s12551-015-0188-0.
  • Nordstrom LJ, Clark CA, Andersen B, et al. Effect of ethylene glycol, urea, and N-methylated glycines on DNA thermal stability: the role of dna base pair composition and hydration. Biochemistry. 2006; 45:9604–9614. doi: 10.1021/bi052469i.
  • Beig A, Miller JM, Dahan A. Accounting for the solubility-permeability interplay in oral formulation development for poor water solubility drugs: the effect of PEG-400 on carbamazepine absorption. Eur J Pharm Biopharm. 2012;81:386–391. doi: 10.1016/j.ejpb.2012.02.012.
  • Ghoshdastidar D, Ghosh D, Senapati S. High nucleobase-solubilizing ability of low-viscous ionic liquid/water mixtures: measurements and mechanism. J Phys Chem B. 2016;120:492–503. doi: 10.1021/acs.jpcb.5b07179.
  • Lee JS, Oviedo JP, Bandara YMND, et al. Detection of nucleotides in hydrated ssDNA via 2D h-BN nanopore with ionic-liquid/salt–water interface. Electrophoresis. 2021;42:991–1002. doi: 10.1002/elps.202000356.
  • Nishimura N, Nomura Y, Nakamura N, et al. DNA strands robed with ionic liquid moiety. Biomaterials. 2005;26:5558–5563. doi: 10.1016/j.biomaterials.2005.02.005.
  • Zhang L, Qu Y, Gu J, et al. Photoliquefiable DNA-surfactant ionic crystals: anhydrous self-healing biomaterials at room temperature. Acta Biomater. 2021; Jul128:143–149. doi: 10.1016/j.actbio.2021.04.039.
  • Han J, Guo Y, Wang H, et al. Sustainable Bioplastic Made from Biomass DNA and Ionomers. J Am Chem Soc. 2021;143:19486–19497. doi: 10.1021/jacs.1c08888.
  • Rossi B, Tortora M, Catalini S, et al. An insight into thermal stability of DNA in hydrated ionic liquids from multi-wavelengths UV Resonance Raman experiments. Phys Chem Chem Phys. 2021;23:15980–15988. doi: 10.1039/D1CP01970H.
  • Ding Y, Zhang L, Xie J, et al. Binding characteristics and molecular mechanism of interaction between ionic liquid and DNA. J Phys Chem B. 2010; 114:2033–2043. doi: 10.1021/jp9104757.
  • Chandran A, Ghoshdastidar D, Senapati S. Groove binding mechanism of ionic liquids: a key factor in long-term stability of DNA in hydrated ionic liquids? J Am Chem Soc. 2012; 134:20330–20339. doi: 10.1021/ja304519d.
  • Bottari C, Mancini I, Mele A, et al. Conformational stability of DNA in hydrated ionic liquid by synchrotron-based UV resonance raman. In: Lérondel G, Cho Y-H, Kawata S, Taguchi A, editors. UV and Higher Energy Photonics: From Materials to Applications 2019. SPIE; 2019. p. 24. doi: 10.1117/12.2529077.
  • Bottari C, Catalini S, Foggi P, et al. Base-specific pre-melting and melting transitions of DNA in presence of ionic liquids probed by synchrotron-based UV resonance Raman scattering. J Mol Liq. 2021; 330(10):115433. doi: 10.1016/j.molliq.2021.115433.
  • Wang H, Wang J, Zhang S. Binding Gibbs energy of ionic liquids to calf thymus DNA: a fluorescence spectroscopy study. Phys Chem Chem Phys. 2011;13:3906–3910. doi: 10.1039/c0cp01815e.
  • Mishra A, Ekka MK, Maiti S. Influence of ionic liquids on thermodynamics of small molecule-dna interaction: the binding of ethidium bromide to calf thymus DNA. J Phys Chem B. 2016;120:2691–2700. doi: 10.1021/acs.jpcb.5b11823.
  • Singh PK, Sujana J, Mora AK, et al. Probing the DNA-ionic liquid interaction using an ultrafast molecular rotor. J Photochem Photobiol A Chem. 2012;246:16–22. doi: 10.1016/j.jphotochem.2012.07.006.
  • Meng Z, Kubar T, Mu Y, et al. A molecular dynamics-quantum mechanics theoretical study of dna-mediated charge transport in hydrated ionic liquids. J Chem Theory Comput. 2018;14:2733–2742. doi: 10.1021/acs.jctc.7b01201.
  • Jumbri K, Micaelo NM, Abdul Rahman MB. Solvation free energies of nucleic acid bases in ionic liquids. Mol Simul. 2017;43:19–27. doi: 10.1080/08927022.2016.1227075.
  • Cardoso L, Micaelo NM. DNA molecular solvation in neat ionic liquids. Chemphyschem. 2011;12:275–277. doi: 10.1002/cphc.201000645.
  • Andrade UMS, Castro ASB, Oliveira PHF, et al. Imidazolium-based ionic liquids binding to DNA: Mechanical effects and thermodynamics of the interactions. Int J Biol Macromol. 2022; Aug214:500–511. doi: 10.1016/j.ijbiomac.2022.06.069.
  • Jumbri K, Abdul Rahman MB, Abdulmalek E, et al. An insight into structure and stability of DNA in ionic liquids from molecular dynamics simulation and experimental studies. Phys Chem Chem Phys. 2014;16:14036–14046. doi: 10.1039/c4cp01159g.
  • Jumbri K, Ahmad H, Abdulmalek E, et al. Binding energy and biophysical properties of ionic liquid-DNA complex: understanding the role of hydrophobic interactions. J Mol Liq. 2016;223:1197–1203. doi: 10.1016/j.molliq.2016.09.040.
  • Del Olmo L, Lage-Estebanez I, López R, et al. Understanding the structure and properties of cholinium amino acid based ionic liquids. J Phys Chem B. 2016;120:10327–10335. doi: 10.1021/acs.jpcb.6b06969.
  • Pabbathi A, Samanta A. Spectroscopic and molecular docking study of the interaction of dna with a morpholinium ionic liquid. J Phys Chem B. 2015;119:11099–11105. doi: 10.1021/acs.jpcb.5b02939.
  • Fujita K, MacFarlane DR, Forsyth M, et al. Solubility and stability of cytochrome c in hydrated ionic liquids: effect of oxo acid residues and kosmotropicity. Biomacromolecules. 2007; 8:2080–2086. doi: 10.1021/bm070041o.
  • Domínguez de María P, Maugeri Z. Ionic liquids in biotransformations: from proof-of-concept to emerging deep-eutectic-solvents. Curr Opin Chem Biol. 2011;15:220–225. doi: 10.1016/j.cbpa.2010.11.008.
  • Lin Y, Zhao A, Tao Y, et al. Ionic liquid as an efficient modulator on artificial enzyme system: toward the realization of high-temperature catalytic reactions. J Am Chem Soc. 2013; 135:4207–4210. doi: 10.1021/ja400280f.
  • Vijayaraghavan R, Izgorodin A, Ganesh V, et al. Long-term structural and chemical stability of DNA in hydrated ionic liquids. Angew Chem Int Ed Engl. 2010; 49:1631–1633. doi: 10.1002/anie.200906610.
  • Mamajanov I, Engelhart AE, Bean HD, et al. DNA and RNA in anhydrous media: uplex, triplex, and G-quadruplex secondary structures in a deep eutectic solvent. Angew Chem Int Ed Engl. 2010;49:6310–6314. doi: 10.1002/anie.201001561.
  • Maity A, Singh A, Singh N. Differential stability of DNA based on salt concentration. Eur Biophys J. 2017; 46:33–40. doi: 10.1007/s00249-016-1132-3.
  • Tulsiyan KD, Jena S, Kar RK, et al. Structural dynamics of RNA in the presence of choline amino acid based ionic liquid: a spectroscopic and computational outlook. 2021;7(10):1688–1697.
  • Shukla SK, Mikkola JP. Use of ionic liquids in protein and DNA chemistry. Front Chem. 2020;8:1–23. doi: 10.3389/fchem.2020.598662.
  • Tateishi-Karimata H, Sugimoto N. Structure, stability and behaviour of nucleic acids in ionic liquids. Nucleic Acids Res. 2014;42:8831–8844. doi: 10.1093/nar/gku499.
  • Francisco M, González ASB, García de Dios SL, et al. Comparison of a low transition temperature mixture (LTTM) formed by lactic acid and choline chloride with choline lactate ionic liquid and the choline chloride salt: physical properties and vapour–liquid equilibria of mixtures containing water and ethanol. RSC Adv. 2013;3:23553. doi: 10.1039/c3ra40303c.
  • Bhatt J, Pereira MM, Prasad K. Simultaneous morphological transformation of metal salt and conformations of DNA in a bio-based ionic liquid. Int J Biol Macromol. 2019;135:926–930. doi: 10.1016/j.ijbiomac.2019.06.012.
  • Sahoo DK, Jena S, Dutta J, et al. Critical assessment of the interaction between DNA and choline amino acid ionic liquids: evidences of multimodal binding and stability enhancement. ACS Cent Sci. 2018; 4:1642–1651. doi: 10.1021/acscentsci.8b00601.
  • Stellwagen E, Muse JM, Stellwagen NC. Monovalent cation size and DNA conformational stability. Biochemistry. 2011;50:3084–3094. doi: 10.1021/bi1015524.
  • Pal S, Paul S. Understanding the role of reline, a natural DES, on temperature-induced conformational changes of C-Kit G-quadruplex DNA: a molecular dynamics study. J Phys Chem B. 2020; 124:3123–3136. doi: 10.1021/acs.jpcb.0c00644.
  • Saha D, Kulkarni M, Mukherjee A. Water modulates the ultraslow dynamics of hydrated ionic liquids near CG rich DNA: consequences for DNA stability. Phys Chem Chem Phys. 2016;18:32107–32115. doi: 10.1039/c6cp05959g.
  • Haque A, Khan I, Hassan SI, et al. Interaction studies of cholinium-based ionic liquids with calf thymus DNA: spectrophotometric and computational methods. J Mol Liq. 2017;237:201–207. doi: 10.1016/j.molliq.2017.04.068.
  • Tateishi-Karimata H, Sugimoto N. A-T base pairs are more stable than G-C base pairs in a hydrated ionic liquid. Angew Chem Int Ed Engl. 2012;51:1416–1419. doi: 10.1002/anie.201106423.
  • Rees WA, Korte J, Von Hippel PH, et al. Betaine can eliminate the base pair composition dependence of DNA melting. Biochemistry. 1993;32:137–144. doi: 10.1021/bi00052a019.
  • Hong J, Capp MW, Anderson CF, et al. Preferential interactions of glycine betaine and of urea with DNA: implications for DNA hydration and for effects of these solutes on DNA stability. Biochemistry. 2004;43:14744–14758. doi: 10.1021/bi049096q.
  • Janosik SM. The thermal stability of oligonucleotide duplexes is sequence independent in tetraalkylammonium salt solutions: application to identifying recombinant DNA clones. . 1998;42:1.
  • Nakano M, Tateishi-Karimata H, Tanaka S, et al. Choline ion interactions with DNA atoms explain unique stabilization of A-T base pairs in DNA duplexes: a microscopic view. J Phys Chem B. 2014;118:379–389. doi: 10.1021/jp406647b.
  • Portella G, Germann MW, Hud NV, et al. MD and NMR analyses of choline and TMA binding to duplex DNA: on the origins of aberrant sequence-dependent stability by alkyl cations in aqueous and water-free solvents. J Am Chem Soc. 2014;136:3075–3086. doi: 10.1021/ja410698u.
  • Sequeira RA, Bhatt J, Prasad K. Recent trends in processing of proteins and dna in alternative solvents: a sustainable approach. Sustain Chem. 2020; 1:116–137. doi: 10.3390/suschem1020010.
  • El Achkar T, Fourmentin S, Greige-Gerges H. Deep eutectic solvents: An overview on their interactions with water and biochemical compounds. J Mol Liq. 2019; 288:111028. doi: 10.1016/j.molliq.2019.111028.
  • Dai Y, van Spronsen J, Witkamp GJ, et al. Natural deep eutectic solvents as new potential media for green technology. Anal Chim Acta. 2013;766:61–68. doi: 10.1016/j.aca.2012.12.019.
  • Yusof R, Jumbri K, Ahmad H, et al. Binding of tetrabutylammonium bromide based deep eutectic solvent to dna by spectroscopic analysis. Spectrochim Acta A Mol Biomol Spectrosc. 2021;253:119543. doi: 10.1016/j.saa.2021.119543.
  • De La Harpe K, Kohl FR, Zhang Y, et al. Excited-state dynamics of a dna duplex in a deep eutectic solvent probed by femtosecond time-resolved IR spectroscopy. J Phys Chem A. 2018;122:2437–2444. doi: 10.1021/acs.jpca.7b12677.
  • Zhang Y, de La Harpe K, Hariharan M, et al. Excited-state dynamics of mononucleotides and DNA strands in a deep eutectic solvent. Faraday Discuss. 2018;207:267–282. doi: 10.1039/c7fd00205j.
  • Tortora M, Vigna J, Mancini I, et al. Effect of hydrated deep eutectic solvents on the thermal stability of DNA. Crystals. 2021; 11:1057. doi: 10.3390/cryst11091057.
  • Gállego I, Grover MA, Hud NV. Folding and imaging of DNA nanostructures in anhydrous and hydrated deep-eutectic solvents. Angew Chem Int Ed Engl. 2015;54:6765–6769. doi: 10.1002/anie.201412354.
  • Kosinski R, Mukhortava A, Pfeifer W, et al. Sites of high local frustration in DNA origami. Nat Commun. 2019;10:1–12. doi: 10.1038/s41467-019-09002-6.
  • Bhanjadeo MM, Nayak AK, Subudhi U. Cerium chloride stimulated controlled conversion of B-to-Z DNA in self-assembled nanostructures. Biochem Biophys Res Commun. 2017;482:916–921. doi: 10.1016/j.bbrc.2016.11.133.
  • Bujold KE, Lacroix A, Sleiman HF. DNA nanostructures at the Interface with Biology. Chem. 2018; 4:495–521. doi: 10.1016/j.chempr.2018.02.005.
  • Ghoshdastidar D, Senapati S. Dehydrated DNA in B-form: ionic liquids in rescue. Nucleic Acids Res. 2018;46:4344–4353. doi: 10.1093/nar/gky253.
  • Rich A, Zhang S. Z-DNA: The long road to biological function. Nat Rev Genet. 2003;4:566–572. doi: 10.1038/nrg1115.
  • Garai A, Ghoshdastidar D, Senapati S, et al. Ionic liquids make DNA rigid. J Chem Phys. 2018;149(4):045104.
  • Satpathi S, Sengupta A, Hridya VM, et al. A green solvent induced DNA Package. Sci Rep. 2015; 5:9137. doi: 10.1038/srep09137.
  • Jeong KB, Luo K, Lim MC, et al. Reduction of DNA folding by ionic liquids and its effects on the analysis of dna–protein interaction using solid-state nanopore. Small. 2018;14:1801375. doi: 10.1002/smll.201801375.
  • Gu Z, He Z, Chen F, et al. Ionic liquid decelerates single-stranded DNA transport through molybdenum disulfide nanopores. ACS Appl Mater Interfaces. 2022;14:32618–32624. ; doi: 10.1021/acsami.2c03335.
  • Sarkar S, Rajdev P, Singh PC. Hydrogen bonding of ionic liquids in the groove region of DNA controls the extent of its stabilization: synthesis, spectroscopic and simulation studies. Phys Chem Chem Phys. 2020;22:15582–15591. doi: 10.1039/d0cp01548b.
  • Zhang C, Chen J, Sun R, et al. The recent development of hybridization chain reaction strategies in biosensors. ACS Sens. 2020; 5:2977–3000. doi: 10.1021/acssensors.0c01453.
  • Tateishi-Karimata H, Sugimoto N. Chemical biology of non-canonical structures of nucleic acids for therapeutic applications. Chem Commun. 2020;56:2379–2390. doi: 10.1039/c9cc09771f.
  • Kankia B, Kankia B. Quadruplex-based reactions for dynamic DNA nanotechnology. J Phys Chem B. 2020;124:4263–4269. doi: 10.1021/acs.jpcb.0c02540.
  • Ebrahimi A, Ravan H, Khajouei S. DNA nanotechnology and bioassay development. TrAC - Trends Anal Chem. 2019;114:126–142. doi: 10.1016/j.trac.2019.03.007.
  • Nakano S, Ayusawa T, Tanino Y, et al. Stabilization of DNA loop structures by large cations. J Phys Chem B. 2019;123(36):7687–7694
  • Satpathi S, Kulkarni M, Mukherjee A, et al. Ionic liquid induced G-quadruplex formation and stabilization: spectroscopic and simulation studies. Phys Chem Chem Phys. 2016;18:29740–29746. doi: 10.1039/c6cp05732b.
  • Di Antonio M, Ponjavic A, Radzevičius A, et al. Single-molecule visualization of DNA G-quadruplex formation in live cells. Nat Chem. 2020;12:832–837. doi: 10.1038/s41557-020-0506-4.
  • Nishio M, Tsukakoshi K, Ikebukuro K. G-quadruplex: flexible conformational changes by cations, ph, crowding and its applications to biosensing. Biosens Bioelectron. 2021;178:113030. doi: 10.1016/j.bios.2021.113030.
  • Matsumoto S, Sugimoto N. New insights into the functions of nucleic acids controlled by cellular microenvironments. Top Curr Chem. 2021; 379:17.
  • Xiao F, Chen Z, Wei Z, et al. Hydrophobic interaction: a promising driving force for the biomedical applications of nucleic acids. Adv Sci. 2020;7:2001048. doi: 10.1002/advs.202001048.
  • de Xammar Oro JR, Grigera JR. On the thermal stability of DNA in solution of mixed solvents. J Biol Phys. 1995;21:151–154. doi: 10.1007/BF00712343.
  • Bonner G, Klibanov AM. Structural stability of DNA in nonaqueous solvents. Biotechnol Bioeng. 2000;68:339–344. doi: 10.1002/(SICI)1097-0290(20000505)68:3<339::AID-BIT12>3.0.CO;2-O.
  • Abe H, Abe N, Shibata A, et al. Structure formation and catalytic activity of DNA dissolved in organic solvents. Angew Chem Int Ed Engl. 2012;51:6475–6479. doi: 10.1002/anie.201201111.
  • Behera AK, Schlund KJ, Mason AJ, et al. Enhanced deoxyribozyme-catalyzed RNA ligation in the presence of organic cosolvents. Biopolymers. 2013;99:382–391. doi: 10.1002/bip.22191.
  • Fujita K, Takuya H, Tsukakoshi K, et al. The state of water molecules induces changes in the topologies and interactions of G-quadruplex DNA aptamers in hydrated ionic liquid. J Mol Liq. 2022;366:120175. doi: 10.1016/j.molliq.2022.120175.
  • Tateishi-Karimata H, Nakano M, Sugimoto N. Comparable stability of Hoogsteen and Watson-Crick base Pairs in ionic liquid choline dihydrogen phosphate. Sci Rep. 2014;4:3593. doi: 10.1038/srep03593.
  • Marušič M, Tateishi-Karimata H, Sugimoto N, et al. Structural foundation for DNA behavior in hydrated ionic liquid: an NMR study. Biochimie. 2015;108:169–177. doi: 10.1016/j.biochi.2014.11.015.
  • Nakano M, Tateishi-Karimata H, Tanaka S, et al. Affinity of molecular ions for DNA structures is determined by solvent-accessible surface area. J Phys Chem B. 2014;118:9583–9594. doi: 10.1021/jp505107g.
  • Fujita K, Ohno H. phosphatStable G-quadruplex structure in a hydrated ion pair: cholinium cation and dihydrogen e anion. Chem Commun. 2012;48:5751–5753. doi: 10.1039/c2cc30554b.
  • Tateishi-Karimata H, Nakano M, Pramanik S, et al. I-Motifs are more stable than G-quadruplexes in a hydrated ionic liquid. Chem Commun. 2015;51:6909–6912. doi: 10.1039/c5cc00666j.
  • Sarkar S, Singh PC. The combined action of cations and anions of ionic liquids modulates the formation and stability of G-quadruplex DNA. Phys Chem Chem Phys. 2021;23:24497–24504. doi: 10.1039/d1cp03730g.
  • Seviour T, Winnerdy FR, Wong LL, et al. The biofilm matrix scaffold of Pseudomonas aeruginosa contains G-quadruplex extracellular DNA structures. NPJ Biofilms Microbiomes. 2021; 7:27. doi: 10.1038/s41522-021-00197-5.
  • Pandey PK, Rawat K, Aswal VK, et al. Imidazolium based ionic liquid induced DNA gelation at remarkably low concentration. Colloids Surfaces A Physicochem Eng Asp. 2018;538:184–191. doi: 10.1016/j.colsurfa.2017.10.083.
  • Kamal Mohamed SM, Murali Sankar R, Kiran MS, et al. Facile preparation of biocompatible and transparent silica aerogels as ionogels using choline dihydrogen phosphate ionic liquid. Appl Sci. 2020; 11:206. doi: 10.3390/app11010206.
  • Gu C, Peng Y, Li J, et al. Supramolecular G4 Eutectogels of Guanosine with Solvent-Induced Chiral Inversion and Excellent Electrochromic Activity. Angew Chem Int Ed Engl. 2020; 59:18768–18773. doi: 10.1002/anie.202009332.
  • Zhao C, Ren J, Qu X. G-Quadruplexes form ultrastable parallel structures in deep eutectic solvent. Langmuir. 2013; 29:1183–1191. doi: 10.1021/la3043186.
  • Aslanyan L, Ko J, Kim BG, et al. Effect of urea on G-Quadruplex stability. J Phys Chem B. 2017; 121:6511–6519. doi: 10.1021/acs.jpcb.7b03479.
  • Monhemi H, Housaindokht MR, Moosavi-Movahedi AA, et al. How a protein can remain stable in a solvent with high content of urea: insights from molecular dynamics simulation of Candida antarctica lipase B in urea : choline chloride deep eutectic solvent. Phys Chem Chem Phys. 2014;16:14882–14893. doi: 10.1039/c4cp00503a.
  • Pal S, Paul S. Effect of hydrated and nonhydrated choline chloride–urea deep eutectic solvent (reline) on thrombin-binding g-quadruplex aptamer (TBA): a classical molecular dynamics simulation study. J Phys Chem C. 2019;123:11686–11698. doi: 10.1021/acs.jpcc.9b01111.
  • Lannan FM, Mamajanov I, Hud NV. Human telomere sequence DNA in water-free and high-viscosity solvents: G-quadruplex folding governed by Kramers rate theory. J Am Chem Soc. 2012;134:15324–15330. doi: 10.1021/ja303499m.
  • Rajagopal SK, Hariharan M. Non-natural G-quadruplex in a non-natural environment. Photochem Photobiol Sci. 2014;13:157–161. doi: 10.1039/c3pp50199j.
  • Chang T, He S, Amini R, et al. Functional nucleic acids under unusual conditions. ChemBioChem. 2021;22:2368–2383. doi: 10.1002/cbic.202100087.
  • Machado I, Özalp VC, Rezabal E, et al. DNA aptamers are functional molecular recognition sensors in protic ionic liquids. Chemistry. 2014; 20:11820–11825. doi: 10.1002/chem.201403354.
  • Chaou T, Vialet B, Azéma L. DNA aptamer selection in methanolic media: adenine-aptamer as proof-of-concept. Methods. 2016;97:11–19. doi: 10.1016/j.ymeth.2016.01.002.
  • Arcella A, Portella G, Collepardo-Guevara R, et al. Structure and properties of DNA in apolar solvents. J Phys Chem B. 2014; 118:8540–8548. doi: 10.1021/jp503816r.
  • Svigelj R, Dossi N, Toniolo R, et al. Selection of anti-gluten DNA aptamers in a deep eutectic solvent. Angew Chem Int Ed Engl. 2018;57:12850–12854. doi: 10.1002/anie.201804860.
  • Ferreira ESC, Voroshylova IV, Pereira CDS, et al. Improved force field model for the deep eutectic solvent ethaline: reliable physicochemical properties. J Phys Chem B. 2016;120:10124–10137. acs.jpcb. doi: 10.1021/acs.jpcb.6b07233.
  • Chidchob P, Sleiman HF. Recent advances in DNA nanotechnology. Curr Opin Chem Biol. 2018;46:63–70. doi: 10.1016/j.cbpa.2018.04.012.
  • Damase TR, Allen PB. Designed and evolved nucleic acid nanotechnology: contrast and complementarity. Bioconjug Chem. 2019;30:2–12. doi: 10.1021/acs.bioconjchem.8b00810.
  • Rothemund PWK. Folding DNA to create nanoscale shapes and patterns. Nature. 2006;440:297–302. doi: 10.1038/nature04586.
  • Li C, Luo M, Wang J, et al. Rigidified DNA triangle-protected molecular beacon from endogenous nuclease digestion for monitoring microRNA expression in living cell rigidified DNA triangle-protected molecular beacon from endogenous nuclease digestion for monitoring microRNA expression. ACS Sens. 2020;5(8):2378–2387.
  • Asiri AM, Agarwal S, Gupta VK. Dynamic DNA nanostructures in biomedicine: beauty, utility and limits. J Control Release. 2019;315:166–185.
  • Dunn KE. The business of DNA nanotechnology: commercialization of origami and other technologies. Molecules. 2020;25:377. doi: 10.3390/molecules25020377.
  • Madsen M, Gothelf KV. Chemistries for DNA nanotechnology. Chem Rev. 2019;119:6384–6458. doi: 10.1021/acs.chemrev.8b00570.
  • Svigelj R, Dossi N, Grazioli C, et al. Deep eutectic solvents (DESs) and their application in biosensor development. Sensors. 2021; Jun 2221:4263. doi: 10.3390/s21134263.
  • Khimji I, Kelly EY, Helwa Y, et al. Visual optical biosensors based on DNA-functionalized polyacrylamide hydrogels. Methods. 2013;64:292–298. doi: 10.1016/j.ymeth.2013.08.021.
  • Neves MC, Pereira P, Pedro AQ, et al. Improved ionic-liquid-functionalized macroporous supports able to purify nucleic acids in one-step. Mater Today Bio. 2020;8Nov;(Iii)::100086. doi: 10.1016/j.mtbio.2020.100086.
  • Peng X, Clark KD, Ding X, et al. Coupling oligonucleotides possessing a poly-cytosine tag with magnetic ionic liquids for sequence-specific DNA analysis. Chem Commun (Camb). 2018;54:10284–10287. doi: 10.1039/c8cc05954c.
  • Santra K, Clark KD, Maity N, et al. Exploiting fluorescence spectroscopy to identify magnetic ionic liquids suitable for the isolation of oligonucleotides. J Phys Chem B. 2018;122:7747–7756. doi: 10.1021/acs.jpcb.8b05580.
  • Clark KD, Nacham O, Yu H, et al. Extraction of DNA by magnetic ionic liquids: tunable solvents for rapid and selective DNA analysis. Anal Chem. 2015; Feb 387:1552–1559. doi: 10.1021/ac504260t.
  • Ding X, Clark KD, Varona M, et al. Magnetic ionic liquid-enhanced isothermal nucleic acid amplification and its application to rapid visual DNA analysis. Anal Chim Acta. 2019;1045:132–140. doi: 10.1016/j.aca.2018.09.014.
  • Peng X, Fang S, Ji B, et al. DNA nanostructure-programmed cell entry via corner angle-mediated molecular interaction with membrane receptors. Nano Lett. 2021;21:6946–6951. doi: 10.1021/acs.nanolett.1c02191.
  • Emaus MN, Anderson JL. Allelic discrimination between circulating tumor DNA fragments enabled by a multiplex-qPCR assay containing DNA-enriched magnetic ionic liquids. Anal Chim Acta. 2020;1124:184–193. doi: 10.1016/j.aca.2020.04.078.
  • Shi Y, Liu Y-L, Lai P-Y, et al. Ionic liquids promote PCR amplification of DNA. Chem Commun (Camb). 2012;48:5325–5327. doi: 10.1039/c2cc31740k.
  • Sivapragasam M, Moniruzzaman M, Goto M. Recent advances in exploiting ionic liquids for biomolecules: solubility, stability and applications. Biotechnol J. 2016;11:1000–1013. doi: 10.1002/biot.201500603.
  • Zhao H. DNA stability in ionic liquids and deep eutectic solvents. J Chem Technol Biotechnol. 2015;90:19–25. doi: 10.1002/jctb.4511.
  • Tateishi-Karimata H, Sugimoto N. Biological and nanotechnological applications using interactions between ionic liquids and nucleic acids. Biophys Rev. 2018;10:931–940. doi: 10.1007/s12551-018-0422-7.
  • Ma C, Laaksonen A, Liu C, et al. The peculiar effect of water on ionic liquids and deep eutectic solvents. Chem Soc Rev. 2018;47:8685–8720. doi: 10.1039/c8cs00325d.
  • Kist JA, Mitchell-Koch KR, Baker GA. The study and application of biomolecules in deep eutectic solvents. 2020;
  • Gomes JM, Silva SS, Reis RL. Biocompatible ionic liquids: Fundamental behaviours and applications. Chem Soc Rev. 2019;48:4317–4335. doi: 10.1039/c9cs00016j.
  • Sugimoto N, Endoh T, Takahashi S, et al. Chemical biology of double helical and non-double helical nucleic acids: “To B or Not To B, that is the question. BCSJ. 2021; Jul 1594:1970–1998. doi: 10.1246/bcsj.20210131.
  • Menhaj AB, Smith BD, Liu J. Exploring the thermal stability of DNA-linked gold nanoparticles in ionic liquids and molecular solvents. Chem Sci. 2012;3:3216–3220. doi: 10.1039/c2sc20565c.
  • Tateishi-Karimata H, Pramanik S, Sugimoto N. DNA sensor’s selectivity enhancement and protection from contaminating nucleases due to a hydrated ionic liquid. Analyst. 2015;140:4393–4398. doi: 10.1039/c5an00545k.
  • Huang Y, Wang S, Wang Z, et al. Task-specific ionic liquid-enabled mercury sensor for sensitive detection of total mercury in food digestion solution. Sensors Actuators B Chem. 2019;285:62–67. doi: 10.1016/j.snb.2019.01.025.
  • Svigelj R, Dossi N, Pizzolato S, et al. Truncated aptamers as selective receptors in a gluten sensor supporting direct measurement in a deep eutectic solvent. Biosens Bioelectron. 2020;165Jun;:112339. doi: 10.1016/j.bios.2020.112339.
  • Svigelj R, Dossi N, Grazioli C, et al. Paper-based aptamer-antibody biosensor for gluten detection in a deep eutectic solvent (DES). Anal Bioanal Chem. 2022;414:3341–3348. Oct 6; doi: 10.1007/s00216-021-03653-5.
  • Hansen BB, Spittle S, Chen B, et al. Deep eutectic solvents: a review of fundamentals and applications. Chem Rev. 2021;121(3)1232–1285.
  • Kong DM, Wang N, Guo XX, et al. “Turn-on” detection of Hg2+ ion using a peroxidase-like split G-quadruplex-hemin DNAzyme. Analyst. 2010;135:545–549. doi: 10.1039/b924014d.
  • Chen Z, Liu C, Cao F, et al. DNA metallization: principles, methods, structures, and applications. Chem Soc Rev. 2018;47:4017–4072. doi: 10.1039/c8cs00011e.
  • Li N, Shang Y, Han Z, et al. Fabrication of metal nanostructures on DNA templates. ACS Appl Mater Interfaces. 2019;11:13835–13852. doi: 10.1021/acsami.8b16194.
  • Kumar V, Parmar VS, Malhotra SV. Structural modifications of nucleosides in ionic liquids. Biochimie. 2010; 92:1260–1265. doi: 10.1016/j.biochi.2010.02.019.
  • Mondal D, Bhatt J, Sharma M, et al. A facile approach to prepare a dual functionalized DNA based material in a bio-deep eutectic solvent. Chem Commun. 2014;50:3989–3992. doi: 10.1039/c4cc00145a.
  • Bhatt J, Mondal D, Devkar RV, et al. Synthesis of functionalized N-doped graphene DNA hybrid material in a deep eutectic solvent. Green Chem. 2016;18:4297–4302. doi: 10.1039/C6GC00853D.
  • Chakraborty S, Mruthunjayappa MH, Aruchamy K, et al. Facile process for metallizing dna in a multitasking deep eutectic solvent for ecofriendly C–C coupling reaction and nitrobenzene reduction. ACS Sustainable Chem Eng. 2019; 7:14225–14235. doi: 10.1021/acssuschemeng.9b03224.
  • Rivilla I, de Cózar A, Schäfer T, et al. Catalysis of a 1,3-dipolar reaction by distorted DNA incorporating a heterobimetallic platinum (II) and copper (II) complex. Chem Sci. 2017;8:7038–7046. doi: 10.1039/c7sc02311a.
  • Fan H, Zhao Z, Yan G, et al. A smart DNAzyme-MnO2 nanosystem for efficient gene silencing. Angew Chem. 2015;127:4883–4887. doi: 10.1002/ange.201411417.
  • Itoh T. Ionic liquids as tool to improve enzymatic organic synthesis. Chem Rev. 2017;117:10567–10607. doi: 10.1021/acs.chemrev.7b00158.
  • Schindl A, Hagen ML, Muzammal S, et al. Proteins in ionic liquids: reactions, applications, and futures. Front Chem. 2019;7:1–31. doi: 10.3389/fchem.2019.00347.
  • Li L, Xu S, Yan H, et al. Nucleic acid aptamers for molecular diagnostics and therapeutics: advances and perspectives. Angew Chem Int Ed. 2021;60:2221–2231. doi: 10.1002/anie.202003563.
  • Nishimura N, Ohno H. Design of successive ion conduction paths in DNA films with ionic liquids. J Mater Chem. 2002;12:2299–2304. doi: 10.1039/b202972c.
  • Morimitsu Y, Matsuno H, Ohta N, et al. mechanical stabilization of deoxyribonucleic acid solid films based on hydrated ionic liquid. Biomacromolecules. 2020; 21:464–471. doi: 10.1021/acs.biomac.9b01207.
  • Jalalvand AR, Shokri F, Yari A. Co-operation of electrochemistry and chemometrics to develop a novel electrochemical aptasensor based on generation of first- and second-order data for selective and sensitive determination of the prostate specific antigen biomarker. Microchem J. 2022;183:108026. doi: 10.1016/j.microc.2022.108026.
  • Mahmoudi-Moghaddam H, Tajik S, Beitollahi H. A new electrochemical DNA biosensor based on modified carbon paste electrode using graphene quantum dots and ionic liquid for determination of topotecan. Microchem J. 2019;150:104085. doi: 10.1016/j.microc.2019.104085.
  • Huang JY, Zhao L, Lei W, et al. A high-sensitivity electrochemical aptasensor of carcinoembryonic antigen based on graphene quantum dots-ionic liquid-nafion nanomatrix and DNAzyme-assisted signal amplification strategy. Biosens Bioelectron. 2018;99:28–33. doi: 10.1016/j.bios.2017.07.036.
  • Shahdost-Fard F, Salimi A, Sharifi E, et al. Fabrication of a highly sensitive adenosine aptasensor based on covalent attachment of aptamer onto chitosan-carbon nanotubes-ionic liquid nanocomposite. Biosens Bioelectron. 2013;48:100–107. doi: 10.1016/j.bios.2013.03.060.
  • Mahyari M, Hooshmand SE, Sepahvand H, et al. Gold nanoparticles anchored onto covalent poly deep eutectic solvent functionalized graphene: An electrochemical aptasensor for the detection of C-reactive protein. Mater Chem Phys. 2021; 269:124730. doi: 10.1016/j.matchemphys.2021.124730.
  • Ke G, Su D, Li Y, et al. An accurate, high-speed, portable bifunctional electrical detector for COVID-19. Sci China Mater. 2021; 64:739–747. doi: 10.1007/s40843-020-1577-y.
  • Sharma M, Mondal D, Singh N, et al. High concentration DNA solubility in bio ionic liquids with long lasting chemical and structural stability at room temperature. RSC Adv. 2015;5:40546–40551. doi: 10.1039/C5RA03512K.
  • Rizan N, Tajuddin HA, Tan YS, et al. Effect of ionic liquid on the long-term structural and chemical stability of basidiomycetes DNAs integrated within Schottky-like junctions. Appl Phys A. 2021;127:142. doi: 10.1007/s00339-021-04303-4.
  • Clark KD, Sorensen M, Nacham O, et al. Preservation of DNA in nuclease-rich samples using magnetic ionic liquids. RSC Adv. 2016;6:39846–39851. doi: 10.1039/C6RA05932E.
  • Mazid RR, Cooper A, Zhang Y, et al. Enhanced enzymatic degradation resistance of plasmid DNA in ionic liquids. RSC Adv. 2015;5:43839–43844. doi: 10.1039/C5RA05518K.
  • Sharma G, Sequeira RA, Pereira MM, et al. Are ionic liquids and deep eutectic solvents the same?: Fundamental investigation from DNA dissolution point of view. J Mol Liq. 2021; Apr328:115386. doi: 10.1016/j.molliq.2021.115386.
  • Singh N, Sharma M, Mondal D, et al. Very high concentration solubility and long-term stability of DNA in an ammonium-based ionic liquid: A suitable medium for nucleic acid packaging and preservation. ACS Sustainable Chem Eng. 2017;5:1998–2005. doi: 10.1021/acssuschemeng.6b02842.
  • Mondal D, Sharma M, Mukesh C, et al. Improved solubility of DNA in recyclable and reusable bio-based deep eutectic solvents with long-term structural and chemical stability. Chem Commun. 2013;49:9606–9608. doi: 10.1039/c3cc45849k.
  • Mukesh C, Prasad K. Formation of multiple structural formats of DNA in a bio-deep eutectic solvent. Macromol Chem Phys. 2015;216:1061–1066. doi: 10.1002/macp.201500009.
  • Pedro A, Pereira P, Quental MV, et al. Cholinium-based Good’s buffers ionic liquids as remarkable stabilizers and recyclable preservation media for recombinant small RNAs. ACS Sustain Chem Eng. 2018;6(12):16645–16656.
  • Mazid RR, Divisekera U, Yang W, et al. Biological stability and activity of siRNA in ionic liquids. Chem Commun. 2014; 50:13457–13460. doi: 10.1039/c4cc05086j.
  • Mirjafari A. Long-term DNA preservation and storage at ambient temperature. US Patent App. 2020;16/:2020.
  • Rahman MH, Senapati S. Effects of ionic liquids on aqueous urea solutions: insights into the ionic liquid-assisted protein renaturation. J Phys Chem B. 2021;125:4808–4818. doi: 10.1021/acs.jpcb.1c00586.
  • Chen L, Mullen GE, Le Roch M, et al. On the formation of a protic ionic liquid in nature. Angew Chem Int Ed Engl. 2014; 53:11762–11765. doi: 10.1002/anie.201404402.
  • Marchel M, Cieśliński H, Boczkaj G. Thermal instability of choline chloride-based deep eutectic solvents and its influence on their toxicity─important limitations of DESs as sustainable materials. Ind Eng Chem Res. 2022;61:11288–11300. doi: 10.1021/acs.iecr.2c01898.
  • Jadhav NR, Bhosale SP, Bhosale SS, et al. Ionic liquids: formulation avenues, drug delivery and therapeutic updates. J Drug Deliv Sci Technol. 2021; 65:102694. doi: 10.1016/j.jddst.2021.102694.
  • Agatemor C, Ibsen KN, Tanner EEL, et al. Ionic liquids for addressing unmet needs in healthcare. Bioeng Transl Med. 2018; 3:7–25. doi: 10.1002/btm2.10083.
  • Sarker SR, Ball AS, Bhargava SK, et al. Evaluation of plasmid DNA stability against ultrasonic shear stress and its: In vitro delivery efficiency using ionic liquid [Bmim][PF6]. RSC Adv. 2019;9:29225–29231. doi: 10.1039/c9ra03414e.
  • Sarkar S, Chandra Singh P. Anions of ionic liquids are important players in the rescue of dna damage. J Phys Chem Lett. 2020; 11:10150–10156. doi: 10.1021/acs.jpclett.0c03016.
  • Zhang Y, Chen X, Lan J, et al. Synthesis and biological applications of imidazolium-based polymerized ionic liquid as a gene delivery vector. Chem Biol Drug Des. 2009;74:282–288. doi: 10.1111/j.1747-0285.2009.00858.x.
  • Soni SK, Sarkar S, Mirzadeh N, et al. Self-assembled functional nanostructure of plasmid DNA with ionic liquid [Bmim][PF6]: enhanced efficiency in bacterial gene transformation. Langmuir. 2015;31:4722–4732. doi: 10.1021/acs.langmuir.5b00402.
  • Tanner EEL, Wiraja C, Curreri CA, et al. Stabilization and topical skin delivery of framework nucleic acids using ionic liquids. Adv Therap. 2020;3:2000041. doi: 10.1002/adtp.202000041.
  • Mandal A, Kumbhojkar N, Reilly C, et al. Treatment of psoriasis with NFKBIZ siRNA using topical ionic liquid formulations. Sci Adv. 2020;6:eabb6049. doi: 10.1126/sciadv.abb6049.
  • Vermeij P, Kets E, Dirks C, et al. Liquid vaccines of live enveloped viruses. 2020.

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