Single-molecule analysis of DNA base-stacking energetics using patterned DNA nanostructures – Nature Nanotechnology

Watson, J. D. & Crick, F. H. Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 171, 737–738 (1953).

Article  CAS  Google Scholar 

Kool, E. T. Hydrogen bonding, base stacking, and steric effects in DNA replication. Annu. Rev. Biophys. Biomol. Struct. 30, 1–22 (2001).

Article  CAS  Google Scholar 

Yakovchuk, P., Protozanova, E. & Frank-Kamenetskii, M. D. Base-stacking and base-pairing contributions into thermal stability of the DNA double helix. Nucleic Acids Res. 34, 564–574 (2006).

Article  CAS  Google Scholar 

Schulz, E. C. et al. Intermolecular base stacking mediates RNA–RNA interaction in a crystal structure of the RNA chaperone Hfq. Sci. Rep. 7, 9903 (2017).

Article  Google Scholar 

Kervio, E., Hochgesand, A., Steiner, U. E. & Richert, C. Templating efficiency of naked DNA. Proc. Natl Acad. Sci. USA 107, 12074–12079 (2010).

Article  CAS  Google Scholar 

Gerling, T., Wagenbauer, K. F., Neuner, A. M. & Dietz, H. Dynamic DNA devices and assemblies formed by shape-complementary, non-base pairing 3D components. Science 347, 1446–1452 (2015).

Article  CAS  Google Scholar 

Uehara, S. et al. 3′ Poly (dA)-tailed thrombin DNA aptamer to increase DNase-resistance and clotting inhibitory activity. Bull. Chem. Soc. Jpn 81, 1485–1491 (2008).

Article  CAS  Google Scholar 

Do, N. Q., Lim, K. W., Teo, M. H., Heddi, B. & Phan, A. T. Stacking of G-quadruplexes: NMR structure of a G-rich oligonucleotide with potential anti-HIV and anticancer activity. Nucleic Acids Res. 39, 9448–9457 (2011).

Article  CAS  Google Scholar 

Modi, S. et al. A DNA nanomachine that maps spatial and temporal pH changes inside living cells. Nat. Nanotechnol. 4, 325–330 (2009).

Article  CAS  Google Scholar 

Surana, S., Shenoy, A. R. & Krishnan, Y. Designing DNA nanodevices for compatibility with the immune system of higher organisms. Nat. Nanotechnol. 10, 741–747 (2015).

Article  CAS  Google Scholar 

Sigl, C. et al. Programmable icosahedral shell system for virus trapping. Nat. Mater. 20, 1281–1289 (2021).

Article  CAS  Google Scholar 

Hellmeier, J. et al. DNA origami demonstrate the unique stimulatory power of single pMHCs as T cell antigens. Proc. Natl Acad. Sci. USA 118, e2016857118 (2021).

Article  CAS  Google Scholar 

Woo, S. & Rothemund, P. W. K. Programmable molecular recognition based on the geometry of DNA nanostructures. Nat. Chem. 3, 620–627 (2011).

Article  CAS  Google Scholar 

Wang, R., Kuzuya, A., Liu, W. & Seeman, N. C. Blunt-ended DNA stacking interactions in a 3-helix motif. Chem. Commun. 46, 4905–4907 (2010).

Article  CAS  Google Scholar 

Pumm, A.-K. et al. A DNA origami rotary ratchet motor. Nature 607, 492–498 (2022).

Article  CAS  Google Scholar 

Bommarito, S., Peyret, N. & SantaLucia, J. Jr Thermodynamic parameters for DNA sequences with dangling ends. Nucleic Acids Res. 28, 1929–1934 (2000).

Article  CAS  Google Scholar 

Petersheim, M. & Turner, D. H. Base-stacking and base-pairing contributions to helix stability: thermodynamics of double-helix formation with CCGG, CCGGp, CCGGAp, ACCGGp, CCGGUp, and ACCGGUp. Biochemistry 22, 256–263 (1983).

Article  CAS  Google Scholar 

Gotoh, O. & Tagashira, Y. Stabilities of nearest-neighbor doublets in double-helical DNA determined by fitting calculated melting profiles to observed profiles. Biopolymers 20, 1033–1042 (1981).

Article  CAS  Google Scholar 

Vologodskii, A. V., Amirikyan, B., Lyubchenko, Y. L. & Frank-Kamenetskii, M. Allowance for heterogeneous stacking in the DNA helix-coil transition theory. J. Biomol. Struct. Dyn. 2, 131–148 (1984).

Article  CAS  Google Scholar 

Breslauer, K. J., Frank, R., Blöcker, H. & Marky, L. A. Predicting DNA duplex stability from the base sequence. Proc. Natl Acad. Sci. USA 83, 3746–3750 (1986).

Article  CAS  Google Scholar 

Delcourt, S. G. & Blake, R. Stacking energies in DNA. J. Biol. Chem. 266, 15160–15169 (1991).

Article  CAS  Google Scholar 

Doktycz, M. J., Goldstein, R. F., Paner, T. M., Gallo, F. J. & Benight, A. S. Studies of DNA dumbbells. I. Melting curves of 17 DNA dumbbells with different duplex stem sequences linked by T4 endloops: Evaluation of the nearest‐neighbor stacking interactions in DNA. Biopolymers 32, 849–864 (1992).

Article  CAS  Google Scholar 

SantaLucia, J., Allawi, H. T. & Seneviratne, P. A. Improved nearest-neighbor parameters for predicting DNA duplex stability. Biochemistry 35, 3555–3562 (1996).

Article  CAS  Google Scholar 

Sugimoto, N., Nakano, S.-i, Yoneyama, M. & Honda, K.-I. Improved thermodynamic parameters and helix initiation factor to predict stability of DNA duplexes. Nucleic Acids Res. 24, 4501–4505 (1996).

Article  CAS  Google Scholar 

SantaLucia, J. Jr A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics. Proc. Natl Acad. Sci. USA 95, 1460–1465 (1998).

Article  CAS  Google Scholar 

Protozanova, E., Yakovchuk, P. & Frank-Kamenetskii, M. D. Stacked–unstacked equilibrium at the nick site of DNA. J. Mol. Biol. 342, 775–785 (2004).

Article  CAS  Google Scholar 

Lane, M. J. et al. The thermodynamic advantage of DNA oligonucleotide ‘stacking hybridization’ reactions: energetics of a DNA nick. Nucleic Acids Res. 25, 611–617 (1997).

Article  CAS  Google Scholar 

Pyshnyi, D. & Ivanova, E. Thermodynamic parameters of coaxial stacking on stacking hybridization of oligodeoxyribonucleotides. Russ. Chem. Bull. 51, 1145–1155 (2002).

Article  CAS  Google Scholar 

Kilchherr, F. et al. Single-molecule dissection of stacking forces in DNA. Science 353, aaf5508 (2016).

Article  Google Scholar 

Abraham Punnoose, J. et al. High-throughput single-molecule quantification of individual base stacking energies in nucleic acids. Nat. Commun. 14, 631 (2023).

Article  CAS  Google Scholar 

Rieu, M. et al. Parallel, linear, and subnanometric 3D tracking of microparticles with Stereo Darkfield Interferometry. Sci. Adv. 7, eabe3902 (2021).

Article  CAS  Google Scholar 

Rothemund, P. W. Folding DNA to create nanoscale shapes and patterns. Nature 440, 297–302 (2006).

Article  CAS  Google Scholar 

Schnitzbauer, J., Strauss, M. T., Schlichthaerle, T., Schueder, F. & Jungmann, R. Super-resolution microscopy with DNA-PAINT. Nat. Protoc. 12, 1198–1228 (2017).

Article  CAS  Google Scholar 

Jungmann, R. et al. Single-molecule kinetics and super-resolution microscopy by fluorescence imaging of transient binding on DNA origami. Nano Lett. 10, 4756–4761 (2010).

Article  CAS  Google Scholar 

Ganji, M., Schlichthaerle, T., Eklund, A. S., Strauss, S. & Jungmann, R. Quantitative assessment of labeling probes for super-resolution microscopy using designer DNA nanostructures. ChemPhysChem 22, 911–914 (2021).

Article  CAS  Google Scholar 

Vasiliskov, V. A., Prokopenko, D. V. & Mirzabekov, A. D. Parallel multiplex thermodynamic analysis of coaxial base stacking in DNA duplexes by oligodeoxyribonucleotide microchips. Nucleic Acids Res. 29, 2303–2313 (2001).

Article  CAS  Google Scholar 

Strauss, S. & Jungmann, R. Up to 100-fold speed-up and multiplexing in optimized DNA-PAINT. Nat. Methods 17, 789–791 (2020).

Article  CAS  Google Scholar 

Schickinger, M., Zacharias, M. & Dietz, H. Tethered multifluorophore motion reveals equilibrium transition kinetics of single DNA double helices. Proc. Natl Acad. Sci. USA 115, E7512–E7521 (2018).

Article  CAS  Google Scholar 

Eklund, A. S., Ganji, M., Gavins, G., Seitz, O. & Jungmann, R. Peptide-PAINT super-resolution imaging using transient coiled coil interactions. Nano Lett. 20, 6732–6737 (2020).

Article  CAS  Google Scholar 

Cisse, I. I., Kim, H. & Ha, T. A rule of seven in Watson–Crick base-pairing of mismatched sequences. Nat. Struct. Mol. Biol. 19, 623–627 (2012).

Article  CAS  Google Scholar 

Wong, K.-Y. & Pettitt, B. M. The pathway of oligomeric DNA melting investigated by molecular dynamics simulations. Biophys. J. 95, 5618–5626 (2008).

Article  CAS  Google Scholar 

Andrews, R. et al. Transient DNA binding to gapped DNA substrates links DNA sequence to the single-molecule kinetics of protein–DNA interactions. Preprint at bioRxiv https://doi.org/10.1101/2022.02.27.482175 (2022).

Ganji, M., Docter, M., Le Grice, S. F. & Abbondanzieri, E. A. DNA binding proteins explore multiple local configurations during docking via rapid rebinding. Nucleic Acids Res. 44, 8376–8384 (2016).

Article  CAS  Google Scholar 

Hertel, S. et al. The stability and number of nucleating interactions determine DNA hybridization rates in the absence of secondary structure. Nucleic Acids Res. 50, 7829–7841 (2022).

Article  CAS  Google Scholar 

Zacharias, M. Base-pairing and base-stacking contributions to double-stranded DNA formation. J. Phys. Chem. B 124, 10345–10352 (2020).

Article  CAS  Google Scholar 

Pyshnyi, D. V. et al. Thermodynamic analysis of stacking hybridization of oligonucleotides with DNA template. J. Biomol. Struct. Dyn. 19, 555–570 (2001).

Article  CAS  Google Scholar 

Krueger, A., Protozanova, E. & Frank-Kamenetskii, M. D. Sequence-dependent basepair opening in DNA double helix. Biophys. J. 90, 3091–3099 (2006).

Article  CAS  Google Scholar 

Ouldridge, T. E., Louis, A. A. & Doye, J. P. K. Structural, mechanical, and thermodynamic properties of a coarse-grained DNA model. J. Chem. Phys. 134, 085101 (2011).

Article  Google Scholar 

Maffeo, C., Luan, B. & Aksimentiev, A. End-to-end attraction of duplex DNA. Nucleic Acids Res. 40, 3812–3821 (2012).

Article  CAS  Google Scholar 

Rohloff, J. C. et al. Nucleic acid ligands with protein-like side chains: modified aptamers and their use as diagnostic and therapeutic agents. Mol. Ther. Nucleic Acids 3, e201 (2014).

Article  CAS  Google Scholar 

He, Y. et al. Hierarchical self-assembly of DNA into symmetric supramolecular polyhedra. Nature 452, 198–201 (2008).

Article  CAS  Google Scholar 

Wade, O. K. et al. 124-color super-resolution imaging by engineering DNA-PAINT blinking kinetics. Nano Lett. 19, 2641–2646 (2019).

Article  CAS  Google Scholar 

Ho, H. N., Zalami, D., Köhler, J., van Oijen, A. M. & Ghodke, H. Identification of multiple kinetic populations of DNA-binding proteins in live cells. Biophys. J. 117, 950–961 (2019).

Article  CAS  Google Scholar 

Jungmann, R. et al. Multiplexed 3D cellular super-resolution imaging with DNA-PAINT and Exchange-PAINT. Nat. Methods 11, 313–318 (2014).

Article  CAS  Google Scholar