Structural Landscape of the Transition from an ssDNA Dumbbell Plus Its Complementary Hairpin to a dsDNA Microcircle Via a Kissing Loop Intermediate
Abstract
:1. Introduction
2. Results and Discussion
2.1. D42 Dumbbell and P42 Hairpin
2.2. Proposed Kissing Loop Interaction as a Pre-Annealing Step
2.3. Singly Nicked and Covalently Closed DNA Microcircle
2.4. Post-Ligation Pre-Release DNA Microcircle
3. Materials and Methods
3.1. Construction of the D42 Dumbbell and the P42 Hairpin
3.2. Construction of the Kissing Loop
3.3. Construction of the 42-bp Microcircle
3.4. Construction of the Post-Ligation Pre-Release T4 DNA Ligase–DNA Complexes
3.5. Solvation and Electroneutrality
3.6. Molecular Dynamics Simulations
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Sample Availability
References
- Engler, M.J.; Richardson, C.C. DNA Ligases. In The Enzymes, 3rd ed.; Boyer, P.D., Ed.; Nucleic Acids Part B; Academic Press Inc.: New York, NY, USA, 1982; Volume 15, pp. 3–29. [Google Scholar]
- Li, J.; Mohammed-Elsabagh, M.; Paczkowski, F.; Li, Y. Circular nucleic acids: Discovery, functions and applications. ChemBioChem 2020, 21, 1547–1566. [Google Scholar] [CrossRef]
- Hong, F.; Zhang, F.; Liu, Y.; Yan, H. DNA origami: Scaffolds for creating higher order structures. Chem. Rev. 2017, 117, 12584–12640. [Google Scholar] [CrossRef]
- Wang, J.; Li, S.; Xu, J.; Lu, Y.; Lin, M.; Wang, C.; Zhang, C.; Lin, G.; Jia, L. A functionalized dumbbell probe-based cascading exponential amplification DNA machine enables amplified probing of microRNAs. Chem. Commun. 2020, 56, 1681–1684. [Google Scholar] [CrossRef]
- Cyrill, S.L.; Ghosh, A.; Loh, P.S.; Tan, G.S.X.; Patzel, V. Universal template-assisted, cloning-free method for the generation of small RNA-expressing dumbbell-shaped DNA vectors. Mol. Ther.-Methods Clin. Dev. 2019, 15, 149–156. [Google Scholar] [CrossRef]
- Kool, E.T. Circular Oligonucleotides: New concepts in oligonucleotide design. Annu. Rev. Biophys. Biomol. Struct. 1996, 25, 1–28. [Google Scholar] [CrossRef]
- Kuhn, H.; Frank-Kamenetskii, M.D.; Demidov, V.V. High-purity preparation of a large DNA dumbbell. Antisense Nucleic Acid Drug Dev. 2001, 11, 149–153. [Google Scholar] [CrossRef]
- Travers, A. DNA Dynamics: Bubble ‘n’ Flip for DNA Cyclisation? Curr. Biol. 2005, 15, R377–R379. [Google Scholar] [CrossRef] [Green Version]
- Mitchell, J.S.; Laughton, C.A.; Harris, S.A. Atomistic simulations reveal bubbles, kinks and wrinkles in supercoiled DNA. Nucleic Acids Res. 2011, 39, 3928–3938. [Google Scholar] [CrossRef] [Green Version]
- Du, Q.; Kotlyar, A.; Vologodskii, A. Kinking the double helix by bending deformation. Nucleic Acids Res. 2007, 36, 1120–1128. [Google Scholar] [CrossRef] [Green Version]
- Harrison, R.M.; Romano, F.; Ouldridge, T.E.; Louis, A.; Doye, J.P.K. Identifying physical causes of apparent enhanced cyclization of short DNA molecules with a coarse-grained model. J. Chem. Theory Comput. 2019, 15, 4660–4672. [Google Scholar] [CrossRef] [Green Version]
- Pasi, M.; Mornico, D.; Volant, S.; Juchet, A.; Batisse, J.; Bouchier, C.; Parissi, V.; Ruff, M.; Lavery, R.; Lavigne, M. DNA minicircles clarify the specific role of DNA structure on retroviral integration. Nucleic Acids Res. 2016, 44, 7830–7847. [Google Scholar] [CrossRef] [Green Version]
- Harris, S.A.; Laughton, C.A.; Liverpool, T.B. Mapping the phase diagram of the writhe of DNA nanocircles using atomistic molecular dynamics simulations. Nucleic Acids Res. 2007, 36, 21–29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, H.; Zhang, Y.; Ou-Yang, Z.-C.; Lindsay, S.M.; Feng, X.-Z.; Balagurumoorthy, P.; Harrington, R.E. Conformation and rigidity of DNA microcircles containing waf1 response element for p53 regulatory protein. J. Mol. Biol. 2001, 306, 225–236. [Google Scholar] [CrossRef] [PubMed]
- Wang, Q.; Irobalieva, R.N.; Chiu, W.; Schmid, M.F.; Fogg, J.M.; Zechiedrich, L.; Pettitt, B.M. Influence of DNA sequence on the structure of minicircles under torsional stress. Nucleic Acids Res. 2017, 45, 7633–7642. [Google Scholar] [CrossRef]
- Wang, Q.; Pettitt, B.M. Sequence affects the cyclization of DNA minicircles. J. Phys. Chem. Lett. 2016, 7, 1042–1046. [Google Scholar] [CrossRef] [Green Version]
- Wolters, M.; Wittig, B. Construction of a 42 base pair double stranded DNA microcircle. Nucleic Acids Res. 1989, 17, 5163–5172. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Drozdetski, A.V.; Mukhopadhyay, A.; Onufriev, A.V. Strongly bent double-stranded DNA: Reconciling theory and experiment. Front. Phys. 2019, 7, 195. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barth, A.; Kobbe, D.; Focke, M. DNA–DNA kissing complexes as a new tool for the assembly of DNA nanostructures. Nucleic Acids Res. 2016, 44, 1502–1513. [Google Scholar] [CrossRef]
- Feng, B.; Sosa, R.P.; Mårtensson, A.K.F.; Jiang, K.; Tong, A.; Dorfman, K.D.; Takahashi, M.; Lincoln, P.; Bustamante, C.J.; Westerlund, F.; et al. Hydrophobic catalysis and a potential biological role of DNA unstacking induced by environment effects. Proc. Natl. Acad. Sci. USA 2019, 116, 17169–17174. [Google Scholar] [CrossRef] [Green Version]
- Rice, P.A.; Yang, S.-W.; Mizuuchi, K.; Nash, H.A. Crystal Structure of an IHF-DNA Complex: A protein-induced DNA U-turn. Cell 1996, 87, 1295–1306. [Google Scholar] [CrossRef] [Green Version]
- Walther, J.; Orozco, M. MC_DNA: A Web Server for the Detailed Study of the Structure and Dynamics of DNA and Chromatin Fibers. Available online: http://mmb.irbbarcelona.org/MCDNA/ (accessed on 29 April 2021).
- Shi, K.; Bohl, T.E.; Park, J.; Zasada, A.; Malik, S.; Banerjee, S.; Tran, V.; Li, N.; Yin, Z.; Kurniawan, F.; et al. T4 DNA ligase structure reveals a prototypical ATP-dependent ligase with a unique mode of sliding clamp interaction. Nucleic Acids Res. 2018, 46, 10474–10488. [Google Scholar] [CrossRef]
- Boniecki, M.J.; Lach, G.; Dawson, W.K.; Tomala, K.; Lukasz, P.; Soltysinski, T.; Rother, K.M.; Bujnicki, J.M. SimRNA: A coarse-grained method for RNA folding simulations and 3D structure prediction. Nucleic Acids Res. 2016, 44, e63. [Google Scholar] [CrossRef]
- Schrodinger, LLC. The PyMOL Molecular Graphics System, Version 1.8; Schrodinger, LLC: New York, NY, USA, 2015.
- Lebars, I.; Legrand, P.; Aimé, A.; Pinaud, N.; Fribourg, S.; Di Primo, C. Exploring TAR–RNA aptamer loop–loop interaction by X-ray crystallography, UV spectroscopy and surface plasmon resonance. Nucleic Acids Res. 2008, 36, 7146–7156. [Google Scholar] [CrossRef] [Green Version]
- Macke, T.; Case, D.A. Modeling unusual nucleic acid structures. In Molecular Modeling of Nucleic Acids; Leontes, N.B., SantaLucia, J., Eds.; American Chemical Society: Washington, DC, USA, 1998; pp. 379–393. [Google Scholar]
- Case, D.A.; Ben-Shalom, I.Y.; Brozell, S.R.; Cerutti, D.S.; Cheatham, T.E.; Cruzeiro, V.W.D., III; Darden, T.A.; Duke, R.E.; Ghoreishi, D.; Gilson, M.K.; et al. AMBER 2018; University of California: San Francisco, CA, USA, 2018. [Google Scholar]
- Mills, A.; Gago, F. Atomistic insight into sequence-directed DNA bending and minicircle formation propensity in the absence and presence of phased A-tracts. J. Comput. Mol. Des. 2020, 34, 253–265. [Google Scholar] [CrossRef]
- Waterhouse, A.; Bertoni, M.; Bienert, S.; Studer, G.; Tauriello, G.; Gumienny, R.; Heer, F.T.; de Beer, T.A.P.; Rempfer, C.; Bordoli, L.; et al. SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Res. 2018, 46, W296–W303. [Google Scholar] [CrossRef] [Green Version]
- Maier, J.A.; Martinez, C.; Kasavajhala, K.; Wickstrom, L.; Hauser, K.E.; Simmerling, C. ff14SB: Improving the accuracy of protein side chain and backbone parameters from ff99SB. J. Chem. Theory Comput. 2015, 11, 3696–3713. [Google Scholar] [CrossRef] [Green Version]
- Li, P.; Merz, K.M. Taking into account the ion-induced dipole interaction in the nonbonded model of ions. J. Chem. Theory Comput. 2014, 10, 289–297. [Google Scholar] [CrossRef] [Green Version]
- Wang, H.; Laughton, C.A. Molecular modelling methods to quantitate drug-DNA interactions. Methods Mol. Biol. 2010, 613, 119–131. [Google Scholar] [CrossRef]
- Iwasa, J.H. The scientist as illustrator. Trends Immunol. 2016, 37, 247–250. [Google Scholar] [CrossRef] [Green Version]
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Mills, A.; Gago, F. Structural Landscape of the Transition from an ssDNA Dumbbell Plus Its Complementary Hairpin to a dsDNA Microcircle Via a Kissing Loop Intermediate. Molecules 2021, 26, 3017. https://doi.org/10.3390/molecules26103017
Mills A, Gago F. Structural Landscape of the Transition from an ssDNA Dumbbell Plus Its Complementary Hairpin to a dsDNA Microcircle Via a Kissing Loop Intermediate. Molecules. 2021; 26(10):3017. https://doi.org/10.3390/molecules26103017
Chicago/Turabian StyleMills, Alberto, and Federico Gago. 2021. "Structural Landscape of the Transition from an ssDNA Dumbbell Plus Its Complementary Hairpin to a dsDNA Microcircle Via a Kissing Loop Intermediate" Molecules 26, no. 10: 3017. https://doi.org/10.3390/molecules26103017