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High-throughput single-molecule quantification of individual base stacking energies in nucleic acids

Author

Listed:
  • Jibin Abraham Punnoose

    (University at Albany, State University of New York)

  • Kevin J. Thomas

    (University at Albany, State University of New York)

  • Arun Richard Chandrasekaran

    (University at Albany, State University of New York)

  • Javier Vilcapoma

    (University at Albany, State University of New York)

  • Andrew Hayden

    (University at Albany, State University of New York)

  • Kacey Kilpatrick

    (University at Albany, State University of New York
    University at Albany, State University of New York)

  • Sweta Vangaveti

    (University at Albany, State University of New York)

  • Alan Chen

    (University at Albany, State University of New York
    University at Albany, State University of New York)

  • Thomas Banco

    (University at Albany, State University of New York)

  • Ken Halvorsen

    (University at Albany, State University of New York)

Abstract

Base stacking interactions between adjacent bases in DNA and RNA are important for many biological processes and in biotechnology applications. Previous work has estimated stacking energies between pairs of bases, but contributions of individual bases has remained unknown. Here, we use a Centrifuge Force Microscope for high-throughput single molecule experiments to measure stacking energies between adjacent bases. We found stacking energies strongest between purines (G|A at −2.3 ± 0.2 kcal/mol) and weakest between pyrimidines (C|T at −0.5 ± 0.1 kcal/mol). Hybrid stacking with phosphorylated, methylated, and RNA nucleotides had no measurable effect, but a fluorophore modification reduced stacking energy. We experimentally show that base stacking can influence stability of a DNA nanostructure, modulate kinetics of enzymatic ligation, and assess accuracy of force fields in molecular dynamics simulations. Our results provide insights into fundamental DNA interactions that are critical in biology and can inform design in biotechnology applications.

Suggested Citation

  • Jibin Abraham Punnoose & Kevin J. Thomas & Arun Richard Chandrasekaran & Javier Vilcapoma & Andrew Hayden & Kacey Kilpatrick & Sweta Vangaveti & Alan Chen & Thomas Banco & Ken Halvorsen, 2023. "High-throughput single-molecule quantification of individual base stacking energies in nucleic acids," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36373-8
    DOI: 10.1038/s41467-023-36373-8
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    References listed on IDEAS

    as
    1. Emily M. Harcourt & Anna M. Kietrys & Eric T. Kool, 2017. "Chemical and structural effects of base modifications in messenger RNA," Nature, Nature, vol. 541(7637), pages 339-346, January.
    2. Darren Yang & Andrew Ward & Ken Halvorsen & Wesley P. Wong, 2016. "Multiplexed single-molecule force spectroscopy using a centrifuge," Nature Communications, Nature, vol. 7(1), pages 1-7, April.
    3. Jessica L. Childs-Disney & Ewa Stepniak-Konieczna & Tuan Tran & Ilyas Yildirim & HaJeung Park & Catherine Z. Chen & Jason Hoskins & Noel Southall & Juan J. Marugan & Samarjit Patnaik & Wei Zheng & Chr, 2013. "Induction and reversal of myotonic dystrophy type 1 pre-mRNA splicing defects by small molecules," Nature Communications, Nature, vol. 4(1), pages 1-11, October.
    4. Brian J. Cafferty & David M. Fialho & Jaheda Khanam & Ramanarayanan Krishnamurthy & Nicholas V. Hud, 2016. "Spontaneous formation and base pairing of plausible prebiotic nucleotides in water," Nature Communications, Nature, vol. 7(1), pages 1-8, September.
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