Thermodynamic parameters to predict stability of RNA/DNA hybrid duplexes
Abstract
The thermodynamic parameters (delta H degree, delta S degree, and delta G degree 37) for 16 nearest-neighbor sets and one initiation factor are presented here in order to predict stability of RNA/DNA hybrid duplexes. To determine the nearest-neighbor parameters, thermodynamics for 68 different hybrid sequences (136 single-stranded oligonucleotides) with 5-13 nucleotide length including several duplexes with identical nearest-neighbors were measured by UV melting procedure. These sequences were selected to have many different combinations of nearest-neighbor pairs, and so that the number of the 16 nearest-neighbor sequences in the oligomers were as equal as possible. The structures of the hybrids were also investigated by measuring circular dichroism spectra. Comparing delta G degree 37 values of the hybrids with DNA/DNA and RNA/RNA parameters reported previously (Breslauer, K.J., Frank, R., Blöcker, H., & Marky, L.A. (1986) Proc. Natl. Acad. Sci. U.S.A. 83, 3746-3750; Freier, S.M., Kierzek, R., Jaeger, J.A., Sugimoto, N., Caruthers, M.H., Neilson, T., & Turner, D.H. (1986) Proc. Natl. Acad. Sci. U.S.A. 83, 9373-9377), RNA/RNA double helix is the most stable of the three kinds of helixes with the same nearest-neighbor sequences. Which is more stable between DNA/DNA and RNA/DNA hybrid duplexes depends on its sequence. Calculated thermodynamic values of hybrid formation with the present parameters reproduce the experimental values within reasonable errors.
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The energy terms used for stacking and mismatches have an error of around 5-10%.
“These energy terms have an error of around 5–10% (32,33,35).”
From The prebiotic evolutionary advantage of transferring genetic information from RNA to DNA (2011) · cites this paper as [35]
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MethodFurther Characterization of the Helicase Activity of eIF4A
Rogers, G. W., Lima, W. F., & Merrick, W. C. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m007560200 · Cited by 145 · see citing works
Effects of single-walled carbon nanotubes on the polymerase chain reaction
Cui, D., Tian, F., Kong, Y., et al. (2003) · Nanotechnology · doi:10.1088/0957-4484/15/1/030 · Cited by 145 · see citing works
Josephs, E. A., Koçak, D. D., Fitzgibbon, C. J., McMenemy, J., Gersbach, C. A., & Marszałek, P. E. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv892 · Cited by 139 · see citing works
“Sequence-dependent DNA:DNA hybridization free energies G◦(x)DNA:DNA were obtained from (30); sequence-dependent RNA:DNA hybridization free energies G◦(x)RNA:DNA were obtained from (31); and G◦(x)RNA:DNA values in cases of introduced point mismatches rG·dG, rC·dC, rA·dA and rU·dT were obtained from (32) (under slightly…”
BackgroundTemperature dependence of thermodynamic properties for DNA/DNA and RNA/DNA duplex formation.
Wu, P., Nakano, S., & Sugimoto, N. (2002) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2002.02970.x · Cited by 132 · see citing works
“It should be noted that the published NN-model parameters were generally extracted from the temperature-independent thermodynamic data [17,19,21,22,25].”
InfluentialSelf-citationMELTING, computing the melting temperature of nucleic acid duplex
Novère, N. L. (2001) · Bioinform. · doi:10.1093/bioinformatics/17.12.1226 · Cited by 142 · see citing works
“…et al. (1986); SantaLucia et al. (1996); Sugimoto et al. (1996), and Allawi and SantaLucia (1997) (the default) for the homoduplexes DNA/DNA, of Freier et al. (1986) and Xia et al. (1998) (the default) for the homoduplexes RNA/RNA, and of Sugimoto et al. (1995) for the heteroduplexes DNA/RNA.”
Target site selection for an RNA-cleaving catalytic DNA
Cairns, M. J., Hopkins, T. M., Witherington, C., et al. (1999) · Nature Biotechnology · doi:10.1038/8658 · Cited by 140 · see citing works
“To gain some appreciation of the relationship between heteroduplex stability and cleavage activity, the ΔG° was predicted for each deoxyribozyme (by the nearest neighbor metho”
MethodRoberts, C. C., Bandaru, R., & Switzer, C. (1997) · Journal of the American Chemical Society · doi:10.1021/ja970123s · Cited by 139 · see citing works
Mitigating off-target effects in CRISPR/Cas9-mediated in vivo gene editing
Han, H. A., Pang, J. K. S., & Soh, B.-S. (2020) · Journal of Molecular Medicine · doi:10.1007/s00109-020-01893-z · Cited by 143 · see citing works
“The underlying mechanism behind this change in specificity is unknown and intriguing given that an increase in GC content usually stabilises the hybridisation of RNA to DNA [51].”
BackgroundGuo, P., Haque, F., Hallahan, B. J., Reif, R. D., & Li, H. (2012) · Nucleic Acid Therapeutics · doi:10.1089/nat.2012.0350 · Cited by 130 · see citing works
“, 2010), base stacking properties (Searle and Williams, 1993; Sugimoto et al., 1995), and various in vivo attributes (Chang and Tinoco, 1994; Guo et al.”
InfluentialInterplay between DNA sequence and negative superhelicity drives R-loop structures
Stolz, R., Sulthana, S., Hartono, S. R., Malig, M., Benham, C., & Chédin, F. (2019) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1819476116 · Cited by 118 · see citing works
Structure, stability and behaviour of nucleic acids in ionic liquids
Tateishi‐Karimata, H., & Sugimoto, N. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku499 · Cited by 129 · see citing works
“Buffer containing 4 M NaCl was used, given that previous quantitative analyses of DNA duplex stabilities were performed in this solution (56).”
MethodSelf-citationLi, H., Lee, T., Dziubla, T. D., Pi, F., Guo, S., Xu, J., Li, C., Haque, F., Liang, X., & Guo, P. (2015) · Nano Today · doi:10.1016/j.nantod.2015.09.003 · Cited by 129 · see citing works
Yang, S., Chen, S., Liu, S., Tang, X., Qin, L., Qiu, G.-H., Chen, J.-X., & Chen, W. (2015) · Analytical Chemistry · doi:10.1021/acs.analchem.5b03084 · Cited by 123 · see citing works
Catalytic Nucleic Acids: From Lab to Applications
Sun, L., Cairns, M. J., Saravolac, E. G., Baker, A., & Gerlach, W. L. (2000) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01455-8 · Cited by 121 · see citing works
“Factors other than length that tend to increase the heteroduplex stability include the general GC content and specific pyrimidine’s content of the DNA component (Ratmeyer et al., 1994; Sugimoto et al., 1995; Gyi et al., 1998).”
Lin, Y., & Wilson, J. H. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00739-07 · Cited by 120 · see citing works
“Due to the exceptional stability of rG:dC base pairs (68), R-loops tend to form when the template FIG.”
BackgroundA Simple, Cost-Effective, and Robust Method for rRNA Depletion in RNA-Sequencing Studies
Culviner, P. H., Guegler, C. K., & Laub, M. T. (2020) · mBio · doi:10.1128/mbio.00010-20 · Cited by 121 · see citing works
“We used the default nearest-neighbor calculation table for RNA-DNA 218 hybrids(12).”
MethodFelder, S., Meierhoff, K., Sane, A. P., et al. (2001) · The Plant Cell · doi:10.1105/tpc.010090 · Cited by 121 · see citing works
“Because RNA-RNA hybrids are more stable than DNA-RNA hybrids under the chosen hybridization conditions (Sugimoto et al., 1995), this concurrent reaction results in psbT-psbH nonprocessed RNAs that have hybridized both the psbN RNA and the 5 psbH single-stranded DNA probe.”
BackgroundToulokhonov, I., & Landick, R. C. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00439-8 · Cited by 119 · see citing works
“…termination and bypass ( G‡, Flap Domain Mediates Pause Hairpin Action 1131 Molecular Cell 1132 (A) Structures of intrinsic terminators with the G of formation (in kcal/mol at 1 M NaCl and 37 C) for the terminator hairpin alone (red; Zuker, 2003) and the 8 bp hybrid (black; Sugimoto et al., 1995).”
BackgroundActivation of different split functionalities on re-association of RNA–DNA hybrids
Afonin, K. A., Viard, M., Martins, A. N., Lockett, S., Maciag, A. E., Freed, E. O., Heldman, E., Jaeger, L., Blumenthal, R. P., & Shapiro, B. A. (2013) · Nature Nanotechnology · doi:10.1038/nnano.2013.44 · Cited by 117 · see citing works
Jang, K., Jeong, S., Kang, D. Y., Sp, N., Yang, Y. M., & Kim, D. (2020) · Scientific Reports · doi:10.1038/s41598-020-61432-1 · Cited by 113 · see citing works
Mechanistic Approach to the Problem of Hybridization Efficiency in Fluorescent In Situ Hybridization
Yilmaz, L. S., & Noguera, D. R. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.12.7126-7139.2004 · Cited by 113 · see citing works
Farasat, I., & Salis, H. M. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004724 · Cited by 110 · see citing works
“These nearest-neighbor free energies are designated as ΔG and ΔG, and may be calculated using previously developed free energy models that have been parameterized using calorimetry measurements [52,53,54,55].”
BackgroundMethodInfluentialDeveloping RT-LAMP assays for rapid diagnosis of SARS-CoV-2 in saliva
Huang, X., Tang, G., Ismail, N., & Wang, X. (2021) · EBioMedicine · doi:10.1016/j.ebiom.2021.103736 · Cited by 110 · see citing works
“25,26 To avoid potential primer cross-reactivity due to low sequence complexity, a stretch of continuous same nucleotides was not allowed (4 C’s, 4 G’s, 5 A’s, or 5 T’s).”
Hu, Y., Rolfs, A., Bhullar, B., Murthy, T. V. S., Zhu, C., Berger, M. F., Camargo, A. A., Kelley, F., McCarron, S., Jepson, D., et al. (2007) · Genome Research · doi:10.1101/gr.6037607 · Cited by 109 · see citing works
“For Phases Three and Four, first-step PCR, optimal gene-specific primers were designed using a modified nearestneighbor algorithm (Sugimoto et al. 1995).”
MethodTranscriptional Pausing at +62 of the HIV-1 Nascent RNA Modulates Formation of the TAR RNA Structure
Palangat, M., Meier, T. I., Keene, R. G., & Landick, R. C. (1998) · Molecular Cell · doi:10.1016/s1097-2765(00)80103-3 · Cited by 108 · see citing works
“2 kcal/mol more stable than Does the HIV-1 Pause Play a Rolea 39-terminal hybrid (Sugimoto et al., 1995).”
BackgroundA Boost for the Emerging Field of RNA Nanotechnology
Shukla, G. C., Haque, F., Tor, Y., Wilhelmsson, L. M., Toulmé, J., Isambert, H., Guo, P., Rossi, J. J., Tenenbaum, S. A., & Shapiro, B. A. (2011) · ACS Nano · doi:10.1021/nn200989r · Cited by 107 · see citing works
Poliovirus RNA-dependent RNA Polymerase (3Dpol) Is Sufficient for Template Switchingin Vitro
Arnold, J. J., & Cameron, C. E. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.5.2706 · Cited by 106 · see citing works
Thermodynamics of base pairing
Turner, D. H. (1996) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(96)80047-9 · Cited by 104 · see citing works
Microarrays for identifying binding sites and probing structure of RNAs
Kierzek, R., Turner, D. H., & Kierzek, E. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku1303 · Cited by 103 · see citing works
“In this approach: (i) the probes are 5- or 6-nucleotides long and based on the natural 2′-O-methylated backbone because single-stranded regions within natural RNAs are short and 2′-O-methylRNA/RNA duplexes are more stable (38) than RNA/RNA (39) or DNA/RNA (40) duplexes, and (ii) the probes are modified to make hybridi…”
BackgroundInfluentialRNA nanotechnology for computer design and in vivo computation
Meikang Qiu, A., Khisamutdinov, E. F., Zhao, Z. J., Pan, C., Choi, J., Leontis, N. B., & Guo, P. (2013) · Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences · doi:10.1098/rsta.2012.0310 · Cited by 103 · see citing works
“RNA secondary structures are stabilized largely by nearest-neighbour interactions that can be measured in model systems [77,78].”
BackgroundManaging the sequence-specificity of antisense oligonucleotides in drug discovery
Hagedorn, P., Hansen, B. R., Koch, T., & Lindow, M. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx056 · Cited by 104 · see citing works
“Thermodynamic parameters are different for DNA– RNA binding compared with DNA–DNA binding (82,83) and DNA–RNA binding is also affected by chemical modifications such as LNA (84,85).”
BackgroundKankia, B. I., & Marky, L. A. (1999) · The Journal of Physical Chemistry B · doi:10.1021/jp991614x · Cited by 103 · see citing works
Chen, S. X., & Seelig, G. (2016) · Journal of the American Chemical Society · doi:10.1021/jacs.6b00277 · Cited by 101 · see citing works
CRISPR/Cas9 gRNA activity depends on free energy changes and on the target PAM context
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The α‐ L ‐Threofuranosyl‐(3′→2′)‐oligonucleotide System (‘TNA'): Synthesis and Pairing Properties
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Hendrix, D. A. (2019) · doi:10.5399/osu/1140 · Cited by 100 · see citing works
Suppression of Smooth Muscle Cell Proliferation by a c-myc RNA-cleaving Deoxyribozyme
Sun, L., Cairns, M. J., Gerlach, W. L., et al. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.24.17236 · Cited by 99 · see citing works
- Authors
- Sugimoto, N., Nakano, S.-I., Katoh, M., Matsumura, A., Nakamuta, H., Ohmichi, T., Yoneyama, M., & Sasaki, M.
- Affiliations
- Konan University (JP)
- Venue
- Biochemistry
- Publisher
- American Chemical Society (ACS)
- Published
- 1995-09-05
- Volume
- 34
- Issue
- 35
- Pages
- 11211-11216
- ISSN
- 0006-2960 (ISSN-L)
- 1520-4995
- OpenAlex
- W2010759469
- Semantic Scholar
- 5a5921b07eda10a7cfa0f9410e5f8048ae2d9247
- Cited by
- 697
- References
- 23
- Citations by year
- 2026: 23 · 2025: 21 · 2024: 35 · 2023: 19 · 2022: 23 · 2021: 23 · 2020: 25 · 2019: 27 · 2018: 17 · 2017: 23 · 2016: 23 · 2015: 23 · 2014: 27 · 2013: 30 · 2012: 26
- FWCI
- 2.85
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biochemistry (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Advanced biosensing and bioanalysis techniques
- Keywords
- hybrid stability, oligonucleotide duplexes, UV melting, circular dichroism, initiation factors
- MeSH terms
- Base Sequence, Circular Dichroism, DNA, Drug Stability, Molecular Sequence Data, Nucleic Acid Conformation, Nucleic Acid Hybridization, Oligodeoxyribonucleotides, Oligoribonucleotides, RNA, Thermodynamics, Molecular Structure
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