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  1. Article ; Online: Dynamic basis for dA•dGTP and dA•d8OGTP misincorporation via Hoogsteen base pairs.

    Gu, Stephanie / Szymanski, Eric S / Rangadurai, Atul K / Shi, Honglue / Liu, Bei / Manghrani, Akanksha / Al-Hashimi, Hashim M

    Nature chemical biology

    2023  Volume 19, Issue 7, Page(s) 900–910

    Abstract: Replicative errors contribute to the genetic diversity needed for evolution but in high frequency can lead to genomic instability. Here, we show that DNA dynamics determine the frequency of misincorporating the A•G mismatch, and altered dynamics explain ... ...

    Abstract Replicative errors contribute to the genetic diversity needed for evolution but in high frequency can lead to genomic instability. Here, we show that DNA dynamics determine the frequency of misincorporating the A•G mismatch, and altered dynamics explain the high frequency of 8-oxoguanine (8OG) A•8OG misincorporation. NMR measurements revealed that A
    MeSH term(s) Humans ; Base Pairing ; DNA/chemistry ; DNA Damage ; Mutagenesis
    Chemical Substances DNA (9007-49-2)
    Language English
    Publishing date 2023-04-24
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural
    ZDB-ID 2202962-X
    ISSN 1552-4469 ; 1552-4450
    ISSN (online) 1552-4469
    ISSN 1552-4450
    DOI 10.1038/s41589-023-01306-5
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  2. Article: Probing conformational transitions towards mutagenic Watson–Crick-like G·T mismatches using off-resonance sugar carbon R1ρ relaxation dispersion

    Rangadurai, Atul / Szymanski, Eric S. / Kimsey, Isaac / Shi, Honglue / Al-Hashimi, Hashim M.

    Journal of biomolecular NMR. 2020 Sept., v. 74, no. 8-9

    2020  

    Abstract: NMR off-resonance R₁ᵨ relaxation dispersion measurements on base carbon and nitrogen nuclei have revealed that wobble G·T/U mismatches in DNA and RNA duplexes exist in dynamic equilibrium with short-lived, low-abundance, and mutagenic Watson–Crick-like ... ...

    Abstract NMR off-resonance R₁ᵨ relaxation dispersion measurements on base carbon and nitrogen nuclei have revealed that wobble G·T/U mismatches in DNA and RNA duplexes exist in dynamic equilibrium with short-lived, low-abundance, and mutagenic Watson–Crick-like conformations. As Watson–Crick-like G·T mismatches have base pairing geometries similar to Watson–Crick base pairs, we hypothesized that they would mimic Watson–Crick base pairs with respect to the sugar-backbone conformation as well. Using off-resonance R₁ᵨ measurements targeting the sugar C3′ and C4′ nuclei, a structure survey, and molecular dynamics simulations, we show that wobble G·T mismatches adopt sugar-backbone conformations that deviate from the canonical Watson–Crick conformation and that transitions toward tautomeric and anionic Watson–Crick-like G·T mismatches restore the canonical Watson–Crick sugar-backbone. These measurements also reveal kinetic isotope effects for tautomerization in D₂O versus H₂O, which provide experimental evidence in support of a transition state involving proton transfer. The results provide additional evidence in support of mutagenic Watson–Crick-like G·T mismatches, help rule out alternative inverted wobble conformations in the case of anionic G·T⁻, and also establish sugar carbons as new non-exchangeable probes of this exchange process.
    Keywords DNA ; RNA ; carbon ; isotopes ; molecular dynamics ; mutagens ; nitrogen ; sugars ; surveys ; tautomerization
    Language English
    Dates of publication 2020-09
    Size p. 457-471.
    Publishing place Springer Netherlands
    Document type Article
    ZDB-ID 1081696-3
    ISSN 0925-2738
    ISSN 0925-2738
    DOI 10.1007/s10858-020-00337-7
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  3. Article ; Online: Structural basis for impaired 5' processing of a mutant tRNA associated with defects in neuronal homeostasis.

    Lai, Lien B / Lai, Stella M / Szymanski, Eric S / Kapur, Mridu / Choi, Edric K / Al-Hashimi, Hashim M / Ackerman, Susan L / Gopalan, Venkat

    Proceedings of the National Academy of Sciences of the United States of America

    2022  Volume 119, Issue 10, Page(s) e2119529119

    Abstract: SignificanceUnderstanding and treating neurological disorders are global priorities. Some of these diseases are engendered by mutations that cause defects in the cellular synthesis of transfer RNAs (tRNAs), which function as adapter molecules that ... ...

    Abstract SignificanceUnderstanding and treating neurological disorders are global priorities. Some of these diseases are engendered by mutations that cause defects in the cellular synthesis of transfer RNAs (tRNAs), which function as adapter molecules that translate messenger RNAs into proteins. During tRNA biogenesis, ribonuclease P catalyzes removal of the transcribed sequence upstream of the mature tRNA. Here, we focus on a cytoplasmic tRNA
    MeSH term(s) Animals ; Base Pairing ; Cerebral Cortex/enzymology ; Homeostasis ; Magnesium/metabolism ; Mice ; Models, Molecular ; Neurons/metabolism ; Nucleic Acid Conformation ; Point Mutation ; Protein Processing, Post-Translational ; RNA, Transfer/chemistry ; RNA, Transfer/genetics ; RNA, Transfer/metabolism ; Ribonuclease P/isolation & purification ; Ribonuclease P/metabolism ; Substrate Specificity
    Chemical Substances RNA, Transfer (9014-25-9) ; Ribonuclease P (EC 3.1.26.5) ; Magnesium (I38ZP9992A)
    Language English
    Publishing date 2022-03-01
    Publishing country United States
    Document type Journal Article
    ZDB-ID 209104-5
    ISSN 1091-6490 ; 0027-8424
    ISSN (online) 1091-6490
    ISSN 0027-8424
    DOI 10.1073/pnas.2119529119
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  4. Article ; Online: Probing conformational transitions towards mutagenic Watson-Crick-like G·T mismatches using off-resonance sugar carbon R

    Rangadurai, Atul / Szymanski, Eric S / Kimsey, Isaac / Shi, Honglue / Al-Hashimi, Hashim M

    Journal of biomolecular NMR

    2020  Volume 74, Issue 8-9, Page(s) 457–471

    Abstract: NMR off-resonance ... ...

    Abstract NMR off-resonance R
    MeSH term(s) Base Pair Mismatch ; Base Pairing ; Carbon/chemistry ; DNA/chemistry ; Hydrogen Bonding ; Models, Molecular ; Molecular Structure ; Nuclear Magnetic Resonance, Biomolecular ; Nucleic Acid Conformation ; Sugars/chemistry ; Thymine
    Chemical Substances Sugars ; Carbon (7440-44-0) ; DNA (9007-49-2) ; Thymine (QR26YLT7LT)
    Language English
    Publishing date 2020-08-12
    Publishing country Netherlands
    Document type Journal Article
    ZDB-ID 1081696-3
    ISSN 1573-5001 ; 0925-2738
    ISSN (online) 1573-5001
    ISSN 0925-2738
    DOI 10.1007/s10858-020-00337-7
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  5. Article ; Online: Direct NMR Evidence that Transient Tautomeric and Anionic States in dG·dT Form Watson-Crick-like Base Pairs.

    Szymanski, Eric S / Kimsey, Isaac J / Al-Hashimi, Hashim M

    Journal of the American Chemical Society

    2017  Volume 139, Issue 12, Page(s) 4326–4329

    Abstract: The replicative and translational machinery utilizes the unique geometry of canonical G·C and A·T/U Watson-Crick base pairs to discriminate against DNA and RNA mismatches in order to ensure high fidelity replication, transcription, and translation. There ...

    Abstract The replicative and translational machinery utilizes the unique geometry of canonical G·C and A·T/U Watson-Crick base pairs to discriminate against DNA and RNA mismatches in order to ensure high fidelity replication, transcription, and translation. There is growing evidence that spontaneous errors occur when mismatches adopt a Watson-Crick-like geometry through tautomerization and/or ionization of the bases. Studies employing NMR relaxation dispersion recently showed that wobble dG·dT and rG·rU mismatches in DNA and RNA duplexes transiently form tautomeric and anionic species with probabilities (≈0.01-0.40%) that are in concordance with replicative and translational errors. Although computational studies indicate that these exceptionally short-lived and low-abundance species form Watson-Crick-like base pairs, their conformation could not be directly deduced from the experimental data, and alternative pairing geometries could not be ruled out. Here, we report direct NMR evidence that the transient tautomeric and anionic species form hydrogen-bonded Watson-Crick-like base pairs. A guanine-to-inosine substitution, which selectively knocks out a Watson-Crick-type (G)N2H
    MeSH term(s) Anions/chemistry ; Base Pair Mismatch ; Base Pairing ; DNA/chemistry ; Guanine/chemistry ; Nuclear Magnetic Resonance, Biomolecular ; Nucleic Acid Conformation ; RNA/chemistry ; Thymine/chemistry
    Chemical Substances Anions ; Guanine (5Z93L87A1R) ; RNA (63231-63-0) ; DNA (9007-49-2) ; Thymine (QR26YLT7LT)
    Language English
    Publishing date 2017-03-20
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural
    ZDB-ID 3155-0
    ISSN 1520-5126 ; 0002-7863
    ISSN (online) 1520-5126
    ISSN 0002-7863
    DOI 10.1021/jacs.7b01156
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  6. Article: Direct NMR Evidence that Transient Tautomeric and Anionic States in dG·dT Form Watson–Crick-like Base Pairs

    Szymanski, Eric S / Al-Hashimi Hashim M / Kimsey Isaac J

    Journal of the American Chemical Society. 2017 Mar. 29, v. 139, no. 12

    2017  

    Abstract: The replicative and translational machinery utilizes the unique geometry of canonical G·C and A·T/U Watson–Crick base pairs to discriminate against DNA and RNA mismatches in order to ensure high fidelity replication, transcription, and translation. ... ...

    Abstract The replicative and translational machinery utilizes the unique geometry of canonical G·C and A·T/U Watson–Crick base pairs to discriminate against DNA and RNA mismatches in order to ensure high fidelity replication, transcription, and translation. There is growing evidence that spontaneous errors occur when mismatches adopt a Watson–Crick-like geometry through tautomerization and/or ionization of the bases. Studies employing NMR relaxation dispersion recently showed that wobble dG·dT and rG·rU mismatches in DNA and RNA duplexes transiently form tautomeric and anionic species with probabilities (≈0.01–0.40%) that are in concordance with replicative and translational errors. Although computational studies indicate that these exceptionally short-lived and low-abundance species form Watson–Crick-like base pairs, their conformation could not be directly deduced from the experimental data, and alternative pairing geometries could not be ruled out. Here, we report direct NMR evidence that the transient tautomeric and anionic species form hydrogen-bonded Watson–Crick-like base pairs. A guanine-to-inosine substitution, which selectively knocks out a Watson–Crick-type (G)N2H₂···O2(T) hydrogen bond, significantly destabilized the transient tautomeric and anionic species, as assessed by lack of any detectable chemical exchange by imino nitrogen rotating frame spin relaxation (R₁ᵨ) experiments. An ¹⁵N R₁ᵨ NMR experiment targeting the amino nitrogen of guanine (dG-N2) provides direct evidence for Watson–Crick (G)N2H₂···O2(T) hydrogen bonding in the transient tautomeric state. The strategy presented in this work can be generally applied to examine hydrogen-bonding patterns in nucleic acid transient states including in other tautomeric and anionic species that are postulated to play roles in replication and translational errors.
    Keywords amino nitrogen ; DNA ; geometry ; guanine ; hydrogen bonding ; ionization ; nitrogen ; nuclear magnetic resonance spectroscopy ; oxygen ; RNA ; stable isotopes ; translation (genetics)
    Language English
    Dates of publication 2017-0329
    Size p. 4326-4329.
    Publishing place American Chemical Society
    Document type Article
    ZDB-ID 3155-0
    ISSN 1520-5126 ; 0002-7863
    ISSN (online) 1520-5126
    ISSN 0002-7863
    DOI 10.1021%2Fjacs.7b01156
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  7. Article ; Online: Why are Hoogsteen base pairs energetically disfavored in A-RNA compared to B-DNA?

    Rangadurai, Atul / Zhou, Huiqing / Merriman, Dawn K / Meiser, Nathalie / Liu, Bei / Shi, Honglue / Szymanski, Eric S / Al-Hashimi, Hashim M

    Nucleic acids research

    2018  Volume 46, Issue 20, Page(s) 11099–11114

    Abstract: A(syn)-U/T and G(syn)-C+ Hoogsteen (HG) base pairs (bps) are energetically more disfavored relative to Watson-Crick (WC) bps in A-RNA as compared to B-DNA by >1 kcal/mol for reasons that are not fully understood. Here, we used NMR spectroscopy, optical ... ...

    Abstract A(syn)-U/T and G(syn)-C+ Hoogsteen (HG) base pairs (bps) are energetically more disfavored relative to Watson-Crick (WC) bps in A-RNA as compared to B-DNA by >1 kcal/mol for reasons that are not fully understood. Here, we used NMR spectroscopy, optical melting experiments, molecular dynamics simulations and modified nucleotides to identify factors that contribute to this destabilization of HG bps in A-RNA. Removing the 2'-hydroxyl at single purine nucleotides in A-RNA duplexes did not stabilize HG bps relative to WC. In contrast, loosening the A-form geometry using a bulge in A-RNA reduced the energy cost of forming HG bps at the flanking sites to B-DNA levels. A structural and thermodynamic analysis of purine-purine HG mismatches reveals that compared to B-DNA, the A-form geometry disfavors syn purines by 1.5-4 kcal/mol due to sugar-backbone rearrangements needed to sterically accommodate the syn base. Based on MD simulations, an additional penalty of 3-4 kcal/mol applies for purine-pyrimidine HG bps due to the higher energetic cost associated with moving the bases to form hydrogen bonds in A-RNA versus B-DNA. These results provide insights into a fundamental difference between A-RNA and B-DNA duplexes with important implications for how they respond to damage and post-transcriptional modifications.
    MeSH term(s) Base Pairing/physiology ; DNA/chemistry ; DNA, B-Form/chemistry ; Energy Metabolism ; Hydrogen Bonding ; Magnetic Resonance Spectroscopy ; Models, Molecular ; Nucleic Acid Conformation ; Purines/chemistry ; Pyrimidines/chemistry ; RNA/chemistry ; Thermodynamics
    Chemical Substances DNA, B-Form ; Purines ; Pyrimidines ; RNA (63231-63-0) ; DNA (9007-49-2) ; pyrimidine (K8CXK5Q32L) ; purine (W60KTZ3IZY)
    Language English
    Publishing date 2018-10-03
    Publishing country England
    Document type Journal Article ; Research Support, N.I.H., Extramural
    ZDB-ID 186809-3
    ISSN 1362-4962 ; 1362-4954 ; 0301-5610 ; 0305-1048
    ISSN (online) 1362-4962 ; 1362-4954
    ISSN 0301-5610 ; 0305-1048
    DOI 10.1093/nar/gky885
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  8. Article ; Online: A flow cytometric method for estimating S-phase duration in plants.

    Mickelson-Young, Leigh / Wear, Emily / Mulvaney, Patrick / Lee, Tae-Jin / Szymanski, Eric S / Allen, George / Hanley-Bowdoin, Linda / Thompson, William

    Journal of experimental botany

    2016  Volume 67, Issue 21, Page(s) 6077–6087

    Abstract: The duration of the DNA synthesis stage (S phase) of the cell cycle is fundamental in our understanding of cell cycle kinetics, cell proliferation, and DNA replication timing programs. Most S-phase duration estimates that exist for plants are based on ... ...

    Abstract The duration of the DNA synthesis stage (S phase) of the cell cycle is fundamental in our understanding of cell cycle kinetics, cell proliferation, and DNA replication timing programs. Most S-phase duration estimates that exist for plants are based on indirect measurements. We present a method for directly estimating S-phase duration by pulse-labeling root tips or actively dividing suspension cells with the halogenated thymidine analog 5-ethynl-2'-deoxyuridine (EdU) and analyzing the time course of replication with bivariate flow cytometry. The transition between G
    MeSH term(s) Arabidopsis/cytology ; Arabidopsis/growth & development ; DNA, Plant/metabolism ; Deoxyuridine/analogs & derivatives ; Deoxyuridine/metabolism ; Flow Cytometry/methods ; G1 Phase/physiology ; G2 Phase/physiology ; Hordeum/cytology ; Hordeum/growth & development ; Meristem/cytology ; Meristem/growth & development ; Oryza/cytology ; Oryza/growth & development ; S Phase/physiology ; Triticum/cytology ; Triticum/growth & development ; Zea mays/cytology ; Zea mays/growth & development
    Chemical Substances DNA, Plant ; 5-ethynyl-2'-deoxyuridine (G373S00W2J) ; Deoxyuridine (W78I7AY22C)
    Language English
    Publishing date 2016-10-03
    Publishing country England
    Document type Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
    ZDB-ID 2976-2
    ISSN 1460-2431 ; 0022-0957
    ISSN (online) 1460-2431
    ISSN 0022-0957
    DOI 10.1093/jxb/erw367
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  9. Article ; Online: Dynamic basis for dG•dT misincorporation via tautomerization and ionization.

    Kimsey, Isaac J / Szymanski, Eric S / Zahurancik, Walter J / Shakya, Anisha / Xue, Yi / Chu, Chia-Chieh / Sathyamoorthy, Bharathwaj / Suo, Zucai / Al-Hashimi, Hashim M

    Nature

    2018  Volume 554, Issue 7691, Page(s) 195–201

    Abstract: Tautomeric and anionic Watson-Crick-like mismatches have important roles in replication and translation errors through mechanisms that are not fully understood. Here, using NMR relaxation dispersion, we resolve a sequence-dependent kinetic network ... ...

    Abstract Tautomeric and anionic Watson-Crick-like mismatches have important roles in replication and translation errors through mechanisms that are not fully understood. Here, using NMR relaxation dispersion, we resolve a sequence-dependent kinetic network connecting G•T/U wobbles with three distinct Watson-Crick mismatches: two rapidly exchanging tautomeric species (G
    MeSH term(s) Animals ; Anions ; Base Pair Mismatch/genetics ; DNA/biosynthesis ; DNA/chemistry ; DNA/genetics ; DNA Replication ; DNA-Directed DNA Polymerase/metabolism ; Guanine/chemistry ; Guanine/metabolism ; Humans ; Hydrogen-Ion Concentration ; Kinetics ; Magnetic Resonance Spectroscopy ; Mutagenesis ; Probability ; Rats ; Thymine/chemistry ; Thymine/metabolism
    Chemical Substances Anions ; Guanine (5Z93L87A1R) ; DNA (9007-49-2) ; DNA-Directed DNA Polymerase (EC 2.7.7.7) ; Thymine (QR26YLT7LT)
    Language English
    Publishing date 2018-01-31
    Publishing country England
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
    ZDB-ID 120714-3
    ISSN 1476-4687 ; 0028-0836
    ISSN (online) 1476-4687
    ISSN 0028-0836
    DOI 10.1038/nature25487
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  10. Article ; Online: Genomic Analysis of the DNA Replication Timing Program during Mitotic S Phase in Maize (

    Wear, Emily E / Song, Jawon / Zynda, Gregory J / LeBlanc, Chantal / Lee, Tae-Jin / Mickelson-Young, Leigh / Concia, Lorenzo / Mulvaney, Patrick / Szymanski, Eric S / Allen, George C / Martienssen, Robert A / Vaughn, Matthew W / Hanley-Bowdoin, Linda / Thompson, William F

    The Plant cell

    2017  Volume 29, Issue 9, Page(s) 2126–2149

    Abstract: All plants and animals must replicate their DNA, using a regulated process to ensure that their genomes are completely and accurately replicated. DNA replication timing programs have been extensively studied in yeast and animal systems, but much less is ... ...

    Abstract All plants and animals must replicate their DNA, using a regulated process to ensure that their genomes are completely and accurately replicated. DNA replication timing programs have been extensively studied in yeast and animal systems, but much less is known about the replication programs of plants. We report a novel adaptation of the "Repli-seq" assay for use in intact root tips of maize (
    MeSH term(s) Base Sequence ; Chromosomes, Plant/genetics ; DNA Replication Timing/genetics ; DNA Transposable Elements/genetics ; Genes, Plant ; Genomics ; Meristem/cytology ; Meristem/genetics ; Mitosis/genetics ; Models, Genetic ; S Phase/genetics ; Tandem Repeat Sequences/genetics ; Time Factors ; Transcription, Genetic ; Zea mays/cytology ; Zea mays/genetics
    Chemical Substances DNA Transposable Elements
    Language English
    Publishing date 2017-08-25
    Publishing country United States
    Document type Journal Article
    ZDB-ID 623171-8
    ISSN 1532-298X ; 1040-4651
    ISSN (online) 1532-298X
    ISSN 1040-4651
    DOI 10.1105/tpc.17.00037
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