Visualizing DNA polymerase ι catalyze Hoogsteen-directed DNA synthesis

Abstract Translesion synthesis polymerases efficiently incorporate nucleotides opposite DNA lesions. Pol ι, for example, bypasses minor-groove and exocyclic purine adducts. Conventional X-ray crystallography showed that this enzyme incorporates nucleotides by forming Hoogsteen base pairs with the in...

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Main Authors: Zach Frevert, Devin T. Reusch, Melissa S. Gildenberg, Sarah M. Jordan, Benjamin J. Ryan, Bret D. Freudenthal, M. Todd Washington
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-61245-8
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author Zach Frevert
Devin T. Reusch
Melissa S. Gildenberg
Sarah M. Jordan
Benjamin J. Ryan
Bret D. Freudenthal
M. Todd Washington
author_facet Zach Frevert
Devin T. Reusch
Melissa S. Gildenberg
Sarah M. Jordan
Benjamin J. Ryan
Bret D. Freudenthal
M. Todd Washington
author_sort Zach Frevert
collection DOAJ
description Abstract Translesion synthesis polymerases efficiently incorporate nucleotides opposite DNA lesions. Pol ι, for example, bypasses minor-groove and exocyclic purine adducts. Conventional X-ray crystallography showed that this enzyme incorporates nucleotides by forming Hoogsteen base pairs with the incoming nucleotide rather than Watson-Crick base pairs. While this revealed the structural basis of nucleotide selection during nucleotide binding, it did not allow the visualization of the process of phosphodiester bond formation or the detection of reaction intermediates that form during nucleotide incorporation. Here, we use a combination of time-lapse crystallography and molecular dynamics simulations to examine the mechanism of pol ι-catalyzed nucleotide incorporation. We show that this enzyme maintains Hoogsteen base pairing with the incoming dNTP during the entire reaction. We also show that pol ι possesses a pyrophosphatase activity that generates two monophosphates within its active site. Our findings provide insights into the features of pol ι’s active site that allow it to translocate along DNA and catalyze processive DNA synthesis.
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spelling doaj-art-734cfdc2dd0441aab5fcf723f08418362025-08-20T03:45:34ZengNature PortfolioNature Communications2041-17232025-07-0116111110.1038/s41467-025-61245-8Visualizing DNA polymerase ι catalyze Hoogsteen-directed DNA synthesisZach Frevert0Devin T. Reusch1Melissa S. Gildenberg2Sarah M. Jordan3Benjamin J. Ryan4Bret D. Freudenthal5M. Todd Washington6Department of Biochemistry and Molecular Biology, University of Iowa College of MedicineDepartment of Biochemistry and Molecular Biology, University of Iowa College of MedicineDepartment of Biochemistry and Molecular Biology, University of Iowa College of MedicineDepartment of Biochemistry and Molecular Biology, University of Iowa College of MedicineDepartment of Biochemistry and Molecular Biology, University of Kansas Medical CenterDepartment of Biochemistry and Molecular Biology, University of Kansas Medical CenterDepartment of Biochemistry and Molecular Biology, University of Iowa College of MedicineAbstract Translesion synthesis polymerases efficiently incorporate nucleotides opposite DNA lesions. Pol ι, for example, bypasses minor-groove and exocyclic purine adducts. Conventional X-ray crystallography showed that this enzyme incorporates nucleotides by forming Hoogsteen base pairs with the incoming nucleotide rather than Watson-Crick base pairs. While this revealed the structural basis of nucleotide selection during nucleotide binding, it did not allow the visualization of the process of phosphodiester bond formation or the detection of reaction intermediates that form during nucleotide incorporation. Here, we use a combination of time-lapse crystallography and molecular dynamics simulations to examine the mechanism of pol ι-catalyzed nucleotide incorporation. We show that this enzyme maintains Hoogsteen base pairing with the incoming dNTP during the entire reaction. We also show that pol ι possesses a pyrophosphatase activity that generates two monophosphates within its active site. Our findings provide insights into the features of pol ι’s active site that allow it to translocate along DNA and catalyze processive DNA synthesis.https://doi.org/10.1038/s41467-025-61245-8
spellingShingle Zach Frevert
Devin T. Reusch
Melissa S. Gildenberg
Sarah M. Jordan
Benjamin J. Ryan
Bret D. Freudenthal
M. Todd Washington
Visualizing DNA polymerase ι catalyze Hoogsteen-directed DNA synthesis
Nature Communications
title Visualizing DNA polymerase ι catalyze Hoogsteen-directed DNA synthesis
title_full Visualizing DNA polymerase ι catalyze Hoogsteen-directed DNA synthesis
title_fullStr Visualizing DNA polymerase ι catalyze Hoogsteen-directed DNA synthesis
title_full_unstemmed Visualizing DNA polymerase ι catalyze Hoogsteen-directed DNA synthesis
title_short Visualizing DNA polymerase ι catalyze Hoogsteen-directed DNA synthesis
title_sort visualizing dna polymerase ι catalyze hoogsteen directed dna synthesis
url https://doi.org/10.1038/s41467-025-61245-8
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