Uracil Accumulation and Mutagenesis Dominated by Cytosine Deamination in CpG Dinucleotides in Mice Lacking UNG and SMUG1
Abstract
Both a DNA lesion and an intermediate for antibody maturation, uracil is primarily processed by base excision repair (BER), either initiated by uracil-DNA glycosylase (UNG) or by single-strand selective monofunctional uracil DNA glycosylase (SMUG1). The relative in vivo contributions of each glycosylase remain elusive. To assess the impact of SMUG1 deficiency, we measured uracil and 5-hydroxymethyluracil, another SMUG1 substrate, in Smug1-/- mice. Here, we found that 5-hydroxymethyluracil accumulated in Smug1-/- tissues and correlated with 5-hydroxymethylcytosine levels. The highest increase was found in brain, which contained about 26-fold higher genomic 5-hydroxymethyluracil levels than the wild type. Smug1-/- mice did not accumulate uracil in their genome and Ung-/- mice showed slightly elevated uracil levels. Contrastingly, Ung-/-Smug1-/- mice showed a synergistic increase in uracil levels with up to 25-fold higher uracil levels than wild type. Whole genome sequencing of UNG/SMUG1-deficient tumours revealed that combined UNG and SMUG1 deficiency leads to the accumulation of mutations, primarily C to T transitions within CpG sequences. This unexpected sequence bias suggests that CpG dinucleotides are intrinsically more mutation prone. In conclusion, we showed that SMUG1 efficiently prevent genomic uracil accumulation, even in the presence of UNG, and identified mutational signatures associated with combined UNG and SMUG1 deficiency.
- Authors:
-
[6];
[4];
[8];
[1]
- Univ. of Oslo (Norway). Dept. of Clinical Molecular Biology; Akershus Univ. Hospital, Lorenskog (Norway)
- Norwegian Univ. of Science and Technology, Trondheim (Norway); Liaison Committee for Education, Research and Innovation in Central Norway, Trondheim (Norway)
- Univ. of Oslo (Norway). Dept. of Informatics
- Medical Research Council (MRC), Cambridge (United Kingdom). Lab. of Molecular Biology (MRC-LMB)
- Univ. of Oslo (Norway). Dept. of Clinical Molecular Biology; Akershus Univ. Hospital, Lorenskog (Norway); LifeTechnologies AS, Oslo (Norway)
- Los Alamos National Lab. (LANL), Los Alamos, NM (United States); Univ. of New Mexico Comprehensive Cancer Center, Albuquerque, NM (United States)
- Norwegian Univ. of Science and Technology, Trondheim (Norway
- Univ. of Oslo (Norway). Dept. of Informatics; Oslo University Hospital, Oslo (Norway). Dept. of Microbiology
- Norwegian Univ. of Science and Technology, Trondheim (Norway)
- Publication Date:
- Research Org.:
- Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
- Sponsoring Org.:
- USDOE National Nuclear Security Administration (NNSA); USDOE Laboratory Directed Research and Development (LDRD) Program; Norwegian Research Council; Norwegian Cancer Society; European Union (EU)
- OSTI Identifier:
- 1392805
- Report Number(s):
- LA-UR-16-28917
Journal ID: ISSN 2045-2322
- Grant/Contract Number:
- AC52-06NA25396; 4501723–2013; 2014001; 609020
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Scientific Reports
- Additional Journal Information:
- Journal Volume: 7; Journal Issue: 1; Journal ID: ISSN 2045-2322
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Biological Science; Base excision repair; DNA
Citation Formats
Alsøe, Lene, Sarno, Antonio, Carracedo, Sergio, Domanska, Diana, Dingler, Felix, Lirussi, Lisa, SenGupta, Tanima, Tekin, Nuriye Basdag, Jobert, Laure, Alexandrov, Ludmil B., Galashevskaya, Anastasia, Rada, Cristina, Sandve, Geir Kjetil, Rognes, Torbjørn, Krokan, Hans E., and Nilsen, Hilde. Uracil Accumulation and Mutagenesis Dominated by Cytosine Deamination in CpG Dinucleotides in Mice Lacking UNG and SMUG1. United States: N. p., 2017.
Web. doi:10.1038/s41598-017-07314-5.
Alsøe, Lene, Sarno, Antonio, Carracedo, Sergio, Domanska, Diana, Dingler, Felix, Lirussi, Lisa, SenGupta, Tanima, Tekin, Nuriye Basdag, Jobert, Laure, Alexandrov, Ludmil B., Galashevskaya, Anastasia, Rada, Cristina, Sandve, Geir Kjetil, Rognes, Torbjørn, Krokan, Hans E., & Nilsen, Hilde. Uracil Accumulation and Mutagenesis Dominated by Cytosine Deamination in CpG Dinucleotides in Mice Lacking UNG and SMUG1. United States. https://doi.org/10.1038/s41598-017-07314-5
Alsøe, Lene, Sarno, Antonio, Carracedo, Sergio, Domanska, Diana, Dingler, Felix, Lirussi, Lisa, SenGupta, Tanima, Tekin, Nuriye Basdag, Jobert, Laure, Alexandrov, Ludmil B., Galashevskaya, Anastasia, Rada, Cristina, Sandve, Geir Kjetil, Rognes, Torbjørn, Krokan, Hans E., and Nilsen, Hilde. Thu .
"Uracil Accumulation and Mutagenesis Dominated by Cytosine Deamination in CpG Dinucleotides in Mice Lacking UNG and SMUG1". United States. https://doi.org/10.1038/s41598-017-07314-5. https://www.osti.gov/servlets/purl/1392805.
@article{osti_1392805,
title = {Uracil Accumulation and Mutagenesis Dominated by Cytosine Deamination in CpG Dinucleotides in Mice Lacking UNG and SMUG1},
author = {Alsøe, Lene and Sarno, Antonio and Carracedo, Sergio and Domanska, Diana and Dingler, Felix and Lirussi, Lisa and SenGupta, Tanima and Tekin, Nuriye Basdag and Jobert, Laure and Alexandrov, Ludmil B. and Galashevskaya, Anastasia and Rada, Cristina and Sandve, Geir Kjetil and Rognes, Torbjørn and Krokan, Hans E. and Nilsen, Hilde},
abstractNote = {Both a DNA lesion and an intermediate for antibody maturation, uracil is primarily processed by base excision repair (BER), either initiated by uracil-DNA glycosylase (UNG) or by single-strand selective monofunctional uracil DNA glycosylase (SMUG1). The relative in vivo contributions of each glycosylase remain elusive. To assess the impact of SMUG1 deficiency, we measured uracil and 5-hydroxymethyluracil, another SMUG1 substrate, in Smug1-/- mice. Here, we found that 5-hydroxymethyluracil accumulated in Smug1-/- tissues and correlated with 5-hydroxymethylcytosine levels. The highest increase was found in brain, which contained about 26-fold higher genomic 5-hydroxymethyluracil levels than the wild type. Smug1-/- mice did not accumulate uracil in their genome and Ung-/- mice showed slightly elevated uracil levels. Contrastingly, Ung-/-Smug1-/- mice showed a synergistic increase in uracil levels with up to 25-fold higher uracil levels than wild type. Whole genome sequencing of UNG/SMUG1-deficient tumours revealed that combined UNG and SMUG1 deficiency leads to the accumulation of mutations, primarily C to T transitions within CpG sequences. This unexpected sequence bias suggests that CpG dinucleotides are intrinsically more mutation prone. In conclusion, we showed that SMUG1 efficiently prevent genomic uracil accumulation, even in the presence of UNG, and identified mutational signatures associated with combined UNG and SMUG1 deficiency.},
doi = {10.1038/s41598-017-07314-5},
journal = {Scientific Reports},
number = 1,
volume = 7,
place = {United States},
year = {Thu Aug 03 00:00:00 EDT 2017},
month = {Thu Aug 03 00:00:00 EDT 2017}
}
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Works referenced in this record:
hUNG2 Is the Major Repair Enzyme for Removal of Uracil from U:A Matches, U:G Mismatches, and U in Single-stranded DNA, with hSMUG1 as a Broad Specificity Backup
journal, August 2002
- Kavli, Bodil; Sundheim, Ottar; Akbari, Mansour
- Journal of Biological Chemistry, Vol. 277, Issue 42
Intra- and inter-allelic ordering of T cell receptor ? chain gene assembly
journal, March 2005
- Khor, Bernard; Sleckman, Barry?P.
- European Journal of Immunology, Vol. 35, Issue 3
Identification of high excision capacity for 5-hydroxymethyluracil mispaired with guanine in DNA of Escherichia coli MutM, Nei and Nth DNA glycosylases
journal, February 2003
- Hori, M.
- Nucleic Acids Research, Vol. 31, Issue 4
Initial sequencing and comparative analysis of the mouse genome
journal, January 2002
- Consortium, Mouse Genome Sequencing
- Nature, Vol. 420, Issue 6915, p. 520-562
Identification of high excision capacity for 5-hydroxymethyluracil mispaired with guanine in DNA of Escherichia coli MutM, Nei and Nth DNA glycosylases
journal, February 2003
- Hori, M.
- Nucleic Acids Research, Vol. 31, Issue 4
From FastQ Data to High‐Confidence Variant Calls: The Genome Analysis Toolkit Best Practices Pipeline
journal, October 2013
- Auwera, Geraldine A.; Carneiro, Mauricio O.; Hartl, Christopher
- Current Protocols in Bioinformatics, Vol. 43, Issue 1
Genome-wide CRISPR screen identifies PRC2 and KMT2D-COMPASS as regulators of distinct EMT trajectories that contribute differentially to metastasis
journal, April 2022
- Zhang, Yun; Donaher, Joana Liu; Das, Sunny
- Nature Cell Biology, Vol. 24, Issue 4
Signatures of mutational processes in human cancer
journal, August 2013
- Alexandrov, Ludmil B.; Nik-Zainal, Serena; Wedge, David C.
- Nature, Vol. 500, Issue 7463
Tet oxidizes thymine to 5-hydroxymethyluracil in mouse embryonic stem cell DNA
journal, May 2014
- Pfaffeneder, Toni; Spada, Fabio; Wagner, Mirko
- Nature Chemical Biology, Vol. 10, Issue 7
Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples
journal, February 2013
- Cibulskis, Kristian; Lawrence, Michael S.; Carter, Scott L.
- Nature Biotechnology, Vol. 31, Issue 3
Oxidation of Thymine to 5-Formyluracil in DNA Promotes Misincorporation of dGMP and Subsequent Elongation of a Mismatched Primer Terminus by DNA Polymerase
journal, January 2001
- Masaoka, Aya; Terato, Hiroaki; Kobayashi, Mutsumi
- Journal of Biological Chemistry, Vol. 276, Issue 19
Strikingly different properties of uracil-DNA glycosylases UNG2 and SMUG1 may explain divergent roles in processing of genomic uracil
journal, June 2012
- Doseth, Berit; Ekre, Cecilie; Slupphaug, Geir
- DNA Repair, Vol. 11, Issue 6
A Mammalian Cell Line Deficient in Activity of the DNA Repair Enzyme 5-Hydroxymethyluracil-DNA Glycosylase Is Resistant to the Toxic Effects of the Thymidine Analog 5 -Hydroxymethyl-2′-Deoxyuridine
journal, December 1992
- Boorstein, Robert J.; Chiu, Lai-No; Teebor, George W.
- Molecular and Cellular Biology, Vol. 12, Issue 12
Tissue-Specific Differences in DNA Modifications (5-Hydroxymethylcytosine, 5-Formylcytosine, 5-Carboxylcytosine and 5-Hydroxymethyluracil) and Their Interrelationships
journal, December 2015
- Gackowski, Daniel; Zarakowska, Ewelina; Starczak, Marta
- PLOS ONE, Vol. 10, Issue 12
DNA glycosylase activities for thymine residues oxidized in the methyl group are functions of the hNEIL1 and hNTH1 enzymes in human cells
journal, January 2005
- Zhang, Qiu-Mei; Yonekura, Shin-Ichiro; Takao, Masashi
- DNA Repair, Vol. 4, Issue 1
Extracts of proliferating and non-proliferating human cells display different base excision pathways and repair fidelity
journal, July 2009
- Akbari, Mansour; Peña-Diaz, Javier; Andersen, Sonja
- DNA Repair, Vol. 8, Issue 7
A mammalian cell line deficient in activity of the DNA repair enzyme 5-hydroxymethyluracil-DNA glycosylase is resistant to the toxic effects of the thymidine analog 5-hydroxymethyl-2'-deoxyuridine.
journal, December 1992
- Boorstein, R. J.; Chiu, L. N.; Teebor, G. W.
- Molecular and Cellular Biology, Vol. 12, Issue 12
C → T mutagenesis and γ-radiation sensitivity due to deficiency in the Smug1 and Ung DNA glycosylases
journal, May 2005
- An, Qian; Robins, Peter; Lindahl, Tomas
- The EMBO Journal, Vol. 24, Issue 12
Deciphering Signatures of Mutational Processes Operative in Human Cancer
journal, January 2013
- Alexandrov, Ludmil B.; Nik-Zainal, Serena; Wedge, David C.
- Cell Reports, Vol. 3, Issue 1
Genome-wide Profiling of 5-Formylcytosine Reveals Its Roles in Epigenetic Priming
journal, April 2013
- Song, Chun-Xiao; Szulwach, Keith E.; Dai, Qing
- Cell, Vol. 153, Issue 3
dbSNP: the NCBI database of genetic variation
journal, January 2001
- Sherry, S. T.
- Nucleic Acids Research, Vol. 29, Issue 1
Replication of DNA templates containing 5-formyluracil, a major oxidative lesion of thymine in DNA
journal, October 1997
- Zhang, Q.
- Nucleic Acids Research, Vol. 25, Issue 20
Mutational Processes Molding the Genomes of 21 Breast Cancers
journal, May 2012
- Nik-Zainal, Serena; Alexandrov, Ludmil B.; Wedge, David C.
- Cell, Vol. 149, Issue 5
DNA deaminases induce break-associated mutation showers with implication of APOBEC3B and 3A in breast cancer kataegis
journal, April 2013
- Taylor, Benjamin JM; Nik-Zainal, Serena; Wu, Yee Ling
- eLife, Vol. 2
Mammalian 5-Formyluracil−DNA Glycosylase. 2. Role of SMUG1 Uracil−DNA Glycosylase in Repair of 5-Formyluracil and Other Oxidized and Deaminated Base Lesions †
journal, May 2003
- Masaoka, Aya; Matsubara, Mayumi; Hasegawa, Rei
- Biochemistry, Vol. 42, Issue 17
Mammalian 5-Formyluracil−DNA Glycosylase. 2. Role of SMUG1 Uracil−DNA Glycosylase in Repair of 5-Formyluracil and Other Oxidized and Deaminated Base Lesions †
journal, May 2003
- Masaoka, Aya; Matsubara, Mayumi; Hasegawa, Rei
- Biochemistry, Vol. 42, Issue 17
Instability and decay of the primary structure of DNA
journal, April 1993
- Lindahl, Tomas
- Nature, Vol. 362, Issue 6422
5-Hydroxymethylcytosine Marks Sites of DNA Damage and Promotes Genome Stability
journal, February 2016
- Kafer, Georgia Rose; Li, Xuan; Horii, Takuro
- Cell Reports, Vol. 14, Issue 6
A robust, sensitive assay for genomic uracil determination by LC/MS/MS reveals lower levels than previously reported
journal, September 2013
- Galashevskaya, Anastasia; Sarno, Antonio; Vågbø, Cathrine B.
- DNA Repair, Vol. 12, Issue 9
Nuclear and mitochondrial splice forms of human uracil-DNA glycosylase contain a complex nuclear localisation signal and a strong classical mitochondrial localisation signal, respectively
journal, October 1998
- Otterlei, M.; Haug, T.; Nagelhus, T. A.
- Nucleic Acids Research, Vol. 26, Issue 20
Fast and accurate long-read alignment with Burrows–Wheeler transform
journal, January 2010
- Li, Heng; Durbin, Richard
- Bioinformatics, Vol. 26, Issue 5
Integrative genomics viewer
journal, January 2011
- Robinson, James T.; Thorvaldsdóttir, Helga; Winckler, Wendy
- Nature Biotechnology, Vol. 29, Issue 1
Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples
journal, February 2013
- Cibulskis, Kristian; Lawrence, Michael S.; Carter, Scott L.
- Nature Biotechnology, Vol. 31, Issue 3
Uracil–DNA glycosylases SMUG1 and UNG2 coordinate the initial steps of base excision repair by distinct mechanisms
journal, May 2007
- Pettersen, Henrik Sahlin; Sundheim, Ottar; Gilljam, Karin Margaretha
- Nucleic Acids Research, Vol. 35, Issue 12
Germline ablation of SMUG1 DNA glycosylase causes loss of 5-hydroxymethyluracil- and UNG-backup uracil-excision activities and increases cancer predisposition of Ung−/−Msh2−/− mice
journal, March 2012
- Kemmerich, Kristin; Dingler, Felix A.; Rada, Cristina
- Nucleic Acids Research, Vol. 40, Issue 13
Active DNA demethylation by DNA repair: Facts and uncertainties
journal, August 2016
- Schuermann, David; Weber, Alain R.; Schär, Primo
- DNA Repair, Vol. 44
Tissue-Specific Differences in DNA Modifications (5-Hydroxymethylcytosine, 5-Formylcytosine, 5-Carboxylcytosine and 5-Hydroxymethyluracil) and Their Interrelationships
journal, December 2015
- Gackowski, Daniel; Zarakowska, Ewelina; Starczak, Marta
- PLOS ONE, Vol. 10, Issue 12
Nuclear and mitochondrial uracil-DNA glycosylases are generated by alternative splicing and transcription from different positions in the UNG gene
journal, February 1997
- Nilsen, H.; Otterlei, M.; Haug, T.
- Nucleic Acids Research, Vol. 25, Issue 4
Cell cycle-specific UNG2 phosphorylations regulate protein turnover, activity and association with RPA
journal, December 2007
- Hagen, Lars; Kavli, Bodil; Sousa, Mirta M. L.
- The EMBO Journal, Vol. 27, Issue 1
Excision of deaminated cytosine from the vertebrate genome: role of the SMUG1 uracil-DNA glycosylase
journal, August 2001
- Nilsen, H.
- The EMBO Journal, Vol. 20, Issue 15
A framework for variation discovery and genotyping using next-generation DNA sequencing data
journal, April 2011
- DePristo, Mark A.; Banks, Eric; Poplin, Ryan
- Nature Genetics, Vol. 43, Issue 5
A framework for variation discovery and genotyping using next-generation DNA sequencing data
journal, April 2011
- DePristo, Mark A.; Banks, Eric; Poplin, Ryan
- Nature Genetics, Vol. 43, Issue 5
The Human Base Excision Repair Enzyme SMUG1 Directly Interacts with DKC1 and Contributes to RNA Quality Control
journal, January 2013
- Jobert, Laure; Skjeldam, Hanne K.; Dalhus, Bjørn
- Molecular Cell, Vol. 49, Issue 2
Methotrexate-induced misincorporation of uracil into DNA
journal, April 1980
- Goulian, M.; Bleile, B.; Tseng, B. Y.
- Proceedings of the National Academy of Sciences, Vol. 77, Issue 4
Excision of deaminated cytosine from the vertebrate genome: role of the SMUG1 uracil-DNA glycosylase
journal, August 2001
- Nilsen, H.
- The EMBO Journal, Vol. 20, Issue 15
Family-Wide Comparative Analysis of Cytidine and Methylcytidine Deamination by Eleven Human APOBEC Proteins
journal, June 2017
- Ito, Fumiaki; Fu, Yang; Kao, Shen-Chi A.
- Journal of Molecular Biology, Vol. 429, Issue 12
Deamination, Oxidation, and C–C Bond Cleavage Reactivity of 5-Hydroxymethylcytosine, 5-Formylcytosine, and 5-Carboxycytosine
journal, September 2013
- Schiesser, Stefan; Pfaffeneder, Toni; Sadeghian, Keyarash
- Journal of the American Chemical Society, Vol. 135, Issue 39
The Human Genome Browser at UCSC
journal, May 2002
- Kent, W. J.; Sugnet, C. W.; Furey, T. S.
- Genome Research, Vol. 12, Issue 6
The Genomic HyperBrowser: an analysis web server for genome-scale data
journal, April 2013
- Sandve, Geir K.; Gundersen, Sveinung; Johansen, Morten
- Nucleic Acids Research, Vol. 41, Issue W1
VSEARCH: a versatile open source tool for metagenomics
journal, January 2016
- Rognes, Torbjørn; Flouri, Tomáš; Nichols, Ben
- PeerJ, Vol. 4
Nuclear and mitochondrial splice forms of human uracil-DNA glycosylase contain a complex nuclear localisation signal and a strong classical mitochondrial localisation signal, respectively
journal, October 1998
- Otterlei, M.; Haug, T.; Nagelhus, T. A.
- Nucleic Acids Research, Vol. 26, Issue 20
A robust, sensitive assay for genomic uracil determination by LC/MS/MS reveals lower levels than previously reported
journal, September 2013
- Galashevskaya, Anastasia; Sarno, Antonio; Vågbø, Cathrine B.
- DNA Repair, Vol. 12, Issue 9
Uracil excision by endogenous SMUG 1 glycosylase promotes efficient I g class switching and impacts on A : T substitutions during somatic mutation
journal, May 2014
- Dingler, Felix A.; Kemmerich, Kristin; Neuberger, Michael S.
- European Journal of Immunology, Vol. 44, Issue 7
Deamination, Oxidation, and C–C Bond Cleavage Reactivity of 5-Hydroxymethylcytosine, 5-Formylcytosine, and 5-Carboxycytosine
journal, September 2013
- Schiesser, Stefan; Pfaffeneder, Toni; Sadeghian, Keyarash
- Journal of the American Chemical Society, Vol. 135, Issue 39
The Human Genome Browser at UCSC
journal, May 2002
- Kent, W. J.; Sugnet, C. W.; Furey, T. S.
- Genome Research, Vol. 12, Issue 6
The enigmatic thymine DNA glycosylase
journal, April 2007
- Cortazar, D.; Kunz, C.; Saito, Y.
- DNA Repair, Vol. 6, Issue 4
Mbd4 inactivation increases C->T transition mutations and promotes gastrointestinal tumor formation
journal, November 2002
- Wong, E.; Yang, K.; Kuraguchi, M.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 23
Cell cycle-specific UNG2 phosphorylations regulate protein turnover, activity and association with RPA
journal, December 2007
- Hagen, Lars; Kavli, Bodil; Sousa, Mirta M. L.
- The EMBO Journal, Vol. 27, Issue 1
dbSNP: the NCBI database of genetic variation
journal, January 2001
- Sherry, S. T.
- Nucleic Acids Research, Vol. 29, Issue 1
Enigmatic 5-hydroxymethyluracil: Oxidatively modified base, epigenetic mark or both?
journal, January 2016
- Olinski, Ryszard; Starczak, Marta; Gackowski, Daniel
- Mutation Research/Reviews in Mutation Research, Vol. 767
Patterns of somatic mutation in human cancer genomes
journal, March 2007
- Greenman, Christopher; Stephens, Philip; Smith, Raffaella
- Nature, Vol. 446, Issue 7132
Base Excision by Thymine DNA Glycosylase Mediates DNA-Directed Cytotoxicity of 5-Fluorouracil
journal, April 2009
- Kunz, Christophe; Focke, Frauke; Saito, Yusuke
- PLoS Biology, Vol. 7, Issue 4
biobambam: tools for read pair collation based algorithms on BAM files
journal, June 2014
- Tischler, German; Leonard, Steven
- Source Code for Biology and Medicine, Vol. 9, Issue 1
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
journal, July 2010
- McKenna, A.; Hanna, M.; Banks, E.
- Genome Research, Vol. 20, Issue 9
Uracil-DNA Glycosylase in Base Excision Repair and Adaptive Immunity: SPECIES DIFFERENCES BETWEEN MAN AND MOUSE
journal, March 2011
- Doseth, Berit; Visnes, Torkild; Wallenius, Anders
- Journal of Biological Chemistry, Vol. 286, Issue 19
Active DNA demethylation by DNA repair: Facts and uncertainties
journal, August 2016
- Schuermann, David; Weber, Alain R.; Schär, Primo
- DNA Repair, Vol. 44
Nuclear and mitochondrial uracil-DNA glycosylases are generated by alternative splicing and transcription from different positions in the UNG gene
journal, February 1997
- Nilsen, H.; Otterlei, M.; Haug, T.
- Nucleic Acids Research, Vol. 25, Issue 4
Uracil-DNA Glycosylase (UNG)-Deficient Mice Reveal a Primary Role of the Enzyme during DNA Replication
journal, June 2000
- Nilsen, Hilde; Rosewell, Ian; Robins, Peter
- Molecular Cell, Vol. 5, Issue 6
Mbd4 inactivation increases C->T transition mutations and promotes gastrointestinal tumor formation
journal, November 2002
- Wong, E.; Yang, K.; Kuraguchi, M.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 23
Deciphering Signatures of Mutational Processes Operative in Human Cancer
journal, January 2013
- Alexandrov, Ludmil B.; Nik-Zainal, Serena; Wedge, David C.
- Cell Reports, Vol. 3, Issue 1
Germline ablation of SMUG1 DNA glycosylase causes loss of 5-hydroxymethyluracil- and UNG-backup uracil-excision activities and increases cancer predisposition of Ung−/−Msh2−/− mice
journal, March 2012
- Kemmerich, Kristin; Dingler, Felix A.; Rada, Cristina
- Nucleic Acids Research, Vol. 40, Issue 13
Identification of a new uracil-DNA glycosylase family by expression cloning using synthetic inhibitors
journal, February 1999
- Haushalter, Karl A.; Todd Stukenberg, P.; Kirschner, Marc W.
- Current Biology, Vol. 9, Issue 4
The Genomic HyperBrowser: an analysis web server for genome-scale data
journal, April 2013
- Sandve, Geir K.; Gundersen, Sveinung; Johansen, Morten
- Nucleic Acids Research, Vol. 41, Issue W1
Characterization of DNA glycosylase activity by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry
journal, November 2009
- Darwanto, Agus; Farrel, Alvin; Rogstad, Daniel K.
- Analytical Biochemistry, Vol. 394, Issue 1
C → T mutagenesis and γ-radiation sensitivity due to deficiency in the Smug1 and Ung DNA glycosylases
journal, May 2005
- An, Qian; Robins, Peter; Lindahl, Tomas
- The EMBO Journal, Vol. 24, Issue 12
The Sequence Alignment/Map format and SAMtools
journal, June 2009
- Li, H.; Handsaker, B.; Wysoker, A.
- Bioinformatics, Vol. 25, Issue 16
Definitive Identification of Mammalian 5-Hydroxymethyluracil DNA N -Glycosylase Activity as SMUG1
journal, August 2001
- Boorstein, Robert J.; Cummings, Archie; Marenstein, Dina R.
- Journal of Biological Chemistry, Vol. 276, Issue 45
Instability and decay of the primary structure of DNA
journal, April 1993
- Lindahl, Tomas
- Nature, Vol. 362, Issue 6422
DNA glycosylase activities for thymine residues oxidized in the methyl group are functions of the hNEIL1 and hNTH1 enzymes in human cells
journal, January 2005
- Zhang, Qiu-Mei; Yonekura, Shin-Ichiro; Takao, Masashi
- DNA Repair, Vol. 4, Issue 1
The enigmatic thymine DNA glycosylase
journal, April 2007
- Cortazar, D.; Kunz, C.; Saito, Y.
- DNA Repair, Vol. 6, Issue 4
Strikingly different properties of uracil-DNA glycosylases UNG2 and SMUG1 may explain divergent roles in processing of genomic uracil
journal, June 2012
- Doseth, Berit; Ekre, Cecilie; Slupphaug, Geir
- DNA Repair, Vol. 11, Issue 6
Replication of DNA templates containing 5-formyluracil, a major oxidative lesion of thymine in DNA
journal, October 1997
- Zhang, Q.
- Nucleic Acids Research, Vol. 25, Issue 20
Mutational Processes Molding the Genomes of 21 Breast Cancers
journal, May 2012
- Nik-Zainal, Serena; Alexandrov, Ludmil B.; Wedge, David C.
- Cell, Vol. 149, Issue 5
The effect of methotrexate on levels of dUTP in animal cells.
journal, November 1980
- Goulian, M.; Bleile, B.; Tseng, B. Y.
- Journal of Biological Chemistry, Vol. 255, Issue 22
DNA N-glycosidases: properties of uracil-DNA glycosidase from Escherichia coli.
journal, May 1977
- Lindahl, T.; Ljungquist, S.; Siegert, W.
- Journal of Biological Chemistry, Vol. 252, Issue 10
Works referencing / citing this record:
Uracil–DNA glycosylase UNG1 isoform variant supports class switch recombination and repairs nuclear genomic uracil
journal, March 2019
- Sarno, Antonio; Lundbæk, Marie; Liabakk, Nina Beate
- Nucleic Acids Research, Vol. 47, Issue 9
A Tumor-Promoting Phorbol Ester Causes a Large Increase in APOBEC3A Expression and a Moderate Increase in APOBEC3B Expression in a Normal Human Keratinocyte Cell Line without Increasing Genomic Uracils
journal, October 2018
- Siriwardena, Sachini U.; Perera, Madusha L. W.; Senevirathne, Vimukthi
- Molecular and Cellular Biology, Vol. 39, Issue 1
Portrait of a cancer: mutational signature analyses for cancer diagnostics
journal, May 2019
- Van Hoeck, Arne; Tjoonk, Niels H.; van Boxtel, Ruben
- BMC Cancer, Vol. 19, Issue 1
Telomere maintenance: regulating hTERC fate through RNA modifications
journal, October 2019
- Lirussi, Lisa; Nilsen, Hilde
- Molecular & Cellular Oncology, Vol. 6, Issue 6
Integrative genomic analysis identifies associations of molecular alterations to APOBEC and BRCA1/2 mutational signatures in breast cancer
journal, June 2019
- Trevino, Victor
- Molecular Genetics & Genomic Medicine, Vol. 7, Issue 8
Portrait of a cancer: mutational signature analyses for cancer diagnostics
journal, May 2019
- Van Hoeck, Arne; Tjoonk, Niels H.; van Boxtel, Ruben
- BMC Cancer, Vol. 19, Issue 1
Telomere maintenance: regulating hTERC fate through RNA modifications
journal, October 2019
- Lirussi, Lisa; Nilsen, Hilde
- Molecular & Cellular Oncology, Vol. 6, Issue 6