Uracil Accumulation and Mutagenesis Dominated by Cytosine Deamination in CpG Dinucleotides in Mice Lacking UNG and SMUG1

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

doi:10.1038/s41598-017-07314-5

Title: Uracil Accumulation and Mutagenesis Dominated by Cytosine Deamination in CpG Dinucleotides in Mice Lacking UNG and SMUG1

Journal Article · Thu Aug 03 00:00:00 EDT 2017 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-017-07314-5· OSTI ID:1392805

Alsøe, Lene ^[1]; Sarno, Antonio ^[2]; Carracedo, Sergio ^[1]; Domanska, Diana ^[3]; Dingler, Felix ^[4]; Lirussi, Lisa ^[1]; SenGupta, Tanima ^[1]; Tekin, Nuriye Basdag ^[1]; Jobert, Laure ^[5];

^[6]; Galashevskaya, Anastasia ^[7];

^[4]; Sandve, Geir Kjetil ^[3];

^[8]; Krokan, Hans E. ^[9];

^[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)

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); USDOE Laboratory Directed Research and Development (LDRD) Program; Norwegian Research Council; Norwegian Cancer Society; European Union (EU)

Grant/Contract Number:: AC52-06NA25396; 4501723–2013; 2014001; 609020

OSTI ID:: 1392805

Report Number(s):: LA-UR-16-28917

Journal Information:: Scientific Reports, Vol. 7, Issue 1; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 32 works

Citation information provided by
Web of Science

References (60)

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 Kavli, Bodil; Sundheim, Ottar; Akbari, Mansour Journal of Biological Chemistry, Vol. 277, Issue 42 https://doi.org/10.1074/jbc.M207107200	journal	August 2002
Intra- and inter-allelic ordering of T cell receptor ? chain gene assembly Khor, Bernard; Sleckman, Barry?P. European Journal of Immunology, Vol. 35, Issue 3 https://doi.org/10.1002/eji.200425806	journal	March 2005
Identification of high excision capacity for 5-hydroxymethyluracil mispaired with guanine in DNA of Escherichia coli MutM, Nei and Nth DNA glycosylases Hori, M. Nucleic Acids Research, Vol. 31, Issue 4 https://doi.org/10.1093/nar/gkg223	journal	February 2003
Initial sequencing and comparative analysis of the mouse genome Consortium, Mouse Genome Sequencing Nature, Vol. 420, Issue 6915, p. 520-562 https://doi.org/10.1038/nature01262	journal	January 2002
From FastQ Data to High‐Confidence Variant Calls: The Genome Analysis Toolkit Best Practices Pipeline Auwera, Geraldine A.; Carneiro, Mauricio O.; Hartl, Christopher Current Protocols in Bioinformatics, Vol. 43, Issue 1 https://doi.org/10.1002/0471250953.bi1110s43	journal	October 2013
Genome-wide CRISPR screen identifies PRC2 and KMT2D-COMPASS as regulators of distinct EMT trajectories that contribute differentially to metastasis Zhang, Yun; Donaher, Joana Liu; Das, Sunny Nature Cell Biology, Vol. 24, Issue 4 https://doi.org/10.1038/s41556-022-00877-0	journal	April 2022
Signatures of mutational processes in human cancer Alexandrov, Ludmil B.; Nik-Zainal, Serena; Wedge, David C. Nature, Vol. 500, Issue 7463 https://doi.org/10.1038/nature12477	journal	August 2013
Tet oxidizes thymine to 5-hydroxymethyluracil in mouse embryonic stem cell DNA Pfaffeneder, Toni; Spada, Fabio; Wagner, Mirko Nature Chemical Biology, Vol. 10, Issue 7 https://doi.org/10.1038/nchembio.1532	journal	May 2014
Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples Cibulskis, Kristian; Lawrence, Michael S.; Carter, Scott L. Nature Biotechnology, Vol. 31, Issue 3 https://doi.org/10.1038/nbt.2514	journal	February 2013
Oxidation of Thymine to 5-Formyluracil in DNA Promotes Misincorporation of dGMP and Subsequent Elongation of a Mismatched Primer Terminus by DNA Polymerase Masaoka, Aya; Terato, Hiroaki; Kobayashi, Mutsumi Journal of Biological Chemistry, Vol. 276, Issue 19 https://doi.org/10.1074/jbc.M008598200	journal	January 2001
Strikingly different properties of uracil-DNA glycosylases UNG2 and SMUG1 may explain divergent roles in processing of genomic uracil Doseth, Berit; Ekre, Cecilie; Slupphaug, Geir DNA Repair, Vol. 11, Issue 6 https://doi.org/10.1016/j.dnarep.2012.03.003	journal	June 2012
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 Boorstein, Robert J.; Chiu, Lai-No; Teebor, George W. Molecular and Cellular Biology, Vol. 12, Issue 12 https://doi.org/10.1128/mcb.12.12.5536-5540.1992	journal	December 1992
Tissue-Specific Differences in DNA Modifications (5-Hydroxymethylcytosine, 5-Formylcytosine, 5-Carboxylcytosine and 5-Hydroxymethyluracil) and Their Interrelationships Gackowski, Daniel; Zarakowska, Ewelina; Starczak, Marta PLOS ONE, Vol. 10, Issue 12 https://doi.org/10.1371/journal.pone.0144859	journal	December 2015
DNA glycosylase activities for thymine residues oxidized in the methyl group are functions of the hNEIL1 and hNTH1 enzymes in human cells Zhang, Qiu-Mei; Yonekura, Shin-Ichiro; Takao, Masashi DNA Repair, Vol. 4, Issue 1 https://doi.org/10.1016/j.dnarep.2004.08.002	journal	January 2005
Extracts of proliferating and non-proliferating human cells display different base excision pathways and repair fidelity Akbari, Mansour; Peña-Diaz, Javier; Andersen, Sonja DNA Repair, Vol. 8, Issue 7 https://doi.org/10.1016/j.dnarep.2009.04.002	journal	July 2009
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. Boorstein, R. J.; Chiu, L. N.; Teebor, G. W. Molecular and Cellular Biology, Vol. 12, Issue 12 https://doi.org/10.1128/MCB.12.12.5536	journal	December 1992
C → T mutagenesis and γ-radiation sensitivity due to deficiency in the Smug1 and Ung DNA glycosylases An, Qian; Robins, Peter; Lindahl, Tomas The EMBO Journal, Vol. 24, Issue 12 https://doi.org/10.1038/sj.emboj.7600689	journal	May 2005
Deciphering Signatures of Mutational Processes Operative in Human Cancer Alexandrov, Ludmil B.; Nik-Zainal, Serena; Wedge, David C. Cell Reports, Vol. 3, Issue 1 https://doi.org/10.1016/j.celrep.2012.12.008	journal	January 2013
Genome-wide Profiling of 5-Formylcytosine Reveals Its Roles in Epigenetic Priming Song, Chun-Xiao; Szulwach, Keith E.; Dai, Qing Cell, Vol. 153, Issue 3 https://doi.org/10.1016/j.cell.2013.04.001	journal	April 2013
dbSNP: the NCBI database of genetic variation Sherry, S. T. Nucleic Acids Research, Vol. 29, Issue 1 https://doi.org/10.1093/nar/29.1.308	journal	January 2001
Replication of DNA templates containing 5-formyluracil, a major oxidative lesion of thymine in DNA Zhang, Q. Nucleic Acids Research, Vol. 25, Issue 20 https://doi.org/10.1093/nar/25.20.3969	journal	October 1997
Mutational Processes Molding the Genomes of 21 Breast Cancers Nik-Zainal, Serena; Alexandrov, Ludmil B.; Wedge, David C. Cell, Vol. 149, Issue 5 https://doi.org/10.1016/j.cell.2012.04.024	journal	May 2012
DNA deaminases induce break-associated mutation showers with implication of APOBEC3B and 3A in breast cancer kataegis Taylor, Benjamin JM; Nik-Zainal, Serena; Wu, Yee Ling eLife, Vol. 2 https://doi.org/10.7554/elife.00534	journal	April 2013
Mammalian 5-Formyluracil−DNA Glycosylase. 2. Role of SMUG1 Uracil−DNA Glycosylase in Repair of 5-Formyluracil and Other Oxidized and Deaminated Base Lesions ^† Masaoka, Aya; Matsubara, Mayumi; Hasegawa, Rei Biochemistry, Vol. 42, Issue 17 https://doi.org/10.1021/bi0273213	journal	May 2003
Instability and decay of the primary structure of DNA Lindahl, Tomas Nature, Vol. 362, Issue 6422 https://doi.org/10.1038/362709a0	journal	April 1993
5-Hydroxymethylcytosine Marks Sites of DNA Damage and Promotes Genome Stability Kafer, Georgia Rose; Li, Xuan; Horii, Takuro Cell Reports, Vol. 14, Issue 6 https://doi.org/10.1016/j.celrep.2016.01.035	journal	February 2016
A robust, sensitive assay for genomic uracil determination by LC/MS/MS reveals lower levels than previously reported Galashevskaya, Anastasia; Sarno, Antonio; Vågbø, Cathrine B. DNA Repair, Vol. 12, Issue 9 https://doi.org/10.1016/j.dnarep.2013.05.002	journal	September 2013
Nuclear and mitochondrial splice forms of human uracil-DNA glycosylase contain a complex nuclear localisation signal and a strong classical mitochondrial localisation signal, respectively Otterlei, M.; Haug, T.; Nagelhus, T. A. Nucleic Acids Research, Vol. 26, Issue 20 https://doi.org/10.1093/nar/26.20.4611	journal	October 1998
Fast and accurate long-read alignment with Burrows–Wheeler transform Li, Heng; Durbin, Richard Bioinformatics, Vol. 26, Issue 5 https://doi.org/10.1093/bioinformatics/btp698	journal	January 2010
Integrative genomics viewer Robinson, James T.; Thorvaldsdóttir, Helga; Winckler, Wendy Nature Biotechnology, Vol. 29, Issue 1 https://doi.org/10.1038/nbt.1754	journal	January 2011
Uracil–DNA glycosylases SMUG1 and UNG2 coordinate the initial steps of base excision repair by distinct mechanisms Pettersen, Henrik Sahlin; Sundheim, Ottar; Gilljam, Karin Margaretha Nucleic Acids Research, Vol. 35, Issue 12 https://doi.org/10.1093/nar/gkm372	journal	May 2007
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 Kemmerich, Kristin; Dingler, Felix A.; Rada, Cristina Nucleic Acids Research, Vol. 40, Issue 13 https://doi.org/10.1093/nar/gks259	journal	March 2012
Active DNA demethylation by DNA repair: Facts and uncertainties Schuermann, David; Weber, Alain R.; Schär, Primo DNA Repair, Vol. 44 https://doi.org/10.1016/j.dnarep.2016.05.013	journal	August 2016
Nuclear and mitochondrial uracil-DNA glycosylases are generated by alternative splicing and transcription from different positions in the UNG gene Nilsen, H.; Otterlei, M.; Haug, T. Nucleic Acids Research, Vol. 25, Issue 4 https://doi.org/10.1093/nar/25.4.750	journal	February 1997
Cell cycle-specific UNG2 phosphorylations regulate protein turnover, activity and association with RPA Hagen, Lars; Kavli, Bodil; Sousa, Mirta M. L. The EMBO Journal, Vol. 27, Issue 1 https://doi.org/10.1038/sj.emboj.7601958	journal	December 2007
Excision of deaminated cytosine from the vertebrate genome: role of the SMUG1 uracil-DNA glycosylase Nilsen, H. The EMBO Journal, Vol. 20, Issue 15 https://doi.org/10.1093/emboj/20.15.4278	journal	August 2001
A framework for variation discovery and genotyping using next-generation DNA sequencing data DePristo, Mark A.; Banks, Eric; Poplin, Ryan Nature Genetics, Vol. 43, Issue 5 https://doi.org/10.1038/ng.806	journal	April 2011
The Human Base Excision Repair Enzyme SMUG1 Directly Interacts with DKC1 and Contributes to RNA Quality Control Jobert, Laure; Skjeldam, Hanne K.; Dalhus, Bjørn Molecular Cell, Vol. 49, Issue 2 https://doi.org/10.1016/j.molcel.2012.11.010	journal	January 2013
Methotrexate-induced misincorporation of uracil into DNA Goulian, M.; Bleile, B.; Tseng, B. Y. Proceedings of the National Academy of Sciences, Vol. 77, Issue 4 https://doi.org/10.1073/pnas.77.4.1956	journal	April 1980
Family-Wide Comparative Analysis of Cytidine and Methylcytidine Deamination by Eleven Human APOBEC Proteins Ito, Fumiaki; Fu, Yang; Kao, Shen-Chi A. Journal of Molecular Biology, Vol. 429, Issue 12 https://doi.org/10.1016/j.jmb.2017.04.021	journal	June 2017
Deamination, Oxidation, and C–C Bond Cleavage Reactivity of 5-Hydroxymethylcytosine, 5-Formylcytosine, and 5-Carboxycytosine Schiesser, Stefan; Pfaffeneder, Toni; Sadeghian, Keyarash Journal of the American Chemical Society, Vol. 135, Issue 39 https://doi.org/10.1021/ja403229y	journal	September 2013
The Human Genome Browser at UCSC Kent, W. J.; Sugnet, C. W.; Furey, T. S. Genome Research, Vol. 12, Issue 6 https://doi.org/10.1101/gr.229102	journal	May 2002
The Genomic HyperBrowser: an analysis web server for genome-scale data Sandve, Geir K.; Gundersen, Sveinung; Johansen, Morten Nucleic Acids Research, Vol. 41, Issue W1 https://doi.org/10.1093/nar/gkt342	journal	April 2013
VSEARCH: a versatile open source tool for metagenomics Rognes, Torbjørn; Flouri, Tomáš; Nichols, Ben PeerJ, Vol. 4 https://doi.org/10.7717/peerj.2584	journal	January 2016
Uracil excision by endogenous SMUG 1 glycosylase promotes efficient I g class switching and impacts on A : T substitutions during somatic mutation Dingler, Felix A.; Kemmerich, Kristin; Neuberger, Michael S. European Journal of Immunology, Vol. 44, Issue 7 https://doi.org/10.1002/eji.201444482	journal	May 2014
The enigmatic thymine DNA glycosylase Cortazar, D.; Kunz, C.; Saito, Y. DNA Repair, Vol. 6, Issue 4 https://doi.org/10.1016/j.dnarep.2006.10.013	journal	April 2007
Mbd4 inactivation increases C->T transition mutations and promotes gastrointestinal tumor formation Wong, E.; Yang, K.; Kuraguchi, M. Proceedings of the National Academy of Sciences, Vol. 99, Issue 23 https://doi.org/10.1073/pnas.232579299	journal	November 2002
Enigmatic 5-hydroxymethyluracil: Oxidatively modified base, epigenetic mark or both? Olinski, Ryszard; Starczak, Marta; Gackowski, Daniel Mutation Research/Reviews in Mutation Research, Vol. 767 https://doi.org/10.1016/j.mrrev.2016.02.001	journal	January 2016
Patterns of somatic mutation in human cancer genomes Greenman, Christopher; Stephens, Philip; Smith, Raffaella Nature, Vol. 446, Issue 7132 https://doi.org/10.1038/nature05610	journal	March 2007
Base Excision by Thymine DNA Glycosylase Mediates DNA-Directed Cytotoxicity of 5-Fluorouracil Kunz, Christophe; Focke, Frauke; Saito, Yusuke PLoS Biology, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pbio.1000091	journal	April 2009
biobambam: tools for read pair collation based algorithms on BAM files Tischler, German; Leonard, Steven Source Code for Biology and Medicine, Vol. 9, Issue 1 https://doi.org/10.1186/1751-0473-9-13	journal	June 2014
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data McKenna, A.; Hanna, M.; Banks, E. Genome Research, Vol. 20, Issue 9 https://doi.org/10.1101/gr.107524.110	journal	July 2010
Uracil-DNA Glycosylase in Base Excision Repair and Adaptive Immunity: SPECIES DIFFERENCES BETWEEN MAN AND MOUSE Doseth, Berit; Visnes, Torkild; Wallenius, Anders Journal of Biological Chemistry, Vol. 286, Issue 19 https://doi.org/10.1074/jbc.M111.230052	journal	March 2011
Uracil-DNA Glycosylase (UNG)-Deficient Mice Reveal a Primary Role of the Enzyme during DNA Replication Nilsen, Hilde; Rosewell, Ian; Robins, Peter Molecular Cell, Vol. 5, Issue 6 https://doi.org/10.1016/s1097-2765(00)80271-3	journal	June 2000
Identification of a new uracil-DNA glycosylase family by expression cloning using synthetic inhibitors Haushalter, Karl A.; Todd Stukenberg, P.; Kirschner, Marc W. Current Biology, Vol. 9, Issue 4 https://doi.org/10.1016/S0960-9822(99)80087-6	journal	February 1999
Characterization of DNA glycosylase activity by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry Darwanto, Agus; Farrel, Alvin; Rogstad, Daniel K. Analytical Biochemistry, Vol. 394, Issue 1 https://doi.org/10.1016/j.ab.2009.07.015	journal	November 2009
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
Definitive Identification of Mammalian 5-Hydroxymethyluracil DNA N -Glycosylase Activity as SMUG1 Boorstein, Robert J.; Cummings, Archie; Marenstein, Dina R. Journal of Biological Chemistry, Vol. 276, Issue 45 https://doi.org/10.1074/jbc.m106953200	journal	August 2001
The effect of methotrexate on levels of dUTP in animal cells. Goulian, M.; Bleile, B.; Tseng, B. Y. Journal of Biological Chemistry, Vol. 255, Issue 22 https://doi.org/10.1016/S0021-9258(19)70353-6	journal	November 1980
DNA N-glycosidases: properties of uracil-DNA glycosidase from Escherichia coli. Lindahl, T.; Ljungquist, S.; Siegert, W. Journal of Biological Chemistry, Vol. 252, Issue 10 https://doi.org/10.1016/S0021-9258(17)40386-3	journal	May 1977

Cited By (5)

Uracil–DNA glycosylase UNG1 isoform variant supports class switch recombination and repairs nuclear genomic uracil Sarno, Antonio; Lundbæk, Marie; Liabakk, Nina Beate Nucleic Acids Research, Vol. 47, Issue 9 https://doi.org/10.1093/nar/gkz145	journal	March 2019
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 Siriwardena, Sachini U.; Perera, Madusha L. W.; Senevirathne, Vimukthi Molecular and Cellular Biology, Vol. 39, Issue 1 https://doi.org/10.1128/mcb.00238-18	journal	October 2018
Portrait of a cancer: mutational signature analyses for cancer diagnostics Van Hoeck, Arne; Tjoonk, Niels H.; van Boxtel, Ruben BMC Cancer, Vol. 19, Issue 1 https://doi.org/10.1186/s12885-019-5677-2	journal	May 2019
Telomere maintenance: regulating hTERC fate through RNA modifications Lirussi, Lisa; Nilsen, Hilde Molecular & Cellular Oncology, Vol. 6, Issue 6 https://doi.org/10.1080/23723556.2019.1670489	journal	October 2019
Integrative genomic analysis identifies associations of molecular alterations to APOBEC and BRCA1/2 mutational signatures in breast cancer Trevino, Victor Molecular Genetics & Genomic Medicine, Vol. 7, Issue 8 https://doi.org/10.1002/mgg3.810	journal	June 2019

Similar Records

Role of uracil-DNA glycosylase in mutation avoidance by Streptococcus pneumoniae

Journal Article · Tue Jan 01 00:00:00 EST 1991 · Journal of Bacteriology; (USA) · OSTI ID:1392805

Chen, Jau-Der; Lacks, S A

Uracil-DNA glycosylase causes 5-bromodeoxyuridine photosensitization in Escherichia coli K-12

Journal Article · Sat Sep 01 00:00:00 EDT 1990 · Journal of Bacteriology; (USA) · OSTI ID:1392805

Yamamoto, Y; Fujiwara, Y

Poxvirus uracil-DNA glycosylase-An unusual member of the family I uracil-DNA glycosylases: Poxvirus Uracil-DNA Glycosylase

Journal Article · Wed Nov 02 00:00:00 EDT 2016 · Protein Science · OSTI ID:1392805

Schormann, Norbert; Zhukovskaya, Natalia; Bedwell, Gregory; +6 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Biological Science
Base excision repair
DNA

Title: Uracil Accumulation and Mutagenesis Dominated by Cytosine Deamination in CpG Dinucleotides in Mice Lacking UNG and SMUG1

Citation Formats

References (60)

Cited By (5)

Similar Records

Related Subjects