Characterization of Oxidative Guanine Damage and Repair in Mammalian Telomeres

Wang, Zhilong; Rhee, David B.; Lu, Jian; Bohr, Christina T.; Zhou, Fang; Vallabhaneni, Haritha; de Souza-Pinto, Nadja C.; Liu, Yie

doi:10.1371/journal.pgen.1000951

Characterization of Oxidative Guanine Damage and Repair in Mammalian Telomeres

Journal Article · Thu May 13 00:00:00 EDT 2010 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1000951· OSTI ID:1627283

Wang, Zhilong ^[1]; Rhee, David B. ^[2]; Lu, Jian ^[3]; Bohr, Christina T. ^[3]; Zhou, Fang ^[3]; Vallabhaneni, Haritha ^[3]; de Souza-Pinto, Nadja C. ^[3]; Liu, Yie ^[3]

National Institutes of Health (NIH), Baltimore, MD (United States). National Inst. on Aging. Lab. of Molecular Gerontology; DOE/OSTI
National Institutes of Health (NIH), Baltimore, MD (United States). National Inst. on Aging. Lab. of Molecular Gerontology; Univ. of Tennessee, Knoxville, TN (United States). Graduate School of Genome Science and Technology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
National Institutes of Health (NIH), Baltimore, MD (United States). National Inst. on Aging. Lab. of Molecular Gerontology

8-oxo-7,8-dihydroguanine (8-oxoG) and 2,6-diamino-4-hydroxy-5-formamidopyrimidine (FapyG) are among the most common oxidative DNA lesions and are substrates for 8-oxoguanine DNA glycosylase (OGG1)–initiated DNA base excision repair (BER). Mammalian telomeres consist of triple guanine repeats and are subject to oxidative guanine damage. Here, we investigated the impact of oxidative guanine damage and its repair by OGG1 on telomere integrity in mice. The mouse cells were analyzed for telomere integrity by telomere quantitative fluorescence in situ hybridization (telomere–FISH), by chromosome orientation–FISH (CO–FISH), and by indirect immunofluorescence in combination with telomere–FISH and for oxidative base lesions by Fpg-incision/Southern blot assay. In comparison to the wild type, telomere lengthening was observed in Ogg1 null (Ogg1^-/-) mouse tissues and primary embryonic fibroblasts (MEFs) cultivated in hypoxia condition (3% oxygen), whereas telomere shortening was detected in Ogg1^-/- mouse hematopoietic cells and primary MEFs cultivated in normoxia condition (20% oxygen) or in the presence of an oxidant. In addition, telomere length abnormalities were accompanied by altered telomere sister chromatid exchanges, increased telomere single- and double-strand breaks, and preferential telomere lagging- or G-strand losses in Ogg1^-/- mouse cells. Oxidative guanine lesions were increased in telomeres in Ogg1^-/- mice with aging and primary MEFs cultivated in 20% oxygen. Furthermore, oxidative guanine lesions persisted at high level in Ogg1^-/- MEFs after acute exposure to hydrogen peroxide, while they rapidly returned to basal level in wild-type MEFs. These findings indicate that oxidative guanine damage can arise in telomeres where it affects length homeostasis, recombination, DNA replication, and DNA breakage repair. Our studies demonstrate that BER pathway is required in repairing oxidative guanine damage in telomeres and maintaining telomere integrity in mammals.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1627283

Journal Information:: PLoS Genetics, Journal Name: PLoS Genetics Journal Issue: 5 Vol. 6; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (83)

Mutagenesis by 8-oxoguanine: an enemy within Grollman, Arthur P.; Moriya, Masaaki Trends in Genetics, Vol. 9, Issue 7 https://doi.org/10.1016/0168-9525(93)90089-z	journal	July 1993
Flap Endonuclease 1 Contributes to Telomere Stability Saharia, Abhishek; Guittat, Lionel; Crocker, Sandra Current Biology, Vol. 18, Issue 7 https://doi.org/10.1016/j.cub.2008.02.071	journal	April 2008
8-OxoG retards the activity of the ligase III/XRCC1 complex during the repair of a single-strand break, when present within a clustered DNA damage site Lomax, Martine E.; Cunniffe, Siobhan; O’Neill, Peter DNA Repair, Vol. 3, Issue 3 https://doi.org/10.1016/j.dnarep.2003.11.006	journal	March 2004
Formamidopyrimidines in DNA: Mechanisms of formation, repair, and biological effects Dizdaroglu, Miral; Kirkali, Güldal; Jaruga, Pawel Free Radical Biology and Medicine, Vol. 45, Issue 12 https://doi.org/10.1016/j.freeradbiomed.2008.07.004	journal	December 2008
Cytotoxicity and mutagenicity of endogenous DNA base lesions as potential cause of human aging Akbari, Mansour; Krokan, Hans E. Mechanisms of Ageing and Development, Vol. 129, Issue 7-8 https://doi.org/10.1016/j.mad.2008.01.007	journal	July 2008
Checkpoint kinase phosphorylation in response to endogenous oxidative DNA damage in repair-deficient stationary-phase Saccharomyces cerevisiae Pawar, Vaibhav; Jingjing, Liu; Patel, Nila Mechanisms of Ageing and Development, Vol. 130, Issue 8 https://doi.org/10.1016/j.mad.2009.06.002	journal	August 2009
Telomere length mediates the effects of telomerase on the cellular response to genotoxic stress Rubio, Miguel A.; Davalos, Albert R.; Campisi, Judith Experimental Cell Research, Vol. 298, Issue 1 https://doi.org/10.1016/j.yexcr.2004.04.004	journal	August 2004
Site-specific DNA damage at GGG sequence by oxidative stress may accelerate telomere shortening Oikawa, Shinji; Kawanishi, Shosuke FEBS Letters, Vol. 453, Issue 3 https://doi.org/10.1016/s0014-5793(99)00748-6	journal	June 1999
Base excision repair in yeast and mammals Memisoglu, Asli; Samson, Leona Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 451, Issue 1-2 https://doi.org/10.1016/s0027-5107(00)00039-7	journal	June 2000
TRF2 Protects Human Telomeres from End-to-End Fusions van Steensel, Bas; Smogorzewska, Agata; de Lange, Titia Cell, Vol. 92, Issue 3 https://doi.org/10.1016/s0092-8674(00)80932-0	journal	February 1998
Switching and Signaling at the Telomere Blackburn, Elizabeth H. Cell, Vol. 106, Issue 6 https://doi.org/10.1016/s0092-8674(01)00492-5	journal	September 2001
CDC17: An essential gene that prevents telomere elongation in yeast Carson, M.; Hartwell, L. Cell, Vol. 42, Issue 1 https://doi.org/10.1016/s0092-8674(85)80120-3	journal	August 1985
Accumulation of single-strand breaks is the major cause of telomere shortening in human fibroblasts von Zglinicki, Thomas; Pilger, Rita; Sitte, Nicolle Free Radical Biology and Medicine, Vol. 28, Issue 1 https://doi.org/10.1016/s0891-5849(99)00207-5	journal	January 2000
XRCC1 keeps DNA from getting stranded Thompson, Larry H.; West, Mary G. Mutation Research/DNA Repair, Vol. 459, Issue 1 https://doi.org/10.1016/s0921-8777(99)00058-0	journal	February 2000
Tankyrase promotes telomere elongation in human cells Smith, Susan; de Lange, Titia Current Biology, Vol. 10, Issue 20 https://doi.org/10.1016/s0960-9822(00)00752-1	journal	October 2000
DNA Damage Foci at Dysfunctional Telomeres Takai, Hiroyuki; Smogorzewska, Agata; de Lange, Titia Current Biology, Vol. 13, Issue 17 https://doi.org/10.1016/s0960-9822(03)00542-6	journal	September 2003
ERCC1/XPF Removes the 3′ Overhang from Uncapped Telomeres and Represses Formation of Telomeric DNA-Containing Double Minute Chromosomes Zhu, Xu-Dong; Niedernhofer, Laura; Kuster, Bernhard Molecular Cell, Vol. 12, Issue 6 https://doi.org/10.1016/s1097-2765(03)00478-7	journal	December 2003
Mammalian Telomeres Resemble Fragile Sites and Require TRF1 for Efficient Replication Sfeir, Agnel; Kosiyatrakul, Settapong T.; Hockemeyer, Dirk Journal of End-to-End-testing, Vol. 138, Issue 1 https://doi.org/10.1016/s9999-9994(09)20370-9	journal	July 2009
Site-Specific Oxidation at GG and GGG Sequences in Double-Stranded DNA by Benzoyl Peroxide as a Tumor Promoter Kawanishi, Shosuke; Oikawa, Shinji; Murata, Mariko Biochemistry, Vol. 38, Issue 51 https://doi.org/10.1021/bi990890z	journal	November 1999
Control of telomere length by the human telomeric protein TRF1 van Steensel, Bas; de Lange, Titia Nature, Vol. 385, Issue 6618 https://doi.org/10.1038/385740a0	journal	February 1997
Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells Hegde, Muralidhar L.; Hazra, Tapas K.; Mitra, Sankar Cell Research, Vol. 18, Issue 1 https://doi.org/10.1038/cr.2008.8	journal	January 2008
Telomere length regulation: coupling DNA end processing to feedback regulation of telomerase Shore, David; Bianchi, Alessandro The EMBO Journal, Vol. 28, Issue 16 https://doi.org/10.1038/emboj.2009.195	journal	July 2009
Deletion of Ogg1 DNA glycosylase results in telomere base damage and length alteration in yeast Lu, Jian; Liu, Yie The EMBO Journal, Vol. 29, Issue 2 https://doi.org/10.1038/emboj.2009.355	journal	November 2009
A DNA damage checkpoint response in telomere-initiated senescence Fagagna, Fabrizio d'Adda di; Reaper, Philip M.; Clay-Farrace, Lorena Nature, Vol. 426, Issue 6963 https://doi.org/10.1038/nature02118	journal	November 2003
Telomere length dynamics in human lymphocyte subpopulations measured by flow cytometry Rufer, Nathalie; Dragowska, Wieslawa; Thornbury, Gayle Nature Biotechnology, Vol. 16, Issue 8 https://doi.org/10.1038/nbt0898-743	journal	August 1998
Ku70 stimulates fusion of dysfunctional telomeres yet protects chromosome ends from homologous recombination Celli, Giulia B.; Denchi, Eros Lazzerini; de Lange, Titia Nature Cell Biology, Vol. 8, Issue 8 https://doi.org/10.1038/ncb1444	journal	July 2006
POT1 protects telomeres from a transient DNA damage response and determines how human chromosomes end Hockemeyer, Dirk; Sfeir, Agnel J.; Shay, Jerry W. The EMBO Journal, Vol. 24, Issue 14 https://doi.org/10.1038/sj.emboj.7600733	journal	June 2005
Dysfunctional telomeres activate an ATM-ATR-dependent DNA damage response to suppress tumorigenesis Guo, Xiaolan; Deng, Yibin; Lin, Yahong The EMBO Journal, Vol. 26, Issue 22 https://doi.org/10.1038/sj.emboj.7601893	journal	October 2007
Two distinct pathways of cell death triggered by oxidative damage to nuclear and mitochondrial DNAs Oka, Sugako; Ohno, Mizuki; Tsuchimoto, Daisuke The EMBO Journal, Vol. 27, Issue 2 https://doi.org/10.1038/sj.emboj.7601975	journal	January 2008
ORC binding to TRF2 stimulates OriP replication Atanasiu, Constandache; Deng, Zhong; Wiedmer, Andreas EMBO reports, Vol. 7, Issue 7 https://doi.org/10.1038/sj.embor.7400730	journal	June 2006
A genome-wide telomere screen in yeast: The long and short of it all Edmonds, Dawn; Breitkreutz, Bobby-Joe; Harrington, Lea Proceedings of the National Academy of Sciences, Vol. 101, Issue 26 https://doi.org/10.1073/pnas.0403378101	journal	June 2004
An increase in telomere sister chromatid exchange in murine embryonic stem cells possessing critically shortened telomeres Wang, Y.; Erdmann, N.; Giannone, R. J. Proceedings of the National Academy of Sciences, Vol. 102, Issue 29 https://doi.org/10.1073/pnas.0504635102	journal	July 2005
The metabolic syndrome resulting from a knockout of the NEIL1 DNA glycosylase Vartanian, V.; Lowell, B.; Minko, I. G. Proceedings of the National Academy of Sciences, Vol. 103, Issue 6 https://doi.org/10.1073/pnas.0507444103	journal	January 2006
Telomere dysfunction as a cause of genomic instability in Werner syndrome Crabbe, L.; Jauch, A.; Naeger, C. M. Proceedings of the National Academy of Sciences, Vol. 104, Issue 7 https://doi.org/10.1073/pnas.0609410104	journal	February 2007
DNA damage and repair in telomeres: relation to aging. Kruk, P. A.; Rampino, N. J.; Bohr, V. A. Proceedings of the National Academy of Sciences, Vol. 92, Issue 1 https://doi.org/10.1073/pnas.92.1.258	journal	January 1995
Telomeres in the mouse have large inter-chromosomal variations in the number of T2AG3 repeats Zijlmans, J. M. J. M.; Martens, U. M.; Poon, S. S. S. Proceedings of the National Academy of Sciences, Vol. 94, Issue 14 https://doi.org/10.1073/pnas.94.14.7423	journal	July 1997
Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage Klungland, A.; Rosewell, I.; Hollenbach, S. Proceedings of the National Academy of Sciences, Vol. 96, Issue 23 https://doi.org/10.1073/pnas.96.23.13300	journal	November 1999
Sequence-specific DNA Cleavage by Fe ²⁺ -mediated Fenton Reactions Has Possible Biological Implications Henle, Ernst S.; Han, Zhengxu; Tang, Ning Journal of Biological Chemistry, Vol. 274, Issue 2 https://doi.org/10.1074/jbc.274.2.962	journal	January 1999
ReviewThe Defense Mechanisms in Mammalian Cells against Oxidative Damage in Nucleic Acids and their Involvement in the Suppression of Mutagenesis and Cell Death Nakabeppu, Yusaku; Tsuchimoto, Daisuke; Furuichi, Masato Free Radical Research, Vol. 38, Issue 5 https://doi.org/10.1080/10715760410001688348	journal	May 2004
Cells deficient in oxidative DNA damage repair genes Myh and Ogg1 are sensitive to oxidants with increased G 2 /M arrest and multinucleation Xie, Yali; Yang, Hanjing; Miller, Jeffrey H. Carcinogenesis, Vol. 29, Issue 4 https://doi.org/10.1093/carcin/bgn033	journal	February 2008
The number of vertebrate repeats can be regulated at yeast telomeres by Rap1-independent mechanisms Brevet, V. The EMBO Journal, Vol. 22, Issue 7 https://doi.org/10.1093/emboj/cdg155	journal	April 2003
Oxidative damage in telomeric DNA disrupts recognition by TRF1 and TRF2 Opresko, P. L. Nucleic Acids Research, Vol. 33, Issue 4 https://doi.org/10.1093/nar/gki273	journal	February 2005
Base excision repair processing of abasic site/single-strand break lesions within clustered damage sites associated with XRCC1 deficiency Mourgues, Sophie; Lomax, Martine E.; O’Neill, Peter Nucleic Acids Research, Vol. 35, Issue 22 https://doi.org/10.1093/nar/gkm947	journal	November 2007
Functional links between telomeres and proteins of the DNA-damage response d'Adda di Fagagna, F. Genes & Development, Vol. 18, Issue 15 https://doi.org/10.1101/gad.1214504	journal	August 2004
Shelterin: the protein complex that shapes and safeguards human telomeres de Lange, T. Genes & Development, Vol. 19, Issue 18 https://doi.org/10.1101/gad.1346005	journal	September 2005
Senescence Induced by Altered Telomere State, Not Telomere Loss Karlseder, J. Science, Vol. 295, Issue 5564 https://doi.org/10.1126/science.1069523	journal	March 2002
Defective Telomere Lagging Strand Synthesis in Cells Lacking WRN Helicase Activity Crabbe, L. Science, Vol. 306, Issue 5703 https://doi.org/10.1126/science.1103619	journal	December 2004
The Recombination Protein RAD52 Cooperates with the Excision Repair Protein OGG1 for the Repair of Oxidative Lesions in Mammalian Cells de Souza-Pinto, Nadja C.; Maynard, Scott; Hashiguchi, Kazunari Molecular and Cellular Biology, Vol. 29, Issue 16 https://doi.org/10.1128/mcb.00265-09	journal	June 2009
8-Oxoguanine Formation Induced by Chronic UVB Exposure Makes Ogg1 Knockout Mice Susceptible to Skin Carcinogenesis Kunisada, Makoto; Sakumi, Kunihiko; Tominaga, Yohei Cancer Research, Vol. 65, Issue 14 https://doi.org/10.1158/0008-5472.can-05-0724	journal	July 2005
Mutagenesis and carcinogenesis caused by the oxidation of nucleic acids Nakabeppu, Yusaku; Sakumi, Kunihiko; Sakamoto, Katsumi Biological Chemistry, Vol. 387, Issue 4 https://doi.org/10.1515/bc.2006.050	journal	January 2006
Mutagenesis by 8-oxoguanine: an enemy within Grollman, Arthur P.; Moriya, Masaaki Trends in Genetics, Vol. 9, Issue 7 https://doi.org/10.1016/0168-9525(93)90089-Z	journal	July 1993
Site-specific DNA damage at GGG sequence by oxidative stress may accelerate telomere shortening Oikawa, Shinji; Kawanishi, Shosuke FEBS Letters, Vol. 453, Issue 3 https://doi.org/10.1016/S0014-5793(99)00748-6	journal	June 1999
Base excision repair in yeast and mammals Memisoglu, Asli; Samson, Leona Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 451, Issue 1-2 https://doi.org/10.1016/S0027-5107(00)00039-7	journal	June 2000
TRF2 Protects Human Telomeres from End-to-End Fusions van Steensel, Bas; Smogorzewska, Agata; de Lange, Titia Cell, Vol. 92, Issue 3 https://doi.org/10.1016/S0092-8674(00)80932-0	journal	February 1998
Switching and Signaling at the Telomere Blackburn, Elizabeth H. Cell, Vol. 106, Issue 6 https://doi.org/10.1016/S0092-8674(01)00492-5	journal	September 2001
CDC17: An essential gene that prevents telomere elongation in yeast Carson, M.; Hartwell, L. Cell, Vol. 42, Issue 1 https://doi.org/10.1016/S0092-8674(85)80120-3	journal	August 1985
Base excision repair of 8-hydroxyguanine protects DNA from endogenous oxidative stress Boiteux, Serge; Radicella, J. Pablo Biochimie, Vol. 81, Issue 1-2 https://doi.org/10.1016/S0300-9084(99)80039-X	journal	January 1999
Accumulation of single-strand breaks is the major cause of telomere shortening in human fibroblasts von Zglinicki, Thomas; Pilger, Rita; Sitte, Nicolle Free Radical Biology and Medicine, Vol. 28, Issue 1 https://doi.org/10.1016/S0891-5849(99)00207-5	journal	January 2000
XRCC1 keeps DNA from getting stranded Thompson, Larry H.; West, Mary G. Mutation Research/DNA Repair, Vol. 459, Issue 1 https://doi.org/10.1016/S0921-8777(99)00058-0	journal	February 2000
Tankyrase promotes telomere elongation in human cells Smith, Susan; de Lange, Titia Current Biology, Vol. 10, Issue 20 https://doi.org/10.1016/S0960-9822(00)00752-1	journal	October 2000
DNA Damage Foci at Dysfunctional Telomeres Takai, Hiroyuki; Smogorzewska, Agata; de Lange, Titia Current Biology, Vol. 13, Issue 17 https://doi.org/10.1016/S0960-9822(03)00542-6	journal	September 2003
ERCC1/XPF Removes the 3′ Overhang from Uncapped Telomeres and Represses Formation of Telomeric DNA-Containing Double Minute Chromosomes Zhu, Xu-Dong; Niedernhofer, Laura; Kuster, Bernhard Molecular Cell, Vol. 12, Issue 6 https://doi.org/10.1016/S1097-2765(03)00478-7	journal	December 2003
Pot1 Deficiency Initiates DNA Damage Checkpoint Activation and Aberrant Homologous Recombination at Telomeres Wu, Ling; Multani, Asha S.; He, Hua Cell, Vol. 126, Issue 1 https://doi.org/10.1016/j.cell.2006.05.037	journal	July 2006
Mammalian Telomeres Resemble Fragile Sites and Require TRF1 for Efficient Replication Sfeir, Agnel; Kosiyatrakul, Settapong T.; Hockemeyer, Dirk Cell, Vol. 138, Issue 1 https://doi.org/10.1016/j.cell.2009.06.021	journal	July 2009
Site-Specific DNA Damage at the GGG Sequence by UVA Involves Acceleration of Telomere Shortening ^† Oikawa, Shinji; Tada-Oikawa, Saeko; Kawanishi, Shosuke Biochemistry, Vol. 40, Issue 15 https://doi.org/10.1021/bi002721g	journal	April 2001
Mapping of the Hot Spots for DNA Damage by One-Electron Oxidation: Efficacy of GG Doublets and GGG Triplets as a Trap in Long-Range Hole Migration Saito, Isao; Nakamura, Takashi; Nakatani, Kazuhiko Journal of the American Chemical Society, Vol. 120, Issue 48 https://doi.org/10.1021/ja981888i	journal	November 1998
Experimental and Theoretical Studies on the Selectivity of GGG Triplets toward One-Electron Oxidation in B-Form DNA Yoshioka, Yasunori; Kitagawa, Yasutaka; Takano, Yu Journal of the American Chemical Society, Vol. 121, Issue 38 https://doi.org/10.1021/ja991032t	journal	September 1999
POT1 as a terminal transducer of TRF1 telomere length control Loayza, Diego; de Lange, Titia Nature, Vol. 423, Issue 6943 https://doi.org/10.1038/nature01688	journal	May 2003
Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1 Denchi, Eros Lazzerini; de Lange, Titia Nature, Vol. 448, Issue 7157 https://doi.org/10.1038/nature06065	journal	August 2007
Telomere-driven replicative senescence is a stress response Zglinicki, Thomas von; Petrie, Joanne; Kirkwood, Thomas B. L. Nature Biotechnology, Vol. 21, Issue 3 https://doi.org/10.1038/nbt0303-229b	journal	March 2003
A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length Askree, S. H.; Yehuda, T.; Smolikov, S. Proceedings of the National Academy of Sciences, Vol. 101, Issue 23 https://doi.org/10.1073/pnas.0401263101	journal	May 2004
Evidence that MutY and MutM combine to prevent mutations by an oxidatively damaged form of guanine in DNA. Michaels, M. L.; Cruz, C.; Grollman, A. P. Proceedings of the National Academy of Sciences, Vol. 89, Issue 15 https://doi.org/10.1073/pnas.89.15.7022	journal	August 1992
Repair of Formamidopyrimidines in DNA Involves Different Glycosylases Hu, Jingping; de Souza-Pinto, Nadja C.; Haraguchi, Kazuhiro Journal of Biological Chemistry, Vol. 280, Issue 49 https://doi.org/10.1074/jbc.M508772200	journal	December 2005
PARP1 Is a TRF2-associated Poly(ADP-Ribose)Polymerase and Protects Eroded Telomeres Gomez, Marla; Wu, Jun; Schreiber, Valérie Molecular Biology of the Cell, Vol. 17, Issue 4 https://doi.org/10.1091/mbc.E05-07-0672	journal	April 2006
Frequent recombination in telomeric DNA may extend the proliferative life of telomerase-negative cells Bailey, S. M. Nucleic Acids Research, Vol. 32, Issue 12 https://doi.org/10.1093/nar/gkh691	journal	July 2004
NEIL1 excises 3' end proximal oxidative DNA lesions resistant to cleavage by NTH1 and OGG1 Parsons, J. L.; Zharkov, D. O.; Dianov, G. L. Nucleic Acids Research, Vol. 33, Issue 15 https://doi.org/10.1093/nar/gki816	journal	August 2005
Involvement of human ORC and TRF2 in pre-replication complex assembly at telomeres Tatsumi, Yasutoshi; Ezura, Kai; Yoshida, Kazumasa Genes to Cells, Vol. 13, Issue 10 https://doi.org/10.1111/j.1365-2443.2008.01224.x	journal	October 2008
The Recombination Protein RAD52 Cooperates with the Excision Repair Protein OGG1 for the Repair of Oxidative Lesions in Mammalian Cells de Souza-Pinto, Nadja C.; Maynard, Scott; Hashiguchi, Kazunari Molecular and Cellular Biology, Vol. 29, Issue 16 https://doi.org/10.1128/MCB.00265-09	journal	June 2009
Specific DNA replication mutations affect telomere length in Saccharomyces cerevisiae. Adams, A. K.; Holm, C. Molecular and Cellular Biology, Vol. 16, Issue 9 https://doi.org/10.1128/MCB.16.9.4614	journal	September 1996
Overlapping Specificities of Base Excision Repair, Nucleotide Excision Repair, Recombination, and Translesion Synthesis Pathways for DNA Base Damage in Saccharomyces cerevisiae Swanson, Rebecca L.; Morey, Natalie J.; Doetsch, Paul W. Molecular and Cellular Biology, Vol. 19, Issue 4 https://doi.org/10.1128/MCB.19.4.2929	journal	April 1999
Deficiencies in Mouse *Myh* and *Ogg1* Result in Tumor Predisposition and G to T Mutations in Codon 12 of the *K-Ras* Oncogene in Lung Tumors Xie, Yali; Yang, Hanjing; Cunanan, Cristina Cancer Research, Vol. 64, Issue 9 https://doi.org/10.1158/0008-5472.CAN-03-3834	journal	May 2004
8-Oxoguanine Formation Induced by Chronic UVB Exposure Makes Ogg1 Knockout Mice Susceptible to Skin Carcinogenesis Kunisada, Makoto; Sakumi, Kunihiko; Tominaga, Yohei Cancer Research, Vol. 65, Issue 14 https://doi.org/10.1158/0008-5472.CAN-05-0724	journal	July 2005
Mutagenesis and carcinogenesis caused by the oxidation of nucleic acids Nakabeppu, Yusaku; Sakumi, Kunihiko; Sakamoto, Katsumi Biological Chemistry, Vol. 387, Issue 4 https://doi.org/10.1515/BC.2006.050	journal	January 2006

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The relationship of telomere length to baseline corticosterone levels in nestlings of an altricial passerine bird in natural populations Quirici, Verónica; Guerrero, Claudia Jimena; Krause, Jesse S. Frontiers in Zoology, Vol. 13, Issue 1 https://doi.org/10.1186/s12983-016-0133-5	journal	January 2016
Defective Repair of Oxidative Base Lesions by the DNA Glycosylase Nth1 Associates with Multiple Telomere Defects Vallabhaneni, Haritha; O'Callaghan, Nathan; Sidorova, Julia PLoS Genetics, Vol. 9, Issue 7 https://doi.org/10.1371/journal.pgen.1003639	journal	July 2013
Association between Urinary Excretion of Cortisol and Markers of Oxidatively Damaged DNA and RNA in Humans Joergensen, Anders; Broedbaek, Kasper; Weimann, Allan PLoS ONE, Vol. 6, Issue 6 https://doi.org/10.1371/journal.pone.0020795	journal	June 2011
Up-Regulation of leucocytes Genes Implicated in Telomere Dysfunction and Cellular Senescence Correlates with Depression and Anxiety Severity Scores Teyssier, Jean-Raymond; Chauvet-Gelinier, Jean-Christophe; Ragot, Sylviane PLoS ONE, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pone.0049677	journal	November 2012
Senescence of Primary Amniotic Cells via Oxidative DNA Damage Menon, Ramkumar; Boldogh, Istvan; Urrabaz-Garza, Rheanna PLoS ONE, Vol. 8, Issue 12 https://doi.org/10.1371/journal.pone.0083416	journal	December 2013
ATM Deficiency Accelerates DNA Damage, Telomere Erosion, and Premature T Cell Aging in HIV-Infected Individuals on Antiretroviral Therapy Zhao, Juan; Nguyen, Lam Ngoc Thao; Nguyen, Lam Nhat Frontiers in Immunology, Vol. 10 https://doi.org/10.3389/fimmu.2019.02531	journal	November 2019
Interactive Roles of DNA Helicases and Translocases with the Single-Stranded DNA Binding Protein RPA in Nucleic Acid Metabolism Awate, Sanket; Brosh, Jr., Robert International Journal of Molecular Sciences, Vol. 18, Issue 6 https://doi.org/10.3390/ijms18061233	journal	June 2017
Initiation of human parturition: signaling from senescent fetal tissues via extracellular vesicle mediated paracrine mechanism Menon, Ramkumar Obstetrics & Gynecology Science, Vol. 62, Issue 4 https://doi.org/10.5468/ogs.2019.62.4.199	journal	January 2019
Telomerase activity, telomere length and hTERT DNA methylation in peripheral blood mononuclear cells from monozygotic twins with discordant smoking habits: Telomerase Activity and Tobacco Smoke Marcon, Francesca; Siniscalchi, Ester; Andreoli, Cristina Environmental and Molecular Mutagenesis, Vol. 58, Issue 8 https://doi.org/10.1002/em.22127	journal	August 2017
Single-molecule counting of oxidative DNA damage in telomeres from cancer cells Zhang, Yan; Hua, Ruo-nan; Xiang, Dongxue Chemical Communications, Vol. 55, Issue 53 https://doi.org/10.1039/c9cc03766g	journal	January 2019
Poly(ADP-ribose) Polymerase 1 (PARP-1) Binds to 8-Oxoguanine-DNA Glycosylase (OGG1) Noren Hooten, Nicole; Kompaniez, Kari; Barnes, Janice Journal of Biological Chemistry, Vol. 286, Issue 52 https://doi.org/10.1074/jbc.m111.255869	journal	December 2011
Neil2 -null Mice Accumulate Oxidized DNA Bases in the Transcriptionally Active Sequences of the Genome and Are Susceptible to Innate Inflammation Chakraborty, Anirban; Wakamiya, Maki; Venkova-Canova, Tatiana Journal of Biological Chemistry, Vol. 290, Issue 41 https://doi.org/10.1074/jbc.m115.658146	journal	August 2015
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
DNA profiling, telomere analysis and antioxidant properties as tools for monitoring ex situ seed longevity Donà, M.; Balestrazzi, A.; Mondoni, A. Annals of Botany, Vol. 111, Issue 5 https://doi.org/10.1093/aob/mct058	journal	March 2013
Deletion of the major peroxiredoxin Tsa1 alters telomere length homeostasis Lu, Jian; Vallabhaneni, Haritha; Yin, Jinhu Aging Cell, Vol. 12, Issue 4 https://doi.org/10.1111/acel.12085	journal	May 2013
Telomere length in reproduction Thilagavathi, J.; Venkatesh, S.; Dada, R. Andrologia, Vol. 45, Issue 5 https://doi.org/10.1111/and.12008	journal	August 2012
Reactive oxygen species impact on sperm DNA and its role in male infertility Bui, A. D.; Sharma, R.; Henkel, R. Andrologia, Vol. 50, Issue 8 https://doi.org/10.1111/and.13012	journal	April 2018
Telomere length and dynamics predict mortality in a wild longitudinal study Barrett, Emma L. B.; Burke, Terry A.; Hammers, Martijn Molecular Ecology, Vol. 22, Issue 1 https://doi.org/10.1111/mec.12110	journal	November 2012
Tissue-specific telomere dynamics in hibernating arctic ground squirrels ( Urocitellus parryii ) Wilbur, Sara M.; Barnes, Brian M.; Kitaysky, Alexander S. Journal of Experimental Biology https://doi.org/10.1242/jeb.204925	journal	January 2019
Telomere shortening and ionizing radiation: A possible role in vascular dysfunction? Sabatino, Laura; Picano, Eugenio; Andreassi, Maria Grazia International Journal of Radiation Biology, Vol. 88, Issue 11 https://doi.org/10.3109/09553002.2012.709307	journal	August 2012

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