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
Abstract
Oxidative DNA damage is unavoidably and continuously generated by oxidant byproducts of normal cellular metabolism. The DNA damage repair genes, mutY and mutM, prevent G to T mutations caused by reactive oxygen species in Escherichia coli, but it has remained debatable whether deficiencies in their mammalian counterparts, Myh and Ogg1, are directly involved in tumorigenesis. Here, we demonstrate that deficiencies in Myh and Ogg1 predispose 65.7% of mice to tumors, predominantly lung and ovarian tumors, and lymphomas. Remarkably, subsequent analyses identified G to T mutations in 75% of the lung tumors at an activating hot spot, codon 12, of the K-ras oncogene, but none in their adjacent normal tissues. Moreover, malignant lung tumors were increased with combined heterozygosity of Msh2, a mismatch repair gene involved in oxidative DNA damage repair as well. Thus, oxidative DNA damage appears to play a causal role in tumorigenesis, and codon 12 of K-ras is likely to be an important downstream target in lung tumorigenesis. The multiple oxidative repair genes are required to prevent mutagenesis and tumor formation. The mice described here provide a valuable model for studying the mechanisms of oxidative DNA damage in tumorigenesis and investigating preventive or therapeutic approaches.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
ogg1 or ogg1/mth1 knock-out mice have 20-fold higher levels of 8-oxoguanine in mtDNA and half the life expectancy relative to wild-type mice, but no increase in mtDNA mutations.
“The ogg1 or ogg1/mth1 knock-out mice have 20-fold higher levels of 8-oxoguanine in mtDNA (de Souza-Pinto et al., 2001) and half the life expectancy relative to wild-type (WT) mice (Xie et al., 2004), but no increase in mtDNA mutations (Halsne et al., 2012).”
From Role of the mitochondrial DNA replication machinery in mitochondrial DNA mutagenesis, aging and age-related diseases (2017) · cites this paper as Xie et al., 2004
Cites
Hanahan, D., & Weinberg, R. A. (2000) · Cell · doi:10.1016/s0092-8674(00)81683-9 · Cited by 29,219 · see citing works
p53 Mutations in Human Cancers
Hollstein, M., Sidransky, D., Vogelstein, B., & Harris, C. C. (1991) · Science · doi:10.1126/science.1905840 · Cited by 8,018 · see citing works
ras oncogenes in human cancer: a review.
Bos, J. L. (1989) · PubMed · Cited by 5,061 · see citing works
The multistep nature of cancer
Vogelstein, B., & Kinzler, K. W. (1993) · Trends in Genetics · doi:10.1016/0168-9525(93)90209-z · Cited by 1,858 · see citing works
Inherited variants of MYH associated with somatic G:C→T:A mutations in colorectal tumors
Tassan, N. A. A., Chmiel, N. H., Maynard, J. H., Fleming, N. I., Livingston, A. L., Williams, G. T., Hodges, A., Davies, D. R., David, S. S., Sampson, J. R., et al. (2002) · Nature Genetics · doi:10.1038/ng828 · Cited by 1,392 · see citing works
Somatic activation of the K-ras oncogene causes early onset lung cancer in mice
Johnson, L., Mercer, K., Greenbaum, D., Bronson, R. T., Crowley, D., Tuveson, D. A., & Jacks, T. (2001) · Nature · doi:10.1038/35074129 · Cited by 1,179 · see citing works
Mice lacking serum paraoxonase are susceptible to organophosphate toxicity and atherosclerosis
Shih, D. M., Gu, L., Xia, Y.-R., Navab, M., Li, W., Hama, S. Y., Castellani, L. W., Furlong, C. E., Costa, L. G., Fogelman, A. M., et al. (1998) · Nature · doi:10.1038/28406 · Cited by 1,078 · see citing works
Multiple Colorectal Adenomas, Classic Adenomatous Polyposis, and Germ-Line Mutations inMYH
Sieber, O. M., Lipton, L. R., Crabtree, M., Heinimann, K., Fidalgo, P. O., Phillips, R. K. S., Bisgaard, M.-L., Orntoft, T. F., Aaltonen, L. A., Hodgson, S. V., et al. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa025283 · Cited by 859 · see citing works
Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage
Klungland, A., Rosewell, I., Hollenbach, S., Larsen, E., Daly, G., Epe, B., Seeberg, E., Lindahl, T., & Barnes, D. E. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.23.13300 · Cited by 807 · see citing works
Self-citationde Wind, N., Dekker, M., Berns, A. J. M., Radman, M., & Riele, H. T. (1995) · Cell · doi:10.1016/0092-8674(95)90319-4 · Cited by 780 · see citing works
Michaels, M. L., & Miller, J. H. (1992) · Journal of Bacteriology · doi:10.1128/jb.174.20.6321-6325.1992 · Cited by 693 · see citing works
Self-citationMichaels, M. L., Cruz, C., Grollman, A. P., & Miller, J. H. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.15.7022 · Cited by 595 · see citing works
Self-citationThe Human OGG1 Gene: Structure, Functions, and Its Implication in the Process of Carcinogenesis
Boiteux, S., & Radicella, J. P. (2000) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.2000.1773 · Cited by 478 · see citing works
Walther, J. B., Loh, T., & Granka, L. A. (2005) · Journal of Language and Social Psychology · doi:10.1177/0261927x04273036 · Cited by 436 · see citing works
MSH2 deficient mice are viable and susceptible to lymphoid tumours
Reitmair, A. H., Schmits, R., Ewel, A., Bapat, B. V., Redston, M. S., Mitri, A., Waterhouse, P. D., Mittrücker, H., Wakeham, A. C., Liu, B., et al. (1995) · Nature Genetics · doi:10.1038/ng0995-64 · Cited by 376 · see citing works
Self-citationMmh / Ogg1 gene inactivation results in accumulation of 8-hydroxyguanine in mice
Minowa, O., Arai, T., Hirano, M., Monden, Y., Nakai, S., Fukuda, M., Itoh, M., Takano, H., Hippou, Y., Aburatani, H., et al. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.050404497 · Cited by 348 · see citing works
You, M., Candrian, U., Maronpot, R. R., Stoner, G. D., & Anderson, M. W. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.9.3070 · Cited by 336 · see citing works
Asami, S. (1997) · Carcinogenesis · doi:10.1093/carcin/18.9.1763 · Cited by 290 · see citing works
Mutagenesis and carcinogenesis: Endogenous and exogenous factors
Ames, B. N. (1989) · Environmental and Molecular Mutagenesis · doi:10.1002/em.2850140614 · Cited by 260 · see citing works
Asami, S., Hirano, T., Yamaguchi, R., Tomioka, Y., Itoh, H., & Kasai, H. (1996) · PubMed · Cited by 250 · see citing works
Ogg1 knockout-associated lung tumorigenesis and its suppression by Mth1 gene disruption.
Sakumi, K., Tominaga, Y., Furuichi, M., Xu, P., Tsuzuki, T., Sekiguchi, M., & Nakabeppu, Y. (2003) · PubMed · Cited by 237 · see citing works
Association of the hOGG1 Ser326Cys polymorphism with lung cancer risk.
Marchand, L. L., Donlon, T. A., Lum‐Jones, A., Seifried, A., & Wilkens, L. R. (2002) · PubMed · Cited by 230 · see citing works
The Mammalian Mismatch Repair Pathway Removes DNA 8-oxodGMP Incorporated from the Oxidized dNTP Pool
Colussi, C., Parlanti, E., Degan, P., Aquilina, G., Barnes, D., Macpherson, P., Karran, P., Crescenzi, M., Eugenia Dogliotti, Y., & Bignami, M. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00863-1 · Cited by 228 · see citing works
Self-citationNi, T. T., Marsischky, G., & Kolodner, R. D. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80346-9 · Cited by 222 · see citing works
DeWeese, T. L., Shipman, J. M., Larrier, N., Buckley, N. M., Kidd, L. R., Groopman, J. D., Cutler, R. G., Riele, H. T., & Nelson, W. G. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.20.11915 · Cited by 188 · see citing works
Osterod, M. (2001) · Carcinogenesis · doi:10.1093/carcin/22.9.1459 · Cited by 187 · see citing works
Functional Expression of hMYH, a Human Homolog of the Escherichia coli MutY Protein
Slupska, M. M., Luther, W. M., Chiang, J., Yang, H., & Miller, J. H. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.19.6210-6213.1999 · Cited by 174 · see citing works
Self-citationYang, H. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.3.743 · Cited by 132 · see citing works
Self-citationModeling human lung cancer in mice: similarities and shortcomings
Tuveson, D. A., & Jacks, T. (1999) · Oncogene · doi:10.1038/sj.onc.1203107 · Cited by 131 · see citing works
Shibata, D. K., Hawes, D., Li, Z. H., Hernández, A., Spruck, C., & Nichols, P. W. (1992) · PubMed Central · Cited by 124 · see citing works
Self-citationHernandez‐Boussard, T., & Hainaut, P. L. (1998) · Environmental Health Perspectives · doi:10.1289/ehp.98106385 · Cited by 121 · see citing works
Arai, T. (2002) · Carcinogenesis · doi:10.1093/carcin/23.12.2005 · Cited by 117 · see citing works
Haplo-insufficiency? Let me count the ways: Figure 1.Preprint
Quon, K. C., & Berns, A. J. M. (2001) · Genes & Development · doi:10.1101/gad.949001 · Cited by 109 · see citing works
Parental bias of Ki-ras oncogenes detected in lung tumors from mouse hybrids.
You, M., Wang, Y., Stoner, G. D., You, L., Maronpot, R. M., Reynolds, S. H., & Anderson, M. W. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.13.5804 · Cited by 93 · see citing works
Female embryonic lethality in mice nullizygous for both Msh2 and p53
Cranston, A. N., Bocker, T., Reitmair, A. H., Palazzo, J., Wilson, T., Mak, T. W., & Fishel, R. A. (1997) · Nature Genetics · doi:10.1038/ng0997-114 · Cited by 71 · see citing works
Self-citationLung Cancer Patients Have Increased 8‐Hydroxydeoxyguanosine Levels in Peripheral Lung Tissue DNA
Inoue, M., Osaki, T., Noguchi, M., Hirohashi, S., Yasumoto, K., & Kasai, H. (1998) · Japanese Journal of Cancer Research · doi:10.1111/j.1349-7006.1998.tb03272.x · Cited by 64 · see citing works
Mammalian Ogg1/Mmh gene plays a major role in repair of the 8-hydroxyguanine lesion in DNA
Nishimura, S. (2001) · Progress in nucleic acid research and molecular biology · doi:10.1016/s0079-6603(01)68093-0 · Cited by 30 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Krokan, H. E., & Bjoras, M. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a012583 · Cited by 1,322 · see citing works
Base-excision repair of oxidative DNA damage
David, S. S., O'Shea, V. L., & Kundu, S. (2007) · Nature · doi:10.1038/nature05978 · Cited by 1,238 · see citing works
Trends in oxidative aging theories
Muller, F. L., Lustgarten, M. S., Jang, Y., Richardson, A., & Van Remmen, H. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.03.034 · Cited by 1,053 · see citing works
Oxidative Stress, Mitochondrial Dysfunction, and Aging
Cui, H., Kong, Y., & Zhang, H. (2011) · Journal of Signal Transduction · doi:10.1155/2012/646354 · Cited by 1,036 · see citing works
Repair and Genetic Consequences of Endogenous DNA Base Damage in Mammalian Cells
Barnes, D. E., & Lindahl, T. (2004) · Annual Review of Genetics · doi:10.1146/annurev.genet.38.072902.092448 · Cited by 753 · see citing works
Self-citationRelationships among smoking, oxidative stress, inflammation, macromolecular damage, and cancer
Caliri, A. W., Tommasi, S., & Nia, A. B. (2021) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2021.108365 · Cited by 689 · see citing works
Base excision repair of oxidative DNA damage and association with cancer and aging
Maynard, S., Schurman, S. H., Harboe, C., de Souza-Pinto, N. C., & Bohr, V. A. (2008) · Carcinogenesis · doi:10.1093/carcin/bgn250 · Cited by 685 · see citing works
Robertson, A. B., Klungland, A., Rognes, T., & Leiros, I. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-8736-z · Cited by 652 · see citing works
DNA‐damage repair; the good, the bad, and the ugly
Hakem, R. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.15 · Cited by 547 · see citing works
Peto's Paradox: evolution's prescription for cancer prevention
Caulin, A. F., & Maley, C. C. (2011) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2011.01.002 · Cited by 384 · see citing works
The mechanics of base excision repair, and its relationship to aging and disease
WILSONIII, D., & Bohr, V. A. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.10.017 · Cited by 342 · see citing works
Role of oxidatively induced DNA lesions in human pathogenesis
Sedelnikova, O. A., Redon, C. E., Dickey, J. S., Nakamura, A., Georgakilas, A. G., & Bonner, W. M. (2010) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2009.12.005 · Cited by 339 · see citing works
Base excision repair and cancer
Wallace, S. S., Murphy, D. L., & Sweasy, J. B. (2012) · Cancer Letters · doi:10.1016/j.canlet.2011.12.038 · Cited by 329 · see citing works
8-Oxoguanine: from oxidative damage to epigenetic and epitranscriptional modification
Hahm, J. Y., Park, J., Jang, E.-S., & Chi, S. W. (2022) · Experimental & Molecular Medicine · doi:10.1038/s12276-022-00822-z · Cited by 337 · see citing works
Oxidatively induced DNA damage: Mechanisms, repair and disease
Dizdaroğlu, M. (2012) · Cancer Letters · doi:10.1016/j.canlet.2012.01.016 · Cited by 296 · see citing works
Targeted and Persistent 8-Oxoguanine Base Damage at Telomeres Promotes Telomere Loss and Crisis
Fouquerel, E., Barnes, R. P., Uttam, S., Watkins, S. C., Bruchez, M. P., & Opresko, P. L. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.04.024 · Cited by 275 · see citing works
Mutagenesis and carcinogenesis caused by the oxidation of nucleic acids
Nakabeppu, Y., Sakumi, K., Sakamoto, K., Tsuchimoto, D., Tsuzuki, T., & Nakatsu, Y. (2006) · Biological Chemistry · doi:10.1515/bc.2006.050 · Cited by 255 · see citing works
Oxidatively induced DNA damage and its repair in cancer
Dizdaroğlu, M. (2014) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2014.11.002 · Cited by 254 · see citing works
Nakabeppu, Y. (2014) · International Journal of Molecular Sciences · doi:10.3390/ijms150712543 · Cited by 206 · see citing works
Paz-Elizur, T., Sevilya, Z., Leitner‐Dagan, Y., Elinger, D., Roisman, L. C., & Livneh, Z. (2008) · Cancer Letters · doi:10.1016/j.canlet.2008.02.032 · Cited by 202 · see citing works
Eukaryotic Base Excision Repair: New Approaches Shine Light on Mechanism
Beard, W. A., Horton, J. K., Prasad, R., & Wilson, S. H. (2019) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-013118-111315 · Cited by 204 · see citing works
Characterization of Oxidative Guanine Damage and Repair in Mammalian Telomeres
Wang, Z., Rhee, D. B., Lü, J., Bohr, C. T., Fang, Z., Vallabhaneni, H., de Souza-Pinto, N. C., & Liu, Y. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1000951 · Cited by 192 · see citing works
MUTYH-associated polyposis (MAP)
Nielsen, M., Morreau, H. M., Vasen, H. F. A., & Hes, F. J. (2010) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2010.05.011 · Cited by 191 · see citing works
Not breathing is not an option: How to deal with oxidative DNA damage
Markkanen, E. (2017) · DNA repair · doi:10.1016/j.dnarep.2017.09.007 · Cited by 192 · see citing works
DeBalsi, K. L., Hoff, K. E., & Copeland, W. C. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2016.04.006 · Cited by 180 · see citing works
8-oxoguanine causes spontaneous de novo germline mutations in mice
Ohno, M., Sakumi, K., Fukumura, R., Furuichi, M., Iwasaki, Y., Hokama, M., Ikemura, T., Tsuzuki, T., Gondo, Y., & Nakabeppu, Y. (2014) · Scientific Reports · doi:10.1038/srep04689 · Cited by 177 · see citing works
DNA replication fidelity and cancer
Preston, B. D., Albertson, T. M., & Herr, A. J. (2010) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2010.10.009 · Cited by 160 · see citing works
Boiteux, S., Coste, F., & Castaing, B. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.11.042 · Cited by 161 · see citing works
Russo, M. T., Luca, G. D., Degan, P., Parlanti, E., Eugenia Dogliotti, Y., Barnes, D. E., Lindahl, T. L., Yang, H., Miller, J. H., & Bignami, M. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-0355 · Cited by 160 · see citing works
Self-citationRepair of Oxidative DNA Damage and Cancer: Recent Progress in DNA Base Excision Repair
Scott, T. L., Rangaswamy, S., Wicker, C. A., & Izumi, T. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5529 · Cited by 156 · see citing works
Oxidation Status of Human OGG1-S326C Polymorphic Variant Determines Cellular DNA Repair Capacity
Bravard, A., Vacher, M., Moritz, E., Vaslin, L., Hall, J. A., Epe, B., & Radicella, J. P. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-3943 · Cited by 151 · see citing works
Oxidative damage to purines in DNA: Role of mammalian Ogg1
Klungland, A., & Bjelland, S. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.10.012 · Cited by 150 · see citing works
8-Oxoguanine causes neurodegeneration during MUTYH-mediated DNA base excision repair
Sheng, Z., Oka, S., Tsuchimoto, D., Abolhassani, N., Nomaru, H., Sakumi, K., Yamada, H., & Nakabeppu, Y. (2012) · Journal of Clinical Investigation · doi:10.1172/jci65053 · Cited by 146 · see citing works
MUTYH-Null Mice Are Susceptible to Spontaneous and Oxidative Stress–Induced Intestinal Tumorigenesis
Sakamoto, K., Tominaga, Y., Yamauchi, K., Nakatsu, Y., Sakumi, K., Yoshiyama, K., Egashira, A., Kura, S., Yao, T., Tsuneyoshi, M., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-4802 · Cited by 141 · see citing works
Base Excision Repair and its Role in Maintaining Genome Stability
Baute, J., & Depicker, A. (2008) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409230802309905 · Cited by 139 · see citing works
Pathways for repairing and tolerating the spectrum of oxidative DNA lesions
Berquist, B. R., & Wilson, D. M. (2012) · Cancer Letters · doi:10.1016/j.canlet.2012.02.001 · Cited by 136 · see citing works
Oxidative stress and 8-oxoguanine repair are enhanced in colon adenoma and carcinoma patients
Obtułowicz, T., Swoboda, M., Speina, E., Gackowski, D., Różalski, R., Siomek, A., Janik, J., Janowska, B., Cieśla, J., Jawień, A., et al. (2010) · Mutagenesis · doi:10.1093/mutage/geq028 · Cited by 136 · see citing works
Hollander, M. C., Philburn, R. T., Patterson, A. D., Velasco-Miguel, S., Friedberg, E. C., Linnoila, R. I., & Fornace, A. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503133102 · Cited by 135 · see citing works
Dimerization and opposite base-dependent catalytic impairment of polymorphic S326C OGG1 glycosylase
Hill, J. W. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl060 · Cited by 130 · see citing works
Base Excision Repair: Mechanisms and Impact in Biology, Disease, and Medicine
Gohil, D., Sarker, A. H., & Roy, R. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241814186 · Cited by 136 · see citing works
Hansen, R. D., Sæbø, M., Skjelbred, C. F., Nexø, B. A., Hagen, P. C., Bock, G., Lothe, I. M. B., Johnson, E., Aase, S., Hansteen, I., et al. (2005) · Cancer Letters · doi:10.1016/j.canlet.2005.04.019 · Cited by 128 · see citing works
Chan, M. K., Ocampo-Hafalla, M. T., Vartanian, V. L., Jaruga, P., Kırkalı, G., Koenig, K. L., Brown, S. M., Lloyd, R. S., Dizdaroğlu, M., & Teebor, G. W. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.03.001 · Cited by 124 · see citing works
Knasmüller, S., Nersesyan, A. K., Mišík, M., Gerner, C., Mikulits, W., Ehrlich, V. A., Hoelzl, C., Szakmary, A., & Wagner, K. (2008) · British Journal Of Nutrition · doi:10.1017/s0007114508965752 · Cited by 124 · see citing works
The role of melatonin, a multitasking molecule, in retarding the processes of ageing
Majidinia, M., Reiter, R. J., Shakouri, S. K., & Yousefi, B. (2018) · Ageing Research Reviews · doi:10.1016/j.arr.2018.07.010 · Cited by 123 · see citing works
DNA Oxidation and Excision Repair Pathways
Lee, T.-H., & Kang, T.-H. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20236092 · Cited by 116 · see citing works
Poly(ADP-ribose) Polymerase 1 (PARP-1) Binds to 8-Oxoguanine-DNA Glycosylase (OGG1)
Hooten, N. N., Kompaniez, K., Barnes, J., Lohani, A., & Evans, M. K. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.255869 · Cited by 116 · see citing works
Oxidative Stress, Mitochondrial Dysfunction and the Mitochondria Theory of Aging
Kong, Y., Trabucco, S. E., & Zhang, H. (2014) · Interdisciplinary topics in gerontology and geriatrics · doi:10.1159/000358901 · Cited by 112 · see citing works
Huang, M., & Kolodner, R. D. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.02.008 · Cited by 111 · see citing works
Base excision repair, aging and health span
Xu, G., Herzig, M. C. S., Rotrekl, V., & Walter, C. A. (2008) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2008.03.001 · Cited by 110 · see citing works
The DNA Damage Response and Inflammation in Cancer
Klapp, V., Álvarez-Abril, B., Leuzzi, G., Kroemer, G., Ciccia, A., & Galluzzi, L. (2023) · Cancer Discovery · doi:10.1158/2159-8290.cd-22-1220 · Cited by 110 · see citing works
Neven, K. Y., Saenen, N. D., Tarantini, L., Janssen, B. G., Lefebvre, W., Vanpoucke, C., Bollati, V., & Nawrot, T. S. (2018) · The Lancet Planetary Health · doi:10.1016/s2542-5196(18)30049-4 · Cited by 103 · see citing works
DNA Repair and Cell Cycle Control Genes and the Risk of Young-Onset Lung Cancer
Landi, S., Gemignani, F., Canzian, F., Gaborieau, V., Barale, R., Landi, D., Szeszenia‐Dabrowska, N., Zaridze, D. G., Lissowska, J., Rudnai, P., et al. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-1039 · Cited by 103 · see citing works
Mazzei, F., Viel, A., & Bignami, M. (2013) · Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis · doi:10.1016/j.mrfmmm.2013.03.003 · Cited by 95 · see citing works
Significance of error‐avoiding mechanisms for oxidative DNA damage in carcinogenesis
Tsuzuki, T., Nakatsu, Y., & Nakabeppu, Y. (2007) · Cancer Science · doi:10.1111/j.1349-7006.2007.00409.x · Cited by 98 · see citing works
Oxidized Base Damage and Single-Strand Break Repair in Mammalian Genomes
Hegde, M. L., Izumi, T., & MITRA, S. P. (2012) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-387665-2.00006-7 · Cited by 97 · see citing works
Different DNA repair strategies to combat the threat from 8-oxoguanine
Russo, M. T., Luca, G. D., Degan, P., & Bignami, M. (2006) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2006.03.007 · Cited by 95 · see citing works
Mechanism of oxidative DNA damage repair and relevance to human pathology
D’Errico, M., Parlanti, E., & Eugenia Dogliotti, Y. (2007) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2007.10.003 · Cited by 91 · see citing works
Nohmi, T., Kim, S.-R., & Yamada, M. (2005) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2005.03.033 · Cited by 89 · see citing works
Gorini, F., Scala, G., Cooke, M. S., Majello, B., & Amente, S. (2020) · DNA repair · doi:10.1016/j.dnarep.2020.103027 · Cited by 88 · see citing works
AlkB Homologue 2–Mediated Repair of Ethenoadenine Lesions in Mammalian DNA
Ringvoll, J., Moen, M. N., Nordstrand, L. M., Meira, L. B., Pang, B., Bekkelund, A., Dedon, P. C., Bjelland, S., Samson, L. D., Falnes, P. Ø., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0796 · Cited by 87 · see citing works
Oka, S., & Nakabeppu, Y. (2011) · Cancer Science · doi:10.1111/j.1349-7006.2011.01869.x · Cited by 84 · see citing works
NTHL1 and MUTYH polyposis syndromes: two sides of the same coin?
Weren, R. D. A., Ligtenberg, M. J. L., van Kessel, A. G., de Voer, R. M., Hoogerbrugge, N., & Kuiper, R. P. (2017) · The Journal of Pathology · doi:10.1002/path.5002 · Cited by 84 · see citing works
Touati, E., Michel, V., Thiberge, J., Avé, P., Huerre, M., Bourgade, F., Klungland, A., & Labigne-Roussel, A. (2006) · Helicobacter · doi:10.1111/j.1523-5378.2006.00442.x · Cited by 82 · see citing works
On the epigenetic role of guanosine oxidation
Giorgio, M., Dellino, G. I., Gambino, V., Roda, N., & Pelicci, P. G. (2019) · Redox Biology · doi:10.1016/j.redox.2019.101398 · Cited by 81 · see citing works
Oxidized guanine lesions and hOgg1 activity in lung cancer
Mambo, E., Chatterjee, A., de Souza-Pinto, N. C., Mayard, S., Hogue, B. A., Hoque, M. O., Dizdaroğlu, M., Bohr, V. A., & Sidransky, D. (2005) · Oncogene · doi:10.1038/sj.onc.1208669 · Cited by 78 · see citing works
MUTYH DNA glycosylase: the rationale for removing undamaged bases from the DNA
Markkanen, E., Dorn, J., & Hübscher, U. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00018 · Cited by 77 · see citing works
Is Base Excision Repair a Tumor Suppressor Mechanism?
Sweasy, J. B., Lang, T., & DiMaio, D. (2006) · Cell Cycle · doi:10.4161/cc.5.3.2414 · Cited by 77 · see citing works
Widespread transcriptional gene inactivation initiated by a repair intermediate of 8-oxoguanine
Allgayer, J., Kitsera, N., Bartelt, S., Epe, B., & Khobta, A. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw473 · Cited by 77 · see citing works
A MUTYH germline mutation is associated with small intestinal neuroendocrine tumors
Dumanski, J. P., Rasi, C., Björklund, P., Davies, H., Ali, A. S., Grönberg, M., Welin, S., Sørbye, H., Grønbæk, H., Cunningham, J. L., et al. (2017) · Endocrine Related Cancer · doi:10.1530/erc-17-0196 · Cited by 77 · see citing works
Batra, V. K., Shock, D. D., Beard, W. A., McKenna, C. E., & Wilson, S. H. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1112235108 · Cited by 75 · see citing works
Oxygenation of the Newborn: A Molecular Approach
Saugstad, O. D., Sejersted, Y., Solberg, R., Wollen, E. J., & Bjørås, M. (2012) · Neonatology · doi:10.1159/000337345 · Cited by 76 · see citing works
Kauppila, J. H. K., Bonekamp, N. A., Mourier, A., Isokallio, M. A., Just, A., Kauppila, T. E. S., Stewart, J. B., & Larsson, N. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky456 · Cited by 77 · see citing works
Variant base excision repair proteins: Contributors to genomic instability
Nemec, A. A., Wallace, S. S., & Sweasy, J. B. (2010) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2010.10.010 · Cited by 74 · see citing works
Phosphorylation of human oxoguanine DNA glycosylase ( -OGG1) modulates its function
Hu, J. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki636 · Cited by 74 · see citing works
Arai, T., Kelly, V. P., Minowa, O., Noda, T., & Nishimura, S. (2006) · Toxicology · doi:10.1016/j.tox.2006.01.004 · Cited by 73 · see citing works
Ferk, F., Kundi, M., Brath, H., Szekeres, T., Al-Serori, H., Mišík, M., Saiko, P., Marculescu, R., Wagner, K., & Knasmüller, S. (2017) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201700482 · Cited by 73 · see citing works
8-Oxoguanine incorporation into DNA repeats in vitro and mismatch recognition by MutS
Macpherson, P. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki813 · Cited by 73 · see citing works
Kovvuru, P., Mancilla, P. E., Shirode, A. B., Murray, T. M., Begley, T. J., & Reliene, R. (2014) · Nanotoxicology · doi:10.3109/17435390.2014.902520 · Cited by 72 · see citing works
MTH1 as a nucleotide pool sanitizing enzyme: Friend or foe?
Nakabeppu, Y., Ohta, E., & Abolhassani, N. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.11.002 · Cited by 68 · see citing works
Toward a genetics of cancer resistance
Klein, G. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811616106 · Cited by 67 · see citing works
Yasuniwa, Y., Izumi, H., Wang, K., Shimajiri, S., Sasaguri, Y., Kawai, K., Kasai, H., Shimada, T., Miyake, K., Kashiwagi, E., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015330 · Cited by 65 · see citing works
Bai, H. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki209 · Cited by 65 · see citing works
Oxidative Stress and the DNA Mismatch Repair Pathway
Brierley, D. J., & Martin, S. A. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4994 · Cited by 64 · see citing works
A Role for Oxidized DNA Precursors in Huntington's Disease–Like Striatal Neurodegeneration
Luca, G. D., Russo, M. T., Degan, P., Tiveron, C., Zijno, A., Meccia, E., Ventura, I., Mattei, E., Nakabeppu, Y., Crescenzi, M., et al. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000266 · Cited by 64 · see citing works
Robinson, P. S., Thomas, L. E., Abascal, F., Jung, H., Harvey, L. M. R., West, H. D., Ólafsson, S., Lee, B. C. H., Coorens, T. H. H., Lee-Six, H., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-31341-0 · Cited by 63 · see citing works
OGG1 expression and OGG1 Ser326Cys polymorphism and risk of lung cancer in a prospective study
Hatt, L., Loft, S. H., Risom, L., Möller, P., Sørensen, M., Raaschou‐Nielsen, O., Overvad, K., Tjønneland, A. M., & Vogel, U. B. (2007) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2007.11.002 · Cited by 63 · see citing works
Eiberger, W., Volkmer, B., Amouroux, R., Dhérin, C., Radicella, J. P., & Epe, B. (2008) · DNA repair · doi:10.1016/j.dnarep.2008.03.002 · Cited by 60 · see citing works
DNA Damage Induced by Hyperoxia
Barker, G. F., Manzo, N. D., Cotich, K. L., Shone, R., & Waxman, A. B. (2006) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2005-0340oc · Cited by 57 · see citing works
Futile short-patch DNA base excision repair of adenine:8-oxoguanine mispair
Hashimoto, K. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh909 · Cited by 57 · see citing works
Mechanisms of Base Substitution Mutagenesis in Cancer Genomes
Bacolla, A., Cooper, D. N., & Vásquez, K. M. (2014) · Genes · doi:10.3390/genes5010108 · Cited by 55 · see citing works
Oxidatively damaged DNA and its repair in colon carcinogenesis
Tudek, B., & Speina, E. (2012) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2012.04.003 · Cited by 55 · see citing works
Dutta, A., Yang, C., Sengupta, S., MITRA, S. P., & Hegde, M. L. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1820-z · Cited by 55 · see citing works
Arai, T., Fukae, J., Hatano, T., Kubo, S.-I., Ohtsubo, T., Nakabeppu, Y., Mori, H., Mizuno, Y., & Hattori, N. (2006) · Acta Neuropathologica · doi:10.1007/s00401-006-0081-9 · Cited by 54 · see citing works
de Padula, M. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh831 · Cited by 55 · see citing works
Ming, X., Matter, B. A., Song, M., Veliath, E., Shanley, R., Jones, R. A., & Tretyakova, N. Y. (2014) · Journal of the American Chemical Society · doi:10.1021/ja411636j · Cited by 54 · see citing works
The Evolution of Human Cancer Gene Duplications across Mammals
Tollis, M., Schneider‐Utaka, A. K., & Maley, C. C. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msaa125 · Cited by 56 · see citing works
Russo, M. T., Luca, G. D., Casorelli, I., Degan, P., Molatore, S., Barone, F., Mazzei, F., Pannellini, T., Musiani, P., & Bignami, M. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-3292 · Cited by 52 · see citing works
Frataxin Deficiency Promotes Excess Microglial DNA Damage and Inflammation that Is Rescued by PJ34
Shen, Y., McMackin, M. Z., Shan, Y., Raetz, A. G., David, S. S., & Cortopassi, G. A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0151026 · Cited by 52 · see citing works
Base Excision Repair in the Immune System: Small DNA Lesions With Big Consequences
Stratigopoulou, M., van Dam, T. P., & Guikema, J. E. J. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01084 · Cited by 51 · see citing works
The role of MYH and microsatellite instability in the development of sporadic colorectal cancer
Colebatch, A. J., Hitchins, M. P., Williams, R., Meagher, A. P., Hawkins, N. J., & Ward, R. L. (2006) · British Journal of Cancer · doi:10.1038/sj.bjc.6603421 · Cited by 52 · see citing works
- Authors
- Xie, Y., Yang, H., Cunanan, C., Okamoto, K., Shibata, D., Pan, J., Barnes, D. E., Lindahl, T., McIlhatton, M., Fishel, R., & Miller, J. H.
- Affiliations
- University of California, Los Angeles (US)
- University of Southern California (US)
- Cancer Research UK (GB)
- Thomas Jefferson University (US)
- Venue
- Cancer Research
- Published
- 2004-05-01
- Volume
- 64
- Issue
- 9
- Pages
- 3096-3102
- ISSN
- 0008-5472 (ISSN-L)
- 1538-7445
- OpenAlex
- W2137854060
- Cited by
- 291
- References
- 38
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 7 · 2023: 4 · 2022: 8 · 2021: 15 · 2020: 10 · 2019: 16 · 2018: 11 · 2017: 10 · 2016: 11 · 2015: 11 · 2014: 14 · 2013: 15 · 2012: 17
- FWCI
- 7.22
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cancer Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ca085952-04)
- National Cancer Institute (CA 85952)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Carcinogens and Genotoxicity Assessment
- Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
- Keywords
- MUTYH, OGG1, oxidative DNA damage, lung cancer, cancer susceptibility, MutY, formamidopyrimidine-DNA glycosylase, MSH2, DNA mismatch repair, oxidative DNA damage repair, mutagenesis, lymphoma, ovarian neoplasms, reactive oxygen species, mouse model
- MeSH terms
- Animals, Codon, DNA Damage, DNA-Binding Proteins, Female, Humans, Lung Neoplasms, Lymphoma, Male, Mice, Inbred C57BL, Ovarian Neoplasms, Oxidation-Reduction, Proto-Oncogene Proteins, Genes, ras, Point Mutation, Mice, Knockout, Genetic Predisposition to Disease, DNA Glycosylases, Mice, MutS Homolog 2 Protein
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
