Current Gerontology and Geriatrics Research
Volume 2011 (2011), Article ID 859415, 15 pages
http://dx.doi.org/10.1155/2011/859415
Metabolism, Genomics, and DNA Repair in the Mouse Aging Liver
1Centre de Recherche en Cancérologie de l'Université Laval, Hôpital Hôtel-Dieu de Québec, 9 McMahon Street Quebec City, QC, Canada G1R 2J6
2Departmento de Bioquímica, Instituto de Química, Universiade de São Paulo, Avenue Prof. Lineu Prestes, 748, 05508-900 São Paulo, SP, Brazil
3Laboratory of Molecular Gerontology, National Institute on Aging, National Institutes of Health, 5600 Nathan Shock Drive, Baltimore, MD 21224, USA
Received 27 December 2010; Accepted 11 February 2011
Academic Editor: Victoria Cogger
Copyright © 2011 Michel Lebel et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Linked References
- D. G. Le Couteur, A. Warren, V. C. Cogger et al., “Old age and the hepatic sinusoid,” Anatomical Record, vol. 291, no. 6, pp. 672–683, 2008. View at Publisher · View at Google Scholar · View at Scopus
- S. N. Hilmer, V. C. Cogger, R. Fraser, A. J. McLean, D. Sullivan, and D. G. Le Couteur, “Age-related changes in the hepatic sinusoidal endothelium impede lipoprotein transfer in the rat,” Hepatology, vol. 42, no. 6, pp. 1349–1354, 2005. View at Publisher · View at Google Scholar · View at Scopus
- K. Turnheim, “When drug therapy gets old: pharmacokinetics and pharmacodynamics in the elderly,” Experimental Gerontology, vol. 38, no. 8, pp. 843–853, 2003. View at Publisher · View at Google Scholar · View at Scopus
- R. M. Wright and R. W. Warpula, “Geriatric pharmacology: safer prescribing for the elderly patient,” Journal of the American Podiatric Medical Association, vol. 94, no. 2, pp. 90–97, 2004. View at Google Scholar · View at Scopus
- S. X. Cao, J. M. Dhahbi, P. L. Mote, and S. R. Spindler, “Genomic profiling of short- and long-term caloric restriction effects in the liver of aging mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 19, pp. 10630–10635, 2001. View at Publisher · View at Google Scholar · View at Scopus
- D. L. Smith Jr., T. R. Nagy, and D. B. Allison, “Calorie restriction: what recent results suggest for the future of ageing research,” European Journal of Clinical Investigation, vol. 40, no. 5, pp. 440–450, 2010. View at Publisher · View at Google Scholar · View at Scopus
- L. J. Niedernhofer, G. A. Garinis, A. Raams et al., “A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis,” Nature, vol. 444, no. 7122, pp. 1038–1043, 2006. View at Publisher · View at Google Scholar · View at Scopus
- P. Alexander, “The role of DNA lesions in the processes leading to aging in mice,” Symposia of the Society for Experimental Biology, vol. 21, pp. 29–50, 1967. View at Google Scholar · View at Scopus
- J. C. Mirsalis, G. S. Provost, C. D. Matthews et al., “Induction of hepatic mutations in lacI transgenic mice,” Mutagenesis, vol. 8, no. 3, pp. 265–271, 1993. View at Google Scholar · View at Scopus
- G. R. Stuart and B. W. Glickman, “Through a glass, darkly: reflections of mutation from lacI transgenic mice,” Genetics, vol. 155, no. 3, pp. 1359–1367, 2000. View at Google Scholar · View at Scopus
- H. J. Jorg-Martus, M. E. T. Dolle, J. A. Gossen, M. E. T. I. Boerrigter, and J. Vijg, “Use of transgenic mouse models for studying somatic mutations in aging,” Mutation Research, vol. 338, no. 1–6, pp. 203–213, 1995. View at Publisher · View at Google Scholar · View at Scopus
- G. R. Stuart, Y. Oda, J. G. De Boer, and B. W. Glickman, “Mutation frequency and specificity with age in liver, bladder and brain of lacI transgenic mice,” Genetics, vol. 154, no. 3, pp. 1291–1300, 2000. View at Google Scholar · View at Scopus
- J. A. Gossen, W. J. F. De Leeuw, C. H. T. Tan et al., “Efficient rescue of integrated shuttle vectors from transgenic mice: a model for studying mutations in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 20, pp. 7971–7975, 1989. View at Google Scholar · View at Scopus
- R. R. Swiger, B. Myhr, and J. D. Tucker, “The LacZ transgene in Muta(TM)Mouse maps to chromosome 3,” Mutation Research, vol. 325, no. 4, pp. 145–148, 1994. View at Publisher · View at Google Scholar · View at Scopus
- M. E. T. Dolle, H. Giese, C. L. Hopkins, H. J. Martus, J. M. Hausdorff, and J. Vijg, “Rapid accumulation of genome rearrangements in liver but not in brain of old mice,” Nature Genetics, vol. 17, no. 4, pp. 431–434, 1997. View at Google Scholar · View at Scopus
- M. E. T. I. Boerrigter, M. E. T. Dolle, H. J. Martus, J. A. Gossen, and J. Vijg, “Plasmid-based transgenic mouse model for studying in vivo mutations,” Nature, vol. 377, no. 6550, pp. 657–659, 1995. View at Google Scholar · View at Scopus
- J. Vijg and M. E. T. Dolle, “Large genome rearrangements as a primary cause of aging,” Mechanisms of Ageing and Development, vol. 123, no. 8, pp. 907–915, 2002. View at Publisher · View at Google Scholar · View at Scopus
- S. Gupta, “Hepatic polyploidy and liver growth control,” Seminars in Cancer Biology, vol. 10, no. 3, pp. 161–171, 2000. View at Publisher · View at Google Scholar · View at Scopus
- S. Celton-Morizur, G. Merlen, D. Couton, and C. Desdouets, “Polyploidy and liver proliferation: central role of insulin signaling,” Cell Cycle, vol. 9, no. 3, pp. 460–466, 2010. View at Google Scholar · View at Scopus
- G. R. Gorla, H. Malhi, and S. Gupta, “Polyploidy associated with oxidative injury attenuates proliferative potential of cells,” Journal of Cell Science, vol. 114, no. 16, pp. 2943–2951, 2001. View at Google Scholar · View at Scopus
- D. Harman, “Aging: a theory based on free radical and radiation chemistry,” Journal of Gerontology, vol. 11, no. 3, pp. 298–300, 1956. View at Google Scholar · View at Scopus
- M. Meydani, R. D. Lipman, S. N. Han et al., “The effect of long-term dietary supplementation with antioxidants,” Annals of the New York Academy of Sciences, vol. 854, pp. 352–360, 1998. View at Publisher · View at Google Scholar · View at Scopus
- M. M. Page, E. L. Robb, K. D. Salway, and J. A. Stuart, “Mitochondrial redox metabolism: aging, longevity and dietary effects,” Mechanisms of Ageing and Development, vol. 131, no. 4, pp. 242–252, 2010. View at Publisher · View at Google Scholar · View at Scopus
- A. Boveris, “Mitochondrial production of superoxide radical and hydrogen peroxide,” Advances in Experimental Medicine and Biology, vol. 78, pp. 67–82, 1977. View at Google Scholar · View at Scopus
- A. J. Kowaltowski, N. C. de Souza-Pinto, R. F. Castilho, and A. E. Vercesi, “Mitochondria and reactive oxygen species,” Free Radical Biology and Medicine, vol. 47, no. 4, pp. 333–343, 2009. View at Publisher · View at Google Scholar · View at Scopus
- M. Dizdaroglu, “Characterization of free radical-induced damage to DNA by the combined use of enzymatic hydrolysis and gas chromatography-mass spectrometry,” Journal of Chromatography, vol. 367, no. 2, pp. 357–366, 1986. View at Google Scholar · View at Scopus
- K. C. Cheng, D. S. Cahill, H. Kasai, S. Nishimura, and L. A. Loeb, “8-hydroxyguanine, an abundant form of oxidative DNA damage, causes G → T and A → C substitutions,” Journal of Biological Chemistry, vol. 267, no. 1, pp. 166–172, 1992. View at Google Scholar · View at Scopus
- K. A. Hill, A. Halangoda, P. W. Heinmoeller et al., “Tissue-specific time courses of spontaneous mutation frequency and deviations in mutation pattern are observed in middle to late adulthood in big blue mice,” Environmental and Molecular Mutagenesis, vol. 45, no. 5, pp. 442–454, 2005. View at Publisher · View at Google Scholar · View at Scopus
- M. E. T. Dolle, W. K. Snyder, D. B. Dunson, and J. Vijg, “Mutational fingerprints of aging,” Nucleic Acids Research, vol. 30, no. 2, pp. 545–549, 2002. View at Google Scholar · View at Scopus
- Y. Hong, R. B. Cervantes, E. Tichy, J. A. Tischfield, and P. J. Stambrook, “Protecting genomic integrity in somatic cells and embryonic stem cells,” Mutation Research, vol. 614, no. 1-2, pp. 48–55, 2007. View at Publisher · View at Google Scholar · View at Scopus
- L. Mikkelsen, K. Bialkowski, L. Risom, M. Løhr, S. Loft, and P. Møller, “Aging and defense against generation of 8-oxo-7,8-dihydro-2′-deoxyguanosine in DNA,” Free Radical Biology and Medicine, vol. 47, no. 5, pp. 608–615, 2009. View at Publisher · View at Google Scholar · View at Scopus
- R. K. Zahn, G. Zahn-Daimler, S. Ax et al., “DNA damage susceptibility and repair in correlation to calendric age and longevity,” Mechanisms of Ageing and Development, vol. 119, no. 3, pp. 101–112, 2000. View at Publisher · View at Google Scholar · View at Scopus
- N. E. López-Diazguerrero, A. Luna-López, M. C. Gutiérrez-Ruiz, A. Zentella, and M. Königsberg, “Susceptibility of DNA to oxidative stressors in young and aging mice,” Life Sciences, vol. 77, no. 22, pp. 2840–2854, 2005. View at Publisher · View at Google Scholar · View at Scopus
- M. L. Hamilton, H. Van Remmen, J. A. Drake et al., “Does oxidative damage to DNA increase with age?” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 18, pp. 10469–10474, 2001. View at Publisher · View at Google Scholar · View at Scopus
- C. S. Fu, S. B. Harris, P. Wilhelmi, and R. L. Walford, “Lack of effect of age and dietary restriction on DNA single-stranded breaks in brain, liver, and kidney of (C3H x C57BL/10)F1 mice,” Journals of Gerontology, vol. 46, no. 2, pp. B78–B80, 1991. View at Google Scholar · View at Scopus
- R. M. Anson, S. Sentürker, M. Dizdaroglu, and V. A. Bohr, “Measurement of oxidatively induced base lesions in liver from Wistar rats of different ages,” Free Radical Biology and Medicine, vol. 27, no. 3-4, pp. 456–462, 1999. View at Publisher · View at Google Scholar · View at Scopus
- A. Collins, C. Gedik, N. Vaughan et al., “Comparative analysis of baseline 8-oxo-7,8-dihydroguanine in mammalian cell DNA, by different methods in different laboratories: an approach to consensus,” Carcinogenesis, vol. 23, no. 12, pp. 2129–2133, 2002. View at Publisher · View at Google Scholar · View at Scopus
- J. Hu, N. C. De Souza-Pinto, K. Haraguchi et al., “Repair of formamidopyrimidines in DNA involves different glycosylases: role of the OGG1, NTH1, and NEIL1 enzymes,” Journal of Biological Chemistry, vol. 280, no. 49, pp. 40544–40551, 2005. View at Publisher · View at Google Scholar · View at Scopus
- H. J. Helbock, K. B. Beckman, M. K. Shigenaga et al., “DNA oxidation matters: the HPLC-electrochemical detection assay of 8-oxo-deoxyguanosine and 8-oxo-guanine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 1, pp. 288–293, 1998. View at Google Scholar · View at Scopus
- C. W. Greider, “Telomere length regulation,” Annual Review of Biochemistry, vol. 65, pp. 337–365, 1996. View at Google Scholar · View at Scopus
- G. M. Martin, “Genetic and environmental modulations of chromosomal stability: their roles in aging and oncogenesis,” Annals of the New York Academy of Sciences, vol. 621, pp. 401–417, 1991. View at Google Scholar · View at Scopus
- S. Petersen, G. Saretzki, and T. Von Zglinicki, “Preferential accumulation of single-stranded regions in telomeres of human fibroblasts,” Experimental Cell Research, vol. 239, no. 1, pp. 152–160, 1998. View at Publisher · View at Google Scholar · View at Scopus
- Z. Wang, D. B. Rhee, J. Lu et al., “Characterization of oxidative guanine damage and repair in mammalian telomeres,” PLoS Genetics, vol. 6, no. 5, Article ID e1000951, 2010. View at Publisher · View at Google Scholar · View at Scopus
- P. L. Opresko, J. Fan, S. Danzy, D. M. Wilson, and V. A. Bohr, “Oxidative damage in telomeric DNA disrupts recognition by TRF1 and TRF2,” Nucleic Acids Research, vol. 33, no. 4, pp. 1230–1239, 2005. View at Publisher · View at Google Scholar · View at Scopus
- G. Z. Li, M. S. Eller, R. Firoozabadi, and B. A. Gilchrest, “Evidence that exposure of the telomere 3′ overhang sequence induces senescence,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 2, pp. 527–531, 2003. View at Publisher · View at Google Scholar · View at Scopus
- E. Sahin, S. Colla, M. Liesa et al., “Telomere dysfunction induces metabolic and mitochondrial compromise,” Nature, vol. 470, no. 7334, pp. 359–365, 2011. View at Publisher · View at Google Scholar
- C. Wang, D. Jurk, M. Maddick, G. Nelson, C. Martin-ruiz, and T. Von Zglinicki, “DNA damage response and cellular senescence in tissues of aging mice,” Aging Cell, vol. 8, no. 3, pp. 311–323, 2009. View at Publisher · View at Google Scholar · View at Scopus
- J. W. Gaubatz and B. H. Tan, “Introduction, distribution, and removal of 7-methylguanine in different liver chromatin fractions of young and old mice,” Mutation Research, vol. 375, no. 1, pp. 25–35, 1997. View at Publisher · View at Google Scholar · View at Scopus
- R. K. Zahn, G. Zahn-Daimler, S. Ax, M. Hosokawa, and T. Takeda, “Assessment of DNA-protein crosslinks in the course of aging in two mouse strains by use of a modified alkaline filter elution applied to whole tissue samples,” Mechanisms of Ageing and Development, vol. 108, no. 2, pp. 99–112, 1999. View at Publisher · View at Google Scholar · View at Scopus
- M. E. T. I. Boerrigter, J. Y. Wei, and J. Vijg, “Induction and repair of benzo[a]pyrene-DNA adducts in C57BL/6 and BALB/c mice: association with aging and longevity,” Mechanisms of Ageing and Development, vol. 82, no. 1, pp. 31–50, 1995. View at Publisher · View at Google Scholar · View at Scopus
- J. E. A. Leakey, H. C. Cunny, J. Bazare et al., “Effects of aging and caloric restriction on hepatic drug metabolizing enzymes in the Fisher 344 rat. I: the cytochrome P-450 dependent monooxygenase system,” Mechanisms of Ageing and Development, vol. 48, no. 2, pp. 145–155, 1989. View at Google Scholar · View at Scopus
- D. C. Cabelof, J. J. Raffoul, S. Yanamadala, C. Ganir, Z. Guo, and A. R. Heydari, “Attenuation of DNA polymerase β-dependent base excision repair and increased DMS-induced mutagenicity in aged mice,” Mutation Research, vol. 500, no. 1-2, pp. 135–145, 2002. View at Google Scholar · View at Scopus
- R. K. Singhal, R. Prasad, and S. H. Wilson, “DNA polymerase β conducts the gap-filling step in uracil-initiated base excision repair in a bovine testis nuclear extract,” Journal of Biological Chemistry, vol. 270, no. 2, pp. 949–957, 1995. View at Publisher · View at Google Scholar · View at Scopus
- H. Nilsen and H. E. Krokan, “Base excision repair in a network of defence and tolerance,” Carcinogenesis, vol. 22, no. 7, pp. 987–998, 2001. View at Google Scholar · View at Scopus
- A. JA. Podlutsky, I. I. Dianova, V. N. Podust, V. A. Bohr, and G. L. Dianov, “Human DNA polymerase β initiates DNA synthesis during long-patch repair of reduced AP sites in DNA,” EMBO Journal, vol. 20, no. 6, pp. 1477–1482, 2001. View at Publisher · View at Google Scholar · View at Scopus
- A. Klungland and T. Lindahl, “Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1),” EMBO Journal, vol. 16, no. 11, pp. 3341–3348, 1997. View at Publisher · View at Google Scholar · View at Scopus
- B. Pascucci, M. Stucki, Z. O. Jónsson, E. Dogliotti, and U. Hübscher, “Long patch base excision repair with purified human proteins. DNA ligase I as patch size mediator for DNA polymerases δ and ε,” Journal of Biological Chemistry, vol. 274, no. 47, pp. 33696–33702, 1999. View at Publisher · View at Google Scholar · View at Scopus
- M. Sukhanova, S. Khodyreva, and O. Lavrik, “Poly(ADP-ribose) polymerase 1 regulates activity of DNA polymerase β in long patch base excision repair,” Mutation Research, vol. 685, no. 1-2, pp. 80–89, 2010. View at Publisher · View at Google Scholar · View at Scopus
- N. C. De Souza-Pinto, B. A. Hogue, and V. A. Bohr, “DNA repair and aging in mouse liver: 8-oxodG glycosylase activity increase in mitochondrial but not in nuclear extracts,” Free Radical Biology and Medicine, vol. 30, no. 8, pp. 916–923, 2001. View at Publisher · View at Google Scholar · View at Scopus
- J. W. Gaubatz and B. H. Tan, “Aging affects the levels of DNA damage in postmitotic cells,” Annals of the New York Academy of Sciences, vol. 719, pp. 97–107, 1994. View at Google Scholar · View at Scopus
- G. W. Intano, E. J. Cho, C. A. McMahan, and C. A. Walter, “Age-related base excision repair activity in mouse brain and liver nuclear extracts,” Journals of Gerontology A, vol. 58, no. 3, pp. 205–211, 2003. View at Google Scholar · View at Scopus
- G. Xu, M. Herzig, V. Rotrekl, and C. A. Walter, “Base excision repair, aging and health span,” Mechanisms of Ageing and Development, vol. 129, no. 7-8, pp. 366–382, 2008. View at Publisher · View at Google Scholar · View at Scopus
- N. C. Souza-Pinto, D. L. Croteau, E. K. Hudson, R. G. Hansford, and V. A. Bohr, “Age-associated increase in 8-oxo-deoxyguanosine glycosylase/AP lyase activity in rat mitochondria,” Nucleic Acids Research, vol. 27, no. 8, pp. 1935–1942, 1999. View at Publisher · View at Google Scholar · View at Scopus
- Z. M. Guo, A. Heydari, and A. Richardson, “Nucleotide excision repair of actively transcribed versus nontranscribed DNA in rat hepatocytes: effect of age and dietary restriction,” Experimental Cell Research, vol. 245, no. 1, pp. 228–238, 1998. View at Publisher · View at Google Scholar · View at Scopus
- Z. A. Medvedev, “Age changes of chromatin. A review,” Mechanisms of Ageing and Development, vol. 28, no. 2-3, pp. 139–154, 1984. View at Google Scholar · View at Scopus
- M. K. Thakur, “Age-related changes in the structure and function of chromatin: a review,” Mechanisms of Ageing and Development, vol. 27, no. 3, pp. 263–286, 1984. View at Publisher · View at Google Scholar · View at Scopus
- D. Goukassian, F. Gad, M. Yaar, M. S. Eller, U. S. Nehal, and B. A. Gilchrest, “Mechanisms and implications of the age-associated decrease in DNA repair capacity,” FASEB Journal, vol. 14, no. 10, pp. 1325–1334, 2000. View at Google Scholar · View at Scopus
- B. Schumacher, J. H. Hoeijmakers, and G. A. Garinis, “Sealing the gap between nuclear DNA damage and longevity,” Molecular and Cellular Endocrinology, vol. 299, no. 1, pp. 112–117, 2009. View at Publisher · View at Google Scholar · View at Scopus
- H. Li, J. R. Mitchell, and P. Hasty, “DNA double-strand breaks: a potential causative factor for mammalian aging?” Mechanisms of Ageing and Development, vol. 129, no. 7-8, pp. 416–424, 2008. View at Publisher · View at Google Scholar · View at Scopus
- R. Kusumoto, L. Dawut, C. Marchetti et al., “Werner protein cooperates with the XRCC4-DNA ligase IV complex in end-processing,” Biochemistry, vol. 47, no. 28, pp. 7548–7556, 2008. View at Publisher · View at Google Scholar · View at Scopus
- D. B. Lombard, K. F. Chua, R. Mostoslavsky, S. Franco, M. Gostissa, and F. W. Alt, “DNA repair, genome stability, and aging,” Cell, vol. 120, no. 4, pp. 497–512, 2005. View at Publisher · View at Google Scholar · View at Scopus
- U. Rass, S. A. Compton, J. Matos et al., “Mechanism of Holliday junction resolution by the human GEN1 protein,” Genes and Development, vol. 24, no. 14, pp. 1559–1569, 2010. View at Publisher · View at Google Scholar
- O. A. Sedelnikova, I. Horikawa, D. B. Zimonjic, N. C. Popescu, W. M. Bonner, and J. C. Barrett, “Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks,” Nature Cell Biology, vol. 6, no. 2, pp. 168–170, 2004. View at Publisher · View at Google Scholar · View at Scopus
- K. Ren and S. Peña De Ortiz, “Non-homologous DNA end joining in the mature rat brain,” Journal of Neurochemistry, vol. 80, no. 6, pp. 949–959, 2002. View at Publisher · View at Google Scholar · View at Scopus
- V. N. Vyjayanti and K. S. Rao, “DNA double strand break repair in brain: reduced NHEJ activity in aging rat neurons,” Neuroscience Letters, vol. 393, no. 1, pp. 18–22, 2006. View at Publisher · View at Google Scholar · View at Scopus
- J. H. Um, S. J. Kim, D. W. Kim et al., “Tissue-specific changes of DNA repair protein Ku and mtHSP70 in aging rats and their retardation by caloric restriction,” Mechanisms of Ageing and Development, vol. 124, no. 8-9, pp. 967–975, 2003. View at Publisher · View at Google Scholar · View at Scopus
- E. S. Han, S. G. Hilsenbeck, A. Richardson, and J. F. Nelson, “cDNA expression arrays reveal incomplete reversal of age-related changes in gene expression by calorie restriction,” Mechanisms of Ageing and Development, vol. 115, no. 3, pp. 157–174, 2000. View at Publisher · View at Google Scholar · View at Scopus
- M. J. McKay, C. Troelstra, P. Van Der Spek et al., “Sequence conservation of the rad21 Schizosaccharomyces pombe DNA double- strand break repair gene in human and mouse,” Genomics, vol. 36, no. 2, pp. 305–315, 1996. View at Publisher · View at Google Scholar · View at Scopus
- C. D. Berdanier and H. B. Everts, “Mitochondrial DNA in aging and degenerative disease,” Mutation Research, vol. 475, no. 1-2, pp. 169–184, 2001. View at Publisher · View at Google Scholar · View at Scopus
- C. Meissner, “Mutations of mitochondrial DNA—cause or consequence of the ageing process?” Zeitschrift fur Gerontologie und Geriatrie, vol. 40, no. 5, pp. 325–333, 2007. View at Publisher · View at Google Scholar · View at Scopus
- U. Lakshmipathy and C. Campbell, “Double strand break rejoining by mammalian mitochondrial extracts,” Nucleic Acids Research, vol. 27, no. 4, pp. 1198–1204, 1999. View at Publisher · View at Google Scholar · View at Scopus
- P. A. Mason, E. C. Matheson, A. G. Hall, and R. N. Lightowlers, “Mismatch repair activity in mammalian mitochondria,” Nucleic Acids Research, vol. 31, no. 3, pp. 1052–1058, 2003. View at Publisher · View at Google Scholar · View at Scopus
- N. C. de Souza-Pinto, P. A. Mason, K. Hashiguchi et al., “Novel DNA mismatch-repair activity involving YB-1 in human mitochondria,” DNA Repair, vol. 8, no. 6, pp. 704–719, 2009. View at Publisher · View at Google Scholar · View at Scopus
- M. Berneburg, Y. Kamenisch, J. Krutmann, and M. Röcken, “'To repair or not to repair—no longer a question': repair of mitochondrial DNA shielding against age and cancer,” Experimental Dermatology, vol. 15, no. 12, pp. 1005–1015, 2006. View at Publisher · View at Google Scholar · View at Scopus
- M. D. Aamann, M. M. Sorensen, C. Hvitby et al., “Cockayne syndrome group B protein promotes mitochondrial DNA stability by supporting the DNA repair association with the mitochondrial membrane,” FASEB Journal, vol. 24, no. 7, pp. 2334–2346, 2010. View at Publisher · View at Google Scholar · View at Scopus
- M. Khaidakov, R. H. Heflich, M. G. Manjanatha, M. B. Myers, and A. Aidoo, “Accumulation of point mutations in mitochondrial DNA of aging mice,” Mutation Research, vol. 526, no. 1-2, pp. 1–7, 2003. View at Publisher · View at Google Scholar · View at Scopus
- E. K. Hudson, B. A. Hogue, N. C. Souza-Pinto et al., “Age-associated change in mitochondrial DNA damage,” Free Radical Research, vol. 29, no. 6, pp. 573–579, 1998. View at Google Scholar · View at Scopus
- L. Piko, A. J. Hougham, and K. J. Bulpitt, “Studies of sequence heterogeneity of mitochondrial DNA from rat and mouse tissues: evidence for an increased frequency of deletions/additions with aging,” Mechanisms of Ageing and Development, vol. 43, no. 3, pp. 279–293, 1988. View at Google Scholar · View at Scopus
- S. M. Tanhauser and P. J. Laipis, “Multiple deletions are detectable in mitochondrial DNA of aging mice,” Journal of Biological Chemistry, vol. 270, no. 42, pp. 24769–24775, 1995. View at Publisher · View at Google Scholar · View at Scopus
- B. Szczesny, T. K. Hazra, J. Papaconstantinou, S. Mitra, and I. Boldogh, “Age-dependent deficiency in import of mitochondrial DNA glycosylases required for repair of oxidatively damaged bases,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 19, pp. 10670–10675, 2003. View at Publisher · View at Google Scholar · View at Scopus
- A. Trifunovic, A. Wredenberg, M. Falkenberg et al., “Premature ageing in mice expressing defective mitochondrial DNA polymerase,” Nature, vol. 429, no. 6990, pp. 417–423, 2004. View at Publisher · View at Google Scholar · View at Scopus
- C. C. Kujoth, A. Hiona, T. D. Pugh et al., “Medicine: mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging,” Science, vol. 309, no. 5733, pp. 481–484, 2005. View at Publisher · View at Google Scholar · View at Scopus
- A. Trifunovic, A. Hansson, A. Wredenberg et al., “Somatic mtDNA mutations cause aging phenotypes without affecting reactive oxygen species production,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 50, pp. 17993–17998, 2005. View at Publisher · View at Google Scholar · View at Scopus
- D. C. Haines, S. Chattopadhyay, and J. M. Ward, “Pathology of aging B6;129 mice,” Toxicologic Pathology, vol. 29, no. 6, pp. 653–661, 2001. View at Publisher · View at Google Scholar · View at Scopus
- D. Edgar, I. Shabalina, Y. Camara et al., “Random point mutations with major effects on protein-coding genes are the driving force behind premature aging in mtDNA mutator mice,” Cell Metabolism, vol. 10, no. 2, pp. 131–138, 2009. View at Publisher · View at Google Scholar · View at Scopus
- H. Gu, J. D. Marth, P. C. Orban, H. Mossmann, and K. Rajewsky, “Deletion of a DNA polymerase β gene segment in T cells using cell type-specific gene targeting,” Science, vol. 265, no. 5168, pp. 103–106, 1994. View at Google Scholar · View at Scopus
- D. L. Ludwig, M. A. MacInnes, Y. Takiguchi et al., “A murine AP-endonuclease gene-targeted deficiency with post-implantation embryonic progression and ionizing radiation sensitivity,” Mutation Research, vol. 409, no. 1, pp. 17–29, 1998. View at Publisher · View at Google Scholar · View at Scopus
- R. S. Tebbs, M. L. Flannery, J. J. Meneses et al., “Requirement for the Xrcc1 DNA base excision repair gene during early mouse development,” Developmental Biology, vol. 208, no. 2, pp. 513–529, 1999. View at Publisher · View at Google Scholar · View at Scopus
- N. Puebla-Osorio, D. B. Lacey, F. W. Alt, and C. Zhu, “Early embryonic lethality due to targeted inactivation of DNA ligase III,” Molecular and Cellular Biology, vol. 26, no. 10, pp. 3935–3941, 2006. View at Publisher · View at Google Scholar · View at Scopus
- A. Klungland, I. Rosewell, S. Hollenbach et al., “Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 23, pp. 13300–13305, 1999. View at Publisher · View at Google Scholar · View at Scopus
- O. Minowa, T. Arai, M. Hirano et al., “Mmh/Ogg1 gene inactivation results in accumulation of 8-hydroxyguanine in mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 8, pp. 4156–4161, 2000. View at Publisher · View at Google Scholar · View at Scopus
- M. Osterod, S. Hollenbach, J. G. Hengstler, D. E. Barnes, T. Lindahl, and B. Epe, “Age-related and tissue-specific accumulation of oxidative DNA base damage in 7,8-dihydro-8-oxoguanine-DNA glycosylase (Ogg1) deficient mice,” Carcinogenesis, vol. 22, no. 9, pp. 1459–1463, 2001. View at Google Scholar · View at Scopus
- T. Tsuzuki, A. Egashira, and S. Kura, “Analysis of MTH1 gene function in mice with targeted mutagenesis,” Mutation Research, vol. 477, no. 1-2, pp. 71–78, 2001. View at Publisher · View at Google Scholar · View at Scopus
- M. Takao, S. I. Kanno, T. Shiromoto et al., “Novel nuclear and mitochondrial glycosylases revealed by disruption of the mouse Nth1 gene encoding an endonuclease III homolog for repair of thymine glycols,” EMBO Journal, vol. 21, no. 13, pp. 3486–3493, 2002. View at Publisher · View at Google Scholar · View at Scopus
- B. Karahalil, N. C. De Souza-Pinto, J. L. Parsons, R. H. Elder, and V. A. Bohr, “Compromised incision of oxidized pyrimidines in liver mitochondria of mice deficient in NTH1 and OGG1 glycosylases,” Journal of Biological Chemistry, vol. 278, no. 36, pp. 33701–33707, 2003. View at Publisher · View at Google Scholar · View at Scopus
- A. Shibata, D. Maeda, H. Ogino et al., “Role of Parp-1 in suppressing spontaneous deletion mutation in the liver and brain of mice at adolescence and advanced age,” Mutation Research, vol. 664, no. 1-2, pp. 20–27, 2009. View at Publisher · View at Google Scholar · View at Scopus
- V. Vartanian, B. Lowell, I. G. Minko et al., “The metabolic syndrome resulting from a knockout of the NEIL1 DNA glycosylase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 6, pp. 1864–1869, 2006. View at Publisher · View at Google Scholar · View at Scopus
- R. H. Eckel, S. M. Grundy, and P. Z. Zimmet, “The metabolic syndrome,” Lancet, vol. 365, no. 9468, pp. 1415–1428, 2005. View at Publisher · View at Google Scholar · View at Scopus
- H. Dou, S. Mitra, and T. K. Hazra, “Repair of oxidized bases in DNA bubble structures by human DNA glycosylases NEIL1 and NEIL2,” Journal of Biological Chemistry, vol. 278, no. 50, pp. 49679–49684, 2003. View at Publisher · View at Google Scholar · View at Scopus
- M. E. T. Dolle, R. A. Busuttil, A. M. Garcia et al., “Increased genomic instability is not a prerequisite for shortened lifespan in DNA repair deficient mice,” Mutation Research, vol. 596, no. 1-2, pp. 22–35, 2006. View at Publisher · View at Google Scholar · View at Scopus
- M. Murai, Y. Enokido, N. Inamura et al., “Early postnatal ataxia and abnormal cerebellar development in mice lacking Xeroderma pigmentosum group A and Cockayne syndrome group B DNA repair genes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 23, pp. 13379–13384, 2001. View at Publisher · View at Google Scholar · View at Scopus
- J. McWhir, J. Selfridge, D. J. Harrison, S. Squires, and D. W. Melton, “Mice with DNA repair gene (ERCC-1) deficiency have elevated levels of p53, liver nuclear abnormalities and die before weaning,” Nature Genetics, vol. 5, no. 3, pp. 217–224, 1993. View at Publisher · View at Google Scholar
- G. Weeda, I. Donker, J. De Wit et al., “Disruption of mouse ERCC1 results in a novel repair syndrome with growth failure, nuclear abnormalities and senescence,” Current Biology, vol. 7, no. 6, pp. 427–439, 1997. View at Google Scholar · View at Scopus
- J. Y. Park, M.-O. Cho, S. Leonard et al., “Homeostatic imbalance between apoptosis and cell renewal in the liver of premature aging XpdTTD mice,” PLoS ONE, vol. 3, no. 6, Article ID e2346, 2008. View at Publisher · View at Google Scholar
- S. W. P. Wijnhoven, R. B. Beems, M. Roodbergen et al., “Accelerated aging pathology in ad libitum fed Xpd mice is accompanied by features suggestive of caloric restriction,” DNA Repair, vol. 4, no. 11, pp. 1314–1324, 2005. View at Publisher · View at Google Scholar · View at Scopus
- E. Nevedomskaya, A. Meissner, S. Goraler et al., “Metabolic profiling of accelerated aging ERCC1 mice,” Journal of Proteome Research, vol. 9, no. 7, pp. 3680–3687, 2010. View at Publisher · View at Google Scholar · View at Scopus
- I. van der Pluijm, G. A. Garinis, R. M. Brandt et al., “Impaired genome maintenance suppresses the growth hormone–insulin-like growth factor 1 axis in mice with Cockayne syndrome,” PLoS biology, vol. 5, no. 1, p. e2, 2006. View at Publisher · View at Google Scholar
- S. Espejel, M. Martín, P. Klatt, J. Martín-Caballero, J. M. Flores, and M. A. Blasco, “Shorter telomeres, accelerated ageing and increased lymphoma in DNA-PKcs-deficient mice,” EMBO Reports, vol. 5, no. 5, pp. 503–509, 2004. View at Publisher · View at Google Scholar · View at Scopus
- H. Vogel, D. S. Lim, G. Karsenty, M. Finegold, and P. Hasty, “Deletion of Ku86 causes early onset of senescence in mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 19, pp. 10770–10775, 1999. View at Publisher · View at Google Scholar · View at Scopus
- R. A. Busuttil, D. P. Muñoz, A. M. Garcia et al., “Effect of Ku80 deficiency on mutation frequencies and spectra at a lacZ reporter locus in mouse tissues and cells,” PLoS ONE, vol. 3, no. 10, Article ID e3458, 2008. View at Publisher · View at Google Scholar
- N. C. Teoh, Y. Y. Dan, K. Swisshelm et al., “Defective DNA strand break repair causes chromosomal instability and accelerates liver carcinogenesis in mice,” Hepatology, vol. 47, no. 6, pp. 2078–2088, 2008. View at Publisher · View at Google Scholar · View at Scopus
- M. L. Rossi, A. K. Ghosh, and V. A. Bohr, “Roles of Werner syndrome protein in protection of genome integrity,” DNA Repair, vol. 9, no. 3, pp. 331–344, 2010. View at Publisher · View at Google Scholar · View at Scopus
- M. Lebel and P. Leder, “A deletion within the murine Werner syndrome helicase induces sensitivity to inhibitors of topoisomerase and loss of cellular proliferative capacity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 22, pp. 13097–13102, 1998. View at Publisher · View at Google Scholar · View at Scopus
- D. B. Lombard, C. Beard, B. Johnson et al., “Mutations in the WRN gene in mice accelerate mortality in a p53-null background,” Molecular and Cellular Biology, vol. 20, no. 9, pp. 3286–3291, 2000. View at Publisher · View at Google Scholar · View at Scopus
- G. Moore, S. Knoblaugh, K. Gollahon, P. Rabinovitch, and W. Ladiges, “Hyperinsulinemia and insulin resistance in Wrn null mice fed a diabetogenic diet,” Mechanisms of Ageing and Development, vol. 129, no. 4, pp. 201–206, 2008. View at Publisher · View at Google Scholar · View at Scopus
- S. Chang, A. S. Multani, N. G. Cabrera et al., “Essential role of limiting telomeres in the pathogenesis of Werner syndrome,” Nature Genetics, vol. 36, no. 8, pp. 877–882, 2004. View at Publisher · View at Google Scholar · View at Scopus
- X. Du, J. Shen, N. Kugan et al., “Telomere shortening exposes functions for the mouse Werner and Bloom syndrome genes,” Molecular and Cellular Biology, vol. 24, no. 19, pp. 8437–8446, 2004. View at Publisher · View at Google Scholar · View at Scopus
- L. Massip, C. Garand, R. V. N. Turaga, F. Deschênes, E. Thorin, and M. Lebel, “Increased insulin, triglycerides, reactive oxygen species, and cardiac fibrosis in mice with a mutation in the helicase domain of the Werner syndrome gene homologue,” Experimental Gerontology, vol. 41, no. 2, pp. 157–168, 2006. View at Publisher · View at Google Scholar · View at Scopus
- L. Massip, C. Garand, E. R. Paquet et al., “Vitamin C restores healthy aging in a mouse model for Werner syndrome,” FASEB Journal, vol. 24, no. 1, pp. 158–172, 2010. View at Publisher · View at Google Scholar · View at Scopus
- A. Labbe, C. Garand, V. C. Cogger et al., “Resveratrol improves insulin resistance hyperglycemia and hepatosteatosis but not hypertriglyceridemia, inflammation, and life span in a mouse model for werner syndrome,” Journals of Gerontology A, vol. 66, no. 3, pp. 264–278, 2011. View at Google Scholar
- C. K. Lee, R. G. Klopp, R. Weindruch, and T. A. Prolla, “Gene expression profile of aging and its retardation by caloric restriction,” Science, vol. 285, no. 5432, pp. 1390–1393, 1999. View at Publisher · View at Google Scholar · View at Scopus
- A. A. Lachaud, S. Auclair-Vincent, L. Massip, E. Audet-Walsh, M. Lebel, and A. Anderson, “Werner's syndrome helicase participates in transcription of phenobarbital-inducible CYP2B genes in rat and mouse liver,” Biochemical Pharmacology, vol. 79, no. 3, pp. 463–470, 2010. View at Publisher · View at Google Scholar · View at Scopus
- F. V. Pallardó, A. Lloret, M. Lebel et al., “Mitochondrial dysfunction in some oxidative stress-related genetic diseases: Ataxia-Telangiectasia, Down Syndrome, Fanconi Anaemia and Werner Syndrome,” Biogerontology, vol. 11, pp. 401–419, 2010. View at Publisher · View at Google Scholar · View at Scopus
- J. Sastre, F. V. Pallardó, R. Plá et al., “Aging of the liver: age-associated mitochondrial damage in intact hepatocytes,” Hepatology, vol. 24, no. 5, pp. 1199–1205, 1996. View at Publisher · View at Google Scholar · View at Scopus
- C. Musicco, V. Capelli, V. Pesce et al., “Accumulation of overoxidized Peroxiredoxin III in aged rat liver mitochondria,” Biochimica et Biophysica Acta, vol. 1787, no. 7, pp. 890–896, 2009. View at Publisher · View at Google Scholar · View at Scopus
- J. A. Baur, K. J. Pearson, N. L. Price et al., “Resveratrol improves health and survival of mice on a high-calorie diet,” Nature, vol. 444, no. 7117, pp. 337–342, 2006. View at Publisher · View at Google Scholar
- N. L. Nadon, R. Strong, R. A. Miller et al., “Design of aging intervention studies: the NIA interventions testing program,” Age, vol. 30, no. 4, pp. 187–199, 2008. View at Publisher · View at Google Scholar
- R. K. Minor, J. S. Allard, C. M. Younts, T. M. Ward, and R. De Cabo, “Dietary interventions to extend life span and health span based on calorie restriction,” Journals of Gerontology A, vol. 65, no. 7, pp. 695–703, 2010. View at Publisher · View at Google Scholar · View at Scopus