Dysregulation of DAF-16/FOXO3A-mediated stress responses accelerates oxidative DNA damage induced aging

Redox Biology - Tập 18 - Trang 191-199 - 2018
Aditi U. Gurkar1, Andria R. Robinson2, Yuxiang Cui3, Xuesen Li1, Shailaja K. Allani4, Amanda Webster1, Mariya Muravia1, Mohammad Fallahi1, Herbert Weissbach4, Paul D. Robbins1, Yinsheng Wang3, Eric E. Kelley5, Claudette M. St. Croix6, Laura J. Niedernhofer1, Matthew S. Gill1
1Department of Molecular Medicine, Center on Aging, The Scripps Research Institute, Jupiter, FL, United States
2Department of Human Genetics, University of Pittsburgh Graduate School of Public Health, Pittsburgh, PA, United States
3Environmental Toxicology Graduate Program and Department of Chemistry, University of California, Riverside, Riverside, CA, United States
4Center for Molecular Biology and Biotechnology, Florida Atlantic University, Jupiter, FL, United States
5Department of Physiology and Pharmacology, West Virginia University, Morgantown, WV, United States
6Department of Cell Biology, Center for Biologic Imaging, University of Pittsburgh, Pittsburgh, PA, United States

Tài liệu tham khảo

Kirkwood, 2005, Understanding the odd science of aging, Cell, 120, 437, 10.1016/j.cell.2005.01.027 Kennedy, 2014, Geroscience: linking aging to chronic disease, Cell, 159, 709, 10.1016/j.cell.2014.10.039 Gregg, 2011, Physiological consequences of defects in ERCC1-XPF DNA repair endonuclease, DNA Repair (Amst.), 10, 781, 10.1016/j.dnarep.2011.04.026 Gray, 1997, The Werner syndrome protein is a DNA helicase, Nat. Genet, 17, 100, 10.1038/ng0997-100 Armstrong, 2014, Aging and risk of severe, disabling, life-threatening, and fatal events in the childhood cancer survivor study, J. Clin. Oncol., 32, 1218, 10.1200/JCO.2013.51.1055 Jacob, 2013, Markers of oxidant stress that are clinically relevant in aging and age-related disease, Mech. Ageing Dev., 134, 139, 10.1016/j.mad.2013.02.008 Chen, 2016, The cell-cycle arrest and apoptotic functions of p53 in tumor initiation and progression, Cold Spring Harb. Perspect. Med, 6, a026104, 10.1101/cshperspect.a026104 Sharpless, 2007, How stem cells age and why this makes us grow old, Nat. Rev. Mol. Cell Biol., 8, 703, 10.1038/nrm2241 Rodier, 2009, Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion, Nat. Cell Biol., 11, 973, 10.1038/ncb1909 Baker, 2016, Naturally occurring p16(Ink4a)-positive cells shorten healthy lifespan, Nature, 530, 184, 10.1038/nature16932 Coppe, 2010, A human-like senescence-associated secretory phenotype is conserved in mouse cells dependent on physiological oxygen, PLoS One, 5, e9188, 10.1371/journal.pone.0009188 Milo, 2015, How Quickly Do Different Cells in the Body Replace Themselves? Mullaart, 1990, Increased levels of DNA breaks in cerebral cortex of Alzheimer's disease patients, Neurobiol. Aging, 11, 169, 10.1016/0197-4580(90)90542-8 Madabhushi, 2014, DNA damage and its links to neurodegeneration, Neuron, 83, 266, 10.1016/j.neuron.2014.06.034 Kim, 2008, Deregulation of HDAC1 by p25/Cdk5 in neurotoxicity, Neuron, 60, 803, 10.1016/j.neuron.2008.10.015 Lapierre, 2012, Lessons from C. elegans: signaling pathways for longevity, Trends Endocrinol. Metab.: TEM, 23, 637, 10.1016/j.tem.2012.07.007 Lans, 2013, DNA damage leads to progressive replicative decline but extends the life span of long-lived mutant animals, Cell death Differ., 20, 1709, 10.1038/cdd.2013.126 Shaposhnikov, 2015, Lifespan and stress resistance in drosophila with overexpressed DNA repair genes, Sci. Rep., 5, 15299, 10.1038/srep15299 Hyun, 2008, Longevity and resistance to stress correlate with DNA repair capacity in Caenorhabditis elegans, Nucleic Acids Res., 36, 1380, 10.1093/nar/gkm1161 Mueller, 2014, DAF-16/FOXO and EGL-27/GATA promote developmental growth in response to persistent somatic DNA damage, Nat. Cell Biol., 16, 1168, 10.1038/ncb3071 Boyd, 2010, Nucleotide excision repair genes are expressed at low levels and are not detectably inducible in Caenorhabditis elegans somatic tissues, but their function is required for normal adult life after UVC exposure, Mutat. Res., 683, 57, 10.1016/j.mrfmmm.2009.10.008 Astin, 2008, Nucleotide excision repair and the degradation of RNA pol II by the Caenorhabditis elegans XPA and Rsp5 orthologues, RAD-3 and WWP-1, DNA Repair, 7, 267, 10.1016/j.dnarep.2007.10.004 Fensgard, 2010, A two-tiered compensatory response to loss of DNA repair modulates aging and stress response pathways, Aging (Albany NY), 2, 133, 10.18632/aging.100127 A.U. Gurkar, M.S. Gill, L.J. Niedernhofer, Genome stability and ageing. ed Olsen MSGaA (Springer), 2016. Wang, 2012, The oxidative DNA lesions 8,5'-cyclopurines accumulate with aging in a tissue-specific manner, Aging Cell, 11, 714, 10.1111/j.1474-9726.2012.00828.x Niedernhofer, 2006, A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis, Nature, 444, 1038, 10.1038/nature05456 Dolle, 2011, Broad segmental progeroid changes in short-lived Ercc1(-/Delta7) mice, Pathobiol. Aging Age Relat. Dis., 1 Wang, 2011, Quantification of oxidative DNA lesions in tissues of Long-Evans Cinnamon rats by capillary high-performance liquid chromatography-tandem mass spectrometry coupled with stable isotope-dilution method, Anal. Chem., 83, 2201, 10.1021/ac103099s Agostinho, 2013, Combinatorial regulation of meiotic holliday junction resolution in C. elegans by HIM-6 (BLM) helicase, SLX-4, and the SLX-1, MUS-81 and XPF-1 nucleases, PLoS Genet, 9, e1003591, 10.1371/journal.pgen.1003591 Craig, 2012, Methods for studying the DNA damage response in the Caenorhabdatis elegans germ line, Methods Cell Biol., 107, 321, 10.1016/B978-0-12-394620-1.00011-4 Saito, 2009, Caenorhabditis elegans HIM-18/SLX-4 interacts with SLX-1 and XPF-1 and maintains genomic integrity in the germline by processing recombination intermediates, PLoS Genet., 5, e1000735, 10.1371/journal.pgen.1000735 Lans, 2010, Involvement of global genome repair, transcription coupled repair, and chromatin remodeling in UV DNA damage response changes during development, PLoS Genet., 6, e1000941, 10.1371/journal.pgen.1000941 O'Neil, 2013, Joint molecule resolution requires the redundant activities of MUS-81 and XPF-1 during Caenorhabditis elegans meiosis, PLoS Genet, 9, e1003582, 10.1371/journal.pgen.1003582 Saito, 2013, Interplay between structure-specific endonucleases for crossover control during Caenorhabditis elegans meiosis, PLoS Genet, 9, e1003586, 10.1371/journal.pgen.1003586 Ermolaeva, 2013, DNA damage in germ cells induces an innate immune response that triggers systemic stress resistance, Nature, 501, 416, 10.1038/nature12452 Kashiyama, 2013, Malfunction of nuclease ERCC1-XPF results in diverse clinical manifestations and causes Cockayne syndrome, xeroderma pigmentosum, and Fanconi anemia, Am. J. Hum. Genet, 92, 807, 10.1016/j.ajhg.2013.04.007 Tian, 2004, Growth retardation, early death, and DNA repair defects in mice deficient for the nucleotide excision repair enzyme XPF, Mol. Cell Biol., 24, 1200, 10.1128/MCB.24.3.1200-1205.2004 Mori, 2018, ERCC4 variants identified in a cohort of patients with segmental progeroid syndromes, Hum. Mutat., 39, 255, 10.1002/humu.23367 Shore, 2012, Induction of cytoprotective pathways is central to the extension of lifespan conferred by multiple longevity pathways, PLoS Genet., 8, e1002792, 10.1371/journal.pgen.1002792 Henderson, 2001, daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans, Curr. Biol., 11, 1975, 10.1016/S0960-9822(01)00594-2 Murphy, 2003, Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans, Nature, 424, 277, 10.1038/nature01789 Lithgow, 1995, Thermotolerance and extended life-span conferred by single-gene mutations and induced by thermal stress, Proc. Natl. Acad. Sci. USA, 92, 7540, 10.1073/pnas.92.16.7540 Harper, 2011, Fibroblasts from long-lived bird species are resistant to multiple forms of stress, J. Exp. Biol., 214, 1902, 10.1242/jeb.054643 Bansal, 2014, Transcriptional regulation of Caenorhabditis elegans FOXO/DAF-16 modulates lifespan, Longev. Health., 3, 5, 10.1186/2046-2395-3-5 Tullet, 2008, Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans, Cell, 132, 1025, 10.1016/j.cell.2008.01.030 Schumacher, 2001, The C. elegans homolog of the p53 tumor suppressor is required for DNA damage-induced apoptosis, Curr. Biol., 11, 1722, 10.1016/S0960-9822(01)00534-6 Renault, 2011, The pro-longevity gene FoxO3 is a direct target of the p53 tumor suppressor, Oncogene, 30, 3207, 10.1038/onc.2011.35 Wolff, 2006, SMK-1, an essential regulator of DAF-16-mediated longevity, Cell, 124, 1039, 10.1016/j.cell.2005.12.042 Shchedrina, 2011, Analyses of fruit flies that do not express selenoproteins or express the mouse selenoprotein, methionine sulfoxide reductase B1, reveal a role of selenoproteins in stress resistance, J. Biol. Chem., 286, 29449, 10.1074/jbc.M111.257600 Willcox, 2008, FOXO3A genotype is strongly associated with human longevity, Proc. Natl. Acad. Sci. USA, 105, 13987, 10.1073/pnas.0801030105 Anselmi, 2009, Association of the FOXO3A locus with extreme longevity in a southern Italian centenarian study, Rejuvenation Res, 12, 95, 10.1089/rej.2008.0827 Flachsbart, 2009, Association of FOXO3A variation with human longevity confirmed in German centenarians, Proc. Natl. Acad. Sci. USA, 106, 2700, 10.1073/pnas.0809594106 Soerensen, 2010, Replication of an association of variation in the FOXO3A gene with human longevity using both case-control and longitudinal data, Aging Cell, 9, 1010, 10.1111/j.1474-9726.2010.00627.x Morris, 2015, FOXO3: a major gene for human longevity--a mini-review, Gerontology, 61, 515, 10.1159/000375235 R, 2018, Spontaneous DNA damage to the nuclear genome promotes senescence, T redox imbalance and aging, Redox Biol., 17, 259, 10.1016/j.redox.2018.04.007 Kyoung Kim, 2005, Down-regulation of a forkhead transcription factor, FOXO3a, accelerates cellular senescence in human dermal fibroblasts, J. Gerontol. A Biol. Sci. Med Sci., 60, 4, 10.1093/gerona/60.1.4 Yao, 2012, SIRT1 protects against emphysema via FOXO3-mediated reduction of premature senescence in mice, J. Clin. Invest, 122, 2032, 10.1172/JCI60132 Fuhrmann-Stroissnigg, 2017, Identification of HSP90 inhibitors as a novel class of senolytics, Nat. Commun., 8, 422, 10.1038/s41467-017-00314-z Gregg, 2012, A mouse model of accelerated liver aging caused by a defect in DNA repair, Hepatology, 55, 609, 10.1002/hep.24713 Minniti, 2009, Methionine sulfoxide reductase A expression is regulated by the DAF-16/FOXO pathway in Caenorhabditis elegans, Aging Cell, 8, 690, 10.1111/j.1474-9726.2009.00521.x Yermolaieva, 2004, Methionine sulfoxide reductase A protects neuronal cells against brief hypoxia/reoxygenation, Proc. Natl. Acad. Sci. USA, 101, 1159, 10.1073/pnas.0308215100 Ruan, 2002, High-quality life extension by the enzyme peptide methionine sulfoxide reductase, Proc. Natl. Acad. Sci. USA, 99, 2748, 10.1073/pnas.032671199 Koc, 2004, Methionine sulfoxide reductase regulation of yeast lifespan reveals reactive oxygen species-dependent and -independent components of aging, Proc. Natl. Acad. Sci. USA, 101, 7999, 10.1073/pnas.0307929101 Berman, 2006, Germ-cell loss extends C. elegans life span through regulation of DAF-16 by kri-1 and lipophilic-hormone signaling, Cell, 124, 1055, 10.1016/j.cell.2006.01.039 Daitoku, 2011, Regulation of FoxO transcription factors by acetylation and protein-protein interactions, Biochim. Et. Biophys. Acta, 1813, 1954, 10.1016/j.bbamcr.2011.03.001 Rinner, 2007, An integrated mass spectrometric and computational framework for the analysis of protein interaction networks, Nat. Biotechnol., 25, 345, 10.1038/nbt1289 Nemoto, 2004, Nutrient availability regulates SIRT1 through a forkhead-dependent pathway, Science, 306, 2105, 10.1126/science.1101731 Wang, 2008, Biochemical and structural characterization of an intramolecular interaction in FOXO3a and its binding with p53, J. Mol. Biol., 384, 590, 10.1016/j.jmb.2008.09.025 Tilstra, 2012, NF-kappaB inhibition delays DNA damage-induced senescence and aging in mice, J. Clin. Invest, 122, 2601, 10.1172/JCI45785 Miyaguchi, 2009, P53 negatively regulates the transcriptional activity of FOXO3a under oxidative stress, Cell Biol. Int, 33, 853, 10.1016/j.cellbi.2009.04.017 Jayaraman, 1997, Identification of redox/repair protein Ref-1 as a potent activator of p53, Genes Dev., 11, 558, 10.1101/gad.11.5.558 Liu, 2011, p53, oxidative stress, and aging, Antioxid. Redox Signal, 15, 1669, 10.1089/ars.2010.3644 Ventura, 2009, p53/CEP-1 increases or decreases lifespan, depending on level of mitochondrial bioenergetic stress, Aging Cell, 8, 380, 10.1111/j.1474-9726.2009.00482.x Baruah, 2014, CEP-1, the Caenorhabditis elegans p53 homolog, mediates opposing longevity outcomes in mitochondrial electron transport chain mutants, PLoS Genet., 10, e1004097, 10.1371/journal.pgen.1004097 Vermeij, 2016, Restricted diet delays accelerated ageing and genomic stress in DNA-repair-deficient mice, Nature, 537, 427, 10.1038/nature19329 Brenner, 1974, The genetics of Caenorhabditis elegans, Genetics, 77, 71, 10.1093/genetics/77.1.71