DNA damage in obesity: Initiator, promoter and predictor of cancer

Mutation Research/Reviews in Mutation Research - Tập 778 - Trang 23-37 - 2018
Moonisah Usman1, Emanuela V. Volpi1
1Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, 115 New Cavendish Street, London W1W 6UW, UK

Tài liệu tham khảo

Renehan, 2008, Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies, Lancet, 371, 569, 10.1016/S0140-6736(08)60269-X Arnold, 2016, Obesity and cancer: an update of the global impact, Cancer Epidemiol., 41, 8, 10.1016/j.canep.2016.01.003 Kyrgiou, 2017, Adiposity and cancer at major anatomical sites: umbrella review of the literature, BMJ, 28, 356 Mazzarella, 2015, Why does obesity promote cancer? Epidemiology, biology, and open questions, Ecancermedicalscience, 9, 554 Fernández-Sánchez, 2011, Inflammation, oxidative stress, and obesity, Int. J. Mol. Sci., 12, 3117, 10.3390/ijms12053117 Hanahan, 2016, Hallmarks of cancer: the next generation, Cell, 144, 646 Wiseman, 1996, Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer, Biochem. J., 313, 17, 10.1042/bj3130017 Xu, 2014, Oxidative stress preferentially induces a subtype of micronuclei and mediates the genomic instability caused by p53 dysfunction, Mutat. Res. Mol. Mech. Mutagen., 770, 1, 10.1016/j.mrfmmm.2014.08.004 Finkel, 2011, Signal transduction by reactive oxygen species, J. Cell Biol., 194 Codoñer-Franch, 2011, Oxidant mechanisms in childhood obesity: the link between inflammation and oxidative stress, Transl. Res., 158, 369, 10.1016/j.trsl.2011.08.004 Ohshima, 2003, Chemical basis of inflammation-induced carcinogenesis, Arch. Biochem. Biophys., 417, 3, 10.1016/S0003-9861(03)00283-2 Chielle, 2016, Adipocytokines, inflammatory and oxidative stress markers of clinical relevance altered in young overweight/obese subjects, Clin. Biochem., 49, 548, 10.1016/j.clinbiochem.2016.01.003 Ellulu, 2016, Obesity can predict and promote systemic inflammation in healthy adults, Int. J. Cardiol., 215, 318, 10.1016/j.ijcard.2016.04.089 Park, 2005, Relationship of obesity and visceral adiposity with serum concentrations of CRP, TNF-α and IL-6, Diabetes Res. Clin. Pract., 69, 29, 10.1016/j.diabres.2004.11.007 Schipper, 2012, Systemic inflammation in childhood obesity: circulating inflammatory mediators and activated CD14++ monocytes, Diabetologia, 55, 2800, 10.1007/s00125-012-2641-y Lee, 2014, Cellular and molecular players in adipose tissue inflammation in the development of obesity-induced insulin resistance, Biochim. Biophys. Acta, 1842, 446, 10.1016/j.bbadis.2013.05.017 Mittal, 2014, Reactive oxygen species in inflammation and tissue injury, Antioxid. Redox Signal., 20, 1126, 10.1089/ars.2012.5149 Kern, 2003, Adiponectin expression from human adipose tissue, Diabetes, 52, 1779, 10.2337/diabetes.52.7.1779 Ouchi, 1999, Novel modulator for endothelial adhesion molecules adipocyte-derived plasma protein adiponectin, Circulation, 100, 2473, 10.1161/01.CIR.100.25.2473 Mantzoros, 2004, Adiponectin and breast cancer risk, J. Clin. Endocrinol. Metab., 89, 1102, 10.1210/jc.2003-031804 Ishikawa, 2005, Plasma adiponectin and gastric cancer, Clin. Cancer Res., 11, 466, 10.1158/1078-0432.466.11.2 Wei, 2005, Low plasma adiponectin levels and risk of colorectal cancer in men: a prospective study, J. Natl. Cancer Inst., 97, 1688, 10.1093/jnci/dji376 Petridou, 2006, Adiponectin in relation to childhood myeloblastic leukaemia, Br. J. Cancer, 94, 156, 10.1038/sj.bjc.6602896 Goktas, 2005, Prostate cancer and adiponectin, Urology, 65, 1168, 10.1016/j.urology.2004.12.053 Haghiac, 2012, Increased death of adipose cells, a path to release cell‐free DNA into systemic circulation of obese women, Obesity, 20, 2213, 10.1038/oby.2012.138 Nishimoto, 2016, Obesity-induced DNA released from adipocytes stimulates chronic adipose tissue inflammation and insulin resistance, Sci. Adv., 2, 10.1126/sciadv.1501332 Weisberg, 2003, Obesity is associated with macrophage accumulation in adipose tissue, J. Clin. Invest., 112, 1796, 10.1172/JCI200319246 Tamir, 1996, DNA damage by nitric oxide, Chem. Res. Toxicol., 9, 821, 10.1021/tx9600311 Baik, 1996, Increased oxidative DNA damage in helicobacter pylori-infected human gastric mucosa, Cancer Res., 56, 1279 Bernstein, 2001, Cancer risk in patients with inflammatory bowel disease, Cancer, 91, 854, 10.1002/1097-0142(20010215)91:4<854::AID-CNCR1073>3.0.CO;2-Z Shawki, 2014, Increased DNA damage in hepatitis C virus-related hepatocellular carcinoma, DNA Cell Biol., 33, 884, 10.1089/dna.2014.2417 Tezal, 2005, Is periodontitis associated with oral neoplasms?, J. Periodontol., 76, 406, 10.1902/jop.2005.76.3.406 Izano, 2016, Chronic inflammation and risk of colorectal and other obesity‐related cancers: the health, aging and body composition study, Int. J. Cancer, 138, 1118, 10.1002/ijc.29868 Boden, 2008, Obesity and free fatty acids, Endocrinol. Metab. Clin. North Am., 37, 635, 10.1016/j.ecl.2008.06.007 Vincent, 2006, Biomarkers and potential mechanisms of obesity-induced oxidant stress in humans, Int. J. Obes., 30, 400, 10.1038/sj.ijo.0803177 Olusi, 2002, Obesity is an independent risk factor for plasma lipid peroxidation and depletion of erythrocyte cytoprotectic enzymes in humans, Int. J. Obes. Relat. Metab. Disord., 26, 10.1038/sj.ijo.0802066 Niedernhofer, 2003, Malondialdehyde, a product of lipid peroxidation, is mutagenic in human cells, J. Biol. Chem., 278, 31426, 10.1074/jbc.M212549200 VanderVeen, 2003, Induction of frameshift and base pair substitution mutations by the major DNA adduct of the endogenous carcinogen malondialdehyde, Proc. Natl. Acad. Sci. U. S. A., 100, 14247, 10.1073/pnas.2332176100 Del Rio, 2005, A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress, Nutr. Metab. Cardiovasc. Dis., 15, 316, 10.1016/j.numecd.2005.05.003 Chen, 2015, Visfatin and oxidative stress influence endothelial progenitor cells in obese populations, Endocr. Res., 40, 83, 10.3109/07435800.2014.952016 Ustundag, 2007, Oxidative status and serum leptin levels in obese prepubertal children, Cell Biochem. Funct., 25, 479, 10.1002/cbf.1334 Gönenç, 2001, Plasma malondialdehyde (MDA) levels in breast and lung cancer patients, J. Clin. Pharm. Ther., 26, 141, 10.1046/j.1365-2710.2001.00334.x Friedman, 1992, Restoration of insulin responsiveness in skeletal muscle of morbidly obese patients after weight loss. Effect on muscle glucose transport and glucose transporter GLUT4, J. Clin. Invest., 89, 701, 10.1172/JCI115638 Shah, 2003, Elevated Free fatty acids impair glucose metabolism in women decreased stimulation of muscle glucose uptake and suppression of splanchnic glucose production during combined hyperinsulinemia and hyperglycemia, Diabetes, 52, 38, 10.2337/diabetes.52.1.38 Lin, 2005, The hyperglycemia-induced inflammatory response in adipocytes the role of reactive oxygen species, J. Biol. Chem., 280, 4617, 10.1074/jbc.M411863200 Renehan, 2006, Obesity and cancer risk: the role of the insulin–IGF axis, Trends Endocrinol. Metab., 17, 328, 10.1016/j.tem.2006.08.006 Li, 2001, Free insulin‐like growth factor‐I and breast cancer risk, Int. J. Cancer, 91, 736, 10.1002/1097-0215(200002)9999:9999<::AID-IJC1111>3.0.CO;2-# Renehan, 2003, Acromegaly and colorectal cancer: a comprehensive review of epidemiology, biological mechanisms, and clinical implications, Horm. Metab. Res., 35, 712, 10.1055/s-2004-814150 Yang, 2005, Activated IGF-1R inhibits hyperglycemia-induced DNA damage and promotes DNA repair by homologous recombination, Am. J. Physiol., 289, F1144 Frystyk, 1995, Free insulin-like growth factors in human obesity, Metabolism, 44, 37, 10.1016/0026-0495(95)90219-8 Kaaks, 2000, Plasma androgens, IGF-1, body size, and prostate cancer risk: a synthetic review, Prostate Cancer Prostatic Dis., 3, 157, 10.1038/sj.pcan.4500421 Selby, 1990, Sex hormone binding globulin: origin, function and clinical significance, Ann. Clin. Biochem. Int. J. Biochem. Med., 27, 532, 10.1177/000456329002700603 Clemons, 2001, Estrogen and the risk of breast cancer, N. Engl. J. Med., 344, 276, 10.1056/NEJM200101253440407 Siiteri, 1980, 499 Caldon, 2010, Cell cycle proteins in epithelial cell differentiation: implications for breast cancer, Cell Cycle, 9, 1918, 10.4161/cc.9.10.11474 Roy, 1999, Estrogen, DNA damage and mutations, Mutat. Res. Mol. Mech. Mutagen., 424, 107, 10.1016/S0027-5107(99)00012-3 Ozata, 2002, Increased oxidative stress and hypozincemia in male obesity, Clin. Biochem., 35, 627, 10.1016/S0009-9120(02)00363-6 Amirkhizi, 2010, Is obesity associated with increased plasma lipid peroxidation and oxidative stress in women?, ARYA Atheroscler., 2 Erdeve, 2004, Antioxidant superoxide dismutase activity in obese children, Biol. Trace Elem. Res., 98, 219, 10.1385/BTER:98:3:219 Kilic, 2016, Oxidative stress status in childhood obesity: a potential risk predictor, Med. Sci. Monit., 22, 3673, 10.12659/MSM.897965 Albuali, 2014, Evaluation of oxidant-antioxidant status in overweight and morbidly obese Saudi children, World J. Clin. Pediatr., 3, 6, 10.5409/wjcp.v3.i1.6 Sfar, 2013, Antioxidant enzymes activities in obese Tunisian children, Nutr. J., 12, 18, 10.1186/1475-2891-12-18 YOUEN, 2006, vol. 359, 353 Sentürker, 1997, Oxidative DNA base damage and antioxidant enzyme levels in childhood acute lymphoblastic leukemia, FEBS Lett., 416, 286, 10.1016/S0014-5793(97)01226-X Elchuri, 2005, CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life, Oncogene, 24, 367, 10.1038/sj.onc.1208207 Asaduzzaman Khan, 2010, Antioxidant enzymes and cancer, Chin. J Cancer Res., 22, 87, 10.1007/s11670-010-0087-7 Srivastava, 2016, Evaluation of oxidant-antioxidant status in tissue samples in oral cancer: a case control study, Dent. Res. J. (Isfahan), 13, 181, 10.4103/1735-3327.178210 Hecht, 2016, The role of oxidative stress on breast cancer development and therapy, Tumor Biol., 37, 4281, 10.1007/s13277-016-4873-9 Via, 2012, The malnutrition of obesity: micronutrient deficiencies that promote diabetes, ISRN Endocrinol., 2012 Ames, 2001, DNA damage from micronutrient deficiencies is likely to be a major cause of cancer, Mutat. Res., 475, 7, 10.1016/S0027-5107(01)00070-7 Vimaleswaran, 2013, Causal relationship between obesity and vitamin D status: bi-directional Mendelian randomization analysis of multiple cohorts, PLoS Med., 10, 10.1371/journal.pmed.1001383 Bao, 2008, Protective role of 1α, 25‐dihydroxyvitamin D3 against oxidative stress in nonmalignant human prostate epithelial cells, Int. J. Cancer, 122, 2699, 10.1002/ijc.23460 Hanchette, 1992, Geographic patterns of prostate cancer mortality. Evidence for a protective effect of ultraviolet radiation, Cancer, 70, 2861, 10.1002/1097-0142(19921215)70:12<2861::AID-CNCR2820701224>3.0.CO;2-G Crasta, 2012, DNA breaks and chromosome pulverization from errors in mitosis, Nature, 482, 53, 10.1038/nature10802 Hatch, 2013, Catastrophic nuclear envelope collapse in cancer cell micronuclei, Cell, 154, 47, 10.1016/j.cell.2013.06.007 Mackenzie, 2017, cGAS surveillance of micronuclei links genome instability to innate immunity, Nature, 548, 461, 10.1038/nature23449 Bonassi, 2006, An increased micronucleus frequency in peripheral blood lymphocytes predicts the risk of cancer in humans, Carcinogenesis, 28, 625, 10.1093/carcin/bgl177 Murgia, 2008, Validation of micronuclei frequency in peripheral blood lymphocytes as early cancer risk biomarker in a nested case-control study, Mutat. Res.-Fundam. Mol. Mech. Mutagen., 639, 27, 10.1016/j.mrfmmm.2007.10.010 Bolognesi, 1999, Chromosomal damage and ageing: effect on micronuclei frequency in peripheral blood lymphocytes, Age Ageing, 28, 393, 10.1093/ageing/28.4.393 Milosevic-Djordjevic, 2002, Micronuclei and ageing in a sample of Yugoslavian population, Russ. J. Genet., 38, 201, 10.1023/A:1014342312959 Orta, 2012, The effect of aging on micronuclei frequency and proliferation in human peripheral blood lymphocytes, Indian J. Hum. Genet., 18, 95, 10.4103/0971-6866.96671 Ferraz, 2016, Effects of age on the frequency of micronuclei and degenerative nuclear abnormalities, Rev. Bras. Geriatr. Gerontol., 19, 627, 10.1590/1809-98232016019.150155 Sanchez-Flores, 2018, Frailty syndrome and genomic instability in older adults: suitability of the cytome micronucleus assay as a diagnostic tool, J. Gerontol. A Biol. Sci. Med. Sci., 73, 864, 10.1093/gerona/glx258 Yesilada, 2006, Increased micronucleus frequencies in peripheral blood lymphocytes in women with polycystic ovary syndrome, Eur. J. Endocrinol., 154, 563, 10.1530/eje.1.02117 Andreassi, 2011, The association of micronucleus frequency with obesity, diabetes and cardiovascular disease, Mutagenesis, 26, 77, 10.1093/mutage/geq077 Donmez-Altuntas, 2014, Evaluation of chromosomal damage, cytostasis, cytotoxicity, oxidative DNA damage and their association with body-mass index in obese subjects, Mutat. Res. Toxicol. Environ. Mutagen., 771, 30, 10.1016/j.mrgentox.2014.06.006 Scarpato, 2011, Nuclear damage in peripheral lymphocytes of obese and overweight Italian children as evaluated by the γ-H2AX focus assay and micronucleus test, FASEB J., 25, 685, 10.1096/fj.10-168427 Dass Singh, 2017, Infant birth outcomes are associated with DNA damage biomarkers as measured by the cytokinesis block micronucleus cytome assay: the DADHI study, Mutagenesis, 32, 355, 10.1093/mutage/gex001 Cho, 2017, Genomic health status assessed by a cytokinesis-block micronucleus cytome assay in a healthy middle-aged Korean population, Mutat. Res., 814, 7, 10.1016/j.mrgentox.2016.11.008 Croco, 2016, Genetic instability and aging under the scrutiny of comparative biology: a meta-analysis of spontaneous micronuclei frequency, Mech. Ageing Dev., 156, 34, 10.1016/j.mad.2016.04.004 Wickliffe, 2016, Diet‐induced obesity increases the frequency of Pig‐a mutant erythrocytes in male C57BL/6J mice, Environ. Mol. Mutagen., 57, 668, 10.1002/em.22058 Almeida, 2010, Micronuclei formation in liver fibrosis samples from patients infected by hepatitis C virus, Genet. Mol. Biol., 33, 418, 10.1590/S1415-47572010005000061 Suzuki, 2017, Mutations induced by 8-hydroxyguanine (8-oxo-7, 8-dihydroguanine), a representative oxidized base, in mammalian cells, Genes Environ., 39, 2, 10.1186/s41021-016-0051-y Ramon, 1999, Effects of 8-oxo-7, 8-dihydro-2′-deoxyguanosine on the binding of the transcription factor Sp1 to its cognate target DNA sequence (GC box), Free Radic. Res., 31, 217, 10.1080/10715769900300781 Black, 2001, Sp1 and krüppel-like factor family of transcription factors in cell growth regulation and cancer, J. Cell. Physiol., 188, 143, 10.1002/jcp.1111 Ba, 2018, 8-Oxoguanine DNA glycosylase 1: beyond repair of the oxidatively modified base lesions, Redox Biol., 14, 669, 10.1016/j.redox.2017.11.008 Cooke, 2006, Does measurement of oxidative damage to DNA have clinical significance?, Clin. Chim. Acta, 365, 30, 10.1016/j.cca.2005.09.009 Burns, 2013, Evidence for APOBEC3B mutagenesis in multiple human cancers, Nat. Genet., 45, 977, 10.1038/ng.2701 Kaur, 2016, Salivary 8-hydroxy-2-deoxyguanosine, malondialdehyde, vitamin C, and vitamin E in oral pre-cancer and cancer: diagnostic value and free radical mechanism of action, Clin. Oral Investig., 20, 315, 10.1007/s00784-015-1506-4 Romano, 2000, 8-Hydroxy-2′-deoxyguanosine in cervical cells: correlation with grade of dysplasia and human papillomavirus infection, Carcinogenesis, 21, 1143, 10.1093/carcin/21.6.1143 Oberdoerffer, 2007, The role of nuclear architecture in genomic instability and ageing, Nat. Rev. Mol. Cell Biol., 8, 692, 10.1038/nrm2238 Chen, 1995, Oxidative DNA damage and senescence of human diploid fibroblast cells, Proc. Natl. Acad. Sci. U. S. A., 92, 4337, 10.1073/pnas.92.10.4337 Xu, 2015, The changes of 8-OHdG, hOGG1, APE1 and Pol β in lenses of patients with age-related cataract, Curr. Eye Res., 40, 378, 10.3109/02713683.2014.924148 Rubio-Perez, 2015, Effects of an antioxidant beverage on biomarkers of oxidative stress in Alzheimer’s patients, Eur. J. Nutr., 1 Kikuchi, 2002, systemic increase of oxidative nucleic acid damage in Parkinson’s disease and multiple system atrophy, Neurobiol. Dis., 9, 244, 10.1006/nbdi.2002.0466 Nishikawa, 2003, Evaluation of urinary 8-hydroxydeoxy-guanosine as a novel biomarker of macrovascular complications in type 2 diabetes, Diabetes Care, 26, 1507, 10.2337/diacare.26.5.1507 de la Maza, 2006, Weight increase and overweight are associated with DNA oxidative damage in skeletal muscle, Clin. Nutr., 25, 968, 10.1016/j.clnu.2006.02.008 Hofer, 2006, DNA oxidative damage and strand breaks in young healthy individuals: a gender difference and the role of life style factors, Free Radic. Res., 40, 707, 10.1080/10715760500525807 Mizoue, 2007, Body mass index and oxidative DNA damage: a longitudinal study, Cancer Sci., 98, 1254, 10.1111/j.1349-7006.2007.00511.x Cejvanovic, 2016, Markers of oxidative stress in obese men with and without hypertension, Scand. J. Clin. Lab. Invest., 76, 620, 10.1080/00365513.2016.1230776 El Wakkad, 2011, Relationship between obesity and 8—hydr0xy—2—de0xy guanosine as an oxidative marker in obese, J. Med. Sci., 11, 231, 10.3923/jms.2011.231.235 Protano, 2014, Biomarkers of oxidative stress to nucleic acids: background levels and effects of body mass index and life-style factors in an urban paediatric population, Sci. Total Environ., 500–501, 44, 10.1016/j.scitotenv.2014.08.095 Ramachandra, 2015, Urinary biomarkers of oxidative stress and insulin resistance in childhood obesity, FASEB J., 29 Demirbag, 2006, DNA damage in metabolic syndrome and its association with antioxidative and oxidative measurements, Int. J. Clin. Pract., 60, 1187, 10.1111/j.1742-1241.2006.01042.x Kobayashi, 2004, Molecular mechanism of the recruitment of NBS1/hMRE11/hRAD50 complex to DNA double-strand breaks: NBS1 binds to gamma-H2AX through FHA/BRCT domain, J. Radiat. Res., 45, 473, 10.1269/jrr.45.473 Khanna, 2001, DNA double-strand breaks: signaling, repair and the cancer connection, Nat. Genet., 27, 247, 10.1038/85798 Tu, 2013, γh2AX foci formation in the absence of DNA damage: mitotic H2AX phosphorylation is mediated by the DNA-PKcs/CHK2 pathway, FEBS Lett., 587, 3437, 10.1016/j.febslet.2013.08.028 Nikolova, 2014, The gammaH2AX assay for genotoxic and nongenotoxic agents: comparison of H2AX phosphorylation with cell death response, Toxicol Sci., 140, 103, 10.1093/toxsci/kfu066 Nikolova, 2017, Genotoxicity testing: comparison of the gammaH2AX focus assay with the alkaline and neutral comet assays, Mutat Res., 822, 10, 10.1016/j.mrgentox.2017.07.004 Zhou, 2013, Novel prognostic markers for patients with triple-negative breast cancer, Hum Pathol., 44, 2180, 10.1016/j.humpath.2013.03.021 Bartkova, 2005, DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis, Nature, 434, 864, 10.1038/nature03482 Mei, 2015, Phospho-histone H2AX is a diagnostic and prognostic marker for epithelial ovarian cancer, Int. J. Clin. Exp. Pathol., 8, 5597 Gorgoulis, 2005, Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions, Nature, 434, 907, 10.1038/nature03485 Sedelnikova, 2004, Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks, Nat. Cell Biol., 6, 168, 10.1038/ncb1095 Wang, 2009, DNA damage response and cellular senescence in tissues of aging mice, Aging Cell, 8, 311, 10.1111/j.1474-9726.2009.00481.x Schurman, 2012, Age-related disease association of endogenous? ?-H2AX foci in mononuclear cells derived from leukapheresis, PLoS One, 7, 3, 10.1371/journal.pone.0045728 Redon, 2011, Recent developments in the use of γ -H2AX as a quantitative DNA double-strand break biomarker, Aging (Albany N.Y.), 3, 168 Villaret, 2010, Adipose tissue endothelial cells from obese human subjects: differences among depots in angiogenic, metabolic, and inflammatory gene expression and cellular senescence, Diabetes, 59, 2755, 10.2337/db10-0398 Azzarà, 2016, Different repair kinetic of DSBs induced by mitomycin C in peripheral lymphocytes of obese and normal weight adolescents, Mutat. Res. Mol. Mech. Mutagen., 789, 9, 10.1016/j.mrfmmm.2016.05.001 Azzarà, 2017, Increased level of DNA damage in some organs of obese Zucker rats by γ-H2AX analysis, Environ. Mol. Mutagen., 58, 477, 10.1002/em.22115 Ostling, 1984, Microelectrophoretic study of radiation-induced DNA damages in individual mammalian cells, Biochem. Biophys. Res. Commun., 123, 291, 10.1016/0006-291X(84)90411-X Olive, 2006, The comet assay: a method to measure DNA damage in individual cells, Nat. Protoc., 1, 23, 10.1038/nprot.2006.5 Apostolou, 2014, Use of the comet assay technique for quick and reliable prediction of in vitro response to chemotherapeutics in breast and colon cancer, J. Biol. Res., 21, 14 Katarkar, 2014, Comparative evaluation of genotoxicity by micronucleus assay in the buccal mucosa over comet assay in peripheral blood in oral precancer and cancer patients, Mutagen, 29, 325, 10.1093/mutage/geu023 López-Diazguerrero, 2005, Susceptibility of DNA to oxidative stressors in young and aging mice, Life Sci., 77, 2840, 10.1016/j.lfs.2005.05.034 Piperakis, 2009, The use of comet assay in measuring DNA damage and repair efficiency in child, adult, and old age populations, Cell Biol. Toxicol., 25, 65, 10.1007/s10565-007-9046-6 Bukhari, 2010, Plasma homocysteine and DNA damage profiles in normal and obese subjects in the Pakistani population, Mol. Biol. Rep., 37, 289, 10.1007/s11033-009-9686-0 Gandhi, 2012, Assessment of DNA damage in obese individuals, Res. J. Biol., 02, 37 Tomasello, 2011, DNA damage in normal-weight obese syndrome measured by Comet assay, Med. J. Nutr. Metab., 4, 99, 10.1007/s12349-010-0035-6 Tenorio, 2013, The influence of sleep deprivation and obesity on DNA damage in female Zucker rats, Clinics, 68, 385, 10.6061/clinics/2013(03)OA16 Ibero-Baraibar, 2015, Assessment of DNA damage using comet assay in middle-aged overweight/obese subjects after following a hypocaloric diet supplemented with cocoa extract, Mutagen, 30, 139, 10.1093/mutage/geu056 Smith, 2003, DNA damage and breast cancer risk, Carcinogenesis, 24, 883, 10.1093/carcin/bgg037 De Lange, 1995, 10 telomere dynamics and genome instability in human cancer, Cold Spring Harb. Monogr. Arch., 29, 265 Olovnikov, 1973, A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon, J. Theor. Biol., 41, 181, 10.1016/0022-5193(73)90198-7 Allsopp, 1992, Telomere length predicts replicative capacity of human fibroblasts, Proc. Natl. Acad. Sci. U. S. A., 89, 10114, 10.1073/pnas.89.21.10114 Xi, 2013, Telomere, aging and age-related diseases, Aging Clin. Exp. Res., 25, 139, 10.1007/s40520-013-0021-1 Hochstrasser, 2012, Telomere length is age-dependent and reduced in monocytes of Alzheimer patients, Exp. Gerontol., 47, 160, 10.1016/j.exger.2011.11.012 Wang, 2008, Telomere length and risk of Parkinson’s disease, Mov. Disord., 23, 302, 10.1002/mds.21867 Steer, 2007, Reduced telomere length in rheumatoid arthritis is independent of disease activity and duration, Ann. Rheum. Dis., 66, 476 Ishikawa, 2011, Accelerated in vivo epidermal telomere loss in Werner syndrome, Aging (Albany N.Y.), 3, 417 Decker, 2009, Telomere length in Hutchinson-Gilford progeria syndrome, Mech. Ageing Dev., 130, 377, 10.1016/j.mad.2009.03.001 Fernandez, 2014, Transformation resistance in a premature aging disorder identifies a tumor-protective function of BRD4, Cell Rep., 9, 248, 10.1016/j.celrep.2014.08.069 Broberg, 2005, Constitutional short telomeres are strong genetic susceptibility markers for bladder cancer, Carcinogenesis, 26, 1263, 10.1093/carcin/bgi063 Zhu, 2016, The association between telomere length and cancer risk in population studies, Sci. Rep., 6, 22243, 10.1038/srep22243 Qu, 2013, Association of leukocyte telomere length with breast cancer risk: nested case-control findings from the Shanghai women’s health study, Am. J. Epidemiol., 177, 617, 10.1093/aje/kws291 Skinner, 2012, Telomere length and pancreatic cancer: a case-control study, Cancer Epidemiol. Biomark. Prev., 21, 2095, 10.1158/1055-9965.EPI-12-0671 Risques, 2007, Leukocyte telomere length predicts cancer risk in Barrett’s esophagus, Cancer Epidemiol. Biomark. Prev., 16, 2649, 10.1158/1055-9965.EPI-07-0624 Jang, 2008, Telomere length and the risk of lung cancer, Cancer Sci., 99, 1385, 10.1111/j.1349-7006.2008.00831.x Lan, 2013, Longer telomere length in peripheral white blood cells Is associated with risk of lung cancer and the rs2736100 (CLPTM1L-TERT) polymorphism in a prospective cohort study among women in China, PLoS One, 8 Ernst, 2016, Telomere dysfunction and chromothripsis, Int. J. Cancer, 138, 2905, 10.1002/ijc.30033 Valdes, 2005, Obesity, cigarette smoking, and telomere length in women, Lancet (London, England), 366, 662, 10.1016/S0140-6736(05)66630-5 Nordfjäll, 2008, Telomere length is associated with obesity parameters but with a gender difference, Obesity, 16, 2682, 10.1038/oby.2008.413 Kim, 2009, Obesity and weight gain in adulthood and telomere length, Cancer Epidemiol. Biomark. Prev., 18, 816, 10.1158/1055-9965.EPI-08-0935 Moreno-Navarrete, 2010, Telomere length of subcutaneous adipose tissue cells is shorter in obese and formerly obese subjects, Int. J. Obes., 34, 1345, 10.1038/ijo.2010.49 Diaz, 2010, Telomere length and adiposity in a racially diverse sample, Int. J. Obes., 34, 261, 10.1038/ijo.2009.198 Zannolli, 2008, Telomere length and obesity, Acta Paediatr., 97, 952, 10.1111/j.1651-2227.2008.00783.x Al-Attas, 2010, Telomere length in relation to insulin resistance, inflammation and obesity among Arab youth, Acta Pædiatrica, 99, 896, 10.1111/j.1651-2227.2010.01720.x Buxton, 2011, Childhood obesity is associated with shorter leukocyte telomere length, J. Clin. Endocrinol. Metab., 96, 1500, 10.1210/jc.2010-2924 Zhu, 2011, Leukocyte telomere length in healthy white and black adolescents: relations to race, sex, adiposity, adipokines and physical activity, J. Pediatr., 158, 215, 10.1016/j.jpeds.2010.08.007 Park, 2012, The impact of childhood obesity on morbidity and mortality in adulthood: a systematic review, Obes. Rev., 13, 985, 10.1111/j.1467-789X.2012.01015.x Hardikar, 2015, Obesity and inflammation markers in relation to leukocyte telomere length in a cross-sectional study of persons with Barrett’s esophagus, BMC Obes., 2, 32, 10.1186/s40608-015-0063-3 Rode, 2014, Increased body mass index, elevated C-reactive protein, and short telomere length, J. Clin. Endocrinol. Metab., 99, E1671, 10.1210/jc.2014-1161 Rehkopf, 2016, Leukocyte telomere length in relation to 17 biomarkers of cardiovascular disease risk: a cross-sectional study of US adults, PLOS Med., 13 Frayling, 2007, A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity, Science, 316, 889, 10.1126/science.1141634 Rhee, 2012, Early determinants of obesity: genetic, epigenetic, and in utero influences, Int. J. Pediatr., 2012 Luperini, 2015, Gene polymorphisms and increased DNA damage in morbidly obese women, Mutat. Res., 776, 111, 10.1016/j.mrfmmm.2015.01.004 Long, 2013, Evaluating genome-wide association study-identified breast cancer risk variants in African–American women, PLoS One, 8, 10.1371/journal.pone.0058350 Kusinska, 2012, Influence of genomic variation in FTO at 16q12.2, MC4R at 18q22 and NRXN3 at 14q31 genes on breast cancer risk, Mol. Biol. Rep., 39, 2915, 10.1007/s11033-011-1053-2 McCullough, 2015, Genetic polymorphisms in DNA repair and oxidative stress pathways may modify the association between body size and postmenopausal breast cancer, Ann. Epidemiol., 25, 263, 10.1016/j.annepidem.2015.01.009 Rupérez, 2014, Genetics of oxidative stress in obesity, Int. J. Mol. Sci., 15, 3118, 10.3390/ijms15023118 Stathopoulou, 2015, Genetic determinants of leucocyte telomere length in children: a neglected and challenging field, Paediatr. Perinat. Epidemiol., 29, 146, 10.1111/ppe.12173 Kwok, 2014, Bariatric surgery and its impact on cardiovascular disease and mortality: a systematic review and meta-analysis, Int. J. Cardiol., 173, 20, 10.1016/j.ijcard.2014.02.026 Ashrafian, 2015, Bariatric surgery or non-surgical weight loss for obstructive sleep apnoea? A systematic review and comparison of meta-analyses, Obes. Surg., 25, 1239, 10.1007/s11695-014-1533-2 Lassailly, 2015, Bariatric surgery reduces features of nonalcoholic steatohepatitis in morbidly obese patients, Gastroenterology, 149, 376 Rubino, 2010, Metabolic surgery to treat type 2 diabetes: clinical outcomes and mechanisms of action, Annu. Rev. Med., 61, 393, 10.1146/annurev.med.051308.105148 Casagrande, 2014, Incidence of cancer following bariatric surgery: systematic review and meta-analysis, Obes. Surg., 24, 1499, 10.1007/s11695-014-1276-0 Himbert, 2017, Effects of intentional weight loss on markers of oxidative stress, DNA repair and telomere length–a systematic review, Obes. Facts, 10, 648, 10.1159/000479972 Fejfer, 2017, Oxidative modification of biomolecules in the nonstimulated and stimulated saliva of patients with morbid obesity treated with bariatric surgery, Biomed. Res. Int., 2017, 10.1155/2017/4923769 Kocael, 2014, The effects on oxidative DNA damage of laparoscopic gastric band applications in morbidly obese patients, Can. J. Surg., 57, 183, 10.1503/cjs.008113 Mitterberger, 2014, Bariatric surgery and diet-induced long-term caloric restriction protect subcutaneous adipose-derived stromal/progenitor cells and prolong their life span in formerly obese humans, Exp. Gerontol., 56, 106, 10.1016/j.exger.2014.03.030 O’Callaghan, 2009, Weight loss in obese men is associated with increased telomere length and decreased abasic sites in rectal mucosa, Rejuvenation Res., 12, 169, 10.1089/rej.2008.0819 Formichi, 2014, Weight loss associated with bariatric surgery does not restore short telomere length of severe obese patients after 1 year, Obes. Surg., 24, 2089, 10.1007/s11695-014-1300-4 Bankoglu, 2017, Reduction of DNA damage in peripheral lymphocytes of obese patients after bariatric surgery-mediated weight loss, Mutagenesis García-Calzón, 2014, Telomere length as a biomarker for adiposity changes after a multidisciplinary intervention in overweight/obese adolescents: the EVASYON study, PLoS One, 9 Soares, 2016, Diet-induced weight loss reduces DNA damage and cardiometabolic risk factors in overweight/obese women with polycystic ovary syndrome, Ann. Nutr. Metab., 68, 220, 10.1159/000444130 Pardini, 2017, Increased micronucleus frequency in peripheral blood lymphocytes predicts the risk of bladder cancer, Br. J. Cancer, 116, 202, 10.1038/bjc.2016.411 Varga, 2006, On the difference of micronucleus frequencies in peripheral blood lymphocytes between breast cancer patients and controls, Mutagenesis, 21, 313, 10.1093/mutage/gel035 Santos, 2010, Basal levels of DNA damage detected by micronuclei and comet assays in untreated breast cancer patients and healthy women, Clin. Exp. Med., 10, 87, 10.1007/s10238-009-0079-4 Bolognesi, 2014, Clinical application of micronucleus test: a case-control study on the prediction of breast cancer risk/susceptibility. Scarfi MR, editor, PLoS One, 9 Maffei, 2014, Micronucleus frequency in human peripheral blood lymphocytes as a biomarker for the early detection of colorectal cancer risk, Mutagen, 29221 Aires, 2011, Micronuclei as biomarkers for evaluating the risk of malignant transformation in the uterine cervix, Genet. Mol. Res., 10, 1558, 10.4238/vol10-3gmr1156 Kiraz, 2016, Micronucleus testing as a cancer detector: endometrial hyperplasia to carcinoma, Arch. Gynecol. Obstet., 293, 1065, 10.1007/s00404-015-3867-y El-Zein, 2006, Cytokinesis-blocked micronucleus assay as a novel biomarker for lung cancer risk, Cancer Res., 66, 6449, 10.1158/0008-5472.CAN-06-0326 Chang, 2011, Micronuclei levels in peripheral blood lymphocytes as a potential biomarker for pancreatic cancer risk, Carcinogenesis, 32, 210, 10.1093/carcin/bgq247 Bonassi, 2007, An increased micronucleus frequency in peripheral blood lymphocytes predicts the risk of cancer in humans, Carcinogenesis, 28, 625 Moran, 2008, Genome instability is increased in lymphocytes of women with polycystic ovary syndrome and is correlated with insulin resistance, Mutat. Res. Mol. Mech. Mutagen., 639, 55, 10.1016/j.mrfmmm.2007.11.007 Murugaiyan, 2015, Urinary 8-hydroxydeoxyguanosine as a marker of oxidative stress induced genetic toxicity in oral cancer patients, Indian J. Dent. Res., 26, 226, 10.4103/0970-9290.162880 Kuo, 2007, Urinary 8-hydroxy-2′-deoxyguanosine (8-OHdG) and genetic polymorphisms in breast cancer patients, Mutat. Res. Toxicol. Environ. Mutagen., 631, 62, 10.1016/j.mrgentox.2007.04.009 Himmetoglu, 2009, DNA oxidation and antioxidant status in breast cancer, J. Investig. Med., 57, 720, 10.2310/JIM.0b013e3181adfb5b Chang, 2008, Evaluation of oxidative stress in colorectal cancer patients, Biomed. Environ. Sci., 21, 286, 10.1016/S0895-3988(08)60043-4 Guo, 2016, Association between oxidative DNA damage and risk of colorectal cancer: sensitive determination of urinary 8-hydroxy-2′-deoxyguanosine by UPLC–MS/MS analysis, Sci. Rep., 6, 32581, 10.1038/srep32581 Diakowska, 2007, Oxidative DNA damage and total antioxidant status in serum of patients with esophageal squamous cell carcinoma, Hepatogastroenterology, 54, 1701 PYLVÄS, 2011, Elevated serum 8-OHdG Is associated with poor prognosis in epithelial ovarian cancer, Anticancer Res., 31, 1411 Miyake, 2004, Oxidative Dna damage in patients with prostate cancer and its response to treatment, J. Urol., 171, 1533, 10.1097/01.ju.0000116617.32728.ca Zhao, 2015, Measurement of DNA damage in peripheral blood by the γ-H2AX assay as predictor of colorectal cancer risk, DNA Repair. (Amst.), 53, 24, 10.1016/j.dnarep.2017.03.001 YI-C, 2015, High expression of phospho-H2AX predicts a poor prognosis in colorectal cancer, Anticancer Res., 35, 2447 Kim, 2010, Double strand break of DNA in gastric adenoma and adenocarcinoma, Korean J. Gastroenterol., 55, 19, 10.4166/kjg.2010.55.1.19 Wasco, 2008, Expression of gamma-H2AX in melanocytic lesions, Hum. Pathol., 39, 1614, 10.1016/j.humpath.2008.03.007 Hu, 2015, Abnormal expression of DNA double-strand breaks related genes, ATM and GammaH2AX, in thyroid carcinoma, Int. J. Endocrinol., 2015 Kattimuthu, 2012, DNA damage in patients of carcinoma breast a clinical study by using comet assay, J. Anat. Soc. India, 61, 149, 10.1016/S0003-2778(12)80022-0 Schabath, 2003, Genetic instability in bladder cancer assessed by the comet assay, J. Natl. Cancer Inst., 95, 540, 10.1093/jnci/95.7.540 Rawat, 2018, Evaluation of DNA damage in peripheral blood leukocytes in oral potentially malignant and malignant disorders by comet assay, Clin. Cancer Investig. J., 7, 50, 10.4103/ccij.ccij_66_17 Buchynska, 2017, DNA damage in tumor cells and peripheral blood lymphocytes of endometrial cancer patients assessed by the comet assay, Exp. Oncol., 39, 299, 10.31768/2312-8852.2017.39(4):299-303 Shen, 2007, Short telomere length and breast cancer risk: a study in sister sets, Cancer Res., 67 Liu, 2009, Constitutive telomere length and gastric cancer risk: case-control analysis in Chinese Han population, Cancer Sci., 100, 1300, 10.1111/j.1349-7006.2009.01169.x Mirabello, 2010, Leukocyte telomere length in a population-based case–control study of ovarian cancer: a pilot study, Cancer Causes Control., 21, 77, 10.1007/s10552-009-9436-6 Meeker, 2002, Telomere shortening is an early somatic DNA alteration in human prostate tumorigenesis, Cancer Res., 62, 6405 Han, 2009, A prospective study of telomere length and the risk of skin cancer, J. Invest. Dermatol., 129, 415, 10.1038/jid.2008.238 Cassidy, 2010, Associations between diet, lifestyle factors, and telomere length in women, Am. J. Clin. Nutr., 91, 1273, 10.3945/ajcn.2009.28947 Lee, 2011, Inverse association between adiposity and telomere length: the fels longitudinal study, Am. J. Hum. Biol., 23, 100, 10.1002/ajhb.21109 Njajou, 2012, Shorter telomeres are associated with obesity and weight gain in the elderly, Int. J. Obes., 36, 1176, 10.1038/ijo.2011.196 Cui, 2013, Associations of leukocyte telomere length with body anthropometric indices and weight change in Chinese women, Obesity (Silver Spring), 21, 2582, 10.1002/oby.20321