Effects of combined physical exercise training on DNA damage and repair capacity: role of oxidative stress changes

Abstract

Regular physical exercise has been shown to be one of the most important lifestyle influences on improving functional performance, decreasing morbidity and all causes of mortality among older people. However, it is known that acute physical exercise may induce an increase in oxidative stress and oxidative damage in several structures, including DNA. Considering this, the purpose of this study was to identify the effects of 16 weeks of combined physical exercise in DNA damage and repair capacity in lymphocytes. In addition, we aimed to investigate the role of oxidative stress involved in those changes. Fifty-seven healthy men (40 to 74 years) were enrolled in this study. The sample was divided into two groups: the experimental group (EG), composed of 31 individuals, submitted to 16 weeks of combined physical exercise training; and the control group (CG), composed of 26 individuals, who did not undergo any specifically orientated physical activity. We observed an improvement of overall physical performance in the EG, after the physical exercise training. A significant decrease in DNA strand breaks and FPG-sensitive sites was found after the physical exercise training, with no significant changes in 8-oxoguanine DNA glycosylase enzyme activity. An increase was observed in antioxidant activity, and a decrease was found in lipid peroxidation levels after physical exercise training. These results suggest that physical exercise training induces protective effects against DNA damage in lymphocytes possibly related to the increase in antioxidant capacity.

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References

  1. ACSM. American College of Sports Medicine position stand (2009) Progression models in resistance training for healthy adults. Med Sci Sports Exerc 41(3):687–708

    Article  Google Scholar 

  2. Akcay T, Saygili I, Andican G, Yalcin V (2003) Increased formation of 8-hydroxy-2′-deoxyguanosine in peripheral blood leukocytes in bladder cancer. Urol Int 71(3):271–274

    CAS  PubMed  Article  Google Scholar 

  3. Alessio HM (1993) Exercise-induced oxidative stress. Med Sci Sport Exer 25(2):218–224

    CAS  Article  Google Scholar 

  4. Ascensao A, Magalhaes J, Soares J, Oliveira J, Duarte JA (2003) Exercise and cardiac oxidative stress. Rev Port Cardiol 22(5):651–678

    PubMed  Google Scholar 

  5. Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78(2):547–581

    CAS  PubMed  Google Scholar 

  6. Cadore EL, Izquierdo M, Alberton CL et al (2012) Strength prior to endurance intra-session exercise sequence optimizes neuromuscular and cardiovascular gains in elderly men. Exp Gerontol 47(2):164–169

    PubMed  Article  Google Scholar 

  7. Chodzko-Zajko WJ, Proctor DN, Fiatarone Singh MA et al (2009) American College of Sports Medicine position stand. Exercise and physical activity for older adults. Med Sci Sports Exerc 41(7):1510–1530

    PubMed  Article  Google Scholar 

  8. Collins AR, Gaivao I (2007) DNA base excision repair as a biomarker in molecular epidemiology studies. Mol Asp Med 28(3–4):307–322

    CAS  Article  Google Scholar 

  9. Collins AR, Gedik CM, Olmedilla B, Southon S, Bellizzi M (1998) Oxidative DNA damage measured in human lymphocytes: large differences between sexes and between countries, and correlations with heart disease mortality rates. FASEB J 12(13):1397–1400

    CAS  PubMed  Google Scholar 

  10. Collins AR, Oscoz AA, Brunborg G et al (2008) The comet assay: topical issues. Mutagenesis 23(3):143–151

    CAS  PubMed  Article  Google Scholar 

  11. Craig CL, Marshall AL, Sjostrom M et al (2003) International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 35(8):1381–1395

    PubMed  Article  Google Scholar 

  12. Donnelly JE, Blair SN, Jakicic JM, Manore MM, Rankin JW, Smith BK, American College of Sports Medicine Position Stand (2009) Appropriate physical activity intervention strategies for weight loss and prevention of weight regain for adults. Med Sci Sports Exerc 41(2):459–471

    PubMed  Article  Google Scholar 

  13. Fenech M, Bonassi S (2011) The effect of age, gender, diet and lifestyle on DNA damage measured using micronucleus frequency in human peripheral blood lymphocytes. Mutagenesis 26(1):43–49

    CAS  PubMed  Article  Google Scholar 

  14. Fisher-Wellman K, Bloomer RJ (2009) Acute exercise and oxidative stress: a 30-year history. Dyn Med 8:1

    PubMed Central  PubMed  Article  Google Scholar 

  15. Fogarty MC, Hughes CM, Burke G et al (2011) Exercise-induced lipid peroxidation: implications for deoxyribonucleic acid damage and systemic free radical generation. Environ Mol Mutagen 52(1):35–42

    CAS  PubMed  Article  Google Scholar 

  16. Gaivao I, Piasek A, Brevik A, Shaposhnikov S, Collins AR (2009) Comet assay-based methods for measuring DNA repair in vitro; estimates of inter- and intra-individual variation. Cell Biol Toxicol 25(1):45–52

    CAS  PubMed  Article  Google Scholar 

  17. Garber CE, Blissmer B, Deschenes MR et al (2011) American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc 43(7):1334–1359

    PubMed  Article  Google Scholar 

  18. Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177(2):751–766

    CAS  PubMed  Google Scholar 

  19. Halliwell B (2000) Why and how should we measure oxidative DNA damage in nutritional studies? How far have we come? Am J Clin Nutr 72(5):1082–1087

    CAS  PubMed  Google Scholar 

  20. Hannon-Fletcher MP, O’Kane MJ, Moles KW, Weatherup C, Barnett CR, Barnett YA (2000) Levels of peripheral blood cell DNA damage in insulin dependent diabetes mellitus human subjects. Mutat Res 460(1):53–60

    CAS  PubMed  Article  Google Scholar 

  21. Huang Y, Zhang M, Zou H et al (2013) Genetic damage and lipid peroxidation in workers occupationally exposed to organic bentonite particles. Mutat Res 751(1):40–44

    CAS  PubMed  Article  Google Scholar 

  22. Huang XY, Eungpinichpong W, Silsirivanit A, Nakmareong S, Wu XH (2014) Tai chi improves oxidative stress response and DNA damage/repair in young sedentary females. J Phys Ther Sci 26(6):825–829

    PubMed Central  PubMed  Article  Google Scholar 

  23. Izquierdo M, Ibanez J, HA K, Kraemer WJ, Larrion JL, Gorostiaga EM (2004) Once weekly combined resistance and cardiovascular training in healthy older men. Med Sci Sports Exerc 36(3):435–443

    PubMed  Article  Google Scholar 

  24. Izquierdo M, Hakkinen K, Ibanez J, Kraemer WJ, Gorostiaga EM (2005) Effects of combined resistance and cardiovascular training on strength, power, muscle cross-sectional area, and endurance markers in middle-aged men. Eur J Appl Physiol 94(1–2):70–75

    PubMed  Article  Google Scholar 

  25. Jiang J, Zhou J, Yao Y et al (2013) Copy number variations of DNA repair genes and the age-related cataract: Jiangsu Eye Study. Invest Ophthalmol Vis Sci 54(2):932–938

    CAS  PubMed  Article  Google Scholar 

  26. Kasai H, Crain PF, Kuchino Y, Nishimura S, Ootsuyama A, Tanooka H (1986) Formation of 8-hydroxyguanine moiety in cellular DNA by agents producing oxygen radicals and evidence for its repair. Carcinogenesis 7(11):1849–1851

    CAS  PubMed  Article  Google Scholar 

  27. Kemi OJ, Haram PM, Loennechen JP et al (2005) Moderate vs. high exercise intensity: differential effects on aerobic fitness, cardiomyocyte contractility, and endothelial function. Cardiovasc Res 67(1):161–172

    CAS  PubMed  Article  Google Scholar 

  28. Lambertucci RH, Levada-Pires AC, Rossoni LV, Curi R, Pithon-Curi TC. Effects of aerobic exercise training on antioxidant enzyme activities and mRNA levels in soleus muscle from young and aged rats. Mech Ageing Dev. Dec 23 2006

  29. Lombard DB, Chua KF, Mostoslavsky R, Franco S, Gostissa M, Alt FW (2005) DNA repair, genome stability, and aging. Cell 120(4):497–512

    CAS  PubMed  Article  Google Scholar 

  30. Lopes C, Aro A, Azevedo A, Ramos E, Barros H (2007) Intake and adipose tissue composition of fatty acids and risk of myocardial infarction in a male Portuguese community sample. J Am Diet Assoc 107(2):276–286

    CAS  PubMed  Article  Google Scholar 

  31. Malins DC, Johnson PM, Wheeler TM, Barker EA, Polissar NL, Vinson MA (2001) Age-related radical-induced DNA damage is linked to prostate cancer. Cancer Res 61(16):6025–6028

    CAS  PubMed  Google Scholar 

  32. Matsuo T, Saotome K, Seino S, et al. Low-volume, high-intensity, aerobic interval exercise for sedentary adults: [Formula: see text]O, cardiac mass, and heart rate recovery. Eur J Appl Physiol. Jun 11 2014

  33. Mergener M, Martins MR, Antunes MV et al (2009) Oxidative stress and DNA damage in older adults that do exercises regularly. Clin Biochem 42(16–17):1648–1653

    CAS  PubMed  Article  Google Scholar 

  34. Metcalf BS, Curnow JS, Evans C, Voss LD, Wilkin TJ (2002) Technical reliability of the CSA activity monitor: the earlybird study. Med Sci Sports Exerc 34(9):1533–1537

    PubMed  Article  Google Scholar 

  35. Mota MP, Peixoto FM, Soares JF et al (2010) Influence of aerobic fitness on age-related lymphocyte DNA damage in humans: relationship with mitochondria respiratory chain and hydrogen peroxide production. Age (Dordr) 32(3):337–346

    CAS  Article  Google Scholar 

  36. Nakamoto H, Kaneko T, Tahara S et al (2007) Regular exercise reduces 8-oxodG in the nuclear and mitochondrial DNA and modulates the DNA repair activity in the liver of old rats. Exp Gerontol 42(4):287–295

    CAS  PubMed  Article  Google Scholar 

  37. Nalapareddy K, Jiang H, Guachalla Gutierrez LM, Rudolph KL (2008) Determining the influence of telomere dysfunction and DNA damage on stem and progenitor cell aging: what markers can we use? Exp Gerontol 43(11):998–1004

    CAS  PubMed  Article  Google Scholar 

  38. Ortenblad N, Madsen K, Djurhuus MS (1997) Antioxidant status and lipid peroxidation after short-term maximal exercise in trained and untrained humans. Am J Physiol 272(4 Pt 2):R1258–R1263

    CAS  PubMed  Google Scholar 

  39. Ozgen M, Reese RN, Tulio AZ, Scheerens JC, Miller AR (2006) Modified 2,2-azino-bis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS) method to measure antioxidant capacity of selected small fruits and comparison to ferric reducing antioxidant power (FRAP) and 2,2′-diphenyl-1-picrylhydrazyl (DPPH) methods. J Agr Food Chem 54(4):1151–1157

    CAS  Article  Google Scholar 

  40. Parise G, Brose AN, Tarnopolsky MA (2005) Resistance exercise training decreases oxidative damage to DNA and increases cytochrome oxidase activity in older adults. Exp Gerontol 40(3):173–180

    CAS  PubMed  Article  Google Scholar 

  41. Peddireddy V, Siva Prasad B, Gundimeda SD, Penagaluru PR, Mundluru HP (2012) Assessment of 8-oxo-7, 8-dihydro-2′-deoxyguanosine and malondialdehyde levels as oxidative stress markers and antioxidant status in non-small cell lung cancer. Biomarkers 17(3):261–268

    CAS  PubMed  Article  Google Scholar 

  42. Radak Z, Taylor AW, Ohno H, Goto S (2001) Adaptation to exercise-induced oxidative stress: from muscle to brain. Exerc Immunol Rev 7:90–107

    CAS  PubMed  Google Scholar 

  43. Radak Z, Kumagai S, Nakamoto H, Goto S (2007) 8-Oxoguanosine and uracil repair of nuclear and mitochondrial DNA in red and white skeletal muscle of exercise-trained old rats. J Appl Physiol 102(4):1696–1701

    CAS  PubMed  Article  Google Scholar 

  44. Rikli RE, Jones CJ (1999) Development and validation of a functional fitness test for community-residing older adults. J Aging Phys Activ 7(2):129–161

    Google Scholar 

  45. Shigenaga MK, Hagen TM, Ames BN (1994) Oxidative damage and mitochondrial decay in aging. Proc Natl Acad Sci U S A 91(23):10771–10778

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  46. Siu PM, Pei XM, Teng BT, Benzie IF, Ying M, Wong SH (2011) Habitual exercise increases resistance of lymphocytes to oxidant-induced DNA damage by upregulating expression of antioxidant and DNA repairing enzymes. Exp Physiol 96(9):889–906

    CAS  PubMed  Article  Google Scholar 

  47. Su S, Yao Y, Zhu R et al (2013) The associations between single nucleotide polymorphisms of DNA repair genes, DNA damage, and age-related cataract: Jiangsu Eye Study. Invest Ophthalmol Vis Sci 54(2):1201–1207

    CAS  PubMed  Article  Google Scholar 

  48. Takeshima N, Rogers ME, Islam MM, Yamauchi T, Watanabe E, Okada A (2004) Effect of concurrent aerobic and resistance circuit exercise training on fitness in older adults. Eur J Appl Physiol 93(1–2):173–182

    PubMed  Article  Google Scholar 

  49. Trigo M, Canudo N, Branco F, Silva D (2010) Estudo das propriedades psicométricas da perceived stress scale (PSS) na população portuguesa. Psychologica 53:353–378

    Article  Google Scholar 

  50. Trost SG, McIver KL, Pate RR (2005) Conducting accelerometer-based activity assessments in field-based research. Med Sci Sports Exerc 37(11):S531–S543

    PubMed  Article  Google Scholar 

  51. UNESCO. Universal declaration on bioethics and human rights. 2006; http://unesdoc.unesco.org/images/0014/001461/146180E.pdf

  52. Vincent HK, Bourguignon C, Vincent KR (2006) Resistance training lowers exercise-induced oxidative stress and homocysteine levels in overweight and obese older adults. Obesity 14(11):1921–1930

    CAS  PubMed  Article  Google Scholar 

  53. Willett WC (1998) Invited commentary: comparison of food frequency questionnaires. Am J Epidemiol 148:1157–1159, discussion 1162-1155

    CAS  PubMed  Article  Google Scholar 

  54. Wills ED. Evaluation of lipid peroxidation in lipids and biological membranes. Biochemical Toxicology: A practical Approach ed. Oxford: IRL1987

  55. Wilson DM, Sofinowski TM, McNeill DR (2003) Repair mechanisms for oxidative DNA damage. Front Biosci 8:963–981

    Article  Google Scholar 

  56. Wilson DM 3rd, Bohr VA, McKinnon PJ (2008) DNA damage, DNA repair, ageing and age-related disease. Mech Ageing Dev 129(7–8):349–352

    CAS  PubMed Central  PubMed  Article  Google Scholar 

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Funding

This work was supported by the Foundation of Science and Technology (FCT) for the research grant SFRH/BD/66438/2009 to JS and for the project entitled Physical exercise role on humans’ lymphocytes DNA damage reduction: possible influence of oxidative stress and DNA repair capacity PTDC/DES/121575/2010. We also would like to acknowledge FCT and FEDER/COMPETE under the references PEst-C/AGR/UI4033/2014.

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Correspondence to Jorge Pinto Soares.

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Soares, J.P., Silva, A.M., Oliveira, M.M. et al. Effects of combined physical exercise training on DNA damage and repair capacity: role of oxidative stress changes. AGE 37, 61 (2015). https://doi.org/10.1007/s11357-015-9799-4

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Keywords

  • Physical exercise training
  • DNA damage
  • FPG-sensitive sites
  • DNA repair
  • Antioxidant capacity
  • MDA