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Effects of micronutrients on DNA repair

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Abstract

Background

DNA repair is an essential cellular function, which, by removing DNA damage before it can cause mutations, contributes crucially to the prevention of cancer. Interest in the influence of micronutrients on DNA repair activity is prompted by the possibility that the protective effects of fruits and vegetables might thus be explained. Two approaches to measuring repair—monitoring cellular removal of DNA damage and incubating cell extract with specifically damaged DNA in an in vitro assay—have been applied in cell culture, whole animal studies, and human trials. In addition, there are numerous investigations at the level of expression of DNA repair–related genes.

Results

Depending on the pathway studied and the phytochemical or food tested, there are varied reports of stimulation, inhibition or no effect on DNA repair. The clearest findings are from human supplementation trials in which lymphocytes are assessed for their repair capacity ex vivo. Studying cellular repair of strand breaks is complicated by the fact that lymphocytes appear to repair them very slowly. Applying the in vitro repair assay to human lymphocytes has revealed stimulatory effects on repair of oxidised bases by various micronutrients or a fruit- and vegetable-rich diet, while other studies have failed to demonstrate effects.

Conclusions

Despite varied results from different studies, it seems clear that micronutrients can influence DNA repair, usually but not always enhancing activity. Different modes of DNA repair are likely to be subject to different regulatory mechanisms. Measures of gene expression tend to be a poor guide to repair activity, and there is no substitute for phenotypic assays.

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References

  1. WCRF/AICR (2007) Food, nutrition, physical activity, and the prevention of cancer. American Institute for Cancer Research, Washington, pp 1–517

    Google Scholar 

  2. Møller P, Loft S (2006) Dietary antioxidants and beneficial effect on oxidatively damaged DNA. Free Rad Biol Med 41:388–415

    Article  Google Scholar 

  3. Hoelzl C, Knasmüller S, Misik M, Collins A, Dusinska M, Nersesyan A (2009) Use of single cell gel electrophoresis assays for the detection of DNA-protective effects of dietary factors in humans: recent results and trends. Mutat Res 681:68–79

    Article  CAS  Google Scholar 

  4. ESCODD, Gedik CM, Collins A (2005) Establishing the background level of base oxidation in human lymphocyte DNA: results of an interlaboratory validation study. FASEB J 19:82–84

    CAS  Google Scholar 

  5. D’Autréaux B, Toledano MB (2007) ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Natl Rev Mol Cell Biol 8:813–824

    Article  Google Scholar 

  6. Miller ER III, Pastor-Barriuso R, Dalal D, Riemersma RA, Appel LJ, Guallar E (2005) Meta-analysis: high-dosage vitamin E supplementation may increase all-cause mortality. Ann Intern Med 142:37–46

    CAS  Google Scholar 

  7. Bjelakovic G, Nikolova D, Gluud LL, Simonetti RG, Gluud C (2007) Mortality in randomized trials of antioxidant supplements for primary and secondary prevention: systematic review and meta-analysis. JAMA 297:842–857

    Article  CAS  Google Scholar 

  8. Hwang ES, Bowen PE (2007) DNA damage, a biomarker of carcinogenesis: its measurement and modulation by diet and environment. Crit Rev Food Sci Nutr 47:27–50

    Article  CAS  Google Scholar 

  9. Collins AR, Azqueta A (2012) DNA repair as a biomarker in human biomonitoring studies; further applications of the comet assay. Mutat Res. doi:10.1016/j.mrfmmm.2011.03.005

  10. Collins AR (2004) The comet assay for DNA damage and repair. Mol Biotech 26:249–261

    Article  CAS  Google Scholar 

  11. Collins AR, Horvathova E (2001) Oxidative DNA damage, antioxidants and DNA repair; applications of the comet assay. Biochem Soc Trans 29:337–341

    Article  CAS  Google Scholar 

  12. Paz-Elizur T, Elinger D, Leitner-Dagan Y, Blumenstein S, Krupsky M, Berrebi A, Schechtman E, Livneh Z (2007) Development of an enzymatic DNA repair assay for molecular epidemiology studies: distribution of OGG activity in healthy individuals. DNA Repair 6:45–60

    Article  CAS  Google Scholar 

  13. Elliott RM, Astley S, Southon S, Archer DB (2000) Measurement of cellular repair activities for oxidative DNA damage. Free Rad Biol Med 28:1438–1446

    Article  CAS  Google Scholar 

  14. Sauvaigo S, Guerniou V, Rapin D, Gasparutto D, Caillat S, Favier A (2004) An oligonucleotide microarray for the monitoring of repair enzyme activity toward different DNA base damage. Analyt Biochem 333:182–192

    Article  CAS  Google Scholar 

  15. Millau JF, Raffin AL, Caillat S, Claudet C, Arras G, Ugolin N, Douki T, Ravanat JL, Breton J, Oddos T, Dumontet C, Sarasin A, Chevillard S, Favier A, Sauvaigo S (2008) A microarray to measure repair of damaged plasmids by cell lysates. Lab Chip 8:1713–1722

    Article  CAS  Google Scholar 

  16. Collins AR, Dusinska M, Horvathova E, Munro E, Savio M, Stetina R (2001) Inter-individual differences in DNA base excision repair activity measured in vitro with the comet assay. Mutagenesis 16:297–301

    Article  CAS  Google Scholar 

  17. Langie SAS, Knaapen AM, Brauers KJJ, van Berlo D, van Schooten F-J, Godschalk RWL (2006) Development and validation of a modified comet assay to phenotypically assess nucleotide excision repair. Mutagenesis 21:153–158

    Article  CAS  Google Scholar 

  18. Gaivão 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 25:45–52

    Article  Google Scholar 

  19. Langie SA, Cameron KM, Waldron KJ, Fletcher KP, von Zglinicki T, Mathers JC (2011) Measuring DNA repair incision activity of mouse tissue extracts towards singlet oxygen-induced DNA damage: a comet-based in vitro repair assay. Mutagenesis 3:461–471

    Article  Google Scholar 

  20. Astley SB, Elliott RM, Archer DB, Southon S (2002) Increased cellular carotenoid levels reduce the persistence of DNA single-strand breaks after oxidative challenge. Nutr Cancer 43:202–213

    Article  CAS  Google Scholar 

  21. Glei M, Liegibel UM, Ebert MN, Böhm V, Pool-Zobel BL (2002) Beta-carotene reduces bleomycin-induced genetic damage in human lymphocytes. Toxicol Appl Pharm 179:65–73

    Article  CAS  Google Scholar 

  22. Lorenzo Y, Azqueta A, Luna L, Bonilla F, Dominguez G, Collins AR (2009) The carotenoid β-cryptoxanthin stimulates the repair of DNA oxidation damage in addition to acting as an antioxidant in human cells. Carcinogenesis 30:308–314

    Article  CAS  Google Scholar 

  23. Aherne SA, O’Brien NM (2000) Lack of effect of the flavonoids, myricetin, quercetin, and rutin, on repair of H2O2-induced DNA single-strand breaks in Caco-2, HepG2 and V79 cells. Nutr Cancer 38:106–115

    Article  CAS  Google Scholar 

  24. Duthie SJ, Collins AR, Duthie GG, Dobson VL (1997) Quercetin and myricetin protect against hydrogen peroxide-induced DNA damage (strand breaks and oxidised pyrimidines) in human lymphocytes. Mutat Res 393:223–231

    CAS  Google Scholar 

  25. Min K, Ebeler SE (2009) Quercetin inhibits hydrogen peroxide-induced DNA damage and enhances DNA repair in Caco-2 cells. Food Chem Toxicol 47:2716–2722

    Article  CAS  Google Scholar 

  26. Ramos AA, Azqueta A, Pereira-Wilson C, Collins AR (2010) Polyphenolic compounds from Salvia species protect cellular DNA from oxidation and stimulate DNA repair in cultured human cells. J Agric Food Chem 58:7465–7471

    Article  CAS  Google Scholar 

  27. Ramos AA, Pereira-Wilson C, Collins AR (2010) Protective effects of ursolic acid and luteolin against oxidative DNA damage include enhancement of DNA repair in Caco-2 cells. Mutat Res 692:6–11

    Article  CAS  Google Scholar 

  28. Bacon JR, Williamson G, Garner RC, Lappin G, Langouët S, Bao Y (2003) Sulforaphane and quercetin modulate PhIP-DNA adduct formation in human HepG2 cells and hepatocytes. Carcinogenesis 24:1903–1911

    Article  CAS  Google Scholar 

  29. Niture SK, Velu CS, Smith QR, Bhat GJ, Srivenugopal KS (2006) Increased expression of the MGMT repair protein mediated by cysteine prodrugs and chemopreventative natural products in human lymphocytes and tumor cell lines. Carcinogenesis 28:378–389

    Article  Google Scholar 

  30. Gatz SA, Keimling M, Baumann C, Dörk T, Debatin KM, Fulda S, Wiesmüller L (2008) Resveratrol modulates DNA double-strand break repair pathways in an ATM/ATR-p53- and -Nbs1-dependent manner. Carcinogenesis 29:519–527

    Article  CAS  Google Scholar 

  31. Williams JD, Jacobson MK (2010) Photobiological implications of folate depletion and repletion in cultured human keratinocytes. J Photochem Photobiol B Biol 99:49–61

    Article  CAS  Google Scholar 

  32. Bouhlel I, Valenti K, Kilani S, Skandrani I, Ben Sghaier M, Mariotte AM, Dijoux-Franca MG, Ghedira K, Hininger-Favier I, Laporte F, Chekir-Ghedira L (2008) Antimutagenic, antigenotoxic and antioxidant activities of Acacia salicina extracts (ASE) and modulation of cell gene expression by H2O2 and ASE treatment. Toxicol In Vitro 22:1264–1272

    Article  CAS  Google Scholar 

  33. Bagnyukova TV, Powell CL, Pavliv O, Tryndyak VP, Pogribny IP (2008) Induction of oxidative stress and DNA damage in rat brain by a folate/methyl-deficient diet. Brain Res 1237:44–51

    Article  CAS  Google Scholar 

  34. Duthie SJ, Grant G, Pirie LP, Watson AJ, Margison GP (2010) Folate deficiency alters hepatic and colon MGMT and OGG-1 DNA repair protein expression in rats but has no effect on genome-wide DNA methylation. Cancer Prev Res 3:92–100

    Article  CAS  Google Scholar 

  35. Klaude M, von der Decken A (1988) O6-methylguanine-DNA methyltransferase levels in tissues of methionine-cysteine deficient subadult and adult mice. Comp Biochem Physiol C 91:603–606

    Article  CAS  Google Scholar 

  36. Henning SM, Mckee RW, Swendseid ME (1989) Hepatic poly(ADP ribose) polymerase activity in methyl donor-deficient rats. J Nutr 119:1528–1531

    CAS  Google Scholar 

  37. Althaus FR, Kleczowska HE, Malanga M, Müntener CR, Pleschke JM, Ebner M, Auer B (1999) Poly ADP-ribosylation: a DNA break signal mechanism. Mol Cell Biochem 193:5–11

    Article  CAS  Google Scholar 

  38. James SJ, Miller BJ, Basnakian AG, Pogribny IP, Pogribna M, Muskhelishvili L (1997) Apoptosis and proliferation under conditions of deoxynucleotide pool imbalance in liver of folate/methyl deficient rats. Carcinogenesis 18:287–293

    Article  CAS  Google Scholar 

  39. Pogribny IP, Basnakian AG, Miller BJ, Lopatina NG, Poirier LA, James SJ (1995) Breaks in genomic DNA and within the p53 gene are associated with hypomethylation in livers of folate/methyl-deficient rats. Cancer Res 55:1894–1901 (Erratum in: Cancer Res 1995, 55:2711)

    CAS  Google Scholar 

  40. Zhang JZ, Henning SM, Swendseid ME (1993) Poly(ADP-Ribose) polymerase activity and DNA strand breaks are affected in tissues of niacin-deficient rats. J Nutr 123:1349–1355

    CAS  Google Scholar 

  41. Rawling JM, Jackson TM, Driscoll ER, Kirkland JB (1994) Dietary niacin deficiency lowers tissue poly(ADP-ribose) and NAD+ concentrations in Fischer-344 rats. J Nutr 124:1597–1603

    CAS  Google Scholar 

  42. Henning SM, Swendseid ME, Coulson WF (1997) Male rats fed methyl- and folate-deficient diets with or without niacin develop hepatic carcinomas associated with decreased tissue NAD concentrations and altered poly(ADP-ribose) polymerase activity. J Nutr 127:30–36

    CAS  Google Scholar 

  43. Song Y, Leonard SW, Traber MG, Ho E (2009) Zinc deficiency affects DNA damage, oxidative stress, antioxidant defenses, and DNA repair in rats. J Nutr 139:1626–1631

    Article  CAS  Google Scholar 

  44. Song Y, Elias V, Loban A, Scrimgeour AG, Ho E (2010) Marginal zinc deficiency increases oxidative DNA damage in the prostate after chronic exercise. Free Rad Biol Med 48:82–88

    Article  CAS  Google Scholar 

  45. Webster RP, Gawde MD, Bhattacharya RK (1996) Effect of different vitamin A status on carcinogen-induced DNA damage and repair enzymes in rats. In Vivo 10:113–118

    CAS  Google Scholar 

  46. Webster RP, Gawde MD, Bhattacharya RK (1996) Modulation by dietary copper of aflatoxin B1-induced activity of DNA repair enzymes poly (ADP-ribose) polymerase, DNA polymerase beta and DNA ligase. In Vivo 10:533–536

    CAS  Google Scholar 

  47. Sheng Y, Pero RW, Olsson AR, Bryngelsson C, Hua J (1998) DNA repair enhancement by a combined supplement of carotenoids, nicotinamide, and zinc. Cancer Det Prev 22:284–292

    Article  CAS  Google Scholar 

  48. Webster RP, Gawde MD, Bhattacharya RK (1996) Protective effect of rutin, a flavonol glycoside, on the carcinogen induced DNA damage and repair enzymes in rats. Cancer Lett 109:185–191

    Article  CAS  Google Scholar 

  49. Aiyer HS, Vadhanam MV, Stoyanova R, Caprio GD, Clapper ML, Gupta RC (2008) Dietary berries and ellagic acid prevent oxidative DNA damage and modulate expression of DNA repair genes. Int J Mol Sci 9:327–341

    Article  Google Scholar 

  50. Vaid M, Sharma SD, Katiyar SK (2010) Proanthocyanidins inhibit photocarcinogenesis through enhancement of DNA repair and xeroderma pigmentosum group A-dependent mechanism. Cancer Prev Res 3:1621–1629

    Article  CAS  Google Scholar 

  51. Croteau DL, de Souza-Pinto NC, Harboe C, Keijzers G, Zhang Y, Becker K, Sheng S, Bohr VA (2010) DNA repair and the accumulation of oxidatively damaged DNA are affected by fruit intake in mice. J Gerontol A Biol Sci Med Sci 65:1300–1311

    Article  Google Scholar 

  52. Langie SA, Kowalczyk P, Tudek B, Zabielski R, Dziaman T, Olinski R, van Schooten FJ, Godschalk RW (2010) The effect of oxidative stress on nucleotide-excision repair in colon tissue of newborn piglets. Mutat Res 1–2:75–80

    Google Scholar 

  53. Langie SAS, Kowalczyk P, Tomaszewski B, Maas LM, Moonen EJ, Godschalk RWL, Tudek B, van Schooten FJ, Zabielski R, Mathers JC (2012) Redox regulation and epigenetic regulation of the APE1 gene in the brain of young piglets: the effect of early life exposures. Abstracts from the 9th International Comet Assay Workshop held in Kusadasi, Turkey; 13–16 Sep 2011. Mutagenesis (in press)

  54. Taylor EM, Lehmann AR (1998) Conservation of eukaryotic DNA repair mechanisms. Int J Radiat Biol 74:277–286

    Article  CAS  Google Scholar 

  55. Collins AR, Ma A, Duthie SJ (1995) The kinetics of repair of oxidative DNA damage (strand breaks and oxidised pyrimidines) in human cells. Mutat Res 336:69–77

    CAS  Google Scholar 

  56. Collins AR, Duthie SJ, Fillion L, Gedik CM, Vaughan N, Wood SG (1997) Oxidative DNA damage in human cells: the influence of antioxidants and DNA repair. Biochem Soc Trans 25:326–331

    CAS  Google Scholar 

  57. Torbergsen AC, Collins AR (2000) Recovery of human lymphocytes from oxidative DNA damage; the apparent enhancement of DNA repair by carotenoids is probably simply an antioxidant effect. Eur J Nutr 39:80–85

    Article  CAS  Google Scholar 

  58. Astley S, Elliott RM, Archer DB, Southon S (2004) Evidence that dietary supplementation with carotenoids and carotenoid-rich foods modulates the DNA damage: repair balance in human lymphocytes. Br J Nutr 91:63–72

    Article  CAS  Google Scholar 

  59. Tomasetti M, Alleva R, Borghi B, Collins AR (2001) In vivo supplementation with coenzyme Q10 enhances the recovery of human lymphocytes from oxidative DNA damage. FASEB J 15:1425–1427

    CAS  Google Scholar 

  60. Guarnieri S, Loft S, Riso P, Porrini M, Risom L, Poulsen H, Dragsted LO, Møller P (2008) DNA repair phenotype and dietary antioxidant supplementation. Br J Nutr 99:1018–1024

    Article  CAS  Google Scholar 

  61. Collins AR, Harrington V, Drew J, Melvin R (2003) Nutritional modulation of DNA repair in a human intervention study. Carcinogenesis 24:511–515

    Article  CAS  Google Scholar 

  62. Brevik A, Karlsen A, Azqueta A, Estaban AT, Blomhoff R, Collins A (2011) Both base excision repair and nucleotide excision repair in humans are influenced by nutritional factors. Cell Biochem Funct 29:36–42

    Article  CAS  Google Scholar 

  63. Riso P, Martini D, Møller P, Loft S, Bonacina G, Moro M, Porrini M (2010) DNA damage and repair activity after broccoli intake in young healthy smokers. Mutagenesis 25:595–602

    Article  CAS  Google Scholar 

  64. Caple F, Williams EA, Spiers A, Tyson J, Burtle B, Daly AK, Mathers JC, Hesketh JE (2010) Inter-individual variation in DNA damage and base excision repair in young, healthy non-smokers: effects of dietary supplementation and genotype. Br J Nutr 103:1585–1593

    Article  CAS  Google Scholar 

  65. Basten GP, Duthie SJ, Pirie L, Vaughan N, Hill MH, Powers HJ (2006) Sensitivity of markers of DNA stability and DNA repair activity to folate supplementation in healthy volunteers. Br J Cancer 94:1942–1947

    Article  CAS  Google Scholar 

  66. Langie SAS, Wilms LC, Hämäläinen S, Kleinjans JCS, Godschalk RWL, van Schooten FJ (2010) Modulation of nucleotide excision repair in human lymphocytes by genetic and dietary factors. Br J Nutr 103:490–501

    Article  CAS  Google Scholar 

  67. Guarrera S, Sacerdote C, Fiorini L, Marsala R, Polidoro S, Gamberini S, Saletta F, Malaveille C, Talaska G, Vineis P, Matullo G (2007) Expression of DNA repair and metabolic genes in response to a flavonoid-rich diet. Br J Nutr 98:525–534

    Article  CAS  Google Scholar 

  68. Bøhn SK, Myhrstad MC, Thoresen M, Holden M, Karlsen A, Tunheim SH, Erlund I, Svendsen M, Seljeflot I, Moskaug JØ, Duttaroy AK, Laake P, Arnesen H, Tonstad S, Collins A, Drevon CA, Blomhoff R (2010) Blood cell gene expression associated with cellular stress defense is modulated by antioxidant-rich food in a randomised controlled clinical trial of male smokers. BMC Med. http://www.biomedcentral.com/1741-7015/8/54

  69. Møller P, Vogel U, Pedersen A, Dragsted LO, Sandström B, Loft S (2003) No effect of 600 grams fruit and vegetables per day on oxidative DNA damage and repair in healthy nonsmokers. Cancer Epi Biomark Prev 12:1016–1022

    Google Scholar 

  70. Premkumar VG, Yuvaraj S, Shanthi P, Sachdanandam P (2008) Co-enzyme Q10, riboflavin and niacin supplementation on alteration of DNA repair enzyme and DNA methylation in breast cancer patients undergoing tamoxifen therapy. Br J Nutr 100:1179–1182

    Article  CAS  Google Scholar 

  71. Mathers JC, Strathdee G, Relton CL (2010) Induction of epigenetic alterations by dietary and other environmental factors. In: Herceg Z, Ushijima T (eds) Advances in genetics, vol 71. Academic Press, Burlington, pp 1–39

    Google Scholar 

  72. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 1:6–21

    Article  Google Scholar 

  73. Jones PA, Takai D (2001) The role of DNA methylation in mammalian epigenetics. Science 293:1068–1070

    Article  CAS  Google Scholar 

  74. Zawia NH, Lahiri DK, Cardozo-Pelaez F (2009) Epigenetics, oxidative stress, and Alzheimer disease. Free Radic Biol Med 9:1241–1249

    Article  Google Scholar 

  75. Fang MZ, Wang Y, Ai N, Hou Z, Sun Y, Lu H, Welsh W, Yang CS (2003) Tea polyphenol (2)-epigallocatechin-3-gallate inhibits DNA methyltransferase and reactivates methylation-silenced genes in cancer cell lines. Cancer Res 63:7563–7570

    CAS  Google Scholar 

  76. Fang MZ, Chen D, Sun Y, Jin Z, Christman JK, Yang CS (2005) Reversal of hypermethylation and reactivation of p16INK4a, RARbeta, andMGMT genes by genistein and other isoflavones from soy. Clin Cancer Res 11:7033–7041

    Article  CAS  Google Scholar 

  77. Langie SA, Tomaszewski B, Cameron KM, Fletcher KP, Lisanti S, Godschalk RW, van Schooten FJ, von Zglinicki T, Mathers JC (2011) The ageing brain: effects on DNA repair and DNA methylation in mice. In: Abstracts of UKEMS/Dutch EMS-sponsored workshop on biomarkers of exposure and oxidative DNA damage and 7th GUM 32P-Postlabelling Workshop, Münster, Germany; March 28–29, 2011. Mutagenesis 26:706

  78. Halliwell B (1994) Free radicals, antioxidants, and human disease: curiosity, cause, or consequence? Lancet 344:721–724

    Article  CAS  Google Scholar 

  79. Dusinska M, Lietava J, Olmedilla B, Raslova K, Southon S, Collins AR (1999) Indicators of oxidative stress, antioxidants and human health. In: Basu TK, Temple NJ, Garg ML (eds) Antioxidants in human health. CAB International, Wallingford, pp 411–422

  80. Obtulowicz T, Swoboda M, Speina E, Gackowski D, Rozalski R, Siomek A, Janik J, Janowska B, Ciesla JM, Jawien A, Banaszkiewicz Z, Guz J, Dziaman T, Szpila A, Olinski R, Tudek B (2010) Oxidative stress and 8-oxoguanine repair are enhanced in colon adenoma and carcinoma patients. Mutagenesis 25:463–471

    Article  CAS  Google Scholar 

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Acknowledgments

AA thanks the Ministerio de Educación y Ciencia (‘Juan de la Cierva’ programme, 2009) of the Spanish Government for its contribution to the financial support for this work. The Centre for Brain Ageing & Vitality is funded through the Lifelong Health and Wellbeing cross-council initiative by the MRC, BBSRC, EPSRC and ESRC.

Conflict of interest

The authors declare that they have no conflict of interest in preparing this review article.

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Authors and Affiliations

  1. Department of Nutrition, Institute of Basic Medical Sciences, University of Oslo, Blindern, PB 1046, 0316, Oslo, Norway

    Andrew R. Collins

  2. Department of Nutrition, Food Science and Toxicology, Schools of Pharmacy and Sciences, University of Navarra, Irunlarrea 1, 31008, Pamplona, Spain

    Amaya Azqueta

  3. Centre for Brain Ageing and Vitality, Human Nutrition Research Centre, Institute for Ageing and Health, Newcastle University, Campus for Ageing and Vitality, Newcastle upon Tyne, NE4 5PL, UK

    Sabine A. S. Langie

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  1. Andrew R. Collins
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Correspondence to Andrew R. Collins.

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Collins, A.R., Azqueta, A. & Langie, S.A.S. Effects of micronutrients on DNA repair. Eur J Nutr 51, 261–279 (2012). https://doi.org/10.1007/s00394-012-0318-4

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