Skip to main content
Log in

Pro-oxidative effects of melanoidin–copper complexes on isolated and cellular DNA

  • Original paper
  • Published:
European Food Research and Technology Aims and scope Submit manuscript

Abstract

High molecular weight Maillard reaction products (melanoidins) are described to possess metal-chelating properties. Whereas in food systems, this ability contributes to antioxidant properties, the consequences on biological systems are not quite clear. The study was aimed to evaluate the implication of metal complexation by melanoidins on DNA damage. Melanoidins prepared with d-glucose and different l-amino acids under water-free reaction conditions were charged with cupric ions. The effect on isolated DNA was investigated by the PM2 assay and on cellular systems in the human colon carcinoma cell line HCT-116 by alkaline unwinding. Independent of the amino acid composition, pure melanoidins (MW >14 kDa) did not cause significant DNA damage. By charging melanoidins with Cu2+ ions, a considerable DNA strand breaking activity was detectable, which was again amplified in an oxidative milieu (addition of hydrogen peroxide). Since Cu2+ normally does not provoke the formation of reactive oxygen species (ROS) via Fenton-type reaction, the results obtained have to be attributed to reducing properties of melanoidins. Thus, in melanoidin–copper complexes redox cycling may take place leading to Cu+ which subsequently undergoes Fenton-type and Haber–Weiss reactions. As a consequence, ROS are formed, which may explain the generation of DNA strand breaks.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Gomyo T, Horikoshi M (1976) On the interaction of melanoidin with metallic ions. Agr Biol Chem 40:33–40

    Article  CAS  Google Scholar 

  2. Rendleman JA Jr (1987) Complexation of calcium by melanoidin and its role in determining bioavailability. J Food Sci 52:1699–1705

    Article  CAS  Google Scholar 

  3. Morales FJ, Fernandez-Fraguas C, Jimenez-Perez S (2005) Iron-binding ability of melanoidins from food and model systems. Food Chem 90:821–827

    Article  CAS  Google Scholar 

  4. Wijewickreme AN, Kitts DD, Durance TD (1997) Reaction conditions influence the elementary composition and metal chelating affinity of nondialyzable model Maillard reaction products. J Agric Food Chem 45:4577–4583

    Article  CAS  Google Scholar 

  5. O’Brien J, Morrissey PA (1997) Metal ion complexation by products of the Maillard reaction. Food Chem 58:17–27

    Article  Google Scholar 

  6. Rendleman JA, Inglett GE (1990) The influence of Cu2+ in the Maillard reaction. Carbohydr Res 201:311–326

    Article  CAS  Google Scholar 

  7. Cosovic B, Vojvodic V, Boskovic N, Plavsic M, Lee C (2010) Characterization of natural and synthetic humic substances (melanoidins) by chemical composition and adsorption measurements. Org Geochem 41:200–205

    Article  CAS  Google Scholar 

  8. Plavsic M, Cosovic B, Lee C (2006) Copper complexing properties of melanoidins and marine humic material. Sci Total Environ 366:310–319

    Article  CAS  Google Scholar 

  9. Yoshimura Y, Iijima T, Watanabe T, Nakazawa H (1997) Antioxidative effect of Maillard reaction products using glucose-glycine model system. J Agric Food Chem 45:4106–4109

    Article  CAS  Google Scholar 

  10. Borrelli RC, Fogliano V, Monti SM, Ames JM (2002) Characterization of melanoidins from a glucose-glycine model system. Eur Food Res Technol 215:210–215

    Article  CAS  Google Scholar 

  11. Delgado-Andrade C, Seiquer I, Navarro MP (2004) Bioavailability of iron from a heat treated glucose-lysine model food system: assays in rats and in Caco-2 cells. J Sci Food Agric 84:1507–1513

    Article  CAS  Google Scholar 

  12. Seiquer I, Aspe T, Vaquero P, Navarro MP (2001) Effects of heat treatment of casein in the presence of reducing sugars on calcium bioavailability: in vitro and in vivo assays. J Agric Food Chem 49:1049–1055

    Article  CAS  Google Scholar 

  13. Garcia MM, Seiquer I, Delgado-Andrade C, Galdo G, Navarro MP (2009) Intake of Maillard reaction products reduces iron bioavailability in male adolescents. Mol Nutr Food Res 53:1551–1560

    Article  CAS  Google Scholar 

  14. Homma S, Murata M (1995) Characterization of metal-chelating compounds in instant coffee. In: ASIC, 19th Colloque, Kyoto, pp 183–191

  15. Navarro PM, Aspe T, Seiquer I (2000) Zinc transport in Caco-2 cells and zinc balance in rats: influence of the heat treatment of a casein-glucose-fructose mixture. J Agric Food Chem 48:3589–3596

    Article  CAS  Google Scholar 

  16. Wijewickreme AN, Kitts DD (1997) Influence of reaction conditions on the oxidative behavior of model Maillard reaction products. J Agric Food Chem 45:4571–4576

    Article  CAS  Google Scholar 

  17. Rivero D, Perez-Magarino S, Gonzales-Sanjose ML, Valls-Belles V, Codoner P, Muniz P (2005) Inhibition of induced DNA oxidative damages by beers: correlation with the content of polyphenols and melanoidins. J Agric Food Chem 53:3637–3642

    Article  CAS  Google Scholar 

  18. Rehner G, Walter T (1991) Wirkung von Maillard Produkten und Lysinoalanin auf die Bioverfügbarkeit von Eisen, Kupfer und Zink. Z Ernährungswiss 30:50–55

    Article  CAS  Google Scholar 

  19. Maillard M-N, Billaud C, Chow Y-N, Ordonaud C, Nicolas J (2007) Free radical scavenging, inhibition of polyphenoloxidase activity and copper chelating properties of model Maillard systems. LWT Food Sci Technol 40:1434–1444

    Article  CAS  Google Scholar 

  20. Rufián-Henares JA, de la Cueva SP (2009) Antimicrobial activity of coffee melanoidins-a study of their metal-chelating properties. J Agric Food Chem 57:432–438

    Article  Google Scholar 

  21. Einarsson H, Snygg BG, Eriksson C (1983) Inhibition of bacterial growth by Maillard reaction products. J Agric Food Chem 31:1043–1047

    Article  CAS  Google Scholar 

  22. Rufian-Henares JA, Morales FJ (2008) Antimicrobial activity of melanoidins against Escherichia coli is mediated by a membrane-damage mechanism. J Agric Food Chem 56:2357–2362

    Article  Google Scholar 

  23. Cämmerer B, Kroh LW (1995) Investigation of the influence of reaction conditions on the elementary composition of melanoidins. Food Chem 53:55–59

    Article  Google Scholar 

  24. Schwerdtle T, Walter I, Mackiw I, Hartwig A (2003) Induction of oxidative DNA damage by arsenite and its trivalent and pentavalent methylated metabolites in cultured human cells and isolated DNA. Carcinogenesis 24:967–974

    Article  CAS  Google Scholar 

  25. Hartwig A, Dally H, Schlepegrell R (1996) Sensitive analysis of oxidative DNA damage in mammalian cells: use of the bacterial Fpg protein in combination with alkaline unwinding. Toxicol Lett 88:85–90

    Article  CAS  Google Scholar 

  26. Rohn S, Rawel HM, Kroll J (2004) Antioxidant activity of protein-bound quercetin. J Agric Food Chem 52:4725–4729

    Article  CAS  Google Scholar 

  27. Cämmerer B, Kroh LW (1996) Investigation of the contribution of radicals to the mechanism of the early stage of the Maillard reaction. Food Chem 57:217–221

    Article  Google Scholar 

  28. Yen G-C, Liao C-M, Wu S-C (2002) Influence of Maillard reaction products on DNA damage in human lymphocytes. J Agric Food Chem 50:2970–2976

    Article  CAS  Google Scholar 

  29. Taylor JLS et al (2004) Gentoxicity of melanoidin fractions derived from a standard glucose/glycine model. J Agric Food Chem 52:318–323

    Article  CAS  Google Scholar 

  30. Wagner K-H, Reichhold S, Koschutnig K, Chériot S, Billaud C (2007) The potential antimutagenic and antioxidant effects of Maillard reaction products used as “natural antibrowning” agents. Mol Nutr Food Res 51:496–504

    Article  CAS  Google Scholar 

  31. Glösl S et al (2004) Genotoxicity and mutagenicity of melanoidins isolated from a roasted glucose-glycine model in human lymphocyte cultures, intestinal Caco-2 cells and in the Salmonella typhimurium strains TA98 and TA102 applying the AMES test. Food Chem Toxicol 42:1487–1495

    Article  Google Scholar 

  32. Cheriot S, Billaud C, Pöchtrager S, Wagner K-H, Nicolas J (2009) A comparison study between antioxidant and mutagenic properties of cysteine glucose-derived Maillard reaction products and neoformed products from heated cysteine and hydroxymethylfurfural. Food Chem 114:132–138

    Article  CAS  Google Scholar 

  33. Yen G-C, Tsai L-C, Lii J-D (1992) Antimutagenic effect of Maillard Browning products obtained from amino acids and sugars. Food Chem Toxicol 30:127–132

    CAS  Google Scholar 

  34. Summa C et al (2008) Radical scavenging activity, anti-bacterial and mutagenic effects of cocoa bean Maillard reaction products with degree of roasting. Mol Nutr Food Res 52:342–351

    Article  CAS  Google Scholar 

  35. Manzocco L, Calligaris S, Mastrocola D, Nicoli MC, Lerici CR (2001) Review of nonenzymatic browning and antioxidant capacity in processed foods. Trends Food Sci Technol 11:340–346

    Article  Google Scholar 

  36. Rufián-Hernares JA, Delgado-Andrade C, Moralez FJ (2006) Assessing the antioxidant and pro-oxidant activity of phenolic compounds by means of their copper reducing activity. Eur Food Res Technol 223:225–231

    Article  Google Scholar 

  37. Gunther MR, Hanna PM, Mason RP, Cohen MS (1995) Hydroxyl radical formation from cuprous ion and hydrogen peroxide: a spin-trapping study. Arch Biochem Biophys 316:515–522

    Article  CAS  Google Scholar 

  38. Kennedy LJ, Moore K, Caulfield JL, Tannenbaum SR, Dedon PC (1997) Quantitation of 8-oxoguanine and strand breaks produced by four oxidizing agents. Chem Res Toxicol 10:386–392

    Article  CAS  Google Scholar 

  39. Schwerdtle T et al (2007) Impact of copper on the induction and repair of oxidative DNA damage, poly(ADP-ribosyl)ation and PARP-1 activity. Mol Nutr Food Res 51:201–210

    Article  CAS  Google Scholar 

  40. Hamann I, Schwerdtle T, Hartwig A (2009) Establishment of a non-radioactive cleavage assay to assess the DNA repair capacity towards oxidatively damaged DNA in subcellular and cellular systems and the impact of copper. Mutat Res 669:122–130

    Article  CAS  Google Scholar 

  41. Macomber L, Rensing C, Imlay JA (2007) Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli. J Bacteriol 189:1616–1626

    Article  CAS  Google Scholar 

  42. Gorren ACF, Schrammel A, Schmidt K, Mayer B (1996) Decomposition of S-nitrosoglutathione in the presence of copper ions and glutathione. Arch Biochem Biophys 330:219–228

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bettina Cämmerer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cämmerer, B., Chodakowski, K., Gienapp, C. et al. Pro-oxidative effects of melanoidin–copper complexes on isolated and cellular DNA. Eur Food Res Technol 234, 663–670 (2012). https://doi.org/10.1007/s00217-012-1675-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00217-012-1675-1

Keywords

Navigation