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N ε-(carboxymethyl)-l-lysine content in cheese, meat and fish products is affected by the presence of copper during elaboration process

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Abstract

Formation of dietary advanced glycation end products has been extensively studied, principally with the aim to decrease their intake. In this work, the relationship between copper potentially present during food elaboration and N ε-(carboxymethyl)-l-lysine (CML) concentrations, has been examined for the first time. For CML determination, a reversed phase liquid chromatography-electrospray ionization-ion trap tandem mass spectrometry procedure, based on acid hydrolysis, ethyl chloroformate derivatization and quantification in MRM mode was set-up, yielding method quantification limit of 98 µg kg−1; copper was determined by ICP-MS. For eleven commercial cheeses, CML and Cu were found in the ranges 3.70–8.58 µg g−1 and 0.08–15.5 µg g−1, respectively, suggesting an inverse relation between these two parameters. For beef, chicken, Mexican pork “carnitas” and salmon, the CML concentration was lower in the item cooked in Cu casserole while element concentration was increased, as compared to this same raw material prepared in Teflon™ (except for “carnitas”). Concentration-dependent effect of Cu, manifest by decreased CML formation, was confirmed evaluating conversion percentage of chemically protected lysine (ZLys) to ZCML in the absence and in the presence of different Cu concentrations (50.0% and 20.4% conversion for Cu:ZLys molar ratio 0:1 and 0.04:1, respectively). Consistent results obtained in the analysis of three different sample types point to the inhibitory effect of copper during CML formation; however, it should be stressed that Cu is only one parameter within a complex set of factors/conditions involved in glycation process. Although better understanding of the observed effect at molecular level is needed, the results obtained in this work strongly suggest beneficial effect of copper, inhibiting glycation process during food elaboration.

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References

  1. Poulsen MW, Hedegaard RV, Andersen JM, de Courten B, Bügel S, Nielsen J, Skibsted LH, Dragsted LO (2013) Advanced glycation end products in food and their effects on health. Food Chem Toxicol 60:10–37

    Article  CAS  Google Scholar 

  2. Lapolla A, Traldi P, Fedel D (2005) Importance of measuring products of non-enzymatic glycation of proteins. Clin Biochem 38:103–115

    Article  CAS  Google Scholar 

  3. Ames JM (2008) Determination of N ε-(carboxymethyl)lysine in foods and related systems. Ann N Y Acad Sci 1126:20–24

    Article  CAS  Google Scholar 

  4. Tessier JF (2010) The Maillard reaction in the human body. The main discoveries and factors that affect glycation. Pathol Biol 58:214–219

    Article  CAS  Google Scholar 

  5. Nguyen HT, van der Fels-Klerx HJ, van Boekel MAJS (2014) N-(carboxymethyl)lysine: a review on analytical methods, formation, and occurence in processed food, and health impact. Food Rev Int 30:36–52

    Article  CAS  Google Scholar 

  6. Thorpe SR, Bayens JW (2002) CML: a brief history. Int Congr Ser 1245:91–99

    Article  CAS  Google Scholar 

  7. Tessier FJ, Birlouez-Aragon I (2012) Health effects of dietary Maillard reaction products: the results of ICARE and other studies. Amino Acids 42:1119–1131

    Article  CAS  Google Scholar 

  8. Vistoli G, De Maddis D, Cipak A, Zarkovic N, Carini M, Aldini G (2013) Advanced glycoxidation and lipoxidation end products (AGEs and ALEs): an overview of their mechanisms of formation. Free Radic Res 47(Suppl. 1):3–27

    Article  CAS  Google Scholar 

  9. Bodiga VL, Eda SR, Bodiga S (2014) Advanced glycation end products: role in pathology of diabetic cardiomyopathy. Heart Fail Rev 19:49–63

    Article  CAS  Google Scholar 

  10. Kumar Pasupulati A, Chitra PS, Reddy GB (2016) Advanced glycation end products mediated cellular and molecular events in the pathology of diabetic nephropathy. Biomol Concepts 7:293–309

    Article  CAS  Google Scholar 

  11. Van Puyvelde K, Mets T, Njemini R, Beyer I, Bautmans I (2014) Effect of advanced glycation end product intake on inflammation and aging: a systematic review. Nutr Rev 72:638–650

    Article  Google Scholar 

  12. Delgado-Andrade C (2016) Carboxymethyl-lysine: thirty years of investigation in the field of AGE formation. Food Funct 7:46–57

    Article  CAS  Google Scholar 

  13. Hull GLJ, Woodside JV, Ames JM, Cusk GJ (2013) Validation study to compare effects of processing protocols on measured N ε-(carboxymethyl)lysine and N ε-(carboxyethyl)lysine in blood. J Clin Biochem Nutr 53:129–133

    Article  CAS  Google Scholar 

  14. Hull GLJ, Woodside JV, Ames JM, Cuskelly GJ (2012) N ε-(carboxymethyl)lysine content of foods commonly consumed in a Western style diet. Food Chem 131:170–174

    Article  CAS  Google Scholar 

  15. Assar S, Moloney C, Lima M, Magee R, Ames JM (2009) Determination of N ε-(carboxymethyl)lysine in food systems by ultra performance liquid chromatography–mass spectrometry. Amino Acids 36:317–326

    Article  CAS  Google Scholar 

  16. Chen G, Smith JS (2015) Determination of advanced glycation endproducts in cooked meat products. Food Chem 168:190–195

    Article  CAS  Google Scholar 

  17. Scheijen JLJM, Clevers E, Engelen L, Dagnelie PC, Brouns F, Stehouwer CDA, Schalkwijk CG (2016) Analysis of advanced glycation endproducts in selected food items by ultra-performance liquid chromatography tandem mass spectrometry: presentation of a dietary AGE database. Food Chem 190:1145–1150

    Article  CAS  Google Scholar 

  18. Sun X, Tang J, Wang J, Rasco BA, Lai K, Huang Y (2016) Formation of N ε-carboxymethyllysine and N ε-carboxyethyllysine in ground beef during heating as affected by fat, nitrite and erythorborate. J Food Meas Charact. doi:10.1007/s11694-016-9400-6

    Google Scholar 

  19. Zhou Y, Lin Q, Jin C, Cheng L, Zheng X, Dai M, Zhang Y (2015) Simultaneous analysis of N ε-(carboxymethyl)lysine and N ε-(carboxyethyl)lysine in foods by ultra-performance liquid chromatography-mass spectrometry with derivatization by 9-fluorenylmethyl chloroformate. J Food Sci 80:C207–C217

    Article  CAS  Google Scholar 

  20. Srey C, Hull GL, Connolly L, Elliott CT, del Castillo MD, Ames JM (2010) Effect of inhibitor compounds on Nε-(carboxymethyl) lysine (CML) and N ε-(carboxyethyl) lysine (CEL) formation in model foods. J Food Agric Chem 58:12036–12041

    Article  CAS  Google Scholar 

  21. Roldan M, Loebner J, Degen J, Henle T, Antequera T, Ruiz-Carrascal J (2015) Advanced glycation end products, physico-chemical and sensory characteristics of cooked lamb loins affected by cooking method and addition of flavour precursors. Food Chem 168:487–495

    Article  CAS  Google Scholar 

  22. Akıllıoglu HG, Gökmen V (2016) Kinetic evaluation of the inhibition of protein glycation during heating. Food Chem 196:1117–1124

    Article  Google Scholar 

  23. Wilker D, Heinrich AB, Kroh LW (2015) Model studies on the antioxidative effect of polyphenols in thermally treated d-glucose/l-alanine solutions with added metal ions. J Agric Food Chem 63:10973–10979

    Article  CAS  Google Scholar 

  24. Nashalian O, Yaylayan VA (2015) Sugar-conjugated bis(glycinato)copper(II) complexes and their modulating influence on the Maillard reaction. J Agric Food Chem 63:4353–4360

    Article  CAS  Google Scholar 

  25. Ramonaityte DT, Keršiene M, Adams A, Tehrani KA, De Kimpe N (2009) The interaction of metal ions with Maillard reaction products in a lactose–glycine model system. Food Res Int 42:331–336

    Article  CAS  Google Scholar 

  26. Baraka-Vidot J, Navarra G, Leone M, Bourdon E, Militello V, Rondeau P (2014) Deciphering metal-induced oxidative damages on glycated albumin structure and function. Biochim Biophys Acta 1840:1712–1724

    Article  CAS  Google Scholar 

  27. Arasteh A, Farahi S, Habibi-Rezaei M, Moosavi-Movahedi AA (2014) Glycated albumin: an overview of the in vitro models of an in vivo potential disease marker. J Diabetes Metab Disord 13:49. doi:10.1186/2251-6581-13-49

    Article  Google Scholar 

  28. Ramirez Segovia AS, Wrobel K, Acevedo Aguilar FJ, Corrales Escobosa AR, Wrobel K (2017) Effect of Cu(II) on in vitro glycation of human serum albumin by methylglyoxal: a LC–MS-based proteomic approach. Metallomics 9:132–140

    Article  CAS  Google Scholar 

  29. Rodríguez LM, Alatossava T (2008) Effects of copper supplement on growth and viability of strains used as starters and adjunct cultures for Emmental cheese manufacture. J Appl Microbiol 105:1098–1106

    Article  Google Scholar 

  30. Rodriguez ML, Ritvanen T, Joutsjoki V, Rekonen J, Alatossava T (2011) The role of copper in the manufacture of Finnish Emmental cheese. J Dairy Sci 94:4831–4842

    Article  Google Scholar 

  31. Gomez Ojeda A, Wrobel K, Corrales Escobosa AR, Torres Elguera JC, Garay-Sevilla ME, Wrobel K (2015) Molybdenum and copper in four varieties of common bean (Phaseolus vulgaris): new data of potential utility in designing healthy diet for diabetic patients. Biol Trace Elem Res 163:244–254

    Article  Google Scholar 

  32. ICH (2012) ICH harmonized tripartite guideline. Validation of analytical procedures: text and methodology (Q2/R1). http://www.ish.org/fileadmin/Public_Web_Site/ICH_Products/Guidelines/Quality/Q2_R1/Step4/Q2_R1_Guideline.pdf. Accessed 20 Apr 2017

  33. Jaramillo Ortiz S, Wrobel K, Corrales Escobosa AR, Wrobel K (2015) Effect of different chemical agents on the formation of N ε-carboxymethyl-lysine using glyoxylic acid a universal metabolite associated with the development and progression of diabetes. Acta Univ 25:17–21

    Google Scholar 

  34. Husek P (1998) Chloroformates in gas chromatography as general purpose derivatizing agents. J Chromatogr B 717:57–91

    Article  CAS  Google Scholar 

  35. Petrovic R, Futas J, Chandoga J, Jakus V (2005) Rapid and simple method for determination of N ε-(carboxymethyl)lysine and N ε-(carboxyethyl)lysine in urine using gas chromatography/mass spectrometry. Biomed Chromatogr 19:649–654

    Article  CAS  Google Scholar 

  36. Bakircioglu D, Kurtulus YB, Ucar G (2011) Determination of some traces metal levels in cheese samples packaged in plastic and tin containers by ICP-OES after dry, wet and microwave digestion. Food Chem Toxicol 49:202–207

    Article  CAS  Google Scholar 

  37. Montanari A (2015) Inorganic contaminants of food as a function of packaging features. In: Barona C, Bolzani L, Caruso G, Monatanri A, Parisi S, Steinka I (eds) Food packaging hygiene. Springer International Publishing, pp 17–41

  38. Lemos Batista B, Grotto D, Hornos Carneiro MF, Barbosa FJ (2012) Evaluation of the concentration of nonessential and essential elements in chicken, pork, and beef samples produced in Brazil. J Toxicol Environ Health Part A 75:1269–1279

    Article  Google Scholar 

  39. Gerber N, Brogioli R, Hattendorf B, Scheeder MRL, Wenk C, Gunther D (2009) Variability of selected trace elements of different meat cuts determined by ICP-MS and DRC-ICPMS. Animal 3:166–172

    Article  CAS  Google Scholar 

  40. Saiki MK, Martin BA, Thompson LD, Welsh D (2001) Copper, cadmium, and zinc concentrations in juvenile chinook salmon and selected fish-forage organisms (aquatic insects) in the upper Sacramento River, California. Water Air Soil Pollut 132:127–139

    Article  CAS  Google Scholar 

  41. Uribarri J, Woodruff S, Goodman S, Cai W, Chen X, Pyzik R, Yong A, Striker GE, Vlassara H (2010) Advanced glycation end products in foods and a practical guide to their reduction in the diet. J Am Diet Assoc 110:911–916

    Article  Google Scholar 

  42. Tanaka A, Kaneto H, Miyatsuka T, Yamamoto K, Yoshiuchi K, Yamasaki Y, Shimomura I, Matsuoka TA, Matsuhisa M (2009) Role of copper ion in the pathogenesis of type 2 diabetes. Endocr J 56:699–706

    Article  CAS  Google Scholar 

  43. Meyer JA, Spencer DM (2009) A perspective on the role of metals in diabetes: past findings and possible future directions. Metallomics 1:32–49

    Article  CAS  Google Scholar 

  44. Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology 283:65–87

    Article  CAS  Google Scholar 

  45. Tarwadi KV, Agte VV (2011) Effect of micronutrients on methylglyoxal-mediated in vitro glycation of albumin. Biol Trace Elem Res 143:717–725

    Article  CAS  Google Scholar 

  46. Saari JT, Dahlen GM (1999) Early and advanced glycation end-products are increased in dietary copper deficiency. J Nutr Biochem 10:210–214

    Article  CAS  Google Scholar 

  47. Conato C, Contino A, Maccarrone G, Magri A, Remelli M, Tabbi G (2000) Copper(II) complexes with l-lysine and l-ornithine: is the side-chain involved in the coordination? A thermodynamic and spectroscopic study. Thermochim Acta 362:13–23

    Article  CAS  Google Scholar 

  48. Argirova MD, Ortwerth BJ (2003) Activation of protein-bound copper ions during early glycation: study on two proteins. Arch Biochem Biophys 420:176–184

    Article  CAS  Google Scholar 

  49. Nashalian O, Yaylayan VA (2014) Thermally induced oxidative decarboxylation of copper complexes of amino acids and formation of Strecker aldehyde. J Agric Food Chem 62:8518–8523

    Article  CAS  Google Scholar 

  50. Corrales Escobosa AR, Wrobel K, Yanez Barrientos E, Jaramillo Ortiz S, Ramirez Segovia AS, Wrobel K (2015) Effect of different glycation agents on Cu(II) binding to human serum albumin studied by liquid chromatography, nitrogen microwave plasma atomic emission spectrometry, inductively coupled plasma mass spectrometry and high resolution molecular mass spectrometry. Anal Bioanal Chem 407:1149–1157

    Article  CAS  Google Scholar 

  51. Seneviratne C, Dombi GW, Liu W, Dain JA (2011) The in vitro glycation of human serum albumin in the presence of Zn (II). J Inorg Biochem 105:1548–1554

    Article  CAS  Google Scholar 

  52. Macru A, Stanila A, Rusu D, Rusu M, Cozar O, David L (2007) Spectroscopic studies of copper (II) complexes with some amino acids. J Optron Adv Mater 9:741–746

    Google Scholar 

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Acknowledgements

The financial support from National Council of Science and Technology, Mexico (CONACYT), Project 123732, is gratefully acknowledged. The authors thankfully acknowledge the support from the University of Guanajuato, Projects 800/2016 and 721/2016.

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Authors and Affiliations

  1. Department of Chemistry, University of Guanajuato, L. de Retana 5, 36000, Guanajuato, Mexico

    Sarahi Jaramillo Ortiz, Kazimierz Wrobel, Francisco Javier Acevedo-Aguilar, Alma Rosa Corrales Escobosa, Eunice Yanez Barrientos & Katarzyna Wrobel

  2. Department of Medical Sciences, University of Guanajuato, L. de Retana 5, 36000, Guanajuato, Mexico

    Armando Gomez Ojeda & Ma Eugenia Garay-Sevilla

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  1. Sarahi Jaramillo Ortiz
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  2. Kazimierz Wrobel
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Correspondence to Katarzyna Wrobel.

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Jaramillo Ortiz, S., Wrobel, K., Gomez Ojeda, A. et al. N ε-(carboxymethyl)-l-lysine content in cheese, meat and fish products is affected by the presence of copper during elaboration process. Eur Food Res Technol 244, 225–234 (2018). https://doi.org/10.1007/s00217-017-2949-4

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