Abstract
The Maillard reaction, also called glycation, is one of the major chemical reactions responsible for most yellow-to-brown colors and aromas in cooked foods. This reaction between reducing sugars and amino functions on proteins affects not only the flavor of food, but also leads to the formation of an heterogenous group of structurally-modified amino acids. Some of these, known as “advanced glycation end products” (AGEs), have been found in both foods and human biological fluids, tissues and organs. Except for those that are formed over long periods in vivo at 37 °C, AGEs in the body originate from the digestion and absorption of dietary sources. A high or chronic exposure to dietary AGEs (dAGEs) is suspected as potentially detrimental to human health and studies in the field of food safety have begun to focus their attention on the metabolic transit of dAGEs. This review presents some important findings in this field, with a focus on NƐ-carboxymethyllysine, and presents the evidence for and against an association between intake of dAGEs and their presence in the body. New and promising avenues of research are described, and some future directions outlined.
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References
Finot, P.A., Bujard, E., Mottu, F., Mauron, J.: Availability of the true Schiff's bases of lysine. Chemical evaluation of the Schiff's base between lysine and lactose in milk. Adv. Exp. Med. Biol. 86B, 343–365 (1977)
Hellwig, M., Auerbach, C., Müller, N., Samuel, P., Kammann, S., Beer, F., Gunzer, F., Henle, T.: Metabolization of the Advanced Glycation End Product N-ε-Carboxymethyllysine (CML) by Different Probiotic E. coli Strains. J. Agric. Food Chem. 67, 1963–1972 (2019)
Liardon, L., De Weck-Gaudard, D., Philippossian, G., Finot, P.A.: Identification of N-epsilon-carboxymethyllysine: a new Maillard reaction product in rat urine. J. Agric. Food Chem. 35, 427–431 (1987)
Rérat, A., Calmes, R., Vaissade, P., Finot, P.A.: Nutritional and metabolic consequences of the early Maillard reaction of heat treated milk in the pig. Significance for man. Eur. J. Nutr. 41, 1–11 (2002)
Alamir, I., Niquet-Léridon, C., Jacolot, P., Rodriguez, C., Orosco, M., Anton, P.M., Tessier, F.J.: Digestibility of extruded proteins and metabolic transit of Nε-carboxymethyllysine in rats. Amino Acids. 44, 1441–1149 (2013)
Hellwig, M., Geissler, S., Matthes, R., Peto, A., Silow, C., Brandsch, M., Henle, T.: Transport of free and peptide-bound glycated amino acids: synthesis, transepithelial flux at Caco-2 cell monolayers, and interaction with apical membrane transport proteins. Chembiochem. 12, 1270–1279 (2011)
Tessier, F.J., Birlouez-Aragon, I.: Health effects of dietary Maillard reaction products – the results of ICARE and other studies. Amino Acids. 42, 1119–1131 (2012)
Birlouez-Aragon, I., Saavedra, G., Tessier, F.J., Galinier, A., Ait-Ameur, L., Lacoste, F., Niamba, C.N., Alt, N., Somoza, V., Lecerf, J.M.: A diet based on high-heat-treated foods promotes risk factors for diabetes mellitus and cardiovascular diseases. Am. J. Clin. Nutr. 91, 1–7 (2010)
Delgado-Andrade, C., Tessier, F.J., Niquet-Léridon, C., Seiquer, I., Navarro, P.: Study of the urinary and faecal excretion of ne-carboxymethyllysine in young human volunteers. Amino Acids. 43, 595–602 (2012)
Lacroix, M., Bon, C., Bos, C., Léonil, J., Benamouzig, R., Luengo, C., Fauquant, J., Tomé, D., Gaudichon, C.: Ultra high temperature treatment, but not pasteurization. Affects the Postprandial Kinetics of Milk Proteins in Humans. J. Nutr. 138, 2342–2347 (2008)
Seiquer, I., Diaz-Alguacil, J., Delgado-Andrade, C., Lopez-Frias, M., Munoz Hoyos, A., Galdo, G., Navarro, M.P.: Diets rich in Maillard reaction products affect protein digestibility in adolescent males aged 11–14 y. Am. J. Clin. Nutr. 83, 1082–1088 (2006)
Delgado-Andrade, C., Fogliano, V.: Dietary advanced glycosylation end-products (dAGEs) and Melanoidins formed through the Maillard reaction: physiological consequences of their intake. Annu. Rev. Food Sci. Technol. 9, 271–291 (2018)
Helou, C., Marier, D., Jacolot, P., Abdennebi-Najar, L., Niquet-Léridon, C., Tessier, F.J., Gadonna-Widehem, P.: Microorganisms and Maillard reaction products: a review of the literature and recent findings. Amino Acids. 46, 267–277 (2014)
Helou, C., Denis, S., Spatz, M., Marier, D., Rame, V., Alric, M., Tessier, F.J., Gadonna-Widehem, P.: Insights into bread melanoidins: fate in the upper digestive tract and impact on the gut microbiota using in vitro system. Food Funct. 6, 3737–3745 (2015)
Borrelli, R., Fogliano, V.: Bread crust melanoidins as potential prebiotic ingredients. Mol. Nutr. Food Res. 49, 673–678 (2005)
Gniechwitz, D., Reichardt, N., Meiss, E., Ralph, J., Steinhart, H., Blaut, M., Bunzel, M.: Characterization and fermentability of an ethanol soluble high molecular weight coffee fraction. J. Agric. Food Chem. 56, 5960–5969 (2008)
Koschinsky, T., He, C.J., Mitsuhashi, T., Bucala, R., Liu, C., Buenting, C., Heitmann, K., Vlassara, H.: Orally absorbed reactive glycation products (glycotoxins): an environmental risk factor in diabetic nephropathy. Proc. Natl. Acad. Sci. U. S. A. 94, 6474–6479 (1997)
Faist, V., Erbersdobler, H.F.: Metabolic transit and in vivo effects of melanoidins and precursor compounds deriving from the Maillard reaction. Ann. Nutr. Metab. 45, 1–12 (2001)
Förster, A., Kühne, Y., Henle, T.: Studies on absorption and elimination of dietary Maillard reaction products. Ann. N.Y. Acad. Sci. 1043, 474–481 (2005)
Finot, P.A.: The absorption and metabolism of modified amino acids in processed foods. J. AOAC Int. 88, 894–903 (2005)
Tessier, F.J., Niquet, C., Rhazi, L., Hedhili, K., Navarro, P., Seiquer, I., Delgado-Andrade, C.: NƐ-carboxymethyllysine: it’s origin in selected foods and its urinary and faecal excretion in healthy humans. In Maillard Reaction: Interface between Aging, Nutrition and Metabolism. Merlin Thomas & Forbes (Eds.): RSC Publishing, Special publication No. 332, 144–150 (2010)
Erbersdobler, H.F., Gunsser, I., Weber, G.: Abbau von Fructoselysin durch die darmflora. Zentralbl. Vet. Med. A17, 573–575 (1970)
Souba, W.W., Pacitti, A.J.: How amino acids get into cells: mechanisms, models, menus, and mediators. J. Parenter. Enter. Nutr. 16, 569–578 (1992)
Semba, R.D., Ang, A., Talegawkar, S., Crasto, C., Dalal, M., Jardack, P., Traber, M.G., Ferrucci, L., Arab, L.: Dietary intake associated with serum versus urinary carboxymethyl-lysine, a major advanced glycation end product, in adults: the energetics study. Eur. J. Clin. Nutr. 66, 3–9 (2012)
Karachalias, N., Babaei-Jadidi, R., Rabbani, N., Thornalley, P.: Increased protein damage in renal glomeruli, retina, nerve, plasma and urine and its prevention by thiamine and benfotiamine therapy in a rat model of diabetes. Diabetologia. 53, 1506–1516 (2010)
Scheijen, J.L.J.M., Hanssen, N.M.J., van Greevenbroek, M.M., Van der Kallen, C.J., Feskens, E.J.M., Stehouwer, C.D.A., Schalkwijk, C.G.: Dietary intake of advanced glycation endproducts is associated with higher levels of advanced glycation endproducts in plasma and urine: the CODAM study. Clin. Nutr. 37, 919–925 (2018)
Roncero-Ramos, I., Delgado-Andrade, C., Tessier, F.J., Niquet-Léridon, C., Strauch, C., Monnier, V.M., Navarro, M.P.: Metabolic transit of Nε-carboxymethyl-lysine after consumption of AGEs from bread crust. Food Funct. 4, 1032–1039 (2013)
Bergmann, R., Helling, R., Heichert, C., Scheunemann, M., Mäding, P., Wittrisch, H., Johannsen, B., Henle, T.: Radio fluorination and positron emission tomography (PET) as a new approach to study the in vivo distribution and elimination of the advanced glycation endproducts N epsilon-carboxymethyllysine (CML) and N epsilon-carboxyethyllysine (CEL). Nahrung. 45, 182–188 (2001)
Xu, H., Wang, Z., Wang, Y., Hu, S., Liu, N.: Biodistribution and elimination study of Fluorine-18 labeled ne-Carboxymethyl-lysine following Intragastric and intravenous administration. PLoS One. 8, e57897 (2013)
Scholz, G., Baumeyer, A., Buetler, T., Latado, H., Moser, M., Foerster, A., Henle, T.: Metabolic fate (ADME) study of 14C-labeled specific AGE-modified β- lactoglobulin preparations in Sprague Dawley rats. Abstract book of the 11th International Symposium on the Maillard reaction 2012; S4.4: 183
Tessier, F.J., Niquet-Léridon, C., Jacolot, P., Jouquand, C., Genin, M., Schmidt, A.M., Grossin, N., Boulanger, E.: Quantitative assessment of organ distribution of dietary protein-bound 13 C-labeled Nɛ -carboxymethyllysine after a chronic oral exposure in mice. Mol. Nutr. Food Res. 60, 2446–2456 (2016)
Guilbaud, A., Howsam, M., Niquet-Léridon, C., Delguste, F., Fremont, M., Lestavel, S., Maboudou, P., Garat, A., Schraen, S., Onraed, B., Foligné, B., Boulanger, E., Tessier, F.J.: The effect of Lactobcaillus fermentum ME-3 treatment on glycation and diabetic complications. Mol. Nutr. Food Res. 64, 1901018 (2020). https://doi.org/10.1002/mnfr.201901018
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Tessier, F.J., Boulanger, E. & Howsam, M. Metabolic transit of dietary advanced glycation end-products - the case of NƐ-carboxymethyllysine. Glycoconj J 38, 311–317 (2021). https://doi.org/10.1007/s10719-020-09950-y
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DOI: https://doi.org/10.1007/s10719-020-09950-y