Abstract
Emerging evidence from laboratory researches has highlighted the bioactivity of food melanoidins and melanoproteins. Whilst such studies have been carried out with different in vitro systems, information about melanoidins absorption and bio-availability are scarce. However, they are generally considered as poorly absorbable and bio-available compounds. Therefore, we present a review in which the gastro-intestinal tract is hypothesized to be the main site of action of food melanoidins and melanoproteins biological activity. We described recent data supporting this hypothesis both in vitro model systems and in vivo. Importantly, we focused this review only on the effect of melanoidins and melanoproteins extracted from food. Most of the studies had been carried out using water-soluble carbohydrate-based melanoidins isolated from different food sources (beer, barley coffee, coffee). In bakery products, melanoidins are protein-based structure (melanoproteins) which are largely insoluble in water. Dietary melanoidins and melanoproteins have been demonstrated to exert in vitro antioxidant and metal chelating ability in the gastro-intestinal tract reducing the formation of lipid hydroperoxides and advanced lipid oxidation end products during the digestion of meat. The reduction in the formation of these pro-atherogenic compounds has been shown to be followed by a decrease in their absorption in human volunteers. Food melanoidins have also shown in vitro anti-caries and prebiotic activities. We conclude by underlining the possible role of food melanoidins in the prevention of gastro-intestinal tract cancers. We hope this review will stimulate further research on food melanoidins and their biological activities in the gastro-intestinal tract.
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References
Acar O, Gokmen V, Pellegrini N et al (2009) Direct evaluation of the total antioxidant capacity of raw and roasted pulses, nuts and seeds. Eur J Food Sci Technol 229:961–969
Alamir I, Niquet-Leridon C, Jacolot P et al (2013) Digestibility of extruded proteins and metabolic transit of N-epsilon-carboxymethyllysine in rats. Amino Acids 44:1441–1449
Argirova MD, Stefanova ID, Krustev AD (2013) New biological properties of coffee melanoidins. Food Funct 4:1204–1208
Bekedam EK, Loots MJ, Schols HA et al (2008) Roasting effects on formation mechanisms of coffee brew melanoidins. J Agric Food Chem 56:7138–7145
Bellesia A, Tagliazucchi D (2014) Cocoa brew inhibits in vitro α-glucosidase activity: the role of polyphenols and high molecular compounds. Food Res Int 63:439–445
Borrelli RC, Fogliano V (2005) Bread crust melanoidins as potential prebiotic ingredients. Mol Nutr Food Res 49:673–678
Borrelli RC, Visconti A, Mennella C et al (2002) Chemical characterization and antioxidant properties of coffee melanoidins. J Agric Food Chem 50:6527–6533
Borrelli RC, Mennella C, Barba F et al (2003) Characterization of coloured compounds obtained by enzymatic extraction of bakery products. Food Chem Toxicol 41:1367–1374
Center MM, Jemal A, Ward E (2009) International trends in colorectal cancer incidence rates. Cancer Epidemiol Biomarkers Prev 18:1688–1694
Coelho C, Ribeiro M, Cruz ACS, Dominques MRM, Coimbra MA, Bunzel M, Nunes FM (2014) Nature of phenolic compounds in coffee melanoidins. J Agric Food Chem 62:7843–7853
Crowe FL, Key TJ, Appleby TN et al (2012) Dietary fibre intake and ischaemic hearth disease mortality: the European Prospective Investigation into Cancer and Nutrition-Hearth study. Eur J Clin Nutr 66:950–956
Daglia M, Tarsi R, Papetti A et al (2002) Antiadhesive effect of green and roasted coffee on Streptococcus mutans’ adhesive properties on saliva-coated hydroxyapatite beads. J Agric Food Chem 50:1225–1229
De Marco LM, Fischer S, Henle T (2011) High molecular weight coffee melanoidins are inhibitors for matrix metalloproteases. J Agric Food Chem 59:11417–11423
Del Pino-García R, González-SanJosé ML, Rivero-Pérez MD et al (2012) Influence of degree of roasting on the antioxidant capacity and genoprotective effect of instant coffee: contribution of the melanoidin fraction. J Agric Food Chem 60:10530–10539
Delgado-Andrade C (2014) Maillard reaction products: some considerations on their health effects. Clin Chem Lab Med 52:53–60
Delgado-Andrade C, Tessier FJ, Niquet-Leridon C et al (2013) Study of the urinary and faecal excretion of N (epsilon)-carboxymethyllysine in young human volunteers. Amino Acids 43:595–602
Edwards BK, Ward E, Kohler BA et al (2010) Annual report to the nation on the status of cancer, 1975–2006, featuring colorectal cancer trends and impact of interventions (risk factors, screening, and treatment) to reduce future rates. Cancer 116:544–573
Faist V, Erbersdobler HF (2001) Metabolic transit and in vivo effects of melanoidins and precursor compounds deriving from the Maillard reaction. Ann Nutr Met 45:1–12
Finot PA, Magnenat E (1981) Metabolic transit of early and advanced Maillard products. Prog Food Nutr Sci 5:193–207
Fogliano V, Morales FJ (2011) Estimation of dietary intake of melanoidins from coffee and bread. Food Funct 2:117–123
Förster A, Kühne Y, Henle T (2005) Studies on absorption and elimination of dietary Maillard reaction products. Ann N Y Acad Sci 1043:474–481
Gniechwitz D, Reichardt N, Meiss E et al (2008a) Characterization and fermentability of an ethanol soluble high molecular weight coffee fraction. J Agric Food Chem 56:5960–5969
Gniechwitz D, Reichardt N, Ralph J et al (2008b) Isolation and characterization of a coffee melanoidin fraction. J Sci Food Agric 88:2153–2160
Goya L, Delgado-Andrade C, Rufián-Henares JA et al (2007) Effect of coffee melanoidins on human hepatoma HepG2 cells. Protection against oxidative stress induced by tert-butylhydroperoxide. Mol Nutr Food Res 51:536–545
Hellwig M, Matthes R, Peto A, Löbner J, Henle T (2014) N-ε-fructosyllysine and N-ε-carboxymethyllysine, but bot lysinoalanine, are available for the absorption after simulated gastrointestinal digestion. Amino Acids 46:289–299
Hiramoto S, Itoh K, Shizuuchi S et al (2004) Melanoidin, a food protein-derived advanced Maillard reaction product, suppresses Helicobacter pylori in vitro and in vivo. Helicobacter 9:429–435
Hodge JE (1953) Chemistry of browning reactions in model systems. J Agric Food Chem 1:928–943
Icatlo FC, Kuroki M, Kobayashi C et al (2003) Affinity purification of Helicobacter pylori urease: relevance to gastric mucosa adherence by urease protein. J Biol Chem 273:18130–18138
Jaquet M, Rochat I, Moulin J et al (2009) Impact of coffee consumption on the gut microbiota: a human volunteer study. Int J Food Microbiol 130:117–121
Je Y, Liu W, Giovannucci E (2009) Coffee consumption and risk of colorectal cancer: a systematic review and meta-analysis of prospective cohort studies. Int J Cancer 124:1662–1668
Kuntcheva MJ, Obretenov TD (1996) Isolation and characterization of melanoidins from beer. Z Lebensm Unters Forsch 202:238–243
Lamb A, Chen LF (2013) Role of the Helicobacter pylori-induced inflammatory response in the development of gastric cancer. J Cell Biochem 114:491–497
Langner E, Nunes FM, Pożarowski P et al (2011) Antiproliferative activity of melanoidins isolated from heated potato fiber (Potex) in glioma cell culture model. J Agric Food Chem 59:2708–2716
Langner E, Nunes FM, Pożarowski P et al (2013) Melanoidins isolated from heated potato fiber (Potex) affect human colon cancer cells growth via modulation of cell cycle and proliferation regulatory proteins. Food Chem Toxicol 57:246–255
Leclercq C, Arcella D, Piccinelli R et al (2009) The Italian national food consumption survey INRAN-SCAI 2005–06: main results in terms of food consumption. Public Health Nutr 12:2504–2532
Li W, Khor TO, Xu C et al (2008) Activation of Nrf2-antioxidant signaling attenuates NF-κB-inflammatory response and elicits apoptosis. Biochem Pharmacol 76:1485–1489
Li G, Ma D, Zhang Y et al (2013) Coffee consumption and risk of colorectal cancer: a meta-analysis of observational studies. Public Health Nutr 16:346–357
Lindenmeier M, Faist V, Hofmann T (2002) Structural and functional characterization of pronyl-lysine, a novel protein modification in bread crust melanoidins showing in vitro antioxidative and Phase I/II enzyme modulating activity. J Agric Food Chem 50:6997–7006
Martin MA, Ramos S, Mateos R et al (2009) Biscuit melanoidins of different molecular masses protect human HepG2 cells against oxidative stress. J Agric Food Chem 57:7250–7258
Mesías M, Seiquer I, Navarro MP (2009a) Influence of diets rich in Maillard reaction products on calcium bioavailability. Assays in male adolescents and in Caco-2 cells. J Agric Food Chem 57:9532–9538
Mesías M, Seiquer I, Delgado-Andrade C et al (2009b) Intake of Maillard reaction products reduces iron bioavailability in male adolescents. Mol Nutr Food Res 53:1551–1560
Morales FJ, Somoza V, Fogliano V (2012) Physiological relevance of dietary melanoidins. Amino Acids 42:1097–1109
Moreira ASP, Fernando MN, Domingues R et al (2012) Coffee melanoidins: structures, mechanisms of formation and potential health impacts. Food Funct 3:903–915
Murphy N, Norat T, Ferrari P et al (2012) Dietary fibre intake and risks of cancers of the colon and rectum in the European Prospective Investigation into Cancer and Nutrition (EPIC). PLoS One 7:e39361
Nakano M, Kubota M, Owada S et al (2013) The pentosidine concentration in human blood specimens is affected by heating. Amino Acids 44:1451–1456
Nakayama T, Oishi K (2013) Influence of coffee (Coffea arabica) and galacto-oligosaccharide consumption on intestinal microbiota and the host response. FEMS Microbiol Lett 343:161–168
Nunes FM, Coimbra MA (2007) Melanoidins from coffee infusions: fractionation, chemical characterization, and effect of the degree of roast. J Agric Food Chem 55:3967–3977
Papetti A, Pruzzo C, Daglia M et al (2007) Effect of barley coffee on the adhesive properties of oral streptococci. J Agric Food Chem 55:278–284
Pastoriza S, Rufián-Henares JA (2014) Contribution of melanoidins to the antioxidant capacity of the Spanish diet. Food Chem 164:438–445
Pérez-Jiménez J, Díaz-Rubio ME, Mesías M, Morales FJ, Saura-Calixto F (2014) Evidence for the formation of maillardized insoluble dietary fiber in bread: a specific kind of dietary fiber in thermally processed food. Food Res Int 55:391–396
Reichardt N, Gniechwitz D, Steinhart H et al (2009) Characterization of high molecular weight coffee fractions and their fermentation by human intestinal microbiota. Mol Nutr Food Res 53:287–299
Rivero D, Pérez-Magariño S, González-Sanjosé ML et al (2005) Inhibition of induced DNA oxidative damage by beers: correlation with the content of polyphenols and melanoidins. J Agric Food Chem 53:3637–3642
Rombouts I, Lagrain B, Brijs K et al (2012) Cross-linking of wheat gluten proteins during production of hard pretzels. Amino Acids 42:2429–2438
Ronca G, Palmieri L, Maltinti S et al (2003) Relationship between iron and protein content of dish and polyphenol content in accompanying wines. Drugs Exp Clin Res 29:271–286
Roncero-Ramos I, Delgado-Andrade C, Alonso-Olalla R et al (2012) Effects of bread crust-derived Maillard reaction products on phosphorous balance in rats. Eur J Nutr 51:871–879
Roncero-Ramos I, Delgado-Andrade C, Haro A et al (2013a) Effects of dietary bread crust Maillard reaction products on calcium and bone metabolism in rats. Amino Acids 44:1409–1418
Roncero-Ramos I, Delgado-Andrade C, Morales FJ et al (2013b) Influence of Maillard products from bread crust on magnesium bioavailability in rats. J Sci Food Agric 93:2002–2007
Roncero-Ramos I, Delgado-Andrade C, Tessier FJ et al (2013c) Metabolic transit of N(ε)-carboxymethyl-lysine after consumption of AGEs from bread crust. Food Funct 4:1032–1039
Roncero-Ramos I, Niquet-Léridon C, Strauch C et al (2014) An advanced glycation end product (AGE)-rich diets promoted N(ε)-carboxymethyl-lysine accumulation in the cardiac tissue and tendons of rats. J Agric Food Chem 62:6001–6006
Rufián-Henares JA, Morales FJ (2007) Effect of in vitro enzymatic digestion on antioxidant activity of coffee melanoidins and fractions. J Agric Food Chem 55:10016–10021
Rufián-Henares JA, Morales FJ (2008a) Microtiter plate-based assay for screening antimicrobial activity of melanoidins against E. coli and S. aureus. Food Chem 111:1069–1074
Rufián-Henares JA, Morales FJ (2008b) Antimicrobial activity of melanoidins against Escherichia coli is mediated by a membrane-damage mechanism. J Agric Food Chem 56:2357–2362
Sauer T, Raithel M, Kressel J et al (2013) Activation of the transcription factor Nrf2 in macrophages, Caco-2 cells and intact human gut tissue by Maillard reaction products and coffee. Amino Acids 44:1427–1439
Saura-Calixto F (2011) Dietary fiber as a carrier of dietary antioxidants; an essential physiological function. J Agric Food Chem 59:43–49
Selvam JP, Aranganathan S, Nalini N (2009a) Inhibitory effect of bread crust antioxidant pronyl lysine on two different categories of colonic premalignant lelsions induced by 1,2-dimethylhydrazine. Eur J Cancer Prev 18:291–302
Selvam JP, Aranganathan S, Gopalan R et al (2009b) Chemopreventive efficacy of pronyl-lysine on lipid peroxidation and antioxidant status in rat colon carcinogenesis. Fundam Clin Pharmacol 23:293–302
Senadheera D, Cvitkovitch DG (2008) Quorum sensing and biofilm formation by Streptococcus mutans. Adv Exp Med Biol 631:178–188
Serpen A, Capuano E, Fogliano V, Gökmen V (2007) A new procedure to measure the antioxidant activity of insoluble food components. J Agric Food Chem 55:7676–7681
Silvan JM, Morales FJ, Saura-Calixto F (2010) Conceptual study on maillardized dietary fiber in coffee. J Agric Food Chem 58:12244–12249
Sirota R, Gorelik S, Harris RM et al (2013) Coffee polyphenols protect human plasma from postprandial carbonyl modifications. Mol Nutr Food Res 57:916–919
Slattery ML, Edwards SL, Boucher KM et al (1999) Lifestyle and colon cancer: an assessment of factors associated with risk. Am J Epidemiol 150:869–877
Somoza V, Wenzel E, Lindenmeier M et al (2005) Influence of feeding malt, bread crust, and a pronylated protein on the activity of chemopreventive enzymes and antioxidantive defense parameters in vivo. J Agric Food Chem 53:8176–8182
Somoza V, Wenzel E, Weiß C et al (2006) Dose-dependent utilization of casein-linked lysinoalanine, N(epsilon)-fructoselysine and N(epsilon)-carboxymethyllysine in rats. Mol Nutr Food Res 50:833–841
Stauder M, Papetti A, Mascherpa D et al (2010) Antiadhesion and antibiofilm activities of high molecular weight coffee components against Streptococcus mutans. J Agric Food Chem 58:11662–11666
Summa C, McCourt J, Cämmerer B 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
Tagliazucchi D, Verzelloni E (2014) Relationship between the chemical composition and the biological activities of food melanoidins. Food Sci Biotechnol 23:561–568
Tagliazucchi D, Verzelloni E, Conte A (2008) Antioxidant properties of traditional balsamic vinegar and boiled must model systems. Eur Food Res Technol 227:835–843
Tagliazucchi D, Verzelloni E, Conte A (2010) Effect of dietary melanoidins on lipid peroxidation during simulated gastro-intestinal digestion: their possible role in the prevention of oxidative damage. J Agric Food Chem 58:2513–2519
Verzelloni E, Tagliazucchi D, Conte A (2010) From balsamic to healthy: traditional balsamic vinegar melanoidins inhibit lipid peroxidation during simulated gastric digestion of meat. Food Chem Toxicol 48:2097–2102
Verzelloni E, Tagliazucchi D, Del Rio D et al (2011) Antiglycative and antioxidative properties of coffee fractions. Food Chem 124:1430–1435
Vitaglione P, Fogliano V, Pellegrini N (2012) Coffee, colon function, and colorectal cancer. Food Funct 3:916–922
Wang H, Qian H, Yao W (2011) Melanoidins produced by the Maillard reaction: structure and biological activity. Food Chem 128:573–584
Wilkinson J, Clapper ML (1997) Detoxification enzymes and chemoprevention. Proc Soc Exp Biol Med 216:192–200
Willett WC (1999) Goals for nutrition in the year 2000. CA Cancer J Clin 49:331–352
Yu X, Bao Z, Zou J et al (2011) Coffee consumption and risk of cancers: a meta-analysis of cohort studies. BMC Cancer 11:96
Zucker S, Vacirca J (2004) Role of matrix metalloproteinases (MMPs) in colorectal cancer. Cancer Metastasis Rev 23:101–117
Zucker S, Cao J, Chen WT (2000) Critical appraisal of the use of matrix metalloproteinase inhibitors in cancer treatment. Oncogene 56:6642–6650
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Tagliazucchi, D., Bellesia, A. The gastro-intestinal tract as the major site of biological action of dietary melanoidins. Amino Acids 47, 1077–1089 (2015). https://doi.org/10.1007/s00726-015-1951-z
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DOI: https://doi.org/10.1007/s00726-015-1951-z