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Reactions of QuinonesMechanisms, Structures, and Prospects for Food Research Andreas Schieber*
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Institute of Nutritional and Food Sciences, Molecular Food Technology, University of Bonn, Endenicher Allee 19b, D-53115 Bonn, Germany ABSTRACT: Oxidation of plant phenolics leads to quinones, which are unstable intermediates that may react with nucleophiles. Quinones play an important role in the enzymatic browning of fruits and vegetables and may form covalent adducts with amino acids, peptides, and proteins. These reactions may alter both the physicochemical and immunological properties of food proteins. Quinones trap odoriferous compounds and contribute to the formation of aroma compounds through Strecker degradation of amino acids. Oxidative dimerization of chlorogenic acids in the presence of amino acids leads to the formation of green benzacridines, which are a promising alternative to chlorophylls as food colorants. KEYWORDS: phenolic compounds, reactions, quinones, Michael addition, benzacridines
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INTRODUCTION Plants are sessile organisms and lack the ability to escape from stresses by changing their habitats. Therefore, they need to develop different strategies for their survival. For this purpose, plants produce an enormous number of secondary metabolites in an effort to protect themselves against various types of biotic and abiotic stresses, such as microbial or herbivore attacks, excessive sunlight, extreme temperature conditions, drought, and high salinity. The number of secondary plant metabolites identified thus far is estimated at 200 000. In addition to being part of the defense system of plants, secondary metabolites also serve as allelochemicals in plant−plant interactions and crosskingdom interactions.1 While the sheer number is already impressive, it is the chemical heterogeneity of secondary plant metabolites that is truly remarkable. They include, among others, nitrogen-containing compounds, such as alkaloids, nonproteinogenic amino acids, amines, glucosinolates, cyanogenic glycosides, and alkylamides, and components without nitrogen, such as terpenoids, polyacetylenes, anthraquinones, and phenolic compounds.2 Among the above-mentioned secondary plant metabolites, phenolic compounds have attracted the interest of researchers from the food and nutritional sciences as well as from allied disciplines because of the numerous roles that they play in foods as antioxidants, preservatives, colorants, and astringent and bitter compounds and because of their putative health benefits. Phenolic compounds are a chemically extremely diverse class of plant metabolites that can broadly be classified into simple phenols (e.g., hydroxybenzoic and hydroxycinnamic acids, coumarins, hydroquinones, and vanillin), xanthones, such as mangiferin with a C6−C1−C6 backbone, stilbenes (C6−C2−C6), flavonoids (C6−C3−C6), and polyphenols, such as gallotannins, condensed tannins, and phlorotannins. The flavonoid subclass alone constitutes more than 10 000 compounds. While phenolic compounds are ubiquitously found in the plant kingdom, the profile of phenolics varies considerably among plants and may therefore be used for chemotaxonomic and authentication purposes.3 © 2018 American Chemical Society
Phenolics may exert their protective activity toward herbivores and microorganisms through various mechanisms,4 among them oxidation to quinones, which are electrondeficient and, hence, reactive molecules that may readily interact with nucleophiles. Quinones may directly inhibit microorganisms or render nutrients unavailable for the herbivores, for example, by derivatization of proteins. In the past 2 decades, a large number of investigations have been dedicated to polyphenol−protein interactions. Although several reviews are available on various aspects of these reactions,5−9 the dynamics in research observed during the past few years necessitates a brief summary of the most important aspects in an effort to highlight the tremendous potential of this topic and to facilitate cross-disciplinary collaboration, with the focus of this paper being on covalent interactions.
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FORMATION AND PROPERTIES OF QUINONES FROM PLANT PHENOLICS The three key enzymes involved in the oxidation of phenols are catechol oxidase, laccase, and peroxidase, with the first two enzymes belonging to polyphenol oxidases (PPOs). 10 Phenolics are oxidized by PPOs after disintegration of the plant tissue and exposure to molecular oxygen. Peroxidases use phenolic compounds as hydrogen donors and reduce hydrogen peroxide. PPOs may either oxidize o-diphenols to quinones (catecholase or diphenolase activity) or catalyze the hydroxylation of monophenols (cresolase or monophenolase activity) to o-diphenols. Laccases oxidize both o- and p-diphenols to their respective quinones, a reaction that takes place in botrytized wines. In addition to enzymatic conversions, quinones may be formed from hydroquinones and catechols also by autoxidation processes, that is, through oxidation by Received: Revised: Accepted: Published: 13051
September 24, 2018 November 20, 2018 November 24, 2018 November 25, 2018 DOI: 10.1021/acs.jafc.8b05215 J. Agric. Food Chem. 2018, 66, 13051−13055
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molecular oxygen.11 Furthermore, chemical oxidation of odiphenols may be achieved by means of autoxidation at elevated pH values, by sodium metaperiodate (NaIO4), cerium ammonium nitrate, chloranil, or the Fenton reagent [Fe2+/ ethylenediaminetetraacetic acid (EDTA)/H2O2]. Sodium metaperiodate has been shown to yield a profile of oxidation products that is similar to that obtained by PPOs.12 A general scheme of quinone formation is shown in Figure 1. Quinones
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IMPORTANCE OF THE REACTIONS OF QUINONES WITH AMINO ACIDS, PEPTIDES, AND PROTEINS Interactions of oxidized phenolics with proteins are more widespread in nature than we may think and not limited to the plant kingdom and food science. For example, cuticle sclerotization of the insect exoskeleton involves the enzymatic oxidation of the o-diphenols N-β-alanyldopamine, N-acetyldopamine, and 3,4-dihydroxyphenylethanol to their quinones, followed by their reaction with cuticle protein side chains. The resulting cross-linkage of proteins leads to cuticle hardening and stabilization.16 Interestingly, the action of a prophenoloxidase in the insect gut detoxifies phenolic compounds that would otherwise be detrimental to the animal.17 In crustaceans, such as shrimps, crabs, and lobsters, a process referred to as melanosis leads to the development of an undesired discoloration caused by enzymatic oxidation of phenols and the reaction of the quinones with amino acids, which is followed by non-enzymatic oxidation and melanin formation.18 During processing, the plant tissue is usually disintegrated, which inevitably causes enzymatic oxidation and quinone formation unless PPO has been inactivated, e.g., by thermal treatment. The o-diphenols chlorogenic acids and catechins are preferred substrates of PPO, but other compounds bearing a 1,2-dihydroxyarene structure may also be converted to quinones in the presence of oxygen. Reaction of the quinones with amino acids, proteins, phenols, and other quinones leads to browning, which is well-known to occur in apples, avocados, bananas, tea, and potatoes.19 It is worth mentioning that, while strategies for the prevention of enzymatic browning are available, the structures formed by the above-mentioned reactions are still poorly understood. Investigations on the reactions of phenolic compounds are challenging for several reasons. In particular, the large number of potential reaction partners, which include both phenolic and non-phenolic food constituents, and the resultant reaction products has hampered comprehensive studies. Furthermore, the quinones as intermediates are extremely reactive and hard to intercept, a situation that may be compared to deoxyosones emerging as intermediates during the Maillard reaction. Model systems designed to simplify studies may be useful but do not reflect the complex conditions in real life samples. Finally, lowmolecular-weight phenolics covalently bound to high-molecular-weight compounds, such as proteins, are hard to characterize. The mechanisms of the reactions between chlorogenic acid and proteins proposed in the 1980s and 1990s assumed the formation of quinones and Michael addition of nucleophiles, primarily the ε-amino group of lysine or the thiol group of cysteine.5,20,21 These reviews were most inspiring, and indeed, such reactions do take place, as seen from the formation of the so-called grape reaction product (2-S-glutathionylcaftaric acid) in grapes and wine.22 Also, the groups of Kroll, Rohn, and Rawel demonstrated by matrix-assisted laser desorption/ ionization−time-of-flight (MALDI−TOF) mass spectrometry an incremental increase in the mass of intact proteins when chlorogenic acid was reacted with proteins in alkaline solution.23 However, systematic studies by Japanese groups revealed that chlorogenic acid may form a dimer via a semiquinone-type radical, which cyclizes and subsequently reacts with a primary amino compound to a green benzacridine derivative (Figure 3).24,25 In the same way, tert-butyloxycarbonyl-L-lysine may react with caffeoquinone in model
Figure 1. Quinone formation exemplified for (top) chlorogenic acid (R = quinic acid) and (bottom) (+)-catechin.
formed from enzymatic or chemical oxidation are electrondeficient, highly reactive intermediates, which may readily react with nucleophiles in a so-called Michael addition. Nucleophilic additions to quinones are considered irreversible because they lead to the formation of stable aromatic systems.11,13 Prominent nucleophiles in foods are thiol and thioether groups and primary and secondary amino groups, the reaction of which leads to covalent bonds with the phenol moiety. It should be mentioned that, in addition to being Michael acceptors, quinones may also give rise to reactive oxygen species via redox cycling with their semiquinone radical anions (Figure 2). The redox cycling may be induced both enzymatically and non-enzymatically and results in the formation of superoxide radical anions, hydrogen peroxide, and hydroxyl radicals. Therefore, such reactions are of particular concern when they take place in biological systems.14,15
Figure 2. Simplified scheme of redox reactions of quinones (adapted from ref 14, with modifications). Nu = nucleophile. 13052
DOI: 10.1021/acs.jafc.8b05215 J. Agric. Food Chem. 2018, 66, 13051−13055
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formulations, we also obtained green-pigmented foamy structures based on whipped egg white (unpublished). When proteins are extracted from sunflower seeds or meal using alkaline solutions, the extract turns green because of the relatively large amounts of chlorogenic acids present in sunflower seeds. Because the green pigmentation of the protein is undesired in many applications, processes have been established to separate the phenolic acids using adsorber resins to obtain purified proteins.31 However, the development of the green pigment may be exploited for coloring purposes, which provides opportunities for diversification of sunflower proteins.8 In addition to the above-discussed formation of benzacridine derivatives, several other reactions of quinones that are of importance to food science have been reported. For example, adduct formation between quinones and thiol groups in myofibrillar proteins was suggested as a novel antioxidative mechanism.32 Covalent conjugation of ovotransferrin to catechin via lysine and glutamic acid residues led to enhanced antioxidative activity of the protein.33 Interestingly, chlorogenic acid−ovalbumin conjugates showed reduced allergenic capacity,34 which offers new opportunities to produce hypoallergenic foods without the need to subject proteins to partial hydrolysis, which may lead to the formation of bitter peptides. Oxidized grape phenolic compounds (catechin, epicatechin, and caftaric acid) trapped 3-sulfanylhexan-1-ol (3SH), suggesting that these reactions are responsible for the loss of 3SH during winemaking and aging.35 While the covalent binding of aroma compounds is undesired because it impairs the sensory characteristics of foods, such reactions may also be utilized for the removal of off-flavors, especially because many of them contain amino or thiol groups. On the other hand, amino acid−quinone reactions have been shown to cause the formation of volatile aldehydes via Strecker degradation (Figure 4).36,37 The modification of amines by oxidized polyphenols may be used to inhibit or modulate the Maillard reaction, but it needs to be taken into account that these conversions may lead to reduced bioavailability of lysine.38
Figure 3. Benzacridine formed by the reaction of the ε-amino group of lysine and chlorogenic acid quinone. R1 = quinic acid.
systems.26 Later, it was demonstrated that the reaction of the α-amino group of amino acids with the chlorogenic acid dimer yields benzacridine derivatives that contain only the amino group, whereas the reaction with other amino groups, for example, in β-alanine or lysine, leads to the formation of benzacridines with the complete amino acid attached.27 Benzacridines may also occur in protein-bound form, as shown for whey proteins.28 Alkaline treatment of sunflower meal protects proteins from ruminal degradation by inducing their derivatization with oxidized chlorogenic acids, which was accompanied by the formation of a green color caused by benzacridines.29 Because of the limited availability of natural green colors and the notorious instability of chlorophylls, green benzacridine derivatives are promising candidates for use in foods. The benzacridine derivative of lysine was used for the coloring of calcium alginate beds, soymilk, and cow milk and showed a remarkable stability during heating. Another interesting application was the detection of fish deterioration, which is accompanied by the release of volatile amines. These amines cause a pH increase, which leads to a color change from red to green of matrices impregnated with the benzacridine−lysine derivative at pH 3. Initial assays conducted using human cell lines did not show significant toxicity.30 In addition to liquid
Figure 4. General scheme of the Strecker degradation of amino acids in the presence of quinones. 13053
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sequence, may even have multifunctional properties, such as antioxidant and emulsifying activities. There is an evident paradox between applying phenolic compounds to foods as natural antioxidants and antimicrobials and compromising food quality and safety because these phenolics may interact with proteins and alter their chemical, physical, and biological properties. Therefore, there is an urgent need to investigate their reactions in more detail to obtain a better view of the structures that are formed during processing and storage. Such investigations should be conducted not only employing conventional processes, such as blanching, pasteurization, and sterilization, but also “novel” technologies, for example, high-pressure processing, pulsed electric field treatment, and others. These studies would not only enhance our knowledge about the chemical changes taking place in foods but also aid in the assessment of whether or not food produced by means of these technologies are substantially equivalent.
Quinones may react not only with amino and thiol compounds but also induce significant changes to other food constituents. The enzymatic oxidation of chlorogenic acid in the presence of all-trans-β-carotene led to substantial isomerization to 9-cis-β-carotene,39 which is remarkable because the cis isomers of β-carotene have a much lower provitamin A activity than the all-trans isomer. An interesting facet of the oxidative conversion of plant phenolics is the potential effect on the antimicrobial properties of the resulting quinones. Many phenolic compounds have a more or less pronounced antimicrobial activity, and because phenolics are used both as antioxidants and antimicrobials,40 it would be worth investigating whether any changes caused to phenolics added as natural antioxidants also affect their antimicrobial properties. A recent study conducted on cocoa polyphenols showed that alkalized cocoa powder extracts had higher antibacterial activity against Gram negative bacteria than extracts obtained from non-alkalized powders.41 It remains to be determined whether the alkali-induced oxidation of catechins to their quinones may be the reason for these observations.
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AUTHOR INFORMATION
Corresponding Author
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[email protected].
RECOMMENDATIONS FOR FUTURE RESEARCH From the above considerations, it becomes evident that quinones formed from plant phenolics bear huge potential that has only insufficiently been tapped. In the following, some recommendations for future investigations are given. It is remarkable that quantitative studies on benzacridines are missing, which is probably due to the lack of reference compounds. Therefore, it is crucial to develop efficient and standardized methods for the synthesis of benzacridin derivatives, preferably with different amino acid moieties. Countercurrent chromatography methods might be useful for the isolation of benzacridines, followed by preparative highperformance liquid chromatography (HPLC) if necessary. For their characterization, high-resolution mass spectrometry and nuclear magnetic resonance (NMR) spectroscopy are strongly recommended. Additionally, their stability in solution and during dry storage should be monitored. The availability of sufficiently large quantities will allow for investigations into their toxicological potential, which is a prerequisite before benzacridines can be considered for use as food colorants. Furthermore, we need to keep in mind that benzacridines are still Michael acceptors that may react with proteins and, thus, alter their immunological properties. In a worst case, this protein haptenation may be a trigger of allergic reactions. Also, the legal status of benzacridines needs to be established. In the context of both aspects it is worth mentioning that benzacridines may be formed from whipped egg white and coffee powder, that is, two components wellestablished as food, and that the preparation of the so-called “moss cake” is based on these ingredients. After clarification of toxicological and regulatory issues, comprehensive investigations are needed into the effects of processing and storage on the stability of benzacridines. Different food matrices, in particular, varying pH conditions, also need to be considered. When it finally comes to the recovery of precursors of benzacridines, side streams of plant food processing may be considered as an abundant, sustainable, and cost-efficient source of chlorogenic acids.42 Considering that benzacridines have been shown to be bound to proteins,28 it should be possible to obtain peptides by enzymatic hydrolysis that are colored or, depending upon their amino acid composition and
ORCID
Andreas Schieber: 0000-0002-1082-9547 Notes
The author declares no competing financial interest.
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DEDICATION Dedicated to Prof. Dr. habil. Dr. h.c. Reinhold Carle, University of Hohenheim, Stuttgart, Germany, on the occasion of his retirement.
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REFERENCES
(1) Kessler, A.; Kalske, A. Plant secondary metabolite diversity and species interactions. Annu. Rev. Ecol. Evol. Syst. 2018, 49, 115−138. (2) Wink, M. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 2003, 64, 3− 19. (3) Schulze-Kaysers, N.; Feuereisen, M. M.; Schieber, A. Phenolic compounds in edible species of the Anacardiaceae familyA review. RSC Adv. 2015, 5, 73301−73314. (4) Sanchez Maldonado, A. F.; Schieber, A.; Gänzle, M. G. Plant defence mechanisms and enzymatic transformation products and their potential applications in food preservation: Advantages and limitations. Trends Food Sci. Technol. 2015, 46, 49−59. (5) Friedman, M. Chemistry, biochemistry, and dietary role of potato polyphenols. A review. J. Agric. Food Chem. 1997, 45, 1523− 1540. (6) Bittner, S. When quinones meet amino acids: Chemical, physical and biological consequences. Amino Acids 2006, 30, 205−224. (7) Le Bourvellec, C.; Renard, C. M. G. C. Interactions between polyphenols and macromolecules: Quantification methods and mechanisms. Crit. Rev. Food Sci. Nutr. 2012, 52, 213−248. (8) Wildermuth, S. R.; Young, E. E.; Were, L. M. Chlorogenic acid oxidation and its reaction with sunflower proteins to form greencolored complexes. Compr. Rev. Food Sci. Food Saf. 2016, 15, 829− 843. (9) Perez-Gregorio, M. R.; Simal-Gándara, J. A critical review of the characterization of polyphenol−protein interactions and of their potential use for improving food quality. Curr. Pharm. Des. 2017, 23, 2742−2753. (10) Pourcel, L.; Routaboul, J.-M.; Cheynier, V.; Lepiniec, L.; Debeaujon, I. Flavonoid oxidation in plants: From biochemical 13054
DOI: 10.1021/acs.jafc.8b05215 J. Agric. Food Chem. 2018, 66, 13051−13055
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Journal of Agricultural and Food Chemistry properties to physiological functions. Trends Plant Sci. 2007, 12, 29− 36. (11) Uchimiya, M.; Stone, A. T. Reversible redox chemistry of quinones: Impact on biogeochemical cycles. Chemosphere 2009, 77, 451−458. (12) Antolovich, M.; Bedgood, D. R., Jr.; Bishop, A. G.; Jardine, D.; Prenzler, P. D.; Robards, K. LC−MS investigation of oxidation products of phenolic antioxidants. J. Agric. Food Chem. 2004, 52, 962−971. (13) Kutyrev, A. A.; Moskva, V. V. Nucleophilic reactions of quinones. Russ. Chem. Rev. 1991, 60, 72−88. (14) Bolton, J. L.; Trush, M. A.; Penning, T. M.; Dryhurst, G.; Monks, T. J. Role of quinones in toxicology. Chem. Res. Toxicol. 2000, 13, 135−160. (15) Bolton, J. L.; Dunlap, T. Formation and biological targets of quinones: Cytotoxic versus cytoprotective effects. Chem. Res. Toxicol. 2017, 30, 13−37. (16) Kramer, K. J.; Kanost, M. R.; Hopkins, T. L.; Jiang, H.; Zhu, Y. C.; Xu, R.; Kerwin, J. L.; Turecek, F. Oxidative conjugation of catechols with proteins in insect skeletal systems. Tetrahedron 2001, 57, 385−392. (17) Wu, K.; Zhang, J.; Zhang, Q.; Zhu, S.; Shao, Q.; Clark, K. D.; Liu, Y.; Ling, E. Plant phenolics are detoxified by prophenoloxidase in the insect gut. Sci. Rep. 2015, 5, 16823. (18) Gonçalves, A. A.; de Oliveira, A. R. M. Melanosis in crustaceans: A review. LWTFood Sci. Technol. 2016, 65, 791−799. (19) Tomás-Barberán, F. A.; Espín, J. C. Phenolic compounds and related enzymes as determinants of quality in fruits and vegetables. J. Sci. Food Agric. 2001, 81, 853−876. (20) Hurrell, R. F.; Finot, P. A.; Cuq, J. L. Protein-polyphenol reactions. 1. Nutritional and metabolic consequences of the reaction between oxidized caffeic acid and lysine residues of casein. Br. J. Nutr. 1982, 47, 191−211. (21) Matheis, G.; Whitaker, J. R. Modification of proteins by polyphenol oxidase and peroxidase and their products. J. Food Biochem. 1984, 8, 137−162. (22) Cejudo-Bastante, M. J.; Pérez-Coello, M. S.; HermosínGutiérrez, I. Identification of new derivatives of 2-S-glutathionylcaftaric acid in aged white wines by HPLC-DAD-ESI-MSn. J. Agric. Food Chem. 2010, 58, 11483−11492. (23) Rohn, S. Possibilities and limitations in the analysis of covalent interactions between phenolic compounds and proteins. Food Res. Int. 2014, 65, 13−19. (24) Namiki, M.; Yabuta, G.; Koizumi, Y.; Yano, M. Development of free radical products during the greening reaction of caffeic acid esters (or chlorogenic acid) and a primary amino compound. Biosci., Biotechnol., Biochem. 2001, 65, 2131−2136. (25) Yabuta, G.; Koizumi, Y.; Namiki, K.; Hida, M.; Namiki, M. Structure of green pigment formed by the reaction of caffeic acid esters (or chlorogenic acid) with a primary amino compound. Biosci., Biotechnol., Biochem. 2001, 65, 2121−2130. (26) Schilling, S.; Sigolotto, C.-I.; Carle, R.; Schieber, A. Characterization of covalent addition products of chlorogenic acid quinone with amino acid derivatives in model systems and apple juice by highperformance liquid chromatography/electrospray ionization mass spectrometry. Rapid Commun. Mass Spectrom. 2008, 22, 441−448. (27) Bongartz, V.; Brandt, L.; Gehrmann, M. L.; Zimmermann, B. F.; Schulze-Kaysers, N.; Schieber, A. Evidence for the formation of benzacridine derivatives in alkaline-trated sunflower meal and model solutions. Molecules 2016, 21, 91. (28) Ali, M.; Homann, T.; Khalil, M.; Kruse, H.-P.; Rawel, H. Milk whey protein modification by coffee-specific phenolics: Effect on structural and functional properties. J. Agric. Food Chem. 2013, 61, 6911−6920. (29) Bongartz, V.; Böttger, C.; Wilhelmy, N.; Schulze-Kaysers, N.; Südekum, K.-H.; Schieber, A. Protection of protein from ruminal degradation by alkali-induced oxidation of chlorogenic acid in sunflower meal. J. Anim. Physiol. Anim. Nutr. 2018, 102, e209−e215.
(30) Iacomino, M.; Weber, F.; Gleichenhagen, M.; Pistorio, V.; Panzella, L.; Pizzo, E.; Schieber, A.; d’Ischia, M.; Napolitano, A. Stable benzacridine pigments by oxidative coupling of chlorogenic acid with amino acids and proteins: Toward natural product-based green food coloring. J. Agric. Food Chem. 2017, 65, 6519−6528. (31) Weisz, G. M.; Schneider, L.; Schweiggert, U.; Kammerer, D. R.; Carle, R. Sustainable sunflower processingI. Development of a process for the adsorptive decolorization of sunflower [Helianthus annuus L.] protein extracts. Innovative Food Sci. Emerging Technol. 2010, 11, 733−741. (32) Jongberg, S.; Gislason, N. E.; Lund, M. N.; Skibsted, L. H.; Waterhouse, A. L. Thiol-quinone adduct formation in myofibrillar proteins detected by LC-MS. J. Agric. Food Chem. 2011, 59, 6900− 6905. (33) You, J.; Luo, Y.; Wu, J. Conjugation of ovotransferrin with catechin shows improved antioxidant activity. J. Agric. Food Chem. 2014, 62, 2581−2587. (34) Lu, Y.; Li, S.; Xu, H.; Zhang, T.; Lin, X.; Wu, X. Effect of covalent interaction with chlorogenic acid on the allergenic capacity of ovalbumin. J. Agric. Food Chem. 2018, 66, 9794−9800. (35) Nikolantonaki, M.; Jourdes, M.; Shinoda, K.; Teissedre, P.-L.; Quideau, S.; Darriet, P. Identification of adducts between an odoriferous volatile thiol and oxidized grape phenolic compounds: Kinetic study of adduct formation under chemical and enzymatic oxidation conditions. J. Agric. Food Chem. 2012, 60, 2647−2656. (36) Rizzi, G. P. Formation of Strecker aldehydes from polyphenolderived quinones and α-amino acids in a nonenzymic model system. J. Agric. Food Chem. 2006, 54, 1893−1897. (37) Delgado, R. M.; Zamora, R.; Hidalgo, F. J. Contribution of phenolic compounds to food flavors: Strecker-type degradation of amines and amino acids produced by o- and p-diphenols. J. Agric. Food Chem. 2015, 63, 312−318. (38) Lund, M. N.; Ray, C. A. Control of Maillard reactions in foods: Strategies and chemical mechanisms. J. Agric. Food Chem. 2017, 65, 4537−4552. (39) De Rigal, D.; Gauillard, F.; Richard-Forget, F. Changes in the carotenoid content of apricot (Prunus armeniaca, var Bergeron) during enzymatic browning: β-Carotene inhibition of chlorogenic acid degradation. J. Sci. Food Agric. 2000, 80, 763−768. (40) Papuc, C.; Goran, G. V.; Predescu, C. N.; Nicorescu, V.; Stefan, G. Plant polyphenols as antioxidant and antibacterial agents for shelflife extension of meat and meat products: Classification, structures, sources, and action mechanisms. Compr. Rev. Food Sci. Food Saf. 2017, 16, 1243−1268. (41) Todorovic, V.; Milenkovic, M.; Vidovic, B.; Todorovic, Z.; Sobajic, S. Correlation between antimicrobial, antioxidant activity, and polyphenols of alkalized/nonalkalized cocoa powders. J. Food Sci. 2017, 82, 1020−1027. (42) Schieber, A. Side streams of plant food processing as a source of valuable compounds: Selected examples. Annu. Rev. Food Sci. Technol. 2017, 8, 97−112.
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