Dietary protein oxidation: A silent threat to human health?

Critical Reviews in Food Science and Nutrition

Volumn 57, Issue 17, 2017, Pages 3781-3793

  Estevez M ^a   Luna, C ^b  

^a UNIVERSITY OF EXTREMADURA   (Spain)

^b Medical Hospital   (Spain)

Author keywords

Cancer; dietary antioxidants; inflammatory bowel disease; oxidative stress; oxidized proteins

Indexed keywords

FOOD STORAGE; HEALTH RISKS; NUTRITION; OXIDATIVE STRESS; PROTEINS;

AGE-RELATED DISEASE; CANCER; GASTROINTESTINAL TRACT; HEALTH DISORDERS; INFLAMMATORY BOWEL DISEASE; PATHOLOGICAL CONDITIONS; PROTEIN FUNCTIONALITIES; PROTEIN OXIDATION;

OXIDATION;

ANTIOXIDANT;

DIET; FOOD QUALITY; HUMAN; METABOLISM; OXIDATION REDUCTION REACTION; PROTEIN INTAKE;

ANTIOXIDANTS; DIET; DIETARY PROTEINS; FOOD QUALITY; HUMANS; OXIDATION-REDUCTION;

EID: 85015106188     PISSN: 10408398     EISSN: 15497852     Source Type: Journal    
DOI: 10.1080/10408398.2016.1165182     Document Type: Article

References (143)

1. Akagawa, K., Sasaki, D., Kurota, Y., and Suyama, K., (2005). Formation of α-aminoadipic and γ-glutamic semialdehydes in proteins by the Maillard reaction. Ann. N Y Acad. Sci. 1043:129–134.
2. Aldini, G., Domingues, M. R., Spickett, C. M., Domingues, P., Altomare, A., Sanchez-Gomez, F. J., Oeste, C. L., and Perez-Sala, D., (2015). Protein lipoxidation:Detection strategies and challenges. Redox Biol. 5:253–266.
3. Astruc, T., Marinova, P., Labas, R., Gatellier, P., and Santé-Lhoutellier, V., (2007). Detection and localization of oxidized proteins in muscle cells by fluorescence microscopy. J. Agric. Food Chem. 55:9554–9558.
4. Aw, T. Y., (1999). Molecular and cellular responses to oxidative stress and changes in oxidation-reduction imbalance in the intestine. Am. J. Clin. Nutr. 70:557–565.
5. Awada, M., Soulage, C. O., Meynier, A., Debard, C., Plaisancié, P., Benoit, B., Picard, G., Loizon, E., Chauvin, M.-A., Estienne, M., Peretti, N., Guichardant, M., Lagarde, M., Genot, C., and Michalski, M.-C., (2012). Dietary oxidized n-3 PUFA induce oxidative stress and inflammation:Role of intestinal absorption of 4-HHE and reactivity in intestinal cells. J. Lipid Res. 53:2069–2080.
6. Bao, Y., and Ertbjerg, P., (2015). Relationship between oxygen concentration, shear force and protein oxidation in modified atmosphere packaged pork. Meat Sci. 110:174–179.
7. Bastide, N. M., Chenni, F., Audebert, M., Santarelli, R. L., Taché, S., Naud, N., Baradat, M., Jouanin, I., Surya, R., Hobbs, D. A., Kuhnle, G. G., Raymond-Letron, I., Gueraud, F., Corpet, D. E., and Pierre, F. H. F., (2015). A central role for heme iron in colon carcinogenesis associated with red meat intake. Cancer Res. 75:870–879.
8. Bastide, N. M., Pierre, F. H. F., and Corpet, D. E., (2011). Heme iron from meat and risk of colorectal cancer:A meta-analysis and a review of the mechanisms involved. Cancer Prev. Res. 4:177–184.
9. Baxter, J. H., Lai, C.-S., Phillips, R. R., Dowlati, L., Chio, J. J., Luebbers, S. T., Dimler, S. R., and Johns, P. W., (2007). Direct determination of methionine sulfoxide in milk proteins by enzyme hydrolysis/high-performance liquid chromatography. J. Chromatogr. A. 1157:10–16.
10. Bekhit, A. E.-D. A., Hopkins, D. L., Fahri, F. T., and Ponnampalam, E. N., (2013). Oxidative processes in muscle systems and fresh meat:Sources, markers, and remedies. Compr. Rev. Food Sci. F. 12:565–597.
11. Berlett, B. S., and Stadtman, E. R., (1997). Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 272:20313–20316.
12. Carail, M., Goupy, P., Reynaud, E., Dangles, O., and Caris-Veyrat, C., (2013). Oxidative cleavage products of lycopene:Production and reactivity in a biomimetic experimental model of oxidative stress. ACS Symp. Series. 1134:191–205.
13. Chan, S. W., Dunlop, R. A., Rowe, A., Double, K. L., and Rodgers, K. J., (2012). L-DOPA is incorporated into brain proteins of patients treated for Parkinson's disease, inducing toxicity in human neuroblastoma cells in vitro. Exp. Neurol. 238:29–37.
14. Chang, D., Wang, F., Zhao, Y.-S., and Pan, H.-Z., (2008). Evaluation of oxidative stress in colorectal cancer patients. Biomed. Environ. Sci. 21:286–289.
15. Chen, H., Diao, J., Li, Y., Chen, Q., and Kong, B., (2016). The effectiveness of clove extracts in the inhibition of hydroxyl radical oxidation-induced structural and rheological changes in porcine myofibrillar protein. Meat Sci. 111:60–66.
16. Chen, Y., and Guillemin, G. J., (2009). Kynurenine pathway metabolites in humans:Disease and healthy states. Int. J. Tryp. Res. 2:1–19.
17. Chevion, M., Berenshtein, E., and Stadtman, E. R., (2000). Human studies related to protein oxidation:Protein carbonyl content as a marker of damage. Free Rad. Res. 33:S99–S108.
18. Cooke, M. S., Evans, M. D., Dizdaroglu, M., and Lunec, J., (2003). Oxidative DNA damage:Mechanisms, mutation, and disease. ASEB J. 17:1195–1214.
19. Dakin, H. D., (1906). The oxidation of amido-acids with the production of substances of biological importance. J. Biol. Chem. 1:171–176.
20. Dakin, H. D., (1908a). The oxidation of leucine, a-amino-isovaleric acid and a-amino-valeric acid with hydrogen peroxide. J. Biol. Chem. 4:63–76.
21. Dakin, H. D., (1908b). Note on the oxidation of glutamic acid by means of hydrogen peroxide. J. Biol. Chem. 5:409–411.
22. Dalle-Donne, I., Aldini, G., Carini, M., Colombo, R., Rossi, R., and Milzani, A., (2006). Protein carbonylation, cellular dysfunction, and disease progression. J. Cell. Mol. Med. 10:389–406.
23. Dalle-Donne, I., Giustarini, D., Colombo, R., Rossi, R., and Milzani, A., (2003). Protein carbonylation in human diseases. Trends Mol. Med. 9:169–176.
24. Dalsgaard, T. K., Bakman, M., Hammershoj, M., Sorensen, J., Nebel, C., Albrechtsen, R., Vognsen, L., and Nielsen, J. H., (2012). Light-induced protein and lipid oxidation in low-fat cheeses:Effect on degree of enzymatic hydrolysis. Int. J. Dairy Technol. 65:57–63.
25. Dalsgaard, T. K., Otzen, D., Nielsen, J. H., and Larsen, L. B., (2007). Changes in structures of milk proteins upon photo-oxidation. J. Agric. Food Chem. 55:10968–10976.
26. Davies, M. J., (2003). Singlet oxygen-mediated damage to proteins and its consequences. Biochem. Biophys. Res. Comm. 305:761–770.
27. Davies, M. J., (2005). The oxidative environment and protein damage. Biochim. Biophys. Acta. 1703:93–109.
28. Decker, E. A., Xiong, Y. L., Calvert, J. T., Crum, A. D., and Blanchard, S. P., (1993). Chemical, physical, and functional properties of oxidized turkey white muscle myofibrillar proteins. J. Agric. Food Chem. 41:186–189.
29. Dever, J. T., and Elfarra, A. A., (2008). L-Methionine-dl-sulfoxide metabolism and toxicity in freshly isolated mouse hepatocytes:Gender differences and inhibition with aminooxyacetic acid. Drug Metabol. Disp. 36:2252–2260.
30. Di Luccia, A., La Gatta, B., Nicastro, A., Petrella, G., Lamacchia, C., and Picariello, G., (2015). Protein modifications in cooked pork products investigated by a proteomic approach. Food Chem. 172:447–455.
31. Dunlop, R. A., Brunk, U. T., and Rodgers, K. J., (2011). Proteins containing oxidized amino acids induce apoptosis in human monocytes. Biochem. J. 435:207–216.
32. Dunlop, R. A., Dean, R. T., and Rodgers, K. J., (2008). The impact of specific oxidized amino acids on protein turnover in J774 cells. Biochem. J. 410:131–140.
33. Dunlop, R. A., Main, B. J., and Rodgers, K. J., (2015). The deleterious effects of non-protein amino acids from desert plants on human and animal health. J. Arid Environ. 112:152–158.
34. Ehrenshaft, M., Deterding, L. J., and Mason, R. P., (2015). Tripping up trp:Modification of protein tryptophan residues by reactive oxygen species, modes of detection, and biological consequences. Free Rad. Biol. Med. 89:220–228.
35. Esterbauer, H., Gebicki, J., Puhl, H., and Jurgens, G., (1992). The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Rad. Biol. Med. 13:341–390.
36. Esterbauer, H., Muskiet, F., and Horrobin, D. F., (1993). Cytotoxicity and genotoxicity of lipid-oxidation products. Am. J. Clin. Nutr. 57:779S–786S.
37. Esterbauer, H., Schaur, R. J., and Zollner, H., (1991). Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Rad. Biol. Med. 11:81–128.
38. Estévez, M., (2011). Protein carbonyls in meat systems:A review. Meat Sci. 89:259–279.
39. Estévez, M., (2015). Oxidative damage to poultry:From farm to fork. Poult. Sci. 94:1368–1378.
40. Estévez, M., and Heinonen, M., (2010). Effect of phenolic compounds on the formation of α-aminoadipic and γ-glutamic semialdehydes from myofibrillar proteins oxidized by copper, iron and myoglobin. J. Agric. Food Chem. 58:4448–4455.
41. Estévez, M., Kylli, P., Puolanne, E., Kivikari, R., and Heinonen, M., (2008). Fluorescence spectroscopy as a novel approach for the assessment of myofibrillar protein oxidation in oil-in-water emulsions. Meat Sci. 80:1290–1296.
42. Estévez, M., Ollilainen, V., and Heinonen, M., (2009). Analysis of protein oxidation markers–α-aminoadipic and gamma-glutamic semialdehydes–in food proteins by using LC-ESI-multi-stage tandem MS. J. Agric. Food Chem. 57:3901–3910.
43. Estévez, M., Ventanas, S., and Heinonen, M., (2011). Formation of Strecker aldehydes between protein carbonyls–α-aminoadipic and γ-glutamic semialdehydes–and leucine and isoleucine. Food Chem. 128:1051–1057.
44. Fang, W., Sun, J., Li, Z. L., Le, G., and Shi, Y., (2012). Effect of oxidated food protein on mice gut flora and redox state. Chin. J. Microecol. 24:193–196.
45. Feng, X., Li, C., Ullah, N., Cao, J., Lan, Y., Ge, W., Hackman, R. M., Li, Z., and Chen, L., (2015). Susceptibility of whey protein isolate to oxidation and changes in physicochemical, structural, and digestibility characteristics. J. Dairy Sci. 98:7602–7613.
46. Finkel, T., and Holbrook, N. J., (2000). Oxidants, oxidative stress and the biology of ageing. Nature. 408:239–247.
47. Fontana, L., Weiss, E. P., Villareal, D. T., Klein, S., and Holloszy, J. O., (2008). Long-term effects of calorie or protein restriction on serum IGF-1 and IGFBP-3 concentration in humans. Aging Cell. 7:681–687.
48. Frederiksen, A. M., Lund, M. N., Andersen, M. L., and Skibsted, L. H., (2008). Oxidation of porcine myosin by hypervalent myoglobin:The role of thiol groups. J. Agric. Food Chem. 56:3297–3304.
49. Fucci, L., Oliver, C. N., Coon, M. J., and Stadtman, E. R., (1983). Inactivation of key metabolic enzymes by mixed function oxidation reactions:possible implication in protein turnover and ageing. Proc. Natl. Acad. Sci. USA. 80:1521–1525.
50. Ganhão, R., Morcuende, D., and Estévez, M., (2010b). Tryptophan depletion and formation of α-aminoadipic and γ-glutamic semialdehydes in porcine burger patties with added phenolic-rich fruit extracts. J. Agric. Food Chem. 58:3541–3548.
51. Ganhão, Rde. D., and Estévez, M., (2010a). Protein oxidation in emulsified cooked burger patties with added fruit extracts:Influence on colour and texture deterioration during chill storage. Meat Sci. 85:402–409.
52. Goicoechea, E., Brandon, E. F. A., Blokland, M. H., and Guillen, M. D., (2011). Fate in digestion in vitro of several food components, including some toxic compounds coming from omega-3 and omega-6 lipids. Food Chem. Toxicol. 49:115–124.
53. Gong, C.-X., Liu, F., Grundke-Iqbal, I., and Iqbal, K., (2005). Post-translational modifications of tau protein in Alzheimer's disease. J. Neural Transm. 112:813–838.
54. Goupy, P., Vulcain, E., Caris-Veyrat, C., and Dangles, O., (2007). Dietary antioxidants as inhibitors of the heme-induced peroxidation of linoleic acid:Mechanism of action and synergism. Free Rad. Biol. Med. 43:933–946.
55. Guéraud, F., Tache, S., Steghens, J.-P., Milkovic, L., Borovic-Sunjic, S., Zarkovic, N., Gaultier, E., Naud, N., Héliès-Toussaint, C., Pierre, F., and Priymenko, N., (2015). Dietary polyunsaturated fatty acids and heme iron induce oxidative stress biomarkers and a cancer promoting environment in the colon of rats. Free Rad. Biol. Med. 83:192–200.
56. Gurbuz, G., and Heinonen, M., (2015). LC-MS investigations on interactions between isolated β-lactoglobulin peptides and lipid oxidation product malondialdehyde. Food Chem. 175:300–305.
57. Gurer-Orhan, H., Ercal, N., Mare, S., Pennathur, S., Orhan, H., and Heinecke, J. W., (2006). Misincorporation of free m-tyrosine into cellular proteins:A potential cytotoxic mechanism for oxidized amino acids. Biochem. J. 395:277–284.
58. Hensley, K., Hall, N., Subramaniam, R., Cole, P., Harris, M., Aksenov, M., Aksenova, M., Gabbita, S. P., Wu, J. F., Carney, J. M., Lovell, M., Markesbery, W. R., and Butterfield, D. A., (1995). Brain regional correspondence between Alzheimer's disease histopathology and biomarkers of protein oxidation. J. Neurochem. 65:2146–2156.
59. Hou, J. K., Abraham, B., and El-Serag, H., (2011). Dietary intake and risk of developing inflammatory bowel disease:A systematic review of the literature. Am. J. Gastroent. 106:563–573.
60. IARC. (2015). Carcinogenicity of consumption of red and processed meat. The Lancet. 16:1599–1600.
61. Ishii, N., Fujii, M., Hartman, P. S., Tsuda, M., Yasuda, K., Senoo-Matsuda, N., Yanase, S., Ayusawa, D., and Suzuki, K., (1998). A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes. Nature. 394:694–697.
62. Jongberg, S., Gislason, N. E., Lund, M. N., Skibsted, L. H., and Waterhouse, A. L., (2011). Thiol-quinone adduct formation in myofibrillar proteins detected by LC-MS. J. Agric. Food Chem. 59:6900–6905.
63. Kenmogne-Domguia, H. B., Moisan, S., Viau, M., Genot, C., and Meynier, A., (2014). The initial characteristics of marine oil emulsions and the composition of the media inflect lipid oxidation during in vitro gastrointestinal digestion. Food Chem. 152:146–154.
64. Keshavarzian, A., Banan, A., Farhadi, A., Komanduri, S., Mutlu, E., Zhang, Y., and Fields, J. Z., (2003). Increases in free radicals and cytoskeletal protein oxidation and nitration in the colon of patients with inflammatory bowel disease. Gut. 52:720–728.
65. Keshavarzian, A., Morgan, G., Sedghi, S., Gordon, J. H., and Doria, M., (1990). Role of reactive oxygen metabolites in experimental colitis. Gut. 31:786–790.
66. Keszthelyi, D., Troost, F. J., Jonkers, D. M., Van Donkelaar, E. L., Dekker, J., Buurman, W. A., and Masclee, A. A., (2012). Does acute tryptophan depletion affect peripheral serotonin metabolism in the intestine? Am. J. Clin. Nutr. 95:603–608.
67. Keszthelyi, D., Troost, F. J., Jonkers, D. M., Leue, C., and Masclee, A. A. M., (2013). Decreased levels of kynurenic acid in the intestinal mucosa of IBS patients:Relation to serotonin and psychological state. J. Phycosom. Res. 74:501–504.
68. Keszthelyi, D., Troost, F.J., and Masclee, A. A. M., (2009). Understanding the role of tryptophan and serotonin metabolism in gastrointestinal function. Neurogastroenterology and Motility, 21:1239–1249.
69. Koivumäki, T., Gürbüz, G., Poutanen, M., and Heinonen, M., (2012). A Novel LC-MS application to investigate oxidation of peptides isolated from β-lactoglobulin. J. Agric. Food Chem. 60:6799–6805.
70. Lametsch, R., Lonergan, S. M., and Huff-Lonergan, E., (2008). Disulfide bond within µ-calpain active site inhibits activity and autolysis. Biochim. Biophys. Acta. 1784:1215–1221.
71. Larsson, K., Cavonius, L., Alminger, M., and Undeland, I., (2012). Oxidation of cod liver oil during gastrointestinal in vitro digestion. J. Agric. Food Chem. 60:7556–7564.
72. Leclere, J., Birlouez-Aragon, I., and Meli, M., (2002). Fortification of milk with iron-ascorbate promotes lysine glycation and tryptophan oxidation. Food Chem. 76:491–499.
73. Leuratti, C., Watson, M. A., Deag, E. J., Welch, A., Singh, R., Gottschalg, E., Marnett, L. J., Atkin, W., Day, N. E., Shuker, D. E. G., and Bingham, S. A., (2002). Detection of malondialdehyde DNA adducts in human colorectal mucosa:Relationship with diet and the presence of adenomas. Cancer Epidemiol. Biomarkers Prev. 11:267–273.
74. Levine, R. L., Garland, D., Oliver, C. N., Amici, A., Climent, I., Lenz, A. G., Ahn, B. W., Shaltiel, S., and Stadtman, E. R., (1990). Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 186:464–478.
75. Li, Z. L., Mo, L., Le, G., and Shi, Y., (2014). Oxidized casein impairs antioxidant defense system and induces hepatic and renal injury in mice. Food Chem. Toxicol. 64:86–93.
76. Li, Z. L., Shi, Y., Le, G., Ding, Y., and Zhao, Q., (2015). 24-Week exposure to oxidized tyrosine induces hepatic fibrosis involving activation of the MAPK/TGF-β1 signaling pathway in Sprague–Dawley rats model. Oxid. Med. Cell Longev. Article ID 763272.
77. Li, Z. L., Wu, L., Le, G., and Shi, Y., (2013). Effect of oxidized casein on the oxidative damage of blood and digestive organs in mice. Acta Nutr. Sin. 35:39–43.
78. Lorrain, B., Dangles, O., Loonis, M., Armand, M., and Dufour, C., (2012). Dietary iron-initiated lipid oxidation and its inhibition by polyphenols in gastric conditions. J. Agric. Food Chem. 60:9074–9081.
79. Lund, M. N., Heinonen, M., Baron, C. P., and Estévez, M., (2011). Protein oxidation in muscle foods:A review. Mol. Nutr. Food Res. 55:83–95.
80. Lund, M. N., Luxford, C., Skibsted, L. H., and Davies, M. J., (2008). Oxidation of myosin by haem proteins generates myosin radicals and protein cross-links. Biochem. J. 410:565–574.
81. Martinez, J., Nieto, G., Castillo, J., and Ros, G., (2014). Influence of in vitro gastrointestinal digestion and/or grape seed extract addition on antioxidant capacity of meat emulsions. LWT Food Sci. Technol. 59:834–840.
82. Mehrabi, S., Wallace, L., Cohen, S., and Yao, X., and Aikhionbare, F., (2015). Differential measurements of oxidatively modified proteins in colorectal adenopolyps. Int. J. Clin. Med. 6:289–299.
83. Meltretter, J., Wust, J., and Pischetsrieder, M., (2014). Modified peptides as indicators for thermal and nonthermal reactions in processed milk. J. Agric. Food Chem. 62:10903–1091.
84. Mesquita, C. S., Oliveira, R., Bento, F., Geraldo, D., Rodrigues, J. V., and Marcos, J. C., (2014). Simplified 2,4-dinitrophenylhydrazine spectrophotometric assay for quantification of carbonyls in oxidized proteins. Anal.Biochem. 458:69–71.
85. Monnier, V. M., (2007). Dietary advanced lipoxidation products as risk factors for human health–a call for data. Mol. Nutr. Food Res. 51:1091–1093.
86. Morrissey, P. A., Sheehy, P. J. A., Galvin, K., Kerry, J. P., and Buckley, D. J., (1998). Lipid stability in meat and meat products. Meat Sci. 49:S73–S86.
87. Nedić, O., Robajac, D., Šunderić, M., Miljuš, G., Crossed, D., Signukanović, B., and Malenković, V., (2013). Detection and identification of oxidized insulin-like growth factor-binding proteins and receptors in patients with colorectal carcinoma. Free Rad. Biol. Med. 65:1195–1200.
88. Nunes, C., Ferreira, E., Freitas, V., Almeida, L., Barbosa, R. M., and Laranjinha, J., (2013). Intestinal anti-inflammatory activity of red wine extract:Unveiling the mechanisms in colonic epithelial cells. Food Funct. 4:373–383.
89. Pazos, M., Da Rocha, A. P., Roepstorff, P., and Rogowska-Wrzesinska, A., (2011). Fish proteins as targets of ferrous-catalyzed oxidation:Identification of protein carbonyls by fluorescent labeling on two-dimensional gels and MALDI-TOF/TOF mass spectrometry. J. Agric. Food Chem. 59:7962–7977.
90. Pazos, M., Maestre, R., Gallardo, J. M., and Medina, I., (2013). Proteomic evaluation of myofibrillar carbonylation in chilled fish mince and its inhibition by catechin. Food Chem. 136:64–72.
91. Pierre, F., Freeman, A., Tache, S., Van Der Meer, R., and Corpet, D. E., (2004). Beef meat and blood sausage promote the formation of azoxymethane-induced mucin-depleted foci and aberrant crypt foci in rat colons. J. Nutr. 134:2711–2716.
92. Pierre, F., Peiro, G., Tache, S., Cross, A. J., Bingham, S. A., Gasc, N., Gottardi, G., Corpet, D. E., and Gueraud, F., (2006). New marker of colon cancer risk associated with heme intake:1,4-Dihydroxynonane mercapturic acid. Cancer Epidem. Biomark. Prev. 15:2274–2279.
93. Pierre, F., Taché, S., Petit, C. R., Van der Meer, R., and Corpet, D. E., (2003). Meat and cancer:Haemoglobin and haemin in a low-calcium diet promote colorectal carcinogenesis at the aberrant crypt stage in rats. Carcinogenesis, 24:1683–1690.
94. Polyak, K., Xia, Y., Zweier, J. L., Kinzler, K. W., and Vogelstein, B., (1997). A model for p53-induced apoptosis. Nature. 389:300–305.
95. Promeyrat, A., Sayd, T., Laville, E., Chambon, C., Lebret, B., and Gatellier, Ph., (2011). Early post-mortem sarcoplasmic proteome of porcine muscle related to protein oxidation. Food Chem. 127:1097–1104.
96. Raes, K., Doolaege, E. H. A., Deman, S., Vossen, E., and De Smet, S., (2015). Effect of carnosic acid, quercetin and α-tocopherol on lipid and protein oxidation in an in vitro simulated gastric digestion model. Int. J. Food Sci. Nutr. 66:216–221.
97. Requena, J. R., Chao, C.-C., Levine, R. L., and Stadtman, E. R., (2001). Glutamic and aminoadipic semialdehydes are the main carbonyl products of metal-catalyzed oxidation of proteins. Proc. Natl. Acad. Sci. USA. 98:69–74.
98. Rysman, T., Jongberg, S., Van Royen, G., Van Weyenberg, S., De Smet, S., and Lund, M. N., (2014). Protein thiols undergo reversible and irreversible oxidation during chill storage of ground beef as detected by 4,4′-dithiodipyridine. J. Agric. Food Chem. 62:12008–12014.
99. Salminen, H., and Heinonen, M., (2008). Plant phenolics affect oxidation of tryptophan. J. Agric. Food Chem. 56:7472–7481.
100. Santé-Lhoutellier, V., Aubry, L., and Gatellier, P., (2007). Effect of oxidation on in vitro digestibility of skeletal muscle myofibrillar proteins. J. Agric. Food Chem. 55:5343–5348.
101. Schuessler, H., and Schilling, K., (1984). Oxygen effect in the radiolysis of proteins. Part 2. Bovine serum albumin. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 45:267–281.
102. Seiquer, I., Rueda, A., Olalla, M., and Cabrera-Vique, C., (2015). Assessing the bioavailability of polyphenols and antioxidant properties of extra virgin argan oil by simulated digestion and Caco-2 cell assays.Comparative study with extra virgin olive oil. Food Chem. 188:496–503.
103. Sell, D. R., Strauch, C. M., Shen, W., and Monnier, V. M., (2007). 2-Aminoadipic acid is a marker of protein carbonyl oxidation in the aging human skin:Effects of diabetes, renal failure and sepsis. Biochem. J. 404:269–277.
104. Shacter, E., (2000). Quantification and significance of protein oxidation in biological samples. Drug Metabol. Rev. 32:307–326.
105. Siddhuraju, P., and Becker, K., (2001). Rapid reversed-phase high performance liquid chromatographic method for the quantification of L-Dopa (L-3,4-dihydroxyphenylalanine), non-methylated and methylated tetrahydroisoquinoline compounds from Mucuna beans. Food Chem. 72:389–394.
106. Sies, H., Stahl, W., and Sevanian, A., (2005). Nutritional, dietary and postprandial oxidative stress. J. Nutr. 135:96–972.
107. Skibsted, L. H., (2011). Nitric oxide and quality and safety of muscle based foods. Nitric Oxide. 24:176–183.
108. Smith, M. A., Richey Harris, P. L., Sayre, L. M., Beckman, J. S., and Perry, G., (1997). Widespread peroxynitrite-mediated damage in Alzheimer's disease. J. Neurosci. 17:2653–2657.
109. Smith, M. A., Richey, P. L., Taneda, S., Kutty, R. K., Sayre, L. M., Monnier, V. M., and Perry, G., (1994). Advanced Maillard reaction end products, free radicals, and protein oxidation in Alzheimer's disease. Ann N Y Acad Sci. 738:447–454.
110. Smith, M. A., Rottkamp, C. A., Nunomura, A., Raina, A. K., and Perry, G., (2000). Oxidative stress in Alzheimer's disease. Biochim. Biophys. Acta. 1502:139–144.
111. Soglia, F., Petracci, M., and Ertbjerg, P., (2016). Novel DNPH-based method for determination of protein carbonylation in muscle and meat. Food Chem. 197:670–675.
112. Soladoye, O. P., Juarez, M. L., Aalhus, J. L., Shand, P., and Estevez, M., (2015). Protein oxidation in processed meat:Mechanisms and potential implications on human health. Compr. Rev. Food Sci. F. 14:106–122.
113. Stadtman, E. R., (1990). Metal ion-catalyzed oxidation of proteins:Biochemical mechanism and biological consequences. Free Rad. Biol. Med. 9:315–325.
114. Stadtman, E. R., (1993). Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annual Rev. Biochem. 62:797–821.
115. Szijarto, I. A., Molnar, G. A., Mikolas, E., Fisi, V., Cseh, J., Laczy, B., Kovács, T., Böddi, K., Takátsy, A., Gollasch, M., Koller, A., and Wittmann, I., (2014). Elevated vascular level of ortho -Tyrosine contributes to the impairment of insulin-induced arterial relaxation. Horm. Metab. Res. 46:749–752.
116. Taha, R., Seidman, E., Mailhot, G., Boudreau, F., Gendron, F.-P., Beaulieu, J.-F., Menard, D., Delvin, E., Amre, D., and Levy, E., (2010). Oxidative stress and mitochondrial functions in the intestinal Caco-2/15 Cell Line. PLoS One. 5:e11817.
117. Timm-Heinrich, M., Eymard, S., Baron, C. P., Nielsen, H. H., and Jacobsen, C., (2013). Oxidative changes during ice storage of rainbow trout (Oncorhynchus mykiss) fed different ratios of marine and vegetable feed ingredients. Food Chem. 136:1220–1230.
118. Trnková, L., Boušová, I., Staňková, V., and Dršata, J., (2015). Study on the interaction of catechins with human serum albumin using spectroscopic and electrophoretic techniques. J. Mol. Struct. 985:243–250.
119. Turski, M. P., Turska, M., Zgrajka, W., Kuc, D., and Turski, W. A., (2009). Presence of kynurenic acid in food and honeybee products. Amino Acids. 36:75–80.
120. Turski, W. A., Malaczewska, J., Marciniak, S., Bednarski, J., Turski, M. P., Jabłonski, M., and Siwicki, A. K., (2014). On the toxicity of kynurenic acid in vivo and in vitro. Pharmacological Reports 66:1127–1133.
121. Ursini, F., and Sevanian, A., (2002). Postprandial oxidative stress. Biol. Chem. 383:599–605.
122. Utrera, M., and Estévez, M., (2012a). Analysis of tryptophan oxidation by fluorescence spectroscopy:Effect of metal-catalyzed oxidation and selected phenolic compounds. Food Chem. 135:88–93.
123. Utrera, M., and Estévez, M., (2012b). Oxidation of myofibrillar proteins and impaired functionality:Underlying mechanisms of the carbonylation pathway. J. Agric. Food Chem. 60:8002–8011.
124. Utrera, M., and Estévez, M., (2013). Oxidative damage to poultry, pork, and beef during frozen storage through the analysis of novel protein oxidation markers. J. Agric. Food Chem. 61:7987–7993.
125. Utrera, M., Rodríguez-Carpena, J.-G., Morcuende, D., and Estévez, M., (2012). Formation of lysine-derived oxidation products and loss of tryptophan during processing of porcine patties with added avocado byproducts. J. Agric. Food Chem. 60:3917–3926.
126. Valko, M., Rhodes, C. J., Moncol, J., Izakovic, M., and Mazur, M., (2006). Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 160:1–40.
127. Van Hecke, T., Vanden Bussche, J., Vanhaecke, L., Vossen, E., Van Camp, J., and De Smet, S., (2014a). Nitrite curing of chicken, pork, and beef inhibits oxidation but does not affect N-nitroso compound (NOC)-specific DNA adduct formation during in vitro digestion. J. Agric. Food Chem. 62:1980–1988.
128. Van Hecke, T., Vossen, E., Hemeryck, L. Y., Vanden Bussche, J., Vanhaecke, L., and De Smet, S., (2015). Increased oxidative and nitrosative reactions during digestion could contribute to the association between well-done red meat consumption and colorectal cancer. Food Chem. 187:29–36.
129. Van Hecke, T., Vossen, E., Vanden Bussche, J., Raes, K., Vanhaecke, L., and De Smet, S., (2014b). Fat content and nitrite-curing influence the formation of oxidation products and NOC-specific DNA adducts during in vitro digestion of meat. PLoS One. 9:e101122.
130. Villaverde, A., and Estévez, M., (2013). Carbonylation of myofibrillar proteins through the maillard pathway:Effect of reducing sugars and reaction temperature. J. Agric. Food Chem. 61:3140–3147.
131. Villaverde, A., Ventanas, J., and Estévez, M., (2014). Nitrite promotes protein carbonylation and strecker aldehyde formation in experimental fermented sausages:Are both events connected?. Meat Sci. 62:665–672.
132. Wang, B., Koivumäki, T., Kylli, P., Heinonen, M., and Poutanen, M., (2014). Protein-phenolic interaction of tryptic digests of β-lactoglobulin and cloudberry ellagitannin. J. Agric. Food Chem. 62:5028–5037.
133. Wang, N., Wang, X.-T., Ding, W., and Wang, Z.-D., (2015). Effect of dose rate on lipid and protein oxidation and the properties of beef proteins. Modern Food Sci. Technol. 31:122–128 and 191.
134. Wang, T. J., Ngo, D., Psychogios, N., Dejam, A., Larson, M. G., Vasan, R. S., Ghorbani, A., O'Sullivan, J., Cheng, S., Rhee, E. P., Sinha, S., McCabe, E., Fox, C. S., O'Donnell, C. J., Ho, J. E., Florez, J. C., Magnusson, M., Pierce, K. A., Souza, A. L., Yu, Y., Carter, C., Light, P. E., Melander, O., Clish, C. B., and Gerszten, R. E., (2013). 2-Aminoadipic acid is a biomarker for diabetes risk. J. Clin. Invest. 123:4309–4317.
135. Wu, P., Xie, F., Xue, M., Xu, X., He, S., Lin, M., and Bai, L., (2015). Advanced oxidation protein products decrease the expression of calcium transport channels in small intestinal epithelium via the p44/42 MAPK signaling pathway. Eur. J. Cell Biol. 94:190–203.
136. Xie, F., Sun, S., Xu, A., Zheng, S., Xue, M., Wu, P., Zeng, J. H., and Bai, L., (2014). Advanced oxidation protein products induce intestine epithelial cell death through a redox-dependent, c-jun N-terminal kinase and poly (ADP-ribose) polymerase-1-mediated pathway. Cell Death Dis. 5:e1006.
137. Xiong, Y. L., (2000). Protein oxidation and implications for muscle foods quality. In:Antioxidants in Muscle Foods, pp. 85–111. Decker, E. A., Faustman, C., and Lopez-Bote, C. J., Eds., Wiley, New York, NY.
138. Xiong, Y. L., and Decker, E. A., (1995). Alterations of muscle proteins functionality by oxidative and antioxidative processes. J. Mus. Foods. 6:139–160.
139. Xiong, Y. L., Decker, E. A., Robe, G. H., and Moody, W. G., (1993). Gelation of crude myofibrillar protein isolated from beef heart under antioxidative conditions. J. Food Sci. 58:1241–1244.
140. Xiong, Y., and Foegeding, E. A., (2015). Protein oxidation–the less appreciated sibling of lipid oxidation. J. Food Sci. 80:iii.
141. Yeh, C.-C., Lai, C.-Y., Hsieh, L.-L., Tang, R., Wu, F.-Y., and Sung, F.-C., (2010). Protein carbonyl levels, glutathione S-transferase polymorphisms and risk of colorectal cancer. Carcinogenesis. 31:228–233.
142. Youngman, L. D., Park, J.-Y. K., and Ames, B. N., (1992). Protein oxidation associated with aging is reduced by dietary restriction of protein or calories. Proc. Natl. Acad. Sci. USA. 89:9112–9116.
143. Zhao, J., Chen, J., Zhu, H., and Xiong, Y. L., (2012). Mass spectrometric evidence of malonaldehyde and 4-hydroxynonenal adductions to radical-scavenging soy peptides. J. Agric. Food Chem. 60:9727–9736.