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http://dx.doi.org/10.5851/kosfa.2019.e96

The Role of Meat Protein in Generation of Oxidative Stress and Pathophysiology of Metabolic Syndromes  

Ahmad, Muhammad Ijaz (Key Laboratory of Meat Processing and Quality Control, MOE, Nanjing Agricultural University)
Ijaz, Muhammad Umair (Key Laboratory of Meat Processing and Quality Control, MOE, Nanjing Agricultural University)
Haq, Ijaz ul (Key Laboratory of Meat Processing and Quality Control, MOE, Nanjing Agricultural University)
Li, Chunbao (Key Laboratory of Meat Processing and Quality Control, MOE, Nanjing Agricultural University)
Publication Information
Food Science of Animal Resources / v.40, no.1, 2020 , pp. 1-10 More about this Journal
Abstract
Various processing methods have a great impact on the physiochemical and nutritional properties of meat that are of health concern. Hence, the postmortem processing of meat by different methods is likely to intensify the potential effects on protein oxidation. The influence of meat protein oxidation on the modulation of the systemic redox status and underlying mechanism is well known. However, the effects of processed meat proteins isolated from different sources on gut microbiota, oxidative stress biomarkers, and metabolomic markers associated with metabolic syndromes are of growing interest. The application of advanced methodological approaches based on OMICS, and mass spectrometric technologies has enabled to better understand the molecular basis of the effect of processed meat oxidation on human health and the aging process. Animal studies indicate the involvement of dietary proteins isolated from different sources on health disorders, which emphasizes the impact of processed meat protein on the richness of bacterial taxa such as (Mucispirillum, Oscillibacter), accompanied by increased expression of lipogenic genes. This review explores the most recent evidences on meat processing techniques, meat protein oxidation, underlying mechanisms, and their potential effects on nutritional value, gut microbiota composition and possible implications on human health.
Keywords
diet; processed meat protein; oxidative stress; metabolic syndromes;
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1 Zhang X, Lu P, Xue W, Wu D, Wen C, Zhou Y. 2017. An evaluation of heat on protein oxidation of soy protein isolate or soy protein isolate mixed with soybean oil in vitro and its consequences on redox status of broilers at early age. Asian-Australas J Anim Sci 30:1135-1142.   DOI
2 Zhou F, Sun W, Zhao M. 2015. Controlled formation of emulsion gels stabilized by salted myofibrillar protein under malondialdehyde (MDA)-induced oxidative stress. J Agric Food Chem 63:3766-3777.   DOI
3 Bax ML, Aubry L, Ferreira C, Daudin JD, Gatellier P, Remond D, Sante-Lhoutellier V. 2012. Cooking temperature is a key determinant of in vitro meat protein digestion rate: Investigation of underlying mechanisms. J Agric Food Chem 60:2569-2576.   DOI
4 Berardo A, De Maere H, Stavropoulou DA, Rysman T, Leroy F, De Smet S. 2016. Effect of sodium ascorbate and sodium nitrite on protein and lipid oxidation in dry fermented sausages. Meat Sci 121:359-364.   DOI
5 Berardo A, Devreese B, De Maere H, Stavropoulou DA, Van Royen G, Leroy F, De Smet S. 2017. Actin proteolysis during ripening of dry fermented sausages at different pH values. Food Chem 221:1322-1332.   DOI
6 Chan DS, Lau R, Aune D, Vieira R, Greenwood DC, Kampman E, Norat T. 2011. Red and processed meat and colorectal cancer incidence: Meta-analysis of prospective studies. PLOS ONE 6:e20456.   DOI
7 Dean RT, Fu S, Stocker R, Davies MJ. 1997. Biochemistry and pathology of radical-mediated protein oxidation. Biochem J 15:1-18.   DOI
8 Du Y, Zhang H, Montano S, Hegestam J, Ekberg NR, Holmgren A, Brismar K, Ungerstedt JS. 2013. Plasma glutaredoxin activity in healthy subjects and patients with abnormal glucose levels or overt type 2 diabetes. Acta Diabetol 51:225-232.   DOI
9 Engelman HM, Alekel DL, Hanson LN, Kanthasamy AG, Reddy MB. 2005. Blood lipid and oxidative stress responses to soy protein with isoflavones and phytic acid in postmenopausal women. Am J Clin Nutr 81:590-596.   DOI
10 Milkovska-Stamenova S, Mnatsakanyan R, Hoffmann R. 2017. Protein carbonylation sites in bovine raw milk and processed milk products. Food Chem 229:417-424.   DOI
11 Mitra B, Lametsch R, Akcan T, Ruiz-Carrascal J. 2018. Pork proteins oxidative modifications under the influence of varied time-temperature thermal treatments: A chemical and redox proteomics assessment. Meat Sci 140:134-144.   DOI
12 Moschen AR, Kaser S, Tilg H. 2013. Non-alcoholic steatohepatitis: A microbiota-driven disease. Trends Endocrinol Metab 24:537-545.   DOI
13 Org E, Parks, BW, Joo JW, Emert B, Schwartzman W, Kang EY, Mehrabian M, Pan C, Knight R, Gunsalus R, Drake TA, Eskin E, Lusis AJ. 2015. Genetic and environmental control of host-gut microbiota interactions. Genome Res 25:1558-1569.   DOI
14 Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI. 2004. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101:15718-15723.   DOI
15 Estevez M. 2011. Protein carbonyls in meat systems: A review. Meat Sci 89:259-279.   DOI
16 Estevez M. 2015. Oxidative damage to poultry: From farm to fork. Poult Sci 94:1368-1378.   DOI
17 Oddy WH, Herbison CE, Jacoby P, Ambrosini GL, O'Sullivan TA, Ayonrinde OT, Olynyk JK, Black LJ, Beilin LJ, Mori TA, Hands BP, Adams LA. 2013. The Western dietary pattern is prospectively associated with nonalcoholic fatty liver disease in adolescence. Am J Gastroenterol 108:778-785.   DOI
18 Oliveira CP, de Costa LC, Tatai C, Della Bina BI, Janiszewski M, Lima ES, Abdalla DS, Lopasso FP, Laurindo FR, Laudanna AA. 2002. Oxidative stress in the pathogenesis of nonalcoholic fatty liver disease, in rats fed with a cholinedeficient diet. J Cell Mol Med 6:399-406.   DOI
19 Philo JS, Arakawa T. 2009. Mechanisms of protein aggregation. Curr Pharm Biotechnol 10:348-351.   DOI
20 Roskams T, Yang SQ, Koteish A, Durnez A, DeVos R, Huang X, Achten R, Verslype C, Diehl AM. 2003. Oxidative stress and oval cell accumulation in mice and humans with alcoholic and nonalcoholic fatty liver disease. Am J Pathol163:1301-1311.   DOI
21 Gatellier P, Kondjoyan A, Portanguen S, Sante-Lhoutellier V. 2010. Effect of cooking on protein oxidation in n-3 polyunsaturated fatty acids enriched beef. Implication on nutritional quality. Meat Sci 85:645-650.   DOI
22 Estradaetal PD, Berton-Carabin CC, Schlangen M, Haagsma A, Pierucci APTR, van der Goot AJ. 2018. Protein oxidation in plant protein-based fibrous products: Effect of encapsulated iron and process conditions. J Agric Food Chem 66:11105-11112.   DOI
23 Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, de Vos WM, Cani PD. 2013. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci USA 110:9066-9071.   DOI
24 Fu J, Bonder MJ, Cenit MC, Tigchelaar EF, Maatman A, Dekens, JA, Brandsma E, Marczynska J, Imhann F, Weersma RK, Franke L, Poon TW, Xavier RJ, Gevers D, Hofker MH, Wijmenga C, Zhernakova A. 2015. The gut microbiome contributes to a substantial proportion of the variation in blood lipids. Circ Res 117:817-824.   DOI
25 Gurbuz G, Heinonen M. 2015. LC-MS investigations on interactions between isolated ${\beta}$-lactoglobulin peptides and lipid oxidation product malondialdehyde. Food Chem 175:300-305.   DOI
26 Sante-Lhoutellier V, Aubry L, Gatellier P. 2007. Effect of oxidation on in vitro digestibility of skeletal muscle myofibrillar proteins. J Agric Food Chem 55:5343-5348.   DOI
27 Rysman T, Utrera M, Morcuende D, Van Royen G, Van Weyenberg S, De Smet S, Estevez M. 2016. Apple phenolics as inhibitors of the carbonylation pathway during in vitro metal-catalyzed oxidation of myofibrillar proteins. Food Chem 211:784-790.   DOI
28 Sante-Lhoutellier V, Astruc T, Marinova P, Greve E, Gatellier P. 2008. Effect of meat cooking on physicochemical state and in vitro digestibility of myofibrillar proteins. J Agric Food Chem 56:1488-1494.   DOI
29 He J, Zhou G, Bai Y, Wang C, Zhu S, Xu X, Li C. 2018. The effect of meat processing methods on changes in disulfide bonding and alteration of protein structures: Impact on protein digestion products. RSC Adv 8:17595-17605.   DOI
30 Hernandez EA, Kahl S, Seelig A, Begovatz P, Irmler M, Kupriyanova YM, Nowotny B, Nowotny P, Herder C, Barosa C, Carvalho F, Rozman J, Neschen S, Jones JG, Beckers J, de Angelis MH, Roden M. 2017. Acute dietary fat intake initiates alterations in energy metabolism and insulin resistance. J Clin Invest 127:695-708.   DOI
31 Sayd T, Chambon C, Sante-Lhoutellier V. 2016. Quantification of peptides released during in vitro digestion of cooked meat. Food Chem 197:1311-1323.   DOI
32 Shacter E. 2000. Quantification and significance of protein oxidation in biological samples. Drug Metab Rev 32:307-326.   DOI
33 Shelton MD, Kern TS, Mieyal JJ. 2007. Glutaredoxin regulates nuclear factor kappa-B and intercellular adhesion molecule in Muller cells: Model of diabetic retinopathy. J Biol Chem 282:12467-12474.   DOI
34 Skibsted LH. 2011. Nitric oxide and quality and safety of muscle based foods. Nitric Oxide 24:176-183.   DOI
35 Smith F, Clark JE, Overman BL, Tozel CC, Huang JH, Rivier JE, Blikslager AT, Moeser AJ. 2009. Early weaning stress impairs development of mucosal barrier function in the porcine intestine. Am J Physiol Gastrointest Liver Physiol 298:G352-G363.
36 Soladoye OP, Juarez ML, Aalhus JL, Shand P, Estevez M. 2015. Protein oxidation in processed meat: Mechanisms and potential implications on human health. Compr Rev Food Sci Food Saf 14:106-122.   DOI
37 Jakobsen LM, Yde CC, Van Hecke T, Jessen R, Young JF, De Smet S, Bertram HC. 2017. Impact of red meat consumption on the metabolome of rats. Mol Nutr Food Res 61:1600387-1600393.   DOI
38 Hu L, Ren S, Shen Q, Chen J, Ye X, Ling J. 2017. Proteomic study of the effect of different cooking methods on protein oxidation in fish fillets. RSC Adv 7:27496-27505.   DOI
39 IARC. 2015. Carcinogenicity of consumption of red and processed meat. Lancet 16:1599-1600.   DOI
40 Ijaz MU, Ahmed MI, Zou X, Hussain M, Zhang M, Zhao F, Xu X, Zhou G, Li C. 2018. Beef, casein, and soy proteins differentially affect lipid metabolism, triglycerides accumulation and gut microbiota of high-fat diet-fed C57BL/6J mice. Front Microbiol 9:2200.   DOI
41 Jongberg S, Skov SH, Torngren MA, Skibsted LH, Lund MN. 2011. Effect of white grape extract and modified atmosphere packaging on lipid and protein oxidation in chill stored beef patties. Food Chem 128:276-283.   DOI
42 Koeth RA, Wang Z, Levison BS, Buffa JA, Org E, Sheehy BT, Britt EB, Fu X, Wu Y, Li L, Smith JD, DiDonato JA, Chen J, Li H, Wu GD, Lewis JD, Warrier M, Brown JM, Krauss RM, Tang WHW, Bushman FD, Lusis AJ, Hazen SL. 2013. Intestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med 19:576-585.   DOI
43 Jiang J, Xiong YL. 2016. Natural antioxidants as food and feed additives to promote health benefits and quality of meat products: A review. Meat Sci 120:107-117.   DOI
44 Kaur L, Maudens E, Haisman DR, Boland MJ, Singh H. 2014. Microstructure and protein digestibility of beef: The effect of cooking conditions as used in stews and curries. LWT-Food Sci Technol 55:612-620.   DOI
45 Kirpich IA, Marsano LS, McClain CJ. 2015. Gut-liver axis, nutrition, and non-alcoholic fatty liver disease. Clin Biochem 48:923-930.   DOI
46 Stadtman ER. 2006. Protein oxidation and aging. Free Radic Res 40:1250-1258.   DOI
47 Soladoye OP, Shand P, Dugan MER, Gariepy C, Aalhus JL, Estevez M, Juarez M. 2017. Influence of cooking methods and storage time on lipid and protein oxidation and heterocyclic aromatic amines production in bacon. Food Res Int 99:660-669.   DOI
48 Song S, Hooiveld GJ, Li M, Zhao F, Zhang W, Xu X, Muller M, Li C, Zhou G. 2016. Dietary soy and meat proteins induce distinct physiological and gene expression changes in rats. Sci Rep 6:20036.   DOI
49 Song S, Hua C, Zhao F, Li M, Fu Q, Hooiveld GJEJ, Muller M, Li C, Zhou G. 2018. Purified dietary red and white meat proteins show beneficial effects on growth and metabolism of young rats compared to casein and soy protein. J Agric Food Chem 66:9942-9951.   DOI
50 Sun W, Zhao M, Yang B, Zhao H, Cui C. 2011. Oxidation of sarcoplasmic proteins during processing of Cantonese sausage in relation to their aggregation behaviour and in vitro digestibility. Meat Sci 88:462-467.   DOI
51 Suman SP, Hunt MC, Nair MN, Rentfrow G. 2014. Improving beef color stability: Practical strategies and underlying mechanisms. Meat Sci 98:490-504.   DOI
52 Tremaroli V, Backhed F. 2012. Functional interactions between the gut microbiota and host metabolism. Nature 489:242-249.   DOI
53 Turner KM, Keogh JB, Meikle PJ, Clifton PM. 2017. Changes in lipids and inflammatory markers after consuming diets high in red meat or dairy for four weeks. Nutrients 9:886-891.   DOI
54 Utrera M, Morcuende D, Ganhao R, Estevez M. 2015. Role of phenolics extracting from Rosa canina L. on meat protein oxidation during frozen storage and beef patties processing. Food Bioproc Technol 8:854-864.   DOI
55 Aesif SW, Kuipers I, Van der Velden J, Tully JE, Guala AS, Anathy V, Sheely JI, Reynaert NL, Wouters EF, van der Vliet A, Janssen-Heininger YM. 2011. Activation of the glutaredoxin-1 gene by nuclear factor ${\kappa}B$ enhances signaling. Free Radic Biol Med 51:1249-1257.   DOI
56 Zhu Y, Shi X, Lin X, Ye K, Xu X, Li C, Zhou G. 2017. Beef, chicken, and soy proteins in diets induce different gut microbiota and metabolites in rats. Front Microbiol 8:1395.   DOI
57 Ahmad MI, Zou X, Ijaz, UM, Hussain M. Liu C, Xu X, Zhou G, Li C. 2019. Processed meat protein promoted inflammation and hepatic lipogenesis by upregulating Nrf2/Keap1 signaling pathway in Glrx-deficient mice. J Agric Food Chem 67:8794-8809.   DOI
58 Aalhus J, Dugan M. 2014. Spoilage, factors affecting (b) oxidative and enzymatic. In Encyclopedia of meat sciences. 2nd ed. Dikeman M, Devine C (ed). Academic Press, London, UK. pp 394-400.
59 Ley RE, Turnbaugh PJ, Klein S, Gordon JI. 2006. Microbial ecology: Human gut microbes associated with obesity. Nature 444:1022-1023.   DOI
60 Le Roy T, Llopis M, Lepage P, Bruneau A, Rabot S, Bevilacqua C, Martin P, Philippe C, Walker F, Bado A, Perlemuter G, Cassard-Doulcier AM, Gerard P. 2013. Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice. Gut 62:1787-1794.   DOI
61 Li L, Liu Y, Zou X, He J, Xu X, Zhou G, Li C. 2017. In vitro protein digestibility of pork products is affected by the method of processing. Food Res Int 92:88-94.   DOI
62 Liu Z, Xiong YL, Chen J. 2011. Morphological examinations of oxidatively stressed pork muscle and myofibrils upon salt marination and cooking to elucidate the water-binding potential. J Agric Food Chem 59:13026-13034.   DOI
63 Martinaud A, Mercier Y, Marinova P, Tassy C, Gatellier P, Renerre M. 1997. Comparison of oxidative processes on myofibrillar proteins from beef during maturation and by different model oxidation systems. J Agric Food Chem 45:2481-2487.   DOI
64 Liu X, Xavier C, Jann J, Wu H. 2016. Salvianolic acid B (Sal B) protects retinal pigment epithelial cells from oxidative stress-induced cell death by activating glutaredoxin 1 (Grx1). Int J Mol Sci 17:1835-1840.   DOI
65 Lund MN, Heinonen M, Baron CP, Estevez M. 2011. Protein oxidation in muscle foods: A review. Mol Nutr Food Res 55:83-95.   DOI
66 Mann JP, Raponi M, Nobili V. 2017. Clinical implications of understanding the association between oxidative stress and pediatric NAFLD. Expert Rev Gastroenterol Hepatol 11:371-382.   DOI
67 Miele L, Dall'armi V, Cefalo C, Nedovic B, Arzani D, Amore R, Rapaccini G, Gasbarrini A, Ricciardi W, Grieco A, Boccia S. 2014. A case-control study on the effect of metabolic gene polymorphisms, nutrition, and their interaction on the risk of non-alcoholic fatty liver disease. Genes Nutr 9:383-391.   DOI
68 Xiong Y. 2000. Protein oxidation and implications for muscle foods quality. In Antioxidants in muscle foods. Decker EA, Faustman C, Lopez-Bote CJ (ed). Wiley, New York, NY. pp 85-111.
69 Wen S, Zhou G, Li L, Xu X, Yu X, Bai Y, Li C. 2015. Effect of cooking on in vitro digestion of pork proteins: A peptidomic perspective. J Agric Food Chem 63:250-261.   DOI
70 Wruck W, Adjaye J. 2017. Meta-analysis reveals up-regulation of cholesterol processes in non-alcoholic and down-regulation in alcoholic fatty liver disease. World J Hepatol 9:443-454.   DOI
71 Xiong YL, Park D, Ooizumi T. 2009. Variation in the cross-linking pattern of porcine myofibrillar protein exposed to three oxidative environments. J Agric Food Chem 57:153-159.   DOI
72 Yang F, Yi M, Liu Y, Wang Q, Hu Y, Deng H. 2018. Glutaredoxin-1 silencing induces cell senescence via p53/p21/p16 signaling axis. J Proteome Res 17:1091-1100.   DOI
73 Youngman LD, Park JY, Ames BN. 1992. Protein oxidation associated with aging is reduced by dietary restriction of protein or calories. Proc Natl Acad Sci 89:9112-9116.   DOI
74 Zelber-Sagi S, Ivancovsky-Wajcman D, Fliss Isakov N, Webb M, Orenstein D, Shibolet O, Kariv R. 2018. High red and processed meat consumption is associated with non-alcoholic fatty liver disease and insulin resistance. J Hepatol 68:1239-1246.   DOI