Structural and functional properties of food protein-derived antioxidant peptides
Ifeanyi D. Nwachukwu
Department of Food and Human Nutritional Sciences, University of Manitoba, Winnipeg, Canada
Search for more papers by this authorCorresponding Author
Rotimi E. Aluko
Department of Food and Human Nutritional Sciences, University of Manitoba, Winnipeg, Canada
Richardson Centre for Functional Foods and Nutraceuticals, University of Manitoba, Winnipeg, Canada
Correspondence
Rotimi E. Aluko, Department of Food and Human Nutritional Sciences, University of Manitoba, Winnipeg, Manitoba R3T 2N2, Canada.
Email: [email protected]
Search for more papers by this authorIfeanyi D. Nwachukwu
Department of Food and Human Nutritional Sciences, University of Manitoba, Winnipeg, Canada
Search for more papers by this authorCorresponding Author
Rotimi E. Aluko
Department of Food and Human Nutritional Sciences, University of Manitoba, Winnipeg, Canada
Richardson Centre for Functional Foods and Nutraceuticals, University of Manitoba, Winnipeg, Canada
Correspondence
Rotimi E. Aluko, Department of Food and Human Nutritional Sciences, University of Manitoba, Winnipeg, Manitoba R3T 2N2, Canada.
Email: [email protected]
Search for more papers by this author[Correction added on 30 January 2019: this article has been added to the issue after an inadvertent omission.]
Abstract
The aim of this work is to provide a timely examination of the structure–activity relationship of antioxidative peptides. The main production approach involves enzymatic hydrolysis of animal and plant proteins to produce protein hydrolyzates, which can be further processed by membrane ultrafiltration into size-based peptide fractions. The hydrolyzates and peptide fractions can also be subjected to separation by column chromatography to obtain pure peptides. Although the structural basis for enhanced antioxidant activity varies, protein hydrolyzates and peptide fractions that contain largely low molecular weight peptides have generally been shown to be potent antioxidants. In addition to having hydrophobic amino acids such as Leu or Val in their N-terminal regions, protein hydrolyzates, and peptides containing the nucleophilic sulfur-containing amino acid residues (Cys and Met), aromatic amino acid residues (Phe, Trp, and Tyr) and/or the imidazole ring-containing His have been generally found to possess strong antioxidant properties.
Practical applications
High levels of reactive oxygen species (ROS) in addition to the presence of metal cations can lead to oxidative stress, which promotes reactions that cause destruction of critical cellular biopolymers, such as proteins, lipids, and nucleic acids. Oxidative stress could be due to insufficient levels of natural cellular antioxidants, which enables accumulation of ROS to toxic levels. A proposed approach to ameliorating oxidative stress is the provision of exogenous peptides that can be consumed to complement cellular antioxidants. Food protein-derived peptides consist of amino acids joined by peptides bonds just like glutathione, a very powerful natural cellular antioxidant. Therefore, this review provides a timely summary of the in vitro and in vivo reactions impacted by antioxidant peptides and the postulated mechanisms of action, which could aid development of potent antioxidant agents. The review also serves as a resource material for identifying novel antioxidant peptide sources for the formulation of functional foods and nutraceuticals.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
REFERENCES
- Agrawal, H., Joshi, R., & Gupta, M. (2016). Isolation, purification and characterization of antioxidative peptide of pearl millet (Pennisetum glaucum) protein hydrolysate. Food Chemistry, 204, 365–372. https://doi.org/10.1016/j.foodchem.2016.02.127
- Ajibola, C. F., Fashakin, J. B., Fagbemi, T. N., & Aluko, R. E. (2011). Effect of peptide size on antioxidant properties of African yam bean seed (Sphenostylis stenocarpa) protein hydrolysate fractions. International Journal of Molecular Sciences, 12, 6685–6702. https://doi.org/10.3390/ijms12106685
- Alashi, A. M., Blanchard, C. L., Mailer, R. J., Agboola, S. O., Mawson, A. J., He, R., … Aluko, R. E. (2014). Antioxidant properties of Australian canola meal protein hydrolysates. Food Chemistry, 146, 500–506. https://doi.org/10.1016/j.foodchem.2013.09.081
- Aluko, R. E. (2012). Functional foods and nutraceuticals (pp. 37–61). New York, NY: Springer Science+Business Media LLC.
10.1007/978-1-4614-3480-1_3 Google Scholar
- Alzahrani, M. A. J., Perera, C. O., & Hemar, Y. (2018). Production of bioactive proteins and peptides from the diatom Nitzschia laevis and comparison of their in vitro antioxidant activities with those from Spirulina platensis and Chlorella vulgaris. International Journal of Food Science & Technology, 53, 676–682.
- Babini, E., Tagliazucchi, D., Martini, S., Dei Più, L., & Gianotti, A. (2017). LC-ESI-QTOF-MS identification of novel antioxidant peptides obtained by enzymatic and microbial hydrolysis of vegetable proteins. Food Chemistry, 228, 186–196. https://doi.org/10.1016/j.foodchem.2017.01.143
- Cai, L., Wu, X., Zhang, Y., Li, X., Ma, S., & Li, J. (2015). Purification and characterization of three antioxidant peptides from protein hydrolysate of grass carp (Ctenopharyngodon idella) skin. Journal of Functional Foods, 16, 234–242. https://doi.org/10.1016/j.jff.2015.04.042
- Chai, H.-J., Wu, C.-J., Yang, S.-H., Li, T.-L., & Pan, B. S. (2016). Peptides from hydrolysate of lantern fish (Benthosema pterotum) proved neuroprotective in vitro and in vivo. Journal of Functional Foods, 24, 438–449. https://doi.org/10.1016/j.jff.2016.04.009
- Chen, J., Cui, C., Zhao, H., Wang, H., Zhao, M., Wang, W., & Dong, K. (2018). The effect of high solid concentrations on enzymatic hydrolysis of soya bean protein isolate and antioxidant activity of the resulting hydrolysates. International Journal of Food Science & Technology, 53, 954–961. https://doi.org/10.1111/ijfs.13668
- Cheung, L. K. Y., Aluko, R. E., Cliff, M. A., & Li-Chan, E. C. Y. (2015). Effects of exopeptidase treatment on antihypertensive activity and taste attributes of enzymatic whey protein hydrolysates. Journal of Functional Foods, 13, 262–275. https://doi.org/10.1016/j.jff.2014.12.036
- Chi, C.-F., Hu, F.-Y., Wang, B., Li, T., & Ding, G.-F. (2015). Antioxidant and anticancer peptides from the protein hydrolysate of blood clam (Tegillarca granosa) muscle. Journal of Functional Foods, 15, 301–313. https://doi.org/10.1016/j.jff.2015.03.045
- Cotabarren, J., Rosso, A. M., Tellechea, M., García-Pardo, J., Rivera, J. L., ObregóN, W. D., & Parisi, M. G. (2019). Adding value to the chia (Salvia hispanica L.) expeller: Production of bioactive peptides with antioxidant properties by enzymatic hydrolysis with Papain. Food Chemistry, 274, 848–856. https://doi.org/10.1016/j.foodchem.2018.09.061
- Edens, L., Dekker, P., Van Der Hoeven, R., Deen, F., De Roos, A., & Floris, R. (2005). Extracellular prolyl endoprotease from Aspergillus niger and its use in the debittering of protein hydrolysates. Journal of Agricultural and Food Chemistry, 53, 7950–7957.
- Egusa Saiga, A., & Nishimura, T. (2013). Antioxidative properties of peptides obtaine from porcine myofibrillar proteins by a proteasetreatment in an Fe (II)-induced aqueous lipid peroxidation system. Bioscience, Biotechnology, and Biochemistry, 77, 2201–2204.
- Feng, Y.-X., Ruan, G.-R., Jin, F., Xu, J., & Wang, F.-J. (2018). Purification, identification, and synthesis of five novel antioxidant peptides from Chinese chestnut (Castanea mollissima Blume) protein hydrolysates. LWT Food Science and Technology, 92, 40–46. https://doi.org/10.1016/j.lwt.2018.01.006
- Gallego, M., Mora, L., & Toldrá, F. (2018). Characterisation of the antioxidant peptide AEEEYPDL and its quantification in Spanish dry-cured ham. Food Chemistry, 258, 8–15. https://doi.org/10.1016/j.foodchem.2018.03.035
- Girgih, A. T., Alashi, A. M., He, R., Malomo, S. A., Raj, P., Netticadan, T., & Aluko, R. E. (2014). A novel hemp seed meal protein hydrolysate reduces oxidative stress factors in spontaneously hypertensive rats. Nutrients, 6, 5652–5666.
- Girgih, A. T., He, R., Hasan, F. M., Udenigwe, C. C., Gill, T. A., & Aluko, R. E. (2015). Evaluation of the in vitro antioxidant properties of a Cod (Gadus morhua) protein hydrolysate and peptide fractions. Food Chemistry, 173, 652–659. https://doi.org/10.1016/j.foodchem.2014.10.079
- Girgih, A. T., He, R., Malomo, S. A., Offengenden, M., Wu, J., & Aluko, R. E. (2014). Structural and functional characterization of hemp seed (Cannabis sativa L.) protein-derived antioxidant and antihypertensive peptides. Journal of Functional Foods, 6, 384–394.
- Girgih, A. T., Udenigwe, C. C., & Aluko, R. E. (2011). In vitro antioxidant properties of hempseed (Cannabis sativa L.) protein hydrolysate fractions. Journal of American Oil Chemists’ Society, 88, 381–389. https://doi.org/10.1007/s11746-010-1686-7
- Girgih, A. T., Udenigwe, C. C., & Aluko, R. E. (2013). Reverse-phase HPLC separation of hemp seed (Cannabis sativa L.) protein hydrolysate produced peptide fractions with enhanced antioxidant capacity. Plant Foods for Human Nutrition, 68, 39–46.
- Girgih, A. T., Udenigwe, C. C., Hasan, F. M., Gill, T. A., & Aluko, R. E. (2013). Antioxidant properties of Salmon (Salmo salar) protein hydrolysate and peptide fractions isolated by reverse-phase HPLC. Food Research International, 52, 315–322.
- Görlach, A., Dimova, E. Y., Petry, A., Martínez-Ruiz, A., Hernansanz-Agustín, P., Rolo, A. P., … Kietzmann, T. (2015). Reactive oxygen species, nutrition, hypoxia and diseases: Problems solved? Redox Biology, 6, 372–385.
- Harnedy, P. A., O’Keeffe, M. B., & Fitzgerald, R. J. (2017). Fractionation and identification of antioxidant peptides from an enzymatically hydrolysed Palmaria palmata protein isolate. Food Research International, 100, 416–422. https://doi.org/10.1016/j.foodres.2017.07.037
- He, R., Girgih, A. T., Malomo, S. A., Ju, X., & Aluko, R. E. (2013). Antioxidant activities of enzymatic rapeseed protein hydrolysates and the membrane ultrafiltration fractions. Journal of Functional Foods, 5, 219–227. https://doi.org/10.1016/j.jff.2012.10.008
- He, R., Ju, X., Yuan, J., Wang, L., Girgih, A. T., & Aluko, R. E. (2012). Antioxidant activities of rapeseed peptides produced by solid state fermentation. Food Research International, 49, 432–438. https://doi.org/10.1016/j.foodres.2012.08.023
- Humiski, L., & Aluko, R. E. (2007). Physicochemical and bitterness properties of enzymatic pea protein hydrolysates. Journal of Food Science, 72, S605–S611. https://doi.org/10.1111/j.1750-3841.2007.00475.x
- Hwang, C. F., Chen, Y. A., Luo, C., & Chiang, W. D. (2016). Antioxidant and antibacterial activities of peptide fractions from flaxseed protein hydrolysed by protease from Bacillus altitudinis HK02. International Journal of Food Science & Technology, 51, 681–689.
- Ishibashi, N., Ono, I., Kato, K., Shigenaga, T., Shinoda, I., Okai, H., & Fukui, S. (1988). Role of the hydrophobic amino acid residue in the bitterness of peptides. Agricultural and Biological Chemistry, 52, 91–94. https://doi.org/10.1080/00021369.1988.10868631
- Je, J.-Y., Park, S. Y., Hwang, J.-Y., & Ahn, C.-B. (2015). Amino acid composition and in vitro antioxidant and cytoprotective activity of abalone viscera hydrolysate. Journal of Functional Foods, 16, 94–103. https://doi.org/10.1016/j.jff.2015.04.023
- Jemil, I., Abdelhedi, O., Nasri, R., Mora, L., Jridi, M., Aristoy, M.-C., … Nasri, M. (2017). Novel bioactive peptides from enzymatic hydrolysate of Sardinelle (Sardinella aurita) muscle proteins hydrolysed by Bacillus subtilis A26 proteases. Food Research International, 100, 121–133. https://doi.org/10.1016/j.foodres.2017.06.018
- Jin, D.-X., Liu, X.-L., Zheng, X.-Q., Wang, X.-J., & He, J.-F. (2016). Preparation of antioxidative corn protein hydrolysates, purification and evaluation of three novel corn antioxidant peptides. Food Chemistry, 204, 427–436. https://doi.org/10.1016/j.foodchem.2016.02.119
- Ketnawa, S., Wickramathilaka, M., & Liceaga, A. M. (2018). Changes on antioxidant activity of microwave-treated protein hydrolysates after simulated gastrointestinal digestion: Purification and identification. Food Chemistry, 254, 36–46. https://doi.org/10.1016/j.foodchem.2018.01.133
- Kilara, A., & Chandan, R. C. (2011). Enzyme-modified dairy ingredients. In A. Kilara & R. C. Chandan (Eds.), Dairy ingredients for food processing (pp. 317–333). Hoboken, NJ: Blackwell Publishing Ltd.
- Kim, M. R., Choi, S. Y., & Lee, C. H. (1999). Molecular characterization and bitter taste formation of tryptic hydrolysis of 11S glycinin. Journal of Microbiology and Biotechnology, 9, 509–513.
- Leung, R., Venus, C., Zeng, T., & Tsopmo, A. (2018). Structure-function relationships of hydroxyl radical scavenging and chromium-VI reducing cysteine-tripeptides derived from rye secalin. Food Chemistry, 254, 165–169. https://doi.org/10.1016/j.foodchem.2018.01.190
- Lin, H. M., Deng, S.-G., & Huang, S.-B. (2014). Antioxidant activities of ferrous-chelating peptides isolated from five types of low-value fish protein hydrolysates. Journal of Food Biochemistry, 38, 627–633. https://doi.org/10.1111/jfbc.12103
- Liu, C., Ren, D., Li, J., Fang, L., Wang, J., Liu, J., & Min, W. (2018). Cytoprotective effect and purification of novel antioxidant peptides from hazelnut (C. heterophylla Fisch) protein hydrolysates. Journal of Functional Foods, 42, 203–215. https://doi.org/10.1016/j.jff.2017.12.003
- Liu, X., Zheng, X., Song, Z., Liu, X., Kopparapu, N. K., Wang, X., & Zheng, Y. (2015). Preparation of enzymatic pretreated corn gluten meal hydrolysate and in vivo evaluation of its antioxidant activity. Journal of Functional Foods, 18, 1147–1157. https://doi.org/10.1016/j.jff.2014.10.013
- Liu, Y., Wan, S., Liu, J., Zou, Y., & Liao, S. (2017). Antioxidant activity and stability study of peptides from enzymatically hydrolyzed male silkmoth. Journal of Food Processing and Preservation, 41, e13081. https://doi.org/10.1111/jfpp.13081
- Lobo, V., Patil, A., Phatak, A., & Chandra, N. (2010). Free radicals, antioxidants and functional foods: Impact on human health. Pharmacognosy Reviews, 4, 118–126. https://doi.org/10.4103/0973-7847.70902
- Luo, F., Xing, R., Wang, X., Yang, H., & Li, P. (2018). Antioxidant activities of Rapana venosa meat and visceral mass during simulated gastrointestinal digestion and their membrane ultrafiltration fractions. International Journal of Food Science & Technology, 53, 395–403.
- Ma, Y., Wu, Y., & Li, L. (2018). Relationship between primary structure or spatial conformation and functional activity of antioxidant peptides from Pinctada fucata. Food Chemistry, 264, 108–117. https://doi.org/10.1016/j.foodchem.2018.05.006
- Mada, S. B., Reddi, S., Kumar, N., Kumar, R., Kapila, S., Kapila, R., … Ahmad, N. (2017). Antioxidative peptide from milk exhibits antiosteopenic effects through inhibition of oxidative damage and bone-resorbing cytokines in ovariectomized rats. Nutrition, 43–44, 21–31. https://doi.org/10.1016/j.nut.2017.06.010
- Mamelona, J., Saint-Louis, R., & Pelletier, É. (2010). Nutritional composition and antioxidant properties of protein hydrolysates prepared from echinoderm byproducts. International Journal of Food Science & Technology, 45, 147–154. https://doi.org/10.1111/j.1365-2621.2009.02114.x
- Marques, M. R., Soares Freitas, R. A. M., Corrêa Carlos, A. C., Siguemoto, É. S., Fontanari, G. G., & Arêas, J. A. G. (2015). Peptides from cowpea present antioxidant activity, inhibit cholesterol synthesis and its solubilisation into micelles. Food Chemistry, 168, 288–293. https://doi.org/10.1016/j.foodchem.2014.07.049
- Nazeer, R. A., Kumar, N. S. S., & Ganesh, R. J. (2012). In vitro and in vivo studies on the antioxidant activity of fish peptide isolated from the croaker (Otolithes ruber) muscle protein hydrolysate. Peptides, 35, 261–268. https://doi.org/10.1016/j.peptides.2012.03.028
- Nwachukwu, I. D., & Aluko, R. E. (2018). Antioxidant properties of flaxseed protein hydrolysates: Influence of hydrolytic enzyme concentration and peptide size. Journal of the American Oil Chemists' Society, 95, 1105–1118.
- O’Sullivan, S. M., Lafarga, T., Hayes, M., & O’Brien, N. M. (2017). Bioactivity of bovine lung hydrolysates prepared using papain, pepsin, and Alcalase. Journal of Food Biochemistry, 41, e12406. https://doi.org/10.1111/jfbc.12406
- Pan, D., Guo, Y., & Jiang, Y. (2011). Anti-fatigue and antioxidative activities of peptides isolated from milk proteins. Journal of Food Biochemistry, 35, 1130–1144. https://doi.org/10.1111/j.1745-4514.2010.00440.x
- Park, S. Y., Kim, Y.-S., Ahn, C.-B., & Je, J.-Y. (2016). Partial purification and identification of three antioxidant peptides with hepatoprotective effects from blue mussel (Mytilus edulis) hydrolysate by peptic hydrolysis. Journal of Functional Foods, 20, 88–95. https://doi.org/10.1016/j.jff.2015.10.023
- Phongthai, S., D’Amico, S., Schoenlechner, R., Homthawornchoo, W., & Rawdkuen, S. (2018). Fractionation and antioxidant properties of rice bran protein hydrolysates stimulated by in vitro gastrointestinal digestion. Food Chemistry, 240, 156–164. https://doi.org/10.1016/j.foodchem.2017.07.080
- Pownall, T. L., Udenigwe, C. C., & Aluko, R. E. (2010). Amino acid composition and antioxidant properties of pea seed (Pisum sativum L.) enzymatic protein hydrolysate fractions. Journal of Agricultural and Food Chemistry, 58, 4712–4718. https://doi.org/10.1021/jf904456r
- Pownall, T. L., Udenigwe, C. C., & Aluko, R. E. (2011). Effects of cationic property on the in vitro antioxidant activities of pea protein hydrolysate fractions. Food Research International, 44, 1069–1074. https://doi.org/10.1016/j.foodres.2011.03.017
- Qiu, X., Chen, S., & Dong, S. (2014). Effects of silver carp antioxidant peptide on the lipid oxidation of sierra fish fillets (Scomberomorus niphonius) during frozen storage. Journal of Food Biochemistry, 38, 167–174.
- Rahman, M. S., Hee Choi, Y., Seok Choi, Y., Alam, M. B., Han Lee, S., & Cheol Yoo, J. (2018). A novel antioxidant peptide, purified from Bacillus amyloliquefaciens, showed strong antioxidant potential via Nrf-2 mediated heme oxygenase-1 expression. Food Chemistry, 239, 502–510. https://doi.org/10.1016/j.foodchem.2017.06.106
- Rajabzadeh, M., Pourashouri, P., Shabanpour, B., & Alishahi, A. (2018). Amino acid composition, antioxidant and functional properties of protein hydrolysates from the roe of rainbow trout (Oncorhynchus mykiss). International Journal of Food Science & Technology, 53, 313–319.
- Ryan, J. T., Ross, R. P., Bolton, D., Fitzgerald, G. F., & Stanton, C. (2011). Bioactive peptides from muscle sources: Meat and fish. Nutrients, 3, 765–791. https://doi.org/10.3390/nu3090765
- Sae-Leaw, T., Karnjanapratum, S., O’ Callaghan, Y. C., O’ Keeffe, M. B., Fitzgerald, R. J., O’ Brien, N. M., & Benjakul, S. (2017). Purification and identification of antioxidant peptides from gelatin hydrolysate of seabass skin. Journal of Food Biochemistry, 41, e12350.
- Saisavoey, T., Sangtanoo, P., Reamtong, O., & Karnchanatat, A. (2016). Antioxidant and anti-Inflammatory effects of defatted rice bran (Oryza Sativa L.) protein hydrolysates on Raw 264.7 macrophage cells. Journal of Food Biochemistry, 40, 731–740.
- Samaranayaka, A. G. P., & Li-Chan, E. C. Y. (2011). Food-derived peptidic antioxidants: A review of their production, assessment, and potential applications. Journal of Functional Foods, 3, 229–254. https://doi.org/10.1016/j.jff.2011.05.006
- Sarmadi, B. H., & Ismail, A. (2010). Antioxidative peptides from food proteins: A review. Peptides, 31, 1949–1956. https://doi.org/10.1016/j.peptides.2010.06.020
- Shavandi, A., Hu, Z., Teh, S., Zhao, J., Carne, A., Bekhit, A., & Bekhit, A. E. (2017). Antioxidant and functional properties of protein hydrolysates obtained from squid pen chitosan extraction effluent. Food Chemistry, 227, 194–201. https://doi.org/10.1016/j.foodchem.2017.01.099
- Siow, H.-L., & Gan, C.-Y. (2016). Extraction, identification, and structure–activity relationship of antioxidative and α-amylase inhibitory peptides from cumin seeds (Cuminum cyminum). Journal of Functional Foods, 22, 1–12. https://doi.org/10.1016/j.jff.2016.01.011
- Su, S., Wan, Y., Guo, S., Zhang, C., Zhang, T., & Liang, M. (2018). Effect of peptide–phenolic interaction on the antioxidant capacity of walnut protein hydrolysates. International Journal of Food Science & Technology, 53, 508–515. https://doi.org/10.1111/ijfs.13610
- Sun, C., Wu, W., Yin, Z., Fan, L., Ma, Y., Lai, F., & Wu, H. (2018). Effects of simulated gastrointestinal digestion on the physicochemical properties, erythrocyte haemolysis inhibitory ability and chemical antioxidant activity of mulberry leaf protein and its hydrolysates. International Journal of Food Science & Technology, 53, 282–295. https://doi.org/10.1111/ijfs.13584
- Suwal, S., Ketnawa, S., Liceaga, A. M., & Huang, J.-Y. (2018). Electro-membrane fractionation of antioxidant peptides from protein hydrolysates of rainbow trout (Oncorhynchus mykiss) byproducts. Innovative Food Science and Emerging Technologies, 45, 122–131. https://doi.org/10.1016/j.ifset.2017.08.016
- Torres-Fuentes, C., Contreras, M. D. M., Recio, I., Alaiz, M., & Vioque, J. (2015). Identification and characterization of antioxidant peptides from chickpea protein hydrolysates. Food Chemistry, 180, 194–202. https://doi.org/10.1016/j.foodchem.2015.02.046
- Tsopmo, A., Romanowski, A., Banda, L., Lavoie, J. C., Jenssen, H., & Friel, J. K. (2011). Novel anti-oxidative peptides from enzymatic digestion of human milk. Food Chemistry, 126, 1138–1143. https://doi.org/10.1016/j.foodchem.2010.11.146
- Udenigwe, C. C., & Aluko, R. E. (2011). Chemometric analysis of the amino acid requirements of antioxidant food protein hydrolysates. International Journal of Molecular Sciences, 12, 3148–3161. https://doi.org/10.3390/ijms12053148
- Udenigwe, C. C., & Aluko, R. E. (2012). Food protein-derived bioactive peptides: Production, processing, and potential health benefits. Journal of Food Science, 77, R11–R24. https://doi.org/10.1111/j.1750-3841.2011.02455.x
- Verbon, E. H., Post, J. A., & Boonstra, J. (2012). The influence of reactive oxygen species on cell cycle progression in mammalian cells. Gene, 511, 1–6. https://doi.org/10.1016/j.gene.2012.08.038
- Vilcacundo, R., Miralles, B., Carrillo, W., & Hernández-Ledesma, B. (2018). In vitro chemopreventive properties of peptides released from quinoa (Chenopodium quinoa Willd.) protein under simulated gastrointestinal digestion. Food Research International, 105, 403–411. https://doi.org/10.1016/j.foodres.2017.11.036
- Wang, B., Wang, C., Huo, Y., & Li, B. (2016). The absorbates of positively charged peptides from casein show high inhibition ability of LDL oxidation in vitro: Identification of intact absorbed peptides. Journal of Functional Foods, 20, 380–393. https://doi.org/10.1016/j.jff.2015.11.012
- Wang, L., Ding, L., Xue, C., Ma, S., Du, Z., Zhang, T., & Liu, J. (2018). Corn gluten hydrolysate regulates the expressions of antioxidant defense and ROS metabolism relevant genes in H2O2-induced HepG2 cells. Journal of Functional Foods, 42, 362–370. https://doi.org/10.1016/j.jff.2017.12.056
- Wong, F.-C., Xiao, J., Ong, M. G. L., Pang, M.-J., Wong, S.-J., Teh, L.-K., & Chai, T.-T. (2019). Identification and characterization of antioxidant peptides from hydrolysate of blue-spotted stingray and their stability against thermal, pH and simulated gastrointestinal digestion treatments. Food Chemistry, 271, 614–622. https://doi.org/10.1016/j.foodchem.2018.07.206
- Wu, J., Huo, J., Huang, M., Zhao, M., Luo, X., & Sun, B. (2017). Structural characterization of a tetrapeptide from sesame flavor-type Baijiu and its preventive effects against AAPH-induced oxidative stress in HepG2 Cells. Journal of Agricultural and Food Chemistry, 65, 10495–10504. https://doi.org/10.1021/acs.jafc.7b04815
- Wu, Y., Wang, J., Li, L., Yang, X., Wang, J., & Hu, X. (2018). Purification and identification of an antioxidant peptide from Pinctada fucata muscle. CyTA-Journal of Food, 16, 11–19.
- Xie, N., Liu, S., Wang, C., & Li, B. (2014). Stability of casein antioxidant peptide fractions during in vitro digestion/Caco-2 cell model: Characteristics of the resistant peptides. European Food Research and Technology, 239, 577–586. https://doi.org/10.1007/s00217-014-2253-5
- Xing, L., Ge, Q., Jiang, D., Gao, X., Liu, R., Cao, S., … Zhang, W. (2018). Caco-2 cell-based electrochemical biosensor for evaluating the antioxidant capacity of Asp-Leu-Glu-Glu isolated from dry-cured Xuanwei ham. Biosensors and Bioelectronics, 105, 81–89. https://doi.org/10.1016/j.bios.2018.01.020
- Xu, F., Wang, L., Ju, X., Zhang, J., Yin, S., Shi, J., … Yuan, Q. (2017). Transepithelial transport of YWDHNNPQIR and its metabolic fate with cytoprotection against oxidative stress in human intestinal Caco-2 cells. Journal of Agricultural and Food Chemistry, 65, 2056–2065.
- Xu, J., Li, Y., Regenstein, J., & Su, X. (2017). In vitro and in vivo anti-oxidation and anti-fatigue effect of monkfish liver hydrolysate. Food Bioscience, 18, 9–14.
- Yang, P., Ke, H., Hong, P., Zeng, S., & Cao, W. (2011). Antioxidant activity of bigeye tuna (Thunnus obesus) head protein hydrolysate prepared with Alcalase. International Journal of Food Science & Technology, 46, 2460–2466. https://doi.org/10.1111/j.1365-2621.2011.02768.x
- Yang, R., Li, X., Lin, S., Zhang, Z., & Chen, F. (2017). Identification of novel peptides from 3 to 10 kDa pine nut (Pinus koraiensis) meal protein, with an exploration of the relationship between their antioxidant activities and secondary structure. Food Chemistry, 219, 311–320. https://doi.org/10.1016/j.foodchem.2016.09.163
- Young, D., Nau, F., Pasco, M., & Mine, Y. (2011). Identification of hen egg yolk-derived phosvitin phosphopeptides and their effects on gene expression profiling against oxidative stress-induced Caco-2 cells. Journal of Agricultural and Food Chemistry, 59, 9207–9218. https://doi.org/10.1021/jf202092d
- Yu, G.-C., Lv, J., He, H., Huang, W., & Han, Y. (2012). Hepatoprotective effects of corn peptides against carbon tetrachloride-induced liver injury in mice. Journal of Food Biochemistry, 36, 458–464. https://doi.org/10.1111/j.1745-4514.2011.00551.x
- Zhang, C., Alashi, A. M., Singh, N., Liu, K., Chelikani, P., & Aluko, R. E. (2018). Beef protein-derived peptides as bitter taste receptor T2R4 blockers. Journal of Agricultural and Food Chemistry, 66, 4902–4912.
- Zhang, Q., Tong, X., Qi, B., Wang, Z., Li, Y., Sui, X., & Jiang, L. (2018). Changes in antioxidant activity of Alcalase-hydrolyzed soybean hydrolysate under simulated gastrointestinal digestion and transepithelial transport. Journal of Functional Foods, 42, 298–305.
- Zhao, T., Xu, J., Zhao, H., Jiang, W., Guo, X., Zhao, M., … Su, G. (2017). Antioxidant and anti-acetylcholinesterase activities of anchovy (Coilia mystus) protein hydrolysates and their memory-improving effects on scopolamine-induced amnesia mice. International Journal of Food Science and Technology, 52, 504–510.
- Zheng, Z., Si, D., Ahmad, B., Li, Z., & Zhang, R. (2018). A novel antioxidative peptide derived from chicken blood corpuscle hydrolysate. Food Research International, 106, 410–419. https://doi.org/10.1016/j.foodres.2017.12.078
- Zhou, K., Canning, C., & Sun, S. (2013). Effects of rice protein hydrolysates prepared by microbial proteases and ultrafiltration on free radicals and meat lipid oxidation. LWT - Food Science and Technology, 50, 331–335. https://doi.org/10.1016/j.lwt.2012.05.002
- Zhou, Q.-W., Ding, H.-C., Li, D.-F., Zhang, Y.-P., Dai, Z.-Y., & Zho, T. (2016). Antioxidant activity of enzymatic hydrolysate derived from hairtail surimi wash water using an immobilized chymotrypsin–trypsin column reactor. Journal of Food Biochemistry, 40, 39–46. https://doi.org/10.1111/jfbc.12185
- Zou, T. B., He, T. P., Li, H. B., Tang, H. W., & Xia, E. Q. (2016). The Structure-activity relationship of the antioxidant peptides from natural proteins. Molecules, 21, 72. https://doi.org/10.3390/molecules21010072