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Purification and characterization of antioxidant peptides from yak (Bos grunniens) bone hydrolysates and evaluation of cellular antioxidant activity

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Abstract

In this study, papain and alcalase were used to generate antioxidant peptides from yak bone protein. The antioxidant activities of hydrolysates in vitro were evaluated by 2,2′-azinobios-(3-ethylbenzothiazoline-6-sulphonic acid) radical scavenging activity, total reducing power, ferrous ion chelating ability and hydroxyl radical scavenging activity. The hydrolysates generated by alcalase possessed the best antioxidant activity among unhydrolyzed protein and samples treated by papain, but the antioxidant activity decreased after simulated gastrointestinal digestion in vitro. The products of simulated gastrointestinal digestion were separated by ultrafiltration and high performance liquid chromatography, and the amino acid sequences of peptides were identified by mass spectrometry. The digestion sites within peptides were predicted by a bioinformatics strategy, and ten peptides were selected for synthesis. Among 10 synthetic peptides, Gly-Phe-Hyp-Gly-Ala-Asp-Gly-Val-Ala, Gly-Gly-Pro-Gln-Gly-Pro-Arg and Gly-Ser-Gln-Gly-Ser-Gln-Gly-Pro-Ala possessed strong antioxidant activities, among which Gly-Phe-Hyp-Gly-Ala-Asp-Gly-Val-Ala had a significant cytoprotective effect in Caco-2 cells under oxidative stress induced by H2O2, which reduced the formation of reactive oxygen species and malondialdehyde, and improved the activity of antioxidant enzymes in cells. These results showed that yak bone peptides exhibited strong antioxidant activity and have a potential value as a new type of natural antioxidant.

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References

  • Agrawal H, Joshi R, Gupta M (2016) Isolation, purification and characterization of antioxidative peptide of pearl millet (Pennisetum glaucum) protein hydrolysate. Food Chem 204:365–372

    Article  CAS  Google Scholar 

  • Chalamaiah M, Hemalatha R, Jyothirmayi T (2012) Fish protein hydrolysates: proximate composition, amino acid composition, antioxidant activities and applications: a review. Food Chem 135:3020–3038

    Article  CAS  Google Scholar 

  • Chalamaiah M, Yu W, Wu J (2018) Immunomodulatory and anticancer protein hydrolysates (peptides) from food proteins: a review. Food Chem 245:205–222

    Article  CAS  Google Scholar 

  • Chen S, Tsai ML, Huang J, Chen R (2009) In vitro antioxidant activities of low-molecular-weight polysaccharides with various functional groups. J Agr Food Chem 57:2699–2704

    Article  CAS  Google Scholar 

  • Chen G, Cheng L, Xu H, Song H, Lv Y, Yang C, Sun N (2011) Functions of different yak bone peptides. Int J Food Prop 14:1136–1141

    Article  CAS  Google Scholar 

  • Cheng Y, Wang Z, Xu S (2006) Antioxidant properties of wheat germ protein hydrolysates evaluated in vitro. J Cent South Univ T 13:160–165

    Article  CAS  Google Scholar 

  • Devi S, Kumar N, Kapila S, Mada SB, Reddi S, Vij R, Kapila R (2017) Buffalo casein derived peptide can alleviates H2O2 induced cellular damage and necrosis in fibroblast cells. Exp Toxicol Pathol 69:485–495

    Article  CAS  Google Scholar 

  • Feng Y, Ruan G, Jin F, Xu J, Wang F (2018) Purification, identification, and synthesis of five novel antioxidant peptides from Chinese chestnut (Castanea mollissima Blume) protein hydrolysates. LWT-Food Sci Technol 92:40–46

    Article  CAS  Google Scholar 

  • Gao S, Hong H, Zhang C, Wang K, Zhang B, Han QA, Luo Y (2019) Immunomodulatory effects of collagen hydrolysates from yak (Bos grunniens) bone on cyclophosphamide-induced immunosuppression in BALB/c mice. J Funct Foods 60:103420

    Article  CAS  Google Scholar 

  • Giménez B, Alemán A, Montero P, Gómez-Guillén MC (2009) Antioxidant and functional properties of gelatin hydrolysates obtained from skin of sole and squid. Food Chem 114:976–983

    Article  Google Scholar 

  • Girgih AT, He R, Hasan FM, Udenigwe CC, Gill TA, Aluko RE (2015) Evaluation of the in vitro antioxidant properties of a cod (Gadus morhua) protein hydrolysate and peptide fractions. Food Chem 173:652–659

    Article  CAS  Google Scholar 

  • Guo Y, Zhang T, Jiang B, Miao M, Mu W (2014) The effects of an antioxidative pentapeptide derived from chickpea protein hydrolysates on oxidative stress in Caco-2 and HT-29 cell lines. J Funct Foods 7:719–726

    Article  CAS  Google Scholar 

  • Hadgson EK, Fridovich I (1975) The interaction of bovine erythrocyte superoxide dismutase with hydrogen peroxide: inactivation of the inzyme. Biochemistry-US 14:5294–5299

    Article  Google Scholar 

  • Himaya SWA, Ryu B, Ngo DH, Kim SK (2012) Peptide isolated from Japanese flounder skin gelatin protects against cellular oxidative damage. J Agr Food Chem 60:9112–9119

    Article  CAS  Google Scholar 

  • Jeevithan E, Bao B, Bu Y, Zhou Y, Zhao Q, Wu W (2014) Type II collagen and gelatin from silvertip shark (Carcharhinus albimarginatus) cartilage: Isolation, purification, physicochemical and antioxidant properties. Mar Drugs 12:3852–3873

    Article  CAS  Google Scholar 

  • Kim SK, Kim YT, Byun HG, Nam KS, Joo DS, Shahidi F (2001) Isolation and characterization of antioxidative peptides from gelatin hydrolysate of Alaska pollack skin. J Agr Food Chem 49:1984–1989

    Article  CAS  Google Scholar 

  • Kumar NSS, Nazeer RA, Jaiganesh R (2012) Purification and identification of antioxidant peptides from the skin protein hydrolysate of two marine fishes, horse mackerel (Magalaspis cordyla) and croaker (Otolithes ruber). Amino Acids 42:1641–1649

    Article  Google Scholar 

  • Lassoued I, Mora L, Nasri R, Jridi M, Toldrá F, Aristoy MC, Nasri M (2015) Characterization and comparative assessment of antioxidant and ACE inhibitory activities of thornback ray gelatin hydrolysates. J Funct Foods 13:225–238

    Article  CAS  Google Scholar 

  • Li Y, Li B (2013) Characterization of structure–antioxidant activity relationship of peptides in free radical systems using QSAR models: Key sequence positions and their amino acid properties. J Theor Biol 318:29–43

    Article  CAS  Google Scholar 

  • Li F, Jia D, Yao K (2009a) Amino acid composition and functional properties of collagen polypeptide from yak (Bos grunniens) bone. LWT-Food Sci Technol 42:945–949

    Article  CAS  Google Scholar 

  • Li F, Jia D, Yao K (2009b) Amino acid composition and functional properties of collagen polypeptide from yak (Bos grunniens) bone. LWT-Food Sci Technol 42:945–949

    Article  CAS  Google Scholar 

  • Liang R, Zhang Z, Lin S (2017) Effects of pulsed electric field on intracellular antioxidant activity and antioxidant enzyme regulating capacities of pine nut (Pinus koraiensis) peptide QDHCH in HepG2 cells. Food Chem 237:793–802

    Article  CAS  Google Scholar 

  • Rajapakse N, Mendis E, Byun HG, Kim SK (2005a) Purification and in vitro antioxidative effects of giant squid muscle peptides on free radical-mediated oxidative systems. J Nutr Biochem 16:562–569

    Article  CAS  Google Scholar 

  • Rajapakse N, Mendis E, Jung WK, Je JY, Kim SK (2005b) Purification of a radical scavenging peptide from fermented mussel sauce and its antioxidant properties. Food Res Int 38:175–182

    Article  CAS  Google Scholar 

  • Saiga AI, Tanabe S, Nishimura T (2003) Antioxidant activity of peptides obtained from porcine myofibrillar proteins by protease treatment. J Agr Food Chem 51:3661–3667

    Article  CAS  Google Scholar 

  • Sakanaka S, Tachibana Y (2006) Active oxygen scavenging activity of egg-yolk protein hydrolysates and their effects on lipid oxidation in beef and tuna homogenates. Food Chem 95:243–249

    Article  CAS  Google Scholar 

  • Samaranayaka AG, Kitts DD, Li-Chan EC (2010) Antioxidative and angiotensin-I-converting enzyme inhibitory potential of a Pacific hake (Merluccius productus) fish protein hydrolysate subjected to simulated gastrointestinal digestion and Caco-2 cell permeation. J Agr Food Chem 58(3):1535–1542

    Article  CAS  Google Scholar 

  • Segura-Campos M, Chel-Guerrero L, Betancur-Ancona D, Hernandez-Escalante VM (2011) Bioavailability of bioactive peptides. Food Rev Int 27:213–226

    Article  CAS  Google Scholar 

  • Vilailak K, Soottawat B, Duangporn K, Fereidoon S (2007) Antioxidative activity and functional properties of protein hydrolysate of yellow Stripe trevally (Selaroides leptolepis) as influenced by the degree of hydrolysis and enzyme type. Food Chem 102:1317–1327

    Article  Google Scholar 

  • Wang L, Ding L, Yu Z, Zhang T, Ma S, Liu J (2016) Intracellular ROS scavenging and antioxidant enzyme regulating capacities of corn gluten meal-derived antioxidant peptides in HepG2 cells. Food Res Int 90:33–41

    Article  CAS  Google Scholar 

  • Wijeratne SS, Cuppett SL, Schlegel V (2005) Hydrogen peroxide induced oxidative stress damage and antioxidant enzyme response in Caco-2 human colon cells. J Agric and Food Chem 53:8768–8774

    Article  CAS  Google Scholar 

  • Wu R, Wu C, Liu D, Yang X, Huang J, Zhang J, Li H (2015) Overview of antioxidant peptides derived from marine resources: the sources, characteristic, purification, and evaluation methods. Appl Biochem Biotech 176:1815–1833

    Article  CAS  Google Scholar 

  • 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. Eur Food Res Technol 239:577–586

    Article  CAS  Google Scholar 

  • Young IS, Woodside JV (2001) Antioxidants in health and disease. J Clin Pathol 54:176–186

    Article  CAS  Google Scholar 

  • Zhang F, Qu J, Thakur K, Zhang J, Mocan A, Wei Z (2019) Purification and identification of an antioxidative peptide from peony (Paeonia suffruticosa Andr.) seed dreg. Food Chem 285:266–274

    Article  CAS  Google Scholar 

  • Zhao J, Xu Z, Chen A, You X, Zhao Y, He W, Yang S (2019) Identification of meat from yak and cattle using SNP markers with integrated allele-specific polymerase chain reaction–capillary electrophoresis method. Meat Sci 148:120–126

    Article  CAS  Google Scholar 

  • Zhuang Y, Sun L, Zhao X, Wang J, Hou H, Li B (2009) Antioxidant and melanogenesis-inhibitory activities of collagen peptide from jellyfish (Rhopilema esculentum). J Sci Food Agr 89:1722–1727

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key R&D Program of China (award number 2017YFD0400201).

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Correspondence to Yongkang Luo.

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Sun, X., Wang, K., Gao, S. et al. Purification and characterization of antioxidant peptides from yak (Bos grunniens) bone hydrolysates and evaluation of cellular antioxidant activity. J Food Sci Technol 58, 3106–3119 (2021). https://doi.org/10.1007/s13197-020-04814-7

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  • DOI: https://doi.org/10.1007/s13197-020-04814-7

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