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Antioxidant activity and protective effects of Saccharomyces cerevisiae peptide fractions against H2O2-induced oxidative stress in Caco-2 cells

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Abstract

Oxidative stress is one of the most causes of some severe diseases and the spoilage of foods. Protein hydrolysates containing antioxidant peptides are a suitable candidate to replace synthetic antioxidant. In the present study, the in vitro and cellular antioxidant properties of Saccharomyces cerevisiae protein hydrolysate and the peptide fractions have been reported. The peptide protective role was evaluated in H2O2-stimulated Caco-2 cells to consider cell viability, cellular lipid and protein oxidation, and the level of cellular antioxidant enzymes such as Catalase (CAT) and Glutathione-S-transferase (GST). The peptide fractions showed a significant ferric reducing antioxidant power (67.10–93.52 µm FeSO4/mg protein), and < 3 kDa peptide fraction with 59.5% inhibitory effect on the 7th day, exhibited the most inhibitory activity toward linoleic acid peroxidation. Ultrafiltered fractions ( < 3 kDa and 3–5 kDa) significantly (P ≤ 0.05) decreased the levels of malondialdehyde (MDA) and protein carbonyl and the production of CAT and GST enzymes as protective responses of cells under oxidative stress by H2O2. This study confirms the antioxidant activity of yeast protein hydrolysate and peptide fractions and their potential to reduce cellular oxidative stress and thus validates their potential use as a valuable ingredient of functional foods.

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References

  1. P. Pietta, Flavonoids as antioxidants. J. Nat. Prod. 63, 1035–1042 (2000)

    CAS  PubMed  Google Scholar 

  2. M.N. Diaz, B. Frei, J.A. Vita, J.R. Keaney, Antioxidants and atherosclerotic heart disease. N. Engl. J. Med. 337, 408–416 (1997)

    CAS  PubMed  Google Scholar 

  3. A.M. Giuffrè, C. Zappia, M. Capocasale, Physicochemical stability of blood orange juice during frozen storage. Int. J. Food Prop. 20, 1930–1943 (2017)

    Google Scholar 

  4. U. Szymanowska, B. Baraniak, A. Bogucka-Kocka, Antioxidant, anti-inflammatory, and postulated cytotoxic activity of phenolic and anthocyanin-rich fractions from Polana Raspberry (Rubus idaeus L.) fruit and juice-in vitro study. Molecules 23, E1812 (2018)

    PubMed  Google Scholar 

  5. A. Caridi, R. Sidari, A.M. Giuffre, T.M. Pellicano, V. Sicari, C. Zappia, M. Poinanaet, Test of four generations of Saccharomyces cerevisiae concerning their effect on antioxidant phenolic compounds in wine. Eur. Food Res. Technol. 243, 1287–1294 (2007)

    Google Scholar 

  6. C. Torres-Fuentes, M.D. MarContreras, Identification and characterization of antioxidant peptides from chickpea protein hydrolysates. Food Chem. 180, 194–202 (2015)

    CAS  PubMed  Google Scholar 

  7. A. DaValos, M. Miguel, B. Bartolome, R. Lopez-Fandino, Antioxidant activity of peptides derived from egg white proteins by enzymatic hydrolysis. J. Food Pro. 67, 1939–1944 (2004)

    CAS  Google Scholar 

  8. H.L. Jang, A.M. Liceaga, K.Y. Yoon, Purification, characterization and stability of an antioxidant peptide derived from sandfish (Arctoscopus japonicus) protein hydrolysates. J. Funct. Foods 20, 433–442 (2016)

    CAS  Google Scholar 

  9. I.D. Nwachukwu, R.E. Aluko, Structural and functional properties of food protein-derived antioxidant peptides. J. Food Biochem. 43, e12761 (2019)

    PubMed  Google Scholar 

  10. R.J. Elias, S.S. Kellerby, E.A. Decker, Antioxidant activity of proteins and peptides. Crit. Rev. Food Sci. Nutr. 48, 430–441 (2008)

    CAS  PubMed  Google Scholar 

  11. M. Mirzaei, S. Mirdamadi, M.R. Ehsani, M. Aminlari, E. Hosseini, Purification and identification of antioxidant and ACE-inhibitory peptide from Saccharomyces cerevisiae protein hydrolysate. J. Funct. Foods 19, 259–268 (2015)

    CAS  Google Scholar 

  12. M. Mirzaei, S. Mirdamadi, M.R. Ehsani, M. Aminlari, Production of antioxidant and ACE-inhibitory peptides from Kluyveromyces marxianus protein hydrolysates: purification and molecular docking. J. Food Drug Anal. 26, 696–705 (2017)

    PubMed  Google Scholar 

  13. J.M. Alcaide-Hidalgo, E. Pueyo, M.C. Polo, A.J. Martinez-Rodriguez, Bioactive peptides released from Saccharomyces cerevisiae under accelerated autolysis in a wine model system. J. Food Sci. 72, 276–279 (2007)

    Google Scholar 

  14. A. Moure, H. Domínguez, J. Parajó, Antioxidant properties of ultrafiltrationrecovered soy protein fractions from industrial effluents and their hydrolysates. Process Biochem. 41, 447–456 (2006)

    CAS  Google Scholar 

  15. Z. Qian, W. Jung, S. Kim, Free radical scavenging activity of a novel antioxidative peptide purified from hydrolysate of bullfrog skin Rana catesbeiana Shaw. Bioresour. Technol. 99, 1690–1698 (2008)

    CAS  PubMed  Google Scholar 

  16. C. Wu, H. Chen, C. Shiau, Free amino acids and peptides as related to antioxidant properties in protein hydrolysates of mackerel (Scomber austriasicus). Food Res. Int. 36, 949–957 (2003)

    CAS  Google Scholar 

  17. N. Rajapakse, E. Mendis, W.K. Jung, J.Y. Je, S.K. Kim, Purification of a radical scavenging peptide from fermented mussel sauce and its antioxidant properties. Food Res. Int. 38, 175–182 (2005)

    CAS  Google Scholar 

  18. Y. Shi, J.K. Nolan, B. Jiang, R. Tsao, Y. Mine, Peptides derived from eggshell membrane improve antioxidant enzyme activity and glutathione synthesis against oxidative damage in Caco-2 cells. J. Funct. Foods 11, 571–580 (2014)

    CAS  Google Scholar 

  19. M. Homayouni-Tabrizi, A. Asoodeh, M. Soltani, Cytotoxic and antioxidant capacity of camel milk peptides: effects of isolated peptide on superoxide dismutase and catalase gene expression. J. Food Drug Anal. 25, 567–575 (2017)

    CAS  PubMed  Google Scholar 

  20. H. Yin, X. Pan, Z. Song, S. Wang, L. Yang, G. Sun, Protective effect of wheat peptides against indomethacin-induced oxidative stress in IEC-6 cells. Nutrients 6, 564–574 (2014)

    PubMed  PubMed Central  Google Scholar 

  21. B. Ryu, S.W. Himaya, Z.J. Qian, S.H. Lee, S.K. Kim, Prevention of hydrogen peroxide-induced oxidative stress in HDF cells by peptides derived from seaweed pipefish, Syngnathus schlegeli. Peptides 32, 639–647 (2011)

    CAS  PubMed  Google Scholar 

  22. C. Wiriyaphan, H. Xiao, E.A. Decker, J. Yongsawatdigul, Chemical and cellular antioxidative properties of threadfin bream (Nemipterus spp.) surimi byproduct hydrolysates fractionated by ultrafiltration. Food Chem. 15, 7–15 (2015)

    Google Scholar 

  23. A.L. Rao, G.G. Sankar, Caco-2 cells: an overview. Asian J. Pharm. Res. Health Care 1, 260–275 (2009)

    Google Scholar 

  24. I.F.F. Benzie, J.J. Strain, The ferric reducing ability of plasma (FRAP) as a measure of ‘‘antioxidant power’’: the FRAP assay. Anal. Biochem. 239, 70–76 (1996)

    CAS  PubMed  Google Scholar 

  25. T. Osawa, M. Namiki, A novel yype of antioxidant isolated from leaf wax of leaves. Agric. Biol. Chem. 45, 735–739 (1981)

    CAS  Google Scholar 

  26. H. Mitsuda, K. Yasumoto, K. Iwami, Antioxidative action of indole compounds during the autoxidation of Linoleic acid. Eiyo To Shokuryo 19, 210–214 (1966)

    CAS  Google Scholar 

  27. T. Mosmann, Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55–63 (1983)

    CAS  PubMed  Google Scholar 

  28. G. Colombo, M. Clerici, M.E. Garavaglia, D. Giustarini, R. Rossi, A. Milzani, I. Dalle-Donne, A step-by-step protocol for assaying protein carbonylation in biological samples. J. Chromatogr. B 15, 178–190 (2015)

    Google Scholar 

  29. H. Aebi, Catalase in vitro. Methods Enzymol. 105, 121–126 (1984)

    CAS  PubMed  Google Scholar 

  30. W.H. Habig, M.J. Pabst, W.B. Jakoby, Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249, 7130–7139 (1974)

    CAS  PubMed  Google Scholar 

  31. H.M.M. Hassan, Antioxidant and immunostimulating activities of yeast (Saccharomyces cerevisiae) autolysates. World Appl. Sci. J. 15, 1110–1119 (2011)

    CAS  Google Scholar 

  32. E.Y. Jung, H.S. Lee, J.W. Choi, K.S. Ra, M.R. Kim, H.J. Suh, Glucose tolerance and antioxidant activity of spent brewer's yeast hydrolysate with a high content of Cyclo-His-Pro (CHP). J. Food Sci. 76, 272–278 (2011)

    Google Scholar 

  33. R. Yang, X. Li, S. Lin, Z. Zhang, F. Chen, 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 Chem. 219, 311–320 (2017)

    CAS  PubMed  Google Scholar 

  34. D. Huang, B. Ou, R.L. Prior, The chemistry behind antioxidant capacity assays. J. Agric. Food Chem. 53, 1841–1856 (2005)

    CAS  PubMed  Google Scholar 

  35. A.G.P. Samaranayaka, E.C.Y. Li-Chan, Food-derived peptidic antioxidants: a review of their production, assessment, and potential applications. J. Funct. Foods 3, 229–254 (2011)

    CAS  Google Scholar 

  36. A.T. Girgih, C.C. Udenigwe, R.E. Aluko, In vitro antioxidant properties of Hemp seed (Cannabis sativa L.) protein hydrolysate fractions. J. Am. Oil Chem. Soc. 88, 381–389 (2011)

    CAS  Google Scholar 

  37. A. Bougatef, N. Nedjar-Arroume, L. Manni, R. Ravallec, A. Barkia, D. Guillochon, M. Nasri, Purification and identification of novel antioxidant peptides from enzymatic hydrolysates of sardinelle (Sardinella aurita) by-products proteins. Food Chem. 118, 559–565 (2010)

    CAS  Google Scholar 

  38. J.-Y. Je, P.-J. Park, S.-K. Kim, Antioxidant activity of a peptide isolated from Alaska pollack (Theragra chalcogramma) frame protein hydrolysate. Food Res. Int. 38, 45–50 (2005)

    CAS  Google Scholar 

  39. H.-M. Chen, K. Muramoto, F. Yamauchi, K. Nokihara, Antioxidant activity of designed peptides based on the antioxidative peptide isolated from digests of a soybean protein. J. Agric. Food Chem. 44, 2619–2623 (1996)

    Google Scholar 

  40. Q. Sun, H. Shen, Y. Luo, Antioxidant activity of hydrolysates and peptide fractions derived from porcine hemoglobin. J. Food Sci. Technol. 48, 53–60 (2011)

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  42. G. Longjian, Z. Mouming, L. Wenzhi, Y. Lijun, W. Jufang, W. Haiyan, R. Jiaoyan, Chemical and cellular antioxidant activity of two novel peptides designed based on glutathione structure. Food Chem. Toxicol. 50, 4085–4091 (2012)

    Google Scholar 

  43. D. Janero, Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic. Biol. Med. 9, 515–540 (1990)

    CAS  PubMed  Google Scholar 

  44. D. Weber, M.J. Davies, T. Grune, Determination of protein carbonyls in plasma, cell extracts, tissue homogenates, isolated proteins: Focus on sample preparation and derivatization conditions. Redox Biol. 5, 367–380 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  45. B. Kong, X. Peng, Y.L. Xiong, X. Zhao, Protection of lung fibroblast MRC-5 cells against hydrogen peroxide-induced oxidative damage by 01–28kDa antioxidative peptides isolated from whey protein hydrolysate. Food Chem. 135, 540–547 (2012)

    CAS  PubMed  Google Scholar 

  46. X.-H. Zhao, Y. Fu, N. Yue, In vitro cytoprotection of modified casein hydrolysates by plastein reaction on rat hepatocyte cells. CyTA J. Food 12, 40–47 (2014)

    CAS  Google Scholar 

  47. K. Sowmya, M.L. Bhat, R.K. Bajaj, S. Kapila, R. Kapila, Buffalo milk casein derived decapeptide (YQEPVLGPVR) having bifunctional anti-inflammatory and antioxidative features under cellular milieu. Int. J. Peptide Res. Ther. 25, 623–633 (2018)

    Google Scholar 

  48. A. Dua, N. Kaur, P. Gupta, A. Mittall, S.K. Gupta, Oxidative stress induced cell damage and antioxidant enzyme response in human lymphocytes. Int. J. Pharm. Biol. Arch. 8, 33–39 (2017)

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  50. N. Polidoros Alexios, G. Scandalios John, Role of hydrogen peroxide and different classes of antioxidants in the regulation of catalase and glutathione S-transferase gene expression in maize (Zea mays L). Physiologia. Plantarum 106, 112–120 (2002).

    CAS  Google Scholar 

  51. S. Katayama, S. Ishikawa, M.Z. Fan, Y. Mine, Oligophosphopeptides derived from egg yolk phosvitin up-regulate gamma-glutamylcysteine synthetase and antioxidant enzymes against oxidative stress in Caco-2 cells. J. Agric. Food Chem. 55, 2829–2835 (2007)

    CAS  PubMed  Google Scholar 

  52. E. Birben, U.M. Sahiner, C. Sackesen, S. Erzurum, O. Kalayci, Oxidative stress and antioxidant defense. WAO J. 5, 9–19 (2012)

    CAS  Google Scholar 

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Acknowledgements

This work has been supported by Iran National Science Foundation (INSF) (Grant Number: 95824648). We gratefully acknowledge the Persian Type Culture Collection (PTCC) of the Iranian Research Organization for Science and Technology (IROST) for supplying the strain of yeast used in this study. The authors wish to thank Sanaz Jafari for her help on this project.

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Correspondence to Mahta Mirzaei or Saeed Mirdamadi.

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Mirzaei, M., Mirdamadi, S. & Safavi, M. Antioxidant activity and protective effects of Saccharomyces cerevisiae peptide fractions against H2O2-induced oxidative stress in Caco-2 cells. Food Measure 13, 2654–2662 (2019). https://doi.org/10.1007/s11694-019-00186-5

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