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Preventive effect of Nile tilapia hydrolysate against oxidative damage of HepG2 cells and DNA mediated by H2O2 and AAPH

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Abstract

Antioxidant activities of protein hydrolysate prepared from Nile tilapia protein isolate using Alcalase (HA), Alcalase followed by papain (HAPa) and their Sephadex G-25 fractions (FHA and FHAPa) were investigated in both chemical and cellular based models. Amongst all samples, FHAPa showed the highest chemical antioxidant activities, however it had no metal chelation activity. Cellular antioxidant ability of HA, HAPa and their fractions against H2O2 and AAPH induced oxidative damage of HepG2 cell and DNA were tested. When cells were pretreated with all hydrolysates or fractions at different concentrations (0.5–2 mg/mL) in the absence and presence of 50 μM Trolox, cell viability was in the range of 91.10–111.40 %. However, no difference in cell viability was observed among samples having various concentrations (P > 0.05). Cell reactive oxygen species (ROS) generation as mediated by H2O2 and AAPH decreased with treatment of hydrolysates or their fractions, especially in combination with 50 μM Trolox. FHAPa effectively inhibited H2O2 and peroxyl radical induced DNA scission in a dose dependent manner. Therefore, Nile tilapia protein hydrolysates could serve as a functional food ingredient.

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References

  • Benjakul S, Morrissey MT (1997) Protein hydrolysates from Pacific whiting solid wastes. J Agric Food Chem 45(9):3423–3430

    Article  CAS  Google Scholar 

  • Benzie IF, Strain J (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239(1):70–76

    Article  CAS  Google Scholar 

  • Binsan W, Benjakul S, Visessanguan W, Roytrakul S, Tanaka M, Kishimura H (2008) Antioxidative activity of mungoong, an extract paste, from the cephalothorax of white shrimp (Litopenaeus vannamei). Food Chem 106(1):185–193

    Article  CAS  Google Scholar 

  • Chai HJ, Chan YL, Li TL, Shiau CY, Wu CJ (2013) Evaluation of lanternfish (Benthosema pterotum) hydrolysates as antioxidants against hydrogen peroxide induced oxidative injury. Food Res Int 54(1):1409–1418

    Article  CAS  Google Scholar 

  • Chandrasekara A, Shahidi F (2011) Inhibitory activities of soluble and bound millet seed phenolics on free radicals and reactive oxygen species. J Agric Food Chem 59(1):428–436

    Article  CAS  Google Scholar 

  • Chen HM, Muramoto K, Yamauchi F, Nokihara K (1996) Antioxidant activity of designed peptides based on the antioxidative peptide isolated from digests of a soybean protein. J Agric Food Chem 44(9):2619–2623

    Article  Google Scholar 

  • Choe E, Min DB (2005) Chemistry and reactions of reactive oxygen species in foods. J Food Sci 70(9):R142–R159

    Article  CAS  Google Scholar 

  • Elisia I, Kitts DD (2008) Anthocyanins inhibit peroxyl radical-induced apoptosis in Caco-2 cells. Mol Cell Biochem 312(1–2):139–145

    Article  CAS  Google Scholar 

  • García-Nebot MJ, Recio I, Hernández-Ledesma B (2014) Antioxidant activity and protective effects of peptide lunasin against oxidative stress in intestinal Caco-2 cells. Food Chem Toxicol 65:155–161

    Article  Google Scholar 

  • Guo H, Kouzuma Y, Yonekura M (2009) Structures and properties of antioxidative peptides derived from royal jelly protein. Food Chem 113(1):238–245

    Article  CAS  Google Scholar 

  • Halldorsdottir SM, Sveinsdottir H, Freysdottir J, Kristinsson HG (2014) Oxidative processes during enzymatic hydrolysis of cod protein and their influence on antioxidant and immunomodulating ability. Food Chem 142:201–209

    Article  CAS  Google Scholar 

  • Himaya S, Ryu B, Ngo DH, Kim SK (2012) Peptide Isolated from Japanese flounder skin gelatin protects against cellular oxidative damage. J Agric Food Chem 60(36):9112–9119

    Article  CAS  Google Scholar 

  • Je JY, Lee KH, Lee MH, Ahn CB (2009) Antioxidant and antihypertensive protein hydrolysates produced from tuna liver by enzymatic hydrolysis. Food Res Int 42(9):1266–1272

    Article  CAS  Google Scholar 

  • Je JY, Qian ZJ, Lee SH, Byun HG, Kim SK (2008) Purification and antioxidant properties of bigeye tuna (Thunnus obesus) dark muscle peptide on free radical-mediated oxidative systems. J Med Food 11(4):629–637

    Article  CAS  Google Scholar 

  • Kim GN, Kwon YI, Jang HD (2011) Protective mechanism of quercetin and rutin on 2,2′-azobis(2-amidinopropane)dihydrochloride or Cu2+-induced oxidative stress in HepG2 cells. Toxicol in Vitro 25(1):138–144

    Article  CAS  Google Scholar 

  • Kim SY, Je JY, Kim SK (2007) Purification and characterization of antioxidant peptide from hoki (Johnius belengerii) frame protein by gastrointestinal digestion. J Nutr Biochem 18(1):31–38

    Article  CAS  Google Scholar 

  • Kittiphattanabawon P, Benjakul S, Visessanguan W, Shahidi F (2012) Gelatin hydrolysate from blacktip shark skin prepared using papaya latex enzyme: antioxidant activity and its potential in model systems. Food Chem 135(3):1118–1126

    Article  CAS  Google Scholar 

  • Kittiphattanabawon P, Benjakul S, Visessanguan W, Shahidi F (2013) Inhibition of angiotensin converting enzyme, human LDL cholesterol and DNA oxidation by hydrolysates from blacktip shark gelatin. LWT Food Sci Technol 51(1):177–182

    Article  CAS  Google Scholar 

  • Klompong V, Benjakul S, Yachai M, Visessanguan W, Shahidi F, Hayes KD (2009) Amino acid composition and antioxidative peptides from protein hydrolysates of yellow stripe trevally (Selaroides leptolepis). J Food Sci 74(6):C126–C133

    Article  CAS  Google Scholar 

  • Lima CF, Fernandes-Ferreira M, Pereira-Wilson C (2006) Phenolic compounds protect HepG2 cells from oxidative damage: relevance of glutathione levels. Life Sci 79(21):2056–2068

    Article  CAS  Google Scholar 

  • Mendis E, Rajapakse N, Byun HG, Kim SK (2005) Investigation of jumbo squid (Dosidicus gigas) skin gelatin peptides for their in vitro antioxidant effects. Life Sci 77(17):2166–2178

    Article  CAS  Google Scholar 

  • Owuor ED, Kong ANT (2002) Antioxidants and oxidants regulated signal transduction pathways. Biochem Pharmacol 64(10):765–770

    Article  CAS  Google Scholar 

  • Poli G, Leonarduzzi G, Biasi F, Chiarpotto E (2004) Oxidative stress and cell signalling. Curr Med Chem 11(9):1163–1182

    Article  CAS  Google Scholar 

  • Qian ZJ, Jung WK, Kim SK (2008) Free radical scavenging activity of a novel antioxidative peptide purified from hydrolysate of bullfrog skin, Rana Catesbeiana Shaw. Bioresour Technol 99(6):1690–1698

    Article  CAS  Google Scholar 

  • Raghavan S, Kristinsson HG (2008) Antioxidative efficacy of alkali-treated tilapia protein hydrolysates: a comparative study of five enzymes. J Agric Food Chem 56(4):1434–1441

    Article  CAS  Google Scholar 

  • Ren J, Zhao M, Shi J, Wang J, Jiang Y, Cui C, Kakuda Y, Xue SJ (2008) Purification and identification of antioxidant peptides from grass carp muscle hydrolysates by consecutive chromatography and electrospray ionization-mass spectrometry. Food Chem 108(2):727–736

    Article  CAS  Google Scholar 

  • Robinson HW, Hogden CG (1940) The biuret reaction in the deter serum proteins. J Biol Chem 135(2):707–725

    CAS  Google Scholar 

  • Saiga A, Tanabe S, Nishimura T (2003) Antioxidant activity of peptides obtained from porcine myofibrillar proteins by protease treatment. J Agric Food Chem 51(12):3661–3667

    Article  CAS  Google Scholar 

  • Samaranayaka AG, Kitts DD, Li-Chan ECY (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 Agric Food Chem 58(3):1535–1542

    Article  CAS  Google Scholar 

  • Samaranayaka AG, Li-Chan EC (2011) Food-derived peptidic antioxidants: a review of their production, assessment, and potential applications. J Funct Foods 3(4):229–254

    Article  CAS  Google Scholar 

  • Steel RGD, Torrie JH (1980) Principles and procedures of statistics: a biometrical approach. McGraw-Hill, New York

    Google Scholar 

  • Surguladze N, Thompson KM, Beard JL, Connor JR, Fried MG (2004) Interactions and reactions of ferritin with DNA. J Biol Chem 279(15):14694–14702

    Article  CAS  Google Scholar 

  • Theodore AE, Raghavan S, Kristinsson HG (2008) Antioxidative activity of protein hydrolysates prepared from alkaline-aided channel catfish protein isolates. J Agric Food Chem 56(16):7459–7466

    Article  CAS  Google Scholar 

  • Wang B, Gong YD, Li ZR, Yu D, Chi CF, Ma JY (2014) Isolation and characterisation of five novel antioxidant peptides from ethanol-soluble proteins hydrolysate of spotless smoothhound (Mustelus griseus) muscle. J Funct Foods 6:176–185

    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 Food Chem 53(22):8768–8774

    Article  CAS  Google Scholar 

  • Wiriyaphan C, Chitsomboon B, Yongsawadigul J (2012) Antioxidant activity of protein hydrolysates derived from threadfin bream surimi byproducts. Food Chem 132(1):104–111

    Article  CAS  Google Scholar 

  • Yarnpakdee S, Benjakul S, Kristinsson H, Kishimura H (2014) Antioxidant and sensory properties of protein hydrolysate derived from Nile tilapia (Oreochromis niloticus) by one- and two-step hydrolysis. J Food Sci Technol. doi:10.1007/s13197-014-1394-7

    Google Scholar 

  • You L, Zhao M, Regenstein JM, Ren J (2011) In vitro antioxidant activity and in vivo anti-fatigue effect of loach (Misgurnus anguillicaudatus) peptides prepared by papain digestion. Food Chem 124(1):188–194

    Article  CAS  Google Scholar 

  • Zhang QX, Ling YF, Sun Z, Zhang L, Yu HX, Kamau SM, Lu RR (2012) Protective effect of whey protein hydrolysates against hydrogen peroxide-induced oxidative stress on PC12 cells. Biotechnol Lett 34(11):2001–2006

    Article  CAS  Google Scholar 

  • Zhang SB, Wang Z, Xu SY (2008) Antioxidant and antithrombotic activities of rapeseed peptides. J Am Oil Chem Soc 85(6):521–527

    Article  CAS  Google Scholar 

  • Zhu L, Chen J, Tang X, Xiong YL (2008) Reducing, radical scavenging, and chelation properties of in vitro digests of Alcalase-treated zein hydrolysate. J Agric Food Chem 56(8):2714–2721

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Thailand Research Fund under the Royal Golden Jubilee Ph.D. Programme to Suthasinee Yarnpakdee (PHD/0226/2552) and the Grant-in-Aid for dissertation from Graduate School, Prince of Songkla University, Thailand. Matis Ltd-Icelandic Food and Biotech R & D in Reykjavik and Matis-Biotechnology Centre in Saudarkrokur were also acknowledged for instrument support and their facilities. The TRF Distinguished Research Professor Grant was also acknowledged. 

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Authors and Affiliations

  1. Department of Food Technology, Faculty of Agro-Industry, Prince of Songkla University, Hat Yai, Songkhla, 90112, Thailand

    Suthasinee Yarnpakdee & Soottawat Benjakul

  2. Division of Biotechnology and Biomolecules, Matis - Icelandic Food and Biotechnology R & D, Vinlandsleid 12, 113, Reykjavik, Iceland

    Hordur G. Kristinsson

  3. Department of Food Science and Human Nutrition, University of Florida, Gainesville, FL, 32611, USA

    Hordur G. Kristinsson

  4. Division of Biotechnology and Biomolecules, Matis-Biotechnology Center, Haeyri 1, 550, Saudarkrokur, Iceland

    Hilma Eiðsdóttir Bakken

Authors
  1. Suthasinee Yarnpakdee
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  2. Soottawat Benjakul
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  3. Hordur G. Kristinsson
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  4. Hilma Eiðsdóttir Bakken
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Correspondence to Soottawat Benjakul.

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Yarnpakdee, S., Benjakul, S., Kristinsson, H.G. et al. Preventive effect of Nile tilapia hydrolysate against oxidative damage of HepG2 cells and DNA mediated by H2O2 and AAPH. J Food Sci Technol 52, 6194–6205 (2015). https://doi.org/10.1007/s13197-014-1672-4

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  • DOI: https://doi.org/10.1007/s13197-014-1672-4

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