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Bioactive peptides with radical scavenging and cancer cell cytotoxic activities derived from Flathead (Platycephalus fuscus) by-products

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Abstract

Peptide fractions extracted from Flathead by-products were evaluated for in vitro free radical scavenging and cancer cell cytotoxic activities. The degree of hydrolysis (DH), presence of protease and molecular weight (MW) influenced the 2,2-diphenyl-1-pycryl-hydrazyl (DPPH) and 2,2-azino-bis-3-ethylbenzothiazoline-6-sulphonic (ABTS) radical scavenging activities (RSA) of Flathead peptide fraction. Low MW peptides (<3 kDa), obtained from overnight incubation with added an exogenous protease, significantly inhibited free radicals and showed the highest RSA of 94.03 and 82.89 % against DPPH· and ABTS·+, respectively. The presence of bioactive peptides during H2O2 exposure increased viability of T4056 normal cells. Furthermore, peptide fractions <3 kDa inhibited the growth of HT-29 colon cancer cells up to 91.04 %, although the activity was found to be non-selective. Further purification revealed a novel peptide, Met-Gly-Pro-Pro-Gly-Leu-Ala-Gly-Ala-Pro-Gly-Glu-Ala-Gly-Arg, with RSA properties. These results indicated that peptides extracted from Flathead by-products have a potential to be used as natural antioxidants and/or chemo-protective agents.

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Abbreviations

ABTS:

2,2-Azino-bis-3-ethylbenzothiazoline-6-sulphonic

AFP:

Acid fungal protease

DH:

Degree of hydrolysis

DPPH:

2,2-Diphenyl-1-pycryl-hydrazyl

FPH:

Fish protein hydrolysate

MW:

Molecular weight

MWCO:

Molecular weight cut off

ON:

Incubated overnight without the addition of AFP

ONE:

Incubated overnight with the addition of AFP

ROS:

Reactive oxygen species

RSA:

Radical scavenging activity

UF:

Unfractionated

UH:

Unhydrolysed/Control

References

  1. Je JY, Park PJ, Kim SK (2005) Antioxidant activity of a peptide isolated from Alaska pollack (Theragra chalcogramma) frame protein hydrolysate. Food Res Int 38(1):45–50

    Article  CAS  Google Scholar 

  2. Perchellet J, Perchellet E, Gali H, Gao X (1995) Oxidant stress and multistage carcinogenesis. In: Mukhtar H (ed) Skin cancer: mechanisms and human relevance. CRC Press, Boca Raton, pp 145–180

    Google Scholar 

  3. Nelson KK, Ranganathan AC, Mansouri J, Rodriguez AM, Providence KM, Rutter JL, Pumiglia K, Bennett JA, Melendez JA (2003) Elevated sod2 activity augments matrix metalloproteinase expression: evidence for the involvement of endogenous hydrogen peroxide in regulating metastasis. Clin Cancer Res 9(1):424–432

    CAS  Google Scholar 

  4. Jiménez-Estrada M, Velázquez-Contreras C, Garibay-Escobar A, Sierras-Canchola D, Lapizco-Vázquez R, Ortiz-Sandoval C, Burgos-Hernández A, Robles-Zepeda RE (2013) In vitro antioxidant and antiproliferative activities of plants of the ethnopharmacopeia from northwest of Mexico. BMC Complement Altern Med 13(1):12

    Article  Google Scholar 

  5. Bennett L, Logan A, Terefe NS, Singh T, Warner R (2013) Measuring the oxidation potential in foods. In: Bartosz G (ed) Food oxidants and antioxidants. Chemical and functional properties of food components. CRC Press, Boca Raton, pp 47–78

    Google Scholar 

  6. Elias RJ, Kellerby SS, Decker EA (2008) Antioxidant activity of proteins and peptides. Crit Rev Food Sci Nutr 48(5):430–441

    Article  CAS  Google Scholar 

  7. Bougatef A, Hajji M, Balti R, Lassoued I, Triki-Ellouz Y, Nasri M (2009) Antioxidant and free radical-scavenging activities of smooth hound (Mustelus mustelus) muscle protein hydrolysates obtained by gastrointestinal proteases. Food Chem 114(4):1198–1205

    Article  CAS  Google Scholar 

  8. Nazeer RA, Srividhya TS (2011) Antioxidant peptides from the protein hydrolysates of conus betulinus. Int J Pept Res Ther 17(3):231–237

    Article  CAS  Google Scholar 

  9. Alemán A, Pérez-Santín E, Bordenave-Juchereau S, Arnaudin I, Gómez-Guillén MC, Montero P (2011) Squid gelatin hydrolysates with antihypertensive, anticancer and antioxidant activity. Food Res Int 44:1044–1051

    Article  Google Scholar 

  10. Bernardini RD, Harnedy P, Bolton D, Kerry J, O’Neill E, Mullen AM, Hayes M (2011) Antioxidant and antimicrobial peptidic hydrolysates from muscle protein sources and by-products. Food Chem 124:1296–1307

    Article  Google Scholar 

  11. Ryan JT, Ross RP, Bolton D, Fitzgerald GF, Stanton C (2011) Bioactive peptides from muscle sources: meat and fish. Nutrients 3:765–791

    Article  CAS  Google Scholar 

  12. Intarasirisawat R, Benjakul S, Visessanguan W, Wu J (2012) Antioxidative and functional properties of protein hydrolysate from defatted skipjack (Katsuwonous pelamis) roe. Food Chem 135(4):3039–3048

    Article  CAS  Google Scholar 

  13. Samaranayaka AGP, Li-Chan ECY (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 

  14. Barkia A, Bougatef ALI, Khaled HB, Nasri M (2010) Antioxidant activities of sardinelle heads and/or viscera protein hydrolysates prepared by enzymatic treatments. J Food Biochem 34:303–320

    Article  Google Scholar 

  15. Samaranayaka AGP, Li-Chan ECY (2008) Autolysis-assisted production of fish protein hydrolysates with antioxidant properties from Pacific hake (Merluccius productus). Food Chem 107(2):768–776

    Article  CAS  Google Scholar 

  16. Pihlanto A, Korhonen H (2003) Bioactive peptides and proteins. In: Taylor SL (ed) Advances in food and nutrition research, vol 47. Academic Press, San Diego, USA, pp 175–276

    Google Scholar 

  17. Muro C, Riera F, Fernández A (2013) Advancements in the fractionation of milk biopeptides by means of membrane processes. Bioact Food Pept Health Dis: 241

  18. Kailola PJ, Williams MJ, Stewart PC, Reichelt RE, McNee A, Grieve C (1993) Australian fisheries resources. Bureau of Resource Sciences, Canberra

    Google Scholar 

  19. Gagnon MM, Holdway DA (2002) EROD activity, serum SDH and PAH biliary metabolites in sand flathead (Platycephalus bassensis) collected in Port Phillip Bay, Australia. Mar Pollut Bull 44(3):230–237

    Article  CAS  Google Scholar 

  20. Nurdiani R, Dissanayake M, Street WE, Donkor ON, Singh TK, Vasiljevic T (2016) In vitro study of selected physiological and physicochemical properties of fish protein hydrolysates from 4 Australian fish species. Int Food Res J 23(5)

  21. Nurdiani R, Dissanayake M, Street WE, Donkor ON, Singh TK, Vasiljevic T (2015) Sustainable use of marine resources—turning waste into food ingredients. Int J Food Sci Technol 50(11):2329–2339

    Article  CAS  Google Scholar 

  22. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1):248–254

    Article  CAS  Google Scholar 

  23. Hoyle NT, Merritt JH (1994) Quality of fish-protein hyrdolysates from herring (Clupea harengus). J Food Sci 59(1):76–79

    Article  CAS  Google Scholar 

  24. AOAC (2005) Official methods of analysis. Association of Official Analytical Chemists, Washington DC

    Google Scholar 

  25. Sah BNP, Vasiljevic T, McKechnie S, Donkor ON (2015) Effect of refrigerated storage on probiotic viability and the production and stability of antimutagenic and antioxidant peptides in yogurt supplemented with pineapple peel. J Dairy Sci 98(9):5905–5916

    Article  CAS  Google Scholar 

  26. Ozgen M, Reese RN, Tulio AZ, Scheerens JC, Miller AR (2006) Modified 2,2-Azino-bis-3-ethylbenzothiazoline-6-sulfonic Acid (ABTS) method to measure antioxidant capacity of selected small fruits and comparison to ferric reducing antioxidant power (FRAP) and 2,2′-Diphenyl-1-picrylhydrazyl (DPPH) Methods. J Agric Food Chem 54(4):1151–1157

    Article  CAS  Google Scholar 

  27. Zhong S, Ma C, Lin YC, Luo Y (2011) Antioxidant properties of peptide fractions from silver carp (Hypophthalmichthys molitrix) processing by-product protein hydrolysates evaluated by electron spin resonance spectrometry. Food Chem 126(4):1636–1642

    Article  CAS  Google Scholar 

  28. Ahmed Z, Donkor O, Street WA, Vasiljevic T (2015) Calpains- and cathepsins-induced myofibrillar changes in post-mortem fish: impact on structural softening and release of bioactive peptides. Trends Food Sci Technol 45(1):130–146

    Article  CAS  Google Scholar 

  29. van der Ven C, Gruppen H, de Bont DBA, Voragen AGJ (2002) Optimisation of the angiotensin converting enzyme inhibition by whey protein hydrolysates using response surface methodology. Int Dairy J 12(10):813–820

    Article  Google Scholar 

  30. Yang J-I, Liang W-S, Chow C-J, Siebert KJ (2009) Process for the production of tilapia retorted skin gelatin hydrolysates with optimized antioxidative properties. Process Biochem 44(10):1152–1157

    Article  CAS  Google Scholar 

  31. Sabeena Farvin KH, Andersen LL, Nielsen HH, Jacobsen C, Jakobsen G, Johansson I, Jessen F (2014) Antioxidant activity of Cod (Gadus morhua) protein hydrolysates: in vitro assays and evaluation in 5% fish oil-in-water emulsion. Food Chem 149:326–334

    Article  CAS  Google Scholar 

  32. Ranathunga S, Rajapakse N, Kim S-K (2006) Purification and characterization of antioxidative peptide derived from muscle of conger eel (Conger myriaster). Eur Food Res Technol 222(3):310–315

    Article  CAS  Google Scholar 

  33. Wu H-C, Chen H-M, Shiau C-Y (2003) Free amino acids and peptides as related to antioxidant properties in protein hydrolysates of mackerel (Scomber austriasicus). Food Res Int 36(9–10):949–957

    Article  CAS  Google Scholar 

  34. You L, Zhao M, Regenstein JM, Ren J (2010) Purification and identification of antioxidative peptides from loach (Misgurnus anguillicaudatus) protein hydrolysate by consecutive chromatography and electrospray ionization-mass spectrometry. Food Res Int 43(4):1167–1173

    Article  CAS  Google Scholar 

  35. Fan J, He J, Zhuang Y, Sun L (2012) Purification and identification of antioxidant peptides from enzymatic hydrolysates of tilapia (Oreochromis niloticus) frame protein. Molecules 17(11):12836–12850

    Article  CAS  Google Scholar 

  36. Jia J, Zhou Y, Lu J, Chen A, Li Y, Zheng G (2010) Enzymatic hydrolysis of Alaska pollack (Theragra chalcogramma) skin and antioxidant activity of the resulting hydrolysate. J Sci Food Agric 90(4):635–640

    CAS  Google Scholar 

  37. Alemán A, Giménez B, Pérez-Santin E, Gómez-Guillén M, Montero P (2011) Contribution of Leu and Hyp residues to antioxidant and ACE-inhibitory activities of peptide sequences isolated from squid gelatin hydrolysate. Food Chem 125(2):334–341

    Article  Google Scholar 

  38. Cheung IWY, Cheung LKY, Tan NY, Li-Chan ECY (2012) The role of molecular size in antioxidant activity of peptide fractions from Pacific hake (Merluccius productus) hydrolysates. Food Chem 134(3):1297–1306

    Article  CAS  Google Scholar 

  39. Huang GR, Zhao J, Jiang JX (2011) Effect of defatting and enzyme type on antioxidative activity of shrimp processing byproducts hydrolysate. Food Sci Biotechnol 20(3):651–657

    Article  CAS  Google Scholar 

  40. Raghavan S, Kristinsson HG, Leeuwenburgh C (2008) Radical scavenging and reducing ability of tilapia (Oreochromis niloticus) protein hydrolysates. J Agric Food Chem 56(21):10359–10367

    Article  CAS  Google Scholar 

  41. 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 

  42. Kong B, Peng X, Xiong YL, Zhao X (2012) Protection of lung fibroblast MRC-5 cells against hydrogen peroxide-induced oxidative damage by 0.1–2.8 kDa antioxidative peptides isolated from whey protein hydrolysate. Food Chem 135(2):540–547

    Article  CAS  Google Scholar 

  43. Cheeseman K, Slater T (1993) An introduction to free radical biochemistry. Br Med Bull 49(3):481–493

    Article  CAS  Google Scholar 

  44. Liu L-X, Zhang W-H, Jiang H-C (2003) Current treatment for liver metastases from colorectal cancer. World J Gastroenterol 9(2):193–200

    Article  Google Scholar 

  45. Rodrigues EG, Dobroff AS, Taborda CP, Travassos LR (2009) Antifungal and antitumor models of bioactive protective peptides. An Acad Bras Ciênc 81:503–520

    Article  CAS  Google Scholar 

  46. 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. J Funct Foods 15:301–313

    Article  CAS  Google Scholar 

  47. Hoelder S, Clarke PA, Workman P (2012) Discovery of small molecule cancer drugs: successes, challenges and opportunities. Mol Oncol 6(2):155–176

    Article  CAS  Google Scholar 

  48. Batista I (2013) Biological activities of fish-protein hydrolysates. In: Kim SK (ed) Marine proteins and peptides. Wiley, West Sussex, UK, pp 111–138

    Chapter  Google Scholar 

  49. Ngo D-H, Ryu B, Kim S-K (2014) Active peptides from skate (Okamejei kenojei) skin gelatin diminish angiotensin-I converting enzyme activity and intracellular free radical-mediated oxidation. Food Chem 143:246–255

    Article  CAS  Google Scholar 

  50. Mendis E, Rajapakse N, Kim SK (2005) Antioxidant properties of a radical-scavenging peptide purified from enzymatically prepared fish skin gelatin hydrolysate. J Agric Food Chem 53(3):581–587

    Article  CAS  Google Scholar 

  51. Chi C-F, Wang B, Wang Y-M, Zhang B, Deng S-G (2015) Isolation and characterization of three antioxidant peptides from protein hydrolysate of bluefin leatherjacket (Navodon septentrionalis) heads. J Funct Foods 12:1–10

    Article  Google Scholar 

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Acknowledgments

We are gratefully acknowledged the Indonesian Department of Higher Education (DIKTI) for providing financial support and Barwon Foods, Geelong, for supplying the fish samples. The authors acknowledge with gratitude the assistance of Dr. David Steer for peptide identification.

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Authors and Affiliations

  1. Advanced Food Systems Research Unit, College of Health and Biomedicine, Victoria University, Werribee Campus, P.O. Box 14428, Melbourne, VIC, 8001, Australia

    Rahmi Nurdiani, Todor Vasiljevic & Osaana N. Donkor

  2. Faculty of Fisheries and Marine Sciences, University of Brawijaya, Jalan Veteran, Malang, East Java, 65145, Indonesia

    Rahmi Nurdiani

  3. College of Engineering and Science, Victoria University, Werribee campus, Melbourne, Australia

    Thomas Yeager

  4. Commonwealth Scientific and Industrial Research Organization-Agriculture and Food, 671 Sneydes Road, Werribee, VIC, 3030, Australia

    Tanoj K. Singh

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  1. Rahmi Nurdiani
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  2. Todor Vasiljevic
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  5. Osaana N. Donkor
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Correspondence to Osaana N. Donkor.

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Nurdiani, R., Vasiljevic, T., Yeager, T. et al. Bioactive peptides with radical scavenging and cancer cell cytotoxic activities derived from Flathead (Platycephalus fuscus) by-products. Eur Food Res Technol 243, 627–637 (2017). https://doi.org/10.1007/s00217-016-2776-z

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