Advertisement

Applied Biochemistry and Biotechnology

, Volume 172, Issue 6, pp 2877–2893 | Cite as

Fractionation of Protein Hydrolysates of Fish and Chicken Using Membrane Ultrafiltration: Investigation of Antioxidant Activity

  • Graciela Salete Centenaro
  • Myriam Salas-Mellado
  • Carla Pires
  • Irineu Batista
  • Maria L. Nunes
  • Carlos PrenticeEmail author
Article

Abstract

In this work, chicken and fish peptides were obtained using the proteolytic enzymes α-Chymotrypsin and Flavourzyme. The muscle was hydrolyzed for 4 h, and the resulting peptides were evaluated. Hydrolysates were produced from Argentine croaker (Umbrina canosai) with a degree of hydrolysis (DH) of 25.9 and 27.6 % and from chicken (Gallus domesticus) with DH of 17.8 and 20.6 % for Flavourzyme and α-Chymotrypsin, respectively. Membrane ultrafiltration was used to separate fish and chicken hydrolysates from Flavourzyme and α-Chymotrypsin based on molecular weight cutoff of >1,000, <1,000 and >500, and <500 Da, to produce fractions (F1,000, F1,000–500, and F500) with antioxidant activity. Fish hydrolysates produced with Flavourzyme (FHF) and α-Chymotrypsin showed 60.8 and 50.9 % of peptides with a molecular weight of <3 kDa in its composition, respectively. To chicken hydrolysates produced with Flavourzyme and α-Chymotrypsin (CHC) was observed 83 and 92.4 % of peptides with a molecular weight of <3 kDa. The fraction that showed, in general, higher antioxidant potential was F1,000 from FHF. When added 40 mg/mL of FHF and CHC, 93 and 80 % of lipid oxidation in ground beef homogenates was inhibited, respectively. The composition of amino acids indicated higher amino acids hydrophobic content and amino acids containing sulfuric residues for FHF, which showed antioxidant potential.

Keywords

Antioxidant activity Chicken Fish Hydrolysate Peptides Ultrafiltration membranes 

Notes

Acknowledgments

This work was supported by CAPES of Brazil through a scholarship granted to the first author by PhD Program in Brazil with the Foreign Internship-PDEE (Process BEX: 0076/10-4) and developed at the Fisheries and Marine Research Institute (IPMA, I. P./DMRM) in Lisbon, Portugal. The authors also thank support from the European Project Chill-On (FP 6-409 016333-2) and CNPq of Brazil (Grant 305055/2006-2).

References

  1. 1.
    Sarmadi, B. H., & Ismail, A. (2010). Antioxidative peptides from food proteins: a review. Peptides, 31, 1949–1956.CrossRefGoogle Scholar
  2. 2.
    Kim, E. K., Lee, S. J., Jeon, B. T., Moon, S. H., Kim, B., Park, T. K., Han, J. S., & Park, P. J. (2009). Purification and characterisation of antioxidative peptides from enzymatic hydrolysates of venison protein. Food Chemistry, 114, 1365–1370.CrossRefGoogle Scholar
  3. 3.
    Chan, K. M., & Decker, E. A. (1994). Endogenous skeletal muscle antioxidants. Critical Reviews in Food Science and Nutrition, 34, 403–426.CrossRefGoogle Scholar
  4. 4.
    Decker, E. A., Livisay, S. A., & Zhou, S. (2000). Mechanisms of endogenous skeletal muscle antioxidants: chemical and physical aspects. In E. A. Decker, C. Faustman, & C. J. Lopez-Bote (Eds.), Antioxidants in muscle foods (pp. 25–60). New York: Wiley.Google Scholar
  5. 5.
    Guiotto, A., Calderan, A., Ruzza, P., & Borin, G. (2005). Carnosine and carnosine-related antioxidants: a review. Current Medicinal Chemistry, 12, 2293–2315.CrossRefGoogle Scholar
  6. 6.
    Brown, C. E. (1981). Interactions among carnosine, anserine, ophidine and copper in biochemical adaptation. Journal of Theoretical Biology, 88, 245–256.CrossRefGoogle Scholar
  7. 7.
    Young, J. F., Therkildsen, M., Ekstrand, B., Che, B. N., Larsen, M. K., Oksbjerg, N., & Stagsted, J. (2013). Novel aspects of health promoting compounds in meat. Meat Science, 95, 904–911.CrossRefGoogle Scholar
  8. 8.
    Meisel, H., & Fitzgerald, R. J. (2003). Biofunctional peptides from milk proteins: mineral binding and cytomodulatory effects. Current Pharmaceutical Design, 9, 1289–1295.CrossRefGoogle Scholar
  9. 9.
    Sun, J., He, H., & Xie, B. J. (2004). Novel antioxidant peptides from fermented mushroom Ganoderma lucidum. Journal of Agricultural and Food Chemistry, 52, 6646–6652.CrossRefGoogle Scholar
  10. 10.
    Gauthier, S. F., Pouliot, Y., & Saint-Sauveur, D. (2006). Immunomodulatory peptides obtained by the enzymatic hydrolysis of whey proteins. International Dairy Journal, 16, 1315–1323.CrossRefGoogle Scholar
  11. 11.
    McCann, K. B., Shiell, B. J., Michalski, W. P., Lee, A., Wan, J., Roginski, H., & Coventry, M. J. (2006). Isolation and characterization of a novel antibacterial peptide from bovine αS1-casein. International Dairy Journal, 16, 316–323.CrossRefGoogle Scholar
  12. 12.
    Shimizu, M., Sawashita, N., Morimatsu, F., Ichikawa, J., Taguchi, Y., Ijiri, Y., et al. (2008). Antithrombotic papain-hydrolyzed peptides isolated from pork meat. Thrombosis Research, 123, 753–757.CrossRefGoogle Scholar
  13. 13.
    Zhong, F., Liu, J., Ma, J., & Shoemaker, C. F. (2007). Preparation of hypocholesterol peptides from soy protein and their hypocholesterolemic effect in mice. Food Research International, 40, 661–667.CrossRefGoogle Scholar
  14. 14.
    Jia, J., Maa, H., Zhao, W., Wang, Z., Tian, W., Luo, L., & He, R. (2010). The use of ultrasound for enzymatic preparation of ACE-inhibitory peptides from wheat germ protein. Food Chemistry, 119, 336–342.CrossRefGoogle Scholar
  15. 15.
    Mendis, E., Rajapakse, N., & Kim, S. K. (2005). Antioxidant properties of radical-scavenging peptide purified from enzymatically prepared fish skin gelatin hydrolysate. Journal of Agricultural and Food Chemistry, 53, 581–587.CrossRefGoogle Scholar
  16. 16.
    Wu, H. C., Pan, B. S., Chang, C. L., & Shiau, C. Y. (2005). Low-molecular-weight peptides as related to antioxidant properties of chicken essence. Journal of Food and Drug Analysis, 13, 176–183.Google Scholar
  17. 17.
    Je, J. Y., Lee, K. H., Lee, M. H., & Ahn, C. B. (2009). Antioxidant and antihypertensive protein hydrolysates produced from tuna liver by enzymatic hydrolysis. Food Research International, 42, 1266–1272.CrossRefGoogle Scholar
  18. 18.
    Aewsiri, T., Benjakul, S., Visessanguan, W., Wierenga, P. A., & Gruppen, H. (2010). Antioxidative activity and emulsifying properties of cuttlefish skin gelatin–tannic acid complex as influenced by types of interaction. Innovative Food Science and Emerging Technologies, 11, 712–720.CrossRefGoogle Scholar
  19. 19.
    Bougatef, A., Nedjar-Arroume, N., Manni, L., Ravallec, R., Barkia, A., Guillochon, D., & Nasri, M. (2010). Purification and identification of novel antioxidant peptides from enzymatic hydrolysates of sardinelle (Sardinella aurita) by-products proteins. Food Chemistry, 118, 559–565.CrossRefGoogle Scholar
  20. 20.
    Centenaro, G. S., Mellado, M. S., & Prentice-Hernández, C. (2011). Antioxidant activity of protein hydrolysates of fish and chicken bones. Advance Journal of Food Science and Technology, 3, 280–288.Google Scholar
  21. 21.
    Guérard, F., Sellos, D., & Le Gal, Y. (2005). Fish and shellfish upgrading, traceability. Advances in Biochemical Engineering/Biotechnology, 96, 127–163.CrossRefGoogle Scholar
  22. 22.
    Gulcin, I., Buyukokuroglu, M. E., Oktay, M., & Kufrevioglu, O. I. (2003). Antioxidant and analgesic activities of turpentine of Pinus nigra Arn. subsp. Pallsiana (Lamb). Holmboe. Journal of Ethnopharmacology, 86, 51–58.CrossRefGoogle Scholar
  23. 23.
    Ekanayake, P., Lee, Y. D., & Lee, J. (2004). Antioxidant activity of flesh and skin of Eptatretus burgeri (Hag Fish) and Enedrias nebulosus (White spotted Eel). Food Science and Technology International, 10, 0171–0177.CrossRefGoogle Scholar
  24. 24.
    Shih, F. F., & Daigle, K. W. (2003). Antioxidant properties of milled-rice co-products and their effects on lipid oxidation in ground beef. Journal of Food Science, 68, 2672–2675.CrossRefGoogle Scholar
  25. 25.
    Maillard, M.-N., Soum, M.-H., Boivin, P., & Berset, C. (1996). Antioxidant activity of barley and malt: relationship with phenolic content. LWT-Food Science and Technology, 29, 238–244.CrossRefGoogle Scholar
  26. 26.
    Park, P. J., Jung, W. K., Nam, K. S., Shahidi, F., & Kim, S. K. (2001). Purification and characterization of antioxidative peptides from protein hydrolysate of lecithin-free egg yolk. Journal of the American Oil Chemists Society, 78, 651–656.CrossRefGoogle Scholar
  27. 27.
    Qian, Z.-J., Jung, W.-K., & Kim, S.-K. (2008). Free radical scavenging activity of a novel antioxidative peptide purified from hydrolysate of bullfrog skin, Rana catesbeiana Shaw. Bioresource Technology, 99, 1690–1698.CrossRefGoogle Scholar
  28. 28.
    Foh, M. B. K., Qixing, J., Amadou, I., & Xia, W. S. (2010). Influence of ultrafiltration on antioxidant activity of tilapia (Oreochromis niloticus) protein hydrolysate. Advance Journal of Food Science and Technology, 2, 227–235.Google Scholar
  29. 29.
    Adler-Nissen, J. (1979). Determination of the degree of hydrolysis of food protein hydrolysates by trinitrobenzenesulfonic acid. Journal of Agricultural and Food Chemistry, 27, 1256–1262.CrossRefGoogle Scholar
  30. 30.
    Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680–685.CrossRefGoogle Scholar
  31. 31.
    Pires, C., Batista, I., Godinho, V., & Nunes, M. L. (2008). Functional and biochemical characterization of proteins remaining in solution after isoelectric precipitation. Journal of Aquatic Food Product Technology, 17, 60–72.CrossRefGoogle Scholar
  32. 32.
    Chung, S. K., Osawa, T., & Kawakishi, S. (1997). Hydroxyl radical scavenging effect of spices and scavengers from Brown Mustard (Brassica nigra). Bioscience, Biotechnology, and Biochemistry, 61, 118–124.CrossRefGoogle Scholar
  33. 33.
    Shimada, K., Fujikawa, K., Yahara, K., & Nakamura, T. (1992). Antioxidative properties of xanthan on the antioxidation of soybean oil in cyclodextrin emulsion. Journal of Agricultural Food and Chemistry, 40(6), 945–948.CrossRefGoogle Scholar
  34. 34.
    Re, R., Pellegrini, N., Proteggente, A., Panala, A., Yang, M., & Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radicals Biology and Medicine, 26, 1231–1237.CrossRefGoogle Scholar
  35. 35.
    Oyaizu, M. (1988). Antioxidative activities of browning products of glucosamine fractionated by organic solvent and thin-layer chromatography. Nippon Shokuhin Kogyo Gakkaishi, 35, 771–775.CrossRefGoogle Scholar
  36. 36.
    Sakanaka, S., Tachibana, Y., Ishihara, N., & Juneja, L. R. (2005). Antioxidant properties of casein calcium peptides and their effects on lipid oxidation in beef homogenates. Journal of Agricultural and Food Chemistry, 53, 464–468.CrossRefGoogle Scholar
  37. 37.
    Spackman, D. H., Stein, W. H., & Moore, S. (1958). Automatic recording apparatus for use in the chromatography of amino acids. Analytical Chemistry, 30, 1190–1206.CrossRefGoogle Scholar
  38. 38.
    Souissi, N., Bougatef, A., Triki-Ellouz, Y., & Nasri, M. (2007). Biochemical and functional properties of sardinella (Sardinella aurita) by-product hydrolysates. Food Technology and Biotechnology, 45, 187–194.Google Scholar
  39. 39.
    Kristinsson, H. G., & Rasco, B. A. (2000). Biochemical and functional properties of Atlantic salmon (Salmo salar) muscle hydrolyzed with various alkaline proteases. Journal of Agriculture and Food Chemistry, 48, 657–666.CrossRefGoogle Scholar
  40. 40.
    Guérard, F., Dufosse, L., De La Broise, D., & Binet, A. (2001). Enzymatic properties of proteins from yellowfin tuna (Thunnus albacares) wastes using Alcalase. Journal of Molecular Catalysis B: Enzymatic, 11, 1051–1059.CrossRefGoogle Scholar
  41. 41.
    Kurozawa, L. E., Park, K. J., & Hubinger, M. D. (2009). Influência das condições de processo na cinética de hidrólise enzimática de carne de frango. Ciência e Tecnologia de Alimentos, 29, 557–566.CrossRefGoogle Scholar
  42. 42.
    Rebeca, B. D., Pena-Vera, M. T., & Diaz-Castaneda, M. (1991). Production of fish protein hydrolysates with bacterial proteases, yield and nutritional value. Journal of Food Science, 56, 309–314.CrossRefGoogle Scholar
  43. 43.
    Klompong, V., Benjakul, S., Kantachote, D., & Shahidi, F. (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 Chemistry, 102, 1317–1327.CrossRefGoogle Scholar
  44. 44.
    Rossini, K., Noreña, C. P. Z., Cladera-Olivera, F., & Brandelli, A. (2009). Casein peptides with inhibitory activity on lipid oxidation in beef homogenates and mechanically deboned poultry meat. LWT-Food Science and Technology, 42, 862–867.CrossRefGoogle Scholar
  45. 45.
    Kristinsson, H. G., & Rasco, B. A. (2000). Fish protein hydrolysates: production, biochemical and functional properties. Critical Reviews in Food Science and Nutrition, 40(1), 43–81.CrossRefGoogle Scholar
  46. 46.
    Jeon, Y. J., Byun, H. G., & Kim, S. K. (1999). Improvement of functional properties of cod frame protein hydrolysates using ultrafiltration membranes. Process Biochemistry, 35, 471–478.CrossRefGoogle Scholar
  47. 47.
    Picot, L., Ravallec, R., Fouchereau-Péron, M., Vandanjon, L., Jaouen, P., Chaplain-Derouiniot, M., et al. (2010). Impact of ultrafiltration and nanofiltration of an industrial fish protein hydrolysate on its bioactive properties. Journal of the Science of Food and Agriculture, 90, 1819–1826.Google Scholar
  48. 48.
    Ren, J., Zhao, M., Shi, J., Wang, J., Jiang, Y., Cui, C., et al. (2008). Optimization of antioxidant peptide production from grass carp sarcoplasmic protein using response surface methodology. LWT-Food Science and Technology, 41, 1624–1632.CrossRefGoogle Scholar
  49. 49.
    Chabeaud, A., Dutournié, P., Guérard, F., Vandanjon, L., & Bourseau, P. (2009). Application of response surface methodology to optimise the antioxidant activity of a saithe (Pollachius virens) hydrolysate. Marine Biotechnology, 11, 445–455.CrossRefGoogle Scholar
  50. 50.
    Frankel, E. N., & Meyer, A. S. (2000). The problems of using one-dimensional methods to evaluate multifunctional food and biological antioxidants. Journal of the Science of Food and Agriculture, 80, 1925–1941.CrossRefGoogle Scholar
  51. 51.
    Je, J. Y., Qian, Z.-J., Byun, H.-G., & Kim, S.-K. (2007). Purification and characterization of an antioxidant peptide obtained from tuna backbone protein by enzymatic hydrolysis. Process Biochemistry, 42, 840–846.CrossRefGoogle Scholar
  52. 52.
    Miliauskas, G., Venskutonisa, P. R., & Van Beekb, T. A. (2004). Screening of radical scavenging activity of some medicinal and aromatic plant extracts. Food Chemistry, 85, 231–237.CrossRefGoogle Scholar
  53. 53.
    Phanturat, P., Benjakul, S., Visessanguan, W., & Roytrakul, S. (2010). Use of pyloric caeca extract from bigeye snapper (Priacanthus macracanthus) for the production of gelatin hydrolysate with antioxidative activity. LWT - Food Science and Technology, 43, 86–97.CrossRefGoogle Scholar
  54. 54.
    Kong, B. H., & Xiong, Y. L. (2006). Antioxidant activity of zein hydrolysates in a liposome system and the possible mode of action. Journal of Agricultural and Food Chemistry, 54, 6059–6068.CrossRefGoogle Scholar
  55. 55.
    Kitts, D. D. (2005). Antioxidant properties of caseinphosphopeptides. Trends in Food Science and Technology, 16, 549–554.CrossRefGoogle Scholar
  56. 56.
    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 Research International, 36, 949–957.CrossRefGoogle Scholar
  57. 57.
    Je, J. Y., Kim, S.-Y., & Kim, S.-K. (2005). Preparation and antioxidative activity of hoki frame protein hydrolysate using ultrafiltration membranes. European Food Research Technology, 221, 157–162.CrossRefGoogle Scholar
  58. 58.
    Pihlanto, A. (2006). Antioxidative peptides derived from milk proteins. International Dairy Journal, 16, 1306–1314.CrossRefGoogle Scholar
  59. 59.
    Lee, B. J., & Hendricks, D. G. (1997). Antioxidant effects of l-carnosine on liposomes and beef homogenates. Journal Food Science, 62, 931–934.CrossRefGoogle Scholar
  60. 60.
    Rajapakse, N., Mendis, E., Byun, H. G., & Kim, S. K. (2005). Purification and in vitro antioxidative effects of giant squid muscle peptides on free radical-mediated oxidative systems. Journal of Nutritional Biochemistry, 16, 562–569.CrossRefGoogle Scholar
  61. 61.
    Je, J. Y., Park, P. J., & Kim, S. K. (2005). Antioxidant activity of a peptide isolated from Alaska pollack (Theragra chalcogramma) frame protein hydrolysate. Food Research International, 38, 45–50.CrossRefGoogle Scholar
  62. 62.
    Dong, S., Zeng, M., Wang, D., Liu, Z., Zhao, Y., & Yang, H. (2008). Antioxidant and biochemical properties of protein hydrolysates prepared from Silver carp (Hypophthalmichthys molitrix). Food Chemistry, 107, 1485–1493.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Graciela Salete Centenaro
    • 1
  • Myriam Salas-Mellado
    • 1
  • Carla Pires
    • 2
  • Irineu Batista
    • 2
  • Maria L. Nunes
    • 2
  • Carlos Prentice
    • 1
    Email author
  1. 1.Laboratory of Food Technology, School of Chemistry and FoodFederal University of Rio Grande (FURG)Rio GrandeBrazil
  2. 2.Portuguese Institute of Sea and Atmosphere (IPMA, I. P./DMRM)LisbonPortugal

Personalised recommendations