Advertisement

Antiproliferative and antioxidative activities of cuttlefish (Sepia pharaonis) protein hydrolysates as affected by degree of hydrolysis

  • Ali Hamzeh
  • Masoud RezaeiEmail author
  • Saber Khodabandeh
  • Ali Motamedzadegan
  • Mehrdad Noruzinia
Original Paper

Abstract

Bioactivities (including antioxidative and antiproliferative properties) of cuttlefish mantle protein hydrolysates (CPH) with the degree of hydrolysis (DH) of 20.9, 25.5, 30.6, 35.3 and 40.6% (shortened as 20, 25, 30, 35 and 40%, respectively) prepared using alcalase were evaluated. The results indicated that the CPH with 20, 30 and 40% DH showed the greatest activity against DPPH radical scavenging [5.2 µmol TE (torolox equivalent)/g sample], reducing power (0.4 absorbance at 700 nm) and total antioxidant capacity (0.6 mg ascorbic acid equivalent/g sample), which were 2.5, 6.5 and 13.8 times higher than the cuttlefish mantle protein isolate (CPI), respectively. The CPH with the DH of 20% had the highest effect against MDA-231 and T47D cancer cell lines with growth inhibition of 78.2 and 66.2%, which were 6.5 and 6 times higher activities compared to the CPI, respectively. The amino acid profile of CPH indicated that glutamine (15.7%) and asparagine (10.9%) were predominant.

Keywords

Antioxidant Antiproliferate Protein hydrolysate Cuttlefish Sepia pharaonis 

Notes

Acknowledgements

The authors would like to thank Tarbiat Modares University for the financial support and Prof. Joe M. Regenstein for the editing.

References

  1. 1.
    S. Umayaparvathi, S. Meenakshi, V. Vimalraj, M. Arumugam, G. Sivagami, T. Balasubramanian, Antioxidant activity and anticancer effect of bioactive peptide from enzymatic hydrolysate of oyster (Saccostrea cucullata). Biomed. Prev. Nutr. 4, 343–353 (2014)CrossRefGoogle Scholar
  2. 2.
    G.M. Suarez-Jimenez, A. Burgos-Hernandez, J.M. Ezquerra-Brauer, Bioactive peptides and depsipeptides with anticancer potential: sources from marine animals. Mar. Drugs 10, 963–986 (2012)CrossRefGoogle Scholar
  3. 3.
    N.P. Möller, K.E. Scholz-Ahrens, N. Roos, J. Schrezenmeir, Bioactive peptides and proteins from foods: indication for health effects. Eur. J. Nutr. 47, 171–182 (2008)CrossRefGoogle Scholar
  4. 4.
    R. Slizyte, K. Rommi, R. Mozuraityte, P. Eck, K. Five, T. Rustad, Bioactivities of fish protein hydrolysates from defatted salmon backbones. Biotechnol. Rep. 11, 99–109 (2016)CrossRefGoogle Scholar
  5. 5.
    O. Villamil, H. Váquiro, J.F. Solanilla, Fish viscera protein hydrolysates: production, potential applications and functional and bioactive properties. Food Chem. 224, 160–171 (2017)CrossRefGoogle Scholar
  6. 6.
    A. Alemán, E. Pérez-santín, S. Bordenave-juchereau, I. Arnaudin, M.C. Gómez-guillén, P. Montero, Squid gelatin hydrolysates with antihypertensive, anticancer and antioxidant activity. Food Res. Int. 44, 1044–1051 (2011)CrossRefGoogle Scholar
  7. 7.
    S.Y. Naqash, R.A. Nazeer, Optimization of enzymatic hydrolysis conditions for the production of antioxidant peptides from muscles of Nemipterus japonicus and Exocoetus volitans using response surface methodology. Amino Acids 43, 337–345 (2012)CrossRefGoogle Scholar
  8. 8.
    S. Benjakul, S. Yarnpakdee, T. Senphan, S.M. Halldorsdottir, H.G. Kristinsson, in Fish Protein Hydrolysates: Production, Bioactivities, and Applications in Antioxidants and Functional Components in Aquatic Foods, ed. by H.G. By, Kristinsson eds. (Wiley, Oxford, 2014), pp. 237–281Google Scholar
  9. 9.
    L. Picot, S. Bordenave, S. Didelot, I. Fruitier-Arnaudin, F. Sannier, G. Thorkelsson, J.P. Bergé, F. Guérard, A. Chabeaud, J.M. Piot, Antiproliferative activity of fish protein hydrolysates on human breast cancer cell lines. Process Biochem. 41, 1217–1222 (2006)CrossRefGoogle Scholar
  10. 10.
    K.C. Hsu, C.Y. Eunice, L. Chan, C.L. Jao, Antiproliferative activity of peptides prepared from enzymatic hydrolysates of tuna dark muscle on human breast cancer cell line MCF-7. Food Chem. 126, 617–622 (2011)CrossRefGoogle Scholar
  11. 11.
    G.M. Suárez-jiménez, R.M. Robles-sánches, G. Yépiz-plascencia, In vitro antioxidant, antimutagenic and antiproliferative activities of collagen hydrolysates of jumbo squid (Dosidicus gigas) byproducts. Food Sci. Technol. 35(3), 421–427 (2015)CrossRefGoogle Scholar
  12. 12.
    J. Je, P. Park, S. Kim, Antioxidant activity of a peptide isolated from Alaska pollack (Theragra chalcogramma) frame protein hydrolysate. Food Res. Int. 38, 45–50 (2005)CrossRefGoogle Scholar
  13. 13.
    K. Elavarasan, N. Kumar, B.A. Shamasundar, Antioxidant and functional properties of fish protein hydrolysates from fresh water carp (Catla catla) as influenced by the nature of enzyme. J. Food Process. Preserv. 38, 1207–1214 (2014)CrossRefGoogle Scholar
  14. 14.
    M. Ovissipour, B. Rasco, G. Shiroodi, M. Modanlow, M. Nemati, Antioxidant activity of protein hydrolysates from whole anchovy sprat (Clupeonella engrauliformis) prepared using endogenous enzymes and commercial proteases. J. Sci. Food Agric. 93, 1718–1726 (2012)CrossRefGoogle Scholar
  15. 15.
    P.J. García-moreno, I. Batista, C. Pires, M.N. Bandarra, F.J. Espejo-carpio, A. Guadix, E.M. Guadix, Antioxidant activity of protein hydrolysates obtained from discarded Mediterranean fish species. Food Res. Int. 65, 469–476 (2014)CrossRefGoogle Scholar
  16. 16.
    N. Ktari, N. Fakhfakh, R. Balti, H.B. Khaled, A. Bougatef, M. Nasri, Effect of degree of hydrolysis and protease type on the antioxidant activity of protein hydrolysates from cuttlefish (Sepia officinalis) by-products. Process Biochem. 22, 436–448 (2013)Google Scholar
  17. 17.
    E. Soufi-Kechao, M. Derouiniot-Chaplin, R.B. Amar, P. Jaouen, J.P. Berge, Recovery of valuable marine compounds from cuttlefish by-product hydrolysates: combination of enzyme bioreactor and membrane technologies. C. R. Chim. 20, 975–985 (2017)CrossRefGoogle Scholar
  18. 18.
    N.T. Hoyle, J.H. Merritt, Quality of fish protein hydrolysate from herring (Clupea harengus). J. Food Sci. 59, 76–79 (1994)CrossRefGoogle Scholar
  19. 19.
    AOAC. Official Method of Analysis of AOAC International. 18th edn., (Methods 934.01, 920.153, 954.01, and 991.36. (Association of Official Analytical Chemists, Gaithersburg, 2005)Google Scholar
  20. 20.
    F.R. Antoine, C.I. Wei, R.C. Littell, M.R. Marshall, HPLC method for analysis of free amino acids in fish using o-phthaldialdehyde pre-column derivatization. Agric. Food Chem. 47, 5100–5107 (1999)CrossRefGoogle Scholar
  21. 21.
    E. Sotoudeh, J. Amiri Moghaddam, G. Shahhosseini, M.S. Aramli, Effect of dietary gamma-irradiated and fermented soybean meal on the growth performance, body composition, and digestive enzymes activity of Caspian brown trout, Salmo trutta caspius, juvenile. J. Word Aquacult. Soc. 47, 830–842 (2016)CrossRefGoogle Scholar
  22. 22.
    W. Binsan, S. Benjakul, W. Visessanguan, S. Roytrakul, N. Faithong, M. Tanaka, H. Kishimura, Composition, antioxidative and oxidative stability of mungoong, a shrimp extract paste, from the cephalothorax of white shrimp. J. Food Lipids 15, 97–118 (2008)CrossRefGoogle Scholar
  23. 23.
    M. Oyaizu, Studies on products of browning reactions: antioxidative activities of products of browning reaction prepared from glucosamine. Jpn. J. Nutr. 44, 307–315 (1986)CrossRefGoogle Scholar
  24. 24.
    P. Prieto, M. Pineda, M. Aguilar, Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal. Biochem. 269, 337–341 (1999)CrossRefGoogle Scholar
  25. 25.
    A. Hamzeh, M. Moslemi, M. Karaminasab, M.A. Khanlar, R. Faizbakhsh, M. Batebi Navai, R. Tahergorabi, Amino acid composition of roe from wild and farmed beluga sturgeon (Huso huso). J. Agric. Sci. Technol. 17, 357–364 (2015)Google Scholar
  26. 26.
    R. Balti, A. Bougatef, N.E. Ali, D. Zekri, A. Barkia, M. Nasri, Influence of degree of hydrolysis on functional properties and angiotensin I-converting enzyme-inhibitory activity of protein hydrolysates from cuttlefish (Sepia officinalis) by-products. J. Sci. Food Agric. 90, 2006–2014 (2010)Google Scholar
  27. 27.
    M. Chalamaiah, B. Dinesh kumar, R. Hemalatha, T. Jyothirmayi, Fish protein hydrolysates: Proximate composition, amino acid composition, antioxidant activities and applications: a review. Food Chem. 135, 3020–3038 (2012)CrossRefGoogle Scholar
  28. 28.
    S.N. Jhaveri, P.A. Karakoltsidis, J. Montecalvo, S.M. Constantinides, Chemical composition and protein quality of some Southern New England marine species. J. Food Sci. 49, 110–113 (1984)CrossRefGoogle Scholar
  29. 29.
    A. Abedian-Kenari, J.M. Regenstein, S.V. Hosseini, M. Rezaei, R. Tahergorabi, R.M. Nazari, M. Moghaddasi, S.A. Kaboli, Amino acid and fatty acid composition of cultured Beluga (Huso huso) of different ages. J. Aquat. Food Prod. Technol. 18, 245–265 (2009)CrossRefGoogle Scholar
  30. 30.
    Y. Cheng, Y.L. Xiong, J. Chen, Antioxidant and emulsifying properties of potato protein hydrolysate in soybean oil-in-water emulsions. Food Chem. 120, 101–108 (2010)CrossRefGoogle Scholar
  31. 31.
    R. Intarasirisawat, S. Benjakul, W. Visessanguan, J. Wu, Antioxidative and functional properties of protein hydrolysate from defatted skipjack (Katsuwonous pelamis) roe. Food Chem. 135, 3039–3048 (2012)CrossRefGoogle Scholar
  32. 32.
    H. Zhuang, N. Tang, S.T. Dong, B. Sun, J.B. Liu, Optimisation of antioxidant peptide preparation from corn gluten meal. J. Sci. Food Agric. 93, 3264–3270 (2013)CrossRefGoogle Scholar
  33. 33.
    A. Hamzeh, S. Benjakul, T. Senphan, Comparative study on antioxidant activity of hydrolysates from splendid squid (Loligo formosana) gelatin and protein isolate prepared using protease from hepatopancreas of Pacific white shrimp (Litopenaeus vannamei). J. Food Sci. Technol. 53, 3615–3623 (2016)CrossRefGoogle Scholar
  34. 34.
    V. Klompong, S. Benjakul, D. Kantachote, F. Shahidi, 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 (2007)CrossRefGoogle Scholar
  35. 35.
    H.C. Wu, H.M. Chen, C.Y. 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)CrossRefGoogle Scholar
  36. 36.
    L. You, M. Zhao, C. Cui, H. Zhao, B. Yang, Effect of degree of hydrolysis on the antioxidant activity of loach (Misgurnus anguillicaudatus) protein hydrolysates. Innov. Food Sci. Emerg. 10, 235–240 (2009)CrossRefGoogle Scholar
  37. 37.
    A. Bougatef, M. Hajji, R. Balti, I. Lassoued, Y. Triki-Ellouz, M. Nasri, Antioxidant and free radical-scavenging activities of smooth hound (Mustelus mustelus) muscle protein hydrolysates obtained by gastrointestinal proteases. Food Chem. 114, 1198–1205 (2009)CrossRefGoogle Scholar
  38. 38.
    Q. Sun, H. Shen, Y. Luo, Antioxidant activity of hydrolysates and peptide fractions derived from porcine hemoglobin. J. Food Sci. Technol. 48(1), 53–60 (2011)CrossRefGoogle Scholar
  39. 39.
    Y.W. Li, B. Li, 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 (2013)CrossRefGoogle Scholar
  40. 40.
    C.F. Chi, F.Y. Hu, B. Wang, T. Li, G.F. Ding, Antioxidant and anticancer peptides from the protein hydrolysate of blood clam (Tegillarca granosa) muscle. J. Funct. Foods 15, 301–313 (2015)CrossRefGoogle Scholar
  41. 41.
    C. Chen, Y.J. Chi, M.Y. Zhao, W. Xu, Influence of degree of hydrolysis on functional properties, antioxidant and ACE inhibitory activities of egg white protein hydrolysate. Food Sci. Biotechnol. 21, 27–34 (2012)CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  • Ali Hamzeh
    • 1
  • Masoud Rezaei
    • 1
    Email author
  • Saber Khodabandeh
    • 2
  • Ali Motamedzadegan
    • 3
  • Mehrdad Noruzinia
    • 4
  1. 1.Department of Seafood ProcessingTarbiat Modares UniversityNoorIran
  2. 2.Department of Marine BiologyTarbiat Modares UniversityNoorIran
  3. 3.Department of Food ScienceAgricultural Sciences and Natural Resources University of SariSariIran
  4. 4.Department of HematologyTarbiat Modares UniversityTehranIran

Personalised recommendations