Skip to main content

ACE Inhibitory and Antioxidant Activities of Novel Peptides from Scorpaena notata By-product Protein Hydrolysate

Abstract

This study describes the isolation of angiotensin I converting enzyme and antioxidative peptides from head protein hydrolysate of red scorpionfish (Scorpaena notata) prepared by treatment with a protease from the fungus Penicillium digitatum. After ultrafiltration, three peptides were isolated by a two-step procedure: size exclusion chromatography on a Toyopearl HW-40 followed by reversed-phase high performance liquid chromatography (RP-HPLC) with a high purification yield of 2.22 mg of peptide/g of initial protein. Active peptides were then identified by nanoscale liquid chromatography coupled to tandem mass spectrometry (nanoLC/MS–MS), corresponding to the following sequences: Gln–Gln–Pro–His–Ser–Arg–Ser–Lys–Gly–Phe–Pro–Gly–Pro (1424.724 Da), Gly–Gln–Lys–Ser–Val–Pro–Glu–Val–Arg (1000.565 Da) and Val–Glu–Gly–Lys–Ser–Pro–Asn–Val (830.448 Da). Peptides D-I, E-I and F-I showed high angiotensin-I converting enzyme inhibitory activity with an IC50 values of 0.98, 1.69 and 1.44 µM, respectively as well as a synergistic antioxidant activity between the different fractions. Thus, we have demonstrated that underutilized wastes can be valorized by production of peptides that can be used as potential therapeutic compounds active against oxidative stress and hypertension.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Adler-Nissen J (1986) A review of food hydrolysis specific areas. In: Adler-Nissen J (ed) Enzymic hydrolysis of food proteins. Elsevier Applied Science Publishers, Copenhagen, pp 57–109

    Google Scholar 

  • Aissaoui N, Abidi F, Mahat S, Marzouki MN (2014) Purification and biochemical characterization of a novel protease from Penicillium digitatum—Use in bioactive peptides production. J Basic Microbiol 54:178–189

    Article  Google Scholar 

  • Arihara K (2006) Strategies for designing novel functional meat products. Meat Sci 74:219–229

    CAS  Article  PubMed  Google Scholar 

  • Balti R, Nedjar-Arroume N, Adjé EY, Guillochon D, Nasri M (2010a) Analysis of novel angiotensin I-converting enzyme inhibitory peptides from enzymatic hydrolysates of cuttlefish (Sepia officinalis) muscle proteins. J Agric Food Chem 58:3840–3846

    CAS  Article  PubMed  Google Scholar 

  • Balti R, Nedjar-Arroume N, Bougatef A, Guillochon D, Nasri M (2010b) Three novel angiotensin I-converting enzyme (ACE) inhibitory peptides from cuttlefish (Sepia officinalis) using digestive proteases. Food Res Int 43:1136–1143

    CAS  Article  Google Scholar 

  • Batista I, Ramos C, Coutinho J, Bandarra NM, Nunes ML (2010) Characterization of protein hydrolysates and lipids obtained from black scabbardfish (Aphanopus carbo) by-products and antioxidative activity of the hydrolysates produced. Process Biochem 45:18–24

    CAS  Article  Google Scholar 

  • 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 114:1198–1205

    CAS  Article  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254

    CAS  Article  PubMed  Google Scholar 

  • Byun HG, Kim SK (2001) Purification and characterization of angiotensin I converting enzyme (ACE) inhibitory peptides from Alaska pollack (Theragra chalcogramma) Skin. Process Biochem 36:1155–1162

    CAS  Article  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 44:2619–2623

    Article  Google Scholar 

  • Fahmi A, Morimura S, Guo HC, Shigematsu T, Kida K, Uemura Y (2004) Production of angiotensin I converting enzyme inhibitory peptides from sea bream scale. Process Biochem 39:1195–1200

    CAS  Article  Google Scholar 

  • FAO (2014) The state of world fisheries and aquaculture 2012: opportunities and challenges. Food and Agricultural Organization of the United Nation, Rome, pp 4–7

    Google Scholar 

  • Fujita H, Yoshikawa M (1999) LKPNM: a prodrug-type ACE-inhibitory peptide derived from fish protein. Immunopharmacol 44:123–127

    CAS  Article  Google Scholar 

  • Gu Y, Wu J (2013) LC–MS/MS coupled with QSAR modeling in characterizing of angiotensin I-converting enzyme inhibitory peptides from soybean proteins. Food Chem 141:2682–2690

    CAS  Article  PubMed  Google Scholar 

  • Intarasirisawat R, Benjakul S, Wu J, Visessanguan W (2014) Isolation of antioxidative and ACE inhibitory peptides from protein hydrolysate of skipjack (Katsuwana pelamis) roe. J Funct Foods 5:1854–1862

    Article  Google Scholar 

  • Je JY, Park PJ, Kwon JY, Kim SK (2004) A novel angiotensin I converting enzyme inhibitory peptide from Alaska pollack (Theragra chalcogramma) frame protein hydrolysate. J Agric Food Chem 52:7842–7845

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Jung WK, Mendis E, Je JY, Park PJ, Son BW, Kim HC, Choi YK, Kim SK (2006) Angiotensin I-converting enzyme inhibitory peptide from yellowfin sole (Limanda aspera) frame protein and its antihypertensive effect in spontaneously hypertensive rats. Food Chem 94:26–32

    CAS  Article  Google Scholar 

  • Kim HM, Shin DR, Yoo OJ, Lee H, Lee JO (2003) Crystal structure of drosophila angiotensin I-converting enzyme bound to captopril and lisinopril. FEBS Lett 538:65–70

    CAS  Article  PubMed  Google Scholar 

  • Lee SH, Qian ZJ, Kim SK (2010) A novel angiotensin I converting enzyme inhibitory peptide from tuna frame protein hydrolysate and its antihypertensive effect in spontaneously hypertensive rats. Food Chem 118:96–102

    CAS  Article  Google Scholar 

  • Lee JK, Jeon JK, Byun HG (2014) Antihypertensive effect of novel angiotensin I converting enzyme inhibitory peptide from chum salmon (Oncorhynchus keta) skin in spontaneously hypertensive rats. J Funct Foods 7:381–389

    CAS  Article  Google Scholar 

  • Lun HH, Lan CX, Yun SC, Zhong ZY, Cheng ZB (2006) Analysis of novel angiotensin-I-converting enzyme inhibitory peptides from protease-hydrolyzed marine shrimp Acetes chinensis. J Pept Sci 12:726–733

    Article  Google Scholar 

  • Matsufuji H, Matsui T, Seki E, Osajima K, Nakashima M, Osajima Y (1994) Angiotensin I-converting enzyme inhibitory peptides in an alkaline protease hydrolyzate derived from sardine muscle. Biosci Biotechnol Biochem 58:2244–2245

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Mendis E, Rakapakse N, Kim SK (2005b) Antioxidant properties of a radical scavenging peptide purified from enzymatically prepared fish skin gelatin hydrolysates. J Agric Food Chem 53:581–587

    CAS  Article  PubMed  Google Scholar 

  • Nakamura Y, Yamamoto N, Sakai K, Okubo A, Yamazaki S, Takano T (1995) Purification and characterization of angiotensin I converting-enzyme inhibitors from sour milk. J Dairy Sci 78:777–783

    CAS  Article  PubMed  Google Scholar 

  • Natesh R, Schwager SL, Sturrock ED, Acharya KR (2003) Crystal structure of the human angiotensin-converting enzyme–lisinopril complex. Nature 421:551–554

    CAS  Article  PubMed  Google Scholar 

  • Norris R, FitzGerald RJ (2013) Antihypertensive peptides from food proteins. In: Hernandez-Ledezma B, Hseih B (eds) Bioactive food peptides in health and disease. In Tech, Croatia, pp 45–72

    Google Scholar 

  • Ordines F, Quetglas A, Massutı´ E, Moranta J (2009) Habitat preferences and life history of the red scorpion fish, Scorpaena notata in the Mediterranean. Estuar Coast Shelf Sci 85:537–546

    Article  Google Scholar 

  • Rajapakse N, Mendis E, Jung WK, Je JY, Kim SK (2005) Purification of a radical scavenging peptide from fermented mussel sauce and its antioxidant properties. Food Res Int 38:175–182

    CAS  Article  Google Scholar 

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

    CAS  Article  PubMed  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 51:3661–3667

    CAS  Article  PubMed  Google Scholar 

  • Sharma S, Singh R, Rana R (2011) Bioactive peptides. Int J Bioautomation 15:223–250

    CAS  Google Scholar 

  • Suetsuna K, Nakano T (2000) Identification of an antihypertensive peptide from peptic digest of wakame (Undaria pinnatifida). J Nutr Biochem 11:450–454

    CAS  Article  PubMed  Google Scholar 

  • Tsai JS, Chen JL, Pan BS (2008) ACE-inhibitory peptides identified from the muscle protein hydrolysate of hard clam (Meretrix lusoria). Process Biochem 43:743–747

    CAS  Article  Google Scholar 

  • Tsuge N, Eikawa Y, Nomura Y, Yamamoto M, Sugisawa K (1991) Antioxidant activity of peptides prepared by enzymatic hydrolysis of egg-white albumin. Nippon Nogeik Kaishi–J Japan Soci Biosci Biotechnol Agrochem 65:1635–1641

    CAS  Google Scholar 

  • Wang B, Li L, Chi CF, Maa JH, Luo HY, Xu YF (2013) Purification and characterization of a novel antioxidant peptide derived from blue mussel (Mytilus edulis) protein hydrolysate. Food Chem 138:1713–1719

    CAS  Article  PubMed  Google Scholar 

  • Wijesekara I, Kim SK (2010) Angiotensin-I-converting enzyme (ACE) inhibitors from marine resources: prospects in the pharmaceutical industry. Mar Drugs 8:1080–1093

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Wu J, Ding X (2002) Characterization of inhibition and stability of soy-protein derived angiotensin I-converting enzyme inhibitory peptides. Food Res Int 35:367–375

    CAS  Article  Google Scholar 

  • Yen GC, Wu JY (1999) Antioxidant and radical properties of extracts from Ganoderma tsugae. Food Chem 65:375–379

    CAS  Article  Google Scholar 

  • 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 43:1167–1173

    CAS  Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the financial project of LIP-MB Laboratory, INSAT, Carthage University, Ministry of Higher Education and Scientific Research of Tunisia.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Neyssene Aissaoui.

Ethics declarations

Conflict of Interest

The authors declare that they have no competing interests.

Human Rights and Informed Consent

This manuscript does not contain any studies with human subjects performed by any of authors.

Additional information

Ferid Abidi and Julie Hardouin are the authors contributed equally to this work.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Aissaoui, N., Abidi, F., Hardouin, J. et al. ACE Inhibitory and Antioxidant Activities of Novel Peptides from Scorpaena notata By-product Protein Hydrolysate. Int J Pept Res Ther 23, 13–23 (2017). https://doi.org/10.1007/s10989-016-9536-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10989-016-9536-6

Keywords

  • Angiotensin-I converting enzyme
  • Antioxidant peptides
  • Protein hydrolysate
  • Scorpaena notata