Abstract
Abalone gonads were hydrolyzed using alcalase followed by papain to produce angiotensin I-converting enzyme (ACE) inhibitory peptides. Gel filtration column chromatography analysis showed that the molecular weight of the fraction with high ACE inhibitory activity was below 1 kDa, which occupied 93.1 % of total hydrolysate. The ACE inhibitory peptide was purified by a series of column chromatographies, and the sequence of purified peptide was further identified as Ala–Met–Asn (AMN) by automated Edman degradation method. The triple peptide was then synthesized and had an ACE inhibitory activity with IC50 value of 106.24 μg/mL. After gastrointestinal digestion, the peptide still remained bioactivity. Lineweaver–Burk plots indicated that AMN acts as a non-competitive inhibitor against ACE. Our present study suggested that AMN derived from abalone gonad by-products may be used as an ideal nutrient for development of functional foods.
Similar content being viewed by others
References
Kearney PM, Whelton M, Reynolds K, Muntner P, Whelton PK, He J (2005) Global burden of hypertension: analysis of worldwide data. Lancet 365:217–223
Skeggs LT, Kahn JR, Shumway NP (1956) Preparation and function of the hypertensin converting enzyme. J Exp Med 103:295–299
Eriksson U, Danilczyk U, Penninger JM (2002) Just the beginning: novel functions for angiotensin-converting enzymes. Curr Biol 12:R745–R752
Riordan JF (2003) Angiotensin I-converting enzyme and its relatives. Genome Biol 4:225
Ferreira SH, Bartelt DC, Greene LJ (1970) Isolation of bradykinin-potentiating peptides from Bothrops jararaca venom. Biochemistry 9:2583–2593
Yu Y, Hu J, Miyaguchi Y, Bai X, Du Y, Lin B (2006) Isolation and characterization of angiotensin I-converting enzyme inhibitory peptides derived from porcine hemoglobin. Peptides 27:2950–2956
Asoodeh A, Memarpoor Yazdi M, Chamani J (2012) Purification and characterisation of angiotensin I-converting enzyme inhibitory peptides from lysozyme hydrolysates. Food Chem 131:291–295
Holder A, Birke A, Eisele T, Klaiber I, Fischer L, Hinrichs J (2013) Selective isolation of angiotensin I-converting enzyme-inhibitory peptides from micellar casein and β-casein hydrolysates via ultrafiltration. Int Dairy J 31:34–40
Tomatsu M, Shimakage A, Shinbo M, Yamada S, Takahashi S (2013) Novel angiotensin I-converting enzyme inhibitory peptides derived from soya milk. Food Chem 136:612–616
Gómez-Guillén M, Giménez B, López-Caballero M, Montero M (2011) Functional and bioactive properties of collagen and gelatin from alternative sources: a review. Food Hydrocolloid 25:1813–1827
Di Bernardini R, Mullen AM, Bolton D, Kerry J, O’Neill E, Hayes M (2012) Assessment of the angiotensin I-converting enzyme (ACE-I) inhibitory and antioxidant activities of hydrolysates of bovine brisket sarcoplasmic proteins produced by papain and characterisation of associated bioactive peptidic fractions. Meat Sci 90:226–235
Fujita H, Yoshikawa M (1999) LKPNM: a prodrug-type ACE-inhibitory peptide derived from fish protein. Immunopharma 44:123–127
Zhuang Y, Sun L, Li B (2012) Production of the angiotensin I-converting enzyme (ACE)-inhibitory peptide from hydrolysates of jellyfish (Rhopilema esculentum) collagen. Food Bioprocess Technol 5:1622–1629
Je JY, Park JY, Jung WK, Park PJ, Kim SK (2005) Isolation of angiotensin I converting enzyme (ACE) inhibitor from fermented oyster sauce, Crassostrea gigas. Food Chem 90:809–814
Ni H, Li L, Guo SS, Li HH, Jiang R, Hu SQ (2012) Isolation and identification of an angiotensin I-converting enzyme inhibitory peptide from yeast (Saccharomyces cerevisiae). Curr Anal Chem 8:180–185
Friedman DI, Amidon GL (1990) Characterization of the intestinal transport parameters for small peptide drugs. J Control Release 13:141–146
Vermeirssen V, Camp JV, Verstraete W (2004) Bioavailability of angiotensin I-converting enzyme inhibitory peptides. Br J Nutr 92:357–366
Lee SJ, Kim YS, Kim SE, Kim EK, Hwang JW, Park TK, Kim BK, Moon SH, Jeon BT, Jeon YJ (2012) Purification and characterization of a novel angiotensin I-converting enzyme inhibitory peptide derived from an enzymatic hydrolysate of duck skin byproducts. J Agric Food Chem 60:10035–10040
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
Sheih I, Fang TJ, Wu TK (2009) Isolation and characterisation of a novel angiotensin I-converting enzyme (ACE) inhibitory peptide from the algae protein waste. Food Chem 115:279–284
Anonymous (2013) China fisheries yearbook. China Agricultural Press, Beijing, pp 213
Zhu BW, Wang LS, Zhou DY, Li DM, Sun LM, Yang JF, Wu HT, Zhou XQ, Tada M (2008) Antioxidant activity of sulphated polysaccharide conjugates from abalone (Haliotis discus hannai Ino). Eur Food Res Technol 227:1663–1668
Zhu BW, Zhou DY, Li T, Yan S, Yang JF, Li DM, Dong XP, Murata Y (2010) Chemical composition and free radical scavenging activities of a sulphated polysaccharide extracted from abalone gonad (Haliotis Discus Hannai Ino). Food Chem 121:712–718
Helrich K (1990) Official methods of analysis of the association of official analytical chemists, 15th edn. Association of Official Analytical Chemists Inc., Arlington, p 807
Cushman D, Cheung H (1971) Spectrophotometric assay and properties of the angiotensin-converting enzyme of rabbit lung. Biochem Pharmacol 20:1637–1648
Schägger H (2006) Tricine-SDS-PAGE. Nat Protoc 1:16–22
Cai QF, Liu GM, Li T, Hara K, Wang XC, Su WJ, Cao MJ (2010) Purification and characterization of parvalbumins, the major allergens in Red Stingray (Dasyatis akajei). J Agric Food Chem 58:12964–12969
Bush K, Henry PR, Slusarchyk DS (1984) Muraceins–muramyl peptides produced by Nocardia orientalis as angiotensin-converting enzyme inhibitors. I. Taxonomy, fermentation and biological properties. J Antibiot 37:330–335
Alting AC, Meijer RJ, van Beresteijn EC (1997) Incomplete elimination of the ABBOS epitope of bovine serum albumin under simulated gastrointestinal conditions of infants. Diabetes Care 20:875–880
Intarasirisawat R, Benjakul S, Wu J, Visessanguan W (2013) Isolation of antioxidative and ACE inhibitory peptides from protein hydrolysate of skipjack (Katsuwana pelamis) roe. J Funct Foods 5:1854–1862
Balti R, Nedjar-Arroume N, Bougatef A, Guillochon D, Nasri M (2010) Three novel angiotensin I-converting enzyme (ACE) inhibitory peptides from cuttlefish (Sepia officinalis) using digestive proteases. Food Res Int 43:1136–1143
Li Y, Zhou J, Huang K, Sun Y, Zeng X (2012) Purification of a novel angiotensin I-converting enzyme (ACE) inhibitory peptide with an antihypertensive effect from loach (Misgurnus anguillicaudatus). J Agric Food Chem 60:1320–1325
Rao S, Sun J, Liu Y, Zeng H, Su Y, Yang Y (2012) ACE inhibitory peptides and antioxidant peptides derived from in vitro digestion hydrolysate of hen egg white lysozyme. Food Chem 135:1245–1252
Dai CH, Ma HL, Luo L, Yin XL (2013) Angiotensin I-converting enzyme (ACE) inhibitory peptide derived from Tenebrio molitor (L.) larva protein hydrolysate. Eur Food Res Technol 236:681–689
Natesh R, Schwager SL, Sturrock ED, Acharya KR (2003) Crystal structure of the human angiotensin-converting enzyme–lisinopril complex. Nature 421:551–554
Murray B, FitzGerald R (2007) Angiotensin converting enzyme inhibitory peptides derived from food proteins: biochemistry, bioactivity and production. Curr Pharm Design 13:773–791
Cheung HS, Wang Fl, Ondetti MA, Sabo EF, Cushman DW (1980) Binding of peptide substrates and inhibitors of angiotensin-converting enzyme. Importance of the COOH-terminal dipeptide sequence. J Biol Chem 255:401–407
Si D, Wang Y, Zhou YH, Guo Y, Wang J, Zhou H, Li ZS, Fawcett JP (2009) Mechanism of CYP2C9 inhibition by flavones and flavonols. Drug Metab Dispos 37:629–634
Jao CL, Huang SL, Hsu KC (2012) Angiotensin I-converting enzyme inhibitory peptides: inhibition mode, bioavailability, and antihypertensive effects. BioMedicine 2:30–136
Jang JH, Jeong SC, Kim JH, Lee YH, Ju YC, Lee JS (2011) Characterisation of a new antihypertensive angiotensin I-converting enzyme inhibitory peptide from Pleurotus cornucopiae. Food Chem 127:412–418
Lau CC, Abdullah N, Shuib AS, Aminudin N (2014) Novel angiotensin I-converting enzyme inhibitory peptides derived from edible mushroom Agaricus bisporus (J.E. Lange) Imbach identified by LC-MS/MS. Food Chem 148:396–401
Ni H, Li L, Liu G, Hu SQ (2012) Inhibition mechanism and model of an angiotensin I-converting enzyme (ACE)-inhibitory hexapeptide from yeast (Saccharomyces cerevisiae). PLoS ONE 7:e37077
Acknowledgments
This study was sponsored by the National Natural Scientific Foundation of China (No. 31271838), the Key Project of the Ministry of Science and Technology of China (2012BAD38B09), the Public Science and Technology Research Fund Project of Ocean (201305015-3), and the Science and Technology Bureau of Xiamen (3502Z20133020).
Conflict of interest
None.
Compliance with Ethics Requirements
This article does not contain any studies with human or animal subjects.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wu, Q., Cai, QF., Tao, ZP. et al. Purification and characterization of a novel angiotensin I-converting enzyme inhibitory peptide derived from abalone (Haliotis discus hannai Ino) gonads. Eur Food Res Technol 240, 137–145 (2015). https://doi.org/10.1007/s00217-014-2315-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00217-014-2315-8