Antioxidant and antihypertensive protein hydrolysates in fish products – a review K., Tkaczewska J., Migdał W. (2018): Antioxidant and antihypertensive protein hydrolysates in fish products – a review. Czech J. Food Sci., 36: 195-207.
download PDF

Fish proteins are a good source of bioactive peptides (BAPs). Such BAPs are derived through enzymatic hydrolysis of food proteins and can potentially by applied as health-promoting factors against chronic non-communicable diseases (NCDs), including arterial hypertension, cardiovascular disease and obesity. Antihypertensive and antioxidant BAPs derived from fish could represent a good alternative to synthetic drugs. This article reviews the literature on BAPs derived from fish and fish products, with an emphasis on antihypertensive and antioxidant properties and the impact of technological processes on the activity of BAPs. The review shows that BAPs isolated from fish exhibit quite good stability when applied under moderate physical conditions and after simulated in vitro digestion. Processing can increase the susceptibility of peptides to digestion in the digestive tract as well as improving absorption and immune system responses. Therefore, it is important to determine the optimal conditions under which proteins (and peptides) can be processed in order to maintain their bioactivity. Future research efforts on BAPs should be directed towards an elucidation of their activity after technological processes.

Balti Rafik, Nedjar-Arroume Naima, Bougatef Ali, Guillochon Didier, Nasri Moncef (2010): Three novel angiotensin I-converting enzyme (ACE) inhibitory peptides from cuttlefish (Sepia officinalis) using digestive proteases. Food Research International, 43, 1136-1143
Benhabiles M.S., Abdi N., Drouiche N., Lounici H., Pauss A., Goosen M.F.A., Mameri N. (2012): Fish protein hydrolysate production from sardine solid waste by crude pepsin enzymatic hydrolysis in a bioreactor coupled to an ultrafiltration unit. Materials Science and Engineering: C, 32, 922-928
Borawska J., Darewicz M., Pliszka M., Vegarud G.E. (2016a): Antioxidant properties of salmon (Salmo salar L.) protein fraction hydrolysates revealed following their ex vivo digestion and in vitro hydrolysis. Journal of the Science of Food and Agriculture, 96: 2764–2772.
Borawska J., Darewicz M., Vegarud G.E., Minkiewicz P. (2016b): Antioxidant properties of carp (Cyprinus carpio L.) protein ex vivo and in vitro hydrolysates. Food Chemistry, 194: 770–779.
Borawska J., Darewicz M., Vegarud G.E., Iwaniak A., Minkiewicz P. (2015): Ex vivo digestion of carp muscle tissue – ACE inhibitory and antioxidant activities of the obtained hydrolysates. Food & Function, 6: 211–218.
Bruno Benjamin J, Miller Geoffrey D, Lim Carol S (2013): Basics and recent advances in peptide and protein drug delivery. Therapeutic Delivery, 4, 1443-1467
Chalamaiah M., Jyothirmayi T., Diwan Prakash V., Dinesh Kumar B. (2015): Antioxidant activity and functional properties of enzymatic protein hydrolysates from common carp (Cyprinus carpio) roe (egg). Journal of Food Science and Technology, 52, 5817-5825
Chalamaiah M., Jyothirmayi T., Bhaskarachary K., Vajreswari A., Hemalatha R., Dinesh Kumar B. (2013): Chemical composition, molecular mass distribution and antioxidant capacity of rohu (Labeo rohita) roe (egg) protein hydrolysates prepared by gastrointestinal proteases. Food Research International, 52, 221-229
Cheison Seronei Chelulei, Wang Zhang, Xu Shi-Ying (2007): Preparation of Whey Protein Hydrolysates Using a Single- and Two-Stage Enzymatic Membrane Reactor and Their Immunological and Antioxidant Properties:  Characterization by Multivariate Data Analysis. Journal of Agricultural and Food Chemistry, 55, 3896-3904
Chen Jiwang, Wang Yimei, Zhong Qixin, Wu Yongning, Xia Wenshui (2012): Purification and characterization of a novel angiotensin-I converting enzyme (ACE) inhibitory peptide derived from enzymatic hydrolysate of grass carp protein. Peptides, 33, 52-58
Choonpicharn Sadabpong, Jaturasitha Sanchai, Rakariyatham Nuansri, Suree Nuttee, Niamsup Hataichanoke (2015): Antioxidant and antihypertensive activity of gelatin hydrolysate from Nile tilapia skin. Journal of Food Science and Technology, 52, 3134-3139
Darewicz M., Borawska J., Pliszka M. (2016): Carp proteins as a source of bioactive peptides – an in silico approach. Czech Journal of Food Sciences, 34, 111-117
Darewicz M., Borawska J., Minkiewicz P., Iwaniak A., Starowicz P. (2015a): Biologicznie aktywne peptydy uwalniane z białek żywności. Żywność. Nauka. Technologia. Jakość, 3: 26–41.
Darewicz M., Borawska J., Pliszka M., Świtaj M. (2015b): Białka pstrąga tęczowego potencjalnym źródłem bioaktywnych peptydów – badania in silico. Trendy w żywieniu człowieka, 37–46.
Darewicz Małgorzata, Borawska Justyna, Vegarud Gerd, Minkiewicz Piotr, Iwaniak Anna (2014): Angiotensin I-Converting Enzyme (ACE) Inhibitory Activity and ACE Inhibitory Peptides of Salmon (Salmo salar) Protein Hydrolysates Obtained by Human and Porcine Gastrointestinal Enzymes. International Journal of Molecular Sciences, 15, 14077-14101
Darewicz Małgorzata, Dziuba Bartłomiej, Minkiewicz Piotr, Dziuba Jerzy (2011): The Preventive Potential of Milk and Colostrum Proteins and Protein Fragments. Food Reviews International, 27, 357-388
Di Bernardini Roberta, Harnedy Pádraigín, Bolton Declan, Kerry Joseph, O’Neill Eileen, Mullen Anne Maria, Hayes Maria (2011): Antioxidant and antimicrobial peptidic hydrolysates from muscle protein sources and by-products. Food Chemistry, 124, 1296-1307
Elavarasan K., Shamasundar B.A., Badii Faraha, Howell Nazlin (2016): Angiotensin I-converting enzyme (ACE) inhibitory activity and structural properties of oven- and freeze-dried protein hydrolysate from fresh water fish (Cirrhinus mrigala). Food Chemistry, 206, 210-216
Erdmann Kati, Cheung Belinda W.Y., Schröder Henning (2008): The possible roles of food-derived bioactive peptides in reducing the risk of cardiovascular disease. The Journal of Nutritional Biochemistry, 19, 643-654
Ferraro V., Carvalho A.P., Piccirillo C., Santos M.M., Castro P.M., Pintado M.E. (2013): Extraction of high added value biological compounds from sardine, sardinetype fish and mackerel canning residues – a review. Materials Science & Engineering C, Materials for biological applications, 33: 3111–3120.
Fu Yu, Young Jette F., Dalsgaard Trine K., Therkildsen Margrethe (2015): Separation of angiotensin I-converting enzyme inhibitory peptides from bovine connective tissue and their stability towards temperature, pH and digestive enzymes. International Journal of Food Science & Technology, 50, 1234-1243
Fujita H., Yokoyama K., Yasumoto R., Yoshikawa M. (1995): Antihypertensive effect of thermolysin digest of dried bonito in spontaneously hypertensive rat. Clinical and Experimental Pharmacology and Physiology. Supplement, 22: 304–305.
Garcia-Mora P., Peñas E., Frias J., Gomez R., Martinez-Villaluenga C. (2015): High-pressure improves enzymatic proteolysis and the release of peptides with angiotensin I converting enzyme inhibitory and antioxidant activities from lentil proteins. Food Chemistry, 171, 224-232
Gringer Nina, Safafar Hamed, du Mesnildot Axelle, Nielsen Henrik H., Rogowska-Wrzesinska Adelina, Undeland Ingrid, Baron Caroline P. (2016): Antioxidative low molecular weight compounds in marinated herring (Clupea harengus) salt brine. Food Chemistry, 194, 1164-1171
Gu Rui-Zeng, Li Chen-Yue, Liu Wen-Ying, Yi Wei-Xue, Cai Mu-Yi (2011): Angiotensin I-converting enzyme inhibitory activity of low-molecular-weight peptides from Atlantic salmon (Salmo salar L.) skin. Food Research International, 44, 1536-1540
Halldorsdottir Sigrun M., Sveinsdottir Holmfridur, Gudmundsdottir Agusta, Thorkelsson Gudjon, Kristinsson Hordur G. (2014): High quality fish protein hydrolysates prepared from by-product material with Fucus vesiculosus extract. Journal of Functional Foods, 9, 10-17
Han Y., Byun S.-H., Park Y.-H., Kim S.-B. (2015): Bioactive properties of enzymatic hydrolysates from abdominal skin gelatin of yellowfin tuna (Thunnus albacares). Food Science & Technology, 50: 1996–2003.
He Rong, Alashi Adeola, Malomo Sunday A., Girgih Abraham T., Chao Dongfang, Ju Xingrong, Aluko Rotimi E. (2013): Antihypertensive and free radical scavenging properties of enzymatic rapeseed protein hydrolysates. Food Chemistry, 141, 153-159
Hsu Kuo-Chiang (2010): Purification of antioxidative peptides prepared from enzymatic hydrolysates of tuna dark muscle by-product. Food Chemistry, 122, 42-48
Huang Bo-Bin, Lin Hsin-Chieh, Chang Yu-Wei (2015): Analysis of proteins and potential bioactive peptides from tilapia (Oreochromis spp.) processing co-products using proteomic techniques coupled with BIOPEP database. Journal of Functional Foods, 19, 629-640
Hwang Jyh-Sheng (2010): Impact of processing on stability of angiotensin I-converting enzyme (ACE) inhibitory peptides obtained from tuna cooking juice. Food Research International, 43, 902-906
Je Jae-Young, Lee Ka-Hwa, Lee Mi Hyun, Ahn Chang-Bum (2009): Antioxidant and antihypertensive protein hydrolysates produced from tuna liver by enzymatic hydrolysis. Food Research International, 42, 1266-1272
JE J, PARK P, BYUN H, JUNG W, KIM S (2005): Angiotensin I converting enzyme (ACE) inhibitory peptide derived from the sauce of fermented blue mussel,. Bioresource Technology, 96, 1624-1629
Kim Hyun-Jin, Kang Seong-Gook, Jaiswal Lily, Li Jinglei, Choi Ju-Hee, Moon Sang-Mi, Cho Jeong-Yong, Ham Kyung-Sik (2016): Identification of four new angiotensin I-converting enzyme inhibitory peptides from fermented anchovy sauce. Applied Biological Chemistry, 59, 25-31
Kim Sung-Rae, Byun Hee-Guk (2012): The Novel Angiotensin I Converting Enzyme Inhibitory Peptide from Rainbow Trout Muscle Hydrolysate. Fisheries and aquatic sciences, 15, 183-190
Kim Se-Kwon, Wijesekara Isuru (2010): Development and biological activities of marine-derived bioactive peptides: A review. Journal of Functional Foods, 2, 1-9
Kristinsson Hordur G., Rasco Barbara A. (2000): Fish Protein Hydrolysates: Production, Biochemical, and Functional Properties. Critical Reviews in Food Science and Nutrition, 40, 43-81
Lafarga Tomas, Hayes Maria (2016): Bioactive protein hydrolysates in the functional food ingredient industry: Overcoming current challenges. Food Reviews International, 33, 217-246
Lassoued Imen, Mora Leticia, Barkia Ahmed, Aristoy M-Concepción, Nasri Moncef, Toldrá Fidel (2015): Bioactive peptides identified in thornback ray skin's gelatin hydrolysates by proteases from Bacillus subtilis and Bacillus amyloliquefaciens. Journal of Proteomics, 128, 8-17
Lee Sang-Hoon, Qian Zhong-Ji, Kim Se-Kwon (2010): A novel angiotensin I converting enzyme inhibitory peptide from tuna frame protein hydrolysate and its antihypertensive effect in spontaneously hypertensive rats. Food Chemistry, 118, 96-102
Lemes Ailton, Sala Luisa, Ores Joana, Braga Anna, Egea Mariana, Fernandes Kátia (2016): A Review of the Latest Advances in Encrypted Bioactive Peptides from Protein-Rich Waste. International Journal of Molecular Sciences, 17, 950-
Leygonie Coleen, Britz Trevor J., Hoffman Louwrens C. (2012): Impact of freezing and thawing on the quality of meat: Review. Meat Science, 91, 93-98
Li Ying, Yu Jianmei (2015): Research Progress in Structure-Activity Relationship of Bioactive Peptides. Journal of Medicinal Food, 18, 147-156
Li Xue, Luo Yongkang, Shen Huixing, You Juan (2012): Antioxidant activities and functional properties of grass carp (Ctenopharyngodon idellus) protein hydrolysates. Journal of the Science of Food and Agriculture, 92, 292-298
Li-Chan Eunice CY (2015): Bioactive peptides and protein hydrolysates: research trends and challenges for application as nutraceuticals and functional food ingredients. Current Opinion in Food Science, 1, 28-37
Łuczyńska Joanna, Tońska Elzbieta, Borejszo Zbigniew (2011): CONTENT OF MACRO- AND MICROELEMENTS, AND FATTY ACIDS IN MUSCLES OF SALMON (SALMO SALAR L.), RAINBOW TROUT (ONCORHYNCHUS MYKISS WALB.), AND CARP (CYPRINUS CARPIO L.). Zywnosc.Nauka.Technologia.Jakosc/Food.Science.Technology.Quality, , -
Madureira A.R., Tavares T., Gomes A.M.P., Pintado M.E., Malcata F.X. (2010): Invited review: Physiological properties of bioactive peptides obtained from whey proteins. Journal of Dairy Science, 93, 437-455
Manikkam V., Vasiljevic T., Donkor O. N., Mathai M. L. (2014): A Review of Potential Marine-derived Hypotensive and Anti-obesity Peptides. Critical Reviews in Food Science and Nutrition, 56, 92-112
Mora L., Gallego M., Reig M., Toldrá F. (2017): Challenges in the quantitation of naturally generated bioactive peptides in processed meats. Trends in Food Science & Technology, 69: 306–314.
Mora Leticia, Reig Milagro, Toldrá Fidel (2014): Bioactive peptides generated from meat industry by-products. Food Research International, 65, 344-349
Möller Niels Peter, Scholz-Ahrens Katharina Elisabeth, Roos Nils, Schrezenmeir Jürgen (2008): Bioactive peptides and proteins from foods: indication for health effects. European Journal of Nutrition, 47, 171-182
Murray B., FitzGerald R. (2007): Angiotensin Converting Enzyme Inhibitory Peptides Derived from Food Proteins: Biochemistry, Bioactivity and Production. Current Pharmaceutical Design, 13, 773-791
Neves Adriana C., Harnedy Pádraigín A., O’Keeffe Martina B., FitzGerald Richard J. (2017): Bioactive peptides from Atlantic salmon ( Salmo salar ) with angiotensin converting enzyme and dipeptidyl peptidase IV inhibitory, and antioxidant activities. Food Chemistry, 218, 396-405
Ovissipour Mahmoudreza, Rasco Barbara, Shiroodi Setareh Ghorban, Modanlow Maryam, Gholami Sanaz, Nemati Mahrokh (2013): Antioxidant activity of protein hydrolysates from whole anchovy sprat ( Clupeonella engrauliformis ) prepared using endogenous enzymes and commercial proteases. Journal of the Science of Food and Agriculture, 93, 1718-1726
Phadke G., Elavarasan K., Shamasundar B.A. (2014): Angiotensin-I converting enzyme (ACE) inhibitory activity and antioxidant activity of fermented fish product ngari as influenced by fermentation period. International Journal of Pharma and Bio Sciences, 5: 134–142.
Power O., Fernández A., Norris R., Riera F.A., FitzGerald R.J. (2014): Selective enrichment of bioactive properties during ultrafiltration of a tryptic digest of β-lactoglobulin. Journal of Functional Foods, 9, 38-47
Rajapakse Niranjan, Mendis Eresha, Jung Won-Kyo, Je Jae-Young, Kim Se-Kwon (2005): Purification of a radical scavenging peptide from fermented mussel sauce and its antioxidant properties. Food Research International, 38, 175-182
Rao Qinchun, Klaassen Kamdar Andre, Labuza Theodore P. (2013): Storage Stability of Food Protein Hydrolysates—A Review. Critical Reviews in Food Science and Nutrition, 56, 1169-1192
Rao R.K. (1991): Biologically active peptides in the gastrointestinal lumen. Life Sciences, 48, 1685-1704
Rasika D.M.D., Ranadheera C.S., Vidanarachchi J.K. (2013): Applications of Marine-derived Peptides and Proteins in the Food Industry. In: Kim S.-K. (ed.): Marine Proteins and Peptides Biological Activities and Applications. Oxford, Wiley-Blackwell: 545–587.
Rasyad F., Huang T.C., Hsu J.L., Fadjar M. (2016): Screening of Novel angiotensin I converting enzyme inhibitory peptides derived from enzymatic hydrolysis of salmon protamine. Journal of Life Science and Biomeicine, 6: 100–105
Rombenso Artur N., Trushenski Jesse T., Schwarz Michael H. (2016): Fish oil replacement in feeds for juvenile Florida Pompano: Composition of alternative lipid influences degree of tissue fatty acid profile distortion. Aquaculture, 458, 177-186
Rousseau-Ralliard D., Goirand F., Tardivel S., Lucas A., Algaron F., Mollé D., Robert V., Auchère D., Boudier J.-F., Gaillard J.-L., Monnet V., Tauzin J., Grynberg A. (2010): Inhibitory effect of αS1- and αS2-casein hydrolysates on angiotensin I-converting enzyme in human endothelial cells in vitro, rat aortic tissue ex vivo, and renovascular hypertensive rats in vivo. Journal of Dairy Science, 93, 2906-2921
Saito Koichiro, Jin Dong-Hao, Ogawa Tomohisa, Muramoto Koji, Hatakeyama Eiko, Yasuhara Tadashi, Nokihara Kiyoshi (2003): Antioxidative Properties of Tripeptide Libraries Prepared by the Combinatorial Chemistry. Journal of Agricultural and Food Chemistry, 51, 3668-3674
Savjani Ketan T., Gajjar Anuradha K., Savjani Jignasa K. (2012): Drug Solubility: Importance and Enhancement Techniques. ISRN Pharmaceutics, 2012, 1-10
Singh Brij Pal, Vij Shilpa, Hati Subrota (2014): Functional significance of bioactive peptides derived from soybean. Peptides, 54, 171-179
Skanderby M. (1994): Protein hydrolysates: their functionality and applications. European Food Research and Technology, 10: 141
Slizyte Rasa, Rommi Katariina, Mozuraityte Revilija, Eck Peter, Five Kathrine, Rustad Turid (2016): Bioactivities of fish protein hydrolysates from defatted salmon backbones. Biotechnology Reports, 11, 99-109
Song Ru, Wei Rong-bian, Ruan Guang-qiang, Luo Hong-yu (2015): Isolation and identification of antioxidative peptides from peptic hydrolysates of half-fin anchovy (Setipinna taty). LWT - Food Science and Technology, 60, 221-229
Toopcham Tidarat, Roytrakul Sittiruk, Yongsawatdigul Jirawat (2015): Characterization and identification of angiotensin I-converting enzyme (ACE) inhibitory peptides derived from tilapia using Virgibacillus halodenitrificans SK1-3-7 proteinases. Journal of Functional Foods, 14, 435-444
Traore S., Aubry L., Gatellier P., Przybylski W., Jaworska D., Kajak-Siemaszko K., Santé-Lhoutellier V. (2012): Effect of heat treatment on protein oxidation in pig meat. Meat Science, 91, 14-21
Tsai Jenn-Shou, Chen Jia-Ling, Pan Bonnie Sun (2008): ACE-inhibitory peptides identified from the muscle protein hydrolysate of hard clam (Meretrix lusoria). Process Biochemistry, 43, 743-747
Vieira Elsa F., Ferreira Isabel M.P.L.V.O. (2016): Antioxidant and antihypertensive hydrolysates obtained from by-products of cannery sardine and brewing industries. International Journal of Food Properties, 20, 662-673
Wang J., Hu J., Cui J., Bai X., Dua Y., Miyaguchi Y., Lin B. (2008a): Purification and identification of a ACE-inhibitory peptide from oyster proteins hydrolyzate and the antihypertensive effect of hydrolyzate in spontaneously hypertensive rats. Food Chemistry, 111: 302–308.
Wang J.R., Teng D., Tian Z.G. (2008b): Preparation and mechanism of functional antioxidant peptides. Natural Product Research and Development, 20: 371–375
Wiriyaphan Chompoonuch, Chitsomboon Benjamart, Yongsawadigul Jirawat (2012): Antioxidant activity of protein hydrolysates derived from threadfin bream surimi byproducts. Food Chemistry, 132, 104-111
Wu Jianping, Aluko Rotimi E., Nakai Shuryo (2006): Structural Requirements of Angiotensin I-Converting Enzyme Inhibitory Peptides:  Quantitative Structure−Activity Relationship Study of Di- and Tripeptides. Journal of Agricultural and Food Chemistry, 54, 732-738
Yang Ping, Ke Hongqiao, Hong Pengzhi, Zeng Shaokui, Cao Wenhong (2011): Antioxidant activity of bigeye tuna (Thunnus obesus) head protein hydrolysate prepared with Alcalase. International Journal of Food Science & Technology, 46, 2460-2466
Yokoyama Keiichi, Chiba Hideo, Yoshikawa Masaaki (2014): Peptide Inhibitors for Angiotensin I-Converting Enzyme from Thermolysin Digest of Dried Bonitot. Bioscience, Biotechnology, and Biochemistry, 56, 1541-1545
Yongsawatdigul Jirawat, Hemung Bung-Orn (2010): Structural Changes and Functional Properties of Threadfin Bream Sarcoplasmic Proteins Subjected to pH-Shifting Treatments and Lyophilization. Journal of Food Science, 75, C251-C257
Yongsawatdigul J., Park J.W. (2003): Thermal denaturation and aggregation of threadfin bream actomyosin. Food Chemistry, 83, 409-416
Zhang R., Chen J., Jiang V., Yin L., Zhang X. (2016a): Antioxidant and hypoglycaemic effects of tilapia skin collagen peptide in mice. International Journal of Food Science and Technology, 51: 2157–2163.
Zhang C., Zhang N., Li Z., Tian Y., Zhang L., Zheng B. (2016b): Stability of antioxidant peptides prepared from large yellow croaker (Pseudosciaena crocea). Current Topics in Nutraceutical Research, 14: 37–47.
Zhao Tiantian, Xu Jucai, Zhao Hongwei, Jiang Weiwen, Guo Xiaolei, Zhao Mouming, Sun-Waterhouse Dongxiao, Zhao Qiangzhong, Su Guowan (2017): Antioxidant and anti-acetylcholinesterase activities of anchovy ( Coilia mystus ) protein hydrolysates and their memory-improving effects on scopolamine-induced amnesia mice. International Journal of Food Science & Technology, 52, 504-510
Zhu Y.H., Liu R., Wu H., Wang L.C. (2012): Progress of structure—activity relationship of bioactive peptides. China Journal of Traditional Chinese Medicine and Pharmacy, 27: 2625–2628. (in Chinese)
download PDF

© 2019 Czech Academy of Agricultural Sciences