Preparation, Characterization, and Cytoprotective Effects on HUVECs of Fourteen Novel Angiotensin-I-Converting Enzyme Inhibitory Peptides From Protein Hydrolysate of Tuna Processing By-Products

To effectively utilize skipjack tuna (Katsuwonus pelamis) processing by-products to prepare peptides with high angiotensin-I-converting enzyme (ACE) inhibitory (ACEi) activity, Neutrase was selected from five kinds of protease for hydrolyzing skipjack tuna dark muscle, and its best hydrolysis conditions were optimized as enzyme dose of 1.6%, pH 6.7, and temperature of 50°C using single factor and response surface experiments. Subsequently, 14 novel ACEi peptides were prepared from the high ACEi protein hydrolysate and identified as TE, AG, MWN, MEKS, VK, MQR, MKKS, VKRT, IPK, YNY, LPRS, FEK, IRR, and WERGE. MWN, MEKS, MKKS, and LPRS displayed significantly ACEi activity with IC50 values of 0.328 ± 0.035, 0.527 ± 0.030, 0.269 ± 0.006, and 0.495 ± 0.024 mg/mL, respectively. Furthermore, LPRS showed the highest increasing ability on nitric oxide (NO) production among four ACEi peptides combining the direct increase and reversing the negative influence of norepinephrine (NE), and MKKS showed the highest ability on directly decreasing and reversing the side effects of NE on the secretion level of endothelin-1 (ET-1) among four ACEi peptides. These findings demonstrate that seafood by-product proteins are potential ACEi peptide sources and prepared ACEi peptides from skipjack tuna dark muscle, which are beneficial components for functional food against hypertension and cardiovascular diseases.

[1]  Bin Wang,et al.  Preparation, Identification, Molecular Docking Study and Protective Function on HUVECs of Novel ACE Inhibitory Peptides from Protein Hydrolysate of Skipjack Tuna Muscle , 2022, Marine drugs.

[2]  Bin Wang,et al.  Antioxidant peptides from protein hydrolysate of skipjack tuna milt: Purification, identification, and cytoprotection on H2O2 damaged human umbilical vein endothelial cells , 2022, Process Biochemistry.

[3]  Xiang Liu,et al.  Association of morning hypertension with chronic kidney disease progression and cardiovascular events in patients with chronic kidney disease and hypertension. , 2022, Nutrition, metabolism, and cardiovascular diseases : NMCD.

[4]  Bin Wang,et al.  Twelve Antioxidant Peptides From Protein Hydrolysate of Skipjack Tuna (Katsuwonus pelamis) Roe Prepared by Flavourzyme: Purification, Sequence Identification, and Activity Evaluation , 2022, Frontiers in Nutrition.

[5]  Yu Sun,et al.  A Solution for Sustainable Utilization of Aquaculture Waste: A Comprehensive Review of Biofloc Technology and Aquamimicry , 2022, Frontiers in Nutrition.

[6]  S. Benjakul,et al.  Comparative Study of Astaxanthin, Cholesterol, Fatty Acid Profiles, and Quality Indices Between Shrimp Oil Extracted From Hepatopancreas and Cephalothorax , 2021, Frontiers in Nutrition.

[7]  Yuting Lu,et al.  Separation and identification of ACE inhibitory peptides from lizard fish proteins hydrolysates by metal affinity-immobilized magnetic liposome. , 2021, Protein expression and purification.

[8]  Susan García Fillería,et al.  Antioxidant and angiotensin I-converting enzyme (ACE) inhibitory peptides of rainbow trout (Oncorhynchus mykiss) viscera hydrolysates subjected to simulated gastrointestinal digestion and intestinal absorption , 2021, LWT.

[9]  Yue-Zhen Wang,et al.  Antioxidant peptides from Antarctic Krill (Euphausia superba) hydrolysate: Preparation, identification and cytoprotection on H2O2-induced oxidative stress , 2021 .

[10]  Bahar Tokur,et al.  Optimization of hydrolysis conditions for the production of protein hydrolysates from fish wastes using response surface methodology , 2021, Food Bioscience.

[11]  J. Beltrán,et al.  Innovative Development of Pasta with the Addition of Fish By-Products from Two Species , 2021, Foods.

[12]  W. Jin,et al.  Anti-inflammatory and Antioxidant Activity of Peptides From Ethanol-Soluble Hydrolysates of Sturgeon (Acipenser schrenckii) Cartilage , 2021, Frontiers in Nutrition.

[13]  N. Bandarra,et al.  Characterization of Protein Hydrolysates from Fish Discards and By-Products from the North-West Spain Fishing Fleet as Potential Sources of Bioactive Peptides , 2021, Marine drugs.

[14]  D. Pan,et al.  Angiotensin I-Converting enzyme (ACE) inhibitory and dipeptidyl Peptidase-4 (DPP-Ⅳ) inhibitory activity of umami peptides from Ruditapes philippinarum , 2021 .

[15]  D. Pan,et al.  Novel Umami Peptide IPIPATKT with Dual Dipeptidyl Peptidase-IV and Angiotensin I-Converting Enzyme Inhibitory Activities. , 2021, Journal of agricultural and food chemistry.

[16]  Mouming Zhao,et al.  Identification of post-digestion angiotensin-I converting enzyme (ACE) inhibitory peptides from soybean protein Isolate: Their production conditions and in silico molecular docking with ACE. , 2020, Food chemistry.

[17]  Ila Joshi,et al.  Isolation and characterization of angiotensin I-converting enzyme (ACE-I) inhibition and antioxidant peptide from by-catch shrimp (Oratosquilla woodmasoni) waste , 2020 .

[18]  Kai Lin,et al.  ACE inhibitory peptide KYIPIQ derived from yak milk casein induces nitric oxide production in HUVECs and diffuses via a transcellular mechanism in Caco-2 monolayers , 2020 .

[19]  Bin Wang,et al.  Antioxidant Peptides from Collagen Hydrolysate of Redlip Croaker (Pseudosciaena polyactis) Scales: Preparation, Characterization, and Cytoprotective Effects on H2O2-Damaged HepG2 Cells , 2020, Marine drugs.

[20]  Bin Wang,et al.  Antioxidant Peptides from the Protein Hydrolysate of Monkfish (Lophius litulon) Muscle: Purification, Identification, and Cytoprotective Function on HepG2 Cells Damage by H2O2 , 2020, Marine drugs.

[21]  E. Ferrer,et al.  Aquaculture and its by-products as a source of nutrients and bioactive compounds. , 2020, Advances in food and nutrition research.

[22]  Bin Wang,et al.  Cytoprotective Effect of Antioxidant Pentapeptides from the Protein Hydrolysate of Swim Bladders of Miiuy Croaker (Miichthys miiuy) against H2O2-Mediated Human Umbilical Vein Endothelial Cell (HUVEC) Injury , 2019, International journal of molecular sciences.

[23]  L. Bazinet,et al.  Antihypertensive and Angiotensin-I-Converting Enzyme (ACE)-Inhibitory Peptides from Fish as Potential Cardioprotective Compounds , 2019, Marine drugs.

[24]  Bin Wang,et al.  Gelatin and Antioxidant Peptides from Gelatin Hydrolysate of Skipjack Tuna (Katsuwonus pelamis) Scales: Preparation, Identification and Activity Evaluation , 2019, Marine drugs.

[25]  Bin Wang,et al.  Antioxidant Peptides from the Protein Hydrolysate of Spanish Mackerel (Scomberomorous niphonius) Muscle by in Vitro Gastrointestinal Digestion and Their In Vitro Activities , 2019, Marine drugs.

[26]  Bin Wang,et al.  Identification and Active Evaluation of Antioxidant Peptides from Protein Hydrolysates of Skipjack Tuna (Katsuwonus pelamis) Head , 2019, Antioxidants.

[27]  Bin Wang,et al.  Eight antihypertensive peptides from the protein hydrolysate of Antarctic krill (Euphausia superba): Isolation, identification, and activity evaluation on human umbilical vein endothelial cells (HUVECs). , 2019, Food research international.

[28]  W. Kuo,et al.  Bioactive Peptide VHVV Upregulates the Long-Term Memory-Related Biomarkers in Adult Spontaneously Hypertensive Rats , 2019, International journal of molecular sciences.

[29]  M. Nasri,et al.  Basic and recent advances in marine antihypertensive peptides: Production, structure-activity relationship and bioavailability , 2019, Trends in Food Science & Technology.

[30]  C. Tan,et al.  Identification, structure-activity relationship and in silico molecular docking analyses of five novel angiotensin I-converting enzyme (ACE)-inhibitory peptides from stone fish (Actinopyga lecanora) hydrolysates , 2019, PloS one.

[31]  Bin Wang,et al.  Ten new pentapeptides from protein hydrolysate of miiuy croaker (Miichthys miiuy) muscle: Preparation, identification, and antioxidant activity evaluation , 2019, LWT.

[32]  Bin Wang,et al.  Purification and Characterization of Antioxidant Peptides Derived from Protein Hydrolysate of the Marine Bivalve Mollusk Tergillarca granosa , 2019, Marine drugs.

[33]  C. Lammi,et al.  Multifunctional peptides for the prevention of cardiovascular disease: A new concept in the area of bioactive food-derived peptides , 2019, Journal of Functional Foods.

[34]  Bin Wang,et al.  Preparation and Characterization of Gelatin and Antioxidant Peptides from Gelatin Hydrolysate of Skipjack Tuna (Katsuwonus pelamis) Bone Stimulated by in vitro Gastrointestinal Digestion , 2019, Marine drugs.

[35]  Jianping Wu,et al.  Molecular interactions, bioavailability, and cellular mechanisms of angiotensin-converting enzyme inhibitory peptides. , 2018, Journal of food biochemistry.

[36]  Zhuangwei Zhang,et al.  Identification and Molecular Docking Study of a Novel Angiotensin-I Converting Enzyme Inhibitory Peptide Derived from Enzymatic Hydrolysates of Cyclina sinensis , 2018, Marine drugs.

[37]  Bin Wang,et al.  Preparation, identification, and activity evaluation of ten antioxidant peptides from protein hydrolysate of swim bladders of miiuy croaker (Miichthys miiuy) , 2018, Journal of Functional Foods.

[38]  Y. Liu,et al.  Processing Optimization and Characterization of Angiotensin-Ι-Converting Enzyme Inhibitory Peptides from Lizardfish (Synodus macrops) Scale Gelatin , 2018 .

[39]  In Seong Yoon,et al.  Chemical composition and functional properties of roe concentrates from skipjack tuna (Katsuwonus pelamis) by cook‐dried process , 2018, Food science & nutrition.

[40]  F. Shahidi,et al.  Protein hydrolysate from turkey meat and optimization of its antioxidant potential by response surface methodology , 2018, Poultry science.

[41]  Adem Gharsallaoui,et al.  Peptides from Fish By-product Protein Hydrolysates and Its Functional Properties: an Overview , 2018, Marine Biotechnology.

[42]  Fidel Toldrá,et al.  In silico analysis and molecular docking study of angiotensin I-converting enzyme inhibitory peptides from smooth-hound viscera protein hydrolysates fractionated by ultrafiltration. , 2018, Food chemistry.

[43]  Munehiro Yoshida,et al.  Dietary Tuna Dark Muscle Protein Attenuates Hepatic Steatosis and Increases Serum High-Density Lipoprotein Cholesterol in Obese Type-2 Diabetic/Obese KK-Ay Mice. , 2017, Journal of food science.

[44]  P. Gatta state of world fisheries and aquaculture , 2017 .

[45]  J. Yongsawatdigul,et al.  Angiotensin converting enzyme (ACE) inhibitory peptides derived from the simulated in vitro gastrointestinal digestion of cooked chicken breast , 2017 .

[46]  Z. Tong,et al.  Separation and Characterization of Angiotensin I Converting Enzyme (ACE) Inhibitory Peptides from Saurida elongata Proteins Hydrolysate by IMAC-Ni2+ , 2017, Marine drugs.

[47]  Yajun Zheng,et al.  Purification, characterization, synthesis, in vitro ACE inhibition and in vivo antihypertensive activity of bioactive peptides derived from oil palm kernel glutelin-2 hydrolysates , 2017 .

[48]  Haixia Chen,et al.  A novel antioxidant and ACE inhibitory peptide from rice bran protein: Biochemical characterization and molecular docking study , 2017 .

[49]  P. Montero,et al.  Enhancement of ACE and prolyl oligopeptidase inhibitory potency of protein hydrolysates from sardine and tuna by-products by simulated gastrointestinal digestion. , 2016, Food & function.

[50]  Sun Joo Park,et al.  Angiotensin I-converting enzyme inhibitory peptides from an enzymatic hydrolysate of flounder fish (Paralichthys olivaceus) muscle as a potent anti-hypertensive agent , 2016 .

[51]  A. Sila,et al.  Antioxidant peptides from marine by-products: Isolation, identification and application in food systems. A review , 2016 .

[52]  S. Deng,et al.  Purification and identification of three novel antioxidant peptides from protein hydrolysate of bluefin leatherjacket (Navodon septentrionalis) skin , 2015 .

[53]  Li Tao,et al.  Antioxidant and anticancer peptides from the protein hydrolysate of blood clam (Tegillarca granosa) muscle , 2015 .

[54]  Eun-Young Kim,et al.  Peptide derived from desalinated boiled tuna extract inhibits adipogenesis through the downregulation of C/EBP-α and PPAR-γ in 3T3-L1 adipocytes. , 2015, International journal of molecular medicine.

[55]  Won‐Kyo Jung,et al.  Angiotensin-I converting enzyme inhibitory peptides from antihypertensive skate (Okamejei kenojei) skin gelatin hydrolysate in spontaneously hypertensive rats. , 2015, Food chemistry.

[56]  Bin Wang,et al.  Influence of Amino Acid Compositions and Peptide Profiles on Antioxidant Capacities of Two Protein Hydrolysates from Skipjack Tuna (Katsuwonus pelamis) Dark Muscle , 2015, Marine drugs.

[57]  S. Deng,et al.  Isolation and characterization of three antioxidant peptides from protein hydrolysate of bluefin leatherjacket (Navodon septentrionalis) heads , 2015 .

[58]  Bin Wang,et al.  Characterization of acid-and pepsin-soluble collagens from spines and skulls of skipjack tuna (Katsuwonus pelamis). , 2014, Chinese journal of natural medicines.

[59]  P. T. Lakshmanan,et al.  Isolation and characterization of gelatin from the skins of skipjack tuna (Katsuwonus pelamis), dog shark (Scoliodon sorrakowah), and rohu (Labeo rohita) , 2014 .

[60]  C. Barry‐Ryan,et al.  Structure elucidation of ACE-inhibitory and antithrombotic peptides isolated from mackerel skin gelatine hydrolysates. , 2014, Journal of the science of food and agriculture.

[61]  Dai-Hung Ngo,et al.  Active peptides from skate (Okamejei kenojei) skin gelatin diminish angiotensin-I converting enzyme activity and intracellular free radical-mediated oxidation. , 2014, Food chemistry.

[62]  S. Deng,et al.  Isolation and characterization of three antioxidant pentapeptides from protein hydrolysate of monkfish (Lophius litulon) muscle , 2014 .

[63]  S. Deng,et al.  Isolation and Characterization of Collagen and Antioxidant Collagen Peptides from Scales of Croceine Croaker (Pseudosciaena crocea) , 2013, Marine drugs.

[64]  Bin Wang,et al.  Purification and characterisation of a novel antioxidant peptide derived from blue mussel (Mytilus edulis) protein hydrolysate. , 2013, Food chemistry.

[65]  Bin Wang,et al.  Isolation and characterization of acid soluble collagens and pepsin soluble collagens from the skin and bone of Spanish mackerel (Scomberomorous niphonius) , 2013 .

[66]  J. Chamani,et al.  Identification of a novel angiotensin-I converting enzyme inhibitory peptide from ostrich egg white and studying its interactions with the enzyme , 2013 .

[67]  Xiaoe Chen,et al.  Optimization of antioxidant hydrolysate production from flying squid muscle protein using response surface methodology , 2012 .

[68]  Se-kwon Kim,et al.  A novel angiotensin I converting enzyme inhibitory peptide from tuna frame protein hydrolysate and its antihypertensive effect in spontaneously hypertensive rats , 2010 .

[69]  S. Klomklao,et al.  Biochemical properties of two isoforms of trypsin purified from the intestine of skipjack tuna (Katsuwonus pelamis). , 2009 .

[70]  P. Mahadevan,et al.  An overview , 2007, Journal of Biosciences.

[71]  Se-Kwon Kim,et al.  Bioactive compounds from marine processing byproducts – A review , 2006 .

[72]  M. Pasdar,et al.  Design, synthesis, and anticancer activity of phosphonic acid diphosphate derivative of adenine-containing butenolide and its water-soluble derivatives of paclitaxel with high antitumor activity. , 2003, Bioorganic & medicinal chemistry.

[73]  M. Alaiz,et al.  Production of ace inhibitory peptides by digestion of chickpea legumin with alcalase , 2003 .