Novel angiotensin I-converting enzyme inhibitory peptides from protease hydrolysates of Qula casein: Quantitative structure-activity relationship modeling and molecular docking study

Journal of Functional Foods

Volumn 32, Issue , 2017, Pages 266-277

  Lin, Kai ^a   Zhang, Lan wei ^a,b   Han, Xue ^a   Cheng, Da you ^a  

^a HARBIN INSTITUTE OF TECHNOLOGY   (China)

^b OCEAN UNIVERSITY OF CHINA   (China)

Author keywords

ACE inhibitory peptides; Chemically synthesis; Enzymatic hydrolysis; Molecular docking; QSAR model; Qula casein

Indexed keywords

EID: 85014738292     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2017.03.008     Document Type: Article

References (61)

1. Alemán, A., Gómez-Guillén, M., Montero, P., Identification of ACE-inhibitory peptides from squid skin collagen after in vitro gastrointestinal digestion. Food Research International 54:1 (2013), 790–795.
2. Asoodeh, A., Yazdi, M.M., Chamani, J., Purification and characterisation of angiotensin I converting enzyme inhibitory peptides from lysozyme hydrolysates. Food Chemistry 131:1 (2012), 291–295.
3. Babij, K., Dąbrowska, A., Szołtysik, M., The evaluation of dipeptidyl peptidase (DPP)-IV, a-Glucosidase and angiotensin converting enzyme (ACE) inhibitory activities of whey proteins hydrolyzed with serine protease isolated from Asian pumpkin (Cucurbita ficifolia). International Journal of Peptide Research and Therapeutics 20 (2014), 483–491.
4. Barbana, C., Boye, J.I., Angiotensin I-converting enzyme inhibitory properties of lentil protein hydrolysates: Determination of the kinetics of inhibition. Food Chemistry 127:1 (2011), 94–101.
5. Corrêa, A.P.F., Daroit, D.J., Coelho, J., Meira, S.M., Lopes, F.C., Segalin, J., Brandelli, A., Antioxidant, antihypertensive and antimicrobial properties of ovine milk caseinate hydrolyzed with a microbial protease. Journal of the Science of Food and Agriculture 91:12 (2011), 2247–2254.
6. Di Bernardini, R., Mullen, A.M., Bolton, D., Kerry, J., O'Neill, E., Hayes, M., 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 Science 90:1 (2012), 226–235.
7. Fu, Y., Young, J.F., Dalsgaard, T.K., Therkildsen, M., 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 50:5 (2015), 1234–1243.
8. Fu, Y., Young, J.F., Løkke, M.M., Lametsch, R., Aluko, R.E., Therkildsen, M., Revalorisation of bovine collagen as a potential precursor of angiotensin I-converting enzyme (ACE) inhibitory peptides based on in silico and in vitro protein digestions. Journal of Functional Foods 24 (2016), 196–206.
9. García-Moreno, P.J., Espejo-Carpio, F.J., Guadix, A., Guadix, E.M., Production and identification of angiotensin I-converting enzyme (ACE) inhibitory peptides from Mediterranean fish discards. Journal of Functional Foods 18 (2015), 95–105.
10. Girgih, A.T., Udenigwe, C.C., Li, H., Adebiyi, A.P., Aluko, R.E., Kinetics of enzyme inhibition and antihypertensive effects of hemp seed (Cannabis sativa L.) protein hydrolysates. Journal of the American Oil Chemists' Society 88:11 (2011), 1767–1774.
11. Gómez-Ruiz, J.Á., Ramos, M., Recio, I., Identification of novel angiotensin-converting enzyme-inhibitory peptides from ovine milk proteins by CE-MS and chromatographic techniques. Electrophoresis 28:22 (2007), 4202–4211.
12. Gu, Y., Majumder, K., Wu, J., QSAR-aided in silico approach in evaluation of food proteins as precursors of ACE inhibitory peptides. Food Research International 44:8 (2011), 2465–2474.
13. Guo, Y., Pan, D., Tanokura, M., Optimisation of hydrolysis conditions for the production of the angiotensin-I converting enzyme (ACE) inhibitory peptides from whey protein using response surface methodology. Food Chemistry 114:1 (2009), 328–333.
14. He, R., Aluko, R.E., Ju, X.R., Evaluating molecular mechanism of hypotensive peptides interactions with renin and angiotensin converting enzyme. PLoS ONE, 9(3), 2014, e91051.
15. Holder, A., Birke, A., Eisele, T., Klaiber, I., Fischer, L., Hinrichs, J., Selective isolation of angiotensin-I-converting enzyme-inhibitory peptides from micellar casein and β-casein hydrolysates via ultrafiltration. International Dairy Journal 31:1 (2013), 34–40.
16. Horwitz, W., & Horwitz, W. (2000). Official methods of analysis of AOAC International.
17. Jiang, J., Chen, S., Ren, F., Luo, Z., Zeng, S.S., Yak milk casein as a functional ingredient: preparation and identification of angiotensin-I-converting enzyme inhibitory peptides. Journal of Dairy Research 74:01 (2007), 18–25.
18. Jiang, Z., Tian, B., Brodkorb, A., Huo, G., Production, analysis and in vivo evaluation of novel angiotensin-I-converting enzyme inhibitory peptides from bovine casein. Food Chemistry 123:3 (2010), 779–786.
19. Kembhavi, A.A., Kulkarni, A., Pant, A., Salt-tolerant and thermostable alkaline protease from Bacillus subtilis NCIM No. 64. Applied Biochemistry and Biotechnology 38:1–2 (1993), 83–92.
20. Khantaphant, S., Benjakul, S., Kishimura, H., Antioxidative and ACE inhibitory activities of protein hydrolysates from the muscle of brownstripe red snapper prepared using pyloric caeca and commercial proteases. Process Biochemistry 46:1 (2011), 318–327.
21. Kleekayai, T., Harnedy, P.A., O'Keeffe, M.B., Poyarkov, A.A., CunhaNeves, A., Suntornsuk, W., FitzGerald, R.J., Extraction of antioxidant and ACE inhibitory peptides from Thai traditional fermented shrimp pastes. Food Chemistry 176 (2015), 441–447.
22. Lau, C.C., Abdullah, N., Shuib, A.S., Aminudin, N., Novel angiotensin I-converting enzyme inhibitory peptides derived from edible mushroom Agaricus bisporus (JE Lange) Imbach identified by LC–MS/MS. Food Chemistry 148 (2014), 396–401.
23. Li, G., Le, G., Shi, Y., Shrestha, S., Angiotensin I–converting enzyme inhibitory peptides derived from food proteins and their physiological and pharmacological effects. Nutrition Research 24:7 (2004), 469–486.
24. Li, H., Ma, Y., Li, Q., Wang, J., Cheng, J., Xue, J., Shi, J., The chemical composition and nitrogen distribution of Chinese yak (Maiwa) milk. International Journal of Molecular Sciences 12:8 (2011), 4885–4895.
25. Lim, C.W., Kim, Y.K., Yeun, S.m., Lee, M.H., Moon, H.S., Yoon, N.Y., Lee, D.S., Purification and characterization of angiotensin-1 converting enzyme (ACE)-inhibitory peptide from the jellyfish, Nemopilema nomurai. African Journal of Biotechnology 12:15 (2013), 1888–1893.
26. Luna-Vital, D.A., de Mejía, E.G., Mendoza, S., Loarca-Piña, G., Peptides present in the non-digestible fraction of common beans (Phaseolus vulgaris L.) inhibit the angiotensin-I converting enzyme by interacting with its catalytic cavity independent of their antioxidant capacity. Food & Function 6:5 (2015), 1470–1479.
27. Miguel, M., Contreras, M., Recio, I., Aleixandre, A., ACE-inhibitory and antihypertensive properties of a bovine casein hydrolysate. Food Chemistry 112:1 (2009), 211–214.
28. Murray, B., FitzGerald, R., Angiotensin converting enzyme inhibitory peptides derived from food proteins: Biochemistry, bioactivity and production. Current Pharmaceutical Design 13:8 (2007), 773–791.
29. Nagai, T., Nagashima, T., Abe, A., Suzuki, N., Antioxidative activities and angiotensin I-converting enzyme inhibition of extracts prepared from chum salmon (Oncorhynchus keta) cartilage and skin. International Journal of Food Properties 9:4 (2006), 813–822.
30. Nongonierma, A., Fitzgerald, D., Learnings from quantitative structure activity relationship (QSAR) studies with respect to food protein-derived bioactive peptides: A review. RSC Advances 6 (2016), 75400–75413.
31. Norris, R., Poyarkov, A., O'Keeffe, M.B., FitzGerald, R.J., Characterisation of the hydrolytic specificity of Aspergillus niger derived prolyl endoproteinase on bovine β-casein and determination of ACE inhibitory activity. Food Chemistry 156 (2014), 29–36.
32. Onuh, J.O., Girgih, A.T., Aluko, R.E., Aliani, M., Inhibitions of renin and angiotensin converting enzyme activities by enzymatic chicken skin protein hydrolysates. Food Research International 53:1 (2013), 260–267.
33. Pan, D., Cao, J., Guo, H., Zhao, B., Studies on purification and the molecular mechanism of a novel ACE inhibitory peptide from whey protein hydrolysate. Food Chemistry 130:1 (2012), 121–126.
34. Pihlanto, A., Virtanen, T., Korhonen, H., Angiotensin I converting enzyme (ACE) inhibitory activity and antihypertensive effect of fermented milk. International Dairy Journal 20:1 (2010), 3–10.
35. Pihlanto-Leppälä, A., Bioactive peptides derived from bovine whey proteins: Opioid and ace-inhibitory peptides. Trends in Food Science & Technology 11:9 (2000), 347–356.
36. Pralea, D., Dumitrascu, L., Borda, D., Stănciuc, N., Functional properties of sodium caseinate hydrolysates as affected by the extent of chymotrypsinolysis. Journal of Agroalimentary Processes and Technologies 17:3 (2011), 308–314.
37. Quirós, A., Ramos, M., Muguerza, B., Delgado, M.A., Miguel, M., Aleixandre, A., Recio, I., Identification of novel antihypertensive peptides in milk fermented with Enterococcus faecalis. International Dairy Journal 17:1 (2007), 33–41.
38. Rao, S., Sun, J., Liu, Y., Zeng, H., Su, Y., Yang, Y., ACE inhibitory peptides and antioxidant peptides derived from in vitro digestion hydrolysate of hen egg white lysozyme. Food Chemistry 135:3 (2012), 1245–1252.
39. Rohit, A., Sathisha, K., Aparna, H., A variant peptide of buffalo colostrum β-lactoglobulin inhibits angiotensin I-converting enzyme activity. European Journal of Medicinal Chemistry 53 (2012), 211–219.
40. Rojas-Ronquillo, R., Cruz-Guerrero, A., Flores-Nájera, A., Rodríguez-Serrano, G., Gómez-Ruiz, L., Reyes-Grajeda, J.P., García-Garibay, M., Antithrombotic and angiotensin-converting enzyme inhibitory properties of peptides released from bovine casein by Lactobacillus casei Shirota. International Dairy Journal 26:2 (2012), 147–154.
41. Rui, X., Boye, J.I., Simpson, B.K., Prasher, S.O., Angiotensin I-converting enzyme inhibitory properties of Phaseolus vulgaris bean hydrolysates: Effects of different thermal and enzymatic digestion treatments. Food Research International 49:2 (2012), 739–746.
42. Schägger, H., Tricine–SDS-PAGE. Nature Protocols 1 (2006), 16–22.
43. Shanmugam, V., Kapila, S., Sonfack, T.K., Kapila, R., Antioxidative peptide derived from enzymatic digestion of buffalo casein. International Dairy Journal 42 (2015), 1–5.
44. Shen, H.Y., Tian, G.L., Ye, Y.H., Wang, J.B., Non-coded amino acids as acyl donor substrates for peptide bond formation catalyzed by thermoase in toluene. Journal of Molecular Catalysis B: Enzymatic 37:1 (2005), 26–29.
45. Sheng, Q., Li, J., Alam, M.S., Fang, X., Guo, M., Gross composition and nutrient profiles of Chinese yak (Maiwa) milk. International Journal of Food Science & Technology 43:3 (2008), 568–572.
46. Silva-Sánchez, C., De La Rosa, A.B., León-Galván, M., De Lumen, B., de León-Rodríguez, A., de Mejía, E.G., Bioactive peptides in amaranth (Amaranthus hypochondriacus) seed. Journal of Agricultural and Food Chemistry 56:4 (2008), 1233–1240.
47. Spellman, D., McEvoy, E., O'cuinn, G., FitzGerald, R., Proteinase and exopeptidase hydrolysis of whey protein: Comparison of the TNBS, OPA and pH stat methods for quantification of degree of hydrolysis. International Dairy Journal 13:6 (2003), 447–453.
48. Stokes, J., Kannel, W.B., Wolf, P.A., D'Agostino, R.B., Cupples, L.A., Blood pressure as a risk factor for cardiovascular disease. The Framingham Study-30 years of follow-up. Hypertension, 13(5 Suppl), 1989, I13, 10.1161/01.HYP.13.5_Suppl.I13.
49. Tomatsu, M., Shimakage, A., Shinbo, M., Yamada, S., Takahashi, S., Novel angiotensin I-converting enzyme inhibitory peptides derived from soya milk. Food Chemistry 136:2 (2013), 612–616.
50. Udenigwe, C.C., Bioinformatics approaches, prospects and challenges of food bioactive peptide research. Trends in Food Science & Technology 36:2 (2014), 137–143.
51. Wang, X., Chen, H., Fu, X., Li, S., Wei, J., A novel antioxidant and ACE inhibitory peptide from rice bran protein: Biochemical characterization and molecular docking study. LWT-Food Science and Technology 75 (2017), 93–99.
52. Webb, A.J., Fischer, U., Mehta, Z., Rothwell, P.M., Effects of antihypertensive-drug class on interindividual variation in blood pressure and risk of stroke: A systematic review and meta-analysis. The Lancet 375:9718 (2010), 906–915.
53. White, B.L., Sanders, T.H., Davis, J.P., Potential ACE-inhibitory activity and nanoLC-MS/MS sequencing of peptides derived from aflatoxin contaminated peanut meal. LWT - Food Science and Technology 56:2 (2014), 537–542.
54. Wold, S., Sjöström, M., Eriksson, L., PLS-regression: A basic tool of chemometrics. Chemometrics and Intelligent Laboratory Systems 58:2 (2001), 109–130.
55. Wu, J., Aluko, R.E., Nakai, S., Structural requirements of angiotensin I-converting enzyme inhibitory peptides: quantitative structure-activity relationship modeling of peptides containing 4–10 amino acid residues. QSAR & Combinatorial Science 25:10 (2006), 873–880.
56. Wu, Q., Cai, Q., Tao, Z., Sun, L., Shen, J., Zhang, L., Cao, M., Purification and characterization of a novel angiotensin I-converting enzyme inhibitory peptide derived from abalone (Haliotis discus hannai Ino) gonads. European Food Research and Technology 240:1 (2015), 137–145.
57. Wu, J., Ding, X., Characterization of inhibition and stability of soy-protein-derived angiotensin I-converting enzyme inhibitory peptides. Food Research International 35:4 (2002), 367–375.
58. Wu, Q., Jia, J., Yan, H., Du, J., Gui, Z., A novel angiotensin-I converting enzyme (ACE) inhibitory peptide from gastrointestinal protease hydrolysate of silkworm pupa (Bombyx mori) protein: Biochemical characterization and molecular docking study. Peptides 68 (2015), 17–24.
59. Wu, H., Xu, N., Sun, X., Yu, H., Zhou, C., Hydrolysis and purification of ACE inhibitory peptides from the marine microalga Isochrysis galbana. Journal of Applied Phycology 27:1 (2015), 351–361.
60. Zarei, M., Forghani, B., Ebrahimpour, A., Abdul-Hamid, A., Anwar, F., Saari, N., In vitro and in vivo antihypertensive activity of palm kernel cake protein hydrolysates: Sequencing and characterization of potent bioactive. Industrial Crops and Products 76 (2015), 112–120.
61. Zhang, Y., Olsen, K., Grossi, A., Otte, J., Effect of pretreatment on enzymatic hydrolysis of bovine collagen and formation of ACE-inhibitory peptides. Food Chemistry 141:3 (2013), 2343–2354.