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ORIGINAL ARTICLE
In Vitro Characterization of Fluted Pumpkin Leaf Protein Hydrolysates and Ultrafiltration of Peptide Fractions: Antioxidant and Enzyme-Inhibitory Properties
| 1 | Department of Food and Human Nutritional Sciences, University of Manitoba, R3T 2N2 Winnipeg, Canada |
| 2 | Department of Food Science & Technology, Obafemi Awolowo University, 220002 Ile-Ife, Nigeria |
| 3 | Department of Soil and Land Resources Management, Faculty of Agriculture, Obafemi Awolowo University, 220002 Ile-Ife, Nigeria |
| 4 | Department of Agronomy, Faculty of Agriculture, Obafemi Awolowo University, 220002 Ile-Ife, Nigeria |
CORRESPONDING AUTHOR
Akinsola Albert Famuwagun
Food Science and Technology, Obafemi Awolowo University, 2200055, Ile-Ife, Nigeria
Food Science and Technology, Obafemi Awolowo University, 2200055, Ile-Ife, Nigeria
Submission date: 2020-08-25
Final revision date: 2020-11-10
Acceptance date: 2020-11-12
Online publication date: 2020-12-09
Publication date: 2020-12-09
Pol. J. Food Nutr. Sci. 2020;70(4):429–443
KEYWORDS
fluted pumpkin leafprotein hydrolysatesmembrane ultrafiltrationantioxidant activityantidiabetic activityantihypertensive activity
TOPICS
SpectrometryAmino acids/Minerals AvailabilityFood bioactivesNutraceuticalsBioactive peptidesChemical and enzymatic modificationInteractions
ABSTRACT
Hydrolysates were produced using Alcalase (AH), chymotrypsin (CH), pepsin (PH), and trypsin (TH), and also fluted pumpkin leaf protein isolate (FLI) as a substrate. AH had the lowest degree of hydrolysis (16.37%) but exhibited overall superior antioxidant and enzyme inhibitory properties. Therefore, it was fractionated by membrane ultrafiltration to give <1, 1-3, 3-5, 5-10, and >10 kDa peptide fractions. Gel permeation chromatography showed that the molecular weight of the FLI was 19.77 kDa and that of the hydrolysates was below 7.5 kDa. The hydrolysate peptides had a high content of hydrophobic amino acids but low levels of sulfur-containing amino acids, when compared to protein of FLI. Peptide sequence analysis showed that the hydrolysates consisted of dipeptides, tripeptides, and tetrapeptides with molecular weights below 500 Da. The hydrolysates were also stronger inhibitors of linoleic acid oxidation, α-amylase, α-glucosidase, and angiotensin converting enzyme (ACE) than FLI. Among the fractions, the <1 and 1-3 kDa were the most effective free radical scavengers and metal chelators in addition to their strong inhibitory activities against α-amylase, α-glucosidase, and ACE. We conclude that the AH and low molecular weight peptide fraction (<3 kDa) could find applications in formulating foods with various bioactive properties.
FUNDING
This research was supported by the International Development Research Centre and Global Affairs Canada through the Canadian International Food Security Research Fund, Project 107983 on synergizing indigenous vegetables and fertilizer micro-dosing innovations among West African farmers.
REFERENCES (70)
1.
Ajibola, C.F., Fashakin, J.B., Fagbemi, T.N., Aluko, R.E. (2011). Effect of peptide size on antioxidant properties of african yam bean seed (Sphenostylis stenocarpa) protein hydrolysate fractions. International Journal of Molecular Sciences, 12, 6685-6702.
2.
Alashi, A.M., Blanchard, C.L., Mailer, R.J., Agboola, S.O., Mawson, A.J., Rong, H., Malomo, S.A., Girgih, A.T., Aluko, R.E. (2014). Blood pressure lowering effects of Australian canola protein hydrolysates in spontaneously hypertensive rats. Food Research International, 55, 281–287.
3.
Aletor, O., Oshodi, A.A., Ipinmoroti, K. (2002). Chemical composition of common leafy vegetables and functional properties of their leaf protein concentrates. Food Chemistry, 78(1), 63-68.
4.
Aluko, R.E. (2015). Antihypertensive peptides from food proteins. Annual Review of Food Science and Technology, 6(1), 235-262.
5.
Arise, R.O., Yekeen, A., Ekun, O. (2016). In-vitro antioxidant and α-amylase inhibitory properties of watermelon seed protein hydrolysates. Environmental and Experimental Biology, 14(4), 163–172.
6.
Awosika, T.O., Aluko, R.E. (2019). Inhibition of the in vitro activities of α-amylase, α-glucosidase and pancreatic lipase by yellow field pea (Pisum sativum L.) protein hydrolysates. International Journal of Food Science and Technology, 54(6), 2021-2034.
7.
Benzie, I.F.F., Strain, J.J. (1996). Ferric reducing ability of plasma (FRAP) as a measure of antioxidant power: The FRAP assay. Analytical Biochemistry, 239(1), 70-76.
8.
Bleakley, S., Hayes, M., O’Shea, N., Gallagher, E., Lafarga, T. (2017). Predicted release and analysis of novel ACE‐I, renin, and DPP‐IV inhibitory peptides from common oat (Avena sativa) protein hydrolysates using in silico analysis. Foods, 6(12), art. no. 108.
9.
Boschin, G., Scigliuolo, G.M., Resta, D., Arnoldi, A. (2014). ACE-inhibitory activity of enzymatic protein hydrolysates from lupin and other legumes. Food Chemistry, 145, 34–40.
10.
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 Chemistry, 114(4), 1198–1205.
11.
Cao, W., Zhang, W.C., Hong, P., Ji, H., Hao, J. (2010). Purification and identification of an ACE inhibitory peptide from the peptic hydrolysate of Acetes chinensis and its antihypertensive effects in spontaneously hypertensive rats. International Journal of Food Science and Technology, 45(5), 959-965.
12.
Chalamaiah, M., Yu, W., Wu, J. (2018). Immunomodulatory and anticancer protein hydrolysates(peptides) from food proteins: a review. Food Chemistry, 245, 205–222.
13.
Charoenphun, N., Cheirsilp, B., Sirinupong, N. (2013). Calcium binding peptides derived from tilapia (Oreochromis niloticus) protein hydrolysates. European Food Research Technology, 236, 57-63.
14.
Chen, C., Chi, Y.J., Zhao, M.Y., Lv, L. (2012). Purification and identification of antioxidant peptides from egg whiteprotein hydrolysate. Amino Acids, 43, 457–466.
15.
Dhanda, S., Singh, H., Singh, J., Singh, T.P. (2008) Functional characterization and specific effects of various peptides on enzymatic activity of a DPP-III homologue from goat brain. Journal of Enzyme Inhibition and Medicinal Chemistry, 23(2), 174-181.
16.
Dorman, H.J.D., Peltoketo, A., Hiltunen, R., Tikkanen, M.J. (2003). Characterization of the antioxidant properties of deodorised aqueous extracts from selected Lamiaceae herbs. Food Chemistry, 83(2), 255–262.
17.
Elias, R.J., Kellerby, S.S., Decker, E.A. (2008). Antioxidant activity of proteins and peptides. Critical Reviews in Food Science and Nutrition, 48(5), 430-441.
18.
Famuwagun, A.A., Alashi, A.M., Gbadamosi, S.O., Taiwo, K.A., Oyedele, D.J., Adebooye, O.C., Aluko, R.E. (2020). Comparative study of the structural and functional properties of protein isolates prepared from edible vegetable leaves. International Journal of Food Properties, 23(1), 955-970.
19.
Filho, J.G., Rodrigues, J.M., Valadares, A.C.F., de Almeida, A.B., Valencia Mejia, E., Fernandes, K.F., Lemes, A.C., Alves, C.C.F., Sousa, H.A.F., da Silva, E.R., Egea, M.B., Dyszy, F.H. (2020). Bioactive properties of protein hydrolysate of cottonseed byproduct: Antioxidant, antimicrobial, and angiotensin converting enzyme (ACE) inhibitory. Waste and Biomass Valorization, 2020.
20.
Gbadamosi, S.O., Famuwagun, A.A. (2016). Studies on the proximate, functional and antioxidant properties of fermented and unfermented Kariya (Hildergardia barterii) seed protein hydrolysates obtained by enzymatic hydrolysis. British Journal of Biotechnology, 14, 1-14.
21.
Geng, X., Tian, G., Zhang, W., Zhao, Y., Zhao, L., Wang, H., Ng, T.B. (2016). A tricholoma matsutake peptide with angiotensin converting enzyme inhibitory and antioxidative activities and antihypertensive effects in spontaneously hypertensive rats. Scientific Reports, 6, art. no. 24130.
22.
Girgih, A., Udenigwe, C., Li, H., Adebiyi, A., Aluko, R. (2011). Kinetics of enzyme inhibition and antihypertensive effects of hemp seed (Cannabis sativa L.) protein hydrolysates. Journal of the American Oil Chemists’ Society, 88(11), 1767–1774.
23.
Gong, K., Deng, L., Shi, A., Liu, H., Liu, L., Hu, H., Adhikari, B., Wang, Q. (2017). High‐pressure microfluidisation pretreatment disaggregates peanut protein isolates to prepare antihypertensive peptide fractions. International Journal of Food Science and Technology, 52(8), 1760–1769.
24.
Habtamu, A.M., Abdalbasit, A., Gasmalla, R.Y., Wei, Z. (2019). Evaluation of the in vitro α-amylase enzyme inhibition potential of commercial dried Laver (Porphyra Species) Seaweed protein hydrolysate. Turkish Journal of Fisheries and Aquatic Sciences, 18(4), 547-556.
25.
He, R., Girgih, A.T., Malomo, S.A., Ju, X., Aluko, R.E. (2013). Antioxidant activities of enzymatic rapeseed protein hydrolysates and the membrane ultrafiltration fractions. Journal of Functional Foods, 5, 219–227.
26.
Horton, H.R., Moran, L.A., Ochs, R.S., Rawn, J.D., Scrimgeour, K.G. (2002c). Properties of Enzymes. In Principles of Biochemistry.3rd Edition. Prentice Education, NJ, pp. 242-244.
27.
Jamdar, S.N., Rajalakshmi, V., Sharma, A. (2012). Antioxidant and ACE inhibitory properties of poultry viscera protein hydrolysate and its peptide fractions. Journal of Food Biochemistry, 36(4), 494–501.
28.
Jia, X., Ding, C., Dong, L., Yuan, S., Zhang, Z., Chen, Y., Yuan, M. (2013). Comparison of the chemical and functional properties of protein hydrolysates from different mature degree hawk teas. Journal of Food and Nutrition Research, 1(6), 138-144.
29.
Kim, S.R., Byun, H.G. (2012). The novel angiotensin I converting enzyme inhibitory peptides from rainbow trout muscle hydrolysate. Fisheries and Aquatic Sciences, 15(3), 183-190.
30.
Kim, Y.M., Wang, M.H., Rhee, H.I. (2004). A novel alpha glucosidase inhibitor from pine bark. Carbohydrate Research, 339, 715–727.
31.
Koopman, R., Crombach, N., Gijsen, A.P., Walrand, S., Fauquant, J., Kies A.K., van Loon, L.J.C. (2009). Ingestion of a protein hydrolysate is accompanied by an accelerated in vivo digestion and absorption rate when compared with its intact protein. American Journal of Clinical Nutrition, 90(1), 106–115.
32.
Kwon, Y., Apostolidis, E., Shetty, K. (2008). Inhibitory potential of wine and tea against alpha amylase and alpha glucosidase for management of hypertensive linked to type 2 diabetes. Journal of Food Biochemistry, 32(1), 15-31.
33.
Lacroix, I.M.E., Li-Chan, E.C.Y. (2012). Evaluation of the potential of dietary proteins as precursors of dipeptidyl peptidase (DPP)-IV inhibitors by an in-silico approach. Journal of Functional Foods, 4(2), 403–422.
34.
Li, Y., Jiang, B., Zhang, T., Mu, W., Liu, J. (2008). Antioxidant and free radical scavenging activities of chickpea protein hydrolysate (CPH). Food Chemistry, 106(2), 444–450.
35.
Malomo S.A., He, R., Aluko, R.E. (2014). Structural and functional properties of hemp seed protein products. Journal of Food Science, 79, C1512–C1521.
36.
Malomo, S.A., Aluko, R.E. (2019). Kinetics of acetylcholinesterase inhibition by hemp seed protein-derived peptides. Journal Food Biochemistry, 43(7), art. no. e12897.
37.
McCarthy, A.L., O’Callaghan, Y.C., O’Brien, N.M. (2013). Protein hydrolysates from agricultural crops-bioactivity and potential for functional food development. Agriculture, 3, 112-130.
38.
Medina-Godoy, S., Ambriz-Pérez, D.L., Fuentes-Gutierrez, C., Germán-Báez, L.J., Gutiérrez-Dorado, R., Reyes-Moreno, C., Valdez-Ortiz, A. (2012). Angiotensin-converting enzyme inhibitory and antioxidative activities and functional characterization of protein hydrolysates of hard-to-cook chickpeas. Journal of the Science of Food and Agriculture, 92(9), 1974-1981.
39.
Mirzaei, M., Aminlari, M., Hosseini, E. (2016). Antioxidant, ACE-Inhibitory and antibacterial activities of Kluyveromyces marxianus protein hydrolysates and their peptide fractions. Functional Foods in Health and Disease, 6(7), 425-439.
40.
Mirzaei, M.M., Mirdamadi, S., Ehsani, M.R., Aminlari, M., Hosseini, E. (2015). Purification and identification of antioxidant and ACE-inhibitory peptide from Saccharomyces cerevisiae protein hydrolysate. Journal of Functional Foods, 19, 259–268.
41.
Muhamyankaka, V., Shoemaker, C.F., Nalwoga, M., Zhang, X.M. (2013). Physicochemical properties of hydrolysates from enzymatic hydrolysis of pumpkin (Cucurbita moschata) protein meal. International Food Research Journal, 20(5), 2227-2240.
42.
Nam, K.A., You, S.G., Kim, S.M. (2008). Molecular and physical characteristics of squid (Todarodes pacificus) skin collagens and biological properties of their enzymatic hydrolysates. Journal of Food Science, 73(4), C243–C255.
43.
Nnamezie, A.A., Famuwagun, A.A., Gbadamosi, S.O. (2019). Changes in some nutritional and sensory properties of treated and stored fluted pumpkin leaf. Annals. Food Science and Technology, 20(1), 65-81.
44.
Odiaka, N.I. (2001). Survey on the production and supply of Telfairia occidentalis in Makurdi, Benue State Nigeria. African Journal of Food Science, 2, 12-18.
45.
Olagunju, A.I., Omoba, O.S., Enujiugha, V.N., Alashi. A.M., Aluko, R.E. (2018). Pigeon pea enzymatic protein hydrolysates and ultrafiltration peptide fractions as potential sources of antioxidant peptides: An in vitro study. LWT - Food Science and Technology, 97, 269-278.
46.
Olusola, A.O., Ekun, O.E. (2018). Alpha-Amylase inhibitory properties and in vitro anti-oxidant potentials of cowpea seed protein hydrolysates. AASCIT Communications, 6(1), 1-12.
47.
Ortiz-Martinez, M., Winkler, R., García-Lara, S. (2014). Preventive and therapeutic potential of peptides from cereals against cancer. Journal of Proteomics, 111, 165–183.
48.
Paiva, L., Lima, E., Isabel, N., Baptista, J. (2017). Angiotensin I-Converting Enzyme (ACE) inhibitory activity, antioxidant properties, phenolic content and amino acid profiles of Fucus spiralis L. protein hydrolysate fractions. Marine Drugs, 15(10), art. no. 311.
49.
Park, B.Y., Yoon, K.Y. (2019). Biological activity of enzymatic hydrolysates and the membrane ultrafiltration fractions from perilla seed meal protein. Czech Journal of Food Sciences, 37(3), 180–185.
50.
Pihlanto, A., Mäkinen, S. (2017). The function of renin and the role of food-derived peptides as direct renin inhibitors. In A.N. Tolekova (Ed.), Renin-Angiotensin System-Past, Present And Future. InTech Open, London, UK, pp. 241–258.
51.
Pinciroli, M., Aphalo, P., Nardo, A.E., Añón, M.C., Quiroga, A.V. (2019). Broken rice as a potential functional ingredient with inhibitory activity of renin and angiotensin-converting enzyme (ACE). Plant Foods for Human Nutrition, 74(3), 405-413.
52.
Rajapakse, N., Mendis, E., Byun, H.G., Kim, S.K. (2005). Purification and in vitro antioxidative effects of giant squid muscle peptides on free radical-mediated oxidative systems. Journal of Nutritional Biochemistry, 16(9), 562–569.
53.
Ramada, M.H.S., Brand, G.D., Abrão, F.Y., Oliveira, M., Filho, J.L.C., Galbieri, R., Gramacho, K.P., Prates, M.V., Bloch, C. (2017). Encrypted antimicrobial peptides from plant proteins. Scientific Reports, 7, art. no. 13263.
54.
Saidi, S., Deratani, A., Belleville M.P., Amar, R.B. (2014). Antioxidant properties of peptide fractions from tuna dark muscle protein by-product hydrolysate produced by membrane fractionation process. Food Research International, 65, 329–336.
55.
Sentandreu, M.A., Toldrá, F. (2006). A rapid, simple and sensitive fluorescence method for the assay of angiotensin-I converting enzyme. Food Chemistry, 97, 546-554.
56.
Tavano, O.L. (2013). Protein hydrolysis using proteases: an important tool for food biotechnology. Journal of Molecular Catalysis and Biological Enzymology, 90, 1–11.
57.
Thamnarathip, P., Jangchud, K., Nitisinprasert, S., Vardhanabhuti, B. (2016). Identification of peptide molecular weight from rice bran protein hydrolysate with high antioxidant activity. Journal of Cereal Science, 69, 329–335.
58.
The UniProt Consortium (2019). UniProt: a worldwide hub of protein knowledge. Nucleic Acids Research, 47(D1), D506-D515.
59.
Udenigwe, C.C., Aluko, R.E. (2012). Food protein-derived bioactive peptides; Production, processing, and potential health benefits. Journal of Food Science, 77(1), R11–R24.
60.
Udenigwe, C.C., Lin, Y.S., Hou, W.C., Aluko, R.E. (2009). Kinetics of the inhibition of renin and angiotensin, I-converting enzyme by flaxseed protein hydrolysate fractions. Journal of Functional Foods, 1, 199-207.
61.
Udousoro, I., Ekanem, P. (2013). Assessment of proximate compositions of twelve edible vegetables in Nigeria. International Journal of Modern Chemistry, 4(2), 79-89.
62.
Venuste, M., Zhang, X., Shoemaker, C.F., Karangwa, E., Abbas, S., Kamdem, P.E. (2013). Influence of enzymatic hydrolysis and enzyme type on the nutritional and antioxidant properties of pumpkin meal hydrolysates. Food and Function, 4, 811–820.
63.
Wang, R., Zhao, H., Pan, X., Orfila, C., Lu, W., Ma, Y. (2019). Preparation of bioactive peptides with antidiabetic, antihypertensive, and antioxidant activities and identification of α‐glucosidase inhibitory peptides from soy protein. Food Science and Nutrition, 7(5), 1848-1856.
64.
Wasswa, J., Tang, J., Gu, X.-H., Yuan, X.-Q. (2007). Influence of the extent of enzymatic hydrolysis on the functional properties of protein hydrolysate from grass carp (Ctenopharyngodon idella) skin. Food Chemistry, 104, 1698-1704.
65.
Wei, Y.-H., Lu, C.-Y., Wei, C.-Y., Ma, Y.-S., Lee, H.-C. (2001). Oxidative stress in human aging and mitochondrial disease-consequences of defective mitochondrial respiration and impaired antioxidant enzyme system. Chinese Journal of Physiology, 44(1), 1–11.
66.
Xie, Z., Huang, J., Xu, X., Jin, Z. (2008). Antioxidant activity of peptides isolated from alfalfa leaf protein hydrolysate. Food Chemistry, 111, 370–376.
67.
Yoshikawa, T., Naito, Y. (2002). What is oxidative stress? Japanese Medical Association Journal, 45(7), 271–276.
68.
Zhang, Y., Lee, E.T., Devereux, R.B., Yeh, J., Best, L.G., Fabsitz, R.R., Howard, B.V. (2006). Prehypertension, diabetes, and cardiovascular disease risk in a population-based sample: The strong heart study. Hypertension, 47, 410–414.
69.
Zhao, Y., Li, B., Dong, S., Liu, Z., Zhao, X., Wang, J., Zeng, M.A. (2009). Novel ACE inhibitory peptide isolated from Acaudina molpadioidea hydrolysate. Peptides, 30, 1028–1033.
70.
Zhu, K.X., Zhou, H.M., Qian, H.F. (2006). Antioxidant and free radical-scavenging activities of wheat germ protein hydrolysates (WGPH) prepared with Alcalase. Process Biochemistry, 41, 1296–1302.
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