Search for Author, Title, Keyword
ORIGINAL ARTICLE
Antioxidant Activity of Hybrid Sturgeon (Huso dauricus × Acipenser schrenckii) Protein Hydrolysate Prepared Using Bromelain, Its Fractions and Purified Peptides
,
 
,
 
,
 
 
 
More details
Hide details
1
Key Laboratory of Fermentation Resource and Application in Sichuan Higher Education, Faculty of Agriculture, Forestry and Food Engineering, Yibin University, Yibin, 644000, Sichuan, China
2
Department of Agricultural Engineering, Faculty of Agriculture, Foods and Environment, Sana’a University, Sana’a, Yemen
3
Food and Dairy Science and Technology Department, Faculty of Environmental Agricultural Science, Arish University, North Sinai, Egypt
CORRESPONDING AUTHOR
Yuxia Wang   

Key Laboratory of Fermentation Resource and Application in Sichuan Higher Education, Faculty of Agriculture, Forestry and Food Engineering, Yibin University, Yibin, 644000, Sichuan, China
Submission date: 2021-10-11
Final revision date: 2022-01-30
Acceptance date: 2022-02-01
Online publication date: 2022-03-01
Publication date: 2022-03-01
 
Pol. J. Food Nutr. Sci. 2022;72(1):79–89
 
KEYWORDS
TOPICS
ABSTRACT
Protein hydrolysates could be a natural and safer source of antioxidant peptides. The purpose of this study was to optimize the hydrolysis of Huso dauricus × Acipenser schrenckii sturgeon proteins using bromelain and purify antioxidant peptides from hydrolysate. The degree of hydrolysis of 18.69% was obtained under the optimal conditions and hydrolysate had 94.76% solubility, 902 nm particle size and high antioxidant activity. The IC50 for DPPH and ABTS•+ scavenging activity were 3.14 and 3.81 mg/mL, respectively. The fraction of hydrolysate with a molecular weight of <1 kDa exhibited the highest antiradical activity against DPPH with IC50 of 2.10 mg/mL. In turn, the IC50 of the most active fraction after the Sephadex G-15 separation was 1.77 mg/mL. The reverse phase high performance liquid chromatography (RP-HPLC) was used to purify the peptides from this fraction. The peptide with histidine, leucine and glycine (MW of 0.2955 kDa) exhibited the highest antioxidant activity (IC50 of 1.33 mg/mL). The obtained fractions and peptides with antioxidant activity could be used as natural substitutes for synthetic antioxidants, especially in food and pharmaceuticals.
FUNDING
This work supported by Key Laboratory of Solid-state Fermentation Resource Utilization of Sichuan Province (2015GTY001), and the Scientific Research Fund of Sichuan Provincial Education Department (18TD0041).
 
REFERENCES (60)
1.
Abraha, B., Mahmud, A., Admassu, H., Habte-Tsion, H.-M., Xia, W., Yang, F. (2018). Production of biscuit from Chinese sturgeon fish fillet powder (Acipeneser sinensis): A snack food for children. Journal of Aquatic Food Product Technology, 27(10), 1048-1062. https://doi.org/10.1080/104988....
 
2.
Adjimani, J.P., Asare, P. (2015). Antioxidant and free radical scavenging activity of iron chelators. Toxicology Reports, 2, 721-728. https://doi.org/10.1016/j.toxr....
 
3.
Ahn, C.-B., Kim, J.-G., Je, J.-Y. (2014). Purification and antioxidant properties of octapeptide from salmon byproduct protein hydrolysate by gastrointestinal digestion. Food Chemistry, 147, 78-83. https://doi.org/10.1016/j.food....
 
4.
Ang, S.-S., Ismail-Fitry, M.R. (2019). Production of different mushroom protein hydrolysates as potential flavourings in chicken soup using stem bromelain hydrolysis. Food Technology and Biotechnology, 57(4), 472-480. https://doi.org/10.17113/ftb.5....
 
5.
AOAC. (1998). Official Methods of Analysis of AOAC International, 16th ed., 4th rev. ed., AOAC International.
 
6.
Bahari, A.N., Saari, N., Salim, N., Ashari, S.E. (2020). Response factorial design analysis on papain-generated hydrolysates from Actinopyga lecanora for determination of antioxidant and antityrosinase activities. Molecules, 25(11), art. no. 2663. https://doi.org/10.3390/molecu....
 
7.
Bhaskar, N., Benila, T., Radha, C., Lalitha, R.G. (2008). Optimization of enzymatic hydrolysis of visceral waste proteins of Catla (Catla catla) for preparing protein hydrolysate using a commercial protease. Bioresource Technology, 99(2), 335-343. https://doi.org/10.1016/j.bior....
 
8.
Billard, R., Lecointre, G. (2000). Biology and conservation of sturgeon and paddlefish. Reviews in Fish Biology and Fisheries, 10 (4), 355-392. https://doi.org/10.1023/A:1012....
 
9.
Bronzi, P., Chebanov, M., Michaels, J.T., Wei, Q., Rosenthal, H., Gessner, J. (2019). Sturgeon meat and caviar production: Global update 2017. Journal of Applied Ichthyology, 35(1), 257-266. https://doi.org/10.1111/jai.13....
 
10.
Centenaro, G.S., Centenaro, M.S., Hernandez, C.P. (2011). Antioxidant activity of protein hydrolysates of fish and chicken bones. Advance Journal of Food Science and Technology 3(4), 280-288.
 
11.
Chalamaiah, M., Jyothirmayi, T., Bhaskarachary, K., Vajreswari, A., Hemalatha, R., Kumar, B.D. (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(1), 221-229. https://doi.org/10.1016/j.food....
 
12.
Chalamaiah, M., Jyothirmayi, T., Diwan, P.V., Kumar, B.D. (2015). Antioxidant activity and functional properties of enzymatic protein hydrolysates from common carp (Cyprinus carpio) roe (egg). Journal of Food Science and Technology, 52(9), 5817-5825. https://doi.org/10.1007/s13197....
 
13.
Chi, C.-F., Wang, B., Deng, Y.-Y., Wang, Y.-M., Deng, S.-G., Ma, J.-Y. (2014). Isolation and characterization of three antioxidant pentapeptides from protein hydrolysate of monkfish (Lophius litulon) muscle. Food Research International, 55, 222-228. https://doi.org/10.1016/j.food....
 
14.
Chi, C.-F., Wang, B., Wang, Y.-M., Zhang, B., Deng, S.-G. (2015a). Isolation and characterization of three antioxidant peptides from protein hydrolysate of bluefin leatherjacket (Navodon septentrionalis) heads. Journal of Functional Foods, 12, 1-10. https://doi.org/10.1016/j.jff.....
 
15.
Chi, C.-F., Wang, B., Hu, F.-Y., Wang, Y.-M., Zhang, B., Deng, S.-G., Wu, C.-W. (2015b). Purification and identification of three novel antioxidant peptides from protein hydrolysate of bluefin leatherjacket (Navodon septentrionalis) skin. Food Research International, 73, 124-129. https://doi.org/10.1016/j.food....
 
16.
De Quadros, C.D.C., Lima, K.O., Bueno, C.H.L., Fogaça, F.H.d. S., Da Rocha, M., Prentice, C. (2019). Evaluation of the antioxidant and antimicrobial activity of protein hydrolysates and peptide fractions derived from Colossoma macropomum and their effect on ground beef lipid oxidation. Journal of Aquatic Food Product Technology, 28(6), 677-688. https://doi.org/10.1080/104988....
 
17.
Do Evangelho, J.A., Vanier, N.L., Pinto, V.Z., De Berrios, J.J., Dias, A.R.G., Da Rosa Zavareze, E. (2017). Black bean (Phaseolus vulgaris L.) protein hydrolysates: Physicochemical and functional properties. Food Chemistry, 214, 460-467. https://doi.org/10.1016/j.food....
 
18.
Eberhardt, A., López, E.C., Ceruti, R.J., Marino, F., Mammarella, E.J., Manzo, R.M., Sihufe, G.A. (2019). Influence of the degree of hydrolysis on the bioactive properties of whey protein hydrolysates using Alcalase®. International Journal of Dairy Technology, 72(4), 573-584. https://doi.org/10.1111/1471-0....
 
19.
Elavarasan, K., Shamasundar, B.A. (2016). Effect of oven drying and freeze drying on the antioxidant and functional properties of protein hydrolysates derived from freshwater fish (Cirrhinus mrigala) using papain enzyme. Journal of Food Science and Technology, 53(2), 1303-1311. https://doi.org/10.1007/s13197....
 
20.
Famuwagun, A.A., Alashi, A.M., Gbadamosi, S.O., Taiwo, K.A., Oyedele, D.J., Adobooye, O., Aluko, R.E. (2020). In vitro characterization of fluted pumpkin leaf protein hydrolysates and ultrafiltration of peptide fractions: Antioxidant and enzyme-inhibitory properties. Polish Journal of Food and Nutrition Sciences, 70(4), 429-443. https://doi.org/10.31883/pjfns....
 
21.
Fan, J., He, J., Zhuang, Y., Sun, L. (2012). Purification and identification of antioxidant peptides from enzymatic hydrolysates of tilapia (Oreochromis niloticus) frame protein. Molecules, 17(11), 12836-12850. https://doi.org/10.3390/molecu....
 
22.
Galla, N.R., Pamidighantam, P.R., Akula, S., Karakala, B. (2012). Functional properties and in vitro antioxidant activity of roe protein hydrolysates of Channa striatus and Labeo rohita. Food Chemistry, 135(3), 1479-1484. https://doi.org/10.1016/j.food....
 
23.
Gao, R., Shen, Y., Shu, W., Bai, F., Jin, W., Wang, J., Yuan, L. (2020). Optimization of enzymatic conditions of sturgeon muscles and their anti-inflammatory potential. Journal of Food Quality, 2020, art. no. 9698134. https://doi.org/10.1155/2020/9....
 
24.
García-Moreno, P.J., Pérez-Gálvez, R., Espejo-Carpio, F.J., Ruiz-Quesada, C., Pérez-Morilla, A.I., Martínez‐Agustín, O., Guadix, A., Guadix, E.M. (2017). Functional, bioactive and antigenicity properties of blue whiting protein hydrolysates: Effect of enzymatic treatment and degree of hydrolysis. Journal of the Science of Food and Agriculture, 97(1), 299-308. https://doi.org/10.1002/jsfa.7....
 
25.
Ghanbari, R., Zarei, M., Ebrahimpour, A., Abdul-Hamid, A., Ismail, A., Saari, N. (2015). Angiotensin-I converting enzyme (ACE) inhibitory and anti-oxidant activities of sea cucumber (Actinopyga lecanora) hydrolysates. International Journal of Molecular Sciences, 16(12), 28870-28885. https://doi.org/10.3390/ijms16....
 
26.
Guérard, F., Guimas, L., Binet, A. (2002). Production of tuna waste hydrolysates by a commercial neutral protease preparation. Journal of Molecular Catalysis B: Enzymatic, 19, 489-498. https://doi.org/10.1016/S1381-....
 
27.
Halim, N.R.A., Azlan, A., Yusof, H.M., Sarbon, N.M. (2018). Antioxidant and anticancer activities of enzymatic eel (Monopterus sp.) protein hydrolysate as influenced by different molecular weight. Biocatalysis and Agricultural Biotechnology, 16, 10-16. https://doi.org/10.1016/j.bcab....
 
28.
Hong, J., Chen, T.-T., Hu, P., Yang, J., Wang, S.-Y. (2014). Purification and characterization of an antioxidant peptide (GSQ) from Chinese leek (Allium tuberosum Rottler) seeds. Journal of Functional Foods, 10, 144-153. https://doi.org/10.1016/j.jff.....
 
29.
Jang, H.L., Liceaga, A.M., Yoon, K.Y. (2016). Purification, characterisation and stability of an antioxidant peptide derived from sandfish (Arctoscopus japonicus) protein hydrolysates. Journal of Functional Foods, 20, 433-442. https://doi.org/10.1016/j.jff.....
 
30.
Jin, J., Chu, Z., Chen, X., Liang, X. (2020). Responses of hybrid sturgeon (Huso dauricus♀× Acipenser schrenckii♂) to oral administration of phosphorus. Aquaculture Research, 51(4), 1428-1436. https://doi.org/10.1111/are.14....
 
31.
Kong, X., Guo, M., Hua, Y., Cao, D., Zhang, C. (2008). Enzymatic preparation of immunomodulating hydrolysates from soy proteins. Bioresource Technology, 99 (18), 8873-8879. https://doi.org/10.1016/j.bior....
 
32.
Ktari, N., Fakhfakh, N., Balti, R., Ben Khaled, H., Nasri, M., Bougatef, A. (2013). Effect of degree of hydrolysis and protease type on the antioxidant activity of protein hydrolysates from cuttlefish (Sepia officinalis) by-products. Journal of Aquatic Food Product Technology, 22(5), 436-448. https://doi.org/10.1080/104988....
 
33.
Latorres, J., Rios, D., Saggiomo, G., Wasielesky, W., Prentice-Hernandez, C. (2018). Functional and antioxidant properties of protein hydrolysates obtained from white shrimp (Litopenaeus vannamei). Journal of Food Science and Technology, 55(2), 721-729. https://doi.org/10.1007/s13197....
 
34.
Luo, L., Li, T., Xing, W., Xue, M., Ma, Z., Jiang, N., Li, W. (2015). Effects of feeding rates and feeding frequency on the growth performances of juvenile hybrid sturgeon, Acipenser schrenckii Brandt♀× A. baeri Brandt♂. Aquaculture, 448, 229-233. https://doi.org/10.1016/j.aqua....
 
35.
Marson, G.V., Da Costa Machado, M.T., De Castro, R.J.S., Hubinger, M.D. (2019). Sequential hydrolysis of spent brewer's yeast improved its physico-chemical characteristics and antioxidant properties: A strategy to transform waste into added-value biomolecules. Process Biochemistry, 84, 91-102. https://doi.org/10.1016/j.proc....
 
36.
Naqash, S.Y., Nazeer, R. (2013). Antioxidant and functional properties of protein hydrolysates from pink perch (Nemipterus japonicus) muscle. Journal of Food Science and Technology, 50(5), 972-978. https://doi.org/10.1007/s13197....
 
37.
Noman, A., Qixing, J., Xu, Y., Abed, S.M., Obadi, M., Ali, A.H., AL-Bukhaiti, W.Q., Xia, W. (2020a). Effects of ultrasonic, microwave, and combined ultrasonic-microwave pretreatments on the enzymatic hydrolysis process and protein hydrolysate properties obtained from Chinese sturgeon (Acipenser sinensis). Journal of Food Biochemistry, 44(8), art. no. e13292. https://doi.org/10.1111/jfbc.1....
 
38.
Noman, A., Ali, A.H., AL‐Bukhaiti, W.Q., Mahdi, A.A., Xia, W. (2020b). Structural and physicochemical characteristics of lyophilized Chinese sturgeon protein hydrolysates prepared by using two different enzymes. Journal of Food Science, 85(10), 3313-3322. https://doi.org/10.1111/1750-3....
 
39.
Noman, A., Qixing, J., Xu, Y., Ali, A.H., Al-Bukhaiti, W.Q., Abed, S.M., Xia, W. (2019). Influence of degree of hydrolysis on chemical composition, functional properties, and antioxidant activities of Chinese sturgeon (Acipenser sinensis) hydrolysates obtained by using alcalase 2.4 L. Journal of Aquatic Food Product Technology, 28(6), 583-597. https://doi.org/10.1080/104988....
 
40.
Noman, A., Xu, Y., AL-Bukhaiti, W.Q., Abed, S.M., Ali, A.H., Ramadhan, A.H., Xia, W. (2018). Influence of enzymatic hydrolysis conditions on the degree of hydrolysis and functional properties of protein hydrolysate obtained from Chinese sturgeon (Acipenser sinensis) by using papain enzyme. Process Biochemistry, 67, 19-28. https://doi.org/10.1016/j.proc....
 
41.
Ovissipour, M., Rasco, B., Shiroodi, S.G., Modanlow, M., Gholami, S., Nemati, M. (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(7), 1718-1726. https://doi.org/10.1002/jsfa.5....
 
42.
Pérez-Vega, J.A., Olivera-Castillo, L., Gómez-Ruiz, J.Á., Hernández-Ledesma, B. (2013). Release of multifunctional peptides by gastrointestinal digestion of sea cucumber (Isostichopus badionotus). Journal of Functional Foods, 5(2), 869-877. https://doi.org/10.1016/j.jff.....
 
43.
Priatni, S., Harimadi, K., Buana, E., Kosasih, W., Rohmatussolihat, R. (2020). Production and characterization of spray-dried swamp eel (Monopterus albus) protein hydrolysate prepared by papain. Sains Malaysiana, 49(3), 545-552. https://doi.org/10.17576/jsm-2....
 
44.
Saidi, S., Deratani, A., Belleville, M.-P., Amar, R.B. (2014). Production and fractionation of tuna by-product protein hydrolysate by ultrafiltration and nanofiltration: Impact on interesting peptides fractions and nutritional properties. Food Research International, 65, Part C, 453-461. https://doi.org/10.1016/j.food....
 
45.
Salwanee S., Aida, W.M.W., Mamot, S., Maskat, M.Y., Ibrahim, S. (2013). Effects of enzyme concentration, temperature, pH and time on the degree of hydrolysis of protein extract from viscera of tuna (Euthynnus affinis) by using alcalase. Sains Malaysiana, 42(3), 279-287.
 
46.
Samaranayaka, A.G., Li-Chan, E.C. (2011). Food-derived peptidic antioxidants: A review of their production, assessment, and potential applications. Journal of Functional Foods, 3(4), 229-254. https://doi.org/10.1016/j.jff.....
 
47.
Tan, X., Qi, L., Fan, F., Guo, Z., Wang, Z., Song, W., Du, M. (2018). Analysis of volatile compounds and nutritional properties of enzymatic hydrolysate of protein from cod bone. Food Chemistry, 264, 350-357. https://doi.org/10.1016/j.food....
 
48.
Taylor, W. (1957). Formol titration: an evaluation of its various modifications. Analyst, 82(976), 488-498. https://doi.org/10.1039/an9578....
 
49.
Tian, X., Zheng, J., Xu, B., Ye, J., Yang, Z., Yuan, F. (2020). Optimization of extraction of bioactive peptides from monkfish (Lophius litulon) and characterization of their role in H2O2-induced lesion. Marine Drugs, 18(9), art. no. 468. https://doi.org/10.3390/md1809....
 
50.
Villamil, O., Váquiro, H., Solanilla, J.F. (2017). Fish viscera protein hydrolysates: Production, potential applications and functional and bioactive properties. Food Chemistry, 224, 160-171. https://doi.org/10.1016/j.food....
 
51.
Wang, X., Yu, H., Xing, R., Liu, S., Chen, X., Li, P. (2019). Preparation and identification of antioxidative peptides from pacific herring (Clupea pallasii) protein. Molecules, 24 (10), art. no. 1946. https://doi.org/10.3390/molecu....
 
52.
Wang, Y.-Y., Wang, C.-Y., Wang, S.-T., Li, Y.-Q., Mo, H.-Z., He, J.-X. (2021). Physicochemical properties and antioxidant activities of tree peony (Paeonia suffruticosa Andr.) seed protein hydrolysates obtained with different proteases. Food Chemistry, 345, art. no. 128765. https://doi.org/10.1016/j.food....
 
53.
Wang, Z., Liu, X., Xie, H., Liu, Z., Rakariyatham, K., Yu, C., Shahidi, F., Zhou, D. (2021). Antioxidant activity and functional properties of Alcalase-hydrolyzed scallop protein hydrolysate and its role in the inhibition of cytotoxicity in vitro. Food Chemistry, 344, art. no. 128566. https://doi.org/10.1016/j.food....
 
54.
Zaky, A.A., Liu, Y., Han, P., Ma, A., Jia, Y. (2020). Effect of flavorzyme digestion on the antioxidant capacities of ultra-filtrated rice bran protein hydrolysates. Journal of Food Processing and Preservation, 44 (8), art. no. e14551. https://doi.org/10.1111/jfpp.1....
 
55.
Zhang, F., Qu, J., Thakur, K., Zhang, J.-G., Mocan, A., Wei, Z.-J. (2019). Purification and identification of an antioxidative peptide from peony (Paeonia suffruticosa Andr.) seed dreg. Food Chemistry, 285, 266-274. https://doi.org/10.1016/j.food....
 
56.
Zhang, L., Zhao, G.-X., Zhao, Y.-Q., Qiu, Y.-T., Chi, C.-F., Wang, B. (2019). Identification and active evaluation of antioxidant peptides from protein hydrolysates of skipjack tuna (Katsuwonus pelamis) head. Antioxidants, 8(8), art. no. 318. https://doi.org/10.3390/antiox....
 
57.
Zhang, N., Zhang, C., Chen, Y., Zheng, B. (2017). Purification and characterization of antioxidant peptides of Pseudosciaena crocea protein hydrolysates. Molecules, 22(1), art. no. 57. https://doi.org/10.3390/molecu....
 
58.
Zhang, Y., Wang, J., Zhu, Z., Li, X., Sun, S., Wang, W., Sadiq, F.A. (2021). Identification and characterization of two novel antioxidant peptides from silkworm pupae protein hydrolysates. European Food Research and Technology, 247(2), 343-352. https://doi.org/10.1007/s00217....
 
59.
Zheng, Z., Li, J., Li, J., Sun, H., Liu, Y. (2019). Physicochemical and antioxidative characteristics of black bean protein hydrolysates obtained from different enzymes. Food Hydrocolloids, 97, art. no. 105222. https://doi.org/10.1016/j.food....
 
60.
Zou, T.-B., He, T.-P., Li, H.-B., Tang, H.-W., Xia, E.-Q. (2016). The structure-activity relationship of the antioxidant peptides from natural proteins. Molecules, 21(1), art. no. 72. https://doi.org/10.3390/molecu....
 
eISSN:2083-6007
ISSN:1230-0322