Antioxidant properties of Klunzinger’s mullet ( Liza klunzingeri ) protein hydrolysates prepared with enzymatic hydrolysis using a commercial protease and microbial hydrolysis with Bacillus licheniformis
Restricted accessResearch articleFirst published online April, 2022
Antioxidant properties of Klunzinger’s mullet ( Liza klunzingeri ) protein hydrolysates prepared with enzymatic hydrolysis using a commercial protease and microbial hydrolysis with Bacillus licheniformis
Antioxidant activity of Klunzinger's mullet (Liza klunzingeri) muscle hydrolysates obtained using Bacillus licheniformis fermentation and enzymatic hydrolysis was determined. Hydrolysates obtained after 6 days of fermentation with B. licheniformis showed the highest free radical scavenging activity, metal chelating ability and ferric reducing antioxidant power (FRAP) (P ≤ 0.05). Microbial fermentation led to a higher percentage of small peptides and higher solubility compared with Alcalase hydrolysis (P ≤ 0.05). Hydrolysates showing the highest antioxidant properties attenuated serum, liver, and kidney oxidative stress biomarkers in male Wister rats stressed by carbon tetrachloride (P ≤ 0.05). At 300 mg/kg oral administration, hydrolysates increased serum, renal, and hepatic total antioxidant capacity (TAC) (P ≤ 0.05) and reduced their elevated levels of malondialdehyde (MDA), nitric oxide (NO•), and serum liver enzymes (AST, ALP, and ALT) (P ≤ 0.05). The hydrolysates were able to ameliorate hepatic damage by reducing necrosis, fatty changes, and inflammation. Results showed the antioxidant and hepato-toxic protective activities of Klunzinger’s mullet muscle hydrolysates obtained using microbial fermentation, which may, therefore, potentially be considered as a functional food ingredient.
Abdel-HamidMOsmanAEl-HadaryARomeihESitohyMLiL. (2020).
Hepatoprotective action of papain-hydrolyzed buffalo milk protein on carbon tetrachloride oxidative stressed albino rats. Journal of Dairy Science103(2): 1884–1893.
2.
AdewoleSSalakoADohertyONaickerT. (2007).
Effect of melatonin on carbon tetrachloride-induced kidney injury in Wistar rats. African Journal of Biomedical Research10(2): 153–164.
3.
AlemánAPérez-SantínEBordenave-JuchereauSArnaudinIGómez-GuillénMCMonteroP. (2011).
Squid gelatin hydrolysates with antihypertensive, anticancer and antioxidant activity. Food Research International44(4): 1044–1051.
4.
Aluko RE. (2015). Amino acids, peptides, and proteins as antioxidants for food preservation. In: F Shahidi (Ed), Handbook of Antioxidants for Food Preservation. UK: Woodhead Publishing, pp. 105–140.
5.
BenzieIFStrainJJ. (1996).
The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Analytical Biochemistry239(1): 70–76.
6.
CamargoTRRamosPMonserratJMPrenticeCFernandesCJZambuzziWF, et al. (2021).
Biological activities of the protein hydrolysate obtained from two fishes common in the fisheries bycatch. Food Chemistry 342: 128361.
7.
DeckerEAWelchB. (1990).
Role of ferritin as a lipid oxidation catalyst in muscle food. Journal of Agricultural and Food Chemistry38(3): 674–677.
8.
DongSZengMWangDLiuZZhaoYYangH. (2008).
Antioxidant and biochemical properties of protein hydrolysates prepared from silver carp (Hypophthalmichthys molitrix). Food Chemistry107(4): 1485–1493.
9.
FathyMKhalifaEMFawzyMA. (2019).
Modulation of inducible nitric oxide synthase pathway by eugenol and telmisartan in carbon tetrachloride-induced liver injury in rats. Life Sciences216: 207–214.
10.
GanieSAHaqEHamidAQurishiYMahmoodZZargarBA, et al. (2011).
Carbon tetrachloride induced kidney and lung tissue damages and antioxidant activities of the aqueous rhizome extract of Podophyllum hexandrum. BMC Complementary and Alternative Medicine11(1): 17.
11.
GiampieriFAlvarez-SuarezJMMazzoniLForbes-HernandezTYGasparriniMGonzàlez-ParamàsAM, et al. (2014).
An anthocyanin-rich strawberry extract protects against oxidative stress damage and improves mitochondrial functionality in human dermal fibroblasts exposed to an oxidizing agent. Food & Function5(8): 1939–1948.
12.
He R, Girgih AT, Malomo SA, Ju X and Aluko RE. (2013). Antioxidant activities of enzymatic rapeseed protein hydrolysates and the membrane ultrafiltration fractions. Journal of Functional Foods 5(1): 219–227.
13.
HeRJuXYuanJWangLGirgihATAlukoRE. (2012).
Antioxidant activities of rapeseed peptides produced by solid state fermentation. Food Research International49(1): 432–438.
14.
HeSWangFNingZYangBWangY. (2014).
Preparation of anchovy (Engraulis japonicus) protein hydrolysates with high free radical-scavenging activity using endogenous and commercial enzymes. Food Science and Technology International20(8): 567–578.
15.
JamshidzadehAHeidariRRazmjouMKarimiFMoeinMRFarshadO, et al. (2015).
An in vivo and in vitro investigation on hepatoprotective effects of Pimpinella anisum seed essential oil and extracts against carbon tetrachloride-induced toxicity. Iranian Journal of Basic Medical Sciences18(2): 205.
16.
JemilIAbdelhediOMoraLNasriRAristoyMCJridiM, et al. (2016).
Peptidomic analysis of bioactive peptides in zebra blenny (Salaria basilisca) muscle protein hydrolysate exhibiting antimicrobial activity obtained by fermentation with Bacillus mojavensis A21. Process Biochemistry51(12): 2186–2197.
17.
Karthikeyan R, Anantharaman P, Chidambaram N, Balasubramanian T, Somasundaram ST. (2012). Padina boergessenii ameliorates carbon tetrachloride induced nephrotoxicity in Wistar rats. Journal of King Saud University-Science 24(3): 227–232.
18.
KhaledHBGhlissiZChtourouYHakimAKtariNFatmaMA, et al. (2012).
Effect of protein hydrolysates from sardinelle (Sardinella aurita) on the oxidative status and blood lipid profile of cholesterol-fed rats. Food Research International45(1): 60–68.
19.
KhiariZMasonB. (2018).
Comparative dynamics of fish by-catch hydrolysis through chemical and microbial methods. Lwt – Food Science and Technology97: 135–143.
20.
KtariNSalemRBSBBkhairiaISlimaSBNasriRSalahRB, et al. (2020).
Functional properties and biological activities of peptides from zebra blenny protein hydrolysates fractionated using ultrafiltration. Food Bioscience34: 100539.
21.
LiuWHouTShiWGuoDHeH. (2018).
Hepatoprotective effects of selenium-biofortified soybean peptides on liver fibrosis induced by tetrachloromethane. Journal of Functional Foods50: 183–191.
22.
LiuYLiXChenZYuJWangFWangJ. (2014).
Characterization of structural and functional properties of fish protein hydrolysates from surimi processing by-products. Food Chemistry151: 459–465.
23.
MarwellMAKHaasSMBieberLLTolbertNE. (1978).
A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein sample. Analytical Biochemistry87(1): 206–210.
24.
MontalvoGEBVandenbergheLPDSSoccolVTde CarvalhoJCSoccolCR. (2020).
The antihypertensive, antimicrobial and anticancer peptides from arthrospira with therapeutic potential: A mini review. Current Molecular Medicine20(8): 593–606.
25.
NajafianLBabjiAS. (2012).
A review of fish-derived antioxidant and antimicrobial peptides: Their production, assessment, and applications. Peptides33(1): 178–185.
26.
Namıduru ES, Tarakçoğlu M, Namıduru M, Kocabaş R, Erbağcı B, Meram I, et al. (2011). Increased serum nitric oxide and malondialdehyde levels in patients with acute intestinal amebiasis. Asian Pacific Journal of Tropical Biomedicine 1(6): 478–481.
27.
Nguyen Q, Hettiarachchy N, Rayaprolu S, Jayanthi S, Thallapuranam S and Chen P. (2016). Physicochemical properties and ACE-I inhibitory activity of protein hydrolysates from a non-genetically modified soy cultivar. Journal of the American Oil Chemists’ Society 93(4): 595–606.
28.
NikooMBenjakulSYasemiMGavlighiHAXuX. (2019).
Hydrolysates from rainbow trout (Oncorhynchus mykiss) processing by-product with different pretreatments: Antioxidant activity and their effect on lipid and protein oxidation of raw fish emulsion. Lwt – Food Science and Technology108: 120–128.
29.
NikooMRegensteinJMNooriFGheshlaghiSP. (2021).
Autolysis of rainbow trout (Oncorhynchus mykiss) by-products: Enzymatic activities, lipid and protein oxidation, and antioxidant activity of protein hydrolysates. Lwt – Food Science and Technology140: 110702.
30.
NikooMXuXRegensteinJMNooriF. (2021).
Autolysis of pacific white shrimp (Litopenaeus vannamei) processing by-products: Enzymatic activities, lipid and protein oxidation, and antioxidant activity of hydrolysates. Food Bioscience39: 100844.
31.
RabieiSRezaeiMAbasianZKhezriMNikooMRafieian-KopaeiM, et al. (2019a).
The protective effect of Liza klunzingeri protein hydrolysate on carbon tetrachloride-induced oxidative stress and toxicity in male rats. Iranian Journal of Basic Medical Sciences22(10): 1203.
32.
RabieiSRezaeiMAsgharzadeSNikooMRafieia-KopaiM. (2019b).
Antioxidant and cytotoxic properties of protein hydrolysates obtained from enzymatic hydrolysis of Klunzinger’s mullet (Liza klunzingeri) muscle. Brazilian Journal of Pharmaceutical Sciences55: e18304.
33.
SalehiARabieiZSetorkiM. (2018).
Effect of gallic acid on chronic restraint stress-induced anxiety and memory loss in male BALB/c mice. Iranian Journal of Basic Medical Sciences21(12): 1232–1237.
34.
SarteshniziRASahariMAGavlighiHARegensteinJMNikooM. (2019).
Antioxidant activity of Sind sardine hydrolysates with pistachio green hull (PGH) extracts. Food Bioscience27: 37–45.
35.
ShimadaKCheftelJC. (1989).
Sulfhydryl group/disulfide bond interchange reactions during heat-induced gelation of whey protein isolate. Journal of Agricultural and Food Chemistry37(1): 161–168.
36.
SiesHBerndtCJonesDP. (2017).
Oxidative stress. Annual Review of Biochemistry86: 715–748.
37.
SiowHLGanCY. (2016).
Extraction, identification, and structure–activity relationship of antioxidative and α-amylase inhibitory peptides from cumin seeds (Cuminum cyminum). Journal of Functional Foods22: 1–12.
38.
SlizyteRRommiKMozuraityteREckPFiveKRustadT. (2016).
Bioactivities of fish protein hydrolysates from defatted salmon backbones. Biotechnology Reports (Amsterdam, Netherlands)11: 99–109.
39.
SreelathaSPadmaPRUmadeviM. (2009).
Protective effects of Coriandrum sativum extracts on carbon tetrachloride-induced hepatotoxicity in rats. Food and Chemical Toxicology47(4): 702–708.
40.
SrivastavaAShivanandappaT. (2010).
Hepatoprotective effect of the root extract of Decalepis hamiltonii against carbon tetrachloride-induced oxidative stress in rats. Food Chemistry118(2): 411–417.
41.
SunXUdenigweCC. (2020).
Chemistry and biofunctional significance of bioactive peptide interactions with food and gut components. Journal of Agricultural and Food Chemistry68(46): 12972–12977.
42.
Theodore AE, Raghavan S and Kristinsson HG. (2008). Antioxidative activity of protein hydrolysates prepared from alkaline-aided channel catfish protein isolates. Journal of Agricultural and Food Chemistry 56(16): 7459–7466.
43.
ThomasCEAustSD. (1986).
Free radicals and environmental toxins. Annals of Emergency Medicine15(9): 1075–1083.
44.
TkaczewskaJBorczakBPiątkowskaEKapusta-DuchJMorawskaMCzechT. (2019).
Effect of protein hydrolysates from carp (Cyprinus carpio) skin gelatine on oxidative stress biomarkers and other blood parameters in healthy rats. Journal of Functional Foods60: 103411.
45.
UdenigweCCFoglianoV. (2017).
Food matrix interaction and bioavailability of bioactive peptides: Two faces of the same coin? Journal of Functional Foods35: 9–12.
46.
UstyolLDemirörenKKandemirIErtenRBulanKKabaS, et al. (2017).
Comparative nephroprotective effects of silymarin, N-acetylcysteine, and thymoquinone against carbon tetrachloride-induced nephrotoxicity in rats. Iranian Red Crescent Medical Journal19(1): e37746.
47.
VázquezJAFraguasJMirónJValcárcelJPérez-MartínRIAnteloLT. (2020).
Valorisation of fish discards assisted by enzymatic hydrolysis and microbial bioconversion: Lab and pilot plant studies and preliminary sustainability evaluation. Journal of Cleaner Production246: 119027.
48.
WangBGongYDLiZRYuDChiCFMaJY. (2014).
Isolation and characterisation of five novel antioxidant peptides from ethanol-soluble proteins hydrolysate of spotless smoothhound (Mustelus griseus) muscle. Journal of Functional Foods6: 176–185.
49.
WangZLiuXXieHLiuZRakariyathamKYuC, et al. (2020).
Antioxidant activity and functional properties of alcalase-hydrolyzed scallop protein hydrolysate and its role in the inhibition of cytotoxicity in vitro. Food Chemistry344: 128566.
50.
WongFWYChanWYLeeSST. (1998).
Resistance to carbon tetrachloride-induced hepatotoxicity in mice which lack CYP2E1 expression. Toxicology and Applied Pharmacology153(1): 109–118.
51.
XiaoCZhouFZhaoMSuGSunB. (2018).
Chicken breast muscle hydrolysates ameliorate acute alcohol-induced liver injury in mice through alcohol dehydrogenase (ADH) activation and oxidative stress reduction. Food & Function9(2): 774–784.
52.
ZhangHTsaoR. (2016).
Dietary polyphenols, oxidative stress and antioxidant and anti-inflammatory effects. Current Opinion in Food Science8: 33–42.
53.
ZhangLLuYFengXLiuQLiYHaoJ, et al. (2020).
Hepatoprotective effects of Pleurotus ostreatus protein hydrolysates yielded by pepsin hydrolysis. Catalysts10(6): 595.
54.
ZhaoLLuoY-CWangC-TJiB-P. (2011).
Antioxidant activity of protein hydrolysates from aqueous extract of velvet antler (Cervus elaphus) as influenced by MW and enzymes. Natural Product Communications6(11): 1683–1688.
