Immunomodulatory Activity of Low Molecular-Weight Peptides from Nibea japonica in RAW264.7 Cells via NF-κB Pathway
Tóm tắt
In this study, a low molecular-weight (Mw) peptide named NJP (<1 kDa), was purified from a protein hydrolysate of Nibea japonica by ultrafiltration, and its immunomodulatory effect on RAW264.7 cells was evaluated. The lactate dehydrogenase (LDH) and MTT assays were performed to explore the cytotoxicity of NJP. The results showed that NJP promoted cell proliferation and had no significant toxic effects on RAW264.7 cells. Moreover, the cells formed multiple pseudopodia indicating that they were in activated state. Further tests showed that NJP significantly promoted phagocytic capacity, and the secretion of proinflammatory cytokines tumor necrosis factor-α (TNF-α), interleukin-6 (IL-6), and interleukin-1β (IL-1β). It also increased the synthesis of nitric oxide (NO) by upregulating inducible nitric oxide synthase (iNOS) protein level. Flow cytometry revealed that NJP promoted cell cycle progression and increased the percentage of cells in G0/G1 phase. NJP promoted IκBα degradation, p65 and nuclear factor (NF)-κB activation and translocation by up-regulating IKKα/β protein expression. In conclusion, these results indicated that NJP exerts immunomodulatory effects on RAW264.7 cells through the NF-κB signaling pathway. Therefore, NJP can be incorporated in the production of functional foods or nutraceuticals.
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Erdmann, 2008, The possible roles of food-derived bioactive peptides in reducing the risk of cardiovascular disease, J. Nutr. Biochem., 19, 643, 10.1016/j.jnutbio.2007.11.010
Kitts, 2003, Bioactive Proteins and Peptides from Food Sources. Applications of Bioprocesses used in Isolation and Recovery, Curr. Pharm. Des., 9, 1309, 10.2174/1381612033454883
Jeon, 1999, Improvement of functional properties of cod frame protein hydrolysates using ultrafiltration membranes, Process. Biochem., 35, 471, 10.1016/S0032-9592(99)00098-9
Shen, 2017, Current knowledge of intestinal absorption of bioactive peptides, Food Funct., 8, 4306, 10.1039/C7FO01185G
Yang, C., You, L., Yin, X., Liu, Y., Leng, X., Wang, W., Sai, N., and Ni, J. (2018). Heterophyllin B Ameliorates Lipopolysaccharide-Induced Inflammation and Oxidative Stress in RAW 264.7 Macrophages by Suppressing the PI3K/Akt Pathways. Molecules, 23.
Li, 2017, Immunomodulatory activity of small molecular (≤3 kDa) Coix glutelin enzymatic hydrolysate, CyTA J. Food, 15, 41
Zhang, 2016, In vitro anti-inflammatory and antioxidant activities and protein quality of high hydrostatic pressure treated squids (Todarodes pacificus), Food Chem., 203, 258, 10.1016/j.foodchem.2016.02.072
Fernando, 2016, Potential anti-inflammatory natural products from marine algae, Environ. Toxicol. Pharmacol., 48, 22, 10.1016/j.etap.2016.09.023
Ahn, 2012, Antioxidant and anti-inflammatory peptide fraction from salmon byproduct protein hydrolysates by peptic hydrolysis, Food Res. Int., 49, 92, 10.1016/j.foodres.2012.08.002
Sripokar, 2019, Antioxidant and functional properties of protein hydrolysates obtained from starry triggerfish muscle using trypsin from albacore tuna liver, Biocatal. Agric. Biotechnol., 17, 447, 10.1016/j.bcab.2018.12.013
Chalamaiah, 2018, Immunomodulatory and anticancer protein hydrolysates (peptides) from food proteins: A review, Food Chem., 245, 205, 10.1016/j.foodchem.2017.10.087
Chi, 2015, Antioxidant and anticancer peptides from the protein hydrolysate of blood clam (Tegillarca granosa) muscle, J. Funct. Foods, 15, 301, 10.1016/j.jff.2015.03.045
Beaulieu, 2013, Élise Detection of antibacterial activity in an enzymatic hydrolysate fraction obtained from processing of Atlantic rock crab (Cancer irroratus) by-products, PharmaNutrition, 1, 149, 10.1016/j.phanu.2013.05.004
Beaulieu, 2010, Evidence of Antibacterial Activities in Peptide Fractions Originating from Snow Crab (Chionoecetes opilio) By-Products, Probiotics Antimicrob. Proteins, 2, 197, 10.1007/s12602-010-9043-6
Harnedy, 2011, Antioxidant and antimicrobial peptidic hydrolysates from muscle protein sources and by-products, Food Chem., 124, 1296, 10.1016/j.foodchem.2010.07.004
Cheung, 2015, Marine Peptides: Bioactivities and Applications, Mar. Drugs, 13, 4006, 10.3390/md13074006
Batatinha, 2019, Nutrients, immune system, and exercise: Where will it take us?, Nutrition, 61, 151, 10.1016/j.nut.2018.09.019
Ketha, 2018, Purification, structural characterization of an arabinogalactan from green gram (Vigna radiata) and its role in macrophage activation, J. Funct. Foods, 50, 127, 10.1016/j.jff.2018.09.029
Chalamaiah, 2014, Immunomodulatory effects of protein hydrolysates from rohu (Labeo rohita) egg (roe) in BALB/c mice, Food Res. Int., 62, 1054, 10.1016/j.foodres.2014.05.050
Yu, F., Zhang, Z., Luo, L., Zhu, J., Huang, F., Yang, Z., Tang, Y., and Ding, G. (2018). Identification and Molecular Docking Study of a Novel Angiotensin-I Converting Enzyme Inhibitory Peptide Derived from Enzymatic Hydrolysates of Cyclina sinensis. Mar. Drugs, 16.
Yang, 2009, Immunomodulatory effects of marine oligopeptide preparation from Chum Salmon (Oncorhynchus keta) in mice, Food Chem., 113, 464, 10.1016/j.foodchem.2008.07.086
Morris, 2007, Immunostimulant activity of an enzymatic protein hydrolysate from green microalga Chlorella vulgaris on undernourished mice, Enzyme Microb. Technol., 40, 456, 10.1016/j.enzmictec.2006.07.021
Duarte, 2006, Immunomodulating capacity of commercial fish protein hydrolysate for diet supplementation, Immunobiology, 211, 341, 10.1016/j.imbio.2005.12.002
Chai, 2013, Growth, feed utilization, body composition and swimming performance of giant croaker, Nibea japonica Temminck and Schlegel, fed at different dietary protein and lipid levels, Aquac. Nutr., 19, 928, 10.1111/anu.12038
Tang, Y., Jin, S., Li, X., Li, X., Hu, X., Chen, Y., Huang, F., Yang, Z., Yu, F., and Ding, G. (2018). Physicochemical Properties and Biocompatibility Evaluation of Collagen from the Skin of Giant Croaker (Nibea japonica). Mar. Drugs, 16.
Yu, F., Zong, C., Jin, S., Zheng, J., Chen, N., Huang, J., Chen, Y., Huang, F., Yang, Z., and Tang, Y. (2018). Optimization of Extraction Conditions and Characterization of Pepsin-Solubilised Collagen from Skin of Giant Croaker (Nibea japonica). Mar. Drugs, 16.
Halim, 2016, Functional and bioactive properties of fish protein hydolysates and peptides: A comprehensive review, Trends Food Sci. Technol., 51, 24, 10.1016/j.tifs.2016.02.007
Granath, 1967, Molecular weight distribution analysis by gel chromatography on sephadex, J. Chromatogr. A, 28, 69, 10.1016/S0021-9673(01)85930-6
Hu, Z., Yang, P., Zhou, C., Li, S., and Hong, P. (2017). Marine Collagen Peptides from the Skin of Nile Tilapia (Oreochromis niloticus): Characterization and Wound Healing Evaluation. Mar. Drugs, 15.
Li, 2013, Influence of average molecular weight on antioxidant and functional properties of cartilage collagen hydrolysates from Sphyrna lewini, Dasyatis akjei and Raja porosa, Food Res. Int., 51, 283, 10.1016/j.foodres.2012.12.031
Park, 2014, Antioxidant and Anti-Inflammatory Activities of Protein Hydrolysates from Mytilus Edulis and Ultrafiltration Membrane Fractions, J. Food Biochem., 38, 460, 10.1111/jfbc.12070
Halim, 2018, Antioxidant and anticancer activities of enzymatic eel (Monopterus sp.) protein hydrolysate as influenced by different molecular weight, Biocatal. Agric. Biotechnol., 16, 10, 10.1016/j.bcab.2018.06.006
Razali, 2015, Antioxidant activity and functional properties of fractionated cobia skin gelatin hydrolysate at different molecular weight, Int. Food Res. J., 22, 651
Ghassem, 2011, Purification and identification of ACE inhibitory peptides from Haruan (Channa striatus) myofibrillar protein hydrolysate using HPLC–ESI-TOF MS/MS, Food Chem., 129, 1770, 10.1016/j.foodchem.2011.06.051
Lassoued, 2015, Bioactive peptides identified in thornback ray skin’s gelatin hydrolysates by proteases from Bacillus subtilis and Bacillus amyloliquefaciens, J. Proteomics, 128, 8, 10.1016/j.jprot.2015.06.016
Hou, 2012, Preparation of immunomodulatory hydrolysates from Alaska pollock frame, J. Sci. Food Agric., 92, 3029, 10.1002/jsfa.5719
He, 2015, Enzymatic hydrolysis optimization of Paphia undulata and lymphocyte proliferation activity of the isolated peptide fractions, J. Sci. Food Agric., 95, 1544, 10.1002/jsfa.6859
Xu, 2016, Protective effects of Se-containing protein hydrolysates from Se-enriched rice against Pb2+-induced cytotoxicity in PC12 and RAW264.7 cells, Food Chem., 202, 396, 10.1016/j.foodchem.2016.02.021
Wang, 2018, Structure characterization of one polysaccharide from Lepidium meyenii Walp., and its antioxidant activity and protective effect against H2O2 -induced injury RAW264.7 cells, Int. J. Boil. Macromol., 118, 816, 10.1016/j.ijbiomac.2018.06.117
Ren, 2018, Hazelnut protein-derived peptide LDAPGHR shows anti-inflammatory activity on LPS-induced RAW264.7 macrophage, J. Funct. Foods, 46, 449, 10.1016/j.jff.2018.04.024
Li, W., Ye, S., Zhang, Z., Tang, J., Jin, H., Huang, F., Yang, Z., Tang, Y., Chen, Y., and Ding, G. (2019). Purification and Characterization of a Novel Pentadecapeptide from Protein Hydrolysates of Cyclina sinensis and Its Immunomodulatory Effects on RAW264.7 Cells. Mar. Drugs, 17.
Li, 2015, Activation of RAW264.7 cells by a polysaccharide isolated from Antarctic bacterium Pseudoaltermonas sp. S-5, Carbohydr. Polym., 130, 97, 10.1016/j.carbpol.2015.04.070
Chao, 2018, Effects of Salvia miltiorrhiza Polysaccharides on Lipopolysaccharide-Induced Inflammatory Factor Release in RAW264.7 Cells, J. Interferon Cytokine Res., 38, 29, 10.1089/jir.2017.0087
Qi, 2016, Characterization and immunostimulating effects on murine peritoneal macrophages of a novel protein isolated from Panax quinquefolius L., J. Ethnopharmacol., 193, 700, 10.1016/j.jep.2016.10.034
Wang, 2019, Immunomodulation of ADPs-1a and ADPs-3a on RAW264.7 cells through NF-κB/MAPK signaling pathway, Int. J. Boil. Macromol., 132, 1024, 10.1016/j.ijbiomac.2019.04.031
Lorsbach, 1993, Expression of the nitric oxide synthase gene in mouse macrophages activated for tumor cell killing. Molecular basis for the synergy between interferon-gamma and lipopolysaccharide, J. Boil. Chem., 268, 1908, 10.1016/S0021-9258(18)53940-5
Surayot, 2015, Characterization and immunomodulatory activities of polysaccharides from Spirogyra neglecta (Hassall) Kützing, Biosci. Biotechnol. Biochem., 79, 1, 10.1080/09168451.2015.1043119
Liu, 2018, Oligopeptide derived from solid-state fermented cottonseed meal significantly affect the immunomodulatory in BALB/c mice treated with cyclophosphamide, Food Sci. Biotechnol., 27, 1791, 10.1007/s10068-018-0414-1
Meram, 2017, Anti-inflammatory effects of egg yolk livetins (α, β, and γ-livetin) fraction and its enzymatic hydrolysates in lipopolysaccharide-induced RAW 264.7 macrophages, Food Res. Int., 100, 449, 10.1016/j.foodres.2017.07.032
Jiang, S., Jia, Y., Tang, Y., Zheng, D., Han, X., Yu, F., Chen, Y., Huang, F., Yang, Z., and Ding, G. (2019). Anti-Proliferation Activity of a Decapeptide from Perinereies aibuhitensis toward Human Lung Cancer H1299 Cells. Mar. Drugs, 17.
Wu, 2015, Chitooligosaccharides from the shrimp chitosan hydrolysate induces differentiation of murine RAW264.7 macrophages into dendritic-like cells, J. Funct. Foods, 12, 70, 10.1016/j.jff.2014.10.004
DiDonato, 2012, NF-κB and the link between inflammation and cancer, Immunol. Rev., 246, 379, 10.1111/j.1600-065X.2012.01099.x
Wen, 2019, Immunomodulatory effect of low molecular-weight seleno-aminopolysaccharide on immunosuppressive mice, Int. J. Boil. Macromol., 123, 1278, 10.1016/j.ijbiomac.2018.10.099
Zhang, 2013, Immunomodulatory effect of Ganoderma atrum polysaccharide on CT26 tumor-bearing mice, Food Chem., 136, 1213, 10.1016/j.foodchem.2012.08.090
Yang, 2019, Acetylation of polysaccharide from Morchella angusticeps peck enhances its immune activation and anti-inflammatory activities in macrophage RAW264.7 cells, Food Chem. Toxicol., 125, 38, 10.1016/j.fct.2018.12.036
Hu, X.-Y., Li, W., Kong, X.-D., Han, H.B., Tang, Y.-P., Yu, F.-M., Yang, Z.-S., and Ding, G.-F. (2019, July 08). Optimization of Extraction Technology of Immunologically Active Peptides from Nibea Japonica by Response Surface Methodology. Available online: http://kns.cnki.net/kcms/detail/11.1759.ts.20190430.1115.016.html.
Qin, 2011, Preparation and antioxidant activity of enzymatic hydrolysates from purple sea urchin (Strongylocentrotus nudus) gonad, LWT, 44, 1113, 10.1016/j.lwt.2010.10.013
Liu, 2017, Antioxidant Activity and Stability Study of Peptides from Enzymatically Hydrolyzed Male Silkmoth, J. Food Process. Preserv., 41, e13081, 10.1111/jfpp.13081
Cheng, 2013, Polygonum viviparum L. inhibits the lipopolysaccharide-induced inflammatory response in RAW264.7 macrophages through haem oxygenase-1 induction and activation of the Nrf2 pathway, J. Sci. Food Agric., 93, 491, 10.1002/jsfa.5795
Karnjanapratum, 2016, Antioxidant, immunomodulatory and antiproliferative effects of gelatin hydrolysate from unicorn leatherjacket skin, J. Sci. Food Agric., 96, 3220, 10.1002/jsfa.7504
Ovrevik, 2012, Mono-2-ethylhexylphthalate (MEHP) induces TNF-α release and macrophage differentiation through different signalling pathways in RAW264.7 cells, Toxicol. Lett., 209, 43, 10.1016/j.toxlet.2011.11.016
Luo, 2017, The Correlation Between In Vitro Antioxidant Activity and Immunomodulatory Activity of Enzymatic Hydrolysates from Selenium-Enriched Rice Protein, J. Food Sci., 82, 517, 10.1111/1750-3841.13595
Yu, 2013, Macrophage Immunomodulatory Activity of a Purified Polysaccharide Isolated from Ganoderma atrum, Phytother. Res., 27, 186, 10.1002/ptr.4698
Benjakul, 2016, Antioxidant, immunomodulatory and antiproliferative effects of gelatin hydrolysates from seabass (Lates calcarifer) skins, Int. J. Food Sci. Technol., 51, 1545, 10.1111/ijfs.13123