ORIGINAL ARTICLE
Cytoprotective Effect of Morchella esculenta Protein Hydrolysate and Its Derivative Against H2O2-Induced Oxidative Stress
| 1 | College of Light Industry and Food Engineering, Nanjing Forestry University, Nanjing 210037, China |
| 2 | College of Life and Health Sciences, Anhui Science and Technology University, Fengyang 233100, China |
| 3 | Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, China |
CORRESPONDING AUTHOR
Caie Wu
Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, China
Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, China
Online publish date: 2019-06-28
Submission date: 2019-04-16
Final revision date: 2019-06-12
Acceptance date: 2019-06-19
KEYWORDS
TOPICS
Functional foodsFunctional propertiesMaillard or browning reactionsFood bioactivesMushroomsBioactive peptidesChemical and enzymatic modification
ABSTRACT
Morchella protein hydrolysate (MPH) and its glycosylated derivative (G-MPH) may possess the potential as natural antioxidants. However, knowledge about the protective effects of MPH and G-MPH on cellular oxidative damage is limited. This study evaluated whether MPH and G-MPH protected Caco-2 cells from H2O2-induced oxidative injury and explored the potential mechanisms of protection. The results showed that, under H2O2 stress, both MPH and G-MPH significantly increased cell viability, suppressed intracellular ROS and MDA production, increased cellular antioxidant capacity, and activated Nrf2 signaling pathway. More importantly, MPH and G-MPH significantly inhibited the H2O2-induced apoptosis via restoring the loss of mitochondrial membrane potential and regulating the protein expressions of Bax, Bcl-2, and caspase-3. These data indicate that MPH and G-MPH can protect Caco-2 cells against oxidative injury by improving cellular antioxidant responses and inhibiting apoptosis. Therefore, MPH and G-MPH can have a broad application potential as promising ingredients of nutraceutical products or functional foods.
FUNDING
This work was supported by the grant from the Doctorate Fellowship Foundation of Nanjing Forestry University (2014), the Natural Science Foundation of Anhui Provincial Department of Education (Project No. KJ2017A515), the Postgraduate Research & Practice Innovation Program of Jiangsu Province (Project No. KYLX15_0916), the Natural Science Foundation of Jiangsu province (Project No. BK20150883), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).
REFERENCES (40)
1.
Chang, H.T., Jan, C.R., Liang, W.Z. (2018). Protective effects of a phenolic glycoside compound curculigoside on H2O2-induced oxidative stress and cytotoxicity in normal human breast epithelial cells. Journal of Functional Foods, 41, 171–182.
2.
Chen, J.C., Wang, R.F., Wang, T.Y., Ding, Q.L., Khalil, A., Xu, S.T., Lin, A.J., Yao, H.Q., Xie, W.J., Zhu, Z.Y., Xu, J.Y., (2017). Antioxidant properties of novel dinners derived from natural beta-elemene through inhibiting H2O2-induced apoptosis. ACS Medicinal Chemistry Letters, 8(4), 443–448.
3.
Cuadrado, A., Moreno-Murciano, P., Pedraza-Chaverri, J. (2009). The transcription factor Nrf2 as a new therapeutic target in Parkinson’s disease. Expert Opinion on Therapeutic Targets, 13(3), 319–329.
4.
Desagher, S., Martinou, J.C. (2000). Mitochondria as the central control point of apoptosis. Trends in Cell Biology, 10(9), 369–377.
5.
Fernandez-Checa, J.C., Fernandez, A., Morales, A., Mari, M., Garcia-Ruiz, C., Colell, A. (2010). Oxidative stress and altered mitochondrial function in neurodegenerative diseases: Lessons from mouse models. CNS & Neurological Disorders - Drug Targets, 9(4), 439–454.
6.
Hu, J., Yu, Q. W., Zhao, F., Ji, J. Z., Jiang, Z. Z., Chen, X., Gao, P., Ren, Y.R., Shao, S., Zhang, L.Y., Yan, M. (2015). Protection of quercetin against triptolide-induced apoptosis by suppressing oxidative stress in rat Leydig cells. Chemico-Biological Interactions, 240, 38–46.
7.
Je, J.Y., Lee, D.B. (2015). Nelumbo nucifera leaves protect hydrogen peroxide-induced hepatic damage via antioxidant enzymes and HO-1/Nrf2 activation. Food & Function, 6(6), 1911–1918.
8.
Jiao, W., Wang, Y., Kong, L., Ou-yang, T., Meng, Q., Fu, Q., Hu, Z.Z. (2018). CART peptide activates the Nrf2/HO-1 antioxidant pathway and protects hippocampal neurons in a rat model of Alzheimer’s disease. Biochemical and Biophysical Research Communications, 501(4), 1016–1022.
9.
Jin, M.M., Zhang, L., Yu, H.X., Meng, J., Sun, Z., Lu, R.R. (2013). Protective effect of whey protein hydrolysates on H2O2-induced PC12 cells oxidative stress via a mitochondria-mediated pathway. Food Chemistry, 141(2), 847–852.
10.
Lee, J.Y., Lee, S.H., Kim, H.J., Ha, J.M., Lee, S.H., Lee, J.H., Ha, B.J. (2004). The preventive inhibition of chondroitin sulfate against the CCl4-induced oxidative stress of subcellular level. Archives of Pharmacal Research, 27(3), 340–345.
11.
Li, J.Q., Ichikawa, T., Janicki, J.S., Cui, T.X. (2009). Targeting the Nrf2 pathway against cardiovascular disease. Expert Opinion on Therapeutic Targets, 13(7), 785–794.
12.
Li, T.G., Chen, B., Du, M., Song, J.J., Cheng, X., Wang, X., Mao, X. (2017). Casein glycomacropeptide hydrolysates exert cytoprotective effect against cellular oxidative stress by up-regulating HO-1 expression in HepG2 cells. Nutrients, 9(1), art. no. 31.
13.
Li, Y., Li, J.H., Huang, H., Yang, M.F., Zhuang, D.G., Cheng, X.M., Zhang, H.Z., Fu, X.L. (2016). Microcystin-LR induces mitochondria-mediated apoptosis in human bronchial epithelial cells. Experimental and Therapeutic Medicine, 12(2), 633–640.
14.
Liu, C.L., Xie, L.X., Li, M., Durairajan, S.S. K., Goto, S., Huang, J.D. (2007). Salvianolic acid B inhibits hydrogen peroxide-induced endothelial cell apoptosis through regulating PI3K/Akt signaling. PLoS One, 2(12), art. no. e1321.
15.
Mańdziuk, S., Dudzisz-Sledź, M., Korszeń-Pilecka, I., Milanowski, J., Wojcierowski, J., Korobowicz, E. (2003). Expression of p53 gene in stage IIIA non-small cell lung cancer in patients after neoadjuvant chemotherapy with Vepesid and Cisplatin. Annales Universitatis Mariae Curie-Sklodowska. Sectio D: Medicina, 58(1), 154–157.
16.
Mariani, E., Polidori, M.C., Cherubini, A., Mecocci, P. (2005). Oxidative stress in brain aging, neurodegenerative and vascular diseases: An overview. Journal of Chromatography. B, Analytical Technologies in the Biomedical and Life Sciences, 827(1), 65–75.
17.
Morifuji, M., Ishizaka, M., Baba, S., Fukuda, K., Matsumoto, H., Koga, J., Kanegae, M., Higuchi, M. (2010). Comparison of different sources and degrees of hydrolysis of dietary protein: Effect on plasma amino acids, dipeptides, and insulin responses in human subjects. Journal of Agricultural and Food Chemistry, 58(15), 8788–8797.
18.
Neuzil, J., Tomasetti, M., Mellick, A.S., Alleva, R., Salvatore, B.A., Birringer, M., Fariss, M. . (2004). Vitamin E analogues: A new class of inducers of apoptosis with selective anti-cancer effects. Current Cancer Drug Targets, 4(4), 355–372.
19.
Nguyen, T., Nioi, P., Pickett, C.B. (2009). The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. The Journal of Biological Chemistry, 284(20), 13291–13295.
20.
Pan, W.J., Ding, Q.Y., Wang, Y., Wang, D.D., Lu, Y.M., Yang, W.W., Cai, Z.N., Cheng, X.D., Zhang, W.N., Chen, Y. (2018). A bioactive polysaccharide TLH-3 isolated from Tricholoma lobayense protects against oxidative stress-induced premature senescence in cells and mice. Journal of Functional Foods, 42, 159–170.
21.
Pyo, M.C., Yang, S.Y., Chun, S.H., Oh, N.S., Lee, K.W. (2016). Protective effects of Maillard reaction products of whey protein concentrate against oxidative stress through an Nrf2-dependent pathway in HepG2 cells. Biological & Pharmaceutical Bulletin, 39(9), 1437–1447.
22.
Ruiz-Roca, B., Delgado-Andrade, C., Navarro, M.P., Seiquer, I. (2011). Effects of Maillard reaction products from glucose-lysine model systems on oxidative stress markers and against oxidative induction by hydrogen peroxide in Caco-2 cells. Journal of Food and Nutrition Research, 50(4), 237–248.
23.
Seifried, H.E., Anderson, D.E., Fisher, E.I., Milner, J.A. (2007). A review of the interaction among dietary antioxidants and reactive oxygen species. The Journal of Nutritional Biochemistry, 18(9), 567–579.
24.
Shen, R., Liu, D.S., Hou, C.C., Liu, D., Zhao, L.X., Cheng, J., Wang, D.G., Bai, D.C., (2017). Protective effect of Potentilla anserina polysaccharide on cadmium-induced nephrotoxicity in vitro and in vivo. Food & Function, 8(10), 3636–3646.
25.
Shi, Y.N., Kovacs-Nolan, J., Jiang, B., Tsao, R., Mine, Y. (2014). Peptides derived from eggshell membrane improve antioxidant enzyme activity and glutathione synthesis against oxidative damage in Caco-2 cells. Journal of Functional Foods, 11, 571–580.
26.
Wang, Z.J., Xie, J.H., Kan, L.J., Wang, J.Q., Shen, M.Y., Li, W.J., Nie, S.P., Xie, M.Y., (2015). Sulfated polysaccharides from Cyclocarya paliurus reduce H2O2-induced oxidative stress in RAW 264.7 cells. International Journal of Biological Macromolecules, 80, 410–417.
27.
Xia, T., Yao, J.H., Zhang, J., Zheng, Y., Song, J., Wang, M. (2017). Protective effects of Shanxi aged vinegar against hydrogen peroxide-induced oxidative damage in LO2 cells through Nrf2-mediated antioxidant responses. RSC Advances, 7(28), 17377–17386.
28.
Xu, Z., Fang, Y., Chen, Y., Yang, W.J., Ma, N., Pei, F., Kimatu, B.M., Hu, Q.H., Qiu, W.F., (2016). Protective effects of Se-containing protein hydrolysates from Se-enriched rice against Pb2+-induced cytotoxicity in PC12 and RAW264.7 cells. Food Chemistry, 202, 396–403.
29.
Xue, S., Chen, Y.X., Qin, S.K., Yang, A.Z., Wang, L., Xu, H.J., Geng, H.Y. (2014). Raltitrexed induces mitochondrial-mediated apoptosis in SGC7901 human gastric cancer cells. Molecular Medicine Reports, 10(4), 1927–1934.
30.
Yamaguchi, M., Okamoto, K., Kusano, T., Matsuda, Y., Suzuki, G., Fuse, A., Yokota, H. (2015). The effects of xanthine oxidoreductase inhibitors on oxidative stress markers following global brain ischemia reperfusion injury in C57BL/6 mice. PLoS One, 10(7), art. no. e0133980.
31.
Yang, S.Y., Lee, S., Pyo, M.C., Jeon, H., Kim, Y., Lee, K.W. (2017). Improved physicochemical properties and hepatic protection of Maillard reaction products derived from fish protein hydrolysates and ribose. Food Chemistry, 221, 1979–1988.
32.
Yoon, S.O., Kim, M.M., Park, S.J., Kim, D., Chung, J., Chung, A.S. (2001). Selenite suppresses hydrogen peroxide-induced cell apoptosis through inhibition of ASK1/JNK and activation of PI3-K/Akt pathways. The FASEB Journal, 15(13), 111–113.
33.
Zamora-Sillero, J., Ramos, P., Monserrat, J.M., Prentice, C. (2018). Evaluation of the antioxidant activity in vitro and in hippocampal HT-22 cells system of protein hydrolysates of common carp (Cyprinus carpio) by-product. Journal of Aquatic Food Product Technology, 27(1), 21–34.
34.
Zha, F.C., Wei, B.B., Chen, S.J., Dong, S.Y., Zeng, M.Y., Liu, Z.Y. (2015). The Maillard reaction of a shrimp by-product protein hydrolysate: Chemical changes and inhibiting effects of reactive oxygen species in human HepG2 cells. Food & Function, 6(6), 1919–1927.
35.
Zhang, H.J., Chen, R.C., Sun, G.B., Yang, L.P., Xu, X.D., Sun, X.B. (2018a). Protective effects of total flavonoids from Clinopodium chinense (Benth.) O. Ktze on myocardial injury in vivo and in vitro via regulation of Akt/Nrf2/HO-1 pathway. Phytomedicine, 40, 88–97.
36.
Zhang, Q., Wu, C.E., Fan, G.J., Li, T.T., Sun, Y.J. (2018b). Improvement of antioxidant activity of Morchella esculenta protein hydrolysate by optimized glycosylation reaction. CyTA - Journal of Food, 16(1), 238–246.
37.
Zhang, Q., Wu, C.E., Fan, G.J., Li, T.T., Wen, X. (2018c). Characteristics and enhanced antioxidant activity of glycated Morchella esculenta protein isolate. Food Science and Technology (Campinas), 38(1), 126–133.
38.
Zhang, Q.Z., Tong, X.H., Sui, X.N., Wang, Z.J., Qi, B.K., Li, Y., Jiang, L.Z. (2018d). Antioxidant activity and protective effects of alcalase-hydrolyzed soybean hydrolysate in human intestinal epithelial Caco-2 cells. Food Research International, 111, 256–264.
39.
39 Zhang, X.X., Wang, L., Wang, R., Luo, X.H., Li, Y.A., Chen, Z.X. (2016). Protective effects of rice dreg protein hydrolysates against hydrogen peroxide-induced oxidative stress in HepG-2 cells. Food & Function, 7(3), 1429–1437.
40.
Zhou, Y.F., Guo, B., Ye, M.J., Liao, R.F., Li, S.L. (2016). Protective effect of rutin against H2O2-induced oxidative stress and apoptosis in human lens epithelial cells. Current Eye Research, 41(7), 933–942.
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