Effects of Curcumin on Oxidative Stress and Ferroptosis in Acute Ammonia Stress-Induced Liver Injury in Gibel Carp (Carassius gibelio)

International Journal of Molecular Sciences - Tập 24 Số 7 - Trang 6441
Liyun Wu1,2,3, Bo Dong1,2,3, Qiaozhen Chen1,2,3, Yu Wang1,2,3, Dong Han1,2,3, Xiaoming Zhu1,3, Haokun Liu1,3, Zhimin Zhang1,3, Jing Wang1,3, Shouqi Xie1,4,2, Junyan Jin1,3
1State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China
2University of Chinese Academy of Sciences, Beijing, 100049, China
3of and , of , of , ,
4The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing 100101, China

Tóm tắt

This study investigated the potential role of curcumin (CUR) in preventing oxidative stress and ferroptosis induced by ammonia exposure in gibel carp. Experimental fish (initial weight: 11.22 ± 0.10 g, n = 150) were fed diets supplemented with or without 0.5% CUR for 56 days, followed by a 24 h ammonia (32.5 mg/L) exposure. Liver damages (aspartate aminotransferase (AST), alanine aminotransferase (ALT), adenosine deaminase (ADA), and alkaline phosphatase (ALP)) and oxidative stress enzyme activities (reactive oxygen species (ROS), malondialdehyde (MDA); and the content of antioxidant capacity (T-AOC), superoxide dismutase (SOD), and glutathione peroxidase (GPx)) were induced by ammonia stress. The antioxidant capacity was decreased, as indicated by inhibited gene expression of nuclear factor erythroid 2-related factor 2 (nrf2), heme oxygenase-1 (ho-1), catalase (cat), and sod. Ferroptosis was induced by ammonia stress, as suggested by upregulated mRNA levels of nuclear receptor coactivator 4 (ncoa4), transferrin receptor 1 (tfr1), and iron-responsive element-binding protein 2 (ireb2), and downregulated expression of glutathione peroxidase 4 (gpx4), ferroportin (fpn), and ferritin heavy chain 1 (fth1). In addition, both mRNA and protein levels of ferroptosis markers acyl-CoA synthetase long-chain family member 4 (ACSL4) and prostaglandin-endoperoxide synthase 2 (PTGS2) were upregulated, while cystine/glutamate antiporter (SLC7A11) was downregulated. However, liver injury and ferroptosis in fish induced by ammonia could be attenuated by CUR. Collectively, these findings demonstrate that CUR ameliorates oxidative stress and attenuates ammonia stress-induced ferroptosis. This study provides a new perspective on potential preventive strategies against ammonia stress in gibel carp by dietary CUR.

Từ khóa


Tài liệu tham khảo

Cheng, 2015, Effects of ammonia exposure on apoptosis, oxidative stress and immune response in pufferfish (Takifugu obscurus), Aquat. Toxicol., 164, 61, 10.1016/j.aquatox.2015.04.004

Xu, Z.K., Cao, J., Qin, X.M., Qiu, W.Q., Mei, J., and Xie, J. (2021). Toxic effects on bioaccumulation, hematological parameters, oxidative stress, immune responses and tissue structure in fish exposed to ammonia nitrogen: A review. Animals, 11.

Luo, 2017, Effect of dietary iron (Fe) levels on growth performance, hepatic lipid metabolism and antioxidant responses in juvenile yellow catfish Pelteobagrus fulvidraco, Aquacult. Nutr., 23, 1475, 10.1111/anu.12523

Liu, 2013, Effects of dietary protein level on growth performance, muscle composition, blood composition, and digestive enzyme activity of wuchang bream (Megalobrama amblycephala) fry, Isr. J. Aquacult-Bamid., 65, 9

Hoseini, 2019, Antioxidant, enzymatic and hematological responses of common carp (Cyprinus carpio) fed with myrcene- or menthol-supplemented diets and exposed to ambient ammonia, Aquaculture, 506, 246, 10.1016/j.aquaculture.2019.03.048

Chapman, 2018, Nrf2 and the hallmarks of cancer, Cancer Cell, 34, 21, 10.1016/j.ccell.2018.03.022

Kong, 2021, Effects of dietary curcumin inhibit deltamethrin-induced oxidative stress, inflammation and cell apoptosis in Channa argus via Nrf2 and NF-κB signaling pathways, Aquaculture, 540, 736744, 10.1016/j.aquaculture.2021.736744

Yang, 2016, Ferroptosis: Death by lipid peroxidation, Trends Cell Biol., 26, 165, 10.1016/j.tcb.2015.10.014

Gao, 2018, To eat or not to eat-the metabolic flavor of ferroptosis, Curr. Opin. Cell Biol., 51, 58, 10.1016/j.ceb.2017.11.001

Li, 2017, Inhibition of neuronal ferroptosis protects hemorrhagic brain, JCI Insight, 2, e90777, 10.1172/jci.insight.90777

Wang, 2017, Characterization of ferroptosis in murine models of hemochromatosis, Hepatology, 66, 449, 10.1002/hep.29117

Chen, 2021, Ferroptosis: Machinery and regulation, Autophagy, 17, 2054, 10.1080/15548627.2020.1810918

Dixon, 2012, Ferroptosis: An iron-dependent form of nonapoptotic cell death, Cell, 149, 1060, 10.1016/j.cell.2012.03.042

Yang, 2014, Regulation of ferroptotic cancer cell death by GPX4, Cell, 156, 317, 10.1016/j.cell.2013.12.010

Angeli, 2017, Ferroptosis inhibition: Mechanisms and opportunities, Trends Pharmacol. Sci., 38, 489, 10.1016/j.tips.2017.02.005

Alagawany, 2021, Curcumin and its different forms: A review on fish nutrition, Aquaculture, 532, 736030, 10.1016/j.aquaculture.2020.736030

Wang, 2022, Curcumin mitigates aflatoxin B1-induced liver injury via regulating the NLRP3 inflammasome and Nrf2 signaling pathway, Food Chem. Toxicol., 161, 112823, 10.1016/j.fct.2022.112823

Food and Agriculture Organization of the United Nations (2022). The State of World Fisheries and Aquaculture, FAO Fisheries and Aquaculture Department.

Qi, 2017, Ammonia exposure alters the expression of immune-related and antioxidant enzymes-related genes and the gut microbial community of crucian carp (Carassius auratus), Fish Shellfish Immunol., 70, 485, 10.1016/j.fsi.2017.09.043

Jiang, 2016, Effects of dietary curcumin supplementation on growth performance, intestinal digestive enzyme activities and antioxidant capacity of crucian carp Carassius auratus, Aquaculture, 463, 174, 10.1016/j.aquaculture.2016.05.040

Ming, 2020, Optimal dietary curcumin improved growth performance, and modulated innate immunity, antioxidant capacity and related genes expression of NF-κB and Nrf2 signaling pathways in grass carp (Ctenopharyngodon idella) after infection with Aeromonas hydrophila, Fish Shellfish Immunol., 97, 540, 10.1016/j.fsi.2019.12.074

Dawood, 2021, The regulatory roles of yucca extract on the growth rate, hepato-renal function, histopathological alterations, and immune-related genes in common carp exposed with acute ammonia stress, Aquaculture, 534, 736287, 10.1016/j.aquaculture.2020.736287

Goorden, 2013, Liver disorders in adults: ALT and AST, Ned. Tijdschr. Geneeskd., 157, A6443

Schieber, 2014, ROS function in redox signaling and oxidative Stress, Curr. Biol., 24, R453, 10.1016/j.cub.2014.03.034

Lee, J.Y., Kim, W.K., Bae, K.H., Lee, S.C., and Lee, E.W. (2021). Lipid metabolism and ferroptosis. Biology-Basel, 10.

Gan, 2022, Ammonia triggers ferroptosis in macrophages of yellow catfish Pelteobagrus fulvidraco, Aquacult. Res., 53, 568, 10.1111/are.15600

Jin, 2016, Dichlorodiphenyldichloroethylene exposure reduces r-GCS via suppressed Nrf2 in HepG2 cells, Environ. Toxicol., 31, 350, 10.1002/tox.22049

Li, L., Huang, W., Wang, S., Sun, K., Zhang, W., Ding, Y., Zhang, L., Tumen, B., Ji, L., and Liu, C. (2018). Astragaloside IV attenuates acetaminophen-induced liver injuries in mice by activating the Nrf2 signaling pathway. Molecules, 23.

He, 2021, Effect of acute ammonia toxicity on inflammation, oxidative stress and apoptosis in head kidney macrophage of Pelteobagrus fulvidraco and the alleviation of curcumin, Comp. Biochem. Phys. C, 248, 109098

Zhang, X.J., Zhou, L., Lu, W.J., Du, W.X., Mi, X.Y., Li, Z., Li, X.Y., Wang, Z.W., Wang, Y., and Duan, M. (2021). Comparative transcriptomic analysis reveals an association of gibel carp fatty liver with ferroptosis pathway. BMC Genom., 22.

Cheng, 2015, Iron regulatory protein 1 suppresses hypoxia-induced iron uptake proteins expression and decreases iron levels in HepG2 cells, J. Cell. Biochem., 116, 1919, 10.1002/jcb.25147

Di Sanzo, M., Quaresima, B., Biamonte, F., Palmieri, C., and Faniello, M.C. (2020). FTH1 pseudogenes in cancer and cell metabolism. Cells-Basel, 9.

Zheng, 2020, The metabolic underpinnings of ferroptosis, Cell Metab., 32, 920, 10.1016/j.cmet.2020.10.011

Doll, 2017, ACSL4 dictates ferroptosis sensitivity by shaping cellular lipid composition, Nat. Chem. Biol., 13, 91, 10.1038/nchembio.2239

Jiang, 2015, Ferroptosis as a p53-mediated activity during tumour suppression, Nature, 520, 57, 10.1038/nature14344

Herencia, 2019, Curcumin reduces renal damage associated with rhabdomyolysis by decreasing ferroptosis-mediated cell death, FASEB J., 33, 8961, 10.1096/fj.201900077R

Wu, 2023, Resveratrol attenuated oxidative stress and inflammatory and mitochondrial dysfunction induced by acute ammonia exposure in gibel carp (Carassius gibelio), Ecotoxicol. Environ. Saf., 251, 114544, 10.1016/j.ecoenv.2023.114544

Cao, 2018, Effects of dietary fishmeal replacement with Spirulina platensis on the growth, feed utilization, digestion and physiological parameters in juvenile gibel carp (Carassis auratus gibelio var. CAS III), Aquacult. Res., 49, 1320, 10.1111/are.13590

Dong, B., Wu, L.Y., Chen, Q.Z., Xu, W.J., Li, D.G., Han, D., Zhu, X.M., Liu, H.K., Yang, Y.X., and Xie, S.Q. (2022). Tolerance assessment of Atractylodes macrocephala polysaccharide in the diet of largemouth bass (Micropterus salmoides). Antioxidants, 11.

Li, 2021, Differential regulation of endoplasmic reticulum stress-induced autophagy and apoptosis in two strains of gibel carp (Carassius gibelio) exposed to acute waterborne cadmium, Aquat. Toxicol., 231, 105721, 10.1016/j.aquatox.2020.105721

Wu, 2022, Emodin alleviates acute hypoxia-induced apoptosis in gibel carp (Carassius gibelio) by upregulating autophagy through modulation of the AMPK/mTOR pathway, Aquaculture, 548, 737689, 10.1016/j.aquaculture.2021.737689