Volume 42 Issue 5
Sep.  2021
Turn off MathJax
Article Contents
Sheng-Yu Luo, Cheng Liu, Jie Ding, Xin-Ming Gao, Jing-Qian Wang, Yi-Bo Zhang, Chen Du, Cong-Cong Hou, Jun-Quan Zhu, Bao Lou, Xiong-Fei Wu, Wei-Liang Shen. Scavenging reactive oxygen species is a potential strategy to protect Larimichthys crocea against environmental hypoxia by mitigating oxidative stress. Zoological Research, 2021, 42(5): 592-605. doi: 10.24272/j.issn.2095-8137.2021.079
Citation: Sheng-Yu Luo, Cheng Liu, Jie Ding, Xin-Ming Gao, Jing-Qian Wang, Yi-Bo Zhang, Chen Du, Cong-Cong Hou, Jun-Quan Zhu, Bao Lou, Xiong-Fei Wu, Wei-Liang Shen. Scavenging reactive oxygen species is a potential strategy to protect Larimichthys crocea against environmental hypoxia by mitigating oxidative stress. Zoological Research, 2021, 42(5): 592-605. doi: 10.24272/j.issn.2095-8137.2021.079

Scavenging reactive oxygen species is a potential strategy to protect Larimichthys crocea against environmental hypoxia by mitigating oxidative stress

doi: 10.24272/j.issn.2095-8137.2021.079
Funds:  This work was supported by the NSFC-Zhejiang Joint Fund for the Integration of Industrialization and Informatization (U1809212), Scientific and Technical Project of Zhejiang Province (2016C02055-7), Scientific and Technical Project of Ningbo City (2021Z002, 2015C110005), Ningbo Science and Technology Plan Projects (2018A610228), Teaching and Research Project of Ningbo University (XYL19023), Collaborative Innovation Center for Zhejiang Marine High-efficiency and Healthy Aquaculture, K.C. Wong Magna Fund in Ningbo University
More Information
  • The large yellow croaker (Larimichthys crocea), which is an economically important mariculture fish in China, is often exposed to environmental hypoxia. Reactive oxygen species (ROS) homeostasis is essential for the maintenance of normal physiological conditions in an organism. Direct evidence that environmental hypoxia leads to ROS overproduction is scarce in marine fish. Furthermore, the sources of ROS overproduction in marine fish under hypoxic stress are poorly known. In this study, we investigated the effects of hypoxia on redox homeostasis in L. crocea and the impact of impaired redox homeostasis on fish. We first confirmed that hypoxia drove ROS production mainly via the mitochondrial electron transport chain and NADPH oxidase complex pathways in L. crocea and its cell line (large yellow croaker fry (LYCF) cells). We subsequently detected a marked increase in the antioxidant systems of the fish. However, imbalance between the pro-oxidation and antioxidation systems ultimately led to excessive ROS and oxidative stress. Cell viability showed a remarkable decrease while oxidative indicators, such as malondialdehyde, protein carbonylation, and 8-hydroxy-2 deoxyguanosine, showed a significant increase after hypoxia, accompanied by tissue damage. N-acetylcysteine (NAC) reduced ROS levels, alleviated oxidative damage, and improved cell viability in vitro. Appropriate uptake of ROS scavengers (e.g., NAC and elamipretide Szeto-Schiller-31) and inhibitors (e.g., apocynin, diphenylene iodonium, and 5-hydroxydecanoate) may be effective at overcoming hypoxic toxicity. Our findings highlight previously unstudied strategies of hypoxic toxicity resistance in marine fish.
  • loading
  • [1]
    Almeida AS, Figueiredo-Pereira C, Vieira HLA. 2015. Carbon monoxide and mitochondria-modulation of cell metabolism, redox response and cell death. Frontiers in Physiology, 6: 33.
    [2]
    Baldissera MD, de Freitas Souza C, Boaventura TP, Nakayama CL, Baldisserotto B, Luz RK. 2020. Involvement of the phosphoryl transfer network in gill bioenergetic imbalance of pacamã (Lophiosilurus alexandri) subjected to hypoxia: notable participation of creatine kinase. Fish Physiology and Biochemistry, 46(1): 405−416. doi: 10.1007/s10695-019-00728-0
    [3]
    Balogh E, Tóth A, Méhes G, Trencsényi G, Paragh G, Jeney V. 2019. Hypoxia triggers osteochondrogenic differentiation of vascular smooth muscle cells in an HIF-1 (hypoxia-inducible factor 1)-dependent and reactive oxygen species-dependent manner. Arteriosclerosis, Thrombosis, and Vascular Biology, 39(6): 1088−1099. doi: 10.1161/ATVBAHA.119.312509
    [4]
    Breitburg D, Levin LA, Oschlies A, Grégoire M, Chavez FP, Conley DJ, et al. 2018. Declining oxygen in the global ocean and coastal waters. Science, 359(6371): eaam7240. doi: 10.1126/science.aam7240
    [5]
    Brownlee M. 2005. The pathobiology of diabetic complications: a unifying mechanism. Diabetes, 54(6): 1615−1625. doi: 10.2337/diabetes.54.6.1615
    [6]
    Chang CW, Su YC, Her GM, Ken CF, Hong JR. 2011. Betanodavirus induces oxidative stress-mediated cell death that prevented by anti-oxidants and zfcatalase in fish cells. PLoS One, 6(10): e25853. doi: 10.1371/journal.pone.0025853
    [7]
    Couto N, Wood J, Barber J. 2016. The role of glutathione reductase and related enzymes on cellular redox homoeostasis network. Free Radical Biology and Medicine, 95: 27−42. doi: 10.1016/j.freeradbiomed.2016.02.028
    [8]
    Datta S, Mazumder S, Ghosh D, Dey S, Bhattacharya S. 2009. Low concentration of arsenic could induce caspase-3 mediated head kidney macrophage apoptosis with JNK–p38 activation in Clarias batrachus. Toxicology and Applied Pharmacology, 241(3): 329−338. doi: 10.1016/j.taap.2009.09.007
    [9]
    DeCoursey TE. 2016. The intimate and controversial relationship between voltage-gated proton channels and the phagocyte NADPH oxidase. Immunological Reviews, 273(1): 194−218. doi: 10.1111/imr.12437
    [10]
    Diaz RJ. 2001. Overview of hypoxia around the world. Journal of Environmental Quality, 30(2): 275−281. doi: 10.2134/jeq2001.302275x
    [11]
    Ding J, Liu C, Luo SY, Zhang YB, Gao XM, Wu XF, et al. 2020. Transcriptome and physiology analysis identify key metabolic changes in the liver of the large yellow croaker (Larimichthys crocea) in response to acute hypoxia. Ecotoxicology and Environmental Safety, 189: 109957. doi: 10.1016/j.ecoenv.2019.109957
    [12]
    Domarecka E, Skarzynska M, Szczepek AJ, Hatzopoulos S. 2020. Use of zebrafish larvae lateral line to study protection against cisplatin-induced ototoxicity: a scoping review. International Journal of Immunopathology and Pharmacology, 34: 2058738420959554.
    [13]
    Doughan AK, Harrison DG, Dikalov SI. 2008. Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circulation Research, 102(4): 488−496. doi: 10.1161/CIRCRESAHA.107.162800
    [14]
    Drummond GR, Selemidis S, Griendling KK, Sobey CG. 2011. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nature Reviews Drug Discovery, 10(6): 453−471. doi: 10.1038/nrd3403
    [15]
    Ezeriņa D, Takano Y, Hanaoka K, Urano Y, Dick TP. 2018. N-acetyl cysteine functions as a fast-acting antioxidant by triggering intracellular H2S and sulfane sulfur production. Cell Chemical Biology, 25(4): 447−459.e4. doi: 10.1016/j.chembiol.2018.01.011
    [16]
    Fishery Administration of the Ministry of Agriculture and Rural Areas, National Fisheries Technology Extension Center, China Society of Fisheries. 2020. China Fishery Statistical Yearbook 2020. Beijing: China Agricultural Press. (in Chinese)
    [17]
    Fransen M, Nordgren M, Wang B, Apanasets O. 2012. Role of peroxisomes in ROS/RNS-metabolism: implications for human disease. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, 1822(9): 1363−1373. doi: 10.1016/j.bbadis.2011.12.001
    [18]
    Gimenez M, Schickling BM, Lopes LR, Miller FJ Jr. 2016. Nox1 in cardiovascular diseases: regulation and pathophysiology. Clinical Science, 130(3): 151−165. doi: 10.1042/CS20150404
    [19]
    Gong YS, Hu K, Yang LQ, Guo J, Gao YQ, Song FL, et al. 2017. Comparative effects of EtOH consumption and thiamine deficiency on cognitive impairment, oxidative damage, and β-amyloid peptide overproduction in the brain. Free Radical Biology and Medicine, 108: 163−173. doi: 10.1016/j.freeradbiomed.2017.03.019
    [20]
    Guérin P, El Mouatassim S, Ménézo Y. 2001. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Human Reproduction Update, 7(2): 175−189. doi: 10.1093/humupd/7.2.175
    [21]
    Gurunathan S, Jeyaraj M, Kang MH, Kim JH. 2020. Melatonin enhances palladium-nanoparticle-induced cytotoxicity and apoptosis in human lung epithelial adenocarcinoma cells A549 and H1229. Antioxidants, 9(4): 357. doi: 10.3390/antiox9040357
    [22]
    Guzy RD, Hoyos B, Robin E, Chen H, Liu LP, Mansfield KD, et al. 2005. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metabolism, 1(6): 401−408. doi: 10.1016/j.cmet.2005.05.001
    [23]
    Hansen T, Galougahi KK, Celermajer D, Rasko N, Tang O, Bubb KJ, et al. 2016. Oxidative and nitrosative signalling in pulmonary arterial hypertension — Implications for development of novel therapies. Pharmacology & Therapeutics, 165: 50−62.
    [24]
    Hernansanz-Agustín P, Ramos E, Navarro E, Parada E, Sánchez-López N, Peláez-Aguado L, et al. 2017. Mitochondrial complex I deactivation is related to superoxide production in acute hypoxia. Redox Biology, 12: 1040−1051. doi: 10.1016/j.redox.2017.04.025
    [25]
    Holowiecki A, O'Shields B, Jenny MJ. 2017. Spatiotemporal expression and transcriptional regulation of heme oxygenase and biliverdin reductase genes in zebrafish (Danio rerio) suggest novel roles during early developmental periods of heightened oxidative stress. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 191: 138−151.
    [26]
    Jastroch M, Divakaruni AS, Mookerjee S, Treberg JR, Brand MD. 2010. Mitochondrial proton and electron leaks. Essays in Biochemistry, 47: 53−67. doi: 10.1042/bse0470053
    [27]
    Kigawa G, Nakano H, Kumada K, Kitamura N, Takeuchi S, Hatakeyama T, et al. 2000. Improvement of portal flow and hepatic microcirculatory tissue flow with N-acetylcysteine in dogs with obstructive jaundice produced by bile duct ligation. The European Journal of Surgery, 166(1): 77−84. doi: 10.1080/110241500750009753
    [28]
    Kim I, Rodriguez-Enriquez S, Lemasters JJ. 2007. Selective degradation of mitochondria by mitophagy. Archives of Biochemistry and Biophysics, 462(2): 245−253. doi: 10.1016/j.abb.2007.03.034
    [29]
    Klein JA, Ackerman SL. 2003. Oxidative stress, cell cycle, and neurodegeneration. The Journal of Clinical Investigation, 111(6): 785−793. doi: 10.1172/JCI200318182
    [30]
    Labunskyy VM, Hatfield DL, Gladyshev VN. 2014. Selenoproteins: molecular pathways and physiological roles. Physiological Reviews, 94(3): 739−777. doi: 10.1152/physrev.00039.2013
    [31]
    Leng N, Dawson JA, Thomson JA, Ruotti V, Rissman AI, Smits BMG, et al. 2013. EBSeq: an empirical bayes hierarchical model for inference in RNA-seq experiments. Bioinformatics, 29(8): 1035−1043. doi: 10.1093/bioinformatics/btt087
    [32]
    Leonarduzzi G, Sottero B, Poli G. 2010. Targeting tissue oxidative damage by means of cell signaling modulators: the antioxidant concept revisited. Pharmacology & Therapeutics, 128(2): 336−374.
    [33]
    Leung TM, Nieto N. 2013. CYP2E1 and oxidant stress in alcoholic and non-alcoholic fatty liver disease. Journal of Hepatology, 58(2): 395−398. doi: 10.1016/j.jhep.2012.08.018
    [34]
    Liu L, Tu X, Shen YF, Chen WC, Zhu B, Wang GX. 2017. The replication of spring viraemia of carp virus can be regulated by reactive oxygen species and NF-κB pathway. Fish & Shellfish Immunology, 67: 211−217.
    [35]
    Liu W, Liu XX, Wu CW, Jiang LH. 2018. Transcriptome analysis demonstrates that long noncoding RNA is involved in the hypoxic response in Larimichthys crocea. Fish Physiology and Biochemistry, 44(5): 1333−1347. doi: 10.1007/s10695-018-0525-x
    [36]
    Lu JM, Risbood P, Kane CT Jr, Hossain MT, Anderson L, Hill K, et al. 2017. Characterization of potent and selective iodonium-class inhibitors of NADPH oxidases. Biochemical Pharmacology, 143: 25−38. doi: 10.1016/j.bcp.2017.07.007
    [37]
    Lu Q, Wainwright MS, Harris VA, Aggarwal S, Hou YL, Rau T, et al. 2012. Increased NADPH oxidase-derived superoxide is involved in the neuronal cell death induced by hypoxia-ischemia in neonatal hippocampal slice cultures. Free Radical Biology and Medicine, 53(5): 1139−1151. doi: 10.1016/j.freeradbiomed.2012.06.012
    [38]
    Luo SY, Gao XM, Ding J, Liu C, Du C, Hou CC, et al. 2019. Transcriptome sequencing reveals the traits of spermatogenesis and testicular development in large yellow croaker (Larimichthys crocea). Genes, 10(12): 958. doi: 10.3390/genes10120958
    [39]
    Lushchak VI, Bagnyukova TV, Lushchak OV, Storey JM, Storey KB. 2005. Hypoxia and recovery perturb free radical processes and antioxidant potential in common carp (Cyprinus carpio) tissues. The International Journal of Biochemistry & Cell Biology, 37(6): 1319−1330.
    [40]
    Mahfouz ME, Hegazi MM, El-Magd MA, Kasem EA. 2015. Metabolic and molecular responses in Nile tilapia, Oreochromis niloticus during short and prolonged hypoxia. Marine and Freshwater Behaviour and Physiology, 48(5): 319−340. doi: 10.1080/10236244.2015.1055915
    [41]
    Mani AR, Ippolito S, Ollosson R, Moore KP. 2006. Nitration of cardiac proteins is associated with abnormal cardiac chronotropic responses in rats with biliary cirrhosis. Hepatology, 43(4): 847−856. doi: 10.1002/hep.21115
    [42]
    Martínez ML, Raynard EL, Rees BB, Chapman LJ. 2011. Oxygen limitation and tissue metabolic potential of the African fish Barbus neumayeri: roles of native habitat and acclimatization. BMC Ecology, 11(1): 2. doi: 10.1186/1472-6785-11-2
    [43]
    Meneshian A, Bulkley GB. 2002. The physiology of endothelial xanthine oxidase: from urate catabolism to reperfusion injury to inflammatory signal transduction. Microcirculation, 9(3): 161−175. doi: 10.1038/sj.mn.7800136
    [44]
    Ming JH, Ye JY, Zhang YX, Yang X, Shao XP, Qiang J, et al. 2019. Dietary optimal reduced glutathione improves innate immunity, oxidative stress resistance and detoxification function of grass carp (Ctenopharyngodon idella) against microcystin-LR. Aquaculture, 498(1): 594−605.
    [45]
    Mukhopadhyay P, Horváth B, Zsengellėr Z, Bátkai S, Cao ZX, Kechrid M, et al. 2012. Mitochondrial reactive oxygen species generation triggers inflammatory response and tissue injury associated with hepatic ischemia-reperfusion: therapeutic potential of mitochondrially targeted antioxidants. Free Radical Biology and Medicine, 53(5): 1123−1138. doi: 10.1016/j.freeradbiomed.2012.05.036
    [46]
    Mustafa SA, Al-Subiai SN, Davies SJ, Jha AN. 2011. Hypoxia-induced oxidative DNA damage links with higher level biological effects including specific growth rate in common carp, Cyprinus carpio L. Ecotoxicology, 20(6): 1455−1466. doi: 10.1007/s10646-011-0702-5
    [47]
    Nordberg J, Arnér ESJ. 2001. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radical Biology and Medicine, 31(11): 1287−1312. doi: 10.1016/S0891-5849(01)00724-9
    [48]
    Oró D, Yudina T, Fernández-Varo G, Casals E, Reichenbach V, Casals G, et al. 2016. Cerium oxide nanoparticles reduce steatosis, portal hypertension and display anti-inflammatory properties in rats with liver fibrosis. Journal of Hepatology, 64(3): 691−698. doi: 10.1016/j.jhep.2015.10.020
    [49]
    Pacher P, Beckman JS, Liaudet L. 2007. Nitric oxide and peroxynitrite in health and disease. Physiological Reviews, 87(1): 315−424. doi: 10.1152/physrev.00029.2006
    [50]
    Rahman MS, Thomas P. 2011. Characterization of three IGFBP mRNAs in Atlantic croaker and their regulation during hypoxic stress: potential mechanisms of their upregulation by hypoxia. American Journal of Physiology: Endocrinology and Metabolism, 301(4): E637−E648. doi: 10.1152/ajpendo.00168.2011
    [51]
    Rahman MS, Thomas P. 2017. Molecular and biochemical responses of hypoxia exposure in Atlantic croaker collected from hypoxic regions in the northern Gulf of Mexico. PLoS One, 12(9): e0184341. doi: 10.1371/journal.pone.0184341
    [52]
    Saxena S, Vekaria H, Sullivan PG, Seifert AW. 2019. Connective tissue fibroblasts from highly regenerative mammals are refractory to ROS-induced cellular senescence. Nature Communications, 10(1): 4400. doi: 10.1038/s41467-019-12398-w
    [53]
    Schulte PM. 2014. What is environmental stress? Insights from fish living in a variable environment. Journal of Experimental Biology, 217(1): 23−34. doi: 10.1242/jeb.089722
    [54]
    Selvaraj V, Yeager-Armstead M, Murray E. 2012. Protective and antioxidant role of selenium on arsenic trioxide-induced oxidative stress and genotoxicity in the fish hepatoma cell line PLHC-1. Environmental Toxicology and Chemistry, 31(12): 2861−2869. doi: 10.1002/etc.2022
    [55]
    Sommer N, Pak O, Schörner S, Derfuss T, Krug A, Gnaiger E, et al. 2010. Mitochondrial cytochrome redox states and respiration in acute pulmonary oxygen sensing. European Respiratory Journal, 36: 1056−1066. doi: 10.1183/09031936.00013809
    [56]
    Sommer N, Strielkov I, Pak O, Weissmann N. 2016. Oxygen sensing and signal transduction in hypoxic pulmonary vasoconstriction. European Respiratory Journal, 47(1): 288−303. doi: 10.1183/13993003.00945-2015
    [57]
    Suzuki S, Pitchakarn P, Sato S, Shirai T, Takahashi S. 2013. Apocynin, an NADPH oxidase inhibitor, suppresses progression of prostate cancer via Rac1 dephosphorylation. Experimental and Toxicologic Pathology, 65(7–8): 1035−1041.
    [58]
    Szeto HH. 2008. Mitochondria-targeted cytoprotective peptides for ischemia-reperfusion injury. Antioxidants & Redox Signaling, 10(3): 601−619.
    [59]
    Tezel G. 2006. Oxidative stress in glaucomatous neurodegeneration: mechanisms and consequences. Progress in Retinal and Eye Research, 25(5): 490−513. doi: 10.1016/j.preteyeres.2006.07.003
    [60]
    Viscomi C, Burlina AB, Dweikat I, Savoiardo M, Lamperti C, Hildebrandt T, et al. 2010. Combined treatment with oral metronidazole and N-acetylcysteine is effective in ethylmalonic encephalopathy. Nature Medicine, 16(8): 869−871. doi: 10.1038/nm.2188
    [61]
    Wang QF, Shen WL, Hou CC, Liu C, Wu XF, Zhu JQ. 2017. Physiological responses and changes in gene expression in the large yellow croaker Larimichthys crocea following exposure to hypoxia. Chemosphere, 169: 418−427. doi: 10.1016/j.chemosphere.2016.11.099
    [62]
    Waypa GB, Chandel NS, Schumacker PT. 2001. Model for hypoxic pulmonary vasoconstriction involving mitochondrial oxygen sensing. Circulation Research, 88(12): 1259−1266. doi: 10.1161/hh1201.091960
    [63]
    Wischhusen P, Larroquet L, Durand T, Oger C, Galano JM, Rocher A, et al. 2020. Oxidative stress and antioxidant response in rainbow trout fry exposed to acute hypoxia is affected by selenium nutrition of parents and during first exogenous feeding. Free Radical Biology and Medicine, 155: 99−113. doi: 10.1016/j.freeradbiomed.2020.05.006
    [64]
    Yang S, Yan T, Wu H, Xiao Q, Fu HM, Luo J, et al. 2017. Acute hypoxic stress: effect on blood parameters, antioxidant enzymes, and expression of HIF-1alpha and GLUT-1 genes in largemouth bass (Micropterus salmoides). Fish & Shellfish Immunology, 67: 449−458.
    [65]
    Yang YT, Wang Z, Wang J, Lyu FM, Xu KX, Mu WJ. 2021. Histopathological, hematological, and biochemical changes in high-latitude fish Phoxinus lagowskii exposed to hypoxia. Fish Physiology and Biochemistry, 47(4): 919−938. doi: 10.1007/s10695-021-00947-4
    [66]
    Zhang GS, Mao JQ, Liang FF, Chen JW, Zhao C, Yin SW, et al. 2016. Modulated expression and enzymatic activities of Darkbarbel catfish, Pelteobagrus vachelli for oxidative stress induced by acute hypoxia and reoxygenation. Chemosphere, 151: 271−279. doi: 10.1016/j.chemosphere.2016.02.072
    [67]
    Zhao KS, Zhao GM, Wu DL, Soong Y, Birk AV, Schiller PW, et al. 2004. Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial swelling, oxidative cell death, and reperfusion injury. The Journal of Biological Chemistry, 279(33): 34682−34690. doi: 10.1074/jbc.M402999200
    [68]
    Zhao LL, Cui C, Liu Q, Sun JL, He K, Adam AA, et al. 2020. Combined exposure to hypoxia and ammonia aggravated biological effects on glucose metabolism, oxidative stress, inflammation and apoptosis in largemouth bass (Micropterus salmoides). Aquatic Toxicology, 224: 105514. doi: 10.1016/j.aquatox.2020.105514
  • ZR-2021-079 Supplementary Materials.zip
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(7)  / Tables(1)

    Article Metrics

    Article views (695) PDF downloads(100) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return