Research Studies
Study Tracker
Combined Effects of Fluoride and Dietary Seleno-L-Methionine at Environmentally Relevant Concentrations on Female Zebrafish (Danio rerio) Liver: Histopathological Damages, Oxidative Stress and Inflammation.Abstract
Original abstract online at
https://link.springer.com/article/10.1007/s12011-023-03837-3
Fluoride, a global environmental pollutant, is ubiquitous in aquatic environments and coexists with selenium, which can cause complex effects on exposed organisms. However, data on the interaction of fluoride and selenium remain scarce. In this study, female zebrafish (Danio rerio) were exposed to fluoride (80 mg/L sodium fluoride) and/or dietary selenomethionine (Se-Met) for 30, 60 and 90 days, the effects on the liver of zebrafish were investigated. The results indicated that an increase in fluoride burden, inhibited growth and impaired liver morphology were recorded after fluoride exposure. Furthermore, fluoride alone caused oxidative stress and inflammation in the liver, as reflected by the increase in ROS and MDA contents, the reduction of anti-oxidative enzymes, the altered immune related enzymes (ACP, AKP, LZM and MPO) and the expression of IL-6, IL-1B, TNF-a, IL-10 and TGF-B. In contrast, co-exposure to fluoride and Se-Met decreased fluoride burden and restored growth. Furthermore, dietary Se-Met alleviated oxidative stress, inflammation and impaired morphology in liver trigger by fluoride. However, dietary Se-Met alone increased the activities of SOD and CAT. These results demonstrate that the protective effect of dietary Se-Met against chronic fluoride toxicity at a certain level.
Data Availability
The datasets used in the current study are available from the corresponding author on reasonable request.
References
-
Chen J, Xue W, Cao J, Song J, Jia R, Li M (2016) Fluoride caused thyroid endocrine disruption in male zebrafish (Danio rerio). Aquat Toxicol 171:48–58. https://doi.org/10.1016/j.aquatox.2015.12.010
-
Cao J, Feng C, Xie L, Li L, Chen J, Yun S, Guo W, Wang T, Wu Y, Meng R (2020) Sesamin attenuates histological alterations, oxidative stress and expressions of immune-related genes in liver of zebrafish (Danio rerio) exposed to fluoride. Fish Shellfish Immun 106:715–723. https://doi.org/10.1016/j.fsi.2020.08.039
-
Fawell J, Bailey K, Chilton J, Dahi E, Magara Y (2013) Fluoride in drinking-water. 12: 10–20. https://doi.org/10.2166/9781780405803
-
Tian L, Zhu X, Wang L, Peng F, Xu B (2021) Distribution, occurrence mechanisms, and management of high fluoride levels in the water, sediment, and soil of Shahu Lake, China. Appl Geochem 126(4):104869. https://doi.org/10.1016/j.apgeochem.2021.104869
-
Firdous MN (2007) Toxic fluoride and arsenic contaminated groundwater in the Lahore and Kasur districts, Punjab, Pakistan and possible contaminant sources. Environ Pollut 145:839–849. https://doi.org/10.1016/j.envpol.2006.05.007
-
Shamsuddin MKN, Suratman S, Ramli MF, Sulaiman WNA, Sefie A (2016) Hydrochemical assessment of surfacewater and groundwater quality at bank infiltration site. IOP Conf Series 136(1):12073. https://doi.org/10.1088/1757-899X/136/1/012073
-
Tekle-Haimanot R, Melaku Z, Kloos H, Reimann C, Fantaye W, Zerihun L, Bjorvatn K (2006) The geographic distribution of fluoride in surface and groundwater in Ethiopia with an emphasis on the Rift Valley. Sci Total Environ 367(1):182–190. https://doi.org/10.1016/j.scitotenv.2005.11.003
-
Wang X, Bo X, Yao Q, Wu M, Wang H (2019) The effect of fluorine exposure on morphological indicators and intestinal microbial community in Bufo gargarizans tadpoles. Ecol Indic 98:763–771. https://doi.org/10.1016/j.ecolind.2018.11.070
-
Li M, Cao J, Zhao Y, Wu P, Li X, Khodaei F, Han Y, Wang J (2020) Fluoride impairs ovary development by affecting oogenesis and inducing oxidative stress and apoptosis in female zebrafish (Danio rerio). Chemosphere 256:127105. https://doi.org/10.1016/j.chemosphere.2020.127105
-
Chen J, Luo Y, Cao J, Xie L (2021) Fluoride exposure changed the expression of microRNAs in gills of male zebrafish (Danio rerio). Aquat Toxicol 233(2):105789. https://doi.org/10.1016/j.aquatox.2021.105789
-
Fan Y, Su J, Wang Z, Deng L, Zhang H (2021) Impact of C/N ratio on the fate of simultaneous Ca2+ precipitation, F– removal, and denitrification in quartz sand biofilm reactor. Chemosphere 273:129667. https://doi.org/10.1016/j.chemosphere.2021.129667
-
Lomonosov IS, Grebenshchikova VI, Sklyarova OA, Bryukhanova NN, Noskov DA, Yanovskii LM, Didenkov YN (2011) Toxic (mercury, berillium) and biogenic (selenium, fluorine) elements in aquatic ecosystems of Baikal Natural Territory. Water Resour 38(2):199–210. https://doi.org/10.1134/S0097807811020084
-
Njuguna SM, Onyango JA, Githaiga KB, Gituru RW, Yan X (2020) Application of multivariate statistical analysis and water quality index in health risk assessment by domestic use of river water. Case study of tana river in Kenya. Process Saf Environ 133:149–158. https://doi.org/10.1016/j.psep.2019.11.006
-
Han S, Li F, Wang S, Li H, Yuan L, Liu J, Shen H, Zhang X, Li C, Wu X (2021) Groundwater resource and eco-environmental problem of the Yellow River Basin. China Geol. 48(4):1001–1019. https://doi.org/10.12029/gc20210402
-
Peckham S, Awofeso N (2014) Water fluoridation: a critical review of the physiological effects of ingested fluoride as a public health intervention. Sci World J 26:293019. https://doi.org/10.1155/2014/293019
-
Wang X, Yang Y, Zhang H, Liu J (2017) Safety assessment and comparison of sodium selenite and bioselenium obtained from yeast in mice. Biomed Res Int 2017:3980972. https://doi.org/10.1155/2017/3980972
-
Xie L, Wu X, Chen H, Dong W, Cazan AM, Klerks PL (2016) A low level of dietary selenium has both beneficial and toxic effects and is protective against Cd-toxicity in the least killifish Heterandria formosa. Chemosphere 161:358–364. https://doi.org/10.1016/j.chemosphere.2016.07.035
-
Jamwal A, Lemire D, Driessnack M, Naderi M, Niyogi S (2018) Interactive effects of chronic dietary selenomethionine and cadmium exposure in rainbow trout (Oncorhynchus mykiss): a preliminary study. Chemosphere 197:550–559. https://doi.org/10.1016/j.chemosphere.2018.01.087
-
Liu H, Li X, Lei H, Li D, Chen H, Schlenk D, Yan B, Yongju L, Xie L (2021) Dietary seleno-l-methionine alters the microbial communities and causes damage in the gastrointestinal tract of Japanese Medaka Oryzias latipes. Environ Sci Technol 55(24):16515–16525. https://doi.org/10.1021/acs.est.1c04533
-
Cogun HY, F?rat Ö, F?rat Ö, Yüzerero?lu TA, Gök G, Kargin F, Kötemen Y (2012) Protective effect of selenium against mercury-induced toxicity on hematological and biochemical parameters of Oreochromis niloticus. J Biochem Mol Toxic 26(3):117–122. https://doi.org/10.1002/jbt.20417
-
Zhang X, Chen J, Wang G, Chen H, Cao J, Xie L, Luo Y (2022) Interactive effects of fluoride and seleno-l-methionine at environmental related concentrations on zebrafish (Danio rerio) liver via the gut-liver axis. Fish Shellfish Immunol 127:690–702. https://doi.org/10.1016/j.fsi.2022.07.006
-
Zhao Y, Wang J, Zhang J, Sun Z, Niu R, Manthari RK, Ommati MM, Wang S, Wang J (2022) Fluoride exposure induces mitochondrial damage and mitophagy via activation of the IL-17A pathway in hepatocytes. Sci Total Environ 804:150184. https://doi.org/10.1016/j.scitotenv.2021.150184
-
Barbier O, Arreola-Mendoza L, Del Razo LM (2010) Molecular mechanisms of fluoride toxicity. Chem-Biol Interact 188(2):319–333. https://doi.org/10.1016/j.cbi.2010.07.011
-
Agalakova NI, Gusev GP (2012) Fluoride induces oxidative stress and ATP depletion in the rat erythrocytes in vitro. Environ Toxicol Pharmacol 34(2):334–337. https://doi.org/10.1016/j.etap.2012.05.006
-
Cao J, Chen J, Wang J, Jia R, Xue W, Luo Y, Gan X (2013) Effects of fluoride on liver apoptosis and Bcl-2, Bax protein expression in freshwater teleost, Cyprinus carpio. Chemosphere 91(8):1203–1212. https://doi.org/10.1016/j.chemosphere.2013.01.037
-
Elia AC, Prearo M, Pacini N, Dörr AJM, Abete MC (2011) Effects of selenium diets on growth, accumulation and antioxidant response in juvenile carp. Ecotox Environ Safe 74(2):166–173. https://doi.org/10.1016/j.ecoenv.2010.04.006
-
Wang G, Wang T, Zhang X, Chen J, Feng C, Yun S, Cheng Y, Cheng F, Cao J (2022) Sex-specific effects of fluoride and lead exposures on histology, antioxidant physiology, and immune system in the liver of zebrafish (Danio rerio). Ecotoxicology 31(3):396–414. https://doi.org/10.1007/s10646-022-02519-5
-
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101–1108. https://doi.org/10.1038/nprot.2008.73
-
Camargo JA (2003) Fluoride toxicity to aquatic organisms: a review. Chemosphere 50(3):251–264. https://doi.org/10.1016/s0045-6535(02)00498-8
-
Wu Y, Zhang X, Chen J, Cao J, Feng C, Luo Y, Lin Y (2022) Self-recovery study of fluoride-induced ferroptosis in the liver of zebrafish (Danio rerio). Aquat Toxicol 251:106275. https://doi.org/10.1016/j.aquatox.2022.106275
-
Dang F, Wang WX (2011) Antagonistic interaction of mercury and selenium in a marine fish is dependent on their chemical species. Environ Sci Technol 45(7):3116–3122. https://doi.org/10.1021/es103705a
-
Du X, Li H, Wang Z, Qiu S, Liu Q, Ni J (2013) Selenoprotein P and selenoprotein M block Zn2+-mediated A?42 aggregation and toxicity. Metallomics 5(7):861–870. https://doi.org/10.1039/c3mt20282h
-
Khan MA, Wang F (2009) Mercury-selenium compounds and their toxicological significance: toward a molecular understanding of the mercury-selenium antagonism. Environ Toxicol Chem 28(8):1567–1577. https://doi.org/10.1897/08-375.1
-
Guo J, Wu P, Cao J, Luo Y, Chen J, Wang G, Guo W, Wang T, He X (2019) The PFOS disturbed immunomodulatory functions via nuclear Factor-?B signaling in liver of zebrafish (Danio rerio). Fish Shellfish Immun 91:87–98. https://doi.org/10.1016/j.fsi.2019.05.018
-
Zhuang S, Feng Z, Chen L, Wang WR (2009) Growth inhibition of siberian sturgeon (Acipenser Baerii) from dietary and waterborne fluoride. Fluoride 42(2):137–141. https://doi.org/10.1093/eurpub/ckp037
-
Chen J, Cao J, Wang J, Jia R, Xue W, Li Y, Luo Y, Xie L (2013) Effects of fluoride on growth, body composition, and serum biochemical profile in a freshwater teleost, Cyprinus carpio. Environ Toxicol Chem 32(10):2315–2321. https://doi.org/10.1002/etc.2305
-
Yoshitomi B, Nagano I (2012) Effect of dietary fluoride derived from Antarctic krill (Euphausia superba) meal on growth of yellowtail (Seriola quinqueradiata). Chemosphere 86(9):891–897. https://doi.org/10.1016/j.chemosphere.2011.10.042
-
Zhang X, Wang G, Wang T, Chen J, Feng C, Yun S, Cheng Y, Cheng F, Cao J (2022) Selenomethionine alleviated fluoride-induced toxicity in zebrafish (Danio rerio) embryos by restoring oxidative balance and rebuilding inflammation homeostasis. Aquat Toxicol 242:106019. https://doi.org/10.1016/j.aquatox.2021.106019
-
Saffari S, Keyvanshokooh S, Zakeri M, Johari SA, Pasha Zanoosi H (2017) Effects of different dietary selenium sources (sodium selenite, selenomethionine and nanoselenium) on growth performance, muscle composition, blood enzymes and antioxidant status of common carp (Cyprinus carpio). Aquacult Nutr 23(3):611–617. https://doi.org/10.1111/anu.12428
-
Neamat-Allah A, Mahmoud EA, Abd EH (2019) Efficacy of dietary nano-selenium on growth, immune response, antioxidant, transcriptomic profile and resistance of Nile tilapia, Oreochromis niloticus against Streptococcus iniae infection. Fish Shellfish Immun 94:280–287. https://doi.org/10.1016/j.fsi.2019.09.019
-
Chen H, Li J, Yan L, Cao J, Li D, Huang G, Shi W, Dong W, Zha J, Ying G (2020) Subchronic effects of dietary selenium yeast and selenite on growth performance and the immune and antioxidant systems in Nile tilapia Oreochromis niloticus. Fish Shellfish Immun 97:283–293. https://doi.org/10.1016/j.fsi.2019.12.053
-
Li X, Liu H, Li D, Lei H, Wei X, Schlenk D, Mu J, Chen H, Yan B, Xie L (2021) Dietary seleno-l-methionine causes alterations in neurotransmitters, ultrastructure of the brain, and behaviors in zebrafish (Danio rerio). Environ Sci Technol 55(17):11894–11905. https://doi.org/10.1021/acs.est.1c03457
-
Zuo H, Chen L, Kong M, Qiu L, Wu P, Yang Y, Chen K (2018) Toxic effects of fluoride on organisms. Life Sci 198:18–24. https://doi.org/10.1016/j.lfs.2018.02.001
-
Yu YM, Zhou BH, Yang YL, Guo CX, Zhao J, Wang HW (2022) Estrogen deficiency aggravates fluoride-induced liver damage and lipid metabolism disorder in rats. Biol Trace Elem Res 200(6):2767–2776. https://doi.org/10.1007/s12011-021-02857-1
-
Flora SJ, Mittal M (2015) Preventing fluoride toxicity with selenium. Fluorine 18:308–326. https://doi.org/10.1039/9781782628507-00308
-
Xie Z, Luan H, Zhang Y, Wang M, Cao D, Yang J, Tang J, Fan S, Wu X, Hua R (2020) Interactive effects of diclofenac and copper on bioconcentration and multiple biomarkers in crucian carp (Carassius auratus). Chemosphere 242:125141. https://doi.org/10.1016/j.chemosphere.2019.125141
-
Ahmed NF, Sadek KM, Soliman MK, Khalil RH, Khafaga AF, Ajarem JS, Maodaa SN, Allam AA (2020) Moringa Oleifera leaf extract repairs the oxidative misbalance following sub-chronic exposure to sodium fluoride in Nile Tilapia Oreochromis niloticus. Animals (Basel) 10(4):626. https://doi.org/10.3390/ani10040626
-
Yadav SS, Kumar R, Khare P, Tripathi M (2015) Oxidative stress biomarkers in the freshwater fish, heteropneustes fossilis (Bloch) exposed to sodium fluoride: antioxidant defense and role of ascorbic acid. Toxicol Int 22(1):71–76. https://doi.org/10.4103/0971-6580.172261
-
Limwachirakhom R, Triwutanon S, Chumkam S, Jintasataporn O (2022) Effects of chromium-L-methionine in combination with a zinc amino acid complex or selenomethionine on growth performance, intestinal morphology, and antioxidative enzymes in red Tilapia Oreochromis spp. Animals (Basel) 12(17):2182. https://doi.org/10.3390/ani12172182
-
Gao J, Tian X, Yan X, Wang Y, Wei J, Wang X, Yan X, Song G (2021) Selenium exerts protective effects against fluoride-induced apoptosis and oxidative stress and altered the expression of Bcl-2/caspase family. Biol Trace Elem Res 199(2):682–692. https://doi.org/10.1007/s12011-020-02185-w
-
Wang X, Shen Z, Wang C, Li E, Qin JG, Chen L (2019) Dietary supplementation of selenium yeast enhances the antioxidant capacity and immune response of juvenile Eriocheir Sinensis under nitrite stress. Fish Shellfish Immun 87:22–31. https://doi.org/10.1016/j.fsi.2018.12.076
-
Yu X, Hussein S, Li L, Liu Q, Ban Z, Jiang H (2022) Effect of dihydroquercetin on energy metabolism in LPS-induced inflammatory mice. Biomed Res Int 2022:6491771. https://doi.org/10.1155/2022/6491771
-
Wang H, Tan JT, Emelyanov A, Korzh V, Gong Z (2005) Hepatic and extrahepatic expression of vitellogenin genes in the zebrafish, Danio rerio. Gene 356:91–100. https://doi.org/10.1016/j.gene.2005.03.041
-
Kim SH, Johnson VJ, Shin TY, Sharma RP (2004) Selenium attenuates lipopolysaccharide-induced oxidative stress responses through modulation of p38 MAPK and NF-kappaB signaling pathways. Exp Biol Med 229(2):203–213. https://doi.org/10.1177/153537020422900209
Funding
This work was supported by the Shanxi Provincial Central Leading Local Science and Technology Development Fund Project (YDZJSX20231A043), the Shanxi Scholarship Council of China (2020–061), the Shanxi Provincial Key Research and Development Project (201903D221009), the earmarked fund for Modern Agro-industry Technology Research System (2022HX027), and the National Natural Science Foundation of China (31502141; 31440087).
Ethics declarations
Competing interests
The authors declare no competing interests.
Conflict of Interest
The authors declare no competing interests.
Supplementary Information
Below is the link to the electronic supplementary material.
