Volume 13 Issue 1
Jan.  2023
Turn off MathJax
Article Contents
WANG J,YAN Z G,ZHANG T X,et al.Chronic toxic effects of BDE-209 on the intestinal tract of zebrafish (Danio Rerio)[J].Journal of Environmental Engineering Technology,2023,13(1):413-422 doi: 10.12153/j.issn.1674-991X.20210869
Citation: WANG J,YAN Z G,ZHANG T X,et al.Chronic toxic effects of BDE-209 on the intestinal tract of zebrafish (Danio Rerio)[J].Journal of Environmental Engineering Technology,2023,13(1):413-422 doi: 10.12153/j.issn.1674-991X.20210869

Chronic toxic effects of BDE-209 on the intestinal tract of zebrafish (Danio Rerio)

doi: 10.12153/j.issn.1674-991X.20210869
  • Received Date: 2021-12-29
  • Taking the model organism zebrafish (Danio Rerio) as the research object, the toxic effects and molecular mechanism of chronic exposure of decabromodiphenyl ether (BDE-209) on intestinal tissue were explored. Zebrafish were exposed to different concentrations of BDE-209 (6, 60, and 600 μg/L, dimethyl sulfoxide solvent control) for 28 d. The intestinal tissue of zebrafish was pathologically examined by hematoxylin-eosin (H & E) staining. The contents of biomarkers related to oxidative stress and inflammatory response in the intestine were analyzed by biochemical indicators and ELISA experiments. The relative expression of genes related to the intestinal barrier, inflammatory response, and apoptosis was analyzed by real-time qPCR. The results showed that BDE-209 exposure resulted in thinning of the intestinal wall, increase of vacuolation in intestinal villi and external longitudinal muscle, damage of intestinal wall and cilia, and down-regulation of intestinal ZO-1, Claudin-2, and Tjp2a mRNA relative expression to affect intestinal physical barrier function. BDE-209 exposure increased the contents of reactive oxygen species (ROS), malondialdehyde (MDA), catalase (CAT), and superoxide dismutase (SOD) in the intestine, indicating that BDE-209 exposure caused intestinal oxidative stress. In addition, BDE-209 exposure up-regulated the contents of pro-inflammatory cytokines tumor necrosis factor α (TNF-α) and interleukin 1β (IL-1β) and the content of lipopolysaccharide (LPS) in the intestine, leading to increased intestinal inflammatory response, and increased the expression of p53, Bax, Caspase3 gene and down-regulated Bcl2 gene expression, promoting the apoptosis of zebrafish intestine.

     

  • loading
  • [1]
    AKORTIA E, OKONKWO J O, LUPANKWA M, et al. A review of sources, levels, and toxicity of polybrominated diphenyl ethers (PBDEs) and their transformation and transport in various environmental compartments[J]. Environmental Reviews,2016,24(3):253-273. doi: 10.1139/er-2015-0081
    [2]
    SHAOYONG W K, ZHANG W R, WANG C Y, et al. BDE-209 caused gut toxicity through modulating the intestinal barrier, oxidative stress, autophagy, inflammation, and apoptosis in mice[J]. Science of the Total Environment,2021,776:146018. doi: 10.1016/j.scitotenv.2021.146018
    [3]
    WANG J, YAN Z G, ZHENG X, et al. Health risk assessment and development of human health ambient water quality criteria for PBDEs in China[J]. Science of the Total Environment,2021,799:149353. doi: 10.1016/j.scitotenv.2021.149353
    [4]
    WU Z N, HAN W, YANG X, et al. The occurrence of polybrominated diphenyl ether (PBDE) contamination in soil, water/sediment, and air[J]. Environmental Science and Pollution Research International,2019,26(23):23219-23241. doi: 10.1007/s11356-019-05768-w
    [5]
    SHARKEY M, HARRAD S, ABOU-ELWAFA ABDALLAH M, et al. Phasing-out of legacy brominated flame retardants: the UNEP Stockholm Convention and other legislative action worldwide[J]. Environment International,2020,144:106041. doi: 10.1016/j.envint.2020.106041
    [6]
    YANG M, QI H, JIA H L, et al. Polybrominated diphenyl ethers in air across China: levels, compositions, and gas-particle partitioning[J]. Environmental Science & Technology,2013,47(15):8978-8984.
    [7]
    MADDELA N R, VENKATESWARLU K, KAKARLA D, et al. Inevitable human exposure to emissions of polybrominated diphenyl ethers: a perspective on potential health risks[J]. Environmental Pollution,2020,266:115240. doi: 10.1016/j.envpol.2020.115240
    [8]
    WU Z N, HE C, HAN W, et al. Exposure pathways, levels and toxicity of polybrominated diphenyl ethers in humans: a review[J]. Environmental Research,2020,187:109531. doi: 10.1016/j.envres.2020.109531
    [9]
    GIBSON E A, SIEGEL E L, ENIOLA F, et al. Effects of polybrominated diphenyl ethers on child cognitive, behavioral, and motor development[J]. International Journal of Environmental Research and Public Health,2018,15(8):1636. doi: 10.3390/ijerph15081636
    [10]
    MAKEY C M, MCCLEAN M D, BRAVERMAN L E, et al. Polybrominated diphenyl ether exposure and reproductive hormones in North American men[J]. Reproductive Toxicology,2016,62:46-52. doi: 10.1016/j.reprotox.2016.04.009
    [11]
    CARY T L, ORTIZ-SANTALIESTRA M E, KARASOV W H. Immunomodulation in post-metamorphic northern leopard frogs, Lithobates pipiens, following larval exposure to polybrominated diphenyl ether[J]. Environmental Science & Technology,2014,48(10):5910-5919.
    [12]
    PEREIRA L C, CABRAL MIRANDA L F, FRANCO-BERNARDES M F, et al. Mitochondrial damage and apoptosis: key features in BDE-153-induced hepatotoxicity[J]. Chemico-Biological Interactions,2018,291:192-201. doi: 10.1016/j.cbi.2018.06.021
    [13]
    NOYES P D, HAGGARD D E, GONNERMAN G D, et al. Advanced morphological-behavioral test platform reveals neurodevelopmental defects in embryonic zebrafish exposed to comprehensive suite of halogenated and organophosphate flame retardants[J]. Toxicological Sciences:an Official Journal of the Society of Toxicology,2015,145(1):177-195. doi: 10.1093/toxsci/kfv044
    [14]
    ZHU Y P, LI X Y, LIU J H, et al. The effects of decabromodiphenyl ether on glycolipid metabolism and related signaling pathways in mice[J]. Chemosphere,2019,222:849-855. doi: 10.1016/j.chemosphere.2019.02.003
    [15]
    LI C Y, DEMPSEY J L, WANG D, et al. PBDEs altered gut microbiome and bile acid homeostasis in male C57BL/6 mice[J]. Drug Metabolism and Disposition:the Biological Fate of Chemicals,2018,46(8):1226-1240. doi: 10.1124/dmd.118.081547
    [16]
    SECOMBE K R, COLLER J K, GIBSON R J, et al. The bidirectional interaction of the gut microbiome and the innate immune system: implications for chemotherapy‐induced gastrointestinal toxicity[J]. International Journal of Cancer,2019,144(10):2365-2376. doi: 10.1002/ijc.31836
    [17]
    GUO P, WU C M. Gut microbiota brings a novel way to illuminate mechanisms of natural products in vivo[J]. Chinese Herbal Medicines,2017,9(4):301-306. doi: 10.1016/S1674-6384(17)60109-6
    [18]
    GONG X, LI X, BO A, et al. The interactions between gut microbiota and bioactive ingredients of traditional Chinese medicines: a review[J]. Pharmacological Research,2020,157:104824. doi: 10.1016/j.phrs.2020.104824
    [19]
    CHEN L G, HU C Y, LOK-SHUN LAI N, et al. Acute exposure to PBDEs at an environmentally realistic concentration causes abrupt changes in the gut microbiota and host health of zebrafish[J]. Environmental Pollution,2018,240:17-26. doi: 10.1016/j.envpol.2018.04.062
    [20]
    LUO T, WANG X Y, JIN Y X. Low concentrations of imidacloprid exposure induced gut toxicity in adult zebrafish (Danio rerio)[J]. Comparative Biochemistry and Physiology Part C:Toxicology & Pharmacology,2021,241:108972.
    [21]
    廖伟, 刘大庆, 冯承莲, 等.不同生长阶段斑马鱼对Cu2+的毒性响应差异[J]. 环境科学研究,2020,33(3):626-633.

    LIAO W, LIU D Q, FENG C L, et al. Difference in toxicity response of zebrafish to Cu2+ at different life stages[J]. Research of Environmental Sciences,2020,33(3):626-633.
    [22]
    BRUGMAN S. The zebrafish as a model to study intestinal inflammation[J]. Developmental & Comparative Immunology,2016,64:82-92.
    [23]
    宋志慧, 孙欣欣, 李捍东.斑马鱼对3种氯酚的富集作用及其SOD酶活性应激反应研究[J]. 环境工程技术学报,2014,4(4):287-292. doi: 10.3969/j.issn.1674-991X.2014.04.047

    SONG Z H, SUN X X, LI H D. Study on bioconcentration of three chlorophenols in zebrafish and SOD activity stress action[J]. Journal of Environmental Engineering Technology,2014,4(4):287-292. doi: 10.3969/j.issn.1674-991X.2014.04.047
    [24]
    CHEN Q, YU L Q, YANG L H, et al. Bioconcentration and metabolism of decabromodiphenyl ether (BDE-209) result in thyroid endocrine disruption in zebrafish larvae[J]. Aquatic Toxicology,2012,110/111:141-148. doi: 10.1016/j.aquatox.2012.01.008
    [25]
    LI W, ZHU L F, ZHA J M, et al. Effects of decabromodiphenyl ether (BDE-209) on mRNA transcription of thyroid hormone pathway and spermatogenesis associated genes in Chinese rare minnow (Gobiocypris rarus)[J]. Environmental Toxicology,2014,29(1):1-9. doi: 10.1002/tox.20767
    [26]
    LIVAK K J, SCHMITTGEN T D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method[J]. Methods,2001,25(4):402-408. doi: 10.1006/meth.2001.1262
    [27]
    ABBASI G, LI L, BREIVIK K. Global historical stocks and emissions of PBDEs[J]. Environmental Science & Technology,2019,53(11):6330-6340.
    [28]
    JING L, SUN Y M, WANG Y W, et al. Cardiovascular toxicity of decabrominated diphenyl ethers (BDE-209) and decabromodiphenyl ethane (DBDPE) in rats[J]. Chemosphere,2019,223:675-685. doi: 10.1016/j.chemosphere.2019.02.115
    [29]
    HAN Z H, LI Y F, ZHANG S H, et al. Prenatal transfer of decabromodiphenyl ether (BDE-209) results in disruption of the thyroid system and developmental toxicity in zebrafish offspring[J]. Aquatic Toxicology,2017,190:46-52. doi: 10.1016/j.aquatox.2017.06.020
    [30]
    LIANG R Y, CHEN J, SHI Y J, et al. Toxicological effects on earthworms (Eisenia fetida) exposed to sub-lethal concentrations of BDE-47 and BDE-209 from a metabolic point[J]. Environmental Pollution,2018,240:653-660. doi: 10.1016/j.envpol.2018.04.145
    [31]
    NIKLASSON L, SUNDH H, FRIDELL F, et al. Disturbance of the intestinal mucosal immune system of farmed Atlantic salmon (Salmo salar), in response to long-term hypoxic conditions[J]. Fish & Shellfish Immunology,2011,31(6):1072-1080.
    [32]
    CHANG X L, LI H, FENG J C, et al. Effects of cadmium exposure on the composition and diversity of the intestinal microbial community of common carp (Cyprinus carpio L.)[J]. Ecotoxicology and Environmental Safety,2019,171:92-98. doi: 10.1016/j.ecoenv.2018.12.066
    [33]
    CHANG X L, WANG X F, FENG J C, et al. Impact of chronic exposure to trichlorfon on intestinal barrier, oxidative stress, inflammatory response and intestinal microbiome in common carp (Cyprinus carpio L.)[J]. Environmental Pollution,2020,259:113846. doi: 10.1016/j.envpol.2019.113846
    [34]
    WANG Y H, WANG B B, WANG Q Q, et al. Intestinal toxicity and microbial community disorder induced by bisphenol F and bisphenol S in zebrafish[J]. Chemosphere,2021,280:130711. doi: 10.1016/j.chemosphere.2021.130711
    [35]
    SUN Y C, ZHANG J, SONG W T, et al. Vitamin E alleviates phoxim-induced toxic effects on intestinal oxidative stress, barrier function, and morphological changes in rats[J]. Environmental Science and Pollution Research International,2018,25(26):26682-26692. doi: 10.1007/s11356-018-2666-y
    [36]
    YU G J, OU W H, LIAO Z B, et al. Intestinal homeostasis of juvenile tiger puffer Takifugu rubripes was sensitive to dietary arachidonic acid in terms of mucosal barrier and microbiota[J]. Aquaculture,2019,502:97-106. doi: 10.1016/j.aquaculture.2018.12.020
    [37]
    DING Z L, KONG Y Q, SHAO X P, et al. Growth, antioxidant capacity, intestinal morphology, and metabolomic responses of juvenile Oriental River prawn (Macrobrachium nipponense) to chronic lead exposure[J]. Chemosphere,2019,217:289-297. doi: 10.1016/j.chemosphere.2018.11.034
    [38]
    YI H, ZHANG L, GAN Z, et al. High therapeutic efficacy of Cathelicidin-WA against postweaning diarrhea via inhibiting inflammation and enhancing epithelial barrier in the intestine[J]. Scientific Reports,2016,6:25679. doi: 10.1038/srep25679
    [39]
    CAPALDO C T, POWELL D N, KALMAN D. Layered defense: how mucus and tight junctions seal the intestinal barrier[J]. Journal of Molecular Medicine (Berlin, Germany),2017,95(9):927-934. doi: 10.1007/s00109-017-1557-x
    [40]
    曾晨, 郭少娟, 杨立新.汞、镉、铅、砷单一和混合暴露的毒性效应及机理研究进展[J]. 环境工程技术学报,2018,8(2):221-230. doi: 10.3969/j.issn.1674-991X.2018.02.030

    ZENG C, GUO S J, YANG L X. Toxic effects and mechanisms of exposure to single and mixture of mercury, cadmium, lead and arsenic[J]. Journal of Environmental Engineering Technology,2018,8(2):221-230. doi: 10.3969/j.issn.1674-991X.2018.02.030
    [41]
    WANG W T, ZHAO X S, REN X, et al. Antagonistic effects of multi-walled carbon nanotubes and BDE-47 in zebrafish (Danio rerio): oxidative stress, apoptosis and DNA damage[J]. Aquatic Toxicology,2020,225:105546. doi: 10.1016/j.aquatox.2020.105546
    [42]
    ZHANG J W, ZHANG C, DU Z K, et al. Emerging contaminant 1, 3, 6, 8-tetrabromocarbazole induces oxidative damage and apoptosis during the embryonic development of zebrafish (Danio rerio)[J]. Science of the Total Environment,2020,743:140753. doi: 10.1016/j.scitotenv.2020.140753
    [43]
    郭少娟, 张元元, 王菲菲, 等.大气颗粒物对斑马鱼胚胎的毒性及机制研究进展[J]. 环境工程技术学报,2020,10(3):338-345. doi: 10.12153/j.issn.1674-991X.20190155

    GUO S J, ZHANG Y Y, WANG F F, et al. A review of toxicity and mechanism of atmospheric particulate matter on zebrafish embryos[J]. Journal of Environmental Engineering Technology,2020,10(3):338-345. doi: 10.12153/j.issn.1674-991X.20190155
    [44]
    焦周光, 胡凌飞, 李娜, 等.大气PM2.5对大鼠心肌细胞的毒性作用[J]. 环境科学研究,2018,31(9):1636-1644.

    JIAO Z G, HU L F, LI N, et al. Toxic effects on rat cardiac myocytes from atmospheric PM2.5 particles[J]. Research of Environmental Sciences,2018,31(9):1636-1644.
    [45]
    COSTA L G, GIORDANO G. Is decabromodiphenyl ether (BDE-209) a developmental neurotoxicant[J]. NeuroToxicology,2011,32(1):9-24. doi: 10.1016/j.neuro.2010.12.010
    [46]
    CHAO S J, HUANG C P, CHEN P C, et al. Uptake of BDE-209 on zebrafish embryos as affected by SiO2 nanoparticles[J]. Chemosphere,2018,205:570-578. doi: 10.1016/j.chemosphere.2018.04.075
    [47]
    RAJPUT I R, YAQOOB S, SUN Y J, et al. Polybrominated diphenyl ethers exert genotoxic effects in pantropic spotted dolphin fibroblast cell lines[J]. Environmental Pollution,2021,271:116131. doi: 10.1016/j.envpol.2020.116131
    [48]
    VALAVANIDIS A, VLAHOGIANNI T, DASSENAKIS M, et al. Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants[J]. Ecotoxicology and Environmental Safety,2006,64(2):178-189. doi: 10.1016/j.ecoenv.2005.03.013
    [49]
    ZHANG T X, YAN Z G, ZHENG X, et al. Effects of acute ammonia toxicity on oxidative stress, DNA damage and apoptosis in digestive gland and gill of Asian clam (Corbicula fluminea)[J]. Fish & Shellfish Immunology,2020,99:514-525.
    [50]
    MENG S L, CHEN X, GYIMAH E, et al. Hepatic oxidative stress, DNA damage and apoptosis in adult zebrafish following sub-chronic exposure to BDE-47 and BDE-153[J]. Environmental Toxicology,2020,35(11):1202-1211. doi: 10.1002/tox.22985
    [51]
    MAO X B, YANG Q, CHEN D W, et al. Benzoic acid used as food and feed additives can regulate gut functions[J]. BioMed Research International,2019,2019:5721585.
    [52]
    NOUGAYRÈDE J P, HOMBURG S, TAIEB F, et al. Escherichia coli induces DNA double-strand breaks in eukaryotic cells[J]. Science,2006,313(5788):848-851. doi: 10.1126/science.1127059
    [53]
    DING W K, SHANGGUAN Y Y, ZHU Y Q, et al. Negative impacts of microcystin-LR and glyphosate on zebrafish intestine: linked with gut microbiota and microRNAs[J]. Environmental Pollution,2021,286:117685. doi: 10.1016/j.envpol.2021.117685
    [54]
    NEVES A, ROSA S, GONÇALVES J, et al. Screening of five essential oils for identification of potential inhibitors of IL-1-induced Nf-kappaB activation and NO production in human chondrocytes: characterization of the inhibitory activity of alpha-pinene[J]. Planta Medica,2010,76(3):303-308. doi: 10.1055/s-0029-1186085
    [55]
    HE X, WEI Z, WANG J, et al. Alpinetin attenuates inflammatory responses by suppressing TLR4 and NLRP3 signaling pathways in DSS-induced acute colitis[J]. Scientific Reports,2016,6:28370. doi: 10.1038/srep28370
    [56]
    ZHA L Y, CHEN J D, SUN S X, et al. Soyasaponins can blunt inflammation by inhibiting the reactive oxygen species-mediated activation of PI3K/Akt/NF-kB pathway[J]. PLoS One,2014,9(9):e107655. doi: 10.1371/journal.pone.0107655
    [57]
    JIN Y X, ZHENG S S, FU Z W. Embryonic exposure to cypermethrin induces apoptosis and immunotoxicity in zebrafish (Danio rerio)[J]. Fish & Shellfish Immunology,2011,30(4/5):1049-1054.
    [58]
    HO C J, LIN R W, ZHU W H, et al. Transcription-independent and-dependent p53-mediated apoptosis in response to genotoxic and non-genotoxic stress[J]. Cell Death Discovery,2019,5:131. doi: 10.1038/s41420-019-0211-5
    [59]
    YUAN F, WANG J L, LI R X, et al. A new regulatory mechanism between P53 and YAP crosstalk by SIRT1 mediated deacetylation to regulate cell cycle and apoptosis in A549 cell lines[J]. Cancer Management and Research,2019,11:8619-8633. doi: 10.2147/CMAR.S214826
    [60]
    OGUNDELE O M, SANYA O J. Bax modulates neuronal survival while p53 is unaltered after Cytochrome C induced oxidative stress in the adult olfactory bulb in vivo[J]. Annals of Neurosciences,2015,22(1):19-25.
    [61]
    JIA G, WANG Q, WANG R, et al. Tubeimoside-1 induces glioma apoptosis through regulation of bax/bcl-2 and the ROS/cytochrome C/caspase-3 pathway[J]. OncoTargets and Therapy,2015,8:303-311. ⊗
  • 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(4)  / Tables(1)

    Article Metrics

    Article Views(653) PDF Downloads(60) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return