Oxidative Damage and Genetic Toxicity Induced by DBP in Earthworms (Eisenia fetida)
Abstract
Di-n-butyl phthalate (DBP) is one of the most ubiquitous plasticizers used worldwide. However, it has negatives effects on the soil, water, atmosphere, and other environmental media and can cause serious pollution. According to the artificial soil test and previous studies, this study was conducted to evaluate the toxicity of earthworms induced by DBP at different concentrations (0, 0.1, 1.0, 10, and 50 mg kg−1) on the 7th, 14th, 21st, and 28th days of exposure. The variations in the antioxidant activities of enzymes, such as catalase (CAT), peroxidase (POD), superoxide dismutase (SOD), and glutathione-S-transferase (GST), in the amounts of malondialdehyde (MDA) and reactive oxygen species (ROS) and in the amount of DNA damage were measured to evaluate the toxic impact of DBP in earthworms. Upon exposure to DBP, the SOD, CAT, POD, and GST activities were significantly increased, with the exception of the 0.1 mg kg−1 treatment dose. High concentrations of DBP (10 and 50 mg kg−1) induced superfluous ROS to be produced and caused the MDA content to increase significantly. Therefore, we proposed that DBP led to DNA damage in earthworm coelomocytes in a dose-dependent manner, which means that DBP is a source of oxidative damage and genetic toxicity in earthworms.
Notes
Funding
This study under the auspices of the National Key Research and Development Project of China (Grant number 2016YFD0800304) and Natural Science Foundation of Shandong (Grant number ZR2017MD023).
Compliance with Ethical Standards
Conflict of interest
The authors declare no conflict of interest.
Ethical Approval
All applicable international, national, and/or institutional guidelines for the care and use of animals (Eisenia fetida) were followed.
References
- Alam MS, Ohsako S, Matsuwaki T, Zhu XB, Tsunekawa N, Kanai Y, Sone H, Tohyama C, Kurohmaru M (2010) Induction of spermatogenic cell apoptosis in prepubertal rat testes irrespective of testicular steroidogenesis: a possible estrogenic effect of di(n-butyl) phthalate. Reproduction 139(2):427–437CrossRefGoogle Scholar
- Beauchamp C, Fridovicich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–278CrossRefGoogle Scholar
- Clewell RA, Kremer JJ, Williams CC, Campbell JL, Sochaski MA, Andersen ME, Borghoff SJ (2009) Kinetics of selected di-n-butyl phthalate metabolites and fetal testosterone following repeated and single administration in pregnant rats. Toxicology 255(1–2):80–90CrossRefGoogle Scholar
- Coleman DC, Ingham ER (1988) Carbon, nitrogen, phosphorus and sulfur cycling in terrestrial ecosystems. Biogeochemistry 5:3–6CrossRefGoogle Scholar
- Cooke MS, Evans MD, Dizdaroglu M, Lunec J (2003) Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J 17(10):1195–1214CrossRefGoogle Scholar
- Daiem MMA, Rivera-Utrilla J, Ocampo-Perez R, Mendez-Diaz JD, Sanchez-Polo M (2012) Environmental impact of phthalic acid esters and their removal from water and sediments by different technologies–a review. J Environ Manag 109:164–178CrossRefGoogle Scholar
- Du L, Li G, Liu M, Li Y, Yin S, Zhao J (2015) Biomarker responses in earthworms (eisenia fetida) to soils contaminated with di-n-butyl phthalates. Environ Sci Pollut Res 22(6):4660–4669CrossRefGoogle Scholar
- Gao J, Chi J (2015) Biodegradation of phthalate acid esters by different marine microalgal species. Mar Pollut Bull 99(1–2):70–75CrossRefGoogle Scholar
- Ge W, Yan S, Wang J, Zhu L, Chen A, Wang J (2015) Oxidative stress and DNA damage induced by imidacloprid in zebrafish (danio rerio). J Agric Food Chem 63(6):1856–1862CrossRefGoogle Scholar
- Greenwald RA (1987) Handbook of methods for oxygen radical research. Free Radical Biol Med 3(2):161Google Scholar
- Guo X, Wang L, Wang X, Liu H (2013) Occurrence and environmental risk assessment of PAEs in Weihe river near Xi’an city, China. Water Sci Technol 67(5):948–958CrossRefGoogle Scholar
- Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione s-transferases: the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139Google Scholar
- Han Y, Zhu L, Wang J, Wang J, Xie H, Zhang S (2014) Integrated assessment of oxidative stress and DNA damage in earthworms (Eisenia fetida) exposed to azoxystrobin. Ecotoxicol Environ Saf 107:214–219CrossRefGoogle Scholar
- Hassanzadeh N, Esmaili SA, Khodabandeh S, Bahramifar N (2014) Occurrence and distribution of two phthalate esters in the sediments of the Anzali wetlands on the coast of the Caspian Sea (Iran). Mar Pollut Bull 89(1–2):128–135CrossRefGoogle Scholar
- Jayawardena I, Godakumbura PI, Prashantha MA (2016) Migration of BTEX and phthalates from natural rubber latex balloons obtained from the Sri Lankan market. Springerplus 5:20CrossRefGoogle Scholar
- Jiang JT, Zhong C, Zhu YP, Xu DL, Wood K, Sun WL, Li EH, Liu ZH, Zhao W, Ruan Y, Xia SJ (2016) Prenatal exposure to di-n-butyl phthalate (DBP) differentially alters androgen cascade in undeformed versus hypospadiac male rat offspring. Reprod Toxicol 61:75–81CrossRefGoogle Scholar
- Kochba J, Lavee S, Spiegel-Roy P (1977) Differences in peroxidase activity and soenzymes in embryogenic and non-embryogenic ‘Shamouti’ orange ovular callus lines. Plant Cell Physiol 18:463–467Google Scholar
- Kosmehl T, Hallare AV, Braunbeck T, Hollert H (2008) DNA damage induced by genotoxicants in zebrafish (Danio rerio) embryos after contact exposure to freeze-dried sediment and sediment extracts from laguna lake (the Philippines) as measured by the comet assay. Mutat Res 650(1):1–14CrossRefGoogle Scholar
- Lawler J (2003) Hindlimb unloading increases oxidative stress and disrupts antioxidant capacity in skeletal muscle. Free Radic Biol Med 35(1):9–16CrossRefGoogle Scholar
- Liao CS, Yen JH, Wang YS (2009) Growth inhibition in chinese cabbage (Brassica rapa var. Chinensis) growth exposed to di-n-butyl phthalate. J Hazard Mater 163(2–3):625–631CrossRefGoogle Scholar
- Liu W, Zhu LS, Wang J, Wang JH, Xie H, Song Y (2009) Assessment of the genotoxicity of endosulfan in earthworm and white clover plants using the comet assay. Arch Environ Contam Toxicol 56(4):742–746CrossRefGoogle Scholar
- Liu SB, Ma Z, Sun WL, Sun XW, Hong Y, Ma L, Qin C, Stratton HJ, Liu Q, Jiang JT (2012) The role of androgen-induced growth factor (FGF8) on genital tubercle development in a hypospadiac male rat model of prenatal exposure to di-n-butyl phthalate. Toxicology 293(1–3):53–58CrossRefGoogle Scholar
- Lu Y, Tang F, Wang Y, Zhao J, Zeng X, Luo Q, Wang L (2009) Biodegradation of dimethyl phthalate, diethyl phthalate and di-n-butyl phthalate by rhodococcus sp. L4 isolated from activated sludge. J Hazard Mater 168(2–3):938–943CrossRefGoogle Scholar
- Massicotte JP (1994) Oxidative processes as indicators of chemical stress in marine bivalves. Aquat Ecosyst Health 3:101–111CrossRefGoogle Scholar
- Matsumoto M, Hirata-Koizumi M, Ema M (2008) Potential adverse effects of phthalic acid esters on human health: a review of recent studies on reproduction. Regul Toxicol Pharmacol 50(1):37–49CrossRefGoogle Scholar
- Mishra PC, Dash MC (1980) Digestive enzymes of some earthworms. Experientia 36(10):1156–1157CrossRefGoogle Scholar
- Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410CrossRefGoogle Scholar
- Motohashi M, Wempe MF, Mutou T, Takahashi H, Kansaku N, Ikegami M, Inomata T, Asari M, Wakui S (2016) Male rats exposed in utero to di(n-butyl) phthalate: age-related changes in leydig cell smooth endoplasmic reticulum and testicular testosterone-biosynthesis enzymes/proteins. Reprod Toxicol 59:139–146CrossRefGoogle Scholar
- OECD (1984) Test 207: Earthworm, acute toxicity tests. In: Organization for economic cooperation and development. OECD guidelines for testing of chemicals. Organization for Economic Cooperation and Development (OECD). Paris, FranceGoogle Scholar
- OECD (2004) Test 202: Daphnia sp-acute immobilisation test. In: Organization for testing of chemicals. Organization for the Economic Cooperation and Development, Paris, FranceGoogle Scholar
- Pavlica M, Klobucar GIV, Mojaš N, Erben R, Papeš D (2009) Detection of DNA damage in haemocytes of zebra mussel using comet assay. Mutat Res 490:209–214CrossRefGoogle Scholar
- Pérez-Feás C, Barciela-Alonso MC, Bermejo-Barrera P (2011) Presence of phthalates in contact lens and cleaning solutions. Microchem J 99(1):108–113CrossRefGoogle Scholar
- Reineme P, Prade L, Hof P, Neuefeind T, Huber R, Zettl R, Palme K, Schell J, Koelln I, Bartunik HD, Bieseler B (1996) Three-dimensional structure of glutathione s-transferase from arabidopsis thaliana at 2.2 a resolution: structural characterization of herbicide-conjugating plant glutathione s-transferases and a novel active site architecture. J Mol Biol 255:289–309CrossRefGoogle Scholar
- Seitz N, Bottcher M, Keiter S, Kosmehl T, Manz W, Hollert H, Braunbeck T (2008) A novel statistical approach for the evaluation of comet assay data. Mutat Res 652(1):38–45CrossRefGoogle Scholar
- Sen N, Liu X, Craig ZR (2015) Short term exposure to di-n-butyl phthalate (DBP) disrupts ovarian function in young CD-1 mice. Reprod Toxicol 53:15–22CrossRefGoogle Scholar
- Sforzini S, Boeri M, Dagnino A, Oliveri L, Bolognesi C, Viarengo A (2012) Genotoxicity assessment in Eisenia andrei coelomocytes: a study of the induction of DNA damage and micronuclei in earthworms exposed to B[a]P- and TCDD-spiked soils. Mutat Res 746(1):35–41CrossRefGoogle Scholar
- Sha Y, Xia X, Yang Z, Huang GH (2007) Distribution of PAEs in the middle and lower reaches of the yellow river, China. Environ Monit Assess 124(1–3):277–287CrossRefGoogle Scholar
- Shugart LR (2000) DNA damage as a biomarker of exposure. Ecotoxicology 9:329–340CrossRefGoogle Scholar
- Singh NP, Mccoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175:184–191CrossRefGoogle Scholar
- Singh S, Eapen S, D’souza SF (2006) Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. Chemosphere 62(2):233–246CrossRefGoogle Scholar
- Song Y, Zhu LS, Wang J, Wang JH, Liu W, Xie H (2009) DNA damage and effects on antioxidative enzymes in earthworm (Eisenia fetida) induced by atrazine. Soil Biol Biochem 41(5):905–909CrossRefGoogle Scholar
- Sun LW, Qu MM, Li YQ, Wu YL, Chen YG, Kong ZM, Liu ZT (2004) Toxic effects of aminophenols on aquatic life using the zebrafish embryo test and the comet assay. Bull Environ Contam Toxicol 73(4):628–634CrossRefGoogle Scholar
- Swan SH (2008) Environmental phthalate exposure in relation to reproductive outcomes and other health endpoints in humans. Environ Res 108(2):177–184CrossRefGoogle Scholar
- Teil MJ, Blanchard M, Chevreuil M (2006) Atmospheric fate of phthalate esters in an urban area (Paris-France). Sci Total Environ 354(2–3):212–223CrossRefGoogle Scholar
- US EPA (1991) Risk Assessment Guidance for Superfund (RAGS): Volume I-Humman Health Evaluation Manual(HHEM) (Part B, Development of Risk-Based Preliminary Remediation Goals). Office of Emergency and Remedial Response, Washington DC, EPA/540/R-92/003, OSWER Directive 9285.7-01B, NTIS PB92-963333.r)Google Scholar
- Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Safe 64(2):178–189CrossRefGoogle Scholar
- Vitali M, Guidotti M, Macilenti G, Cremisini C (1997) Phthalate esters in freshwaters as markers of contamination sources—a site study in Italy. Environ Int 23(3):337–347CrossRefGoogle Scholar
- Wang XH (2010) Effects of DBP/DEHP on soil microbial biomass carbon and enzyme in single and complex pollution with Pb. dissertation. University of Dongbei NormalGoogle Scholar
- Wang XF, Xing ML, Shen Y, Zhu X, Xu LH (2006) Oral administration of Cr(VI) induced oxidative stress, DNA damage and apoptotic cell death in mice. Toxicology 228(1):16–23CrossRefGoogle Scholar
- Wang JH, Zhu LS, Meng Y, Wang J, Xie H, Zhang QM (2012) The combined stress effects of atrazine and cadmium on the earthworm Eisenia fetida. Environ Toxicol Chem 31(9):2035–2040CrossRefGoogle Scholar
- Winston GW, Giulio RTD (1991) Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat Toxicol 19(2):137–161CrossRefGoogle Scholar
- Xie Z, Wang J, Dai F, Jin X, Wu K, Chen Q, Wang Y (2016) Effects of maternal exposure to di-n-butyl phthalate during pregnancy and breastfeeding on ovarian development and function of F1 female rats. Environ Toxicol Pharmacol 43:38–43CrossRefGoogle Scholar
- Xue Y, Gu X, Wang X, Sun C, Xu X, Sun J, Zhang B (2009) The hydroxyl radical generation and oxidative stress for the earthworm Eisenia fetida exposed to tetrabromobisphenol A. Ecotoxicology 18(6):693–699CrossRefGoogle Scholar
- Yan S, Wang J, Zhu L, Chen A, Wang J (2015) Toxic effects of nitenpyram on antioxidant enzyme system and DNA in zebrafish (Danio rerio) livers. Ecotoxicol Environ Safe 122:54–60CrossRefGoogle Scholar
- Yang CF, Wang CC, Chen CH (2013) Di-n-butyl phthalate removal using mixed cultures in batch reactors. Int Biodeterior Biodegrad 85:587–591CrossRefGoogle Scholar
- Zhang QF, Li YY, Pang CH, Lu CM, Wang BS (2005) Nacl enhances thylakoid-bound sod activity in the leaves of c3 halophyte Suaeda salsa L. Plant Sci 168(2):423–430CrossRefGoogle Scholar
- Zhang Q, Zhu L, Wang J, Xie H, Wang J, Han Y, Yang J (2013) Oxidative stress and lipid peroxidation in the earthworm Eisenia fetida induced by low doses of fomesafen. Environ Sci Pollut Res 20(1):201–208CrossRefGoogle Scholar
- Zhang Y, Du N, Wang L, Zhang H, Zhao J, Sun G, Wang P (2015) Physical and chemical indices of cucumber seedling leaves under dibutyl phthalate stress. Environ Sci Pollut Res 22(5):3477–3488CrossRefGoogle Scholar
- Zheng LP, Feng YH, Zhao X, Xu J, Lin YS (2010) Toxicity effects of chlordane and mirex contaminated soil on earthworm. J Agro-Environ Sci 29(10):1924–1929Google Scholar
- Zhou Q, Mrowietz U, Rostami-Yazdi M (2009) Oxidative stress in the pathogenesis of psoriasis. Free Radic Biol Med 47(7):891–905CrossRefGoogle Scholar