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Stereoselective metabolism and potential adverse effects of chiral fungicide triadimenol on Eremias argus

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Abstract

Reptiles are an important part of vertebrates and are the primitive terrestrial vertebrates. However, lots of reptile species are endangered or susceptible to extinction. It is no doubt that contaminants are one of the important reasons for the decline of the lizard population. In this study, the selective metabolism of triadimenol (TN) in the male Eremias argus lizards and the toxic effects of TN on lizards were studied. TN chiral isomers were separated and detected by HPLC-MS/MS system with Lux Cellulose-1 column. Tissue distribution experiments showed the existence of stereoselectivity biotransformation of TN enantiomers among organs in lizards, and RR-TN preferentially emerged over the other enantiomers. The antioxidant enzymes (SOD, CAT, GST) activities and MDA content assays demonstrated that TN induced oxidative stress in most organs, especially in the liver, and the histopathology analysis showed the severe liver and testis damage caused by 14-day continuous TN gavage. The reproductive effects of TN-induced reflected in the increased sex hormone testosterone. This research confirms that TN could induce hepatic and reproductive toxicity of E. argus lizard.

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References

  • Abdollahi M, Ranjbar A, Shadnia S, Nikfar S, Rezaie A (2004) Pesticides and oxidative stress: a review. Med Sci Mon Int Med J Exp Clin Res 10:RA141

    CAS  Google Scholar 

  • Agirman N, Bedil B, Kendirlioglu G, Cetin AK (2015) Toxic effects of fungicides (penconazole and triadimenol) on growth and protein amount of Scenedesmus acutus. J Chem Soc Pak 37:1220–1225

    CAS  Google Scholar 

  • Amaral MJ, Sanchez-Hernandez JC, Bicho RC, Carretero MA, Valente R, Faustino AMR, Soares AMVM, Mann RM (2012) Biomarkers of exposure and effect in a lacertid lizard (Podarcis bocagei Seoane) exposed to chlorpyrifos. Environ Toxicol Chem 31:2345–2353

    CAS  Google Scholar 

  • Arias-Estévez M, López-Periago E, Martínez-Carballo E, Simal-Gándara J, Mejuto JC, García-Río L (2008) The mobility and degradation of pesticides in soils and the pollution of groundwater resources. Agric Ecosyst Environ 123:247–260

    Google Scholar 

  • Barzilai A, Yamamoto K-I (2004) DNA damage responses to oxidative stress. DNA repair 3:1109–1115

    CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels ☆. Anal Biochem 44:276

    CAS  Google Scholar 

  • Biggs AR, Hagley EAC (1988) Effects of two sterol-inhibiting fungicides on populations of pest and beneficial arthropods on apple. Agric Ecosyst Environ 20:235–244

    CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  Google Scholar 

  • Bridges CM (2001) Ecotoxicology of amphibians and reptiles. Ecotoxicology 10:323–324

    Google Scholar 

  • Ceballos G, Ehrlich PR, Dirzo R (2017) Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines. Proc Natl Acad Sci U S A 114:E6089

    CAS  Google Scholar 

  • Chen L, Xu P, Diao J, Di S, Li R, Zhou Z (2016) Distribution, metabolism and toxic effects of beta-cypermethrin in lizards (Eremias argus) following Oral administration. J Hazard Mater 306:87–94

    CAS  Google Scholar 

  • Chen L, Wang D, Tian Z, Di S, Zhang W, Wang F, Zhou Z, Diao J (2017) Comparative toxic responses of male and female lizards (Eremias argus) exposed to (S)-metolachlor-contaminated soil. Environ Pollut 227:476–483

    CAS  Google Scholar 

  • Chu SH, Liao PH, Chen PJ (2016) Developmental exposures to an azole fungicide triadimenol at environmentally relevant concentrations cause reproductive dysfunction in females of medaka fish. Chemosphere 152:181

    CAS  Google Scholar 

  • Cnubben NH, Rietjens IM, Wortelboer H, van Zanden J, van Bladeren PJ (2001) The interplay of glutathione-related processes in antioxidant defense. Environ Toxicol Pharmacol 10:141–152

    CAS  Google Scholar 

  • Crofton KM (1996) A structure-activity relationship for the neurotoxicity of triazole fungicides. Toxicol Lett 84:155–159

    CAS  Google Scholar 

  • Del RD, Stewart AJ, Pellegrini N (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis Nmcd 15:316

    Google Scholar 

  • Edwards D (2006) Reregistration eligibility decision for triadimefon and tolerence reassessment for Triadimenol. US Environmental Protection Agency, Washington

    Google Scholar 

  • EPA US (2006): Triadimefon reregistration eligibility decision (RED) and triadimenol tolerance reassessment and risk management decision (TRED) fact sheet. In: Office of Pesticide Programs USEPA, editor. Washington

  • Gardner SC, Oberdörster E, Gardner SC, Oberdörster E (2006) Toxicology of reptiles. Toxicol Rep 43:1043

    Google Scholar 

  • Goth L (1991) A simple method for determination of serum catalase activity and revision of reference range. Clin Chim Acta 196:143–151

    CAS  Google Scholar 

  • Han F (2006) Measurement of organ coefficient in four experimental animals. J Anim Sci Vet Med 9(4):1582–1589

    Google Scholar 

  • Han X, Gelein R, Corson N, Wade-Mercer P, Jiang J, Biswas P, Finkelstein JN, Elder A, Oberdörster G (2011) Validation of an LDH assay for assessing nanoparticle toxicity. Toxicology 287:99–104

    CAS  Google Scholar 

  • Hans-Rudolf B, Müller MD, Thomas P, Balmer ME (2002) Environmental behavior of the chiral acetamide pesticide metalaxyl: enantioselective degradation and chiral stability in soil. Environ Sci Technol 36:221–226

    Google Scholar 

  • Harner T, Wiberg K, Norstrom R (2000) Enantiomer fractions are preferred to enantiomer ratios for describing chiral signatures in environmental analysis. Environ Sci Technol 34:218–220

    CAS  Google Scholar 

  • Hayes JD, Pulford DJ (1995) The glut athione S-Transferase supergene family: regulation of GST and the contribution of the lsoenzymes to Cancer Chemoprotection and drug resistance part II. Crit Rev Biochem Mol Biol 30:521–600

    Google Scholar 

  • Hodgson E (2004): A textbook of modern toxicology. John Wiley & Sons

  • Holbrook JJ, Liljas A, Steindel SJ, Rossmann MG (1975): 4 lactate dehydrogenase. In: Boyer PD (editor), the enzymes. Academic press, pp. 191-292

  • Hopkins WA (2000) Reptile toxicology: challenges and opportunities on the last frontier in vertebrate ecotoxicology. Environ Toxicol Chem 19:2391–2393

    CAS  Google Scholar 

  • Huang Y, Zhang W, Huangyuan LI (2003) Effect of cadmium on body weight and organ coefficient of ovaries in female rats. Occup Health

  • IUCN (2017) IUCN Red List of Threatened Species, 2017th edn. International Union for Conservation of Nature, Gland, p 2

  • Jacobson ER (2007) Infectious diseases and pathology of reptiles: a color atlas and text. Int J Nonlinear Sci Numer Simul 9:167–173

    Google Scholar 

  • Jones DP (1982) Intracellular catalase function: analysis of the catalatic activity by product formation in isolated liver cells. Arch Biochem Biophys 214:806–814

    CAS  Google Scholar 

  • Kenneke JF, Mazur CS, Ritger SE, Sack TJ (2008) Mechanistic investigation of the noncytochrome P450-mediated metabolism of triadimefon to triadimenol in hepatic microsomes. Chem Res Toxicol 21:1997–2004

    CAS  Google Scholar 

  • Leaver MJ, George SG (1998) A piscine glutathione S -transferase which efficiently conjugates the end-products of lipid peroxidation. Mar Environ Res 46:71–74

    CAS  Google Scholar 

  • Li Y, Dong F, Liu X, Xu J, Li J, Kong Z, Chen X, Liang X, Zheng Y (2012a) Simultaneous enantioselective determination of triazole fungicides in soil and water by chiral liquid chromatography/tandem mass spectrometry. J Chromatogr A 1224:51–60

    CAS  Google Scholar 

  • Li Y, Dong F, Liu X, Xu J, Li J, Kong Z, Chen X, Zheng Y (2012b) Environmental behavior of the chiral triazole fungicide fenbuconazole and its chiral metabolites: enantioselective transformation and degradation in soils. Environ Sci Technol 46:2675–2683

    CAS  Google Scholar 

  • Li Y, Dong F, Liu X, Xu J, Han Y, Zheng Y (2014) Chiral fungicide triadimefon and triadimenol: Stereoselective transformation in greenhouse crops and soil, and toxicity to Daphnia magna. J Hazard Mater 265:115–123

    CAS  Google Scholar 

  • Lionetto MG, Caricato R, Calisi A, Giordano ME, Schettino T (2013) Acetylcholinesterase as a biomarker in environmental and occupational medicine: new insights and future perspectives. Biomed Res Int 2013:321213

    Google Scholar 

  • Lv X, Pan L, Wang J, Lu L, Yan W, Zhu Y, Xu Y, Guo M, Zhuang S (2017) Effects of triazole fungicides on androgenic disruption and CYP3A4 enzyme activity ☆. Environ Pollut 222:504–512

    CAS  Google Scholar 

  • Maitra SK, Sarkar R (1996) Influence of methyl parathion on gametogenic and acetylcholinesterase activity in the testis of whitethroated munia (Lonchura malabarica). Arch Environ Contam Toxicol 30:384–389

    CAS  Google Scholar 

  • Marler CA, Moore MC (1991) Supplementary feeding compensates for testosterone-induced costs of aggression in male mountain spiny lizards, Sceloporus jarrovi. Anim Behav 42:209–219

    Google Scholar 

  • Menegola E, Broccia ML, Di RF, Massa V, Giavini E (2005a) Study on the common teratogenic pathway elicited by the fungicides triazole-derivatives. Toxicol Vitro Int J Publ Association with Bibra 19:737–748

    CAS  Google Scholar 

  • Menegola E, Broccia ML, Renzo FD, Massa V, Giavini E (2005b) Craniofacial and skeletal defects induced by the fungicide tradimefon in the mouse. Birth Defects Res Part B Dev Rep Toxicol 74:185–195

    CAS  Google Scholar 

  • Moser VC, Macphail RC (1989) Neurobehavioral effects of triadimefon, a triazole fungicide, in male and female rats ☆. Neurotoxicol Teratol 11:285–293

    CAS  Google Scholar 

  • Nillos MG, Gan J, Schlenk D (2010) Chirality of organophosphorus pesticides: analysis and toxicity. J Chromatogr B 878:1277–1284

    CAS  Google Scholar 

  • Odokuma EI, Omokaro EI (2015) Comp Histol Ana Verteb Liver 3:1

    Google Scholar 

  • Ortizsantaliestra ME, Maia JP, Egeaserrano A, Lopes I (2018) Validity of fish, birds and mammals as surrogates for amphibians and reptiles in pesticide toxicity assessment. Ecotoxicology 27:819–833 1–15

    CAS  Google Scholar 

  • Ott M, Gogvadze V, Orrenius S, Zhivotovsky B (2007) Mitochondria, oxidative stress and cell death. Apoptosis 12:913–922

    CAS  Google Scholar 

  • Reeves R, Thiruchelvam M, Coryslechta DA (2004) Expression of behavioral sensitization to the cocaine-like fungicide triadimefon is blocked by pretreatment with AMPA, NMDA and DA D1 receptor antagonists. Brain Res 1008:155–167

    CAS  Google Scholar 

  • Regoli F, Giuliani ME (2014) Oxidative pathways of chemical toxicity and oxidative stress biomarkers in marine organisms. Mar Environ Res 93:106

    CAS  Google Scholar 

  • Runes HB, And JJJ, Field JA (1999) Method for the analysis of triadimefon and ethofumesate from dislodgeable foliar residues on turfgrass by solid-phase extraction and in-vial elution. J Agric Food Chem 47:3252

    CAS  Google Scholar 

  • Sample BE, Aplin MS, Efroymson RA, Suter Ii GW, Welsh CJE (1997): Methods and tools for estimation of the exposure of terrestrial wildlife to contaminants. ORNL/TM-13391. Prepared for US Department of Energy by oak Ridge National Laboratory

  • Sanchezhernandez JC, Sanchez BM (2010) Lizard cholinesterases as biomarkers of pesticide exposure: enzymological characterization. Environ Toxicol Chem 21:2319–2325

    Google Scholar 

  • Schäfer RB, Caquet T, Siimes K, Mueller R, Lagadic L, Liess M (2007) Effects of pesticides on community structure and ecosystem functions in agricultural streams of three biogeographical regions in Europe. Sci Total Environ 382:272

    Google Scholar 

  • Schieber M, Chandel NS (2014) ROS function in redox signaling and oxidative stress. Curr Biol 24:R453–R462

    CAS  Google Scholar 

  • Schmedes A, Holmer G (1989) A new thiobarbituric acid (TBA) method for determining free malondialdehyde (MDA) and hydroperoxides selectively as a measure of lipid peroxidation. J Am Oil Chem Soc 66:813–817

    CAS  Google Scholar 

  • Schuppe I, Moldéus P, Cotgreave IA (1992) Protein-specific S-thiolation in human endothelial cells during oxidative stress. Biochem Pharmacol 44:1757

    CAS  Google Scholar 

  • Shen Q, Li J, Xu P, Li W, Zhuang G, Wang Y (2017) Enantioselective metabolism of triadimefon and its chiral metabolite triadimenol in lizards. Ecotoxicol Environ Saf 143:159–165

    CAS  Google Scholar 

  • Simon H-U, Haj-Yehia A, Levi-Schaffer F (2000) Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5:415–418

    CAS  Google Scholar 

  • Singh N (2005) Factors affecting triadimefon degradation in soils. J Agric Food Chem 53:70–75

    CAS  Google Scholar 

  • Soreq H, Seidman S (2001) Acetylcholinesterase—new roles for an old actor. Nat Rev Neurosci 2:294–302

    CAS  Google Scholar 

  • Walker QD, Mailman RB (1996) Triadimefon and triadimenol: effects on monoamine uptake and release. Toxicol Appl Pharmacol 139:227–233

    CAS  Google Scholar 

  • Wang Q, Qiu J, Zhu W, Jia G, Li J, Bi C, Zhou Z (2006) Stereoselective degradation kinetics of theta-cypermethrin in rats. Environ Sci Technol 40:721

    CAS  Google Scholar 

  • Wang Z, Zhao J, Li F, Gao D, Xing B (2010) Adsorption and inhibition of acetylcholinesterase by different nanoparticles. Chemosphere 79:86–92

    CAS  Google Scholar 

  • Wang Y, Guo B, Gao Y, Xu P, Zhang Y, Li J, Wang H (2014a) Stereoselective degradation and toxic effects of benalaxyl on blood and liver of the Chinese lizard Eremias argus. Pestic Biochem Physiol 108:34–41

    CAS  Google Scholar 

  • Wang Y, Yu D, Xu P, Guo B, Zhang Y, Li J, Wang H (2014b) Stereoselective metabolism, distribution, and bioaccumulation brof triadimefon and triadimenol in lizards. Ecotoxicol Environ Saf 107:276

    CAS  Google Scholar 

  • Ward WO, Delker DA, Hester SD, Thai S-F, Wolf DC, Allen JW, Nesnow S (2006) Transcriptional profiles in liver from mice treated with hepatotumorigenic and nonhepatotumorigenic triazole conazole fungicides: propiconazole, triadimefon, and myclobutanil. Toxicol Pathol 34:863–878

    CAS  Google Scholar 

  • Weir SM, Suski JG, Salice CJ (2010) Ecological risk of anthropogenic pollutants to reptiles: evaluating assumptions of sensitivity and exposure. Environ Pollut 158:3596

    CAS  Google Scholar 

  • While GM, Isaksson C, Mcevoy J (2010) Repeatable intra-individual variation in plasma testosterone concentration and its sex-specific link to aggression in a social lizard. Horm Behav 58:208–213

    CAS  Google Scholar 

  • Wingfield JC, Ball GF, Dufty AM, Hegner RE, Ramenofsky M (1987) Testosterone and aggression in birds. Am Sci 75:602–608

    Google Scholar 

  • Ye J, Zhao M, Liu J, Liu W (2010) Enantioselectivity in environmental risk assessment of modern chiral pesticides. Environ Poll (Barking, Essex : 1987) 158:2371–2383

    CAS  Google Scholar 

  • Yinghuan W, Huili W, Yanfeng Z, Jianzhong L (2012) Application of reptiles in toxicology research: a review. Asian J Ecotoxicol 7:585–592

    Google Scholar 

  • Zhang JF, Liu H, Sun YY, Wang XR, Wu JC, Xue YQ (2005) Responses of the antioxidant defenses of the Goldfish Carassius auratus, exposed to 2,4-dichlorophenol. Environ Toxicol Pharmacol 19:185–190

    CAS  Google Scholar 

  • Zhao Q, Shao L, Hu X, Wu G, Du J, Xia J, Qiu H (2013) Lipoxin a4 preconditioning and postconditioning protect myocardial ischemia/reperfusion injury in rats. Mediat Inflamm 2013:231351

    Google Scholar 

  • Zipper C, Suter MJF, Haderlein SB, Michael Gruhl A, Kohler HPE (1998) Changes in the enantiomeric ratio of (R)- to (S)-mecoprop indicate in situ biodegradation of this chiral herbicide in a polluted aquifer. Environ.sci.technol 32:2070–2076

    CAS  Google Scholar 

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This work was supported by fund from the National Natural Science Foundation of China (Contract Grant number: 21577171).

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Wang, Z., Tian, Z., Chen, L. et al. Stereoselective metabolism and potential adverse effects of chiral fungicide triadimenol on Eremias argus. Environ Sci Pollut Res 27, 7823–7834 (2020). https://doi.org/10.1007/s11356-019-07205-4

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