Skip to main content
SpringerLink
Log in

Influence of difenoconazole on lipid metabolism in marine medaka (Oryzias melastigma)

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Difenoconazole (DFZ) is a triazole fungicide that inhibits the biosynthesis of sterols in cell membranes and is widely used in agriculture for effectively treating fungal infections. However, there are few studies available addressing the effects of DFZ on lipid metabolism in marine fishes. The present study was conducted to investigate the effects of DFZ on lipid metabolism in marine medaka (Oryzias melastigma). After exposure to 1, 10, 100 and 1000 ng/L DFZ for 180 days, an increase in condition factor (CF), total lipids and polyunsaturated fatty acids (PUFA) contents accompanied with a decrease in saturated fatty acids was observed in the muscle of DFZ-exposed fish. The expression of peroxisome proliferator-activated receptor γ as well as retinoid X receptors in the muscle was up-regulated, which would be responsible for the lipid accumulation in the muscle. The elevation of Δ6-desaturase (FADS2) and Δ9-desaturase (SCD) mRNA levels in the muscle and liver might result in the increase of PUFA content. The increased CF index and total lipid amounts indicated that DFZ exposure could affect the health of fish. ∑SFA (sum of saturated fatty acids) and DHA (docosahexaenoic acid; 22:6n-3) concentrations decreased, and the levels of ∑PUFA and ∑n-6PUFA increased in the muscle, which suggested that DFZ exposure could change lipid metabolism and profiles in fish.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Auwerx J (1999) PPARγ, the ultimate thrifty gene. Diabetologia 42:1033–1049

    Article  CAS  Google Scholar 

  • Berger J, Moller DE (2002) The mechanisms of action of PPARs. Annu Rev Med 53:409–435

    Article  CAS  Google Scholar 

  • Bervoets L, Blust R (2003) Metal concentrations in water, sediment and gudgeon (Gobio gobio) from a pollution gradient: relationship with fish condition factor. Environ Pollut 126:9–19

    Article  CAS  Google Scholar 

  • Cahu C, Salen P, De Lorgeril M (2004) Farmed and wild fish in the prevention of cardiovascular diseases: assessing possible differences in lipid nutritional values. Nutr Metab Cardiovas 14:34–41

    Article  CAS  Google Scholar 

  • Carlson EA, Li Y, Zelikoff JT (2002) Exposure of Japanese medaka (Oryzias latipes) to benzo[a]pyrene suppresses immune function and host resistance against bacterial challenge. Aquat Toxicol 56:289–301

    Article  CAS  Google Scholar 

  • Cheng HL, Ji NJ, Peng YX, Shen X, Xu JH, Dong ZG, Wu CC (2011) Molecular characterization and tissue-specific expression of the acetyl-CoA carboxylase gene from Grass carp, Ctenopharyngodon idella. Gene 487:46–51

    Article  CAS  Google Scholar 

  • Chevillotte E, Rieusset J, Roques M, Desage M, Vidal H (2001) The regulation of uncoupling protein-2 gene expression by omega-6 polyunsaturated fatty acids in human skeletal muscle cells involves multiple pathways, including the nuclear receptor peroxisome proliferator-activated receptor beta. J Biol Chem 276:10853–10860

    Article  CAS  Google Scholar 

  • Cho HP, Nakamura M, Clarke SD (1999a) Cloning, expression, and fatty acid regulation of the human Δ-5 desaturase. J Biol Chem 274:37335–37339

    Article  CAS  Google Scholar 

  • Cho HP, Nakamura MT, Clarke SD (1999b) Cloning, expression, and nutritional regulation of the mammalian Δ-6 desaturase. J Biol Chem 274:471–477

    Article  CAS  Google Scholar 

  • Clements WH, Rees DE (1997) Effects of heavy metals on prey abundance, feeding habits, and metal uptake of brown trout in the Arkansas River, Colorado. Trans Am Fish Soc 126:774–785

    Article  CAS  Google Scholar 

  • Costet P, Legendre C, Moré J, Edgar A, Galtier P, Pineau T (1998) Peroxisome proliferator-activated receptor α-isoform deficiency leads to progressive dyslipidemia with sexually dimorphic obesity and steatosis. J Biol Chem 273:29577–29585

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ducheix S, Lobaccaro J, Martin P, Guillou H (2011) Liver X receptor: an oxysterol sensor and a major player in the control of lipogenesis. Chem Phys Lipids 164:500–514

    Article  CAS  Google Scholar 

  • Fernandes CE, da Silva Vasconcelos MA, de Almeida Ribeiro M, Sarubbo LA, Andrade SAC, de Melo Filho AB (2014) Nutritional and lipid profiles in marine fish species from Brazil. Food Chem 160:67–71

    Article  CAS  Google Scholar 

  • Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  Google Scholar 

  • Fulco AJ, Mead JF (1959) Metabolism of essential fatty acids VIII. Origin of 5, 8, 11-eicosatrienoic acid in the fat-deficient rat. J Biol Chem 234:1411–1416

    CAS  Google Scholar 

  • Goetz AK, Ren H, Schmid JE, Blystone CR, Thillainadarajah I, Best DS, Nichols HP, Strader LF, Wolf DC, Narotsky MG (2007) Disruption of testosterone homeostasis as a mode of action for the reproductive toxicity of triazole fungicides in the male rat. Toxicol Sci 95:227–239

    Article  CAS  Google Scholar 

  • Grimaldi PA (2007) Regulatory functions of PPARβ in metabolism: implications for the treatment of metabolic syndrome. Biochim Biophys Acta 1771:983–990

    Article  CAS  Google Scholar 

  • Guillou H, Zadravec D, Martin PG, Jacobsson A (2010) The key roles of elongases and desaturases in mammalian fatty acid metabolism: insights from transgenic mice. Prog Lipid Res 49:186–199

    Article  CAS  Google Scholar 

  • Hester SD, Nesnow S (2008) Transcriptional responses in thyroid tissues from rats treated with a tumorigenic and a non-tumorigenic triazole conazole fungicide. Toxicol Appl Pharm 227:357–369

    Article  CAS  Google Scholar 

  • Huynh MD, Kitts DD (2009) Evaluating nutritional quality of pacific fish species from fatty acid signatures. Food Chem 114:912–918

    Article  CAS  Google Scholar 

  • Inoue K, Takei Y (2002) Diverse adaptability in Oryzias species to high environmental salinity. Zool Sci 19:727–734

    Article  Google Scholar 

  • Jakobsson A, Westerberg R, Jacobsson A (2006) Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog Lipid Res 45:237–249

    Article  CAS  Google Scholar 

  • Jankowska B, Zakęś Z, Żmijewski T, Szczepkowski M (2010) Fatty acid profile of muscles, liver and mesenteric fat in wild and reared perch (Perca fluviatilis L.). Food Chem 118:764–768

    Article  CAS  Google Scholar 

  • Kersten S (2002) Peroxisome proliferator activated receptors and obesity. Eur J Pharm 440:223–234

    Article  CAS  Google Scholar 

  • Kliewer SA, Sundseth SS, Jones SA, Brown PJ, Wisely GB, Koble CS, Devchand P, Wahli W, Willson TM, Lenhard JM (1997) Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors α and γ. Proc Nat Acad Sci 94:4318–4323

    Article  CAS  Google Scholar 

  • Kliewer SA, Moore JT, Wade L, Staudinger JL, Watson MA, Jones SA, McKee DD, Oliver BB, Willson TM, Zetterstrom RH, Perlmann T, Lehmann JM (1998) Orphan nuclear receptors: shifting endocrinology into reverse. Cell 92:73–82

    Article  CAS  Google Scholar 

  • Kolanowski W, Laufenberg G (2006) Enrichment of food products with polyunsaturated fatty acids by fish oil addition. Eur Food Res Technol 222:472–477

    Article  CAS  Google Scholar 

  • Konwick BJ, Garrison AW, Avants JK, Fisk AT (2006) Bioaccumulation and biotransformation of chiral triazole fungicides in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 80:372–381

    Article  CAS  Google Scholar 

  • Kopecka-Pilarczyk J, Correia AD (2009) Biochemical response in gilthead seabream (Sparus aurata) to in vivo exposure to pyrene and fluorine. J Experi Mar Biol Ecol 372:49–57

    Article  CAS  Google Scholar 

  • Lee CH, Olson P, Hevener A, Mehl I, Chong LW, Olefsky JM, Gonzalez FJ, Ham J, Kang H, Peters JM, Evans RM (2006) PPARdelta regulates glucose metabolism and insulin sensitivity. Proc Natl Acad Sci USA 103:3444–3449

    Article  CAS  Google Scholar 

  • Lobon-Cervia J, Montaes C, De Sostoa A (1991) Influence of environment upon the life history of gudgeon, Gobio gobio (L.): a recent and successful colonizer of the Iberian Peninsula. J Fish Biol 39:285–300

    Article  Google Scholar 

  • McNamara RK, Jandacek R, Rider T, Tso P, Cole-Strauss A, Lipton JW (2011) Differential effects of antipsychotic medications on polyunsaturated fatty acid biosynthesis in rats: relationship with liver delta6-desaturase expression. Schizophr Res 129:57–65

    Article  Google Scholar 

  • Metzger D, Imai T, Jiang M, Takukawa R, Desvergne B, Wahli W, Chambon P (2005) Functional role of RXRs and PPARγ in mature adipocytes. Prostag Leukotr Ess 73:51–58

    Article  CAS  Google Scholar 

  • Mu X, Wang K, Chai T, Zhu L, Yang Y, Zhang J, Pang S, Wang C, Li X (2015) Sex specific response in cholesterol level in zebrafish (Danio rerio) after long-term exposure of difenoconazole. Environ Pollut 175:147–157

    Article  Google Scholar 

  • Muhlhausler BS, Ailhaud GP (2013) Omega-6 polyunsaturated fatty acids and the early origins of obesity. Curr Opin Endocrinol Diabetes Obes 20:56–61

    Article  CAS  Google Scholar 

  • Özogul Y, Özogul F (2007) Fatty acid profiles of commercially important fish species from the Mediterranean, Aegean and Black Seas. Food Chem 100:1634–1638

    Article  Google Scholar 

  • Pershadsingh HA (2006) Treating the metabolic syndrome using angiotensin receptor antagonists that selectively modulate peroxisome proliferator-activated receptor-γ. Int J Biochem Cell Biol 38:766–781

    Article  CAS  Google Scholar 

  • Petri D, Glover CN, Ylving S, Kolås K, Fremmersvik G, Waagbø R, Berntssen MHG (2006) Sensitivity of Atlantic salmon (Salmo salar) to dietary endosulfan as assessed by haematology, blood biochemistry, and growth parameters. Aquat Toxicol 80:207–216

    Article  CAS  Google Scholar 

  • Pettinelli P, Obregón A, Videla L (2011) Molecular mechanisms of steatosis in nonalcoholic fatty liver disease. Nutr Hosp 26:441–450

    CAS  Google Scholar 

  • Reddy JK, Hashimoto T (2001) Peroxisomal β-oxidation and peroxisome proliferator-activated receptor α: an adaptive metabolic system. Annu Rev Nutr 21:193–230

    Article  CAS  Google Scholar 

  • Rekanović E, Mihajlović M, Potočnik I (2010) In vitro sensitivity of Fusarium graminearum (Schwabe) to difenoconazole, prothioconazole and thiophanate-methyl. Pestic Phytomed (Belgrade) 25:325–333

    Article  Google Scholar 

  • Rockett JC, Narotsky MG, Thompson KE, Thillainadarajah I, Blystone CR, Goetz AK, Ren H, Best DS, Murrell RN, Nichols HP (2006) Effect of conazole fungicides on reproductive development in the female rat. Reprod Toxicol 22:647–658

    Article  CAS  Google Scholar 

  • Rosen ED, Spiegelman BM (2001) PPARγ: a nuclear regulator of metabolism, differentiation, and cell growth. J Biol Chem 276:37731–37734

    Article  CAS  Google Scholar 

  • Schupp M, Clemenz M, Gineste R, Witt H, Janke J, Helleboid S, Hennuyer N, Ruiz P, Unger T, Staels B (2005) Molecular characterization of new selective peroxisome proliferator–activated receptor γ modulators with angiotensin receptor blocking activity. Diabetes 54:3442–3452

    Article  CAS  Google Scholar 

  • Schupp M, Lee LD, Frost N, Umbreen S, Schmidt B, Unger T, Kintscher U (2006) Regulation of peroxisome proliferator-activated receptor gamma activity by losartan metabolites. Hypertension 47:586–589

    Article  CAS  Google Scholar 

  • Sun L, Zhang J, Zuo Z, Chen Y, Wang X, Huang X, Wang C (2011) Influence of triphenyltin exposure on the hypothalamus–pituitary–gonad axis in male Sebastiscus marmoratus. Aquat Toxicol 104:263–269

    Article  CAS  Google Scholar 

  • Sun L, Li J, Zuo Z, Chen M, Wang C (2013) Chronic exposure to paclobutrazol causes hepatic steatosis in male rockfish Sebastiscus marmoratus and the mechanism involved. Aquat Toxicol 126:148–153

    Article  CAS  Google Scholar 

  • Tietz N (1976) Total lipids. In: Tietz N (ed) Fundamentals of Clinical Chemistry, 2nd edn. WB Saunders, Philadelphia, pp 492–494

    Google Scholar 

  • Tully DB, Bao W, Goetz AK, Blystone CR, Ren H, Schmid JE, Strader LF, Wood CR, Best DS, Narotsky MG (2006) Gene expression profiling in liver and testis of rats to characterize the toxicity of triazole fungicides. Toxicol App Pharm 215:260–273

    Article  CAS  Google Scholar 

  • Valfré F, Caprino F, Turchini G (2003) The health benefit of seafood. Vet Res Commun 27:507–512

    Article  Google Scholar 

  • Voortman T, van den Hooven EH, Braun KVE, van den Broek M, Bramer WM, Chowdhurry R, Franco OH (2015) Effects of polyunsaturated fatty acid intake and status during pregnancy, lactation, and early childhood on cardiometabolic health: a systematic review. Prog Lipid Res 59:67–87

    Article  CAS  Google Scholar 

  • Zheng SL, Chen B, Qiu XY, Chen M, Ma ZY, Yu XG (2016) Distribution and risk assessment of 82 pesticides in Jiulong River and estuary in South China. Chemosphere 144:1177–1192

    Article  CAS  Google Scholar 

  • Zhong H, Dong L, Dong Q, Ke C, Fu J, Wang X, Liu C, Dai L (2012) Quantitative analysis of aberrant fatty acid composition of zebrafish hepatic lipids induced by organochlorine pesticide using stable isotope-coded transmethylation and gas chromatography-mass spectrometry. Anal Bioanal Chem 404:207–216

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (41376118).

Author information

Authors and Affiliations

  1. Key Laboratory of Ministry of Education for Subtropical Wetland Ecosystem Research, College of the Environment and Ecology, Xiamen University, Xiamen, People’s Republic of China

    Yan Li, Lemeng Zhang, Chonggang Wang & Meng Chen

  2. State Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, People’s Republic of China

    Xiaocui Dong, Zhenghong Zuo & Chonggang Wang

Authors
  1. Xiaocui Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lemeng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhenghong Zuo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chonggang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Meng Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Meng Chen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest

Ethical standards

The procedures described in the present paper respect national and international safety regulations and ethical principles for animal welfare.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 58 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dong, X., Li, Y., Zhang, L. et al. Influence of difenoconazole on lipid metabolism in marine medaka (Oryzias melastigma). Ecotoxicology 25, 982–990 (2016). https://doi.org/10.1007/s10646-016-1655-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-016-1655-5

Keywords

Search

Navigation