Skip to main content
SpringerLink
Log in

Proteomic Analysis of Hepatic Tissue in Adult Female Zebrafish (Danio rerio) Exposed to Atrazine

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Atrazine (ATZ), the most common herbicide, is a frequently observed contaminant in freshwater ecosystems. In the present study, two-dimensional gel electrophoresis and matrix-assisted laser desorption/ionization tandem time-of-flight-mass spectrometry, combined with histopathological analysis, were used to detect the hepatic damage in adult female zebrafish (Danio rerio) exposed to ATZ. More than 600 hepatic protein spots were detected in each gel with silver staining, and most of the proteins ranged from 20 to 70 kD and pH 4–9. Through comparison and analysis, 7 proteins were found to be upregulated >2-fold, whereas 6 protein spots were downregulated >2-fold after 10 and 1000 μg/l ATZ exposures for 14 days, which had caused histological effects in zebrafish livers. We found that these changed proteins were associated with a variety of cellular biological processes, such as response to oxidative stress, oncogenesis, etc. The results demonstrated that ATZ comprehensively influenced a variety of cellular and biological processes in zebrafish. The information presented in this study will be helpful in fully understanding the mechanism of the potential effects induced by ATZ 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
Fig. 4

Similar content being viewed by others

References

  • Anderson NL, Anderson NG (1998) Proteome and proteomics: new technologies, new concepts, and new words. Electrophoresis 19:1853–1861

    Article  CAS  Google Scholar 

  • Bogyo M, James HH (2003) Proteomics and genomics. Curr Opin Chem Biol 7:2–4

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Cañestro C, Godoy L, Gonzàlez-Duarte R, Albalat R (2003) Comparative expression analysis of Adh3 during arthropod, urochordate, cephalochordate, and vertebrate development challenges its predicted housekeeping role. Evol Dev 5:157–162

    Article  Google Scholar 

  • Culine S, Honore N, Closson V, Droz JP, Extra JM, Marty M et al (1994) A small GTP-binding protein is frequently overexpressed in peripheral blood mononuclear cells from patients with solid tumours. Eur J Cancer 30:670–674

    Article  Google Scholar 

  • Czarnecka AM, Campanella C, Zummo G, Cappello F (2006) Heat shock protein 10 and signal transduction: a “capsula eburnean” of carcinogenesis? Cell Stress Chaperones 11:287–294

    Article  CAS  Google Scholar 

  • Dong X, Zhu L, Wang J, Wang J, Xie H, Hou X et al (2009) Effects of atrazine on cytochrome P450 enzymes of zebrafish (Danio rerio). Chemosphere 77:404–412

    Article  CAS  Google Scholar 

  • Drosten M, Dhawahir A, Sum EY, Urosevic J, Lechuga CG, Esteban LM et al (2010) Genetic analysis of Ras signalling pathways in cell proliferation, migration and survival. EMBO J 29:1091–1104

    Article  CAS  Google Scholar 

  • Emili AQ, Cageny G (2000) Large scale functional analysis using peptide or protein arrays. Nat Biotechnol 18:393–397

    Article  CAS  Google Scholar 

  • Estonius M, Hoog JO, Danielsson O, Jomvall H (1994) Residues specific for class I11 alcohol dehydrogenase. Site-directed mutagenesis of the human enzyme. Biochemistry 33:15080–15085

    Article  CAS  Google Scholar 

  • Fan W, Yanase T, Morinaga H, Gondo S, Okabe T, Nomura M et al (2007) Atrazine induced aromatase expression is SF-1 dependent: implications for endocrine disruption in wildlife and reproductive cancers in humans. Environ Health Perspect 115:720–727

    Article  Google Scholar 

  • Forné I, Abián J, Cerdà J (2010) Fish proteome analysis: model organisms and non-sequenced species. Proteomics 10:858–872

    Article  Google Scholar 

  • Furuhashi M, Hotamisligil GS (2008) Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nat Rev Drug Discov 7:489–503

    Article  CAS  Google Scholar 

  • Ge J, Cong J, Sun Y, Li G, Zhou Z, Qian C et al (2010) Determination of endocrine disrupting chemicals in surface water and industrial wastewater from Beijing, China. Bull Environ Contam Toxicol 84:401–405

    Article  CAS  Google Scholar 

  • Gfrerer M, Wenzl T, Quan X, Platzer B, Lankmayr E (2002) Occurrence of triazines in surface and drinking water of Liaoning Province in Eastern China. J Biochem Biophys Methods 53:217–228

    Article  CAS  Google Scholar 

  • Goodsell DS (1999) The molecular perspective: the ras oncogene. Oncologist 4:263–264

    CAS  Google Scholar 

  • Iborra FJ, Renau-Piqueras J, Portoles M, Boleda MD, Guerri C, Pares X (1992) Immunocytochemical and biochemical demonstration of formaldhyde dehydrogenase (class III alcohol dehydrogenase) in the nucleus. J Histochem Cytochem 40:1865–1878

    Article  CAS  Google Scholar 

  • Izaki K, Kinouchi H, Watanabe K, Owada Y, Okubo A, Itoh H et al (2001) Induction of mitochondrial heat shock protein 60 and 10 mRNAs following transient focal cerebral ischemia in the rat. Mol Brain Res 88:4–25

    Article  Google Scholar 

  • Jin YX, Chen YY, Jiang YH, Xu MK (2006) Proteome analysis of the silkworm (Bombyx mori. L) colleterial gland during different development stage. Arch Insect Biochem Physiol 61:42–50

    Article  CAS  Google Scholar 

  • Jin YX, Wang WY, Xu C, Fu ZW, Liu WP (2008) Induction of hepatic estrogen-responsive gene transcription by permethrin enantiomers in male adult zebrafish. Aquat Toxicol 88:146–152

    Article  CAS  Google Scholar 

  • Jin YX, Zhang XX, Lu DZ, Sun LW, Qian HF, Liu WP et al (2010a) Histopathological and proteomic analysis of hepatic tissue from adult male zebrafish exposed to 17β-estradiol. Environ Toxicol Pharmacol 29:91–95

    Article  CAS  Google Scholar 

  • Jin YX, Zhang XX, Shu LJ, Chen LF, Sun LW, Qian HF et al (2010b) Oxidative stress response and gene expression with atrazine exposure in adult female zebrafish (Danio rerio). Chemosphere 78:846–852

    Article  CAS  Google Scholar 

  • Karrow NA, McCay JA, Brown RD, Musgrove DL, Guo TL, Germolec DR et al (2005) Oral exposure to atrazine modulates cell-mediated immune function and decreases host resistance to the B16F10 tumor model in female B6C3F1 mice. Toxicology 2009:15–28

    Article  Google Scholar 

  • Kling P, Norman A, Andersson PL, Norrgren L, Förlin L (2008) Gender-specific proteomic responses in zebrafish liver following exposure to a selected mixture of brominated flame retardants. Ecotoxicol Environ Saf 71:319–327

    Article  CAS  Google Scholar 

  • Liang Y, Minami H, Sato F (2008) Isolation of herbicide-resistant 4-hydroxyphenylpyruvate dioxygenase from cultured Coptis japonica cells. Biosci Biotechnol Biochem 72:3059–3062

    Article  CAS  Google Scholar 

  • Liu Y, Wang JS, Wei YH, Zhang HX, Xu MQ, Dai JY (2008) Induction of time-dependent oxidative stress and related transcriptional effects of perfluorododecanoic acid in zebrafish liver. Aquat Toxicol 89:242–250

    Article  CAS  Google Scholar 

  • McElroy JA, Gangnon RE, Newcomb PA, Kanarek MS, Anderson HA, Brook JV et al (2007) Risk of breast cancer for women living in rural areas from adult exposure to atrazine from well water in Wisconsin. J Expo Sci Environ Epidemiol 17:207–214

    Article  CAS  Google Scholar 

  • Moran GR (2005) 4-Hydroxyphenylpyruvate dioxygenase. Arch Biochem Biophys 433:117–128

    Article  CAS  Google Scholar 

  • Nabby-Hansen S, Waterfield MD, Cramer R (2001) Proteomics-post-genomic cartography to understand gene function. Trends Pharmacol Sci 22:376–384

    Article  Google Scholar 

  • Oka T, Tooi O, Mitsui N, Miyahara M, Ohnishi Y, Takase M et al (2008) Effect of atrazine on metamorphosis and sexual differentiation in Xenopus laevis. Aqua Toxicol 87:215–226

    Article  CAS  Google Scholar 

  • Osborne N, Sherry J, Rendell JL, Currie S (2007) The role of hsp90 in 17a-ethynylestradiol-induced endocrine disruption in rainbow trout hepatocytes. Ecotoxicol Environ Saf 68:13–19

    Article  CAS  Google Scholar 

  • Rhee JS, Raisuddin S, Lee KW, Seo JS, Ki JS, Kim IC et al (2009) Heat shock protein (Hsp) gene responses of the intertidal copepod Tigriopus japonicus to environmental toxicants. Comp Biochem Phys C 149:104–112

    Google Scholar 

  • Rusiecki JA, De Roos A, Lee WJ, Dosemeci M, Lubin JH, Hoppin JA et al (2004) Cancer incidence among pesticide applicators exposed to atrazine in the Agricultural Health Study. J Natl Cancer Inst 96:1375–1382

    Article  CAS  Google Scholar 

  • Salaberria I, Hansen BH, Asensio V, Olsvik PA, Andersen RA, Jenssen BM (2009) Effects of atrazine on hepatic metabolism and endocrine homeostasis in rainbow trout (Oncorhynchus mykiss). Toxicol Appl Pharmacol 234:98–106

    Article  CAS  Google Scholar 

  • Sanchez BC, Ralston-Hooper KJ, Kowalski KA, Inerowicz HD, Adamec J, Sepúlveda MS (2009) Liver proteome response of largemouth bass (Micropterus salmoides) exposed to several environmental contaminants: potential insights into biomarker development. Aquat Toxicol 95:52–59

    Article  CAS  Google Scholar 

  • Sanderson JT, Seinen W, Giesy JP, van den Berg M (2000) 2-Chloros-triazine herbicides induce aromatase (CYP19) activity in H295R human adrenocortical carcinoma cells: a novel mechanism for estrogenicity? Toxicol Sci 54:121–127

    Article  CAS  Google Scholar 

  • Sanghani PC, Robinson H, Bennett-Lovsey R, Hurley TD, Bosron WF (2003) Structure-function relationships in human class III alcohol dehydrogenase (formaldehyde dehydrogenase). Chem Biol Interact 143(44):195–200

    Article  Google Scholar 

  • Sass JB, Colangelo A (2006) European Union bans atrazine, while the United States negotiates continued use. Int J Occup Environ Health 12:260–267

    CAS  Google Scholar 

  • Shaw M, Furnas MJ, Fabricius K, Haynes D, Carter S, Eaglesham G et al (2010) Monitoring pesticides in the Great Barrier Reef. Mar Pollut Bull 60:113–122

    Article  CAS  Google Scholar 

  • Slipicevic A, Jørgensen K, Skrede M, Katrine A, Rosnes R, Trøen G, Davidson B, Flørenes VA (2008) The fatty acid binding protein 7 (FABP7) is involved in proliferation and invasion of melanoma cells. BMC Cancer 8:276

    Article  Google Scholar 

  • Song Y, Zhu LS, Xie H, Wang J, Wang JH, Liu W et al (2009) Effects of atrazine on DNA damage and antioxidative enzymes in Vicia faba. Environ Toxicol Chem 28:1055–1062

    Article  CAS  Google Scholar 

  • Suzawa M, Ingraham HA (2008) The herbicide atrazine activates endocrine gene networks via non-steroidal NR5A nuclear receptors in fish and mammalian cells. PloS One 3:e2117

    Article  Google Scholar 

  • Thornton BJ, Elthon TE, Cerny RL, Siegfried BD (2010) Proteomic analysis of atrazine exposure in Drosophila melanogaster (Diptera: Drosophilidae). Chemosphere 81:235–241

    Article  CAS  Google Scholar 

  • United States Department of Agriculture National Agricultural Statistical Service (2008) Agricultural chemical use database. http://www.pestmanagment.info/nass/

  • Unwin RD, Smith DL, Blinco D, Wilson CL, Miller CJ, Evans CA et al (2006) Quantitative proteomics reveals posttranslational control as a regulatory factor in primary hematopoietic stem cells. Blood 107:4687–4694

    Article  CAS  Google Scholar 

  • Wennerberg K, Rossman KL, Channing J, Der CJ (2005) The Ras superfamily at a glance. J Cell Sci 118:843 (National Agricultural Statistical Service 846)

    Article  CAS  Google Scholar 

  • Wit MD, Keil D, Remmerie N, van der Ven K, van den Brandhof EJ, Knapen D et al (2008) Molecular targets of TBBPA in zebrafish analysed through integration of genomic and proteomic approaches. Chemosphere 74:96 (National Agricultural Statistical Service 105)

    Article  Google Scholar 

  • Yang C, Pflugrath JW, Camper DL, Foster ML, Pernich DJ, Walsh TA (2004) Structural basis for herbicidal inhibitor selectivity revealed by comparison of crystal structures of plant and mammalian 4-hydroxyphenylpyruvate dioxygenases. Biochemistry 43:10414 (National Agricultural Statistical Service 10423)

    Article  CAS  Google Scholar 

  • Zheng Y, Quilliam LA (2003) Activation of the Ras superfamily of small GTPases. EMBO Rep 4:463–468

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from National Basic Research Program of China (Grant No. 2010CB126100) and the National Natural Science Foundation of China (Grant No. 20837002).

Author information

Authors and Affiliations

  1. College of Biological and Environmental Engineering, Zhejiang University of Technology, Hangzhou, 310032, China

    Yuanxiang Jin, Xiangxiang Zhang & Zhengwei Fu

  2. College of Life Science, Zhejiang Chinese Medical University, Hangzhou, 310053, China

    Dezhao Lu

Authors
  1. Yuanxiang Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiangxiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dezhao Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhengwei Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhengwei Fu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jin, Y., Zhang, X., Lu, D. et al. Proteomic Analysis of Hepatic Tissue in Adult Female Zebrafish (Danio rerio) Exposed to Atrazine. Arch Environ Contam Toxicol 62, 127–134 (2012). https://doi.org/10.1007/s00244-011-9678-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-011-9678-7

Keywords

Search

Navigation