Mechanistic toxicity study of perfluorooctanoic acid in zebrafish suggests mitochondrial dysfunction to play a key role in PFOA toxicity

Chemosphere

Volumn 91, Issue 6, 2013, Pages 844-856

  Hagenaars, A ^a   Vergauwen, L ^a   Benoot, D ^a   Laukens, K ^a   Knapen, D ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Mitochondrial dysfunction; Perfluorinated compounds; PFOA; Proteomics; Transcriptomics; Zebrafish

Indexed keywords

AQUATIC ORGANISMS; CELL DEATH; CELL PROLIFERATION; METABOLISM; MOLECULAR BIOLOGY; TISSUE HOMEOSTASIS; TOXICITY;

MITOCHONDRIAL DYSFUNCTION; PERFLUORINATED COMPOUNDS; PFOA; PROTEOMICS; TRANSCRIPTOMICS; ZEBRAFISH;

MITOCHONDRIA;

GLYCOGEN; PERFLUOROOCTANOIC ACID;

APOPTOSIS; AQUATIC ENVIRONMENT; BIOACCUMULATION; CARBOHYDRATE; CONCENTRATION (COMPOSITION); CYPRINID; DOSE-RESPONSE RELATIONSHIP; ECOTOXICOLOGY; GENE EXPRESSION; HOMEOSTASIS; HORMONE; MITOCHONDRION; ORGANIC POLLUTANT; POLLUTION EXPOSURE; PROTEOMICS; TOXICITY TEST;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARBOHYDRATE METABOLISM; CELL ORGANELLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENVIRONMENTAL EXPOSURE; FEMALE; GENETIC TRANSCRIPTION; GLYCOGEN LIVER LEVEL; MALE; MEMBRANE PERMEABILITY; MICROARRAY ANALYSIS; NONHUMAN; OXIDATIVE STRESS; PROTEOMICS; REPRODUCTION; SEX DIFFERENCE; TRANSCRIPTOMICS; TWO DIMENSIONAL GEL ELECTROPHORESIS; ZEBRA FISH;

DANIO RERIO; TELEOSTEI;

EID: 84875674984     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2013.01.056     Document Type: Article

References (41)

1. Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959, 37:911-917.
2. Chen Y., McMillan-Ward E., Kong J., Israels S.J., Gibson S.B. Mitochondrial electron-transport-chain inhibitors of complexes I and II induce autophagic cell death mediated by reactive oxygen species. J. Cell Sci. 2007, 120:4155-4166.
3. Conesa A., Götz S., García-Gómez J.M., Terol J., Talón M., Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21(18):3674-3676.
4. De Coen W.M., Janssen C.R. The use of biomarkers in Daphnia Magna toxicity testing: IV. Cellular energy allocation: a new methodology to assess the energy budget of toxicant-stressed Daphnia populations. J. Aquat. Ecosyst. Stress Recov. 1997, 6:43-55.
5. De Wit M., Keil D., Remmerie N., van der Ven K., van den Brandhof E., Knapen D., Witters E., De Coen W. Molecular targets of TBBPA in zebrafish analysed through integration of genomic and proteomic approaches. Chemosphere 2008, 74:96-105.
6. Desagher S., Martinou J.C. Mitochondria as the central point of apoptosis. Trends Cell Biol. 2000, 10:369-377.
7. DeWitt J.C., Peden-Adams M.M., Keller J.M., Germolec D.R. Immunotoxicity of perfluorinated compounds: recent developments. Toxicol. Pathol. 2012, 40:300-311.
8. Edgar R., Domrachev M., Lash A.E. Gene Expression Omnibus: NCBI gene expression and hybridisation array data repository. Nucleic Acids Res. 2002, 30(1):207-210.
9. Gilliland F.D., Mandel J.S. Mortality among employees of a perfluorooctanoic acid production plant. J. Occup. Med. 1993, 35:950-954.
10. Greenbaum D., Colangelo C., Williams K., Gerstein M. Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol. 2003, 4(9):17.
11. Guruge K.S., Yeung L.W.Y., Yamanaka N., Miyazaki S., Lam P.K.S., Giesy J.P., Jones P.D., Yamashita N. Gene expression profiles in rat liver treated with perfluorooctanoic acid (PFOA). Toxicol. Sci. 2006, 89(1):93-107.
12. Halestrap A.P., Brennerb C. The adenine nucleotide translocase: a central component of the mitochondrial permeability transition pore and key player in cell death. Curr. Med. Chem. 2003, 10(16):1507-1525.
13. Halestrap A.P., Woodfield K.Y., Connern C.P. Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase. J. Biol. Chem. 1997, 272:3346-3354.
14. Hu X.-Z., Hu D.-C. Effects of perfluorooctanoate and perflurooctane sulfonate exposure on hepatoma Hep G2 cells. Arch. Toxicol. 2009, 83:851-861.
15. Hu W.Y., Jones P.D., Upham B.L., Trosko J.E., Lau C., Giesy J.P. Inhibition of gap-junction intercellular communication by perfluorinated compounds in rat liver and dolphin kidney epithelial cell lines in vitro and Sprague-Dawley rats in vivo. Toxicol. Sci. 2002, 68:429-436.
16. Kissa E. Fluorinated Surfactants and Repellents 2001, Marcel Dekker, Inc., New York, USA, pp. 1-615. second ed.
17. Knapen D., Vergauwen L., Laukens K., Blust R. Best practices for hybridisation design in two-colour microarray analysis. Trends Biotechnol. 2009, 27(7):406-414.
18. Lau C., Thibodeaux J.R., Hanson R.G., Narotsky M.G., Rogers J.M., Lindstrom A.B., Strynar M.J. Effects of perfluorooctanoic acid exposure during pregnancy in the mouse. Toxicol. Sci. 2006, 90:510-518.
19. Lee J.J., Schultz I.R. Sex differences in the uptake and disposition of perfluorooctanoic acid in fathead minnows after oral dosing. Environ. Sci. Technol. 2010, 44:491-496.
20. Liu C., Yu K., Shi X., Wang J., Lam P.K., Wu R.S., Zhou B. Induction of oxidative stress and apoptosis by PFOS and PFOA in primary cultured hepatocytes of freshwater tilapia (Oreochromis niloticus). Aquat. Toxicol. 2007, 82:135-143.
21. Luebker D.J., Hansen K.J., Bass N.M., Butenhoff J.L., Seacat A.M. Interactions of fluorochemicals with rat liver fatty acid-binding protein. Toxicology 2002, 176:175-185.
22. Marouga R., David S., Hawkins E. The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal. Bioanal. Chem. 2005, 382:669-678.
23. Nie L., Wu G., Culley D.E., Scholten J.C.M., Zhang W. Integrative analysis of transcriptomic and proteomic data: challenges, solutions and applications. Crit. Rev. Biotechnol. 2007, 27:63-75.
24. Oakes K.D., Sibley P.K., Solomon K.R., Mabury S.A., van Der Kraak G.J. Impact of perfluorooctanoic acid on fathead minnow (Pimephales promeslas) fatty acyl-CoA oxidase activity, circulating steroids, and reproduction in outdoor microcosms. Environ. Toxicol. Chem. 2004, 23(8):1912-1919.
25. O'Rourke B., Cortassa S., Aon M.A. Mitochondrial ion channels: gatekeepers of life and death. Physiology 2005, 20:303-315.
26. Panaretakis T., Shabalina I.G., Grandér D., Shoshan M.C., DePierre J.W. Reactive oxygen species and mitochondria mediate the induction of cell death in human hepatoma HepG2 cells by the rodent peroxisome proliferator and hepatocarcinogen, perfluorooctanoic acid. Toxicol. Appl. Pharmacol. 2001, 173:56-64.
27. Powley C.R., George S.W., Ryan T.W., Buck R.C. Matrix-effect free analytical methods for determination of perfluorinated carboxylic acids in environmental matrixes. Anal. Chem. 2005, 77(19):6353-6358.
28. R Development Core Team (2008). R: a language and environment for statistical computing. Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org.
29. Ritchie M.E., Silver J.D., Oshlack A., Holmes M., Diyagama D., Holloway A., Smyth G.K. A comparison of background correction methods for two-colour microarrays. Bioinformatics 2007, 23:2700-2707.
30. Roe J.H., Dailey R.E. Determination of glycogen with the anthrone reagent. Anal. Biochem. 1966, 15:245-250.
31. Rowe C.L., Hopkins W.A., Zehnder C., Congdon J.D. Metabolic costs incurred by crayfish (Procambarus acutus) in a trace element-polluted habitat: further evidence of similar responses among diverse taxonomic groups. Comp. Biochem. Physiol. 2001, 129C:275-283.
32. Smyth G.K. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 2004, 3(1). Article 3.
33. Smyth G.K., Speed T. Normalization of cDNA microarray data. Methods 2003, 31(4):265-273.
34. Starkov A.A., Wallace K.B. Structural determinants of fluorochemical-induced mitochondrial dysfunction. Toxicol. Sci. 2002, 66:244-252.
35. Taniyasu S., Kannan K., So M.K., Gulkowska A., Sinclair E., Okazawa T., Yamashita N. Analysis of fluorotelomer alcohols, fluorotelomer acids, and short- and lang-chain perfluorinated acids in water and biota. J. Chromatogr. A 2005, 1093:89-97.
36. Vanden Heuvel J.P., Davis J.W., Sommers R., Peterson R.E. Renal excretion of perfluorooctanoic acid in male rats: inhibitory effect of testosterone. J. Biochem. Toxicol. 2006, 7(1):31-36.
37. Walters M.W., Bjork J.A., Wallace K.B. Perfluorooctanoic acid stimulated mitochondrial biogenesis and gene transcription in rats. Toxicology 2009, 264:10-15.
38. Wei Y., Chan L.L., Wang D., Zhang H., Wang J., Dai J. Proteomic analysis of hepatic protein profiles in rare minnow (Gobiocypris rarus) exposed to perfluorooctanoic acid. J. Proteome Res. 2008, 7:1729-1739.
39. Wei Y., Liu Y., Wang J., Tao Y., Dai J. Toxicogenomic analysis of the hepatic effects of perfluorooctanoic acid on rare minnows (Gobiocypris rarus). Toxicol. Appl. Pharmacol. 2008, 226:285-297.
40. Yamashita N., Yeung L.W.Y., Taniyasu S., Kwok K.Y., Petrick G., Gamo T., Guruge K.S., Lam P.K.S., Loganathan B.G. Global distribution of PFOS and related chemicals. Global Contamination Trends of Persistent Organic Chemicals 2011, 593-628. CRC Press, Florida. B.G. Loganathan, P.K.S. Lam (Eds.).
41. Yang J.H. Perfluorooctanoic acid induces peroxisomal fatty acid oxidation and cytokine expression in the liver of male Japanese medaka (Oryzias latipes). Chemosphere 2010, 81(4):548-552.