Lipid peroxidation and oxidative stress responses of salmon fed a diet containing perfluorooctane sulfonic- or perfluorooctane carboxylic acids

Comparative Biochemistry and Physiology - C Toxicology and Pharmacology

Volumn 154, Issue 4, 2011, Pages 288-295

  Arukwe, Augustine ^a   Mortensen, Anne S ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

Atlantic salmon; Lipid peroxidation; Organ differences; Oxidative stress; PFOA; PFOS; PPARs

Indexed keywords

ACYL COENZYME A OXIDASE; MESSENGER RNA; PERFLUOROOCTANESULFONIC ACID; PERFLUOROOCTANOIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; REACTIVE OXYGEN METABOLITE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; KIDNEY PARENCHYMA; LIPID PEROXIDATION; LIVER; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SALMON;

MAMMALIA; SALMO SALAR;

EID: 80052593219     PISSN: 15320456     EISSN: 18781659     Source Type: Journal    
DOI: 10.1016/j.cbpc.2011.06.012     Document Type: Article

References (61)

1. A. Arukwe Toxicological housekeeping genes: do they really keep the house? Environ. Sci. Technol. 40 2006 7944 7949 (Pubitemid 46012601)
2. C. Batista-Pinto, P. Rodrigues, E. Rocha, and A. Lobo-da-Cunha Identification and organ expression of peroxisome proliferator activated receptors in brown trout (Salmo trutta f. fario) Biochim. Biophys. Acta 1731 2005 88 94 (Pubitemid 41715170)
3. K.S. Betts Perfluoroalkyl acids-what is the evidence telling us? Environ Health Perspect. 115 2007 A251 A256
4. L.B. Biegel, M.E. Hurtt, S.R. Frame, J.C. O'Connor, and J.C. Cook Mechanisms of extrahepatic tumor induction by peroxisome proliferators in male CD rats Toxicol. Sci. 60 2001 44 55 (Pubitemid 32229826)
5. J.A. Bjork, and K.B. Wallace Structure-activity relationships and human relevance for perfluoroalkyl acid-induced transcriptional activation of peroxisome proliferation in liver cell cultures Toxicol. Sci. 111 2009 89 99
6. N.A. Bonekamp, A. Volkl, H.D. Fahimi, and M. Schrader Reactive oxygen species and peroxisomes: struggling for balance Biofactors 35 2009 346 355
7. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding Anal. Biochem. 72 1976 248 254
8. O. Braissant, and W. Wahli Differential expression of peroxisome proliferator-activated receptor-α, -β, and -γ during rat embryonic development Endocrinology 139 1998 2748 2754 (Pubitemid 28512383)
9. T.P. Dalton, A. Puga, and H.G. Shertzer Induction of cellular oxidative stress by aryl hydrocarbon receptor activation Chem. Biol. Interact. 141 2002 77 95 (Pubitemid 35223206)
10. M. Dawn-Linsley, F.J. Ekinci, D. Ortiz, E. Rogers, and T.B. Shea Monitoring thiobarbituric acid-reactive substances (TBARs) as an assay for oxidative damage in neuronal cultures and central nervous system J. Neurosci. Methods 141 2005 219 222 (Pubitemid 40126660)
11. K.T. Eriksen, O. Raaschou-Nielsen, M. Sorensen, M. Roursgaard, S. Loft, and P. Moller Genotoxic potential of the perfluorinated chemicals PFOA, PFOS, PFBS, PFNA and PFHxA in human HepG2 cells Mutat. Res. 700 2010 39 43
12. W.A. Gebbink, C.E. Hebert, and R.J. Letcher Perfluorinated carboxylates and sulfonates and precursor compounds in herring gull eggs from colonies spanning the Laurentian Great Lakes of North America Environ. Sci. Technol. 43 2009 7443 7449
13. J.P. Giesy, and K. Kannan Perfluorochemical surfactants in the environment Environ. Sci. Technol. 36 2002 146A 152A (Pubitemid 34279825)
14. B. Gonzalez-Flecha, and B. Demple Genetic responses to free radicals. Homeostasis and gene control Ann. N. Y. Acad. Sci. 899 2000 69 87 (Pubitemid 30352777)
15. S. Green PPAR: a mediator of peroxisome proliferator action Mutat. Res. 333 1995 101 109 (Pubitemid 26024120)
16. K.S. Guruge, L.W. Yeung, N. Yamanaka, S. Miyazaki, P.K. Lam, J.P. Giesy, P.D. Jones, and N. Yamashita Gene expression profiles in rat liver treated with perfluorooctanoic acid (PFOA) Toxicol. Sci. 89 2006 93 107 (Pubitemid 43013759)
17. K.J. Hansen, L.A. Clemen, M.E. Ellefson, and H.O. Johnson Compound-specific, quantitative characterization of organic fluorochemicals in biological matrices Environ. Sci. Technol. 35 2001 766 770 (Pubitemid 32173716)
18. K.J. Hansen, H.O. Johnson, J.S. Eldridge, J.L. Butenhoff, and L.A. Dick Quantitative characterization of trace levels of PFOS and PFOA in the Tennessee River Environ. Sci. Technol. 36 2002 1681 1685 (Pubitemid 34310933)
19. K. Harada, K. Inoue, A. Morikawa, T. Yoshinaga, N. Saito, and A. Koizumi Renal clearance of perfluorooctane sulfonate and perfluorooctanoate in humans and their species-specific excretion Environ. Res. 99 2005 253 261
20. K. Harada, A. Koizumi, N. Saito, K. Inoue, T. Yoshinaga, C. Date, S. Fujii, N. Hachiya, I. Hirosawa, S. Koda, Y. Kusaka, K. Murata, K. Omae, S. Shimbo, K. Takenaka, T. Takeshita, H. Todoriki, Y. Wada, T. Watanabe, and M. Ikeda Historical and geographical aspects of the increasing perfluorooctanoate and perfluorooctane sulfonate contamination in human serum in Japan Chemosphere 66 2007 293 301 (Pubitemid 44791402)
21. F.M. Hekster, R.W.P.M. Laane, and P. DeVoogt Environmental and toxicity effects of perfluoroalkylated substances Rev. Environ. Cont. Toxicol. 179 2003 99 121
22. M. Hermes-Lima, and K.B. Storey Role of antioxidant defenses in the tolerance of severe dehydration by anurans. The case of the leopard frog Rana pipiens Mol. Cell. Biochem. 189 1998 79 89 (Pubitemid 28556551)
23. N.J. Hickey, D. Crump, S.P. Jones, and S.W. Kennedy Effects of 18 perfluoroalkyl compounds on mRNA expression in chicken embryo hepatocyte cultures Toxicol. Sci. 111 2009 311 320
24. P.T. Hoff, K. Van de Vijver, W. Van Dongen, E.L. Esmans, R. Blust, and W.M. De Coen Perfluorooctane sulfonic acid in bib (Trisopterus luscus) and plaice (Pleuronectes platessa) from the Western Scheldt and the Belgian North Sea: distribution and biochemical effects Environ. Toxicol. Chem. 22 2003 608 614 (Pubitemid 36231830)
25. P.T. Hoff, W. Van Dongen, E.L. Esmans, R. Blust, and W.M. De Coen Evaluation of the toxicological effects of perfluorooctane sulfonic acid in the common carp (Cyprinus carpio) Aquat. Toxicol. 62 2003 349 359 (Pubitemid 36197691)
26. M. Houde, J.W. Martin, R.J. Letcher, K.R. Solomon, and D.C.G. Muir Environmental and biological monitoring of polyfluoroalkyl compounds: a critical review Environ. Sci. Technol. 40 2006 3463 3473 (Pubitemid 43830953)
27. X.Z. Hu, and D.C. Hu Effects of perfluorooctanoate and perfluorooctane sulfonate exposure on hepatoma Hep G2 cells Arch. Toxicol. 83 2009 851 861
28. W. Hu, P.D. Jones, T. Celius, and J.P. Giesy Identification of genes responsive to PFOS using gene expression profiling Environ. Toxicol. Pharmacol. 19 2005 57 70 (Pubitemid 39601903)
29. K. Inoue, F. Okada, R. Ito, M. Kawaguchi, N. Okanouchi, and H. Nakazawa Determination of perfluorooctane sulfonate, perfluorooctanoate and perfluorooctane sulfonylamide in human plasma by column-switching liquid chromatography-electrospray mass spectrometry coupled with solid-phase extraction J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 810 2004 49 56 (Pubitemid 39195023)
30. J.P. Kamat, T.P. Devasagayam, K.I. Priyadarsini, and H. Mohan Reactive oxygen species mediated membrane damage induced by fullerene derivatives and its possible biological implications Toxicol. 155 2000 55 61 (Pubitemid 32056314)
31. G.L. Kennedy Jr., J.L. Butenhoff, G.W. Olsen, J.C. O'Connor, A.M. Seacat, R.G. Perkins, L.B. Biegel, S.R. Murphy, and D.G. Farrar The toxicology of perfluorooctanoate Crit. Rev. Toxicol. 34 2004 351 384 (Pubitemid 38888064)
32. E. Kissa Fluorinated surfactants: synthesis, properties, and applications 1994 Marcel Dekker New York
33. H.J. Lehmler Synthesis of environmentally relevant fluorinated surfactants-a review Chemosphere 58 2005 1471 1496
34. S.C. Lema, I.R. Schultz, N.L. Scholz, J.P. Incardona, and P. Swanson Neural defects and cardiac arrhythmia in fish larvae following embryonic exposure to 2,2′,4,4′-tetrabromodiphenyl ether (PBDE 47) Aquat. Toxicol. 82 2007 296 307 (Pubitemid 46602584)
35. Y. Liu, J. Wang, Y. Wei, H. Zhang, and J. Dai Molecular characterization of cytochrome P450 1A and 3A and the effects of perfluorooctanoic acid on their mRNA levels in rare minnow (Gobiocypris rarus) gills Aquat. Toxicol. 88 2008 183 190
36. Y. Liu, J. Wang, Y. Wei, H. Zhang, M. Xu, and J. Dai Induction of time-dependent oxidative stress and related transcriptional effects of perfluorododecanoic acid in zebrafish liver Aquat. Toxicol. 89 2008 242 250
37. V.I. Lushchak, L.P. Lushchak, A.A. Mota, and M. Hermes-Lima Oxidative stress and antioxidant defenses in goldfish Carassius auratus during anoxia and reoxygenation Am. J. Physiol. Regul. Integr. Comp. Physiol. 280 2001 R100 R107
38. J.W. Martin, M.M. Smithwick, B.M. Braune, P.F. Hoekstra, D.C. Muir, and S.A. Mabury Identification of long-chain perfluorinated acids in biota from the Canadian Arctic Environ. Sci. Technol. 38 2004 373 380 (Pubitemid 38095464)
39. L. Michalik, J. Auwerx, J.P. Berger, V.K. Chatterjee, C.K. Glass, F.J. Gonzalez, P.A. Grimaldi, T. Kadowaki, M.A. Lazar, S. O'Rahilly, C.N.A. Palmer, J. Plutzky, J.K. Reddy, B.M. Spiegelman, B. Staels, and W. Wahli International Union of Pharmacology. LXI. Peroxisome proliferator-activated receptors Pharmacol. Rev. 58 2006 726 741 (Pubitemid 44833742)
40. S. Morais, A. Knoll-Gellida, M. Andre, C. Barthe, and P.J. Babin Conserved expression of alternative splicing variants of peroxisomal acyl-CoA oxidase 1 in vertebrates and developmental and nutritional regulation in fish Physiol. Genomics 28 2007 239 252 (Pubitemid 46708767)
41. A.S. Mortensen, R.J. Letcher, M.V. Cangialosi, S. Chu, and A. Arukwe Tissue bioaccumulation patterns, xenobiotic biotransformation and steroid hormone levels in Atlantic salmon (Salmo salar) fed a diet containing perfluoroactane sulfonic or perfluorooctane carboxylic acids Chemosphere 83 2011 1035 1044
42. K. Motojima PPAR-mediated diverse responses in various tissues of mouse Cell. Biochem. Biophys. 32 2000 205 211
43. S. Nakayama, K. Harada, K. Inoue, K. Sasaki, B. Seery, N. Saito, and A. Koizumi Distributions of perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) in Japan and their toxicities Environ. Sci. 12 2005 293 313
44. J.M. O'Brien, A.C. Carew, C. Shaogang, R.J. Letcher, and S.W. Kennedy Perfluorooctane sulfonate (PFOS) toxicity in domestic chicken (Gallus gallus domesticus) embryos in the absence of effects on peroxisome proliferator activated receptor alpha (PPARα)-regulated genes Comp. Biochem. Physiol. Part C 149 2009 524 530
45. J.M. O'Brien, S.W. Kennedy, C. Shaogang, and R.J. Letcher Isomer-specific accumulation of perfluorooctane sulfonate in the liver of chicken embryos exposed in ovo to a technical mixture Environ. Toxicol. Chem. 30 2011 226 231
46. K.D. Oakes, P.K. Sibley, J.W. Martin, D.D. MacLean, K.R. Solomon, S.A. Mabury, and G.J. Van Der Kraak Short-term exposures of fish to perfluorooctane sulfonate: acute effects on fatty acyl-CoA oxidase activity, oxidative stress, and circulating sex steroids Environ. Toxicol. Chem. 24 2005 1172 1181 (Pubitemid 40627939)
47. M. Rakhshandehroo, L.M. Sanderson, M. Matilainen, R. Stienstra, C. Carlberg, P.J. de Groot, M. Muller, and S. Kersten Comprehensive analysis of PPARalpha-dependent regulation of hepatic lipid metabolism by expression profiling PPAR Res. 2007 2007 26839
48. H. Ren, B. Vallanat, D.M. Nelson, L.W.Y. Yeung, K.S. Guruge, P.K.S. Lam, L.D. Lehman-McKeeman, and J.C. Corton Evidence for the involvement of xenobiotic-responsive nuclear receptors in transcriptional effects upon perfluoroalkyl acid exposure in diverse species Reprod. Toxicol. 27 2009 266 277
49. M.B. Rosen, J.E. Schmid, K.P. Das, C.R. Wood, R.D. Zehr, and C. Lau Gene expression profiling in the liver and lung of perfluorooctane sulfonate-exposed mouse fetuses: comparison to changes induced by exposure to perfluorooctanoic acid Reprod. Toxicol. 27 2009 278 288
50. A.M. Seacat, P.J. Thomford, K.J. Hansen, G.W. Olsen, M.T. Case, and J.L. Butenhoff Subchronic toxicity studies on perfluorooctanesulfonate potassium salt in cynomolgus monkeys Toxicol. Sci. 68 2002 249 264 (Pubitemid 34785246)
51. A.M. Seacat, P.J. Thomford, K.J. Hansen, L.A. Clemen, S.R. Eldridge, C.R. Elcombe, and J.L. Butenhoff Sub-chronic dietary toxicity of potassium perfluorooctanesulfonate in rats Toxicology 183 2003 117 131 (Pubitemid 36005393)
52. M.K. So, S. Taniyasu, N. Yamashita, J.P. Giesy, J. Zheng, Z. Fang, S.H. Im, and P.K. Lam Perfluorinated compounds in coastal waters of Hong Kong, South China, and Korea Environ. Sci. Technol. 38 2004 4056 4063 (Pubitemid 39014186)
53. K. Solaas, B.F. Kase, V. Pham, K. Bamberg, M.C. Hunt, and S.E. Alexson Differential regulation of cytosolic and peroxisomal bile acid amidation by PPAR alpha activation favors the formation of unconjugated bile acids J. Lipid. Res. 45 2004 1051 1060 (Pubitemid 38679500)
54. K.B. Storey Oxidative stress: animal adaptations in nature Braz. J. Med. Biol. Res. 29 1996 1715 1733 (Pubitemid 126485423)
55. M.L. Takacs, and B.D. Abbott Activation of mouse and human peroxisome proliferator-activated receptors α, β/δ, γ by perfluorooctanoic acid and perfluorooctane sulfonate Toxicol. Sci. 95 2007 108 117 (Pubitemid 44942782)
56. K.I. Van de Vijver, P.T. Hoff, K. Das, W. Van Dongen, E.L. Esmans, U. Siebert, J.M. Bouquegneau, R. Blust, and W.M. De Coen Baseline study of perfluorochemicals in harbour porpoises (Phocoena phocoena) from Northern Europe Mar. Pollut. Bull. 48 2004 992 997 (Pubitemid 38692356)
57. J.P. Vanden Heuvel, J.T. Thompson, S.R. Frame, and P.J. Gillies Differential activation of nuclear receptors by perfluorinated fatty acid analogs and natural fatty acids: a comparison of human, mouse, and rat peroxisome proliferator-activated receptor-α, -β, and -γ, liver X receptor-β, and retinoid X receptor-α Toxicol. Sci. 92 2006 476 489 (Pubitemid 44018964)
58. Y. Wei, L.L. Chan, D. Wang, H. Zhang, J. Wang, and J. Dai Proteomic analysis of hepatic protein profiles in rare minnow (Gobiocypris rarus) exposed to perfluorooctanoic acid J. Proteome Res. 7 2008 1729 1739
59. Y. Wei, Y. Liu, J. Wang, Y. Tao, and J. Dai Toxicogenomic analysis of the hepatic effects of perfluorooctanoic acid on rare minnows (Gobiocypris rarus) Toxicol. Appl. Pharmacol. 226 2008 285 297 (Pubitemid 351172417)
60. Y. Wei, X. Shi, H. Zhang, J. Wang, B. Zhou, and J. Dai Combined effects of polyfluorinated and perfluorinated compounds on primary cultured hepatocytes from rare minnow (Gobiocypris rarus) using toxicogenomic analysis Aquat. Toxicol. 95 2009 27 36
61. X. Zhang, L. Chen, X.C. Fei, Y.S. Ma, and H.W. Gao Binding of PFOS to serum albumin and DNA: Insight into the molecular toxicity of perfluorochemicals BMC Mol. Biol. 10 2009 16