Mercury contamination in deep-water fish: Transcriptional responses in tusk (Brosme brosme) from a fjord gradient

Aquatic Toxicology

Volumn 144-145, Issue , 2013, Pages 172-185

  Olsvik, Pål A ^a   Lindgren, Michael ^a   Maage, Amund ^a  

^a INSTITUTE OF MARINE RESEARCH   (Norway)

Author keywords

Bioinformatics; Next generation sequencing; Non model fish; Toxicogenomics

Indexed keywords

ALPHA TOCOPHEROL; ARSENIC; ASCORBIC ACID; CADMIUM; CATALASE; FERRITIN; GAMMA TOCOPHEROL; GLUTATHIONE PEROXIDASE 1; LEAD; MERCURY; MESSENGER RNA; METHYLMERCURY; SELENIUM; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TRANSCRIPTOME;

BIOACCUMULATION; COASTAL ZONE; DEEP WATER; ECOTOXICOLOGY; ENVIRONMENTAL STRESS; FISH; FJORD; GENOME; LIPID; MERCURY (ELEMENT); METABOLISM; POLLUTION EFFECT; POLYMERASE CHAIN REACTION; RNA;

ADAPTATION; ANIMAL TISSUE; ARTICLE; BROSME BROSME; ENZYME ACTIVITY; FATTY ACID OXIDATION; FEMALE; FISH; GENETIC TRANSCRIPTION; GENOMICS; LIPID METABOLISM; LIVER; LIVER LEVEL; LIVER TOXICITY; MALE; MASS SPECTROMETRY; MERCURIALISM; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; TRANSCRIPTION REGULATION; WATER CONTAMINATION;

HARDANGERFJORDEN; HORDALAND; NORWAY;

BIOINFORMATICS; NEXT-GENERATION SEQUENCING; NON-MODEL FISH; TOXICOGENOMICS;

ANIMALS; ENVIRONMENTAL MONITORING; GADIFORMES; LIPID METABOLISM; LIVER; MERCURY; OXIDATION-REDUCTION; WATER POLLUTANTS, CHEMICAL;

EID: 84886844585     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2013.10.002     Document Type: Article

References (65)

1. Anders S., Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010, 11:R106.
2. Anderson G.J., Frazer D.M. Hepatic iron metabolism. Semin. Liver Dis. 2005, 25:420-432.
3. Arosio P., Levi S. Cytosolic and mitochondrial ferritins in the regulation of cellular iron homeostasis and oxidative damage. Biochim. Biophys. Acta 2010, 1800:783-792.
4. Baatrup E., Danscher G. Cytochemical demonstration of mercury deposits in trout liver and kidney following methyl mercury intoxication: differentiation of two mercury pools by selenium. Ecotoxicol. Environ. Saf. 1987, 14:129-141.
5. Batchelar K.L., Kidd K.A., Drevnick P.E., Munkittrick K.R., Burgess N.M., Roberts A.P., Smith J.D. Evidence of impaired health in yellow perch (Perca flavescens) from a biological mercury hotspot in northeastern north America. Environ. Toxicol. Chem. 2013, 32:627-637.
6. Beckvar N., Dillon T.M., Read L.B. Approaches for linking whole-body fish tissue residues of mercury or DDT to biological effects thresholds. Environ. Toxicol. Chem. 2005, 24:2094-2105.
7. Berg K., Puntervoll P., Valdersnes S., Goksøyr A. Responses in the brain proteome of Atlantic cod (Gadus morhua) exposed to methylmercury. Aquat. Toxicol. 2010, 100:51-65.
8. Bjornberg K.A., Vahter M., Grawe K.P., Berglund M. Methyl mercury exposure in Swedish women with high fish consumption. Sci. Total Environ. 2005, 341:45-52.
9. Bloom N.S. On the chemical form of mercury in edible fish and marine invertebrate tissue. Can. J. Fish. Aquat. Sci. 1992, 49:1010-1017.
10. Brown A.R., Bickley L.K., Le Page G., Hosken D.J., Paull G.C., Hamilton P.B., Owen S.F., Robinson J., Sharpe A.D., Tyler C.R. Are toxicological responses in laboratory (inbred) zebrafish representative of those in outbred (wild) populations? - a case study with an endocrine disrupting chemical. Environ. Sci. Technol. 2011, 45:4166-4172.
11. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., Vandesompele J., Wittwer C.T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55:611-622.
12. Cambier S., Gonzalez P., Durrieu G., Maury-Brachet R., Boudou A., Bourdineaud J.P. Serial analysis of gene expression in the skeletal muscles of zebrafish fed with a methylmercury-contaminated diet. Environ. Sci. Technol. 2010, 44:469-475.
13. Ceccatelli S., Dare E., Moors M. Methylmercury-induced neurotoxicity and apoptosis. Chem. Biol. Interact. 2010, 188:301-308.
14. Chapman L., Chan H.M. The influence of nutrition on methyl mercury intoxication. Environ. Health Perspect. 2000, 108:29-56.
15. Chumchal M.M., Rainwater T.R., Osborn S.C., Roberts A.P., Abel M.T., Cobb G.P., Smith P.N., Bailey F.C. Mercury speciation and biomagnification in the food web of Caddo Lake, Texas and Louisiana, USA, a subtropical freshwater ecosystem. Environ. Toxicol. Chem. 2011, 30:1153-1162.
16. Cole D.C., Kearney J., Sanin L.H., Leblanc A., Weber J.P. Blood mercury levels among Ontario anglers and sport-fish eaters. Environ. Res. 2004, 95:305-314.
17. Cizdziel J., Hinners T., Cross C., Pollard J. Distribution of mercury in the tissues of five species of freshwater fish from Lake Mead, USA. J. Environ. Monit. 2003, 5:802-807.
18. Comparative Toxicogenomics Database (CTD). Url:. http://ctdbase.org/.
19. Davidson P.W., Leste A., Benstrong E., Burns C.M., Valentin J., Sloane-Reeves J., Huang L.S., Miller W.A., Gunzler D., van Wijngaarden E., Watson G.E., Zareba G., Shamlaye C.F., Myers G.J. Fish consumption, mercury exposure, and their associations with scholastic achievement in the Seychelles Child Development Study. Neurotoxicology 2010, 31:439-447.
20. Depew D.C., Basu N., Burgess N.M., Campbell L.M., Devlin E.W., Drevnick P.E., Hammerschmidt C.R., Murphy C.A., Sandheinrich M.B., Wiener J.G. Toxicity of dietary methylmercury to fish: derivation of ecologically meaningful threshold concentrations. Environ. Toxicol. Chem. 2012, 31:1536-1547.
21. Diez S. Human health effects of methylmercury exposure. Rev. Environ. Contam. Toxicol. 2009, 198:111-132.
22. Di Giulio R.T., Meyer J.N. Reactive oxygen species and oxidative stress. The Toxicology of Fishes 2008, 273-324. CRC Press, Boca Raton. R.T. Di Giulio, D.E. Hinton (Eds.).
23. Di Toyama T., Sumi D., Shinkai Y., Yasutake A., Taguchi K., Tong K.I., Yamamoto M., Kumagai Y. Cytoprotective role of Nrf2/Keap1 system in methylmercury toxicity. Biochem. Biophys. Res. Commun. 2007, 363:645-650.
24. Drevnick P.E., Roberts A.P., Otter R.R., Hammerschmidt C.R., Klaper R., Oris J.T. Mercury toxicity in livers of northern pike (Esox lucius) from Isle Royale, USA. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2008, 147:331-338.
25. Grabherr M.G., Haas B.J., Yassour M., Levin J.Z., Thompson D.A., Amit I., Adiconis X., Fan L., Raychowdhury R., Zeng Q.D., Chen Z.H., Mauceli E., Hacohen N., Gnirke A., Rhind N., di Palma F., Birren B.W., Nusbaum C., Lindblad-Toh K., Friedman N., Regev A. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 2011, 29:644-652.
26. Gonzalez P., Dominique Y., Massabuau J.C., Boudou A., Bourdineaud J.P. Comparative effects of dietary methylmercury on gene expression in liver, skeletal muscle, and brain of the zebrafish (Danio rerio). Environ. Sci. Technol. 2005, 39:3972-3980.
27. Grieb T.M., Driscoll C.T., Gloss S.P., Schofield C.L., Bowie G.L., Porcella D.B. Factors affecting mercury accumulation in fish in the Upper Michigan Peninsula. Environ. Toxicol. Chem. 1990, 9:919-930.
28. Hu Y.H., Zheng W.J., Sun L. Identification and molecular analysis of a ferritin subunit from red drum (Sciaenops ocellatus). Fish Shellfish Immunol. 2010, 28:678-686.
29. Johansson L.H., Borg L.A.H. A spectrophotometric method for determination of catalase activity in small tissue samples. Analyt. Biochem. 1988, 174:331-336.
30. Julshamn K., Maage A., Nordli H.S., Grobecker K.H., Jorhem L., Fecher P. Determination of arsenic, cadmium, mercury and lead by ICP-MS in foods after pressure digestion. NMKL Collaborative Study. J. AOAC Int. 2007, 90:844-856.
31. Julshamn K., Frantzen S., Valdersnes S., Nilsen B., Maage A., Nederaas K. Concentration of mercury, arsenic, cadmium and lead in fillets of Greenland halibut (Reinhardtius hippoglossoides) caught off the coast of northern Norway. Mar. Biol. Res. 2011, 7:733-745.
32. Kensler T.W., Wakabayashi N., Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 2007, 47:89-116.
33. Kidd K., Batchelar K. Mercury. Homeostasis and Toxicology of Non-essential Metals 2012, 237-295. Academic Press, Amsterdam. C.M. Wood, A.P. Farrell, C.J. Brauner (Eds.).
34. Klaper R., Rees C.B., Drevnick P., Weber D., Sandheinrich M., Carvan M.J. Gene expression changes related to endocrine function and decline in reproduction in fathead minnow (Pimephales promelas) after dietary methylmercury exposure. Environ. Health Perspect. 2006, 114:1337-1343.
35. Klaper R., Carter B.J., Richter C.A., Drevnick P.E., Sandheinrich M.B., Tillitt D.E. Use of a 15 k gene microarray to determine gene expression changes in response to acute and chronic methylmercury exposure in the fathead minnow Pimephales promelas Rafinesque. J. Fish Biol. 2008, 72:2207-2280.
36. Kvangarsnes K., Frantzen S., Julshamn K., Sæthre L.J., Nedreaas K., Maage A. Distribution of mercury in a gadoid fish species, tusk (Brosme brosme), and its implication for food safety. J. Food Sci. Eng. 2012, 2:603-615.
37. Lee P.D.K., Giudice L.C., Conover C.A., Powell D.R. Insulin-like growth factor binding protein-1: recent findings and new directions. Proc. Soc. Exp. Biol. Med. 1997, 216:319-357.
38. Lee W.K., Abouhamed M., Thevenod F. Caspase-dependent and -independent pathways for cadmium-induced apoptosis in cultured kidney proximal tubule cells. Am. J. Physiol. Renal Physiol. 2006, 291:F823-F832.
39. Lindberg S., Bullock R., Ebinghaus R., Engstrom D., Feng X., Fitzgerald W., Pirrone N., Prestbo E., Seigneur C. A synthesis of progress and uncertainties in attributing the sources of mercury in deposition. Ambio 2007, 36:19-32. Panel on Source Attribution of Atmospheric Mercury.
40. Liu Q., Basu N., Goetz G., Jiang N., Hutz R.J., Tonellato P.J., Carvan M.J. Differential gene expression associated with dietary methylmercury (MeHg) exposure in rainbow trout (Oncorhynchus mykiss) and zebrafish (Danio rerio). Ecotoxicology 2013, 10.1007/s10646-013-1066-9.
41. Maage A., Bjelland O., Olsvik P., Nilsen B., Julshamn K. Contaminants in fish and seafood products 2011. Miljøgifter i fisk og fiskevarer 2011: Kvikksølv i djupvassfisk og skaldyr frå Hardangerfjorden samt miljøgifter i marine oljer. NIFES report. Norwegian, Summary in English 2012, 1-31.
42. McGeer J.C., Niyogi S., Smith D.S. Cadmium. Homeostasis and Toxicology of Non-essential Metals 2012, 125-184. Academic Press, Amsterdam. C.M. Wood, A.P. Farrell, C.J. Brauner (Eds.).
43. Moran P.W., Aluru N., Black R.W., Vijayan M.M. Tissue contaminants and associated transcriptional response in trout liver from high elevation lakes of Washington. Environ. Sci. Technol. 2007, 41:6591-6597.
44. Morel F.M.M., Kraepiel A.M.L., Amyot M. The chemical cycle and bioaccumulation of mercury. Annu. Rev. Ecol. Syst. 1998, 29:543-566.
45. Nøstbakken O.J., Martin S.A., Cash P., Torstensen B.E., Amlund H., Olsvik P.A. Dietary methylmercury alters the proteome in Atlantic salmon (Salmo salar) kidney. Aquat. Toxicol. 2012, 108:70-77.
46. Nøstbakken O.J., Bredal I.L., Olsvik P.A., Huang T.S., Torstensen B.E. Effect of marine omega 3 fatty acids on methylmercury-induced toxicity in fish and mammalian cells in vitro. J. Biomed. Biotechnol. 2012, Article ID 417652, 13 pp. 10.1155/2012/417652.
47. Olsvik P.A., Amlund H., Torstensen B.E. Dietary lipids modulate methylmercury toxicity in Atlantic salmon. Food Chem. Toxicol. 2011, 49:3258-3271.
48. Olsvik P.A., Brattas M., Lie K.K., Goksøyr A. Transcriptional responses in juvenile Atlantic cod (Gadus morhua) after exposure to mercury-contaminated sediments obtained near the wreck of the German WW2 submarine U-864, and from Bergen Harbor, Western Norway. Chemosphere 2011, 83:552-563.
49. Richter C.A., Garcia-Reyero N., Martyniuk C., Knoebl I., Pope M., Wright-Osment M.K., Denslow N.D., Tillitt D.E. Gene expression changes in female zebrafish (Danio rerio) brain in response to acute exposure to methylmercury. Environ. Toxicol. Chem. 2011, 30:301-308.
50. Roesijadi G. Metallothionein and its role in toxic metal regulation. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 1996, 113:117-123.
51. Ruus A., Green N.W. Monitoring the environmental quality in the Sørfjord 2006. Contaminants in organisms. Overvåking av miljøforholdene i Sørfjorden 2006, Delrapport 3, Miljøgifter i organismer, Norsk institutt for vannforskning. Norwegian, Summary in English 2007, 23-24.
52. Ruus A., Skei J., Green N., Schøyen M. Monitoring the environmental quality in the Sørfjord 2009. Contaminants in organisms. Overvåking av miljøforholdene i Sørfjorden 2009. Metaller i vannmassene, Miljøgifter i organismer. Rapport til KLIF, NIVA-rapport 6018-2010. Norwegian, Summary in English 2010, 1-92.
53. Rutkute K., Nikolova-Karakashian M.N. Regulation of insulin-like growth factor binding protein-1 expression during aging. Biochem. Biophys. Res. Commun. 2007, 361:263-269.
54. Sandheinrich M.B., Wiener J.G. Methylmercury in freshwater fish: recent advances in assessing toxicity of environmental relevant exposures. Environmental Contaminants in Biota Interpreting Tissue Concentrations 2010, Taylor and Francis, Boca Raton. W.N. Beyer, J.P. Meador (Eds.).
55. Schmedes A., Holmer G. 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. 1989, 66:813-817.
56. Søfteland L., Holen E., Olsvik P.A. Toxicological application of primary hepatocyte cell cultures of Atlantic cod (Gadus morhua) - effects of BNF, PCDD and Cd. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2010, 151:401-411.
57. Ung C.Y., Lam S.H., Hlaing M.M., Winata C.L., Korzh S., Mathavan S., Gong Z. Mercury-induced hepatotoxicity in zebrafish: in vivo mechanistic insights from transcriptome analysis, phenotype anchoring and targeted gene expression validation. BMC Genomics 2010, 11:212.
58. Valdersnes S., Maage A., Fliegel D., Julshamn K. A method for the routine determination of methylmercury in marine tissue by GC isotope dilution-ICP-MS. J. AOAC Int. 2012, 95:6.
59. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. RESEARCH0034.
60. Verma S., Tonk I. Effects of sublethal concentrations of mercury on the composition of liver, muscles, and ovary of Notopterus notopterus. Water Air Soil Pollut. 1983, 20:287-292.
61. Wang X., Falcone T., Attaran M.D., Goldberg J.M., Agarwal A., Sharma R.K. Vitamin C and Vitamin E supplementation reduce oxidative stress-induced embryo toxicity and improve the blastocyst development rate. Fertil. Steril. 2002, 78:1272-1277.
62. Wheeler C.R., Salzman J.A., Elsayed N.M., Omaye S.T., Korte D.W. Automated assays for superoxide dismutase, catalase, glutathione peroxidase, and glutathione reductase activity. Anal. Biochem. 1990, 184:193-199.
63. Wiener J.G., Krabbenhoft D.P., Heinz G.H., Scheuhammer A.M. Ecotoxicology of mercury. Handbook of Ecotoxicology 2003, 409-463. Lewis Publishers, Boca Raton, FL. D.J. Hoffman, B.A. Rattner, G.A. Burton, J. Cairns (Eds.).
64. Yadetie F., Karlsen O.A., Lanzen A., Berg K., Olsvik P., Hogstrand C., Goksoyr A. Global transcriptome analysis of Atlantic cod (Gadus morhua) liver after in vivo methylmercury exposure suggests effects on energy metabolism pathways. Aquat. Toxicol. 2013, 126:314-325.
65. Yu F., Wang Z.R., Ju B., Wang Y.Q., Wang J., Bai D.C. Apoptotic effect of organophosphorus insecticide chlorpyrifos on mouse retina in vivo via oxidative stress and protection of combination of vitamins C and E. Exp. Toxicol. Pathol. 2008, 59:415-423.