Skip to main content

Advertisement

SpringerLink
Log in

Review on Methods for Determination of Metallothioneins in Aquatic Organisms

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

One aspect of environmental degradation in coastal areas is pollution from toxic metals, which are persistent and are bioaccumulated by marine organisms, with serious public health implications. A conventional monitoring system of environmental metal pollution includes measuring the level of selected metals in the whole organism or in respective organs. However, measuring only the metal content in particular organs does not give information about its effect at the subcellular level. Therefore, the evaluation of biochemical biomarker metallothionein may be useful in assessing metal exposure and the prediction of potential detrimental effects induced by metal contamination. There are some methods for the determination of metallothioneins including spectrophotometric method, electrochemical methods, chromatography, saturation-based methods, immunological methods, electrophoresis, and RT-PCR. In this paper, different methods are discussed briefly and the comparison between them will be presented.

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

Similar content being viewed by others

References

  1. Margoshes M, Vallee BL (1957) A cadmium protein from equine kidney cortex. J Am Chem Soc 79:4813–4814

    Article  CAS  Google Scholar 

  2. Palmiter RD, Findley SD, Whitmore TE, Durnam DM (1992) MT-III, a brain-specific member of the metallothionein gene family. Proc Natl Acad Sci USA 89:6333–6337

    Article  PubMed  CAS  Google Scholar 

  3. Kameo S, Nakai K, Kurokawa N, Kanehisa T, Naganuma A, Satoh H (2005) Metal components analysis of metallothionein-III in the brain sections of metallothionein-I and metallothionein-II null mice exposed to mercury vapor with HPLC/ICP-MS. Anal Bioanal Chem 381:1514–1519

    Article  PubMed  CAS  Google Scholar 

  4. Decataldo A, Di Leo A, Giandomenico S, Cardellicchio N (2004) Association of metals (mercury, cadmium and zinc) with metallothionein-like proteins in storage organs of stranded dolphins from the Mediterranean Sea (Southern Italy). J Environ Monit 6:361–367

    Article  PubMed  CAS  Google Scholar 

  5. Doki Y, Monden M (2004) Can metallothionein be a useful molecular marker for selecting hepatocellular carcinoma patients for platinum-based chemotherapy? J Gastroenterol 39:1228–1229

    Article  PubMed  Google Scholar 

  6. Nordberg G, Jin T, Leffler P, Svensson M, Zhou T, Nordberg M (2000) Metallothioneins and diseases with special reference to cadmium poisoning. Analusis 28(5):396–400

    Article  CAS  Google Scholar 

  7. Theocharis SE, Margeli AP, Klijanienko JT, Kouraklis GP (2004) Metallothionein expression in human neoplasia. Histopathology 45:103–118

    Article  PubMed  CAS  Google Scholar 

  8. Prusa R, Blastik O, Potesil D, Trnkova L, Zehnalek J, Adam V, Petrlova J, Jelen F (2005) Analytic method for determination of metallothioneins as tumor markers. Clin Chem 51:A56–A56

    Google Scholar 

  9. Raspor B, Dragun Z, Erk M, Ivankovic D, Pavicic J (2004) Is the digestive gland of Mytilus galloprovincialis a tissue of choice for estimating cadmium exposure by means of metallothioneins? Sci Total Environ 333:99–108

    Article  PubMed  CAS  Google Scholar 

  10. Swierzcek S, Abuknesha RA, Chivers I, Baranovska I, Cunningham P, Price RG (2004) Enzyme-immunoassay for the determination of metallothionein in human urine: application to environmental monitoring. Biomarkers 9:331–340

    Article  PubMed  CAS  Google Scholar 

  11. Ivankovic D, Pavicic J, Erk M, Filipovic-Marijic V, Raspor B (2005) Evaluation of the Mytilus galloprovincialis Lam. Digestive gland metallothionein as a biomarker in a long-term field study: seasonal and spatial variability. Mar Pollut Bull 50:1303–1313

    Article  PubMed  CAS  Google Scholar 

  12. Zorita I, Strogyloudi E, Buxens A, Mazon LI, Papathanassiou E, Soto M, Cajaraville MP (2005) Application of two SH-based methods for metallothionein determination in mussels and intercalibration of the spectrophotometric method: laboratory and field studies in the Mediterranean Sea. Biomarkers 10:342–359

    Article  PubMed  CAS  Google Scholar 

  13. Křížková S, Zítka O, Adam V, Beklová M, Horna A, Svobodová Z, Sures B, Trnková L, Zeman L, Kizek R (2007) Possibilities of electrochemical techniques in metallothionein and lead detection in fish tissues. Czech J Anim Sci 52:143–148

    Google Scholar 

  14. Romero-Isart N, Vašák M (2002) Advances in the structure and chemistry of metallothioneins. J Inorg Biochem 88:388–396

    Article  PubMed  CAS  Google Scholar 

  15. Langston WJ, Bebianno MJ, Burt GR (1998) Metal handling strategies in molluscs. In: Langston WJ, Bebianno MJ (eds) Metal metabolism in aquatic environments. Chapman and Hall, London, p 449

  16. Leung KMY, Svavarsson J, Crane M, Morritt D (2002) Influence of static and fluctuating salinity on cadmium uptake and metallothionein expression by the dogwhelk Nucella lapillus (L.). J Exp Mar Biol Ecol 274(2):175–189

    Article  CAS  Google Scholar 

  17. Ross K, Cooper N, Bidwell JR, Elder J (2002) Genetic diversity and metal tolerance of two marine species: a comparison between populations from contaminated and reference sites. Mar Pollut Bull 44:671–679

    Article  PubMed  CAS  Google Scholar 

  18. Pedersen SN, Lundebye AK, Depledge MH (1997) Field application of metallothionein and stress protein biomarkers in the shore crab (Carcinus maenas) exposed to trace metals. Aquat Toxicol 37:183–200

    Article  CAS  Google Scholar 

  19. Schlenk D, Brouwer M (1991) Isolation of three copper metallothionein isoforms from the blue crab (Callinectes sapidus). Aquat Toxicol 20:25–34

    Article  CAS  Google Scholar 

  20. Pavicic J, Skreblin M, Krebar I, Tusek-Zidaric M, Stegnar P (1994) Embryo–larval tolerance of Mytilus galloprovincialis, exposed to elevated seawater metal concentrations: I. Toxic effects of Cd, Zn and Hg in relation to the metallothionein level. Comp Biochem Physiol C Comp Pharmacol Toxicol 107:249–257

    Google Scholar 

  21. Stuhlbacher A, Bradley MC, Naylor C, Calow P (1992) Induction of cadmium tolerance in two clones of Daphnia magna straus. Comp Biochem Physiol C 101(3):571–577

    Article  PubMed  CAS  Google Scholar 

  22. Amiard JC, Amiard-Triquet C, Barka S, Pellerin J, Rainbow PS (2006) Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat Toxicol 76:160–202

    Article  PubMed  CAS  Google Scholar 

  23. Isani G, Andreani G, Kindt M, Carpene E (2000) Metallothioneins (MTs) in marine mollusks. Cell Mol Biol 46(2):311–330

    PubMed  CAS  Google Scholar 

  24. Noel-Lambot F, Bouquegneau JM, Frankenne F, Disteche A (1978) Le role des metallothioneines dans le stockage des metaux; XLIX:13.

  25. Olsson PE, Haux C (1986) Increased hepatic metallothionein content correlates to cadmium accumulation in environmentally exposed perch (Perca fluviatilis). Aquat Toxicol 9:231–242

    Article  CAS  Google Scholar 

  26. Wan M, Hunziker PE, Kagi JHR (1993) Induction of metallothionein synthesis by cadmium and zinc in cultured rabbit kidney cells (RK-13). Biochem J 292:609–615

    PubMed  CAS  Google Scholar 

  27. Costa PM, Repolho T, Caeiro S, Diniz ME, Moura I, Costa MH (2008) Modelling metallothionein induction in the liver of Sparus aurata exposed to metal-contaminated sediments. Ecotoxicol Environ Saf 71(1):117–124

    Article  PubMed  CAS  Google Scholar 

  28. Gonzalez-Bellavista A, Atrian S, Muñoz M, Capdevila M, Fabregas E (2009) Novel potentiometric sensors based on polysulfone immobilized metallothioneins as metal-ionophores. Talanta 77:1528–1533

    Article  PubMed  CAS  Google Scholar 

  29. Filipovic V, Raspor B (2007) Metallothionein in intestine of red mullet, Mullus barbatus as a biomarker of copper exposure in the coastal marine areas. Mar Pollut Bull 54:935–940

    Article  CAS  Google Scholar 

  30. Raspor B, Paic M, Erk M (2001) Analysis of metallothioneins by the modified Brdicka procedure. Talanta 55:109–115

    Article  PubMed  CAS  Google Scholar 

  31. Dabrio M, Rodriguez AR, Bordin G, Bebianno MJ, De Ley M, Sestakova I, Vasak M, Nordberg M (2002) Recent developments in quantification methods for metallothionein. J Inorg Biochem 88:123–134

    Article  PubMed  CAS  Google Scholar 

  32. Húska D, Zítka O, Adam V, Beklová M, Křížková S, Zeman L, Horna A, Havel L, Zehnálek J, Kizek R (2007) A sensor for investigating the interaction between biologically important heavy metals and glutathione. Czech J Anim Sci 52:37–43

    Google Scholar 

  33. El Hourch M, Dudoit A, Amiard JC (2003) Optimization of new voltammetric method for the determination of metallothionein. Electrochim Acta 48:4083–4088

    Article  CAS  Google Scholar 

  34. Klein D, Bartsch R, Summer KH (1990) Quantitation of Cu-containing metallothionein by a Cd-saturation method. Anal Biochem 189:35–39

    Article  PubMed  CAS  Google Scholar 

  35. Eaton DL, Toal BF (1983) A simplified method for quantitating metallothionein in biological tissues. Sci Total Environ 28:375–384

    Article  PubMed  CAS  Google Scholar 

  36. Scheuhammer AM, Cherian MG (1991) Quantification of metallothionein by silver saturation. Meth Enzymol 205:78–83

    Article  PubMed  CAS  Google Scholar 

  37. Ng TY, Rainbow PS, Amiard TC, Amiard JC, Wang WX (2007) Metallothionein turnover, cytosolic distribution and the uptake of Cd by the green mussel Perna viridis. Aquat Toxicol 84:153–161

    Article  PubMed  CAS  Google Scholar 

  38. Marie V, Baudrimont M, Boudou A (2006) Cadmium and zinc bioaccumulation and metallothionein response in two freshwater bivalves (Corbicula fluminea and Dreissena polymorpha) transplanted along a polymetallic gradient. Chemosphere 65:609–617

    Article  PubMed  CAS  Google Scholar 

  39. Viarengo A, Ponzano E, Donderob F (1997) A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic mollusks. Mar Environ Res 44(1):69–84

    Article  CAS  Google Scholar 

  40. Lobinski R, Chassaigne H, Szpunar J (1998) Analysis for metallothioneins using coupled techniques. Talanta 46:271–289

    Article  PubMed  CAS  Google Scholar 

  41. Campenhout KV, Infante HG, Adams F, Blust R (2004) Induction and binding of Cd, Cu, and Zn to metallothionein in carp (Cyprinus carpio) using HPLC–ICP–TOFMS. Toxicol Sci 80:276–287

    Article  PubMed  CAS  Google Scholar 

  42. Miyairi S, Naganuma A (2002) Metallothionein determination by isocratic HPLC with fluorescence derivatization. Meth Mol Biol 186:273–283

    CAS  Google Scholar 

  43. Ghazi IE, Menge S, Miersch J, Chafik A, Benhra A, Elamrani MK, Krauss GJ (2004) Quantification of metallothionein-like proteins in the mussel Mytilus galloprovincialis using RP–HPLC fluorescence detection. Environ Sci Technol 37:5739–5744

    Article  CAS  Google Scholar 

  44. Ndayibagira A, Sunahara GI, Robidoux PY (2007) Rapid isocratic HPLC quantification of metallothionein-like proteins as biomarkers for cadmium exposure in the earthworm Eisenia Andrei. Soil Biol Biochem 39:194–201

    Article  CAS  Google Scholar 

  45. Infante HG, Van Campenhout K, Blust R, Adams FC (2006) Anion-exchange high performance liquid chromatography hyphenated to inductively coupled plasma-isotope dilution-time-of-flight mass spectrometry for speciation analysis of metal complexes with metallothionein isoforms in gibel carp (Carassius auratus gibelio) exposed to environmental metal pollution. J Chromatogr A 1121:184–190

    Article  PubMed  CAS  Google Scholar 

  46. Santiago-Rivas S, Moreda-Pineiro A, Bermejo-Barrera A, Bermejo-Barrera P (2007) Fractionation metallothionein-like proteins in mussels with on line metal detection by high performance liquid chromatography–inductively coupled plasma–optical emission spectrometry. Talanta 71:1580–1586

    Article  PubMed  CAS  Google Scholar 

  47. Campenhout KV, Infante HG, Goemans G, Belpaire C, Adams F, Blust R, Bervoets L (2008) A field survey of metal binding to metallothionein and other cytosolic ligands in liver of eels using an on-line isotope dilution method in combination with size exclusion (SE) high pressure liquid chromatography (HPLC) coupled to inductively coupled plasma time-of-flight mass spectrometry (ICP-TOFMS). Sci Total Environ 394:379–389

    Article  PubMed  CAS  Google Scholar 

  48. Wang J, Dreessen D, Wiederin DR, Houk RS (2001) Measurement of trace elements in proteins extracted from liver by size exclusion chromatography-inductively coupled plasma-mass spectrometry with a magnetic sector mass spectrometer. Anal Biochem 288:89–96

    Article  PubMed  CAS  Google Scholar 

  49. Rodrıguez-Cea A, Arias ARL, Fernandez de la Campa MR, Moreira JC, Sanz-Medel A (2006) Metal speciation of metallothionein in white sea catfish, Netuma barba, and pearl cichlid, Geophagus brasiliensis, by orthogonal liquid chromatography coupled to ICP-MS detection. Talanta 69:963–969

    Article  PubMed  CAS  Google Scholar 

  50. Prange A, Schaumloffel D (2002) Hyphenated techniques for the characterization and quantification of metallothionein isoforms. Anal Bioanal Chem 373:441–453

    Article  PubMed  CAS  Google Scholar 

  51. Schaumloffel D, Prange A, Marx G, Heumann KG, Bratter P (2002) Characterization and quantification of metallothionein isoforms by capillary electrophoresis–inductively coupled plasma-isotope-dilution mass spectrometry. Anal Bioanal Chem 372:155–163

    Article  PubMed  CAS  Google Scholar 

  52. Infante HG, Campenhout KV, Schaumloffel D, Blust R, Adams FC (2003) Multi-element speciation of metalloproteins in fish tissue using size-exclusion chromatography coupled on-line with ICP-isotope dilution-time-of-flight-mass spectrometry. Analyst 128:651–657

    Article  CAS  Google Scholar 

  53. Rodrıguez-Cea A, Fernandez de la Campa MR, Blanco Gonzalez E, Andon Fernandez B, Sanz-Medel A (2003) Metal speciation analysis in eel (Anguilla anguilla) metallothioneins by anionic exchange-FPLC–isotope dilution-ICP-MS. J Anal At Spectrom 18:1357–1364

    Article  CAS  Google Scholar 

  54. Patton WF (2002) Detection technologies in proteome analysis. J Chromatogr B 771:3–31

    Article  CAS  Google Scholar 

  55. Profrock D, Leonhard P, Ruck W, Prange A (2005) Development and characterisation of a new interface for coupling capillary LC with collision-cell ICP-MS and its application for phosphorylation profiling of tryptic protein digests. Anal Bioanal Chem 381:194–204

    Article  PubMed  CAS  Google Scholar 

  56. Montes-Bayon M, Profrock D, Sanz-Medel A, Prange A (2006) Direct comparison of capillary electrophoresis and capillary liquid chromatography hyphenated to collision-cell inductively coupled plasma mass spectrometry for the investigation of Cd-, Cu- and Zn-containing metalloproteins. J Chromatogr A 1114:138–144

    Article  PubMed  CAS  Google Scholar 

  57. Lobinski R (2001) Elemental speciation analysis by capillary electrophoresis with ICP MS and electrospray mass spectrometric detection. Anal Sci 17:i41–i44

    Google Scholar 

  58. Todoli JL, Mermet JM (2006) Sample introduction systems for the analysis of liquid microsamples by ICP-AES and ICP-MS. Spectrochim Acta Part B 61(3):239–283

    Article  CAS  Google Scholar 

  59. Alvarez-Llamas G, Rosario Fernandez de la Campa M, Sanz-Medel A (2003) Sample stacking capillary electrophoresis with ICP-(Q)MS detection for Cd, Cu and Zn speciation in fish liver metallothioneins. J Anal At Spectrom 18:460–466

    Article  CAS  Google Scholar 

  60. Gómez-Ariza JL, Garcia-Barrera T, Lorenzo F, Bernal V, Villegas MJ, Oliveira V (2004) Use of mass spectrometry techniques for the characterization of metal bound to proteins (metallomics) in biological systems. Anal Chim Acta 524:15–22

    Article  CAS  Google Scholar 

  61. Mounicou S, Poleé K, Chassaigne H, Potin-Gautier M, Lobinski R (2000) Characterization of metal complexes with metallothioneins by capillary zone electrophoresis (CZE) with ICP-MS and electrospray (ES)-MS detection. J Anal At Spectrom 15:635–642

    Article  CAS  Google Scholar 

  62. Minami T, Ichida S, Kubo K (2002) Study of metallothionein using capillary zone electrophoresis. J Chromatogr B 781:303–311

    Article  CAS  Google Scholar 

  63. Polec-Pawlak K, Schaumloffel D, Szpunar J, Prange A, Lobinski R (2002) Analysis for metal complexes with metallothionein in rat liver by capillary zone electrophoresis using ICP double-focussing sector-field isotope dilution MS and electrospray MS detection. J Anal Atom Spectrom 17:908–912

    Article  CAS  Google Scholar 

  64. Schaumloffel D, Lobinski R (2005) Isotope dilution technique for quantitative analysis of endogenous trace element species in biological systems. Int J Mass Spectrom 242:217–223

    Article  CAS  Google Scholar 

  65. Honda RT, Araujo RM, Horta BB, Val AL, Demasi M (2005) One-step purification of metallothionein extracted from two different sources. J Chromatogr B 820:205–210

    Article  CAS  Google Scholar 

  66. Haselberg R, de Jong GJ, Somsen GW (2007) Capillary electrophoresis–mass spectrometry for the analysis of intact proteins. J Chromatogr A 1159:81–109

    Article  PubMed  CAS  Google Scholar 

  67. Znidarsic N, Tusek-Znidaric M, Falnoga I, Scancar J, Strus J (2005) Metallothionein-like proteins and zinc–copper interaction in the hindgut of Porcellio scaber (Crustacea: Isopoda) exposed to zinc. Biol Trace Elem Res 106:253–264

    Article  PubMed  CAS  Google Scholar 

  68. Bettmer J, Montes Bayón M, Ruiz Encinar J, Fernández Sánchez ML, Fernández R, de la Campa M, Sanz Medel A (2009) The emerging role of ICP-MS in proteomic analysis. J protomics 72:989–1005

    Article  CAS  Google Scholar 

  69. Moffatt P, Denizeau F (1997) Metallothionein in physiological and physiopathological processes. Drug Metab Rev 29:261–307

    Article  PubMed  CAS  Google Scholar 

  70. Onosaka S, Cherian G (1982) Comparison of metallothionein determination by polarographic and cadmium-saturation methods. Toxicol Appl Pharmacol 63:270–274

    Article  PubMed  CAS  Google Scholar 

  71. Knapen D, Reynders H, Bervoets L, Verheyen E, Blust R (2007) Metallothionein gene and protein expression as a biomarker for metal pollution in natural gudgeon populations. Aquat Toxicol 82:163–172

    Article  PubMed  CAS  Google Scholar 

  72. Rhee J, Raisuddin Sh, Hwang D, Lee K, Kim I, Lee J (2009) Differential expression of metallothionein (MT) gene by trace metals and endocrine-disrupting chemicals in the hermaphroditic mangrovekillifish, Kryptolebias marmoratus. Ecotoxicol Environ Saf 72:206–212

    Article  PubMed  CAS  Google Scholar 

  73. Romeo M, Cosson RP, Gnassia-Barelli M, Risso C, Stien X, Lafaurie M (1997) Metallothionein determination in the liver of the sea bass Dicentrarchus labrax treated with copper and B(a)P. Mar Environ Res 44(3):275–284

    Article  CAS  Google Scholar 

  74. Dieter HH, Müller L, Abel J, Summer KH (1987) Metallothionein-determination in biological materials: interlaboratory comparison of 5 current methods. Experientia Suppl 52:351–358

    PubMed  CAS  Google Scholar 

  75. Nolan CV, Shaikh ZA (1986) Determination of metallothionein in tissues by radioimmunoassay and by cadmium saturation method. Anal Biochem 154(1):213–223

    Article  PubMed  CAS  Google Scholar 

  76. Waalkes MP, Garvey JS, KLaassen CD (1985) Comparison of methods of metallothionein quantification: cadmium radioassay, mercury radioassay, and radioimmunoassay. Toxicol Appl Pharmacol 79(3):524–527

    Article  PubMed  CAS  Google Scholar 

  77. Jebali J, Banni M, Gerbej H, Boussetta H, Lopez-Barea J, Alhama J (2008) Metallothionein induction by Cu, Cd and Hg in Dicentrarchus labrax liver: assessment by RP-HPLC with fluorescence detection and spectrophotometry. Mar Environ Res 65:358

    Article  PubMed  CAS  Google Scholar 

  78. Romero-Ruiz A, Alhama J, Blasco J, Gomez-Ariza JL, Lopez-Barea J (2008) New metallothionein assay in Scrobicularia plana: heating effect and correlation with other biomarkers. Environ Pollut 156(3):1340–1347

    Article  PubMed  CAS  Google Scholar 

  79. Geffard A, Geffard O, Amiard JC, His E, Amiard-Triquet C (2007) Bioaccumulation of metals in sediment elutriates and their effects on growth, condition index and metallothionein contents in oyster larvae. Arch Environ Contam Toxicol 53:57–65

    Article  PubMed  CAS  Google Scholar 

  80. Geffard O, Geffard A, His E, Budzinski H (2003) Assessment of the bioavailability and toxicity of sediment-associated polycyclic aromatic hydrocarbons and heavy metals applied to Crassostrea gigas embryos and larvae. Mar Pollut Bull 46:481–490

    Article  PubMed  CAS  Google Scholar 

  81. Pourang N, Dennis JH, Ghoorchian H (2005) Distribution of heavy metals in Penaeus semisulcatus from Persian Gulf and possible role of metallothionein in their redistribution during storage. Environ Monit Assess 100:71–88

    Article  PubMed  CAS  Google Scholar 

  82. Nunez-Nogueira G, Mouneyrac C, Amiard JC, Rainbow PS (2006) Subcellular distribution of zinc and cadmium in the hepatopancreas and gills of the decapod crustacean Penaeus indicus. Mar Biol 150:197–211

    Article  CAS  Google Scholar 

  83. Berthet B, Mouneyrac C, Amiard JC, Amiard-Triquet C, Berthelot Y, Le Hen A, Mastain O, Rainbow PS, Smith BD (2003) Accumulation and soluble binding of cadmium, copper, and zinc in the polychaete Hediste diversicolor from coastal sites with different trace metal bioavailabilities. Arch Environ Contam Toxicol 45:468–478

    Article  PubMed  CAS  Google Scholar 

  84. Oliveira M, Pacheco M, Santos MA (2008) Organ specific antioxidant responses in golden grey mullet (Liza aurata) following a short-term exposure to phenanthrene. Sci Total Environ 396(1):70–78

    PubMed  CAS  Google Scholar 

  85. Martín-Díaz ML, Blasco J, Sales D, DelValls TA (2008) Field validation of a battery of biomarkers to assess sediment quality in Spanish ports. Environ Pollut A 151:631–640

    Article  CAS  Google Scholar 

  86. Dragun Z, Raspor B, Erk M, Ivankovic D, Pavicic J (2006) The influence of the biometric parameters on metallothionein and metal level in the heat-treated cytosol of the whole soft tissue of transplanted mussels. Environ Monit Assess 114:49–64

    Article  PubMed  CAS  Google Scholar 

  87. Erk M, Muyssen BTA, Ghekier A, Janssen CR (2008) Metallothioneins and cytosolic metals in Neomysis integer exposed to cadmium at different salinities. Mar Environ Res 65:437–444

    Article  PubMed  CAS  Google Scholar 

  88. Oliveira M, Serafim A, Bebianno MJ, Pacheco M, Santos MA (2008) European eel (Anguilla anguilla L.) metallothionein, endocrine, metabolic and genotoxic responses to copper exposure. Ecotoxicol Environ Saf 70:20–26

    Article  PubMed  CAS  Google Scholar 

  89. Bird DJ, Rotchell JM, Hesp SA, Newton LC, Hall NG, Potter IC (2008) To what extent are hepatic concentrations of heavy metals in Anguilla anguilla at a site in a contaminated estuary related to body size and age and reflected in the metallothionein concentrations? Environ Pollut 151:641–651

    Article  PubMed  CAS  Google Scholar 

  90. Ureña R, Peri S, Ramo J, Torreblanca A (2007) Metal and metallothionein content in tissues from wild and farmed Anguilla anguilla at commercial size. Environ Int 33:532–539

    Article  PubMed  Google Scholar 

  91. Fernandes D, Bebianno MJ, Porte C (2008) Hepatic levels of metal and metallothioneins in two commercial fish species of the Northern Iberian shelf. Sci Total Environ 391:159–167

    Article  PubMed  CAS  Google Scholar 

  92. Petrlov J, Krizkova S, Zitk O, Hubalek J, Prusa R, Adam V, Wang J, Beklov M, Sures B, Kizek R (2007) Utilizing a chronopotentiometric sensor technique for metallothionein determination in fish tissues and their host parasites. Sens Actuators B 127:112–119

    Article  CAS  Google Scholar 

  93. Fernandes D, Zanuy S, Bebianno MJ, Porte C (2008) Chemical and biochemical tools to assess pollution exposure in cultured fish. Environ Pollut 152:138–146

    Article  PubMed  CAS  Google Scholar 

  94. Marijic VF, Raspor B (2007) Metal exposure assessment in native fish, Mullus barbatus L., from the Eastern Adriatic Sea. Toxicol Lett 168(3):292–301

    Google Scholar 

  95. Marijic VF, Raspor B (2006) Age- and tissue-dependent metallothionein and cytosolic metal distribution in a native Mediterranean fish, Mullus barbatus, from the Eastern Adriatic Sea. Comp Biochem Physiol C Toxicol Pharmacol 143:382–387

    Article  PubMed  CAS  Google Scholar 

  96. Hardivillier Y, Deni F, Demattei MV, Bustamante P, Laulie M, Cosson R, Metal influence on metallothionein synthesis in the hydrothermal vent mussel Bathymodiolus thermophilus. Comp Biochem Physiol C Pharmacol Toxicol 143: 321-332.

  97. Berthet B, Mouneyrac C, Perez T, Amiard-Triquet C (2005) Metallothionein concentration in sponges (Spongia officinalis) as a biomarker of metal contamination. Comp Biochem Physiol C Toxicol Pharmacol 141:306–313

    Article  PubMed  CAS  Google Scholar 

  98. Geffard A, Amiard-Triquet C, Amiard JC (2005) Do seasonal changes affect metallothionein induction by metals in mussels, Mytilus edulis? Ecotoxicol Environ Saf 61:209–220

    Article  PubMed  CAS  Google Scholar 

  99. Pourang N, Dennis JH (2005) Distribution of trace elements in tissues of two shrimp species from the Persian Gulf and roles of metallothionein in their redistribution. Environ Int 31:325–341

    Article  PubMed  CAS  Google Scholar 

  100. Smaoui-Damak W, Hamza-Chaffai A, Bebianno MJ, Amiard JC (2004) Variation of metallothioneins in gills of the clam Ruditapes decussatus from the Gulf of Gabès (Tunisia). Comp Biochem Physiol C Toxicol Pharmacol 139(4):181–188

    Article  PubMed  CAS  Google Scholar 

  101. Simes C, Bebianno MJ, Moura JJG (2003) Isolation and characterisation of metallothionein from the clam Ruditapes decussates. Aquat Toxicol 63:307–318

    Article  PubMed  CAS  Google Scholar 

  102. Almroth BC, Sturve J, Stephensen E, Holth TF, Frlin L (2008) Protein carbonyls and antioxidant defenses in corkwing wrasse (Symphodus melops) from a heavy metal polluted and a PAH polluted site. Mar Environ Res 66:271–277

    Article  PubMed  CAS  Google Scholar 

  103. Bebianno MJ, Cravo A, Miguel C, Morais S (2003) Metallothionein concentrations in a population of Patella aspera: variation with size. Sci Total Environ 301:151–161

    Article  PubMed  CAS  Google Scholar 

  104. Yang ZB, Zhao YL, Yang J (2007) Effects of copper in water on microstructure of gills and hepatopancreas and its effect on content of metallothionein in Eriocheir sinensis. Arch Environ Contam Toxicol 52:222–228

    Article  PubMed  CAS  Google Scholar 

  105. Chowdhury MJ, Baldisserotto B, Wood CM (2005) Tissue-specific cadmium and metallothionein levels in rainbow trout chronically acclimated to waterborne or dietary cadmium. Arch Environ Contam Toxicol 48:381–390

    Article  PubMed  CAS  Google Scholar 

  106. Li N, Zhao Y, Yang J (2007) Impact of waterborne copper on the structure of gills and hepatopancreas and its impact on the content of metallothionein in juvenile giant freshwater prawn Macrobrachium rosenbergi (Crustacea: Decapoda). Arch Environ Contam Toxicol 52:73–79

    Article  PubMed  CAS  Google Scholar 

  107. Gonzalez P, Baudrimont M, Boudou A, Bourdineaud JP (2006) Comparative effects of direct cadmium contamination on gene expression in gills, liver, skeletal muscles and brain of the zebrafish (Danio rerio). Biometals 19:225–235

    Article  PubMed  CAS  Google Scholar 

  108. Marie V, Gonzalez P, Baudrimont M, Bourdineaud JP, Boudou A (2006) Metallothionein response to cadmium and zinc exposures compared in two freshwater bivalves, Dreissena polymorpha and Corbicula fluminea. Biometals 19(4):399–407

    Article  PubMed  CAS  Google Scholar 

  109. Legeay A, Achard-Joris M, Baudrimont M, Massabuau JC, Bourdineaud JP (2005) Impact of cadmium contamination and oxygenation levels on biochemical responses in the Asiatic clam Corbicula fluminea. Aquat Toxicol 74(3):242–253

    Article  PubMed  CAS  Google Scholar 

  110. Leung KM, Ibrahim H, Dewhurst RE, Morley NG, Crane M, Lewis JW (2003) Concentration of metallothionein-like proteins and heavy metals in the freshwater snail, Lymnaea stagnalis exposed to different levels of waterborne cadmium. Bull Environ Contam Toxicol 71(5):1084–1090

    Article  PubMed  CAS  Google Scholar 

  111. Nga TYT, Rainbow PS, Amiard-Triquet C, Amiard JC, Wang WX (2008) Decoupling of cadmium biokinetics and metallothionein turnover in a marine polychaete after metal exposure. Aquat Toxicol 89:47–54

    Article  CAS  Google Scholar 

  112. Guan R, Wang WX (2006) Comparison between two clones of Daphnia magna: effects of multigenerational cadmium exposure on toxicity, individual fitness, and biokinetics. Aquat Toxicol 76:217–229

    Article  PubMed  CAS  Google Scholar 

  113. Linde AR, Sanchez-Galan S, Valles-Mota P, Vazquez EG (2001) Metallothionein as bioindicator of fdreshwater metal pollution: European eel and brown trout. Ecotoxicol Environ Saf 49:60–63

    Article  PubMed  CAS  Google Scholar 

  114. Steen Redeker E, van Campenhout K, Bervoets L, Reijnders H, Blust R (2007) Subcellular distribution of Cd in the aquatic oligochaete Tubifex tubifex, implications for trophic availability and toxicity. Environ Pollut 148:166–175

    Article  PubMed  CAS  Google Scholar 

  115. Perceval O, Couillard Y, Pinel-Allou B, Bonneris E, Campbell PGC (2006) Long-term trends in accumulated metals (Cd, Cu and Zn) and metallothionein in bivalves from lakes within a smelter-impacted region. Sci Total Environ 369:403–418

    Article  PubMed  CAS  Google Scholar 

  116. Pan L, Zhang H (2006) Metallothionein, antioxidant enzymes and DNA strand breaks as biomarkers of Cd exposure in a marine crab, Charybdis japonica. Comp Biochem Physiol C Comp Pharmacol Toxicol 144:67–75

    Article  CAS  Google Scholar 

  117. De Boeck G, Huong Ngo TT, Van Campenhout K, Blust R (2003) Differential metallothionein induction patterns in three freshwater fish during sublethal copper exposure. Aquat Toxicol 65:413–424

    PubMed  Google Scholar 

  118. Hansen BH, Rømma S, Garmo ØA, Olsvik PA, Andersen RA (2006) Antioxidative stress proteins and their gene expression in brown trout (Salmo trutta) from three rivers with different heavy metal levels. Comp Biochem Physiol C Pharmacol Toxicol 143:263–274

    Article  CAS  Google Scholar 

  119. Olsvik PA, Gundersen P, Andersen RA, Zachariassen KE (2001) Metal accumulation and metallothionein in brown trout, Salmo gairdneri, Rutilus rutilus and Noemachelius barbatulus. Comp Biochem Physiol C Pharmacol Toxicol 128:189–201

    Article  CAS  Google Scholar 

  120. Lavado R, Urena R, Martin-Skilton R, Torreblanca A, del Ramo J, Raldu D, Porte C (2006) The combined use of chemical and biochemical markers to assess water quality along the Ebro River. Environ Pollut 139:330–339

    Article  PubMed  CAS  Google Scholar 

  121. Zhang L, Wang WX (2005) Effects of Zn pre-exposure on Cd and Zn bioaccumulation and metallothionein levels in two species of marine fish. Aquat Toxicol 73:353–369

    Article  PubMed  CAS  Google Scholar 

  122. Bonneris E, Perceval O, Masson S, Hare L, Campbell PGC (2005) Sub-cellular partitioning of Cd, Cu and Zn in tissues of indigenous unionid bivalves living along a metal exposure gradient and links to metal-induced effects. Environl Pollut 135:195–208

    Article  CAS  Google Scholar 

  123. Campbell PGC, Giguere A, Bonneris E, Hare L (2005) Cadmium-handling strategies in two chronically exposed indigenous freshwater organisms—the yellow perch (Perca flavescens) and floater mollusc (Pyganodon grandis). Aquat Toxicol 72:83–97

    Article  PubMed  CAS  Google Scholar 

  124. Perceval O, Couillard Y, Pinel-Alloul B, Giguere A, Campbell PGC (2004) Metal-induced stress in bivalves living along a gradient of Cd contamination: relating sub-cellular metal distribution to population-level responses. Aquat Toxicol 69:327–345

    Article  PubMed  CAS  Google Scholar 

  125. Wu JP, Chen HC (2005) Metallothionein induction and heavy metal accumulation in white shrimp Litopenaeus vannamei exposed to cadmium and zinc. Comp Biochem Physiol C Toxicol Pharmacol 140(3–4):383–394

    Article  PubMed  CAS  Google Scholar 

  126. Silvestre F, Duchene C, Trausch G, Devos P (2005) Tissue-specific cadmium accumulation and metallothionein-like protein levels during acclimation process in the Chinese crab Eriocheir sinensis. Comp Biochem Physiol C Pharmacol Toxicol 140:39–45

    Article  CAS  Google Scholar 

  127. Gillis PL, Reynoldson TB, Dixon DG (2004) Natural variation in a metallothionein-like protein in Tubifex tubifex in the absence of metal exposure. Ecotoxicol Environ Saf 58:22–28

    Article  PubMed  CAS  Google Scholar 

  128. Lecoeur S, Videmann B, Berny P (2004) Evaluation of metallothionein as a biomarker of single and combined Cd/Cu exposure in Dreissena polymorpha. Environ Res 94:184–191

    Article  PubMed  CAS  Google Scholar 

  129. Linde AR, Sanchez-GalaH S, Valles-Mota P, Garcia-Vazquez E (2001) Metallothionein as bioindicator of freshwater metal pollution: European eel and brown trout. Ecotoxicol Environ Saf 49:60–63

    Article  PubMed  CAS  Google Scholar 

  130. De Smet H, De Wachter B, Lobinski R, Blust R (2001) Dynamics of (Cd, Zn)-metallothioneins in gills, liver and kidney of common carp Cyprinus carpio during cadmium exposure. Aquat Toxicol 52:269–281

    Article  PubMed  Google Scholar 

  131. De Smet H, Blust R (2001) Stress responses and changes in protein metabolism in carp Cyprinus carpio during cadmium exposure. Ecotoxicol Environ Saf 48:255–262

    Article  PubMed  CAS  Google Scholar 

  132. Wright J, George S, Martinez-Lara E, Carpenè E, Kindt M (2000) Levels of cellular glutathione and metallothionein affect the toxicity of oxidative stressors in an established carp cell line. Mar Environ Res 50:503–508

    Article  PubMed  CAS  Google Scholar 

  133. Riggio M, Filosa S, Parisi E, Scudiero R (2003) Changes in zinc, copper and metallothionein contents during oocyte growth and early development of the teleost Danio rerio (zebrafish). Comp Biochem Physiol C Pharmacol Toxicol 135:191–196

    Article  CAS  Google Scholar 

  134. Leung KMY, Furness RW (2001) Survival, growth, metallothionein and glycogen levels of Nucella lapillus (L.) exposed to sub-chronic cadmium stress: the influence of nutritional state and prey type. Mar Environ Res 52:173–194

    Article  PubMed  CAS  Google Scholar 

  135. Lavery TJ, Kemper CM, Sanderson K, Schultz CG, Coyle P, Mitchell JG, Seuront L (2009) Heavy metal toxicity of kidney and bone tissues in South Australian adult bottlenose dolphins (Tursiops aduncus). Mar Environ Res 67:1–7

    Article  PubMed  CAS  Google Scholar 

  136. Bouraoui Z, Banni M, Ghedira J, Clerandeau C, Guerbej H, Narbonne JF, Boussetta H (2008) Acute effects of cadmium on liver phase I and phase II enzymes and metallothionein accumulation on sea bream Sparus aurata. Fish Physiol Biochem 34:201–207

    Article  PubMed  CAS  Google Scholar 

  137. Jebali J, Banni M, Guerbej H, Almeida A, Bannaoui A, Boussetta H (2006) Effects of malathion and cadmium on acetylcholinesterase activity and metallothionein levels in the fish Seriola dumerilli. Fish Physiol Biochem 32:93–98

    Article  PubMed  CAS  Google Scholar 

  138. Linde-Arias R, Inácio AF, de Alburquerque C, Freire MM, Moreira JC (2008) Biomarkers in an invasive fish species, Oreochromis niloticus, to assess the effects of pollution in a highly degraded Brazilian river. Sci Total Environ 399:186–192

    Article  PubMed  CAS  Google Scholar 

  139. Pytharopoulou S, Sazakli E, Grintzalis K, Georgiou CD, Leotsinidis M, Kalpaxis DL (2008) Translational responses of Mytilus galloprovincialis to environmental pollution: integrating the responses to oxidative stress and other biomarker responses into a general stress index. Aquat Toxicol 89:18–27

    Article  PubMed  CAS  Google Scholar 

  140. Pytharopoulou S, Kouvela EC, Sazakli E, Leotsinidis M, Kalpaxis DL (2006) Evaluation of the global protein synthesis in Mytilus galloprovincialis in marine pollution monitoring: seasonal variability and correlations with other biomarkers. Aquat Toxicol 80:33–41

    Article  PubMed  CAS  Google Scholar 

  141. Linde-Arias R, Inacio AF, Novo LA, de Alburquerque C, Moreira JC (2008) Multibiomarker approach in fish to assess the impact of pollution in a large Brazilian river, Paraiba do Sul. Environ Pollut 156(3):974–979

    Article  PubMed  CAS  Google Scholar 

  142. Falfushynska HI, Stolyar OB (2009) Responses of biochemical markers in carp Cyprinus carpio from two field sites in Western Ukraine. Ecotoxicol Environ Saf 72(3):729–736

    Article  PubMed  CAS  Google Scholar 

  143. Won EJ, Raisuddin Sh, Shin KH (2008) Evaluation of induction of metallothionein-like proteins (MTLPs) in the polychaetes for biomonitoring of heavy metal pollution in marine sediments. Mar Pollut Bull 57:544–551

    Article  PubMed  CAS  Google Scholar 

  144. Donnin F, Dinelli E, Sangiorgi F, Fabbri E (2007) A biological and geochemical integrated approach to assess the environmental quality of a coastal lagoon (Ravenna, Italy). Environ Int 33:919–928

    Article  CAS  Google Scholar 

  145. Schiedek D, Broeg K, Barsien J, Lehtone KK, Gercke J, Pfeifer S, Vuontisjarvi H, Vuorine PJ, Dedonyte V, Koehler A, Balk L, Schneider R (2006) Biomarker responses as indication of contaminant effects in blue mussel (Mytilus edulis) and female eelpout (Zoarces viviparus) from the southwestern Baltic Sea. Mar Pollut Bull 53:387–405

    Article  PubMed  CAS  Google Scholar 

  146. Domouhtsidou GP, Dailianis S, Kaloyianni M, Dimitriadis VK (2004) Lysosomal membrane stability and metallothionein content in Mytilus galloprovincialis (L.), as biomarkers: combination with trace metal concentrations. Mar Pollut Bull 48:572–586

    Article  PubMed  CAS  Google Scholar 

  147. Vergani L, Grattarola M, Grasselli E, Dondero F, Viarengo A (2007) Molecular characterization and function analysis of MT-10 and MT-20 metallothionein isoforms from Mytilus galloprovincialis. Arch Biochem Biophys 465:247–253

    Article  PubMed  CAS  Google Scholar 

  148. Da Ros L, Moschino V, Guerzoni S, Halldórsson HP (2007) Lysosomal responses and metallothionein induction in the blue mussel Mytilus edulis from the south-west coast of Iceland. Environ Int 33:362–369

    Article  PubMed  CAS  Google Scholar 

  149. Leinio S, Lehtonen KK (2005) Seasonal variability in biomarkers in the bivalves Mytilus edulis and Macoma balthica from the northern Baltic sea. Comp Biochem Physiol C Toxicol Pharmacol 140:408–421

    Article  PubMed  CAS  Google Scholar 

  150. Brown RJ, Galloway TS, Lowe D, Browne MA, Dissanayake MB, Jones A, Depledge MH (2004) Differential sensitivity of three marine invertebrates to copper assessed using multiple biomarkers. Aquat Toxicol 66:267–278

    Article  PubMed  CAS  Google Scholar 

  151. Park H, Ahn IY, Choi HJ, Pyo SH, Lee HE (2007) Cloning, expression and characterization ofmetallothionein from the Antarctic clam Laternula elliptica. Protein Expr Purif 52:82–88

    Article  PubMed  CAS  Google Scholar 

  152. Bouskill NJ, Handy RD, Ford TE, Galloway TS (2006) Differentiating copper and arsenic toxicity using biochemical biomarkers in Asellus aquaticus and Dreissena polymorpha. Ecotoxicol Environ Saf 65:342–349

    Article  PubMed  CAS  Google Scholar 

  153. Hansson T, Schiedek D, Lehtone KK, Vuorinen PJ, Liewenborg B, Noaksso E, Tjarnlund U, Hanson M, Balk L (2006) Biochemical biomarkers in adult female perch (Perca fluviatilis) in a chronically polluted gradient in the Stockholm recipient (Sweden). Mar Pollut Bull 53:451–468

    Article  PubMed  CAS  Google Scholar 

  154. Geracitano LA, Bocchetti R, Monserrat JM, Regoli F, Bianchini A (2004) Oxidative stress responses in two populations of Laeonereis acuta (Polychaeta, Nereididae) after acute and chronic exposure to copper. Mar Environ Res 58:1–17

    Article  PubMed  CAS  Google Scholar 

  155. Campana O, Sarasquete C, Blasco J (2003) Effect of lead on ALA-D activity, metallothionein levels, and lipid peroxidation in blood, kidney, and liver of the toadfish Halobatrachus didactylus. Ecotoxicol Environ Saf 55:116–125

    Article  PubMed  CAS  Google Scholar 

  156. Zanette J, Monserrat JM, Bianchini A (2006) Biochemical biomarkers in gills of mangrove oyster Crassostrea rhizophorae from three Brazilian estuaries. Comp Biochem Physiol C Pharmacol Toxicol 143:187–195

    Article  CAS  Google Scholar 

  157. Choi HJ, Ji J, Chung KH, Ahn IY (2007) Cadmium bioaccumulation and detoxification in the gill and digestive gland of the Antarctic bivalve Laternula elliptica. Comp Biochem Physiol C Pharmacol Toxicol 145:227–235

    Article  CAS  Google Scholar 

  158. Eroglu K, Atli G, Canli M (2005) Effects of metal (Cd, Cu, Zn) interactions on the profiles of metallothionein-like proteins in the Nile fish Oreochromis niloticus. Bull Environ Contam Toxicol 75:390–399

    Article  PubMed  CAS  Google Scholar 

  159. Hyllandt K, Haux C, Hogstrand C, Sletten K, Andersen RA (1994) Properties of cod metallothionein, its presence in different tissues and effects of Cd and Zn treatment. Fish Physiol Biochem 13:81–91

    Article  Google Scholar 

  160. Alhama J, Romero-Ruiz A, Lopez-Barea J (2006) Metallothionein quantification in clams by reversed-phase high-performance liquid chromatography coupled to fluorescence detection after monobromobimane derivatization. J Chromatogr A 1107:52–58

    Article  PubMed  CAS  Google Scholar 

  161. Ryu SK, Park JS, Lee IS (2003) Purification and characterization of a copper-binding protein from Asian periwinkle Littorina brevicula. Comp Biochem Physiol C Pharmacol Toxicol 134:101–107

    Article  Google Scholar 

  162. Santiago-Rivas S, Moreda-Pineiro A, Bermejo-Barrera P, Moreda-Pineiro J, Alonso-Rodrıguez E, Muniategui-Lorenzo S, Lopez-Mahıa P, Prada-Rodrıguez D (2007) Pressurized liquid extraction-assisted mussel cytosol preparation for the determination of metals bound to metallothionein-like proteins. Anal Chim Acta 603:36–43

    Article  PubMed  CAS  Google Scholar 

  163. Mosleh YY, Paris-Palacios S, Ahmed MT, Mahmoud FM, Osman MA, Biagianti-Risbourg S (2007) Effects of chitosan on oxidative stress and metallothioneins in aquatic worm Tubifex tubifex (Oligochaeta, Tubificidae). Chemosphere 67:167–175

    Google Scholar 

  164. Mosleh YY, Paris-Palacios S, Biagianti-Risbourg S (2008) Metallothioneins induction and antioxidative response in aquatic worms Tubifex tubifex (Oligochaeta, Tubificidae) exposed to copper. Chemosphere 64:121–128

    Article  CAS  Google Scholar 

  165. Baykan U, Atli G, Canli M (2007) The effects of temperature and metal exposures on the profiles of metallothionein-like proteins in Oreochromis niloticus. Environ Toxicol Pharmacol 23:33–38

    Article  CAS  PubMed  Google Scholar 

  166. Mosleh YY, Paris-Palacios S, Couderchet M, Biagianti-Risbourg S, Vernet G (2005) Metallothionein induction, antioxidative responses, glycogen and growth changes in Tubifex tubifex (Oligochaete) exposed to the fungicide, fenhexamid. Environ Pollut 135:73–82

    Article  PubMed  CAS  Google Scholar 

  167. del Castillo E, Robinson WE (2008) Nuclear and cytosolic distribution of metallothionein in the blue mussel Mytilus edulis L. Comp Biochem Physiol B Biochem Mol Biol 151(1):46–51

    Article  PubMed  CAS  Google Scholar 

  168. Rose WL, Nisbet RM, Green PG, Norris S, Fan T, Smith EH, Cherr G, Anderson SL (2006) Using an integrated approach to link biomarker responses and physiological stress to growth impairment of cadmium-exposed larval topsmelt. Aquat Toxicol 80:298–308

    Article  PubMed  CAS  Google Scholar 

  169. Carvalho CS, Selistre de Araujo HS, Fernandes MN (2004) Hepatic metallothionein in a teleost (Prochilodus scrofa) exposed to copper at pH 4.5 and pH 8.0. Comp Biochem Physiol B Biochem Mol Biol 137:225–234

    Article  CAS  Google Scholar 

  170. Profrock D, Prange A, Schaumloffel D, Ruck W (2003) Optimization of capillary electrophoresis–inductively coupled plasma mass spectrometry for species analysis of metallothionein-like proteins extracted from liver tissues of Elbe-bream and roe deer. Spectrochim Acta Part B 58(8):1403–1415

    Article  CAS  Google Scholar 

  171. Zaroogian G, Norwood C (2002) Glutathione and metallothionein status in an acute response by Mercenaria mercenaria brown cells to copper in vivo. Ecotoxicol Environ Saf 53:285–292

    Article  PubMed  CAS  Google Scholar 

  172. Woo S, Yum S, Jung JH, Shim WJ, Lee CH, Lee TK (2006) Heavy metal-induced differential gene expression of metallothionein in Javanese medaka, Oryzias javanicus. Mar Biotechnol 8:654–662

    Article  PubMed  CAS  Google Scholar 

  173. Choi CY, An KW, Nelson ER, Habibi HR (2007) Cadmium affects the expression of metallothionein (MT) and glutathione peroxidase (GPX) mRNA in goldfish, Carassius auratus. Comp Biochem Physiol C 145:595–600

    Google Scholar 

  174. Wu SM, Zheng YD, Kuo CH (2008) Expression of mt2 and smt-B upon cadmium exposure and cold shock in zebrafish (Danio rerio). Comp Biochem Physiol C 148:184–193

    Google Scholar 

  175. Man AKY, Woo NYS (2008) Upregulation of metallothionein and glucose-6-phosphate dehydrogenase expression in silver sea bream, Sparus sarba exposed to sublethal levels of cadmium. Aquat Toxicol 89(4):214–221

    Article  PubMed  CAS  Google Scholar 

  176. Wang L, Song L, Ni D, Zhang H, Liu W (2009) Alteration of metallothionein mRNA in bay scallop Argopecten irradians under cadmium exposure and bacteria challenge. Comp Biochem Physiol C Pharmacol Toxicol 149(1):50–57

    Article  CAS  Google Scholar 

  177. Capasso C, Carginale V, Riggio M, Scudiero R, Temussi PA, Trinchella F, Parisi E (2006) Metal detoxification and homeostasis in Antarctic notothenioids. A comparative survey on evolution, expression and functional properties of fish and mammal metallothioneins. Rev Environ Sci Biotechnol 5:253–267

    Article  CAS  Google Scholar 

  178. Cheuk WK, Chan PCY, Chan KM (2008) Cytotoxicities and induction of metallothionein (MT) and metal regulatory element (MRE)-binding transcription factor-1 (MTF-1) messenger RNA levels in the zebrafish (Danio rerio) ZFL and SJD cell lines after exposure to various metal ions. Aquat Toxicol 89(2):103–112

    Article  PubMed  CAS  Google Scholar 

  179. Chan KM, Ku L, Chan PCY, Cheuk WK (2006) Metallothionein gene expression in zebrafish embryo-larvae and ZFL cell-line exposed to heavy metal ions. Mar Environ Res 62:S83–S87

    Article  PubMed  CAS  Google Scholar 

  180. Chen WY, Christopher John JA, Lin CH, Lin HF, Wu SC, Lin CH, Chang CY (2004) Expression of metallothionein gene during embryonic and early larval development in zebrafish. Aquat Toxicol 69:215–227

    Article  PubMed  CAS  Google Scholar 

  181. Ferencz Á, Hermesz E (2008) Identification and characterization of two mtf-1 genes in common carp. Comp Biochem Physiol C Pharmacol Toxicol 148(3):238–243

    Article  CAS  Google Scholar 

  182. Bigot A, Doyen P, Vasseur P, Rodius F (2009) Metallothionein coding sequence identification and seasonal mRNA expression of detoxification genes in the bivalve Corbicula fluminea. Ecotoxicol Environ Saf 72(2):382–387

    Article  PubMed  CAS  Google Scholar 

  183. Gao D, Wang GT, Chen XT, Nie P (2009) Metallothionein-2 gene from the mandarin fish Siniperca chuatsi: cDNA cloning, tissue expression, and immunohistochemical localization. CompBiochem Physiol C Pharmacol Toxicol 149:18–25

    Article  CAS  Google Scholar 

  184. Fasulo S, Mauceri A, Giannetto A, Maisano M, Bianchi N, Parrino V (2008) Expression of metallothionein mRNAs by in situ hybridization in the gills of Mytilus galloprovincialis, from natural polluted environments. Aquat Toxicol 88:62–68

    Article  PubMed  CAS  Google Scholar 

  185. Wu SM, Lin HC, Yang WL (2008) The effects of maternal Cd on the metallothionein expression in tilapia (Oreochromis mossambicus) embryos and larvae. Aquat Toxicol 87(4):296–302

    Article  PubMed  CAS  Google Scholar 

  186. Swain SC, Keusekotten K, Baumeister R, Sturzenbaum SR (2004) C. elegans metallothioneins: new insights into the phenotypic effects of cadmium toxicosis. J Mol Biol 341:951–959

    Article  PubMed  CAS  Google Scholar 

  187. Guo L, Fu C, Miao W (2008) Cloning, characterization, and gene expression analysis of a novel cadmium metallothionein gene in Tetrahymena pigmentosa. Gene 423(1):29

    Article  PubMed  CAS  Google Scholar 

  188. Minghetti M, Leaver MJ, Carpenè E, George SG (2008) Copper transporter 1, metallothionein and glutathione reductase genes are differentially expressed in tissues of sea bream (Sparus aurata) after exposure to dietary or waterborne copper. Comp Biochem Physiol C Pharmacol Toxicol 147:450–459

    Article  CAS  Google Scholar 

  189. Kim JH, Wang SY, Kim IC, Ki JS, Raisuddin S, Lee JS, Han KN (2008) Cloning of a river pufferfish (Takifugu obscurus) metallothionein cDNA and study of its induction profile in cadmium-exposed fish. Chemosphere 71:1251–1259

    Article  PubMed  CAS  Google Scholar 

  190. An KW, Shin HS, Choi CY (2008) Physiological responses and expression of metallothionein (MT) and superoxide dismutase (SOD) mRNAs in olive flounder, Paralichthys olivaceus exposed to benzo[a]pyrene. Comp Biochem Physiol B Biochem Mol Biol 149:534–539

    Article  PubMed  CAS  Google Scholar 

  191. Park H, Ahn IY, Choi HJ, Pyo SH, Lee HE (2007) Cloning, expression and characterization of metallothionein from the Antarctic clam Laternula elliptica. Protein Expres Purif 52:82–88

    Article  CAS  Google Scholar 

  192. Chung MJ, Walker PA, Hogstrand C (2006) Dietary phenolic antioxidant, caffeic acid and Trolox, protect rainbow trout gill cell from nitric oxide-induced apoptosis. Aquat Toxicol 80:321–328

    Article  PubMed  CAS  Google Scholar 

  193. Vergani L, Lanza C, Borghi C, Scarabelli L, Panfoli I, Burlando B, Dondero F, Viarengo A, Gallo G (2007) Effects of growth hormone and cadmium on the transcription regulation of two metallothionein isoforms. Mol Cell Endocrinol 263:29–37

    Article  PubMed  CAS  Google Scholar 

  194. Roberts AP, Oris JT (2004) Multiple biomarker response in rainbow trout during exposure to hexavalent chromium. Comp Biochem Physiol C PharmacolToxicol 138:221–228

    Article  CAS  Google Scholar 

  195. Ng TYT, Wood CM (2008) Trophic transfer and dietary toxicity of Cd from the oligochaete to the rainbow trout. Aquat Toxicol 87:47–59

    Article  PubMed  CAS  Google Scholar 

  196. Wangsongsak A, Utarnpongsa S, Kruatrachue M, Ponglikitmongkol M, Pokethitiyook P, Sumranwanich T (2007) Alterations of organ histopathology and metallolhionein mRNA expression in silver barb, Puntius gonionotus during subchronic cadmium exposure. J Environ Sci 19:1341–1348

    Article  CAS  Google Scholar 

  197. He P, Xu M, Ren H (2007) Cloning and functional characterization of 5′-upstream region of metallothionein-I gene from crucian carp (Carassius cuvieri). Int J Biochem Cell Biol 39:832–841

    Article  PubMed  CAS  Google Scholar 

  198. Migliarini B, Campisi AM, Maradonna F, Truzzi C, Annibaldi A, Scarponi G, Carnevali O (2005) Effects of cadmium exposure on testis apoptosis in the marine teleost Gobius niger. Gen Comp Endocrinol 142:241–247

    Article  PubMed  CAS  Google Scholar 

  199. Knapen D, Redeker ES, Inacio I, De Coen W, Verheyen E, Blust R (2005) New metallothionein mRNAs in Gobio gobio reveal at least three gene duplication events in cyprinid metallothionein evolution. Comp Biochem Physiol C Pharmacol Toxicol 140:347–355

    Article  CAS  Google Scholar 

  200. Tom M, Chen N, Segev M, Herut B, Rinkevich B (2004) Quantifying fish metallothionein transcript by real time PCR for its utilisation as an environmental biomarker. Mar Pollut Bull 48:705–710

    Article  PubMed  CAS  Google Scholar 

  201. Hansen BH, Rømma S, Søfteland IR, Olsvik A, Andersen RA (2006) Induction and activity of oxidative stress-related proteins during waterborne Cu-exposure in brown trout (Salmo trutta). Chemosphere 65:1707–1714

    Article  PubMed  CAS  Google Scholar 

  202. Guinand B, Rolland JL, Bonhomme F (2008) Genetic structure of the common sole (Solea solea) in the Bay of Biscay: nurseries as units of selection? Estuar Coast Shelf Sci 78:316–326

    Article  Google Scholar 

  203. Cheung APL, Lam THJ, Chan KM (2004) Regulation of tilapia metallothionein gene expression by heavy metal ions. Mar Environ Res 58:389–394

    Article  PubMed  CAS  Google Scholar 

  204. Hollis L, Hogstrand C, Wood CM (2001) Tissue-specific cadmium accumulation, metallothionein induction, and tissue zinc and copper levels during chronic sublethal cadmium exposure in juvenile rainbow trout. Arch Environ Contam Toxicol 41:468–474

    Article  PubMed  CAS  Google Scholar 

  205. Mayer GD, Leach A, Kling P, Olsson PE, Hogstrand C (2003) Activation of the rainbow trout metallothionein-A promoter by silver and zinc. Comp Biochem Physiol B Biochem Mol Biol 134:181–188

    Article  PubMed  Google Scholar 

  206. Wu SM, Ho YC, Shih MJ (2007) Effects of Ca2+ or Na+ on metallothionein expression in tilapia larvae (Oreochromis mossambicus) exposed to cadmium or copper. Arch Environ Contam Toxicol 52:229–234

    Article  PubMed  CAS  Google Scholar 

  207. Wu SM, Jong KJ, Lee YJ (2006) Relationships among metallothionein, cadmium accumulation, and cadmium tolerance in three species of fish. Bull Environ Contam Toxicol 76:595–600

    Article  PubMed  CAS  Google Scholar 

  208. Yudkovski Y, Rogowska-Wrzesinska A, Yankelevich I, Shefer E, Heru B, Tom M (2008) Quantitative immunochemical evaluation of fish metallothionein upon exposure to cadmium. Mar Environ Res 65:427–436

    Article  PubMed  CAS  Google Scholar 

  209. Wu SM, Shih MJ, Ho YC (2007) Toxicological stress response and cadmium distribution in hybrid tilapia (Oreochromis sp.) upon cadmium exposure. Comp Biochem Physiol C Pharmacol Toxicol 145:218–226

    Article  CAS  Google Scholar 

  210. Auffret M, Rousseau S, Boutet I, Tanguy A, Baron J, Moraga D, Duchemin M (2006) A multiparametric approach for monitoring immunotoxic responses in mussels from contaminated sites in Western Mediterranea. Ecotoxicol Environ Saf 63:393–405

    Article  PubMed  CAS  Google Scholar 

  211. Chavez-Crooker P, Pozo P, Castro H, Dice MS, Boutet I, Tanguy A, Moraga D, Ahearn GA (2003) Cellular localization of calcium, heavy metals, and metallothionein in lobster (Homarus americanus) hepatopancreas. Comp Biochem Physiol C Pharmacol Toxicol 136:213–224

    Article  CAS  Google Scholar 

  212. Meistertzheim A, Lejart M, Le Goïc N, Thébault M (2009) Sex- gametogenesis, and tidal height-related differences in levels of HSP70 and metallothioneins in the Pacific oyster Crassostrea gigas. Comp Biochem Physiol A 152:234–239

    Google Scholar 

  213. Atif F, Kaur M, Yousuf S, Raisuddin Sh (2006) In vitro free radical scavenging activity of hepatic metallothionein induced in an Indian freshwater fish, Channa punctata Bloch. Chem Biol Interact 162:172–180

    Article  PubMed  CAS  Google Scholar 

  214. Fulladosa E, Deane E, Ng AHY, Woo NYS, Murat JC, Villaescusa I (2006) Stress proteins induced by exposure to sublethal levels of heavy metals in sea bream (Sparus sarba) blood cells. Toxicol in Vitro 20:96–100

    Article  PubMed  CAS  Google Scholar 

  215. Moraga D, Meistertzheim A, Tanguy-Royer S, Boutet I, Tanguy A, Donval A (2005) Stress response in Cu2+ and Cd2+ exposed oyster (Crassostrea gigas): an immunohistochemical approach. Comp Biochem Physiol Part C 141:151–156

    Google Scholar 

Download references

Acknowledgements

The authors thank Professor Monica Nordberg for her kind encouragement and valuable suggestions.

Author information

Authors and Affiliations

  1. Department of Environment, Faculty of Natural Resources, Islamic Azad University (Lahijan Branch), Lahijan, Iran

    Fatemeh Shariati

  2. Department of Chemistry, Faculty of Sciences, Islamic Azad University (Rasht Branch), Rasht, Iran

    Shahab Shariati

Authors
  1. Fatemeh Shariati
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shahab Shariati
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fatemeh Shariati.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shariati, F., Shariati, S. Review on Methods for Determination of Metallothioneins in Aquatic Organisms. Biol Trace Elem Res 141, 340–366 (2011). https://doi.org/10.1007/s12011-010-8740-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-010-8740-z

Keywords

Search

Navigation