Cover Image

Metallothionein - A potential biomarker to assess the metal contamination in marine fishes

Vijay Hemmadi

Abstract


In this review, the fish Metallothionein (MT) is broadly discussed in relation to their utilization as a biomarker to assess the heavy metal contamination in marine ecosystem. Heavy metals are the main marine pollutants whose bioaccumulation in fishes results in deleterious effects on physiology, biochemistry and behavior. To assess the health status of fishes, an early determination of metal levels along with a biomarker like MT will help us to understand the bioavailability and toxicity of the metals. MTs constitute a family of low-molecular-weight, cysteine-rich proteins functioning in the regulation of essential metals and detoxification of both essential and nonessential metals.  Since 1980, MT has been the useful tool for toxicity assessment of metals before sub lethal and lethal damage to organisms because of quick induction of MTs as metals enter the tissue. Various studies conducted on the induction, regulation and estimation of the MT by the metals showed that many variables such as sexual maturity, age, tissue type, metal type, route of exposure, changes in the environmental conditions of the living habitat of the organisms under study and presence of exogenous and endogenous substances do create fluctuations in the level of MT. Keeping in view of the above factors, this review attempts to understand the effectiveness of this biomarker in assessing the health status of the fishes.

Keywords


Biomarker; Heavy Metal; Marine Environment; Metallothionein; Marine Pollution

Full Text:

PDF

References


Singh R, Gautam N, Mishra A and Gupta R, Heavy metals and living system: An overview. Indian Journal of Pharmacology, 43 (3), 2011, 246-253

Singh J, Upadhayay SK, Pathak RK and Gupta V. Accumulation of Heavy Metal in Soil and Paddy Crop (Oryza sativa), Irrigated with Water of Ramgarh Lake, Gorakhpur, UP, India. Environmental Toxicology and Chemistry, 93, 2011, 462-473. .

Mcintyre T, Phytoremediation of heavy metals from soils. Advances in Biochemical Engineering / Biotechnology, 78, 2003, 97–123.

Ruilian Y, Xing Y, Yuanhui Z, Gongren H and Xianglin T, Heavy metal pollution in intertidal sediments from Quanzhou Bay, China. Journal of Environmental Sciences, 20, 2008, 664–669.

Guanghua L, Xiaofan Y, Zhihua L, Haizhou Z and Chao W. Contamination by metals and pharmaceutical in northern Taihu Lake (China) and its relation to integrated biomarker response. Ecotoxicology, 2012, 1002-1004

Utpal Singha Roy, Chattopadhyay B, Datta S and Mukhopadhyay SK, Metallothionein as a Biomarker to Assess the Effects of Pollution on Indian Major Carp Species from Wastewater-Fed Fishponds of East Calcutta Wetlands (a Ramsar Site). Environmental Research, Engineering and Management, 4 (58), 2011, 10-17.

Bayne BL, Brown DA, Burns K, Dixon DR, Ivanovici A, Livingstone DR, Lowe DM, Moore MN, Stebbing ARD and Widdows J, The effects of stress and pollution on marine animals in Environmental Toxicology and Risk Assessment 4 (New York, USA: Praegez Publshers, 1985).

Bucheli TD and Fent K, Induction of cytochrome P450 as a biomarker for environmental contamination in aquatic ecosystems. Critical Reviews in Environmental Science and Technology, 25 (3), 1995, 201-268.

Beliaeff B and Burgeot T, Integrated Biomarker Response: A useful tool for ecological risk assessment. Environmental Toxicology and Chemistry, 21, 2002, 1316.

Livingstone DR, Biotechnology and pollution monitoring: use of molecular biomarker in the aquatic environment. Journal of Chemical Technology and Biotechnology, 57, 1993, 195–211.

Monserrat JM, Geracitano LA and Bianchini A. Current and future prospective using Biomarker to assess pollution in aquatic ecosystem. Comments on toxicology, 9, 2003, 255-269.

Suter GWH, Ecological Risk Assessment (Boca Raten, FL, USA: Lewis Publishers, 1993).

Beyer J, Fish biomarker in marine pollution monitoring: evaluation and validation in laboratory and field studies, University of Bergen, Norway, 1996.

Cajaraville MP, Bebianno MJ, Blasco J, Porte C, Sarasquete C and Viarengo A, The Use of Biomarker to Assess the Impact of Pollution in the Coastal Environment of the Iberian Peninsula: A Practical Approach, Science of the Total Environment, 247, 2000, 295-311.

Cajaraville MP, Bebianno MJ, Blasco J, Porte C, Sarasquete C and Viarengo A, The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Science of the Total Environment, 247, 2000, 201–212

Viarengo A, Lowe D, Bolognesi C, Fabbri E & Koehler A, The Use of Biomarkers in Biomonitoring: a 2-tier Approach Assessing the Level of Pollutant-induced Stress Syndrome in Sentinel Organisms. Comparative Biochemistry and Physiology, 146 C, 2007, 281–300.

Mason AZ and Jenkins KD, Metal detoxification in aquatic organisms. In: Metal speciation and bioavailability in aquatic systems (London, UK: John Wiley & Sons Ltd, 1995)

Depledge MH and Fossi MC, The Role of Biomarker in the Environmental Assesment. Ecotoxicology, 3, 1994, 161-172.

Margoshes M and Vallee BL, A cadmium protein from equine kidney cortex. Journal of American Chemical Society, 79, 1957, 4813-4814.

Decataldo A, Di Leo A, Giandomenico S and Cardelliccho N. Association of metals (Mercury, Cadmium and Zinc) with metallothionein like proteins in storage organs of standard dolphins from the Mediterranean Sea (Southern Italy). Journal of Environmental Monitoring, 6, 2004, 361-367.

Alhaman J, Romero-Ruiz A, Jebali J and Lopez-Barea J, Total metallothionein quantification by reversed-phase high performance liquid chromatography coupled to fluorescence detection monobromobimane derivation. Environmental Research Journal, 5, 2011, 1-17.

Kaegi JH and Schaffer A, Biochemistry of metallothionein. Biochemistry, 27, 1988, 8509-8515.

Roesijadi G, Metallothioneins in metal regulation and toxicity in aquatic animal. Aquatic Toxicology, 22, 1992, 81-114.

Doki Y and Monden M, Can metallothionein be a useful molecular marker for selecting hepatocellular carcinoma patients for platinum based chemotherapy, Journal of Gastroenterology, 39, 2004, 1228-1229.

Prusa R, Blastik O, Potesil D, Trnkova L, Zehnalek J, Adam V, Petrlova J and Jelen F, Analytic method for determination of metallothionenis as tumor biomarker. Clinical Chemistry 51, 2005, A 56-A 56.

Hogstrand C and Haux C, Binding and detoxification of heavy metals in lower vertebrates with reference to metallothionein. Comparative Biochemistry and Physiology, 100C, 1991, 137-141.

Hylland K, Haux C and Hogstrand C, Hepatic metallothionein and heavy metals in dad limanda limanda from the German Bight. Marine Ecology Progress Series, 91,1992, 89-96.

Viarengo A, Ponzano E, Dondero F and Fabbri R, A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic molluscs. Marine Environmental Research, 44, 1997, 69–84

Pavicic J, Skreblin M, Raspor B and Branica M. Metal pollution assessment of marine environment by determination of metal –binding proteins in Mytillus sp. Marine Chemistry, 22, 1987, 235-248.

Paek SM, Soohee C and In-Sook L, Level of heavy metals in the Onsan Bay in Korea and involvement of metals binding proteins in the accumulation of Cadmium in Littorina brevicula. The Korean Journal of Ecology, 22, 1999, 95-100.

UNEP/RAMOGE, Manual on the Biomarkers Recommended for MED POL Biomonitoring Programme, UNEP, Athens, 1999, 92.

George SG, Hodgson PA, Tytler P and Todd K, Inducability of Metallothionein mRNA expression and Cadmium tolerance in larva of teleosts the turbot (Scophthalmus maximus). Fundamental Application of Toxicology, 33, 1996, 91-99.

Smet HD, Wachter BD, Lobinski R and Blust R, Dynamics of (Cd, Zn)- metallothioneins in gills, liver and kidney of common carp (Cyprinus carpio) during cadmium exposure. Aquatic Toxicology, 52, 2001, 269–281.

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

Rovira MS, Fernández-Díaz C, Canavate JP and Blasco J, Effects on metallothionein levels and other stress defenses in Senegal sole larvae exposed to cadmium. Bulletin of Environmental Contamination and Toxicology, 74, 2005, 597–603.

Chen WY, John JAC, Lin CH and Chang CY, Expression pattern of metallothionein, MTF-1 nuclear translocation, and its DNA-binding activity in zebrafish (Danio rerio) induced by zinc and cadmium. Environmental Toxicology and Chemistry, 26, 2007, 110–117.

Lange A, Ausseil O and Segner H, Alterations of tissue glutathione levels and metallothionein mRNA in rainbow trout during single and combined exposure to cadmium and zinc. Comparative Biochemistry and Physiology, 131, 2002, 231–243.

Wu SM, Weng CF, Yu MJ, Lin CC, Chen ST, Hwang JC and Hwang PP, Cadmium-inducible metallothionein in tilapia (Oreochromis mossambicus). Bulletin of Environmental Contamination and Toxicology, 62, 1999, 758–768.

Carginale V, Scudiero R, Capasso C, Capasso A, Kille A, Di Prisco G and Parisi E. Cadmium-induced differential accumulation of metallothionein isoforms in the Antarctic icefish, which exhibits no basal metallothionein protein but high endogenous mRNA levels. Biochemical Journal 332, 1998, 475–481.

Riggioa M, Filosaa S, Parisib E and Scudieroa R, Changes in zinc, copper and metallothionein contents during oocyte growth and early development of the teleost Danio rerio (zebrafish). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 135 (2), 2003, 191–196

Thiele DJ, Metal Regulated Transscription in Eukaryotes. Nucleic Acid Research, 210, 1992, 1183-1188.

Kling P and Olsson PE, Metal regulation of the rainbow trout metallothionein-A gene. In: proceedings of the Seventh International Symposium on Responses of Marine Organisms to Pollutants. 1993

Olsson PE, Kling P, Erkell LJ and Kille P, Structural and functional analysis of the rainbow trout (Oncorhynchus mykiss) metallothionein-A gene. European Journal of Biochemistry, 230, 1995, 344–349.

Olsson PE, Metallothionein in fish: induction and use in environmental monitoring, In: Toxicological aquatic pollution: physiological, molecular and cellular approaches (Cambridge, UK: Cambridge University Press, 1996).

Hylland K, Nissen-Lie T, Christensen PG and Sandvik M, Natural Modulation of hepatic Metallothionein andcytochrome P4501A in flounder, Platichthys flesus. Marine Environmental Research, 46, 1998, 1-5.

Cinier CD, Petit-Ramel M, Faure R and Bortolato M, Cadmium accumulation and metallothionein biosynthesis in Cyprinus carpio tissues. Bulletin of Environmental Contamination and Toxicology, 61, 1998, 793–799

Linde AR, Sanchez-Galan S, Klein D, Garcia-Vazquez E and Summer KH, Metallothionein and heavy metals in Brown trout (salmo trutta) and European eel (Anguilla anguilla): a comparative study. Ecotoxicology Environmental Safety, 44, 1999, 168-173.

Langston WJ, Chesman BS, Burt GR, Pope ND and McEvoy J, Metallothionein in liver of eels (Anguilla Anguilla) from the Thames Estuary: an indicator of environmental quality. Marine Environmental Research, 53, 2002, 263–293.

Kathleen A, Van Cleef Toedt, Lisa AE, Kaplan E and Crivello JF, Killifish metallothionein messenger RNA expression following temperature perturbation and cadmium exposure. Cell Stress Chaperones, 6 (4), 2001, 351–359.

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

Sole M, Potrykus C, Fernandez-Diaz and Blasco J, Variations on the stress defense and metallothionein levels in the Senegal sole, Solea senegalensis, during early larval stages. Fish Physiology and Biochemistry, 30, 2004, 57-66.

Olsson PE and Haux C, Rainbow trout metallothioneins. Inorganica Chimica Acta, 107, 1985, 67-71

Dang ZC, Berntssen HMG, Lundebye KA, Flik G, Bonga SEW and Lock RAC, Metallothionein and Cortisol Receptor Expression in Gills of Atlantic Salmon, Salmo Salar Exposed to Dietery Cadmium. Aquatic Toxicology, 53, 2001, 91-101.

Langstone WJ, Chesman BS, Burt GR, Pope MD and Mc Evoy J, Metallothionein in Liver of Eels Anguilla Anguilla from the Thames Estuary: An Indicator of Environmental Quality. Marine Environmental Research, 53, 2002, 263-293.

Pathiratne A, Chandrasekera LWHU and Pathiratne KAS, Use of Biomarkers in Nile Tilapia (Oreochromis nilticus) to Assess the Impact of Pollution in Bolgoda Lake, An Urban Waterbody in Sri Lanka. Environmental Monitoring and Assessment, 15, 2009, 361-374.

Pedersen SN, Lundebye AK and Depledge MH, Filed application of metallothionein and stress protein biomarker vin the shore crab (Carcinus maenas) exposed to trace metal. Aquatic Toxicology, 37, 1997, 183-200.

Richard P. Cosson, Heavy metal intracellular balance and relationship with metallothionein induction in the liver of carp after contamination by silver, cadmium and mercury following or not pretreatment by zinc. Biometals, 7 (1), 1994, 9-19.

Zafarullah M, Olsson PE and Gedamu L, Endogenous and heavy metal ion induced metallothionein gene expression in salmonid tissues and cell lines. Gene 83 (1), 1989, 85–93.

Li Zhang and Wen-Xiong Wang, Effects of Zn pre-exposure on Cd and Zn bioaccumulation and metallothionein levels in two species of marine fish. Aquatic Toxicology, 73 (4), 2005, 353–369.

Costa M, Zhuang Z, Huang X, Cosentino S, Klein CB, and Salnikow K, Molecular mechanisms of nickel carcinogenesis. Science of the Total Environment, 148, 1994, 191–199.

Chatterjee A and Maiti BI, Induction and turnover of catfish (Heteropneustes fossilis) metallothionein. Molecular and Cellular Biochemistry, 108 (1), 1991, 29-38.

Chowdhury M, Baldisserotto B and Wood CM, Tissue-Specific Cadmium and Metallothionein Levels in Rainbow Trout Chronically Acclimated to Waterborne or Dietary Cadmium. Archives of Environmental Contamination and Toxicology 48 (3), 2005, 381-390.

Cosson RP, Heavy metal intracellular balance and relation with metallothionein induction in the gills of crap after contamination by Ag, Cd and Hg followed by pretreatment with Zn or not. Biological Trace Elemement Research, 46, 1994, 229-245.

Kagi JHR, Evolution, structure and chemical activity of class I metallothioneins: an overview (Basel, Switzerland: Birkhäuser Verlag, 1993)

Shears MA and Fletcher GL, Hepatic metallothionein in the winter flounder (Pseudopleuronectes americanus), Canadian Journal of Zoology, 1985, 1602-1606.

Olsson PE, Åke Larsson and Haux C, Influence of seasonal changes in water temperature on cadmium inducibility of hepatic and renal metallothionein in rainbow trout. Marine Environmental Research, 42 (1-4), 1996, 41–44.

Rotchell JM, Clarke KR, Newton LC and Bird DJ, Hepatic MT’s as a Biomarker for metal contamination: age effect and seasonal variation in European flounder (Pleuronectes flesus) from the Severn Estuary and Bristol Channel. Marine Environmental Research, 52, 2001, 151-171.

Gerpe M, Kling P, Berg AH and Olsson PE, Arctic char (Salvelinus alpinus) metallothionein: cDNA sequence, expression and tissue-specific inhibition of cadmium mediated metallothionein induction by 17β-estradiol, 4-OH-PCB 30 and PCB 104. Environmental Toxicology and Chemistry, 19, 2000, 638–645.

Hyllner SJ, Andersson T, Haux C and Olsson PE, Cortisol induction of metallothionein in primary culture of rainbow trout hepatocytes. Journal of Cellular Physiology 139 (1), 2005, 24–28.

Su-Mei Wu, Yi-Ying Chou and Am-Ni Deng, Effects of Exogenous Cortisol and Progesterone on Metallothionein Expression and Tolerance to Waterborne Cadmium in Tilapia (Oreochromis mossambicus). Zoological Studies 41 (1), 2002, 111-118.

Huggett RJ, Biomarkers: Biochemical, Physilogical and Histological marker of Anthropogenic Stress (Chelsea, MI: Lewis Publishers, 1992).

Dobrio M, Adela R, Rodrigues, Gey Bordin, Maria J, Bebeanno, Mare. A. Ley, Ivan Sestakova, Milan Vossat and Monica Nordberg, Recent Development in Quantification method of MTs. Journal of Inorganic Biochemistry 88, 2002, 23-134.

Lobinski R, Chassaigne H and Szpunar J, Analysis for metallothioneins using coupled techniques. Talanta 46 (2), 1998, 271-89.

Alhama J, Romero-Ruiz A and Lopez–Barea J, Metallothionein quantification in clam by reversed- phase high–performance liquid chromatography coupled to fluorescence detection after monobromobimane derivatization. Journal of chromatography A 1107, 2002, 52-58.

Jebali J, Banni M, Gerbej H, Boussetta H, Lopez-Barea J and Alhama J, Metallothionein induction by Cu, Cd and Hg in Dicentrarchus labrax liver: Assessment by RP-HPLC with florescence detection and spectrophotometry. Marine Envrionmental Research 65, 2008, 358-363.

Romerio-Ruiz A, Alhama J, Blasco J, Luis Gomez-Ariza J and Lopez-Barea J, New Metallothionein assay in Scrobicularia plana: Heating effect and correlation with other biomarkers. Environmental Pollution 156, 2008, 1340-1347.

Apostolova M, Bontchev PR, Nachev C and Sirakova I, Apometallothionein in rat liver. Journal of Chromatography 620 (2), 1993, 191-197.

McCormick CC and Lin LY, Quantification and identification of metallothioneins by gel electrophoresis and silver staining. Methods in Enzymology, 205, 1991, 71.

Conklin DR, Cowan KS and Aschner M, Detection of metallothionein (MT) proteins with radiolabeled [c-14] iodoacetamide. Toxicology methods 6 (3), 1996, 149-155.

Orihuela R, Domenech J, Bofill R, You C, Mackay EA, Kagi JHR, Capdevila M and Atrian S, The metal-binding features of the recombinant mussel (Mytilus edulis) MT-10-IV metallothionein. Journal of Biological Inorganic Chemistry 13, 2008, 801-812.

Adam V, Krizkova S, Zitka O, Trnkova L, Petrlova J, Beklova M and Kizek R, A determination of apo-metallothionein using adsorptive transfer stripping technique in connection with differential pulse voltammetry. Electroanalysis (NY) 19, 2007, 339-347.

Sestakova I and Navratil T, Voltammetric methods in metallothionein research. Bioinorganic Chemistry and Applications 3, 2005, 43-53.

Krizkova S, Fabrik I, Adam V, Kukacka J, Prusa R, Chavis GJ, Trnkova L, Strnadel J, Horak V and Kizek R, Comparison of metallothionein detection by using Brdicka reaction and enzyme-Linked immunosorbent assay employing chicken yolk antibodies. Journal of Sensors 8, 2009, 3106.

Butcher H, Kennette W, Collins O, Demoor J and Koropatnick J, A sensitive time-resolved fluorescent immunoassay for metallothionein protein. Journal of Immunological Methods 272, 2003, 247-256.

Dabrio M, Adela R, Rodriguez, Bordin G, Bebeanno MJ, Ley MA, Sestakova I, Vosak M and Nordberg M, Recent development in quantification method of MTs. Journal of Inorganic Biochemistry 88, 2002, 123-134.

Chan HM, Pringle GA and Cherian MG, Heterogeneity of antibodies to metallothionein isomers and development of a simple enzyme-linked immunosorbent assay. Journal of Biochemical and Molecular Toxicology 7 (4), 1992, 219-227.

Benavente F, Andon B, Gimenez E, Barbosa J and Sanz-Nebot V, Modeling the migration behavior of rabbit liver apothioneins in capillary electrophoresis. Electrophoresis 29 (13), 2008, 2790.

Rosenberg E, The potential of organic (electrospray and atmospheric pressure chemical ionisation) mass spectrometric techniques coupled to liquid-phase separation for speciation analysis. Journal of Chromatography A 1000, 2003, 841-889.

Kaltashov IA, Zhang MX, Eyles SJ and Abzalimov RR, Investigation of structure, dynamics and function of metalloproteins with electrospray ionization mass spectrometry. Analytical and Bioanalytical Chemistry, 386 (3), 2006, 472-481.

Orihuela R, Domenech J, Bofill R, You C, Mackay EA, Kagi JHR, Capdevila M and Atrian S, The metal-binding features of the recombinant mussel Mytilus edulis MT-10-IV metallothionein. Journal of Biological Inorganic Chemistry 13, 2008, 801-812.

Karotki AD and Vasak M, Reaction of human metallothionein-3 with cisplatin and transplatin. Journal of Biological Inorganic Chemistry 14, 2009, 1129-38.

Szpunar J, Advances in analytical methodology for bioinorganic speciation analysis: metallomics, metalloproteomics and heteroatom-tagged proteomics and metabolomics. Analyst 130, 2005, 442-465.

Klaverkamp JF, Wautier K and Baron CL, A modified mercury saturation assay for measuring metallothionein. Aquatic Toxicology 50, 2000, 13-25.

Huang ZY, Shen JC, Zhuang ZX, Wang XR and Lee FSC, Metallothionein as a biomarker for mercury in tissues of rat fed orally with cinnabar. Applied Organometallic Chemistry 18, 2004, 255-261.

Bienengraber M, Forderkunz S, Klein D and Summer KH, Determination of Cu-Containing Metallothionein: Comparison of Ag Saturation Assay, Thiomolybdate Assay and Enzyme-Linked Immunosorbent Assay. Analytical Biochemistry 228, 1995, 69-73.

Olsson PE, Kling P, Erkell LJ and Kille P, Structural and functional analysis of the rainbow trout (Oncorhynchus mykiss) metallothionein-A gene. European Journal of Biochemistry 230, 1995, 344–349.

Rotchell JM, Clarke KR, Newton LC and Bird DJ, Hepatic MT’s as a Biomarker for metal contamination: age effect and seasonal variation in European F European flounder (Pleuronectes flesus) from the Severn Estuary and Bristol Channel. Marine Environmental Research 52, 2001, 151-171.

Hollis L, Hogstrand C and Wood CM, Tissue specific Cadmium accumulation, MT induction and tissue Zn and Cu levels during chronic sub lethal Cadmium exposure in juvenile Rainbow Trout. Archives of Environmental Contamination and Toxicology 41, 2001, 468-474.

Ueng YF, Lai CF, Merg LM, Hug YY and Uerg TH, Effect of Cadmium and Environmental pollution on MTs and Cytochrome P450 in Tilapia. Bulletin of Environmental Contamination and Toxicology 57, 1996, 125-131.

Olsvik PA, Gundersen P, Andersen RA and Zachariassen KE, Metal accumulation and metallothionein in two populations of brown trout, Salmo trutta, exposed to different natural water environments during a runoff episode. Aquatic Toxicology 50, 2000, 301-316.

Burkhardt-Holm P, Bernet D and Hogstrand C, Increase of metallothionein-immunopositive chloride cells in the gills of brown trout and rainbow trout after exposure to sewage treatment plant effluent. Histochemical Journal 31, 1999, 339-346.




DOI: http://dx.doi.org/10.21746/ijbio.2016.04.003

Refbacks

  • There are currently no refbacks.




Copyright (c) 2016 International Journal of Bioassays

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

International Journal of Bioassays is a member of the Publishers International Linking Association, Inc. (PILA), CROSSREF and CROSSMARK (USA). Digital Object Identifier (DOI) will be assigned to all its published content.