Can thiol compounds be used as biomarkers of aquatic ecosystem contamination by cadmium?

Open access

Can thiol compounds be used as biomarkers of aquatic ecosystem contamination by cadmium?

Due to anthropogenic activities, heavy metals still represent a threat for various trophic levels. If aquatic animals are exposed to heavy metals we can obviously observe considerable toxicity. It is well known that an organism affected by cadmium (Cd) synthesize low molecular mass thiol compounds rich in cysteine (Cys), such as metallothioneins (MT) and glutathione (GSH/GSSG). The aim of this study was to summarize the effect of Cd on level of thiol compounds in aquatic organisms, and evaluate that the concentrations of thiol compounds are effective indicators of Cd water pollution and explain their potential use in biomonitoring applications.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • Alvarado NE Buxens A Mazón LI Marigómez I Soto M. (2005). Cellular biomarkers of exposure and biological effect in hepatocytes of turbot (Scophthalmus maximus) exposed to Cd Cu and Zn and after depuration. Aquat Toxicol 74: 110-125.

  • Alvarado NE Quesada I Hylland K Marigomez I Soto M. (2006). Quantitative changes in metallothionein expression in target cell-types in the gills in turbot (Scophthalamus maximus) exposed to Cd Cu Zn and after a depuration treatment. Aquat Toxicol 77: 64-77.

  • 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.

  • Bae H Nam SS Park H-S Park K. (2005). Metallothionein mRNA sequencing and induction by cadmium in gills of the crucian carp (Carassius auratus). J Health Sci 51: 284-290.

  • Baer KN and Thomas P. (1990). Influence of capture stress salinity and reproductive status on zinc associated with metallothionein-like proteins in livers of three marine teleost species. Mar Environ Res 29: 277-287.

  • Belcastro M Marino T Russo N Toscano M. (2009). The role of glutathione in cadmium ion detoxification: Coordination modes and binding properties - A density functional study. J Inorg Biochem 103: 50-57.

  • Berntssen MHG Aspholm OO Hylland K Bonga SEW Lundebye AK. (2001). Tissue metallothionein apoptosis and cell proliferation responses in Atlantic salmon (Salmo salar L.) parr fed elevated dietary cadmium. Comp Bioch Phys 128: 299-310.

  • Bervoets L Blust R. (2003). Metal concentrations in water sediment and gudgeon (Gobio gobio) from a pollution gradient: relationship with fish condition factor. Environ Pollut 126: 9-19.

  • Blahova J Kruzikova K Hilscherova K Grabic R Halirova J Jurcikova J Ocelka T Svobodova Z. (2008). Biliary 1-hydroxypyrene as a biomarker of exposure to polycyclic aromatic hydrocarbons in fish. Neuroendocrinol Lett 29: 663-668.

  • Bonwick GA Fielden PR Davies DH. (1991). Hepatic metallothionein levels in roach (Rutilus rutilus L.) continuously exposed to water-borne cadmium. Comp Biochem Physiol 99C: 119-125.

  • 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.

  • Brouwer M Schlenk D Ringwood AH Brouwer-Hoexum TM. (1992). Metal-specific induction of metallothionein isoforms in the blue crab Callinectes sapidus in response to single- and mixed-metal exposure Arch Biochem Biophys 294: 461.

  • Cajaraville MP Abascal I Etxeberria M Marigómez I. (1995). Lysosomes as cellular markers of environmental pollution: time and dose-dependent responses of the digestive lysosomal system of mussels after petroleum hydrocarbon exposure. Environ Toxicol Water Qual 10: 1-8.

  • Chatterjee S Bhattacharya S. (1984). Detoxification of industrial pollutants by the glutathione and glutathione-S-transferase system in the liver of Anabas testudineus (Bloch). Toxicol Lett 22: 187-193.

  • Correia AD Lima G Costa MH Livingstone DR. (2002). Studies on biomarkers of copper exposure and toxicity in the marine amphipod Gammarus locusta (crustacean). Biomarkers 7: 422-437.

  • Coyle P Philcox JC Carey LC Rofe AM. (2002). Metallothionein: the multipurpose protein. Cell Mol Life Sci 59: 627-647.

  • Dallinger R. (1995). Mechanisms of metal incorporation into cells. In: Cajaraville MP (Ed.) Cell Biology in Environmental toxicology. University of Basque Country Press Service Bilbao p.133-154.

  • Dallinger R Egg M Köck G Hofer R. (1996). The role of metallothionein in cadmium accumulation of Arctic char (Salvelinus alpinus) from high alpine lakes. Aquat Toxicol 38: 47-66.

  • De Boeck G 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.

  • 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.

  • Depledge MH. (1993). The rational basis for the use of biomarkers as ecotoxicological tools. In: Fossi MC Leonzio C. (Eds.) Non-destructive biomarkers in vertebrates. Lewis Publishers Boca Raton pp.261-285.

  • Eaton DL Stacey NH Wong KL Klaassen CD. (1980). Dose-response effects of various metal ions on rat liver metallothionein glutathione heme oxygenase and cytochrome P-450. Toxicol Appl Pharmacol 55: 393-402.

  • Ferreira M Caetano M Costa J Pousao-Ferreira P Vale C Reis-Henriques MA. (2008). Metal accumulation and oxidative stress responses in cultured and wild white seabream from Northwest Atlantic. Sci Total Environ 407: 638-646.

  • Foulkes EC. (1993). Metallothionein and glutathione as determinants of cellular retention and extrusion of cadmium and mercury. Life Sci 52: 1611-1620.

  • Fowler BA Hildebrand CE Kojima Y Webb M. (1987). Nomenclature of metallothionein. In: Kagi JHR Kojima Y. Metallothionein II. Birkhauser - Verlag Basel pp.19-22.

  • Friberg L Kjellström T Nordberg GF. (1986). Cadmium. In: Friberg L Nordberg GF Vouk VB (Eds.). Handbook on the toxicology of metals vol II. Specific metals. Elsevier Amsterdam p 130-184.

  • Glynn AW Olsson P-E. (1991). Cadmium turnover in minnows (Phoxinus phoxinus) pre-exposed to waterborne cadmium. Environ Toxicol Chem 10: 383-394.

  • Gravato C Teles M Oliveira M Santos MA. (2006). Oxidative stress liver bio-transformation and genotoxic effect induced by copper in Anguilla anguilla L. - the influence of pre-exposure of [beta]-naphtoflavone. Chemosphere 65: 1821-30.

  • Haines TA. (1981). Acid precipitation and its consequences for aquatic ecosystems. A review. Transact Am Fish Soc 110: 669-705.

  • Hamer DH. (1986). Metallothionein. Annu Rev Biochem 55: 913-951.

  • Hamilton SJ Mehrle PM Jones JR. (1987). Evaluation of metallothionein measurement as a biological indicator of stress from cadmium to brook trout. Trans Am Fish Soc 116: 551-560.

  • Handy RD and Eddy FB. (1990). The interaction between the surface of rainbow trout Oncorhynchus mykiss and water-borne metal toxicants. Funct Ecol 4: 385-392.

  • Havelkova M Blahova J Kroupova H Randak T Slatinska I Leontovycova D Grabic R Pospisil R Svobodova Z. (2008). Biomarkers of contaminant exposure in Chub (Leuciscus cephalus L.) - Biomonitoring of major rivers in the Czech Republic. Sensors 8: 2589-2603.

  • Hollis LM McGeer JC McDonald DG Wood CM. (1999). Cadmium accumulation gill Cd binding acclimation and physiological effects during long term sublethal Cd exposure in rainbow trout. Aquat Toxicol 46: 101-119.

  • Huang PC. (1993). Metallothionein structure/function interface. In: Metallothionein III: Biological Roles and Medical Implications (Sizuki KT Imura N Kimura M Eds.) Birkhauser Verlag Basel p. 407-426.

  • Huang Z-Y Zhang Q Chen J Zhuang Z-X Wang X-R. (2007). Bioaccumulation of metals and induction of metallothioneins in selected tissues of common carp (Cyprinus carpio L.) co-exposed to cadmium mercury and lead. Appl Organometal Chem 21:101-107.

  • Hylland K haux C Hogstrand C. (1992). Immunological characterization of metallothionein in marine and freshwater fish. Res Mar Org Poll Pri 39: 111-115.

  • Jezierska B Witeska M. (2001). Metal toxicity to fish. University of Podlasie Siedlce. pp 318.

  • Kägi JHR Schäffer A. (1988). Biochemistry of metallothionein. Biochemistry 27: 8509-8515.

  • Kang YJ Clapper JA Enger MD. (1989). Enhanced cadmium cytotoxicity in A549 cells with reduced glutathione levels is due to neither enhanced cadmium accumulation nor reduced metallothionein synthesis. Cell. Biol Toxicol 5: 249-260.

  • Kito H Tazawa T Ose Y Sato T Ishikawa T. (1982a). Formation of metallothionein in fish. Comp Biochem Physiol 73: 129-134.

  • Kito H Tazawa T Ose Y Sato T Ishikawa T. (1982b). Protection of metallothionein against cadmium toxicity. Comp Biochem Physiol C-Pharmacol Toxicol Endocrinol 73: 135-139.

  • Klassen CD Liu J Choundry S. (1999). Metallothionein: an intracellular protein to protect against cadmium toxicity. Annu Rev Pharmaco Toxicol 39: 267-294.

  • Klaverkamp JF Duncan DA. (1987). Acclimation to cadmium toxicity by white suckers: cadmium binding capacity and metal distribution in gill and liver cytosol. Environ Toxicol Chem 6: 275-289.

  • Köck G Triendl M Hofer R. (1996). Seasonal patterns of metal accumulation in Arctic char (Salvelinus alpinus) from an oligotrophic Alpine lake related to temperature. Can J Fish Aquat Sci 53: 780-786.

  • Köhler A Deisemanmn H Lauritzen B. (1992). Histological and cytochemical indices of toxic injury in the liver of dab (Limanda limanda). Mar Ecol Prog Ser 91: 141-153.

  • Kovarova J Kizek R Adam V Harustiakova D Celechovska O Svobodova Z. (2009). Effect of cadmium chloride on metallothionein levels in carp. Sensors 9: 4789-4803.

  • Kuroshima R. (1992). Comparison of cadmium accumulation in tissues between carp (Cyprinus carpio) and red bream (Pagrus major). Nippon Suisan Gakk 58: 1237-1242.

  • Kuroshima R. (1995). Hepatic metallothionein and glutathione levels in red sea bram. Comp Biochem Physiol 110C: 95-100.

  • Lange A Ausseil O Segner H. (2002). Alterations of tissue glutathione levels and metallothionein mRNA in rainbow trout during single and combined exposure to cadmium and zinc. Comp Bioch Physiol 131: 231-243.

  • Lecoeur S Videman B Berny P. (2004). Evaluation of metallothionein as a biomarker of single and combined Cd/Cu exposure in Dresseina polymorpha. Environ Res 94: 184-191.

  • Lowe DM Moore MN Clarke KR. (1981). Effects of oil on digestive cells in mussels: quantitative alterations in cellular and lysosomal structure. Aquat Toxicol 1: 213-226.

  • Maracine M Segner H. (1998). Cytotoxicity of metals in isolated fish cells: Importance of the cellular glutathione status. Compar Biochem Physiol 120A: 83-88.

  • Marigomez I Soto M Carajaville MP Angulo E Giamberini L. (2002). Cellular and subcellular distribution of metals in molluscs. Microsc Res Technol 56: 358-392.

  • Martín -Díaz ML Blasco J Sales D Delvalls TA. (2007). Biomarkers study for sediment quality assessment in spanish ports using the crab Carcinus maenas and the clam Ruditapes phillippinarum. Environ Contam Toxicol 53: 66-76.

  • Mason AZ and Jenkins KD. (1995). Metal detoxification in aquatic organisms. In: Tessier A Turner DR. (Eds.) Metal Speciation and Bioavailability in Aquatic Ecosystems. Wiley New York NY. p. 478-608.

  • Mathiessen P. (2000). Biological effects quality assurance in monitoring programs (BELQUALM). Centre for Environment Fisheries and Aquaculture Science (CEFAS) Remenbrance Avenue Burham-on-Crouch Essex CMO 8HA UK 24p.

  • McCarthy JF Shugard LR. (1990). Biological markers of environmental contamination. In: McCarthy JF Stuart LR (Eds.). Biomarkers of Environmental Contamination. Lewis Publishers Boca Raton Florida p. 3-14.

  • McDonald DG Wood CM. (1993). Branchial mechanisms of acclimation to metals in freshwater fish. In: Rankin JC Jensen JB (Eds.) Fish Ecophysiology Chapmann & Hall London. p. 297-315.

  • McGeer JC Szebedinszky C McDonald DG Wood CM. (2000). Effects of chronic sublethal exposure to waterborne Cu Cd or Zn in rainbow trout 2: tissue specific metal accumulation. Aquat Toxicol 50: 245-256.

  • McGeer JC Nadella S Alsop DH Hollis L Taylor LN McDonald DG Wood CM. (2007). Influence of acclimation and cross-acclimation of metals on acute Cd toxicity and Cd uptake and distribution in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol. 84: 190-197.

  • Meister A and Anderson ME. (1983). Glutathione. Annu Rev Biochem 52: 711-760.

  • Meister A. (1985). The fall and rise of cellular glutathione levels: Enzyme based approaches. Curr Top Cell Regul 26: 383-394.

  • Norey CG Brown MW Cryer A Kay J. (1990). A comparison of accumulation tissue distribution and secretion of cadmium in the different species of freshwater fish. Comp Biochem Physiol 97C: 215-220.

  • Olsson PE Larsson A Maage A. (1989). Induction of metallothionein synthesis in rainbow trout (Salmo gairdneri) during long-term exposure to waterborne cadmium. Fish Physiol Biochem 6: 221-229.

  • Olsson PE Kling P Hogstrand C. (1998). Mechanisms of heavy metal accumulation of toxicity in fish. In: Langston WJ Bebianno MJ (Eds.). Metal Metabolism in Aquatic Environments Chapman and Hall London UK p. 321-350.

  • Olsvik PA Gundersen P Andersen RA Zachariassen KE. (2000). Metal accumulation and metallothionein in two populations of brown trout (Salmo trutta) exposed to different natural water environments during a run-off episode. Aquat Toxicol 50: 301-316.

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

  • Randak T Zlabek V Pulkrabova J Kolarova J Kroupova H Siroka Z Velisek J Svobodova Z Hajslova J. (2009). Effect of pollution on chub in the River Elbe Czech Republic. Ecotoxicol Environ Saf 72: 737-746.

  • Redeker ES van Campenhout K Bervoets L Reijinders H Blust R. (2006). Subcellular distribution of Cd in aquatic oligochaete Tubifex tubifex implication for trophic availability and toxicity. Environ Pollut 148: 166-175.

  • Reed DJ. (1990). Glutathione: Toxicological implications. Annu Rev Toxicol Pharmacol 30: 603-631.

  • Roesjadi G. (1992). Metallothionein in metal regulation and toxicity in aquatic animals. Aquat Toxicol 22: 81-114.

  • Roesijadi G. (1996). Metallothionein and its role in toxic metal regulation. Comp Biochem Physiol 113C: 117-123.

  • Rose WL Nisbet RM Green PG Norris S Fan T Smith EH Cherr GN 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.

  • Santovito G Irato P Piccinni E Albergoni V. (2000). Relationship between metallothionein and metal contants in red-blooded and white-blooded Antarctic teleost. Polar Biol 23: 383-391.

  • Sarkar A Ray D Shrivastava AN Sarker S. (2006). Molecular biomarkers: their significance and application in marine pollution monitoring. Ecotox 15: 333-340.

  • Schlenk D and Rice CD. (1998). Effect of zinc and cadmium treatment on hydrogen-peroxide induced mortality and expression of glutathione and metallothionein in a teleost hepatoma cell line. Aquat Toxicol 43: 121-129.

  • Singhal RK Anderson ME Meister A. (1987). Glutathione a first line defence against cadmium toxicity. FASEB 1: 220-223.

  • Smirnov LP Sukhovskaya IV Nemova NN. (2004). Effects of environmental factors on low-molecular-weight peptides of fishes: A Review Russ J Ecol 36: 41-47.

  • Spry Dj Wiener JG. (1991). Metal bioavailability and toxicity to fish in low-alkalinity lakes: a critical review. Environ Pollut 71: 243-304.

  • Stacey NH Klaassen CD. (1981). Comparison of the effects of metals on cellular injury and lipid peroxidation in isolated rat hepatocytes. J Toxicol Environ Health 7: 139-147.

  • Stephensen E Sturve J Forlin L. (2002). Effects of redox cycling compounds on glutathione content and activity of glutathione-related enzymes in rainbow trout liver. Comp Biochem Physiol 133: 435-442.

  • Sugiyama M. (1994). Role of cellular antioxidants in metal-induced damage. Cell Biol Toxicol 10: 1-22.

  • Suzuki KT Imura N Kimura M. (1993). Metallothionein III. Birkhäuser Basel p.479.

  • Szebedinszky C McGeer JC McDonald DM Wood CM. (2001). Effect of chronic cadmium exposure via the diet or water on internal organ-specific distribution and subsequent gill Cd uptake kinetics in juvenile rainbow trout (Oncorhyncus mykiss). Environ Toxicol Chem 20: 597-607.

  • Thomas P Wofford HW Neff JM. (1982). Effect of cadmium on glutathione content of mullet (Mugil cephalus) tissue. In: Vernberg WB Calabrese A Thurberg FB Vernberg FJ (Eds.). Physiological mechanisms of Marine Pollutant Toxicity. Academic Press NY. p. 109-125.

  • Thomas P Wofford HW. (1993). Effect of cadmium and arochlor 1254 on lipid peroxidation glutathione peroxidase activity and selected antioxidants in atlantic croaker tissues. Aquat Toxicol 27: 159-178.

  • Tom M and Auslander M. (2005). Transcript and protein environmental biomarkers in fish - a review. Chemosphere 59:155-162.

  • Tort L Kargacin B Torres P Giralt M Hidalgo J. (1996). The effect of cadmium exposure and stress on plasma cortisol metallothionein levels and oxidative status in rainbow trout (Oncorhynchus mykiss) liver. Comp Bioch Physiol 114C: 29-34.

  • Vasak M. (1991). Metal removal and substitution in vertebrate and invertebrate metallothioneins. In: Riodan JF Vallee BL (Eds.) Methods in enzymology metallochemistry 205: 452-457.

  • Wiclung A Runn P. (1988). Calcium effects on cadmium uptake redistribution and elimination in minnows (Phoxinus phoxinus) acclimated to different calcium concentrations. Aquat Toxicol 13: 109-122.

  • Winston DW Di Giulio RT. (1991). Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat Toxicol 19: 137-161.

  • Wögrath S Psenner R. (1995). Seasonal annual and long-term variability in the water chemistry of a remote high alpine lake: acid rain versus natural changes. Wat Air Soil Pollut 85: 359-364.

  • Won E-J Raissudin S Shin K-H. (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.

  • Woo S Yum S Jung JH Shim WJ Lee Ch-H Lee T-K. (2006). Heavy metal-induced differential gene expression of metalothionein in Javanese medaka Oryzias javanicus. Mar Biotech 8: 654-662.

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

  • Zorita I Apraiz I Ortiz-Zarragoitia M Orbea A Cancio I Soto M Marigómez I Cajaraville MP. (2007). Assessment of biological effects of environmental pollution along the NW Mediterranean sea using mussels as sentinel organisms. Environ Pollut 148: 236-250.

Search
Journal information
Impact Factor


CiteScore 2018: 1.78

SCImago Journal Rank (SJR) 2018: 0.274
Source Normalized Impact per Paper (SNIP) 2018: 0.671

Cited By
Metrics
All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 299 112 3
PDF Downloads 69 33 4