Environmental Monitoring and Assessment

, Volume 184, Issue 4, pp 2177–2192 | Cite as

Use of metallothioneins as biomarkers for environmental quality assessment in the Gulf of Gabès (Tunisia)

  • Rim Ladhar-Chaabouni
  • Monia Machreki-Ajmi
  • Amel Hamza-Chaffai


Detection and assessment of the impact of pollution on biological resources imply increasing research on early-warning markers such as metallothioneins (MTs) in metal exposure. In this paper, we have collated published information on the use of metallothioneins and metallothionein-like proteins (MTLPs) as biomarkers for environmental quality assessment in the Gulf of Gabès. In this area, some species of fish and bivalve were used as bioindicators of pollution. In these species, an induction of MTs/MTLPs by the essential metals such as Cu and Zn and the non-essential metals such as Cd was observed by different authors who suggest the potential use of these proteins as biomarkers. However, MT concentrations can be influenced by many biotic (sex, maturity stages, and tissues) and abiotic factors (temperature, salinity, and pH). This is essentially the case in field studies where many parameters can randomly affect MT levels, so the endogeneous regulation of MTs must be considered before using MTs as an indicator of heavy metal exposure. Moreover, the use of biomarker cannot be examined independently of the evaluation of techniques that enable its quantification. Therefore, the approach to the use of MTs/MTLP as biomarkers of exposure for an assessment of the physiological status of aquatic organisms is discussed in this paper.


Biomarker Biomonitoring Gulf of Gabès Metallothionein Review 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Amiard, J. C., Amiard-Triquet, C., Barka, S., Pellerin, J., & Rainbow, P. S. (2006). Metallothioneins in aquatic invertebrates: Their role in metal detoxication and their use as biomarkers. Aquatic Toxicology, 76, 160–202.CrossRefGoogle Scholar
  2. Amiard, J. C., & Cosson, R. P. (1997). Les métallothionéines. In L. Lagadic, T. Caquet, J. C. Amiard, & F. Ramade (Eds.), Biomarqueurs en écotoxicologie: Aspects fondamentaux. Paris: Masson.Google Scholar
  3. Andrews, G. K. (2000). Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochemical Pharmacology, 59, 95–104.CrossRefGoogle Scholar
  4. Bakka, A., Johnsen, A. S., Endresen, L., & Rugstad, H. E. (1982). Radioresistance in cells with high content of metallothionein. Experientia, 38, 381–383.CrossRefGoogle Scholar
  5. Banni, M., Dondero, F., Jebali, J., Guerbej, H., Boussetta, H., & Viarengo, A. (2007). Assessment of heavy metal contamination using real-time PCR analysis of mussel metallothionein mt10 and mt20 expression: A validation a long the Tunisian coast. Biomarkers, 12, 369–383.CrossRefGoogle Scholar
  6. Barsyte, D., White, K. N., & Lovejoy, D. A. (1999). Cloning and characterization of metallothionein cDNAs in the mussel Mytilus edulis L. digestive gland. Comparative Biochemistry and Physiology part C, 122, 287–296.CrossRefGoogle Scholar
  7. Baudrimont, M., Metivaud, J., Maury-Brachet, R., Ribeyre, F., & Boudou, A. (1997). Bioaccumulation and metallothionein response in the Asiatic clam (Corbicula fluminea) after experimental exposure to cadmium and inorganic mercury. Environmental Toxicology and Chemistry, 16, 2096–2105.Google Scholar
  8. Beliaeff, B., O’Connor, T. P., & Claisse, D. (1998). Comparison of chemical concentrations in mussels and oysters from the United States and France. Environmental Monitoring and Assessment, 49, 87–95.CrossRefGoogle Scholar
  9. Ben Ayed-Aloulou, F. (2010). Etude de la contamination des sediments superficiels de la frange littorale Sfax-Skhira: Suivi des hydrocarbures des métaux comme bioindicateurs de pollution (p. 177). Thèse de doctorat. Université de Sfax.Google Scholar
  10. Berthet, B., Mouneyrac, P. T., & Amiard-Triquet, C. (2005). Metallothionein concentration in sponges (Spongia officinalis) as a biomarker of metal contamination. Comparative Biochemistry and Physiology part C, 141, 306–313.Google Scholar
  11. 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. Ecotoxicology and Environmental Safety, 72, 382–387.CrossRefGoogle Scholar
  12. Binz, P. A., & Kagi, J. H. R. (1999). Metallothionein: Molecular evolution and classification. In C. Klaassen (Ed.), Metallothionein. Basel: Birkhauser.Google Scholar
  13. Bragigand, V., & Berthet, B. (2003). Some methodological aspects of metallothionein evaluation. Comparative Biochemistry and Physiology Part A, 134, 55–61.CrossRefGoogle Scholar
  14. Braun, W., Vašák, M., Robbins, A. H., Stout, C. D., Wagner, G., Kägi, J. H. R., et al. (1992). Comparison of the NMR solution structure and the X-ray crystal structure of rat metallothionein-2. Proceeding of the National Academy and Sciences, 89, 10124–10128.CrossRefGoogle Scholar
  15. Brugnera, E., Georgiev, O., Radtke, F., Heuchel, R., Baker, E., Sutherland, G. R., et al. (1994). Cloning, chromosomal mapping and characterization of the human metal-regulatory transcription factor MTF-1. Nucleic Acids Research, 22, 3167–3173.CrossRefGoogle Scholar
  16. Burgeot, T., Bocquené, G., Pingray, G., Godefroy, D., Legrand, J., Dimeet, J., et al. (1994). Monitoring biological effects of contamination in marine fish along French coasts by measurement of ethoxyresorufin-Odeethylase activity. Ecotoxicology and Environmental Safety, 29, 131–147.CrossRefGoogle Scholar
  17. C.G.P. (1996). Annuaire des statistiques des pêches en Tunisie. Tunisie: Ministère de l’agriculture.Google Scholar
  18. Chan, K. (1995). Metallothionein: Potential biomarker for monitoring heavy metal pollution in fish around Hong Kong. Marine Pollution Bulletin, 31, 411–415.CrossRefGoogle Scholar
  19. Chang, Y. T., Jong, K. J., Liao, B. K., & Wu, S. M. (2007). Cloning and expression of metallothionein cDNA in the hard clam (Meretrix lusoria) upon cadmium exposure. Aquaculture, 262, 504–513.CrossRefGoogle Scholar
  20. Choi, H. J., Ji, J., Chung, K. H., & Ahn, I. Y. (2007). Cadmium bioaccumulation and detoxification in the gill and digestive gland of the Antarctic bivalve Laternula elliptica. Comparative Biochemistry and Physiology Part C, 145, 227–235.Google Scholar
  21. Choi, Y. K., Jo, P. G., & Choi, C. Y. (2008). Cadmium affects the expression of heat shock protein 90 and metallothionein mRNA in the Pacific oyster Crassostrea gigas. Comparative Biochemistry and Physiology Part C, 147, 286–292.Google Scholar
  22. Cosson, R. P. (2000). Bivalve metallothionein as a biomarker of aquatic ecosystem pollution by trace metals: Limits and perspectives. Cell an Molecular Biology, 46, 259–309.Google Scholar
  23. Cosson, R. P., & Amiard, J. C. (1998). Utilisation des métallothionéines comme biomarqueurs d’exposition aux métaux. In L. Lagadic, T. Caquet, J. C. Amiard, & F. Ramade (Eds.), Utilisation de biomarqueurs pour la surveillance de la qualité de l’environnement. Paris: Lavoisier.Google Scholar
  24. Cosson, R. P., & Amiard, J. C. (2000). Use of metallothionein as biomarkers of exposure to metals. In L. Lagadic, T. Caquet, J. C. Amiard, & Ramade, F. (Eds.), Use of biomarkers for environmental quality assessment. USA: Science Publishers.Google Scholar
  25. Dabrio, M., Rodriguez, A. R., Bordin, G., Bebianno, M. J., De Ley, M., Sestakova, I., et al. (2002). Recent developments in quantification methods for metallothionein. Journal of Inorganic Biochemistry, 88, 123–134.CrossRefGoogle Scholar
  26. Dondero, F., Piacentini, L., Banni, M., Rebelo, M., Burlando, B., & Viarengo, A. (2005). Quantitative PCR analysis of two molluscan metallothionein genes unveils differential expression and regulation. Gene, 345, 259–270.CrossRefGoogle Scholar
  27. Durnam, D. M., & Palmiter, R. D. (1981). Transcriptional regulation of the mouse metallothionein-I gene by heavy metals. Journal of Biological Chemistry, 256, 5712–5716.Google Scholar
  28. Ejnik, J., Munoz, A., Gan, T., Shaw, C. F., & Petering, D. H. (1999). Interprotein metal ion exchange between cadmium-carbonic anhydrase and apo- or zinc-metallothionein. Journal of Biological Inorganic Chemistry, 4, 784–790.CrossRefGoogle Scholar
  29. Engel, D. W., & Roesijadi, G. (1987). Metallothioneins: A monitoring tool. In W. B. Vernberg, A. Calabrese, F. P. Thurberg, & F. J. Vernberg (Eds.), Pollution physiology of estuarine organisms. Columbia: University of South Carolina Press.Google Scholar
  30. Freedman, J. H., Slice, L. W., Dixon, D., Fire, A., & Rubin, C. S. (1993). The novel metallothionein genes of Caenorhabditis elegans. Structural organization and inducible, cell-specific expression. Journal of Biological Chemistry, 268, 2554–2564.Google Scholar
  31. Friedman, R. L., & Stark, G. R. (1985). Alpha-interferon-induced transcription of HLA and metallothionein genes containing homologous upstream sequences. Nature, 314, 637–639.CrossRefGoogle Scholar
  32. Gao, A., Wang, L., & Yuan, H. (2011). Expression of metallothionein cDNA in a freshwater crab, Sinopotamon yangtsekiense, exposed to cadmium. Experimental and Toxicologic Pathology (in press).Google Scholar
  33. Gao, D., Wang, G. T., Chen, X. Y., & Nie, P. (2009). Metallothionein-2 gene from the Mandarin fish Siniperca chuatsi: cDNA cloning, tissue expression, and immunohistochemical localization. Comparative Biochemistry and Physiology Part C, 149, 18–25.Google Scholar
  34. Gargouri, Z., Souissi, M., Souissi, R., Abdeljaoued, S., & Turki, D. (2006). Diagnostic bio-sédimentaire et géochimique du littoral de la frange littorale de Nakta (sud de sfax, Tunisie). revue Méditerranéenne de l’Environnement, 1, 170–184.Google Scholar
  35. Geffard, A., Amiard, J. C., & Amiard-Triquet, C. (2002). Use of metallothionein in gills from oysters (Crassostrea gigas) as a biomarker: Seasonal and intersite fluctuations. Biomarkers, 7, 123–137.CrossRefGoogle Scholar
  36. George, S. G., Hodgson, P. A., Tytler, P., & Todd, K. (1996a). Inducibility of metallothionein mRNA expression and cadmium tolerance in larvae of a marine teleost, the turbot (Scophthalmus maximus). Fundamental and Applied Toxicology, 33, 91–99.CrossRefGoogle Scholar
  37. George, S. G., & Olsson, P. E. (1994). Metallothioneins as indicators of trace metal pollution. In K. J. M. Kramer (Ed.), Biomonitoring of coastal waters and estuaries. Florida: CRC Press.Google Scholar
  38. George, S. G., Todd, K., & Wright, J. (1996b). Regulation of metallothionein in teleosts: Induction of MT mRNA and protein by cadmium in hepatic and extra-hepatic tissues of a marine flatfish, the turbot (Scophthalmus maximus). Comparative Biochemistry and Physiology Part C, 113, 109–115.Google Scholar
  39. Hamer, D. H. (1986). Metallothionein. Annual Review of Biochemistry, 55, 913–951.CrossRefGoogle Scholar
  40. Hamza-Chaffai, A., Amiard, J. C., & Cosson, R. P. (1999). Relationship between metallothioneins and metals in a natural population of clam Ruditapes decussatus from Sfax coast: A non-linear model using box-cox transformation. Comparative Biochemistry and Physiology Part C, 123, 153–163.Google Scholar
  41. Hamza-Chaffai, A., Amiard, J. C., Pellerin, J., Joux, L., & Berthet, B. (2000). The potential use of metallothionein in the clam Ruditapes decussatus as a biomarker of in situ metal exposure. Comparative Biochemistry and Physiology Part C, 127, 185–197.Google Scholar
  42. Hamza-Chaffai, A., Cosson, R. P., Amiard-Triquet, C., & El Abed, A. (1995). Physico-chemical forms of storage of metals (Cd, Cu and Zn) and metallothionein-like proteins in gills and liver of marine fish from the Tunisian coast: Ecotoxicological consequences. Comparative Biochemistry and Physiology Part C, 111, 329–341.CrossRefGoogle Scholar
  43. Hamza-Chaffai, A., Pellerin, J., & Amiard, J. C. (2003). Health assessment of marine bivalve (Ruditapes decussatus) from the gulf of Gabès (Tunisia). Environment International, 28, 609–617.CrossRefGoogle Scholar
  44. Hamza-Chaffai, A., Roméo, M., & El Abed, A. (1997). Heavy metals in different fishes from the Middle Eastern of Tunisia. Bulletin of Environmental Contamination and Toxicology, 56, 766–773.CrossRefGoogle Scholar
  45. Haq, F., Mahoney, M., & Koropatnick, J. (2003). Signaling events for metallothionein induction. Mutation Research, 533, 211–226.CrossRefGoogle Scholar
  46. Hidalgo, J., Aschner, M., Zatta, P., & Vašák, M. (2001). Roles of the metallothionein family of proteins in the central nervous system. Brain Research Bulletin, 55, 133–145.CrossRefGoogle Scholar
  47. Huang, P. C. (1993). Metallothionein structure/function interface. In K. T. Suzuki, N. Imura, & M. Kimura (Eds.), Metallothionein III: Biological roles and medical implications. Basel: Birkhäuser Verlag.Google Scholar
  48. Hylland, K., Sandvik, M., Skalre, J. U., Beyer, J., Egaas, E., & Goksoyr, A. (1996). Biomarkers in flounder (Platichthysflesus): An evaluation of their use in pollution monitoring. Marine Environmental Research, 42, 223–227.CrossRefGoogle Scholar
  49. Illou, S. (1999). Impact des rejets telluriques d’origines domestiques et industrielles sur les environnements côtières: Cas du littoral Nord de la ville de Sfax (Tunisie). Doctorat de spécialité, Université de Tunis II, Tunisie.Google Scholar
  50. Imbert, J., Culotta, V. C., Furst, P., Gedamu, G., & Hamer, D. (1990). Regulation of metallothionein gene transcription by metals. Advances in Inorganic Biochemistry, 8, 140–150.Google Scholar
  51. Isani, G., Andreani, G., Kindt, M., & Carpene, E. (2000). Metallothioneins (MTs) in marine molluscs. Cell and Molecular Biology, 46, 311–330.Google Scholar
  52. Ivanković, D., Pavičić, J., Erk, M., Filipović-Marijić, 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. Marine Pollution Bulletin, 50, 1303–1313.CrossRefGoogle Scholar
  53. Jahroudi, N., Foster, R., Price-Haughey, J., Beitel, G., & Gedamu, L. (1990). Cell-type specific and differential regulation of the human metallothionein genes. Journal of Biological Chemistry, 265, 6506–6511.Google Scholar
  54. Kägi, J. H. R. (1993). Overview of metallothionein. Methods in Enzymology, 205, 613–626.CrossRefGoogle Scholar
  55. Ketata, I. (2008). Etude in situ de la perturbation endocrinienne par les métaux toxiques (Cd, Pb et Hg) chez la palourde Ruditapes decussatus issue de la région du golfe de Gabès, Thèse de doctorat. Université de Sfax. 230pGoogle Scholar
  56. Kim, J. H., Wang, S. Y., Kim, I. C., Ki, J. S., Raisuddin, S., Lee J. S., et al. (2008). Cloning of a river pufferfish (Takifugu obscurus)metallothionein cDNA and study of its induction profile in cadmium-exposed fish. Chemosphere, 71, 1251–1259.CrossRefGoogle Scholar
  57. Kling, P., & Olsson, P. E. (2005). Metallothionein: Structure and regulation. In T. P. Mommsen, & T. W. Moon (Eds.), Biochemistry and Molecular Biology of Fishes (Vol. 6). Amsterdam: Elsevier.Google Scholar
  58. Koizumi, S., Suzuki, K., Ogra, Y., Yamada, H., & Otsuka, F. (1999). Transcriptional activity and regulatory protein binding of metal-responsive elements of the human metallothionein-IIA gene. European Journal of Biochemistry, 259, 635–642.CrossRefGoogle Scholar
  59. Kojima, Y. (1991). Definitions and nomenclature of metallothioneins. Methods in Enzymology, 205, 8–10.CrossRefGoogle Scholar
  60. Kojima, Y., & Kagi, J. H. R. (1978). Metallothionein. Trends in Biochemical Sciences, 3, 90–93.CrossRefGoogle Scholar
  61. Ladhar-Chaabouni, R., Gargouri, R., & Hamza-Chaffai, A. (2007). Effect of cadmium on some biomarkers in the clam Ruditapes decussatus: Metallothionein quantification by using two techniques. International Journal of Environment and Pollution, 30, 593–601.CrossRefGoogle Scholar
  62. Ladhar-Chaabouni, R., Mokdad-Gargouri, R., Denis, F., & Hamza-Chaffai, A. (2008). Cloning and characterization of cDNA probes for the analysis of metallothionein gene expression in the Mediterranean bivalves: Ruditapes decussatus and Cerastoderma glaucum. Molecular Biology Reports. doi: 10.1007/s11033-008-9274-8.Google Scholar
  63. Ladhar-Chaabouni, R., Machreki-Ajmi, M., & Hamza-Chaffai, A. (2009a). Spatial distribution of cadmium and some biomarkers in Cerastoderma glaucum living in a polluted area. Marine Biology Research, 5, 478–486.CrossRefGoogle Scholar
  64. Ladhar-Chaabouni, R., Smaoui-Damak, W., & Hamza-Chaffai, A. (2009b). In vivo variation of some biomarkers with time and cadmium concentration in the cockle Cerastoderma glaucum. Marine Biology Research, 5, 487–495.CrossRefGoogle Scholar
  65. Lagadic, L., Caquet, T., Amiard, J. C., & Ramade F. (1997). Biomarqueurs en écotoxicilogie: Aspects fondamentaux (pp. 417). Paris: Masson.Google Scholar
  66. Lemoine, S., Bigot, Y., Sellos, D., Cosson, R. P., & Laulier, R. (2000). Metallothionein isoforms in Mytillus edulis (Mollusca, bivalvia): Complementary DNA characterization and quantification of expression in different organs after exposure to cadmium, zinc and copper. Marine Biotechnology, 2, 195–203.Google Scholar
  67. Lemoine, S., & Laulier, M. (2003). Potential use of the levels of the mRNA of a specific metallothionein isoform (MT-20) in mussel (Mytilus edulis) as a biomarker of cadmium contamination. Marine Pollution Bulletin, 46, 1450–1455.CrossRefGoogle Scholar
  68. Machreki-Ajmi, M. (2009). Validation des biomarqueurs de pollution chez le mollusque bivalve Cerastoderma glaucum issu du golfe de Gabès: Etude in situ et transplantation in vivo. Thèse de doctorat, Université de Sfax, Tunisie.Google Scholar
  69. Machreki-Ajmi, M., Ketata, I., Ladhar-Chaabouni, R., & Hamza-Chaffai, A. (2008). The effect of in situ cadmium contamination on some biomarkers in Cerastoderma glaucum. Ecotoxicology, 17, 1–11.CrossRefGoogle Scholar
  70. Machreki-Ajmi, M., Rebai, T., & Hamza-Chaffai, A. (2011). Variation of metallothionein-like protein and metal concentrations during the reproductive cycle of the cockle Cerastoderma glaucum from an uncontaminated site: A 1-year study in the Gulf of Gabès area (Tunisia). Marine Biology Research, 7, 261–271.CrossRefGoogle Scholar
  71. Margoshes, M., & Vallee, B. L. (1957). A cadmium protein from equine kidney cortex. Journal of American Chemistry Society, 79, 4813–4820.CrossRefGoogle Scholar
  72. Moilanen, L. H., Tetsunari, F., & Freedman, J. H. (1999). Regulation of metallothionein gene transcription. Journal of Biological Chemistry, 274, 29655–29665.CrossRefGoogle Scholar
  73. Monserrat, J. M., Martinez, P. E., Geracitano, L. A., Amado, L. L., Martins, C. M. G., Pinho, G. L. L., et al. (2007). Pollution biomarkers in estuarine animals: Critical review and new perspectives. Comparative Biochemistry and Physiology Part C, 146, 221–234.Google Scholar
  74. N.A.S. (1980). The International Mussel Watch. Report of a workshop sponsored by the environment studies board. Natural Resources Commission, National Research Council. National Academy of Science. Washington, DC.Google Scholar
  75. Newman, M. C., & Unger, M. A. (2002). Fundamentals of ecotoxicology (Ed). USA: Lewis publishers.Google Scholar
  76. Paek, S. M., Chung, S., & Lee, I. S. (1999). Level of heavy metals in the Onsan Bay in Korea and involvement of metal binding protein in the accumulation of cadmium in Littorina brevicula. Korean Journal of Ecology, 22, 95–100.Google Scholar
  77. Park, H., Ahn, I. Y., Choi, H. J., Pyo, S. H., & Lee, H. E. (2007). Cloning, expression and characterization of metallothionein from the Antarctic clam Laternula elliptic. Protein Expression and Purification, 52, 82–88.CrossRefGoogle Scholar
  78. Paul-Pont, I., Gonzalez, P., Baudrimont, M., Nili, H., & De Montaudouin, X. (2010). Short-term metallothionein inductions in the edible cockle Cerastoderma edule after cadmium or mercury exposure: Discrepancy between mRNA and protein responses. Aquatic Toxicology, 97, 260–267.CrossRefGoogle Scholar
  79. Pavicic, J., Skreblin, M., Raspor, B., Branica, M., Tusek-Znidaric, M., Kregar, I., et al. (1987). Metal pollution assessment of the marine environment by determination of metal-binding proteins in Mytilus sp. Marine Chemistry, 22, 235–248.CrossRefGoogle Scholar
  80. Peakall, D. B., & Shugart, L. R. (1993). Strategy for biomarker research and application in the assessment of environmental health. NATO publ.Google Scholar
  81. Pedersen, S. N., Lundebye, A. K., & Depledge, M. H. (1997). Field application of metallothionein and stress protein biomarkers in the shore crab Carcinus maenas exposed to trace metals. Aquatic Toxicology, 37, 183–200.CrossRefGoogle Scholar
  82. Perceval, O., Couillard, Y., Pinel-Alloul, B., Bonneris, E., & Campbell, P. G. C. (2006). Long-term trends in accumulated metals (Cd, Cu and Zn) and metallothionein in bivalves from lakes within a smelter-impacted region. Science of the Total Environment, 369, 403–418.CrossRefGoogle Scholar
  83. Perceval, O., Pinel-Alloul, B., Méthot, G., Couillard, Y., Giguère, A., Campbell, P. G. C., et al. (2002). Cadmium accumulation and metallothionein synthesis in freshwater bivalves (Pyganodon grandis): Relative influence of the metal exposure gradient versus limnological variability. Environmental Pollution, 118, 5–17.CrossRefGoogle Scholar
  84. Raspor, B., & Pavicic, J. (1991). Induction of metallothionein-like proteins in the digestive gland of Mytilus galloprovincialis after a chronic exposure to the mixture of trace heavy metals. Chemical Speciation and Bioavailability, 3, 39–46.Google Scholar
  85. Rause, W. E. (1990). Phytochelatins. Annual Review of Biochemistry, 59, 61–86.CrossRefGoogle Scholar
  86. Robbins, A. H., McRee, D. E., Williamson, M., Collett, S. A., Xuong, N. H., Furey, W., et al. (1991). Refined structure of Cd, Zn metallothionein at 2.0 Å resolution. Journal of Molecular Biochemistry, 221, 1269–1293.Google Scholar
  87. Roesijadi, G. (2000). Metal transfer as a mechanism for metallothionein-mediated metal detoxification. Cell and Molecular Biology, 46, 393–405.Google Scholar
  88. Roesijadi, G., Bogumil, R., Vasak, M., & Kagi, J. H. (1998). Modulation of DNA binding of a tramtrack zinc finger peptide by the metallothioneinthionein conjugate pair. Journal of Biological Chemistry, 273, 17425–17432.CrossRefGoogle Scholar
  89. Roesijadi, G., & Klerks, P. (1989). A kinetic analysis of Cd-binding to metallothionein and other intracellular ligands in oyster gills. Journal of Experimental Zoology, 251, 1–12.CrossRefGoogle Scholar
  90. Roesijadi, G., Rezvankhah, S., Perez-Matus A., Mitelberg, A., Torruellas, K., & Van Veld, P. A. (2009). Dietary cadmium and benzo(a)pyrene increased intestinal metallothionein expression in the fish Fundulus heteroclitus. Marine Environmental Research, 67, 25–30CrossRefGoogle Scholar
  91. Samson, S., & Gedamu, L. (1998). Molecular analyses of metallothionein gene regulation. Progress in Nucleic Acid Research and Molecular Biology, 59, 257–288.CrossRefGoogle Scholar
  92. Sarkar, A., Ray, D., Shrivastava, A. N., & Sarker, S. (2006). Molecular biomarkers: Their significance and application in marine pollution monitoring. Ecotoxicology, 15, 333–340.CrossRefGoogle Scholar
  93. Seguin, C., & Prevost, J. (1988). Detection of a nuclear protein that interacts with a metal regulatory element of the mouse metallothionein 1 gene. Nucleic Acids Research, 16, 10547–10560.CrossRefGoogle Scholar
  94. Serafim, A., Company, R. M., Bebianno, M. J., & Langston, W. J. (2002). Effect of temperature and size on metallothionein synthesis in the gill of Mytilus galloprovincialis exposed to cadmium. Marine Environmental Research, 54, 361–365.CrossRefGoogle Scholar
  95. Serbaji, M. M. (2000). Utilisation d’un SIG multi-sources pour la compréhension et la gestion intégrée de l’écosystème côtier de la région de Sfax (Tunisie). Doctorat de spécialité, Université de Tunis II, Tunisie.Google Scholar
  96. Smaoui-Damak, W., Berthet, B., & Hamza-Chaffai, A. (2009). In situ potential use of metallothionein as a biomarker of cadmium contamination in Ruditapes decussates. Ecotoxicology and Environmental Safety, 72, 1489–1498.CrossRefGoogle Scholar
  97. Smaoui-Damak, W., Hamza Chaffai, A., Bebianno, M. J., & Amiard, J. C. (2004). Variation of metallothioneins in gills of the clam (Ruditapes decassatus) from the Gulf of Gabès (Tunisia). Comparative Biochemistry and Physiology part C, 139, 181–188.Google Scholar
  98. Smaoui-Damak, W., Hamza-Chaffai, A., Berthet, B., & Amiard, J. C. (2003). Preliminary study of the clam Ruditapes decussatus exposed in situ to metal contamination and originating from the Gulf of Gabès, Tunisia. Bulletin of Environment Contamination and Toxicology, 71, 961–970.CrossRefGoogle Scholar
  99. Suhy, D. A., Simon, K. D., Linzer, D. I., & O’Halloran, T. V. (1999). Metallothionein is part of a zinc-scavenging mechanism for cell survival under conditions of extreme zinc deprivation. Journal of Biology and Chemistry, 274, 9183–9192.CrossRefGoogle Scholar
  100. Thiele, D. J. (1992). Metal-regulated transcription in eukaryotes. Nucleic Acids Research, 20, 1183–1191.CrossRefGoogle Scholar
  101. Thornalley, P. J., & Vasak, M. (1985). Possible role for metallothionein in protection against radiation-induced oxidative stress. Kinetics and mechanism of its reaction with superoxide and hydroxyl radicals. Biochimica et Biophysica Acta, 827, 36–44.CrossRefGoogle Scholar
  102. Tom, M., Chen, N., Segev, M., Herut, B., & Baruch, R. (2004). Quantifying fish metallothionein transcript by real time PCR for its utilization as an environmental biomarker. Marine Pollution Bulletin, 48, 705–710.CrossRefGoogle Scholar
  103. Tom, M., Jakubov, E., Rinkevich, B., & Herut, B. (1999). Monitoring of hepatic metallothionein mRNA levels in the fish Lithognathus mormyrus—Evaluation of transition metal pollution in a Mediterranean coast. Marine Pollution Bulletin, 38, 503–508.CrossRefGoogle Scholar
  104. Unger, M. E., Chen, T. T., Murphy, C. M., Vestling, M. M., Fenselau, C., & Roesijadi, G. (1991). Primary structure of molluscan metallothionein deduced from PCR-amlplified cDNA and mass spectrometry of purified proteins. Biochemica et Biophysica Acta, 1074, 371–377.CrossRefGoogle Scholar
  105. Unger, M. E., & Roesijadi, G. (1993). Increase in metallothionein mRNA accumulation during Cd challenge in oysters preexposed to Cd. Aquatic Toxicology, 34, 185–193.CrossRefGoogle Scholar
  106. Van Straalen, N. M., & Roelofs, D., (Eds.) (2006). An introduction to ecological genomics. Oxford: Oxford Biology University press.Google Scholar
  107. Viarengo, A. (1989). Heavy metals in marine invertebrates: Mechanisms of regulation and toxicity at the cellular level. Aquatic Sciences, 1, 295–317.Google Scholar
  108. Viarengo, A., & Nott, J. A. (1993). Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comparative Biochemistry and Physiology Part C, 104, 355–372.CrossRefGoogle Scholar
  109. Winge, D. R., Nielson, K. B., Gray, W. R., & Hamer, D. H. (1985). Yeast metallothionein. Sequence and metal-binding properties. Journal of Biological Chemistry, 260, 14464–14470.Google Scholar
  110. Wu, S. M., & Hwang, P. P. (2003). Copper or cadmium pretreatment increases the protection against cadmium toxicity in tilapia larvae (Oreochromis mossambicus). Zoological Studies, 42, 179–185.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Rim Ladhar-Chaabouni
    • 1
  • Monia Machreki-Ajmi
    • 1
  • Amel Hamza-Chaffai
    • 1
  1. 1.UR 09-03 Marine Environmental ToxicologySfax UniversitySfaxTunisia

Personalised recommendations