Tissue- and cell-specific expression of metallothionein genes in cadmium- and copper-exposed mussels analyzed by in situ hybridization and RT-PCR

Toxicology and Applied Pharmacology

Volumn 220, Issue 2, 2007, Pages 186-196

  Zorita, I ^a   Bilbao, E ^a   Schad, A ^b   Cancio, I ^a   Soto, M ^a   Cajaraville, M P ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Cadmium; Copper; In situ hybridization; Metallothionein isoforms; Mussel; RT PCR

Indexed keywords

BIOLOGICAL MARKER; CADMIUM; COPPER; ISOPROTEIN; METAL; METALLOTHIONEIN; METALLOTHIONEIN 10; METALLOTHIONEIN 10B; METALLOTHIONEIN 20; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BASOPHIL; BIOACCUMULATION; BLOOD CELL; CELL DENSITY; CELL SPECIFICITY; CELL VOLUME; CONTROLLED STUDY; EXPOSURE; GENE EXPRESSION; GILL; GRANULAR CELL; IN SITU HYBRIDIZATION; INTESTINE EPITHELIUM CELL; INTRON; LYSOSOME; MOLECULAR CLONING; MUSSEL; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PROTEIN FAMILY; PROTEIN INDUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STOMACH; TISSUE SPECIFICITY;

ANIMALS; BASOPHILS; CADMIUM; COPPER; GENE EXPRESSION REGULATION; IMAGE PROCESSING, COMPUTER-ASSISTED; IN SITU HYBRIDIZATION; LYSOSOMES; METALLOTHIONEIN; MYTILUS; MYTILUS EDULIS; ORGAN SPECIFICITY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SILVER STAINING; SPECTROPHOTOMETRY, ATOMIC;

MYTILUS EDULIS; MYTILUS GALLOPROVINCIALIS;

EID: 33947722007     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2007.01.003     Document Type: Article

References (67)

1. Barsyte D., White K.N., and Lovejoy D.A. Cloning and characterization of metallothionein cDNAs in the mussel Mytilus edulis (L.) digestive gland. Comp. Biochem. Physiol. 122 (1999) 287-296
2. Baudrimont M., Lemaire-Gony S., Ribeyre F., Métivaud J., and Boudou A. Seasonal variations of metallothionein concentrations in the Asiatic clam (Corbicula fluminea). Comp. Biochem. Physiol. 118 (1997) 361-367
3. Bebianno M.J., and Langston W.J. Turnover rate of metallothionein and cadmium in Mytilus edulis. Biometals 6 (1993) 239-244
4. Cajaraville M.P., Díez G., Marigómez I.A., and Angulo E. Responses of basophilic cells of the digestive gland of mussels to petroleum hydrocarbon exposure. Dis. Aquat. Org. 9 (1990) 221-228
5. Cajaraville M.P., Robledo Y., Etxeberria M., and Marigómez I. Cellular biomarkers as useful tools in biological monitoring of environmental pollution: molluscan digestive lysosomes. In: Cajaraville M.P. (Ed). Cell Biology in Environmental Toxicology (1995), University of the Basque Country, Press Service, Bilbo 29-55
6. Cajaraville M.P., Bebianno M.J., 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. Sci. Total Environ. 247 (2000) 295-311
7. Ceratto N., Dondero F., Van de Loo J.W., Burlando B., and Viarengo A. Cloning and sequencing of a novel metallothionein gene in Mytilus galloprovincialis Lam. Comp. Biochem. Physiol. 131 (2002) 217-222
8. Chabicovsky M., Niedestatter H., Thaler R., Hödl E., Parson W., Rossmanith W., and Dallinger R. Localization and quantification of Cd- and Cu-specific metallothionein isoform mRNA in cells and organs of the terrestrial gastropod Helix pomatia. Toxicol. Appl. Pharm. 190 (2003) 25-36
9. Ciocan C.M., and Rotchell J.M. Cadmium induction of metallothionein isoforms in juvenile and adult mussel (Mytilus edulis). Environ. Sci. Technol. 38 (2004) 1073-1078
10. Cosson R.P. Bivalve metallothioneins as a biomarker of aquatic ecosystem pollution by trace metals: limits and perspectives. Cell. Mol. Biol. 46 (2000) 295-309
11. Dabrio M., Rodríguez A.R., Bordin G., Bebianno M.J., De Ley M., Sestákova I., Vasak M., and Norberg M. Recent developments in quantification methods for metallothionein. J. Inorg. Biochem. 88 (2002) 123-134
12. Dallinger R., Chabicovsky M., Lagg B., Schipflinger R., Weirich H.G., and Berger B. Isoform-specific quantification of metallothionein in the terrestrial gastropod Helix pomatia: II. A differential biomarker approach under laboratory and field conditions. Environ. Toxicol. Chem. 23 (2004) 902-910
13. Dallinger R., Chabicovsky M., Hodl E., Prem C., Hunziker P., and Manzl C. Copper in Helix pomatia (Gastropoda) is regulated by one single cell type: differently responsive metal pool in rhogocytes. Am. J. Physiol.: Regul., Integr. Comp. Physiol. 289 (2005) 1185-1195
14. Danscher G. Autometallography. A new technique for light and electron microscopic visualization of metals in biological tissues (gold, silver, metal sulphides and metal selenides). Histochemistry 81 (1984) 331-335
15. Dimitriadis V.K., Domouhtsidou G.P., and Cajaraville M.P. Cytochemical and histochemical aspects of the digestive gland cells of the mussel Mytilus galloprovincialis (L.) in relation to function. J. Mol. Histol. 35 (2004) 501-509
16. Domouhtsidou G.P., Dailianis S., Kaloyianni M., and Dimitriadis V.K. Lysosomal membrane stability and metallothionein content in Mytilus galloprovincialis (L.) as biomarkers. Combination with trace metal concentration. Mar. Pollut. Bull. 48 (2004) 572-586
17. Dondero F., Piacentini L., Banni M., Rebelo M., Burlando B., and Viarengo A. Quantitative PCR analysis of two molluscan metallothionein genes unveils differential expression and regulation. Gene 345 (2005) 259-270
18. Ellman G.L. Tissue sulphyhydryl groups. Arch. Biochem. Biophys. 82 (1959) 70-77
19. Franzellitti S., and Fabbri E. Differential HSP70 gene expression in the Mediterranean mussel exposed to various stressors. Biochem. Bioph. Res. Commun. 336 (2005) 1157-1163
20. George S.G. Biochemical and cytological assessments of metal toxicity in marine animals. In: Furness R.W., and Rainbow P.S. (Eds). Heavy Metals in the Marine Environment (1990), CRC Press Inc, Boca Raton, Florida 123-142
21. Geret F., and Cosson R.P. Induction of specific isoforms of metallothionein in mussel tissues after exposure to cadmium and mercury. Arch. Environ. Contam. Toxicol. 42 (2002) 36-42
22. Gunther E., and Walter L. Genetic aspects of the hsp70 multi-family in vertebrates. Experientia 50 (1994) 1001-9987
23. Isani G., Andreani G., Kindt M., and Carpene E. Metallothioneins (MTs) in marine molluscs. Cell. Mol. Biol. 46 (2000) 311-330
24. Ivankovic D., Pavicic J., Kozar S., and Raspor B. Multiple forms of metallothionein from the digestive gland of naturally occurring and cadmium-exposed mussels, Mytilus galloprovincialis. Hegol. Mar. Res. 56 (2002) 95-101
25. Jacob S.T., Ghoshal K., and Sheridan J.F. Induction of metallothionein by stress and its molecular mechanisms. Gene Expression 7 (1999) 301-310
26. Jie H.B., Bailey C.W., Ray B.K., Estes D.M., Kumar N., and Carson C.A. Single copy Babesia microti hsp70. Mol. Biol. Parasitol. 83 (1996) 241-246
27. Kägi J.H.R. Overview of metallothionein. Methods Enzymol. 205 (1991) 613-626
28. Kay R.J., Russnak R.H., Mathias S., and Candido E.P.M. Expression of intron-containing C. elegans heat shock genes in mouse cells demonstrates divergence of 3′ splice recognition sequences between nematodes and vertebrates, and an inhibitory effect of heat shock on mammalian splicing apparatus. Nucleic Acid Res. 15 (1987) 3723-3741
29. Khoo H.W., and Patel K.H. Metallothionein cDNA, promoter, and genomic sequences of the tropical green mussel Perna viridis. J. Exp. Zool. 284 (1999) 445-453
30. Klaasen C.D., Liu J., and Choudhuri S. Metallothionein: an intracellular protein to protect against cadmium toxicity. Annu. Rev. Pharmacol. Toxicol. 39 (1999) 267-294
31. Langston W.J., Bebianno M.J., and Burt G.R. Metal handling strategies in molluscs. In: Langston W.J., and Bebianno M.J. (Eds). Metabolism of Trace Metals in Aquatic Organisms (1998), Chapman and Hall, New York 219-284
32. Lecoeur S., Videmann B., and Berny P. Evaluation of metallothionein as a biomarker of single and combined Cd/Cu exposure in Dreissena polymorpha. Environ. Res. 94 (2004) 184-191
33. Leignel V., and Laulier M. Isolation and characterization of Mytilus edulis metallothionein genes. Comp. Biochem. Physiol. 142 (2006) 12-18
34. Leignel V., Hardiviller Y., and Laulier M. Small metallothionein MT10 genes in coastal and hydrothermal mussels. Mar. Biotech. 7 (2005) 236-244
35. Lemoine S., and Laulier M. 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. Mar. Pollut. Bull. 46 (2003) 1450-1455
36. Lemoine S., Bigot Y., Sellos D., Cosson R.P., and Laulier M. Metallothionein isoforms in Mytilus edulis (Mollusca. Bivalvia): complementary DNA characterization and quantification of expression in different organs after exposure to cadmium, zinc and copper. Mar. Biotech. 2 (2000) 195-203
37. Mackay E., Overnell J., Dumbar B., Davidson I., Hunziker P.E., Kägi J.H.R., and Fothergill J.E. Complete amino acid sequences of five dimeric and four monomeric forms of metallothionein from the edible mussel Mytilus edulis. Eur. J. Biochem. 218 (1993) 183-194
38. Marigómez I., Soto M., and Angulo E. Seasonal variability in the quantitative structure of the digestive tubules of Littorina littorea. Aquat. Living Resour. 5 (1992) 299-305
39. Marigómez I., Soto M., Etxeberria M., and Angulo E. Effects of size, sex, reproduction and trematode infestation on the quantitative structure of digestive tubules in stressed winkles. Zool. J. B. Anat. 123 (1993) 319-336
40. Marigómez I., Soto M., and Cajaraville M.P. Morphofunctional patterns of cell and tissue systems involved in metal handling and metabolism. In: Cajaraville M.P. (Ed). Cell Biology in Environmental Toxicology (1995), University of the Basque Country, Press Service Bilbao 89-134
41. Marigómez I., Cajaraville M.P., Soto M., and Lekube X. Cell-type replacement, a successful strategy of mollusks to adapt to chronic exposure to pollutants. Cuad. Invest. Biol. 20 (1998) 255-258
42. Marigómez I., Soto M., Cajaraville M.P., Angulo E., and Giamberini L. Cellular and subcellular distribution of metals in molluscs. Micros. Res. Tech. 56 (2002) 358-392
43. Marigómez I., Soto M., Orbea A., Cancio I., and Cajaraville M.P. Chapter 14: Biomonitoring of environmental pollution in the Basque coast using molecular, cellular and tissue-level biomarkers: an integrative approach. In: Borja A., and Collins M. (Eds). Oceanography and Marine Environment of the Basque Country. Elsevier Oceanogr. Ser. 70 (2004), Elsevier, Amsterdam 335-364
44. Martoja R., and Martoja-Pierson M. Técnicas de Histología Animal (1970), Toray Masson S.A., Barcelona 350
45. Moore M.N., and Allen J.I. A computational model of the digestive gland epithelial cells of marine mussels and its simulated responses to oil-derived aromatic hydrocarbons. Mar. Environ. Res. 54 (2002) 579-584
46. Morton B. Feeding and digestion in Bivalvia. In: Saleuddin A.S.M., and Wilburg M. (Eds). Mollusca vol 5 (1983), Academic Press, New York 65-147
47. Ortiz-Zarragoitia, M., 2005. Effects of endocrine disruptors on peroxisome proliferation, reproduction and development of model organisms, zebrafish and mussel. PhD Thesis, University of the Basque Country, pp. 164.
48. Roesijadi G. Metallothionein induction as a measure of response to metal exposure in aquatic animals. Environ. Health Perpect. 102 (1994) 91-96
49. Roméo M., and Gnassia-Barelli M. Metal distribution in different tissues and in subcellular fractions of the Mediterranean clam Ruditapes decussatus treated with cadmium, copper, or zinc. Comp. Biochem. Physiol. 111 (1995) 457-463
50. Samson S.L., and Gedamu L. Molecular analyses of metallothionein gene regulation. Prog. Nucleic Acid Res. Mol. Biol. 59 (1998) 257-288
51. Sanger F., Nicklen S., and Coulson A.R. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U.S.A. 74 (1977) 5463-5467
52. Schad A., Fahimi H.D., Völkl A., and Baumgart E. Nonradioactive in situ hybridization for detection of mRNAs encoding for peroxisomal proteins: heterogeneous hepatic lobular distribution after treatment with single dose of bezafibrate. J. Histochem. Cytochem. 44 (1996) 825-834
53. Soto M., and Marigómez I. Metal bioavailability assessment in "Mussels-Watch" programmes by automated image analysis of BSD in digestive cell lysosomes. Mar. Ecol.: Prog. Ser. 156 (1997) 141-150
54. Soto M., Cajaraville M.P., and Marigómez I. Tissue and cell distribution of copper, zinc and cadmium in the mussel, Mytilus galloprovincialis, determined by autometallography. Tissue Cell 28 (1996) 557-568
55. Soto M., Ireland M.P., and Marigómez I. The contribution of metal/shell-weight index in target-tissues to metal body burden in sentinel marine molluscs: 2. Mytilus galloprovincialis. Sci. Total Environ. 198 (1997) 149-160
56. Soto M., Quincoces I., and Marigómez I. Autometallographical procedure for the localization of metal traces in molluscan tissues by light microscopy. J. Histotech. 21 (1998) 123-127
57. Soto M., Ireland M.P., and Marigómez I. Changes in mussel biometry on exposure to metals: implications in estimation of metal bioavailability in "Mussel-Watch" programmes. Sci. Total Environ. 247 (2000) 175-187
58. Soto M., Zaldibar B., Cancio I., Taylor M.G., Turner M., Morgan J.A., and Marigómez I. Subcellular distribution of cadmium and its cellular ligands in mussel digestive gland cells as revealed by combined autometallography and X-ray microprobe analysis. Histochem. J. 34 (2002) 273-280
59. Syasina I.G., Vaschenko M.A., and Zhandan P.M. Morphological alterations in the digestive diverticula of Mizuhopecten yessoensis (Bivalvia: Pectenidae) from polluted areas of Peter the Great Bay, Sea of Japan. Mar. Environ. Res. 44 (1997) 85-98
60. UNEP/RAMOGE. Manual on the Biomarkers Recommended for the MED POL Biomonitoring Programme (1999), UNEP, Athens, Greece 39
61. 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. Mar. Environ. Res. 44 (1997) 69-84
62. Viarengo A., Burlando B., Ceratto N., and Panfoli I. Antioxidant role of metallothioneins: a comparative overview. Cell. Mol. Biol. 46 (2000) 407-417
63. Viarengo A., Lafaurie M., Gabrielides G.P., Fabbri R., Marro A., and Romeo M. Critical evaluation of an exercise undertaken in the framework of the MEDPOL biomonitoring program. Mar. Environ. Res. 49 (2000) 1-18
64. Weibel E.R. Stereological Methods vol. 1 (1979), Academic Press, London 415
65. Yoshino T.P. Histopathological effects of larval digenea on the digestive epithelia of the marine prosobranch Cerithidea californica: fine structural changes in the digestive gland. J. Invert. Pathol. 28 (1976) 209-216
66. Zorita I., Strogyloudi E., Buxens A., Mazón L.I., Papathanassiou E., Soto M., and Cajaraville M.P. 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 (2005) 342-359
67. Zorita I., Ortiz-Zarragoitia M., Soto M., and Cajaraville M.P. Biomarkers in mussels from a copper site gradient (Visnes, Norway): an integrated biochemical, histochemical and histological study. Aquat. Toxicol. 78 (2006) 109-116