Cadmium versus copper toxicity: Insights from an integrated dissection of protein synthesis pathway in the digestive glands of mussel Mytilus galloprovincialis

Journal of Hazardous Materials

Volumn 260, Issue , 2013, Pages 263-271

  Pytharopoulou, S ^a   Kournoutou, G G ^a   Leotsinidis, M ^a   Georgiou, C D ^b   Kalpaxis, D L ^a  

^a UNIVERSITY OF PATRAS   (Greece)

^b UNIVERSITY OF PATRAS   (Greece)

Author keywords

Cadmium; Copper; Mussels; Oxidative stress; Translation

Indexed keywords

ANTIOXIDANT DEFENSE; DIGESTIVE GLANDS; METALLOTHIONEINS; MUSSELS; MYTILUS GALLOPROVINCIALIS; PREINITIATION COMPLEX; PROTEIN SYNTHESIS; RIBOSOMAL SUBUNITS;

BIOSYNTHESIS; COPPER; METALS; MOLLUSCS; OXIDATIVE STRESS; PROTEINS; REPAIR; SHELLFISH; TISSUE; TRANSLATION (LANGUAGES);

CADMIUM;

CADMIUM; COPPER; METALLOTHIONEIN; TRANSFER RNA;

ANTIOXIDANT; BIOACCUMULATION; BIVALVE; CADMIUM; COPPER; DIGESTIVE SYSTEM; ECOTOXICOLOGY; GENE EXPRESSION; POLLUTION EXPOSURE; PROTEIN; TOXICITY TEST;

AMINOACYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; EXOCRINE GLAND; MYTILUS GALLOPROVINCIALIS; NONHUMAN; OXIDATIVE STRESS; PROTEIN SYNTHESIS; RIBOSOME; SIGNAL TRANSDUCTION;

AA-TRNA; ACETYLPHENYLALANYL-TRNA; ACPHE-TRNA; AMINOACYL-TRNA; CADMIUM; COPPER; LABILIZATION PERIOD; LP; MALONDIALDEHYDE; MDA; METALLOTHIONEINS; MICRONUCLEUS; MN; MTS; MUSSELS; OXIDATIVE STRESS; PEPTIDYL TRANSFERASE; PTASE; REACTIVE OXYGEN SPECIES; ROS; SOD; SUPEROXIDE DISMUTASE.; TBARS; THIOBARBITURIC REACTIVE SPECIES; TRANSLATION;

ANIMALS; ANTIOXIDANTS; BIOLOGICAL MARKERS; CADMIUM; COPPER; GASTROINTESTINAL TRACT; MUTAGENICITY TESTS; MUTAGENS; MYTILUS; OXIDATIVE STRESS; TIME FACTORS;

MYTILUS GALLOPROVINCIALIS;

EID: 84879311558     PISSN: 03043894     EISSN: 18733336     Source Type: Journal    
DOI: 10.1016/j.jhazmat.2013.05.031     Document Type: Article

References (64)

1. Bargagli R. Trace metals in Antarctica related to climate change and increasing human impact. Rev. Environ. Contam. Toxicol. 2000, 166:129-173.
2. 2+ in Schizosaccharomyces pombe through amino acid-coded mass tagging and liquid chromatography tandem mass spectrometry. Mol. Cell. Proteomics 2004, 3:596-607.
3. Nzengue Y., Candéias S.M., Sauvaigo S., Douki T., Favier A., Rachidi W., Guiraud P. The toxicity redox mechanisms of cadmium alone or together with copper and zinc homeostasis alteration: its redox biomarkers. J. Trace Elem. Med. Biol. 2011, 25:171-180.
4. Fitsanakis V.A., Aschner M. The importance of glutamate, glycine, and gamma-aminobutyric acid transport and regulation in manganese, mercury and lead neurotoxicity. Toxicol. Appl. Pharmacol. 2005, 204:343-354.
5. Holcik M., Sonenberg N. Translational control in stress and apoptosis. Nat. Rev. Mol. Cell Biol. 2005, 6:318-327.
6. Anderson P., Kedersha N. RNA granules. J. Cell Biol. 2006, 172:803-808.
7. Keene J.D. RNA regulons: coordination of post-transcriptional events. Nat. Rev. Genet. 2007, 8:533-543.
8. Moore M.J. From birth to death: the complex lives of eukaryotic mRNAs. Science 2005, 309:1514-1518.
9. Luparello C., Sirchia R., Longo A. Cadmium as a transcriptional modulator in human cells. Crit. Rev. Toxicol. 2011, 41:75-82.
10. Cuypers A., Plusquin M., Remans T., Jozefczak M., Keunen E., Gielen H., Opdenakker K., Nair A.R., Munters E., Artois T.J., Nawrot T., Vangronsveld J., Smeets K. Cadmium stress: an oxidative challenge. Biometals 2010, 23:927-940.
11. Ivanina A.V., Cherkasov A.S., Sokolova I.M. Effects of cadmium on cellular protein and glutathione synthesis and expression of stress proteins in eastern oysters, Crassostrea virginica (Gmelin). J. Exp. Biol. 2008, 211:577-586.
12. Pytharopoulou S., Grintzalis K., Sazakli E., Leotsinidis M., Georgiou C.D., Kalpaxis D.L. Translational responses and oxidative stress of mussels experimentally exposed to Hg, Cu and Cd: one pattern does not fit at all. Aquat. Toxicol. 2011, 105:157-165.
13. Zorita I., Bilbao E., Schad A., Cancio I., Soto M., Cajaraville M.P. Tissue- and cell-specific expression of metallothionein genes in cadmium- and copper-exposed mussels analyzed by in situ hybridization and RT-PCR. Toxicol. Appl. Pharmacol. 2007, 220:186-196.
14. Shepard J.L., Bradley B.P. Protein expression signatures and lysosomal stability in Mytilus edulis exposed to graded copper concentrations. Mar. Environ. Res. 2000, 50:457-463.
15. Campos A., Tedesco S., Vasconcelos V., Cristobal S. Proteomic research in bivalves: towards the identification of molecular markers of aquatic pollution. J. Proteomics 2012, 75:4346-4359.
16. Muralidharan S., Thompson E., Raftos D., Birch G., Haynes P.A. Quantitative proteomics of heavy metal stress responses in Sydney rock oysters. Proteomics 2012, 12:906-921.
17. Liu F., Wang D.Z., Wang W.X. Cadmium-induced changes in trace element bioaccumulation and proteomics perspective in four marine bivalves. Environ. Toxicol. Chem. 2012, 31:1292-1300.
18. Regoli F., Benedetti M., Giuliani M.E. Antioxidant defenses and acquisition of tolerance to chemical stress. Tolerance to Environmental Contaminants 2011, 153-173. CRC Press, Boca Raton, FL. C. Amiard-Triquet, P.S. Rainbow, M. Roméo (Eds.).
19. Varotto L., Domeneghetti S., Rosani U., Manfrin C., Cajaraville M.P., Raccanelli S., Pallavicini A., Venier P. DNA damage and transcriptional changes in the gills of Mytilus galloprovincialis exposed to nanomolar doses of combined metal salts (Cd, Cu, Hg). PLoS One 2013, 8:e54602. 10.1371/journal.pone.0054602.
20. Pytharopoulou S., Kournoutou G.G., Leotsinidis M., Georgiou C.D., Kalpaxis D.L. Dysfunctions of the translational machinery in digestive glands of mussels exposed to mercury ions. Aquat. Toxicol. 2013, 134-135:23-33.
21. Farina M., Avila D.S., da Rocha J.B.T., Aschner M. Metals, oxidative stress and neurodegeneration: A focus on iron, manganese and mercury. Neurochem. Int. 2013, 62:575-594.
22. Ivanković D., Pavicić J., Erk M., Filipović-Marijić V., Raspor B. 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. 2005, 50:1303-1313.
23. Mol S., Alakavuk D.U. Heavy metals in mussels (Mytilus galloprovincialis) from Marmara Sea, Turkey. Biol. Trace Elem. Res. 2011, 141:184-191.
24. Pellerin J., Amiard J.C. Comparison of bioaccumulation of metals and induction of metallothioneins in two marine bivalves (Mytilus edulis and Mya arenaria). Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2009, 150:186-195.
25. Luo W., Lu Y., Wang T., Kong P., Jiao W., Hu W., Jia J., Naile J.E., Khim J.S., Giesy J.P. Environmental concentrations and bioaccumulations of cadmium and zinc in coastal watersheds along the Chinese Northern Bohai and Yellow Seas. Environ. Toxicol. Chem. 2013, 32:831-840.
26. Rai U.N., Prasad D., Verma S., Upadhyay A.K., Singh N.K. Biomonitoring of metals in Ganga water at different ghats of Haridwar: implications of constructed wetland for sewage detoxification. Bull. Environ. Contam. Toxicol. 2012, 89:805-810.
27. Amado-Filho G.M., Salgado L.T., Rebelo M.F., Rezende C.E., Karez C.S., Pfeiffer W.C. Heavy metals in benthic organisms from Todos os Santos Bay, Brazil. Braz. J. Biol. 2008, 68:95-100.
28. Ivanković D., Pavičić J., Beatović V., Klobučar R.S., Klobučar G.I.V. Inducibility of metallothionein biosynthesis in the whole soft tissue of Zebra mussels Dreissena polymorpha exposed to cadmium, copper, and pentachlorophenol. Environ. Toxicol. 2010, 25:198-211.
29. Fang Y., Yang H., Wang T., Liu B., Zhao H., Chen M. Metallothionein and superoxide dismutase responses to sublethal cadmium exposure in the clam Mactra veneriformis. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2010, 151:325-333.
30. Baraj B., Niencheski F., Fillmann G., De Martinez G.M.C. Assessing the effects of Cu, Cd, and exposure period on metallothionein production in gills of the Brazilian brown mussel Perna perna by using factorial design. Environ. Monit. Assess. 2011, 179:155-162.
31. Geret F., Cosson R.P. Induction of specific isoforms of metallothionein in mussel tissues after exposure to cadmium or mercury. Arch. Environ. Contam. Toxicol. 2002, 42:36-42.
32. Bolognesi C., Landini E., Roggieri P., Fabbri R., Viarengo A. Genotoxicity biomarkers in the assessment of heavy metal effects in mussels: experimental studies. Environ. Mol. Mutagen. 1999, 33:287-292.
33. Georgiou C.D., Papapostolou I., Patsoukis N., Tsegenidis T., Sideris T. An ultrasensitive fluorescent assay for the in vivo quantification of superoxide radical in organisms. Anal. Biochem. 2005, 347:144-151.
34. Bradford M.M. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
35. Zamora R., Alaiz M., Hidalgo F.J. Feed-back inhibition of oxidative stress by oxidized lipid/amino acid reaction products. Biochemistry 1997, 36:15765-15771.
36. Bolognesi C., Fenech M. Mussel micronucleus cytome assay. Nat. Protoc. 2012, 7:1125-1137.
37. Viarengo A., Ponzano E., Dondero F., Fabbri R. A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic mollusks. Mar. Environ. Res. 1997, 44:69-84.
38. Moore M.N. Cellular responses to pollutants. Mar. Pollut. Bull. 1985, 16:134-139.
39. Kalpaxis D.L., Amarantos I., Tsibouxi A., Papapetropoulou M. Regulation of translation initiation in mussels (Mytilus galloprovincialis, lam.) following contamination stress. J. Toxicol. Environ. Health A 2003, 14:481-494.
40. MacKenzie A., Martin W. Loss of endothelium-derived nitric oxide in rabbit aorta by oxidant stress: restoration by superoxide dismutase mimetics. Br. J. Pharmacol. 1998, 124:719-728.
41. Huber K.R., Sridhar R., Griffith E.H., Amma E.L., Roberts J. Superoxide dismutase-like activities of copper(II) complexes tested in serum. Biochim. Biophys. Acta 1987, 915:267-276.
42. Soazig L., Marc L. Potential use of the levels of the mRNA of a specific metallothionein isoform (MT-20) in mussels (Mytilus edulis) as a biomarker of cadmium contamination. Mar. Pollut. Bull. 2003, 46:1450-1455.
43. Vergani L., Grattarola M., Grasselli E., Dondero F., Viarengo A. Molecular characterization and function analysis of MT-10 and MT-20 metallothionein isoforms from Mytilus galloprovincialis. Arch. Biochem. Biophys. 2007, 465:247-253.
44. Viarengo A., Palmero S., Zanicchi G., Capelli R., Orunesu M. Role of metallothioneins in Cu and Cd accumulation and elimination in the gill and digestive gland cells of Mytilus galloprovincialis Lam. Mar. Environ. Res. 1985, 16:23-36.
45. Roesijadi G. Metallothionein and its role in toxic metal regulation. Comp. Biochem. Physiol. C 1996, 113:117-123.
46. Banakou E., Dailianis S. Involvement of Na+/H+ exchanger and respiratory burst enzymes NADPH oxidase and NO synthase, in Cd-induced lipid peroxidation and DNA damage in haemocytes of mussels. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2010, 152:346-352.
47. Zhang H., Cai C., Shi C., Cao H., Han Z., Jia X. Cadmium-induced oxidative stress and apoptosis in the testes of frog Rana limnocharis. Aquat. Toxicol. 2012, 122-123:67-74.
48. Wang L., Xu T., Lei W.W., Liu D.M., Li Y.J., Xuan R.J., Ma J.J. Cadmium-induced oxidative stress and apoptotic changes in the testis of freshwater crab, Sinopotamon henanense. PLoS One 2011, 6:e27853.
49. Marshall R.A., Aitken C.E., Dorywalska M., Puglisi J.D. Translation at the single-molecule level. Annu. Rev. Biochem. 2008, 77:177-203.
50. Thompson D.M., Lu C., Green P.J., Parker R. tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA 2008, 14:2095-2103.
51. Hartwig A. Mechanisms in cadmium-induced carcinogenicity: recent insights. Biometals 2010, 23:951-960.
52. Dong J., Qiu H., Garcia-Barrio M., Anderson J., Hinnebusch A.G. Uncharged tRNA activates GCN2 by displacing the protein kinase moiety from a bipartite tRNA-binding domain. Mol. Cell 2000, 6:269-279.
53. Nelson A.R., Henkin T.M., Agris P.F. tRNA regulation of gene expression: interactions of an mRNA 5'-UTR with a regulatory tRNA. RNA 2006, 12:1254-1261.
54. Grant C.M. Regulation of translation by hydrogen peroxide. Antioxid. Redox Signal. 2011, 15:191-203.
55. Lee S.R., Collins K. Starvation-induced cleavage of the tRNA anticodon loop in Tetrahymena thermophila. J. Biol. Chem. 2005, 280:42744-42749.
56. Groppo R., Richter J.D. Translational control from head to tail. Curr. Opin. Cell Biol. 2009, 21:444-451.
57. Raught B., Gingras A.C Signaling to translation initiation. Translational Control in Biology and Medicine 2007, 369-400. Cold Spring Harbor Laboratory Press, New York. M.B. Mathews, N. Sonenberg, J.W.B. Hershey (Eds.).
58. Lewis S.S., Keller S.J. Identification of copper-responsive genes in an early stage of the fathead minnow Pimephales promelas. Ecotoxicology 2009, 18:281-292.
59. Othumpangat S., Kashon M., Joseph P. Eukaryotic translation initiation factor 4E is a cellular target for toxicity and death due to exposure to cadmium chloride. J. Biol. Chem. 2005, 280:25162-25169.
60. Sormani R., Delannoy E., Lageix S., Bitton F., Lanet E., Saez-Vasquez J., Deragon J.M., Renou J.P., Robaglia C. Sublethal cadmium intoxication in Arabidopsis thaliana impacts translation at multiple levels. Plant Cell Physiol. 2011, 52:436-447.
61. Olarewaju O., Ortiz P.A., Chowdhury W.Q., Chatterjee I., Kinzy T.G. The translocation elongation factor eEF1B plays a role in the oxidative stress response pathway. RNA Biol. 2004, 1:89-94.
62. Argüelles S., Machado A., Ayala A. Adduct formation of 4-hydroxynonenal and malondialdehyde with elongation factor-2 in vitro and in vivo. Free Radic. Biol. Med. 2009, 47:324-330.
63. White-Gilbertson S., Kurtz D.T., Voelkel-Johnson C. The role of protein synthesis in cell cycling and cancer. Mol. Oncol. 2009, 3:402-408.
64. Browne G.J., Proud C.G. Regulation of peptide-chain elongation in mammalian cells. Eur. J. Biochem. 2002, 269:5360-5368.