DNA Damage and Transcriptional Changes in the Gills of Mytilus galloprovincialis Exposed to Nanomolar Doses of Combined Metal Salts (Cd, Cu, Hg)

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Varotto, Laura ^a   Domeneghetti, Stefania ^a   Rosani, Umberto ^a   Manfrin, Chiara ^b   Cajaraville, Miren P ^c   Raccanelli, Stefano ^d   Pallavicini, Alberto ^b   Venier, Paola ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF TRIESTE   (Italy)

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

^d Chimico Ambientale   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; APOPTOSIS INHIBITOR; ARSENIC; CADMIUM; CHROMIUM; COPPER; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; MERCURY; THIONINE; TUBULIN; ZINC;

ARTICLE; ATOMIC ABSORPTION SPECTROMETRY; CONTROLLED STUDY; DNA DAMAGE; DNA MICROARRAY; DOWN REGULATION; GENE EXPRESSION PROFILING; GENOTOXICITY; GILL; MICRONUCLEUS; MUSSEL; MYTILUS GALLOPROVINCIALIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PROCESSING; RNA PURIFICATION; SPRING; TRANSCRIPTION INITIATION; UPREGULATION; WINTER;

ANIMALS; DNA DAMAGE; GENE EXPRESSION REGULATION; GILLS; METALS, HEAVY; MYTILUS; POISONING; TRANSCRIPTION, GENETIC;

MYTILUS GALLOPROVINCIALIS;

EID: 84872760743     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054602     Document Type: Article

References (95)

1. Goldberg ED, (1975) The Mussel Watch- a first step in global marine monitoring. Mar Pollut Bull 6: 111.
2. Nguyen TT, Hayes BJ, Guthridge K, Ab Rahim ES, Ingram BA, (2011) Use of a microsatellite-based pedigree in estimation of heritabilities for economic traits in Australian blue mussel, Mytilus galloprovincialis. J Anim Breed Genet 128(6): 482-90.
3. Lu Q, Hwang DS, Liu Y, Zeng H, (2012) Molecular interactions of mussel protective coating protein, mcfp-1, from Mytilus californianus. Biomaterials 33(6): 1903-11.
4. Connor KM, Gracey AY, (2011) Circadian cycles are the dominant transcriptional rhythm in the intertidal mussel Mytilus californianus. Proc Natl Acad Sci U S A 108(38): 16110-5.
5. Fields PA, Zuzow MJ, Tomanek L, (2012) Proteomic responses of blue mussel (Mytilus) congeners to temperature acclimation. J Exp Biol 215(Pt 7): 1106-16.
6. Philipp EE, Kraemer L, Melzner F, Poustka AJ, Thieme S, et al. (2012) Massively parallel RNA sequencing identifies a complex immune gene repertoire in the lophotrochozoan Mytilus edulis. PLoS One 7(3)e33091.
7. Place SP, Menge BA, Hofmann GE, (2012) Transcriptome profiles link environmental variation and physiological response of Mytilus californianus between Pacific tides. Funct Ecol 26(1): 144-155.
8. Cajaraville MP, Bebianno MJ, Blasco J, Porte C, Sarasquete C, et al. (2000) The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Sci Total Environ 247(2-3): 295-311.
9. Guéguen M, Amiard JC, Arnich N, Badot PM, Claisse D, et al. (2011) Shellfish and residual chemical contaminants: hazards, monitoring, and health risk assessment along French coasts. Rev Environ Contam Toxicol 213: 55-111.
10. Chapman PM, (2008) Environmental risks of inorganic metals and metalloids: A continuing, evolving scientific odyssey. Human Ecol Risk Assess 14(1): 5-40.
11. Lyons BP, Thain JE, Stentiford GD, Hylland K, Davies IM, et al. (2010) Using biological effects tools to define Good Environmental Status under the European Union Marine Strategy Framework Directive. Mar Pollut Bull 60(10): 1647-51.
12. Shaw JP, Dondero F, Moore MN, Negri A, Dagnino A, et al. (2011) Integration of biochemical, histochemical and toxicogenomic indices for the assessment of health status of mussels from the Tamar Estuary, U.K. Mar Environ Res. 72(1-2): 13-24.
13. Campos A, Tedesco S, Vasconcelos V, Cristobal S, (2012) Proteomic research in bivalves: Towards the identification of molecular markers of aquatic pollution. Proteomics 75(14): 4346-59.
14. Maret W, Copsey M, (2012) Metallomics: whence and whither. Metallomics 4(10): 1017-9.
15. Szefer P, Fowler SW, Ikuta K, Osuna FP, Ali AA, et al. (2006) A comparative assessment of heavy metal accumulation in soft parts and byssus of mussels from subarctic, temperate, subtropical and tropical marine environments. Environ Pollut 139(1): 70-8.
16. Kimbrough KL, Johnson WE, Lauenstein GG, Christensen JD, Apeti DA (2008) An Assessment of Two Decades of Contaminant Monitoring in the Nation's Coastal Zone. Silver Spring, MD. NOAA Technical Memorandum NOS NCCOS 74,105 pp. 105.
17. Veltman K, Huijbregts MA, Hendriks AJ, (2010) Integration of biotic ligand models (BLM) and bioaccumulation kinetics into a mechanistic framework for metal uptake in aquatic organisms. Environ Sci Technol 44(13): 5022-8.
18. Sakellari A, Karavoltsos S, Theodorou D, Dassenakis M, Scoullos M (2012) Bioaccumulation of metals (Cd, Cu, Zn) by the marine bivalves M. galloprovincialis, P. radiata, V. verrucosa and C. chione in Mediterranean coastal microenvironments: association with metal bioavailability. Environ Monit Assess (in press).
19. Nieboer E, Richardson DHS, (1980) The replacement of the non-descript term 'heavy metals' by a biologically and chemically significant classification of metal ions. Environ Pollut 1: 3-26.
20. Duffus JH, (2002) "Heavy metals" a meaningless term? (IUPAC Technical Report) Pure Appl Chem 74(5): 793-807.
21. Veltman K, Huijbregts MA, Van Kolck M, Wang WX, Hendriks AJ, (2008) Metal bioaccumulation in aquatic species: quantification of uptake and elimination rate constants using physicochemical properties of metals and physiological characteristics of species. Environ Sci Technol 42(3): 852-8.
22. Marigomez I, Soto M, Cajaraville MP, Angulo E, Giamberini L, (2002) Cellular and subcellular distribution of metals in molluscs. Microsc Res Tech 56: 358-92.
23. Cosson RP, Thiébaut E, (2008) Company R, Castrec-Rouelle M, Colaço A, et al (2008) Spatial variation of metal bioaccumulation in the hydrothermal vent mussel Bathymodiolus azoricus. Mar Environ Res 65(5): 405-15.
24. Kádár E, Santos RS, Powell JJ, (2006) Biological factors influencing tissue compartmentalization of trace metals in the deep-sea hydrothermal vent bivalve Bathymodiolus azoricus at geochemically distinct vent sites of the Mid-Atlantic Ridge. Environ Res 101(2): 221-9.
25. Gómez-Mendikute A, Elizondo M, Venier P, Cajaraville MP (2005) Characterization of mussel gill cells in vivo and in vitro. Cell Tissue Res 321(1), 131-40.
26. Domouhtsidou GP, Dimitriadis VK, (2000) Ultrastructural localization of heavy metals (Hg, Ag, Pb, and Cu) in gills and digestive gland of mussels, Mytilus galloprovincialis (L.). Arch Environ Contam Toxicol 38(4): 472-8.
27. Dimitriadis VK, Domouhtsidou GP, Raftopoulou E, (2003) Localization of Hg and Pb in the palps, the digestive gland and the gills in Mytilus galloprovincialis (L.) using autometallography and X-ray microanalysis. Environ Pollut 125(3): 345-53.
28. Zorita I, Ortiz-Zarragoitia M, Soto M, Cajaraville MP (2006) Biomarkers in mussels from a copper site gradient (Visnes, Norway): an integrated biochemical, histochemical and histological study. Aquat Toxicol (Suppl 1): S109-16.
29. Moore MN, Viarengo A, Donkin P, Hawkins AJ, (2007) Autophagic and lysosomal reactions to stress in the hepatopancreas of blue mussels. Aquat Toxicol 84(1): 80-91.
30. Wang WX, Rainbow PS, (2010) Significance of metallothioneins in metal accumulation kinetics in marine animals. Comp Biochem Physiol C Toxicol Pharmacol 152(1): 1-8.
31. Bolognesi C, Landini E, Roggieri P, Fabbri R, Viarengo A, (1999) Genotoxicity biomarkers in the assessment of heavy metal effects in mussels: experimental studies. Environ Mol Mutagen 33: 287-292.
32. Venier P, De Pittà C, Pallavicini A, Marsano F, Varotto L, et al. (2006) Development of mussel mRNA profiling: Can gene expression trends reveal coastal water pollution? Mutat Res 602: 121-134.
33. Sinicropi MS, Amantea D, Caruso A, Saturnino C, (2010) Chemical and biological properties of toxic metals and use of chelating agents for the pharmacological treatment of metal poisoning. Arch Toxicol 84(7): 501-20.
34. Syversen T, Kaur P, (2012) The toxicology of mercury and its compounds. J Trace Elem Med Biol 26(4): 215-26.
35. EC (2006) COMMISSION REGULATION (EC) No 1881/2006 of 19.12.2006. Setting maximum levels for certain contaminants in foodstuffs. Official Journal of the European Union, L 364/5-24. Accessed on line at http://eurlex.europa.eu.
36. EC (2008) COMMISSION REGULATION (EC) No 629/2008 of 2 July 2008. Amending Regulation (EC) No 1881/2006 setting maximum levels for certain contaminants infoodstuffs. Accessed on line at http://eurlex.europa.eu.
37. van Kolck M, Huijbregts MA, Veltman K, Jan Hendriks A, (2008) Estimating bioconcentration factors, lethal concentrations and critical body residues of metals in the mollusks Perna viridis and Mytilus edulis using ion characteristics. Environ Toxicol Chem 7(2): 272-6.
38. Neşer G, Kontas A, Unsalan D, Uluturhan E, Altay O, et al. (2012) Heavy metals contamination levels at the Coast of Aliaǧa (Turkey) ship recycling zone. Mar Pollut Bull 64(4): 882-7.
39. Balshaw S, Edwards J, Daughtry B, Ross K, (2007) Mercury in seafood: mechanisms of accumulation and consequences for consumer health. Rev Environ Health 22(2): 91-113.
40. Gutiérrez AJ, Lozano G, González T, Ignacio Reguera J, Hardisson A, (2006) Mercury content in tinned molluscs (mussel, cockle, variegated scallop, and razor shell) normally consumed in Spain, 2005. J Food Prot 69(9): 2237-40.
41. Comuzzi C, Lesa B, Aneggi E, Dolcetti G, Goi D, (2011) Salt-assisted thermal desorption of mercury from contaminated dredging sludge. J Hazard Mater 193: 177-82.
42. Lin Y, Vogt R, Larssen T, (2012) Environmental mercury in China: A review. Environ Toxicol Chem 31(11): 2431-2444.
43. Dolcetti L, Venier P, (2002) Susceptibility to genetic damage and cell types in Mediterranean mussels. Mar Environ Res 54(3-5): 487-491.
44. Venier P, Zampieron C, (2005) Evidence of genetic damage in grass gobies and mussels from the Venice lagoon. Environ Int 31(7): 1053-64.
45. Tusher VG, Tibshirani R, Chu G, (2001) Significance Analysis of Microarrays applied to the ionizing radiation exposure. Proc Natl Acad Sci USA 98(9): 5116-5121.
46. Storey JD, Tibshirani R, (2003) Statistical methods for identifying differentially expressed genes in DNA microarrays. Methods Mol Biol 224: 149-57.
47. Dysvik B, Jonassen I, (2001) J-Express: exploring gene expression data using Java. Bioinformatics 17(4): 369-70.
48. Venier P, De Pittà C, Bernante F, Varotto L, De Nardi B, et al. (2009) MytiBase: a knowledgebase of mussel (M. galloprovincialis) transcribed sequences. BMC Genomics 10: 72.
49. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17): 3389-402.
50. Conesa A, Götz S, (2008) Blast2GO: A comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008: 619832.
51. Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27-30. Available at http://www.genome.jp/kegg/pathway.html.
52. The Gene Ontology Consortium (2000) Gene ontology: tool for the unification of biology. Nat Genet 25(1): 25-9. Available at http://www.geneontology.org.
53. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, et al. (2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37: D211-5.
54. The Gene Ontology Consortium (2010). The Gene Ontology in 2010: extensions and refinements. Nucleic Acids Res 38(Database issue):D331-5.
55. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25: 402-408.
56. Dondero F, Piacentini L, Banni M, Rebelo M, Burlando B, et al. (2005) Quantitative PCR analysis of two molluscan metallothionein genes unveils differential expression and regulation. Gene 345: 259-270.
57. Besada V, Fumega J, Vaamonde A, (2002) Temporal trends of Cd, Cu, Hg, Pb and Zn in mussel (Mytilus galloprovincialis) from the Spanish North-Atlantic coast 1991-1999. Sci Total Environ 288(3): 239-53.
58. Raftopoulou EK, Dimitriadis VK, (2011) Comparative study of the accumulation and detoxification of Cu (essential metal) and Hg (nonessential metal) in the digestive gland and gills of mussels Mytilus galloprovincialis, using analytical and histochemical techniques. Chemosphere 83(8): 1155-65.
59. Bolognesi C, Hayashi M, (2011) Micronucleus assay in aquatic animals. Mutagenesis 26(1): 205-13.
60. Fernández B, Campillo JA, Martínez-Gómez C, Benedicto J, (2011) Micronuclei and other nuclear abnormalities in mussels (Mytilus galloprovincialis) as biomarkers of cyto-genotoxic pollution in mediterranean waters. Environ Mol Mutagen 52(6): 479-91.
61. Manfrin C, Dreos R, Battistella S, Beran A, Gerdol M, et al. (2010) Mediterranean mussel gene expression profile induced by okadaic acid exposure. Environ Sci Technol 44(21): 8276-83.
62. Domeneghetti S, Manfrin C, Varotto L, Rosani U, Gerdol M, et al. (2011) How gene expression profiles disclose vital processes and immune responses in Mytilus spp. ISJ 8: 179-189 DOI:1824-307X.
63. Pytharopoulou S, Grintzalis K, Sazakli E, Leotsinidis M, Georgiou CD, et al. (2011) Translational responses and oxidative stress of mussels experimentally exposed to Hg, Cu and Cd: one pattern does not fit at all. Aquat Toxicol 105(1-2): 157-65.
64. Gallo LI, Lagadari M, Piwien-Pilipuk G, Galigniana MD, (2011) The 90-kDa heat-shock protein (Hsp90)-binding immunophilin FKBP51 is a mitochondrial protein that translocates to the nucleus to protect cells against oxidative stress. J Biol Chem 286(34): 30152-60.
65. Abada PB, Larson CA, Manorek G, Adams P, Howell SB, (2012) Sec61β Controls Sensitivity to Platinum-Containing Chemotherapeutic Agents through Modulation of the Copper-Transporting ATPase ATP7A. Mol Pharmacol 82(3): 510-20.
66. Flora SJ, Mittal M, Mehta A, (2008) Heavy metal induced oxidative stress & its possible reversal by chelation therapy. Indian J Med Res 128(4): 501-23.
67. Takahashi S, (2012) Molecular functions of metallothionein and its role in hematological malignancies. J Hematol Oncol 5: 41.
68. Funk AE, Day FA, Brady FO, (1987) Displacement of zinc and copper from copper-induced metallothionein by cadmium and by mercury: in vivo and ex vivo studies. Comp Biochem Physiol C 86(1): 1-6.
69. Ba LA, Doering M, Burkholz T, Jacob C, (2009) Metal trafficking: from maintaining the metal homeostasis to future drug design. Metallomics 1(4): 292-311.
70. Aceto S, Formisano G, Carella F, De Vico G, Gaudio L, (2011) The metallothionein genes of Mytilus galloprovincialis: genomic organization, tissue expression and evolution. Mar Genomics 4(1): 61-8.
71. Strogyloudi E, Angelidis MO, Christides A, Papathanassiou E, (2012) Metal concentrations and metallothionein levels in Mytilus galloprovincialis from Elefsis bay (Saronikos gulf, Greece). Environ Monit Assess 184(12): 7189-205.
72. Vergani L, Grattarola M, Grasselli E, Dondero F, Viarengo A, (2007) Molecular characterization and function analysis of MT-10 and MT-20 metallothionein isoforms from Mytilus galloprovincialis. Arch Biochem Biophys 465(1): 247-53.
73. Zorita I, Bilbao E, Schad A, Cancio I, Soto M, et al. (2007) 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 220(2): 186-96.
74. Fasulo S, Mauceri A, Giannetto A, Maisano M, Bianchi N, et al. (2008) Expression of metallothionein mRNAs by in situ hybridization in the gills of Mytilus galloprovincialis, from natural polluted environments. Aquat Toxicol 88(1): 62-8.
75. Li J, Li L, Zhang S, Li J, Zhang G, (2012) Three ferritin subunits involved in immune defense from bay scallop Argopecten irradians. Fish Shellfish Immunol 32(2): 368-72.
76. Potrykus J, Kosakowska A, (2009) Purification and characterisation of ferritin from the Baltic blue mussel Mytilus trossulus. Oceanol 51(4): 525-539.
77. Gómez-Mendikute A, Cajaraville MP, (2003) Comparative effects of cadmium, copper, paraquat and benzo[a]pyrene on the actin cytoskeleton and production of reactive oxygen species (ROS) in mussel haemocytes. Toxicol In Vitro 17(5-6): 539-46.
78. Singh BK, Tripathi M, Pandey PK, Kakkar P, (2011) Alteration in mitochondrial thiol enhances calcium ion dependent membrane permeability transition and dysfunction in vitro: a cross-talk between mtThiol, Ca(2+), and ROS. Mol Cell Biochem 357(1-2): 373-85.
79. Auffret M, Rousseau S, Boutet I, Tanguy A, Baron J, et al. (2006) A multiparametric approach for monitoring immunotoxic responses in mussels from contaminated sites in Western Mediterranea. Ecotoxicol Environ Saf 63(3): 393-405.
80. Ahmad I, Coelho JP, Mohmood I, Pacheco M, Santos MA, et al. (2011) Immunosuppression in the infaunal bivalve Scrobicularia plana environmentally exposed to mercury and association with its accumulation. Chemosphere 82(11): 1541-6.
81. Thévenod F, (2009) Cadmium and cellular signaling cascades: to be or not to be? Toxicol Appl Pharmacol 1 238(3): 221-39.
82. Harrison JJ, Ceri H, Turner RJ, (2007) Multimetal resistance and tolerance in microbial biofilms. Nat Rev Microbiol 5(12): 928-38.
83. Winterbourn CC, Hampton MB, (2008) Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 45(5): 549-61.
84. Moulis JM, (2010) Cellular mechanisms of cadmium toxicity related to the homeostasis of essential metals. Biometals 23(5): 877-96.
85. Ueki T, Furuno N, Michibata H, (2011) A novel vanadium transporter of the Nramp family expressed at the vacuole of vanadium-accumulating cells of the ascidian Ascidia sydneiensis samea. Biochim Biophys Acta 1810(4): 457-64.
86. Soundararajan R, Lu M, Pearce D, (2012) Organization of the ENaC-regulatory machinery. Crit Rev Biochem Mol Biol 47(4): 349-59.
87. Dürrnagel S, Falkenburger BH, Gründer S, (2012) High Ca2+ permeability of a peptide-gated DEG/ENaC from Hydra. J Gen Physiol 140(4): 391-402.
88. Thévenod F, (2010) Catch me if you can! Novel aspects of cadmium transport in mammalian cells. Biometals 23(5): 857-75.
89. Sen A, Madhivanan K, Mukherjee D, Aguilar RC, (2012) The epsin protein family: coordinators of endocytosis and signaling. Biomol Concepts 3(2): 117-126.
90. Bury NR, Walker PA, Glover CN, (2003) Nutritive metal uptake in teleost fish. J Exp Biol 206(Pt 1): 11-23.
91. Marchi B, Burlando B, Moore MN, Viarengo A, (2004) Mercury- and copper-induced lysosomal membrane destabilisation depends on [Ca2+] dependent phospholipase A2 activation. Aquat Toxicol 10 66(2): 197-204.
92. Chervona Y, Costa M, (2012) The control of histone methylation and gene expression by oxidative stress, hypoxia, and metals. Free Radic Biol Med 53(5): 1041-7.
93. Greenough MA, Camakaris J, Bush AI (2012) Metal dyshomeostasis and oxidative stress in Alzheimer's disease. Neurochem Int (in press).
94. Kryston TB, Georgiev AB, Pissis P, Georgakilas AG, (2011) Role of oxidative stress and DNA damage in human carcinogenesis. Mutat Res 711(1-2): 193-201.
95. Voulgaridou GP, Anestopoulos I, Franco R, Panayiotidis MI, Pappa A, (2011) DNA damage induced by endogenous aldehydes: current state of knowledge. Mutat Res 711(1-2): 13-27.