Zinc causes acute impairment of glutathione metabolism followed by coordinated antioxidant defenses amplification in gills of brown mussels Perna perna

Comparative Biochemistry and Physiology - C Toxicology and Pharmacology

Volumn 159, Issue 1, 2014, Pages 22-30

  Trevisan, Rafael ^a   Flesch, Samira ^a   Mattos, Jacó Joaquim ^a   Milani, Márcio Raimundo ^b   Bainy, Afonso Celso Dias ^a   Dafre, Alcir Luiz ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b FEDERAL UNIVERSITY OF RIO GRANDE   (Brazil)

Author keywords

Bivalves; Glutathione reductase; Metal; Oxidative stress; Peroxiredoxin; Thiol

Indexed keywords

CATALASE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; PEROXIREDOXIN 6; SUPEROXIDE DISMUTASE; ZINC CHLORIDE;

ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; GILL; GLUTATHIONE METABOLISM; HOMEOSTASIS; IMMUNOBLOTTING; LIPID PEROXIDATION; NONHUMAN; OXIDATIVE STRESS; PERNA PERNA; PRIORITY JOURNAL;

BIVALVIA; PERNA PERNA;

BIVALVES; GLUTATHIONE REDUCTASE; METAL; OXIDATIVE STRESS; PEROXIREDOXIN; THIOL;

ANIMALS; ANTIOXIDANTS; BIVALVIA; CHLORIDES; GILLS; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; LIPID PEROXIDATION; METALS, HEAVY; PERNA; PEROXIREDOXIN VI; POISONING; SUPEROXIDE DISMUTASE; ZINC COMPOUNDS;

EID: 84886457506     PISSN: 15320456     EISSN: 18781659     Source Type: Journal    
DOI: 10.1016/j.cbpc.2013.09.007     Document Type: Article

References (97)

1. H. Aebi Catalase in vitro Methods Enzymol. 105 1984 121 126
2. I. Ahmad, I. Mohmood, J.P. Coelho, M. Pacheco, M.A. Santos, A.C. Duarte, and E. Pereira Role of non-enzymatic antioxidants on the bivalves' adaptation to environmental mercury: organ-specificities and age effect in Scrobicularia plana inhabiting a contaminated lagoon Environ. Pollut. 163 2012 218 225
3. T.P. Akerboom, and H. Sies Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples Methods Enzymol. 77 1981 373 382
4. J. Alexander, J. Aeseth, and T. Refsvik Excretion of zinc in rat bile - a role of glutathione Acta Pharmacol. Toxicol. 49 1981 190 194 (Pubitemid 11022922)
5. S.N. Al-Subiai, A.J. Moody, S.A. Mustafa, and A.N. Jha A multiple biomarker approach to investigate the effects of copper on the marine bivalve mollusc, Mytilus edulis Ecotoxicol. Environ. Saf. 74 2011 1913 1920
6. E.S. Arnér, L. Zhong, and A. Holmgren Preparation and assay of mammalian thioredoxin and thioredoxin reductase Methods Enzymol. 300 1999 226 239
7. M.-M. Azevedo, A. Carvalho, C. Pascoal, F. Rodrigues, and F. Cássio Responses of antioxidant defenses to Cu and Zn stress in two aquatic fungi Sci. Total Environ. 377 2007 233 243 (Pubitemid 46660964)
8. A.C. Bainy, E.A. Almeida, I.C. Müller, E.C. Ventura, and I.D. Medeiros Biochemical responses in farmed mussel Perna perna transplanted to contaminated sites on Santa Catarina Island, SC, Brazil Mar. Environ. Res. 50 2000 411 416
9. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
10. P.S. Brocardo, F. Assini, J.L. Franco, P. Pandolfo, Y.M. Müller, R.N. Takahashi, A.L. Dafre, and A.L. Rodrigues Zinc attenuates malathion-induced depressant-like behavior and confers neuroprotection in the rat brain Toxicol. Sci. 97 2007 140 148 (Pubitemid 47072163)
11. M. Candas, R.S. Sohal, S.N. Radyuk, V.I. Klichko, and W.C. Orr Molecular organization of the glutathione reductase gene in Drosophila melanogaster Arch. Biochem. Biophys. 339 1997 323 334 (Pubitemid 27199977)
12. M. Capasso, J.-M. Jeng, M. Malavolta, E. Mocchegiani, and S.L. Sensi Zinc dyshomeostasis: a key modulator of neuronal injury J. Alzheimers Dis. 8 2005 93 108 (discussion 209-215) (Pubitemid 43230132)
13. I. Carlberg, and B. Mannervik Glutathione reductase Methods Enzymol. 113 1985 484 490 (Pubitemid 16195819)
14. C.T. Chasapis, A.C. Loutsidou, C.A. Spiliopoulou, and M.E. Stefanidou Arch. Toxicol. 86 2012 521 534
15. S. Chatterjee, S.I. Feinstein, C. Dodia, E. Sorokina, Y.-C. Lien, S. Nguyen, K. Debolt, D. Speicher, and A.B. Fisher Peroxiredoxin 6 phosphorylation and subsequent phospholipase A2 activity are required for agonist-mediated activation of NADPH oxidase in mouse pulmonary microvascular endothelium and alveolar macrophages J. Biol. Chem. 286 2011 11696 11706
16. B.-C. Chen, W.-Y. Chen, Y.-R. Ju, J.-W. Tsai, L.-J. Jou, S. Singh, and C.-M. Liao Combining bioaccumulation and coping mechanism to enhance long-term site-specific risk assessment for zinc susceptibility of bivalves Chemosphere 84 2011 707 715
17. H. Choi, J.-W. Chang, and Y.-K. Jung Peroxiredoxin 6 interferes with TRAIL-induced death-inducing signalling complex formation by binding to death effector domain caspase Cell Death Differ. 18 2011 405 414
18. K. Chong, and W.X. Wang Comparative studies on the biokinetics of Cd, Cr, and Zn in the green mussel Perna viridis and the Manila clam Ruditapes philippinarum Environ. Pollut. 1987 115 2001 107 121 (Pubitemid 32816312)
19. S. Cooper, L. Hare, and P.G. Campbell Subcellular partitioning of cadmium in the freshwater bivalve, Pyganodon grandis, after separate short-term exposures to waterborne or diet-borne metal Aquat. Toxicol. 100 2010 303 312
20. M.M. Cortese, C.V. Suschek, W. Wetzel, K.-D. Kröncke, and V. Kolb-Bachofen Zinc protects endothelial cells from hydrogen peroxide via Nrf2-dependent stimulation of glutathione biosynthesis Free Radic. Biol. Med. 44 2008 2002 2012
21. A.L. Dafre, I.D. Medeiros, I.C. Müller, E.C. Ventura, and A.C.D. Bainy Antioxidant enzymes and thiol/disulfide status in the digestive gland of the brown mussel Perna perna exposed to lead and paraquat Chem. Biol. Interact. 149 2004 97 105 (Pubitemid 39387213)
22. J. Dap, Q. Liu, H. Hong, and L. Wang Accumulation of lead and zinc and effects on activities of catalase and GPT in the clam Ruditapes philippinarum A Toxicol. Environ. Chem. 67 1998 351 361 (Pubitemid 29062443)
23. E. David, A. Tanguy, and D. Moraga Peroxiredoxin 6 gene: a new physiological and genetic indicator of multiple environmental stress response in Pacific oyster Crassostrea gigas Aquat. Toxicol. 84 2007 389 398 (Pubitemid 47259540)
24. E.A. De Almeida, S. Miyamoto, A.C.D. Bainy, M.H.G. de Medeiros, and P. Di Mascio Protective effect of phospholipid hydroperoxide glutathione peroxidase (PHGPx) against lipid peroxidation in mussels Perna perna exposed to different metals Mar. Pollut. Bull. 49 2004 386 392 (Pubitemid 39485712)
25. M. De Zoysa, W.A. Pushpamali, I. Whang, S.J. Kim, and J. Lee Mitochondrial thioredoxin-2 from disk abalone (Haliotis discus discus): molecular characterization, tissue expression and DNA protection activity of its recombinant protein Comp. Biochem. Physiol. B 149 2008 630 639
26. M. De Zoysa, I. Whang, Y. Lee, S. Lee, J.-S. Lee, and J. Lee Transcriptional analysis of antioxidant and immune defense genes in disk abalone (Haliotis discus discus) during thermal, low-salinity and hypoxic stress Comp. Biochem. Physiol. B 154 2009 387 395
27. V.U. Devi Bio-accumulation and metabolic effects of zinc on marine fouling dreissinid bivalve, Mytilopsis sallei (Recluz) Water Air Soil Pollut. 81 1995 295 304 (Pubitemid 26450633)
28. A. Devos, C. Voiseux, C. Caplat, and B. Fievet Effect of chronic exposure to zinc in young spats of the Pacific oyster (Crassostrea gigas) Environ. Toxicol. Chem. 31 2012 2841 2847
29. G.L. Ellman Tissue sulfhydryl groups Arch. Biochem. Biophys. 82 1959 70 77
30. S. Fathallah, M.N. Medhioub, A. Medhioub, and M.M. Kraiem Toxicity of Hg, Cu and Zn on early developmental stages of the European clam (Ruditapes decussatus) with potential application in marine water quality assessment Environ. Monit. Assess. 171 2010 661 669
31. M. Filipiak, G. Tylko, and E. Pyza Zinc induces caspase-dependent mitochondrial pathway of the programmed cell death in haemocytes of Drosophila melanogaster Biometals 25 2012 507 516
32. A. Formigari, P. Irato, and A. Santon Zinc, antioxidant systems and metallothionein in metal mediated-apoptosis: biochemical and cytochemical aspects Comp. Biochem. Physiol. C Toxicol. Pharmacol. 146 2007 443 459 (Pubitemid 47494685)
33. J.L. Franco, D.B.B. Trivella, R. Trevisan, D.F. Dinslaken, M.R.F. Marques, A.C.D. Bainy, and A.L. Dafre Antioxidant status and stress proteins in the gills of the brown mussel Perna perna exposed to zinc Chem. Biol. Interact. 160 2006 232 240
34. J.L. Franco, T. Posser, P.S. Brocardo, R. Trevisan, M. Uliano-Silva, N.H. Gabilan, A.R.S. Santos, R.B. Leal, A.L.S. Rodrigues, M. Farina, and A.L. Dafre Involvement of glutathione, ERK1/2 phosphorylation and BDNF expression in the antidepressant-like effect of zinc in rats Behav. Brain Res. 188 2008 316 323
35. J.L. Franco, T. Posser, J.J. Mattos, A. Sánchez-Chardi, R. Trevisan, C.S. Oliveira, P.S.M. Carvalho, R.B. Leal, M.R.F. Marques, A.C.D. Bainy, and A.L. Dafre Biochemical alterations in juvenile carp (Cyprinus carpio) exposed to zinc: glutathione reductase as a target Mar. Environ. Res. 66 2008 88 89
36. J.L. Franco, R. Trevisan, T. Posser, D.B.B. Trivella, R. Hoppe, J. Martins Rosa, D. Fernandes Dinslaken, H. Decker, C. Inês Tasca, R. Bainy Leal, M.R. Freire Marques, A.C. Dias Bainy, and A. Luiz Dafre Biochemical alterations in caged Nile tilapia Oreochromis niloticus Ecotoxicol. Environ. Saf. 73 2010 864 872
37. M. Freitas, G. Porto, J.L.F.C. Lima, and E. Fernandes Zinc activates neutrophils' oxidative burst Biometals 23 2010 31 41
38. E.M. García, J.J. Cruz-Motta, O. Farina, and C. Bastidas Anthropogenic influences on heavy metals across marine habitats in the western coast of Venezuela Cont. Shelf Res. 28 2008 2757 2766
39. C.A. Gay, and J.M. Gebicki Perchloric acid enhances sensitivity and reproducibility of the ferric-xylenol orange peroxide assay Anal. Biochem. 304 2002 42 46 (Pubitemid 34492841)
40. I.G. Gazaryan, I.P. Krasinskaya, B.S. Kristal, and A.M. Brown Zinc irreversibly damages major enzymes of energy production and antioxidant defense prior to mitochondrial permeability transition J. Biol. Chem. 282 2007 24373 24380 (Pubitemid 47328020)
41. S.G. George, and B.J.S. Pirie Metabolism of zinc in the mussel, Mytilus edulis (L.): a combined ultrastructural and biochemical study J. Mar. Biol. Assoc. 60 1980 575 590
42. F. Geret, and M.J. Bebianno Does zinc produce reactive oxygen species in Ruditapes decussatus? Ecotoxicol. Environ. Saf. 57 2004 399 409 (Pubitemid 38376273)
43. Y.M. Go, and D.P. Jones Thiol/disulfide redox states in signaling and sensing Crit. Rev. Biochem. Mol. Biol. 48 2013 173 181
44. T.J. Green, T.J. Dixon, E. Devic, R.D. Adlard, and A.C. Barnes Differential expression of genes encoding anti-oxidant enzymes in Sydney rock oysters, Saccostrea glomerata (Gould) selected for disease resistance Fish Shellfish Immunol. 26 2009 799 810
45. Z. Gregus, A.F. Stein, F. Varga, and C.D. Klaassen Effect of lipoic acid on biliary excretion of glutathione and metals Toxicol. Appl. Pharmacol. 114 1992 88 96
46. V. Gunther, U. Lindert, and W. Schaffner The taste of heavy metals: gene regulation by MTF-1 Biochim. Biophys. Acta 1823 2012 1416 1425
47. W.H. Habig, and W.B. Jakoby Assays for differentiation of glutathione S-transferases Methods Enzymol. 77 1981 398 405
48. B.H. Hansen, S. Rømma, ∅.A. Garmo, P.A. Olsvik, and R.A. Andersen Antioxidative stress proteins and their gene expression in brown trout (Salmo trutta) from three rivers with different heavy metal levels Comp. Biochem. Physiol. C 143 2006 263 274 (Pubitemid 44209079)
49. N.W. Kahn, S.L. Rea, S. Moyle, A. Kell, and T.E. Johnson Proteasomal dysfunction activates the transcription factor SKN-1 and produces a selective oxidative-stress response in Caenorhabditis elegans Biochem. J. 409 2008 205 213
50. A. Lafaye, C. Junot, Y. Pereira, G. Lagniel, J.-C. Tabet, E. Ezan, and J. Labarre Combined proteome and metabolite-profiling analyses reveal surprising insights into yeast sulfur metabolism J. Biol. Chem. 280 2005 24723 24730 (Pubitemid 40934561)
51. L. Li, M. Kobayashi, H. Kaneko, Y. Nakajima-Takagi, Y. Nakayama, and M. Yamamoto Molecular evolution of Keap1. Two Keap1 molecules with distinctive intervening region structures are conserved among fish J. Biol. Chem. 283 2008 3248 3255
52. E. Loumaye, G. Ferrer-Sueta, B. Alvarez, J.-F. Rees, A. Clippe, B. Knoops, R. Radi, and M. Trujillo Kinetic studies of peroxiredoxin 6 from Arenicola marina: rapid oxidation by hydrogen peroxide and peroxynitrite but lack of reduction by hydrogen sulfide Arch. Biochem. Biophys. 514 2011 1 7
53. J. Maher, and M. Yamamoto The rise of antioxidant signalling - the evolution and hormetic actions of Nrf2 Toxicol. Appl. Pharmacol. 244 2010 4 15
54. R.M. Martínez-Álvarez, A.E. Morales, and A. Sanz Antioxidant defenses in fish: biotic and abiotic factors Rev. Fish Biol. Fish. 15 2005 75 88 (Pubitemid 43012773)
55. J.M. McCord, and I. Fridovich Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein) J. Biol. Chem. 244 1969 6049 6055
56. C.E. Mize, and R.G. Langdon Hepatic glutathione reductase. I. Purification and general kinetic properties J. Biol. Chem. 237 1962 1589 1595
57. S.R. Nadella, J.L. Fitzpatrick, N. Franklin, C. Bucking, S. Smith, and C.M. Wood Toxicity of dissolved Cu, Zn, Ni and Cd to developing embryos of the blue mussel (Mytilus trossolus) and the protective effect of dissolved organic carbon Comp. Biochem. Physiol. C 149 2009 340 348
58. T.Y. Ng, and W.X. Wang Dynamics of metal subcellular distribution and its relationship with metal uptake in marine mussels Environ. Toxicol. Chem. 24 2005 2365 2372 (Pubitemid 41191770)
59. H. Ohkawa, N. Ohishi, and K. Yagi Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction Anal. Biochem. 95 1979 351 358 (Pubitemid 9194347)
60. O.K. Okamoto, E. Pinto, L.R. Latorre, E.J. Bechara, and P. Colepicolo Antioxidant modulation in response to metal-induced oxidative stress in algal chloroplasts Arch. Environ. Contam. Toxicol. 40 2001 18 24 (Pubitemid 34240900)
61. P.I. Oteiza Zinc and the modulation of redox homeostasis Free Radic. Biol. Med. 53 2012 1748 1759
62. P.I. Oteiza, and G.G. Mackenzie Zinc, oxidant-triggered cell signaling, and human health Mol. Aspects Med. 26 2005 245 255 (Pubitemid 41226495)
63. H. Park, I.-Y. Ahn, H. Kim, J. Cheon, and M. Kim Analysis of ESTs and expression of two peroxiredoxins in the thermally stressed Antarctic bivalve Laternula elliptica Fish Shellfish Immunol. 25 2008 550 559
64. S. Pavlica, F. Gaunitz, and R. Gebhardt Comparative in vitro toxicity of seven zinc-salts towards neuronal PC12 cells Toxicol. in Vitro 23 2009 653 659
65. J. Pellerin, and J.C. Amiard Comparison of bioaccumulation of metals and induction of metallothioneins in two marine bivalves (Mytilus edulis and Mya arenaria) Comp. Biochem. Physiol. C Toxicol. Pharmacol. 150 2009 186 195
66. M. Premanathan, K. Karthikeyan, K. Jeyasubramanian, and G. Manivannan Selective toxicity of ZnO nanoparticles toward gram-positive bacteria and cancer cells by apoptosis through lipid peroxidation Nanomedicine 7 2011 184 192
67. J. Qiu, Y. Liu, M. Yu, Z. Pang, W. Chen, and Z. Xu Identification and functional characterization of MRE-binding transcription factor (MTF) in Crassostrea gigas and its conserved role in metal-induced response Mol. Biol. Rep. 40 2013 3321 3331
68. M.A. Radwan, K.S. El-Gendy, and A.F. Gad Oxidative stress biomarkers in the digestive gland of Theba pisana exposed to heavy metals Arch. Environ. Contam. Toxicol. 58 2010 828 835
69. M.F. Rebelo, W.C. Pfeiffer, H. da Silva Jr., and M.O. Moraes Cloning and detection of metallothionein mRNA by RT-PCR in mangrove oysters (Crassostrea rhizophorae) Aquat. Toxicol. 64 2003 359 362 (Pubitemid 36808798)
70. C. Riva, A. Binelli, F. Rusconi, G. Colombo, A. Pedriali, R. Zippel, and A. Provini A proteomic study using zebra mussels (D. polymorpha) exposed to benzo(α)pyrene: the role of gender and exposure concentrations Aquat. Toxicol. 104 2011 14 22
71. E. Rudolf, and M. Cervinka Zinc pyrithione induces cellular stress signalling and apoptosis in Hep-2 cervical tumor cells: the role of mitochondria and lysosomes Biometals 23 2010 339 354
72. S.E. Sabatini, I. Rocchetta, D.E. Nahabedian, C.M. Luquet, M.R. Eppis, L. Bianchi, and M. del C. Ríos de Molina Oxidative stress and histological alterations produced by dietary copper in the fresh water bivalve Diplodon chilensis Comp. Biochem. Physiol. C 154 2011 391 398
73. F.J. Sánchez-Martín, E. Valera, I. Casimiro, and J.M. Merino Nerve growth factor increases the sensitivity to zinc toxicity and induces cell cycle arrest in PC12 cells Brain Res. Bull. 81 2010 458 466
74. J.S. Seo, K.-W. Lee, J.-S. Rhee, D.-S. Hwang, Y.-M. Lee, H.G. Park, I.-Y. Ahn, and J.-S. Lee Environmental stressors (salinity, heavy metals, H2O2) modulate expression of glutathione reductase (GR) gene from the intertidal copepod Tigriopus japonicus Aquat. Toxicol. 80 2006 281 289 (Pubitemid 44739061)
75. A. Serafim, and M.J. Bebianno Involvement of metallothionein in Zn accumulation and elimination strategies in Ruditapes decussatus Arch. Environ. Contam. Toxicol. 52 2007 189 199 (Pubitemid 44974279)
76. V. Sharma, D. Anderson, and A. Dhawan Zinc oxide nanoparticles induce oxidative stress and genotoxicity in human liver cells (HepG2) J. Biomed. Nanotechnol. 7 2011 98 99
77. M.S. Sharpley, and J. Hirst The inhibition of mitochondrial complex I (NADH:ubiquinone oxidoreductase) by Zn2 + J. Biol. Chem. 281 2006 34803 34809 (Pubitemid 46036519)
78. D. Shi, and W.-X. Wang Understanding the differences in Cd and Zn bioaccumulation and subcellular storage among different populations of marine clams Environ. Sci. Technol. 38 2004 449 456 (Pubitemid 38095473)
79. H. Sies Oxidative stress: introductory remarks H. Sies, Oxidative Stress 1985 Academic Press London 1 8
80. S. Srinivasa Gowd, and P.K. Govil Distribution of heavy metals in surface water of Ranipet industrial area in Tamil Nadu, India Environ. Monit. Assess. 136 2008 197 207 (Pubitemid 350182723)
81. G.P. Sykiotis, and D. Bohmann Keap1/Nrf2 signalling regulates oxidative stress tolerance and lifespan in Drosophila Dev. Cell 14 2008 76 85
82. S. Toppo, L. Flohé, F. Ursini, S. Vanin, and M. Maiorino Catalytic mechanisms and specificities of glutathione peroxidases: variations of a basic scheme Biochim. Biophys. Acta 1790 2009 1486 1500
83. R. Trevisan, D.F. Mello, A.S. Fisher, P.-M. Schuwerack, A.L. Dafre, and A.J. Moody Selenium in water enhances antioxidant defenses and protects against copper-induced DNA damage in the blue mussel Mytilus edulis Aquat. Toxicol. 101 2011 64 71
84. R. Trevisan, M. Arl, C.L. Sacchet, C.S. Engel, N.M. Danielli, D.F. Mello, C. Brocardo, A.F. Maris, and A.L. Dafre Antioxidant deficit in gills of Pacific oyster (Crassostrea gigas) exposed to chlorodinitrobenzene increases menadione toxicity Aquat. Toxicol. 108 2012 85 93
85. B.N. Tripathi, and J.P. Gaur Relationship between copper- and zinc-induced oxidative stress and proline accumulation in Scenedesmus sp Planta 219 2004 397 404 (Pubitemid 39027027)
86. T. Vlahogianni, M. Dassenakis, M.J. Scoullos, and A. Valavanidis Integrated use of biomarkers (superoxide dismutase, catalase and lipid peroxidation) in mussels Mytilus galloprovincialis for assessing heavy metals' pollution in coastal areas from the Saronikos Gulf of Greece Mar. Pollut. Bull. 54 2007 1361 1371
87. J. Voets, E.S. Redeker, R. Blust, and L. Bervoets Differences in metal sequestration between zebra mussels from clean and polluted field locations Aquat. Toxicol. 93 2009 53 60
88. N. Wakabayashi, S.L. Slocum, J.J. Skoko, S. Shin, and T.W. Kensler When NRF2 talks, who's listening? Antioxid. Redox Signal. 13 2010 1649 1663
89. W.X. Wang Comparison of metal uptake rate and absorption efficiency in marine bivalves Environ. Toxicol. Chem. 20 2001 1367 1373
90. A. Wendel Glutathione peroxidase Methods Enzymol. 77 1981 325 333
91. Filho D. Wilhelm, T. Tribess, C. Gaspari, F.D. Claudio, M.A. Torres, and A.R.M. Magalhaes Seasonal changes in antioxidant defenses of the digestive gland of the brown mussel (Perna perna) Aquaculture 203 2001 149 158 (Pubitemid 33141619)
92. G.W. Winston Oxidants and antioxidants in aquatic animals Comp. Biochem. Physiol. C 100 1991 173 176
93. C.C. Winterbourn, and M.B. Hampton Thiol chemistry and specificity in redox signaling Free Radic. Biol. Med. 45 2008 549 561
94. D.A. Wiseman, S. Sharma, and S.M. Black Elevated zinc induces endothelial apoptosis via disruption of glutathione metabolism: role of the ADP translocator Biometals 23 2010 19 30
95. C.K. Wong, R.Y. Cheung, and M.H. Wong Heavy metal concentrations in green-lipped mussels collected from Tolo Harbour and markets in Hong Kong and Shenzhen Environ. Pollut. 109 2000 165 171 (Pubitemid 30163054)
96. T. Xia, M. Kovochich, M. Liong, L. Mädler, B. Gilbert, H. Shi, J.I. Yeh, J.I. Zink, and A.E. Nel Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties Acs Nano 2 2008 2121 2134
97. C.K. Yap, A. Ismail, H. Omar, and S.G. Tan Toxicities and tolerances of Cd, Cu, Pb and Zn in a primary producer (Isochrysis galbana) and in a primary consumer (Perna viridis) Environ. Int. 29 2004 1097 1104 (Pubitemid 38145701)