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Alteration of Heart Tissue Protein Profiles in Acute Cadmium-Treated Scallops Patinopecten yessoensis

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Abstract

Cadmium (Cd) is an extremely toxic metal that induces a wide spectrum of toxic responses in organisms in the environment. In the present study, scallops (Patinopecten yessoensis), after acclimation for 1 week in the laboratory, were subjected to acute Cd chloride (CdCl2) toxicity, and ultramorphological and proteomic changes in their heart tissues were analyzed and compared with those of the nonexposed control group. Electron microscopy showed that ultrastructures of the cytoplasm and mitochondria in scallop hearts were badly damaged, and two-dimensional gel electrophoresis showed 32 protein spots that were differentially expressed after exposure to 10 mg/l CdCl2 for 24 h. Of these spots, 8 were upregulated, 16 were downregulated, and 8 showed low expression. Proteins from these spots were identified using matrix-assisted laser desorption/ionization-time of flight mass spectrometry and database searching. The results indicated that these proteins are involved in the regulation of cell structure, transport, signal transduction, and metabolism. Among other things, four proteins―identified as amino acid adenosine triphosphate (ATP)–binding cassette transporter, glycerol-3-phosphate dehydrogenase (nicotinamide adenine dinucleotide phosphate), nicotinamide adenine dinucleotide oxidase, and ATPase―were demonstrated to be especially associated with Cd toxicity. Some of the other proteins observed in this work are of particular interest in terms of their responses to Cd, which have not been reported previously. These data may provide novel biomarkers for monitoring the Cd contamination level of flowing seawater as well as provide useful insights into the mechanisms of Cd toxicity.

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References

  • Atli G, Canli M (2007) Enzymatic responses to metal exposures in a freshwater fish Oreochromis niloticus. Comp Biochem Physiol C: Toxicol Pharmacol 145:282–287

    Article  Google Scholar 

  • Beard SJ, Hughes MN, Poole RK (1995) Inhibition of the cytochrome bo’-terminated NADH oxidase system in Escherichia coli K-12 by divalent metal cations. FEMS Microbiol Lett 131:205–210

    Article  CAS  Google Scholar 

  • Bebianno MJ, Serafim MA (2003) Variation of metal and metallothionein concentrations in a natural population of Ruditapes decussates. Arch Environ Contam Toxicol 44:53–66

    Article  CAS  Google Scholar 

  • Berrada W, Naya A, Iddar A (2002) Purification and characterization of cytosolic glycerol-3-phosphate dehydrogenase from skeletal muscle of jerboa (Jaculus orientalis). Mol Cell Biochem 231:117–127

    Article  CAS  Google Scholar 

  • Bissell MJ, Rambeck WA, White RC, Bassham JA (1976) Glycerol phosphate shuttle in virus-transformed cells in culture. Science 191:856–858

    Article  CAS  Google Scholar 

  • Bovet L, Feller U, Martinoia E (2005) Possible involvement of plant ABC transporters in cadmium detoxification: a cDNA sub-microarray approach. Environ Int 31:263–267

    Article  CAS  Google Scholar 

  • Canli M, Stagg RM (1996) The effects of in vivo exposure to cadmium, copper, and zinc on the activities of gill ATPases in the Norway lobster Nephrops norvegicus. Arch Environ Contam Toxicol 31:491–501

    Article  Google Scholar 

  • Daud MK, Sun YQ, Dawood M (2009) Cadmium-induced functional and ultrastructural alterations in roots of two transgenic cotton cultivars. J Hazard Mater 161:463–473

    Article  CAS  Google Scholar 

  • de Zwart M, van der Goot H, Timmerman H (1991) Influence of Co(II), Ni(II), Cu(II), Zn(II) and Cd(II) on growth inhibition and enzyme activity of Mycoplasma gallisepticum in the absence or presence of a 2, 2′-bipyridyl type ligand. Eur J Med Chem 26:101–108

    Article  Google Scholar 

  • Dudley RE, Svoboda DJ, Klaassen CD (1984) Time course of cadmium-induced ultrastructural changes in rat liver. Toxicol Appl Pharmacol 76:150–160

    Article  CAS  Google Scholar 

  • Erman JE, Vitello LB (2002) Yeast cytochrome c peroxidase: mechanistic studies via protein engineering. Biochim Biophys Acta 1597:193–220

    Article  CAS  Google Scholar 

  • Everett CJ, Frithsen IL (2008) Association of urinary cadmium and myocardial infarction. Environ Res 106:284–286

    Article  CAS  Google Scholar 

  • Feng LJ, Huang L, Zhuo HQ, Huang HQ (2008) Differential proteins of Panax notoginseng powder inducement identified and analyzed with proteomic techniques in neural connective of Aplysia. Chin J Anal Chem 36:577–582

    Article  CAS  Google Scholar 

  • Fernandez EL, Gustafson AL, Andersson M, Hellman B, Dencker L (2003) Cadmium-induced changes in apoptotic gene expression levels and DNA damage in mouse embryos are blocked by zinc. Toxicol Sci 76:162–170

    Article  CAS  Google Scholar 

  • Gaisser HD, Vries JD, Van Der Goot H, Timmerman H (1987) Inhibition of NADH oxidase and lactate dehydrogenase of Mycoplasma gallisepticum by copper complexes of 2,2′-bipyridyl analogues. Biochem Pharmacol 36:3237–3241

    Article  CAS  Google Scholar 

  • Géret F, Serafim A, Barreira L, Bebianno MJ (2002) Effect of cadmium on antioxidant enzyme activities and lipid peroxidation in the gills of the clam Ruditapes decussates. Biomarkers 7:242–256

    Article  Google Scholar 

  • Grosell M, Wood CM, Walsh PJ (2003) Copper homeostasis and toxicity in the elasmobranch Raja erinacea and the teleost Myoxocephalus octodecemspinosus during exposure to elevated water-borne copper. Comp Biochem Physiol C: Toxicol Pharmacol 135:179–190

    Article  Google Scholar 

  • He XQ, Chen MG, Ma Q (2008) Activation of Nrf2 in defense against cadmium-induced oxidative stress. Chem Res Toxicol 21:1375–1383

    Article  CAS  Google Scholar 

  • Higgins CF (2001) ABC transporters: physiology, structure and mechanism―an overview. Res Microbiol 152:205–210

    Article  CAS  Google Scholar 

  • Jamall IS, Smith JC (1985) Effects of cadmium on glutathione peroxidase, superoxide dismutase, and lipid peroxidation in the rat heart: a possible mechanism of cadmium cardiotoxicity. Toxicol Appl Pharmacol 80:33–42

    Article  CAS  Google Scholar 

  • Jin XF, Yang X, Islam E (2008) Effects of cadmium on ultrastructure and antioxidative defense system in hyperaccumulator and non-hyperaccumulator ecotypes of Sedum alfredii Hance. J Hazard Mater 156:387–397

    Article  CAS  Google Scholar 

  • Lau ATY, Chiu JF (2007) The possible role of cytokeratin 8 in cadmium-induced adaptation and carcinogenesis. Cancer Res 67:2107–2113

    Article  CAS  Google Scholar 

  • Limaye DA, Shaikh ZA (1999) Cytotoxicity of cadmium and characteristics of its transport in cardiomyocytes. Toxicol Appl Pharmacol 154:59–66

    Article  CAS  Google Scholar 

  • Ling XP, Zhu JY, Huang L, Huang HQ (2009) Proteomic changes in response to acute cadmium toxicity in gill tissue of Paralichthys olivaceus. Environ Toxicol Pharmacol 27:212–218

    Article  CAS  Google Scholar 

  • Lionetto MG, Giordano ME, Vilella S, Schettino T (2000) Inhibition of eel enzymatic activities by cadmium. Aquat Toxicol 48:561–571

    Article  CAS  Google Scholar 

  • Maret W, Yetman CA, Jiang LJ (2001) Enzyme regulation by reversible zinc inhibition: glycerol phosphate dehydrogenase as an example. Chem Biol Interact 130–132:891–901

    Article  Google Scholar 

  • Matz CJ, Krone PH (2007) Cell death, stress-responsive transgene activation, and deficits in the olfactory system of larval zebrafish following cadmium exposure. Environ Sci Technol 41:5143–5148

    Article  CAS  Google Scholar 

  • Nagya Z, Montignya C, Leverrier P (2006) Role of the yeast ABC transporter Yor1p in cadmium detoxification. Biochimie 88:1665–1671

    Article  Google Scholar 

  • Navas-Acien A, Silbergeld EK, Sharrett R, Calderon-Aranda E, Selvin E, Guallar E (2005) Metals in urine and peripheral arterial disease. Environ Health Perspect 113:164–169

    Article  CAS  Google Scholar 

  • O’Brien P, Salasinski HJ (1998) Evidence that the reactions of cadmium in the presence of metallothionein can produce hydroxyl radicals. Arch Toxicol 72:690–700

    Article  Google Scholar 

  • Ognjanovi BI, Markovi SD, Pavlovi SZ, Zikic RV, Stajn SA, Saicic ZS (2006) Combined effects of coenzyme Q10 and vitamin E in cadmium induced alterations of antioxidant defense system in the rat heart. Environ Toxicol Pharmacol 22:219–224

    Article  Google Scholar 

  • Park HJ, Reiser COA, Kondruweit S, Erdmann H, Schmid RD, Sprinzl M (1992) Purification and characterization of a NADH oxidase from the thermophile Thermus thermophilus HB8. Eur J Biochem 205:887–893

    Article  Google Scholar 

  • Pettersen AJ, Andersen R, Zachariassen KE (2002) Effects of dietary intake of trace metals on tissue contents of sodium and calcium in mice (Mus musculus). Comp Biochem Physiol C: Toxicol Pharmacol 132:53–60

    Article  Google Scholar 

  • Prozialeck WC, Edwards JR, Woods JM (2006) The vascular endothelium as a target of cadmium toxicity. Life Sci 79:1493–1506

    Article  CAS  Google Scholar 

  • Quig D (1998) Cysteine metabolism and metal toxicity. Altern Med Rev 3:262–270

    CAS  Google Scholar 

  • Rea PA, Li ZS, Lu YP, Drozdowicz YM, Martinoia E (1998) From vacuole GS-X pumps to multispecific ABC transporters. Annu Rev Plant Physiol Plant Mol Biol 49:727–760

    Article  CAS  Google Scholar 

  • Risso-de Faverney C, Devaux A, Lafaurie M, Girard JP, Bailly B, Rahmani R (2001) Cadmium induces apoptosis and genotoxicity in rainbow trout hepatocytes through generation of reactive oxygen species. Aquat Toxicol 53:65–76

    Article  CAS  Google Scholar 

  • Ross RP, Claiborne A (1992) Molecular cloning and analysis of the gene encoding the NADH oxidase from Streptococcus faecalis 10C1: comparison with NADH peroxidase and the flavoprotein disulfide reductases. J Mol Biol 227:658–671

    Article  CAS  Google Scholar 

  • Rustichelli C, Visioli G, Kostecka D (2008) Proteomic analysis in the lichen Physcia adscendens exposed to cadmium stress. Environ Pollut 156:1121–1127

    Article  CAS  Google Scholar 

  • Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336

    Article  CAS  Google Scholar 

  • Stohs SJ, Bagchi D, Hassoun E, Bagchi M (2001) Oxidative mechanisms in the toxicity of chromium and cadmium ions. J Environ Pathol Toxicol Oncol 20:77–88

    CAS  Google Scholar 

  • Suresh A, Sivaramakrishna B, Radhakrishnaiah K (1995) Cadmium induced changes in ion levels and ATPase activities in the muscle of the fry and fingerlings of the freshwater fish, Cyprinus carpio. Chemosphere 30:367–375

    Article  CAS  Google Scholar 

  • Surin BP, Rosenberg H, Cox GB (1985) Phosphate-specific transport system of Escherichia coli: nucleotide sequence and gene-polypeptide relationships. J Bacteriol 161:189–198

    CAS  Google Scholar 

  • Thevenod F, Friedmann JM (1999) Cadmium-mediated oxidative stress in kidney proximal tubule cells induces degradation of Na+/K+-ATPase through proteasomal and endo-/lysosomal proteolytic pathways. FASEB J 13:1751–1761

    CAS  Google Scholar 

  • Tomera JF, Lilford K, Kukulka SP, Friend KD, Harakal C (1994) Divalent cations in hypertension with implications to heart disease: calcium, cadmium interactions. Methods Find Exp Clin Pharmacol 16:97–107

    CAS  Google Scholar 

  • Toury R, Biossanneau E, Stelly N, Dupuis Y, Berville A, Perasso R (1985) Mitochondria alteration in Cd treated rats: general regression of inner membrane cristae and electron transport impairment. Biol Cell 55:71–85

    CAS  Google Scholar 

  • Vallee BL, Ulmer D (1972) Biochemical effects of mercury, cadmium, and lead. Annu Rev Biochem 41:91–128

    Article  CAS  Google Scholar 

  • Varoni MV, Palomba D, Gianorso S, Anania V (2003) Cadmium as an environmental factor of hypertension in animals: new perspectives on mechanisms. Vet Res Commun 27:807–810

    Article  Google Scholar 

  • Waisberg M, Joseph P, Hale B, Beyersmann D (2003) Molecular and cellular mechanisms of cadmium carcinogenesis: a review. Toxicology 192:95–117

    Article  CAS  Google Scholar 

  • Yu XZ, Hong SW, Faustman EM (2008) Cadmium-induced activation of stress signaling pathways: disruption of ubiquitin-dependent protein degradation and apoptosis in primary rat sertoli cell-gonocyte cocultures. Toxicol Sci 104:385–396

    Article  CAS  Google Scholar 

  • Zhuo HQ, Jin HW, Huang HQ, Huang HY, Cai ZW (2007) Stability and splitting produces revealed by matrix-assisted laser desorption ionization-time of flight-mass spectrometry in human serum transferrin. Chin J Anal Chem 35:791–796

    Article  CAS  Google Scholar 

  • Zyadah MA, Abdel-Baky TE (2000) Toxicity and bioaccumulation of copper, zinc, and cadmium in some aquatic organisms. Bull Environ Contam Toxicol 64:740–747

    Article  CAS  Google Scholar 

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Acknowledgments

This work was funded by grants from the State Natural Science Fund (Grants No. 30870515 and 40776060) and 973 Projects (No. 2010CB12640), China. We thank John Hodgkiss for assistance with the English in this manuscript.

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Correspondence to He-Qing Huang.

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Huang, QY., Fang, CW. & Huang, HQ. Alteration of Heart Tissue Protein Profiles in Acute Cadmium-Treated Scallops Patinopecten yessoensis . Arch Environ Contam Toxicol 60, 90–98 (2011). https://doi.org/10.1007/s00244-010-9533-2

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