BioMetals

, Volume 23, Issue 5, pp 927–940

Cadmium stress: an oxidative challenge

  • Ann Cuypers
  • Michelle Plusquin
  • Tony Remans
  • Marijke Jozefczak
  • Els Keunen
  • Heidi Gielen
  • Kelly Opdenakker
  • Ambily Ravindran Nair
  • Elke Munters
  • Tom J. Artois
  • Tim Nawrot
  • Jaco Vangronsveld
  • Karen Smeets
Article

Abstract

At the cellular level, cadmium (Cd) induces both damaging and repair processes in which the cellular redox status plays a crucial role. Being not redox-active, Cd is unable to generate reactive oxygen species (ROS) directly, but Cd-induced oxidative stress is a common phenomenon observed in multiple studies. The current review gives an overview on Cd-induced ROS production and anti-oxidative defense in organisms under different Cd regimes. Moreover, the Cd-induced oxidative challenge is discussed with a focus on damage and signaling as downstream responses. Gathering these data, it was clear that oxidative stress related responses are affected during Cd stress, but the apparent discrepancies observed in between the different studies points towards the necessity to increase our knowledge on the spatial and temporal ROS signature under Cd stress. This information is essential in order to reveal the exact role of Cd-induced oxidative stress in the modulation of downstream responses under a diverse array of conditions.

Keywords

Cadmium Glutathione Oxidative stress Signaling Thiol Antioxidative defense Reactive oxygen species 

References

  1. Al-Nasser IA (2000) Cadmium hepatotoxicity and alterations of the mitochondrial function. Clin Toxicol 38:407–413CrossRefGoogle Scholar
  2. ATSDR (2005) Agency for Toxic Substance and Disease Registry, U.S. Toxicological Profile for Cadmium. Department of Health and Humans Services, Public Health Service, Centers for Disease Control, Atlanta, GAGoogle Scholar
  3. Babu KR, Rajmohan HRR, Rajan BKM et al (2006) Plasma lipid peroxidation and erythrocyte antioxidant enzymes status in workers exposed to cadmium. Toxicol Ind Health 22(8):329–335PubMedGoogle Scholar
  4. Barranco-Medina S, Lázaro J-L, Dietz K-J (2009) The oligomeric conformation of peroxiredoxins links redox state to function. FEBS Lett 583:1809–1816PubMedCrossRefGoogle Scholar
  5. Belyaeva EA, Korotkov SM (2003) Mechanism of primary Cd2+-induced rat liver mitochondria dysfunction: discrete modes of Cd2+ action on calcium and thiol-dependent domains. Toxicol Appl Pharm 192:56–68CrossRefGoogle Scholar
  6. Belyaeva EA, Glazunov VV, Korotkov SM (2002) Cyclosporin A-sensitive permeability transition pore is involved in Cd2+-induced dysfunction of isolated rat liver mitochondria: doubts no more. Arch Biochem Biophys 405:252–264PubMedCrossRefGoogle Scholar
  7. Belyaeva EA, Glazunov VV, Korotkov SM (2004) Cd2+ versus Ca2+-produced mitochondrial membrane permeabilization: a proposed direct participation of respiratory complexes I and III. Chem Biol Interact 150:253–270PubMedCrossRefGoogle Scholar
  8. Belyaeva EA, Dymkowska D, Więckowski MR et al (2006) Reactive oxygen species produced by the mitochondrial respiratory chain are involved in Cd2+-induced injury of rat ascites hepatoma AS-30D cells. Biochim Biophys Acta Bioenerg 1757:1568–1574CrossRefGoogle Scholar
  9. Belyaeva EA, Dymkowska D, Więckowski MR et al (2008) Mitochondria as an important target in heavy metal toxicity in rat hepatoma AS-30D cells. Toxicol Appl Pharm 231:34–42CrossRefGoogle Scholar
  10. Bertin G, Averbeck D (2006) Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). Biochimie 88:1549–1559PubMedCrossRefGoogle Scholar
  11. Biteau B, Labarre J, Toledano (2003) ATP-dependent reduction of cysteine–sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425:980–984PubMedCrossRefGoogle Scholar
  12. Bokoch GM, Knaus UG (2003) NADPH oxidases: not just for leukocytes anymore!. Trends Biochem Sci 28:502–508PubMedCrossRefGoogle Scholar
  13. Boveris A, Cadenas E, Stoppani AO (1976) Role of ubiquinone in the mitochondrial generation of hydrogen peroxide. Biochem J 156:435–444PubMedGoogle Scholar
  14. Brandao R, Weber Santos F, Oliveira R (2009) Involvement of non-enzymatic antioxidant defenses in the protective effect of diphenyl diselenide on testicular damage induced by cadmium in mice. J Trace Elem Med Biol 23:324–333PubMedCrossRefGoogle Scholar
  15. Brigelius-Flohe R (1999) Tissue-specific functions of individual glutathione peroxidases. Free Radic Biol Med 27(9–10):951–965PubMedCrossRefGoogle Scholar
  16. Cameron I, McNamee PM, Markham A et al (1986) The effects of cadmium on succinate and NADH-linked substrate oxidations in rat hepatic mitochondria. J Appl Toxicol 6:325–330PubMedCrossRefGoogle Scholar
  17. Casalino E, Sblano C, Landriscina C (1997) Enzyme activity alteration by cadmium administration to rats: the possibility of iron involvement in lipid peroxidation. Arch Biochem Biophys 346(2):171–179PubMedCrossRefGoogle Scholar
  18. Casalino E, Calzaretti G, Sblano C et al (2002) Molecular inhibitory mechanisms of antioxidant enzymes in rat liver and kidney by cadmium. Toxicology 179(1–2):37–50PubMedCrossRefGoogle Scholar
  19. Chatterjee S, Kundu S, Sengupta S et al (2009) Divergence to apoptosis from ROS induced cell cycle arrest: effect of cadmium. Mutat Res 663:22–31PubMedGoogle Scholar
  20. Chen L, Liu L, Huang S (2008) Cadmium activates the mitogen-activated protein kinase (MAPK) pathway via induction of reactive oxygen species and inhibition of protein phosphatases 2A and 5. Free Radic Biol Med 45:1035–1044PubMedCrossRefGoogle Scholar
  21. Coonse KG, Coonts AJ, Morrison EV et al (2007) Cadmium induces apoptosis in the human osteoblast-like cell line Saos-2. J Toxicol Environ Health A 70:575–581PubMedCrossRefGoogle Scholar
  22. Coutant A, Lebeau J, Bidon-Wagner N et al (2006) Cadmium-induced apoptosis in lymphoblastoid cell line: involvement of caspase-dependent and -independent pathways. Biochimie 88:1815–1822PubMedCrossRefGoogle Scholar
  23. Cuypers A, Smeets K, vangronsveld J (2009) Heavy metal stress in plants. In: Hirt H (ed) Plant stress biology. WILEY-VCH Verlag GmbH & Co., KGaA, Weinheim, pp 161–178CrossRefGoogle Scholar
  24. de Haan JB, Bladier C, Griffiths P et al (1998) Mice with a homozygous null mutation for the most abundant glutathione peroxidase, Gpx1, show increased susceptibility to the oxidative stress-inducing agents paraquat and hydrogen peroxide. J Biol Chem 273(35):22528–22536PubMedCrossRefGoogle Scholar
  25. Dickinson DA, Forman HJ (2002) Cellular glutathione and thiols metabolism. Biochem Pharmacol 64:1019–1026PubMedCrossRefGoogle Scholar
  26. Dorta DJ, Leite S, DeMarco KC et al (2003) A proposed sequence of events for cadmium-induced mitochondrial impairment. J Inorg Biochem 97:251–257PubMedCrossRefGoogle Scholar
  27. Dudley RE, Klaassen CD (1984) Changes in hepatic glutathione concentration modify cadmium-induced hepatotoxicity. Toxicol Appl Pharm 72(3):530–538CrossRefGoogle Scholar
  28. Early JL, Nonavinakere VK, Weaver A (1992) Effect of cadmium and/or selenium on liver mitochondria and rough endoplasmic reticulum in the rat. Toxicol Lett 62:73–83PubMedCrossRefGoogle Scholar
  29. El-Demerdash FM, Yousef MI, Kedwany FS et al (2004) Cadmium-induced changes in lipid peroxidation, blood hematology, biochemical parameters and semen quality of male rats: protective role of vitamin E and b-carotene. Food Chem Toxicol 42:1563–1571PubMedCrossRefGoogle Scholar
  30. Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress part 1: mechanisms involved in metal induced oxidative damage. Curr Top Med Chem 1:529–539PubMedCrossRefGoogle Scholar
  31. Erdogan Z, Erdogan S, Celik S et al (2005) Effects of ascorbic acid on cadmium-induced oxidative stress and performance of broilers. Biol Trace Elem Res 104(1):19–32PubMedCrossRefGoogle Scholar
  32. Fleury C, Mignotte B, Vayssière J-L (2002) Mitochondrial reactive oxygen species in cell death signalling. Biochimie 84:131–141PubMedCrossRefGoogle Scholar
  33. Fotakis G, Cemeli E, Anderson D et al (2005) Cadmium-chloride induced DNA and lysosomal damage in a hepatoma cell line. Toxicol In Vitro 19:481–489PubMedCrossRefGoogle Scholar
  34. Fowler BA (2009) Monitoring human populations for early markers of cadmium toxicity: a review. Toxicol Appl Pharm 238:294–300CrossRefGoogle Scholar
  35. Galán A, García-Bermejo L, Troyano A et al (2001) The role of intracellular oxidation in death induction (apoptosis and necrosis) in human promonocytic cells treated with stress inducers (cadmium, heat, X-rays). Eur J Cell Biol 80:312–320PubMedCrossRefGoogle Scholar
  36. Gao L, Laude K, Cai H (2008) Mitochondrial pathophysiology, reactive oxygen species, and cardiovascular diseases. Vet Clin North Am Small Anim Pract 38:137–155PubMedCrossRefGoogle Scholar
  37. Gong P, Chen FX, Ma GF et al (2008) Endomorphin 1 effectively protects cadmium chloride-induced hepatic damage in mice. Toxicology 251(1–3):35–44PubMedCrossRefGoogle Scholar
  38. Grosicki A (2004) Influence of vitamin C on cadmium absorption and distribution in rats. J Trace Elem Med Biol 18:183–187PubMedCrossRefGoogle Scholar
  39. Haberstroh KMW, Kapron CM (2006) Activation of c-Jun N-terminal kinase by cadmium in mouse embryo neural cells in vitro. Environ Toxicol Pharm 22(1):1–7CrossRefGoogle Scholar
  40. Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141(2):312–322PubMedCrossRefGoogle Scholar
  41. Hamada T, Tanimoto A, Sasaguri Y (1997) Apoptosis induced by cadmium. Apoptosis 2:359–367PubMedCrossRefGoogle Scholar
  42. Hansen JM, Zhang H, Jones DP (2006) Differential oxidation of thioredoxin 1, thioredoxin 2 and glutathione by metal ions. Free Radic Biol Med 40:138–145PubMedCrossRefGoogle Scholar
  43. Hart BA, Lee CH, Shukla A et al (1999) Characterization of cadmium-induced apoptosis in rat lung epithelial cells: evidence for the participation of oxidant stress. Toxicology 133:43–58PubMedCrossRefGoogle Scholar
  44. Hassoun EA, Stohs SJ (1996) Cadmium-induced production of superoxide anion and nitric oxide, DNA single strand breaks and lactate dehydrogenase leakage in J774A.1 cell cultures. Toxicology 112:219–226PubMedCrossRefGoogle Scholar
  45. Hispard F, de Vaufleury A, Martin H et al (2008) Effects of subchronic digestive exposure to organic or inorganic cadmium on biomarkers in rat tissues. Ecotoxicol Environ Saf 70(3):490–498PubMedCrossRefGoogle Scholar
  46. Hodkova A, Kotyzova R, Brtko J et al (2008) Influence of curcumin, resveratrol and sodium selenite on thioredoxin reductase, glutathione peroxidase and iodothyronine-5-deiodinase activity in rats—interaction with cadmium. Toxicol Lett 180S:S32–S246Google Scholar
  47. Hossain S, Liu H-N, Nguyen M et al (2009) Cadmium exposure induces mitochondria-dependent apoptosis in oligodendrocytes. Neurotoxicology 30:544–554PubMedCrossRefGoogle Scholar
  48. Huang T-T, Carlson EJ, Raineri I et al (1999) The use of transgenic and mutant mice to study oxygen free radical metabolism. Ann N Y Acad Sci 893:95–112PubMedCrossRefGoogle Scholar
  49. Hussain T, Shukla GS, Chandra GS (1987) Effects of cadmium on superoxide-dismutase and lipid-peroxidation in liver and kidney of growing rats—in vivo and in vitro studies. Pharmacol Toxicol 60(5):355–358PubMedCrossRefGoogle Scholar
  50. Ishido M, Ohtsubo R, Adachi T et al (2002) Attenuation of both apoptotic and necrotic actions of cadmium by Bcl-2. Environ Health Perspect 110:37–42PubMedCrossRefGoogle Scholar
  51. Jarup L, Åkesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharm 238(3):201–208CrossRefGoogle Scholar
  52. Jarup L, Berglund M, Elinder CG et al (1998) Health effects of cadmium exposure—a review on the literature and a risk estimate. Scand J Work Environ Health 24(S1):1–51PubMedGoogle Scholar
  53. Ježek P, Hlavatá L (2005) Mitochondria in homeostasis of reactive oxygen species in cell, tissues, and organism. Cell Physiol Biochem 37:2478–2503Google Scholar
  54. Jihen EH, Imed M, Fatima H et al (2009) Protective effects of selenium (Se) and zinc (Zn) on cadmium (Cd) toxicity in the liver of the rat: effects on the oxidative stress. Ecotoxicol Environ Saf 72(5):1559–1564CrossRefGoogle Scholar
  55. Jiménez I, Gotteland M, Zarzuelo A et al (1997) Loss of metal binding properties of metallothionein induced by hydrogen peroxide and free radicals. Toxicology 120(1):37–46PubMedCrossRefGoogle Scholar
  56. Jones DP, Go YM, Anderson CL et al (2004) Cysteine/cystine couple as a newly recognized node in the circuitry for biologic redox signaling and control. FASEB J 18:1246–1248PubMedGoogle Scholar
  57. Joseph P (2009) Mechanisms of cadmium carcinogenesis. Toxicol Appl Pharm 238(3):272–279CrossRefGoogle Scholar
  58. Jurczuk M, Brzoska MM, Moniuszko-Jakoniuk J et al (2004) Antioxidant enzymes activity and lipid peroxidation in liver and kidney of rats exposed to cadmium and ethanol. Food Chem Toxicol 42(3):429–438PubMedCrossRefGoogle Scholar
  59. Kamiyama T, Miyakawa H, Li JP et al (1995) Effects of one-year cadmium exposure on livers and kidneys and their relation to glutathione levels. Res Commun Pathol Pharmacol 88(2):177–186Google Scholar
  60. Kara H, Cevik A, Konar V et al (2008) Effects of selenium with vitamin E and melatonin on cadmium-induced oxidative damage in rat liver and kidneys. Biol Trace Elem Res 125(3):236–244PubMedCrossRefGoogle Scholar
  61. Karabulut-Bulan O, Bolkent S, Yanardag R et al (2008) The role of vitamin C, vitamin E, and selenium on cadmium-induced renal toxicity of rats. Drug Chem Toxicol 31(4):413–426PubMedCrossRefGoogle Scholar
  62. Kawata K, Shimazaki R, Okabe S (2009) Comparison of gene expression profiles in HepG2 cells exposed to arsenic, cadmium, nickel, and three model carcinogens for investigating the mechanisms of metal carcinogenesis. Environ Mol Mutagen 50:46–59PubMedCrossRefGoogle Scholar
  63. Kefaloyianni E, Gourgou E, Ferle V et al (2005) Acute thermal stress and various heavy metals induce tissue-specific pro- or anti-apoptotic events via the p38-MAPK signal transduction pathway in Mytilus galloprovincialis (Lam.). J Exp Biol 208(23):4427–4436PubMedCrossRefGoogle Scholar
  64. Kehrer JP (2000) The Haber–Weiss reaction and mechanisms of toxicity. Toxicology 149:43–50PubMedCrossRefGoogle Scholar
  65. Kidd P (1997) Glutathione: systemic protectant against oxidative and free radical damage. Altern Med Rev 2:155–176Google Scholar
  66. Kim JH, Dahms HU, Rhee JS et al (2010) Expression profiles of seven glutathione S-transferase (GST) genes in cadmium-exposed river pufferfish (Takifugu obscurus). Comp Biochem Physiol C Toxicol Pharm 151(1):99–106CrossRefGoogle Scholar
  67. Klaassen Cd, Liu J, Choudhuri S (1999) Metallothionein: an intracellular protein to protect against cadmium toxicity. Annu Rev Pharmacol Toxicol 39:267–294PubMedCrossRefGoogle Scholar
  68. Klaassen CD, Liu J, Diwan BA (2009) Metallothionein protection of cadmium toxicity. Toxicol Appl Pharm 238(3):215–220CrossRefGoogle Scholar
  69. Koizumi T, Yokota T, Shirakura H (1994) Potential mechanism of cadmium-induced cytotoxicity in rat hepatocytes: inhibitory action of cadmium on mitochondrial respiratory activity. Toxicology 92:115–125PubMedCrossRefGoogle Scholar
  70. Koizumi S, Gong PF, Suzuki K (2007) Cadmium-responsive element of the human heme oxygenase-1 gene mediates heat shock factor 1-dependent transcriptional activation. J Biol Chem 282(12):8715–8723PubMedCrossRefGoogle Scholar
  71. Kondoh M, Araragi S, Sato K et al (2002) Cadmium induces apoptosis partly via caspase-9 activation in HL-60 cells. Toxicology 170:111–117PubMedCrossRefGoogle Scholar
  72. Kotelnikova SV, Sokolova NG, Kotelnikov AV (2008) Lipid peroxidation in various organs and tissues of albino rats with cadmium intoxication in winter and summer. Bull Exp Biol Med 146(3):291–292PubMedCrossRefGoogle Scholar
  73. Krause KH (2004) Tissue distribution and putative physiological function of NOX family NADPH oxidases. Jpn J Infect Dis 57:S28–S29PubMedGoogle Scholar
  74. Lasfer M, Vadrot N, Aoudjehane L et al (2008) Cadmium induces mitochondria-dependent apoptosis of normal human hepatocytes. Cell Biol Toxicol 24:55–62PubMedCrossRefGoogle Scholar
  75. Lee W-K, Bork U, Thévenod F (2004) Mitochondria as a target of cadmium nephrotoxicity: induction of swelling and cytochrome c release. Toxicol Mech Methods 14:67–71PubMedCrossRefGoogle Scholar
  76. Lee W-K, Abouhamed M, Thévenod F (2006) Caspase-dependent and -independent pathways for cadmium-induced apoptosis in cultured kidney proximal tubule cells. Am J Physiol Renal Physiol 291:F823–F832PubMedCrossRefGoogle Scholar
  77. Lemarié A, Lagadic-Gossmann D, Morzadec C et al (2004) Cadmium induces caspase-independent apoptosis in liver Hep3B cells: role for calcium in signaling oxidative stress-related impairment of mitochondria and relocation of endonuclease G and apoptosis-inducing factor. Free Radic Biol Med 36:1517–1531PubMedCrossRefGoogle Scholar
  78. Li JM, Shah AM (2003) ROS generation by nonphagocytic NADPH oxidase: potential relevance in diabetic nephropathy. J Am Soc Nephrol 14:S221–S226PubMedCrossRefGoogle Scholar
  79. Li M, Kondo T, Zhao Q-L et al (2000) Apoptosis induced by cadmium in human lymphoma U937 cells through Ca2+-calpain and caspase-mitochondria-dependent pathways. J Biol Chem 275:39702–39709PubMedCrossRefGoogle Scholar
  80. Li GY, Kim M, Kim JH et al (2008) Gene expression profiling in human lung fibroblast following cadmium exposure. Food Chem Toxicol 46:1131–1137PubMedGoogle Scholar
  81. Linster CL, Van Schaftingen E (2007) Vitamin C. Biosynthesis, recycling, degradation in mammals. FEBS J 274(1):1–22PubMedCrossRefGoogle Scholar
  82. Liu J, Corton C, Dix DJ et al (2001) Genetic background, but not metallothionein phenotype dictates sensitivity to cadmium–induced testicular injury in mice. Toxicol Appl Pharm 176(1):1–9CrossRefGoogle Scholar
  83. Liu J, Kadiiska MB, Corton JC et al (2002) Acute cadmium exposure induces stress-related gene expression in wild-type and metallothionein-I/II null mice. Free Radic Biol Med 32:525–535PubMedCrossRefGoogle Scholar
  84. Liu J, Qu W, Kadiiska MB (2009) Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol Appl Pharm 238(3):209–214CrossRefGoogle Scholar
  85. Lopez E, Arce C, Oset-Gasque MJ et al (2006) Cadmium induces reactive oxygen species generation and lipid peroxidation in cortical neurons in culture. Free Radic Biol Med 40:940–951PubMedCrossRefGoogle Scholar
  86. Maret W, Vallee BL (1998) Thiolate ligands in metallothionein confer redox activity on zinc clusters. Proc Natl Acad Sci USA 95:3478–3482PubMedCrossRefGoogle Scholar
  87. Mates JM (2000) Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology. Biog Amines 16(1):53–62Google Scholar
  88. Matsuoka M, Igisu H (1998) Activation of c-Jun NH2-terminal kinase (JNK/SAPK) in LLC-PK1 cells by cadmium. Biochem Biophys Res Commun 251(2):527–532PubMedCrossRefGoogle Scholar
  89. Meyer Y, Siala W, Bashandy T et al (2008) Glutaredoxins and thioredoxins in plants. Biochim Biophys Acta 1783:589–600PubMedCrossRefGoogle Scholar
  90. Mittler R, Vanderauwera S, Gollery M et al (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9(10):490–498PubMedCrossRefGoogle Scholar
  91. Müller L (1986) Consequences of cadmium toxicity in rat hepatocytes: mitochondrial dysfunction and lipid peroxidation. Toxicology 40:285–295PubMedCrossRefGoogle Scholar
  92. Mustafa MG, Cross CE (1971) Pulmonary alveolar macrophage. Oxidative metabolism of isolated cells and mitochondria and effect of cadmium ion on electron- and energy-transfer reactions. Biochemistry 10:4176–4185PubMedCrossRefGoogle Scholar
  93. Nawrot TS, Van Hecke E, Thijs L et al (2008) Cadmium-related mortality and long-term secular trends in the cadmium body burden of an environmentally exposed population. Environ Health Perspect 116(12):1620–1628PubMedCrossRefGoogle Scholar
  94. Neumann C, Krause D, Carman C et al (2003) Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature 424(6948):561–565PubMedCrossRefGoogle Scholar
  95. Newairy AA, Ei-Sharaky AS, Badreldeen MM et al (2007) The hepatoprotective effects of selenium against cadmium toxicity in rats. Toxicology 242(1–3):23–30PubMedCrossRefGoogle Scholar
  96. Nishitai G, Matsuoka M (2008) Differential regulation of HSP70 expression by the JNK kinases SEK1 and MKK7 in mouse embryonic stem cells treated with cadmium. J Cell Biochem 104(5):1771–1780PubMedCrossRefGoogle Scholar
  97. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279PubMedCrossRefGoogle Scholar
  98. Nriagu J (1988) A silent killer of environmental metal poisoning. Environ Pollut 50(1–2):139–161PubMedCrossRefGoogle Scholar
  99. Ognjanovic BI, Pavlovic SZ, Maletic SD (2003) Protective influence of vitamin E on antioxidant defense system in the blood of rats treated with cadmium. Physiol Res 52(5):563–570PubMedGoogle Scholar
  100. Ognjanovic BI, Markovic SD, Pavlovic SZ et al (2008) Effect of chronic cadmium exposure on antioxidant defense system in some tissues of rats: protective effect of selenium. Physiol Res 57(3):403–411PubMedGoogle Scholar
  101. Oh SH, Lim S-C (2006) A rapid and transient ROS generation by cadmium triggers apoptosis via caspase-dependent pathway in HepG2 cells and this is inhibited through N-acetylcysteine-mediated catalase upregulation. Toxicol Appl Pharm 212:212–223CrossRefGoogle Scholar
  102. Oh MJ, Chae GY, Ahn KH (2009) Involvement of oxidised Peroxiredoxin-3 in cadmium- and ceramide-induced apoptosis of human neuroblastoma cells. J Health Sci 55(5):739–749CrossRefGoogle Scholar
  103. Packer L, Weber SU, Rimbach G (2001) Molecular aspects of alpha-tocotrienol antioxidant action and cell signalling. J Nutr 131(2):369S–373SPubMedGoogle Scholar
  104. Papadakis ES, Finegan KG, Wang X et al (2006) The regulation of Bax by c-Jun N-terminal protein kinase (JNK) is a prerequisite to the mitochondrial-induced apoptotic pathway. FEBS Lett 580(5):1320–1326PubMedCrossRefGoogle Scholar
  105. Pathak N, Khandelwal S (2006) Oxidative stress and apoptotic changes in murine splenocytes exposed to cadmium. Toxicology 220(1):26–36PubMedCrossRefGoogle Scholar
  106. Picaud T, Desbois A (2006) Interaction of glutathione reductase with heavy metal: the binding of Hg(II) or Cd(II) to the reduced enzyme affects both the redox dithiol pair and the flavin. Biochemistry 45:15829–15837PubMedCrossRefGoogle Scholar
  107. Poliandri AHB, Machiavelli LI, Quinteros AF et al (2006) Nitric oxide protects the mitochondria of anterior pituitary cells and prevents cadmium-induced cell death by reducing oxidative stress. Free Radic Biol Med 40:679–688PubMedCrossRefGoogle Scholar
  108. Qu W, Diwan BA, Reece JM et al (2005) Cadmium-induced malignant transformation in rat liver cells: role of aberrant oncogene expression and minimal role of oxidative stress. Int J Cancer 114(3):346–355PubMedCrossRefGoogle Scholar
  109. Qu W, Fuquay R, Sakurai T et al (2006) Acquisition of apoptotic resistance in cadmium-induced malignant transformation: specific perturbation of JNK signal transduction pathway and associated metallothionein overexpression. Mol Carcinog 45:561–571PubMedCrossRefGoogle Scholar
  110. Quinn MT, Ammons MCB, DeLeo FR (2006) The expanding role of NADPH oxidases in health and disease: no longer just agents of death and destruction. Clin Sci 111:1–20PubMedCrossRefGoogle Scholar
  111. Rana SV, Verma S (1996) Protective effects of GSH, vitamin E, and selenium on lipid peroxidation in cadmium fed rats. Biol Trace Elem Res 51(2):161–168PubMedCrossRefGoogle Scholar
  112. RC IA (1993) Cadmium and cadmium compounds. IARC Monographs. International Agency for research on Cancer, Lyon, FranceGoogle Scholar
  113. Renugadevi J, Prabu SM (2009) Naringenin protects against cadmium-induced oxidative renal dysfunction in rats. Toxicology 256(1–2):128–134PubMedCrossRefGoogle Scholar
  114. Rhee S, Chae H, Kim K (2005) Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signalling. Free Radic Biol Med 38(12):1543–1552PubMedCrossRefGoogle Scholar
  115. Rockwell P, Martinez J, Papa L et al (2004) Redox regulates COX-2 upregulation and cell death in the neuronal response to cadmium. Cell Signal 16:343–353PubMedCrossRefGoogle Scholar
  116. Salmeen A, Andersen JN, Myers MP et al (2003) Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423:769–773PubMedCrossRefGoogle Scholar
  117. Sancho P, Fernández C, Yuste VJ et al (2006) Regulation of apoptosis/necrosis execution in cadmium-treated human promonocytic cells under different forms of oxidative stress. Apoptosis 11:673–686PubMedCrossRefGoogle Scholar
  118. Schrader M, Fahimi HD (2004) Mammalian peroxisomes and reactive oxygen species. Histochem Cell Biol 122(4):383–393PubMedCrossRefGoogle Scholar
  119. Seifried HE, Anderson DE, Fisher EI et al (2007) A review of the interaction among dietary antioxidants and reactive oxygen species. Nutr Biochem 18:567–579CrossRefGoogle Scholar
  120. Sen Gupta R, Kim J, Gomes C et al (2004) Effect of ascorbic acid supplementation on testicular steroidogenesis and germ cell death in cadmium-treated male rats. Mol Cell Endocrinol 221(1–2):57–66PubMedCrossRefGoogle Scholar
  121. Sheader DL, Williams TD, Lyons BP et al (2006) Oxidative stress response of European flounder (Platichthys flesus) to cadmium determined by a custom cDNA microarray. Mar Environ Res 62:33–44PubMedCrossRefGoogle Scholar
  122. Shih C-M, Ko W-C, Wu J-S et al (2004) Mediating of caspase-independent apoptosis by cadmium through the mitochondria-ROS pathway in MRC-5 fibroblasts. J Cell Biochem 91:384–397PubMedCrossRefGoogle Scholar
  123. Sies H (1997) Impaired endothelial and smooth muscle cell function in oxidative stress. Exp Physiol 82:291–295PubMedGoogle Scholar
  124. Slyuzova OV, Stepanova EV, Temraleeva AD et al (2008) Effects of prenatal and neonatal cadmium intoxication on the intensity of lipid peroxidation and activity of glutathione system in progeny of albino rats. Bull Exp Biol Med 146(1):41–44PubMedCrossRefGoogle Scholar
  125. Souza V, Escobar MD, Gomez-Quiroz L et al (2004) Acute cadmium exposure enhances AP-1 DNA binding and induces cytokines expression and heat shock protein 70 in HepG2 cells. Toxicology 197(3):213–228PubMedCrossRefGoogle Scholar
  126. Souza V, Escobar M, Bucio L et al (2009) NADPH oxidase and ERK1/2 are involved in cadmium induced STAT3 activation in HepG2 cells. Toxicol Lett 187:180–186PubMedCrossRefGoogle Scholar
  127. Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336PubMedCrossRefGoogle Scholar
  128. Suzuki JS, Kodama N, Molotkov A et al (1998) Isolation and identification of metallothionein isoforms (MT-1 and MT-2) in the rat testis. Biochem J 334:695–701PubMedGoogle Scholar
  129. Szuster-Ciesielska A, Stachura A, Slotwinska M et al (2000) The inhibitory effect of zinc on cadmium-induced cell apoptosis and reactive oxygen species (ROS) production in cell cultures. Toxicology 145:159–171PubMedCrossRefGoogle Scholar
  130. Takahashi A, Masuda A, Sun M et al (2004) Oxidative stress-induced apoptosis is associated with alterations in mitochondrial caspase activity and Bcl-2-dependent alterations in mitochondrial pH (pHm). Brain Res Bull 62:497–504PubMedCrossRefGoogle Scholar
  131. Takeshige K, Minakami S (1979) NADH- and NADPH-dependent formation of superoxide anions by bovine heart submitochondrial particles and NADH-ubiquinone reductase preparation. Biochem J 180:129–135PubMedGoogle Scholar
  132. Tandon SK, Singh S, Prasad S (2003) Reversal of cadmium induced oxidative stress by chelating agent, antioxidant or their combination in rat. Toxicol Lett 145(3):211–217PubMedCrossRefGoogle Scholar
  133. Tang W, Shaikh ZA (2001) Renal cortical mitochondrial dysfunction upon cadmium metallothionein administration to Sprague-Dawley rats. J Toxicol Environ Health A 63:221–235PubMedCrossRefGoogle Scholar
  134. Thévenod F (2003) Nephrotoxicity and the proximal tubule: insights from cadmium. Nephron Physiol 93:87–93CrossRefGoogle Scholar
  135. Thévenod F (2009) Cadmium and cellular signaling cascades: to be or not to be? Toxicol Appl Pharm 238(3):221–239CrossRefGoogle Scholar
  136. Thévenod F, Friedmann JM, Katsen AD et al (2000) Up-regulation of multidrug resistance P-glycoprotein via nuclear factor-kappa B activation protects kidney proximal tubule cells from cadmium- and reactive oxygen species-induced apoptosis. J Appl Biol Chem 275:1887–1896Google Scholar
  137. Thijssen S, Cuypers A, Maringwa J et al (2007) Low cadmium exposure triggers a biphasic oxidative stress response in mice kidneys. Toxicology 236(1–2):29–41PubMedCrossRefGoogle Scholar
  138. Turrens JF, Alexandre A, Lehninger AL (1985) Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch Biochem Biophys 237:408–414PubMedCrossRefGoogle Scholar
  139. Vairavamurthy MA, Goldenber WS, Ouyang S et al (2000) The interaction of hydrophilic thiols with cadmium: investigation with a simple model, 3-mercaptopropionic acid. Mar Chem 70:181–189CrossRefGoogle Scholar
  140. Valbonesi P, Ricci L, Franzellitti S et al (2008) Effects of cadmium on MAPK signalling pathways and HSP70 expression in a human trophoblast cell line. Placenta 29(8):725–733PubMedCrossRefGoogle Scholar
  141. Valko M, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208PubMedCrossRefGoogle Scholar
  142. van Montfort RLM, Congreve M, Tisi D et al (2003) Oxidation state of the active-site cyteine in protein tyrosine phosphatase 1B. Nature 423:773–777PubMedCrossRefGoogle Scholar
  143. Vangronsveld J, Van Assche F, Clijsters H (1995) Reclamation of a bare industrial area contaminated by non-ferrous metals: in situ metal immobilization and revegetation. Environ Pollut 87:51–59PubMedCrossRefGoogle Scholar
  144. Waisberg M, Joseph P, Hale B et al (2003) Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192(2–3):95–117PubMedCrossRefGoogle Scholar
  145. Wang YD, Fang J, Leonard SS et al (2004) Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic Biol Med 36(11):1434–1443PubMedCrossRefGoogle Scholar
  146. Wang L, Cao J, Chen D et al (2009) Role of oxidative stress, apoptosis and intracellular homeostasis in primary cultures of rat proximal tubular cells exposed to cadmium. Biol Trace Elem Res 127:53–68PubMedCrossRefGoogle Scholar
  147. Winterbourn CC (1979) Comparison of superoxide with other reducing agents in the biological production of hydroxyl radicals. Biochem J 182:625–628PubMedGoogle Scholar
  148. Wronska-Nofer T, Wisniewska-Knypl J, Dziubaltowska E et al (1999) Prooxidative and genotoxic effect of transition metals (cadmium, nickel, chromium, and vanadium) in mice. Trace Elem Electrol 16(2):87–92Google Scholar
  149. Yalin S, Comelekoglu U, Bagis S et al (2006) Acute effect of single-dose cadmium treatment on lipid peroxidation and antioxidant enzymes in ovariectomized rats. Ecotoxicol Environ Saf 65(1):140–144PubMedCrossRefGoogle Scholar
  150. Yamada H, Uenishi R, Suzuki K et al (2009) Cadmium-induced alterations of gene expression in human cells. Environ Toxicol Pharm 28(1):61–69CrossRefGoogle Scholar
  151. Yang PM, Chen HC, Tsai JS et al (2007) Cadmium induces Ca2+-dependent necrotic cell death through calpain-triggered mitochondrial depolarization and reactive oxygen species-mediated inhibition of nuclear factor-kappa B activity. Chem Res Toxicol 20:406–415PubMedCrossRefGoogle Scholar
  152. Yeh J-H, Huang C-C, Yeh M-Y et al (2009) Cadmium-induced cytosolic Ca2+ elevation and subsequent apoptosis in renal tubular cells. Basic Clin Pharmacol Toxicol 104:345–351PubMedCrossRefGoogle Scholar
  153. Yiin SJ, Sheu JY, Lin TH (2000) Lipid peroxidation in rat adrenal glands after administration cadmium and role of essential metals. J Toxicol Environ Health A 62(1):47–56CrossRefGoogle Scholar
  154. Yokouchi M, Hiramatsu N, Hayakawa H et al (2008) Involvement of selective reactive oxygen species upstream of proapoptotic branches of unfolded protein response. J Biol Chem 283:4252–4260PubMedCrossRefGoogle Scholar
  155. Zalups RK, Ahmad S (2003) Molecular handling of cadmium in transporting epithelia. Toxicol Appl Pharm 186:163–188CrossRefGoogle Scholar
  156. Zhou YJ, Zhang SP, Liu CW et al (2009) The protection of selenium on ROS-mediated apoptosis by mitochondria dysfunction in cadmium-induced LLC-PK1 cells. Toxicol In Vitro 23(2):288–294PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2010

Authors and Affiliations

  • Ann Cuypers
    • 1
  • Michelle Plusquin
    • 1
  • Tony Remans
    • 1
  • Marijke Jozefczak
    • 1
  • Els Keunen
    • 1
  • Heidi Gielen
    • 1
  • Kelly Opdenakker
    • 1
  • Ambily Ravindran Nair
    • 1
  • Elke Munters
    • 1
  • Tom J. Artois
    • 1
  • Tim Nawrot
    • 1
  • Jaco Vangronsveld
    • 1
  • Karen Smeets
    • 1
  1. 1.Centre for Environmental SciencesHasselt UniversityDiepenbeekBelgium

Personalised recommendations