Cadmium-induced oxidative damages in the human BJAB cells correlate with changes in intracellular trace elements levels and zinc transporters expression

Toxicology in Vitro

Volumn 37, Issue , 2016, Pages 169-177

  Nemmiche, Saïd ^a   Guiraud, Pascale ^b  

^a UNIVERSITY OF MOSTAGANEM   (Algeria)

^b UNIVERSITÉ DE LA RÉUNION   (France)

Author keywords

BJAB cells; Cadmium; DMT1; MTF1; Zinc transporters

Indexed keywords

CADMIUM CHLORIDE; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; MALONALDEHYDE; MANGANESE SUPEROXIDE DISMUTASE; METALLOTHIONEIN; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; SUPEROXIDE DISMUTASE; TRACE ELEMENT; UNCLASSIFIED DRUG; ZINC TRANSPORTER; ZINC TRANSPORTER 1; 8-OXO-7-HYDRODEOXYGUANOSINE; CALCIUM CHANNEL T TYPE; CATION TRANSPORT PROTEIN; DEOXYGUANOSINE; HEAVY METAL; SELENIUM;

ARTICLE; B LYMPHOCYTE; BIOACCUMULATION; BJAB CELL LINE; CELL DAMAGE; CELL LEVEL; CELL MEDIATED CYTOTOXICITY; CELL METABOLISM; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; INCUBATION TIME; OXIDATION; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; ANALOGS AND DERIVATIVES; CELL SURVIVAL; DRUG EFFECTS; GENETICS; METABOLISM; TUMOR CELL LINE;

CALCIUM CHANNELS, T-TYPE; CATALASE; CATION TRANSPORT PROTEINS; CELL LINE, TUMOR; CELL SURVIVAL; DEOXYGUANOSINE; DNA DAMAGE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; HUMANS; MALONDIALDEHYDE; METALS, HEAVY; OXIDATIVE STRESS; SELENIUM; SUPEROXIDE DISMUTASE;

EID: 84992183688     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2016.09.014     Document Type: Article

References (53)

1. Akerboom, T.P., Sies, H., Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples. Methods Enzymol. 77 (1981), 373–382.
2. Bannon, D.I., Roger, A., Lees Peter, S.J., Bressler, J.P., Effect of DMT1 knockdown on iron, cadmium, and lead uptake in Caco-2 cells. Am J Physiol Cell Physiol 284 (2003), 44–50.
3. Baselt, R., Disposition of Toxic Drugs and Chemicals in Man. 8th edition, 2008, Biomedical Publications, Foster City, CA, 212–214.
4. Beers, R.F., Sizer, I.W., A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem. 195 (1952), 133–139.
5. Besecker, B.Y., Exline, M.C., Hollyfield, J., Phillips, G., Disilvestro, R.A., Wewers, M.D., Knoell, D.L., A comparison of zinc metabolism, inflammation, and disease severity in critically ill infected and noninfected adults early after intensive care unit admission. Am. J. Clin. Nutr. 93 (2011), 1356–1364.
6. Bridges, C.C., Zalups, R.K., Molecular and ionic mimicry and the transport of toxic metals. Toxicol. Appl. Pharmacol. 204 (2005), 274–308.
7. Chang, X., Jin, T., Chen, L., et al. Metallothionein I isoform mRNA expression in peripheral lymphocytes as a biomarker for occupational cadmium exposure. Exp. Biol. Med. 234 (2009), 666–672.
8. Cousins, R.J., Liuzzi, J.P., Lichten, L.A., Mammalian zinc transport, trafficking, and signals. J. Biol. Chem. 281 (2006), 24085–24089.
9. Endo, T., Kimura, O., Saitoh, H., Sakata, M., Secretory transport of cadmium through intestinal brush border membrane via H +-antiport. Toxicology 150 (2000), 129–136.
10. Filipic, M., Mechanisms of cadmium induced genomic instability. Mutat. Res.: Fundam. Mol. Mech. Mutagen., 2011, 10.1016/j.mrfmmm.2011.09.002.
11. Flohe, L., Gunzler, W.A., Assays of glutathione peroxidase. Methods Enzymol. 105 (1984), 114–121.
12. Fujishiro, H., Doi, M., Enomotobc, S., Himeno, S., High sensitivity of RBL-2H3 cells to cadmium and manganese: an implication of the role of ZIP8. Metallomics, 2011, 10.1039/c1mt00020a.
13. Gedik, C.M., Collins, A., Establishing the background level of base oxidation in human lymphocyte DNA: results of an interlaboratory validation study. FASEB J. 19 (2005), 82–84.
14. Giaginis, C., Gatzidou, E., Theocharis, S., DNA repair systems as targets of cadmium toxicity. Toxicol. Appl. Pharmacol. 213 (2006), 282–290.
15. Giedroc, D.P., Chen, X., Apuy, J.L., Metal response element (MRE) binding transcription factor-1 (MTF-1): structure, function, and regulation. Antioxid. Redox Signal. 3 (2001), 577–596.
16. Haase, H., Ober-Blöbaum, J.L., Engelhardt, G., Hebel, S., Rink, L., Cadmium ions induce monocytic production of tumor necrosis factor-alpha by inhibiting mitogen activated protein kinase dephosphorylation. Toxicol. Letters 198 (2010), 152–158.
17. He L, Wang B, Hay EB, Nebert D. W. (2009). Discovery of ZIP transporters that participate in cadmium damage to testis and kidney. Toxicol. Appl. Pharmacol. 238, 250–257.
18. IARC, International Agency for Research on Cancer, Monographs on the Evaluation of the Carcinogenic Risks to Humans, Beryllium, Cadmium, Mercury and Exposures in the Glass Manufacturing Industry. 1993, IARC Scientific Publications, Lyon, France, 119–238.
19. Jackson, K.A., Helston, R.M., McKay, J.A., O'Neill, E.D., Mathers, J.C., Ford, D., Splice variants of the human zinc transporter ZnT5 (SLC30A5) are differentially localized and regulated by zinc through transcription and mRNA stability. J. Biol. Chem. 282 (2007), 10423–10431.
20. Kitamura, H., Morikawa, H., Kamon, H., Iguchi, M., Hojyo, S., Fukada, T., Yamashita, S., Kaisho, T., Akira, S., Murakami, M., Hirano, T., Toll-like receptor-mediated regulation of zinc homeostasis influences dendritic cell function. Nat. Immunol. 7 (2006), 971–977.
21. Klaassen, C.D., Liu, J., Diwan, B.A., Metallothionein protection of cadmium toxicity. Toxicol. Appl. Pharmacol. 238 (2009), 215–220.
22. Langmade, S.J., Ravinda, R., Daniels, P.J., Andrews, G.K., The transcription factor MTF-1 mediates metal regulation of the mouse ZnT1 gene. J. Biol. Chem. 275 (2000), 34803–34809.
23. Leslie, E.M., Liu, J., Klaassen, C.D., Waalkes, M.P., Acquired cadmium resistance in metallothionein-I/II (−/−) knockout cells: role of the T-type calcium channel Cacnalpha1G in cadmium uptake. Mol. Pharmacol. 69 (2006), 629–639.
24. Lévesque, M., Martineau, C., Jumarie, C., Moreau, R., Characterization of cadmium uptake and cytotoxicity in human osteoblast-like MG-63 cells. Toxicol. Appl. Pharmacol. 231 (2008), 308–317.
25. Lichten, L.A., Cousins, R.J., Mammalian zinc transporters: nutritional and physiologic regulation. Annu. Rev. Nutr. 29 (2009), 153–176.
26. Liu, M.J., Bao, S., Galvez-Peralta, M., Pyle, C.J., Rudawsky, A.C., Pavlovicz, R.E., Killilea, D.W., Li, C., Nebert, D.W., Wewers, M.D., Knoell, D.L., ZIP8 regulates host defense through zinc-mediated inhibition of NF-kB. Cell Rep. 3 (2013), 386–400.
27. Liuzzi, J.P., Cousins, R.J., Mammalian zinc transporters. Annu. Rev. Nutr. 24 (2004), 151–172.
28. Liuzzi, J.P., Bobo, J.A., Lichten, L.A., Samuelson, D.A., Cousins, R.J., Responsive transporter genes within the murine intestinal-pancreatic axis form a basis of zinc homeostasis. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 14355–14360.
29. Luevano, J., Damodaran, C., A review of molecular events of cadmium-induced carcinogenesis. J. Environ. Pathol. Toxicol. Oncol. 33:3 (2014), 183–194.
30. Luparello, C., Sirchia, R., Longo, A., Cadmium as a transcriptional modulator in human cells. Crit. Rev. Toxicol., 2010, 1–8.
31. Mackenzie, B., Takanaga, H., Hubert, N., Rolfs, A., Hediger, M.A., Functional properties of multiple isoforms of human divalent metal-ion transporter 1 (DMT1). Biochem. J. 403 (2007), 59–69.
32. Marklund, S., Marklund, G., Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem./FEBS 47 (1974), 469–474.
33. Martineau, C., Abed, E., Médina, G., Jomphe, L.A., Mantha, M., Jumarie, C., Moreau, R., Involvement of transient receptor potential melastatin-related 7 (TRPM7) channels in cadmium uptake and cytotoxicity in MC3T3-E1 osteoblasts. Toxicol. Lett. 199 (2010), 357–363.
34. Miao, L., Clair, D.K.S., Regulation of superoxide dismutase genes: implications in disease. Free Radic. Biol. Med. 47 (2009), 344–356.
35. Mizzen, C.A., Cartel, N.J., Yu, W.H., Fraser, P.E., McLachlan, D.R., Sensitive detection of metallothioneins-1, -2 and -3 in tissue homogenates by immunoblotting: a method for enhanced membrane transfer and retention. J. Biochem. Biophys. Methods 32:2 (1996), 77–83.
36. Mouron, S.A., Grillo, C.A., Dulout, F.N., Golijow, C.D., A comparative investigation of DNA strand breaks, sister chromatid exchanges and K-ras gene mutations induced by cadmium salts in cultured human cells. Mutat. Res. 568 (2004), 221–231.
37. Naha, P.C., Byrne, H.J., Generation of intracellular reactive oxygen species and genotoxicity effect to exposure of nanosized polyamidoamine (PAMAM) dendrimers in PLHC-1 cells in vitro. Aquat. Toxicol. 132–133:2013 (2013), 61–72.
38. Naha, P.C., Davoren, M., Lyng, F.M., Byrne, H.J., Reactive oxygen species (ROS) induced cytokine production and cytotoxicity of PAMAM dendrimers in J774A.1 cells. Toxicol. Appl. Pharmacol. 246:1–2 (2010), 91–99.
39. Naha, P.C., Chhour, P., Cormode, D.P., Systematic in vitro toxicological screening of gold nanoparticles designed for nanomedicine applications. Toxicol. in Vitro 29:2015 (2015), 1445–1453.
40. Nemmiche, S., Chabane-Sari, D., Guiraud, P., Role of α-tocopherol in cadmium-induced oxidative stress in Wistar rat's blood, liver and brain. Chemico-Biol. Int. 170 (2007), 221–230.
41. Nemmiche, S., Chabane-Sari, D., Kadri, M., Guiraud, P., Cadmium chloride induced oxidative stress and DNA damage in the human Jurkat T cell line is not linked to intracellular trace elements depletion. Toxicol. In Vitro 25 (2011), 191–198.
42. Nemmiche, S., Chabane-Sari, D., Kadri, M., Guiraud, P., Cadmium-induced apoptosis in the BJAB human B cell line: involvement of PKC/ERK1/2/JNK signaling pathways in HO-1 expression. Toxicology 300 (2012), 103–111.
43. Nordberg, G.F., Biomarkers of exposure, effects and susceptibility in humans and their application in studies of interactions among metals in China. Toxicol. Lett. 192 (2010), 45–49.
44. Ohana, E., Sekler, I., Kaisman, T., Kahn, N., Cove, J., Silverman, W.F., Amsterdam, A., Hershfinkel, M., Silencing of ZnT-1 expression enhances heavy metal influx and toxicity. J. Mol. Med. 84 (2006), 753–763.
45. Overbeck, S., Uciechowski, P., Ackland, M.L., Ford, D., Rink, L., Intracellular zinc homeostasis in leukocyte subsets is regulated by different expression of zinc exporters ZnT-1 to ZnT-9. J. Leukoc. Biol., 2008, 10.1189/jlb.0307148.
46. Potts, R.J., Bespalov, I.A., Wallace, S.S., Melamede, R.J., Hart, B.A., Inhibition of oxidative DNA repair in cadmium-adapted alveolar epithelial cells and the potential involvement of metallothionein. Toxicology 161 (2001), 25–38.
47. Rogalska, J., Brzoska, M.M., Roszczenko, A., Moniuszko-Jakoniuk, J., Enhanced zinc consumption prevents cadmium-induced alterations in lipid metabolism in male rats. Chem. Biol. Interact. 177 (2009), 142–152.
48. Ryu, D.Y., Lee, S.J., Park, D.W., Choi, B.S., Klaassen, C.D., Park, J.D., Dietary iron regulates intestinal cadmium absorption through iron transporters in rats. Toxicol. Lett. 152 (2004), 19–25.
49. Thevenod, F., Catch me if you can! Novel aspects of cadmium transport in mammalian cells. Biometals, 2010, 10.1007/s10534-010-9309-1.
50. Urani, C., Melchioretto, P., Gribaldo, L., Regulation of metallothioneins and ZnT-1 transporter expression in human hepatoma cells HepG2 exposed to zinc and cadmium. Toxicol. In Vitro 24 (2010), 370–374.
51. Valentine, R.A., Jackson, K.A., Christie, G.R., Mathers, J.C., Taylor, P.M., Ford, D., ZnT5 variant B is a bidirectional zinc transporter and mediates zinc uptake in human intestinal Caco-2 cells. J. Biol. Chem. 282:19 (2007), 14389–14393.
52. Zalups, R.K., Ahmad, S., Molecular handling of cadmium in transporting epithelia. Toxicol. Appl. Pharmacol. 186 (2003), 163–188.
53. Zharkov, D.O., Rosenquist, T.A., Inactivation of mammalian 8-oxoguanine-DNA glycosylase by cadmium(II): implications for cadmium genotoxicity. DNA Repair 1 (2002), 661–670.