154
Views
1
CrossRef citations to date
0
Altmetric
Article

Toxicity of organochalcogens in human leukocytes is associated, but not directly related with reactive species production, apoptosis and changes in antioxidant gene expression

ORCID Icon, , ORCID Icon, ORCID Icon & ORCID Icon
Pages 1158-1169 | Received 04 Jul 2018, Accepted 11 Oct 2018, Published online: 26 Dec 2018

References

  • Combs GF, Combs SB. The nutritional biochemistry of selenium. Annu Rev Nutr. 1984;4:257–280.
  • Holben DH, Smith AM. The diverse role of selenium within selenoproteins: a review. J Am Diet Assoc. 1999;99:836–843.
  • Hatfield DL, Tsuji PA, Carlson BA, et al. Selenium and selenocysteine: roles in cancer, health, and development. Trends Biochem Sci. 2014;39:112–120.
  • Kryukov GV, Castellano S, Novoselov SV, et al. Characterization of mammalian selenoproteomes. Science. 2003;300:1439–1443.
  • Papp LV, Lu J, Holmgren A, et al. From selenium to selenoproteins: synthesis, identity, and their role in human health. Antioxid Redox Signal. 2007;9:775–806.
  • Zhong L, Arnér ESJ, Holmgren A. Structure and mechanism of mammalian thioredoxin reductase: the active site is a redox-active selenolthiol/selenenylsulfide formed from the conserved cysteine-selenocysteine sequence. Proc Natl Acad Sci USA. 2000;97:5854–5859.
  • Taylor A. Biochemistry of tellurium. Biol Trace Elem Res. 1996;55:231–239.
  • Bienert GP, Schüssler MD, Jahn TP. Metalloids: essential, beneficial or toxic? Major intrinsic proteins sort it out. Trends Biochem Sci. 2008;33:20–26.
  • Pessoa-Pureur R, Heimfarth L, Rocha JB. Signaling mechanisms and disrupted cytoskeleton in the diphenyl ditelluride neurotoxicity. Oxid Med Cell Longev. 2014;2014:1.
  • Nogueira CW, Zeni G, Rocha JBT. Organoselenium and organotellurium compounds: toxicology and pharmacology. Chem Rev. 2004;104:6255–6285.
  • Jamier V, Ba LA, Jacob C. Selenium- and tellurium-containing multifunctional redox agents as biochemical redox modulators with selective cytotoxicity. Chem Eur J. 2010;16:10920–10928.
  • Avila DS, Benedetto A, Au C, et al. Organotellurium and organoselenium compounds attenuate Mn-induced toxicity in Caenorhabditis elegans by preventing oxidative stress. Free Radic Biol Med. 2012;52:1903–1910.
  • Andersson C-M, Brattsand R, Hallberg A, et al. Diaryl tellurides as inhibitors of lipid peroxidation in biological and chemical systems. Free Radic Res. 1994;20:401–410.
  • Jacob C, Arteel GE, Kanda T, et al. Water-soluble organotellurium compounds: catalytic protection against peroxynitrite and release of zinc from metallothionein. Chem Res Toxicol. 2000;13:3–9.
  • Braga AL, Alberto EE, Soares LC, et al. Synthesis of telluroamino acid derivatives with remarkable GPx like activity. Org Biomol Chem. 2009;7:43–45.
  • Alfthan G, Aro A, Arvilommi H, et al. Selenium metabolism and platelet glutathione peroxidase activity in healthy Finnish men: effects of selenium yeast, selenite, and selenate. Am J Clin Nutr. 1991;53:120–125.
  • El-Bayoumy K. The protective role of selenium on genetic damage and on cancer. Mutat Res. 2001;475:123–139.
  • Nogueira CW, Rocha JBT. Toxicology and pharmacology of selenium: emphasis on synthetic organoselenium compounds. Arch Toxicol. 2011;85:1313–1359.
  • Chanaday NL, de Bem AF, Roth GA. Effect of diphenyl diselenide on the development of experimental autoimmune encephalomyelitis. Neurochem Int. 2011;59:1155–1162.
  • Rupil LL, de Bem AF, Roth GA. Diphenyl diselenide-modulation of macrophage activation: down-regulation of classical and alternative activation markers. Innate Immun. 2012;18:627–637.
  • Sies H. Ebselen, a selenoorganic compound as glutathione peroxidase mimic. Free Radic Biol Med. 1993;14:313–323.
  • Mugesh G, Panda A, Singh HB, et al. Glutathione peroxidase-like antioxidant activity of diaryl diselenides: a mechanistic study. J Am Chem Soc. 2001;123:839–850.
  • Zhao R, Holmgren A. A novel antioxidant mechanism of ebselen involving ebselen diselenide, a substrate of mammalian thioredoxin and thioredoxin reductase. J Biol Chem. 2002;277:39456–39462.
  • Barbosa NV, Nogueira CW, Nogara PA, et al. Organoselenium compounds as mimics of selenoproteins and thiol modifier agents. Metallomics. 2017;9:1703–1734.
  • Wood-Allum CA, Barber SC, Kirby J, et al. Impairment of mitochondrial anti-oxidant defence in SOD1-related motor neuron injury and amelioration by ebselen. Brain. 2006;129:1693–1709.
  • Bem A. F d, Fiuza B, Calcerrada P, et al. Protective effect of diphenyl diselenide against peroxynitrite-mediated endothelial cell death: a comparison with ebselen. Nitric Oxide. 2013;31:20–30.
  • Fiuza B, Subelzú N, Calcerrada P, et al. Impact of SIN-1-derived peroxynitrite flux on endothelial cell redox homeostasis and bioenergetics: protective role of diphenyl diselenide via induction of peroxiredoxins. Free Radic Res. 2015;49:122–132.
  • Yamaguchi T, Sano K, Takakura K, et al. Ebselen in acute ischemic stroke: a placebo-controlled, double-blind clinical trial. Ebselen Study Group. Stroke. 1998;29:12–17.
  • Rossato JI, Ketzer LA, Centurião FB, et al. Antioxidant properties of new chalcogenides against lipid peroxidation in rat brain. Neurochem Res. 2002;27:297–303.
  • Lovato FL, Teixeira Da Rocha JB, Dalla Corte CL. Diphenyl diselenide protects against methylmercury-induced toxicity in Saccharomyces cerevisiae via the Yap1 transcription factor. Chem Res Toxicol. 2017;30:1134–1144.
  • Rosa RM, Hoch NC, Furtado GV, et al. DNA damage in tissues and organs of mice treated with diphenyl diselenide. Mutat Res. 2007;633:35–45.
  • Comparsi B, Meinerz DF, Franco JL, et al. Diphenyl ditelluride targets brain selenoproteins in vivo: inhibition of cerebral thioredoxin reductase and glutathione peroxidase in mice after acute exposure. Mol Cell Biochem. 2012;370:173–182.
  • Heimfarth L, Loureiro SO, Dutra MF, et al. In vivo treatment with diphenyl ditelluride induces neurodegeneration in striatum of young rats: implications of MAPK and Akt pathways. Toxicol Appl Pharmacol. 2012;264:143–152.
  • Heimfarth L, Reis KP, Loureiro SO, et al. Exposure of young rats to diphenyl ditelluride during lactation affects the homeostasis of the cytoskeleton in neural cells from striatum and cerebellum. NeuroToxicol. 2012;33:1106–1116.
  • Heimfarth L, Loureiro SO, Dutra MF, et al. Disrupted cytoskeletal homeostasis, astrogliosis and apoptotic cell death in the cerebellum of preweaning rats injected with diphenyl ditelluride. NeuroToxicol. 2013;34:175–188.
  • Meinerz DF, Allebrandt J, Mariano DOC, et al. Differential genotoxicity of diphenyl diselenide (PhSe)2 and diphenyl ditelluride (PhTe)2. PeerJ. 2014;2:e290.
  • Galant LS, Braga MM, de Souza D, et al. Induction of reactive oxygen species by diphenyl diselenide is preceded by changes in cell morphology and permeability in Saccharomyces cerevisiae. Free Radic Res. 2017;51:1–668.
  • Santos DB, Schiar VPP, Paixão MW, et al. Hemolytic and genotoxic evaluation of organochalcogens in human blood cells in vitro. Toxicol in Vitro. 2009;23:1195–1204.
  • Santos DB, Schiar VPP, Ribeiro MCP, et al. Genotoxicity of organoselenium compounds in human leukocytes in vitro. Mutat Res. 2009;676:21–26.
  • Caeran Bueno D, Meinerz DF, Allebrandt J, et al. Cytotoxicity and genotoxicity evaluation of organochalcogens in human leucocytes: a comparative study between ebselen, diphenyl diselenide, and diphenyl ditelluride. BioMed Res Int. 2013;2013:1.
  • Ecker A, Ledur PC, da Silva RS, et al. Chalcogenozidovudine derivatives with antitumor activity: comparative toxicities in cultured human mononuclear cells. Toxicol Sci. 2017;160:30–46.
  • Nguyen T, Sherratt PJ, Pickett CB. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol. 2003;43:233–260.
  • Kensler TW, Wakabayashi N, Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol. 2007;47:89–116.
  • Abolaji AO, Kamdem JP, Lugokenski TH, et al. Involvement of oxidative stress in 4-vinylcyclohexene-induced toxicity in Drosophila melanogaster. Free Radic Biol Med. 2014;71:99–108.
  • Riccardi C, Nicoletti I. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat Protoc. 2006;1:1458–1461.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001;25:402–408.
  • Lugokenski TH, Müller LG, Taube PS, et al. Inhibitory effect of ebselen on lactate dehydrogenase activity from mammals: a comparative study with diphenyl diselenide and diphenyl ditelluride. Drug Chem Toxicol. 2011;34:66–76.
  • Rocha JBT, Saraiva RA, Garcia SC, et al. Aminolevulinate dehydratase (δ-ALA-D) as marker protein of intoxication with metals and other pro-oxidant situations. Toxicol Res. 2012;1:85–102.
  • Puntel RL, Roos DH, Seeger RL, et al. Mitochondrial electron transfer chain complexes inhibition by different organochalcogens. Toxicol in Vitro. 2013;27:59–70.
  • Roy S, Hardej D. Tellurium tetrachloride and diphenyl ditelluride cause cytotoxicity in rat hippocampal astrocytes. Food Chem Toxicol. 2011;49:2564–2574.
  • Kalyanaraman B, Darley-Usmar V, Davies KJA, et al. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic Biol Med. 2012;52:1–6.
  • McCord JM, Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem. 1969;244:6049–6055.
  • Dröge W. Free radicals in the physiological control of cell function. Physiol Rev. 2002;82:47–95.
  • Yoshimura S, Watanabe K, Suemizu H, et al. Tissue specific expression of the plasma glutathione peroxidase gene in rat kidney. J Biochem. 1991;109:918–923.
  • Roveri A, Maiorino M, Nisii C, et al. Purification and characterization of phospholipid hydroperoxide glutathione peroxidase from rat testis mitochondrial membranes. Biochim Biophys Acta. 1994;1208:211–221.
  • Arnér ESJ, Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem. 2000;267:6102–6109.
  • Quispe RL, Jaramillo ML, Galant LS, et al. Diphenyl diselenide protects neuronal cells against oxidative stress and mitochondrial dysfunction: involvement of the glutathione-dependent antioxidant system. Redox Biol. 2019;20:118–129.
  • Zhang G, Nitteranon V, Guo S, et al. Organoselenium compounds modulate extracellular redox by induction of extracellular cysteine and cell surface thioredoxin reductase. Chem Res Toxicol. 2013;26:456–464.
  • Ishii T, Itoh K, Takahashi S, et al. Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J Biol Chem. 2000;275:16023–16029.
  • Sakurai T, Kanayama M, Shibata T, et al. Ebselen, a Seleno-organic antioxidant, as an electrophile. Chem Res Toxicol. 2006;19:1196–1204.
  • Suzuki T, Yamamoto M. Molecular basis of the Keap1-Nrf2 system. Free Radic Biol Med. 2015;88:93–100.
  • Stewart D, Killeen E, Naquin R, et al. Degradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmium. J Biol Chem. 2003;278:2396–2402.
  • Terlinden R, Feige M, Römer A. Determination of the two major metabolites of ebselen in human plasma by high-performance liquid chromatography. J Chromatogr. 1988;430:438–442.
  • Prigol M, Nogueira CW, Zeni G, et al. In vitro metabolism of diphenyl diselenide in rat liver fractions. Conjugation with GSH and binding to thiol groups. Chem Biol Interact. 2012;200:65–72.
  • Adams WJ, Kocsis JJ, Snyder R. Acute toxicity and urinary excretion of diphenyldiselenide. Toxicol Lett. 1989;48:301–310.
  • Wedding JL, Lai B, Vogt S, et al. Investigation into the intracellular fates, speciation and mode of action of selenium-containing neuroprotective agents using XAS and XFM. Biochim Biophys Acta Gen Subj. 2018;1862:2393–2404.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.