Inhibitory effects of selenium on cadmium-induced cytotoxicity in PC12 cells via regulating oxidative stress and apoptosis

Food and Chemical Toxicology

Volumn 114, Issue , 2018, Pages 180-189

  Binte Hossain, Kaniz Fatima ^a   Rahman, Md Mostafizur ^a   Sikder, Md Tajuddin ^a,b   Saito, Takeshi ^a   Hosokawa, Toshiyuki ^a   Kurasaki, Masaaki ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b JAHANGIRNAGAR UNIVERSITY   (Bangladesh)

Author keywords

Apoptosis; Autophagy; Cytochrome c; Glutathione; Glutathione peroxidase; Oxidative stress

Indexed keywords

CADMIUM CHLORIDE; CYTOCHROME C; GENOMIC DNA; GLUTATHIONE; GLUTATHIONE PEROXIDASE 1; LACTATE DEHYDROGENASE; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE 3; SEQUESTOSOME 1; SODIUM SELENITE; CADMIUM; GLUTATHIONE PEROXIDASE; PROTECTIVE AGENT; REACTIVE OXYGEN METABOLITE; SELENIUM;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; BIOACCUMULATION; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; DNA FRAGMENTATION; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME RELEASE; MITOCHONDRION; OXIDATIVE STRESS; PC12 CELL LINE; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; CELL SURVIVAL; CELLS; CYTOLOGY; METABOLISM; RAT;

ANIMALS; APOPTOSIS; AUTOPHAGY; CADMIUM; CELL SURVIVAL; CELLS; CYTOCHROMES C; DNA FRAGMENTATION; GLUTATHIONE; GLUTATHIONE PEROXIDASE; MITOCHONDRIA; OXIDATIVE STRESS; PC12 CELLS; PROTECTIVE AGENTS; RATS; REACTIVE OXYGEN SPECIES; SELENIUM;

EID: 85042429083     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2018.02.034     Document Type: Article

References (63)

1. Abdulah, R., Kobayashi, K., Yamazaki, C., Koyama, H., Molecular targets of selenium in prostate cancer prevention (review). Int. J. Oncol. 39 (2011), 301–309.
2. Armstrong, J.S., Steinauer, K.K., Hornung, B., Irish, J.M., Lecane, P., Birrell, G.W., Peehl, D.M., Knox, S.J., Role of glutathione depletion and reactive oxygen species generation in apoptotic signaling in a human B lymphoma cell line. Cell Death Differ. 9 (2002), 252–263.
3. Battin, E.E., Brumaghim, J.L., Antioxidant activity of sulfur and selenium: a review of reactive oxygen species scavenging, glutathione peroxidase, and metal-binding antioxidant mechanisms. Cell Biochem. Biophys. 55 (2009), 1–23.
4. Brozmanova, J., Manikova, D., Vlckova, V., Chovanec, M., Selenium: a double-edged sword for defense and offence in cancer. Arch. Toxicol. 84 (2010), 919–938.
5. Chatterjee, A., Reduced glutathione: a radioprotector or a modulator of DNA-repair activity?. Nutrients 5 (2013), 525–542 https://doi.org/10.3390/nu5020525.
6. Chen, J.J., Boylan, L.M., Wu, C.K., Spallholz, J.E., Oxidation of glutathione and superoxide generation by inorganic and organic selenium compounds. Biofactors 31 (2007), 55–66.
7. Chen, L., Liu, L., Huang, S., 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 (2008), 1035–1044.
8. Chen, L., Liu, L., Luo, Y., Huang, S., MAPK and mTOR pathways are involved in cadmium-induced neuronal apoptosis. J. Neurochem. 105 (2008), 251–261 https://doi.org/10.1111/j.1471-4159.2007.05133.x.
9. Chen, X., Zhu, Y.H., Cheng, X.Y., Zhang, Z.W., Xu, S.W., The protection of selenium against cadmium-induced cytotoxicity via the heat shock protein pathway in chicken splenic lymphocytes. Molecules 17 (2012), 14565–14572 https://doi.org/10.3390/molecules171214565.
10. Cheng, Y., Sk, U.H., Zhang, Y., Ren, X., Zhang, L., Keener, K.J.H., Sun, Y.W., Liao, J., Amin, S., Sharma, A.K., Yang, J.M., Rational incorporation of selenium into temozolomide elicits superior antitumor activity associated with both apoptotic and autophagic cell death. PLoS One, 7, 2012, e35104.
11. Cummings, B.S., Wills, L.P., Schnellmann, R.G., Measurement of cell death in mammalian cells. Curr. Protoc. Pharmacol., 12, 2004 https://doi.org/10.1002/0471141755.ph1208s56.
12. Cuypers, A., Plusquin, M., Remans, T., Jozefczak, M., Keunen, E., Gielen, H., Opdenakker, K., Nair, A.R., Munters, E., Artois, T.J., et al. Cadmium stress: an oxidative challenge. Biometals 23 (2010), 927–940.
13. Duran, A., Amanchy, R., Linares, J.F., Joshi, J., Baker, S.A., Porollo, A., Hansen, M., Moscat, J., Diaz-Meco, M.T., p62 is a key regulator of nutrient sensing in the mTORC1 pathway. Mol. Cell. 44 (2011), 134–146 https://doi.org/10.1016/j.molcel.2011.06.038.
14. El-Demerdash, F.M., Effects of selenium and mercury on the enzymatic activities and lipid peroxidation in brain, liver, and blood of rats. J. Environ. Sci. Health. B 36 (2001), 489–499.
15. Elmore, S., Apoptosis: a review of programmed cell death. Toxicol. Pathol. 35 (2007), 495–516 https://doi.org/10.1080/01926230701320337.
16. El-Sharaky, A.S., Newairy, A.A., Badreldeen, M.M., Eweda, A.M., Sheweita, S.A., Protective role of selenium against renal toxicity induced by Cadmium in rats. Toxicology 235 (2007), 185–193.
17. El-Shenawy, S.M., Hassan, N.S., Comparative evaluation of the protective effect of selenium and garlic against liver and kidney damage induced by mercury chloride in the rats. Pharmacol. Rep. 60 (2008), 199–208.
18. Fan, T.J., Han, L.H., Cong, R.S., Liang, J., Caspase family proteases and apoptosis. Acta Biochim. Biophys. Sin. 37 (2005), 719–727.
19. Finley, J.W., Bioavailability of selenium from foods. Nutr. Rev. 64 (2006), 146–151.
20. Fordyce, F.M., Selenium deficiency and toxicity in the environment. Essent. Med. Geol., 2013, 375–416 https://doi.org/10.1007/978-94-007-4375-5_16.
21. Gan, L., Liu, Q., Xu, H.B., Zhu, Y.S., Yang, X.L., Effects of selenium overexposure on glutathione peroxidase and thioredoxinreductase gene expressions and activities. Biol. Trace Elem. Res. 89 (2002), 165–175.
22. Guan, L.Y., Han, B.S., Li, Z.S., Hua, F.Y., Huang, F., Wei, W., Yang, Y., Xu, C., Sodium selenite induces apoptosis by ROS-mediated endoplasmic reticulum stress and mitochondrial dysfunction in human acute promyelocytic leukemia NB4 cells. Apoptosis 14 (2009), 218–225.
23. Hatfield, D.L., Berry, M.J., Gladyshev, V.N., Selenium: its Molecular Biology and Role in Human Health. third ed., 2011, Springer Science & Business Media.
24. Higuchi, Y., Chromosomal DNA fragmentation in apoptosis and necrosis induced by oxidative stress. Biochem. Pharmacol. 66 (2003), 1527–1535.
25. Huang, F., Nie, C., Yang, Y., Yue, W., Ren, Y., Shang, Y., Wang, X., Jin, H., Xu, C., Chen, Q., Selenite induces Caspase family proteases and apoptosisCaspase family proteases and apoptosis redox-dependent Bax activation and apoptosis in colorectal cancer cells. Free Radic. Biol. Med. 46 (2009), 1186–1196.
26. Ivanina, A.V., Cherkasov, A.S., Sokolova, I.M., Effects of cadmium on cellular protein and glutathione synthesis and expression of stress proteins in eastern oysters, Crassostreavirginica Gmelin. J. Exp. Biol. 211 (2008), 577–586 https://doi.org/10.1242/jeb.011262.
27. Jiang, C., Yuan, Y., Hu, F., Wang, Q., Zhang, K., Wang, Y., Gu, J., Liu, X., Bian, J., Liu, Z., Cadmium induces PC12 cells apoptosis via an extracellular signal-regulated kinase and c-Jun N-terminal kinase-mediated mitochondrial apoptotic pathway. Biol. Trace Elem. Res. 158 (2014), 249–258 https://doi.org/10.1007/s12011-014-9918-6.
28. Jung, C.H., Ro, S.H., Cao, J., Otto, N.M., Kim, D.H., mTOR regulation of autophagy. FEBS Lett. 584 (2010), 1287–1295 https://doi.org/10.1016/j.febslet.2010.01.017.
29. Kawakami, M., Inagawa, R., Hosokawa, T., Saito, T., Kurasaki, M., Mechanism of apoptosis induced by copper in PC12 cells. Food Chem. Toxicol. 46 (2008), 2157–2164.
30. Kihara, Y., Yustiawati Tanaka, M., Gumiri, S., Ardianor Hosokawa, T., Tanaka, S., Saito, T., Kurasaki, M., Mechanism of the toxicity induced by natural humic acid on human vascular endothelial cells. Environ. Toxicol. 29 (2014), 916–925 https://doi.org/10.1002/tox.21819.
31. Kim, E.H., Sohn, S., Kwon, H.J., Kim, S.U., Kim, M.J., Lee, S.J., Choi, K.S., Sodium selenite induces superoxide-mediated mitochondrial damage and subsequent autophagic cell death in malignant glioma cells. Canc. Res. 67 (2007), 6314–6324.
32. Lau, A., Zhang, J., Chiu, J., Acquired tolerance in cadmium adapted lung epithelial cells: roles of the c-Jun N-terminal kinase signaling pathway and basal level of metallothionein. Toxicol. Appl. Pharmacol. 215 (2006), 1–8.
33. Li, J., Zuo, L., Shen, T., Xu, C.M., Zhang, Z.N., Induction of apoptosis by sodium selenite in human acute promyelocytic leukemia NB4 cells: involvement of oxidative stress and mitochondria. J. Trace Elem. Med. Biol. 17 (2003), 19–26.
34. Li, J.L., Gao, R., Li, S., Wang, J.T., Tang, Z.X., Xu, S.W., Testicular toxicity induced by dietary cadmium in cocks and ameliorative effect by selenium. Biometals 23 (2010), 695–705 https://doi.org/10.1007/s10534-010-9334-0.
35. Li, Z., Meng, J., Xu, T.J., Qin, X.Y., Zhou, X.D., Sodium selenite induces apoptosis in colon cancer cells via Bax-dependent mitochondrial pathway. Eur. Rev. Med. Pharmacol. Sci. 17 (2013), 2166–2171.
36. Liu, Y., Zhang, S.P., Cai, Y.Q., Cytoprotective effects of selenium on cadmium-induced LLC-PK1 cells apoptosis by activating JNK pathway. Toxicol. Vitro 21 (2007), 677–684 https://doi.org/10.1016/j.tiv.2007.01.015.
37. Luo, H., Yang, Y., Huang, F., Li, F., Jiang, Q., Shi, K., Xu, C., Selenite induces apoptosis in colorectal cancer cells via AKT-mediated inhibition of b-catenin survival axis. Canc. Lett. 315 (2012), 78–85.
38. Magalingam, K.B., Radhakrishnan, A., Haleagrahara, N., Protective effects of flavonolisoquercitrin, against 6-hydroxy dopamine (6-OHDA) - induced toxicity in PC12 cells. BMC Res. Notes, 7, 2014, 49.
39. Mizushima, N., The pleiotropic role of autophagy: from protein metabolism to bactericide. Cell Death Differ. 12 (2005), 1535–1541.
40. Nair, A.R., DeGheselle, O., Smeets, K., Kerkhove, E.V., Cuypers, A., Cadmium-induced pathologies: where is the oxidative balance lost (or not)?. Int. J. Mol. Sci. 14 (2013), 6116–6143 https://doi.org/10.3390/ijms14036116.
41. Newairy, A.A., El-Sharaky, A.S., Badreldeen, M.M., Eweda, S.M., Sheweita, S.A., The hepatoprotective effects of selenium against cadmium toxicity in rats. Toxicology 242 (2007), 23–30.
42. Nishina, A., Sekiguchi, A., Fukumoto, R., Koketsu, M., Furukawa, S., Selenazoles (selenium compounds) facilitate survival of cultured rat pheochromocytoma PC12 cells after serum-deprivation and stimulate their neuronal differentiation via activation of Akt and mitogen-activated protein kinase, respectively. Biochem. Biophys. Res. Commun. 352 (2007), 360–365.
43. Pankiv, S., Clausen, T.H., Lamark, T., Brech, A., Bruun, J.A., Outzen, H., Øvervatn, A., Bjørkøy, G., Terje Johansen, T., p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282 (2007), 24131–24145.
44. Puissant, A., Robert, G., Fenouille, N., Luciano, F., Cassuto, J.P., Raynaud, S., Auberger, P., Resveratrol promotes autophagic cell death in chronic myelogenous leukemia cells via JNK-mediated p62/SQSTM1 expression and AMPK activation. Canc. Res. 70 (2010), 1042–1052 https://doi.org/10.1158/0008-5472.
45. Rahman, M.M., Lopez-Uson, A.R., Sikder, M.T., Tan, G., Hosokawa, T., Saito, T., Kurasaki, M., Ameliorative effects of selenium on arsenic-induced cytotoxicity in PC12 cells via modulating autophagy/apoptosis. Chemosphere 196 (2018), 453–466 https://doi.org/10.1016/j.chemosphere.2017.12.149.
46. Rahman, M.M., Ukiana, J., Lopez, R.U., Sikder, M.T., Saito, T., Kurasaki, M., Cytotoxic effects of cadmium and zinc co-exposure in PC12 cells and the underlying mechanism. Chem. Biol. Interact. 269 (2017), 41–49.
47. Rayman, M.P., The importance of selenium to human health. Lancet 356 (2000), 233–241.
48. Rayman, M.P., Selenium and human health. Lancet 379 (2012), 1256–1268.
49. Reeves, M.A., Hoffmann, P.R., The human selenoproteome: recent insights into functions and regulation. Cell. Mol. Life Sci. 66 (2009), 2457–2478.
50. Roy, R., Singh, S.K., Chauhan, L.K.S., Das, M., Tripathi, A., Dwivedi, P.D., Zinc oxide nanoparticles induce apoptosis by enhancement of autophagy via PI3K/Akt/mTOR inhibition. Toxicol. Lett. 227 (2014), 29–40.
51. Schnabel, R., Lubos, E., Messow, C.M., Sinning, C.R., Zeller, T., Wild, P.S., Peetz, D., Handy, D.E., Munzel, T., Loscalzo, J., Lackner, K.J., Blankenberg, S., Selenium supplementation improves antioxidant capacity in vitro and in vivo in patients with coronary artery disease: the Selenium therapy in coronary artery disease patients (SETCAP) study. Am. Heart J. 156:1201 (2008), e1–11 https://doi.org/10.1016/j.ahj.2008.09.004.
52. Spanier, G., Xu, H., Xia, N., Tobias, S., Deng, S., Wojnowski, L., Forstermann, U., Li, H., Resveratrol reduces endothelial oxidative stress by modulating the gene expression of superoxide dismutage 1 (SOD1), glutathione peroxidase 1 (GPX1) and NADPH oxidase subunit (NOX4). J. Physiol. Pharmacol. 60 (2009), 111–116.
53. U.S. Department of health & human services, National Institutes of Health. USDA National Nutrient Database for Standard Reference. Release 25. Nutrient Data Laboratory, 2012 https://ods.od.nih.gov/factsheets/Selenium-HealthProfessional/. (Accessed 22 December 2017)
54. Wallenberg, M., Misra, S., Wasik, A.M., Marzano, C., Bjӧrnstedt, M., Gandin, V., Fernandes, A.P., Selenium induces a multi-targeted cell death process in addition to ROS formation. J. Cell Mol. Med. 18 (2014), 671–684.
55. 3+)-induced apoptosis and differentiation in acute promyelocytic leukemia cells. Cell Death Dis., 6, 2015, e1596 https://doi.org/10.1038/cddis.2014.563.
56. Wang, Y., Wang, K., Huang, H., Gu, X., Teng, X., Alleviative effect of selenium on inflammatory damage caused by lead via inhibiting inflammatory factors and heat shock proteins in chicken testes. Environ. Sci. Pollut. Res. Int. 24 (2017), 13405–13413 https://doi.org/10.1007/s11356-017-8785-z.
57. Yu, L., Wan, F., Dutta, S., Welsh, S., Liu, Z.H., Freundt, E., Baehrecke, E.H., Lenardo, M., Autophagic programmed cell death by selective catalase degradation. Proc. Natl. Acad. Sci. U.S.A. 103 (2006), 4952–4957.
58. Zeng, H., Selenium as an essential micronutrient: roles in cell cycle and apoptosis. Molecules 14 (2009), 1263–1278 https://doi.org/10.3390/molecules14031263.
59. Zhang, J., Zhou, X., Wu, W., Wang, J., Xie, H., Wu, Z., Regeneration of glutathione by α-lipoic acid via Nrf2/ARE signaling pathway alleviates cadmium-induced HepG2 cell toxicity. Environ. Toxicol. Pharmacol. 51 (2017), 30–37.
60. Zhou, N., Xiao, H., Li, T.K., Nur-E-Kamal, A., Liu, L.F., DNA damage-mediated apoptosis induced by selenium compounds. J. Biol. Chem. 278 (2003), 29532–29537.
61. Zhou, Y.J., Zhang, S.P., Liu, C.W., Cai, Y.Q., The protection of selenium on ROS mediated-apoptosis by mitochondria dysfunction in cadmium-induced LLC-PK1 cells. Toxicol. Vitro 23 (2009), 288–294.
62. Zitka, O., Skalickova, S., Gumulec, J., Masarik, M., Adam, V., Hubalek, J., Trnkova, L., Kruseova, J., Eckschlager, T., Kizek, R., Redox status expressed as GSH: GSSG ratio as a marker for oxidative stress in paediatrictumour patients. Oncol. Lett. 4 (2012), 1247–1253.
63. Zuo, L., Li, J., Yang, Y., Wang, X., Shen, T., Xu, C.M., Zhang, Z.N., Sodium selenite induces apoptosis in acute promyelocytic leukemia-derived NB4 cells by a caspase-3-dependent mechanism and a redox pathway different from that of arsenic trioxide. Ann. Hematol. 83 (2004), 751–758.