Cadmium-induced heme-oxygenase-1 expression plays dual roles in autophagy and apoptosis and is regulated by both PKC-δ and PKB/Akt activation in NRK52E kidney cells

Toxicology

Volumn 370, Issue , 2016, Pages 49-59

  So, Keum Young ^a   Oh, Seon Hee ^b  

^a Chosun University   (South Korea)

^b Chosun University College of Medicine   (South Korea)

Author keywords

Autophagy; Cadmium; Heme oxygenase 1; NRK52E cells; Protein kinase B; Protein kinase C

Indexed keywords

CADMIUM; CASPASE 3; CASPASE 7; GLYCOGEN SYNTHASE KINASE 3ALPHA; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEME OXYGENASE 1; INITIATION FACTOR 2ALPHA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PHOSPHOSERINE; PROTEIN KINASE B; PROTEIN KINASE C DELTA; PROTEIN P53; SERINE; ACETYLCYSTEINE; DDIT3 PROTEIN, RAT; GLYCOGEN SYNTHASE KINASE 3; HEME OXYGENASE; HMOX1 PROTEIN, RAT; INITIATION FACTOR 2; PARP1 PROTEIN, RAT;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; BIOACCUMULATION; CELL NUCLEUS; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME INACTIVATION; HOMEOSTASIS; KIDNEY CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL SURVIVAL; CYTOLOGY; DNA DAMAGE; DRUG EFFECTS; GENETICS; IC50; KIDNEY; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ACETYLCYSTEINE; ANIMALS; APOPTOSIS; AUTOPHAGY; CADMIUM; CELL LINE, TUMOR; CELL SURVIVAL; DNA DAMAGE; EUKARYOTIC INITIATION FACTOR-2; GLYCOGEN SYNTHASE KINASE 3; HEME OXYGENASE (DECYCLIZING); INHIBITORY CONCENTRATION 50; KIDNEY; OXIDATIVE STRESS; PHOSPHORYLATION; POLY (ADP-RIBOSE) POLYMERASE-1; PROTEIN KINASE C-DELTA; PROTO-ONCOGENE PROTEINS C-AKT; RATS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR CHOP; UP-REGULATION;

EID: 84988959314     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2016.09.010     Document Type: Article

References (51)

1. Agarwal, A., Nick, H.S., Renal response to tissue injury: lessons from heme oxygenase-1 GeneAblation and expression. J. Am. Soc. Nephrol. 11 (2000), 965–973.
2. Baehrecke, E.H., Autophagy: dual roles in life and death. Nat. Rev. Mol. Cell Biol. 6 (2005), 505–510.
3. Banerjee, P., Basu, A., Wegiel, B., Otterbein, L.E., Mizumura, K., Gasser, M., Waaga-Gasser, A.M., Choi, A.M., Pal, S., Heme oxygenase-1 promotes survival of renal cancer cells through modulation of apoptosis- and autophagy-regulating molecules. J. Biol. Chem. 287 (2012), 32113–32123.
4. Beurel, E., Jope, R.S., The paradoxical pro- and anti-apoptotic actions of GSK3 in the intrinsic and extrinsic apoptosis signaling pathways. Prog. Neurobiol. 79 (2006), 173–189.
5. Biswas, C., Shah, N., Muthu, M., La, P., Fernando, A.P., Sengupta, S., Yang, G., Dennery, P.A., Nuclear heme oxygenase-1 (HO-1) modulates subcellular distribution and activation of Nrf2, impacting metabolic and anti-oxidant defenses. J. Biol. Chem. 289 (2014), 26882–26894.
6. Chargui, A., Zekri, S., Jacquillet, G., Rubera, I., Ilie, M., Belaid, A., et al. Cadmium-induced autophagy in rat kidney: an early biomarker of subtoxic exposure. Toxicol. Sci. 121 (2011), 31–42.
7. Chen, J.L., Lin, H.H., Kim, K.J., Lin, A., Ou, J.H., Ann DK: PKC delta signaling: a dual role in regulating hypoxic stress-induced autophagy and apoptosis. Autophagy 5 (2009), 244–246.
8. Chen, H.H., Chen, Y.T., Huang, Y.W., Tsai, H.J., Kuo, C.C., 4-Ketopinoresinol, a novel naturally occurring ARE activator, induces the Nrf2/HO-1 axis and protects against oxidative stress-induced cell injury via activation of PI3K/AKT signaling. Free Radic. Biol. Med. 52 (2012), 1054–1066.
9. Cook, D., Fry, M.J., Hughes, K., Sumathipala, R., Woodgett, J.R., Dale, T.C., Wingless inactivates glycogen synthase kinase-3 via an intracellular signalling pathway which involves a protein kinase C. EMBO J. 15 (1996), 4526–4536.
10. Forde, J.E., Dale, T.C., Glycogen synthase kinase 3: a key regulator of cellular fate. Cell. Mol. Life Sci. 64 (2007), 1930–1944.
11. Gobe, G., Crane, D., Mitochondria reactive oxygen species and cadmium toxicity in the kidney. Toxicol. Lett. 198 (2010), 49–55.
12. Gomel, R., Xiang, C., Finniss, S., Lee, H.K., Lu, W., Okhrimenko, H., Brodie, C., The localization of protein kinase Cdelta in different subcellular sites affects its proapoptotic and antiapoptotic functions and the activation of distinct downstream signaling pathways. Mol. Cancer Res. 5 (2007), 627–639.
13. Hamada, T., Nakano, S., Iwai, S., Tanimoto, A., Ariyoshi, K., Koide, O., Pathological study on beagles after long-term oral administration of cadmium. Toxicol. Pathol. 19 (1991), 138–147.
14. 2-induced cytotoxicity of COS7 cells through the prevention of intracellular reactive oxygen species accumulation. Biol. Pharm. Bull. 35 (2012), 1126–1131.
15. Kansanen, E., Kuosmanen, S.M., Leinonen, H., Levonen, A.L., The Keap1-Nrf2 pathway: mechanisms of activation and dysregulation in cancer. Redox. Biol. 1 (2013), 45–49.
16. Kim, H.P., Wang, X., Chen, Z.H., Lee, S.J., Huang, M.H., Wang, Y., Ryter, S.W., Choi, A.M., Autophagic proteins regulate cigarette smoke-induced apoptosis: protective role of heme oxygenase-1. Autophagy 7 (2008), 887–895.
17. Lau, A., Wang, X.J., Zhao, F., Villeneuve, N.F., Wu, T., Jiang, T., Sun, Z., White, E., Zhang, D.D., A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62. Mol. Cell. Biol. 30 (2010), 3275–3285.
18. Lawal, A.O., Ellis, E.M., Nrf2-mediated adaptive response to cadmium-induced toxicity involves protein kinase C delta in human 1321 N1 astrocytoma cells. Environ. Toxicol. Pharmacol. 32 (2011), 54–62.
19. Lee, W.K., Abouhamed, M., Thévenod, F., Caspase-dependent and −independent pathways for cadmium-induced apoptosis in cultured kidney proximal tubule cells. Am. J. Physiol. Renal. Physiol. 291 (2006), F823–F832.
20. Liu, Y., Templeton, D.M., Initiation of caspase-independent death in mouse mesangial cells by Cd2+: involvement of p38 kinase and CaMK-II. J. Cell. Physiol. 217 (2008), 307–318.
21. Marciniak, S.J., Yun, C.Y., Oyadomari, S., Novoa, I., Zhang, Y., Jungreis, R., Nagata, K., Harding, H.P., Ron, D., CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 18 (2004), 3066–3077.
22. Meares, G.P., Jope, R.S., Resolution of the nuclear localization mechanism of glycogen synthase kinase-3: functional effects in apoptosis. J. Biol. Chem. 282 (2007), 16989–17001.
23. Miguel, B.G., Rodriguez, M.E., Aller, P., Martinez, A.M., Mata, F., Regulation of cadmium-induced apoptosis by PKCdelta in U937 human promonocytic cells. Biochim. Biophys. Acta 1743 (2005), 215–222.
24. 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.
25. Ogasawara, Y., Takeda, Y., Takayama, H., Nishimoto, S., Ichikawa, K., Ueki, M., Suzuki, T., Ishii, K., Significance of the rapid increase in GSH levels in the protective response to cadmium exposure through phosphorylated Nrf2 signaling in Jurkat T-cells. Free Radic. Biol. Med. 69 (2014), 58–66.
26. Paine, A., Eiz-Vesper, B., Blasczyk, R., Immenschuh, S., Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem. Pharmacol. 80 (2010), 1895–1903.
27. Pap, M., Cooper, G.M., Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J. Biol. Chem. 273 (1998), 19929–19932.
28. Park, C.H., Lee, B.H., Ahn, S.G., Yoon, J.H., Oh, S.H., Serine 9 and tyrosine 216 phosphorylation of GSK-3β differentially regulates autophagy in acquired cadmium resistance. Toxicol. Sci. 135 (2013), 380–389.
29. Prozialeck, W.C., Edwards, J.R., Mechanisms of cadmium-induced proximal tubule injury: new insights with implications for biomonitoring and therapeutic interventions. J. Pharmacol. Exp. Ther. 343 (2012), 2–12.
30. Qi, X., Mochly-Rosen, D., The PKCdelta – Abl complex communicates ER stress to the mitochondria −an essential step in subsequent apoptosis. J. Cell Sci. 121 (2008), 804–813.
31. Rajesh, K., Krishnamoorthy, J., Kazimierczak, U., Tenkerian, C., Papadakis, A.I., Wang, S., Huang, S., Koromilas, A.E., Phosphorylation of the translation initiation factor eIF2α at serine 51 determines the cell fate decisions of Akt in response to oxidative stress. Cell Death Dis., 6, 2015, e1591.
32. Ryter, S.W., Tyrrell, R.M., The heme synthesis and degradation pathways: role in oxidant sensitivity: heme oxygenase has both pro- and antioxidant properties. Free Radic. Biol. Med. 28 (2000), 289–309.
33. Sinha, K., Pal, P.B., Sil, P.C., Cadmium (Cd2+) exposure differentially elicits both cell proliferation and cell death related responses in SK-RC-45. Toxicol. In Vitro 28 (2014), 307–318.
34. Son, Y.O., Pratheeshkumar, P., Roy, R.V., Hitron, J.A., Wang, L., Zhang, Z., Shi, X., Nrf2/p62 signaling in apoptosis resistance and its role in cadmium-induced carcinogenesis. J. Biol. Chem. 289 (2014), 28660–28675.
35. Srisook, K., Jung, N.H., Kim, B.R., Cha, S.H., Kim, H.S., Cha, Y.N., Heme oxygenase-1-mediated partial cytoprotective effect by NO on cadmium-induced cytotoxicity in C6 rat glioma cells. Toxicol. In Vitro. 19 (2005), 31–39.
36. Surolia, R., Karki, S., Kim, H., Yu, Z., Kulkarni, T., Mirov, S.B., Carter, A.B., Rowe, S.M., Matalon, S., Thannickal, V.J., Agarwal, A., Antony, V.B., Heme oxygenase-1-mediated autophagy protects against pulmonary endothelial cell death and development of emphysema in cadmium-treated mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 309 (2015), L280–292.
37. Tan, J., Zhuang, L., Leong, H.S., Iyer, N.G., Liu, E.T., Yu, Q., Pharmacologic modulation of glycogen synthase kinase-3beta promotes p53-dependent apoptosis through a direct Bax-mediated mitochondrial pathway in colorectal cancer cells. Cancer Res. 65 (2005), 9012–9020.
38. Templeton, D.M., Liu, Y., Multiple roles of cadmium in cell death and survival. Chem. Biol. Interact. 188 (2010), 267–275.
39. Tibullo, D., Barbagallo, I., Giallongo, C., Vanella, L., Conticello, C., Romano, A., Saccone, S., Godos, J., Di Raimondo, F., Li Volti, G., Heme oxygenase-1 nuclear translocation regulates bortezomibinduced cytotoxicity and mediates genomic instability in myeloma cells. Oncotarget, 2016, 10.18632/oncotarget.7563.
40. Tronel, C., Rochefort, G.Y., Arlicot, N., Bodard, S., Chalon, S., Antier, D., Oxidative stress is related to the deleterious effects of heme oxygenase-1 in an in vivo neuroinflammatory rat model. Oxid. Med. Cell. Longevity, 2013, 264935.
41. Wang, S.H., Shih, Y.L., Ko, W.C., Wei, Y.H., Shih, C.M., Cadmium-induced autophagy and apoptosis are mediated by a calcium signaling pathway. Cell. Mol. Life Sci. 65 (2008), 3640–3652.
42. Wang, S.H., Shih, Y.L., Kuo, T.C., Ko, W.C., Shih, C.M., Cadmium toxicity toward autophagy through ROS-activated GSK-3beta in mesangial cells. Toxicol. Sci. 108 (2009), 124–131.
43. Wang, Y., Shen, J., Xiong, X., Xu, Y., Zhang, H., Huang, C., Tian, Y., Jiao, C., Wang, X., Li, X., Remote ischemic preconditioning protects against liver ischemia-reperfusion injury via heme oxygenase-1-induced autophagy. PLoS One, 9, 2014, e98834.
44. Wang, Q.W., Wang, Y., Wang, T., Zhang, K.B., Yuan, Y., Bian, J.C., Liu, X.Z., Gu, J.H., Zhu, J.Q., Liu, Z.P., Cadmium-induced autophagy is mediated by oxidative signaling in PC-12 cells and is associated with cytoprotection. Mol. Med. Rep. 12 (2015), 4448–4454.
45. Wilmes, A., Crean, D., Aydin, S., Pfaller, W., Jennings, P., Leonard, M.O., Identification and dissection of the Nrf2 mediated oxidative stress pathway in human renal proximal tubule toxicity. Toxicol. In Vitro 25 (2011), 613–622.
46. Yang, L.Y., Wu, K.H., Chiu, W.T., Wang, S.H., Shih, C.M., The cadmium-induced death of mesangial cells results in nephrotoxicity. Autophagy 5 (2009), 571–572.
47. Yokouchi, M., Hiramatsu, N., Hayakawa, K., Okamura, M., Du, S., Kasai, A., Takano, Y., Shitamura, A., Shimada, T., Yao, J., Kitamura, M., Involvement of selective reactive oxygen species upstream of proapoptotic branches of unfolded protein response. J. Biol. Chem. 283 (2008), 4252–4260.
48. Yorimitsu, T., Klionsky, D.J., Klionsky, D.J., Autophagy: molecular machinery for self-eating. Cell Death Differ. 12 (2005), 1542–1552.
49. Yoshida, T., Sato, M., Posttranslational and direct integration of heme oxygenase into microsomes. Biochem. Biophys. Res. Commun. 163 (1989), 1086–1092.
50. Zhao, M., Xia, L., Chen, G.Q., Protein kinase cδ in apoptosis: a brief overview. Arch. Immunol. Ther. Exp. (Warsz) 60 (2012), 361–372.
51. Zhou, X., Hao, W., Shi, H., Hou, Y., Xu, Q., Calcium homeostasis disruption – a bridge connecting cadmium-induced apoptosis, autophagy and tumorigenesis. Oncol. Res. Treat. 38 (2015), 311–315.