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Article

Anti-apoptotic proteins and catalase-dependent apoptosis resistance in nickel chloride-transformed human lung epithelial cells

  • Authors:
    • Yu-Xiu Yang
    • Xiu-Ling Li
    • Lei Wang
    • Shuang-Yin Han
    • Yan-Rui Zhang
    • Poyil Pratheeshkumar
    • Xin Wang
    • Jian Lu
    • Yuan-Qin Yin
    • Li-Juan Sun
    • Amit Budhraja
    • Andrew J. Hitron
    • Song-Ze Ding
  • View Affiliations / Copyright

    Affiliations: Department of Internal Medicine, Henan Provincial People's Hospital, Zhengzhou University, Zhengzhou, Henan 450000, P.R. China, Graduate Center for Toxicology, College of Medicine, University of Kentucky, Lexington, KY 40536, USA
  • Pages: 936-946
    |
    Published online on: July 3, 2013
       https://doi.org/10.3892/ijo.2013.2004
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Abstract

Chronic exposure to nickel compounds is associated with increased incidence of certain types of human cancer, including lung and nasal cancers. Despite intensive investigation, the oncogenic processes remain poorly understood. Apoptosis resistance is a key feature for tumor cells to escape physiological surveillance and acquire growth advantage over normal cells. Although NiCl2 exposure induces transformation of human lung epithelial cells, little information is available with regard to its molecular mechanisms, it is also not clear if the transformed cells are apoptosis resistant and tumorigenic. We explored the apoptosis resistance properties of nickel chloride‑transformed human lung epithelial cells and the underlying mechanisms. The results showed that transformed BEAS-2B human lung epithelial cells are resistant to NiCl2-induced apoptosis. They have increased Bcl-2, Bcl-xL and catalase protein levels over the passage matched non‑transformed counterparts. The mechanisms of apoptosis resistance are mitochondria‑mediated and caspase-dependent. Forced overexpression of Bcl-2, Bcl-xL and catalase proteins reduced NiCl2-induced cell death; siRNA‑mediated knockdown of their expression sensitized the cells to nickel-induced apoptosis, suggesting that Bcl-2, Bcl-xl and catalase protein expression plays a critical role in apoptosis resistance. Akt also participates in this process, as its overexpression increases Bcl-xL protein expression levels and attenuates NiCl2-induced apoptosis. Furthermore, transformed cells are tumorigenic in a xenograft model. Together, these results demonstrate that nickel-transformed cells are apoptosis‑resistant and tumorigenic. Increased expression of Bcl-2, Bcl-xL and catalase proteins are important mechanisms contributing to transformed cell oncogenic properties.
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View References

1 

Costa M: Molecular mechanisms of nickel carcinogenesis. Annu Rev Pharmacol Toxicol. 31:321–337. 1991. View Article : Google Scholar

2 

Doll R, Morgan LG and Speizer FE: Cancers of the lung and nasal sinuses in nickel workers. Br J Cancer. 24:623–632. 1970. View Article : Google Scholar : PubMed/NCBI

3 

Costa M, Davidson TL, Chen H, et al: Nickel carcinogenesis: epigenetics and hypoxia signaling. Mutat Res. 592:79–88. 2005. View Article : Google Scholar : PubMed/NCBI

4 

Lu H, Shi X, Costa M and Huang C: Carcinogenic effect of nickel compounds. Mol Cell Biochem. 279:45–67. 2005. View Article : Google Scholar

5 

Salnikow K and Zhitkovich A: Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis: nickel, arsenic, and chromium. Chem Res Toxicol. 21:28–44. 2008. View Article : Google Scholar : PubMed/NCBI

6 

Salnikow K and Costa M: Epigenetic mechanisms of nickel carcinogenesis. J Environ Pathol Toxicol Oncol. 19:307–318. 2000.

7 

Davidson T, Chen H, Garrick MD, D’Angelo G and Costa M: Soluble nickel interferes with cellular iron homeostasis. Mol Cell Biochem. 279:157–162. 2005. View Article : Google Scholar : PubMed/NCBI

8 

Pan J, Chang Q, Wang X, et al: Reactive oxygen species-activated Akt/ASK1/p38 signaling pathway in nickel compound-induced apoptosis in BEAS 2B cells. Chem Res Toxicol. 23:568–577. 2010. View Article : Google Scholar : PubMed/NCBI

9 

Pan JJ, Chang QS, Wang X, et al: Activation of Akt/GSK3β and Akt/Bcl-2 signaling pathways in nickel-transformed BEAS-2B cells. Int J Oncol. 39:1285–1294. 2011.

10 

Cory S and Adams JM: The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer. 2:647–656. 2002. View Article : Google Scholar : PubMed/NCBI

11 

Gross A, McDonnell JM and Korsmeyer SJ: BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13:1899–1911. 1999. View Article : Google Scholar : PubMed/NCBI

12 

Pugazhenthi S, Nesterova A, Sable C, et al: Akt/protein kinase B up-regulates Bcl-2 expression through cAMP-response element-binding protein. J Biol Chem. 275:10761–10766. 2000. View Article : Google Scholar : PubMed/NCBI

13 

Ding SZ, Yang YX, Li XL, et al: Epithelial-mesenchymal transition during oncogenic transformation induced by hexavalent chromium involves reactive oxygen species-dependent mechanism in lung epithelial cells. Toxicol Appl Pharmacol. 269:61–71. 2013. View Article : Google Scholar

14 

Zhou BP, Hu MC, Miller SA, et al: HER-2/neu blocks tumor necrosis factor-induced apoptosis via the Akt/NF-kappaB pathway. J Biol Chem. 275:8027–8031. 2000. View Article : Google Scholar : PubMed/NCBI

15 

Ding SZ, Fischer W, Kaparakis-Liaskos M, et al: Helicobacter pylori-induced histone modification, associated gene expression in gastric epithelial cells, and its implication in pathogenesis. PLoS One. 5:e98752010. View Article : Google Scholar

16 

Cossarizza A, Baccarani-Contri M, Kalashnikova G and Franceschi C: A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5,5′,6,6′-tetrachloro-1,1′,3,3′-tetraethylbenzimidazolcarbocyanine iodide (JC-1). Biochem Biophys Res Commun. 197:40–45. 1993.PubMed/NCBI

17 

Cheng EH, Wei MC, Weiler S, et al: BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol Cell. 8:705–711. 2001. View Article : Google Scholar : PubMed/NCBI

18 

Chang Q, Pan J, Wang X, Zhang Z, Chen F and Shi X: Reduced reactive oxygen species-generating capacity contributes to the enhanced cell growth of arsenic-transformed epithelial cells. Cancer Res. 70:5127–5135. 2010. View Article : Google Scholar

19 

Dunnick JK, Elwell MR, Radovsky AE, et al: Comparative carcinogenic effects of nickel subsulfide, nickel oxide, or nickel sulfate hexahydrate chronic exposures in the lung. Cancer Res. 55:5251–5256. 1995.PubMed/NCBI

20 

Oller AR, Costa M and Oberdorster G: Carcinogenicity assessment of selected nickel compounds. Toxicol Appl Pharmacol. 143:152–166. 1997. View Article : Google Scholar : PubMed/NCBI

21 

Zhao J, Shi X, Castranova V and Ding M: Occupational toxicology of nickel and nickel compounds. J Environ Pathol Toxicol Oncol. 28:177–208. 2009. View Article : Google Scholar : PubMed/NCBI

22 

Kim YJ, Ahn JY, Liang P, Ip C, Zhang Y and Park YM: Human prx1 gene is a target of Nrf2 and is up-regulated by hypoxia/reoxygenation: implication to tumor biology. Cancer Res. 67:546–554. 2007. View Article : Google Scholar : PubMed/NCBI

23 

Yip KW and Reed JC: Bcl-2 family proteins and cancer. Oncogene. 27:6398–6406. 2008. View Article : Google Scholar : PubMed/NCBI

24 

Catz SD and Johnson JL: Transcriptional regulation of bcl-2 by nuclear factor kappa B and its significance in prostate cancer. Oncogene. 20:7342–7351. 2001. View Article : Google Scholar : PubMed/NCBI

25 

Bigelow RL, Chari NS, Unden AB, et al: Transcriptional regulation of bcl-2 mediated by the sonic hedgehog signaling pathway through gli-1. J Biol Chem. 279:1197–1205. 2004. View Article : Google Scholar : PubMed/NCBI

26 

Ding J, Zhang X, Li J, et al: Nickel compounds render anti-apoptotic effect to human bronchial epithelial BEAS-2B cells by induction of cyclooxygenase-2 through an IKKbeta/p65-dependent and IKKalpha- and p50-independent pathway. J Biol Chem. 281:39022–39032. 2006. View Article : Google Scholar : PubMed/NCBI

27 

Lawlor MA and Alessi DR: PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? J Cell Sci. 114:2903–2910. 2001.PubMed/NCBI

28 

Morley S, Wagner J, Kauppinen K, Sherman M and Manor D: Requirement for Akt-mediated survival in cell transformation by the dbl oncogene. Cell Signal. 19:211–218. 2007. View Article : Google Scholar : PubMed/NCBI

29 

Bellacosa A, Kumar CC, Di Cristofano A and Testa JR: Activation of AKT kinases in cancer: implications for therapeutic targeting. Adv Cancer Res. 94:29–86. 2005. View Article : Google Scholar : PubMed/NCBI

30 

Manning BD and Cantley LC: AKT/PKB signaling: navigating downstream. Cell. 129:1261–1274. 2007. View Article : Google Scholar : PubMed/NCBI

31 

Li Q, Suen TC, Sun H, Arita A and Costa M: Nickel compounds induce apoptosis in human bronchial epithelial Beas-2B cells by activation of c-Myc through ERK pathway. Toxicol Appl Pharmacol. 235:191–198. 2009. View Article : Google Scholar : PubMed/NCBI

32 

Ding J, He G, Gong W, et al: Effects of nickel on cyclin expression, cell cycle progression and cell proliferation in human pulmonary cells. Cancer Epidemiol Biomarkers Prev. 18:1720–1729. 2009. View Article : Google Scholar : PubMed/NCBI

33 

Kim K, Lee SH, Seo YR, Perkins SN and Kasprzak KS: Nickel(II)-induced apoptosis in murine T cell hybridoma cells is associated with increased fas ligand expression. Toxicol Appl Pharmacol. 185:41–47. 2002. View Article : Google Scholar : PubMed/NCBI

34 

Zhao J, Bowman L, Zhang X, et al: Metallic nickel nano- and fine particles induce JB6 cell apoptosis through a caspase-8/AIF mediated cytochrome c-independent pathway. J Nanobiotechnol. 7:22009. View Article : Google Scholar : PubMed/NCBI

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Copy and paste a formatted citation
Spandidos Publications style
Yang Y, Li X, Wang L, Han S, Zhang Y, Pratheeshkumar P, Wang X, Lu J, Yin Y, Sun L, Sun L, et al: Anti-apoptotic proteins and catalase-dependent apoptosis resistance in nickel chloride-transformed human lung epithelial cells. Int J Oncol 43: 936-946, 2013.
APA
Yang, Y., Li, X., Wang, L., Han, S., Zhang, Y., Pratheeshkumar, P. ... Ding, S. (2013). Anti-apoptotic proteins and catalase-dependent apoptosis resistance in nickel chloride-transformed human lung epithelial cells. International Journal of Oncology, 43, 936-946. https://doi.org/10.3892/ijo.2013.2004
MLA
Yang, Y., Li, X., Wang, L., Han, S., Zhang, Y., Pratheeshkumar, P., Wang, X., Lu, J., Yin, Y., Sun, L., Budhraja, A., Hitron, A. J., Ding, S."Anti-apoptotic proteins and catalase-dependent apoptosis resistance in nickel chloride-transformed human lung epithelial cells". International Journal of Oncology 43.3 (2013): 936-946.
Chicago
Yang, Y., Li, X., Wang, L., Han, S., Zhang, Y., Pratheeshkumar, P., Wang, X., Lu, J., Yin, Y., Sun, L., Budhraja, A., Hitron, A. J., Ding, S."Anti-apoptotic proteins and catalase-dependent apoptosis resistance in nickel chloride-transformed human lung epithelial cells". International Journal of Oncology 43, no. 3 (2013): 936-946. https://doi.org/10.3892/ijo.2013.2004
Copy and paste a formatted citation
x
Spandidos Publications style
Yang Y, Li X, Wang L, Han S, Zhang Y, Pratheeshkumar P, Wang X, Lu J, Yin Y, Sun L, Sun L, et al: Anti-apoptotic proteins and catalase-dependent apoptosis resistance in nickel chloride-transformed human lung epithelial cells. Int J Oncol 43: 936-946, 2013.
APA
Yang, Y., Li, X., Wang, L., Han, S., Zhang, Y., Pratheeshkumar, P. ... Ding, S. (2013). Anti-apoptotic proteins and catalase-dependent apoptosis resistance in nickel chloride-transformed human lung epithelial cells. International Journal of Oncology, 43, 936-946. https://doi.org/10.3892/ijo.2013.2004
MLA
Yang, Y., Li, X., Wang, L., Han, S., Zhang, Y., Pratheeshkumar, P., Wang, X., Lu, J., Yin, Y., Sun, L., Budhraja, A., Hitron, A. J., Ding, S."Anti-apoptotic proteins and catalase-dependent apoptosis resistance in nickel chloride-transformed human lung epithelial cells". International Journal of Oncology 43.3 (2013): 936-946.
Chicago
Yang, Y., Li, X., Wang, L., Han, S., Zhang, Y., Pratheeshkumar, P., Wang, X., Lu, J., Yin, Y., Sun, L., Budhraja, A., Hitron, A. J., Ding, S."Anti-apoptotic proteins and catalase-dependent apoptosis resistance in nickel chloride-transformed human lung epithelial cells". International Journal of Oncology 43, no. 3 (2013): 936-946. https://doi.org/10.3892/ijo.2013.2004
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