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Zinc finger and BTB domain-containing protein 3 is essential for the growth of cancer cells

  • Lim, Ji-Hong (Department of Biomedical Chemistry, College of Biomedical and Health Science, Konkuk University)
  • Received : 2014.04.07
  • Accepted : 2014.05.20
  • Published : 2014.07.31

Abstract

ZBTB3 belongs to the Zinc finger and BTB/POZ domain containing transcription factor family; however, its biological role has rarely been studied. We demonstrate for the first time, to our knowledge, that ZBTB3 is an essential factor for cancer cell growth via the regulation of the ROS detoxification pathway. Suppression of ZBTB3 using two different short hairpin RNAs in human melanoma, lung carcinoma, and breast carcinoma results in diminished cell growth. In addition, we found that suppression of ZBTB3 activates a caspase cascade, including caspase-9, -3, and PARP leading to cellular apoptosis, resulting from failed ROS detoxification. We identified that ZBTB3 plays an important role in the gene expression of ROS detoxification enzymes. Our results reveal that ZBTB3 may play a critical role in cancer cell growth via the ROS detoxification system. Therefore, therapeutic strategies that target ZBTB3 could be used in selective cancer treatments.

Keywords

References

  1. Lee, S. U. and Maeda, T. (2012) POK/ZBTB proteins: an emerging family of proteins that regulate lymphoid development and function. Immunol. Rev. 247, 107-119. https://doi.org/10.1111/j.1600-065X.2012.01116.x
  2. Kelly, K. F and Daniel, J. M. (2006) POZ for effect--POZ-ZF transcription factors in cancer and development. Trends. Cell Biol. 16, 578-587. https://doi.org/10.1016/j.tcb.2006.09.003
  3. Costoya, J. A. (2007) Functional analysis of the role of POK transcriptional repressors. Brief. Funct. Genomic. Proteomic. 6, 8-18. https://doi.org/10.1093/bfgp/elm002
  4. Perez-Torrado, R., Yamada, D. and Defossez, P. A. (2006) Born to bind: the BTB protein-protein interaction domain. Bioessays 28, 1194-1202. https://doi.org/10.1002/bies.20500
  5. Zheng, J., Xiong, D., Sun, X., Wang, J., Hao, M., Ding, T., Xiao, G., Wang, X., Mao, Y., Fu, Y., Shen, K. and Wang, J. (2012) Signification of hypermethylated in cancer 1 (HIC1) as tumor suppressor gene in tumor progression. Cancer Microenviron 5, 285-293. https://doi.org/10.1007/s12307-012-0103-1
  6. Boulay, G., Dubuissez, M., Van Rechem, C., Forget, A., Helin, K., Ayrault, O. and Leprince, D. (2012) Hypermethylated in cancer 1 (HIC1) recruits polycomb repressive complex 2 (PRC2) to a subset of its target genes through interaction with human polycomb-like (hPCL) proteins. J. Biol. Chem. 287, 10509-10524. https://doi.org/10.1074/jbc.M111.320234
  7. Albagli-Curiel, O. (2003) Ambivalent role of BCL6 in cell survival and transformation. Oncogene 22, 507-516. https://doi.org/10.1038/sj.onc.1206152
  8. Polo, J. M., Dell'Oso, T., Ranuncolo, S. M., Cerchietti, L., Beck, D., Da silva, G. F., Prive, G. G., Licht, J. D. and Melnick, A. (2004) Specific peptide interference reveals BCL6 transcriptional and oncogenic mechanisms in B-cell lymphoma cells. Nat. Med. 10, 1329-1335. https://doi.org/10.1038/nm1134
  9. Kim, K., Chadalapaka, G., Lee, S. O., Yamada, D., Sastre-Garau, X., Defossez, P. A., Park, Y. Y., Lee, J. S. and Safe, S. (2012) Identification of oncogenic microRNA-17-92/ZBTB4/specificity protein axis in breast cancer. Oncogene 31, 1034-1044. https://doi.org/10.1038/onc.2011.296
  10. Irani, K., Xia, Y., Zweier, J. L., Sollott, S. J., Der, C. J., Fearon, E. R., Sundaresan, M., Finkel, T. and Goldschmidt-Clermont, P. J. (1997) Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 275, 1649-1652. https://doi.org/10.1126/science.275.5306.1649
  11. Wu, W. S. (2006) The signaling mechanism of ROS in tumor progression. Cancer Metastasis Rev. 25, 695-705.
  12. Finkel, T. (2011) Signal transduction by reactive oxygen species. J. Cell Biol. 194, 7-15. https://doi.org/10.1083/jcb.201102095
  13. Sena, L. A. and Chandel, N. S. (2012) Physiological roles of mitochondrial reactive oxygen species. Mol. Cell 48, 158-167. https://doi.org/10.1016/j.molcel.2012.09.025
  14. Dixon, S. J. and Stockwell, B. R. (2014) The role of iron and reactive oxygen species in cell death. Nat. Chem. Biol. 10, 9-17. https://doi.org/10.1038/nchembio.1416
  15. Trachootham, D., Alexandre, J. and Huang, P. (2009) Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach?. Nat. Rev. Drug. Discov. 8, 579-591. https://doi.org/10.1038/nrd2803
  16. Vazquez, F., Lim, J. H., Chim, H., Bhalla, K., Girnun, G., Pierce, K., Clish, C. B., Granter, S. R., Widlund, H. R., Spiegelman, B. M. and Puigserver, P. (2013) PGC1alpha expression defines a subset of human melanoma tumors with increased mitochondrial capacity and resistance to oxidative stress. Cancer Cell 23, 287-301. https://doi.org/10.1016/j.ccr.2012.11.020
  17. Trachootham, D., Zhou, Y., Zhang, H., Demizu, Y., Chen, Z., Pelicano, H., Chiao, P. J., Achanta, G., Arlinghaus, R. B., Liu, J. and Huang, P. (2006) Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate. Cancer Cell 10, 241-252. https://doi.org/10.1016/j.ccr.2006.08.009
  18. Singh, A., Misra, V., Thimmulappa, R. K., Lee, H., Ames, S., Hoque, M. O., Herman, J. G., Baylin, S. B., Sidransky, D., Gabrielson, E., Brock, M. V. and Biswal, S. (2006) Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer. PLoS Med. 3, e420. https://doi.org/10.1371/journal.pmed.0030420
  19. Park, H. J., Carr, J. R., Wang, Z., Nogueira, V., Hay, N., Tyner, A. L., Lau, L. F., Costa, R. H. and Raychaudhuri, P. (2009) FoxM1, a critical regulator of oxidative stress during oncogenesis. EMBO J. 28, 2908-2918. https://doi.org/10.1038/emboj.2009.239
  20. Raj, L., Ide, T., Gurkar, A. U., Foley, M., Schenone, M., Li, X., Tolliday, N. J., Golub, T. R., Carr, S. A., Shamji, A. F., Stern, A. M., Mandinova, A., Schreiber, S. L. and Lee, S. W. (2011) Selective killing of cancer cells by a small molecule targeting the stress response to ROS. Nature 475, 231-234. https://doi.org/10.1038/nature10167
  21. Barrett, C. W., Smith, J. J., Lu, L. C., Markham, N., Stengel, K. R., Short, S. P., Zhang, B., Hunt, A. A., Fingleton, B. M., Carnahan, R. H., Engel, M. E., Chen, X., Beauchamp, R. D., Wilson, K. T., Hiebert, S. W., Reynolds, A. B. and Williams, C. S. (2012) Kaiso directs the transcriptional corepressor MTG16 to the Kaiso binding site in target promoters. PLoS One 7, e51205. https://doi.org/10.1371/journal.pone.0051205
  22. Cho, J. H., Kim, M. J., Kim, K. J. and Kim, J. R. (2012) POZ/BTB and AT-hook-containing zinc finger protein 1 (PATZ1) inhibits endothelial cell senescence through a p53 dependent pathway. Cell Death Differ. 19, 703-712. https://doi.org/10.1038/cdd.2011.142
  23. Valentino, T., Palmieri, D., Vitiello, M., Pierantoni, G. M., Fusco, A. and Fedele, M. (2013) PATZ1 interacts with p53 and regulates expression of p53-target genes enhancing apoptosis or cell survival based on the cellular context. Cell Death Dis. 4, e963. https://doi.org/10.1038/cddis.2013.500

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