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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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Over-expression of JunB inhibits mitochondrial stress and cytotoxicity in human lymphoma cells exposed to chronic oxidative stress

  • Son, Young-Ok (Graduate Center for Toxicology, University of Kentucky) ;
  • Heo, Jung-Sun (Institute of Oral Biosciences and BK 21 Program, Chonbuk National University) ;
  • Kim, Tae-Geum (Department of Bioactive Material Sciences and Research Center of Bioactive Materials, Chonbuk National University) ;
  • Jeon, Young-Mi (Institute of Oral Biosciences and BK 21 Program, Chonbuk National University) ;
  • Kim, Jong-Ghee (Institute of Oral Biosciences and BK 21 Program, Chonbuk National University) ;
  • Lee, Jeong-Chae (Institute of Oral Biosciences and BK 21 Program, Chonbuk National University)
  • Published : 2010.01.31
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Abstract

Activator protein-1 can induce either cell survival or death, which is controlled by opposing effects of different Jun members. It is generally accepted that c-Jun is pro-apoptotic, but that JunD is anti-apoptotic in stress-exposed cells. Additionally, although there are reports suggesting that JunB plays a protective role, its role in stress-induced apoptosis remains unclear. Here, we investigated the role of JunB in $H_2O_2$-induced cell death using cells that over-expressed the protein or were transfected with si-JunB. Inhibition of JunB expression accelerated $H_2O_2$-mediated loss of mitochondrial membrane potential (MMP) and cytotoxicity. Conversely, over-expression of JunB protein led to significant inhibition of the MMP loss and cell death. The increase in JunB expression also attenuated nuclear relocation of apoptosis-inducing factor and mitochondrial Bcl-2 reduction that occurred following $H_2O_2$ exposure. These results suggest that JunB can signal survival against oxidant-mediated cell death by suppressing mitochondrial stress.

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References

  1. Jacobs-Helber, S. M., Wickrema, A., Birrer, M. J. and Sawyer, S. T. (1998) AP1 regulation of proliferation and initiation of apoptosis in erythropoietin-dependent erythroid cells. Mol. Cell. Biol. 18, 3699-3707 https://doi.org/10.1128/MCB.18.7.3699
  2. Weitzman, J. B., Fiette, L., Matsuo, K. and Yaniv, M. (2000)JunD protects cells from p53-dependent senescence and apoptosis. Mol. Cell 6, 1109-1119 https://doi.org/10.1016/S1097-2765(00)00109-X
  3. Lamb, J. A., Ventura, J. J., Hess, P., Flavell, R. A. and Davis,R. J. (2003) JunD mediates survival signaling by the JNK signal transduction pathway. Mol. Cell 11, 1479-1489 https://doi.org/10.1016/S1097-2765(03)00203-X
  4. Hess, J., Angel, P. and Schorpp-Kistner, M. (2004) AP-1 subunits: quarrel and harmony among siblings. J. Cell Sci. 117, 5965-5973 https://doi.org/10.1242/jcs.01589
  5. Kook, S. H., Son, Y. O., Jang, Y. S., Lee, K. Y., Lee, S. A.,Kim, B. S., Lee, H. J. and Lee J. C. (2008) Inhibition of c-Jun N-terminal kinase sensitizes tumor cells to flavonoidinduced apoptosis through down-regulation of JunD. Toxicol. Appl. Pharmacol. 227, 468-476 https://doi.org/10.1016/j.taap.2007.11.004
  6. Gurzov, E. N., Ortis, F., Bakiri, L., Wagner, E. F. and Eizirik, D. L. (2008) JunB inhibits ER stress and apoptosis in pancreatic beta cells. PLoS One 3, 1-10
  7. Cevik, M. O., Katsuyama, M., Kanda, S., Kaneko, T.,Iwata, K., Ibi, M., Matsuno, K., Kakehi, T., Cui, W.,Sasaki, M. and Yabe-Nishimura, C. (2008) The AP-1 site is essential for the promoter activity of NOX1/NADPH oxidase, a vascular superoxide-producing enzyme: Possible involvement of the ERK1/2-JunB pathway. Biochem. Biophys. Res. Commun. 374, 351-355 https://doi.org/10.1016/j.bbrc.2008.07.027
  8. Shaulian, E. and Karin, M. (2002) AP-1 as a regulator of cell life and death. Nat. Cell Biol. 4, E131-136 https://doi.org/10.1038/ncb0502-e131
  9. Son, Y. O., Jang, Y. S., Heo, J. S., Chung, W. T., Choi, K.C. and Lee, J. C. (2009) Apoptosis-inducing factor plays a critical role in caspase-independent, pyknotic cell death in hydrogen peroxide-exposed cells. Apoptosis 14, 796-808 https://doi.org/10.1007/s10495-009-0353-7
  10. Jeong, S. Y. and Seol, D. W. (2008) The role of mitochondria in apoptosis. BMB Rep. 41, 11-22 https://doi.org/10.5483/BMBRep.2008.41.1.011
  11. Son, Y. O., Kook, S. H., Jang, Y. S., Shi, X. and Lee, J. C.(2009) Critical role of poly (ADP-ribose) polymerase-1 in modulating the mode of cell death caused by continuous oxidative stress. J. Cell. Biochem. 108, 989-997 https://doi.org/10.1002/jcb.22332
  12. Gass, P. and Herdegen, T. (1995) Neuronal expression of AP-1 proteins in excitotoxic neurodegenerative disorders and following nerve fiber lesions. Prog. Neurobiol. 47, 257-290 https://doi.org/10.1016/0301-0082(95)00022-4
  13. Yoshioka, K., Deng, T., Cavigelli, M. and Karin, M. (1995)Antitumor promotion by phenolic antioxidants: inhibition of AP-1 activity through induction of Fra expression. Proc. Natl. Acad. Sci. U.S.A. 92, 4972-4976 https://doi.org/10.1073/pnas.92.11.4972
  14. Hilfiker-Kleiner, D., Hilfiker, A., Kaminski, K., Schaefer, A.,Park, J. K., Michel, K., Quint, A., Yaniv, M., Weitzman, J. B.and Drexler, H. (2005) Lack of JunD promotes pressure overload-induced apoptosis, hypertrophic growth, and angiogenesis in the heart. Circulation 112, 1470-1477 https://doi.org/10.1161/CIRCULATIONAHA.104.518472
  15. Deng, T. and Karin, M. (1993) JunB differs from c-Jun in its DNA-binding and dimerization domains, and represses c-Jun by formation if inactive heterodimers. Genes Dev. 7, 479-490 https://doi.org/10.1101/gad.7.3.479
  16. Kallunki, T., Deng, T., Hibi, M. and Karin, M. (1996) c-Jun can recruit JNK to phosphorylate dimerization partners via specific docking interactions. Cell 87, 929-939 https://doi.org/10.1016/S0092-8674(00)81999-6
  17. Gurzov, E. N., Bakiri, L., Alfaro, J. M., Wagner, E. F. and Izquierdo, M. (2008) Targeting c-Jun and JunB proteins as potential anticancer cell therapy. Oncogene 27, 641-652 https://doi.org/10.1038/sj.onc.1210690
  18. Antonsson, B. (2004) Mitochondrial and the Bcl-2 family proteins in apoptosis signaling pathways. Mol. Cell. Biochem. 256/257, 141-155
  19. Lei, K., Nimnual, A., Zong, W. X., Kennedy, N. J., Flavell, R.A., Thompson, C. B., Bar-Sagi, D. and Davis, R. J. (2002) The Bax subfamily of Bcl2-related proteins is essential for apoptotic signal transduction by c-Jun NH(2)-terminal kinase. Mol. Cell. Biol. 22, 4929-4942 https://doi.org/10.1128/MCB.22.13.4929-4942.2002
  20. Gao, M., Labuda, T., Xia, Y., Gallagher, E., Fang, D., Liu, Y.C. and Karin, M. (2004) Jun turnover is controlled through JNK-dependent phosphorylation of the E3 ligase Itch. Science 306, 271-275 https://doi.org/10.1126/science.1099414
  21. Kang, C. D., Jang, J. H., Kim, K. W., Lee, H. J., Jeong, C. S.,Kim, C. M., Kim, S. H. and Chung, B. S. (1998) Activation of c-jun N-terminal kinase/stress-activated protein kinase and the decreased ratio of Bcl-2 to Bax are associated with the autooxidized dopamine-induced apoptosis in PC12 cells. Neurosci. Lett. 256, 37-40 https://doi.org/10.1016/S0304-3940(98)00751-4
  22. Yamamoto, K., Ichijo, H. and Korsmeyer, S. J. (1999) BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Mol. Cell. Biol. 19, 8469-8478 https://doi.org/10.1128/MCB.19.12.8469
  23. Lee, L., Irani, K. and Finkel, T. (1998) Bcl-2 regulates nonapoptotic signal transduction: inhibition of c-Jun N-terminal kinase (JNK) activation by IL-1 beta and hydrogen peroxide. Mol. Genet. Metab. 64, 19-24 https://doi.org/10.1006/mgme.1998.2704
  24. Xia, Z., Dickens, M., Raingeaud, J., Davis, R. J. and Greenderg,M. E. (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270, 1326-1331 https://doi.org/10.1126/science.270.5240.1326
  25. Park, B. G., Yoo, C. I., Kim, H. T., Jwon, C. H. and Kim,Y. K. (2005) Role of mitogen-activated protein kinases in hydrogen peroxide-induced cell death in osteoblastic cells. Apoptosis 215, 115-125
  26. Son, Y. O., Jang, Y. S., Shi, X. and Lee, J. C. (2009) Activation of JNK and c-Jun is involved in glucose-oxidase-mediated cell death of human lymphoma cells. Mol. Cells In press https://doi.org/10.1007/s10059-009-0149-1
  27. Lee, J. C., Son, Y. O., Choi, K. C. and Jang, Y. S. (2006)Hydrogen peroxide induces apoptosis of BJAB cells due to formation of hydroxyl radicals via intracellular iron-mediated Fenton chemistry in glucose oxidase-mediated oxidative stress. Mol. Cells 22, 21-29
  28. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254 https://doi.org/10.1016/0003-2697(76)90527-3

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