Browse > Article
http://dx.doi.org/10.1007/s10059-009-0149-1

Activation of JNK and c-Jun Is Involved in Glucose Oxidase-Mediated Cell Death of Human Lymphoma Cells  

Son, Young-Ok (Graduate Center for Toxicology, University of Kentucky)
Jang, Yong-Suk (Department of Bioactive Material Sciences and Research Center of Bioactive Materials, Chonbuk National University)
Shi, Xianglin (Graduate Center for Toxicology, University of Kentucky)
Lee, Jeong-Chae (Department of Bioactive Material Sciences and Research Center of Bioactive Materials, Chonbuk National University)
Abstract
Mitogen-activated protein kinases (MAPK) affect the activation of activator protein-1 (AP-1), which plays an important role in regulating a range of cellular processes. However, the roles of these signaling factors on hydrogen peroxide ($H_2O_2$)-induced cell death are unclear. This study examined the effects of $H_2O_2$ on the activation of MAPK and AP-1 by exposing the cells to $H_2O_2$ generated by either glucose oxidase or a bolus addition. Exposing BJAB or Jurkat cells to $H_2O_2$ affected the activities of MAPK differently according to the method of $H_2O_2$ exposure. $H_2O_2$ increased the AP-1-DNA binding activity in these cells, where continuously generated $H_2O_2$ led to an increase in mainly the c-Fos, FosB and c-Jun proteins. The c-Jun-$NH_2$-terminal kinase (JNK)-mediated activation of c-Jun was shown to be related to the $H_2O_2$-induced cell death. However, the suppression of $H_2O_2$-induced oxidative stress by either JNK inhibitor or c-Jun specific antisense transfection was temporary in the cells exposed to glucose oxidase but not to a bolus $H_2O_2$. This was associated with the disruption of death signaling according to the severe and prolonged depletion of reduced glutathione. Overall, these results suggest that $H_2O_2$ may decide differently the mode of cell death by affecting the intracellular redox state of thiol-containing antioxidants, and this depends more closely on the duration exposed to $H_2O_2$ than the concentration of this agent.
Keywords
activator protein-1; antioxidant defense enzymes; human lymphoma cells; hydrogen peroxide; mitogen-activated protein kinase;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
Times Cited By Web Of Science : 3  (Related Records In Web of Science)
연도 인용수 순위
1 Cregan, S.P., Dawson, V.L., and Slack, R.S. (2004). Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene 23, 2785-2796   DOI   ScienceOn
2 Goppelt-Strube, M., and Resch, K. (1987). Polyunsaturated fatty acids are enriched in the plasma membranes of mitogenstimulated T-lymphocytes. Biochim. Biophys. Acta 904, 22-28   DOI   ScienceOn
3 Han, D.H., Hanawa, N., Saberi, B., and Kaplowitz, N. (2006). Hydrogen peroxide and redox modulation sensitize primary mouse hepatocytes to TNF-induced apoptosis. Free Radic. Biol. Med 41, 627-639   DOI   ScienceOn
4 Li, G.Y., and Osborne, N.N. (2008). Oxidative-induced apoptosis to an immortalized ganglion cell line is caspase independent but involves the activation of poly (ADP-ribose) polymerase and apoptosis-inducing factor. Brain Res. 1188, 35-43   DOI   PUBMED   ScienceOn
5 Maheshwari, A., Misro, M.M., Aggarwal, A., Sharma, R.K., and Nandan, D. (2009). Pathways involved in testicular germ cell apoptosis induced by H2O2 in vitro. FEBS J. 276, 870-881
6 Vollgraf, U., Wegner, M., and Richter-Landsberg, C. (1999). Activation of AP-1 and nuclear factor-kappaB transcription factors is involved in hydrogen peroxide-induced apoptotic cell death of oligodendrocytes. J. Neurochem. 73, 2501-2509   DOI   PUBMED
7 Maulik, N., Sato, M., Price, B.D., and Das, D.K. (1998). An essential role of NF-kappaB in tyrosine kinase signaling of p38 MAP kinase regulation of myocardial adaptation to ischemia. FEBS Lett. 429, 365-369   DOI   ScienceOn
8 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. USA 92, 4972-4976   DOI   ScienceOn
9 Hess, J., Angel, P., and Schorpp-Kistner, M. (2004). AP-1 subunits: quarrel and harmony among siblings. J. Cell Sci. 117, 5965- 5973   DOI   ScienceOn
10 Barbouti, A., Amorgianiotis, C., Kolettas, E., Kanavaros, P., and Galaris, D. (2007). Hydrogen peroxide inhibits caspase-dependent apoptosis by inactivating procaspase-9 in an iron-dependent manner. Free Radic. Biol. Med. 43, 1377-1387   DOI   ScienceOn
11 Wang, X., Martindale, J.L., Liu, Y., and Holbrook, N.J. (1998). The cellular response to oxidative stress: influences of mitogenactivated protein kinase signaling pathways on cell survival. Biochem. J. 333, 291-300   DOI
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   DOI   ScienceOn
13 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   DOI   PUBMED   ScienceOn
14 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   DOI   PUBMED
15 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   PUBMED
16 Chang, L., and Karin, M. (2001). Mammalian MAP kinase signaling cascades. Nature 410, 37-40   DOI   ScienceOn
17 Lin, T., and Yang, M.S. (2008). Benzo(α)pyrene-induced necrosis in the HepG(2) cells via PARP-1 activation and NAD(+) depletion. Toxicology 245, 147-153   DOI   PUBMED   ScienceOn
18 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   DOI   PUBMED   ScienceOn
19 Kang, Y.H., Yi, M.J., Kim, M.J., Park, M.T., Bae, S., Kang, C.M., Cho, C.K., Park, I.C., Park, M.J., Rhee, C.H., et al. (2004). Caspase- independent cell death by arsenic trioxide in human cervical cancer cells: reactive oxygen species-mediated poly(ADPribose) polymerase-1 activation signals apoptosis-inducing factor release from mitochondria. Cancer Res. 64, 8960-8967   DOI   ScienceOn
20 Ho, T.C., Yang, Y.C., Cheng, H.C., Wu, A.C., Chen, S.L., Chen, H.K., and Taso, Y.P. (2006). Activation of mitogen-activated protein kinases is essential for hydrogen peroxide-induced apoptosis in retinal pigment epithelial cells. Apoptosis 11, 1899-1908   DOI   ScienceOn
21 Sancho, P., Fernandez, C., Yuste, V.J., Amran, D., Ramos, A.M., de Blas, E., Susin, S.A., and Aller, P. (2006). Regulation of apoptosis/necrosis execution in cadmium-treated human promonocytic cells under different forms of oxidative stress. Apoptosis 11, 673-686   DOI   ScienceOn
22 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 flavonoid-induced apoptosis through down-regulation of JunD. Toxicol. Appl. Pharmacol. 227, 468-476   DOI   ScienceOn
23 Barbouti, A., Doulias, P.T., Nousis, L., Tenopoulou, M., and Galaris, D. (2002). DNA damage and apoptosis in hydrogen peroxideexposed Jurkat cells: bolus addition versus continuous generation of H2O2. Free Radic. Biol. Med. 33, 691-702   DOI   ScienceOn
24 Ishikawa, Y., and Kitamura, M. (2000). Anti-apoptotic effect of quercetin: intervention in the JNK- and ERK-mediated apoptotic pathways. Kidney Int. 58, 1078-1087   DOI   ScienceOn
25 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 peroxideexposed cells. Apoptosis 14, 796-808   DOI   ScienceOn
26 Chiarugi, P. (2008). Src redox regulation: there is more than meets the eye. Mol. Cells 26, 329-337   PUBMED
27 Meister, A., and Anderson, M.E. (1983). Glutathione. Annu. Rev. Biochem. 52, 711-760   DOI   ScienceOn
28 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   DOI   ScienceOn
29 Sen, C.K., and Packer, L. (1996). Antioxidant and redox regulation of gene transcription. FASEB J. 10, 709-720   DOI
30 Park, B.G., Yoo, C.I., Kim, H.T., Kwon, C.H., and Kim, Y.K. (2005). Role of mitogen-activated protein kinases in hydrogen peroxideinduced cell death in osteoblastic cells. Toxicology 215, 115-125   DOI   PUBMED   ScienceOn
31 Suzuki, T., Okuno, H., Yoshida, T., Endo, T., Nishina, H., and Iba, H. (1991). Difference in transcriptional regulatory function between c-Fos and Fra-2. Nucleic Acids Res. 19, 5537-5542   DOI   ScienceOn
32 Jeong, E.J., Lee, I.Y., Choi, J.S., Cheon, I.S., Kang, G., and Choe, J. (2004). Fibroblasts enhance the in vitro survival of human memory and naive B cells by maintaining intracellular levels of glutathione. Mol. Cells 17, 430-437   PUBMED
33 Son, Y.O., Lee, K.Y., Kook, S.H., Lee, H.C., Kim, J.G., Jeon, Y.M., and Jang, Y.S. (2004). Selective effects of quercetin on the cell growth and antioxidant defense system in normal versus transformed mouse hepatic cell lines. Eur. J. Pharmacol. 502, 195- 204   DOI   ScienceOn