JNK-dependent Stat3 phosphorylation contributes to Akt activation in response to arsenic exposure

Toxicological Sciences

Volumn 129, Issue 2, 2012, Pages 363-371

  Liu, Jia ^a,b   Chen, Bailing ^a   Lu, Yongju ^a   Guan, Youfei ^b   Chen, Fei ^a  

^a WAYNE STATE UNIVERSITY   (United States)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; ARSENIC; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE B; SERINE; SMALL INTERFERING RNA; STAT3 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE 1; VASCULOTROPIN;

ANIMAL CELL; ARTICLE; BRONCHUS MUCOSA; CELL MIGRATION; CONTROLLED STUDY; DOSE RESPONSE; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVATION; ENZYME INDUCTION; EPITHELIUM CELL; GENE SILENCING; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ARSENIC; CELL LINE; COCULTURE TECHNIQUES; ENZYME ACTIVATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; INTERLEUKIN-6; MAP KINASE KINASE 4; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SERINE; STAT3 TRANSCRIPTION FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84866624638     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfs199     Document Type: Article

References (46)

1. Androutsellis-Theotokis, A., Leker, R. R., Soldner, F., Hoeppner, D. J., Ravin, R., Poser, S. W., Rueger, M. A., Bae, S. K., Kittappa, R., and McKay, R. D. (2006). Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442, 823-826.
2. Beezhold, K., Liu, J., Kan, H., Meighan, T., Castranova, V., Shi, X., and Chen, F. (2011). miR-190-mediated downregulation of PHLPP contributes to arsenic-induced Akt activation and carcinogenesis. Toxicol. Sci. 123, 411-420.
3. Bernstam, L., and Nriagu, J. (2000). Molecular aspects of arsenic stress. J. Toxicol. Environ. Health. B. Crit. Rev. 3, 293-322.
4. Blando, J. M., Carbajal, S., Abel, E., Beltran, L., Conti, C., Fischer, S., and DiGiovanni, J. (2011). Cooperation between Stat3 and Akt signaling leads to prostate tumor development in transgenic mice. Neoplasia 13, 254-265.
5. Bogoyevitch, M. A., and Arthur, P. G. (2008). Inhibitors of c-Jun N-terminal kinases: Junk no more? Biochim. Biophys. Acta 1784, 76-93.
6. Bogoyevitch, M. A., and Kobe, B. (2006). Uses for JNK: The many and varied substrates of the c-Jun N-terminal kinases. Microbiol. Mol. Biol. Rev. 70, 1061-1095.
7. Brill, L. M., Xiong, W., Lee, K. B., Ficarro, S. B., Crain, A., Xu, Y., Terskikh, A., Snyder, E. Y., and Ding, S. (2009). Phosphoproteomic analysis of human embryonic stem cells. Cell Stem Cell 5, 204-213.
8. Celik, I., Gallicchio, L., Boyd, K., Lam, T. K., Matanoski, G., Tao, X., Shiels, M., Hammond, E., Chen, L., Robinson, K. A., et al. (2008). Arsenic in drinking water and lung cancer: A systematic review. Environ. Res. 108, 48-55.
9. Chang, Q., Zhang, Y., Beezhold, K. J., Bhatia, D., Zhao, H., Chen, J., Castranova, V., Shi, X., and Chen, F. (2009). Sustained JNK1 activation is associated with altered histone H3 methylations in human liver cancer. J. Hepatol. 50, 323-333.
10. Chen, C. L., Hsu, L. I., Chiou, H. Y., Hsueh, Y. M., Chen, S. Y., Wu, M. M., and Chen, C. J.; Blackfoot Disease Study Group. (2004). Ingested arsenic, cigarette smoking, and lung cancer risk: A follow-up study in arseniasis-endemic areas in Taiwan. JAMA 292, 2984-2990.
11. Chen, F. (2012). JNK-induced apoptosis, compensatory growth, and cancer stem cells. Cancer Res. 72, 379-386.
12. Chen, F., Beezhold, K., and Castranova, V. (2009a). JNK1, a potential therapeutic target for hepatocellular carcinoma. Biochim. Biophys. Acta 1796, 242-251.
13. Chen, L., Ovesen, J. L., Puga, A., and Xia, Y. (2009b). Distinct contributions of JNK and p38 to chromium cytotoxicity and inhibition of murine embryonic stem cell differentiation. Environ. Health Perspect. 117, 1124-1130.
14. Chen, F., Lu, Y., Zhang, Z., Vallyathan, V., Ding, M., Castranova, V., and Shi, X. (2001). Opposite effect of NF-kappa B and c-Jun N-terminal kinase on p53-independent GADD45 induction by arsenite. J. Biol. Chem. 276, 11414-11419.
15. Chen, F., Zhang, Z., Bower, J., Lu, Y., Leonard, S. S., Ding, M., Castranova, V., Piwnica-Worms, H., and Shi, X. (2002). Arsenite-induced Cdc25C degradation is through the KEN-box and ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. U.S.A. 99, 1990-1995.
16. Chiu, H. F., Ho, S. C., and Yang, C. Y. (2004). Lung cancer mortality reduction after installation of tap-water supply system in an arseniasis-endemic area in Southwestern Taiwan. Lung Cancer 46, 265-270.
17. Decker, T., and Kovarik, P. (2000). Serine phosphorylation of STATs. Oncogene 19, 2628-2637.
18. Dérijard, B., Hibi, M., Wu, I. H., Barrett, T., Su, B., Deng, T., Karin, M., and Davis, R. J. (1994). JNK1: A protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76, 1025-1037.
19. Galligan, C. L., Siebert, J. C., Siminovitch, K. A., Keystone, E. C., Bykerk, V., Perez, O. D., and Fish, E. N. (2009). Multiparameter phospho-flow analysis of lymphocytes in early rheumatoid arthritis: Implications for diagnosis and monitoring drug therapy. PLoS ONE 4, e6703.
20. Hara, M., Yuasa, S., Shimoji, K., Onizuka, T., Hayashiji, N., Ohno, Y., Arai, T., Hattori, F., Kaneda, R., Kimura, K., et al. (2011). G-CSF influences mouse skeletal muscle development and regeneration by stimulating myoblast proliferation. J. Exp. Med. 208, 715-727.
21. He, G., and Karin, M. (2011). NF-kappaB and STAT3-Key players in liver inflammation and cancer. Cell Res. 21, 159-168.
22. Heck, J. E., Andrew, A. S., Onega, T., Rigas, J. R., Jackson, B. P., Karagas, M. R., and Duell, E. J. (2009). Lung cancer in a U.S. population with low to moderate arsenic exposure. Environ. Health Perspect. 117, 1718-1723.
23. Hopenhayn-Rich, C., Biggs, M. L., and Smith, A. H. (1998). Lung and kidney cancer mortality associated with arsenic in drinking water in Córdoba, Argentina. Int. J. Epidemiol. 27, 561-569.
24. Hui, L., Zatloukal, K., Scheuch, H., Stepniak, E., and Wagner, E. F. (2008). Proliferation of human HCC cells and chemically induced mouse liver cancers requires JNK1-dependent p21 downregulation. J. Clin. Invest. 118, 3943-3953.
25. Hutchins, A. P., and Robson, P. (2009). Unraveling the human embryonic stem cell phosphoproteome. Cell Stem Cell 5, 126-128.
26. Iliopoulos, D., Jaeger, S. A., Hirsch, H. A., Bulyk, M. L., and Struhl, K. (2010). STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer. Mol. Cell 39, 493-506.
27. Iñiguez, M., Berasain, C., Martinez-Ansó, E., Bustos, M., Fortes, P., Pennica, D., Avila, M. A., and Prieto, J. (2006). Cardiotrophin-1 defends the liver against ischemia-reperfusion injury and mediates the protective effect of ischemic preconditioning. J. Exp. Med. 203, 2809-2815.
28. Jelacic, T. M., Thompson, D., Hanson, C., Cmarik, J. L., Nishigaki, K., and Ruscetti, S. (2008). The tyrosine kinase sf-Stk and its downstream signals are required for maintenance of friend spleen focus-forming virus-induced fibroblast transformation. J. Virol. 82, 419-427.
29. Ke, B., Shen, X. D., Ji, H., Kamo, N., Gao, F., Freitas, M. C., Busuttil, R. W., and Kupiec-Weglinski, J. W. (2012). HO-1-STAT3 axis in mouse liver ischemia/reperfusion injury: Regulation of TLR4 innate responses through PI3K/PTEN signaling. J. Hepatol. 56, 359-366.
30. Kim, J. H., Lee, S. C., Ro, J., Kang, H. S., Kim, H. S., and Yoon, S. (2010). Jnk signaling pathway-mediated regulation of Stat3 activation is linked to the development of doxorubicin resistance in cancer cell lines. Biochem. Pharmacol. 79, 373-380.
31. Lim, C. P., and Cao, X. (1999). Serine phosphorylation and negative regulation of Stat3 by JNK. J. Biol. Chem. 274, 31055-31061.
32. Liu, H., Ma, Y., Cole, S. M., Zander, C., Chen, K. H., Karras, J., and Pope, R. M. (2003). Serine phosphorylation of STAT3 is essential for Mcl-1 expression and macrophage survival. Blood 102, 344-352.
33. Luedde, T., Beraza, N., Kotsikoris, V., van Loo, G., Nenci, A., De Vos, R., Roskams, T., Trautwein, C., and Pasparakis, M. (2007). Deletion of NEMO/ IKKgamma in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma. Cancer Cell 11, 119-132.
34. Maeda, S., Kamata, H., Luo, J. L., Leffert, H., and Karin, M. (2005). IKKbeta couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell 121, 977-990.
35. Miyazaki, T., Bub, J. D., and Iwamoto, Y. (2008). c-Jun NH(2)-terminal kinase mediates leptin-stimulated androgen-independent prostate cancer cell proliferation via signal transducer and activator of transcription 3 and Akt. Biochim. Biophys. Acta 1782, 593-604.
36. Olsson, A. K., Dimberg, A., Kreuger, J., and Claesson-Welsh, L. (2006). VEGF receptor signalling - in control of vascular function. Nat. Rev. Mol. Cell Biol. 7, 359-371.
37. Park, E. J., Lee, J. H., Yu, G. Y., He, G., Ali, S. R., Holzer, R. G., Osterreicher, C. H., Takahashi, H., and Karin, M. (2010). Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression. Cell 140, 197-208.
38. Qin, H. R., Kim, H. J., Kim, J. Y., Hurt, E. M., Klarmann, G. J., Kawasaki, B. T., Duhagon Serrat, M. A., and Farrar, W. L. (2008). Activation of signal transducer and activator of transcription 3 through a phosphomimetic serine 727 promotes prostate tumorigenesis independent of tyrosine 705 phosphorylation. Cancer Res. 68, 7736-7741.
39. Shibata, W., Maeda, S., Hikiba, Y., Yanai, A., Sakamoto, K., Nakagawa, H., Ogura, K., Karin, M., and Omata, M. (2008). c-Jun NH2-terminal kinase 1 is a critical regulator for the development of gastric cancer in mice. Cancer Res. 68, 5031-5039.
40. Suissa, Y., Ziv, O., Dinur, T., Arama, E., and Gerlitz, O. (2011). The NAB-Brk signal bifurcates at JNK to independently induce apoptosis and compensatory proliferation. J. Biol. Chem. 286, 15556-15564.
41. Takahashi, H., Ogata, H., Nishigaki, R., Broide, D. H., and Karin, M. (2010). Tobacco smoke promotes lung tumorigenesis by triggering IKKbeta- and JNK1-dependent inflammation. Cancer Cell 17, 89-97.
42. Turkson, J., Bowman, T., Adnane, J., Zhang, Y., Djeu, J. Y., Sekharam, M., Frank, D. A., Holzman, L. B., Wu, J., Sebti, S., et al. (1999). Requirement for Ras/ Rac1-mediated p38 and c-Jun N-terminal kinase signaling in Stat3 transcriptional activity induced by the Src oncoprotein. Mol. Cell. Biol. 19, 7519-7528.
43. Vlotides, G., Chen, Y. H., Eigler, T., Ren, S. G., and Melmed, S. (2009). Fibroblast growth factor-2 autofeedback regulation in pituitary folliculostellate TtT/GF cells. Endocrinology 150, 3252-3258.
44. Wang, Z., Yang, J., Fisher, T., Xiao, H., Jiang, Y., and Yang, C. (2012). Akt activation is responsible for enhanced migratory and invasive behavior of arsenic-transformed human bronchial epithelial cells. Environ. Health Perspect. 120, 92-97.
45. Zhang, Y., Bhatia, D., Xia, H., Castranova, V., Shi, X., and Chen, F. (2006). Nucleolin links to arsenic-induced stabilization of GADD45alpha mRNA. Nucleic Acids Res. 34, 485-495.
46. Zhang, Y., Liu, G., and Dong, Z. (2001). MSK1 and JNKs mediate phosphorylation of STAT3 in UVA-irradiated mouse epidermal JB6 cells. J. Biol. Chem. 276, 42534-42542.