The Korean Journal of Physiology and Pharmacology

The Korean Society of Pharmacology (대한약리학회)
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Long-term Activation of c-Jun N-terminal Kinase through Receptor Interacting Protein is Associated with DNA Damage-induced Cell Death

  • Seok, Jeong-Ho (Department of Pharmacology, Research Institute for Medical Sciences) ;
  • Park, Kyeong-Ah (Department of Pharmacology, Research Institute for Medical Sciences) ;
  • Byun, Hee-Sun (Department of Pharmacology, Research Institute for Medical Sciences) ;
  • Won, Min-Ho (Department of Pharmacology, Research Institute for Medical Sciences) ;
  • Shin, Sang-Hee (Department of Pharmacology, Research Institute for Medical Sciences) ;
  • Choi, Byung-Lyul (Department of Pharmacology, Research Institute for Medical Sciences) ;
  • Lee, Hyun-Ji (Department of Pharmacology, Research Institute for Medical Sciences) ;
  • Kim, Young-Rae (Department of Pharmacology, Research Institute for Medical Sciences) ;
  • Hong, Jang-Hee (Department of Pharmacology, Research Institute for Medical Sciences) ;
  • Park, Jong-Sun (Department of Pharmacology, Research Institute for Medical Sciences) ;
  • Hur, Gang-Min (Department of Pharmacology, Research Institute for Medical Sciences, Daejeon Regional Cancer Center, College of Medicine, Chungnam National University)
  • Published : 2008.08.31
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Abstract

Activation of c-Jun N-terminal kinase (JNK), a member of the mitogen-activated protein kinase family, is an important cellular response that modulates the outcome of the cells which are exposed to the tumor necrosis factor (TNF) or the genotoxic stress including DNA damaging agents. Although it is known that JNK is activated in response to genotoxic stress, neither the pathways to transduce signals to activate JNK nor the primary sensors of the cells that trigger the stress response have been identified. Here, we report that the receptor interacting protein (RIP), a key adaptor protein of TNF signaling, was required to activate JNK in the cells treated with certain DNA damaging agents such as adriamycin (Adr) and 1-${\beta}$-D-arabinofuranosylcytosine (Ara-C) that cause slow and sustained activation, but it was not required when treated with N-methyl-N-nitro-N-nitrosoguanidine (MNNG) and short wavelength UV, which causes quick and transient activation. Our findings revealed that this sustained JNK activation was not mediated by the TNF (tumor necrosis factor) receptor signaling, but it required a functional ATM (ataxia telangiectasia) activity. In addition, JNK inhibitor SP-600125 significantly blocked the Adr-induced cell death, but it did not affect the cell death induced by MNNG. These findings suggest that the sustained activation of JNK mediated by RIP plays an important role in the DNA damage-induced cell death, and that the duration of JNK activation relays a different stress response to determine the cell fate.

Keywords

References

  1. Angel P, Karin M. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim Biophys Acta 1072: 129-157, 1991
  2. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421: 499-506, 2003 https://doi.org/10.1038/nature01368
  3. Bulavin DV, Saito S, Hollander MC, Sakaguchi K, Anderson CW, Appella E, Fornace AJ Jr. Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation. EMBO J 18: 6845-6854, 1999 https://doi.org/10.1093/emboj/18.23.6845
  4. Byun HS, Park KA, Won M, Yang KJ, Shin S, Piao L, Kwak JY, Lee ZW, Park J, Seok JH, Liu ZG, Hur GM. Phorbol 12- myristate 13-acetate protects against tumor necrosis factor (TNF)-induced necrotic cell death by modulating the recruitment of TNF receptor 1-associated death domain and receptor-interacting protein into the TNF receptor 1 signaling complex: Implication for the regulatory role of protein kinase C. Mol Pharmacol 70: 1099-1108, 2006 https://doi.org/10.1124/mol.106.025452
  5. Canman CE, Kastan MB. Signal transduction. Three paths to stress relief. Nature 384: 213-214, 1996 https://doi.org/10.1038/384213a0
  6. Chen YR, Wang X, Templeton D, Davis RJ, Tan TH. The role of c-Jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and gamma radiation. Duration of JNK activation may determine cell death and proliferation. J Biol Chem 271: 31929-31936, 1996 https://doi.org/10.1074/jbc.271.50.31929
  7. Chen G, Goeddel DV. TNF-R1 signaling: a beautiful pathway. Science 296: 1634-1635, 2002. https://doi.org/10.1126/science.1071924
  8. Coso OA, Chiariello M, Yu JC, Teramoto H, Crespo P, Xu N, Miki T, Gutkind JS. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81: 1137-1146, 1995 https://doi.org/10.1016/S0092-8674(05)80018-2
  9. Derijard B, Hibi M, Wu IH, Barrett T, Su B, Deng T, Karin M, Davis RJ. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76: 1025-1037, 1994 https://doi.org/10.1016/0092-8674(94)90380-8
  10. Devary Y, Rosette C, DiDonato JA, Karin M. NF-kappa B activation by ultraviolet light not dependent on a nuclear signal. Science 261: 1442-1445, 1993 https://doi.org/10.1126/science.8367725
  11. Fritz G, Kaina B. Activation of c-Jun N-terminal kinase 1 by UV irradiation is inhibited by wortmannin without affecting c-iun expression. Mol Cell Biol 19: 1768-1774, 1999 https://doi.org/10.1128/MCB.19.3.1768
  12. Hayakawa J, Depatie C, Ohmichi M, Mercola D. The activation of c-Jun NH2-terminal kinase (JNK) by DNA-damaging agents serves to promote drug resistance via activating transcription factor 2 (ATF2)-dependent enhanced DNA repair. J Biol Chem 278: 20582-20592, 2003 https://doi.org/10.1074/jbc.M210992200
  13. Heeres JT, Hergenrother PJ. Poly (ADP-ribose) makes a date with death. Curr Opin Chem Biol 11: 644-653, 2007 https://doi.org/10.1016/j.cbpa.2007.08.038
  14. Houghton JA. Apoptosis and drug response. Curr Opin Oncol 11: 475-481, 1999 https://doi.org/10.1097/00001622-199911000-00008
  15. Hur GM, Lewis J, Yang Q, Lin Y, Nakano H, Nedospasov S, Liu ZG. The death domain kinase RIP has an essential role in DNA damage-induced NF-kappa B activation. Genes Dev 17: 873-882, 2003 https://doi.org/10.1101/gad.1062403
  16. Hur GM, Kim YS, Won M, Choksi S, Liu ZG. The death domain kinase RIP has an important role in DNA damage-induced, p53-independent cell death. J Biol Chem 281: 25011-25017, 2006 https://doi.org/10.1074/jbc.M605577200
  17. Ichijo H, Nishida E, Irie K, ten Dijke P, Saitoh M, Moriguchi T, Takagi M, Matsumoto K, Miyazono K, Gotoh Y. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 275: 90-94, 1997 https://doi.org/10.1126/science.275.5296.90
  18. Karin M, Lin A. NF-kappaB at the crossroads of life and death. Nat Immunol 3: 221-227, 2002 https://doi.org/10.1038/ni0302-221
  19. Kharbanda S, Ren R, Pandey P, Shafman TD, Feller SM, Weichselbaum RR, Kufe DW. Activation of the c-Abl tyrosine kinase in the stress response to DNA-damaging agents. Nature 376: 785-788, 1995 https://doi.org/10.1038/376785a0
  20. Kyriakis JM, Banerjee P, Nikolakaki E, Dai T, Rubie EA, Ahmad MF, Avruch J, Woodgett JR. The stress-activated protein kinase subfamily of c-Jun kinases. Nature 369: 156-160, 1994 https://doi.org/10.1038/369156a0
  21. Lewis C, Low JA. Clinical poly (ADP-ribose) polymerase inhibitors for the treatment of cancer. Curr Opin Investig Drugs 8: 1051-1056, 2007
  22. Lin Y, Devin A, Cook A, Keane MM, Kelliher M, Lipkowitz S, Liu ZG. The death domain kinase RIP is essential for TRAIL (Apo2L)-induced activation of IkappaB kinase and c-Jun N- terminal kinase. Mol Cell Biol 20: 6638-6645, 2000 https://doi.org/10.1128/MCB.20.18.6638-6645.2000
  23. Liu ZG, Baskaran R, Lea-Chou ET, Wood LD, Chen Y, Karin M, Wang JY. Three distinct signalling responses by murine fibroblasts to genotoxic stress. Nature 384: 273-276, 1996 https://doi.org/10.1038/384273a0
  24. Osborn MT, Chambers TC. Role of the stress-activated/c-Jun NH2- terminal protein kinase pathway in the cellular response to adriamycin and other chemotherapeutic drugs. J Biol Chem 271: 30950-30955, 1996 https://doi.org/10.1074/jbc.271.48.30950
  25. Pandey P, Raingeaud J, Kaneki M, Weichselbaum R, Davis RJ, Kufe D, Kharbanda S. Activation of p38 mitogen-activated protein kinase by c-Abl-dependent and independent mechanisms. J Biol Chem 271: 23775-23779, 1996 https://doi.org/10.1074/jbc.271.39.23775
  26. Parra M, Lluis F, Miralles F, Caelles C, Munoz-Canoves P. The cJun N-terminal kinase (JNK) signaling pathway mediates induction of urokinase-type plasminogen activator (uPA) by the alkylating agent MNNG. Blood 96: 1415-1424, 2000
  27. Raingeaud J, Whitmarsh AJ, Barrett T, Derijard B, Davis RJ. MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol Cell Biol 16: 1247-1255, 1996 https://doi.org/10.1128/MCB.16.3.1247
  28. Rosette C, Karin M. Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factor and cytokine receptors. Science 274: 1194-1197, 1996 https://doi.org/10.1126/science.274.5290.1194
  29. Sheikh MS, Antinore MJ, Huang Y, Fornace AJ. Ultraviolet- irradiation-induced apoptosis is mediated via ligand independent activation of tumor necrosis factor receptor 1. Oncogene 17: 2555-2563, 1998 https://doi.org/10.1038/sj.onc.1202292
  30. Shu HB, Takeuchi M, Goeddel DV. The tumor necrosis factor receptor 2 signal transducers TRAF2 and c-IAP1 are components of the tumor necrosis factor receptor 1 signaling complex. Proc Natl Acad Sci 93: 13973-13978, 1996
  31. Tang F, Tang G, Xiang J, Dai Q, Rosner MR, Lin A. The absence of NF-kappaB-mediated inhibition of c-Jun N-terminal kinase activation contributes to tumor necrosis factor alpha-induced apoptosis. Mol Cell Biol 22: 8571-8579, 2002 https://doi.org/10.1128/MCB.22.24.8571-8579.2002
  32. Tobin D, van Hogerlinden M, Toftgard R. UVB-induced association of tumor necrosis factor (TNF) receptor 1/TNF receptor-associated factor-2 mediates activation of Rel proteins. Proc Natl Acad Sci 95: 565-569, 1998
  33. Tournier C, Dong C, Turner TK, Jones SN, Flavell RA, Davis RJ. MKK7 is an essential component of the JNK signal transduction pathway activated by proinflammatory cytokines. Genes Dev 15: 141914-141926, 2001
  34. Wang JY. Regulation of cell death by the Abl tyrosine kinase. Oncogene 19: 5643-5650, 2000 https://doi.org/10.1038/sj.onc.1203878
  35. Yoshida K, Miki Y, Kufe D. Activation of SAPK/JNK signaling by protein kinase Cdelta in response to DNA damage. J Biol Chem 277: 48372-48378, 2002 https://doi.org/10.1074/jbc.M205485200
  36. Zhang Y, Ma WY, Kaji A, Bode AM, Dong Z. Requirement of ATM in UVA-induced signaling and apoptosis. J Biol Chem 277: 3124-3131, 2002 https://doi.org/10.1074/jbc.M110245200
  37. Zhang S, Lin Y, Kim YS, Hande MP, Liu ZG, Shen HM. c-Jun N-terminal kinase mediates hydrogen peroxide-induced cell death via sustained poly (ADP-ribose) polymerase-1 activation. Cell Death Differ 14: 1001-1010, 2007