A nuclear tyrosine phosphorylation circuit: c-Jun as an activator and substrate of c-Abl and JNK

EMBO Journal

Volumn 19, Issue 2, 2000, Pages 273-281

  Barilá, Daniela ^a   Mangano, Raffaella ^a   Gonfloni, Stefania ^a   Kretzschmar, Jana ^a   Moro, Marina ^a,b   Bohmann, Dirk ^a   Superti Furga, Giulio ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b PFIZER INC   (United States)

Author keywords

Abl; JNK; Jun; Nuclear tyrosine phosphorylation; Phosphorylation circuit

Indexed keywords

NUCLEAR PROTEIN; PROTEIN C JUN; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR; TYROSINE;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA TRANSFECTION; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

EID: 0034677210     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.2.273     Document Type: Article

References (49)

1. Agami, R., Blandino, G., Oren, M. and Shaul, Y. (1999) Interaction of c-Abl and p73α and their collaboration to induce apoptosis. Nature, 399, 809-813.
2. Angel, P., Smeal, T., Meek, J. and Karin, M. (1989) Jun and v-jun contain multiple regions that participate in transcriptional activation in an interdependent manner. New Biol., 1, 35-43.
3. Baichwal, V.R. and Tjian, R. (1990) Control of c-Jun activity by interaction of a cell-specific inhibitor with regulatory domain δ: differences between v-and c-Jun. Cell, 63, 815-825.
4. Bannister, A.J., Oehler, T., Wilhelm, D., Angel, P. and Kouzarides, T. (1995) Stimulation of c-Jun activity by CBP: c-Jun residues Ser63/73 are required for CBP induced stimulation in vivo and CBP binding in vitro. Oncogene, 11, 2509-2514.
5. Barilá, D. and Superti-Furga, G. (1998) An intramolecular SH3-domain interaction regulates c-Abl activity. Nature Genet., 18, 280-282.
6. Bell, J.C., Mahadevan, L.C., Colledge, W.H., Frackelton, A.R., Jr. Sargent, M.G. and Foulkes, J.G. (1987) Abel son-transformed fibroblasts contain nuclear phosphotyrosyl-proteins which preferentially bind to murine DNA. Nature, 325, 552-554.
7. Brenner, D.A., O'Hara, M., Angel, P., Chojkier, M. and Karin, M. (1989) Prolonged activation of jun and collagenase genes by tumour necrosis factor-α. Nature, 337, 661-663.
8. Chida, K. and Vogt, P.K. (1992) Nuclear translocation of viral Jun but not of cellular Jun is cell cycle dependent. Proc. Natl Acad. Sci. USA, 89, 4290-4294.
9. Coso, O.A., Chiariello, M., Yu, J.C., Teramoto, H., Crespo, P., Xu, N., Miki, T. and Gutkind, J.S. (1995) The small GTP-binding proteins Rac 1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell, 81, 1137-1146.
10. Feller, S.M., Knudsen, B. and Hanafusa, H. (1994) c-Abl kinase regulates the protein binding activity of c-Crk. EMBO J., 13, 2341-2351.
11. Gonfloni, S., Williams, J.C., Hattula, K., Weijland, A., Wierenga, R.K. and Superti-Furga, G. (1997) The role of the linker between the SH2 domain and catalytic domain in the regulation and function of Src. EMBO J., 16, 7261-7271.
12. Gong, J.G., Costanzo, A., Yang, H.Q., Melino, G., Kaelin, W.G., Jr, Levrero, M. and Wang, J.Y. (1999) The tyrosine kinase c-Abl regulates p73 in apoptotic response to cisplatin-induced DNA damage. Nature, 399, 806-809.
13. Hibi, M., Lin, A., Smeal, T., Minden, A. and Karin, M. (1993) Identification of an oncoprotein-and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev. 7, 2135-2148.
14. Hilberg, F., Aguzzi, A., Howells, N. and Wagner, E.F. (1993) c-jun is essential for normal mouse development and hepatogenesis. Nature, 365, 179-181.
15. Ip, Y.T. and Davis, R.J. (1998) Signal transduction by the c-Jun N-terminal kinase (JNK) - from inflammation to development. Curr. Opin. Cell Biol., 10, 205-219.
16. Johnson, R.S., van Lingen, B., Papaioannou, V.E. and Spiegelman, B.M. (1993) A null mutation at the c-jun locus causes embryonic lethality and retarded cell growth in culture. Genes Dev., 7, 1309-1317.
17. Kamps, M.P. (1991) Determination of phosphoamino acid composition by acid hydrolysis of protein blotted to Immobilon. Methods Enzymol., 201, 21-27.
18. Karin, M. and Hunter, T. (1995) Transcriptional control by protein phosphorylation: signal transmission from the cell surface to the nucleus. Curr. Biol., 5, 747-757.
19. Karin, M., Liu, Z. and Zandi, E. (1997) AP-1 function and regulation. Curr. Opin. Cell Biol., 9, 240-246.
20. Kharbanda, S., Datta, R. and Kufe, D. (1991) Regulation of c-jun gene expression in HL-60 leukemia cells by 1-β-D-arabinofuranosylcytosine. Potential involvement of a protein kinase C dependent mechanism. Biochemistry, 30, 7947-7952.
21. Kharbanda, S., Pandey, P., Ren, R., Mayer, B., Zon, L. and Kufe, D. (1995a) c-Abl activation regulates induction of the SEK1/stress-activated protein kinase pathway in the cellular response to 1-β-D-arabinofuranosylcytosine. J. Biol. Chem., 270, 30278-30281.
22. Kharbanda, S., Ren, R., Pandey, P., Shafman, T.D., Feller, S.M., Weichselbaum, R.R. and Kufe, D.W. (1995b) Activation of the c-Abl tyrosine kinase in the stress response to DNA-damaging agents. Nature, 376, 785-788.
23. Kharbanda, S., Yuan, Z.M., Weichselbaum, R. and Kufe, D. (1998) Determination of cell fate by c-Abl activation in the response to DNA damage. Oncogene, 17, 3309-3318.
24. Koleske, A.J., Gifford, A.M., Scott, M.L., Nee, M., Bronson, R.T., Miczek, K.A. and Baltimore, D. (1998) Essential roles for the Abl and Arg tyrosine kinases in neurulation. Neuron, 6, 1259-1272.
25. Kyriakis, J.M. and Avruch, J. (1996) Protein kinase cascades activated by stress and inflammatory cytokines. BioEssays, 18, 567-577.
26. Lallemand, D., Ham, J., Garbay, S., Bakiri, L., Traincard, F., Jeannequin, O., Pfarr, C.M. and Yaniv, M. (1998) Stress-activated protein kinases are negatively regulated by cell density. EMBO J., 17, 5615-5626.
27. Lee, S.A., Dritschilo, A. and Jung, M. (1998) Impaired ionizing radiation-induced activation of a nuclear signal essential for phosphorylation of c-Jun by dually phosphorylated c-Jun amino-terminal kinases in ataxia telangiectasia fibroblasts. J. Biol. Chem., 273, 32889-32894.
28. Liu, Z.-G., Baskaran, R., Lea-Chou, E.T., Wood, L.D., Chen, Y., Karin, M. and Wang, J.Y.J. (1996) Three distinct signalling responses by murine fibroblasts to genotoxic stress. Nature, 384, 273-276.
29. Mayer, B.J., Hirai, H. and Sakai, R. (1995) Evidence that the SH2 domains promote processive phosphorylation by protein-tyrosine kinases. Curr. Biol., 5, 296-305.
30. Papavassiliou, A.G., Treier, M. and Bohmann, D. (1995) Intramolecular signal transduction in c-Jun. EMBO J., 14, 2014-2019.
31. Raitano, A.B., Halpern, J.R., Hambuch, T.M. and Sawyers, C.L. (1995) The Bcr-Abl leukemia oncogene activates Jun kinase and requires Jun for transformation. Proc. Natl Acad. Sci. USA, 92, 11746-11750.
32. Raitano, A.B., Whang, Y.E. and Sawyers, C.L. (1997) Signal transduction by wild-type and leukemogenic Abl proteins. Biochim. Biophys. Acta, 1333, F201-F216.
33. Renshaw, M.W., Lea-Chou, E. and Wang, J.Y.J. (1996) Rac is required for v-Abl tyrosine kinase to activate mitogenesis. Curr. Biol., 6, 76-83.
34. Rubin, E., Kharbanda, S., Gunji, H., Weichselbaum, R. and Kufe, D. (1992) cis-Diamminedichloroplatinum (II) induces c-jun expression in human myeloid leukemia cells: potential involvement of a protein kinase C-dependent signaling pathway. Cancer Res., 52, 878-882.
35. Sanchez-Perez, I., Murguia, J.R. and Perona, R. (1998) Cisplatin induces a persistent activation of JNK that is related to cell death. Oncogene, 16, 533-540.
36. Sawyers, C.L. (1999) Chronic myeloid leukemia. N. Engl. J. Med., 340, 1330-1340.
37. Schreiber, M., Kolbus, A., Piu, F., Szabowski, A., Mohle-Steinlein, U., Tian, J., Karin, M., Angel, P. and Wagner, E.F. (1999) Control of cell cycle progression by c-Jun is p53 dependent. Genes Dev., 13, 607-619.
38. Songyang, Z. et al. (1993) SH2 domains recognize specific phosphopeptide sequences. Cell, 72, 767-778.
39. Songyang, Z. et al. (1995) Catalytic specificity of protein-tyrosine kinases is critical for selective signalling. Nature, 373, 536-539.
40. Superti-Furga, G. and Courtneidge, S.A. (1995) Structure-function relationships in Src family and related protein tyrosine kinases. BioEssays, 17, 321-330.
41. Taagepera, S., McDonald, D., Loeb, J.E., Whitaker, L.L., McElroy, A.K., Wang, J.Y. and Hope, T.J. (1998) Nuclear-cytoplasmic shuttling of C-ABL tyrosine kinase. Proc. Natl Acad. Sci. USA, 95, 7457-7462.
42. Tanaka, M., Gupta, R. and Mayer, B.J. (1995) Differential inhibition of signaling pathways by dominant-negative SH2/SH3 adapter proteins. Mol. Cell. Biol., 15, 6829-6837.
43. Treier, M., Staszewski, L.M. and Bohmann, D. (1994) Ubiquitin-dependent c-Jun degradation in vivo is mediated by the δ domain. Cell, 78, 787-798.
44. Treisman, R. (1996) Regulation of transcription by MAP kinase cascades. Curr. Opin. Cell Biol., 8, 205-215.
45. Van Etten, R.A. (1999) Cycling, stressed-out and nervous: cellular functions of c-Abl. Trends Cell Biol., 9, 179-186.
46. Wang, J.Y.J. (1993) Abl tyrosine kinase in signal transduction and cell-cycle regulation. Curr. Opin. Genet. Dev., 3, 35-43.
47. Xia, Z., Dickens, M., Raingeaud, J., Davis, R.J. and Greenberg, M.E. (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science, 270, 1326-1331.
48. Yuan, Z.M. et al. (1998) Regulation of Rad51 function by c-Abl in response to DNA damage. J. Biol. Chem., 273, 3799-3802.
49. Yuan, Z.M. et al. (1999) p73 is regulated by tyrosine kinase c-Abl in the apoptotic response to DNA damage. Nature, 399, 814-817.