Serine 58 of 14-3-3ζ is a molecular switch regulating ASK1 and oxidant stress-induced cell death

Molecular and Cellular Biology

Volumn 29, Issue 15, 2009, Pages 4167-4176

  Zhou, Jibin ^a   Shao, Zhili ^a   Kerkela, Risto ^a   Ichijo, Hidenori ^b   Muslin, Anthony J ^c   Pombo, Celia ^d   Force, Thomas ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS SIGNAL REGULATING KINASE 1; PROTEIN SERINE THREONINE KINASE; PROTEIN SOK 1; SERINE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME RELEASE; GENE OVEREXPRESSION; GENE SWITCHING; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

14-3-3 PROTEINS; ANIMALS; APOPTOSIS; CELLS, CULTURED; FIBROBLASTS; HYDROGEN PEROXIDE; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAP KINASE KINASE KINASE 5; MICE; MICE, KNOCKOUT; MUTATION; OXIDANTS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; SERINE;

MAMMALIA;

EID: 67651215903     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01067-08     Document Type: Article

References (45)

1. Aitken, A. 2006. 14-3-3 proteins: a historic overview. Semin. Cancer Biol. 16:162-172.
2. Creasy, C. L., D. M. Ambrose, and J. Chernoff. 1996. The Ste20-like protein kinase, MstI, dimerizes and contains an inhibitory domain. J. Biol. Chem. 271:21049-21053.
3. Creasy, C. L., and J. Chernoff. 1995. Cloning and characterization of a human protein kinase with homology to Ste20. J. Biol. Chem. 270:21695-21700.
4. Datta, S. R., H. Dudek, X. Tao, S. Masters, F. H., Y. Gotoh, and M. E. Greenberg. 1997. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231-241.
5. Dubois, T., C. Rommel, S. Howell, U. Steinhussen, Y. Soneji, N. Morrice, K. Moelling, and A. Aitken. 1997. 14-3-3 is phosphorylated by casein kinase I on residue 233. Phosphorylation at this site in vivo regulates Raf/14-3-3 interaction. J. Biol. Chem. 272:28882-28888.
6. Fujii, K., E. H. Goldman, H. R. Park, L. Zhang, J. Chen, and H. Fu. 2004. Negative control of apoptosis signal-regulating kinase 1 through phosphorylation of Ser-1034. Oncogene 23:5099-5104.
7. Gardino, A. K., S. J. Smerdon, and M. B. Yaffe. 2006. Structural determinants of 14-3-3 binding specificities and regulation of subcellular localization of 14-3-3-ligand complexes: a comparison of the X-ray crystal structures of all human 14-3-3 isoforms. Semin. Cancer Biol. 16:173-182.
8. Goldman, E. H., L. Chen, and H. Fu. 2004. Activation of apoptosis signal-regulating kinase 1 by reactive oxygen species through dephosphorylation at serine 967 and 14-3-3 dissociation. J. Biol. Chem. 279:10442-10449.
9. Hamaguchi, A., E. Suzuki, K. Murayama, T. Fujimura, T. Hikita, K. Iwabuchi, K. Handa, D. A. Withers, S. C. Masters, H. Fu, and S. Hakomori. 2003. Sphingosine-dependent protein kinase-1, directed to 14-3-3, is identified as the kinase domain of protein kinase C delta. J. Biol. Chem. 278:41557-41565.
10. Ichijo, H., E. Nishida, K. Irie, P. ten Dijke, M. Saitoh, T. Moriguchi, M. Takagi, K. Matsumoto, K. Miyazono, and Y. Gotoh. 1997. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 275:90-94.
11. Lau, J. M., X. Jin, J. Ren, J. Avery, B. J. DeBosch, I. Treskov, T. S. Lupu, A. Kovacs, C. Weinheimer, and A. J. Muslin. 2007. The 14-3-3τ phosphoserine-binding protein is required for cardiomyocyte survival. Mol. Cell. Biol. 27:1455-1466.
12. Lehtinen, M. K., Z. Yuan, P. R. Boag, Y. Yang, J. Villen, E. B. Becker, S. DiBacco, N. de la Iglesia, S. Gygi, T. K. Blackwell, and A. Bonni. 2006. A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 125:987-1001.
13. Liu, Q., B. J. Wilkins, Y. J. Lee, H. Ichijo, and J. D. Molkentin. 2006. Direct interaction and reciprocal regulation between ASK1 and calcineurin-NFAT control cardiomyocyte death and growth. Mol. Cell. Biol. 26:3785-3797.
14. Lizcano, J. M., N. Morrice, and P. Cohen. 2000. Regulation of BAD by cAMP-dependent protein kinase is mediated via phosphorylation of a novel site, Ser155. Biochem. J. 349:547-557.
15. Mackintosh, C. 2004. Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem. J. 381:329-342.
16. Megidish, T., J. Cooper, L. Zhang, H. Fu, and S. Hakomori. 1998. A novel sphingosine-dependent protein kinase (SDK1) specifically phosphorylates certain isoforms of 14-3-3 protein. J. Biol. Chem. 273:21834-21845.
17. Megidish, T., T. White, K. Takio, K. Titani, Y. Igarashi, and S. Hakomori. 1995. The signal modulator protein 14-3-3 is a target of sphingosine- or N,N-dimethylsphingosine-dependent kinase in 3T3(A31) cells. Biochem. Biophys. Res. Commun. 216:739-747.
18. Muslin, A. J., J. W. Tanner, P. M. Allen, and A. S. Shaw. 1996. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84:889-897.
19. Nogueira, E., M. Fidalgo, A. Molnar, J. M. Kyriakis, T. Force, J. Zalvide, and C. M. Pombo. 2008. SOK1 translocates from the Golgi to the nucleus upon chemical anoxia and induces apoptotic cell death. J. Biol. Chem. 283:16248-16258.
20. Osada, S., M. Izawa, R. Saito, K. Mizuno, A. Suzuki, S. Hirai, and S. Ohno. 1997. YSK1, a novel mammalian protein kinase structurally related to Ste20 and SPS1, but is not involved in the known MAPK pathways. Oncogene 14:2047-2057.
21. Pombo, C. M., J. V. Bonventre, A. Molnar, J. Kyriakis, and T. Force. 1996. Activation of a human Ste20-like kinase by oxidant stress defines a novel stress response pathway. EMBO J. 15:4537-4546.
22. +]. J. Biol. Chem. 272:29372-29379.
23. Porter, G. W., F. R. Khuri, and H. Fu. 2006. Dynamic 14-3-3/client protein interactions integrate survival and apoptotic pathways. Semin. Cancer Biol. 16:193-202.
24. Powell, D. W., M. J. Rane, Q. Chen, S. Singh, and K. R. McLeish. 2002. Identification of 14-3-3ζ as a protein kinase B/Akt substrate. J. Biol. Chem. 277:21639-21642.
25. Powell, D. W., M. J. Rane, B. A. Joughin, R. Kalmukova, J. H. Hong, B. Tidor, W. L. Dean, W. M. Pierce, J. B. Klein, M. B. Yaffe, and K. R. McLeish. 2003. Proteomic identification of 14-3-3ζ as a mitogen-activated protein kinase-activated protein kinase 2 substrate: role in dimer formation and ligand binding. Mol. Cell. Biol. 23:5376-5387.
26. Preisinger, C., B. Short, V. De Corte, E. Bruyneel, A. Haas, R. Kopajtich, J. Gettemans, and F. A. Barr. 2004. YSK1 is activated by the Golgi matrix protein GM130 and plays a role in cell migration through its substrate 14-3-3ζ. J. Cell Biol. 164:1009-1020.
27. Saitoh, M., H. Nishito, M. Fujii, K. Takeda, K. Tobiume, Y. Sawada, M. Kawabata, K. Miyazono, and H. Ichijo. 1998. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 17:2596-2606.
28. Shen, Y. H., J. Godlewski, A. Bronisz, J. Zhu, M. J. Comb, J. Avruch, and G. Tzivion. 2003. Significance of 14-3-3 self-dimerization for phosphorylation-dependent target binding. Mol. Biol. Cell 14:4721-4733.
29. Sunayama, J., F. Tsuruta, N. Masuyama, and Y. Gotoh. 2005. JNK antagonizes Akt-mediated survival signals by phosphorylating 14-3-3. J. Cell Biol. 170:295-304.
30. Takeda, K., T. Noguchi, I. Naguro, and H. Ichijo. 2008. Apoptosis signal-regulating kinase 1 in stress and immune response. Annu. Rev. Pharmacol. Toxicol. 48:199-225.
31. Thorson, J. A., L. W. Yu, A. L. Hsu, N. Y. Shih, P. R. Graves, J. W. Tanner, P. M. Allen, H. Piwnica-Worms, and A. S. Shaw. 1998. 14-3-3 proteins are required for maintenance of Raf-1 phosphorylation and kinase activity. Mol. Cell. Biol. 18:5229-5238.
32. Tobiume, K., A. Matsuzawa, T. Takahashi, H. Nishito, K. Morita, K. Takeda, O. Minowa, K. Miyazono, T. Noda, and H. Ichijo. 2001. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep. 2:222-228.
33. Tsuruta, F., J. Sunayama, Y. Mori, S. Hattori, S. Shimizu, Y. Tsujimoto, K. Yoshioka, N. Masuyama, and Y. Gotoh. 2004. JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins. EMBO J. 23:1889-1899.
34. Tzivion, G., Z. Luo, and J. Avruch. 1998. A dimeric 14-3-3 protein is an essential cofactor for Raf kinase activity. Nature 394:88-92.
35. van Hemert, M. J., H. Y. Steensma, and G. P. van Heusden. 2001. 14-3-3 proteins: key regulators of cell division, signalling and apoptosis. Bioessays 23:936-946.
36. Wang, H., L. Zhang, R. Liddington, and H. Fu. 1998. Mutations in the hydrophobic surface of an amphipathic groove of 14-3-3ζ disrupt its interaction with Raf-1 kinase. J. Biol. Chem. 273:16297-16304.
37. Woodcock, J. M., J. Murphy, F. C. Stomski, M. C. Berndt, and A. F. Lopez. 2003. The dimeric versus monomeric status of 14-3-3ζ is controlled by phosphorylation of Ser58 at the dimer interface. J. Biol. Chem. 278:36323-36327.
38. Xing, H., S. Zhang, C. Weinheimer, A. Kovacs, and A. J. Muslin. 2000. 14-3-3 proteins block apoptosis and differentially regulate MAPK cascades. EMBO J. 19:349-358.
39. Yaffe, M. B., K. Rittinger, S. Volinia, P. R. Caron, A. Aitken, H. Leffers, S. J. Gamblin, S. J. Smerdon, and L. C. Cantley. 1997. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91:961-971.
40. Yoshida, K., T. Yamaguchi, T. Natsume, D. Kufe, and Y. Miki. 2005. JNK phosphorylation of 14-3-3 proteins regulates nuclear targeting of c-Abl in the apoptotic response to DNA damage. Nat. Cell Biol. 7:278-285.
41. Yuan, Z. Q., R. I. Feldman, G. E. Sussman, D. Coppola, S. V. Nicosia, and J. Q. Cheng. 2003. AKT2 inhibition of cisplatin-induced JNK/p38 and Bax activation by phosphorylation of ASK1: implication of AKT2 in chemoresistance. J. Biol. Chem. 278:23432-23440.
42. Zha, J., H. Harada, E. Yang, J. Jockel, and S. J. Korsmeyer. 1996. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X. Cell 87:619-628.
43. Zhang, L., J. Chen, and H. Fu. 1999. Suppression of apoptosis signal-regulating kinase 1-induced cell death by 14-3-3 proteins. Proc. Natl. Acad. Sci. USA 96:8511-8515.
44. 2 but not tumor necrosis factor. J. Biol. Chem. 280:19036-19044.
45. Zhou, X. M., Y. Liu, G. Payne, R. J. Lutz, and T. Chittenden. 2000. Growth factors inactivate the cell death promoter BAD by phosphorylation of its BH3 domain on Ser155. J. Biol. Chem. 275:25046-25051.