Significance of 14-3-3 Self-Dimerization for Phosphorylation-dependent Target Binding

Molecular Biology of the Cell

Volumn 14, Issue 11, 2003, Pages 4721-4733

  Shen, Ying H ^a   Godlewski, Jakub ^a   Bronisz, Agnieszka ^a   Zhu, Jun ^a   Comb, Michael J ^d   Avruch, Joseph ^b,c   Tzivion, Guri ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d CELL SIGNALING TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; PROTEIN; PROTEIN 14 3 3; RAF PROTEIN; TRANSCRIPTION FACTOR DAF 16; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DIMERIZATION; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REGULATORY MECHANISM;

14-3-3 PROTEINS; ANIMALS; CAENORHABDITIS ELEGANS PROTEINS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; DIMERIZATION; HUMANS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-RAF; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TYROSINE 3-MONOOXYGENASE;

ANIMALIA; EUKARYOTA;

EID: 0345659206     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-12-0821     Document Type: Article

References (46)

1. Borch, J., Bych, K., Roepstorff, P., Palmgren, M.G., and Fuglsang, A.T. (2002). Phosphorylation-independent interaction between 14-3-3 protein and the plant plasma membrane H+-ATPase. Biochem. Soc. Trans. 30, 411-415.
2. Boston, P.F., Jackson, P., Kynoch, P.A., and Thompson, R.J. (1982). Purification, properties, and immunohistochemical localisation of human brain 14-3-3 protein. J. Neurochem. 38, 1466-1474.
3. Boyle, W.J., van der Geer, P., and Hunter, T. (1991). Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 201, 110-149.
4. Cahill, C.M., Tzivion, G., Nasrin, N., Ogg, S., Dore, J., Ruvkan, G., and Alexander-Bridges, M. (2001). Phosphatidylinositol 3-kinase signaling inhibits DAF-16 DNA binding and function via 14-3-3-dependent and 14-3-3-independent pathways. J. Biol. Chem. 276, 13402-13410.
5. Craparo, A., Freund, R., and Gustafson, T.A. (1997). 14-3-3 (epsilon) interacts with the insulin-like growth factor I receptor and insulin receptor substrate I in a phosphoserine-dependent manner. J. Biol. Chem. 272, 11663-11669.
6. Dubois, T., et al. (1997a). Structure and sites of phosphorylation of 14-3-3 protein: role in coordinating signal transduction pathways. J Protein Chem. 16, 513-522.
7. Dubois, T., Rommel, C., Howell, S., Steinhussen, U., Soneji, Y., Morrice, N., Moelling, K., and Aitken, A. (1997b). 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.
8. Fu, H., Subramanian, R.R., and Masters, S.C. (2000). 14-3-3 proteins: structure, function, and regulation. Annu. Rev. Pharmacol. Toxicol. 40, 617-647.
9. Gu, M., and Du, X. (1998). A novel ligand-binding site in the zeta-form 14-3-3 protein recognizing the platelet glycoprotein Ibalpha and distinct from the c-Raf-binding site. J. Biol. Chem. 273, 33465-33471.
10. Hallberg, B. (2002). Exoenzyme S binds its cofactor 14-3-3 through a nonphosphorylated motif. Biochem. Soc. Trans. 30, 401-405.
11. Honda, R., Ohba, Y., and Yasuda, H. (1997). 14-3-3 zeta protein binds to the carboxyl half of mouse weel kinase. Biochem. Biophys. Res. Commun. 230, 262-265.
12. Ichimura, T., Ito, M., Itagaki, C., Takahashi, M., Horigome, T., Omata, S., Ohno, S., and Isobe, T. (1997). The 14-3-3 protein binds its target proteins with a common site located towards the C-terminus. FEBS Lett. 413, 273-276.
13. Ichimura, T., Uchiyama, J., Kunibiro, O., Ito, M., Horigome, T., Omata, S., Shinkai, F., Kaji, H., and Isobe, T. (1995). Identification of the site of interaction of the 14-3-3 protein with phosphorylated tryptophan hydroxylase. J. Biol. Chem. 270, 28515-28518.
14. Ku, N.O., Liao, J., and Omary, M.B. (1998). Phosphorylation of human keratin 18 serine 33 regulates binding to 14-3-3 proteins. EMBO J. 17, 1892-1906.
15. Liu, D., Bienkowska, J., Petosa, C., Collier, R.J., Fu, H., and Liddington, R. (1995). Crystal structure of the zeta isoform of the 14-3-3 protein. Nature 376, 191-194.
16. Liu, Y.C., Liu, Y., Elly, C., Yoshida, H., Lipkowitz, S., and Altman, A. (1997). Serine phosphorylation of Cbl induced by phorbol ester enhances its association with 14-3-3 proteins in T cells via a novel serine-rich 14-3-3-binding motif. J. Biol. Chem. 272, 9979-9985.
17. Luo, K.X., Hurley, T.R., and Sefton, B.M. (1991). Cyanogen bromide cleavage and proteolytic peptide mapping of proteins immobilized to membranes. Methods Enzymol. 201, 149-152.
18. Luo, Z.J., Zhang, X.F., Rapp, U., and Avruch, J. (1995). Identification of the 14.3.3 zeta domains important for self-association and Raf binding. J. Biol. Chem. 270, 23681-23687.
19. Masters, S.C., Pederson, K.J., Zhang, L., Barbieri, J.T., and Fu, H. (1999). Interaction of 14-3-3 with a nonphosphorylated protein ligand, exoenzyme S of Pseudomonas aeruginosa. Biochemistry 38, 5216-5221.
20. Megidish, T., Cooper, J., Zhang, L., Fu, H., and Hakomori, S. (1998). A novel sphingosine-dependent protein kinase (SDK1) specifically phosphorylates certain isoforms of 14-3-3 protein. J. Biol. Chem. 273, 21834-21845.
21. Megidish, T., White, T., Takio, K., Titani, K., Igarashi, Y., and Hakomori, S. (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.
22. Mils, V., Baldin, V., Goubin, F., Pinta, I., Papin, C., Waye, M., Eychene, A., and Ducommun, B. (2000). Specific interaction between 14-3-3 isoforms and the human CDC25B phosphatase. Oncogene 19, 1257-1265.
23. Moore, B.E., and Perez, V.J. (1967). Specific acidic proteins of the nervous system. In: Physiological and Biochemical Aspects of Nervous Integration, ed. F.D. Carlson, Englewood Cliffs, NJ: Prentice Hall, 343-359.
24. Morrison, D.K., Heidecker, G., Rapp, U.R., and Copeland, T.D. (1993). Identification of the major phosphorylation sites of the Raf-1 kinase. J. Biol. Chem. 268, 17309-17316.
25. Muslin, A.J., Tannek, J.W., Allen, P.M., and Shaw, A.S. (1996). Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84, 889-897.
26. Muslin, A.J., and Xing, H. (2000). 14-3-3 proteins: regulation of subcellular localization by molecular interference. Cell Signal. 12, 703-709.
27. Obsil, T., Ghirlando, R., Klein, D.C., Ganguly, S., and Dyda, F. (2001). Crystal structure of the 14-3-3zeta: serotonin n-acetyltransferase complex. A role for scaffolding in enzyme regulation. Cell 105, 257-267.
28. Ogihara, T., et al. (1997). 14-3-3 protein binds to insulin receptor substrate-1, one of the binding sites of which is in the phosphotyrosine binding domain. J. Biol. Chem. 272, 25267-25274.
29. Petosa, C., Masters, S.C., Bankston, L.A., Pohl, J., Wang, B., Fu, H., and Liddington, R.C. (1998). 14-3-3zeta binds a phosphorylated Raf peptide and an unphosphorylated peptide via its conserved amphipathic groove. J. Biol. Chem. 273, 16305-16310.
30. Rittinger, K., Budman, J., Xu, J., Volinia, S., Cantley, L.C., Smerdon, S.J., Gamblin, S.J., and Yaffe, M.B. (1999). Structural analysis of 14-3-3 phosphopeptide complexes identifies a dual role for the nuclear export signal of 14-3-3 in ligand binding. Mol. Cell 4, 153-166.
31. Skoulakis, E.M., and Davis, R.L. (1998). 14-3-3 proteins in neuronal development and function. Mol. Neurobiol. 16, 269-284.
32. Sprenkle, A.B., Davies, S.P., Carling, D., Hardie, D.G., and Sturgill, T.W. (1997). Identification of Raf-1 Ser621 kinase activity from NIH 3T3 cells as AMP-activated protein kinase. FEBS Lett. 403, 254-258.
33. Tzivion, G., and Avruch, J. (2002). 14-3-3 proteins: active cofactors in cellular regulation by serine/threonine phosphorylation. J. Biol. Chem. 277, 3061-3064.
34. Tzivion, G., Luo, Z., and Avruch, J. (1998). A dimeric 14-3-3 protein is an essential cofactor for Raf kinase activity. Nature 394, 88-92.
35. Tzivion, G., Luo, Z.J., and Avruch, J. (2000). Calyculin A-induced vimentin phosphorylation sequesters 14-3-3 and displaces other 14-3-3 partners in vivo. J. Biol. Chem. 275, 29772-29778.
36. Tzivion, G., Shen, Y.H., and Zhu, J. (2001). 14-3-3 proteins; bringing new definitions to scaffolding. Oncogene 20, 6331-6338.
37. van Hemert, M.J., van Heusden, G.P., and Steensma, H.Y. (2001). Yeast 14-3-3 proteins. Yeast 18, 889-895.
38. Wang, B., Yang, H., Liu, Y.C., Jelinek, T., Zhang, L., Ruoslahti, E., and Fu, H. (1999). Isolation of high-affinity peptide antagonists of 14-3-3 proteins by phage display. Biochemistry 38, 12499-12504.
39. Wang, H., Zhang, L., Liddington, R., and Fu, H. (1998). Mutations in the hydrophobic surface of an amphipathic groove of 14-3-3zeta disrupt its interaction with Raf-kinase. J. Biol. Chem. 273, 16297-16304.
40. Wang, Y., Jacobs, C., Hook, K.E., Duan, H., Booher, R.N., and Sun, Y. (2000). Binding of 14-3-3beta to the carboxyl terminus of Weel increases Weel stability, kinase activity, and G2-M cell population. Cell Growth Differ. 11, 211-219.
41. Xiao, B., Smerdon, S.J., Jones, D.H., Dodson, G.G., Soneji, Y., Aitken, A., and Gamblin, S.J. (1995). Structure of a 14-3-3 protein and implications for coordination of multiple signalling pathways. Nature 376, 188-191.
42. Xing, H., Zhang, S., Weinheimer, C., Kovacs, A., and Muslin, A.J. (2000). 14-3-3 proteins block apoptosis and differentially regulate MAPK cascades. EMBO J. 19, 349-358.
43. Yaffe, M.B., Rittinger, K., Volinia, S., Caron, P.R., Aitken, A., Leffers, H., Gamblin, S.J., Smerdon, S.J., and Cantley, L.C. (1997). The structural basis for 14-3-3, phosphopeptide binding specificity. Cell 91, 961-971.
44. Zhai, J., Lin, H., Shamim, M., Schlaepfer, W.W., and Canete-Soler, R. (2001). Identification of a novel interaction of 14-3-3 with p190RhoGEF. J. Biol. Chem. 276, 41318-41324.
45. Zhang, H., Zha, X., Tan, Y., Hornbeck, P.V., Mastrangelo, A.J., Alessi, D.R., Polakiewicz, R.D., and Comb, M.J. (2002). Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs. J. Biol. Chem. 277, 39379-39387.
46. Zhang, L., Wang, H., Liu, D., Liddington, R., and Fu, H. (1997). Raf-1 kinase and exoenzyme S interact with 14-3-3zeta through a common site involving lysine 49. J. Biol. Chem. 272, 13717-13724.