A nonphosphorylated 14-3-3 binding motif on exoenzyme S that is functional in vivo

European Journal of Biochemistry

Volumn 269, Issue 20, 2002, Pages 4921-4929

  Henriksson, Maria L ^a   Francis, Matthew S ^a   Peden, Alex ^b   Aili, Margareta ^a   Stefansson, Kristina ^a   Palmer, Ruth ^a   Aitken, Alastair ^b   Hallberg, Bengt ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

ADP ribosylation; Coenzyme binding site; Cytotoxicity; NAD dependent; Peptide inhibitor

Indexed keywords

EXOENZYME S; ISOPROTEIN; PROTEIN 14 3 3; RAS PROTEIN;

ADENOSINE DIPHOSPHATE RIBOSYLATION; AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CELL STRUCTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; YERSINIA PSEUDOTUBERCULOSIS;

14-3-3 PROTEINS; ADENOSINE DIPHOSPHATE; ADP RIBOSE TRANSFERASES; AMINO ACID SEQUENCE; BACTERIAL TOXINS; BINDING SITES; BINDING, COMPETITIVE; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN ISOFORMS; RAS PROTEINS; SEQUENCE DELETION; TYROSINE 3-MONOOXYGENASE;

BACTERIA (MICROORGANISMS); PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; YERSINIA; YERSINIA PSEUDOTUBERCULOSIS;

EID: 0036408896     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2002.03191.x     Document Type: Article

References (51)

1. Aitken, A. (1995) 14-3-3 Proteins on the MAP. Trends Biochem. Sci. 20, 95-97.
2. Aitken, A., Jones, D., Soneji, Y. & Howell, S. (1995) 14-3-3 Proteins: Biological function and domain structure, Biochem. Soc. Trans. 23, 605-611.
3. Fu, H., Subramanian, R.R. & Masters, S.C. (2000) 14-3-3 Proteins: Structure, function, and regulation. Annu. Rev. Pharmacol Toxicol. 40, 617-647.
4. Su, T.T., Parry, D.H., Donahoe, B., Chien, C.T., O'Farrell, P.H. & Purdy, A. (2001) Cell cycle roles for two 14-3-3 proteins during Drosophila development. J. Cell Sci. 114, 3445-3454.
5. Broadie, K., Rushton, E., Skoulakis, E.M. & Davis, R.L. (1997) Leonardo, a Drosophila 14-3-3 protein involved in learning, regulates presynaptic function. Neuron 19, 391-402.
6. Ford, J.C., al-Khodairy, F., Fotou, E., Sheldrick, K.S., Griffiths, D.J. & Carr, A.M. (1994) 14-3-3 Protein homologs required for the DNA damage checkpoint in fission yeast. Science 265, 533-535.
7. van Heusden, G.P., Griffiths, D.J., Ford, J.C., Chin, A.W.T.F., Schrader, P.A., Carr, A.M. & Steensma, H.Y. (1995) The 14-3-3 proteins encoded by the BMH1 and BMH2 genes are essential in the yeast Saccharomyces cerevisiae and can be replaced by a plant homologue. Eur. J. Biochem. 229, 45-53.
8. Fantl, W.J., Muslin, A.J., Kikuchi, A., Martin, J.A., MacNicol, A.M., Gross, R.W. & Williams, L.T. (1994) Activation of Raf-1 by 14-3-3 proteins. Nature 371, 612-614.
9. Xing, H., Kornfeld, K. & Muslin, A.J. (1997) The protein kinase KSR interacts with 14-3-3 protein and Raf. Curr. Biol. 7, 294-300.
10. Zhang, L., Chen, J. & Fu, H. (1999) Suppression of apoptosis signal-regulating kinase 1-induced cell death by 14-3-3 proteins. Proc. Natl. Acad. Sci. USA 96, 8511-8515.
11. Fanger, G.R., Widmann, C., Porter, A.C., Sather, S., Johnson, G.L. & Vaillancourt, R.R. (1998) 14-3-3 Proteins interact with specific MEK kinases. J. Biol. Chem. 273, 3476-3483.
12. Reuther, G.W., Fu, H., Cripe, L.D., Collier, R.J. & Pendergast, A.M. (1994) Association of the protein kinases c-Bcr and Bcr-Abl with proteins of the 14-3-3 family. Science 266, 129-133.
13. Hausser, A., Storz, P., Link, G., Stoll, H., Liu, Y.C., Altman, A., Pfizenmaier, K. & Johannes, F.J. (1999) Protein kinase C mu is negatively regulated by 14-3-3 signal transduction proteins. J. Biol. Chem. 274, 9258-9264.
14. Zha, J., Harada, H., Yang, E., Jockel, J. & Korsmeyer, S.J. (1996) Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X (L). Cell 87, 619-628.
15. Brunet, A., Bonni, A., Zigmond, M.J., Lin, M.Z., Juo, P., Hu, L.S., Anderson, M.J., Arden, K.C., Blenis, J. & Greenberg, M.E. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868.
16. Liu, D., Bienkowska, J., Petosa, C., Collier, R.J., Fu, H. & Liddington, R. (1995) Crystal structure of the zeta isoform of the 14-3-3 protein. Nature 376, 191-194.
17. Xiao, B., Smerdon, S.J., Jones, D.H., Dodson, G.G., Soneji, Y., Aitken, A. & Gamblin, S.J. (1995) Structure of a 14-3-3 protein and implications for coordination of multiple signalling pathways. Nature 376, 188-191.
18. Wu, K., Lu, G., Sehnke, P. & Ferl, R.J. (1997) The heterologous interactions among plant 14-3-3 proteins and identification of regions that are important for dimerization. Arch. Biochem. Biophys. 339, 2-8.
19. Jones, D.H., Martin, H., Madrazo, J., Robinson, K.A., Nielsen, P., Roseboom, P.H., Patel, Y., Howell, S.A. & Aitken, A. (1995) Expression and structural analysis of 14-3-3 proteins. J. Mol. Biol. 245, 375-384.
20. Wang, H., Zhang, L., Liddington, R. & Fu, H. (1998) Mutations in the hydrophobic surface of an amphipathic groove of 14-3-3zeta disrupt its interaction with Raf-1 kinase. J. Biol. Chem. 273, 16297-16304.
21. Yaffe, M.B., Rittinger, K., Volinia, S., Caron, P.R., Aitken, A., Leffers, H., Gamblin, S.J., Smerdon, S.J. & Cantley, L.C. (1997) The structural basis for 14-3-3: Phosphopeptide binding specificity. Cell. 91, 961-971.
22. Tzivion, G. & Avruch, J. (2002) 14-3-3 Proteins: Active cofactors in cellular regulation by serine/threonine phosphorylation. J. Biol. Chem. 277, 3061-3064.
23. Kimura, M.T., Irie, S., Shoji-Hoshino, S., Mukai, J., Nadano, D., Oshimura, M. & Sato, T.A. (2001) 14-3-3 Is involved in p75 neurotrophin receptor-mediated signal transduction. J. Biol. Chem. 276, 17291-17300.
24. Campbell, J.K., Gurung, R., Romero, S., Speed, C.J., Andrews, R.K., Berndt, M.C. & Mitchell, C.A. (1997) Activation of the 43 kDa inositol polyphosphate 5-phosphatase by 14-3-3zeta. Biochemistry 36, 15363-15370.
25. Muslin, A.J. & Xing, H. (2000) 14-3-3 Proteins: Regulation of subcellular localization by molecular interference. Cell Signal. 12, 703-709.
26. Seimiya, H., Sawada, H., Muramatsu, Y., Shimizu, M., Ohko, K., Yamane, K. & Tsuruo, T. (2000) Involvement of 14-3-3 proteins in nuclear localization of telomerase. EMBO J. 19, 2652-2661.
27. Masters, S.C., Pederson, K.J., Zhang, L., Barbieri, J.T. & Fu, H. (1999) Interaction of 14-3-3 with a nonphosphorylated protein ligand, exoenzyme S of Pseudomonas aeruginosa. Biochemistry 38, 5216-5221.
28. Fu, H., Coburn, J. & Collier, R.J. (1993) The eukaryotic host factor that activates exoenzyme S of Pseudomonas aeruginosa is a member of the 14-3-3 protein family. Proc. Natl. Acad. Sci. USA 90, 2320-2324.
29. Henriksson, M.L., Troller, U. & Hallberg, B. (2000) 14-3-3 Proteins are required for the inhibition of Ras by exoenzyme S. Biochem. J. 349, 697-701.
30. Gu, M.&., 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.
31. Calverley, D.C., Kavanagh, T.J. & Roth, G.J. (1998) Human signaling protein 14-3-3zeta interacts with platelet glycoprotein Ib subunits Ibalpha and Ibbeta. Blood 91, 1295-1303.
32. Andrews, R.K., Harris, S.J., McNally, T. & Berndt, M.C. (1998) Binding of purified 14-3-3 zeta signaling protein to discrete amino acid sequences within the cytoplasmic domain of the platelet membrane glycoprotein Ib-IX-V complex. Biochemistry 37, 638-647.
33. Petosa, C., Masters, S.C., Bankston, L.A., Pohl, J., Wang, B., Fu, H. & Liddington, R.C. (1998) 14-3-3zeta binds a phos-phorylated Raf peptide and an unphosphorylated peptide via its conserved amphipathic groove. J. Biol. Chem. 273, 16305-16310.
34. Henriksson, M.L., Sundin, C., Jansson, A.L., Forsberg, A., Palmer, R.H. & Hallberg, B. (2002) Exosenzyme S show selective ADP-ribosylation and GAP activities towards small GTPases in vivo. Biochem. J., in press.
35. Henriksson, M.L., Rosqvist, R., Telepnev, M., Wolf-Watz, H. & Hallberg, B. (2000) Ras effector pathway activation by epidermal growth factor is inhibited in vivo by exoenzyme S ADP-ribosylation of Ras. Biochem. J. 347, 217-222.
36. McGuffie, E.M., Frank, D.W., Vincent, T.S. & Olson, J.C. (1998) Modification of Ras in eukaryotic cells by Pseudomonas aeruginosa exoenzyme S. Infect Immun. 66, 2607-2613.
37. Goehring, U.M., Schmidt, G., Pederson, K.J., Aktories, K. & Barbieri, J.T. (1999) The N-terminal domain of Pseudomonas aeruginosa exoenzyme S is a GTPase- activating protein for Rho GTPases. J. Biol. Chem. 274, 36369-36372.
38. Frithz-Lindsten, E.Y., Rosqvist, R. & Forsberg, A. (1997) Intra-cellular targeting of exoenzyme S of Pseudomonas aeruginosa via type III-dependent translocation induces phagocytosis resistance, cytotoxicity and disruption of actin microfilaments. Mol. Microbiol. 25, 1125-1139.
39. Dubois, T., Rommel, C., Howell, S., Steinhussen, U., Soneji, Y., Morrice, N., Moelling, K. & Aitken, A. (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.
40. Rodriguez-Viciana, P., Warne, P.H., Khwaja, A., Marte, B.M., Pappin, D., Das, P., Waterfield, M.D., Ridley, A. & Downward, J. (1997) Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras. Cell 89, 457-467.
41. Wiltfang, J., Otto, M., Baxter, H.C., Bodemer, M., Steinacker, P., Bahn, E., Zerr, I., Kornhuber, J., Kretzschmar, H.A., Poser, S., Ruther, E. & Aitken, A. (1999) Isoform pattern of 14-3-3 proteins in the cerebrospinal fluid of patients with Creutzfeldt-Jakob disease. J. Neurochem. 73, 2485-2490.
42. Yahr, T.L., Goranson, J. & Frank, D.W. (1996) Exoenzyme S of Pseudomonas aeruginosa is secreted by a type III pathway. Mol. Microbiol. 22, 991-1003.
43. Francis, M.S. & Wolf-Watz, H. (1998) YopD of Yersinia pseudotuberculosis is translocated into the cytosol of HeLa epithelial cells: Evidence of a structural domain necessary for translocation. Mol. Microbiol. 29, 799-813.
44. Francis, M.S., Aili, M., Wiklund, M.L. & Wolf-Watz, H. (2000) A study of the YopD-lcrH interaction from Yersinia pseudotuberculosis reveals a role for hydrophobic residues within the amphipathic domain of YopD. Mol. Microbiol. 38, 85-102.
45. Francis, M.S., Lloyd, S.A. & Wolf-Watz, H. (2001) The type III secretion chaperone LcrH co-operates with YopD to establish a negative, regulatory loop for control of Yop synthesis in Yersinia pseudotuberculosis. Mol. Microbiol. 42, 1075-1093.
46. Masters, S.C. & Fu, H. (2001) 14-3-3 Proteins mediate an essential anti-apoptotic signal. J. Biol. Chem. 276, 45193-45200.
47. Muslin, A.J., Tanner, J.W., Allen, P.M. & Shaw, A.S. (1996) Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84, 889-897.
48. Sundin, C., Henriksson, M.L., Hallberg, B., Forsberg, A. & Frithz-Lindsten, E. (2001) Exoenzyme T of Pseudomonas aeruginosa elicits cytotoxicity without interfering with Ras signal transduction. Cell. Microbiol. 3, 237-246.
49. Kaufman, M.R., Jia, J., Zeng, L., Ha, U., Chow, M. & Jin, S. (2000) Pseudomonas aeruginosa mediated apoptosis requires the ADP-ribosylating activity of exoS. Microbiology 146, 2531-2541.
50. Suginta, W., Karoulias, N., Aitken, A. & Ashley, R.H. (2001) Chloride intracellular channel protein CLIC4 (p64H1) binds directly to brain dynamin I in a complex containing actin, tubulin and 14-3-3 isoforms. Biochem. J. 359, 55-64.
51. Rittinger, K., Budman, J., Xu, J., Volinia, S., Cantley, L.C., Smerdon, S.J., Gamblin, S.J. & 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.