A robust protocol to map binding sites of the 14-3-3 interactome: Cdc25C requires phosphorylation of both S216 and S263 to bind 14-3-3

Molecular and Cellular Proteomics

Volumn 10, Issue 3, 2011, Pages

  Chan, Perry M ^a,b   Ng, Yuen Wai ^a,b   Manser, Ed ^a,b,c  

^a AGENCY FOR SCIENCE   (Singapore)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^c INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; CELL CYCLE PROTEIN 25C; CELL CYCLE PROTEIN 25C S216; CELL CYCLE PROTEIN 25C S263; INSULIN RECEPTOR SUBSTRATE 1; PROTEIN 14 3 3; PROTEIN KINASE C; PROTEIN P53; PROTEOME; SERINE; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG; AMINO ACID; IMMOBILIZED PROTEIN; PHOSPHOPEPTIDE; PHOSPHOSERINE; PROTEIN TYROSINE PHOSPHATASE;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; BIOINFORMATICS; CONTROLLED STUDY; IMMUNOPRECIPITATION; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; AMINO ACID SUBSTITUTION; CHEMISTRY; HUMAN; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; PHOSPHORYLATION; PROTEIN ANALYSIS; REPRODUCIBILITY; SURFACE PLASMON RESONANCE;

EUKARYOTA;

14-3-3 PROTEINS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO ACIDS; BINDING SITES; CDC25 PHOSPHATASES; HUMANS; IMMOBILIZED PROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHOPEPTIDES; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN KINASE C; REPRODUCIBILITY OF RESULTS; SURFACE PLASMON RESONANCE;

EID: 79953226710     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.005157     Document Type: Article

References (51)

1. Moore, B. W., and Perez, V. J. (1967) Specific Acid Proteins in the Nervous System. Physiological and Biochemical Aspects of Nervous Integration. 343-359, Prentice Hall, New Jersey, U.S.A.
2. Muslin, A. J., Tanner, 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 (Pubitemid 26106858)
3. Hunter, T., and Sefton, B. M. (1980) Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc. Natl. Acad. Sci. U.S.A. 77, 1311-1315
4. Morrison, D. K. (2009) The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development. Trends Cell Biol. 19, 16-23
5. Dougherty, M. K., and Morrison, D. K. (2004) Unlocking the code of 14-3-3. J. Cell Sci. 117, 1875-1884
6. Gardino, A. K., Smerdon, S. J., and Yaffe, M. B. (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
7. Johnson, C., Crowther, S., Stafford, M. J., Campbell, D. G., Toth, R., and MacKintosh, C. (2010) Bioinformatic and experimental survey of 14-3-3- binding sites. Biochem. J. 427, 69-78
8. Bridges, D., and Moorhead, G. B. (2005) 14-3-3 proteins: a number of functions for a numbered protein. Sci. STKE 2005, re10
9. Aitken, A., Collinge, D. B., van Heusden, B. P., Isobe, T., Roseboom, P. H., Rosenfeld, G., and Soll, J. (1992) 14-3-3 proteins: a highly conserved, widespread family of eukaryotic proteins. Trends Biochem. Sci 17, 498-501
10. Jin, J., Smith, F. D., Stark, C., Wells, C. D., Fawcett, J. P., Kulkarni, S., Metalnikov, P., O'Donnell, P., Taylor, P., Taylor, L., Zougman, A., Woodgett, J. R., Langeberg, L. K., Scott, J. D., and Pawson, T. (2004) Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Curr. Biol. 14, 1436-1450
11. Pozuelo Rubio, M., Geraghty, K. M., Wong, B. H., Wood, N. T., Campbell, D. G., Morrice, N., and Mackintosh, C. (2004) 14-3-3-affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation and trafficking. Biochem. J. 379, 395-408 (Pubitemid 38570113)
12. Meek, S. E., Lane, W. S., and Piwnica-Worms, H. (2004) Comprehensive proteomic analysis of interphase and mitotic 14-3-3-binding proteins. J. Biol. Chem. 279, 32046-32054
13. Angrand, P. O., Segura, I., Völkel, P., Ghidelli, S., Terry, R., Brajenovic, M., Vintersten, K., Klein, R., Superti-Furga, G., Drewes, G., Kuster, B., Bouwmeester, T., and Acker-Palmer, A. (2006) Transgenic mouse proteomics identifies new 14-3-3-associated proteins involved in cytoskeletal rearrangements and cell signaling. Mol Cell Proteomics 5, 2211-2227 (Pubitemid 46040629)
14. Benzinger, A., Muster, N., Koch, H. B., Yates, J. R., 3rd, and Hermeking, H. (2005) Targeted proteomic analysis of 14-3-3 sigma, a p53 effector commonly silenced in cancer. Mol Cell Proteomics. 4, 785-795 (Pubitemid 40873007)
15. 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
16. Obenauer, J. C., Cantley, L. C., and Yaffe, M. B. (2003) Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31, 3635-3641
17. Brune, D. C., Hampton, B., Kobayashi, R., Leone, J. W., Linse, K. D., Pohl, J., Thoma, R. S., and Denslow, N. D. (2007) ABRF ESRG 2006 study: Edman sequencing as a method for polypeptide quantitation. J Biomol Tech 18, 306-320
18. Thoma, R. S., Smith, J. S., Sandoval, W., Leone, J. W., Hunziker, P., Hampton, B., Linse, K. D., and Denslow, N. D. (2009) The ABRF Edman Sequencing Research Group 2008 Study: investigation into homopolymeric amino acid N-terminal sequence tags and their effects on automated Edman degradation. J Biomol Tech 20, 216-225
19. 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
20. Yeow-Fong, L., Lim, L., and Manser, E. (2005) SNX9 as an adaptor for linking synaptojanin-1 to the Cdc42 effector ACK1. FEBS Lett. 579, 5040-5048 (Pubitemid 41242850)
21. Yaffe, M. B., Leparc, G. G., Lai, J., Obata, T., Volinia, S., and Cantley, L. C. (2001) A motif-based profile scanning approach for genome-wide prediction of signaling pathways. Nat Biotechnol 19, 348-353
22. Wilson, D. S., Keefe, A. D., and Szostak, J. W. (2001) The use of mRNA display to select high-affinity protein-binding peptides. Proc. Natl. Acad. Sci. U.S.A. 98, 3750-3755
23. Robens, J. M., Lee, Y. F., Ng, E., Hall, C., and Manser, E. (2010) Regulation of IRSp53-dependent filopodial dynamics by antagonism between 14- 3-3 binding and SH3-mediated localization. Mol. Cell. Biol. 30, 829-844
24. Yang, X., Lee, W. H., Sobott, F., Papagrigoriou, E., Robinson, C. V., Grossmann, J. G., Sundström, M., Doyle, D. A., and Elkins, J. M. (2006) Structural basis for protein-protein interactions in the 14-3-3 protein family. Proc. Natl. Acad. Sci. U.S.A. 103, 17237-17242
25. 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 (Pubitemid 32429515)
26. Tokumitsu, H., Hatano, N., Inuzuka, H., Sueyoshi, Y., Yokokura, S., Ichimura, T., Nozaki, N., and Kobayashi, R. (2005) Phosphorylation of Numb family proteins. Possible involvement of Ca2+/calmodulin-dependent protein kinases. J. Biol. Chem. 280, 35108-35118
27. Smith, C. A., Lau, K. M., Rahmani, Z., Dho, S. E., Brothers, G., She, Y. M., Berry, D. M., Bonneil, E., Thibault, P., Schweisguth, F., Le Borgne, R., and McGlade, C. J. (2007) aPKC-mediated phosphorylation regulates asymmetric membrane localization of the cell fate determinant Numb. EMBO J. 26, 468-480 (Pubitemid 46160947)
28. White, R. R., Kwon, Y. G., Taing, M., Lawrence, D. S., and Edelman, A. M. (1998) Definition of optimal substrate recognition motifs of Ca2+-calmodulin-dependent protein kinases IV and II reveals shared and distinctive features. J. Biol. Chem. 273, 3166-3172
29. Göransson, O., Deak, M., Wullschleger, S., Morrice, N. A., Prescott, A. R., and Alessi, D. R. (2006) Regulation of the polarity kinases PAR-1/MARK by 14-3-3 interaction and phosphorylation. J. Cell Sci. 119, 4059-4070
30. Rajagopalan, S., Jaulent, A. M., Wells, M., Veprintsev, D. B., and Fersht, A. R. (2008) 14-3-3 activation of DNA binding of p53 by enhancing its association into tetramers. Nucleic Acids Res. 36, 5983-5991
31. Silhan, J., Obsilova, V., Vecer, J., Herman, P., Sulc, M., Teisinger, J., and Obsil, T. (2004) 14-3-3 protein C-terminal stretch occupies ligand binding groove and is displaced by phosphopeptide binding. J. Biol. Chem. 279, 49113-49119
32. Yang, J., Winkler, K., Yoshida, M., and Kornbluth, S. (1999) Maintenance of G2 arrest in the Xenopus oocyte: a role for 14-3-3-mediated inhibition of Cdc25 nuclear import. EMBO J. 18, 2174-2183 (Pubitemid 29179174)
33. Perdiguero, E., and Nebreda, A. R. (2004) Regulation of Cdc25C activity during the meiotic G2/M transition. Cell Cycle 3, 733-737
34. Kumagai, A., and Dunphy, W. G. (1999) Binding of 14-3-3 proteins and nuclear export control the intracellular localization of the mitotic inducer Cdc25. Genes Dev. 13, 1067-1072
35. Kumagai, A., Yakowec, P. S., and Dunphy, W. G. (1998) 14-3-3 proteins act as negative regulators of the mitotic inducer Cdc25 in Xenopus egg extracts. Mol. Biol. Cell 9, 345-354
36. Peng, C. Y., Graves, P. R., Thoma, R. S., Wu, Z., Shaw, A. S., and Piwnica-Worms, H. (1997) Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science 277, 1501-1505 (Pubitemid 27449237)
37. Peng, C. Y., Graves, P. R., Ogg, S., Thoma, R. S., Byrnes, M. J., 3rd, Wu, Z., Stephenson, M. T., and Piwnica-Worms, H. (1998) C-TAK1 protein kinase phosphorylates human Cdc25C on serine 216 and promotes 14-3-3 protein binding. Cell Growth & Differ. 9, 197-208 (Pubitemid 28354300)
38. Dalal, S. N., Schweitzer, C. M., Gan, J., and DeCaprio, J. A. (1999) Cytoplasmic localization of human cdc25C during interphase requires an intact 14-3-3 binding site. Mol. Cell. Biol. 19, 4465-4479
39. Boutros, R., Dozier, C., and Ducommun, B. (2006) The when and wheres of CDC25 phosphatases. Curr Opin Cell Biol. 18, 185-191 (Pubitemid 43375887)
40. Graves, P. R., Lovly, C. M., Uy, G. L., and Piwnica-Worms, H. (2001) Localization of human Cdc25C is regulated both by nuclear export and 14-3-3 protein binding. Oncogene 20, 1839-1851 (Pubitemid 32458694)
41. Esmenjaud-Mailhat, C., Lobjois, V., Froment, C., Golsteyn, R. M., Monsarrat, B., and Ducommun, B. (2007) Phosphorylation of CDC25C at S263 controls its intracellular localisation. FEBS Lett. 581, 3979-3985 (Pubitemid 47212098)
42. Mackintosh, C. (2004) Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem. J. 381, 329-342
43. Seet, B. T., Berry, D. M., Maltzman, J. S., Shabason, J., Raina, M., Koretzky, G. A., McGlade, C. J., and Pawson, T. (2007) Efficient T-cell receptor signaling requires a high-affinity interaction between the Gads C-SH3 domain and the SLP-76 RxxK motif. EMBO J. 26, 678-689
44. Rhyu, M. S., Jan, L. Y., and Jan, Y. N. (1994) Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 76, 477-491
45. Knoblich, J. A., Jan, L. Y., and Jan, Y. N. (1995) Asymmetric segregation of Numb and Prospero during cell division. Nature 377, 624-627
46. Suzuki, A., Hirata, M., Kamimura, K., Maniwa, R., Yamanaka, T., Mizuno, K., Kishikawa, M., Hirose, H., Amano, Y., Izumi, N., Miwa, Y., and Ohno, S. (2004) aPKC acts upstream of PAR-1b in both the establishment and maintenance of mammalian epithelial polarity. Curr. Biol. 14, 1425-1435
47. Sanchez, Y., Wong, C., Thoma, R. S., Richman, R., Wu, Z., Piwnica-Worms, H., and Elledge, S. J. (1997) Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science 277, 1497-1501 (Pubitemid 27449236)
48. Blasina, A., de Weyer, I. V., Laus, M. C., Luyten, W. H., Parker, A. E., and McGowan, C. H. (1999) A human homologue of the checkpoint kinase Cds1 directly inhibits Cdc25 phosphatase. Curr. Biol. 9, 1-10
49. Wagner, M., Adamczak, R., Porollo, A., and Meller, J. (2005) Linear regression models for solvent accessibility prediction in proteins. J Comput Biol 12, 355-369 (Pubitemid 40586438)
50. Diella, F., Gould, C. M., Chica, C., Via, A., and Gibson, T. J. (2008) Phospho. ELM: a database of phosphorylation sites-update 2008. Nucleic Acids Res. 36, D240-244
51. Ewing, R. M., Chu, P., Elisma, F., Li, H., Taylor, P., Climie, S., McBroom- Cerajewski, L., Robinson, M. D., O'Connor, L., Li, M., Taylor, R., Dharsee, M., Ho, Y., Heilbut, A., Moore, L., Zhang, S., Ornatsky, O., Bukhman, Y. V., Ethier, M., Sheng, Y., Vasilescu, J., Abu-Farha, M., Lambert, J. P., Duewel, H. S., Stewart, I. I., Kuehl, B., Hogue, K., Colwill, K., Gladwish, K., Muskat, B., Kinach, R., Adams, S. L., Moran, M. F., Morin, G. B., Topaloglou, T., and Figeys, D. (2007) Large-scale mapping of human protein-protein interactions by mass spectrometry. Mol Syst Biol 3, 89