Docking interactions in protein kinase and phosphatase networks

Current Opinion in Structural Biology

Volumn 16, Issue 6, 2006, Pages 676-685

  Reményi, Attila ^a   Good, Matthew C ^a   Lim, Wendell A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CYCLIN DEPENDENT KINASE; DOCKING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE;

ALLOSTERISM; ENZYME ACTIVE SITE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; SEQUENCE ANALYSIS;

ALLOSTERIC REGULATION; BINDING SITES; DRUG DESIGN; MAP KINASE SIGNALING SYSTEM; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN CONFORMATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION;

EID: 33947256308     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2006.10.008     Document Type: Review

References (50)

1. Bhattacharyya R.P., Remenyi A., Yeh B.J., and Lim W.A. Domains, motifs, and scaffolds: the role of modular interactions in the evolution and wiring of cell signaling circuits. Annu Rev Biochem 75 (2006) 655-680
2. Miller W.T. Determinants of substrate recognition in nonreceptor tyrosine kinases. Acc Chem Res 36 (2003) 393-400
3. Biondi R.M., and Nebreda A.R. Signalling specificity of Ser/Thr protein kinases through docking-site-mediated interactions. Biochem J 372 (2003) 1-13
4. Lee S., Lin X., Nam N.H., Parang K., and Sun G. Determination of the substrate-docking site of protein tyrosine kinase C-terminal Src kinase. Proc Natl Acad Sci USA 100 (2003) 14707-14712
5. Lee S., Ayrapetov M.K., Kemble D.J., Parang K., and Sun G. Docking-based substrate recognition by the catalytic domain of a protein tyrosine kinase, C-terminal Src kinase (Csk). J Biol Chem 281 (2006) 8183-8189
6. Neduva V., and Russell R.B. Linear motifs: evolutionary interaction switches. FEBS Lett 579 (2005) 3342-3345
7. Letunic I., Copley R.R., Pils B., Pinkert S., Schultz J., and Bork P. SMART 5: domains in the context of genomes and networks. Nucleic Acids Res 34 (2006) D257-D260
8. Finn R.D., Mistry J., Schuster-Bockler B., Griffiths-Jones S., Hollich V., Lassmann T., Moxon S., Marshall M., Khanna A., Durbin R., et al. Pfam: clans, web tools and services. Nucleic Acids Res 34 (2006) D247-D251
9. Neduva V., and Russell R.B. DILIMOT: discovery of linear motifs in proteins. Nucleic Acids Res 34 (2006) W350-W355
10. Davey N.E., Shields D.C., and Edwards R.J. SLiMDisc: short, linear motif discovery, correcting for common evolutionary descent. Nucleic Acids Res 34 (2006) 3546-3554
11. Neduva V., Linding R., Su-Angrand I., Stark A., de Masi F., Gibson T.J., Lewis J., Serrano L., and Russell R.B. Systematic discovery of new recognition peptides mediating protein interaction networks. PLoS Biol 3 (2005) e405. This study demonstrates that linear binding motifs can be detected using data from genome-scale interaction studies. This approach greatly facilitates the discovery of short peptide motifs that mediate protein-protein association.
12. Espanel X., Walchli S., Ruckle T., Harrenga A., Huguenin-Reggiani M., and van Huijsduijnen R.H. Mapping of synergistic components of weakly interacting protein-protein motifs using arrays of paired peptides. J Biol Chem 278 (2003) 15162-15167
13. Espanel X., and van Huijsduijnen R.H. Applying the SPOT peptide synthesis procedure to the study of protein tyrosine phosphatase substrate specificity: probing for the heavenly match in vitro. Methods 35 (2005) 64-72
14. Ceulemans H., and Bollen M. Functional diversity of protein phosphatase-1, a cellular economizer and reset button. Physiol Rev 84 (2004) 1-39
15. Garcia A., Cayla X., Caudron B., Deveaud E., Roncal F., and Rebollo A. New insights in protein phosphorylation: a signature for protein phosphatase 1 interacting proteins. C R Biol 327 (2004) 93-97
16. Egloff M.P., Johnson D.F., Moorhead G., Cohen P.T., Cohen P., and Barford D. Structural basis for the recognition of regulatory subunits by the catalytic subunit of protein phosphatase 1. EMBO J 16 (1997) 1876-1887
17. Terrak M., Kerff F., Langsetmo K., Tao T., and Dominguez R. Structural basis of protein phosphatase 1 regulation. Nature 429 (2004) 780-784. The complex crystal structure between PP1 and its myosin phosphatase targeting subunit (MYPT1) revealed that interactions between the RVxF motif of MYPT1 and the PP1 docking groove represent the single most important contribution to the formation of the PP1-MYPT1 complex.
18. Meiselbach H., Sticht H., and Enz R. Structural analysis of the protein phosphatase 1 docking motif: molecular description of binding specificities identifies interacting proteins. Chem Biol 13 (2006) 49-59. In this study, a more restrictive definition of the RVxF motif is presented based on systematic protein-protein binding analysis and computational modeling. Using this more stringent motif definition, the authors correctly predict novel PP1-binding partners with great accuracy.
19. Gibbons J.A., Weiser D.C., and Shenolikar S. Importance of a surface hydrophobic pocket on protein phosphatase-1 catalytic subunit in recognizing cellular regulators. J Biol Chem 280 (2005) 15903-15911
20. Aramburu J., Garcia-Cozar F., Raghavan A., Okamura H., Rao A., and Hogan P.G. Selective inhibition of NFAT activation by a peptide spanning the calcineurin targeting site of NFAT. Mol Cell 1 (1998) 627-637
21. Li H., Rao A., and Hogan P.G. Structural delineation of the calcineurin-NFAT interaction and its parallels to PP1 targeting interactions. J Mol Biol 342 (2004) 1659-1674. If co-crystallization with docking peptides fails, alternative techniques such as cross-linking and modeling studies combined with experimental validation can still be used to map the docking interaction surface, as was demonstrated in this study of the calcineurin-NFAT system.
22. + channel, TRESK. J Biol Chem 281 (2006) 14677-14682
23. Kusari A.B., Molina D.M., Sabbagh Jr. W., Lau C.S., and Bardwell L. A conserved protein interaction network involving the yeast MAP kinases Fus3 and Kss1. J Cell Biol 164 (2004) 267-277
24. Chang C.I., Xu B.E., Akella R., Cobb M.H., and Goldsmith E.J. Crystal structures of MAP kinase p38 complexed to the docking sites on its nuclear substrate MEF2A and activator MKK3b. Mol Cell 9 (2002) 1241-1249
25. Heo Y.S., Kim S.K., Seo C.I., Kim Y.K., Sung B.J., Lee H.S., Lee J.I., Park S.Y., Kim J.H., Hwang K.Y., et al. Structural basis for the selective inhibition of JNK1 by the scaffolding protein JIP1 and SP600125. EMBO J 23 (2004) 2185-2195
26. Liu S., Sun J.P., Zhou B., and Zhang Z.Y. Structural basis of docking interactions between ERK2 and MAP kinase phosphatase 3. Proc Natl Acad Sci USA 103 (2006) 5326-5331
27. Zhou T., Sun L., Humphreys J., and Goldsmith E.J. Docking interactions induce exposure of activation loop in the MAP kinase ERK2. Structure 14 (2006) 1011-1019
28. Dimitri C.A., Dowdle W., MacKeigan J.P., Blenis J., and Murphy L.O. Spatially separate docking sites on ERK2 regulate distinct signaling events in vivo. Curr Biol 15 (2005) 1319-1324. This study shows that the activity of the ERK2 pathway can be selectively inhibited by mutation of specific docking grooves on the MAPK. Signal flow to DEF-motif-containing substrates or to D-motif-containing substrates can be blocked by mutating the corresponding interaction sites on ERK2.
29. Lee T., Hoofnagle A.N., Kabuyama Y., Stroud J., Min X., Goldsmith E.J., Chen L., Resing K.A., and Ahn N.G. Docking motif interactions in MAP kinases revealed by hydrogen exchange mass spectrometry. Mol Cell 14 (2004) 43-55. The authors demonstrate the value of HXMS in tracking conformational changes of the MAPKs p38 and ERK2. Addition of DEF- and D-motif peptides leads to conformational changes that are inferred from hydrogen-deuterium exchange rates.
30. Vinciguerra M., Vivacqua A., Fasanella G., Gallo A., Cuozzo C., Morano A., Maggiolini M., and Musti A.M. Differential phosphorylation of c-Jun and JunD in response to the epidermal growth factor is determined by the structure of MAPK targeting sequences. J Biol Chem 279 (2004) 9634-9641
31. Takekawa M., Tatebayashi K., and Saito H. Conserved docking site is essential for activation of mammalian map kinase kinases by specific MAP kinase kinase kinases. Mol Cell 18 (2005) 295-306
32. Tatebayashi K., Takekawa M., and Saito H. A docking site determining specificity of Pbs2 MAPKK for Ssk2/Ssk22 MAPKKKs in the yeast HOG pathway. EMBO J 22 (2003) 3624-3634
33. Frodin M., Jensen C.J., Merienne K., and Gammeltoft S. A phosphoserine-regulated docking site in the protein kinase RSK2 that recruits and activates PDK1. EMBO J 19 (2000) 2924-2934
34. Biondi R.M., Cheung P.C., Casamayor A., Deak M., Currie R.A., and Alessi D.R. Identification of a pocket in the PDK1 kinase domain that interacts with PIF and the C-terminal residues of PKA. EMBO J 19 (2000) 979-988
35. Biondi R.M., Komander D., Thomas C.C., Lizcano J.M., Deak M., Alessi D.R., and van Aalten D.M. High resolution crystal structure of the human PDK1 catalytic domain defines the regulatory phosphopeptide docking site. EMBO J 21 (2002) 4219-4228
36. Dajani R., Fraser E., Roe S.M., Young N., Good V., Dale T.C., and Pearl L.H. Crystal structure of glycogen synthase kinase 3 beta: structural basis for phosphate-primed substrate specificity and autoinhibition. Cell 105 (2001) 721-732
37. Cheng K.Y., Noble M.E., Skamnaki V., Brown N.R., Lowe E.D., Kontogiannis L., Shen K., Cole P.A., Siligardi G., and Johnson L.N. The role of the phospho-CDK2/cyclin A recruitment site in substrate recognition. J Biol Chem 281 (2006) 23167-23179
38. Loog M., and Morgan D.O. Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates. Nature 434 (2005) 104-108. For some CDK-cyclins, a substrate-docking groove is found on the cyclin. Two cyclins, Clb5 and Clb2, use distinct mechanisms to enhance the phosphorylation of S-phase and M-phase substrates by CDK1. Efficient substrate phosphorylation by Clb5-CDK1, but not by Clb2-CDK1, requires RXL substrate docking motifs.
39. Remenyi A., Good M.C., Bhattacharyya R.P., and Lim W.A. The role of docking interactions in mediating signaling input, output, and discrimination in the yeast MAPK network. Mol Cell 20 (2005) 951-962. Structural analysis reveals that the yeast Fus3 MAPK interacts with specific and promiscuous D-motif peptides using conformationally distinct modes. The study suggests that induced-fit recognition may allow docking peptides to achieve discrimination by exploiting subtle differences in kinase flexibility. This finding provides a mechanism for how D-motif-containing interaction partners can selectively bind MAPKs through a common docking groove.
40. Bhattacharyya R.P., Remenyi A., Good M.C., Bashor C.J., Falick A.M., and Lim W.A. The Ste5 scaffold allosterically modulates signaling output of the yeast mating pathway. Science 311 (2006) 822-826. An interaction between Fus3 and the Ste5 scaffold is mediated by a 30 amino acid long peptide, which binds to both the N-terminal and the C-terminal kinase lobes via a flexible linker region. Interestingly, in contrast to D-motifs, Ste5 peptide binding in this bipartite fashion increases Fus3 activity by upregulating autoactivation (∼50-fold) of a tyrosine residue in the activation loop.
41. Kang S., Li H., Rao A., and Hogan P.G. Inhibition of the calcineurin-NFAT interaction by small organic molecules reflects binding at an allosteric site. J Biol Chem 280 (2005) 37698-37706
42. Tarrega C., Rios P., Cejudo-Marin R., Blanco-Aparicio C., van den Berk L., Schepens J., Hendriks W., Tabernero L., and Pulido R. ERK2 shows a restrictive and locally selective mechanism of recognition by its tyrosine phosphatase inactivators not shared by its activator MEK1. J Biol Chem 280 (2005) 37885-37894
43. Borsello T., Clarke P.G., Hirt L., Vercelli A., Repici M., Schorderet D.F., Bogousslavsky J., and Bonny C. A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat Med 9 (2003) 1180-1186
44. Kelemen B.R., Hsiao K., and Goueli S.A. Selective in vivo inhibition of mitogen-activated protein kinase activation using cell-permeable peptides. J Biol Chem 277 (2002) 8741-8748
45. Guergnon J., Dessauge F., Dominguez V., Viallet J., Bonnefoy S., Yuste V.J., Mercereau-Puijalon O., Cayla X., Rebollo A., Susin S.A., et al. Use of penetrating peptides interacting with PP1/PP2A proteins as a general approach for a drug phosphatase technology. Mol Pharmacol 69 (2006) 1115-1124
46. Roehrl M.H., Kang S., Aramburu J., Wagner G., Rao A., and Hogan P.G. Selective inhibition of calcineurin-NFAT signaling by blocking protein-protein interaction with small organic molecules. Proc Natl Acad Sci USA 101 (2004) 7554-7559. The authors identify inhibitors of calcineurin-NFAT signaling that act at a docking protein-protein contact rather than at the calcineurin catalytic site. This substrate-selective enzyme inhibition arguably represents a practical advance over inhibition by cyclosporine A, which indiscriminately blocks all signaling downstream of calcineurin.
47. Roehrl M.H., Wang J.Y., and Wagner G. Discovery of small-molecule inhibitors of the NFAT-calcineurin interaction by competitive high-throughput fluorescence polarization screening. Biochemistry 43 (2004) 16067-16075
48. Shoichet B.K. Virtual screening of chemical libraries. Nature 432 (2004) 862-865
49. Hancock C.N., Macias A., Lee E.K., Yu S.Y., Mackerell Jr. A.D., and Shapiro P. Identification of novel extracellular signal-regulated kinase docking domain inhibitors. J Med Chem 48 (2005) 4586-4595
50. Manning G., Whyte D.B., Martinez R., Hunter T., and Sudarsanam S. The protein kinase complement of the human genome. Science 298 (2002) 1912-1934