Examining docking interactions on ERK2 with modular peptide substrates

Biochemistry

Volumn 50, Issue 44, 2011, Pages 9500-9510

  Lee, Sunbae ^a   Warthaka, Mangalika ^a   Yan, Chunli ^b   Kaoud, Tamer S ^a,c   Ren, Pengyu ^b,c   Dalby, Kevin N ^a,b,c  

^a Division of Medicinal Chemistry   (United States)

^b The University of Texas at Austin   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; DOCKING SITES; ENERGETIC COUPLING; INHIBITOR DESIGN; KINETIC DATA; LIGAND RECOGNITION; MODULAR DOCKING; PEPTIDE SUBSTRATES; PROTEIN SUBSTRATE; SEQUENTIAL MECHANISM; SIGNALING COMPLEX; STEADY-STATE KINETICS; STERIC MECHANISM; THERMODYNAMIC LINKAGES;

COMPLEXATION; EMPLOYMENT; PEPTIDES; PHOSPHORYLATION;

SUBSTRATES;

ADENOSINE TRIPHOSPHATE; MITOGEN ACTIVATED PROTEIN KINASE 1; PEPTIDE; TRANSCRIPTION FACTOR ETS 1;

ALLOSTERISM; ARTICLE; COMPARATIVE STUDY; COMPLEX FORMATION; CONTROLLED STUDY; ENERGY TRANSFER; ENZYME ACTIVE SITE; ENZYME KINETICS; ENZYME REGULATION; ENZYME SUBSTRATE; MOLECULAR DOCKING; MOLECULAR INTERACTION; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STEADY STATE; STEREOCHEMISTRY; STEREOSPECIFICITY; THERMODYNAMICS;

ALLOSTERIC REGULATION; AMINO ACID SEQUENCE; CATALYTIC DOMAIN; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING; PROTEIN TRANSPORT; SUBSTRATE SPECIFICITY;

EID: 80155206948     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201103b     Document Type: Article

References (52)

1. Avruch, J. (2007) MAP kinase pathways: the first twenty years Biochim. Biophys. Acta 1773, 1150-1160 (Pubitemid 47125973)
2. Raman, M., Chen, W., and Cobb, M. H. (2007) Differential regulation and properties of MAPKs Oncogene 26, 3100-3112 (Pubitemid 46763006)
3. Barsyte-Lovejoy, D., Galanis, A., and Sharrocks, A. D. (2002) Specificity determinants in MAPK signaling to transcription factors J. Biol. Chem. 277, 9896-9903 (Pubitemid 34968095)
4. Schnieders, M. J., Kaoud, T. S., Yan, C., Dalby, K. N., and Ren, P. Computational Insights for the Discovery of Non-ATP Competitive Inhibitors of MAP Kinases. Curr. Pharm. Des. 2011, in press.
5. Tanoue, T., Maeda, R., Adachi, M., and Nishida, E. (2001) Identification of a docking groove on ERK and p38 MAP kinases that regulates the specificity of docking interactions EMBO J. 20, 466-479 (Pubitemid 32126982)
6. Lee, T., Hoofnagle, A. N., Kabuyama, Y., Stroud, J., Min, X., Goldsmith, E. J., Chen, L., Resing, K. A., and Ahn, N. G. (2004) Docking motif interactions in MAP kinases revealed by hydrogen exchange mass spectrometry Mol. Cell 14, 43-55 (Pubitemid 38469908)
7. Callaway, K. A., Rainey, M. A., Riggs, A. F., Abramczyk, O., and Dalby, K. N. (2006) Properties and regulation of a transiently assembled ERK2.Ets-1 signaling complex Biochemistry 45, 13719-13733 (Pubitemid 44788742)
8. Biondi, R. M. and Nebreda, A. R. (2003) Signalling specificity of Ser/Thr protein kinases through docking-site-mediated interactions Biochem. J. 372, 1-13 (Pubitemid 36609602)
9. Galanis, A., Yang, S. H., and Sharrocks, A. D. (2001) Selective targeting of MAPKs to the ETS domain transcription factor SAP-1 J. Biol. Chem. 276, 965-973 (Pubitemid 32096516)
10. Jacobs, D., Glossip, D., Xing, H., Muslin, A. J., and Kornfeld, K. (1999) Multiple docking sites on substrate proteins form a modular system that mediates recognition by ERK MAP kinase Genes Dev. 13, 163-175 (Pubitemid 29061947)
11. Sheridan, D. L., Kong, Y., Parker, S. A., Dalby, K. N., and Turk, B. E. (2008) Substrate discrimination among mitogen-activated protein kinases through distinct docking sequence motifs J. Biol. Chem. 283, 19511-19520
12. Liu, S., Sun, J. P., Zhou, B., and Zhang, Z. Y. (2006) Structural basis of docking interactions between ERK2 and MAP kinase phosphatase 3 Proc. Natl. Acad. Sci. U.S.A. 103, 5326-5331
13. Tanoue, T., Adachi, M., Moriguchi, T., and Nishida, E. (2000) A conserved docking motif in MAP kinases common to substrates, activators and regulators Nat. Cell Biol. 2, 110-116
14. Piserchio, A., Warthaka, M., Devkota, A. K., Kaoud, T. S., Lee, S., Abramczyk, O., Ren, P., Dalby, K. N., and Ghose, R. (2011) Solution NMR Insights into Docking Interactions Involving Inactive ERK2 Biochemistry 50, 3660-3672
15. Jacobs, D., Beitel, G. J., Clark, S. G., Horvitz, H. R., and Kornfeld, K. (1998) Gain-of-function mutations in the Caenorhabditis elegans lin-1 ETS gene identify a C-terminal regulatory domain phosphorylated by ERK MAP kinase Genetics 149, 1809-1822 (Pubitemid 28375953)
16. Jacobs, D., Glossip, D., Xing, H., Muslin, A. J., and Kornfeld, K. (1999) Multiple docking sites on substrate proteins form a modular system that mediates recognition by ERK MAP kinase Genes Dev. 13, 163-175 (Pubitemid 29061947)
17. Fantz, D. A., Jacobs, D., Glossip, D., and Kornfeld, K. (2001) Docking sites on substrate proteins direct extracellular signal-regulated kinase to phosphorylate specific residues J. Biol. Chem. 276, 27256-27265
18. Lee, S., Warthaka, M., Yan, C., Kaoud, T. S., Piserchio, A., Ghose, R., Ren, P., and Dalby, K. N. (2011) A model of a MAPK*substrate complex in an active conformation: a computational and experimental approach PLoS One 6, e18594
19. Burkhard, K. A., Chen, F., and Shapiro, P. (2011) Quantitative analysis of ERK2 interactions with substrate proteins: roles for kinase docking domains and activity in determining binding affinity J. Biol. Chem. 286, 2477-2485
20. Abramczyk, O., Rainey, M. A., Barnes, R., Martin, L., and Dalby, K. N. (2007) Expanding the repertoire of an ERK2 recruitment site: cysteine footprinting identifies the D-recruitment site as a mediator of Ets-1 binding Biochemistry 46, 9174-9186 (Pubitemid 47255032)
21. Callaway, K., Waas, W. F., Rainey, M. A., Ren, P., and Dalby, K. N. (2010) Phosphorylation of the transcription factor Ets-1 by ERK2: rapid dissociation of ADP and phospho-Ets-1 Biochemistry 49, 3619-3630
22. Dimitri, C. A., Dowdle, W., MacKeigan, J. P., Blenis, J., and Murphy, L. O. (2005) Spatially separate docking sites on ERK2 regulate distinct signaling events in vivo Curr. Biol. 15, 1319-1324 (Pubitemid 41026600)
23. Kaoud, T. S., Devkota, A. K., Harris, R., Rana, M. S., Abramczyk, O., Warthaka, M., Lee, S., Girvin, M. E., Riggs, A. F., and Dalby, K. N. (2011) Activated ERK2 Is a Monomer in Vitro with or without Divalent Cations and When Complexed to the Cytoplasmic Scaffold PEA-15 Biochemistry 50, 4568-4578
24. Gonzalez, F. A., Raden, D. L., and Davis, R. J. (1991) Identification of substrate recognition determinants for human ERK1 and ERK2 protein kinases J. Biol. Chem. 266, 22159-22163 (Pubitemid 21908629)
25. Haycock, J. W. (2002) Peptide substrates for ERK1/2: structure-function studies of serine 31 in tyrosine hydroxylase J. Neurosci. Methods 116, 29-34 (Pubitemid 34465783)
26. Fernandes, N., Bailey, D. E., Vanvranken, D. L., and Allbritton, N. L. (2007) Use of docking peptides to design modular substrates with high efficiency for mitogen-activated protein kinase extracellular signal-regulated kinase ACS Chem. Biol. 2, 665-673 (Pubitemid 350066015)
27. Fernandes, N. and Allbritton, N. L. (2009) Effect of the DEF motif on phosphorylation of peptide substrates by ERK Biochem. Biophys. Res. Commun. 387, 414-418
28. Sheridan, D. L., Kong, Y., Parker, S. A., Dalby, K. N., and Turk, B. E. (2008) Substrate discrimination among mitogen-activated protein kinases through distinct docking sequence motifs J. Biol. Chem. 283, 19511-19520
29. Waas, W. F. and Dalby, K. N. (2002) Transient protein-protein interactions and a random-ordered kinetic mechanism for the phosphorylation of a transcription factor by extracellular-regulated protein kinase 2 J. Biol. Chem. 277, 12532-12540 (Pubitemid 34952611)
30. Waas, W. F., Rainey, M. A., Szafranska, A. E., and Dalby, K. N. (2003) Two rate-limiting steps in the kinetic mechanism of the serine/threonine specific protein kinase ERK2: a case of fast phosphorylation followed by fast product release Biochemistry 42, 12273-12286 (Pubitemid 37296504)
31. Eswar, N., Webb, B., Marti-Renom, M. A., Madhusudhan, M. S., Eramian, D., Shen, M. Y., Pieper, U., and Sali, A. (2006) Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformatics Chapter 5, Unit 5 6.
32. Case, D. A., Cheatham, T. E., III, Darden, T., Gohlke, H., Luo, R., Merz, K. M., Jr., Onufriev, A., Simmerling, C., Wang, B., and Woods, R. J. (2005) The Amber biomolecular simulation programs J. Comput. Chem. 26, 1668-1688 (Pubitemid 43076180)
33. Canagarajah, B. J., Khokhlatchev, A., Cobb, M. H., and Goldsmith, E. J. (1997) Activation mechanism of the MAP kinase ERK2 by dual phosphorylation Cell 90, 859-869 (Pubitemid 27381625)
34. Eldridge, M. D., Murray, C. W., Auton, T. R., Paolini, G. V., and Mee, R. P. (1997) Empirical scoring functions: I. The development of a fast empirical scoring function to estimate the binding affinity of ligands in receptor complexes J. Comput. Aided Mol. Des. 11, 425-445 (Pubitemid 127505895)
35. Jones, G., Willett, P., Glen, R. C., Leach, A. R., and Taylor, R. (1997) Development and validation of a genetic algorithm for flexible docking J. Mol. Biol. 267, 727-748 (Pubitemid 27170693)
36. Segel, I. H. (1975) Enzyme kinetics: behavior and analysis of rapid equilibrium and steady-state enzyme systems, Wiley-Interscience, New York, London.
37. Reinhart, G. D. (1983) The determination of thermodynamic allosteric parameters of an enzyme undergoing steady-state turnover Arch. Biochem. Biophys. 224, 389-401
38. Waas, W. F. and Dalby, K. N. (2001) Purification of a model substrate for transcription factor phosphorylation by ERK2 Protein Expr. Purif. 23, 191-197 (Pubitemid 32930996)
39. Remenyi, A., Good, M. C., and Lim, W. A. (2006) Docking interactions in protein kinase and phosphatase networks Curr. Opin. Struct. Biol. 16, 676-685 (Pubitemid 44827730)
40. Zhou, T. J., Sun, L. G., Humphreys, J., and Goldsmith, E. J. (2006) Docking interactions induce exposure of activation loop in the MAP kinase ERK2 Structure 14, 1011-1019 (Pubitemid 43831663)
41. Ma, W., Shang, Y., Wei, Z., Wen, W., Wang, W., and Zhang, M. (2010) Phosphorylation of DCC by ERK2 is facilitated by direct docking of the receptor P1 domain to the kinase Structure 18, 1502-1511
42. Kovary, K. and Bravo, R. (1992) Existence of different Fos/Jun complexes during the G0-to-G1 transition and during exponential growth in mouse fibroblasts: differential role of Fos proteins Mol. Cell. Biol. 12, 5015-5023
43. Murphy, L. O., Smith, S., Chen, R. H., Fingar, D. C., and Blenis, J. (2002) Molecular interpretation of ERK signal duration by immediate early gene products Nat. Cell Biol. 4, 556-564
44. Murphy, L. O., MacKeigan, J. P., and Blenis, J. (2004) A network of immediate early gene products propagates subtle differences in mitogen-activated protein kinase signal amplitude and duration Mol. Cell. Biol. 24, 144-153 (Pubitemid 38010042)
45. Murphy, L. O. and Blenis, J. (2006) MAPK signal specificity: the right place at the right time Trends Biochem. Sci. 31, 268-275 (Pubitemid 43674354)
46. Roux, P. P., Richards, S. A., and Blenis, J. (2003) Phosphorylation of p90 ribosomal S6 kinase (RSK) regulates extracellular signal-regulated kinase docking and RSK activity Mol. Cell. Biol. 23, 4796-4804 (Pubitemid 36793327)
47. Vomastek, T., Iwanicki, M. P., Burack, W. R., Tiwari, D., Kumar, D., Parsons, J. T., Weber, M. J., and Nandicoori, V. K. (2008) Extracellular signal-regulated kinase 2 (ERK2) phosphorylation sites and docking domain on the nuclear pore complex protein Tpr cooperatively regulate ERK2-Tpr interaction Mol. Cell. Biol. 28, 6954-6966
48. Proft, M. and Struhl, K. (2002) Hog1 kinase converts the Sko1-Cyc8-Tup1 repressor complex into an activator that recruits SAGA and SWI/SNF in response to osmotic stress Mol. Cell 9, 1307-1317 (Pubitemid 34722309)
49. Alepuz, P. M., Jovanovic, A., Reiser, V., and Ammerer, G. (2001) Stress-induced map kinase Hog1 is part of transcription activation complexes Mol. Cell 7, 767-777 (Pubitemid 32436437)
50. Pokholok, D. K., Zeitlinger, J., Hannett, N. M., Reynolds, D. B., and Young, R. A. (2006) Activated signal transduction kinases frequently occupy target genes Science 313, 533-536 (Pubitemid 44148460)
51. de Nadal, E. and Posas, F. (2010) Multilayered control of gene expression by stress-activated protein kinases EMBO J. 29, 4-13
52. Edmunds, J. W. and Mahadevan, L. C. (2004) MAP kinases as structural adaptors and enzymatic activators in transcription complexes J. Cell Sci. 117, 3715-3723 (Pubitemid 39207311)