Erratum: Mechanisms of specificity in protein phosphorylation (Nature Reviews Molecular Cell Biology (2007) 8, (530-541) DOI: 10.1038/nrm2203);Mechanisms of specificity in protein phosphorylation

Nature Reviews Molecular Cell Biology

Volumn 8, Issue 7, 2007, Pages 530-541

  Ubersax, Jeffrey A ^a   Ferrell Jr , James E ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE;

BINDING AFFINITY; BIOCHEMISTRY; CATALYSIS; CELL DIFFERENTIATION; CELL DIVISION; CELL GROWTH; CELL METABOLISM; CELL MOTILITY; HUMAN; HYDROPHOBICITY; KINETICS; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

EID: 34250878954     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm2235     Document Type: Erratum

References (143)

1. Manning, G., Whyte, D. B., Martinez, R., Hunter, T. & Sudarsanam, S. The protein kinase complement of the human genome. Science 298, 1912-1934 (2002). This study catalogues and classifies the complete complement of protein kinases in the human genome.
2. Manning, G., Plowman, G. D., Hunter, T. & Sudarsanam, S. Evolution of protein kinase signaling from yeast to man. Trends Biochem. Sci. 27, 514-520 (2002).
3. Caenepeel, S., Charydczak, G., Sudarsanam, S., Hunter, T. & Manning, G. The mouse kinome: discovery and comparative genomics of all mouse protein kinases. Proc. Natl Acad. Sci. USA 101, 11707-11712 (2004).
4. Zhu, H. et al. Analysis of yeast protein kinases using protein chips. Nature Genet. 26, 283-289 (2000).
5. Pinna, L. A. & Ruzzene, M. How do protein kinases recognize their substrates? Biochim. Biophys. Acta 1314, 191-225 (1996).
6. Cohen, P. The regulation of protein function by multisite phosphorylation - a 25 year update. Trends Biochem. Sci. 25, 596-601 (2000).
7. Echols, N. et al. Comprehensive analysis of amino acid and nucleotide composition in eukaryotic genomes, comparing genes and pseudogenes. Nucleic Acids Res. 30, 2515-2523 (2002).
8. Ptacek, J. et al. Global analysis of protein phosphorylation in yeast. Nature 438, 679-684 (2005). The authors test the ability of 75% of all yeast kinases to phosphorylate 4,400 yeast proteins that were spotted on high-density protein arrays.
9. Ubersax, J. A. et al. Targets of the cyclin-dependent kinase Cdk1. Nature 425, 859-864 (2003). This study screens a yeast proteomic library for proteins that are directly phosphorylated by Cdk1 in whole-cell extracts and identifies ∼ 200 substrates.
10. Hanks, S. K., Quinn, A. M. & Hunter, T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 42-52 (1988).
11. Hanks, S. K. & Hunter, T. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 9, 576-596 (1995).
12. Knighton, D. R. et al. Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253, 407-414 (1991). This first crystal structure of the cAMP-dependent protein kinase PKA is the touchstone for all subsequent structural studies of kinases.
13. Knighton, D. R. et al. 2.0 Å refined crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with a peptide inhibitor and detergent. Acta Crystallogr. D 49, 357-361 (1993).
14. 2+ adenylyl imidodiphosphate and inhibitor peptide PKI(5-24). EMBO J. 12, 849-859 (1993).
15. De Bondt, H. L. et al. Crystal structure of cyclin-dependent kinase 2. Nature 363, 595-602 (1993).
16. Zhang, F., Strand, A., Robbins, D., Cobb, M. H. & Goldsmith, E. J. Atomic structure of the MAP kinase ERK2 at 2.3 A resolution. Nature 367, 704-711 (1994).
17. Jeffrey, P. D. et al. Mechanism of CDK activation revealed by the structure of a cyclin A-CDK2 complex. Nature 376, 313-320 (1995).
18. Xu, W., Harrison, S. C. & Eck, M. J. Three-dimensional structure of the tyrosine kinase c-Src. Nature 385, 595-602 (1997).
19. Lowe, E. D. et al. The crystal structure of a phosphorylase kinase peptide substrate complex: kinase substrate recognition. EMBO J. 16, 6646-6658 (1997).
20. Faux, M. C. & Scott, J. D. More on target with protein phosphorylation: conferring specificity by location. Trends Biochem. Sci. 21, 312-315 (1996).
21. Sim, A. T. & Scott, J. D. Targeting of PKA, PKC and protein phosphatases to cellular microdomains. Cell Calcium 26, 209-217 (1999).
22. Sharrocks, A. D., Yang, S. H. & Galanis, A. Docking domains and substrate-specificity determination for MAP kinases. Trends Biochem. Sci. 25, 448-453 (2000).
23. Adams, J. A. Kinetic and catalytic mechanisms of protein kinases. Chem. Rev. 101, 2271-2290 (2001). A terrific, chemically-orientated review that includes a detailed discussion of the kinetic and catalytic mechanisms of protein kinases.
24. Biondi, R. M. & Nebreda, A. R. Signalling specificity of Ser/Thr protein kinases through docking-site-mediated interactions. Biochem. J. 372, 1-13 (2003).
25. Bhattacharyya, R. P., Remenyi, A., Yeh, B. J. & 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, 655-680 (2006).
26. Remenyi, A., Good, M. C. & Lim, W. A. Docking interactions in protein kinase and phosphatase networks. Curr. Opin. Struct. Biol. 16, 676-685 (2006).
27. Shi, Z., Resing, K. A. & Ahn, N. G. Networks for the allosteric control of protein kinases. Curr. Opin. Struct. Biol. 16, 686-692 (2006).
28. Hubbard, S. R. Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog. EMBO J. 16, 5572-5581 (1997).
29. Brown, N. R., Noble, M. E., Endicott, J. A. & Johnson, L. N. The structural basis for specificity of substrate and recruitment peptides for cyclin-dependent kinases. Nature Cell Biol. 1, 438-443 (1999).
30. Jia, Z., Barford, D., Flint, A. J. & Tonks, N. K. Structural basis for phosphotyrosine peptide recognition by protein tyrosine phosphatase 1B. Science 268, 1754-1758 (1995).
31. Yang, J. et al. Structural basis for substrate specificity of protein-tyrosine phosphatase SHP-1. J. Biol. Chem. 275, 4066-4071 (2000).
32. Andersen, J. N. et al. Structural and evolutionary relationships among protein tyrosine phosphatase domains. Mol. Cell. Biol 21, 7117-7136 (2001).
33. Kemp, B. E., Graves, D. J., Benjamini, E. & Krebs, E. G. Role of multiple basic residues in determining the substrate specificity of cyclic AMP-dependent protein kinase. J. Biol. Chem. 252, 4888-4894 (1977).
34. Hunter, T. Synthetic peptide substrates for a tyrosine protein kinase. J. Biol. Chem. 257, 4843-4848 (1982).
35. Foulkes, J. G., Chow, M., Gorka, C., Frackelton, A. R. Jr & Baltimore, D. Purification and characterization of a protein-tyrosine kinase encoded by the Abelson murine leukemia virus. J. Biol. Chem. 260, 8070-8077 (1985).
36. Kemp, B. E., Bylund, D. B., Huang, T. S. & Krebs, E. G. Substrate specificity of the cyclic AMP-dependent protein kinase. Proc. Natl Acad. Sci. USA 72, 3448-3452 (1975).
37. Daile, P., Carnegie, P. R. & Young, J. D. Synthetic substrate for cyclic AMP-dependent protein kinase. Nature 257, 416-418 (1975).
38. Pearson, R. B. & Kemp, B. E. Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol. 200, 62-81 (1991).
39. Songyang, Z. et al. Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr. Biol. 4, 973-982 (1994). The authors developed a technique for determining the substrate specificity and consensus phosphorylation sites of protein kinases using an orientated library of >2.5 billion peptide substrates.
40. Hutti, J. E. et al. A rapid method for determining protein kinase phosphorylation specificity. Nature Methods 1, 27-29 (2004).
41. Olsen, J. V. et al. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648 (2006).
42. Yaffe, M. B. et al. A motif-based profile scanning approach for genome-wide prediction of signaling pathways. Nature Biotech. 19, 348-353 (2001).
43. Holmes, J. K. & Solomon, M. J. The role of Thr160 phosphorylation of Cdk2 in substrate recognition. Eur. J. Biochem. 268, 4647-4652 (2001).
44. Zheng, J. et al. 2.2 Å refined crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MnATP and a peptide inhibitor. Acta Crystallogr. D 49, 362-365 (1993).
45. Taylor, S. S. et al. Dynamics of signaling by PKA. Biochim. Biophys. Acta 1754, 25-37 (2005).
46. Holland, P. M. & Cooper, J. A. Protein modification: docking sites for kinases. Curr. Biol. 9, R329-R331 (1999).
47. Kallunki, T. et al. JNK2 contains a specificity-determining region responsible for efficient c-Jun binding and phosphorylation. Genes Dev. 8, 2996-3007 (1994).
48. Bardwell, L., Cook, J. G., Chang, E. C., Cairns, B. R. & Thorner, J. Signaling in the yeast pheromone response pathway: specific and high-affinity interaction of the mitogen-activated protein (MAP) kinases Kss1 and Fus3 with the upstream MAP kinase kinase Ste7. Mol. Cell. Biol. 16, 3637-3650 (1996).
49. Bardwell, L. & Thorner, J. A conserved motif at the amino termini of MEKs might mediate high-affinity interaction with the cognate MAPKs. Trends Biochem. Sci. 21, 373-374 (1996).
50. Williams, D. D., Marin, O., Pinna, L. A. & Proud, C. G. Phosphorylated seryl and threonyl, but not tyrosyl, residues are efficient specificity determinants for GSK-3β and Shaggy. FEBS Lett. 448, 86-90 (1999).
51. Biondi, R. M. et al. Identification of a pocket in the PDK1 kinase domain that interacts with PIF and the C-terminal residues of PKA. EMBO J. 19, 979-988 (2000).
52. Adams, P. D. et al. Identification of a cyclin-CDK2 recognition motif present in substrates and p21-like cyclin-dependent kinase inhibitors. Mol. Cell. Biol. 16, 6623-6633 (1996).
53. Schulman, B. A., Lindstrom, D. L. & Harlow, E. Substrate recruitment to cyclin-dependent kinase 2 by a multipurpose docking site on cyclin A. Proc. Natl Acad. Sci. USA 96, 10453-10458 (1998).
54. Chen, Y. G. et al. Determinants of specificity in TGF-β signal transduction. Genes Dev. 12, 2144-2152 (1998).
55. Lo, R. S., Chen, Y. G., Shi, Y., Pavletich, N. P. & Massague, J. The L3 loop: a structural motif determining specific interactions between SMAD proteins and TGF-β receptors. EMBO J. 17, 996-1005 (1998).
56. Tanoue, T., Adachi, M., Moriguchi, T. & Nishida, E. A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nature Cell Biol. 2, 110-116 (2000).
57. Gupta, S., Campbell, D., Derijard, B. & Davis, R. J. Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science 267, 389-393 (1995).
58. Livingstone, C., Patel, G. & Jones, N. ATF-2 contains a phosphorylation-dependent transcriptional activation domain. EMBO J. 14, 1785-1797 (1995).
59. Yang, S. H., Yates, P. R., Whitmarsh, A. J., Davis, R. J. & Sharrocks, A. D. The Elk-1 ETS-domain transcription factor contains a mitogen-activated protein kinase targeting motif. Mol. Cell. Biol. 18, 710-720 (1998).
60. Yang, S. H., Galanis, A. & Sharrocks, A. D. Targeting of p38 mitogen-activated protein kinases to MEF2 transcription factors. Mol. Cell. Biol. 19, 4028-4038 (1999).
61. Lee, T. et al. Docking motif interactions in MAP kinases revealed by hydrogen exchange mass spectrometry. Mol. Cell 14, 43-55 (2004). This study used hydrogen-exchange mass spectroscopy to identify conformational changes in MAPK on binding of DEF-domain and D-domain peptides.
62. Remenyi, A., Good, M. C., Bhattacharyya, R. P. & Lim, W. A. The role of docking interactions in mediating signaling input, output, and discrimination in the yeast MAPK network. Mol. Cell 20, 951-962 (2005). Structural analysis of MAPK bound to three different binding partners, which demonstrates how different D-domain peptides can selectively bind different MAPKs through a common docking groove and have different effects on kinase activity.
63. Jacobs, D., Glossip, D., Xing, H., Muslin, A. J. & Kornfeld, K. Multiple docking sites on substrate proteins form a modular system that mediates recognition by ERK MAP kinase. Genes Dev. 13, 163-175 (1999). This paper identified two important ERK docking sites through the analysis of lin-1 mutations in Caenorhabditis elegans.
64. Jacobs, D., Beitel, G. J., Clark, S. G., Horvitz, H. R. & Kornfeld, K. 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 (1998).
65. 2-terminal UCR regions. J. Biol. Chem. 275, 16609-16617 (2000).
66. Dimitri, C. A., Dowdle, W., MacKeigan, J. P., Blenis, J. & Murphy, L. O. Spatially separate docking sites on ERK2 regulate distinct signaling events in vivo. Curr. Biol. 15, 1319-1324 (2005).
67. Hubbard, S. R. & Till, J. H. Protein tyrosine kinase structure and function. Annu. Rev. Biochem. 69, 373-398 (2000).
68. Deshaies, R. J. & Ferrell, J. E. Jr. Multisite phosphorylation and the countdown to S phase. Cell 107, 819-822 (2001).
69. Chang, C. I., Xu, B. E., Akella, R., Cobb, M. H. & 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, 1241-1249 (2002).
70. Heo, Y. S. et al. Structural basis for the selective inhibition of JNK1 by the scaffolding protein JIP1 and SP600125. EMBO J. 23, 2185-2195 (2004).
71. Miller, M. E. & Cross, F. R. Cyclin specificity: how many wheels do you need on a unicycle? J. Cell Sci. 114, 1811-1820 (2001).
72. Cheng, K. Y. et al. The role of the phospho-CDK2/cyclin A recruitment site in substrate recognition. J. Biol. Chem. 281, 23167-23179 (2006).
73. Archambault, V., Buchler, N. E., Wilmes, G. M., Jacobson, M. D. & Cross, F. R. Two-faced cyclins with eyes on the targets. Cell Cycle 4, 125-130 (2005).
74. Cross, F. R., Yuste-Rojas, M., Gray, S. & Jacobson, M. D. Specialization and targeting of B-type cyclins. Mol. Cell 4, 11-19 (1999).
75. Wilmes, G. M. et al. Interaction of the S-phase cyclin Clb5 with an 'RXL' docking sequence in the initiator protein Orc6 provides an origin-localized replication control switch. Genes Dev. 18, 981-991 (2004).
76. Takeda, D. Y., Wohlschlegel, J. A. & Dutta, A. A bipartite substrate recognition motif for cyclin-dependent kinases. J. Biol. Chem. 276, 1993-1997 (2001).
77. Arvai, A. S., Bourne, Y., Hickey, M. J. & Tainer, J. A. Crystal structure of the human cell cycle protein CksHs1: single domain fold with similarity to kinase N-lobe domain. J. Mol. Biol. 249, 835-842 (1995).
78. Bourne, Y. et al. Crystal structure and mutational analysis of the human CDK2 kinase complex with cell cycle-regulatory protein CksHs1. Cell 84, 863-874 (1996).
79. Patra, D. & Dunphy, W. G. Xe-p9, a Xenopus Suc1/Cks protein, is essential for the Cdc2-dependent phosphorylation of the anaphase-promoting complex at mitosis. Genes Dev. 12, 2549-2559 (1998).
80. Tang, Y. & Reed, S. I. The Cdk-associated protein Cks1 functions both in G1 and G2 in Saccharomyces cerevisiae. Genes Dev. 7, 822-832 (1993).
81. Elia, A. E., Cantley, L. C. & Yaffe, M. B. Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 299, 1228-1231 (2003).
82. Elia, A. E. et al. The molecular basis for phosphodependent substrate targeting and regulation of Plks by the polo-box domain. Cell 115, 83-95 (2003). References 81 and 82 discover and explain the binding of polo-box domains to phosphorylated peptides.
83. Fiol, C. J., Mahrenholz, A. M., Wang, Y., Roeske, R. W. & Roach, P. J. Formation of protein kinase recognition sites by covalent modification of the substrate. Molecular mechanism for the synergistic action of casein kinase II and glycogen synthase kinase 3. J. Biol. Chem. 262, 14042-14048 (1987).
84. Dajani, R. et al. Crystal structure of glycogen synthase kinase 3β: structural basis for phosphate-primed substrate specificity and autoinhibition. Cell 105, 721-732 (2001).
85. Frame, S., Cohen, P. & Biondi, R. M. A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Mol. Cell 7, 1321-1327 (2001).
86. ter Haar, E. et al. Structure of GSK3? reveals a primed phosphorylation mechanism. Nature Struct. Biol. 8, 593-596 (2001).
87. Frodin, M., Jensen, C. J., Merienne, K. & Gammeltoft, S. A phosphoserine-regulated docking site in the protein kinase RSK2 that recruits and activates PDK1. EMBO J. 19, 2924-2934 (2000).
88. Biondi, R. M. et al. High resolution crystal structure of the human PDK1 catalytic domain defines the regulatory phosphopeptide docking site. EMBO J. 21, 4219-4228 (2002).
89. Jackman, M., Firth, M. & Pines, J. Human cyclins B1 and B2 are localized to strikingly different structures: B1 to microtubules, B2 primarily to the Golgi apparatus. EMBO J. 14, 1646-1654 (1995).
90. Hagting, A., Jackman, M., Simpson, K. & Pines, J. Translocation of cyclin B1 to the nucleus at prophase requires a phosphorylation-dependent nuclear import signal. Curr. Biol. 9, 680-689 (1999).
91. Jackman, M., Lindon, C., Nigg, E. A. & Pines, J. Active cyclin B1-Cdk1 first appears on centrosomes in prophase. Nature Cell Biol. 5, 143-148 (2003).
92. Draviam, V. M., Orrechia, S., Lowe, M., Pardi, R. & Pines, J. The localization of human cyclins B1 and B2 determines CDK1 substrate specificity and neither enzyme requires MEK to disassemble the Golgi apparatus. J. Cell Biol. 152, 945-958 (2001). References 89-92 provide compelling evidence for the importance of localization in CDK function.
93. Moore, J. D., Kirk, J. A. & Hunt, T. Unmasking the S-phase-promoting potential of cyclin B1. Science 300, 987-990 (2003).
94. Miller, M. E. & Cross, F. R. Distinct subcellular localization patterns contribute to functional specificity of the Cln2 and Cln3 cyclins of Saccharomyces cerevisiae. Mol. Cell. Biol. 20, 542-555 (2000).
95. Vaudry, D., Stork, P. J., Lazarovici, P. & Eiden, L. E. Signaling pathways for PC12 cell differentiation: making the right connections. Science 296, 1648-1649 (2002).
96. Robinson, M. J., Stippec, S. A., Goldsmith, E., White, M. A. & Cobb, M. H. A constitutively active and nuclear form of the MAP kinase ERK2 is sufficient for neurite outgrowth and cell transformation. Curr. Biol. 8, 1141-1150 (1998).
97. Disatnik, M. H., Buraggi, G. & Mochly-Rosen, D. Localization of protein kinase C isozymes in cardiac myocytes. Exp. Cell Res. 210, 287-297 (1994).
98. Mochly-Rosen, D., Khaner, H. & Lopez, J. Identification of intracellular receptor proteins for activated protein kinase C. Proc. Natl Acad. Sci. USA 88, 3997-4000 (1991).
99. Wong, W. & Scott, J. D. AKAP signalling complexes: focal points in space and time. Nature Rev. Mol. Cell Biol. 5, 959-970 (2004).
100. Brown, G. C. & Kholodenko, B. N. Spatial gradients of cellular phospho-proteins. FEBS Lett. 457, 452-454 (1999).
101. Pawson, T. & Scott, J. D. Signaling through scaffold, anchoring, and adaptor proteins. Science 278, 2075-2080 (1997).
102. van Drogen, F., Stucke, V. M., Jorritsma, G. & Peter, M. MAP kinase dynamics in response to pheromones in budding yeast. Nature Cell Biol. 3, 1051-1059 (2001).
103. Schwartz, M. A. & Madhani, H. D. Principles of MAP kinase signaling specificity in Saccharomyces cerevisiae. Annu. Rev. Genet. 38, 725-748 (2004).
104. Park, S. H., Zarrinpar, A. & Lim, W. A. Rewiring MAP kinase pathways using alternative scaffold assembly mechanisms. Science 299, 1061-1064 (2003). This study demonstrates that the scaffold Ste5 tethers kinase-substrate pairs in space, and that changing the proteins to which Ste5 binds can produce non-natural input-output properties.
105. Howard, P. L., Chia, M. C., Del Rizzo, S., Liu, F. F. & Pawson, T. Redirecting tyrosine kinase signaling to an apoptotic caspase pathway through chimeric adaptor proteins. Proc. Natl Acad. Sci. USA 100, 11267-11272 (2003).
106. Feliciello, A., Gottesman, M. E. & Avvedimento, E. V. The biological functions of A-kinase anchor proteins. J. Mol. Biol. 308, 99-114 (2001).
107. Sierralta, J. & Mendoza, C. PDZ-containing proteins: alternative splicing as a source of functional diversity. Brain Res. Brain Res. Rev. 47, 105-115 (2004).
108. Muller, J., Cacace, A. M., Lyons, W. E., McGill, C. B. & Morrison, D. K. Identification of B-KSR1, a novel brain-specific isoform of KSR1 that functions in neuronal signaling. Mol. Cell. Biol. 20, 5529-5539 (2000).
109. Bhattacharyya, R. P. et al. The Ste5 scaffold allosterically modulates signaling output of the yeast mating pathway. Science 311, 822-826 (2006). This study demonstrates that scaffolds are not passive participants in signalling cascades but can allosterically activate binding partners.
110. Coghlan, V. M. et al. Association of protein kinase A and protein phosphatase 2B with a common anchoring protein. Science 267, 108-111 (1995).
111. Klauck, T. M. et al. Coordination of three signaling enzymes by AKAP79, a mammalian scaffold protein. Science 271, 1589-1592 (1996).
112. Dodge, K. L. et al. mAKAP assembles a protein kinase A/PDE4 phosphodiesterase cAMP signaling module. EMBO J. 20, 1921-1930 (2001).
113. Whitmarsh, A. J., Cavanagh, J., Tournier, C., Yasuda, J. & Davis, R. J. A mammalian scaffold complex that selectively mediates MAP kinase activation. Science 281, 1671-1674 (1998).
114. Yasuda, J., Whitmarsh, A. J., Cavanagh, J., Sharma, M. & Davis, R. J. The JIP group of mitogen-activated protein kinase scaffold proteins. Mol. Cell. Biol. 19, 7245-7254 (1999).
115. Willoughby, E. A., Perkins, G. R., Collins, M. K. & Whitmarsh, A. J. The JNK-interacting protein-1 scaffold protein targets MAPK phosphatase-7 to dephosphorylate JNK. J. Biol. Chem. 278, 10731-10736 (2003).
116. Willoughby, E. A. & Collins, M. K. Dynamic interaction between the dual specificity phosphatase MKP7 and the JNK3 scaffold protein β-arrestin 2. J. Biol. Chem. 280, 25651-25658 (2005).
117. Loog, M. & Morgan, D. O. Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates. Nature 434, 104-108 (2005). This study shows how the intrinsic biochemical properties of different cyclins help to promote the correct timing of CDK substrate phosphorylation during the cell cycle.
118. Kim, S. Y. & Ferrell, J. E. Jr. Substrate competition as a source of ultrasensitivity in the inactivation of WEE1. Cell 128, 1133-1145 (2007).
119. Hopfield, J. J. Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc. Natl Acad. Sci. USA 71, 4135-4139 (1974). This important study describes how kinetic proofreading, driven by phosphate hydrolysis, can increase the specificity of biological processes beyond the level available from free-energy differences in intermediates or kinetic barriers.
120. Swain, P. S. & Siggia, E. D. The role of proofreading in signal transduction specificity. Biophys. J. 82, 2928-2933 (2002).
121. Ferrell, J. E. Jr. & Bhatt, R. R. Mechanistic studies of the dual phosphorylation of mitogen-activated protein kinase. J. Biol. Chem. 272, 19008-19016 (1997).
122. Breitkreutz, A., Boucher, L. & Tyers, M. MAPK specificity in the yeast pheromone response independent of transcriptional activation. Curr. Biol. 11, 1266-1271 (2001).
123. Sabbagh, W. Jr, Flatauer, L. J., Bardwell, A. J. & Bardwell, L. Specificity of MAP kinase signaling in yeast differentiation involves transient versus sustained MAPK activation. Mol. Cell 8, 683-691 (2001).
124. Bao, M. Z., Schwartz, M. A., Cantin, G. T., Yates, J. R. & Madhani, H. D. Pheromone-dependent destruction of the Tec1 transcription factor is required for MAP kinase signaling specificity in yeast. Cell 119, 991-1000 (2004).
125. Chou, S., Huang, L. & Liu, H. Fus3-regulated Tec1 degradation through SCFCdc4 determines MAPK signaling specificity during mating in yeast. Cell 119, 981-990 (2004).
126. McClean, M. N., Mody, A., Broach, J. R. & Ramanathan, S. Cross-talk and decision making in MAP kinase pathways. Nature Genet. 39, 409-414 (2007). References 124-126 demonstrate that input signals will sometimes leak along pathways with shared signalling components; the studies also identify additional mechanisms that ensure that these leaks do not lead to aberrant outputs.
127. Pinna, L. A. & Donella-Deana, A. Phosphorylated synthetic peptides as tools for studying protein phosphatases. Biochim. Biophys. Acta 1222, 415-431 (1994).
128. Hunter, T. & Sefton, B. M. Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc. Natl Acad. Sci. USA 77, 1311-1315 (1980).
129. Alonso, A. et al. Protein tyrosine phosphatases in the human genome. Cell 117, 699-711 (2004).
130. Arena, S., Benvenuti, S. & Bardelli, A. Genetic analysis of the kinome and phosphatome in cancer. Cell Mol. Life Sci. 62, 2092-2099 (2005).
131. Moorhead, G. B., Trinkle-Mulcahy, L. & Ulke-Lemee, A. Emerging roles of nuclear protein phosphatases. Nature Rev. Mol. Cell Biol. 8, 234-244 (2007).
132. Cohen, P. T. Protein phosphatase 1 - targeted in many directions. J. Cell Sci. 115, 241-256 (2002).
133. Gray, C. H., Good, V. M., Tonks, N. K. & Barford, D. The structure of the cell cycle protein Cdc14 reveals a proline-directed protein phosphatase. EMBO J. 22, 3524-3535 (2003).
134. DeLano, W. L. The PyMOL molecular graphics system [online] 〈http://www.pymol.org〉 (2002).
135. Xu, W., Doshi, A., Lei, M., Eck, M. J. & Harrison, S. C. Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Mol. Cell 3, 629-638 (1999).
136. Songyang, Z. et al. A structural basis for substrate specificities of protein Ser/Thr kinases: primary sequence preference of casein kinases I and II, NIMA, phosphorylase kinase, calmodulin-dependent kinase II, CDK5, and Erk1. Mol. Cell. Biol. 16, 6486-6493 (1996).
137. Flotow, H. et al. Phosphate groups as substrate determinants for casein kinase I action. J. Biol. Chem. 265, 14264-14269 (1990).
138. Meggio, F. & Pinna, L. A. One-thousand-and-one substrates of protein kinase CK2? FASEB J. 17, 349-368 (2003).
139. Fiol, C. J., Wang, A., Roeske, R. W. & Roach, P. J. Ordered multisite protein phosphorylation. Analysis of glycogen synthase kinase 3 action using model peptide substrates. J. Biol. Chem. 265, 6061-6065 (1990).
140. Till, J. H., Chan, P. M. & Miller, W. T. Engineering the substrate specificity of the Abl tyrosine kinase. J. Biol. Chem. 274, 4995-5003 (1999).
141. Songyang, Z. et al. Catalytic specificity of protein-tyrosine kinases is critical for selective signalling. Nature 373, 536-539 (1995).
142. Obata, T. et al. Peptide and protein library screening defines optimal substrate motifs for AKT/PKB. J. Biol. Chem. 275, 36108-36115 (2000).
143. Friedmann, M., Nissen, M. S., Hoover, D. S., Reeves, R. & Magnuson, N. S. Characterization of the protooncogene pim-1: kinase activity and substrate recognition sequence. Arch. Biochem. Biophys. 298, 594-601 (1992).