Profiling the kinome: Current capabilities and future challenges

Journal of Proteomics

Volumn 81, Issue , 2013, Pages 43-55

  Knight, James D R ^a   Pawson, Tony ^a,b   Gingras, Anne Claude ^a,b  

^a MOUNT SINAI HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cell signaling; Kinase; Mass spectrometry; Phosphorylation

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYCLIN DEPENDENT KINASE 2; KINOME; PHOSPHOTRANSFERASE; PROTEIN KINASE; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

CATALYSIS; CELL LYSATE; CELL SPECIFICITY; ENZYME ACTIVATION; ENZYME ANALYSIS; ENZYME PHOSPHORYLATION; ENZYME PURIFICATION; GENE EXPRESSION PROFILING; HIGH THROUGHPUT SCREENING; HUMAN; IMMUNOASSAY; MASS SPECTROMETRY; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REVIEW; STIMULUS RESPONSE;

ANIMALS; HUMANS; PROTEIN KINASES; PROTEOME; PROTEOMICS;

EID: 84877798750     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.10.015     Document Type: Review

References (116)

1. 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 U S A 2004, 101:11707-11712.
2. Manning G., Whyte D.B., Martinez R., Hunter T., Sudarsanam S. The protein kinase complement of the human genome. Science 2002, 298:1912-1934.
3. Dhand R., Hiles I., Panayotou G., Roche S., Fry M.J., Gout I., et al. PI 3-kinase is a dual specificity enzyme: autoregulation by an intrinsic protein-serine kinase activity. EMBO J 1994, 13:522-533.
4. Wagner P.D., Vu N.D. Phosphorylation of ATP-citrate lyase by nucleoside diphosphate kinase. J Biol Chem 1995, 270:21758-21764.
5. Fedorov O., Muller S., Knapp S. The (un)targeted cancer kinome. Nat Chem Biol 2010, 6:166-169.
6. Sawyers C.L., Hochhaus A., Feldman E., Goldman J.M., Miller C.B., Ottmann O.G., et al. Imatinib induces hematologic and cytogenetic responses in patients with chronic myelogenous leukemia in myeloid blast crisis: results of a phase II study. Blood 2002, 99:3530-3539.
7. Talpaz M., Silver R.T., Druker B.J., Goldman J.M., Gambacorti-Passerini C., Guilhot F., et al. Imatinib induces durable hematologic and cytogenetic responses in patients with accelerated phase chronic myeloid leukemia: results of a phase 2 study. Blood 2002, 99:1928-1937.
8. Kantarjian H., Sawyers C., Hochhaus A., Guilhot F., Schiffer C., Gambacorti-Passerini C., et al. Hematologic and cytogenetic responses to imatinib mesylate in chronic myelogenous leukemia. N Engl J Med 2002, 346:645-652.
9. Demetri G.D., von Mehren M., Blanke C.D., Van den Abbeele A.D., Eisenberg B., Roberts P.J., et al. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med 2002, 347:472-480.
10. Wooten M.W. In-gel kinase assay as a method to identify kinase substrates. Sci STKE 2002, 2002:pl15.
11. Kameshita I., Fujisawa H. A sensitive method for detection of calmodulin-dependent protein kinase II activity in sodium dodecyl sulfate-polyacrylamide gel. Anal Biochem 1989, 183:139-143.
12. Sevecka M., Wolf-Yadlin A., MacBeath G. Lysate microarrays enable high-throughput, quantitative investigations of cellular signaling. Mol Cell Proteomics 2011, 10. [M110 005363].
13. Ciaccio M.F., Wagner J.P., Chuu C.P., Lauffenburger D.A., Jones R.B. Systems analysis of EGF receptor signaling dynamics with microwestern arrays. Nat Methods 2010, 7:148-155.
14. Pelech S., Sutter C., Zhang H. Kinetworks protein kinase multiblot analysis. Methods Mol Biol 2003, 218:99-111.
15. Stokes M.P., Farnsworth C.L., Moritz A., Silva J.C., Jia X., Lee K.A., et al. PTMScan direct: identification and quantification of peptides from critical signaling proteins by immunoaffinity enrichment coupled with LC-MS/MS. Mol Cell Proteomics 2012, 11:187-201.
16. Bodenmiller B., Zunder E.R., Finck R., Chen T.J., Savig E.S., Bruggner R.V., et al. Multiplexed mass cytometry profiling of cellular states perturbed by small-molecule regulators. Nat Biotechnol 2012, [published online: 2012 Aug 19] http://dx.doi.org/10.1038/nbt.2317.
17. Duncan J.S., Whittle M.C., Nakamura K., Abell A.N., Midland A.A., Zawistowski J.S., et al. Dynamic reprogramming of the kinome in response to targeted MEK inhibition in triple-negative breast cancer. Cell 2012, 149:307-321.
18. Oppermann F.S., Gnad F., Olsen J.V., Hornberger R., Greff Z., Keri G., et al. Large-scale proteomics analysis of the human kinome. Mol Cell Proteomics 2009, 8:1751-1764.
19. Daub H., Olsen J.V., Bairlein M., Gnad F., Oppermann F.S., Korner R., et al. Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol Cell 2008, 31:438-448.
20. Bantscheff M., Eberhard D., Abraham Y., Bastuck S., Boesche M., Hobson S., et al. Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors. Nat Biotechnol 2007, 25:1035-1044.
21. Ong S.E., Blagoev B., Kratchmarova I., Kristensen D.B., Steen H., Pandey A., et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 2002, 1:376-386.
22. Anastassiadis T., Deacon S.W., Devarajan K., Ma H., Peterson J.R. Comprehensive assay of kinase catalytic activity reveals features of kinase inhibitor selectivity. Nat Biotechnol 2011, 29:1039-1045.
23. Bain J., McLauchlan H., Elliott M., Cohen P. The specificities of protein kinase inhibitors: an update. Biochem J 2003, 371:199-204.
24. Bain J., Plater L., Elliott M., Shpiro N., Hastie C.J., McLauchlan H., et al. The selectivity of protein kinase inhibitors: a further update. Biochem J 2007, 408:297-315.
25. Davies S.P., Reddy H., Caivano M., Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 2000, 351:95-105.
26. Davis M.I., Hunt J.P., Herrgard S., Ciceri P., Wodicka L.M., Pallares G., et al. Comprehensive analysis of kinase inhibitor selectivity. Nat Biotechnol 2011, 29:1046-1051.
27. Fabian M.A., Biggs W.H., Treiber D.K., Atteridge C.E., Azimioara M.D., Benedetti M.G., et al. A small molecule-kinase interaction map for clinical kinase inhibitors. Nat Biotechnol 2005, 23:329-336.
28. Dulla K., Daub H., Hornberger R., Nigg E.A., Korner R. Quantitative site-specific phosphorylation dynamics of human protein kinases during mitotic progression. Mol Cell Proteomics 2010, 9:1167-1181.
29. Mori T., Inamori K., Inoue Y., Han X., Yamanouchi G., Niidome T., et al. Evaluation of protein kinase activities of cell lysates using peptide microarrays based on surface plasmon resonance imaging. Anal Biochem 2008, 375:223-231.
30. Lu C.H.S., Liu K., Tan L.P., Yao S.Q. Current chemical biology tools for studying protein phosphorylation and dephosphorylation. Chemistry 2012, 18:28-39.
31. Kubota K., Anjum R., Yu Y., Kunz R.C., Andersen J.N., Kraus M., et al. Sensitive multiplexed analysis of kinase activities and activity-based kinase identification. Nat Biotechnol 2009, 27:933-940.
32. Yu Y., Anjum R., Kubota K., Rush J., Villen J., Gygi S.P. A site-specific, multiplexed kinase activity assay using stable-isotope dilution and high-resolution mass spectrometry. Proc Natl Acad Sci U S A 2009, 106:11606-11611.
33. Shults M.D., Kozlov I.A., Nelson N., Kermani B.G., Melnyk P.C., Shevchenko V., et al. A multiplexed protein kinase assay. Chembiochem 2007, 8:933-942.
34. Shults M.D., Janes K.A., Lauffenburger D.A., Imperiali B. A multiplexed homogeneous fluorescence-based assay for protein kinase activity in cell lysates. Nat Methods 2005, 2:277-283.
35. Diks S.H., Kok K., O'Toole T., Hommes D.W., van Dijken P., Joore J., et al. Kinome profiling for studying lipopolysaccharide signal transduction in human peripheral blood mononuclear cells. J Biol Chem 2004, 279:49206-49213.
36. Kunz R.C., McAllister F.E., Rush J.E., Gygi S.P. A high-throughput, multiplexed kinase assay using a benchtop orbitrap mass spectrometer to investigate the effect of kinase inhibitors on kinase signaling pathways. Anal Chem 2012, 84:6233-6239.
37. Yang S.H., Galanis A., Sharrocks A.D. Targeting of p38 mitogen-activated protein kinases to MEF2 transcription factors. Mol Cell Biol 1999, 19:4028-4038.
38. Cole K.A., Huggins J., Laquaglia M., Hulderman C.E., Russell M.R., Bosse K., et al. RNAi screen of the protein kinome identifies checkpoint kinase 1 (CHK1) as a therapeutic target in neuroblastoma. Proc Natl Acad Sci U S A 2011, 108:3336-3341.
39. Grueneberg D.A., Degot S., Pearlberg J., Li W., Davies J.E., Baldwin A., et al. Kinase requirements in human cells: I. Comparing kinase requirements across various cell types. Proc Natl Acad Sci U S A 2008, 105:16472-16477.
40. Loh S.H., Francescut L., Lingor P., Bahr M., Nicotera P. Identification of new kinase clusters required for neurite outgrowth and retraction by a loss-of-function RNA interference screen. Cell Death Differ 2008, 15:283-298.
41. Moffat J., Grueneberg D.A., Yang X., Kim S.Y., Kloepfer A.M., Hinkle G., et al. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 2006, 124:1283-1298.
42. MacKeigan J.P., Murphy L.O., Blenis J. Sensitized RNAi screen of human kinases and phosphatases identifies new regulators of apoptosis and chemoresistance. Nat Cell Biol 2005, 7:591-600.
43. Rauch J., Volinsky N., Romano D., Kolch W. The secret life of kinases: functions beyond catalysis. Cell Commun Signal 2011, 9:23.
44. Bodenmiller B., Wanka S., Kraft C., Urban J., Campbell D., Pedrioli P.G., et al. Phosphoproteomic analysis reveals interconnected system-wide responses to perturbations of kinases and phosphatases in yeast. Sci Signal 2010, 3:rs4.
45. Bishop A.C., Ubersax J.A., Petsch D.T., Matheos D.P., Gray N.S., Blethrow J., et al. A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 2000, 407:395-401.
46. Bishop A.C., Shah K., Liu Y., Witucki L., Kung C., Shokat K.M. Design of allele-specific inhibitors to probe protein kinase signaling. Curr Biol 1998, 8:257-266.
47. Morgan D.J., Weisenhaus M., Shum S., Su T., Zheng R., Zhang C., et al. Tissue-specific PKA inhibition using a chemical genetic approach and its application to studies on sperm capacitation. Proc Natl Acad Sci U S A 2008, 105:20740-20745.
48. Chen X., Ye H., Kuruvilla R., Ramanan N., Scangos K.W., Zhang C., et al. A chemical-genetic approach to studying neurotrophin signaling. Neuron 2005, 46:13-21.
49. Weiss E.L., Bishop A.C., Shokat K.M., Drubin D.G. Chemical genetic analysis of the budding-yeast p21-activated kinase Cla4p. Nat Cell Biol 2000, 2:677-685.
50. Carlson S.M., White F.M. Using small molecules and chemical genetics to interrogate signaling networks. ACS Chem Biol 2011, 6:75-85.
51. Ultanir S.K., Hertz N.T., Li G., Ge W.P., Burlingame A.L., Pleasure S.J., et al. Chemical genetic identification of NDR1/2 kinase substrates AAK1 and Rabin8 uncovers their roles in dendrite arborization and spine development. Neuron 2012, 73:1127-1142.
52. Zhang C., Kenski D.M., Paulson J.L., Bonshtien A., Sessa G., Cross J.V., et al. A second-site suppressor strategy for chemical genetic analysis of diverse protein kinases. Nat Methods 2005, 2:435-441.
53. Li H., Hah J.M., Lawrence D.S. Light-mediated liberation of enzymatic activity: "small molecule" caged protein equivalents. J Am Chem Soc 2008, 130:10474-10475.
54. Karginov A.V., Ding F., Kota P., Dokholyan N.V., Hahn K.M. Engineered allosteric activation of kinases in living cells. Nat Biotechnol 2010, 28:743-747.
55. Yang J., Symes K., Mercola M., Schreiber S.L. Small-molecule control of insulin and PDGF receptor signaling and the role of membrane attachment. Curr Biol 1998, 8:11-18.
56. Graef I.A., Holsinger L.J., Diver S., Schreiber S.L., Crabtree G.R. Proximity and orientation underlie signaling by the non-receptor tyrosine kinase ZAP70. EMBO J 1997, 16:5618-5628.
57. Luo Z., Tzivion G., Belshaw P.J., Vavvas D., Marshall M., Avruch J. Oligomerization activates c-Raf-1 through a Ras-dependent mechanism. Nature 1996, 383:181-185.
58. Spencer D.M., Graef I., Austin D.J., Schreiber S.L., Crabtree G.R. A general strategy for producing conditional alleles of Src-like tyrosine kinases. Proc Natl Acad Sci U S A 1995, 92:9805-9809.
59. Tanaka K., Kawahara M., Ueda H., Nagamune T. Selection and growth regulation of genetically modified cells with hapten-specific antibody/receptor tyrosine kinase chimera. Biotechnol Prog 2009, 25:1138-1145.
60. Raffioni S., Thomas D., Foehr E.D., Thompson L.M., Bradshaw R.A. Comparison of the intracellular signaling responses by three chimeric fibroblast growth factor receptors in PC12 cells. Proc Natl Acad Sci U S A 1999, 96:7178-7183.
61. Ohashi H., Maruyama K., Liu Y.C., Yoshimura A. Ligand-induced activation of chimeric receptors between the erythropoietin receptor and receptor tyrosine kinases. Proc Natl Acad Sci U S A 1994, 91:158-162.
62. Roussel M.F., Transy C., Kato J.Y., Reinherz E.L., Sherr C.J. Antibody-induced mitogenicity mediated by a chimeric CD2-c-fms receptor. Mol Cell Biol 1990, 10:2407-2412.
63. Gautier A., Deiters A., Chin J.W. Light-activated kinases enable temporal dissection of signaling networks in living cells. J Am Chem Soc 2011, 133:2124-2127.
64. Gautier A., Nguyen D.P., Lusic H., An W., Deiters A., Chin J.W. Genetically encoded photocontrol of protein localization in mammalian cells. J Am Chem Soc 2010, 132:4086-4088.
65. Edwards A.M., Isserlin R., Bader G.D., Frye S.V., Willson T.M., Yu F.H. Too many roads not taken. Nature 2011, 470:163-165.
66. Obenauer J.C., Cantley L.C., Yaffe M.B. Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 2003, 31:3635-3641.
67. Yaffe M.B., Leparc G.G., Lai J., Obata T., Volinia S., Cantley L.C. A motif-based profile scanning approach for genome-wide prediction of signaling pathways. Nat Biotechnol 2001, 19:348-353.
68. Linding R., Jensen L.J., Pasculescu A., Olhovsky M., Colwill K., Bork P., et al. NetworKIN: a resource for exploring cellular phosphorylation networks. Nucleic Acids Res 2008, 36:D695-D699.
69. Miller M.L., Jensen L.J., Diella F., Jorgensen C., Tinti M., Li L., et al. Linear motif atlas for phosphorylation-dependent signaling. Sci Signal 2008, 1:ra2.
70. Songyang Z., Blechner S., Hoagland N., Hoekstra M.F., Piwnica-Worms H., Cantley L.C. Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr Biol 1994, 4:973-982.
71. Obata T., Yaffe M.B., Leparc G.G., Piro E.T., Maegawa H., Kashiwagi A., et al. Peptide and protein library screening defines optimal substrate motifs for AKT/PKB. J Biol Chem 2000, 275:36108-36115.
72. Knebel A., Morrice N., Cohen P. A novel method to identify protein kinase substrates: eEF2 kinase is phosphorylated and inhibited by SAPK4/p38delta. EMBO J 2001, 20:4360-4369.
73. Jaleel M., Nichols R.J., Deak M., Campbell D.G., Gillardon F., Knebel A., et al. LRRK2 phosphorylates moesin at threonine-558: characterization of how Parkinson's disease mutants affect kinase activity. Biochem J 2007, 405:307-317.
74. Peng C., Knebel A., Morrice N.A., Li X., Barringer K., Li J., et al. Pim kinase substrate identification and specificity. J Biochem 2007, 141:353-362.
75. Cuomo M.E., Knebel A., Platt G., Morrice N., Cohen P., Mittnacht S. Regulation of microfilament organization by Kaposi sarcoma-associated herpes virus-cyclin.CDK6 phosphorylation of caldesmon. J Biol Chem 2005, 280:35844-35858.
76. Auld G.C., Campbell D.G., Morrice N., Cohen P. Identification of calcium-regulated heat-stable protein of 24 kDa (CRHSP24) as a physiological substrate for PKB and RSK using KESTREL. Biochem J 2005, 389:775-783.
77. Cartlidge R.A., Knebel A., Peggie M., Alexandrov A., Phizicky E.M., Cohen P. The tRNA methylase METTL1 is phosphorylated and inactivated by PKB and RSK in vitro and in cells. EMBO J 2005, 24:1696-1705.
78. Eyers C.E., McNeill H., Knebel A., Morrice N., Arthur S.J., Cuenda A., et al. The phosphorylation of CapZ-interacting protein (CapZIP) by stress-activated protein kinases triggers its dissociation from CapZ. Biochem J 2005, 389:127-135.
79. Cole A.R., Knebel A., Morrice N.A., Robertson L.A., Irving A.J., Connolly C.N., et al. GSK-3 phosphorylation of the Alzheimer epitope within collapsin response mediator proteins regulates axon elongation in primary neurons. J Biol Chem 2004, 279:50176-50180.
80. Murray J.T., Campbell D.G., Morrice N., Auld G.C., Shpiro N., Marquez R., et al. Exploitation of KESTREL to identify NDRG family members as physiological substrates for SGK1 and GSK3. Biochem J 2004, 384:477-488.
81. Murray J.T., Campbell D.G., Peggie M., Mora A., Cohen P. Identification of filamin C as a new physiological substrate of PKBalpha using KESTREL. Biochem J 2004, 384:489-494.
82. McNeill H., Knebel A., Arthur J.S., Cuenda A., Cohen P. A novel UBA and UBX domain protein that binds polyubiquitin and VCP and is a substrate for SAPKs. Biochem J 2004, 384:391-400.
83. Rousseau S., Morrice N., Peggie M., Campbell D.G., Gaestel M., Cohen P. Inhibition of SAPK2a/p38 prevents hnRNP A0 phosphorylation by MAPKAP-K2 and its interaction with cytokine mRNAs. EMBO J 2002, 21:6505-6514.
84. Cohen P., Knebel A. KESTREL: a powerful method for identifying the physiological substrates of protein kinases. Biochem J 2006, 393:1-6.
85. Troiani S., Uggeri M., Moll J., Isacchi A., Kalisz H.M., Rusconi L., et al. Searching for biomarkers of Aurora-A kinase activity: identification of in vitro substrates through a modified KESTREL approach. J Proteome Res 2005, 4:1296-1303.
86. Jiang W., Jimenez G., Wells N.J., Hope T.J., Wahl G.M., Hunter T., et al. PRC1: a human mitotic spindle-associated CDK substrate protein required for cytokinesis. Mol Cell 1998, 2:877-885.
87. Fukunaga R., Hunter T. MNK1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates. EMBO J 1997, 16:1921-1933.
88. Ptacek J., Devgan G., Michaud G., Zhu H., Zhu X., Fasolo J., et al. Global analysis of protein phosphorylation in yeast. Nature 2005, 438:679-684.
89. Dephoure N., Howson R.W., Blethrow J.D., Shokat K.M., O'Shea E.K. Combining chemical genetics and proteomics to identify protein kinase substrates. Proc Natl Acad Sci U S A 2005, 102:17940-17945.
90. Ubersax J.A., Woodbury E.L., Quang P.N., Paraz M., Blethrow J.D., Shah K., et al. Targets of the cyclin-dependent kinase Cdk1. Nature 2003, 425:859-864.
91. Allen J.J., Lazerwith S.E., Shokat K.M. Bio-orthogonal affinity purification of direct kinase substrates. J Am Chem Soc 2005, 127:5288-5289.
92. Blethrow J.D., Glavy J.S., Morgan D.O., Shokat K.M. Covalent capture of kinase-specific phosphopeptides reveals Cdk1-cyclin B substrates. Proc Natl Acad Sci U S A 2008, 105:1442-1447.
93. Carlson S.M., Chouinard C.R., Labadorf A., Lam C.J., Schmelzle K., Fraenkel E., et al. Large-scale discovery of ERK2 substrates identifies ERK-mediated transcriptional regulation by ETV3. Sci Signal 2011, 4:rs11.
94. Banko M.R., Allen J.J., Schaffer B.E., Wilker E.W., Tsou P., White J.L., et al. Chemical genetic screen for AMPKalpha2 substrates uncovers a network of proteins involved in mitosis. Mol Cell 2011, 44:878-892.
95. Knight J.D., Tian R., Lee R.E., Wang F., Beauvais A., Zou H., et al. A novel whole-cell lysate kinase assay identifies substrates of the p38 MAPK in differentiating myoblasts. Skelet Muscle 2012, 2:5.
96. Bodenmiller B., Mueller L.N., Mueller M., Domon B., Aebersold R. Reproducible isolation of distinct, overlapping segments of the phosphoproteome. Nat Methods 2007, 4:231-237.
97. Xue L., Wang W.H., Iliuk A., Hu L., Galan J.A., Yu S., et al. Sensitive kinase assay linked with phosphoproteomics for identifying direct kinase substrates. Proc Natl Acad Sci U S A 2012, 109:5615-5620.
98. Hornbeck P.V., Kornhauser J.M., Tkachev S., Zhang B., Skrzypek E., Murray B., et al. PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res 2012, 40:D261-D270.
99. Jansson D., Ng A.C., Fu A., Depatie C., Al Azzabi M., Screaton R.A. Glucose controls CREB activity in islet cells via regulated phosphorylation of TORC2. Proc Natl Acad Sci U S A 2008, 105:10161-10166.
100. Statsuk A.V., Shokat K.M. Covalent cross-linking of kinases with their corresponding peptide substrates. Methods Mol Biol 2012, 795:179-190.
101. Suwal S., Pflum M.K. Phosphorylation-dependent kinase-substrate cross-linking. Angew Chem Int Ed Engl 2010, 49:1627-1630.
102. Statsuk A.V., Maly D.J., Seeliger M.A., Fabian M.A., Biggs W.H., Lockhart D.J., et al. Tuning a three-component reaction for trapping kinase substrate complexes. J Am Chem Soc 2008, 130:17568-17574.
103. Liu K., Kalesh K.A., Ong L.B., Yao S.Q. An improved mechanism-based cross-linker for multiplexed kinase detection and inhibition in a complex proteome. Chembiochem 2008, 9:1883-1888.
104. Maly D.J., Allen J.A., Shokat K.M. A mechanism-based cross-linker for the identification of kinase-substrate pairs. J Am Chem Soc 2004, 126:9160-9161.
105. Parang K., Kohn J.A., Saldanha S.A., Cole P.A. Development of photo-crosslinking reagents for protein kinase-substrate interactions. FEBS Lett 2002, 520:156-160.
106. Okada H., Uezu A., Mason F.M., Soderblom E.J., Moseley M.A., Soderling S.H. SH3 domain-based phototrapping in living cells reveals Rho family GAP signaling complexes. Sci Signal 2011, 4:rs13.
107. Ishikawa H.O., Takeuchi H., Haltiwanger R.S., Irvine K.D. Four-jointed is a Golgi kinase that phosphorylates a subset of cadherin domains. Science 2008, 321:401-404.
108. Tagliabracci V.S., Engel J.L., Wen J., Wiley S.E., Worby C.A., Kinch L.N., et al. Secreted kinase phosphorylates extracellular proteins that regulate biomineralization. Science 2012, 336:1150-1153.
109. Crovello C.S., Furie B.C., Furie B. Histidine phosphorylation of P-selectin upon stimulation of human platelets: a novel pathway for activation-dependent signal transduction. Cell 1995, 82:279-286.
110. Attwood P.V. PN bond protein phosphatases. Biochim Biophys Acta 2012, [epub ahead of print 2012 Mar 10].
111. Besant P.G., Attwood P.V., Piggott M.J. Focus on phosphoarginine and phospholysine. Curr Protein Pept Sci 2009, 10:536-550.
112. Besant P.G., Attwood P.V. Mammalian histidine kinases. Biochim Biophys Acta 2005, 1754:281-290.
113. Stock A.M., Robinson V.L., Goudreau P.N. Two-component signal transduction. Annu Rev Biochem 2000, 69:183-215.
114. Robinson V.L., Buckler D.R., Stock A.M. A tale of two components: a novel kinase and a regulatory switch. Nat Struct Biol 2000, 7:626-633.
115. Stewart G.S., Panier S., Townsend K., Al-Hakim A.K., Kolas N.K., Miller E.S., et al. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 2009, 136:420-434.
116. Kolas N.K., Chapman J.R., Nakada S., Ylanko J., Chahwan R., Sweeney F.D., et al. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 2007, 318:1637-1640.