Toward a systems-level view of dynamic phosphorylation networks

Frontiers in Genetics

Volumn 5, Issue AUG, 2014, Pages

  Newman, Robert H ^a   Zhang, Jin ^b   Zhu, Heng ^b,c  

^a NORTH CAROLINA A AND T STATE UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Cell signaling and regulation; Fluorescent biosensors; Kinase substrate relationship; Phosphoproteomics; Protein microarrays; Protein phosphorylation networks; Quantitative mass spectrometry; Systems biology

Indexed keywords

AURORA B KINASE; CALCINEURIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIN DEPENDENT KINASE 1; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE; PROTEIN KINASE C; TRANSCRIPTION FACTOR NFAT;

BIOSENSOR; CELLULAR DISTRIBUTION; COMPUTER MODEL; ELECTROSPRAY; ENZYME ACTIVITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION; HUMAN; HYDROGEN BOND; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; INTRACELLULAR SIGNALING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR INTERACTION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MICROARRAY; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN SYNTHESIS REGULATION; QUANTITATIVE MASS SPECTROMETRY; REVIEW; SPATIOTEMPORAL ANALYSIS; TIME OF FLIGHT MASS SPECTROMETRY;

EID: 84906215563     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2014.00263     Document Type: Review

References (187)

1. Agrawal, U., Reilly, D. T., and Schroeder, C. M. (2013). Zooming in on biological processes with fluorescence nanoscopy. Curr. Opin. Biotechnol. 24, 646-653. doi: 10.1016/j.copbio.2013.02.016
2. Aguilar, H. N., Tracey, C. N., Tsang, S. C., McGinnis, J. M., and Mitchell, B. F. (2011). Phos-tag-based analysis of myosin regulatory light chain phosphorylation in human uterine myocytes. PLoS ONE 6:e20903. doi: 10.1371/journal.pone.0020903
3. Ai, H. W., Baird, M. A., Shen, Y., Davidson, M. W., and Campbell, R. E. (2014). Engineering and characterizing monomeric fluorescent proteins for live-cell imaging applications. Nat. Protoc. 9, 910-928. doi: 10.1038/nprot.2014.054
4. Ai, H. W., Hazelwood, K. L., Davidson, M. W., and Campbell, R. E. (2008). Fluorescent protein FRET pairs for ratiometric imaging of dual biosensors. Nat. Methods 5, 401-403. doi: 10.1038/nmeth.1207
5. Ananthanarayanan, B., Fosbrink, M., Rahdar, M., and Zhang, J. (2007). Live-cell molecular analysis of Akt activation reveals roles for activation loop phosphorylation. J. Biol. Chem. 282, 36634-36641. doi: 10.1074/jbc.M706227200
6. Andersson, L., and Porath, J. (1986). Isolation of phosphoproteins by immobilized metal (Fe3+) affinity chromatography. Anal. Biochem. 154, 250-254. doi: 10.1016/0003-2697(86)90523-3
7. Arencibia, J. M., Pastor-Flores, D., Bauer, A. F., Schulze, J. O., and Biondi, R. M. (2013). AGC protein kinases: from structural mechanism of regulation to allosteric drug development for the treatment of human diseases. Biochim. Biophys. Acta 1834, 1302-1321. doi: 10.1016/j.bbapap.2013.03.010
8. Beausoleil, S. A., Villen, J., Gerber, S. A., Rush, J., and Gygi, S. P. (2006). A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat. Biotechnol. 24, 1285-1292. doi: 10.1038/nbt1240
9. Belal, A. S., Sell, B. R., Hoi, H., Davidson, M. W., and Campbell, R. E. (2014). Optimization of a genetically encoded biosensor for cyclin B1-cyclin dependent kinase 1. Mol. Biosyst. 10, 191-195. doi: 10.1039/c3mb70402e
10. Besant, P. G., and Attwood, P. V. (2010). Histidine phosphorylation in histones and in other mammalian proteins. Methods Enzymol. 471, 403-426. doi: 10.1016/S0076-6879(10)71021-1
11. Biggs, M. J., Milone, M. C., Santos, L. C., Gondarenko, A., and Wind, S. J. (2011). High-resolution imaging of the immunological synapse and T-cell receptor microclustering through microfabricated substrates. J. R. Soc. Interface 8, 1462-1471. doi: 10.1098/rsif.2011.0025
12. Bishop, A. C., Buzko, O., and Shokat, K. M. (2001). Magic bullets for protein kinases. Trends Cell Biol. 11, 167-172. doi: 10.1016/S0962-8924(01)01928-6
13. Blom, N., Sicheritz-Ponten, T., Gupta, R., Gammeltoft, S., and Brunak, S. (2004). Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4, 1633-1649. doi: 10.1002/pmic.200300771
14. Bodenmiller, B., Wanka, S., Kraft, C., Urban, J., Campbell, D., Pedrioli, P. G., et al. (2010). Phosphoproteomic analysis reveals interconnected system-wide responses to perturbations of kinases and phosphatases in yeast. Sci. Signal. 3, rs4. doi: 10.1126/scisignal.2001182
15. Bordbar, A., Monk, J. M., King, Z. A., and Palsson, B. O. (2014). Constraint-based models predict metabolic and associated cellular functions. Nat. Rev. Genet. 15, 107-120. doi: 10.1038/nrg3643
16. Bose, R., Molina, H., Patterson, A. S., Bitok, J. K., Periaswamy, B., Bader, J. S., et al. (2006). Phosphoproteomic analysis of Her2/neu signaling and inhibition. Proc. Natl. Acad. Sci. U.S.A. 103, 9773-9778. doi: 10.1073/pnas.0603948103
17. Breitkreutz, A., Choi, H., Sharom, J. R., Boucher, L., Neduva, V., Larsen, B., et al. (2010). A global protein kinase and phosphatase interaction network in yeast. Science 328, 1043-1046. doi: 10.1126/science.1176495
18. Brinkworth, R. I., Breinl, R. A., and Kobe, B. (2003). Structural basis and prediction of substrate specificity in protein serine/threonine kinases. Proc. Natl. Acad. Sci. U.S.A. 100, 74-79. doi: 10.1073/pnas.0134224100
19. Calleja, V., Alcor, D., Laguerre, M., Park, J., Vojnovic, B., Hemmings, B. A., et al. (2007). Intramolecular and intermolecular interactions of protein kinase B define its activation in vivo. PLoS Biol. 5:e95. doi: 10.1371/journal.pbio.0050095
20. Camacho-Carvajal, M. M., Wollscheid, B., Aebersold, R., Steimle, V., and Schamel, W. W. (2004). Two-dimensional Blue native/SDS gel electrophoresis of multi-protein complexes from whole cellular lysates: a proteomics approach. Mol. Cell Proteomics 3, 176-182. doi: 10.1074/mcp.T300010-MCP200
21. Carlson, H. J., and Campbell, R. E. (2009). Genetically encoded FRET-based biosensors for multiparameter fluorescence imaging. Curr. Opin. Biotechnol. 20, 19-27. doi: 10.1016/j.copbio.2009.01.003
22. Chao, J. A., Yoon, Y. J., and Singer, R. H. (2012). Imaging translation in single cells using fluorescent microscopy. Cold Spring Harb. Perspect. Biol. 4:a012310. doi: 10.1101/cshperspect.a012310
23. Chen, C., and Turk, B. E. (2010). Analysis of serine-threonine kinase specificity using arrayed positional scanning peptide libraries. Curr. Protoc. Mol. Biol. Chapter 18:Unit 18.14. doi: 10.1002/0471142727.mb1814s91
24. Chou, M. F., Prisic, S., Lubner, J. M., Church, G. M., Husson, R. N., and Schwartz, D. (2012). Using bacteria to determine protein kinase specificity and predict target substrates. PLoS ONE 7:e52747. doi: 10.1371/journal.pone.0052747
25. Choudhary, C., and Mann, M. (2010). Decoding signalling networks by mass spectrometry-based proteomics. Nat. Rev. Mol. Cell Biol. 11, 427-439. doi: 10.1038/nrm2900
26. Ciruela, F. (2008). Fluorescence-based methods in the study of protein-protein interactions in living cells. Curr. Opin. Biotechnol. 19, 338-343. doi: 10.1016/j.copbio.2008.06.003
27. Craig, R., and Beavis, R. C. (2003). A method for reducing the time required to match protein sequences with tandem mass spectra. Rapid Commun. Mass Spectrom. 17, 2310-2316. doi: 10.1002/rcm.1198
28. D'hondt, C., Iyyathurai, J., Vinken, M., Rogiers, V., Leybaert, L., Himpens, B., et al. (2013). Regulation of connexin- and pannexin-based channels by post-translational modifications. Biol. Cell 105, 373-398. doi: 10.1111/boc.201200096
29. Day, R. N., and Davidson, M. W. (2009). The fluorescent protein palette: tools for cellular imaging. Chem. Soc. Rev. 38, 2887-2921. doi: 10.1039/b901966a
30. Day, R. N., and Davidson, M. W. (2012). Fluorescent proteins for FRET microscopy: monitoring protein interactions in living cells. Bioessays 34, 341-350. doi: 10.1002/bies.201100098
31. Dayon, L., and Sanchez, J. C. (2012). Relative protein quantification by MS/MS using the tandem mass tag technology. Methods Mol. Biol. 893, 115-127. doi: 10.1007/978-1-61779-885-6_9
32. Dedecker, P., Mo, G. C., Dertinger, T., and Zhang, J. (2012). Widely accessible method for superresolution fluorescence imaging of living systems. Proc. Natl. Acad. Sci. U.S.A. 109, 10909-10914. doi: 10.1073/pnas.1204917109
33. Dephoure, N., Gould, K. L., Gygi, S. P., and Kellogg, D. R. (2013). Mapping and analysis of phosphorylation sites: a quick guide for cell biologists. Mol. Biol. Cell 24, 535-542. doi: 10.1091/mbc.E12-09-0677
34. Derouiche, A., Cousin, C., and Mijakovic, I. (2012). Protein phosphorylation from the perspective of systems biology. Curr. Opin. Biotechnol. 23, 585-590. doi: 10.1016/j.copbio.2011.11.008
35. Deschenes-Simard, X., Kottakis, F., Meloche, S., and Ferbeyre, G. (2014). ERKs in cancer: friends or foes? Cancer Res. 74, 412-419. doi: 10.1158/0008-5472.CAN-13-2381
36. Deswal, S., Beck-Garcia, K., Blumenthal, B., Dopfer, E. P., and Schamel, W. W. (2010). Detection of phosphorylated T and B cell antigen receptor species by Phos-tag SDS- and Blue Native-PAGE. Immunol. Lett. 130, 51-56. doi: 10.1016/j.imlet.2009.12.012
37. Dissmeyer, N., and Schnittger, A. (2011). The age of protein kinases. Methods Mol. Biol. 779, 7-52. doi: 10.1007/978-1-61779-264-9_2
38. Eng, J. K., McCormack, A. L., and Yates, J. R. (1994). An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5, 976-989. doi: 10.1016/1044-0305(94)80016-2
39. Erickson, J. R., Patel, R., Ferguson, A., Bossuyt, J., and Bers, D. M. (2011). Fluorescence resonance energy transfer-based sensor Camui provides new insight into mechanisms of calcium/calmodulin-dependent protein kinase II activation in intact cardiomyocytes. Circ. Res. 109, 729-738. doi: 10.1161/CIRCRESAHA.111.247148
40. Evans, C., Noirel, J., Ow, S. Y., Salim, M., Pereira-Medrano, A. G., Couto, N., et al. (2012). An insight into iTRAQ: where do we stand now? Anal. Bioanal. Chem. 404, 1011-1027. doi: 10.1007/s00216-012-5918-6
41. Frommer, W. B., Davidson, M. W., and Campbell, R. E. (2009). Genetically encoded biosensors based on engineered fluorescent proteins. Chem. Soc. Rev. 38, 2833-2841. doi: 10.1039/b907749a
42. Fujioka, A., Terai, K., Itoh, R. E., Aoki, K., Nakamura, T., Kuroda, S., et al. (2006). Dynamics of the Ras/ERK MAPK cascade as monitored by fluorescent probes. J. Biol. Chem. 281, 8917-8926. doi: 10.1074/jbc.M509344200
43. Gafken, P. R., and Lampe, P. D. (2006). Methodologies for characterizing phosphoproteins by mass spectrometry. Cell Commun. Adhes. 13, 249-262. doi: 10.1080/15419060601077917
44. Gao, X., Lowry, P. R., Zhou, X., Depry, C., Wei, Z., Wong, G. W., et al. (2011). PI3K/Akt signaling requires spatial compartmentalization in plasma membrane microdomains. Proc. Natl. Acad. Sci. U.S.A. 108, 14509-14514. doi: 10.1073/pnas.1019386108
45. Gao, X., and Zhang, J. (2010). FRET-based activity biosensors to probe compartmentalized signaling. Chembiochem 11, 147-151. doi: 10.1002/cbic.200900594
46. Geer, L. Y., Markey, S. P., Kowalak, J. A., Wagner, L., Xu, M., Maynard, D. M., et al. (2004). Open mass spectrometry search algorithm. J. Proteome Res. 3, 958-964. doi: 10.1021/pr0499491
47. Glickman, J.K. (2012). "Assay development for protein kinases" in Source Assay Guidance Manual [Internet] , eds G. S. Sittampalam, N. Gal-Edd, M. Arkin, D. Auld, C. Austin, B. Bejcek, et al. (Bethesda, MD: Eli Lilly & Company and the National Center for Advancing Translational Sciences). (Updated 2012 October 01).
48. Gorreta, F., Carbone, W., and Barzaghi, D. (2012). Genomic profiling: cDNA arrays and oligoarrays. Methods Mol. Biol. 823, 89-105. doi: 10.1007/978-1-60327-216-2_7
49. Grant, D. M., Zhang, W., McGhee, E. J., Bunney, T. D., Talbot, C. B., Kumar, S., et al. (2008). Multiplexed FRET to image multiple signaling events in live cells. Biophys. J. 95, L69-L71. doi: 10.1529/biophysj.108.139204
50. Greenwald, E. C., Polanowska-Grabowska, R. K., and Saucerman, J. J. (2014). Integrating fluorescent biosensor data using computational models. Methods Mol. Biol. 1071, 227-248. doi: 10.1007/978-1-62703-622-1_18
51. Guha, U., Chaerkady, R., Marimuthu, A., Patterson, A. S., Kashyap, M. K., Harsha, H. C., et al. (2008). Comparisons of tyrosine phosphorylated proteins in cells expressing lung cancer-specific alleles of EGFR and KRAS. Proc. Natl. Acad. Sci. U.S.A. 105, 14112-14117. doi: 10.1073/pnas.0806158105
52. Guo, S. (2014). Insulin signaling, resistance, and the metabolic syndrome: insights from mouse models into disease mechanisms. J. Endocrinol. 220, T1-T23. doi: 10.1530/JOE-13-0327
53. Harrold, J. M., Ramanathan, M., and Mager, D. E. (2013). Network-based approaches in drug discovery and early development. Clin. Pharmacol. Ther. 94, 651-658. doi: 10.1038/clpt.2013.176
54. He, L., Han, X., and Ma, B. (2013). De novo sequencing with limited number of post-translational modifications per peptide. J. Bioinform. Comput. Biol. 11, 1350007. doi: 10.1142/S0219720013500078
55. Herbst, K. J., Ni, Q., and Zhang, J. (2009). Dynamic visualization of signal transduction in living cells: from second messengers to kinases. IUBMB Life 61, 902-908. doi: 10.1002/iub.232
56. Hjerrild, M., Stensballe, A., Rasmussen, T. E., Kofoed, C. B., Blom, N., Sicheritz-Ponten, T., et al. (2004). Identification of phosphorylation sites in protein kinase A substrates using artificial neural networks and mass spectrometry. J. Proteome Res. 3, 426-433. doi: 10.1021/pr0341033
57. Ho, M. S., Tsai, P. I., and Chien, C. T. (2006). F-box proteins: the key to protein degradation. J. Biomed. Sci. 13, 181-191. doi: 10.1007/s11373-005-9058-2
58. Honigmann, A., Mueller, V., Hell, S. W., and Eggeling, C. (2013). STED microscopy detects and quantifies liquid phase separation in lipid membranes using a new far-red emitting fluorescent phosphoglycerolipid analogue. Faraday Discuss. 161, 77-89. doi: 10.1039/c2fd20107k
59. Hu, J., Rho, H. S., Newman, R. H., Hwang, W., Neiswinger, J., Zhu, H., et al. (2014). Global analysis of phosphorylation networks in humans. Biochim. Biophys. Acta 1844, 224-231. doi: 10.1016/j.bbapap.2013.03.009
60. Hu, S., Xie, Z., Onishi, A., Yu, X., Jiang, L., Lin, J., et al. (2009). Profiling the human protein-DNA interactome reveals ERK2 as a transcriptional repressor of interferon signaling. Cell 139, 610-622. doi: 10.1016/j.cell.2009.08.037
61. Hu, S., Xie, Z., Qian, J., Blackshaw, S., and Zhu, H. (2011). Functional protein microarray technology. Wiley Interdiscip. Rev. Syst. Biol. Med. 3, 255-268. doi: 10.1002/wsbm.118
62. Huang, S. Y., Tsai, M. L., Chen, G. Y., Wu, C. J., and Chen, S. H. (2007). A systematic MS-based approach for identifying in vitro substrates of PKA and PKG in rat uteri. J. Proteome Res. 6, 2674-2684. doi: 10.1021/pr070134c
63. Huang, Z. X., Zhao, P., Zeng, G. S., Wang, Y. M., Sudbery, I., and Wang, Y. (2014). Phosphoregulation of Nap1 plays a role in septin ring dynamics and morphogenesis in Candida albicans. MBio 5:e00915-13. doi: 10.1128/mBio.00915-13
64. Hunter, T. (1996). Tyrosine phosphorylation: past, present and future. Biochem. Soc. Trans. 24, 307-327.
65. Hunter, T. (2012). Why nature chose phosphate to modify proteins. Philos. Trans. R. Soc. Lond B Biol. Sci. 367, 2513-2516. doi: 10.1098/rstb.2012.0013
66. Jeong, J. S., Jiang, L., Albino, E., Marrero, J., Rho, H. S., Hu, J., et al. (2012). Rapid identification of monospecific monoclonal antibodies using a human proteome microarray. Mol. Cell Proteomics 11:O111. doi: 10.1074/mcp.O111.016253
67. Jia, W., Andaya, A., and Leary, J. A. (2012). Novel mass spectrometric method for phosphorylation quantification using cerium oxide nanoparticles and tandem mass tags. Anal. Chem. 84, 2466-2473. doi: 10.1021/ac203248s
68. Jin, J., and Pawson, T. (2012). Modular evolution of phosphorylation-based signalling systems. Philos. Trans. R. Soc. Lond B Biol. Sci. 367, 2540-2555. doi: 10.1098/rstb.2012.0106
69. Johnson, H., and White, F. M. (2012). Toward quantitative phosphotyrosine profiling in vivo. Semin. Cell Dev. Biol. 23, 854-862. doi: 10.1016/j.semcdb.2012.05.008
70. Kettenbach, A. N., Wang, T., Faherty, B. K., Madden, D. R., Knapp, S., Bailey-Kellogg, C., et al. (2012). Rapid determination of multiple linear kinase substrate motifs by mass spectrometry. Chem. Biol. 19, 608-618. doi: 10.1016/j.chembiol.2012.04.011
71. Khan, P., Idrees, D., Moxley, M. A., Corbett, J. A., Ahmad, F., von Figura, G., et al. (2014). Luminol-based chemiluminescent signals: clinical and non-clinical application and future uses. Appl. Biochem. Biotechnol. 173, 333-355. doi: 10.1007/s12010-014-0850-1
72. Kim, J. H., Lee, J., Oh, B., Kimm, K., and Koh, I. (2004). Prediction of phosphorylation sites using SVMs. Bioinformatics. 20, 3179-3184. doi: 10.1093/bioinformatics/bth382
73. Kinoshita, E., Kinoshita-Kikuta, E., and Koike, T. (2012b). Phos-tag SDS-PAGE systems for phosphorylation profiling of proteins with a wide range of molecular masses under neutral pH conditions. Proteomics 12, 192-202. doi: 10.1002/pmic.201100524
74. Kinoshita, E., Kinoshita-Kikuta, E., Matsubara, M., Aoki, Y., Ohie, S., Mouri, Y., et al. (2009). Two-dimensional phosphate-affinity gel electrophoresis for the analysis of phosphoprotein isotypes. Electrophoresis 30, 550-559. doi: 10.1002/elps.200800386
75. Kinoshita, E., Kinoshita-Kikuta, E., Sugiyama, Y., Fukada, Y., Ozeki, T., and Koike, T. (2012a). Highly sensitive detection of protein phosphorylation by using improved Phos-tag Biotin. Proteomics 12, 932-937. doi: 10.1002/pmic.201100639
76. Kinoshita, E., Takahashi, M., Takeda, H., Shiro, M., and Koike, T. (2004). Recognition of phosphate monoester dianion by an alkoxide-bridged dinuclear zinc(II) complex. Dalton Trans. 1189-1193. doi: 10.1039/b400269e
77. Kinoshita-Kikuta, E., Kinoshita, E., and Koike, T. (2012). Separation and identification of four distinct serine-phosphorylation states of ovalbumin by Phos-tag affinity electrophoresis. Electrophoresis 33, 849-855. doi: 10.1002/elps.201100518
78. Klumpp, S., and Krieglstein, J. (2002). Phosphorylation and dephosphorylation of histidine residues in proteins. Eur. J. Biochem. 269, 1067-1071. doi: 10.1046/j.1432-1033.2002.02755.x
79. Knight, J. D., Tian, R., Lee, R. E., Wang, F., Beauvais, A., Zou, H., et al. (2012). A novel whole-cell lysate kinase assay identifies substrates of the p38 MAPK in differentiating myoblasts. Skelet. Muscle 2:5. doi: 10.1186/2044-5040-2-5
80. Koch, A., and Hauf, S. (2010). Strategies for the identification of kinase substrates using analog-sensitive kinases. Eur. J. Cell Biol. 89, 184-193. doi: 10.1016/j.ejcb.2009.11.024
81. Komatsu, N., Aoki, K., Yamada, M., Yukinaga, H., Fujita, Y., Kamioka, Y., et al. (2011). Development of an optimized backbone of FRET biosensors for kinases and GTPases. Mol. Biol. Cell 22, 4647-4656. doi: 10.1091/mbc.E11-01-0072
82. Kooij, V., Venkatraman, V., Tra, J., Kirk, J., Rowell, J., Blice-Baum, A., et al. (2014). Sizing up models of heart failure: Proteomics from flies to humans. Proteomics Clin. Appl. doi: 10.1002/prca.201300123. [Epub ahead of print].
83. Kosako, H., and Nagano, K. (2011). Quantitative phosphoproteomics strategies for understanding protein kinase-mediated signal transduction pathways. Expert. Rev. Proteomics 8, 81-94. doi: 10.1586/epr.10.104
84. Kozuka-Hata, H., Nasu-Nishimura, Y., Koyama-Nasu, R., Ao-Kondo, H., Tsumoto, K., Akiyama, T., et al. (2012). Phosphoproteome of human glioblastoma initiating cells reveals novel signaling regulators encoded by the transcriptome. PLoS ONE 7:e43398. doi: 10.1371/journal.pone.0043398
85. Kumar, N., Wolf-Yadlin, A., White, F. M., and Lauffenburger, D. A. (2007). Modeling HER2 effects on cell behavior from mass spectrometry phosphotyrosine data. PLoS Comput. Biol. 3:e4. doi: 10.1371/journal.pcbi.0030004
86. Kunkel, M. T., and Newton, A. C. (2009). Spatiotemporal dynamics of kinase signaling visualized by targeted reporters. Curr. Protoc. Chem. Biol. 1, 17-18. doi: 10.1002/9780470559277.ch090106
87. Kunkel, M. T., and Newton, A. C. (2014). Imaging kinase activity at protein scaffolds. Methods Mol. Biol. 1071, 129-137. doi: 10.1007/978-1-62703-622-1_10
88. Lad, C., Williams, N. H., and Wolfenden, R. (2003). The rate of hydrolysis of phosphomonoester dianions and the exceptional catalytic proficiencies of protein and inositol phosphatases. Proc. Natl. Acad. Sci. U.S.A. 100, 5607-5610. doi: 10.1073/pnas.0631607100
89. Lam, A. J., St. Pierre, F., Gong, Y., Marshall, J. D., Cranfill, P. J., Baird, M. A., et al. (2012). Improving FRET dynamic range with bright green and red fluorescent proteins. Nat. Methods 9, 1005-1012. doi: 10.1038/nmeth.2171
90. Leung, G. C., Murphy, J. M., Briant, D., and Sicheri, F. (2009). Characterization of kinase target phosphorylation consensus motifs using peptide SPOT arrays. Methods Mol. Biol. 570, 187-195. doi: 10.1007/978-1-60327-394-7_7
91. Liao, H., Byeon, I. J., and Tsai, M. D. (1999). Structure and function of a new phosphopeptide-binding domain containing the FHA2 of Rad53. J. Mol. Biol. 294, 1041-1049. doi: 10.1006/jmbi.1999.3313
92. Linding, R., Jensen, L. J., Ostheimer, G. J., van Vugt, M. A., Jorgensen, C., Miron, I. M., et al. (2007). Systematic discovery of in vivo phosphorylation networks. Cell 129, 1415-1426. doi: 10.1016/j.cell.2007.05.052
93. Linding, R., Jensen, L. J., Pasculescu, A., Olhovsky, M., Colwill, K., Bork, P., et al. (2008). NetworKIN: a resource for exploring cellular phosphorylation networks. Nucleic Acids Res. 36, D695-D699. doi: 10.1093/nar/gkm902
94. Liu, B. A., Jablonowski, K., Raina, M., Arce, M., Pawson, T., and Nash, P. D. (2006). The human and mouse complement of SH2 domain proteins-establishing the boundaries of phosphotyrosine signaling. Mol. Cell 22, 851-868. doi: 10.1016/j.molcel.2006.06.001
95. Mackenzie, R. W., and Elliott, B. T. (2014). Akt/PKB activation and insulin signaling: a novel insulin signaling pathway in the treatment of type 2 diabetes. Diabetes Metab. Syndr. Obes. 7, 55-64. doi: 10.2147/DMSO.S48260
96. Marfori, M., Mynott, A., Ellis, J. J., Mehdi, A. M., Saunders, N. F., Curmi, P. M., et al. (2011). Molecular basis for specificity of nuclear import and prediction of nuclear localization. Biochim. Biophys. Acta 1813, 1562-1577. doi: 10.1016/j.bbamcr.2010.10.013
97. Medina-Cleghorn, D., and Nomura, D. K. (2013). Chemical approaches to study metabolic networks. Pflugers Arch. 465, 427-440. doi: 10.1007/s00424-012-1201-0
98. Meharena, H. S., Chang, P., Keshwani, M. M., Oruganty, K., Nene, A. K., Kannan, N., et al. (2013). Deciphering the structural basis of eukaryotic protein kinase regulation. PLoS Biol. 11:e1001680. doi: 10.1371/journal.pbio.1001680
99. Mehta, S., and Zhang, J. (2011). Reporting from the field: genetically encoded fluorescent reporters uncover signaling dynamics in living biological systems. Annu. Rev. Biochem. 80, 375-401. doi: 10.1146/annurev-biochem-060409-093259
100. Mehta, S., and Zhang, J. (2014). Using a genetically encoded FRET-based reporter to visualize calcineurin phosphatase activity in living cells. Methods Mol. Biol. 1071, 139-149. doi: 10.1007/978-1-62703-622-1_11
101. Meissner, G. (2010). Regulation of ryanodine receptor ion channels through posttranslational modifications. Curr. Top. Membr. 66, 91-113. doi: 10.1016/S1063-5823(10)66005-X
102. Mertins, P., Yang, F., Liu, T., Mani, D. R., Petyuk, V. A., Gillette, M. A., et al. (2014). Ischemia in tumors induces early and sustained phosphorylation changes in stress kinase pathways but does not affect global protein levels. Mol. Cell Proteomics 13, 1690-1704. doi: 10.1074/mcp.M113.036392
103. Minden, J. S. (2012). DIGE: past and future. Methods Mol. Biol. 854, 3-8. doi: 10.1007/978-1-61779-573-2_1
104. Mok, J., Im, H., and Snyder, M. (2009). Global identification of protein kinase substrates by protein microarray analysis. Nat. Protoc. 4, 1820-1827. doi: 10.1038/nprot.2009.194
105. Mok, J., Kim, P. M., Lam, H. Y., Piccirillo, S., Zhou, X., Jeschke, G. R., et al. (2010). Deciphering protein kinase specificity through large-scale analysis of yeast phosphorylation site motifs. Sci. Signal. 3, ra12. doi: 10.1126/scisignal.2000482
106. Mok, J., Zhu, X., and Snyder, M. (2011). Dissecting phosphorylation networks: lessons learned from yeast. Expert. Rev. Proteomics 8, 775-786. doi: 10.1586/epr.11.64
107. Mujumdar, R. B., Ernst, L. A., Mujumdar, S. R., Lewis, C. J., and Waggoner, A. S. (1993). Cyanine dye labeling reagents: sulfoindocyanine succinimidyl esters. Bioconjug. Chem. 4, 105-111. doi: 10.1021/bc00020a001
108. Mukai, N., Nakanishi, T., Shimizu, A., Takubo, T., and Ikeda, T. (2008). Identification of phosphotyrosyl proteins in vitreous humours of patients with vitreoretinal diseases by sodium dodecyl sulphate-polyacrylamide gel electrophoresis/Western blotting/matrix-assisted laser desorption time-of-flight mass spectrometry. Ann. Clin. Biochem. 45, 307-312. doi: 10.1258/acb.2007.007151
109. Na, S., and Paek, E. (2014). Software eyes for protein post-translational modifications. Mass Spectrom. Rev. doi: 10.1002/mas.21425. [Epub ahead of print].
110. Nabetani, T., Kim, Y. J., Watanabe, M., Ohashi, Y., Kamiguchi, H., and Hirabayashi, Y. (2009). Improved method of phosphopeptides enrichment using biphasic phosphate-binding tag/C18 tip for versatile analysis of phosphorylation dynamics. Proteomics 9, 5525-5533. doi: 10.1002/pmic.200900341
111. Neininger, A., Thielemann, H., and Gaestel, M. (2001). FRET-based detection of different conformations of MK2. EMBO Rep. 2, 703-708. doi: 10.1093/embo-reports/kve157
112. Neves, S. R., Tsokas, P., Sarkar, A., Grace, E. A., Rangamani, P., Taubenfeld, S. M., et al. (2008). Cell shape and negative links in regulatory motifs together control spatial information flow in signaling networks. Cell 133, 666-680. doi: 10.1016/j.cell.2008.04.025
113. Newman, R. H., Fosbrink, M. D., and Zhang, J. (2011). Genetically encodable fluorescent biosensors for tracking signaling dynamics in living cells. Chem. Rev. 111, 3614-3666. doi: 10.1021/cr100002u
114. Newman, R. H., Hu, J., Rho, H. S., Xie, Z., Woodard, C., Neiswinger, J., et al. (2013). Construction of human activity-based phosphorylation networks. Mol. Syst. Biol. 9, 655. doi: 10.1038/msb.2013.12
115. Newman, R. H., and Zhang, J. (2008). Visualization of phosphatase activity in living cells with a FRET-based calcineurin activity sensor. Mol. Biosyst. 4, 496-501. doi: 10.1039/b720034j
116. Ni, Q., Ganesan, A., Aye-Han, N. N., Gao, X., Allen, M. D., Levchenko, A., et al. (2011). Signaling diversity of PKA achieved via a Ca2+-cAMP-PKA oscillatory circuit. Nat. Chem. Biol. 7, 34-40. doi: 10.1038/nchembio.478
117. Niggli, E., Ullrich, N. D., Gutierrez, D., Kyrychenko, S., Polakova, E., and Shirokova, N. (2013). Posttranslational modifications of cardiac ryanodine receptors: Ca(2+) signaling and EC-coupling. Biochim. Biophys. Acta 1833, 866-875. doi: 10.1016/j.bbamcr.2012.08.016
118. Nilsson, C. L. (2012). Advances in quantitative phosphoproteomics. Anal. Chem. 84, 735-746. doi: 10.1021/ac202877y
119. Okamura, H., Aramburu, J., Garcia-Rodriguez, C., Viola, J. P., Raghavan, A., Tahiliani, M., et al. (2000). Concerted dephosphorylation of the transcription factor NFAT1 induces a conformational switch that regulates transcriptional activity. Mol. Cell 6, 539-550. doi: 10.1016/S1097-2765(00)00053-8
120. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P., et al. (2006). Global, in vivo , and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648. doi: 10.1016/j.cell.2006.09.026
121. Olsen, J. V., Macek, B., Lange, O., Makarov, A., Horning, S., and Mann, M. (2007). Higher-energy C-trap dissociation for peptide modification analysis. Nat. Methods 4, 709-712. doi: 10.1038/nmeth1060
122. Olsen, J. V., Vermeulen, M., Santamaria, A., Kumar, C., Miller, M. L., Jensen, L. J., et al. (2010). Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3, ra3. doi: 10.1126/scisignal.2000475
123. Ong, S. E. (2012). The expanding field of SILAC. Anal. Bioanal. Chem. 404, 967-976. doi: 10.1007/s00216-012-5998-3
124. Ortsater, H., Grankvist, N., Honkanen, R. E., and Sjoholm, A. (2014). Protein phosphatases in pancreatic islets. J. Endocrinol. 221, R121-R144. doi: 10.1530/JOE-14-0002
125. Oyama, M., Kozuka-Hata, H., Tasaki, S., Semba, K., Hattori, S., Sugano, S., et al. (2009). Temporal perturbation of tyrosine phosphoproteome dynamics reveals the system-wide regulatory networks. Mol. Cell Proteomics 8, 226-231. doi: 10.1074/mcp.M800186-MCP200
126. Padilla-Parra, S., and Tramier, M. (2012). FRET microscopy in the living cell: different approaches, strengths and weaknesses. Bioessays 34, 369-376. doi: 10.1002/bies.201100086
127. Pastrello, C., Pasini, E., Kotlyar, M., Otasek, D., Wong, S., Sangrar, W., et al. (2014). Integration, visualization and analysis of human interactome. Biochem. Biophys. Res. Commun. 445, 757-773. doi: 10.1016/j.bbrc.2014.01.151
128. Pellegrin, S., Heesom, K. J., Satchwell, T. J., Hawley, B. R., Daniels, G., van den Akker, E., et al. (2012). Differential proteomic analysis of human erythroblasts undergoing apoptosis induced by epo-withdrawal. PLoS ONE 7:e38356. doi: 10.1371/journal.pone.0038356
129. Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. (1999). Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567. doi: 10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2
130. Persson, F., Barkefors, I., and Elf, J. (2013). Single molecule methods with applications in living cells. Curr. Opin. Biotechnol. 24, 737-744. doi: 10.1016/j.copbio.2013.03.013
131. Pierobon, M., Wulfkuhle, J., Liotta, L., and Petricoin, E. (2014). Application of molecular technologies for phosphoproteomic analysis of clinical samples. Oncogene. doi: 10.1038/onc.2014.16. [Epub ahead of print].
132. Popescu, S. C., Popescu, G. V., Bachan, S., Zhang, Z., Gerstein, M., Snyder, M., et al. (2009). MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev. 23, 80-92. doi: 10.1101/gad.1740009
133. Posewitz, M. C., and Tempst, P. (1999). Immobilized gallium(III) affinity chromatography of phosphopeptides. Anal. Chem. 71, 2883-2892. doi: 10.1021/ac981409y
134. Ptacek, J., Devgan, G., Michaud, G., Zhu, H., Zhu, X., Fasolo, J., et al. (2005). Global analysis of protein phosphorylation in yeast. Nature 438, 679-684. doi: 10.1038/nature04187
135. Puig, O., Caspary, F., Rigaut, G., Rutz, B., Bouveret, E., Bragado-Nilsson, E., et al. (2001). The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24, 218-229. doi: 10.1006/meth.2001.1183
136. Reinhardt, H. C., and Yaffe, M. B. (2013). Phospho-Ser/Thr-binding domains: navigating the cell cycle and DNA damage response. Nat. Rev. Mol. Cell Biol. 14, 563-580. doi: 10.1038/nrm3640
137. Rigbolt, K. T., and Blagoev, B. (2012). Quantitative phosphoproteomics to characterize signaling networks. Semin. Cell Dev. Biol. 23, 863-871. doi: 10.1016/j.semcdb.2012.05.006
138. Ritt, M., Guan, J. L., and Sivaramakrishnan, S. (2013). Visualizing and manipulating focal adhesion kinase regulation in live cells. J. Biol. Chem. 288, 8875-8886. doi: 10.1074/jbc.M112.421164
139. Roura, S., Galvez-Monton, C., and Bayes-Genis, A. (2013). Bioluminescence imaging: a shining future for cardiac regeneration. J. Cell Mol. Med. 17, 693-703. doi: 10.1111/jcmm.12018
140. Ruprecht, B., and Lemeer, S. (2014). Proteomic analysis of phosphorylation in cancer. Expert Rev. Proteomics 11, 259-267. doi: 10.1586/14789450.2014.901156
141. Sample, V., Newman, R. H., and Zhang, J. (2009). The structure and function of fluorescent proteins. Chem. Soc. Rev. 38, 2852-2864. doi: 10.1039/b913033k
142. Saucerman, J. J., Zhang, J., Martin, J. C., Peng, L. X., Stenbit, A. E., Tsien, R. Y., et al. (2006). Systems analysis of PKA-mediated phosphorylation gradients in live cardiac myocytes. Proc. Natl. Acad. Sci. U.S.A. 103, 12923-12928. doi: 10.1073/pnas.0600137103
143. Savitski, M. M., Lemeer, S., Boesche, M., Lang, M., Mathieson, T., Bantscheff, M., et al. (2011). Confident phosphorylation site localization using the Mascot Delta Score. Mol. Cell Proteomics 10:M110. doi: 10.1074/mcp.M110.003830
144. Sciarretta, S., Volpe, M., and Sadoshima, J. (2014). Mammalian target of rapamycin signaling in cardiac physiology and disease. Circ. Res. 114, 549-564. doi: 10.1161/CIRCRESAHA.114.302022
145. Shekhawat, S. S., and Ghosh, I. (2011). Split-protein systems: beyond binary protein-protein interactions. Curr. Opin. Chem. Biol. 15, 789-797. doi: 10.1016/j.cbpa.2011.10.014
146. Shirai, A., Matsuyama, A., Yashiroda, Y., Hashimoto, A., Kawamura, Y., Arai, R., et al. (2008). Global analysis of gel mobility of proteins and its use in target identification. J. Biol. Chem. 283, 10745-10752. doi: 10.1074/jbc.M709211200
147. Sipieter, F., Vandame, P., Spriet, C., Leray, A., Vincent, P., Trinel, D., et al. (2013). From FRET imaging to practical methodology for kinase activity sensing in living cells. Prog. Mol. Biol. Transl. Sci. 113, 145-216. doi: 10.1016/B978-0-12-386932-6.00005-3
148. Skrzypski, M. (2008). Quantitative reverse transcriptase real-time polymerase chain reaction (qRT-PCR) in translational oncology: lung cancer perspective. Lung Cancer 59, 147-154. doi: 10.1016/j.lungcan.2007.11.008
149. Song, C., Ye, M., Liu, Z., Cheng, H., Jiang, X., Han, G., et al. (2012). Systematic analysis of protein phosphorylation networks from phosphoproteomic data. Mol. Cell Proteomics 11, 1070-1083. doi: 10.1074/mcp.M111.012625
150. Song, Q., Saucerman, J. J., Bossuyt, J., and Bers, D. M. (2008). Differential integration of Ca2+-calmodulin signal in intact ventricular myocytes at low and high affinity Ca2+-calmodulin targets. J. Biol. Chem. 283, 31531-31540. doi: 10.1074/jbc.M804902200
151. Stasyk, T., Schiefermeier, N., Skvortsov, S., Zwierzina, H., Peranen, J., Bonn, G. K., et al. (2007). Identification of endosomal epidermal growth factor receptor signaling targets by functional organelle proteomics. Mol. Cell Proteomics 6, 908-922. doi: 10.1074/mcp.M600463-MCP200
152. Stynen, B., Tournu, H., Tavernier, J., and Van Dijck, P. (2012). Diversity in genetic in vivo methods for protein-protein interaction studies: from the yeast two-hybrid system to the mammalian split-luciferase system. Microbiol. Mol. Biol. Rev. 76, 331-382. doi: 10.1128/MMBR.05021-11
153. Sun, Y., Rombola, C., Jyothikumar, V., and Periasamy, A. (2013). Forster resonance energy transfer microscopy and spectroscopy for localizing protein-protein interactions in living cells. Cytometry A 83, 780-793. doi: 10.1002/cyto.a.22321
154. Sutandy, F. X., Qian, J., Chen, C. S., and Zhu, H. (2013). Overview of protein microarrays. Curr. Protoc. Protein Sci. Chapter 27:Unit 27.1. doi: 10.1002/0471140864.ps2701s72
155. Syka, J. E., Marto, J. A., Bai, D. L., Horning, S., Senko, M. W., Schwartz, J. C., et al. (2004). Novel linear quadrupole ion trap/FT mass spectrometer: performance characterization and use in the comparative analysis of histone H3 post-translational modifications. J. Proteome Res. 3, 621-626. doi: 10.1021/pr0499794
156. Tasaki, S., Nagasaki, M., Oyama, M., Hata, H., Ueno, K., Yoshida, R., et al. (2006). Modeling and estimation of dynamic EGFR pathway by data assimilation approach using time series proteomic data. Genome Inform. 17, 226-238.
157. Taylor, S. S., and Kornev, A. P. (2011). Protein kinases: evolution of dynamic regulatory proteins. Trends Biochem. Sci. 36, 65-77. doi: 10.1016/j.tibs.2010.09.006
158. Tian, T., and Song, J. (2012). Mathematical modelling of the MAP kinase pathway using proteomic datasets. PLoS ONE 7:e42230. doi: 10.1371/journal.pone.0042230
159. Tsou, P., Zheng, B., Hsu, C. H., Sasaki, A. T., and Cantley, L. C. (2011). A fluorescent reporter of AMPK activity and cellular energy stress. Cell Metab. 13, 476-486. doi: 10.1016/j.cmet.2011.03.006
160. Tsunehiro, M., Meki, Y., Matsuoka, K., Kinoshita-Kikuta, E., Kinoshita, E., and Koike, T. (2013). A Phos-tag-based magnetic-bead method for rapid and selective separation of phosphorylated biomolecules. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 925, 86-94. doi: 10.1016/j.jchromb.2013.02.039
161. Ummanni, R., Mannsperger, H. A., Sonntag, J., Oswald, M., Sharma, A. K., Konig, R., et al. (2014). Evaluation of reverse phase protein array (RPPA)-based pathway-activation profiling in 84 non-small cell lung cancer (NSCLC) cell lines as platform for cancer proteomics and biomarker discovery. Biochim. Biophys. Acta 1844, 950-959. doi: 10.1016/j.bbapap.2013.11.017
162. van Rossum, T., Kengen, S. W., and van der, Oost, J. (2013). Reporter-based screening and selection of enzymes. FEBS J. 280, 2979-2996. doi: 10.1111/febs.12281
163. Violin, J. D., DiPilato, L. M., Yildirim, N., Elston, T. C., Zhang, J., and Lefkowitz, R. J. (2008). beta2-adrenergic receptor signaling and desensitization elucidated by quantitative modeling of real time cAMP dynamics. J. Biol. Chem. 283, 2949-2961. doi: 10.1074/jbc.M707009200
164. Wiechert, W., Schweissgut, O., Takanaga, H., and Frommer, W. B. (2007). Fluxomics: mass spectrometry versus quantitative imaging. Curr. Opin. Plant Biol. 10, 323-330. doi: 10.1016/j.pbi.2007.04.015
165. Wilkins, M. R. (2009). Hares and tortoises: the high- versus low-throughput proteomic race. Electrophoresis 30(Suppl. 1), S150-S155. doi: 10.1002/elps.200900175
166. Woehler, A. (2013). Simultaneous quantitative live cell imaging of multiple FRET-based biosensors. PLoS ONE 8:e61096. doi: 10.1371/journal.pone.0061096
167. Wolf-Yadlin, A., Kumar, N., Zhang, Y., Hautaniemi, S., Zaman, M., Kim, H. D., et al. (2006). Effects of HER2 overexpression on cell signaling networks governing proliferation and migration. Mol. Syst. Biol. 2, 54. doi: 10.1038/msb4100094
168. Wong, Y. H., Lee, T. Y., Liang, H. K., Huang, C. M., Wang, T. Y., Yang, Y. H., et al. (2007). KinasePhos 2.0: a web server for identifying protein kinase-specific phosphorylation sites based on sequences and coupling patterns. Nucleic Acids Res. 35, W588-W594. doi: 10.1093/nar/gkm322
169. Woodard, C. L., Goodwin, C. R., Wan, J., Xia, S., Newman, R., Hu, J., et al. (2013). Profiling the dynamics of a human phosphorylome reveals new components in HGF/c-Met signaling. PLoS ONE 8:e72671. doi: 10.1371/journal.pone.0072671
170. Wu, M., Yang, X., and Chan, C. (2009). A dynamic analysis of IRS-PKR signaling in liver cells: a discrete modeling approach. PLoS ONE 4:e8040. doi: 10.1371/journal.pone.0008040
171. Xue, Y., Li, A., Wang, L., Feng, H., and Yao, X. (2006). PPSP: prediction of PK-specific phosphorylation site with Bayesian decision theory. BMC Bioinformatics 7:163. doi: 10.1186/1471-2105-7-163
172. Xue, Y., Zhou, F., Zhu, M., Ahmed, K., Chen, G., and Yao, X. (2005). GPS: a comprehensive www server for phosphorylation sites prediction. Nucleic Acids Res. 33, W184-W187. doi: 10.1093/nar/gki393
173. Yaffe, M. B. (2002). Phosphotyrosine-binding domains in signal transduction. Nat. Rev. Mol. Cell Biol. 3, 177-186. doi: 10.1038/nrm759
174. 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. doi: 10.1038/86737
175. Yang, C., Zhong, X., and Li, L. (2014). Recent advances in enrichment and separation strategies for mass spectrometry-based phosphoproteomics. Electrophoresis. doi: 10.1002/elps.201400017. [Epub ahead of print].
176. Yip, Y. Y., Yeap, Y. Y., Bogoyevitch, M. A., and Ng, D. C. (2014). cAMP-dependent protein kinase and c-Jun N-terminal kinase mediate stathmin phosphorylation for the maintenance of interphase microtubules during osmotic stress. J. Biol. Chem. 289, 2157-2169. doi: 10.1074/jbc.M113.470682
177. Yoshizaki, H., Aoki, K., Nakamura, T., and Matsuda, M. (2006). Regulation of RalA GTPase by phosphatidylinositol 3-kinase as visualized by FRET probes. Biochem. Soc. Trans. 34, 851-854. doi: 10.1042/BST0340851
178. Zadran, S., Standley, S., Wong, K., Otiniano, E., Amighi, A., and Baudry, M. (2012). Fluorescence resonance energy transfer (FRET)-based biosensors: visualizing cellular dynamics and bioenergetics. Appl. Microbiol. Biotechnol. 96, 895-902. doi: 10.1007/s00253-012-4449-6
179. Zapata-Hommer, O., and Griesbeck, O. (2003). Efficiently folding and circularly permuted variants of the Sapphire mutant of GFP. BMC Biotechnol. 3:5. doi: 10.1186/1472-6750-3-5
180. Zhang, C., Lopez, M. S., Dar, A. C., Ladow, E., Finkbeiner, S., Yun, C. H., et al. (2013). Structure-guided inhibitor design expands the scope of analog-sensitive kinase technology. ACS Chem. Biol. 8, 1931-1938. doi: 10.1021/cb400376p
181. Zhang, H., Zha, X., Tan, Y., Hornbeck, P. V., Mastrangelo, A. J., Alessi, D. R., et al. (2002). Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs. J. Biol. Chem. 277, 39379-39387. doi: 10.1074/jbc.M206399200
182. Zhang, J., and Allen, M. D. (2007). FRET-based biosensors for protein kinases: illuminating the kinome. Mol. Biosyst. 3, 759-765. doi: 10.1039/b706628g
183. Zhang, J., Hupfeld, C. J., Taylor, S. S., Olefsky, J. M., and Tsien, R. Y. (2005a). Insulin disrupts beta-adrenergic signalling to protein kinase A in adipocytes. Nature 437, 569-573. doi: 10.1038/nature04140
184. Zhang, J., Ma, Y., Taylor, S. S., and Tsien, R. Y. (2001). Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering. Proc. Natl. Acad. Sci. U.S.A. 98, 14997-15002. doi: 10.1073/pnas.211566798
185. Zhang, Y., Wolf-Yadlin, A., Ross, P. L., Pappin, D. J., Rush, J., Lauffenburger, D. A., et al. (2005b). Time-resolved mass spectrometry of tyrosine phosphorylation sites in the epidermal growth factor receptor signaling network reveals dynamic modules. Mol. Cell Proteomics 4, 1240-1250. doi: 10.1074/mcp.M500089-MCP200
186. Zhu, H., Cox, E., and Qian, J. (2012). Functional protein microarray as molecular decathlete: a versatile player in clinical proteomics. Proteomics Clin. Appl. 6, 548-562. doi: 10.1002/prca.201200041
187. Zubarev, R. A., Horn, D. M., Fridriksson, E. K., Kelleher, N. L., Kruger, N. A., Lewis, M. A., et al. (2000). Electron capture dissociation for structural characterization of multiply charged protein cations. Anal. Chem. 72, 563-573. doi: 10.1021/ac990811p