Cellular ERK phospho-form profiles with conserved preference for a switch-like pattern

Journal of Proteome Research

Volumn 12, Issue 2, 2013, Pages 637-646

  Hahn, Bettina ^a   D'Alessandro, Lorenza Alice ^b   Depner, Sofia ^b   Waldow, Katharina ^b   Boehm, Martin E ^a   Bachmann, Julie ^b   Schilling, Marcel ^b   Klingmüller, Ursula ^b   Lehmann, Wolf D ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b GERMAN CANCER RESEARCH CENTER   (Germany)

Author keywords

degree of phosphorylation; ERK; mass spectrometry; one source standards; phospho form abundance

Indexed keywords

INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHOPEPTIDE; SCATTER FACTOR;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; CYTOLYSIS; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; LIVER CELL; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; RAT; SIGNAL TRANSDUCTION; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY;

AMINO ACID MOTIFS; ANIMALS; CARBON ISOTOPES; CELL PROLIFERATION; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION; HEPATOCYTE GROWTH FACTOR; HEPATOCYTES; HUMANS; MAP KINASE KINASE KINASES; MAP KINASE SIGNALING SYSTEM; MICE; MOLECULAR SEQUENCE DATA; NITROGEN ISOTOPES; PHOSPHOPROTEINS; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PRIMARY CELL CULTURE; TANDEM MASS SPECTROMETRY;

EID: 84873391339     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr3007232     Document Type: Article

References (47)

1. Widmann, C.; Gibson, S.; Jarpe, M. B.; Johnson, G. L. Mitogen-activated protein kinase: Conservation of a three-kinase module from yeast to human Physiol. Rev. 1999, 79, 143-180
2. Zheng, C. F.; Guan, K. L. Properties of MEKs, the kinases that phosphorylate and activate the extracellular signal-regulated kinases J. Biol. Chem. 1993, 268, 23933-23939
3. Keyse, S. M. Protein phosphatases and the regulation of mitogen-activated protein kinase signalling Curr. Opin. Cell Biol. 2000, 12, 186-192
4. Junttila, M. R.; Li, S. P.; Westermarck, J. Phosphatase-mediated crosstalk between MAPK signalling pathways in the regulation of cell survival FASEB J. 2008, 22, 954-965
5. Millward, T. A.; Zolnierowicz, S.; Hemmings, B. A. Regulation of protein kinase cascades by protein phosphatase 2A Trends Biochem. Sci. 1999, 24, 186-191
6. Keyse, S. M. Protein phosphatases and the regulation of MAP kinase activity Semin. Cell. Dev. Biol. 1998, 9, 143-152
7. Groom, L. A.; Sneddon, A. A.; Alessi, D. R.; Dowd, S.; Keyse, S. M. Differential regulation of the MAP, SAP and RK/p38 kinases by Pyst1, a novel cytosolic dual-specificity phosphatase EMBO J. 1996, 15, 3621-32
8. Markevich, N. I.; Hoek, J. B.; Kholodenko, B. N. Signaling switches and bistability arising from multisite phosphorylation in protein kinase cascades J. Cell Biol. 2004, 164, 353-359
9. Burack, W. R.; Sturgill, T. W. The activating dual phosphorylation of MAPK by MEK is nonprocessive Biochemistry 1997, 36, 5929-5933
10. Ferrell, J. E.; Bhatt, R. R. Mechanistic studies of the dual phosphorylation of mitogen-activated protein kinase J. Biol. Chem. 1997, 272, 19008-19016
11. Zhao, Y.; Zhang, Z. Y. The mechanism of dephosphorylation of extracellular signal-regulated kinase 2 by mitogen-activated protein kinase phosphatase 3 J. Biol. Chem. 2001, 276, 32382-32391
12. Shankaran, H.; Ippolito, D. L.; Chrisler, W. B.; Resat, H.; Bollinger, N.; Opresko, L. K.; Wiley, H. S. Rapid and sustained nuclear-cytoplasmic ERK oscillations induced by epidermal growth factor Mol. Syst. Biol. 2009, 5, 13
13. Lefloch, R.; Pouyssegur, J.; Lenormand, P. Total ERK1/2 activity regulates cell proliferation Cell Cycle 2009, 8, 705-711
14. Saba-El-Leil, M. K.; Vella, F. D. J.; Vernay, B.; Voisin, L.; Chen, L.; Labrecque, N.; Ang, S. L.; Meloche, S. An essential function of the mitogen-activated protein kinase Erk2 in mouse trophoblast development EMBO Rep. 2003, 4, 964-968
15. Nekrasova, T.; Shive, C.; Gao, Y. H.; Kawamura, K.; Guardia, R.; Landreth, G.; Forsthuber, T. G. ERK1-deficient mice show normal T cell effector function and are highly susceptible to experimental autoimmune encephalomyelitis J. Immunol. 2005, 175, 2374-2380
16. Pages, G.; Guerin, S.; Grall, D.; Bonino, F. D.; Smith, A.; Anjuere, F.; Auberger, P.; Pouyssegur, J. Defective thymocyte maturation in p44 MAP kinase (Erk 1) knockout mice Science 1999, 286, 1374-1377
17. Schilling, M.; Maiwald, T.; Hengl, S.; Winter, D.; Kreutz, C.; Kolch, W.; Lehmann, W. D.; Timmer, J.; Klingmüller, U. Theoretical and experimental analysis links isoform-specific ERK signalling to cell fate decisions. Mol. Syst. Biol. 2009, 5.
18. Prabakaran, S.; Everley, R. A.; Landrieu, I.; Wieruszeski, J. M.; Lippens, G.; Steen, H.; Gunawardena, J. Comparative analysis of Erk phosphorylation suggests a mixed strategy for measuring phospho-form distributions Mol. Syst. Biol. 2011, 7, 15
19. Yao, Z.; Dolginov, Y.; Hanoch, T.; Yung, Y. V.; Ridner, G.; Lando, Z.; Zharhary, D.; Seger, R. Detection of partially phosphorylated forms of ERK by monoclonal antibodies reveals spatial regulation of ERK activity by phosphatases FEBS Lett. 2000, 468, 37-42
20. Gerber, S. A.; Rush, J.; Stemman, O.; Kirschner, M. W.; Gygi, S. P. Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 6940-6945
21. Hahn, B.; Boehm, M.; Raia, V.; Zinn, N.; Moller, P.; Klingmüller, U.; Lehmann, W. D. One-source peptide/phosphopeptide standards for accurate phosphorylation degree determination Proteomics 2011, 11, 490-494
22. McKay, M. M.; Morrison, D. K. Integrating signals from RTKs to ERK/MAPK Oncogene 2007, 26, 3113-3121
23. Chang, F.; Steelman, L. S.; Lee, J. T.; Shelton, J. G.; Navolanic, P. M.; Blalock, W. L.; Franklin, R. A.; McCubrey, J. A. Signal transduction mediated by the Ras/Raf/MEK/ERK pathway from cytokine receptors to transcription factors: potential targeting for therapeutic intervention Leukemia 2003, 17, 1263-1293
24. Castoldi, M.; Spasic, M. V.; Altamura, S.; Elmen, J.; Lindow, M.; Kiss, J.; Stolte, J.; Sparla, R.; D'Alessandro, L. A.; Klingmüller, U.; Fleming, R. E.; Longerich, T.; Grone, H. J.; Benes, V.; Kauppinen, S.; Hentze, M. W.; Muckenthaler, M. U. The liver-specific microRNA miR-122 controls systemic iron homeostasis in mice J. Clin. Invest. 2011, 121, 1386-1396
25. Maiwald, T.; Schneider, A.; Busch, H.; Sahle, S.; Gretz, N.; Weiss, T. S.; Kummer, U.; Klingmüller, U. Combining theoretical analysis and experimental data generation reveals IRF9 as a crucial factor for accelerating interferon alpha-induced early antiviral signalling FEBS J. 2010, 277, 4741-4754
26. Bachmann, J.; Raue, A.; Schilling, M.; Boehm, M. E.; Kreutz, C.; Kaschek, D.; Busch, H.; Gretz, N.; Lehmann, W. D.; Timmer, J.; Klingmüller, U. Division of labor by dual feedback regulators controls JAK2/STAT5 signaling over broad ligand range. Mol. Syst. Biol. 2011, 7.
27. Shevchenko, A.; Tomas, H.; Havlis, J.; Olsen, J. V.; Mann, M. In-gel digestion for mass spectrometric characterization of proteins and proteomes Nat. Protoc. 2006, 1, 2856-2860
28. Anderson, N. G.; Maller, J. L.; Tonks, N. K.; Sturgill, T. W. Requirement for integration of signals from 2 distinct phosphorylation pathways for activation of MAP kinase Nature 1990, 343, 651-653
29. Crews, C. M.; Alessandrini, A.; Erikson, R. L. The primary structure of MEK, a protein-kinase that phosphorylates the ERK gene-product Science 1992, 258, 478-480
30. Wolf-Yadlin, A.; Hautaniemi, S.; Lauffenburger, D. A.; White, F. M. Multiple reaction monitoring for robust quantitative proteomic analysis of cellular signaling networks Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 5860-5865
31. Lorenz, K.; Schmitt, J. P.; Schmitteckert, E. M.; Lohse, M. J. A new type of ERK1/2 autophosphorylation causes cardiac hypertrophy Nat. Med. 2009, 15, 75-83
32. Roux, P. P.; Blenis, J. ERK and p38 MAPK-activated protein kinases: A family of protein kinases with diverse biological functions Microbiol. Mol. Biol. Rev. 2004, 68, 320
33. Kolch, W. Meaningful relationships: the regulation of the Ras/Raf/MEK/ERK pathway by protein interactions Biochem. J. 2000, 351, 289-305
34. Bantscheff, M.; Eberhard, D.; Abraham, Y.; Bastuck, S.; Boesche, M.; Hobson, S.; Mathieson, T.; Perrin, J.; Raida, M.; Rau, C.; Reader, V.; Sweetman, G.; Bauer, A.; Bouwmeester, T.; Hopf, C.; Kruse, U.; Neubauer, G.; Ramsden, N.; Rick, J.; Kuster, B.; Drewes, G. Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors Nat. Biotechnol. 2007, 25, 1035-1044
35. Gnad, F.; de Godoy, L. M. F.; Cox, J.; Neuhauser, N.; Ren, S.; Olsen, J. V.; Mann, M. High-accuracy identification and bioinformatic analysis of in vivo protein phosphorylation sites in yeast Proteomics 2009, 9, 4642-4652
36. Oppermann, F. S.; Gnad, F.; Olsen, J. V.; Hornberger, R.; Greff, Z.; Keri, G.; Mann, M.; Daub, H. Large-scale proteomics analysis of the human kinome Mol. Cell. Proteomics 2009, 8, 1751-1764
37. Pan, C.; Gnad, F.; Olsen, J. V.; Mann, M. Quantitative phosphoproteome analysis of a mouse liver cell line reveals specificity of phosphatase inhibitors Proteomics 2008, 8, 4534-4546
38. Savitski, M. M.; Lemeer, S.; Boesche, M.; Lang, M.; Mathieson, T.; Bantscheff, M.; Kuster, B. Confident phosphorylation site localization using the Mascot Delta score. Mol. Cell. Proteomics 2011, 10.
39. Lefloch, R.; Pouyssegur, J.; Lenormand, P. Single and combined silencing of ERK1 and ERK2 reveals their positive contribution to growth signaling depending on their expression levels Mol. Cell. Biol. 2008, 28, 511-527
40. Krens, S. F. G.; Corredor-Adamez, M.; He, S. N.; Snaar-Jagalska, B. E.; Spaink, H. P. ERK1 and ERK2MAPK are key regulators of distinct gene sets in zebrafish embryogenesis. BMC Genomics 2008, 9.
41. Lloyd, A. C. Distinct functions for ERKs? J. Biol. 2006, 5, 13
42. Legewie, S.; Schoeberl, B.; Bluthgen, N.; Herzel, H. Competing docking interactions can bring about bistability in the MAPK cascade Biophys. J. 2007, 93, 2279-2288
43. Huard, J.; Mueller, S.; Gilles, E. D.; Klingmüller, U.; Klamt, S. An integrative model links multiple inputs and signaling pathways to the onset of DNA synthesis in hepatocytes FEBS J. 2012, 279, 3290-313
44. Seger, R.; Ahn, N. G.; Boulton, T. G.; Yancopoulos, G. D.; Panayotatos, N.; Radziejewska, E.; Ericsson, L.; Bratlien, R. L.; Cobb, M. H.; Krebs, E. G. Microtubule-associated protein 2 kinases, ERK1 and ERK2, undergo autophosphorylation on both tyrosine and threonine residues: Implications for their mechanism of activation Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 6142-6
45. Olsen, J. V.; Blagoev, B.; Gnad, F.; Macek, B.; Kumar, C.; Mortensen, P.; Mann, M. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks Cell 2006, 127, 635-648
46. Olsen, J. V.; Vermeulen, M.; Santamaria, A.; Kumar, C.; Miller, M. L.; Jensen, L. J.; Gnad, F.; Cox, J.; Jensen, T. S.; Nigg, E. A.; Brunak, S.; Mann, M. Quantitative Phosphoproteomics Reveals Widespread Full Phosphorylation Site Occupancy During Mitosis. Sci. Signal. 2010, 3.
47. Mayya, V.; Rezual, K.; Wu, L. F.; Fong, M. B.; Han, D. K. Absolute quantification of multisite phosphorylation by selective reaction monitoring mass spectrometry-Determination of inhibitory phosphorylation status of cyclin-dependent kinases Mol. Cell. Proteomics 2006, 5, 1146-1157