Targeted quantitative phosphoproteomics approach for the detection of phospho-tyrosine signaling in plants

Journal of Proteome Research

Volumn 11, Issue 1, 2012, Pages 438-448

  Mithoe, Sharon C ^a   Boersema, Paul J ^b,c   Berke, Lidija ^a   Snel, Berend ^a   Heck, Albert J R ^b   Menke, Frank L H ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Arabidopsis; flagellin; immune signaling; metabolic labeling; mitogen activated protein kinase; phosphoprotein; proteomics; quantification; Tyrosine

Indexed keywords

FLAGELLIN; GLYCOGEN SYNTHASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOTYROSINE; TYROSINE; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; CELL COMPARTMENTALIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; FUNCTIONAL PROTEOMICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; STRUCTURAL PROTEOMICS; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CULTURE TECHNIQUES; CHROMATOGRAPHY, AFFINITY; CONSERVED SEQUENCE; FLAGELLIN; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PEPTIDE MAPPING; PHOSPHOPROTEINS; PHOSPHOTYROSINE; PLANT LEAVES; PROTEOME; PROTEOMICS; SIGNAL TRANSDUCTION;

ANIMALIA; ARABIDOPSIS;

EID: 84855524689     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200893k     Document Type: Article

References (68)

1. Kersten, B.; Agrawal, G. K.; Durek, P.; Neigenfind, J.; Schulze, W.; Walther, D.; Rakwal, R. Plant phosphoproteomics: an update Proteomics 2009, 9 (4) 964-88
2. Pawson, T. Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems Cell 2004, 116 (2) 191-203 (Pubitemid 38167312)
3. Schulze, W. X. Proteomics approaches to understand protein phosphorylation in pathway modulation Curr. Opin. Plant Biol. 2010, 13 (3) 280-87
4. Lee, J.; Rudd, J. J.; Macioszek, V. K.; Scheel, D. Dynamic changes in the localization of MAPK cascade components controlling pathogenesis-related (PR) gene expression during innate immunity in parsley J. Biol. Chem. 2004, 279 (21) 22440-8 (Pubitemid 38679442)
5. Seet, B. T.; Dikic, I.; Zhou, M. M.; Pawson, T. Reading protein modifications with interaction domains Nat. Rev. Mol. Cell. Biol. 2006, 7 (7) 473-83 (Pubitemid 44036453)
6. Ficarro, S. B.; McCleland, M. L.; Stukenberg, P. T.; Burke, D. J.; Ross, M. M.; Shabanowitz, J.; Hunt, D. F.; White, F. M. Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae Nat. Biotechnol. 2002, 20 (3) 301-5 (Pubitemid 34205425)
7. Blagoev, B.; Kratchmarova, I.; Ong, S. E.; Nielsen, M.; Foster, L. J.; Mann, M. A proteomics strategy to elucidate functional protein-protein interactions applied to EGF signaling Nat. Biotechnol. 2003, 21 (3) 315-8 (Pubitemid 36314817)
8. Nuhse, T. S.; Stensballe, A.; Jensen, O. N.; Peck, S. C. Large-scale analysis of in vivo phosphorylated membrane proteins by immobilized metal ion affinity chromatography and mass spectrometry Mol. Cell. Proteomics 2003, 2 (11) 1234-43
9. Pinkse, M. W.; Uitto, P. M.; Hilhorst, M. J.; Ooms, B.; Heck, A. J. Selective isolation at the femtomole level of phosphopeptides from proteolytic digests using 2D-NanoLC-ESI-MS/MS and titanium oxide precolumns Anal. Chem. 2004, 76 (14) 3935-43 (Pubitemid 38943662)
10. Thingholm, T. E.; Jensen, O. N.; Larsen, M. R. Analytical strategies for phosphoproteomics Proteomics 2009, 9 (6) 1451-68
11. Heck, A. J.; Krijgsveld, J. Mass spectrometry-based quantitative proteomics Expert Rev. Proteomics 2004, 1 (3) 317-26
12. Bantscheff, M.; Schirle, M.; Sweetman, G.; Rick, J.; Kuster, B. Quantitative mass spectrometry in proteomics: a critical review Anal. Bioanal. Chem. 2007, 389 (4) 1017-31 (Pubitemid 47482251)
13. Schulze, W. X.; Usadel, B. Quantitation in mass-spectrometry-based proteomics Annu. Rev. Plant Biol. 2010, 61, 491-516
14. Benschop, J. J.; Mohammed, S.; O'Flaherty, M.; Heck, A. J. R.; Slijper, M.; Menke, F. L. H. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis Mol. Cell. Proteomics 2007, 6 (7) 1198-214 (Pubitemid 47099230)
15. de la Fuente van Bentem, S.; Anrather, D.; Dohnal, I.; Roitinger, E.; Csaszar, E.; Joore, J.; Buijnink, J.; Carreri, A.; Forzani, C.; Lorkovic, Z. J.; Barta, A.; Lecourieux, D.; Verhounig, A.; Jonak, C.; Hirt, H. Site-specific phosphorylation profiling of Arabidopsis proteins by mass spectrometry and peptide chip analysis J. Proteome Res. 2008, 7 (6) 2458-70
16. Mithoe, S. C.; Menke, F. L. H. Phosphoproteomics perspective on plant signal transduction and tyrosine phosphorylation Phytochemistry 2011, 72 (10) 997-1006
17. de la Fuente van Bentem, S.; Hirt, H. Protein tyrosine phosphorylation in plants: More abundant than expected? Trends Plant Sci. 2009, 14 (2) 71-6
18. Luan, S. Tyrosine phosphorylation in plant cell signaling Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (18) 11567-9 (Pubitemid 34994438)
19. Rigbolt, K. T.; Prokhorova, T. A.; Akimov, V.; Henningsen, J.; Johansen, P. T.; Kratchmarova, I.; Kassem, M.; Mann, M.; Olsen, J. V.; Blagoev, B. System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation Sci. Signal. 2011, 4 (164) rs3
20. Van Hoof, D.; Munoz, J.; Braam, S. R.; Pinkse, M. W.; Linding, R.; Heck, A. J.; Mummery, C. L.; Krijgsveld, J. Phosphorylation dynamics during early differentiation of human embryonic stem cells Cell Stem Cell 2009, 5 (2) 214-26
21. Lim, W. A.; Pawson, T. Phosphotyrosine signaling: evolving a new cellular communication system Cell 2010, 142 (5) 661-7
22. Blagoev, B.; Ong, S. E.; Kratchmarova, I.; Mann, M. Temporal analysis of phosphotyrosine-dependent signaling networks by quantitative proteomics Nat. Biotechnol. 2004, 22 (9) 1139-45 (Pubitemid 39166852)
23. Del Rosario, A. M.; White, F. M. Quantifying oncogenic phosphotyrosine signaling networks through systems biology Curr. Opin. Genet. Dev. 2010, 20 (1) 23-30
24. Ding, V. M.; Boersema, P. J.; Foong, L. Y.; Preisinger, C.; Koh, G.; Natarajan, S.; Lee, D. Y.; Boekhorst, J.; Snel, B.; Lemeer, S.; Heck, A. J.; Choo, A. Tyrosine phosphorylation profiling in FGF-2 stimulated human embryonic stem cells PLoS One 2011, 6 (3) e17538
25. Sugiyama, N.; Nakagami, H.; Mochida, K.; Daudi, A.; Tomita, M.; Shirasu, K.; Ishihama, Y. Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis Mol. Syst. Biol. 2008, 4
26. Nakagami, H.; Sugiyama, N.; Mochida, K.; Daudi, A.; Yoshida, Y.; Toyoda, T.; Tomita, M.; Ishihama, Y.; Shirasu, K. Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants Plant Physiol. 2010, 153 (3) 1161-74
27. Grimsrud, P. A.; den Os, D.; Wenger, C. D.; Swaney, D. L.; Schwartz, D.; Sussman, M. R.; Ane, J. M.; Coon, J. J. Large-scale phosphoprotein analysis in Medicago truncatula roots provides insight into in vivo kinase activity in legumes Plant Physiol. 2010, 152 (1) 19-28
28. Jaillais, Y.; Hothorn, M.; Belkhadir, Y.; Dabi, T.; Nimchuk, Z. L.; Meyerowitz, E. M.; Chory, J. Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor Genes Dev. 2011, 25 (3) 232-7
29. Ichimura, K.; Mizoguchi, T.; Yoshida, R.; Yuasa, T.; Shinozaki, K. Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6 Plant J. 2000, 24 (5) 655-65 (Pubitemid 32041919)
30. Nuhse, T. S.; Peck, S. C.; Hirt, H.; Boller, T. Microbial elicitors induce activation and dual phosphorylation of the Arabidopsis thaliana MAPK 6 J. Biol. Chem. 2000, 275 (11) 7521-6 (Pubitemid 30159648)
31. Zhang, Y.; Wolf-Yadlin, A.; Ross, P. L.; Pappin, D. J.; Rush, J.; Lauffenburger, D. A.; White, F. M. Time-resolved mass spectrometry of tyrosine phosphorylation sites in the epidermal growth factor receptor signaling network reveals dynamic modules Mol. Cell. Proteomics 2005, 4 (9) 1240-50 (Pubitemid 41448712)
32. Boersema, P. J.; Foong, L. Y.; Ding, V. M.; Lemeer, S.; van Breukelen, B.; Philp, R.; Boekhorst, J.; Snel, B.; den Hertog, J.; Choo, A. B.; Heck, A. J. In-depth qualitative and quantitative profiling of tyrosine phosphorylation using a combination of phosphopeptide immunoaffinity purification and stable isotope dimethyl labeling Mol. Cell. Proteomics 2010, 9 (1) 84-99
33. Rikova, K.; Guo, A.; Zeng, Q.; Possemato, A.; Yu, J.; Haack, H.; Nardone, J.; Lee, K.; Reeves, C.; Li, Y.; Hu, Y.; Tan, Z.; Stokes, M.; Sullivan, L.; Mitchell, J.; Wetzel, R.; Macneill, J.; Ren, J. M.; Yuan, J.; Bakalarski, C. E.; Villen, J.; Kornhauser, J. M.; Smith, B.; Li, D.; Zhou, X.; Gygi, S. P.; Gu, T. L.; Polakiewicz, R. D.; Rush, J.; Comb, M. J. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer Cell 2007, 131 (6) 1190-203 (Pubitemid 350235027)
34. Boersema, P. J.; Raijmakers, R.; Lemeer, S.; Mohammed, S.; Heck, A. J. Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics Nat. Protoc. 2009, 4 (4) 484-94
35. Oh, M. H.; Wang, X.; Kota, U.; Goshe, M. B.; Clouse, S. D.; Huber, S. C. Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassinosteroid signaling in Arabidopsis Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (2) 658-63
36. Chinchilla, D.; Zipfel, C.; Robatzek, S.; Kemmerling, B.; Nurnberger, T.; Jones, J. D. G.; Felix, G.; Boller, T. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence Nature 2007, 448 (7152) 497-500 (Pubitemid 47123516)
37. Cui, H.; Xiang, T.; Zhou, J. M. Plant immunity: a lesson from pathogenic bacterial effector proteins Cell Microbiol. 2009, 11 (10) 1453-61
38. Segonzac, C.; Zipfel, C. Activation of plant pattern-recognition receptors by bacteria Curr. Opin. Microbiol. 2011, 14 (1) 54-61
39. He, P.; Shan, L.; Sheen, J. Elicitation and suppression of microbe-associated molecular pattern-triggered immunity in plant-microbe interactions Cell Microbiol. 2007, 9 (6) 1385-96 (Pubitemid 46774012)
40. Shan, L.; He, P.; Sheen, J. Intercepting Host MAPK Signaling Cascades by Bacterial Type III Effectors Cell Host Microbe 2007, 1 (3) 167-174 (Pubitemid 46706366)
41. Pitzschke, A.; Schikora, A.; Hirt, H. MAPK cascade signalling networks in plant defence Curr. Opin. Plant Biol. 2009, 12 (4) 421-6
42. Colcombet, J.; Hirt, H. Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes Biochem. J. 2008, 413 (2) 217-26
43. Rodriguez, M. C.; Petersen, M.; Mundy, J. Mitogen-activated protein kinase signaling in plants Annu. Rev. Plant Biol. 2010, 61, 621-49
44. Menke, F. L.; van Pelt, J. A.; Pieterse, C. M.; Klessig, D. F. Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis Plant Cell 2004, 16 (4) 897-907 (Pubitemid 38459210)
45. Asai, T.; Tena, G.; Plotnikova, J.; Willmann, M. R.; Chiu, W. L.; Gomez-Gomez, L.; Boller, T.; Ausubel, F. M.; Sheen, J. MAP kinase signalling cascade in Arabidopsis innate immunity Nature 2002, 415 (6875) 977-83 (Pubitemid 34193435)
46. van den Toorn, H. W.; Munoz, J.; Mohammed, S.; Raijmakers, R.; Heck, A. J.; van Breukelen, B. RockerBox: analysis and filtering of massive proteomics search results J. Proteome Res. 2011, 10 (3) 1420-4
47. Yergey, J. A. A general approach to calculating isotopic distributions for mass spectrometry Int. J. Mass Spectrom. Ion Phys. 1983, 52 (2-3) 337-49
48. Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N. S.; Wang, J. T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: a software environment for integrated models of biomolecular interaction networks Genome Res. 2003, 13 (11) 2498-504 (Pubitemid 37428274)
49. Maere, S.; Heymans, K.; Kuiper, M. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks Bioinformatics 2005, 21 (16) 3448-9 (Pubitemid 41222459)
50. Heazlewood, J. L.; Durek, P.; Hummel, J.; Selbig, J.; Weckwerth, W.; Walther, D.; Schulze, W. X. PhosPhAt: a database of phosphorylation sites in Arabidopsis thaliana and a plant-specific phosphorylation site predictor Nucleic Acids Res. 2008, 36 (Database issue) D1015-21
51. Durek, P.; Schmidt, R.; Heazlewood, J. L.; Jones, A.; MacLean, D.; Nagel, A.; Kersten, B.; Schulze, W. X. PhosPhAt: the Arabidopsis thaliana phosphorylation site database. An update Nucleic Acids Res. 2010, 38 (Database issue) D828-34
52. Boekhorst, J.; Boersema, P. J.; Tops, B. B.; van Breukelen, B.; Heck, A. J.; Snel, B. Evaluating experimental bias and completeness in comparative phosphoproteomics analysis PLoS One 2011, 6 (8) e23276
53. Nuhse, T. S.; Stensballe, A.; Jensen, O. N.; Peck, S. C. Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database Plant Cell 2004, 16 (9) 2394-405 (Pubitemid 39247080)
54. Gish, L. A.; Clark, S. E. The RLK/Pelle family of kinases Plant J. 2011, 66 (1) 117-27
55. Oh, M. H.; Clouse, S. D.; Huber, S. C. Tyrosine phosphorylation in brassinosteroid signaling Plant Signal. Behav. 2009, 4, 12
56. Oh, M. H.; Wang, X.; Wu, X.; Zhao, Y.; Clouse, S. D.; Huber, S. C. Autophosphorylation of Tyr-610 in the receptor kinase BAK1 plays a role in brassinosteroid signaling and basal defense gene expression Proc. Natl. Acad. Sci. U.S.A. 2010, 107 (41) 17827-32
57. Jonak, C.; Okresz, L.; Bogre, L.; Hirt, H. Complexity, cross talk and integration of plant MAP kinase signalling Curr. Opin. Plant Biol. 2002, 5 (5) 415-24 (Pubitemid 34961404)
58. Group, M.; Ichimura, K.; Shinozaki, K.; Tena, G.; Sheen, J.; Henry, Y.; Champion, A.; Kreis, M.; Zhang, S.; Hirt, H.; Wilson, C.; Heberle-Bors, E.; Ellis, B. E.; Morris, P. C.; Innes, R. W.; Ecker, J. R.; Scheel, D.; Klessig, D. F.; Machida, Y.; Mundy, J.; Ohashi, Y.; Walker, J. C. Mitogen-activated protein kinase cascades in plants: a new nomenclature Trends Plant Sci. 2002, 7 (7) 301-8 (Pubitemid 36726514)
59. Petersen, M.; Brodersen, P.; Naested, H.; Andreasson, E.; Lindhart, U.; Johansen, B.; Nielsen, H. B.; Lacy, M.; Austin, M. J.; Parker, J. E.; Sharma, S. B.; Klessig, D. F.; Martienssen, R.; Mattsson, O.; Jensen, A. B.; Mundy, J. Arabidopsis map kinase 4 negatively regulates systemic acquired resistance Cell 2000, 103 (7) 1111-20 (Pubitemid 32037397)
60. Meszaros, T.; Helfer, A.; Hatzimasoura, E.; Magyar, Z.; Serazetdinova, L.; Rios, G.; Bardoczy, V.; Teige, M.; Koncz, C.; Peck, S.; Bogre, L. The Arabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellin Plant J. 2006, 48 (4) 485-98 (Pubitemid 44673251)
61. Suarez-Rodriguez, M. C.; Adams-Phillips, L.; Liu, Y.; Wang, H.; Su, S. H.; Jester, P. J.; Zhang, S.; Bent, A. F.; Krysan, P. J. MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants Plant Physiol. 2007, 143 (2) 661-9 (Pubitemid 46940960)
62. Li, H.; Xu, H.; Zhou, Y.; Zhang, J.; Long, C.; Li, S.; Chen, S.; Zhou, J. M.; Shao, F. The phosphothreonine lyase activity of a bacterial type III effector family Science 2007, 315 (5814) 1000-3 (Pubitemid 46281190)
63. Zhang, J.; Shao, F.; Li, Y.; Cui, H.; Chen, L.; Li, H.; Zou, Y.; Long, C.; Lan, L.; Chai, J.; Chen, S.; Tang, X.; Zhou, J. M. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants Cell Host Microbe 2007, 1 (3) 175-85 (Pubitemid 46706361)
64. Takahashi, F.; Mizoguchi, T.; Yoshida, R.; Ichimura, K.; Shinozaki, K. Calmodulin-dependent activation of MAP kinase for ROS homeostasis in Arabidopsis Mol. Cell 2011, 41 (6) 649-60
65. Schwessinger, B.; Roux, M.; Kadota, Y.; Ntoukakis, V.; Sklenar, J.; Jones, A.; Zipfel, C. Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1 PLoS Genet. 2011, 7 (4) e1002046
66. Doczi, R.; Brader, G.; Pettko-Szandtner, A.; Rajh, I.; Djamei, A.; Pitzschke, A.; Teige, M.; Hirt, H. The Arabidopsis Mitogen-Activated Protein Kinase Kinase MKK3 Is Upstream of Group C Mitogen-Activated Protein Kinases and Participates in Pathogen Signaling Plant Cell 2007, tpc.106.050039
67. Bindschedler, L. V.; Palmblad, M.; Cramer, R. Hydroponic isotope labelling of entire plants (HILEP) for quantitative plant proteomics; an oxidative stress case study Phytochemistry 2008, 69 (10) 1962-72
68. Gruhler, A.; Schulze, W. X.; Matthiesen, R.; Mann, M.; Jensen, O. N. Stable isotope labeling of Arabidopsis thaliana cells and quantitative proteomics by mass spectrometry Mol. Cell. Proteomics 2005, 4 (11) 1697-709 (Pubitemid 41749263)