Proteomics approaches to understand protein phosphorylation in pathway modulation

Current Opinion in Plant Biology

Volumn 13, Issue 3, 2010, Pages 279-286

  Schulze, Waltraud X ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEOME; VEGETABLE PROTEIN;

MASS SPECTROMETRY; METABOLISM; PHOSPHORYLATION; PLANT; PROTEIN PROCESSING; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION;

MASS SPECTROMETRY; PHOSPHORYLATION; PLANT PROTEINS; PLANTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; PROTEOMICS; SIGNAL TRANSDUCTION;

EID: 77955873040     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2009.12.008     Document Type: Review

References (66)

1. Brandman O, Meyer T: Feedback loops shape cellular signals in space and time. Science 2008, 322:390-395.
2. Initiative TAG: Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000, 408:796-816.
3. Manning G, Whyte DB, Martinez R, Hunter R, Hunter T, Sudarsanam S: The protein kinase complement of the human genome. Science 2002, 298:1912-1914.
4. Jörgensen C, Linding R: Directional and quantitative phosphorylation networks. Brief Functional Genomics and Proteomics 2008, 7:17-26.
5. Mayya V, Han DK: Phosphoproteomics by mass spectrometry: insights, implications, applications and limitations. Expert Review of Proteomics 2009, 6:605-618.
6. Toroser D, Athwal GS, Huber SC: Site-specific regulatory interaction between spinach leaf sucrose-phosphate synthase and 14-3-3 proteins. FEBS Letters 1998, 435:110-114.
7. Kaiser WM, Huber SC: Post-translational regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers. Journal of Experimental Botany 2001, 52:1981-1989.
8. Steen H, Jebanathirajah JA, Rush J, Morrice N, Kirschner MW: Phosphorylation analysis by mass spectrometry: myths, facts and the consequence for qualitative and quantitative measurements. Molecular and Cellular Proteomics 2006, 5:172-181.
9. Villén J, Beausoleil SA, Gygi SP: Evaluation of the utility of neutral-loss-dependent MS3 strategies in large-scale phosphorylation analysis. Proteomics 2008, 8:4444-4452.
10. Zhang Y, Ficarro SB, Li S, Marto JA: Optimized Orbitrap HCD for quantitative analysis of phosphopeptides. Journal of the American Society of Mass Spectrometry 2009, 20:1425-1434.
11. Molina H, Horn DM, Tang N, Mathivanan S, Pandey A: Global proteomic profiling of phosphopeptides using electron transfer dissociation tandem mass spectrometry. In Proceedings of the National Academy of Sciences of the United States of America 2007, 104:2199-2204.
12. Lehmann WD, Kruger R, Salek M, Hung CW, Wolschin F, Weckwerth W: Neutral loss-based phosphopeptide recognition: a collection of caveats. Journal of Proteome Research 2007, 6:2866-2873.
13. Nühse TS, Stensballe A, Jensen ON, Peck SC: Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 2004, 16:2394-2405.
14. 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. Molecular Systems Biology 2008, 4:e1-7.
15. Reiland S, Messerli G, Baerenfäller K, Gerrits B, Endler A, Grossmann J, GruissemW, Baginsky S: Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiology 2009, 150:889-903.
16. Grimsrud PA, den Os D, Wenger CD, Swaney DL, Schwartz D, Sussman MR, Ane JM, Coon JJ: Large-scale phosphoprotein analysis in Medicago truncatula roots provides insight into in vivo kinase activity in legumes. Plant Physiology 2009, 152:19-28.
17. Tan F, Li G, Chitteti BR, Peng Z: Proteome and phosphoproteome analysis of chromatin associated proteins in rice (Oryza sativa). Proteomics 2007, 7:4511-4527.
18. Jones AM, Maclean D, Studholme DJ, Serna-Sanz A, Andreasson E, Rathjen JP, Peck SC: Phosphoproteomic analysis of nuclei-enriched fractions from Arabidopsis thaliana. Journal of Proteomics 2009, 72:439-451.
19. Whiteman S-A, Serazetdinova L, Jones AM, Sanders D, Rathjen J, Peck SC, Maathuis FJM: Identification of novel proteins and phosphorylation sites in a tonoplast enriched membrane fraction of Arabidopsis thaliana. Proteomics 2008, 8:3536-3547.
20. Schneider T, Schellenberg M, Meyer S, Keller F, Gehrig P, Riedel K, Lee Y, Eberl L, Martinoia E: Quantitative detection of changes in the leaf-mesophyll tonoplast proteome in dependency of a cadmium exposure of barley (Hordeum vulgare L.) plants. Proteomics 2009, 9:2668-2677.
21. Benschop JJ, Mohammed S, O'Flaherty M, Heck AJ, Slijper M, Menke FL: Quantitative phospho-proteomics of early elicitor signalling in Arabidopsis. Molecular and Cellular Proteomics 2007, 6:1705-1713.
22. Li H, Wong WS, Zhu L, Guo HW, Ecker J, Li N: Phosphoproteomic analysis of ethylene-regulated protein phosphorylation in etiolated seedlings of Arabidopsis mutant ein2 using two dimensional separations coupled with a hybrid quad rupole time-of-flight mass spectrometer. Proteomics 2009, 9:1646-1661.
23. Nühse TS, Bottrill AR, Jones AM, Peck SC: Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant Journal 2007, 51:931-940.
24. NiittyläT, Fuglsang AT, Palmgren MG, Frommer WB, Schulze WX: Temporal analysis of sucrose-induced phosphorylation changes in plasma membrane proteins of Arabidopsis. Molecular and Cellular Proteomics 2007, 6:1711-1726.
25. de la Fuente van Bentem S, Anrather D, Dohnal I, Roitinger E, Csaszar E, Joore J, Buijnink J, Carreri A, Forzani C, Lorkovic ZJ et al.: Site-specific phosphorylation profiling of Arabidopsis proteins by mass spectrometry and peptide chip analysis. Journal of Proteome Research 2008, 7:2458-2470.
26. de la Fuente van Bentem S, Anrather D, Roitinger E, Djamei A, Hufnagl T, Barta A, Csaszar E, Dohnal I, Lecourieux D, Hirt H: Phosphoproteomics reveals extensive in vivo phosphorylation of Arabidopsis proteins involved in RNA metabolism. Nucleic Acids Research 2006, 34:3267-3278.
27. Stulemejer IJ, Joosten MH, Jensen ON: Quantitative phosphoproteomics of tomato mounting a hypersensitive response reveals a swift suppression of photosynthetic activity and a differential role for hsp90 isoforms. Journal of Proteome Research 2009, 8:1168-1182.
28. Durek P, Schmidt R, Heazlewood JL, Jones A, MacLean D, Nagel A, Kersten B, Schulze WX: PhosPhAt: The Arabidopsis thaliana phosphorylation site database. An update. Nucleic Acids Research 2010, 38:D828-D834.
29. Ubersax JA, Ferrell JEJ: Mechanisms of specificity in protein phosphorylation. Nature Reviews Molecular Cell Biology 2007, 8:530-541.
30. Piques MC, Schulze WX, Höhne M, Gibon Y, Rohwer J, Stitt M: Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis. Molecular Systems Biology 2009, 5:E1-E17.
31. Lienhard GE: Non-functional phosphorylations? Trends in Biochemical Science 2008, 33:351-352.
32. Lanquar V, Loque D, Hörmann F, Yuan L, Bohner A, Engelsberger WR, Lalonde S, Schulze WX, Von Wiren N, Frommer WB: Feedback inhibition of ammonium uptake by a phospho-dependent allosteric mechanism in Arabidopsis. The Plant Cell 2009, 21:3610-3622.
33. Usadel B, Obayashi T, Mutwil M, Giorgi FM, Bassel GW, Tanimoto M, Chow A, Steinhauser D, Persson S, Provart NJ: Coexpression tools for plant biology: opportunities for hypothesis generation and caveats. Plant, Cell and Environment 2009, 32:1633-1651.
34. Tang W, Deng Z, Oses-Prieto JA, Suzuki N, Zhu S, Zhang X, Burlingame AL, Wang ZY: Proteomics studies of brassinosteroid signal transduction using prefractionation and two-dimensional DIGE. Molecular and Cellular Proteomics 2008, 7:728-738.
35. Olsen JV, 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.
36. Steen H, Jebanathirajah JA, Springer M, Kirschner MW: Stable isotope-free relative and absolute quantitation of protein phosphorylation stoichiometry by MS. In Proceedings of the National Academy of Sciences of the United States of America 2005, 102:3948-3953.
37. Schwartz D, Gygi SP: An iterative statistical approach to the identification of protein phosphorylation motifs from largescale data sets. Nature Biotechnology 2005, 23:1391-1398.
38. Vlad F, Turk BE, Peynot P, Leung J, Merlot S: A versatile strategy to define the phosphorylation preferences of plant protein kinases and screen for putative substrates. Plant Journal 2008, 55:104-117.
39. Ptacek J, Devgan G, Michaud G, Zhu H, Zhu X, Fasolo J, Guo H, Jona G, Breitkreutz A, Sopko R et al.: Global analysis of protein phosphorylation in yeast. Nature 2005, 438:679-684.
40. Popescu SC, Popescu GV, Bachan S, Zhang Z, Gerstein M, Snyder M, Dinesh-Kumar SP: MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes and Development 2009, 23:80-92.
41. Glinski M, Weckwerth W: Differential multisite phosphorylation of the trehalose-6-phosphate synthase gene family in Arabidopsis thaliana: A mass spectrometry-based process for multiparallel peptide library phosphorylation analysis. Molecular and Cellular Proteomics 2005, 4:1614-1625.
42. Fiil BK, Petersen K, Petersen M, Mundy J: Gene regulation by MAP kinase cascades. Current Opinion in Plant Biology 2009, 12:615-621.
43. Pitzschke A, Schikora A, Hirt H: MAPK cascade signalling networks in plant defence. Current Opinion in Plant Biology 2009, 12:421-426.
44. Halford NG, Hey SJ: Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants. Biochemical Journal 2009, 419:247-259.
45. Shin R, Alvarez S, Burch AY, Jez JM, Schachtman DP: Phosphoproteomic identification of targets of the Arabidopsis sucrose nonfermenting-like kinase SnRK2.8 reveals a connection to metabolic processes. In Proceedings of the National Academy of Sciences of the United States of America 2007, 104:6460-6465.
46. Fragoso S, Espíndola L, Páez-Valencia J, Gamboa A, Camacho Y, Martínez-Barajas E, Coello P: SnRK1 isoforms AKIN10 and AKIN11 are differentially regulated in Arabidopsis plants under phosphate starvation. Plant Physiology 2009, 149:1906-1916.
47. Ludwig AA, Romeis T, Jones JD: CDPK-mediated signalling pathways: specificity and cross-talk. Journal of Experimental Botany 2004, 55:181-188.
48. Weinl S, Kudla J: The CBL-CIPK Ca(2+)-decoding signaling network: function and perspectives. New Phytologist 2009, 2009:3.
49. Shiu S-H, Bleecker AB: Plant receptor-like kinase gene family: diversity, function, andsignaling. Science's STKE 2001, 113:1-13.
50. Kim TW, Guan S, Sun Y, Deng Z, Tang W, Shang JX, Sun Y, Burlingam A, Wang ZY: Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nature Cell Biology 2009, 11:1254-1260.
51. Chinchilla D, Boller T, Robatzek S: Flagellin signalling in plant immunity. Advances in Experimental Medicine and Biology 2007, 598:358-371.
52. Hardin SC, Larue CT, Oh MH, Jain V, Huber SC: Coupling oxidative signals to protein phosphorylation via methionine oxidation in Arabidopsis. Biochemical Journal 2009, 422:305-312.
53. Linding R, Jensen LJ, Ostheimer GJ, van Vugt MA, Jorgensen C, Miron IM, Diella F, Colwill K, Taylor L, Elder K et al.: Systematic discovery of in vivo phosphorylation networks. Cell 2007, 129:1415-1426.
54. Yang CY, Chang CH, Yu YL, Lin TC, Lee SA, Yen CC, Yang JM, Lai JM, Hong YR, Tseng TL et al.: PhosphoPOINT: a comprehensive human kinase interactome and phosphoprotein database. Bioinformatics 2008, 24:14-20.
55. Heazlewood JL, Verboom RE, Tonti-Filippini J, Small I, Millar AH: SUBA: the Arabidopsis subcellular database. Nucleic Acids Research 2007, 35:D213-D218.
56. Geisler-Lee J, O'Toole N, Ammar R, Provart NJ, Millar AH, Geisler M: A predicted interactome for Arabidopsis. Plant Physiology 2007, 145:317-329.
57. Bodenmiller B, Mueller LN, Mueller M, Domon B, Aebersold R: Reproducible isolation of distinct, overlapping segments of the phosphoproteome. Nature Methods 2007, 4:231-237.
58. Wolschin F, Lehmann U, Glinski M, Weckwerth W: An integrated strategy for identification and relative quantification of sitespecific protein phosphorylation using liquid chromatography coupled to MS2/MS3. Rapid Communications in Mass Spectrometry 2005, 19:3626-3632.
59. Hegeman AD, Harms AC, Sussman MR, Bunner AE, Harper JF: An isotope labeling strategy for quantifying the degree of phosphorylation at multiple sites in proteins. Journal of the American Society of Mass Spectrometry 2004, 15:647-653.
60. Ulintz PJ, Yocum AK, Bodenmiller B, Aebersold R, Andrews PC, Nesvizhskii A: Comparison of MS(2)-only, MSA, and MS(2)/MS(3) methodologies for phosphopeptide identification. Journal of Proteome Research 2009, 8:887-899.
61. Schroeder MJ, Shabanowitz J, Schwartz JC, Hunt DF, Coon JJ: A neutral loss activation method for improved phosphopeptide sequence analysis by quadrupole ion trap mass spectrometry. Analytical Chemistry 2004, 76:3590-3598.
62. Gao J, Agrawal GK, Thelen JJ, Xu D: P3DB: a plant protein phosphorylation database. Nucleic Acids Research 2009, 37:D960-D962.
63. Gnad F, Ren S, Cox J, Olsen JV, Macek B, Oroshi M, Mann M: PHOSIDA (phosphorylation site database): management, structural and evolutionary investigation, and prediction of phosphosites. Genome Biology 2007, 8:R250.
64. Gould CM, Diella F, Via A, Puntervoll P, Gemünd C, Chabanis-Davidson S, Michael S, Sayadi A, Bryne JC, Chica C et al.: ELM: the status of the 2010 eukaryotic linear motif resource. Nucleic Acids Research 2010, 38:D167-D180.
65. Bodenmiller B, Malmstrom J, Gerrits B, Campbell D, Lam H, Schmidt A, Rinner O, Müller LN, Shannon PT, Pedrioli PG et al.: PhosphoPep - a phosphoproteome resource for systems biology research in Drosophila Kc167 cells. Molecular Systems Biology 2007, 3:139-149.
66. Linding R, Jensen LJ, Pasculescu A, Olhovsky M, Colwill K, Bork P, Yaffe MB, Pawson T: NetworKIN: a resource for exploring cellular phosphorylation networks. Nucleic Acids Research 2007, 36:D695-696.