Improvement of phosphoproteome analyses using FAIMS and decision tree fragmentation. Application to the insulin signaling pathway in drosophila melanogaster S2 cells

Journal of Proteome Research

Volumn 11, Issue 2, 2012, Pages 927-940

  Bridon, Gaëlle ^a,b   Bonneil, Eric ^a   Muratore Schroeder, Tara ^a,c   Caron Lizotte, Olivier ^a   Thibault, Pierre ^a,b  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c Thermo Fisher Scientific   (United States)

Author keywords

casein kinase 2; decision tree fragmentation; FAIMS; insulin stimulation; Orbitrap; phosphorylation; quantitative proteomics; titanium dioxide

Indexed keywords

INSULIN; PHOSPHOPEPTIDE; TITANIUM DIOXIDE;

ARTICLE; COLLISIONALLY ACTIVATED DISSOCIATION; CONTROLLED STUDY; DECISION TREE; DROSOPHILA MELANOGASTER; ELECTRON TRANSPORT; FIELD ASYMMETRIC WAVEFORM ION MOBILITY SPECTROMETRY; FRAGMENTATION REACTION; INSECT CELL; ION MOBILITY SPECTROMETRY; ISOMER; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PHOSPHOPROTEOMICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; SIGNAL TRANSDUCTION;

ALGORITHMS; AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CHROMATOGRAPHY, LIQUID; CLUSTER ANALYSIS; DECISION TREES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; INSULIN; MOLECULAR SEQUENCE DATA; PHOSPHOPEPTIDES; PHOSPHOPROTEINS; PROTEOME; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-AKT; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

DROSOPHILA MELANOGASTER;

EID: 84856675258     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200722s     Document Type: Article

References (54)

1. Kleinnijenhuis, A. J.; Kjeldsen, F.; Kallipolitis, B.; Haselmann, K. F.; Jensen, O. N. Analysis of histidine phosphorylation using tandem MS and ion-electron reactions Anal. Chem. 2007, 79 (19) 7450-7456
2. Brognard, J.; Hunter, T. Protein kinase signaling networks in cancer Curr. Opin. Genet. Dev. 2011, 21 (1) 4-11
3. Moser, K.; White, F. M. Phosphoproteomic analysis of rat liver by high capacity IMAC and LC-MS/MS J. Proteome Res. 2006, 5, 98-104
4. Ndassa, Y. M.; Orsi, C.; Marto, J. A.; Chen, S.; Ross, M. M. Improved immobilized metal affinity chromatography for large-scale phosphoproteomics applications J. Proteome Res. 2006, 5 (10) 2789-2799
5. Tsai, C. F.; Wang, Y. T.; Chen, Y. R.; Lai, C. Y.; Lin, P. Y.; Pan, K. T.; Chen, J. Y.; Khoo, K. H.; Chen, Y. J. Immobilized metal affinity chromatography revisited: pH/acid control toward high selectivity in phosphoproteomics J. Proteome Res. 2008, 7 (9) 4058-4069
6. Ye, J.; Zhang, X.; Young, C.; Zhao, X.; Hao, Q.; Cheng, L.; Jensen, O. N. Optimized IMAC-IMAC protocol for phosphopeptide recovery from complex biological samples J. Proteome Res. 2010, 9 (7) 3561-3573
7. Hilger, M.; Bonaldi, T.; Gnad, F.; Mann, M. System-wide analysis of a phosphatase knock down by quantitative proteomics and phosphoproteomics Mol. Cell. Proteomics 2009, 8 (8) 1908-1920
8. 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 (3) 635-648
9. Trost, M.; English, L.; Lemieux, S.; Courcelles, M.; M., D.; P., T. The phagosomal proteome in interferon-g-activated macrophages Immunity 2009, 30 (1) 143-154
10. Thingholm, T. E.; Jensen, O. N.; Robinson, P. J.; Larsen, M. R. SIMAC (sequential elution from IMAC), a phosphoproteomics strategy for the rapid separation of monophosphorylated from multiply phosphorylated peptides Mol. Cell Proteomics 2008, 7 (4) 661-671
11. Lemeer, S.; Heck, A. J. The phosphoproteomics data explosion Curr. Opin. Chem. Biol. 2009, 13 (4) 414-420
12. Zhang, H.; Zha, X.; Tan, Y.; Hornbeck, P. V.; Mastrangelo, A. J.; Alessi, D. R.; Polakiewicz, R. D.; Comb, M. J. Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs J. Biol. Chem. 2002, 277 (42) 39379-39387
13. Højlund, K.; Bowen, B. P.; Hwang, H.; Flynn, C. R.; Madireddy, L.; Geetha, T.; Langlais, P.; Meyer, C.; Mandarino, L. J.; Yi, Z. In vivo phosphoproteome of human skeletal muscle revealed by phosphopeptide enrichment and HPLC-ESI-MS/MS J. Proteome Res. 2009, 8 (11) 4954-4965
14. Nie, S.; Dai, J.; Ning, Z. B.; Cao, X. J.; Sheng, Q. H.; Zeng, R. Comprehensive profiling of phosphopeptides based on anion exchange followed by flow-through enrichment with titanium dioxide (AFET) J. Proteome Res. 2010, 9 (9) 4585-4594
15. Swaney, D. L.; McAlister, G. C.; Coon, J. J. Decision tree driven tandem mass spectrometry for shotgun proteomics Nat. Methods 2008, 5 (11) 959-964
16. Barnett, D. A.; Ding, L.; Ells, B.; Purves, R. W.; Guevremont, R. Tandem mass spectra of tryptic peptides at signal-to-background ratios approaching unity using electrospray ionization high-field asymmetric waveform ion mobility spectrometry/hybrid quadrupole time-of-flight mass spectrometry Rapid Commun. Mass Spectrom. 2002, 16 (7) 676-680
17. Barnett, D. A.; Ells, B.; Guevremont, R.; Purves, R. W. Application of ESI-FAIMS-MS to the analysis of tryptic peptides J. Am. Soc. Mass Spectrom. 2002, 13 (11) 1282-1291
18. Canterbury, J. D.; Yi, X.; Hoopmann, M. R.; MacCoss, M. J. Assessing the dynamic range and peak capacity of nanoflow LC-FAIMS-MS on an ion trap mass spectrometer for proteomics Anal. Chem. 2008, 80 (18) 6888-6897
19. Merenbloom, S. I.; Koeniger, S. L.; Valentine, S. J.; Plasencia, M. D.; Clemmer, D. E. IMS-IMS and IMS-IMS-IMS/MS for separating peptide and protein fragment ions Anal. Chem. 2006, 78 (8) 2802-2809
20. Saba, J.; Bonneil, E.; Pomies, C.; Eng, K.; Thibault, P. Enhanced sensitivity in proteomics experiments using FAIMS coupled with a hybrid linear ion trap/Orbitrap mass spectrometer J. Proteome Res. 2009, 8 (7) 3355-3366
21. Valentine, S. J.; Ewing, M. A.; Dilger, J. M.; Glover, M. S.; Geromanos, S.; Hughes, C.; Clemmer, D. E. Using ion mobility data to improve peptide identification: intrinsic amino acid size parameters J. Proteome Res. 2011, 10 (5) 2318-2329
22. Venne, K.; Bonneil, E.; Eng, K.; Thibault, P. Improvement in peptide detection for proteomics analyses using NanoLC-MS and high-field asymmetry waveform ion mobility mass spectrometry Anal. Chem. 2005, 77 (7) 2176-2186
23. Shvartsburg, A. A.; Creese, A. J.; Smith, R. D.; Cooper, H. J. Separation of peptide isomers with variant modified sites by high-resolution differential ion mobility spectrometry Anal. Chem. 2010, 82 (19) 8327-8334
24. Shvartsburg, A. A.; Mashkevich, S. V.; Smith, R. D. Feasibility of higher-order differential ion mobility separations using new asymmetric waveforms J. Phys. Chem. A 2006, 110 (8) 2663-2673
25. Tang, K.; Li, F.; Shvartsburg, A. A.; Strittmatter, E. F.; Smith, R. D. Two-dimensional gas-phase separations coupled to mass spectrometry for analysis of complex mixtures Anal. Chem. 2005, 77 (19) 6381-6388
26. Xia, Y. Q.; Wu, S. T.; Jemal, M. LC-FAIMS-MS/MS for quantification of a peptide in plasma and evaluation of FAIMS global selectivity from plasma components Anal. Chem. 2008, 80 (18) 7137-43
27. Xuan, Y.; Creese, A. J.; Horner, J. A.; Cooper, H. J. High-field asymmetric waveform ion mobility spectrometry (FAIMS) coupled with high-resolution electron transfer dissociation mass spectrometry for the analysis of isobaric phosphopeptides Rapid Commun. Mass Spectrom. 2009, 23, 1963-1969
28. Schvartsburg, A. A.; Creese, A. J.; Smith, R. D.; Cooper, H. J. Separation of peptide isomers with variant modified sites by high-resolution differential ion mobility spectrometry Anal. Chem. 2010, 82 (19) 8327-8334
29. Shvartsburg, A. A.; Danielson, W. F.; Smith, R. D. High-resolution differential ion mobility separations using helium-rich gases Anal. Chem. 2010, 82 (6) 2456-62
30. Elias, J. E.; Gygi, S. P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Nat. Methods 2007, 4 (3) 207-214
31. Courcelles, M.; Lemieux, S.; Voisin, L.; Meloche, S.; Thibault, P. ProteoConnections: a bioinformatics platform to facilitate proteome and phosphoproteome analyses Proteomics 2011, 11, 2654-2671
32. 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 (3) 635-648
33. Schwartz, D.; Gygi, S. P. An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets Nat. Biotechnol. 2005, 11 (23) 1391-1398
34. Kearney, P.; Thibault, P. Bioinformatics meets proteomics - bridging the gap between mass spectrometry data analysis and cell biology J. Bioinform. Comput. Biol. 2003, 1 (1) 183-200
35. Bendall, S. C.; Hughes, C.; Campbell, J. L.; Stewart, M. H.; Pittock, P.; Liu, S.; Bonneil, E.; Thibault, P.; Bhatia, M.; Lajoie, G. A. An enhanced mass spectrometry approach reveals human embryonic stem cell growth factors in culture Mol. Cell Proteomics 2009, 8 (3) 421-432
36. Bonneil, E.; Brunet, S.; Jaquinod, M.; Hui, J. P. M.; Forest, A.; Thibault, P. Mass Spectrometry-Based Proteomics Analyses of Integral Membrane Proteins. In Sample Preparation in Biological Mass Spectrometry; Ivanov, A. R.; Lazarev, A. V., Eds.; Springer Science: New York, in press.
37. Singer, D.; Kuhlmann, J.; Muschket, M.; Hoffmann, R. Separation of multiphosphorylated peptide isomers by hydrophilic interaction chromatography on an aminopropyl phase Anal. Chem. 2010, 82 (15) 6409-6414
38. Kwon, H. B.; Kim, S. H.; Kim, S. E.; Jang, I. H.; Ahn, Y.; Lee, W. J.; Choi, K. Y. Drosophila extracellular signal-regulated kinase involves the insulin-mediated proliferation of Schneider cells J. Biol. Chem. 2002, 277 (17) 14853-14858
39. Kim, S. E.; Cho, J. Y.; Kim, K. S.; Lee, S. J.; Lee, K. H.; Choi, K. Y. Drosophila PI3 kinase and Akt involved in insulin-stimulated proliferation and ERK pathway activation in Schneider cells Cell Signal. 2004, 16 (11) 1309-1317
40. Taniguchi, C. M.; Kondo, T.; Sajan, M.; Luo, J.; Bronson, R.; Asano, T.; Farese, R.; Cantley, L. C.; Kahn, C. R. Divergent regulation of hepatic glucose and lipid metabolism by phosphoinositide 3-kinase via Akt and PKClambda/zeta Cell Metab. 2006, 3 (5) 343-353
41. Kular, G.; Loubtchenkov, M.; Swigart, P.; Whatmore, J.; Ball, A.; Cockcroft, S.; Wetzker, R. Co-operation of phosphatidylinositol transfer protein with phosphoinositide 3-kinase gamma in the formylmethionyl- leucylphenylalanine-dependent production of phosphatidylinositol 3,4,5-trisphosphate in human neutrophils Biochem. J. 1997, 325 (Pt 2) 299-301
42. Xu, A. W.; Kaelin, C. B.; Takeda, K.; Akira, S.; Schwartz, M. W.; Barsh, G. S. PI3K integrates the action of insulin and leptin on hypothalamic neurons J. Clin. Invest. 2005, 115 (4) 951-958
43. Britton, J. S.; Lockwood, W. K.; Li, L.; Cohen, S. M.; Edgar, B. A. Drosophila's insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions Dev. Cell 2002, 2 (2) 239-249
44. Frias, M. A.; Thoreen, C. C.; Jaffe, J. D.; Schroder, W.; Sculley, T.; Carr, S. A.; Sabatini, D. M. mSin1 is necessary for Akt/PKB phosphorylation, and its isoforms define three distinct mTORC2s Curr. Biol. 2006, 16 (18) 1865-1870
45. Prescott, G. R.; Jenkins, R. E.; Walsh, C. M.; Morgan, A. Phosphorylation of cysteine string protein on Serine 10 triggers 14-3-3 protein binding Biochem. Biophys. Res. Commun. 2008, 377 (3) 809-814
46. Donkor, J.; Sariahmetoglu, M.; Dewald, J.; Brindley, D. N.; Reue, K. Three mammalian lipins act as phosphatidate phosphatases with distinct tissue expression patterns J. Biol. Chem. 2007, 282 (6) 3450-3457
47. Huffman, T. A.; Mothe-Satney, I.; Lawrence, J. C., Jr. Insulin-stimulated phosphorylation of lipin mediated by the mammalian target of rapamycin Proc. Natl. Acad. Sci. U. S. A. 2002, 99 (2) 1047-1052
48. Peterfy, M.; Harris, T. E.; Fujita, N.; Reue, K. Insulin-stimulated interaction with 14-3-3 promotes cytoplasmic localization of lipin-1 in adipocytes J. Biol. Chem. 2010, 285 (6) 3857-3864
49. Kim, M.; Jung, J.; Lee, K. Roles of ERK, PI3 kinase, and PLC-gamma pathways induced by overexpression of translationally controlled tumor protein in HeLa cells Arch. Biochem. Biophys. 2009, 485 (1) 82-87
50. Yang, J. T.; Laymon, R. A.; Goldstein, L. S. A three-domain structure of kinesin heavy chain revealed by DNA sequence and microtubule binding analyses Cell 1989, 56 (5) 879-889
51. Sossey-Alaoui, K.; Head, K.; Nowak, N.; Cowell, J. K. Genomic organization and expression profile of the human and mouse WAVE gene family Mamm. Genome 2003, 14 (5) 314-322
52. Welsh, G. I.; Stokes, C. M.; Wang, X.; Sakaue, H.; Ogawa, W.; Kasuga, M.; Proud, C. G. Activation of translation initiation factor eIF2B by insulin requires phosphatidyl inositol 3-kinase FEBS Lett. 1997, 410 (2-3) 418-422
53. Kim, S. J.; Kahn, C. R. Insulin regulation of mitogen-activated protein kinase kinase (MEK), mitogen-activated protein kinase and casein kinase in the cell nucleus: a possible role in the regulation of gene expression Biochem. J. 1997, 323 (Pt 3) 621-627
54. Sommercorn, J.; Mulligan, J. A.; Lozeman, F. J.; Krebs, E. G. Activation of casein kinase II in response to insulin and to epidermal growth factor Proc. Natl. Acad. Sci. U. S. A. 1987, 84 (24) 8834-8838