Sample preparation and analytical strategies for large-scale phosphoproteomics experiments

Seminars in Cell and Developmental Biology

Volumn 23, Issue 8, 2012, Pages 843-853

  Kanshin, Evgeny ^a,b   Michnick, Stephen ^b   Thibault, Pierre ^a,b  

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

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Affinity chromatography; Mass spectrometry; Phosphoproteomics; Quantitative proteomics

Indexed keywords

EID: 84868501812     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2012.05.005     Document Type: Review

References (127)

1. Hunter T. Signaling-2000 and beyond. Cell 2000, 100:113-127.
2. Lim Y.P. Mining the tumor phosphoproteome for cancer markers. Clinical Cancer Research 2005, 11:3163-3169.
3. Harsha H.C., Pandey A. Phosphoproteomics in cancer. Molecular Oncology 2010, 4:482-495.
4. Clark S.S., McLaughlin J., Timmons M., Pendergast A.M., Ben-Neriah Y., Dow L.W., et al. Expression of a distinctive BCR-ABL oncogene in Ph1-positive acute lymphocytic leukemia (ALL). Science (New York, NY) 1988, 239:775-777.
5. Schubbert S., Shannon K., Bollag G. Hyperactive Ras in developmental disorders and cancer. Nature Reviews 2007, 7:295-308.
6. Lincova E., Hampl A., Pernicova Z., Starsichova A., Krcmar P., Machala M., et al. Multiple defects in negative regulation of the PKB/Akt pathway sensitise human cancer cells to the antiproliferative effect of non-steroidal anti-inflammatory drugs. Biochemical Pharmacology 2009, 78:561-572.
7. Sweeney C., Miller J.K., Shattuck D.L., Carraway K.L. ErbB receptor negative regulatory mechanisms: implications in cancer. Journal of Mammary Gland Biology and Neoplasia 2006, 11:89-99.
8. Wilson K.S., Roberts H., Leek R., Harris A.L., Geradts J. Differential gene expression patterns in HER2/neu-positive and -negative breast cancer cell lines and tissues. The American Journal of Pathology 2002, 161:1171-1185.
9. Bourne H.R. GTPases: a family of molecular switches and clocks. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 1995, 349:283-289.
10. Bourne H.R. Signal transduction. Team blue sees red. Nature 1995, 376:727-729.
11. Manning G., Whyte D.B., Martinez R., Hunter T., Sudarsanam S. The protein kinase complement of the human genome. Science (New York, NY) 2002, 298:1912-1934.
12. Ubersax J.A., Ferrell J.E. Mechanisms of specificity in protein phosphorylation. Nature Reviews Molecular Cell Biology 2007, 8:530-541.
13. Roy J., Cyert M.S. Cracking the phosphatase code: docking interactions determine substrate specificity. Science Signaling 2009, 2:re9.
14. Breitkreutz A., Choi H., Sharom J.R., Boucher L., Neduva V., Larsen B., et al. A global protein kinase and phosphatase interaction network in yeast. Science (New York, NY) 2010, 328:1043-1046.
15. Levy E.D., Landry C.R., Michnick S.W. Cell signaling. Signaling through cooperation. Science (New York, NY) 2010, 328:983-984.
16. Landry C.R., Levy E.D., Michnick S.W. Weak functional constraints on phosphoproteomes. Trends in Genetics: TIG 2009, 25:193-197.
17. Gnad F., Forner F., Zielinska D.F., Birney E., Gunawardena J., Mann M. Evolutionary constraints of phosphorylation in eukaryotes, prokaryotes, and mitochondria. Molecular and Cellular Proteomics 2010, 9:2642-2653.
18. Miller M., Donat S., Rakette S., Stehle T., Kouwen T.R., Diks S.H., et al. Staphylococcal PknB as the first prokaryotic representative of the proline-directed kinases. PloS ONE 2010, 5:e9057.
19. Olsen J.V., Blagoev B., Gnad F., Macek B., Kumar C., Mortensen P., et al. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127:635-648.
20. Sickmann A., Meyer H.E. Phosphoamino acid analysis. Proteomics 2001, 1:200-206.
21. Reinders J., Sickmann A. State-of-the-art in phosphoproteomics. Proteomics 2005, 5:4052-4061.
22. Kalume D.E., Molina H., Pandey A. Tackling the phosphoproteome: tools and strategies. Current Opinion in Chemical Biology 2003, 7:64-69.
23. Johnson S.A., Hunter T. Kinomics: methods for deciphering the kinome. Nature Methods 2005, 2:17-25.
24. Wu R., Haas W., Dephoure N., Huttlin E.L., Zhai B., Sowa M.E., et al. A large-scale method to measure absolute protein phosphorylation stoichiometries. Nature Methods 2011, 8:677-683.
25. Ham B.M., Yang F., Jayachandran H., Jaitly N., Monroe M.E., Gritsenko M.A., et al. The influence of sample preparation and replicate analyses on HeLa Cell phosphoproteome coverage. Journal of Proteome Research 2008, 7:2215-2221.
26. Gruhler A., Olsen J.V., Mohammed S., Mortensen P., Faergeman N.J., Mann M., et al. Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Molecular and Cellular Proteomics 2005, 4:310-327.
27. Mann M., Ong S.E., Gronborg M., Steen H., Jensen O.N., Pandey A. Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends in Biotechnology 2002, 20:261-268.
28. Nagaraj N., D'Souza R.C., Cox J., Olsen J.V., Mann M. Feasibility of large-scale phosphoproteomics with higher energy collisional dissociation fragmentation. Journal of Proteome Research 2010, 9:6786-6794.
29. Syka J.E., Coon J.J., Schroeder M.J., Shabanowitz J., Hunt D.F. Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:9528-9533.
30. Swaney D.L., McAlister G.C., Coon J.J. Decision tree-driven tandem mass spectrometry for shotgun proteomics. Nature Methods 2008, 5:959-964.
31. Hornbeck P.V., Chabra I., Kornhauser J.M., Skrzypek E., Zhang B. PhosphoSite: a bioinformatics resource dedicated to physiological protein phosphorylation. Proteomics 2004, 4:1551-1561.
32. Diella F., Gould C.M., Chica C., Via A., Gibson T.J. Phospho.ELM: a database of phosphorylation sites-update 2008. Nucleic Acids Research 2008, 36:D240-D244.
33. Gnad F., Ren S., Cox J., Olsen J.V., Macek B., Oroshi M., et al. PHOSIDA (phosphorylation site database): management, structural and evolutionary investigation, and prediction of phosphosites. Genome Biology 2007, 8:R250.
34. Bodenmiller B., Campbell D., Gerrits B., Lam H., Jovanovic M., Picotti P., et al. PhosphoPep-a database of protein phosphorylation sites in model organisms. Nature Biotechnology 2008, 26:1339-1340.
35. Ovelleiro D., Carrascal M., Casas V., Abian J. LymPHOS: design of a phosphosite database of primary human T cells. Proteomics 2009, 9:3741-3751.
36. 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.
37. Steen H., Jebanathirajah J.A., Rush J., Morrice N., Kirschner M.W. Phosphorylation analysis by mass spectrometry: myths, facts, and the consequences for qualitative and quantitative measurements. Molecular and Cellular Proteomics 2006, 5:172-181.
38. Hunter T. When is a lipid kinase not a lipid kinase? When it is a protein kinase. Cell 1995, 83:1-4.
39. Boersema P.J., Mohammed S., Heck A.J. Phosphopeptide fragmentation and analysis by mass spectrometry. Journal of Mass Spectrometry 2009, 44:861-878.
40. Palumbo A.M., Smith S.A., Kalcic C.L., Dantus M., Stemmer P.M., Reid G.E. Tandem mass spectrometry strategies for phosphoproteome analysis. Mass Spectrometry Reviews 2011, 30:600-625.
41. D'Ambrosio C., Salzano A.M., Arena S., Renzone G., Scaloni A. Analytical methodologies for the detection and structural characterization of phosphorylated proteins. Journal of Chromatography 2007, 849:163-180.
42. Dunn J.D., Reid G.E., Bruening M.L. Techniques for phosphopeptide enrichment prior to analysis by mass spectrometry. Mass Spectrometry Reviews 2009, 29:29-54.
43. Morandell S., Stasyk T., Grosstessner-Hain K., Roitinger E., Mechtler K., Bonn G.K., et al. Phosphoproteomics strategies for the functional analysis of signal transduction. Proteomics 2006, 6:4047-4056.
44. Schmelzle K., White F.M. Phosphoproteomic approaches to elucidate cellular signaling networks. Current Opinion in Biotechnology 2006, 17:406-414.
45. Thingholm T.E., Larsen M.R., Ingrell C.R., Kassem M., Jensen O.N. TiO(2)-based phosphoproteomic analysis of the plasma membrane and the effects of phosphatase inhibitor treatment. Journal of Proteome Research 2008, 7:3304-3313.
46. Wu R., Dephoure N., Haas W., Huttlin E.L., Zhai B., Sowa M.E., et al. Correct interpretation of comprehensive phosphorylation dynamics requires normalization by protein expression changes. Molecular and Cellular Proteomics 2011, 10. M111.009654.
47. Chen E.I., Cociorva D., Norris J.L., Yates J.R. Optimization of mass spectrometry-compatible surfactants for shotgun proteomics. Journal of Proteome Research 2007, 6:2529-2538.
48. Carayon K., Leh H., Henry E., Simon F., Mouscadet J.F., Deprez E. A cooperative and specific DNA-binding mode of HIV-1 integrase depends on the nature of the metallic cofactor and involves the zinc-containing N-terminal domain. Nucleic Acids Research 2010, 38:3692-3708.
49. Zhou J., Zhou T., Cao R., Liu Z., Shen J., Chen P., et al. Evaluation of the application of sodium deoxycholate to proteomic analysis of rat hippocampal plasma membrane. Journal of Proteome Research 2006, 5:2547-2553.
50. Wisniewski J.R., Zougman A., Nagaraj N., Mann M. Universal sample preparation method for proteome analysis. Nature Methods 2009, 6:359-362.
51. Zielinska D.F., Gnad F., Wisniewski J.R., Mann M. Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 2010, 141:897-907.
52. Wisniewski J.R., Nagaraj N., Zougman A., Gnad F., Mann M. Brain phosphoproteome obtained by a FASP-based method reveals plasma membrane protein topology. Journal of Proteome Research 2010, 9:3280-3289.
53. Wisniewski J.R., Mann M. Consecutive proteolytic digestion in an enzyme reactor increases depth of proteomic and phosphoproteomic analysis. Analytical Chemistry 2012, 84:2631-2637.
54. Bian Y., Ye M., Song C., Cheng K., Wang C., Wei X., et al. Improve the Coverage for the Analysis of Phosphoproteome of HeLa Cells by a Tandem Digestion Approach. Journal of Proteome Research 2012.
55. Dephoure N., Gygi S.P. A solid phase extraction-based platform for rapid phosphoproteomic analysis. Methods 2011, 54:379-386.
56. Nuhse T., Yu K., Salomon A. Isolation of phosphopeptides by immobilized metal ion affinity chromatography. Current protocols in molecular biology 2007, [edited by Ausubel FM et al., Chapter 18:Unit 18.13].
57. Thingholm T.E., Jensen O.N. Enrichment and characterization of phosphopeptides by immobilized metal affinity chromatography (IMAC) and mass spectrometry. Methods in Molecular Biology (Clifton, NJ 2009, 527:47-56. xi.
58. Tao W.A., Wollscheid B., O'Brien R., Eng J.K., Li X.J., Bodenmiller B., et al. Quantitative phosphoproteome analysis using a dendrimer conjugation chemistry and tandem mass spectrometry. Nature Methods 2005, 2:591-598.
59. Zhou H., Watts J.D., Aebersold R. A systematic approach to the analysis of protein phosphorylation. Nature Biotechnology 2001, 19:375-378.
60. McLachlin D.T., Chait B.T. Improved beta-elimination-based affinity purification strategy for enrichment of phosphopeptides. Analytical Chemistry 2003, 75:6826-6836.
61. Chen M., Su X., Yang J., Jenkins C.M., Cedars A.M., Gross R.W. Facile identification and quantitation of protein phosphorylation via beta-elimination and Michael addition with natural abundance and stable isotope labeled thiocholine. Analytical Chemistry 2010, 82:163-171.
62. Bodenmiller B., Mueller L.N., Pedrioli P.G., Pflieger D., Junger M.A., Eng J.K., et al. An integrated chemical, mass spectrometric and computational strategy for (quantitative) phosphoproteomics: application to Drosophila melanogaster Kc167 cells. Molecular BioSystems 2007, 3:275-286.
63. Frackelton A.R., Ross A.H., Eisen H.N. Characterization and use of monoclonal antibodies for isolation of phosphotyrosyl proteins from retrovirus-transformed cells and growth factor-stimulated cells. Molecular and Cellular Biology 1983, 3:1343-1352.
64. Jedrychowski M.P., Huttlin E.L., Haas W., Sowa M.E., Rad R., Gygi S.P. Evaluation of HCD- and CID-type fragmentation within their respective detection platforms for murine phosphoproteomics. Molecular and Cellular Proteomics 2011, 10. M111 009910.
65. Rikova K., Guo A., Zeng Q., Possemato A., Yu J., Haack H., et al. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007, 131:1190-1203.
66. Gronborg M., Kristiansen T.Z., Stensballe A., Andersen J.S., Ohara O., Mann M., et al. A mass spectrometry-based proteomic approach for identification of serine/threonine-phosphorylated proteins by enrichment with phospho-specific antibodies: identification of a novel protein, Frigg, as a protein kinase A substrate. Molecular and Cellular Proteomics 2002, 1:517-527.
67. Zhang H., Zha X., Tan Y., Hornbeck P.V., Mastrangelo A.J., Alessi D.R., et al. Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs. Journal of Biological Chemistry 2002, 277:39379-39387.
68. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald E.R., Hurov K.E., Luo J., et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science (New York, NY) 2007, 316:1160-1166.
69. Jin J., Smith F.D., Stark C., Wells C.D., Fawcett J.P., Kulkarni S., et al. Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Current Biology 2004, 14:1436-1450.
70. 2 from aqueous solutions: an in situ internal reflection infrared spectroscopic study. Langmuir 1999, 15:2916-2921.
71. Ikeguchi Y., Nakamua H. Determination of organic phosphates by column-switching high performance anion-exchange chromatography using on-line preconcentration on titania. Analytical Sciences 1997, 13:479-483.
72. 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-nano-LC-ESI-MS/MS and titanium oxide precolumns. Analytical Chemistry 2004, 76:3935-3943.
73. Larsen M.R., Thingholm T.E., Jensen O.N., Roepstorff P., Jorgensen T.J. Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Molecular and Cellular Proteomics 2005, 4:873-886.
74. Sugiyama N., Masuda T., Shinoda K., Nakamura A., Tomita M., Ishihama Y. Phosphopeptide enrichment by aliphatic hydroxy acid-modified metal oxide chromatography for nano-LC-MS/MS in proteomics applications. Molecular and Cellular Proteomics 2007, 6:1103-1109.
75. Bodenmiller B., Wanka S., Kraft C., Urban J., Campbell D., Pedrioli P.G., et al. Phosphoproteomic analysis reveals interconnected system-wide responses to perturbations of kinases and phosphatases in yeast. Science Signaling 2010, 3:rs4.
76. Hilger M., Bonaldi T., Gnad F., Mann M. Systems-wide analysis of a phosphatase knock-down by quantitative proteomics and phosphoproteomics. Molecular and Cellular Proteomics 2009, 8:1908-1920.
77. Kanshin E., Michnick S.W., Thibault P. Decoy amino acids enhance the depth and coverage of large-scale phosphoproteomics studies. Proc 60th ASMS Conference on Mass Spectrometry and Allied Topics 2012, ASMS, Vancouver.
78. Ficarro S.B., Parikh J.R., Blank N.C., Marto J.A. Niobium(V) oxide (Nb2O5): application to phosphoproteomics. Analytical Chemistry 2008, 80:4606-4613.
79. Kweon H.K., Hakansson K. Selective zirconium dioxide-based enrichment of phosphorylated peptides for mass spectrometric analysis. Analytical Chemistry 2006, 78:1743-1749.
80. Andersson L., Porath J. Isolation of phosphoproteins by immobilized metal (Fe3+) affinity chromatography. Analytical Biochemistry 1986, 154:250-254.
81. Posewitz M.C., Tempst P. Immobilized gallium(III) affinity chromatography of phosphopeptides. Analytical Chemistry 1999, 71:2883-2892.
82. Collins M.O., Yu L., Husi H., Blackstock W.P., Choudhary J.S., Grant S.G. Robust enrichment of phosphorylated species in complex mixtures by sequential protein and peptide metal-affinity chromatography and analysis by tandem mass spectrometry. Science STKE 2005, 2005:pl6.
83. Kokubu M., Ishihama Y., Sato T., Nagasu T., Oda Y. Specificity of immobilized metal affinity-based IMAC/C18 tip enrichment of phosphopeptides for protein phosphorylation analysis. Analytical Chemistry 2005, 77:5144-5154.
84. Huttlin E.L., Jedrychowski M.P., Elias J.E., Goswami T., Rad R., Beausoleil S.A., et al. A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 2010, 143:1174-1189.
85. Schreiber T.B., Mausbacher N., Soroka J., Wandinger S.K., Buchner J., Daub H. Global analysis of phosphoproteome regulation by the Ser/Thr phosphatase Ppt1 in Saccharomyces cerevisiae. Journal of Proteome Research 2012, 11:2397-2408.
86. Ficarro S.B., McCleland M.L., Stukenberg P.T., Burke D.J., Ross M.M., Shabanowitz J., et al. Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nature Biotechnology 2002, 20:301-305.
87. Ficarro S., Chertihin O., Westbrook V.A., White F., Jayes F., Kalab P., et al. Phosphoproteome analysis of capacitated human sperm. Evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein/p97 during capacitation. Journal of Biological Chemistry 2003, 278:11579-11589.
88. Jensen S.S., Larsen M.R. Evaluation of the impact of some experimental procedures on different phosphopeptide enrichment techniques. Rapid Communications in Mass Spectrometry 2007, 21:3635-3645.
89. 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. Molecular and Cellular Proteomics 2008, 7:661-671.
90. Zhang K. From purification of large amounts of phospho-compounds (nucleotides) to enrichment of phospho-peptides using anion-exchanging resin. Analytical Biochemistry 2006, 357:225-231.
91. Han G., Ye M., Zhou H., Jiang X., Feng S., Jiang X., et al. Large-scale phosphoproteome analysis of human liver tissue by enrichment and fractionation of phosphopeptides with strong anion exchange chromatography. Proteomics 2008, 8:1346-1361.
92. Dai J., Wang L.S., Wu Y.B., Sheng Q.H., Wu J.R., Shieh C.H., et al. Fully automatic separation and identification of phosphopeptides by continuous pH-gradient anion exchange online coupled with reversed-phase liquid chromatography mass spectrometry. Journal of Proteome Research 2009, 8:133-141.
93. Ficarro S.B., Zhang Y., Carrasco-Alfonso M.J., Garg B., Adelmant G., Webber J.T., et al. Online nanoflow multidimensional fractionation for high efficiency phosphopeptide analysis. Molecular and Cellular Proteomics 2011, 10. O111.011064.
94. Beausoleil S.A., Jedrychowski M., Schwartz D., Elias J.E., Villen J., Li J., et al. Large-scale characterization of HeLa cell nuclear phosphoproteins. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:12130-12135.
95. Villen J., Beausoleil S.A., Gerber S.A., Gygi S.P. Large-scale phosphorylation analysis of mouse liver. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:1488-1493.
96. Zhai B., Villen J., Beausoleil S.A., Mintseris J., Gygi S.P. Phosphoproteome analysis of Drosophila melanogaster embryos. Journal of Proteome Research 2008, 7:1675-1682.
97. Sui S., Wang J., Yang B., Song L., Zhang J., Chen M., et al. Phosphoproteome analysis of the human Chang liver cells using SCX and a complementary mass spectrometric strategy. Proteomics 2008, 8:2024-2034.
98. Villen J., Gygi S.P. The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry. Nature Protocols 2008, 3:1630-1638.
99. Olsen J.V., Vermeulen M., Santamaria A., Kumar C., Miller M.L., Jensen L.J., et al. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Science Signaling 2010, 3:ra3.
100. Boulais J., Trost M., Landry C.R., Dieckmann R., Levy E.D., Soldati T., et al. Molecular characterization of the evolution of phagosomes. Molecular Systems Biology 2010, 6:423.
101. McNulty D.E., Annan R.S. Hydrophilic interaction chromatography reduces the complexity of the phosphoproteome and improves global phosphopeptide isolation and detection. Molecular and Cellular Proteomics 2008, 7:971-980.
102. Garbis S.D., Roumeliotis T.I., Tyritzis S.I., Zorpas K.M., Pavlakis K., Constantinides C.A. A novel multidimensional protein identification technology approach combining protein size exclusion prefractionation, peptide zwitterion-ion hydrophilic interaction chromatography, and nano-ultraperformance RP chromatography/nESI-MS2 for the in-depth analysis of the serum proteome and phosphoproteome: application to clinical sera derived from humans with benign prostate hyperplasia. Analytical Chemistry 2011, 83:708-718.
103. Wu C.J., Chen Y.W., Tai J.H., Chen S.H. Quantitative phosphoproteomics studies using stable isotope dimethyl labelling coupled with IMAC-HILIC-nanoLC-MS/MS for estrogen-induced transcriptional regulation. Journal of Proteome Research 2011, 10:1088-1097.
104. Alpert A.J. Electrostatic repulsion hydrophilic interaction chromatography for isocratic separation of charged solutes and selective isolation of phosphopeptides. Analytical Chemistry 2008, 80:62-76.
105. Gan C.S., Guo T., Zhang H., Lim S.K., Sze S.K. A comparative study of electrostatic repulsion-hydrophilic interaction chromatography (ERLIC) versus SCX-IMAC-based methods for phosphopeptide isolation/enrichment. Journal of Proteome Research 2008, 7:4869-4877.
106. Trost M., Bridon G., Desjardins M., Thibault P. Subcellular phosphoproteomics. Mass Spectrometry Reviews 2010, 29:962-990.
107. Nilsson C.L. Advances in quantitative phosphoproteomics. Analytical Chemistry 2012, 84:735-746.
108. Pimienta G., Chaerkady R., Pandey A. SILAC for global phosphoproteomic analysis. Methods in Molecular Biology 2009, 527:107-116. x.
109. Ong S.E., Foster L.J., Mann M. Mass spectrometric-based approaches in quantitative proteomics. Methods 2003, 29:124-130.
110. Neilson K.A., Ali N.A., Muralidharan S., Mirzaei M., Mariani M., Assadourian G., et al. Less label, more free: approaches in label-free quantitative mass spectrometry. Proteomics 2011, 11:535-553.
111. Zhu W., Smith J.W., Huang C.M. Mass spectrometry-based label-free quantitative proteomics. Journal of Biomedicine & Biotechnology 2010, 2010:840518.
112. Pan C., Olsen J.V., Daub H., Mann M. Global effects of kinase inhibitors on signaling networks revealed by quantitative phosphoproteomics. Molecular & Cellular Proteomics: MCP 2009, 8:2796-2808.
113. Monetti M., Nagaraj N., Sharma K., Mann M. Large-scale phosphosite quantification in tissues by a spike-in SILAC method. Nature Methods 2011, 8:655-658.
114. Geiger T., Cox J., Ostasiewicz P., Wisniewski J.R., Mann M. Super-SILAC mix for quantitative proteomics of human tumor tissue. Nature Methods 2010, 7:383-385.
115. Zanivan S., Krueger M., Mann M. In vivo quantitative proteomics: the SILAC mouse. Methods in Molecular Biology 2012, 757:435-450.
116. Reynolds K.J., Yao X., Fenselau C. Proteolytic 18O labelling for comparative proteomics: evaluation of endoprotease Glu-C as the catalytic agent. Journal of Proteome Research 2002, 1:27-33.
117. Fenselau C., Yao X. 18O2-labelling in quantitative proteomic strategies: a status report. Journal of Proteome Research 2009, 8:2140-2143.
118. Jones A.M., Nuhse T.S. Phosphoproteomics using iTRAQ. Methods in Molecular Biology 2011, 779:287-302.
119. Boersema P.J., Raijmakers R., Lemeer S., Mohammed S., Heck A.J. Multiplex peptide stable isotope dimethyl labelling for quantitative proteomics. Nature Protocols 2009, 4:484-494.
120. Evans C., Noirel J., Ow S.Y., Salim M., Pereira-Medrano A.G., Couto N., et al. An insight into iTRAQ: where do we stand now?. Analytical and Bioanalytical Chemistry 2012.
121. Mertins P., Udeshi N.D., Clauser K.R., Mani D.R., Patel J., Ong S.E., et al. iTRAQ labelling is superior to mTRAQ for quantitative global proteomics and phosphoproteomics. Molecular and Cellular Proteomics 2011.
122. Sinclair J., Timms J.F. Quantitative profiling of serum samples using TMT protein labelling, fractionation and LC-MS/MS. Methods 2011, 54:361-369.
123. Dephoure N., Gygi S.P. Hyperplexing: a method for higher-order multiplexed quantitative proteomics provides a map of the dynamic response to rapamycin in yeast. Science Signaling 2012, 5:rs2.
124. Tan C.S., Bader G.D. Phosphorylation sites of higher stoichiometry are more conserved. Nature Methods 2012, 9:317.
125. Hart G.W., Slawson C., Ramirez-Correa G., Lagerlof O. Cross talk between O-GlcNAcylation and phosphorylation: roles in signaling, transcription, and chronic disease. Annual Review of Biochemistry 2011, 80:825-858.
126. Vodermaier H.C. APC/C and SCF: controlling each other and the cell cycle. Current Biology 2004, 14:R787-R796.
127. Hietakangas V., Anckar J., Blomster H.A., Fujimoto M., Palvimo J.J., Nakai A., et al. PDSM, a motif for phosphorylation-dependent SUMO modification. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:45-50.