Enrichment strategies for phosphoproteomics: State-of-the-art

Reviews in Analytical Chemistry

Volumn 31, Issue 1, 2012, Pages 29-41

  Salovska, Barbora ^a,b   Tichy, Ales ^a,b   Rezacova, Martina ^a   Vavrova, Jirina ^b   Novotna, Eva ^b  

^a CHARLES UNIVERSITY   (Czech Republic)

^b UNIVERSITY OF DEFENCE   (Czech Republic)

Author keywords

Metal oxide affi nity chromatography; Phosphopeptide enrichment; Phosphoproteomics

Indexed keywords

EID: 84859762087     PISSN: 07930135     EISSN: None     Source Type: Journal    
DOI: 10.1515/revac-2011-0025     Document Type: Review

References (136)

1. Albuquerque, C. P.; Smolka, M. B.; Payne, S. H.; Bafna, V.; Eng, J.; Zhou, H. A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol. Cell. Proteomics 2008, 7, 1389-1396. (Pubitemid 352038280)
2. Alpert, A. J. Hydrophilic-interaction chromatography for the separation of peptides, nucleic acids and other polar compounds. J. Chromatogr. 1990, 19, 177-196. (Pubitemid 20044236)
3. Alpert, A. J. Electrostatic repulsion hydrophilic interaction chromatography for isocratic separation of charged solutes and selective isolation of phosphopeptides. Anal. Chem. 2008, 80, 62-76. (Pubitemid 351448406)
4. 3+ ) affi nity chromatography. Anal. Biochem. 1986, 154, 250-254. (Pubitemid 16063367)
5. Arrigoni, G.; Resjö, S.; Levander, F.; Nilsson, R.; Degerman, E.; Quadroni, M.; Pinna, L. A.; James, P. Chemical derivatization of phosphoserine and phosphothreonine containing peptides to increase sensitivity for MALDI-based analysis and for selectivity of MS/MS analysis. Proteomics 2006, 6, 757-766. (Pubitemid 43260201)
6. Aryal, U. K.; Ross, A. R. Enrichment and analysis of phosphopeptides under different experimental conditions using titaniumdioxide affi nity chromatography and mass spectrometry. Rapid Commun. Mass. Spectrom. 2010, 24, 219-231.
7. Bai, Z. F.; Wang, H. X. Advances in separation and enrichment approach of phosphoproteome reasearches. Chin. J. Anal. Chem. 2009, 37, 1382-1389.
8. Beausoleil, S. A.; Jedrychowski, M.; Schwartz, D.; Elias, J. E.; Villén, J.; Li, J.; Cohn, M. A.; Cantley, L. C.; Gygi, S. P. Largescale characterization of HeLa cell nuclear phosphoproteins. Proc. Natl. Acad. Sci. USA 2004, 101, 12130-12135. (Pubitemid 39145408)
9. Benschop, J. J.; Mohammed, S.; O ' Flaherty, M.; Heck, A. J.; Slijper, M.; Menke F. L. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol. Cell. Proteomics 2007, 6, 1198-1214. (Pubitemid 47099230)
10. Bernardi, G. Chromatography of nucleic acids on hydroxyapatite. I. Chromatography of native DNA. Biochim. Biophys. Acta 1969, 174, 423-434.
11. Blagoev, B.; Ong, S. E.; Kratchmarova, I.; Mann, M. Temporal analysis of phosphotyrosine-dependent signaling networks by quantitative proteomics. Nat. Biotechnol. 2004, 22, 1139-1145. (Pubitemid 39166852)
12. Blume-Jensen, P.; Hunter T. Oncogenic kinase signalling. Nature 2001, 411, 355-365. (Pubitemid 32467045)
13. Bodenmiller, B.; Mueller, L. N.; Mueller, M.; Domon, B.; Aebersold, R. Reproducible isolation of distinct, overlapping segments of the phosphoproteome. Nat. Methods 2007, 4, 231-237. (Pubitemid 46358873)
14. Brehmer, D.; Godl, K.; Zech. B.; Wissing, J.; Daub, H. Proteomewide identifi cation of cellular targets affected by bisindolylmaleimide-type protein kinase C inhibitors. Mol. Cell. Proteomics 2004, 3, 490-500. (Pubitemid 38714290)
15. 2 -based phosphopeptide enrichment for automated multidimensional liquid chromatography coupled to tandem mass spectrometry. Anal. Chem. 2007, 79, 4666-4673. (Pubitemid 46999584)
16. Carrascal, M.; Ovelleiro, D.; Casas, V.; Gay, M.; Abian, J. Phosphorylation analysis of primary human T lymphocytes using sequential IMAC and titanium oxide enrichment. J. Proteome Res. 2008, 7, 5167-5176.
17. Chen, L.; Giorgianni, F.; Beranova-Giorgianni, S. Characterization of the phosphoproteome in LNCaP prostate cancer cells by in-gel isoelectric focusing and tandem mass spectrometry. J. Proteome Res. 2010, 9, 174-178.
18. Chen, L.; Fang, B.; Giorgianni, F.; Gingrich, J. R.; Beranova-Giorgianni, S. Investigation of phosphoprotein signatures of archived prostate cancer tissue specimens via proteomic analysis. Electrophoresis 2011a, 32, 1984-1991.
19. Chen, X.; Wu, D.; Zhao, Y.; Wong, B. H.; Guo, L. Increasing phosphoproteome coverage and identifi cation of phosphorylation motifs through combination of different HPLC fractionation methods. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2011b, 879, 25-34.
20. Chien, K. Y.; Liu, H. C.; Goshe, M. B. Development and application of a phosphoproteomic method using electrostatic repulsionhydrophilic interaction chromatography (ERLIC), IMAC, and LC-MS/MS analysis to study Marek ' s disease virus infection. J. Proteome Res. 2011, 10, 4041-4053.
21. Cohen, P. The origins of protein phosphorylation. Nat. Cell. Biol. 2002, 4, 127-130.
22. Craig, A. G.; Hoeger, C. A.; Miller, C. L.; Goedken, T.; Rivier, J. E.; Fischer, W. H. Monitoring protein kinase and phosphatase reactions with matrix-assisted laser desorption/ionization mass spectrometry and capillary zone electrophoresis: comparison of the detection effi ciency of peptide-phosphopeptide mixtures. Biol. Mass Spectrom. 1994, 23, 519-528.
23. Dai, J.; Jin, W. H.; Sheng, Q. H.; Shieh, C. H.; Wu, J. R.; Zeng, R. Protein phosphorylation and expression profi ling by Yin-yang multidimensional liquid chromatography (Yin-yang MDLC) mass spectrometry. J. Proteome Res. 2007, 6, 250-262. (Pubitemid 46173677)
24. Dai, J.; Wang, L. S.; Wu, Y. B.; Sheng, Q. H.; Wu, J. R.; Shieh, C. H.; Zeng, R. Fully automatic separation and identifi cation of phosphopeptides by continuous pH-gradient anion exchange online coupled with reversed-phase liquid chromatography mass spectrometry. J. Proteome Res. 2009, 8, 133-141.
25. 5 from aqueous solutions. Spectrochim. Acta A Mol. Biomol. Spectrosc. 2000, 56, 557-565.
26. Dong, J.; Zhou, H.; Wu, R.; Ye, M.; Zou, H. Specifi c capture of phosphopeptides by Zr4 + -modifi ed monolithic capillary column. J. Sep. Sci. 2007, 30, 2917-2923. (Pubitemid 350238323)
27. Edbauer, D.; Cheng, D.; Batterton, M. N.; Wang, C. F.; Duong, D. M.; Yaffe, M. B.; Peng, J.; Sheng, M. Identifi cation and characterization of neuronal mitogen-activated protein kinase substrates using a specifi c phosphomotif antibody. Mol. Cell. Proteomics 2009, 8, 681-695.
28. 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, 301-305. (Pubitemid 34205425)
29. 2Oi ): application to phosphoproteomics. Anal. Chem. 2008, 80, 4606-4613.
30. Gauci, S.; Helbig, A. O.; Slijper, M.; Krijgsveld, J.; Heck, A. J.; Mohammed, S. Lys-N and trypsin cover complementary parts of the phosphoproteome in a refi ned SCX-based approach. Anal. Chem. 2009, 81, 4493-4501.
31. Gilar, M.; Olivova, P.; Daly, A. E.; Gebler, J. C. Orthogonality of separation in two-dimensional liquid chromatography. Anal. Chem. 2005, 77, 6426-6434. (Pubitemid 41436983)
32. Gorbunoff, M. J. The interaction of proteins with hydroxyapatite. Anal. Biochem. 1984, 136, 425-445.
33. Goshe, M. B.; Conrads, T. P.; Panisko, E. A.; Angell, N. H.; Veenstra, T. D.; Smith, R. D. Phosphoprotein isotope-coded affi nity tag approach for isolating and quantitating phosphopeptides in proteome-wide analyses. Anal. Chem. 2001, 73, 2578-2586. (Pubitemid 32880661)
34. Goshe, M. B.; Veenstra, T. D.; Panisko, E. A.; Conrads, T. P.; Angell, N. H.; Smith, R. D. Phosphoprotein isotope-coded affi nity tags: application to the enrichment and identifi cation of low-abundance phosphoproteins. Anal. Chem. 2002, 74, 607-616. (Pubitemid 34131511)
35. Grimsrud, P. A.; Swaney, D. L.; Wenger, C. D.; Beauchene, N. A.; Coon, J. J. Phosphoproteomics for the masses. ACS Chem. Biol. 2010, 5, 105-119.
36. Grønborg, M.; Kristiansen, T. Z.; Stensballe, A.; Andersen, J. S.; Ohara, O.; Mann, M.; Jensen, O. N.; Pandey, A. A mass spectrometry-based proteomic approach for identifi cation of serine/ threonine-phosphorylated proteins by enrichment with phospho-specifi c antibodies: identifi cation of a novel protein, Frigg, as a protein kinase A substrate. Mol. Cell. Proteomics 2002, 1, 517-527.
37. Gruhler, A.; Olsen, J. V.; Mohammed, S.; Mortensen, P.; Faergeman, N. J.; Mann, M.; Jensen, O. N. Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Mol. Cell Proteomics 2005, 4, 310-327 . (Pubitemid 40439774)
38. Han, G.; Ye, M.; Zhou, H.; Jiang, X.; Feng, S.; Jiang, X.; Tian, R.; Wan, D.; Zou, H.; Gu, J. Large-scale phosphoproteome analysis of human liver tissue by enrichment and fractionation of phosphopeptides with strong anion exchange chromatography. Proteomics 2008, 8, 1346-1361. (Pubitemid 351518547)
39. Harsha, H. C.; Pandey, A. Phosphoproteomic in cancer. Mol. Oncol. 2010, 4, 482-495.
40. Helling, S.; Shinde, S.; Brosseron, F.; Schnabel, A.; Müller, T.; Meyer, H. E.; Marcus, K.; Sellergren, B. Ultratrace enrichment of tyrosine phosphorylated peptides on an imprinted polymer. Anal. Chem. 2011, 83, 1862-1865.
41. Hemström, P.; Irgum, K. Hydrophilic interaction chromatography. J. Sep. Sci. 2006, 29, 1784-1821. (Pubitemid 44348484)
42. Holland, C.; Schmid, M.; Zimny-Arndt, U.; Rohloff, J.; Stein, R.; Jungblut, P. R.; Meyer T. F. Quantitative phosphoproteomicsreveals link between Helicobacter pylori infection and RNA splicing modulation in host cells. Proteomics 2011, 11, 2798-2811.
43. Hultquist, D. E. The preparation and characterization of phosphorylated derivatives of histidine. Biochim. Biophys. Acta 1968, 153, 329-340.
44. Hunter, T.; Sefton, B. M. Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc. Natl. Acad. Sci. USA 1980, 77, 1311-1315. (Pubitemid 10072278)
45. Ikeguchi, Y.; Nakamura, H. Determination of organic phosphates by column-switching high performance anion-exchange chromatography using on-line preconcentration on titania. Anal. Sci. 1997, 13, 479-483. (Pubitemid 127479861)
46. Jensen, S. S.; Larsen, M. R. Evaluation of the impact of some experimental procedures on different phosphopeptide enrichmenttechniques. Rapid Commun. Mass. Spectrom. 2007, 21, 3635-3645. (Pubitemid 350124632)
47. Klemm, C.; Otto, S.; Wolf, C.; Haseloff, R. F.; Beyermann, M.; Krause, E. Evaluation of the titanium dioxide approach for MS analysis of phosphopeptides. J. Mass. Spectrom. 2006, 41, 1623-1632. (Pubitemid 46045801)
48. Knezevic, I.; Bachem, S.; Sickmann, A.; Meyer, H. E.; Stülke, J.; Hengstenberg, W. Regulation of the glucose-specifi c phosphotransferase system (PTS) of Staphylococcus carnosus by the antiterminator protein GlcT. Microbiology 2000, 146, 2333-2342.
49. Kugimiya, A.; Takei, H. Selectivity and recovery performance of phosphate-selective molecularly imprinted polymer. Anal. Chim. Acta 2008, 606, 252-256. (Pubitemid 350235372)
50. Kweon, H. K.; Hakansson, K. Selective zirconium dioxide-based enrichment of phosphorylated peptides for mass spectrometric analysis. Anal. Chem. 2006, 78, 1743-1749.
51. Lansdell, T. A.; Tepe, J. J. Isolation of phosphopeptides using solid phase enrichment. Tetrahedron Lett. 2004, 45, 91-93. (Pubitemid 38155858)
52. Larsen, M. R.; Thingholm, T. E.; Jensen, O. N.; Roepstorff, P.; Jørgensen, T. J. Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell Proteomics 2005, 4, 873-886. (Pubitemid 41309146)
53. Lee, A.; Yang, H. J.; Lim, E. S.; Kim, J.; Kim, Y. Enrichment of phosphopeptides using bare magnetic particles. Rapid Commun. Mass. Spectrom. 2008, 22, 2561-2564.
54. Lee, H. J.; Na, K.; Kwon, M. S.; Kim, H.; Kim, K. S.; Paik, Y. K. Quantitative analysis of phosphopeptides in search of the diseasebiomarker from the hepatocellular carcinoma specimen. Proteomics 2009, 9, 3395-3408.
55. Leitner, A.; Sturm, M.; Smatt, J. H.; Järn, M.; Lindén, M.; Mechtler, K.; Lindner, W. Optimizing the performance of tin dioxide microspheres for phosphopeptide enrichment. Anal. Chim. Acta 2009, 638, 51-57.
56. Leitner, A.; Sturm, M.; Hudecz, O.; Mazanek, M.; Smatt, J. H.; Lindén, M.; Lindner, W.; Mechtler, K. Probing the phosphoproteome of HeLa cells using nanocast metal oxide microspheres for phosphopeptide enrichment. Anal. Chem. 2010, 82, 2726-2733.
57. Lemeer, S.; Pinkse, M. W.; Mohammed, S.; van Breukelen, B.; den Hertog, J.; Slijper, M.; Heck, A. J. Online automated in vivozebrafi sh phosphoproteomics: from large-scale analysis down to a single embryo. J. Proteome Res. 2008a, 7, 1555-1564.
58. Lemeer, S.; Jopling, C.; Gouw, J.; Mohammed, S.; Heck, A. J.; Slijper, M.; den Hertog, J. Comparative phosphoproteomics of zebrafi sh Fyn/Yes morpholino knockdown embryos. Mol. Cell. Proteomics 2008b, 7, 2176-2187.
59. 2 core-shell microspheres as affi nityprobes for selective enrichment and direct determination of phosphopeptides using matrix-assisted laser desorption ionization mass spectrometry. J. Proteome Res. 2007, 6, 4498-4510. (Pubitemid 350158525)
60. Li, Y.; Lin, H.; Deng, C.; Yang, P.; Zhang, X. Highly selective and rapid enrichment of phosphorylated peptides using gallium oxidecoated magnetic microspheres for MALDI-TOF-MS and nano-LC-ESI-MS/MS/MS analysis. Proteomics 2008, 8, 238-249. (Pubitemid 351212323)
61. 2 beads ratio on phosphopeptide enrichment selectivity. J. Proteome Res. 2009, 8, 5375-5381.
62. Liang, S. S.; Makamba, H.; Huang, S. Y.; Chen, S. H. Nano-titanium dioxide composites for the enrichment of phosphopeptides. J. Chromatogr. A 2006, 1116, 38-45.
63. 2 surfaces used in the study of regulated, dynamic protein phosphorylation. J. Am. Soc. Mass Spectrom. 2007, 18, 1932-1944. (Pubitemid 47633952)
64. Liao, P. C.; Leykam, J.; Andrews, P. C.; Gage, D. A.; Allison, J. An approach to locate phosphorylation sites in a phosphoprotein: mass mapping by combining specifi c enzymatic degradation with matrix-assisted laser desorption/ionization mass spectrometry. Anal. Biochem. 1994, 219, 9-20. (Pubitemid 24167215)
65. 2 nanoparticle-deposited capillary column by liquid phase deposition and its application in phosphopeptide analysis. J. Chromatogr. A 2008, 1192, 95-102.
66. Lo, C. Y.; Chen, W. Y.; Chen, C. T.; Chen, Y. C. Rapid enrichment of phosphopeptides from tryptic digests of proteins using iron oxide nanocomposites of magnetic particles coated with zirconia as the concentrating probes. J. Proteome Res. 2007, 6, 887-893.
67. Lu, Z.; Duan, J.; He, L.; Hu, Y.; Yin, Y. Mesoporous TiO(2) nanocrystal clusters for selective enrichment of phosphopeptides. Anal. Chem. 2010, 82, 7249-7258.
68. Maccarrone, G.; Kolb, N.; Teplytska, L.; Birg, I.; Zollinger, R.; Holsboer. F.; Turck, C. W. Phospho-peptide enrichment by IEF. Electrophoresis 2006, 27, 4585-4595.
69. Mamone, G.; Picariello, G.; Ferranti, P.; Addeo, F. Hydroxyapatite affi nity chromatography for the highly selective enrichment of mono-and multi-phosphorylated peptides in phosphoproteome analysis. Proteomics 2010, 10, 380-393.
70. Manning, G.; Whyte, D. B.; Martinez, R.; Hunter, T.; Sudarsanam, S. The protein kinase complement of human genome. Science 2002 ,298, 1912-1934. (Pubitemid 35425239)
71. Matsuda, H.; Nakamura, H.; Nakajima, T. New ceramic titania: selective adsorbent for organic phosphates. Anal. Sci. 1990, 6, 911-912.
72. Matthews, H. R. Protein kinases and phosphatases that act on histidine, lysine, or arginine residues in eukaryotic proteins: a possible regulator of the mitogen-activated protein kinase cascade. Pharm. Ther . 1995, 67, 323-350.
73. Mazanek, M.; Mituloviae, G.; Herzog, F.; Stingl, C.; Hutchins, J. R.; Peters, J. M.; Mechtler, K. Titanium dioxide as a chemoaffinity solid phase in offl ine phosphopeptide chromatography prior to HPLC-MS/MS analysis. Nat. Protoc. 2007, 2, 1059-1069. (Pubitemid 46901287)
74. Mazanek, M.; Roitinger, E.; Hudecz, O.; Hutchins, J. R.; Hegemann, B.; MitulovićG.; Taus, T.; Stingl, C.; Peters, J. M.; Mechtler, K. A new acid mix enhances phosphopeptide enrichment on titanium-and zirconium dioxide for mapping of phosphorylation sites on protein complexes. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2010, 878, 515-524.
75. McNulty, D. E.; Annan, R. S. Hydrophilic interaction chromatography reduces the complexity of the phosphoproteome and improves global phosphopeptide isolation and detection. Mol. Cell. Proteomics 2008, 7, 971-980. (Pubitemid 351737096)
76. 2 enrichment method for label-free quantitative phosphoproteomics. Methods . 2011, 54, 370-378.
77. Nelson, C. A.; Szczech, J. R.; Xu, Q.; Lawrence, M. J.; Jin, S.; Ge, Y. Mesoporous zirconium oxide nanomaterials effectivelyenrich phosphopeptides for mass spectrometry-based phosphoproteomics. Chem. Commun. ( Camb. ) 2009, 43, 6607-6609.
78. Nie, S.; Dai, J.; Ning, Z. B.; Cao, X. J.; Sheng, Q. H.; Zeng, R. Comprehensive profi ling of phosphopeptides based on anion exchange followed by fl ow-through enrichment with titanium dioxide (AFET). J. Proteome Res. 2010, 9, 4585-4594.
79. Nilsson, C. L.; Dillon, R.; Devakumar, A.; Shi, S. D.; Greig, M.; Rogers, J. C.; Krastins, B.; Rosenblatt, M.; Kilmer, G.; Major, M.; Kaboord, B. J.; Sarracino, D.; Rezai, T.; Prakash, A.; Lopez, M.; Ji, Y.; Priebe, W.; Lang, F. F.; Colman, H.; Conrad, C. A. Quantitative phosphoproteomic analysis of the STAT3/IL-6/ HIF1alpha signaling network: an initial study in GSC11 glioblastoma stem cells . J. Proteome Res. 2010, 9, 430-443.
80. Nühse, T. S.; Stensballe, A.; Jensen, O. N.; Peck, S. C. Large-scale analysis of in vivo phosphorylated membrane proteins by immobilized metal ion affi nity chromatography and mass spectrometry. Mol. Cell. Proteomics 2003, 2, 1234-1243.
81. Oda, Y.; Nagasu, T.; Chait, B. T. Enrichment analysis of phosphorylated proteins as a tool for probing the phosphoproteome. Nat. Biotechnol. 2001, 19, 379-382. (Pubitemid 32275350)
82. Olsen, J. V.; Blagoev, B.; Gnad, F.; Macek, B.; Kumar, C.; Mortensen, P.; Mann, M. Global, in vivo, and site-specifi c phosphorylation dynamics in signaling networks. Cell 2006, 127, 635-648. (Pubitemid 44647421)
83. 2-enriched phosphopeptides. Anal. Biochem. 2011, 409, 81-88.
84. Pink, M.; Verma, N.; Polato, F.; Bonn, G. K.; Baba, H. A.; Rettenmeier, A. W.; Schmitz-Spanke, S. Precipitation by lanthanum ions: a straightforward approach to isolating phosphoproteins. J. Proteomics 2011, 75, 375-383.
85. Pinkse, M. W. H.; Uitto, P. M.; Hilhorst, M. J.; Ooms, B.; Heck, A. J. R. 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, 3935-3943. (Pubitemid 38943662)
86. Pinkse, M. W. H.; Heck, A. J. R. Essential enrichment strategies in phosphoproteomics. Drug Discov. Today Technol . 2010, 3, 331-337. (Pubitemid 44734723)
87. Pinto, G.; Caira, S.; Cuollo, M.; Lilla, S.; Fierro, O.; Addeo, F. Hydroxyapatite affi nity chromatography for the highly selectiveenrichment of mono-and multi-phosphorylated peptides in phosphoproteome analysis. Proteomics 2010, 10, 380-393.
88. Poot, A. J.; Ruijter, E.; Nuijens, T.; Dirksen, E. H.; Heck, A. J.; Slijper, M.; Rijkers, D. T.; Liskamp, R. M. Selective enrichment of Ser-/Thr-phosphorylated peptides in the presence of Ser-/Thrglycosylated peptides. Proteomics 2006, 6, 6394-6399. (Pubitemid 46048378)
89. Porath, J.; Carlsson, J.; Olsson, I.; Belfrage, G. Metal chelate affi nitychromatography, a new approach to protein fractionation. Nature 1975, 258, 598-599.
90. Posewitz, M. C.; Tempst, P. Immobilized gallium(III) affi nity chromatography of phosphopeptides. Anal. Chem. 1999, 71, 2883-2892. (Pubitemid 29340481)
91. Qi, D.; Lu, J.; Deng, C.; Zhang, X. Development of core-shell structure Fe3O4@Ta2O5 microspheres for selective enrichment ofphosphopeptides for mass spectrometry analysis. J. Chromatogr. A 2009, 1216, 5533-5539.
92. Qi, D.; Mao, Y.; Zhang, X. Phosphate-functionalized magnetic microspheres for immobilization of Zr 4 + ions for selective enrichment of the phosphopeptides. J. Chromatogr. A 2010, 1217, 2606-2617.
93. Qiao, L.; Roussel, C.; Wan, J.; Yang, P.; Girault, H. H.; Liu, B. Specifi c on-plate enrichment of phosphorylated peptides for direct MALDI-TOF MS analysis. J. Proteome Res. 2007, 6, 4763-4769.
94. Reinders, J.; Sickman, A. State-of-the-art in phosphoproteomics. Proteomics 2005, 5, 4052-4061. (Pubitemid 41626073)
95. Rivera, J. G.; Choi, Y. S.; Vujcic, S.; Wood, T. D.; Colón, L. A. Enrichment/isolation of phosphorylated peptides on hafnium oxide prior to mass spectrometric analysis. Analyst. 2009, 134, 31-33.
96. Ruse, C. I.; McClatchy, D. B.; Lu, B.; Cociorva, D.; Motoyama, A.; Park, S. K.; Yates, J. R., 3rd. Motif-specifi c sampling of phosphoproteomes.J. Proteome Res. 2008, 7, 2140-2150.
97. Rush, J.; Moritz, A.; Lee, K. A.; Guo, A.; Goss, V. L.; Spek, E. J.; Zhang, H.; Zha, X. M.; Polakiewicz, R. D.; Comb, M. J. Immunoaffi nity profi ling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol. 2005, 23, 94-101. (Pubitemid 41724631)
98. Sanders, D. A.; Gillece-Castro, B. L.; Stock, A. M.; Burlingame, A. L.; Koshland, D. E. Identifi cation of the site of phosphorylationof the chemotaxis response regulator protein, CheY. J. Biol. Chem. 1989, 264, 21770-21778. (Pubitemid 20028746)
99. Schumacher, J. A.; Crockett, D. K.; Elenitoba-Johnson, K. S.; Lim, M. S. Evaluation of enrichment techniques for mass spectrometry:identifi cation of tyrosine phosphoproteins in cancer cells. J. Mol. Diagn. 2007, 9, 169-177. (Pubitemid 47305083)
100. Sickmann, A.; Meyer, H. E. Phosphoamino acid analysis. Proteomics 2001, 1, 200-206. (Pubitemid 33586716)
101. Simon, E. S.; Young, M.; Chan, A.; Bao, Z. Q.; Andrews, P. C. Improved enrichment strategies for phosphorylated peptides on titanium dioxide using methylesterifi cation and pH gradient elution. Anal. Biochem. 2008, 377, 234-242.
102. Steen, H.; Mann, M. A new derivatization strategy for the analysis of phosphopeptides by precursor ion scanning in positive ion mode. J. Am. Soc. Mass. Spectrom. 2002, 13, 996-1003. (Pubitemid 36876012)
103. 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. Mol. Cell Proteomics 2006, 5, 172-181. (Pubitemid 43169349)
104. Stone, M. D.; Chen, X.; McGowan, T.; Bandhakavi, S.; Cheng, B.; Rhodus, N. L.; Griffin, T. J. Large-scale phosphoproteomics analysis of whole saliva reveals a distinct phosphorylation pattern. J. Proteome Res. 2011, 10, 1728-1736.
105. Sugiyama, N.; Masuda, T.; Shinoda, K.; Nakamura, A.; Tomita, M.; Ishihama, Y. Phosphopeptide enrichment by aliphatic hydroxyl acid-modifi ed metal oxid chromatography. Moll. Cell. Proteomics 2007, 6, 1103-1109. (Pubitemid 47019410)
106. 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, 193.
107. Swaney, D. L.; Wenger, C. D.; Thomson, J. A.; Coon, J. J. Human embryonic stem cell phosphoproteome revealed by electron transfer dissociation tandem mass spectrometry. Proc. Natl. Acad. Sci. USA 2009, 106, 995-1000.
108. Tao, W. A.; Wollscheid, B.; O ' Brien, R.; Eng, J. K.; Li, X. J.; Bodenmiller, B.; Watts, J. D.; Hood, L.; Aebersold, R.Quantitative phosphoproteome analysis using a dendrimer conjugation chemistry and tandem mass spectrometry. Nat. Methods 2005, 2, 591-598. (Pubitemid 41086850)
109. Taouatas, N.; Altelaar, A. F.; Drugan, M. M.; Helbig, A. O.; Mohammed, S.; Heck, A. J. Strong cation exchange-based fractionation of Lys-N-generated peptides facilitates the targeted analysis of post-translational modifi cations. Mol. Cell. Proteomics 2009, 8, 190-200.
110. Tani, K.; Suzuki, Y. Investigation of the ion-exchange behaviour of titania: application as a packing material for ion chromatography. Chromatographia 1997, 46, 623-627. (Pubitemid 27514344)
111. Tani, K.; Sumizawa, T.; Watanabe, M.; Tachibana, M.; Koizumi, H.; Kiba, T. Evaluation of titania as an ion-exchanger and asa ligand-exchanger in HPLC. Chromatographia 2002, 55, 33-37. (Pubitemid 34095151)
112. Thaler, F.; Valsasina, B.; Baldi, R.; Xie, J.; Stewart, A.; Isacchi, A.; Kalisz, H. M.; Rusconi, L. A new approach to phosphoserine andphosphothreonine analysis in peptides and proteins: chemical modifi cation, enrichment via solid-phase reversible binding, and analysis by mass spectrometry. Anal. Bioanal. Chem. 2003, 376, 366-373. (Pubitemid 40878037)
113. Thingholm, T. E.; Jensen, O. N.; Robinson, P. J.; Larsen, M. R. SIMAC (sequential elution from IMAC), a phosphoproteomicsstrategy for the rapid separation of monophosphorylated from multiply phosphorylated peptides. Mol. Cell. Proteomics 2008, 7, 661-671. (Pubitemid 351597478)
114. Thingholm, T. E.; Jensen, O. N.; Larsen, M. R. Analytical strategies for phosphoproteomics. Proteomics 2009, 9, 1451-1469.
115. Tichy, A.; Salovska, B.; Rehulka, P.; Klimentova, J.; Vavrova, J.; Stulik, J.; Hernychova, L. Phosphoproteomics: searching for a needle in a haystack. J. Proteomics 2011, 74, 2786-2797.
116. Tiselius, A.; Hjerten, S.; Levin, O. Protein chromatography on calcium phosphate columns. Arch. Biochem. Biophys. 1956, 65, 132-155.
117. Verma, N.; Bäuerlein, C.; Pink, M.; Rettenmeier, A. W.; Schmitz-Spanke, S. Proteome and phosphoproteome of primary cultured pig urothelial cells. Electrophoresis 2011, 32, 3600-3611.
118. Villén, J.; Beausoleil, S. A.; Gerber, S. A.; Gygi, S. P. Large-scale phosphorylation analysis of mouse liver. Proc. Natl. Acad. Sci.USA 2007, 104, 1488-1493. (Pubitemid 46214617)
119. Wan, H.; Yan, J.; Yu, L.; Zhang, X.; Xue, X.; Li, X.; Liang, X. Zirconia layer coated mesoporous silica microspheres used for highly specifi c phosphopeptide enrichment. Talanta 2010, 82, 1701-1707.
120. Washburn, M. P.; Wolters, D.; Yates, J. R., 3rd. Large-scale analysis of the yeast proteome by multidimensional protein identifi cation technology. Nat. Biotechnol. 2001, 19, 242-247. (Pubitemid 32220565)
121. Weigt, C.; Korte, H.; Pogge von Strandmann, R.; Hengstenberg, W.; Meyer, H. E. Identifi cation of phosphocysteine by electrospray mass spectrometry combined with Edman degradation. J. Chromatogr. A 1995, 712, 141-147.
122. Wilson-Grady, J. T.; Villén, J.; Gygi, S. P. Phosphoproteome analysis of fi ssion yeast. J. Proteome Res. 2008, 7, 1088-1097.
123. Wolschin, F.; Weckwerth, W. Combining metal oxide affi nity chromatography (MOAC) and selective mass spectrometry for robust identifi cation of in vivo protein phosphorylation sites. Plant Methods. 2005, 1, 9.
124. Wolters, D. A.; Washburn, M. P.; Yates, J. R., 3rd. An automated multidimensional protein identifi cation technology for shotgun proteomics. Anal. Chem. 2001, 73, 5683-5690. (Pubitemid 33126725)
125. Wu, J.; Shakey, Q.; Liu, W.; Schuller, A.; Follettie, M. T. Global profi ling of phosphopeptides by titania affi nity enrichment. J. Proteome Res . 2007, 6, 4684-4689.
126. Wu, Y. B.; Dai, J.; Yang, X. L.; Li, S. J.; Zhao, S. L.; Sheng, Q. H.; Tang, J. S.; Zheng, G. Y.; Li, Y. X.; Wu, J. R.; Zeng, R. Concurrent quantifi cation of proteome and phosphoproteome to reveal system-wide association of protein phosphorylation and gene expression. Mol. Cell. Proteomics 2009, 8, 2809-2826.
127. Xu, Y.; Sprung, R.; Kwon, S. W.; Kim, S. C.; Zhao, Y. Isolation of phosphopeptides by pI-difference-based electrophoresis. J. Proteome Res. 2007, 6, 1153-1157.
128. Xue, Y.; Wei, J.; Han, H.; Zhao, L.; Cao, D.; Wang, J.; Yang, X.; Zhang, Y.; Qian, X. Application of open tubular capillary columns coated with zirconium phosphonate for enrichment of phosphopeptides. J. Chromatogr. B 2009, 877, 757-764.
129. Yu, L. R.; Zhu, Z.; Chan, K. C.; Issaq, H. J.; Dimitrov, D. S.; Veenstra, T. D. Improved titanium dioxide enrichment of phoshopeptides from HeLa cells and high confi dent phosphopeptide identifi cation by cross-validation of MS/MS and MS/MS/MS spectra. J.Proteome Res. 2007, 6, 4150-4162. (Pubitemid 350158493)
130. Yu, Y. Q.; Fournier, J., Gilar, M.; Gebler, J. C. Phosphopeptide enrichment using microscale titanium dioxide solid phase extraction. J. Sep. Sci. 2009, 32, 1189-1199.
131. Zhang, H.; Zha, X.; Tan, Y.; Hornbeck, P. V. Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs. J. Biol. Chem. 2002, 277, 39379-39387. (Pubitemid 35190911)
132. Zhang, X.; Ye, J.; Jensen, O. N.; Roepstorff, P. Highly effi cient phosphopeptide enrichment by calcium phosphate precipitation combined with subsequent IMAC enrichment. Mol. Cell. Proteomics 2007, 6, 2032-2042. (Pubitemid 350201876)
133. Zhang, L.; Wang, H.; Liang, Z.; Yang, K.; Zhang, L.; Zhang, Y. Facile preparation of monolithic immobilized metal affi nity chromatography capillary columns for selective enrichment of phosphopeptides. J. Sep. Sci. 2011, 34, 2122-2130.
134. Zhou, H.; Watts, J. D.; Aebersold, R. A systematic approach to the analysis of protein phosphorylation. Nat. Biotechnol. 2001, 19, 375-378. (Pubitemid 32275349)
135. Zhou, H.; Tian, R.; Ye, M.; Xu, S.; Feng, S.; Pan, C.; Jiang, X.; Li, X.; Zou, H. Highly specifi c enrichment of phosphopeptides by zirconium dioxide nanoparticles for phosphoproteome analysis. Electrophoresis 2007, 28, 2201-2215. (Pubitemid 47065147)
136. Zhou, H.; Low, T. Y.; Hennrich, M. L.; van den Toorn, H.; Schwend, T.; Zou, H.; Mohammed, S.; Heck, A. J. Enhancing the identify cation of phosphopeptides from putative basophilic kinase substrates using Ti (IV) based IMAC enrichment. Mol. Cell. Proteomics. 2011, 10, M110.006452.