Recent advances in phosphopeptide enrichment: Strategies and techniques

TrAC - Trends in Analytical Chemistry

Volumn 78, Issue , 2016, Pages 70-83

  Li, Xiao Shui ^a,b   Yuan, Bi Feng ^b   Feng, Yu Qi ^b  

^a CHINA UNIVERSITY OF GEOSCIENCES   (China)

^b WUHAN UNIVERSITY   (China)

Author keywords

Enrichment; Immobilized metal affinity chromatography; Mass spectrometry; Metal oxide affinity chromatography; Phosphopeptide; Strategy; Technique

Indexed keywords

BLAST ENRICHMENT; CHROMATOGRAPHY; MASS SPECTROMETRY; METALS; MOLECULAR BIOLOGY; PLANNING; STRATEGIC PLANNING; SUPPORT VECTOR MACHINES;

IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; METAL OXIDE AFFINITY CHROMATOGRAPHIES; PHOSPHOPEPTIDES; STRATEGY; TECHNIQUE;

AFFINITY CHROMATOGRAPHY;

NANOMATERIAL; PHOSPHOPEPTIDE; POLYMER;

AFFINITY CHROMATOGRAPHY; CHEMICAL PROCEDURES; COPRECIPITATION; DERIVATIZATION; HUMAN; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; IMMUNOPRECIPITATION; INORGANIC SALT AFFINITY CHROMATOGRAPHY; ION EXCHANGE CHROMATOGRAPHY; METAL OXIDE AFFINITY CHROMATOGRAPHY; PHOSPHOPEPTIDE ENRICHMENT; PRECIPITATION; PRIORITY JOURNAL; PROCESS DEVELOPMENT; REVIEW;

EID: 84959513649     PISSN: 01659936     EISSN: 18793142     Source Type: Journal    
DOI: 10.1016/j.trac.2015.11.001     Document Type: Review

References (169)

1. Hunter T. Signaling - 2000 and beyond. Cell 2000, 100:113-127.
2. Ubersax J.A., Ferrell J.E. Mechanisms of specificity in protein phosphorylation. Nat. Rev. Mol. Cell Bio 2007, 8:530-541.
3. Reinders J., Sickmann A. State-of-the-art in phosphoproteomics. Proteomics 2005, 5:4052-4061.
4. Ruprecht B., Lemeer S. Proteomic analysis of phosphorylation in cancer. Expert Rev. Proteomics 2014, 11:259-267.
5. Eyrich B., Sickmann A., Zahedi R.P. Catch me if you can: mass spectrometry-based phosphoproteomics and quantification strategies. Proteomics 2011, 11:554-570.
6. Du J.T., Li Y.M., Zhao Y.F., Nakagawa M., Qin X.R., Nemoto T., et al. MALDI-TOF mass spectrometry study of the phosphorylated tau peptides. Chinese. Chem. Lett 2004, 15:927-930.
7. Seidler J., Zinn N., Haaf E., Boehm M.E., Winter D., Schlosser A., et al. Metal ion-mobilizing additives for comprehensive detection of femtomole amounts of phosphopeptides by reversed phase LC-MS. Amino Acids 2011, 41:311-320.
8. Posewitz M.C., Tempst P. Immobilized gallium(III) affinity chromatography of phosphopeptides. Anal. Chem 1999, 71:2883-2892.
9. Leitner A. Phosphopeptide enrichment using metal oxide affinity chromatography. Trac-Trends Anal. Chem 2010, 29:177-185.
10. Pinto G., Caira S., Cuollo M., Lilla S., Fierro O., Addeo F. Hydroxyapatite as a concentrating probe for phosphoproteomic analyses. J. Chromatogr. B 2010, 878:2669-2678.
11. Zhang X., Ye J.Y., Jensen O.N., Roepstorff P. Highly efficient phosphopeptide enrichment by calcium phosphate precipitation combined with subsequent IMAC enrichment. Mol. Cell. Proteomics 2007, 6:2032-2042.
12. Dong M.M., Wu M.H., Wang F.J., Qin H.Q., Han G.H., Gong J., et al. Coupling strong anion-exchange monolithic capillary with MALDI-TOF MS for sensitive detection of phosphopeptides in protein digest. Anal. Chem 2010, 82:2907-2915.
13. Zhou H.L., Watts J.D., Aebersold R. A systematic approach to the analysis of protein phosphorylation. Nat. Biotechnol 2001, 19:375-378.
14. Ballif B.A., Carey G.R., Sunyaev S.R., Gygi S.P. Large-scale identification and evolution indexing of tyrosine phosphorylation sites from murine brain. J. Proteome Res 2008, 7:311-318.
15. 3+) affinity chromatography. Anal. Biochem 1986, 154:250-254.
16. 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, 2:1234-1243.
17. 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. Nat. Biotechnol 2002, 20:301-305.
18. Brill L.M., Salomon A.R., Ficarro S.B., Mukherji M., Stettler-Gill M., Peters E.C. Robust phosphoproteomic profiling of tyrosine phosphorylation sites from human T cells using immobilized metal affinity chromatography and tandem mass spectrometry. Anal. Chem 2004, 76:2763-2772.
19. Zhou H.J., Xu S.Y., Ye M.L., Feng S., Pan C., Jiang X.G., et al. Zirconium phosphonate-modified porous silicon for highly specific capture of phosphopeptides and MALDI-TOF MS analysis. J. Proteome Res 2006, 5:2431-2437.
20. Zhou H.J., Ye M.L., Dong J., Corradini E., Cristobal A., Heck A.J.R., et al. Robust phosphoproteome enrichment using monodisperse microsphere-based immobilized titanium (IV) ion affinity chromatography. Nat. Protoc 2013, 8:461-480.
21. Qin W.J., Zhang W.J., Song L.N., Zhang Y.J., Qian X.H. Surface initiated atom transfer radical polymerization: access to three dimensional wavelike polymer structure modified capillary columns for online phosphopeptide enrichment. Anal. Chem 2010, 82:9461-9468.
22. Qin H.Q., Wang F.J., Wang P.Y., Zhao L., Zhu J., Yang Q.H., et al. Phosphoric acid functionalized mesoporous organo-silica (EPO) as the adsorbent for in situ enrichment and isotope labeling of endogenous phosphopeptides. Chem. Commun 2012, 48:961-963.
23. Li X.S., Xu L.D., Zhu G.T., Yuan B.F., Feng Y.Q. Zirconium arsenate-modified magnetic nanoparticles: preparation, characterization and application to the enrichment of phosphopeptides. Analyst 2012, 137:959-967.
24. 4+ affinity chromatography microspheres for specific enrichment of phosphopeptides. Anal. Chim. Acta 2009, 636:34-41.
25. 4+-immobilized metal ion affinity chromatography for purification of acidic and basic phosphopeptides. Rapid Commun. Mass Spectrom 2012, 26:2186-2194.
26. Tsai C.F., Hsu C.C., Hung J.N., Wang Y.T., Choong W.K., Zeng M.Y., et al. Sequential phosphoproteomic enrichment through complementary metal-directed immobilized metal ion affinity chromatography. Anal. Chem 2014, 86:685-693.
27. Wang W.H., Dong J.L., Baker G.L., Bruening M.L. Bifunctional polymer brushes for low-bias enrichment of mono- and multi-phosphorylated peptides prior to mass spectrometry analysis. Analyst 2011, 136:3595-3598.
28. Mirza M.R., Rainer M., Messner C.B., Guzel Y., Schemeth D., Stasyk T., et al. A new type of metal chelate affinity chromatography using trivalent lanthanide ions for phosphopeptide enrichment. Analyst 2013, 138:2995-3004.
29. 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.
30. Kweon H.K., Hakansson K. Selective zirconium dioxide-based enrichment of phosphorylated peptides for mass spectrometric analysis. Anal. Chem 2006, 78:1743-1749.
31. Wang Y.B., Chen W., Wu J.S., Guo Y.L., Xia X.H. Highly efficient and of selective enrichment phosphopeptides using porous anodic alumina membrane for MALDI-TOF MS analysis. J. Am. Soc. Mass. Spectrm 2007, 18:1387-1395.
32. 2 enrichment for phosphopeptide analysis by liquid chromatography/tandem mass spectrometry. Rapid Commun. Mass Spectrom 2010, 24:1467-1474.
33. Sturm M., Leitner A., Smatt J.H., Linden M., Lindner W. Tin dioxide microspheres as a promising material for phosphopeptide enrichment prior to liquid chromatography-(tandem) mass spectrometry analysis. Adv. Funct. Mater 2008, 18:2381-2389.
34. Nelson C.A., Szczech J.R., Dooley C.J., Xu Q.G., Lawrence M.J., Zhu H.Y., et al. Effective enrichment and mass spectrometry analysis of phosphopeptides using mesoporous metal oxide nanomaterials. Anal. Chem 2010, 82:7193-7201.
35. Sun S.T., Ma H.T., Han G.H., Wu R.A., Zou H.F., Liu Y.W. Efficient enrichment and identification of phosphopeptides by cerium oxide using on-plate matrix-assisted laser desorption/ionization time-of-flight mass spectrometric analysis. Rapid Commun. Mass Spectrom 2011, 25:1862-1868.
36. Imami K., Sugiyama N., Kyono Y., Tomita M., Ishirama Y. Automated phosphoproteome analysis for cultured cancer cells by two-dimensional nanoLC-MS using a calcined titania/C18 biphasic column. Anal. Sci 2008, 24:161-166.
37. Leitner A., Sturm M., Hudecz O., Mazanek M., Smatt J.H., Linden M., et al. Probing the phosphoproteome of HeLa cells using nanocast metal oxide microspheres for phosphopeptide enrichment. Anal. Chem 2010, 82:2726-2733.
38. Ma R.N., Hu J.J., Cai Z.W., Ju H.X. Highly selective enrichment of phosphopeptides with high-index facets exposed octahedral tin dioxide nanoparticles for mass spectrometric analysis. Talanta 2014, 119:452-457.
39. Yan J.Y., Li X.L., Cheng S.Y., Ke Y.X., Liang X.M. Facile synthesis of titania-zirconia monodisperse microspheres and application for phosphopeptides enrichment. Chem. Commun 2009, 2929-2931.
40. 2-modified macroporous silica foams for advanced enrichment of multi-phosphorylated peptides. Chem. Eur. J. 2009, 15:2504-2508.
41. Zhang Y., Chen C., Qin H.Q., Wu R.A., Zou H.F. The synthesis of Ti-hexagonal mesoporous silica for selective capture of phosphopeptides. Chem. Commun 2010, 46:2271-2273.
42. Wang F.Q., Shi Z.H., Hu F., Xia Z.R., Wang L. Tuning of Ti-doped mesoporous silica for highly efficient enrichment of phosphopeptides in human placenta mitochondria. Anal. Bioanal. Chem 2013, 405:1683-1693.
43. Wu J.H., Xiao K., Zhao Y., Zhang W.P., Guo L., Feng Y.Q. Preparation and characterization of ceria-zirconia composite for enrichment and identification of phosphopeptides. J. Sep. Sci 2010, 33:2361-2368.
44. Wu J.H., Xiao K., Zhao Y., Zhang W.P., Guo L., Feng Y.Q. Synthesis and characterization of silica-zirconia composite for the enrichment of phosphopeptides. Chinese J. Anal. Chem 2010, 38:1231-1237.
45. Wang M.Y., Deng C.H., Li Y., Zhang X.M. Magnetic binary metal oxides affinity probe for highly selective enrichment of phosphopeptides. Acs Appl. Mater. Inter 2014, 6:11775-11782.
46. Larsen M.R., Thingholm T.E., Jensen O.N., Roepstorff P., Jorgensen T.J.D. Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell. Proteomics 2005, 4:873-886.
47. 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. Mol. Cell. Proteomics 2007, 6:1103-1109.
48. Wu J., Shakey Q., Liu W., Schuller A., Follettie M.T. Global profiling of phosphopeptides by titania affinity enrichment. J. Proteome Res 2007, 6:4684-4689.
49. Yu L.R., Zhu Z.Y., Chan K.C., Issaq H.J., Dimitrov D.S., Veenstra T.D. Improved titanium dioxide enrichment of phosphopeptides from HeLa cells and high confident phosphopeptide identification by cross-validation of MS/MS and MS/MS/MS spectra. J. Proteome Res 2007, 6:4150-4162.
50. 2-based phosphopeptide enrichment for automated multidimensional liquid chromatography coupled to tandem mass spectrometry. Anal. Chem 2007, 79:4666-4673.
51. Simon E.S., Young M., Chan A., Bao Z.Q., Andrews P.C. Improved enrichment strategies for phosphorylated peptides on titanium dioxide using methyl esterification and pH gradient elution. Anal. Biochem 2008, 377:234-242.
52. Fonslow B.R., Niessen S.M., Singh M., Wong C.C.L., Xu T., Carvalho P.C., et al. Single-step inline hydroxyapatite enrichment facilitates identification and quantitation of phosphopeptides from mass-limited proteomes with MudPIT. J. Proteome Res 2012, 11:2697-2709.
53. Xu B., Zhou L.P., Wang F.J., Qin H.Q., Zhu J., Zou H.F. Selective capture of phosphopeptides by hierarchical Ti-aluminophosphate-5 molecular sieves. Chem. Commun 2012, 48:1802-1804.
54. Xu B., Chen C., Wang F.J., Bian Y.Y., Cheng K., Qin H.Q., et al. High specific phosphopeptides enrichment by titanium silicalite with post-treatment of desilication. Anal. Methods 2013, 5:2939-2946.
55. Guzel Y., Hussain S., Rainer M., Bonn G.K. Highly selective enrichment of phosphopeptides using aluminum silicate. Anal. Methods 2014, 6:9160-9167.
56. 4 (RE = Yb, Gd, Y) hollow microspheres covered with nanothorns as affinity probes for selectively capturing and labeling phosphopeptides. Chem. Eur. J. 2012, 18:2014-2020.
57. Li L.P., Liu J.Z., Xu L.N., Li Z., Bai Y., Xiao Y.L., et al. GdF3 as a promising phosphopeptide affinity probe and dephospho-labelling medium: experiments and theoretical explanation. Chem. Commun 2014, 50:11572-11575.
58. Li X.S., Chen X., Sun H., Yuan B.F., Feng Y.Q. Perovskite for the highly selective enrichment of phosphopeptides. J. Chromatogr. A 2015, 1376:143-148.
59. Ruse C.I., McClatchy D.B., Lu B.W., Cociorva D., Motoyama A., Park S.K., et al. Motif-specific sampling of phosphoproteomes. J. Proteome Res 2008, 7:2140-2150.
60. Pink M., Verma N., Polato F., Bonn G.K., Baba H.A., Rettenmeier A.W., et al. Precipitation by lanthanum ions: a straightforward approach to isolating phosphoproteins. J. Proteomics 2011, 75:375-383.
61. Guzel Y., Rainer M., Mirza M.R., Bonn G.K. Highly efficient precipitation of phosphoproteins using trivalent europium, terbium, and erbium ions. Anal. Bioanal. Chem 2012, 403:1323-1331.
62. Mirza M.R., Rainer M., Guzel Y., Choudhary I.M., Bonn G.K. A novel strategy for phosphopeptide enrichment using lanthanide phosphate co-precipitation. Anal. Bioanal. Chem 2012, 404:853-862.
63. Guzel Y., Rainer M., Mirza M.R., Messner C.B., Bonn G.K. Highly selective recovery of phosphopeptides using trypsin-assisted digestion of precipitated lanthanide-phosphoprotein complexes. Analyst 2013, 138:2897-2905.
64. Atakay M., Celikbicak O., Salih B. Amine-functionalized sol-gel-based lab-in-a-pipet-tip approach for the fast enrichment and specific purification of phosphopeptides in MALDI-MS applications. Anal. Chem 2012, 84:2713-2720.
65. Chen C.T., Wang L.Y., Ho Y.P. Use of polyethylenimine-modified magnetic nanoparticles for highly specific enrichment of phosphopeptides for mass spectrometric analysis. Anal. Bioanal. Chem 2011, 399:2795-2806.
66. Hennrich M.L., van den Toorn H.W.P., Groenewold V., Heck A.J.R., Mohammed S. Ultra acidic strong cation exchange enabling the efficient enrichment of basic phosphopeptides. Anal. Chem 2012, 84:1804-1808.
67. Kettenbach A.N., Gerber S.A. Rapid and reproducible single-stage phosphopeptide enrichment of complex peptide mixtures: application to general and phosphotyrosine-specific phosphoproteomics experiments. Anal. Chem 2011, 83:7635-7644.
68. 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. Nat. Methods 2005, 2:591-598.
69. McLachlin D.T., Chait B.T. Improved beta-elimination-based affinity purification strategy for enrichment of phosphopeptides. Anal. Chem 2003, 75:6826-6836.
70. Rush J., Moritz A., Lee K.A., Guo A., Goss V.L., Spek E.J., et al. Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol 2005, 23:94-101.
71. 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. Mol. Cell. Proteomics 2002, 1:517-527.
72. Cheng G., Wang Z.G., Liu Y.L., Zhang J.L., Sun D.H., Ni J.Z. Phosphoprotein/phosphopeptide enrichment and analysis based on nanostructured materials. Prog. Chem 2013, 25:620-632.
73. Zhao L., Qin H.Q., Wu R.A., Zou H.F. Recent advances of mesoporous materials in sample preparation. J. Chromatogr. A 2012, 1228:193-204.
74. Li X.S., Zhu G.T., Luo Y.B., Yuan B.F., Feng Y.Q. Synthesis and applications of functionalized magnetic materials in sample preparation. Trac-Trends Anal. Chem 2013, 45:233-247.
75. Zhang Y., Li L.L., Yang P.Y., Lu H.J. On-plate enrichment methods for MALDI-MS analysis in proteomics. Anal. Methods 2012, 4:2622-2631.
76. Najam-Ul-Haq M., Saeed A., Jabeen F., Maya F., Ashiq M.N., Sharif A. Newly developed poly(allyl glycidyl ether/divinyl benzene) polymer for phosphopeptides enrichment and desalting of biofluids. Acs Appl. Mater. Inter 2014, 6:3536-3545.
77. Saeed A., Maya F., Xiao D.N.J., Najam-ul-Haq M., Svec F., Britt D.K. Growth of a highly porous coordination polymer on a macroporous polymer monolith support for enhanced immobilized metal ion affinity chromatographic enrichment of phosphopeptides. Adv. Funct. Mater 2014, 24:5790-5797.
78. Zhao L., Qin H.Q., Hu Z.Y., Zhang Y., Wu R.A., Zou H.F. A poly(ethylene glycol)-brush decorated magnetic polymer for highly specific enrichment of phosphopeptides. Chem. Sci 2012, 3:2828-2838.
79. 4+ affinity chromatography for phosphopeptide enrichment. J. Sep. Sci 2013, 36:3563-3570.
80. 4+-chelated magnetic nanostructured affinity microspheres containing N-methylene phosphonic chitosan for highly selective enrichment and rapid separation of phosphopeptides. J. Mat. Chem. B 2014, 2:6886-6892.
81. Yan Y.H., Zheng Z.F., Li Y., Deng C.H., Zhang X.M. Titanium(IV)-immobilized hydrophilic hierarchically ordered macro-/mesoporous silica for fast enrichment of phosphopeptides. Chempluschem 2014, 79:662-666.
82. 4+-immobilized multilayer polysaccharide coated magnetic nanoparticles for highly selective enrichment of phosphopeptides. J. Mat. Chem. B 2014, 2:4473-4480.
83. He X.M., Zhu G.T., Zhu Y.Y., Chen X., Zhang Z., Wang S.T., et al. Facile preparation of biocompatible sulfhydryl cotton fiber-based sorbents by "thiol ene" click chemistry for biological analysis. Acs Appl. Mater. Inter 2014, 6:17857-17864.
84. Wang P.Y., Zhao L., Wu R., Zhong H., Zou H.F., Yang J., et al. Phosphonic acid functionalized periodic mesoporous organosilicas and their potential applications in selective enrichment of phosphopeptides. J. Phys. Chem. C 2009, 113:1359-1366.
85. Wei X.N., Shi X. Mesoporous zirconium phenylphosphonates for selective enrichment of phosphopeptides. J. Phys. Chem. C 2014, 118:4213-4221.
86. Zhang Y.H., Yu X.J., Wang X.Y., Shan W., Yang P.Y., Tang Y. Zeolite nanoparticles with immobilized metal ions: isolation and MALDI-TOF-MS/MS identification of phosphopeptides. Chem. Commun 2004, 40:2882-2883.
87. Hussain D., Najam-ul-Haq M., Jabeen F., Ashiq M.N., Athar M., Rainer M., et al. Functionalized diamond nanopowder for phosphopeptides enrichment from complex biological fluids. Anal. Chim. Acta 2013, 775:75-84.
88. Yan Y.H., Zheng Z.F., Deng C.H., Li Y., Zhang X.M., Yang P.Y. Hydrophilic polydopamine-coated graphene for metal ion immobilization as a novel immobilized metal ion affinity chromatography platform for phosphoproteome analysis. Anal. Chem 2013, 85:8483-8487.
89. Wu H.T., Hsu C.C., Tsai C.F., Lin P.C., Lin C.C., Chen Y.J. Nanoprobe-based immobilized metal affinity chromatography for sensitive and complementary enrichment of multiply phosphorylated peptides. Proteomics 2011, 11:2639-2653.
90. Xu X.Q., Deng C.H., Gao M.X., Yu W.J., Yang P.Y., Zhang X.M. Synthesis of magnetic microspheres with immobilized metal ions for enrichment and direct determination of phosphopeptides by matrix-assisted laser desorption ionization mass spectrometry. Adv. Mater 2006, 18:3289-3293.
91. Li Y., Qi D.W., Deng C.H., Yang P.Y., Zhang X.M. Cerium ion-chelated magnetic silica microspheres for enrichment and direct determination of phosphopeptides by matrix-assisted laser desorption ionization mass spectrometry. J. Proteome Res 2008, 7:1767-1777.
92. 4+ ions for selective enrichment of the phosphopeptides. J. Chromatogr. A 2010, 1217:2606-2617.
93. Li X.S., Wu J.H., Zhao Y., Zhang W.P., Gao Q., Guo L., et al. Preparation of magnetic polymer material with phosphate group and its application to the enrichment of phosphopeptides. J. Chromatogr. A 2011, 1218:3845-3853.
94. 4+-immobilized magnetic composite microspheres for highly selective enrichment of phosphopeptides. Adv. Funct. Mater 2013, 23:107-115.
95. Wang Z.G., Cheng G., Liu Y.L., Zhang J.L., Sun D.H., Ni J.Z. Novel core-shell Cerium(IV)-immobilized magnetic polymeric microspheres for selective enrichment and rapid separation of phosphopeptides. J. Colloid Interf. Sci 2014, 417:217-226.
96. Lu J., Li Y., Deng C.H. Facile synthesis of zirconium phosphonate-functionalized magnetic mesoporous silica microspheres designed for highly selective enrichment of phosphopeptides. Nanoscale 2011, 3:1225-1233.
97. Li Y.C., Lin Y.S., Tsai P.J., Chen C.T., Chen W.Y., Chen Y.C. Nitrilotriacetic acid-coated magnetic nanoparticles as affinity probes for enrichment of histidine-tagged proteins and phosphorylated peptides. Anal. Chem 2007, 79:7519-7525.
98. 3+-immobilized magnetic nanoparticles for phosphoproteome analysis of the plasma membrane of mouse liver. J. Proteome Res 2008, 7:1078-1087.
99. Wei J.Y., Zhang Y.J., Wang J.L., Tan F., Liu J.F., Cai Y., et al. Highly efficient enrichment of phosphopeptides by magnetic nanoparticles coated with zirconium phosphonate for phosphoproteome analysis. Rapid Commun. Mass Spectrom 2008, 22:1069-1080.
100. Xu Y.D., Bruening M.L., Watson J.T. Use of polymer-modified MALDI-MS probes to improve analyses of protein digests and DNA. Anal. Chem 2004, 76:3106-3111.
101. Dunn J.D., Watson J.T., Bruening M.L. Detection of phosphopeptides using Fe(III)-nitrilotriacetate complexes immobilized on a MALDI plate. Anal. Chem 2006, 78:1574-1580.
102. Dunn J.D., Igrisan E.A., Palumbo A.M., Reid G.E., Bruening M.L. Phosphopeptide enrichment using MALDI plates modified with high-capacity polymer brushes. Anal. Chem 2008, 80:5727-5735.
103. Wang W.H., Bruening M.L. Phosphopeptide enrichment on functionalized polymer microspots for MALDI-MS analysis. Analyst 2009, 134:512-518.
104. Wang W.H., Palumbo A.M., Tan Y.J., Reid G.E., Tepe J.J., Bruening M.L. Identification of p65-associated phosphoproteins by mass spectrometry after on-plate phosphopeptide enrichment using polymer-oxotitanium films. J. Proteome Res 2010, 9:3005-3015.
105. Hoang T., Roth U., Kowalewski K., Belisle C., Steinert K., Karas M. Highly specific capture and direct MALDI MS analysis of phosphopeptides by zirconium phosphonate on self-assembled monolayers. Anal. Chem 2010, 82:219-228.
106. Hou C.Y., Ma J.F., Tao D.Y., Shan Y.C., Liang Z., Zhang L.H., et al. Organic-inorganic hybrid silica monolith based immobilized titanium ion affinity chromatography column for analysis of mitochondrial phosphoproteome. J. Proteome Res 2010, 9:4093-4101.
107. Wang H., Duan J.C., Xu H.J., Zhao L., Liang Y., Shan Y.C., et al. Monoliths with immobilized zirconium ions for selective enrichment of phosphopeptides. J. Sep. Sci 2011, 34:2113-2121.
108. 2 microspheres with high specific surface area for selective enrichment of phosphopeptides by mass spectrometric analysis. J. Chromatogr. A 2010, 1217:2197-2205.
109. 2 nanocrystal clusters for selective enrichment of phosphopeptides. Anal. Chem 2010, 82:7249-7258.
110. Zhang L.Y., Xu J., Sun L.L., Ma J.F., Yang K.G., Liang Z., et al. Zirconium oxide aerogel for effective enrichment of phosphopeptides with high binding capacity. Anal. Bioanal. Chem 2011, 399:3399-3405.
111. 2 aerogel for selective enrichment of phosphopeptides in rat liver mitochondria. Anal. Chim. Acta 2012, 729:26-35.
112. 3 nanocrystal clusters. Acs Appl. Mater. Inter 2013, 5:614-621.
113. 2 nanospheres for efficient phosphopeptide enrichment. J. Mat. Chem. B 2014, 2:1121-1124.
114. He X.M., Zhu G.T., Li X.S., Yuan B.F., Shi Z.G., Feng Y.Q. Rapid enrichment of phosphopeptides by SiO2-TiO2 composite fibers. Analyst 2013, 138:5495-5502.
115. Wan H.H., Yan J.Y., Yu L., Zhang X.L., Xue X.Y., Li X.L., et al. Zirconia layer coated mesoporous silica microspheres used for highly specific phosphopeptide enrichment. Talanta 2010, 82:1701-1707.
116. 2-functionalized mesoporous materials for sensitive analysis of multi-phosphopeptides. Sci. China-Chem 2011, 54:1327-1333.
117. Rainer M., Sonderegger H., Bakry R., Huck C.W., Morandell S., Huber L.A., et al. Analysis of protein phosphorylation by monolithic extraction columns based on poly(divinylbenzene) containing embedded titanium dioxide and zirconium dioxide nano-powders. Proteomics 2008, 8:4593-4602.
118. 2 nanoparticle-deposited capillary column by liquid phase deposition and its application in phosphopeptide analysis. J. Chromatogr. A 2008, 1192:95-102.
119. Fang G.Z., Gao W., Deng Q.L., Qian K., Han H.T., Wang S. Highly selective capture of phosphopeptides using a nano titanium dioxide-multiwalled carbon nanotube nanocomposite. Anal. Biochem 2012, 423:210-217.
120. Tang L.A.L., Wang J.Z., Lim T.K., Bi X.Z., Lee W.C., Lin Q.S., et al. High-performance graphene-titania platform for detection of phosphopeptides in cancer cells. Anal. Chem 2012, 84:6693-6700.
121. Yan Y.H., Zhang X.M., Deng C.H. Designed synthesis of titania nanoparticles coated hierarchially ordered macro/mesoporous silica for selective enrichment of phosphopeptides. Acs Appl. Mater. Inter 2014, 6:5467-5471.
122. 2-modified membranes and investigation of tau protein phosphorylation. Anal. Chem 2013, 85:5699-5706.
123. Pang H., Lu Q.Y., Gao F. Graphene oxide induced growth of one-dimensional fusiform zirconia nanostructures for highly selective capture of phosphopeptides. Chem. Commun 2011, 47:11772-11774.
124. 2 core-shell-structured microspheres and their applications in selectively enriching phosphopeptides and removing phospholipids. J. Chromatogr. A 2013, 1275:9-16.
125. 2 microspheres with yolk-shell structure: designed synthesis and application in highly selective enrichment of phosphopeptides. Langmuir 2014, 30:6602-6611.
126. 2-coated carbon-encapsulated iron nanoparticles. Proteomics 2012, 12:380-390.
127. 2 composites for the highly selective enrichment of phosphopeptides from biological samples. Acs Appl. Mater. Inter 2013, 5:7330-7334.
128. Yan Y.H., Zheng Z.F., Deng C.H., Zhang X.M., Yang P.Y. Selective enrichment of phosphopeptides by titania nanoparticles coated magnetic carbon nanotubes. Talanta 2014, 118:14-20.
129. 2 microspheres with a tunable mesoporous anatase shell for highly selective and effective enrichment of phosphopeptides. ACS Nano 2012, 6:3179-3188.
130. Cheng G., Wang Z.G., Liu Y.L., Zhang J.L., Sun D.H., Ni J.Z. Magnetic affinity microspheres with meso-/macroporous shells for selective enrichment and fast separation of phosphorylated biomolecules. Acs Appl. Mater. Inter 2013, 5:3182-3190.
131. Wu J.H., Li X.S., Zhao Y., Gao Q.A., Guo L., Feng Y.Q. Titania coated magnetic mesoporous hollow silica microspheres: fabrication and application to selective enrichment of phosphopeptides. Chem. Commun 2010, 46:9031-9033.
132. Ji L.Y., Wu J.H., Luo Q., Li X.C., Zheng W., Zhai G.J., et al. Quantitative mass spectrometry combined with separation and enrichment of phosphopeptides by titania coated magnetic mesoporous silica microspheres for screening of protein kinase inhibitors. Anal. Chem 2012, 84:2284-2291.
133. Li X.S., Pan Y.N., Zhao Y., Yuan B.F., Guo L., Feng Y.Q. Preparation of titanium-grafted magnetic mesoporous silica for the enrichment of endogenous serum phosphopeptides. J. Chromatogr. A 2013, 1315:61-69.
134. Li X.S., Su X., Zhu G.T., Zhao Y., Yuan B.F., Guo L., et al. Titanium-containing magnetic mesoporous silica spheres: effective enrichment of peptides and simultaneous separation of nonphosphopeptides and phosphopeptides. J. Sep. Sci 2012, 35:1506-1513.
135. Qiao L., Roussel C., Wan J.J., Yang P.Y., Girault H.H., Liu B.H. Specific on-plate enrichment of phosphorylated peptides for direct MALDI-TOF MS analysis. J. Proteome Res 2007, 6:4763-4769.
136. Torta F., Fusi M., Casari C.S., Bottani C.E., Bachi A. Titanium dioxide coated MALDI plate for on target analysis of phosphopeptides. J. Proteome Res 2009, 8:1932-1942.
137. 2 arrays for on-plate selective enrichment of phosphopeptides and direct MALDI MS analysis. Anal. Chem 2011, 83:1624-1631.
138. Chen C.J., Lai C.C., Tseng M.C., Liu Y.C., Liu Y.H., Chiou L.W., et al. A novel titanium dioxide-polydimethylsiloxane plate for phosphopeptide enrichment and mass spectrometry analysis. Anal. Chim. Acta 2014, 812:105-113.
139. Eriksson A., Bergquist J., Edwards K., Hagfeldt A., Malmstrom D., Hernandez V.A. Optimized protocol for on-target phosphopeptide enrichment prior to matrix-assisted laser desorption-ionization mass spectrometry using mesoporous titanium dioxide. Anal. Chem 2010, 82:4577-4583.
140. Eriksson A.I.K., Bartsch M., Bergquist J., Edwards K., Lind S.B., Hernandez V.A. On-target titanium dioxide-based enrichment for characterization of phosphorylations in the Adenovirus pIIIa protein. J. Chromatogr. A 2013, 1317:105-109.
141. Blacken G.R., Volny M., Vaisar T., Sadilek M., Turecek F. In situ enrichment of phosphopeptides on MALDI plates functionalized by reactive landing of zirconium(IV)-n-propoxide ions. Anal. Chem 2007, 79:5449-5456.
142. Lu J., Liu S.S., Deng C.H. Facile synthesis of alumina hollow spheres for on-plate-selective enrichment of phosphopeptides. Chem. Commun 2011, 47:5334-5336.
143. Krasny L., Pompach P., Strohalm M., Obsilova V., Strnadova M., Novak P., et al. In-situ enrichment of phosphopeptides on MALDI plates modified by ambient ion landing. J. Mass Spectrom 2012, 47:1294-1302.
144. Krenkova J., Foret F. Iron oxide nanoparticle coating of organic polymer-based monolithic columns for phosphopeptide enrichment. J. Sep. Sci 2011, 34:2106-2112.
145. 2 composite monolithic capillary column and its application in enrichment of phosphopeptides. Anal. Chem 2012, 84:7763-7770.
146. Cheng G., Liu Y.L., Wang Z.G., Li S.M., Zhang J.L., Ni J.Z. Yolk-shell magnetic microspheres with mesoporous yttrium phosphate shells for selective capture and identification of phosphopeptides. J. Mat. Chem. B 2013, 1:3661-3669.
147. Krenkova J., Lacher N.A., Svec F. Control of selectivity via nanochemistry: monolithic capillary column containing hydroxyapatite nanoparticles for separation of proteins and enrichment of phosphopeptides. Anal. Chem 2010, 82:8335-8341.
148. 3 nanoparticles after microwave-assisted tryptic digest of phosphoproteins, and their identification by MALDI-MS. Microchim. Acta 2012, 179:83-90.
149. Xu L.N., Li L.P., Jin L., Bai Y., Liu H.W. Guanidyl-functionalized graphene as a bifunctional adsorbent for selective enrichment of phosphopeptides. Chem. Commun 2014, 50:10963-10966.
150. Yu Q., Li X.S., Yuan B.F., Feng Y.Q. Preparation of magnetic hydroxyapatite clusters and their application in the enrichment of phosphopeptides. J. Sep. Sci 2014, 37:580-586.
151. Sun Y., Wang H.F. Ultrathin-yttrium phosphate-shelled polyacrylate-ferriferrous oxide magnetic microspheres for rapid and selective enrichment of phosphopeptides. J. Chromatogr. A 2013, 1316:62-68.
152. Deng Q.L., Wu J.H., Chen Y., Zhang Z.J., Wang Y., Fang G.Z., et al. Guanidinium functionalized superparamagnetic silica spheres for selective enrichment of phosphopeptides and intact phosphoproteins from complex mixtures. J. Mat. Chem. B 2014, 2:1048-1058.
153. Condina M.R., Guthridge M.A., McColl S.R., Hoffmann P. A sensitive magnetic bead method for the detection and identification of tyrosine phosphorylation in proteins by MALDI-TOF/TOF MS. Proteomics 2009, 9:3047-3057.
154. 4 (RE = La, Nd, Eu) affinity nanorods modified on a MALDI plate for rapid capture of target peptides from complex biosamples. Chem. Commun 2013, 49:8492-8494.
155. Cohen P. The regulation of protein function by multisite phosphorylation - a 25 year update. Trends Biochem. Sci 2000, 25:596-601.
156. 2 enrichment in combination with MALDI TOF/TOF MS. Proteomics 2008, 8:4577-4592.
157. Qiao L.A., Bi H.Y., Busnel J.M., Hojeij M., Mendez M., Liu B.H., et al. Controlling the specific enrichment of multi-phosphorylated peptides on oxide materials: aluminium foil as a target plate for laser desorption ionization mass spectrometry. Chem. Sci 2010, 1:374-382.
158. 2 enhances the separation of multi- and monophosphorylated peptides and increases phosphoprotein profiling. J. Proteome Res 2013, 12:2467-2476.
159. Li X.S., Chen X., Yuan B.F., Feng Y.Q. Phosphonate-modified metal oxides for the highly selective enrichment of phosphopeptides. RSC Adv 2015, 5:7832-7841.
160. Mamone G., Picariello G., Ferranti P., Addeo F. Hydroxyapatite affinity chromatography for the highly selective enrichment of mono- and multi-phosphorylated peptides in phosphoproteome analysis. Proteomics 2010, 10:380-393.
161. 6: a novel binary affinity probe for global phosphopeptide detection. Chem. Commun 2013, 49:1762-1764.
162. 4 magnetic nanoparticles. Nat. Commun 2013, 4:1-7.
163. Shiau K.J., Hung S.U., Lee H.W., Wu C.C. Nanodiamond-based two-step sampling of multiply and singly phosphorylated peptides for MALDI-TOF mass spectrometry analysis. Analyst 2011, 136:1922-1927.
164. Li X.L., Guo Z.M., Sheng Q.Y., Xue X.Y., Liang X.M. Sequential elution of multiply and singly phosphorylated peptides with polar-copolymerized mixed-mode RP18/SCX material. Analyst 2012, 137:2774-2776.
165. Fischnaller M., Bakry R., Vallant R.M., Huber L.A., Bonn G.K. C-60-fullerene bound silica for the preconcentration and the fractionation of multiphosphorylated peptides. Anal. Chim. Acta 2013, 761:92-101.
166. Villanueva J., Shaffer D.R., Philip J., Chaparro C.A., Erdjument-Bromage H., Olshen A.B., et al. Differential exoprotease activities confer tumor-specific serum peptidome patterns. J. Clin. Invest 2006, 116:271-284.
167. Zou L.J., Li J., Wan H.H., Li X.L., Liang X.M. Selective enrichment of endogenous serum phosphopeptides with ultrafiltration membrane intercept-titanium dioxide chromatography coupled with nano ultra high pressure liquid chromatography-quadrupole-time of flight mass spectrometry. Chinese J. Anal. Chem 2011, 39:1781-1786.
168. Hu L.H., Zhou H.J., Li Y.H., Sun S.T., Guo L.H., Ye M.L., et al. Profiling of endogenous serum phosphorylated peptides by titanium (IV) immobilized mesoporous silica particles enrichment and MALDI-TOFMS detection. Anal. Chem 2009, 81:94-104.
169. 2 nanocomposite for selective enrichment of endogenous phosphopeptides from a complex sample. RSC Adv 2014, 4:45804-45808.