Phosphoproteomics and cancer research

Clinical and Translational Oncology

Volumn 11, Issue 6, 2009, Pages 356-362

  Ashman, Keith ^a   Villar, Elena López ^a  

^a Centro Nacional de Investigaciones Oncológicas   (Spain)

Author keywords

Cancer; Immobilised metal ion affinity chromatography (IMAC); Kinase signalling; Mass spectrometry (MS); Protein phosphorylation; Titanium dioxide

Indexed keywords

ANTINEOPLASTIC AGENT; PHOSPHOPROTEIN; PROTEIN KINASE INHIBITOR; TITANIUM; TITANIUM DIOXIDE; TUMOR PROTEIN; ZIRCONIUM; ZIRCONIUM OXIDE;

AFFINITY CHROMATOGRAPHY; ANIMAL; BIOLOGY; DRUG ANTAGONISM; DRUG DELIVERY SYSTEM; DRUG EFFECT; GENETICS; HUMAN; IMMUNOPRECIPITATION; ION EXCHANGE CHROMATOGRAPHY; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; MOUSE; NEOPLASM; PEPTIDE MAPPING; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN MICROARRAY; PROTEIN PROCESSING; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; ANTINEOPLASTIC AGENTS; CHROMATOGRAPHY, AFFINITY; CHROMATOGRAPHY, ION EXCHANGE; COMPUTATIONAL BIOLOGY; DRUG DELIVERY SYSTEMS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HUMANS; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MICE; NEOPLASM PROTEINS; NEOPLASMS; PEPTIDE MAPPING; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN ARRAY ANALYSIS; PROTEIN KINASE INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS; SIGNAL TRANSDUCTION; TITANIUM; ZIRCONIUM;

EID: 73349139521     PISSN: 1699048X     EISSN: 16993055     Source Type: Journal    
DOI: 10.1007/s12094-009-0369-z     Document Type: Article

References (100)

1. Yarbro JW (1992) Oncogenes and cancer suppressor genes. Semin Oncol Nurs 8:30.
2. Martin KK, Pilkington GJ (1998) Nm23: an invasion suppressor gene in CNS tumours? Anticancer Res 18:919.
3. Senderowicz AM (2003) Novel small molecule cyclin-dependent kinases modulators in human clinical trials. Cancer Biol Ther 2:S84.
4. Ha TK, An JY, Youn HG et al (2007) Surgical outcome of synchronous second primary cancer in patients with gastric cancer. Yonsei Med J 48:981.
5. Chong PK, Lee H, Kong JW et al (2008) Phosphoproteomics, oncogenic signaling and cancer research. Proteomics 8:4370.
6. Malumbres M, Barbacid M (2009) Cell cycle, CDKs and cancer: a changing paradigm. Nat Rev Cancer 9:153.
7. Sathornsumetee S, Reardon DA (2009) Targeting multiple kinases in glioblastoma multiforme. Exp Opin Investig Drugs 18:277.
8. Wrighton KH, Lin X, Yu PB, Feng XH (2009) TGFbeta can stimulate Smad1 phosphorylation independently of BMP receptors. J Biol Chem 19:8.
9. Futreal PA, Coin L, Marshall M et al (2004) A census of human cancer genes. Nat Rev Cancer 4:177.
10. Forbes SA, Bhamra G, Bamford S et al (2008) The Catalogue of Somatic Mutations in Cancer (COSMIC). Curr Protoc Hum Genet Chapter 10:Unit 10 11.
11. Malumbres M, Barbacid M (2007) Cell cycle kinases in cancer. Curr Opin Genet Dev 17:60.
12. Rane SG, Reddy EP (2000) Janus kinases: components of multiple signaling pathways. Oncogene 19:5662.
13. Reddy EP, Korapati A, Chaturvedi P, Rane S (2000) IL-3 signaling and the role of Src kinases, JAKs and STATs: a covert liaison unveiled. Oncogene 19:2532.
14. Gaestel M, Mengel A, Bothe U, Asadullah K (2007) Protein kinases as small molecule inhibitor targets in inflammation. Curr Med Chem 14:2214.
15. Giamas G, Stebbing J, Vorgias CE, Knippschild U (2007) Protein kinases as targets for cancer treatment. Pharmacogenomics 8:1005.
16. Ralph SJ (2007) An update on malignant melanoma vaccine research: insights into mechanisms for improving the design and potency of melanoma therapeutic vaccines. Am J Clin Dermatol 8:123.
17. Bixby DL, Talpaz M (2008) Efficacy of various doses and schedules of second-generation tyrosine kinase inhibitors. Clin Lymphoma Myeloma 8[SUPPL. 3]:S95.
18. Perez de Castro I, de Carcer G, Montoya G, Malumbres M (2008) Emerging cancer therapeutic opportunities by inhibiting mitotic kinases. Curr Opin Pharmacol 8:375.
19. Traxler P, Bold G, Buchdunger E et al (2001) Tyrosine kinase inhibitors: from rational design to clinical trials. Med Res Rev 21:499.
20. Mann M, Ong SE, Gronborg M et al (2002) Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol 20:261.
21. Mann M, Jensen ON (2003) Proteomic analysis of post-translational modifi cations. Nat Biotechnol 21:255.
22. Jensen ON (2004) Modification-specific proteomics: characterization of post-translational modifi - cations by mass spectrometry. Curr Opin Chem Biol 8:33.
23. Delom F, Chevet E (2006) Phosphoprotein analysis: from proteins to proteomes. Proteome Sci 4:15.
24. Jensen ON (2006) Interpreting the protein language using proteomics. Nat Rev Mol Cell Biol 7:391.
25. Bonilla L, Means G, Lee K, Patterson S (2008) The evolution of tools for protein phosphorylation site analysis: from discovery to clinical application. Biotechniques 44:671.
26. Sopko R, Andrews BJ (2008) Linking the kinome and phosphorylome: a comprehensive review of approaches to find kinase targets. Mol Biosyst 4:920.
27. Virshup DM, Shenolikar S (2009) From promiscuity to precision: protein phosphatases get a makeover. Mol Cell 33:537.
28. Gronborg M, Kristiansen TZ, Stensballe A et al (2002) A mass spectrometry-based proteomic approach for identification of serine/ threoninephosphorylated proteins by enrichment with phospho- specifi c antibodies: identifi cation of a novel protein, Frigg, as a protein kinase A substrate. Mol Cell Proteomics 1:517.
29. Zhang ZY (2005) Functional studies of protein tyrosine phosphatases with chemical approaches. Biochim Biophys Acta 1754:100.
30. Jensen SS, Larsen MR (2007) Evaluation of the impact of some experimental procedures on different phosphopeptide enrichment techniques. Rapid Commun Mass Spectrom 21:3635.
31. Springer WR (1991) A method for quantifying radioactivity associated with protein in silverstained polyacrylamide gels. Anal Biochem 195:172.
32. Wyttenbach A, Tolkovsky AM (2006) Differential phosphoprotein labeling (DIPPL), a method for comparing live cell phosphoproteomes using simultaneous analysis of (33)P- and (32)P-labeled proteins. Mol Cell Proteomics 5:553.
33. Ong SE, Mann M (2005) Mass spectrometrybased proteomics turns quantitative. Nat Chem Biol 1:252.
34. Blaukat A (2004) Identification of G-protein-coupled receptor phosphorylation sites by 2D phosphopeptide mapping. Methods Mol Biol 259:283.
35. Gafken PR, Lampe PD (2006) Methodologies for characterizing phosphoproteins by mass spectrometry. Cell Commun Adhes 13:249.
36. Zhang H, Zha X, Tan Y et al (2002) Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs. J Biol Chem 277:39379.
37. Rush J, Moritz A, Lee KA et al (2005) Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat Biotechnol 23:94.
38. Di Vizio D, Solomon KR, Freeman MR (2008) Cholesterol and cholesterol-rich membranes in prostate cancer: an update. Tumori 94:633.
39. Dietz A, Boehm A, Mozet C et al (2008) Current aspects of targeted therapy in head and neck tumors. Eur Arch Otorhinolaryngol 265[SUPPL. 1]:S3.
40. Huang F, Gu H (2008) Negative regulation of lymphocyte development and function by the Cbl family of proteins. Immunol Rev 224:229.
41. Shah NP (2008) Advanced CML: therapeutic options for patients in accelerated and blast phases. J Natl Compr Canc Netw 6[SUPPL. 2]:S31.
42. Steen H, Kuster B, Mann M (2001) Quadrupole time-of-flight versus triple-quadrupole mass spectrometry for the determination of phosphopeptides by precursor ion scanning. J Mass Spectrom 36:782.
43. Ballif BA, Carey GR, Sunyaev SR, Gygi SP (2008) Large-scale identification and evolution indexing of tyrosine phosphorylation sites from murine brain. J Proteome Res 7:311.
44. Ficarro SB, McCleland ML, Stukenberg PT et al (2002) Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat Biotechnol 20:301.
45. Andersson L, Porath J (1986) Isolation of phosphoproteins by immobilized metal (Fe3+) affinity chromatography. Anal Biochem 154:250.
46. Neville DC, Rozanas CR, Price EM et al (1997) Evidence for phosphorylation of serine 753 in CFTR using a novel metal-ion affinity resin and matrix-assisted laser desorption mass spectrometry. Protein Sci 6:2436.
47. Figeys D, Gygi SP, McKinnon G, Aebersold R (1998) An integrated microfl uidics-tandem mass spectrometry system for automated protein analysis. Anal Chem 70:3728.
48. Li S, Dass C (1999) Iron (III)-immobilized metal ion affinity chromatography and mass spectrometry for the purifi cation and characterization of synthetic phosphopeptides. Anal Biochem 270:9.
49. Posewitz MC, Tempst P (1999) Immobilized gallium(III) affinity chromatography of phosphopeptides. Anal Chem 71:2883.
50. Pinkse MW, Uitto PM, Hilhorst MJ, Ooms B, Heck AJ (2004) Selective isolation at the femtomole level of phosphopeptides from proteolytic digests using 2D-NanoLC-ESI-MS/MS and titanium oxide precolumns. Anal Chem 76:3935.
51. Nuhse TS, Stensballe A, Jensen ON, Peck SC (2003) Large-scale analysis of in vivo phosphorylated membrane proteins by immobilized metal ion affinity chromatography and mass spectrometry. Mol Cell Proteomics 2:1234.
52. Connor PA, Dobson KD, McQuillan J (1999) Infrared Spectroscopy of the TiO2/Aqueous Solution Interface. Langmuir 15:2402.
53. Connor PA, McQuillan A (1999) Phosphate adsorption onto TiO2 from aqueous solutions: an in situ internal refl ection infrared spectroscopic study. Langmuir 15:2916.
54. Pinkse MW, Uitto PM, Hilhorst MJ et al (2004) Selective isolation at the femtomole level of phosphopeptides from proteolytic digests using 2DNanoLC- ESI-MS/MS and titanium oxide precolumns. Anal Chem 76:3935.
55. Larsen MR, Thingholm TE, Jensen ON et al (2005) Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol Cell Proteomics 4:873.
56. Thingholm TE, Larsen MR (2009) The use of titanium dioxide micro-columns to selectively isolate phosphopeptides from proteolytic digests. Methods Mol Biol 527:57.
57. Thingholm TE, Jensen ON, Larsen MR (2009) Enrichment and separation of mono- and multiply phosphorylated peptides using sequential elution from IMAC prior to mass spectrometric analysis. Methods Mol Biol 527:67.
58. Thingholm TE, Jensen ON, Robinson PJ, Larsen MR (2008) SIMAC (sequential elution from IMAC), a phosphoproteomics strategy for the rapid separation of monophosphorylated from multiply phosphorylated peptides. Mol Cell Proteomics 7:661.
59. Kweon HK, Hakansson K (2006) Selective zirconium dioxide-based enrichment of phosphorylated peptides for mass spectrometric analysis. Anal Chem 78:1743.
60. Zhou H, Tian R, Ye M et al (2007) Highly specific enrichment of phosphopeptides by zirconium dioxide nanoparticles for phosphoproteome analysis. Electrophoresis 28:2201.
61. Peng J, Elias JE, Thoreen CC et al (2003) Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J Proteome Res 2:43.
62. Gruhler A, Olsen JV, Mohammed S et al (2005) Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Mol Cell Proteomics 4:310.
63. Villen J, Gygi SP (2008) The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry. Nat Protoc 3:1630.
64. Beausoleil SA, Jedrychowski M, Schwartz D et al (2004) Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc Natl Acad Sci U S A 101:12130.
65. Zhang X, Ye J, Jensen ON, Roepstorff P (2007) Highly efficient phosphopeptide enrichment by calcium phosphate precipitation combined with subsequent IMAC enrichment. Mol Cell Proteomics 6:2032.
66. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silverstained polyacrylamide gels. Anal Chem 68:850.
67. Wilm M, Shevchenko A, Houthaeve T et al (1996) Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379:466.
68. Gobom J, Nordhoff E, Mirgorodskaya E et al (1999) Sample purifi cation and preparation technique based on nano-scale reversed-phase columns for the sensitive analysis of complex peptide mixtures by matrix-assisted laser desorption/ionization mass spectrometry. J Mass Spectrom 34:105.
69. Larsen MR, Graham ME, Robinson PJ, Roepstorff P (2004) Improved detection of hydrophilic phosphopeptides using graphite powder microcolumns and mass spectrometry: evidence for in vivo doubly phosphorylated dynamin I and dynamin III. Mol Cell Proteomics 3:456.
70. Karas M, Hillenkamp F (1988) Laser desorption ionization of proteins with molecular masses exceeding 10, 000 daltons. Anal Chem 60:2299.
71. Fenn JB, Mann M, Meng CK et al (1989) Electrospray ionization for mass spectrometry of large biomolecules. Science 246:64.
72. Shou W, Verma R, Annan RS et al (2002) Mapping phosphorylation sites in proteins by mass spectrometry. Methods Enzymol 351:279.
73. Carr SA, Annan RS, Huddleston MJ (2005) Mapping posttranslational modifi cations of proteins by MS-based selective detection: application to phosphoproteomics. Methods Enzymol 405:82.
74. Dunn JD, Reid GE, Bruening ML (2009) Techniques for phosphopeptide enrichment prior to analysis by mass spectrometry. Mass Spectrom Rev [Epub ahead of print].
75. Cooper HJ, Hakansson K, Marshall AG (2005) The role of electron capture dissociation in biomolecular analysis. Mass Spectrom Rev 24:201.
76. Wu SL, Huhmer AF, Hao Z, Karger BL (2007) On-line LC-MS approach combining collisioninduced dissociation (CID), electron-transfer dissociation (ETD), and CID of an isolated chargereduced species for the trace-level characterization of proteins with post-translational modifi cations. J Proteome Res 6:4230.
77. Steen H, Jebanathirajah JA, Springer M, Kirschner MW (2005) Stable isotope-free relative and absolute quantitation of protein phosphorylation stoichiometry by MS. Proc Natl Acad Sci U S A 102:3948.
78. Latterich M, Abramovitz M, Leyland-Jones B (2008) Proteomics: new technologies and clinical applications. Eur J Cancer 44:2737.
79. Pan S, Aebersold R, Chen R et al (2009) Mass spectrometry based targeted protein quantifi cation: methods and applications. J Proteome Res 8:787.
80. Tedford NC, Hall AB, Graham JR et al (2009) Quantitative analysis of cell signaling and drug action via mass spectrometry-based systems level phosphoproteomics. Proteomics 9:1469.
81. Cox DM, Zhong F, Du M et al (2005) Multiple reaction monitoring as a method for identifying protein posttranslational modifi cations. J Biomol Tech 16:83.
82. Williamson BL, Marchese J, Morrice NA (2006) Automated identification and quantification of protein phosphorylation sites by LC/MS on a hybrid triple quadrupole linear ion trap mass spectrometer. Mol Cell Proteomics 5:337.
83. Wolf-Yadlin A, Hautaniemi S, Lauffenburger DA, White FM (2007) Multiple reaction monitoring for robust quantitative proteomic analysis of cellular signaling networks. Proc Natl Acad Sci U S A 104:5860.
84. Zhang Y, Wolf-Yadlin A, White FM (2007) Quantitative proteomic analysis of phosphotyrosinemediated cellular signaling networks. Methods Mol Biol 359:203.
85. Steen JA, Steen H, Georgi A et al (2008) Different phosphorylation states of the anaphase promoting complex in response to antimitotic drugs: a quantitative proteomic analysis. Proc Natl Acad Sci U S A 105:6069.
86. Zhang Y, Wolf-Yadlin A, Ross PL et al (2005) Time-resolved mass spectrometry of tyrosine phosphorylation sites in the epidermal growth factor receptor signaling network reveals dynamic modules. Mol Cell Proteomics 4:1240.
87. Olsen JV, Blagoev B, Gnad F et al (2006) Global, in vivo, and site-specifi c phosphorylation dynamics in signaling networks. Cell 127:635.
88. Wolf-Yadlin A, Kumar N, Zhang Y et al (2006) Effects of HER2 overexpression on cell signaling networks governing proliferation and migration. Mol Syst Biol 2:54.
89. Kumar C, Mann M (2009) Bioinformatics analysis of mass spectrometry-based proteomics data sets. FEBS Lett.
90. Nichols AM, White FM (2009) Manual validation of peptide sequence and sites of tyrosine phosphorylation from MS/MS spectra. Methods Mol Biol 492:143.
91. Schulze WX, Mann M (2004) A novel proteomic screen for peptide-protein interactions. J Biol Chem 279:10756.
92. Matthiesen R, Trelle MB, Hojrup P et al (2005) VEMS 3.0: algorithms and computational tools for tandem mass spectrometry based identifi cation of post-translational modifications in proteins. J Proteome Res 4:2338.
93. Gnad F, Ren S, Cox J et al (2007) PHOSIDA (phosphorylation site database): management, structural and evolutionary investigation, and prediction of phosphosites. Genome Biol 8:R250.
94. Ingrell CR, Matthiesen R, Jensen ON (2007) Sequence handling by sequence analysis toolbox v1.0. Methods Mol Biol 367:153.
95. Ingrell CR, Miller ML, Jensen ON, Blom N (2007) NetPhosYeast: prediction of protein phosphorylation sites in yeast. Bioinformatics 23:895.
96. Matthiesen R (2007) Virtual Expert Mass Spectrometrist v3.0: an integrated tool for proteome analysis. Methods Mol Biol 367:121.
97. Matthiesen R, Jensen ON (2008) Analysis of mass spectrometry data in proteomics. Methods Mol Biol 453:105.
98. Huang PH, White FM (2008) Phosphoproteomics: unraveling the signaling web. Mol Cell 31:777.
99. de la Fuente van Bentem S, Mentzen WI, de la Fuente A, Hirt H (2008) Towards functional phosphoproteomics by mapping differential phosphorylation events in signaling networks. Proteomics 8:4453.
100. Steen H, Jebanathirajah JA, Rush J et al (2006) Phosphorylation analysis by mass spectrometry: myths, facts, and the consequences for qualitative and quantitative measurements. Mol Cell Proteomics 5:172WW.