Toward a comprehensive characterization of a human cancer cell phosphoproteome

Journal of Proteome Research

Volumn 12, Issue 1, 2013, Pages 260-271

  Zhou, Houjiang ^a,b   Di Palma, Serena ^a,b   Preisinger, Christian ^a,b   Peng, Mao ^a,b   Polat, Ayse Nur ^a,b   Heck, Albert J R ^a,b,c   Mohammed, Shabaz ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

^c Centre for Biomedical Genetics   (Netherlands)

Author keywords

HeLa; Human cancer cell; K562; Mass spectrometry; Phosphoproteomics

Indexed keywords

PHOSPHOPEPTIDE; PHOSPHOPROTEOME; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; FRACTIONATION; HELA CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PARAMETERS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

CHROMATOGRAPHY, AFFINITY; CHROMATOGRAPHY, ION EXCHANGE; HELA CELLS; HUMANS; MASS SPECTROMETRY; NEOPLASMS; PHOSPHOPEPTIDES; PHOSPHOPROTEINS; PROTEOMICS;

EID: 84874093507     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300630k     Document Type: Article

References (65)

1. Pawson, T.; Scott, J. D. Protein phosphorylation in signaling 50 years and counting. Trends Biochem. Sci. 2005, 30 (6), 286-90.
2. Hunter, T. Tyrosine phosphorylation: thirty years and counting. Curr. Opin. Cell Biol. 2009, 21 (2), 140-6.
3. Brognard, J.; Hunter, T. Protein kinase signaling networks in cancer. Curr. Opin. Genet. Dev. 2011, 21 (1), 4-11.
4. Harsha, H. C.; Pandey, A. Phosphoproteomics in cancer. Mol. Oncol. 2010, 4 (6), 482-95.
5. Huttlin, E. L.; Jedrychowski, M. P.; Elias, J. E.; Goswami, T.; Rad, R.; Beausoleil, S. A.; Villen, J.; Haas, W.; Sowa, M. E.; Gygi, S. P. A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 2010, 143 (7), 1174-89.
6. Olsen, J. V.; Blagoev, B.; Gnad, F.; Macek, B.; Kumar, C.; Mortensen, P.; Mann, M. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127 (3), 635-48.
7. Aebersold, R.; Mann, M. Mass spectrometry-based proteomics. Nature 2003, 422 (6928), 198-207.
8. Cox, J.; Mann, M. Quantitative, high-resolution proteomics for data-driven systems biology. Annu. Rev. Biochem. 2011, 80, 273-99.
9. Olsen, J. V.; Vermeulen, M.; Santamaria, A.; Kumar, C.; Miller, M. L.; Jensen, L. J.; Gnad, F.; Cox, J.; Jensen, T. S.; Nigg, E. A.; Brunak, S.; Mann, M. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signaling 2010, 3 (104), ra3.
10. 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 (1), 311-8.
11. Villen, J.; Beausoleil, S. A.; Gerber, S. A.; Gygi, S. P. Large-scale phosphorylation analysis of mouse liver. Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (5), 1488-93.
12. Ballif, B. A.; Villen, J.; Beausoleil, S. A.; Schwartz, D.; Gygi, S. P. Phosphoproteomic analysis of the developing mouse brain. Mol. Cell. Proteomics 2004, 3 (11), 1093-101.
13. Fonslow, B. R.; Niessen, S. M.; Singh, M.; Wong, C. C.; Xu, T.; Carvalho, P. C.; Choi, J.; Park, S. K.; Yates, J. R., 3rd Single-step inline hydroxyapatite enrichment facilitates identification and quantitation of phosphopeptides from mass-limited proteomes with MudPIT. J. Proteome Res. 2012, 11 (5), 2697-709.
14. Leitner, A.; Sturm, M.; Hudecz, O.; Mazanek, M.; Smatt, J. H.; Linden, M.; Lindner, W.; Mechtler, K. Probing the phosphoproteome of HeLa cells using nanocast metal oxide microspheres for phosphopeptide enrichment. Anal. Chem. 2010, 82 (7), 2726-33.
15. Zhou, H.; Low, T. Y.; Hennrich, M. L.; van der Toorn, H.; Schwend, T.; Zou, H.; Mohammed, S.; Heck, A. J. Enhancing the identification of phosphopeptides from putative basophilic kinase substrates using Ti (IV) based IMAC enrichment. Mol. Cell. Proteomics 2011, 10 (10), M110 006452.
16. Dephoure, N.; Zhou, C.; Villen, J.; Beausoleil, S. A.; Bakalarski, C. E.; Elledge, S. J.; Gygi, S. P. A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (31), 10762-7.
17. Van Hoof, D.; Munoz, J.; Braam, S. R.; Pinkse, M. W.; Linding, R.; Heck, A. J.; Mummery, C. L.; Krijgsveld, J. Phosphorylation dynamics during early differentiation of human embryonic stem cells. Cell Stem Cell 2009, 5 (2), 214-26.
18. Brill, L. M.; Xiong, W.; Lee, K. B.; Ficarro, S. B.; Crain, A.; Xu, Y.; Terskikh, A.; Snyder, E. Y.; Ding, S. Phosphoproteomic analysis of human embryonic stem cells. Cell Stem Cell 2009, 5 (2), 204-13.
19. Rigbolt, K. T.; Prokhorova, T. A.; Akimov, V.; Henningsen, J.; Johansen, P. T.; Kratchmarova, I.; Kassem, M.; Mann, M.; Olsen, J. V.; Blagoev, B. System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation. Sci. Signaling 2011, 4 (164), rs3.
20. Phanstiel, D. H.; Brumbaugh, J.; Wenger, C. D.; Tian, S.; Probasco, M. D.; Bailey, D. J.; Swaney, D. L.; Tervo, M. A.; Bolin, J. M.; Ruotti, V.; Stewart, R.; Thomson, J. A.; Coon, J. J. Proteomic and phosphoproteomic comparison of human ES and iPS cells. Nat. Methods 2011, 8 (10), 821-7.
21. Andersson, L.; Porath, J. Isolation of phosphoproteins by immobilized metal (Fe3+) affinity chromatography. Anal. Biochem. 1986, 154 (1), 250-4.
22. Posewitz, M. C.; Tempst, P. Immobilized gallium(III) affinity chromatography of phosphopeptides. Anal. Chem. 1999, 71 (14), 2883-92.
23. Zhou, H.; Xu, S.; Ye, M.; Feng, S.; Pan, C.; Jiang, X.; Li, X.; Han, G.; Fu, Y.; Zou, H. Zirconium phosphonate-modified porous silicon for highly specific capture of phosphopeptides and MALDI-TOF MS analysis. J. Proteome Res. 2006, 5 (9), 2431-7.
24. Zhou, H.; Ye, M.; Dong, J.; Han, G.; Jiang, X.; Wu, R.; Zou, H. Specific phosphopeptide enrichment with immobilized titanium ion affinity chromatography adsorbent for phosphoproteome analysis. J. Proteome Res. 2008, 7 (9), 3957-67.
25. 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-NanoLC-ESI-MS/MS and titanium oxide precolumns. Anal. Chem. 2004, 76 (14), 3935-43.
26. Pinkse, M. W.; Mohammed, S.; Gouw, J. W.; van Breukelen, B.; Vos, H. R.; Heck, A. J. Highly robust, automated, and sensitive online TiO2-based phosphoproteomics applied to study endogenous phosphorylation in Drosophila melanogaster. J. Proteome Res. 2008, 7 (2), 687-97.
27. Beausoleil, S. A.; Jedrychowski, M.; Schwartz, D.; Elias, J. E.; Villen, J.; Li, J.; Cohn, M. A.; Cantley, L. C.; Gygi, S. P. Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (33), 12130-5.
28. 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 refined SCX-based approach. Anal. Chem. 2009, 81 (11), 4493-501.
29. Alpert, A. J.; Petritis, K.; Kangas, L.; Smith, R. D.; Mechtler, K.; Mitulovic, G.; Mohammed, S.; Heck, A. J. Peptide orientation affects selectivity in ion-exchange chromatography. Anal. Chem. 2010, 82 (12), 5253-9.
30. Dai, J.; Jin, W. H.; Sheng, Q. H.; Shieh, C. H.; Wu, J. R.; Zeng, R. Protein phosphorylation and expression profiling by Yin-yang multidimensional liquid chromatography (Yin-yang MDLC) mass spectrometry. J. Proteome Res. 2007, 6 (1), 250-62.
31. Han, G.; Ye, M.; Zhou, H.; Jiang, X.; Feng, S.; 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 (7), 1346-61.
32. Alpert, A. J. Electrostatic repulsion hydrophilic interaction chromatography for isocratic separation of charged solutes and selective isolation of phosphopeptides. Anal. Chem. 2008, 80 (1), 62-76.
33. 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 (5), 971-80.
34. Albuquerque, C. P.; Smolka, M. B.; Payne, S. H.; Bafna, V.; Eng, J.; Zhou, H. A multidimensional chromatography technology for indepth phosphoproteome analysis. Mol. Cell. Proteomics 2008, 7 (7), 1389-96.
35. Motoyama, A.; Xu, T.; Ruse, C. I.; Wohlschlegel, J. A.; Yates, J. R., III. Anion and cation mixed-bed ion exchange for enhanced multidimensional separations of peptides and phosphopeptides. Anal. Chem. 2007, 79 (10), 3623-34.
36. 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 (7), 1198-214.
37. Kettenbach, A. N.; Schweppe, D. K.; Faherty, B. K.; Pechenick, D.; Pletnev, A. A.; Gerber, S. A. Quantitative phosphoproteomics identifies substrates and functional modules of Aurora and Polo-like kinase activities in mitotic cells. Sci. Signaling 2011, 4 (179), rs5.
38. Koch, A.; Krug, K.; Pengelley, S.; Macek, B.; Hauf, S. Mitotic substrates of the kinase aurora with roles in chromatin regulation identified through quantitative phosphoproteomics of fission yeast. Sci. Signaling 2011, 4 (179), rs6.
39. Kettenbach, A. N.; Gerber, S. A. Rapid and reproducible singlestage phosphopeptide enrichment of complex peptide mixtures: application to general and phosphotyrosine-specific phosphoproteomics experiments. Anal. Chem. 2011, 83 (20), 7635-44.
40. Lemeer, S.; Heck, A. J. The phosphoproteomics data explosion. Curr. Opin. Chem. Biol. 2009, 13 (4), 414-20.
41. Ficarro, S. B.; Zhang, Y.; Carrasco-Alfonso, M. J.; Garg, B.; Adelmant, G.; Webber, J. T.; Luckey, C. J.; Marto, J. A. Online nanoflow multidimensional fractionation for high efficiency phosphopeptide analysis. Mol. Cell. Proteomics 2011, 10 (11), O111 011064.
42. Hennrich, M. L.; Groenewold, V.; Kops, G. J.; Heck, A. J.; Mohammed, S. Improving depth in phosphoproteomics by using a strong cation exchange-weak anion exchange-reversed phase multidimensional separation approach. Anal. Chem. 2011, 83 (18), 7137-43.
43. Cantin, G. T.; Yi, W.; Lu, B.; Park, S. K.; Xu, T.; Lee, J. D.; Yates, J. R., III. Combining protein-based IMAC, peptide-based IMAC, and MudPIT for efficient phosphoproteomic analysis. J. Proteome Res. 2008, 7 (3), 1346-51.
44. Boersema, P. J.; Mohammed, S.; Heck, A. J. Phosphopeptide fragmentation and analysis by mass spectrometry. J Mass Spectrom 2009, 44 (6), 861-78.
45. 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. Mol. Cell. Proteomics 2011, 10 (12), M111 009910.
46. Nagaraj, N.; D'Souza, R. C.; Cox, J.; Olsen, J. V.; Mann, M. Feasibility of large-scale phosphoproteomics with higher energy collisional dissociation fragmentation. J. Proteome Res. 2010, 9 (12), 6786-94.
47. Chi, A.; Huttenhower, C.; Geer, L. Y.; Coon, J. J.; Syka, J. E.; Bai, D. L.; Shabanowitz, J.; Burke, D. J.; Troyanskaya, O. G.; Hunt, D. F. Analysis of phosphorylation sites on proteins from Saccharomyces cerevisiae by electron transfer dissociation (ETD) mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (7), 2193-8.
48. 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. U.S.A. 2009, 106 (4), 995-1000.
49. Michalski, A.; Damoc, E.; Lange, O.; Denisov, E.; Nolting, D.; Mueller, M.; Viner, R.; Schwartz, J.; Remes, P.; Belford, M.; Dunyach, J. J.; Cox, J.; Horning, S.; Mann, M.; Makarov, A. Ultra high resolution linear ion trap Orbitrap mass spectrometer (Orbitrap Elite) facilitates top down LC MS/MS and versatile peptide fragmentation modes. Mol. Cell. Proteomics 2012, 11, No. O111.013698.
50. Di Palma, S.; Boersema, P. J.; Heck, A. J.; Mohammed, S. Zwitterionic hydrophilic interaction liquid chromatography (ZICHILIC and ZIC-cHILIC) provide high resolution separation and increase sensitivity in proteome analysis. Anal. Chem. 2011, 83 (9), 3440-7.
51. Di Palma, S.; Stange, D.; van de Wetering, M.; Clevers, H.; Heck, A. J.; Mohammed, S. Highly sensitive proteome analysis of FACS-sorted adult colon stem cells. J. Proteome Res. 2011, 10 (8), 3814-9.
52. Yu, Z.; Han, G.; Sun, S.; Jiang, X.; Chen, R.; Wang, F.; Wu, R.; Ye, M.; Zou, H. Preparation of monodisperse immobilized Ti(4+) affinity chromatography microspheres for specific enrichment of phosphopeptides. Anal. Chim. Acta 2009, 636 (1), 34-41.
53. Raijmakers, R.; Berkers, C. R.; de Jong, A.; Ovaa, H.; Heck, A. J.; Mohammed, S. Automated online sequential isotope labeling for protein quantitation applied to proteasome tissue-specific diversity. Mol. Cell. Proteomics 2008, 7 (9), 1755-62.
54. Frese, C. K.; Altelaar, A. F.; Hennrich, M. L.; Nolting, D.; Zeller, M.; Griep-Raming, J.; Heck, A. J.; Mohammed, S. Improved peptide identification by targeted fragmentation using CID, HCD and ETD on an LTQ-Orbitrap Velos. J. Proteome Res. 2011, 10 (5), 2377-88.
55. Kall, L.; Canterbury, J. D.; Weston, J.; Noble, W. S.; MacCoss, M. J. Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat. Methods 2007, 4 (11), 923-5.
56. Taus, T.; Kocher, T.; Pichler, P.; Paschke, C.; Schmidt, A.; Henrich, C.; Mechtler, K. Universal and confident phosphorylation site localization using phosphoRS. J. Proteome Res. 2011, 10 (12), 5354-62.
57. Data were analyzed through the use of IPA (Ingenuity Systems, www.ingenuity.com).
58. Schwartz, D.; Gygi, S. P. An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nat. Biotechnol. 2005, 23 (11), 1391-8.
59. Mohammed, S.; Heck, A., Jr. Strong cation exchange (SCX) based analytical methods for the targeted analysis of protein posttranslational modifications. Curr. Opin. Biotechnol. 2010, 22 (1), 9-16.
60. Hornbeck, P. V.; Kornhauser, J. M.; Tkachev, S.; Zhang, B.; Skrzypek, E.; Murray, B.; Latham, V.; Sullivan, M. PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res. 2011, 40 (Database issue), D261-70.
61. Diella, F.; Gould, C. M.; Chica, C.; Via, A.; Gibson, T. J. Phospho.ELM: a database of phosphorylation sites update 2008. Nucleic Acids Res. 2008, 36 (Database issue), D240-4.
62. Dhillon, A. S.; Kolch, W. Untying the regulation of the Raf-1 kinase. Arch. Biochem. Biophys. 2002, 404 (1), 3-9.
63. Horita, M.; Andreu, E. J.; Benito, A.; Arbona, C.; Sanz, C.; Benet, I.; Prosper, F.; Fernandez-Luna, J. L. Blockade of the Bcr-Abl kinase activity induces apoptosis of chronic myelogenous leukemia cells by suppressing signal transducer and activator of transcription 5-dependent expression of Bcl-xL. J. Exp. Med. 2000, 191 (6), 977-84.
64. Faderl, S.; Talpaz, M.; Estrov, Z.; O'Brien, S.; Kurzrock, R.; Kantarjian, H. M. The biology of chronic myeloid leukemia. New Engl. J. Med. 1999, 341 (3), 164-72.
65. Fabbro, D. BCR-ABL signaling: A new STATus in CML. Nat. Chem. Biol. 2012, 8 (3), 228-9.