Tandem immunoprecipitation of phosphotyrosine-mass spectrometry (TIPY-MS) indicates C190RF19 becomes tyrosine-phosphorylated And associated with activated epidermal growth factor receptor

Journal of Proteome Research

Volumn 7, Issue 3, 2008, Pages 1067-1077

  Tong, Jiefei ^a,b   Taylor, Paul ^a,b   Jovceva, Eleonora ^a,b   St Germain, Jonathan R ^a,b   Jin, Lily L ^a,b   Nikolic, Ana ^a,b   Gu, Xiaoping ^a,b   Li, Zhi Hua ^a,c   Trudel, Suzanne ^a,c   Moran, Michael F ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

C19orf19; EGFR; Epidermal growth factor; Mass spectrometry; Phospho proteomics; Phosphotyrosine; Protein protein interaction

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GENE PRODUCT; PHOSPHOTYROSINE; PROTEINASE; REGULATOR PROTEIN; TYROSINE;

ANTIGEN ANTIBODY COMPLEX; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; AMINO ACID SEQUENCE; CELL LINE; CHEMISTRY; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; PHOSPHORYLATION;

AMINO ACID SEQUENCE; CELL LINE; HUMANS; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PHOSPHORYLATION; PHOSPHOTYROSINE; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 44449117048     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr7006363     Document Type: Article

References (59)

1. Pawson, T. Specificity in signal transduction: from phosphoty-rosine-SH2 domain interactions to complex cellular systems. Cell 2004, 116 (2), 191-203.
2. Ficarro, S.; McCleland, M.; PT, S.; Burke, D.; Ross, M.; Shabanowitz, J.; Hunt, D.; White, F. Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat. Biotechnol. 2002, 20, 301-305.
3. 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 (3), 310-327.
4. 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), 1093-1101.
5. 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), 12130-12135.
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), 635-648.
7. Stover, D.; Caldwell, J.; Marto, J.; Root, K.; Mestan, J.; Stumm, M.; Ornatsky, O.; Orsi, C; Radosevic, N.; Liao, L.; Fabbro, D.; Moran, M. F. Differential phosphoprofiles of EGF and EGFR kinase inhibitor-treated human tumor cells and mouse xenografts. Clin. Proteomics 2004, 1 (1), 69-80.
8. 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), 1488-1493.
9. 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. Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol. 2005, 23 (1), 94-101.
10. Bodenmiller, B.; Mueller, L. N.; Mueller, M.; Domon, B.; Aebersold, R. Reproducible isolation of distinct, overlapping segments of the phosphoproteome. Nat. Methods 2007, 4 (3), 231-237.
11. Gavin, A. C; Bosche, M.; Krause, R.; Grandi, P.; Marzioch, M.; Bauer, A.; Schultz, J.; Rick, I. M.; Michon, A. M.; Cruciat, C. M.; Remor, M.; Hofert, G; Schelder, M.; Brajenovic, M.; Ruffher, H.; Merino, A.; Klein, K.; Hudak, M.; Dickson, D.; Rudi, T.; Gnau, V.; Bauch, A.; Bastuck, S.; Huhse, B.; Leutwein, C; Heurtier, M. A.; Copley, R. R.; Edelmann, A.; Querfurth, E.; Rybin, V.; Drewes, G.; Raida, M.; Bouwmeester, T.; Bork, P.; Seraphin, B.; Kuster, B.; Neubauer, G.; Superti-Furga, G. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 2002, 415 (6868), 141-147.
12. Ho, Y.; Gruhler, A.; Heilbut, A.; Bader, G. D.; Moore, L; Adams, S. L.; Millar, A.; Taylor, P.; Bennett, K.; Boutilier, K.; Yang, L.; Wolting, C.; Donaldson, I.; Schandorff, S.; Shewnarane, J.; Vo, M.; Taggart, J.; Goudreault, M.; Muskat, B.; Alfarano, C.; Dewar, D.; Lin, Z.; Michalickova, K.; Willems, A. R.; Sassi, H.; Nielsen, P. A.; Rasmussen, K. J.; Andersen, I. R.; Johansen, L. E.; Hansen, L. H.; Jespersen, H.; Podtelejnikov, A.; Nielsen, E.; Crawford, J.; Poulsen, V.; Sorensen, B. D.; Matthiesen, J.; Hendrickson, R. C; Gleeson, F.; Pawson, T.; Moran, M. F.; Durocher, D.; Mann, M.; Hogue, C. W.; Figeys, D.; Tyers, M. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 2002, 415 (6868), 180-183.
13. Gavin, A. C.; Aloy, P.; Grandi, P.; Krause, R.; Boesche, M.; Marzioch, M.; Rau, C; Jensen, L.).; Bastuck, S.; Dumpelfeld, B.; Edelmann, A.; Heurtier, M. A.; Hoffman, V.; Hoefert, C; Klein, K.; Hudak, M.; Michon, A. M.; Schelder, M.; Schirle, M.; Remor, M.; Rudi, T.; Hooper, S.; Bauer, A.; Bouwmeester, T.; Casari, G.; Drewes, G.; Neubauer, G.; Rick, J. M.; Kuster, B.; Bork, P.; Russell, R. B.; Superti-Furga, G. Proteome survey reveals modularity of the yeast cell machinery. Nature 2006, 440 (7084), 631-636.
14. Krogan, N. J.; Cagney, G.; Yu, H.; Zhong, G.; Guo, X.; Ignatchenko, A.; Li, J.; Pu, S.; Datta, N.; Tikuisis, A. P.; Punna, T.; Peregrin-Alvarez, J. M.; Shales, M.; Zhang, X.; Davey, M.; Robinson, M. D.; Paccanaro, A.; Bray, J. E.; Sheung, A.; Beattie, B.; Richards, D. P.; Canadien, V.; Lalev, A.; Mena, F.; Wong, P.; Starostine, A.; Canete, M. M.; Vlasblom, J.; Wu, S.; Orsi, C; Collins, S. R.; Chandran, S.; Haw, R.; Rilstone, J. J.; Gandi, K.; Thompson, N. J.; Musso, G.; St Onge, P.; Ghanny, S.; Lam, M. H.; Butland, G.; Altaf-Ul, A. M.; Kanaya, S.; Shilatifard, A.; O'Shea, E.; Weissman, J. S.; Ingles, C. J.; Hughes, T. R.; Parkinson, J.; Gerstein, M.; Wodak, S. J.; Emili, A.; Greenblatt, J. F. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 2006, 440 (7084), 637-643.
15. Ewing, R. M.; Chu, P.; Elisma, F.; Li, H.; Taylor, P.; Climie, S.; McBroom-Cerajewski, L.; Robinson, M. D.; O'Connor, L.; Li, M.; Taylor, R.; Dharsee, M.; Ho, Y.; Heilbut, A.; Moore, L.; Zhang, S.; Ornatsky, O.; Bukhman, Y. V.; Ethier, M.; Sheng, Y.; Vasilescu, J.; Abu-Farha, M.; Lambert, J. P.; Duewel, H. S.; Stewart, I.I.; Kuehl, B.; Hogue, K.; Colwill, K.; Gladwish, K.; Muskat, B.; Kinach, R.; Adams, S. L.; Moran, M. F.; Morin, G. B.; Topaloglou, T.; Figeys, D. Large-scale mapping of human protein-protein interactions by mass spectrometry. Mol. Syst. Biol. 2007, 3, 89.
16. Jones, R. B.; Gordus, A.; Krall, J. A.; MacBeath, G. A quantitative protein interaction network for the ErbB receptors using protein microarrays. Nature 2006, 439 (7073), 168-174.
17. Schulze, W. X.; Deng, L.; Mann, M. Phosphotyrosine interactome of the ErbB-receptor kinase family. Mol. Syst. Biol. 2005, 1, 2005.0008.
18. Zhang, Y.; Wolf-Yadlin, A.; Ross, P. L.; Pappin, D. J.; Rush, J.; Lauffenburger, D. A.; White, F. M. Time-resolved mass spectrometry of tyrosine phosphorylation sites in the epidermal growth factor receptor signaling network reveals dynamic modules. Mol.Cell. Proteomics 2005, 4 (9), 1240-1250.
19. Thelemann, A.; Petti, F.; Griffin, G.; Iwata, K.; Hunt, T.; Settinari, T.; Fenyo, D.; Gibson, N.; Haley, J. D. Phosphotyrosine signaling networks in epidermal growth factor receptor overexpressing squamous carcinoma cells. Mol. Cell. Proteomics 2005, 4 (4), 356-376.
20. Boeri Erba, E.; Bergatto, E.; Cabodi, S.; Silengo, L.; Tarone, G.; Defilippi, P.; Jensen, O. N. Systematic analysis of the epidermal growth factor receptor by mass spectrometry reveals stimulation-dependent multisite phosphorylation. Mol. Cell. Proteomics 2005, 4 (8), 1107-1121.
21. Blagoev, B.; Kratchmarova, I.; Ong, S. E.; Nielsen, M.; Foster, L. J.; Mann, M. A proteomics strategy to elucidate functional protein-rotein interactions applied to EGF signaling. Nat. Biotechnol. 2003, 21 (3), 315-318.
22. Pandey, A.; Podtelejnikov, A. V.; Blagoev, B.; Bustelo, X. R.; Mann, M.; Lodish, H. F. Analysis of receptor signaling pathways by mass spectrometry: identification of vav-2 as a substrate of the epidermal and platelet-derived growth factor receptors. Proc. Natl. Acad. Sci. U.S.A. 2000, 97 (1), 179-184.
23. Wu, S. L.; Kim, J.; Bandle, R. W.; Liotta, L.; Petricoin, E.; Karger, B. L. Dynamic profiling of the post-translational modifications and interaction partners of epidermal growth factor receptor signaling after stimulation by epidermal growth factor using Extended Range Proteomic Analysis (ERPA). Mol. Cell. Proteomics 2006, 5 (9), 1610-1627.
24. Wolf-Yadlin, A.; Hautaniemi, S.; Lauffenburger, D. A.; White, F. M. Multiple reaction monitoring for robust Quantitative proteomic analysis of cellular signaling networks. Proc. Natl. Acad. Sci. U.S.A 2007, 104 (14), 5860-5865.
25. Kratchmarova, I.; Blagoev, B.; Haack-Sorensen, M.; Kassem, M.; Mann, M. Mechanism of divergent growth factor effects in mesenchymal stem cell differentiation. Science 2005, 308 (5727), 1472-1477.
26. Chen, Y.; Low, T. Y.; Choong, L. Y.; Ray, R. S.; Tan, Y. L.; Toy, W.; Lin, Q.; Ang, B. K.; Wong, C. H.; Lim, S.; Li, B.; Hew, C. L.; Sze, N. S.; Druker, B. J.; Lim, Y. P. Phosphoproteomics identified Endofin, DCBLD2, and KIAA0582 as novel tyrosine phosphorylation targets of EGF signaling and Iressa in human cancer cells. Proteomics 2007, 7 (14), 2384-2397.
27. Lim, Y. P.; Diong, L. S.; Qi, R.; Druker, B. J.; Epstein, R. J. Phosphoproteomic fingerprinting of epidermal growth factor signaling and anticancer drug action in human tumor cells. Mol Cancer Ther 2003, 2 (12), 1369-1377.
28. Blagoev, B.; Ong, S. E.; Kratchmarova, I.; Mann, M. Temporal analysis of phosphotyrosine-dependent signaling networks by quantitative proteomics. Nat. Biotechnol. 2004, 22 (9), 1139-1145.
29. Moran, M. F.; Tong, J.; Taylor, P.; Ewing, R. M. Emerging applications for phospho-proteomics in cancer molecular therapeutics. Biochim. Biophys. Acta 2006, 1766 (2), 230-241.
30. Uetz, P.; Stagljar, I. The interactome of human EGF/ErbB receptors. Mol. Syst. Biol. 2006, 2, 2006.0006.
31. Dierck, K.; Machida, K.; Voigt, A.; Thimm, J.; Horstmann, M.; Fiedler, W.; Mayer, B. J.; Nollau, P. Quantitative multiplexed profiling of cellular signaling networks using phosphotyrosine-specific DNA-tagged SH2 domains. Nat. Methods 2006, 3 (9), 737-744.
32. Gu, T. L.; Popova, L.; Reeves, C; Nardone, J.; Macneill, J.; Rush, J.; Nimer, S. D.; Polakiewicz, R. D. Phosphoproteomic analysis identifies the M0-91 cell line as a cellular model for the study of TEL-TRKC fusion-associated leukemia. Leukemia2007, 21 (3), 563-566.
33. Gu, T. L.; Mercher, T.; Tyner, J. W.; Goss, V. L.; Walters, D. K.; Cornejo, M. G.; Reeves, C.; Popova, L.; Lee, K.; Heinrich, M. C; Rush, J.; Daibata, M.; Miyoshi, I.; Gilliland, D. G.; Druker, B. J.; Polakiewicz, R. D. A novel fusion of RBM6 to CSF1R in acute megakaryoblastic leukemia. Blood 2007, 110 (1), 323-333.
34. Mercher, T.; Wernig, G.; Moore, S. A.; Levine, R. L.; Gu, T. L.; Frohling, S.; Cullen, D.; Polakiewicz, R. D.; Bernard, O. A.; Boggon, T. J.; Lee, B. H.; Gilliland, D. G. JAK2T875N is a novel activating mutation that results in myeloproliferative disease with features of megakaryoblastic leukemia in a murine bone marrow transplantation model. Blood 2006, 108 (8), 2770-2779.
35. Walters, D. K.; Goss, V. L.; Stoffregen, E. P.; Gu, T. L.; Lee, K.; Nardone, J.; McGreevey, L.; Heinrich, M. C; Deininger, M. W.; Polakiewicz, R.; Druker, B. J. Phosphoproteomic analysis of AML cell lines identifies leukemic oncogenes. Leuk. Res. 2006, 30 (9), 1097-1104.
36. Griswold, I. J.; MacPartlin, M.; Bumm, T.; Goss, V. L.; O'Hare, T.; Lee, K. A.; Corbin, A. S.; Stoffregen, E. P.; Smith, C.; Johnson, K.; Moseson, E. M.; Wood, L. J.; Polakiewicz, R. D.; Druker, B. J.; Deininger, M. W. Kinase domain mutants of Bcr-Abl exhibit altered transformation potency, kinase activity, and substrate utilization, irrespective of sensitivity to imatinib. Mol. Cell. Biol. 2006, 26 (16), 6082-6093.
37. Gu, T. L.; Goss, V. L.; Reeves, C.; Popova, L.; Nardone, J.; Macneill, J.; Walters, D. K.; Wang, Y.; Rush, J.; Comb, M. J.; Druker, B. J.; Polakiewicz, R. D. Phosphotyrosine profiling identifies the KG-1 cell line as a model for the study of FGFR1 fusions in acute myeloid leukemia. Blood 2006, 108 (13), 4202-4204.
38. Goss, V. L.; Lee, K. A.; Moritz, A.; Nardone, J.; Spek, E. J.; MacNeill, J.; Rush, J.; Comb, M. J.; Polakiewicz, R. D. A common phosphotyrosine signature for the Bcr-Abl kinase. Blood 2006, 107 (12), 4888-4897.
39. Keller, A.; Nesvizhskii, A. I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 2002, 74 (20), 5383-5392.
40. Nesvizhskii, A. I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 2003, 75 (17), 4646-4658.
41. Posewitz, M. C.; Tempst, P. Immobilized gallium(III) affinity chromatography of phosphopeptides. Anal. Chem. 1999, 71 (14), 2883-2892.
42. 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), 3935-3943.
43. Larsen, M. R.; Graham, M. E.; Robinson, P. J.; Roepstorff, P. 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 2004, 3 (5), 456-465.
44. 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), 250-262.
45. Amoresano, A.; Marino, G.; Cirulli, C.; Quemeneur, E. Mapping phosphorylation sites: a new strategy based on the use of isoto-pically labelled DTT and mass spectrometry. Eur. J. Mass Spectrom.2004, 10 (3), 401-412.
46. Knight, Z. A.; Schilling, B.; Row, R. H.; Kenski, D. M.; Gibson, B. W.; Shokat, K. M. Phosphospecific proteolysis for mapping sites of protein phosphorylation. Nat. Biotechnol. 2003, 21, 1047-1054.
47. 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.
48. Rusnak, F.; Zhou, J.; Hathaway, G. M. Identification of phosphorylated and glycosylated sites in peptides by chemically targeted proteolysis.J. Biomol. Technol. 2002, 13, 228-237.
49. 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.
50. Vosseller, K.; Hansen, K. C; Chalkley, R. J.; Trinidad, J. C.; Wells, L.; Hart, G. W.; Burlingame, A. L. Quantitative analysis of both protein expression and serine/threonine post-translational modifications through stable isotope labeling with dithiothreitol. Proteomics 2005, 5 (2), 388-398.
51. Zhou, H.; Watts, J. D.; Aebersold, R. A systematic approach to the analysis of protein phosphorylation. Nat. Biotechnol. 2001,19,375-378.
52. Gafken, P. R.; Lampe, P. D. Methodologies for characterizing phosphoproteins by mass spectrometry. Cell Commun. Adhes. 2006, 13 (5-6), 249-262.
53. Atherton-Fessler, S.; Parker, L. L.; Geahlen, R. L.; Piwnica-Worms, H. Mechanisms of p34cdc2 regulation. Mol. Cell. Biol. 1993, 13 (3), 1675-1685.
54. Gandhi, T. K.; Zhong, J.; Mathivanan, S.; Karthick, L.; Chandrika, K. N.; Mohan, S. S.; Sharma, S.; Pinkert, S.; Nagaraju, S.; Peri-aswamy, B.; Mishra, G.; Nandakumar, K.; Shen, B.; Deshpande, N.; Nayak, R.; Sarker, M.; Boeke, J. D.; Parmigiani, G.; Schultz, J.; Bader, J. S.; Pandey, A. Analysis of the human protein interactome and comparison with yeast, worm and fly interaction datasets. Nat. Genet. 2006, 38 (3), 285-293.
55. Xia, Z. P.; Chen, Z. J. TRAF2: a double-edged sword? Sci STKE2M5, 2005 (272), pe7.
56. DeYulia, G. J. J.; Carcamo, J. M.; Borquez-Ojeda, O.; Shelton, C. G; Golde, D. W. Hydrogen peroxide generated extracellularly by receptor-ligand interaction facilitates cell signaling. Proc. Natl. Acad. Sci. U.S.A. 2005, 102 (14), 5044-5049.
57. Hoshino, I.; Matsubara, H.; Hanari, N.; Mori, M.; Nishimori, T.; Yoneyama, Y.; Akutsu, Y.; Sakata, H.; Matsushita, K.; Seki, N.; Ochiai, T. Histone deacetylase inhibitor FK228 activates tumor suppressor Prdxl with apoptosis induction in esophageal cancer cells. Clin. Cancer Res. 2005, 11 (21), 7945-7952.
58. Kyte, J.; Doolirde, R. F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 1982,157 (1), 105-132.
59. Rebhan, M.; Chalifa-Caspi, V.; Prilusky, J.; Lancet, D. GeneCards:integrating information about genes, proteins and diseases. Trends Genet. 1997, 13, 163.