Phosphoproteomics in cancer

Molecular Oncology

Volumn 4, Issue 6, 2010, Pages 482-495

  Harsha, H C ^a   Pandey, Akhilesh ^b  

^a International Tech Park Ltd   (India)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Phosphorylation; Protein microarrays; Signal transduction; SILAC

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTINEOPLASTIC AGENT; BOSUTINIB; DASATINIB; GEFITINIB; IMATINIB; N [4 (3 BROMOANILINO) 6 QUINAZOLINYL]ACRYLAMIDE; ONCOPROTEIN; PHOSPHOPROTEIN; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE; PROTEOME; SERINE; THREONINE; TYROSINE;

ACUTE MYELOBLASTIC LEUKEMIA; CANCER THERAPY; CANCER TISSUE; CARCINOGENESIS; CELL CULTURE; CHRONIC MYELOID LEUKEMIA; CLINICAL TRIAL; HUMAN; MASS SPECTROMETRY; NEOPLASM; NONHUMAN; ONCOGENE; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; REVIEW; SIGNAL TRANSDUCTION;

EID: 78349310118     PISSN: 15747891     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molonc.2010.09.004     Document Type: Review

References (127)

1. Amanchy R., Kalume D.E., Iwahori A., Zhong J., Pandey A. Phosphoproteome analysis of HeLa cells using stable isotope labeling with amino acids in cell culture (SILAC). J. Proteome Res. 2005, 4:1661-1671.
2. Amanchy R., Kalume D.E., Pandey A. Stable isotope labeling with amino acids in cell culture (SILAC) for studying dynamics of protein abundance and posttranslational modifications. Sci. STKE 2005, l2.
3. Amanchy R., Zhong J., Hong R., Kim J.H., Gucek M., Cole R.N., Molina H., Pandey A. Identification of c-Src tyrosine kinase substrates in platelet-derived growth factor receptor signaling. Mol. Oncol. 2009, 3:439-450.
4. Amanchy R., Zhong J., Molina H., Chaerkady R., Iwahori A., Kalume D.E., Gronborg M., Joore J., Cope L., Pandey A. Identification of c-Src tyrosine kinase substrates using mass spectrometry and peptide microarrays. J. Proteome Res. 2008, 7:3900-3910.
5. +) affinity chromatography. Anal. Biochem. 1986, 154:250-254.
6. Bain J., McLauchlan H., Elliott M., Cohen P. The specificities of protein kinase inhibitors: an update. Biochem. J. 2003, 371:199-204.
7. Bantscheff M., Eberhard D., Abraham Y., Bastuck S., Boesche M., Hobson S., Mathieson T., Perrin J., Raida M., Rau C., Reader V., Sweetman G., Bauer A., Bouwmeester T., Hopf C., Kruse U., Neubauer G., Ramsden N., Rick J., Kuster B., Drewes G. Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors. Nat. Biotechnol. 2007, 25:1035-1044.
8. Barber T.D., Vogelstein B., Kinzler K.W., Velculescu V.E. Somatic mutations of EGFR in colorectal cancers and glioblastomas. N. Engl. J. Med. 2004, 351:2883.
9. Betts J.C., Blackstock W.P., Ward M.A., Anderton B.H. Identification of phosphorylation sites on neurofilament proteins by nanoelectrospray mass spectrometry. J. Biol. Chem. 1997, 272:12922-12927.
10. Blume-Jensen P., Hunter T. Oncogenic kinase signalling. Nature 2001, 411:355-365.
11. Bose R., Molina H., Patterson A.S., Bitok J.K., Periaswamy B., Bader J.S., Pandey A., Cole P.A. Phosphoproteomic analysis of Her2/neu signaling and inhibition. Proc. Natl. Acad. Sci. U S A 2006, 103:9773-9778.
12. Braconi C., Bracci R., Cellerino R. Molecular targets in gastrointestinal stromal tumors (GIST) therapy. Curr. Cancer Drug Targets 2008, 8:359-366.
13. 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.
14. 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, 5:204-213.
15. Brugge J.S., Erikson R.L. Identification of a transformation-specific antigen induced by an avian sarcoma virus. Nature 1977, 269:346-348.
16. Carr S.A., Huddleston M.J., Annan R.S. Selective detection and sequencing of phosphopeptides at the femtomole level by mass spectrometry. Anal. Biochem. 1996, 239:180-192.
17. Chen E.I., Yates J.R. Cancer proteomics by quantitative shotgun proteomics. Mol. Oncol. 2007, 1:144-159.
18. Choudhary C., Olsen J.V., Brandts C., Cox J., Reddy P.N., Bohmer F.D., Gerke V., Schmidt-Arras D.E., Berdel W.E., Muller-Tidow C., Mann M., Serve H. Mislocalized activation of oncogenic RTKs switches downstream signaling outcomes. Mol. Cell 2009, 36:326-339.
19. Corless C.L., Fletcher J.A., Heinrich M.C. Biology of gastrointestinal stromal tumors. J. Clin. Oncol. 2004, 22:3813-3825.
20. Cunningham D.L., Sweet S.M., Cooper H.J., Heath J.K. Differential phosphoproteomics of fibroblast growth factor signaling: identification of Src family kinase-mediated phosphorylation events. J. Proteome Res. 2010.
21. Daub H., Olsen J.V., Bairlein M., Gnad F., Oppermann F.S., Korner R., Greff Z., Keri G., Stemmann O., Mann M. Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol. Cell 2008, 31:438-448.
22. Davies S.P., Reddy H., Caivano M., Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 2000, 351:95-105.
23. Diks S.H., Kok K., O'Toole T., Hommes D.W., van Dijken P., Joore J., Peppelenbosch M.P. Kinome profiling for studying lipopolysaccharide signal transduction in human peripheral blood mononuclear cells. J. Biol. Chem. 2004, 279:49206-49213.
24. Druker B.J., Talpaz M., Resta D.J., Peng B., Buchdunger E., Ford J.M., Lydon N.B., Kantarjian H., Capdeville R., Ohno-Jones S., Sawyers C.L. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N. Engl. J. Med. 2001, 344:1031-1037.
25. Druker B.J., Tamura S., Buchdunger E., Ohno S., Segal G.M., Fanning S., Zimmermann J., Lydon N.B. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat. Med. 1996, 2:561-566.
26. Ferrajoli A., Faderl S., Ravandi F., Estrov Z. The JAK-STAT pathway: a therapeutic target in hematological malignancies. Curr. Cancer Drug Targets 2006, 6:671-679.
27. Frackelton A.R., Posner M., Kannan B., Mermelstein F. Generation of monoclonal antibodies against phosphotyrosine and their use for affinity purification of phosphotyrosine-containing proteins. Methods Enzymol. 1991, 201:79-92.
28. Gembitsky D.S., Lawlor K., Jacovina A., Yaneva M., Tempst P. A prototype antibody microarray platform to monitor changes in protein tyrosine phosphorylation. Mol. Cell Proteomics 2004, 3:1102-1118.
29. Godl K., Wissing J., Kurtenbach A., Habenberger P., Blencke S., Gutbrod H., Salassidis K., Stein-Gerlach M., Missio A., Cotten M., Daub H. An efficient proteomics method to identify the cellular targets of protein kinase inhibitors. Proc. Natl. Acad. Sci. U S A 2003, 100:15434-15439.
30. Golas J.M., Arndt K., Etienne C., Lucas J., Nardin D., Gibbons J., Frost P., Ye F., Boschelli D.H., Boschelli F. SKI-606, a 4-anilino-3-quinolinecarbonitrile dual inhibitor of Src and Abl kinases, is a potent antiproliferative agent against chronic myelogenous leukemia cells in culture and causes regression of K562 xenografts in nude mice. Cancer Res. 2003, 63:375-381.
31. Gronborg 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 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.
32. Guha U., Chaerkady R., Marimuthu A., Patterson A.S., Kashyap M.K., Harsha H.C., Sato M., Bader J.S., Lash A.E., Minna J.D., Pandey A., Varmus H.E. Comparisons of tyrosine phosphorylated proteins in cells expressing lung cancer-specific alleles of EGFR and KRAS. Proc. Natl. Acad. Sci. U S A 2008, 105:14112-14117.
33. Gulmann C., Sheehan K.M., Conroy R.M., Wulfkuhle J.D., Espina V., Mullarkey M.J., Kay E.W., Liotta L.A., Petricoin E.F. Quantitative cell signalling analysis reveals down-regulation of MAPK pathway activation in colorectal cancer. J. Pathol. 2009, 218:514-519.
34. Guo A., Villen J., Kornhauser J., Lee K.A., Stokes M.P., Rikova K., Possemato A., Nardone J., Innocenti G., Wetzel R., Wang Y., MacNeill J., Mitchell J., Gygi S.P., Rush J., Polakiewicz R.D., Comb M.J. Signaling networks assembled by oncogenic EGFR and c-Met. Proc. Natl. Acad. Sci. U S A 2008, 105:692-697.
35. Hahn C.K., Berchuck J.E., Ross K.N., Kakoza R.M., Clauser K., Schinzel A.C., Ross L., Galinsky I., Davis T.N., Silver S.J., Root D.E., Stone R.M., DeAngelo D.J., Carroll M., Hahn W.C., Carr S.A., Golub T.R., Kung A.L., Stegmaier K. Proteomic and genetic approaches identify Syk as an AML target. Cancer Cell 2009, 16:281-294.
36. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
37. Harsha H.C., Jimeno A., Molina H., Mihalas A.B., Goggins M.G., Hruban R.H., Schulick R.D., Kamath U., Maitra A., Hidalgo M., Pandey A. Activated epidermal growth factor receptor as a novel target in pancreatic cancer therapy. J. Proteome Res. 2008, 7:4651-4658.
38. Harsha H.C., Molina H., Pandey A. Quantitative proteomics using stable isotope labeling with amino acids in cell culture. Nat. Protoc. 2008, 3:505-516.
39. Houseman B.T., Huh J.H., Kron S.J., Mrksich M. Peptide chips for the quantitative evaluation of protein kinase activity. Nat. Biotechnol. 2002, 20:270-274.
40. Huang P.H., Mukasa A., Bonavia R., Flynn R.A., Brewer Z.E., Cavenee W.K., Furnari F.B., White F.M. Quantitative analysis of EGFRvIII cellular signaling networks reveals a combinatorial therapeutic strategy for glioblastoma. Proc. Natl. Acad. Sci. U S A 2007, 104:12867-12872.
41. Hudson M.E., Pozdnyakova I., Haines K., Mor G., Snyder M. Identification of differentially expressed proteins in ovarian cancer using high-density protein microarrays. Proc. Natl. Acad. Sci. U S A 2007, 104:17494-17499.
42. Hunter T., Cooper J.A. Protein-tyrosine kinases. Annu. Rev. Biochem. 1985, 54:897-930.
43. Hunter T., Sefton B.M. Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc. Natl. Acad. Sci. U S A 1980, 77:1311-1315.
44. Hynes N.E., MacDonald G. ErbB receptors and signaling pathways in cancer. Curr. Opin. Cell Biol. 2009, 21:177-184.
45. Jorgensen C., Sherman A., Chen G.I., Pasculescu A., Poliakov A., Hsiung M., Larsen B., Wilkinson D.G., Linding R., Pawson T. Cell-specific information processing in segregating populations of Eph receptor ephrin-expressing cells. Science 2009, 326:1502-1509.
46. Joughin B.A., Naegle K.M., Huang P.H., Yaffe M.B., Lauffenburger D.A., White F.M. An integrated comparative phosphoproteomic and bioinformatic approach reveals a novel class of MPM-2 motifs upregulated in EGFRvIII-expressing glioblastoma cells. Mol. Biosyst. 2009, 5:59-67.
47. Kamps M.P. Generation and use of anti-phosphotyrosine antibodies for immunoblotting. Methods Enzymol. 1991, 201:101-110.
48. Kane S., Sano H., Liu S.C., Asara J.M., Lane W.S., Garner C.C., Lienhard G.E. A method to identify serine kinase substrates. Akt phosphorylates a novel adipocyte protein with a Rab GTPase-activating protein (GAP) domain. J. Biol. Chem. 2002, 277:22115-22118.
49. Karasarides M., Chiloeches A., Hayward R., Niculescu-Duvaz D., Scanlon I., Friedlos F., Ogilvie L., Hedley D., Martin J., Marshall C.J., Springer C.J., Marais R. B-RAF is a therapeutic target in melanoma. Oncogene 2004, 23:6292-6298.
50. Kingsmore S.F. Multiplexed protein measurement: technologies and applications of protein and antibody arrays. Nat. Rev. Drug Discov. 2006, 5:310-320.
51. Knight Z.A., Lin H., Shokat K.M. Targeting the cancer kinome through polypharmacology. Nat. Rev. Cancer 2010, 10:130-137.
52. Kruger M., Kratchmarova I., Blagoev B., Tseng Y.H., Kahn C.R., Mann M. Dissection of the insulin signaling pathway via quantitative phosphoproteomics. Proc. Natl. Acad. Sci. U S A 2008, 105:2451-2456.
53. Krystal G.W., Honsawek S., Litz J., Buchdunger E. The selective tyrosine kinase inhibitor STI571 inhibits small cell lung cancer growth. Clin. Cancer Res. 2000, 6:3319-3326.
54. Kubota K., Anjum R., Yu Y., Kunz R.C., Andersen J.N., Kraus M., Keilhack H., Nagashima K., Krauss S., Paweletz C., Hendrickson R.C., Feldman A.S., Wu C.L., Rush J., Villen J., Gygi S.P. Sensitive multiplexed analysis of kinase activities and activity-based kinase identification. Nat. Biotechnol. 2009, 27:933-940.
55. Larive R.M., Urbach S., Poncet J., Jouin P., Mascre G., Sahuquet A., Mangeat P.H., Coopman P.J., Bettache N. Phosphoproteomic analysis of Syk kinase signaling in human cancer cells reveals its role in cell-cell adhesion. Oncogene 2009, 28:2337-2347.
56. Larsen M.R., Thingholm T.E., Jensen O.N., Roepstorff P., Jorgensen T.J. Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell Proteomics 2005, 4:873-886.
57. Lee J.T., Lehmann B.D., Terrian D.M., Chappell W.H., Stivala F., Libra M., Martelli A.M., Steelman L.S., McCubrey J.A. Targeting prostate cancer based on signal transduction and cell cycle pathways. Cell Cycle 2008, 7:1745-1762.
58. Leroy C., Fialin C., Sirvent A., Simon V., Urbach S., Poncet J., Robert B., Jouin P., Roche S. Quantitative phosphoproteomics reveals a cluster of tyrosine kinases that mediates SRC invasive activity in advanced colon carcinoma cells. Cancer Res. 2009, 69:2279-2286.
59. Levin V.A., Panchabhai S.C., Shen L., Kornblau S.M., Qiu Y., Baggerly K.A. Different changes in protein and phosphoprotein levels result from serum starvation of high-grade glioma and adenocarcinoma cell lines. J. Proteome Res. 2010, 9:179-191.
60. Levinson A.D., Oppermann H., Levintow L., Varmus H.E., Bishop J.M. Evidence that the transforming gene of avian sarcoma virus encodes a protein kinase associated with a phosphoprotein. Cell 1978, 15:561-572.
61. Li H., Ren Z., Kang X., Zhang L., Li X., Wang Y., Xue T., Shen Y., Liu Y. Identification of tyrosine-phosphorylated proteins associated with metastasis and functional analysis of FER in human hepatocellular carcinoma cells. BMC Cancer 2009, 9:366.
62. 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 specific enzymatic degradation with matrix-assisted laser desorption/ionization mass spectrometry. Anal. Biochem. 1994, 219:9-20.
63. Loyet K.M., Stults J.T., Arnott D. Mass spectrometric contributions to the practice of phosphorylation site mapping through 2003: a literature review. Mol. Cell Proteomics 2005, 4:235-245.
64. Luo W., Slebos R.J., Hill S., Li M., Brabek J., Amanchy R., Chaerkady R., Pandey A., Ham A.J., Hanks S.K. Global impact of oncogenic Src on a phosphotyrosine proteome. J. Proteome Res. 2008, 7:3447-3460.
65. Lynch T.J., Bell D.W., Sordella R., Gurubhagavatula S., Okimoto R.A., Brannigan B.W., Harris P.L., Haserlat S.M., Supko J.G., Haluska F.G., Louis D.N., Christiani D.C., Settleman J., Haber D.A. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 2004, 350:2129-2139.
66. Ma Y., Lu Y., Zeng H., Ron D., Mo W., Neubert T.A. Characterization of phosphopeptides from protein digests using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and nanoelectrospray quadrupole time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 2001, 15:1693-1700.
67. Manning G., Whyte D.B., Martinez R., Hunter T., Sudarsanam S. The protein kinase complement of the human genome. Science 2002, 298:1912-1934.
68. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald E.R., Hurov K.E., Luo J., Bakalarski C.E., Zhao Z., Solimini N., Lerenthal Y., Shiloh Y., Gygi S.P., Elledge S.J. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316:1160-1166.
69. 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.
70. Molina H., Horn D.M., Tang N., Mathivanan S., Pandey A. Global proteomic profiling of phosphopeptides using electron transfer dissociation tandem mass spectrometry. Proc. Natl. Acad. Sci. U S A 2007, 104:2199-2204.
71. Muszynska G., Dobrowolska G., Medin A., Ekman P., Porath J.O. Model studies on iron(III) ion affinity chromatography. II. Interaction of immobilized iron(III) ions with phosphorylated amino acids, peptides and proteins. J. Chromatogr. 1992, 604:19-28.
72. Nguyen V., Cao L., Lin J.T., Hung N., Ritz A., Yu K., Jianu R., Ulin S.P., Raphael B.J., Laidlaw D.H., Brossay L., Salomon A.R. A new approach for quantitative phosphoproteomic dissection of signaling pathways applied to T cell receptor activation. Mol. Cell Proteomics 2009, 8:2418-2431.
73. 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.
74. Old W.M., Shabb J.B., Houel S., Wang H., Couts K.L., Yen C.Y., Litman E.S., Croy C.H., Meyer-Arendt K., Miranda J.G., Brown R.A., Witze E.S., Schweppe R.E., Resing K.A., Ahn N.G. Functional proteomics identifies targets of phosphorylation by B-Raf signaling in melanoma. Mol. Cell 2009, 34:115-131.
75. 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, 127:635-648.
76. Oppermann F.S., Gnad F., Olsen J.V., Hornberger R., Greff Z., Keri G., Mann M., Daub H. Large-scale proteomics analysis of the human kinome. Mol. Cell Proteomics 2009, 8:1751-1764.
77. Ostasiewicz P., Zielinska D.F., Mann M., Wisniewski J.R. Proteome, phosphoproteome, and N-glycoproteome are quantitatively preserved in formalin-fixed paraffin-embedded tissue and analyzable by high-resolution mass spectrometry. J. Proteome Res. 2010, 9:3688-3700.
78. Osterberg R. Metal and hydrogen-ion binding properties of o-phosphoserine. Nature 1957, 179:476-477.
79. Pan C., Olsen J.V., Daub H., Mann M. Global effects of kinase inhibitors on signaling networks revealed by quantitative phosphoproteomics. Mol. Cell Proteomics 2009, 8:2796-2808.
80. Parsons D.W., Wang T.L., Samuels Y., Bardelli A., Cummins J.M., DeLong L., Silliman N., Ptak J., Szabo S., Willson J.K., Markowitz S., Kinzler K.W., Vogelstein B., Lengauer C., Velculescu V.E. Colorectal cancer: mutations in a signalling pathway. Nature 2005, 436:792.
81. Paweletz C.P., Charboneau L., Bichsel V.E., Simone N.L., Chen T., Gillespie J.W., Emmert-Buck M.R., Roth M.J., Petricoin I.E., Liotta L.A. Reverse phase protein microarrays which capture disease progression show activation of pro-survival pathways at the cancer invasion front. Oncogene 2001, 20:1981-1989.
82. 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, 76:3935-3943.
83. Posewitz M.C., Tempst P. Immobilized gallium(III) affinity chromatography of phosphopeptides. Anal. Chem. 1999, 71:2883-2892.
84. Ptacek J., Devgan G., Michaud G., Zhu H., Zhu X., Fasolo J., Guo H., Jona G., Breitkreutz A., Sopko R., McCartney R.R., Schmidt M.C., Rachidi N., Lee S.J., Mah A.S., Meng L., Stark M.J., Stern D.F., De Virgilio C., Tyers M., Andrews B., Gerstein M., Schweitzer B., Predki P.F., Snyder M. Global analysis of protein phosphorylation in yeast. Nature 2005, 438:679-684.
85. Rabindran S.K., Discafani C.M., Rosfjord E.C., Baxter M., Floyd M.B., Golas J., Hallett W.A., Johnson B.D., Nilakantan R., Overbeek E., Reich M.F., Shen R., Shi X., Tsou H.R., Wang Y.F., Wissner A. Antitumor activity of HKI-272, an orally active, irreversible inhibitor of the HER-2 tyrosine kinase. Cancer Res. 2004, 64:3958-3965.
86. Remsing Rix L.L., Rix U., Colinge J., Hantschel O., Bennett K.L., Stranzl T., Muller A., Baumgartner C., Valent P., Augustin M., Till J.H., Superti-Furga G. Global target profile of the kinase inhibitor bosutinib in primary chronic myeloid leukemia cells. Leukemia 2009, 23:477-485.
87. Rikova K., Guo A., Zeng Q., Possemato A., Yu J., Haack H., Nardone J., Lee K., Reeves C., Li Y., Hu Y., Tan Z., Stokes M., Sullivan L., Mitchell J., Wetzel R., Macneill J., Ren J.M., Yuan J., Bakalarski C.E., Villen J., Kornhauser J.M., Smith B., Li D., Zhou X., Gygi S.P., Gu T.L., Polakiewicz R.D., Rush J., Comb M.J. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007, 131:1190-1203.
88. Rix U., Hantschel O., Durnberger G., Remsing Rix L.L., Planyavsky M., Fernbach N.V., Kaupe I., Bennett K.L., Valent P., Colinge J., Kocher T., Superti-Furga G. Chemical proteomic profiles of the BCR-ABL inhibitors imatinib, nilotinib, and dasatinib reveal novel kinase and nonkinase targets. Blood 2007, 110:4055-4063.
89. Rix U., Remsing Rix L.L., Terker A.S., Fernbach N.V., Hantschel O., Planyavsky M., Breitwieser F.P., Herrmann H., Colinge J., Bennett K.L., Augustin M., Till J.H., Heinrich M.C., Valent P., Superti-Furga G. A comprehensive target selectivity survey of the BCR-ABL kinase inhibitor INNO-406 by kinase profiling and chemical proteomics in chronic myeloid leukemia cells. Leukemia 2010, 24:44-50.
90. Ross P.L., Huang Y.N., Marchese J.N., Williamson B., Parker K., Hattan S., Khainovski N., Pillai S., Dey S., Daniels S., Purkayastha S., Juhasz P., Martin S., Bartlet-Jones M., He F., Jacobson A., Pappin D.J. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell Proteomics 2004, 3:1154-1169.
91. Ruse C.I., McClatchy D.B., Lu B., Cociorva D., Motoyama A., Park S.K., Yates J.R. Motif-specific sampling of phosphoproteomes. J. Proteome Res. 2008, 7:2140-2150.
92. 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, 23:94-101.
93. Salomon A.R., Ficarro S.B., Brill L.M., Brinker A., Phung Q.T., Ericson C., Sauer K., Brock A., Horn D.M., Schultz P.G., Peters E.C. Profiling of tyrosine phosphorylation pathways in human cells using mass spectrometry. Proc. Natl. Acad. Sci. U S A 2003, 100:443-448.
94. Sano A., Nakamura H. Titania as a chemo-affinity support for the column-switching HPLC analysis of phosphopeptides: application to the characterization of phosphorylation sites in proteins by combination with protease digestion and electrospray ionization mass spectrometry. Anal. Sci. 2004, 20:861-864.
95. Sefton B.M. The viral tyrosine protein kinases. Curr. Top. Microbiol. Immunol. 1986, 123:39-72.
96. Sefton B.M., Hunter T., Beemon K., Eckhart W. Evidence that the phosphorylation of tyrosine is essential for cellular transformation by Rous sarcoma virus. Cell 1980, 20:807-816.
97. Sefton B.M., Hunter T., Raschke W.C. Evidence that the Abelson virus protein functions in vivo as a protein kinase that phosphorylates tyrosine. Proc. Natl. Acad. Sci. U S A 1981, 78:1552-1556.
98. Sharma S.V., Bell D.W., Settleman J., Haber D.A. Epidermal growth factor receptor mutations in lung cancer. Nat. Rev. Cancer 2007, 7:169-181.
99. Sheehan K.M., Calvert V.S., Kay E.W., Lu Y., Fishman D., Espina V., Aquino J., Speer R., Araujo R., Mills G.B., Liotta L.A., Petricoin E.F., Wulfkuhle J.D. Use of reverse phase protein microarrays and reference standard development for molecular network analysis of metastatic ovarian carcinoma. Mol. Cell Proteomics 2005, 4:346-355.
100. Shin J.S., Hong S.W., Lee S.L., Kim T.H., Park I.C., An S.K., Lee W.K., Lim J.S., Kim K.I., Yang Y., Lee S.S., Jin D.H., Lee M.S. Serum starvation induces G1 arrest through suppression of Skp2-CDK2 and CDK4 in SK-OV-3 cells. Int. J. Oncol. 2008, 32:435-439.
101. Spector D.H., Varmus H.E., Bishop J.M. Nucleotide sequences related to the transforming gene of avian sarcoma virus are present in DNA of uninfected vertebrates. Proc. Natl. Acad. Sci. U S A 1978, 75:4102-4106.
102. Stehelin D., Guntaka R.V., Varmus H.E., Bishop J.M. Purification of DNA complementary to nucleotide sequences required for neoplastic transformation of fibroblasts by avian sarcoma viruses. J. Mol. Biol. 1976, 101:349-365.
103. Stensballe A., Andersen S., Jensen O.N. Characterization of phosphoproteins from electrophoretic gels by nanoscale Fe(III) affinity chromatography with off-line mass spectrometry analysis. Proteomics 2001, 1:207-222.
104. Stephens P., Edkins S., Davies H., Greenman C., Cox C., Hunter C., Bignell G., Teague J., Smith R., Stevens C., O'Meara S., Parker A., Tarpey P., Avis T., Barthorpe A., Brackenbury L., Buck G., Butler A., Clements J., Cole J., Dicks E., Edwards K., Forbes S., Gorton M., Gray K., Halliday K., Harrison R., Hills K., Hinton J., Jones D., Kosmidou V., Laman R., Lugg R., Menzies A., Perry J., Petty R., Raine K., Shepherd R., Small A., Solomon H., Stephens Y., Tofts C., Varian J., Webb A., West S., Widaa S., Yates A., Brasseur F., Cooper C.S., Flanagan A.M., Green A., Knowles M., Leung S.Y., Looijenga L.H., Malkowicz B., Pierotti M.A., Teh B., Yuen S.T., Nicholson A.G., Lakhani S., Easton D.F., Weber B.L., Stratton M.R., Futreal P.A., Wooster R. A screen of the complete protein kinase gene family identifies diverse patterns of somatic mutations in human breast cancer. Nat. Genet. 2005, 37:590-592.
105. Stokes M.P., Rush J., Macneill J., Ren J.M., Sprott K., Nardone J., Yang V., Beausoleil S.A., Gygi S.P., Livingstone M., Zhang H., Polakiewicz R.D., Comb M.J. Profiling of UV-induced ATM/ATR signaling pathways. Proc. Natl. Acad. Sci. U S A 2007, 104:19855-19860.
106. 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, 106:995-1000.
107. Unwin R.D., Griffiths J.R., Leverentz M.K., Grallert A., Hagan I.M., Whetton A.D. Multiple reaction monitoring to identify sites of protein phosphorylation with high sensitivity. Mol. Cell Proteomics 2005, 4:1134-1144.
108. 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, 5:214-226.
109. Versele M., Talloen W., Rockx C., Geerts T., Janssen B., Lavrijssen T., King P., Gohlmann H.W., Page M., Perera T. Response prediction to a multitargeted kinase inhibitor in cancer cell lines and xenograft tumors using high-content tyrosine peptide arrays with a kinetic readout. Mol. Cancer Ther. 2009, 8:1846-1855.
110. 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, 30:1097-1104.
111. Walters D.K., Mercher T., Gu T.L., O'Hare T., Tyner J.W., Loriaux M., Goss V.L., Lee K.A., Eide C.A., Wong M.J., Stoffregen E.P., McGreevey L., Nardone J., Moore S.A., Crispino J., Boggon T.J., Heinrich M.C., Deininger M.W., Polakiewicz R.D., Gilliland D.G., Druker B.J. Activating alleles of JAK3 in acute megakaryoblastic leukemia. Cancer Cell 2006, 10:65-75.
112. Wang J.Y. Antibodies for phosphotyrosine: analytical and preparative tool for tyrosyl-phosphorylated proteins. Anal. Biochem. 1988, 172:1-7.
113. Witte O.N., Dasgupta A., Baltimore D. Abelson murine leukaemia virus protein is phosphorylated in vitro to form phosphotyrosine. Nature 1980, 283:826-831.
114. 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, 104:5860-5865.
115. Wulfkuhle J.D., Aquino J.A., Calvert V.S., Fishman D.A., Coukos G., Liotta L.A., Petricoin E.F. Signal pathway profiling of ovarian cancer from human tissue specimens using reverse-phase protein microarrays. Proteomics 2003, 3:2085-2090.
116. Xia Q., Cheng D., Duong D.M., Gearing M., Lah J.J., Levey A.I., Peng J. Phosphoproteomic analysis of human brain by calcium phosphate precipitation and mass spectrometry. J. Proteome Res. 2008, 7:2845-2851.
117. Xia W., Mullin R.J., Keith B.R., Liu L.H., Ma H., Rusnak D.W., Owens G., Alligood K.J., Spector N.L. Anti-tumor activity of GW572016: a dual tyrosine kinase inhibitor blocks EGF activation of EGFR/erbB2 and downstream Erk1/2 and AKT pathways. Oncogene 2002, 21:6255-6263.
118. Yip T.T., Hutchens T.W. Mapping and sequence-specific identification of phosphopeptides in unfractionated protein digest mixtures by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. FEBS Lett. 1992, 308:149-153.
119. Zander L., Bemark M. Identification of genes deregulated during serum-free medium adaptation of a Burkitt's lymphoma cell line. Cell Prolif. 2008, 41:136-155.
120. Zanivan S., Gnad F., Wickstrom S.A., Geiger T., Macek B., Cox J., Fassler R., Mann M. Solid tumor proteome and phosphoproteome analysis by high resolution mass spectrometry. J. Proteome Res. 2008, 7:5314-5326.
121. Zhang G., Neubert T.A. Use of stable isotope labeling by amino acids in cell culture (SILAC) for phosphotyrosine protein identification and quantitation. Methods Mol. Biol. 2009, 527:79-92. xi.
122. Zhang G., Spellman D.S., Skolnik E.Y., Neubert T.A. Quantitative phosphotyrosine proteomics of EphB2 signaling by stable isotope labeling with amino acids in cell culture (SILAC). J. Proteome Res. 2006, 5:581-588.
123. Zhang X., Ye J., 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.
124. 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, 4:1240-1250.
125. Zhong D., Liu X., Khuri F.R., Sun S.Y., Vertino P.M., Zhou W. LKB1 is necessary for Akt-mediated phosphorylation of proapoptotic proteins. Cancer Res. 2008, 68:7270-7277.
126. Zhong D., Xiong L., Liu T., Liu X., Liu X., Chen J., Sun S.Y., Khuri F.R., Zong Y., Zhou Q., Zhou W. The glycolytic inhibitor 2-deoxyglucose activates multiple prosurvival pathways through IGF1R. J. Biol. Chem. 2009, 284:23225-23233.
127. Zhou H., Watts J.D., Aebersold R. A systematic approach to the analysis of protein phosphorylation. Nat. Biotechnol. 2001, 19:375-378.