Dual phosphoproteomics and chemical proteomics analysis of erlotinib and gefitinib interference in acute myeloid leukemia cells

Journal of Proteomics

Volumn 75, Issue 4, 2012, Pages 1343-1356

  Weber, Christoph ^a,b   Schreiber, Thiemo B ^a   Daub, Henrik ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b EVOTEC AG   (Germany)

Author keywords

Acute myeloid leukemia; Chemical proteomics; Kinase inhibitor; Phosphoproteomics; Signal transduction; SILAC

Indexed keywords

ADDUCIN GAMMA; BRUTON TYROSINE KINASE; CD34 ANTIGEN; ERLOTINIB; GEFITINIB; INTERSECTIN; INTERSECTIN 2; MEMBRANE PROTEIN; NUCLEAR FACTOR Y; NUCLEAR FACTOR Y ALPHA; PROTEIN KINASE C DELTA; PROTEIN KINASE SYK; PROTEIN S6; SODIUM PROTON EXCHANGE PROTEIN 1; TRANSGELIN; TRANSGELIN 2; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VIMENTIN;

ACUTE GRANULOCYTIC LEUKEMIA; ARTICLE; BIOINFORMATICS; CANCER CELL CULTURE; CHEMICAL PROTEOMICS; CONTROLLED STUDY; DOWN REGULATION; DRUG TARGETING; DUAL PHOSPHOPROTEOMICS; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEOMICS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL SURVIVAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, LEUKEMIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LEUKEMIA, MYELOID, ACUTE; MASS SPECTROMETRY; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEOMICS; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 84855874661     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.11.004     Document Type: Article

References (74)

1. Estey E., Dohner H. Acute myeloid leukaemia. Lancet 2006, 368:1894-1907.
2. Chen J., Odenike O., Rowley J.D. Leukaemogenesis: more than mutant genes. Nat Rev Cancer 2010, 10:23-36.
3. Renneville A., Roumier C., Biggio V., Nibourel O., Boissel N., Fenaux P., et al. Cooperating gene mutations in acute myeloid leukemia: a review of the literature. Leukemia 2008, 22:915-931.
4. Tallman M.S., Gilliland D.G., Rowe J.M. Drug therapy for acute myeloid leukemia. Blood 2005, 106:1154-1163.
5. Hamilton A., Gallipoli P., Nicholson E., Holyoake T.L. Targeted therapy in haematological malignancies. J Pathol 2010, 220:404-418.
6. Kindler T., Lipka D.B., Fischer T. FLT3 as a therapeutic target in AML: still challenging after all these years. Blood 2010, 116:5089-5102.
7. Zarrinkar P.P., Gunawardane R.N., Cramer M.D., Gardner M.F., Brigham D., Belli B., et al. AC220 is a uniquely potent and selective inhibitor of FLT3 for the treatment of acute myeloid leukemia (AML). Blood 2009, 114:2984-2992.
8. Levis M.J. Will newer tyrosine kinase inhibitors have an impact in AML?. Best Pract Res Clin Haematol 2010, 23:489-494.
9. Blume-Jensen P., Hunter T. Oncogenic kinase signalling. Nature 2001, 411:355-365.
10. Zhang J., Yang P.L., Gray N.S. Targeting cancer with small molecule kinase inhibitors. Nat Rev Cancer 2009, 9:28-39.
11. Stegmeier F., Warmuth M., Sellers W.R., Dorsch M. Targeted cancer therapies in the twenty-first century: lessons from imatinib. Clin Pharmacol Ther 2010, 87:543-552.
12. Pao W., Chmielecki J. Rational, biologically based treatment of EGFR-mutant non-small-cell lung cancer. Nat Rev Cancer 2010, 10:760-774.
13. Boehrer S., Ades L., Braun T., Galluzzi L., Grosjean J., Fabre C., et al. Erlotinib exhibits antineoplastic off-target effects in AML and MDS: a preclinical study. Blood 2008, 111:2170-2180.
14. Boehrer S., Ades L., Galluzzi L., Tajeddine N., Tailler M., Gardin C., et al. Erlotinib and gefitinib for the treatment of myelodysplastic syndrome and acute myeloid leukemia: a preclinical comparison. Biochem Pharmacol 2008, 76:1417-1425.
15. Lindhagen E., Eriksson A., Wickstrom M., Danielsson K., Grundmark B., Henriksson R., et al. Significant cytotoxic activity in vitro of the EGFR tyrosine kinase inhibitor gefitinib in acute myeloblastic leukaemia. Eur J Haematol 2008, 81:344-353.
16. Stegmaier K., Corsello S.M., Ross K.N., Wong J.S., Deangelo D.J., Golub T.R. Gefitinib induces myeloid differentiation of acute myeloid leukemia. Blood 2005, 106:2841-2848.
17. Hahn C.K., Berchuck J.E., Ross K.N., Kakoza R.M., Clauser K., Schinzel A.C., et al. Proteomic and genetic approaches identify Syk as an AML target. Cancer Cell 2009, 16:281-294.
18. Chan G., Pilichowska M. Complete remission in a patient with acute myelogenous leukemia treated with erlotinib for non small-cell lung cancer. Blood 2007, 110:1079-1080.
19. Pitini V., Arrigo C., Altavilla G. Erlotinib in a patient with acute myelogenous leukemia and concomitant non-small-cell lung cancer. J Clin Oncol 2008, 26:3645-3646.
20. Brehmer D., Greff Z., Godl K., Blencke S., Kurtenbach A., Weber M., et al. Cellular targets of gefitinib. Cancer Res 2005, 65:379-382.
21. Karaman M.W., Herrgard S., Treiber D.K., Gallant P., Atteridge C.E., Campbell B.T., et al. A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol 2008, 26:127-132.
22. Sharma K., Weber C., Bairlein M., Greff Z., Keri G., Cox J., et al. Proteomics strategy for quantitative protein interaction profiling in cell extracts. Nat Methods 2009, 6:741-744.
23. Choudhary C., Mann M. Decoding signalling networks by mass spectrometry-based proteomics. Nat Rev Mol Cell Biol 2010, 11:427-439.
24. Schreiber T.B., Mausbacher N., Breitkopf S.B., Grundner-Culemann K., Daub H. Quantitative phosphoproteomics-an emerging key technology in signal-transduction research. Proteomics 2008, 8:4416-4432.
25. Harsha H.C., Pandey A. Phosphoproteomics in cancer. Mol Oncol 2010, 4:482-495.
26. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 2008, 26:1367-1372.
27. Olsen J.V., de Godoy L.M., Li G., Macek B., Mortensen P., Pesch R., et al. Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteomics 2005, 4:2010-2021.
28. Olsen J.V., Vermeulen M., Santamaria A., Kumar C., Miller M.L., Jensen L.J., et al. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal 2010, 3:ra3.
29. Villen J., Gygi S.P. The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry. Nat Protoc 2008, 3:1630-1638.
30. Mann M. Functional and quantitative proteomics using SILAC. Nat Rev Mol Cell Biol 2006, 7:952-958.
31. 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.
32. Bantscheff M., Eberhard D., Abraham Y., Bastuck S., Boesche M., Hobson S., et al. Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors. Nat Biotechnol 2007, 25:1035-1044.
33. Daub H., Olsen J.V., Bairlein M., Gnad F., Oppermann F.S., Korner R., et al. Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol Cell 2008, 31:438-448.
34. Olsen J.V., Blagoev B., Gnad F., Macek B., Kumar C., Mortensen P., et al. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127:635-648.
35. Schroeder M.J., Shabanowitz J., Schwartz J.C., Hunt D.F., Coon J.J. A neutral loss activation method for improved phosphopeptide sequence analysis by quadrupole ion trap mass spectrometry. Anal Chem 2004, 76:3590-3598.
36. Breitling R., Armengaud P., Amtmann A., Herzyk P. Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 2004, 573:83-92.
37. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., et al. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 2003, 4:P3.
38. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
39. Jensen L.J., Kuhn M., Stark M., Chaffron S., Creevey C., Muller J., et al. STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 2009, 37:D412-D416.
40. Cline M.S., Smoot M., Cerami E., Kuchinsky A., Landys N., Workman C., et al. Integration of biological networks and gene expression data using Cytoscape. Nat Protoc 2007, 2:2366-2382.
41. Schwartz D., Gygi S.P. An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nat Biotechnol 2005, 23:1391-1398.
42. Boehrer S., Ades L., Galluzzi L., Tajeddine N., Tailler M., Gardin C., et al. Erlotinib and gefitinib for the treatment of myelodysplastic syndrome and acute myeloid leukemia: a preclinical comparison. Biochem Pharmacol 2008, 76:1417-1425.
43. Choudhary C., Olsen J.V., Brandts C., Cox J., Reddy P.N., Bohmer F.D., et al. Mislocalized activation of oncogenic RTKs switches downstream signaling outcomes. Mol Cell 2009, 36:326-339.
44. Nolen B., Taylor S., Ghosh G. Regulation of protein kinases; controlling activity through activation segment conformation. Mol Cell 2004, 15:661-675.
45. Grant S. Is the focus moving toward a combination of targeted drugs?. Best Pract Res Clin Haematol 2008, 21:629-637.
46. Tsai S.C., Seto E. Regulation of histone deacetylase 2 by protein kinase CK2. J Biol Chem 2002, 277:31826-31833.
47. Pflum M.K., Tong J.K., Lane W.S., Schreiber S.L. Histone deacetylase 1 phosphorylation promotes enzymatic activity and complex formation. J Biol Chem 2001, 276:47733-47741.
48. Tsang E., Giannetti A.M., Shaw D., Dinh M., Tse J.K., Gandhi S., et al. Molecular mechanism of the Syk activation switch. J Biol Chem 2008, 283:32650-32659.
49. Law C.L., Chandran K.A., Sidorenko S.P., Clark E.A. Phospholipase C-gamma1 interacts with conserved phosphotyrosyl residues in the linker region of Syk and is a substrate for Syk. Mol Cell Biol 1996, 16:1305-1315.
50. Walchli S., Aasheim H.C., Skanland S.S., Spilsberg B., Torgersen M.L., Rosendal K.R., et al. Characterization of clathrin and Syk interaction upon Shiga toxin binding. Cell Signal 2009, 21:1161-1168.
51. Kurosaki T., Kurosaki M. Transphosphorylation of Bruton's tyrosine kinase on tyrosine 551 is critical for B cell antigen receptor function. J Biol Chem 1997, 272:15595-15598.
52. Dinh M., Grunberger D., Ho H., Tsing S.Y., Shaw D., Lee S., et al. Activation mechanism and steady state kinetics of Bruton's tyrosine kinase. J Biol Chem 2007, 282:8768-8776.
53. Wahl M.I., Fluckiger A.C., Kato R.M., Park H., Witte O.N., Rawlings D.J. Phosphorylation of two regulatory tyrosine residues in the activation of Bruton's tyrosine kinase via alternative receptors. Proc Natl Acad Sci U S A 1997, 94:11526-11533.
54. Baba Y., Hashimoto S., Matsushita M., Watanabe D., Kishimoto T., Kurosaki T., et al. BLNK mediates Syk-dependent Btk activation. Proc Natl Acad Sci U S A 2001, 98:2582-2586.
55. Rawlings D.J., Scharenberg A.M., Park H., Wahl M.I., Lin S., Kato R.M., et al. Activation of BTK by a phosphorylation mechanism initiated by SRC family kinases. Science 1996, 271:822-825.
56. Murugappan S., Shankar H., Bhamidipati S., Dorsam R.T., Jin J., Kunapuli S.P. Molecular mechanism and functional implications of thrombin-mediated tyrosine phosphorylation of PKCdelta in platelets. Blood 2005, 106:550-557.
57. Rybin V.O., Guo J., Harleton E., Feinmark S.J., Steinberg S.F. Regulatory autophosphorylation sites on protein kinase C-delta at threonine-141 and threonine-295. Biochemistry 2009, 48:4642-4651.
58. Hall K.J., Jones M.L., Poole A.W. Coincident regulation of PKCdelta in human platelets by phosphorylation of Tyr311 and Tyr565 and phospholipase C signalling. Biochem J 2007, 406:501-509.
59. Jo O.D., Martin J., Bernath A., Masri J., Lichtenstein A., Gera J. Heterogeneous nuclear ribonucleoprotein A1 regulates cyclin D1 and c-myc internal ribosome entry site function through Akt signaling. J Biol Chem 2008, 283:23274-23287.
60. Daub H. Kinase inhibitors: narrowing down the real targets. Nat Chem Biol 2010, 6:249-250.
61. Rix U., Superti-Furga G. Target profiling of small molecules by chemical proteomics. Nat Chem Biol 2009, 5:616-624.
62. Dos Santos C., Demur C., Bardet V., Prade-Houdellier N., Payrastre B., Recher C. A critical role for Lyn in acute myeloid leukemia. Blood 2008, 111:2269-2279.
63. Li Z., Xu M., Xing S., Ho W.T., Ishii T., Li Q., et al. Erlotinib effectively inhibits JAK2V617F activity and polycythemia vera cell growth. J Biol Chem 2007, 282:3428-3432.
64. Zhang Z., Shen K., Lu W., Cole P.A. The role of C-terminal tyrosine phosphorylation in the regulation of SHP-1 explored via expressed protein ligation. J Biol Chem 2003, 278:4668-4674.
65. Lu W., Gong D., Bar-Sagi D., Cole P.A. Site-specific incorporation of a phosphotyrosine mimetic reveals a role for tyrosine phosphorylation of SHP-2 in cell signaling. Mol Cell 2001, 8:759-769.
66. Neel B.G., Gu H., Pao L. The 'Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem Sci 2003, 28:284-293.
67. Bentires-Alj M., Paez J.G., David F.S., Keilhack H., Halmos B., Naoki K., et al. Activating mutations of the noonan syndrome-associated SHP2/PTPN11 gene in human solid tumors and adult acute myelogenous leukemia. Cancer Res 2004, 64:8816-8820.
68. Scheper G.C., Proud C.G. Does phosphorylation of the cap-binding protein eIF4E play a role in translation initiation?. Eur J Biochem 2002, 269:5350-5359.
69. Lekmine F., Sassano A., Uddin S., Smith J., Majchrzak B., Brachmann S.M., et al. Interferon-gamma engages the p70 S6 kinase to regulate phosphorylation of the 40S S6 ribosomal protein. Exp Cell Res 2004, 295:173-182.
70. Roux P.P., Shahbazian D., Vu H., Holz M.K., Cohen M.S., Taunton J., et al. RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J Biol Chem 2007, 282:14056-14064.
71. Lal L., Li Y., Smith J., Sassano A., Uddin S., Parmar S., et al. Activation of the p70 S6 kinase by all-trans-retinoic acid in acute promyelocytic leukemia cells. Blood 2005, 105:1669-1677.
72. Beausoleil S.A., Villen J., Gerber S.A., Rush J., Gygi S.P. A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat Biotechnol 2006, 24:1285-1292.
73. Manning G., Whyte D.B., Martinez R., Hunter T., Sudarsanam S. The protein kinase complement of the human genome. Science 2002, 298:1912-1934.
74. Knight Z.A., Shokat K.M. Features of selective kinase inhibitors. Chem Biol 2005, 12:621-637.