A bead-based activity screen for small-molecule inhibitors of signal transduction in chronic myelogenous leukemia cells

Molecular Cancer Therapeutics

Volumn 9, Issue 5, 2010, Pages 1469-1481

  Sylvester, Juliesta E ^a   Kron, Stephen J ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BCR ABL PROTEIN; CRK LIKE PROTEIN; DASATINIB; IMATINIB; INITIATION FACTOR 4E; STAT5 PROTEIN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BCR ABL GENE; CANCER RESISTANCE; CELL LYSATE; CHRONIC MYELOID LEUKEMIA; DRUG EFFICACY; DRUG SCREENING; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; ONCOGENE; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROGNOSIS; PROTEIN DOMAIN; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; CALIBRATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SCREENING ASSAYS, ANTITUMOR; FUSION PROTEINS, BCR-ABL; HUMANS; K562 CELLS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MICROSPHERES; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PYRIDINES; PYRIDONES; PYRIMIDINES; SIGNAL TRANSDUCTION; SMALL MOLECULE LIBRARIES; TIME FACTORS;

EID: 77952133664     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-10-0157     Document Type: Article

References (63)

1. Tefferi A, Vardiman JW. Classification and diagnosis of myeloproliferative neoplasms: the 2008 World Health Organization criteria and point-of-care diagnostic algorithms. Leukemia 2008;22:14-22.
2. Gorre ME, Mohammed M, Ellwood K, et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 2001;293:876-880 (Pubitemid 32743979)
3. Azam M, Latek RR, Daley GQ. Mechanisms of autoinhibition and STI-571/imatinib resistance revealed by mutagenesis of BCR-ABL. Cell 2003;112:831-843 (Pubitemid 36378885)
4. Donato NJ, Wu JY, Stapley J, et al. BCR-ABL independence and LYN kinase overexpression in chronic myelogenous leukemia cells selected for resistance to STI571. Blood 2003;101:690-698 (Pubitemid 36077594)
5. Faderl S, Talpaz M, Estrov Z, O'Brien S, Kurzrock R, Kantarjian HM. The biology of chronic myeloid leukemia. N Engl J Med 1999;341:164-172
6. Sebolt-Leopold JS, English JM. Mechanisms of drug inhibition of signalling molecules. Nature 2006;441:457-462
7. Dancey J, Sausville EA. Issues and progress with protein kinase inhibitors for cancer treatment. Nat Rev Drug Discov 2003;2:296-313. (Pubitemid 37361688)
8. Radich JP, Dai H, Mao M, et al. Gene expression changes associated with progression and response in chronic myeloid leukemia. Proc Natl Acad Sci U S A 2006;103:2794-2799 (Pubitemid 43306628)
9. White D, Saunders V, Lyons AB, et al. In vitro sensitivity to imatinib-induced inhibition of ABL kinase activity is predictive of molecular response in patients with de novo CML. Blood 2005;106:2520-2526
10. Reimer U, Reineke U, Schneider-Mergener J. Peptide arrays: from macro to micro. Curr Opin Biotechnol 2002;13:315-320
11. Houseman BT, Huh JH, Kron SJ, Mrksich M. Peptide chips for the quantitative evaluation of protein kinase activity. Nat Biotechnol 2002;20:270-274 (Pubitemid 34205420)
12. Janes KA, Albeck JG, Peng LX, Sorger PK, Lauffenburger DA, Yaffe MB. A high-throughput quantitative multiplex kinase assay for monitoring information flow in signaling networks: application to sepsis-apoptosis. Mol Cell Proteomics 2003;2:463-473
13. Diks SH, Kok K, O'Toole T, et al. Kinome profiling for studying lipopolysaccharide signal transduction in human peripheral blood mononuclear cells. J Biol Chem 2004;279:49206-49213 (Pubitemid 39625804)
14. Shults MD, Kozlov IA, Nelson N, et al. A multiplexed protein kinase assay. Chembiochem 2007;8:933-942
15. Kubota K, Anjum R, Yu Y, et al. Sensitive multiplexed analysis of kinase activities and activity-based kinase identification. Nat Biotechnol 2009;27:933-940
16. Versele M, Talloen W, Rockx C, et al. Response prediction to a multi-targeted 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
17. Wu D, Mand MR, Veach DR, Parker LL, Clarkson B, Kron SJ. A solid-phase Bcr-Abl kinase assay in 96-well hydrogel plates. Anal Biochem 2008;375:18-26.
18. Mand MR, Wu D, Veach DR, Kron SJ. Cell treatment and lysis in 96 well filter-bottom plates for screening Bcr-Abl activity and inhibition in whole cell extracts. J Biomol Screen 2010. In press. DOI: 10.1177/1087057110363307.
19. Songyang Z, Carraway KL III, Eck MJ, et al. Catalytic specificity of protein-tyrosine kinases is critical for selective signalling. Nature 1995;373:536-539
20. Pisabarro MT, Serrano L. Rational design of specific high-affinity peptide ligands for the Abl-SH3 domain. Biochemistry 1996;35:10634-10640 (Pubitemid 26279642)
21. Bence K, Ma W, Kozasa T, Huang XY. Direct stimulation of Bruton's tyrosine kinase by G(q)-protein á-subunit. Nature 1997;389:296-299 (Pubitemid 27406645)
22. Yamadori T, Baba Y, Matsushita M, et al. Bruton's tyrosine kinase activity is negatively regulated by Sab, the Btk-SH3 domain-binding protein. Proc Natl Acad Sci U S A 1999;96:6341-6346 (Pubitemid 29256667)
23. Donaldson LW, Gish G, Pawson T, Kay LE, Forman-Kay JD. Structure of a regulatory complex involving the Abl SH3 domain, the Crk SH2 domain, and a Crk-derived phosphopeptide. Proc Natl Acad Sci U S A 2002;99:14053-14058 (Pubitemid 35257623)
24. de Jong R, ten Hoeve J, Heisterkamp N, Groffen J. Tyrosine 207 in CRKL is the BCR/ABL phosphorylation site. Oncogene 1997;14:507-513
25. Gouilleux F, Wakao H, Mundt M, Groner B. Prolactin induces phosphorylation of Tyr694 of Stat5 (MGF), a prerequisite for DNA binding and induction of transcription. EMBO J 1994;13:4361-4369 (Pubitemid 24295208)
26. Okutani Y, Kitanaka A, Tanaka T, et al. Src directly tyrosinephosphorylates STAT5 on its activation site and is involved in erythropoietin-induced signaling pathway. Oncogene 2001;20:6643-6650 (Pubitemid 32980292)
27. Giavedoni LD. Simultaneous detection of multiple cytokines and chemokines from nonhuman primates using luminex technology. J Immunol Methods 2005;301:89-101.
28. Snedecor GW, Cochran WG. Statistical methods. 8th ed Ames: Iowa State University Press; 1989.
29. Huntsberger DV, Billingsley P. Elements of statistical inference. 6th ed Boston: Allyn and Bacon; 1987.
30. Owen DB. The power of student's t-test. J Am Stat Assoc 1965;60:320-333
31. Federighi ET. Extended tables of the percentage points of student's t-distribution. J Am Stat Assoc 1959;68:683-691
32. Gutierrez OA, Chavez M, Lissi E. A theoretical approach to some analytical properties of heterogeneous enzymatic assays. Anal Chem 2004;76:2664-2668 (Pubitemid 38585738)
33. Martins TB. Development of internal controls for the Luminex instrument as part of a multiplex seven-analyte viral respiratory antibody profile. Clin Diagn Lab Immunol 2002;9:41-45
34. Hanley B. Variance in multiplex suspension array assays: intraplex method improves reliability. Theor Biol Med Model 2007;4:32. (Pubitemid 47525014)
35. Wu D, Sylvester JE, Parker LL, Zhou G, Kron SJ. Peptide reporters of kinase activity in whole cell lysates. Pept Sci 2010. In press.
36. Parker LL, Brueggemeier SB, Rhee WJ, et al. Photocleavable peptide hydrogel arrays for MALDI-TOF analysis of kinase activity. Analyst 2006;131:1097-1104
37. Druker BJ, Tamura S, Buchdunger E, et al. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med 1996;2:561-566 (Pubitemid 26151518)
38. Lombardo LJ, Lee FY, Chen P, et al. Discovery of N-(2-chloro-6-methyl- phenyl)-2-(6-(4-(2-hydroxyethyl)- piperazin-1-yl)-2-methylpyrimidin-4- ylamino)thiazole-5-carboxamide (BMS-354825), a dual Src/Abl kinase inhibitor with potent antitumor activity in preclinical assays. J Med Chem 2004;47:6658-6661 (Pubitemid 40053752)
39. Wisniewski D, Lambek CL, Liu C, et al. Characterization of potent inhibitors of the Bcr-Abl and the c-kit receptor tyrosine kinases. Cancer Res 2002;62:4244-4255 (Pubitemid 34827279)
40. Thomas J, Wang L, Clark RE, Pirmohamed M. Active transport of imatinib into and out of cells: implications for drug resistance. Blood 2004;104:3739-3745 (Pubitemid 39564452)
41. von Bubnoff N, Veach DR, Miller WT, et al. Inhibition of wild-type and mutant Bcr-Abl by pyrido-pyrimidine-type small molecule kinase inhibitors. Cancer Res 2003;63:6395-6404
42. Tipping AJ, Baluch S, Barnes DJ, et al. Efficacy of dual-specific Bcr-Abl and Src-family kinase inhibitors in cells sensitive and resistant to imatinib mesylate. Leukemia 2004;18:1352-1356 (Pubitemid 39136744)
43. Shah NP, Kasap C, Weier C, et al. Transient potent BCR-ABL inhibition is sufficient to commit chronic myeloid leukemia cells irreversibly to apoptosis. Cancer Cell 2008;14:485-493
44. Seeliger MA, Nagar B, Frank F, Cao X, Henderson MN, Kuriyan J. c-Src binds to the cancer drug imatinib with an inactive Abl/c-Kit conformation and a distributed thermodynamic penalty. Structure 2007;15:299-311. (Pubitemid 46366721)
45. Bantscheff M, Eberhard D, Abraham Y, et al. Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors. Nat Biotechnol 2007;25:1035-1044 (Pubitemid 47517638)
46. Fabian MA, Biggs WH III, Treiber DK, et al. A small molecule-kinase interaction map for clinical kinase inhibitors. Nat Biotechnol 2005;23:329-336
47. Karaman MW, Herrgard S, Treiber DK, et al. A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol 2008;26:127-132
48. Hantschel O, Rix U, Superti-Furga G. Target spectrum of the BCRABL inhibitors imatinib, nilotinib and dasatinib. Leuk Lymphoma 2008;49:615-619 (Pubitemid 351517198)
49. Feller SM, Posern G, Voss J, et al. Physiological signals and oncogenesis mediated through Crk family adapter proteins. J Cell Physiol 1998;177:535-552 (Pubitemid 28541579)
50. Amoui M, Miller WT. The substrate specificity of the catalytic domain of Abl plays an important role in directing phosphorylation of the adaptor protein Crk. Cell Signal 2000;12:637-643
51. Kain KH, Gooch S, Klemke RL. Cytoplasmic c-Abl provides a molecular "Rheostat" controlling carcinoma cell survival and invasion. Oncogene 2003;22:6071-6080
52. Wu D, Nair-Gill E, Sher DA, et al. Assaying Bcr-Abl kinase activity and inhibition in whole cell extracts by phosphorylation of substrates immobilized on agarose beads. Anal Biochem 2005;347:67-76. (Pubitemid 41608569)
53. Saharinen P, Vihinen M, Silvennoinen O. Autoinhibition of Jak2 tyrosine kinase is dependent on specific regions in its pseudokinase domain. Mol Biol Cell 2003;14:1448-1459 (Pubitemid 36547413)
54. O'Hare T, Pollock R, Stoffregen EP, et al. Inhibition of wild-type and mutant Bcr-Abl by AP23464, a potent ATP-based oncogenic protein kinase inhibitor: implications for CML. Blood 2004;104:2532-2539 (Pubitemid 39331857)
55. Rauh-Adelmann C, Moskow JM, Graham JR, et al. Quantitative measurement of epidermal growth factor receptor-mitogen-activated protein kinase signal transduction using a nine-plex, peptide-based immunoassay. Anal Biochem 2008;375:255-264
56. Du J, Bernasconi P, Clauser KR, et al. Bead-based profiling of tyrosine kinase phosphorylation identifies SRC as a potential target for glioblastoma therapy. Nat Biotechnol 2009;27:77-83.
57. Bernsteel DJ, Roman DL, Neubig RR. In vitro protein kinase activity measurement by flow cytometry. Anal Biochem 2008;383:180-185
58. Jilani I, Kantarjian H, Gorre M, et al. Phosphorylation levels of BCR-ABL, CrkL, AKT and STAT5 in imatinib-resistant chronic myeloid leukemia cells implicate alternative pathway usage as a survival strategy. Leuk Res 2008;32:643-649 (Pubitemid 351248958)
59. Hughes TP, Branford S. Monitoring disease response to tyrosine kinase inhibitor therapy in CML. Hematology (Am Soc Hematol Educ Program) 2009:477-487
60. Zhang JH, Chung TD, Oldenburg KR. A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J Biomol Screen 1999;4:67-73.
61. Koren A, Tirosh I, Barkai N. Autocorrelation analysis reveals widespread spatial biases in microarray experiments. BMC Genomics 2007;8:164. (Pubitemid 47054424)
62. Xiaoming H, Syuhei S, Takayuki Y, et al. A quantitative peptide array for evaluation of protein kinase activity. Anal Biochem 2008;372:106-115
63. Busman M, Schey KL, Knapp DR. Identification of the phosphorylation sites in phosphopeptides by positive and negative mode electrospray ionization-tandem mass spectrometry. J Am Soc Mass Spectrom 1996;7:243-249 (Pubitemid 126351271)