Quantitative phosphotyrosine profiling of patient-derived xenografts identifies therapeutic targets in pediatric leukemia

Cancer Research

Volumn 76, Issue 9, 2016, Pages 2766-2777

  Dolai, Sibasish ^a   Sia, Keith C S ^a   Robbins, Alissa K ^a   Zhong, Ling ^a   Heatley, Sue L ^b,c   Vincent, Tiffaney L ^d   Hochgräfe, Falko ^e   Sutton, Rosemary ^a   Kurmasheva, Raushan T ^f   Revesz, Tamas ^g,h   White, Deborah L ^b,c,g   Houghton, Peter J ^f   Smith, Malcolm A ⁱ   Teachey, David T ^d   Daly, Roger J ^j   Raftery, Mark J ^a   Lock, Richard B ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b SOUTH AUSTRALIAN HEALTH AND MEDICAL RESEARCH INSTITUTE   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^e UNIVERSITY OF GREIFSWALD   (Germany)

^f UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^g UNIVERSITY OF ADELAIDE   (Australia)

^h WOMEN S AND CHILDREN S HOSPITAL   (Australia)

ⁱ NATIONAL CANCER INSTITUTE   (United States)

^j MONASH UNIVERSITY   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD135 ANTIGEN; DASATINIB; JANUS KINASE; PROTEIN TYROSINE PHOSPHATASE; RUXOLITINIB; SUNITINIB;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHOSPHORYLATION; B LYMPHOCYTE; CANCER CLASSIFICATION; CELL LABELING; CELL LINEAGE; CELL MEDIATED CYTOTOXICITY; CHILD; CHILDHOOD LEUKEMIA; CLINICAL ARTICLE; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; ENZYME ANALYSIS; FEMALE; GENE EXPRESSION; HIGH RISK PATIENT; HUMAN; HUMAN TISSUE; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; ISOTOPE LABELING; MALE; MOUSE; NONHUMAN; PRE T LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TREATMENT RESPONSE; XENOGRAFT;

EID: 84969506748     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-2786     Document Type: Article

References (52)

1. Dores GM, Devesa SS, Curtis RE, Linet MS, Morton LM. Acute leukemia incidence and patient survival among children and adults in the United States, 2001-2007. Blood 2012;119:34-43.
2. Onciu M. Acute lymphoblastic leukemia. Hematol Oncol Clin North Am 2009;23:655-74.
3. Pui CH, Mullighan CG, Evans WE, Relling MV. Pediatric acute lymphoblastic leukemia: where are we going and how do we get there? Blood 2012;120:1165-74.
4. Hunger SP, Raetz EA, Loh ML, Mullighan CG. Improving outcomes for high-risk ALL: translating new discoveries into clinical care. Pediatr Blood Cancer 2011;56:984-93.
5. Moricke A, Reiter A, Zimmermann M, Gadner H, Stanulla M, Dordelmann M, et al. Risk-adjusted therapy of acute lymphoblastic leukemia can decrease treatment burden and improve survival: treatment results of 2169 unselected pediatric and adolescent patients enrolled in the trial ALL-BFM 95. Blood 2008;111:4477-89.
6. Pui CH, Carroll WL, Meshinchi S, Arceci RJ. Biology, risk stratification, and therapy of pediatric acute leukemias: an update. J Clin Oncol 2011;29:551-65.
7. Cleaver AL, Beesley AH, Firth MJ, Sturges NC, O'Leary RA, Hunger SP, et al. Gene-based outcome prediction in multiple cohorts of pediatric T-cell acute lymphoblastic leukemia: a Children's Oncology Group study. Mol Cancer 2010;9:105.
8. Yeoh EJ, Ross ME, Shurtleff SA, Williams WK, Patel D, Mahfouz R, et al. Classification, subtype discovery, and prediction of outcome in pediatric acute lymphoblastic leukemia by gene expression profiling. Cancer Cell 2002;1:133-43.
9. Ma M, Wang X, Tang J, Xue H, Chen J, Pan C, et al. Early T-cell precursor leukemia: a subtype of high risk childhood acute lymphoblastic leukemia. Front Med 2012;6:416-20.
10. Zhang J, Ding L, Holmfeldt L, Wu G, Heatley SL, Payne-Turner D, et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 2012;481:157-63.
11. Zhang J,Mullighan CG, Harvey RC,Wu G, Chen X, Edmonson M, et al. Key pathways are frequently mutated in high-risk childhood acute lymphoblastic leukemia: a report from the Children's Oncology Group. Blood 2011;118:3080-7.
12. Roberts KG, Morin RD, Zhang J, Hirst M, Zhao Y, Su X, et al. Genetic alterations activating kinase and cytokine receptor signaling in high-risk acute lymphoblastic leukemia. Cancer Cell 2012;22:153-66.
13. Salomon AR, Ficarro SB, Brill LM, Brinker A, Phung QT, Ericson C, et al. Profiling of tyrosine phosphorylation pathways in human cells usingmass spectrometry. Proc Natl Acad Sci U S A 2003;100:443-8.
14. Rush J, Moritz A, Lee KA, Guo A, Goss VL, Spek EJ, et al. Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat Biotechnol 2005;23:94-101.
15. Rikova K, Guo A, Zeng Q, Possemato A, Yu J, Haack H, et al. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007;131:1190-203.
16. Wang H, Kadlecek TA, Au-Yeung BB, Goodfellow HE, Hsu LY, Freedman TS, et al. ZAP-70: an essential kinase in T-cell signaling. Cold Spring Harb Perspect Biol 2010;2:a002279.
17. Baker AF, Dragovich T, Ihle NT, Williams R, Fenoglio-Preiser C, Powis G. Stability of phosphoprotein as a biological marker of tumor signaling. Clin Cancer Res 2005;11:4338-40.
18. Hochgrafe F, Zhang L, O'Toole SA, Browne BC, Pinese M, Porta Cubas A, et al. Tyrosine phosphorylation profiling reveals the signaling network characteristics of Basal breast cancer cells. Cancer Res 2010; 70:9391-401.
19. Lock RB, Liem N, Farnsworth ML, Milross CG, Xue C, Tajbakhsh M, et al. The nonobese diabetic/severe combined immunodeficient (NOD/SCID) mouse model of childhood acute lymphoblastic leukemia reveals intrinsic differences in biologic characteristics at diagnosis and relapse. Blood 2002;99:4100-8.
20. Liem NL, Papa RA, Milross CG, Schmid MA, Tajbakhsh M, Choi S, et al. Characterization of childhood acute lymphoblastic leukemia xenograft models for the preclinical evaluation of new therapies. Blood 2004; 103:3905-14.
21. Monetti M, Nagaraj N, Sharma K, Mann M. Large-scale phosphosite quantification in tissues by a spike-in SILAC method. Nat Methods 2011; 8:655-8.
22. Zhang G, Neubert TA. 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.
23. Goss VL, Lee KA, Moritz A, Nardone J, Spek EJ, MacNeill J, et al. A common phosphotyrosine signature for the Bcr-Abl kinase. Blood 2006;107:4888-97.
24. Thingholm TE, Jorgensen TJ, Jensen ON, Larsen MR. Highly selective enrichment of phosphorylated peptides using titaniumdioxide. Nat Protoc 2006;1:1929-35.
25. Cox J, Matic I, Hilger M, Nagaraj N, Selbach M, Olsen JV, et al. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat Protoc 2009;4:698-705.
26. Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M. Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res 2011;10:1794-805.
27. Anoopkumar-Dukie S, Carey JB, Conere T, O'Sullivan E, van Pelt FN, Allshire A. Resazurin assay of radiation response in cultured cells. Br J Radiol 2005;78:945-7.
28. Maude SL, Dolai S, Delgado-Martin C, Vincent T, Robbins A, Selvanathan A, et al. Efficacy of JAK/STAT pathway inhibition in murine xenograft models of early T-cell precursor (ETP) acute lymphoblastic leukemia. Blood 2015;125:1759-67.
29. Bhadri VA, Cowley MJ, Kaplan W, Trahair TN, Lock RB. Evaluation of the NOD/SCID xenograft model for glucocorticoid-regulated gene expression in childhood B-cell precursor acute lymphoblastic leukemia. BMC Genomics 2011;12:565.
30. Brownlie RJ, Zamoyska R. T cell receptor signalling networks: branched, diversified and bounded. Nat Rev Immunol 2013;13:257-69.
31. Geiger T, Cox J, Ostasiewicz P, Wisniewski JR, Mann M. Super-SILAC mix for quantitative proteomics of human tumor tissue. Nat Methods 2010;7:383-5.
32. Gajadhar AS, Johnson H, Slebos RJ, Shaddox K, Wiles K, Washington MK, et al. Phosphotyrosine signaling analysis in human tumors is confounded by systemic ischemia-driven artifacts and intra-specimen heterogeneity. Cancer Res 2015;75:1495-503.
33. Watts JD, Affolter M, Krebs DL, Wange RL, Samelson LE, Aebersold R. Identification by electrospray ionization mass spectrometry of the sites of tyrosine phosphorylation induced in activated Jurkat T cells on the protein tyrosine kinase ZAP-70. J Biol Chem 1994;269:29520-9.
34. Newman JD, Harrison LC, Eckardt GS, Jack I. Enhanced insulin-receptor tyrosine kinase activity associated with chromosomal translocation (1;19) in a pre-B-cell leukemia line. Int J Cancer 1992;50:500-4.
35. Razumovskaya E, Masson K, Khan R, Bengtsson S, Ronnstrand L. Oncogenic Flt3 receptors display different specificity and kinetics of autophosphorylation. Exp Hematol 2009;37:979-89.
36. Kolb EA, Gorlick R, Houghton PJ, Morton CL, Lock RB, Tajbakhsh M, et al. Initial testing of dasatinib by the pediatric preclinical testing program. Pediatr Blood Cancer 2008;50:1198-206.
37. Maris JM, Courtright J, Houghton PJ, Morton CL, Kolb EA, Lock R, et al. Initial testing (stage 1) of sunitinib by the pediatric preclinical testing program. Pediatr Blood Cancer 2008;51:42-8.
38. Verstovsek S. Ruxolitinib: an oral Janus kinase 1 and Janus kinase 2 inhibitor in the management of myelofibrosis. Postgrad Med 2013;125: 128-35.
39. Scheijen B, Griffin JD. Tyrosine kinase oncogenes in normal hematopoiesis and hematological disease. Oncogene 2002;21:3314-33.
40. Harvey RC, Mullighan CG, Wang X, Dobbin KK, Davidson GS, Bedrick EJ, et al. Identification of novel cluster groups in pediatric high-risk B-precursor acute lymphoblastic leukemia with gene expression profiling: correlation with genome-wide DNA copy number alterations, clinical characteristics, and outcome. Blood 2010;116:4874-84.
41. Harsha HC, Pandey A. Phosphoproteomics in cancer. Mol Oncol 2010; 4:482-95.
42. Gu TL, Nardone J,Wang Y, LoriauxM, Villen J, Beausoleil S, et al. Survey of activated FLT3 signaling in leukemia. PLoS ONE 2011;6:e19169.
43. Storvold GL, Landskron J, Strozynski M, Arntzen MO, Koehler CJ, Kalland ME, et al. Quantitative profiling of tyrosine phosphorylation revealed changes in the activity of the T cell receptor signaling pathway upon cisplatin-induced apoptosis. J Proteomics 2013;91: 344-57.
44. Rubbi L, Titz B, Brown L, Galvan E, Komisopoulou E, Chen SS, et al. Global phosphoproteomics reveals crosstalk between Bcr-Abl and negative feedback mechanisms controlling Src signaling. Sci Signal 2011;4:ra18.
45. Preisinger C, Schwarz JP, Bleijerveld OB, Corradini E, Muller PJ, Anderson KI, et al. Imatinib-dependent tyrosine phosphorylation profiling of Bcr-Abl-positive chronic myeloid leukemia cells. Leukemia 2013;27: 743-6.
46. Hunter T, Sefton BM. Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc Natl Acad Sci U S A 1980;77:1311-5.
47. Deenik W, Beverloo HB, van der Poel-van de Luytgaarde SC,Wattel MM, van Esser JW, Valk PJ, et al. Rapid complete cytogenetic remission after upfront dasatinib monotherapy in a patient with a NUP214-ABL1-positive T-cell acute lymphoblastic leukemia. Leukemia 2009;23: 627-9.
48. Quintas-Cardama A, Tong W, Manshouri T, Vega F, Lennon PA, Cools J, et al. Activity of tyrosine kinase inhibitors against human NUP214-ABL1-positive T cell malignancies. Leukemia 2008;22:1117-24.
49. Frohling S, Scholl C, Levine RL, Loriaux M, Boggon TJ, Bernard OA, et al. Identification of driver and passenger mutations of FLT3 by high-throughput DNA sequence analysis and functional assessment of candidate alleles. Cancer Cell 2007;12:501-13.
50. Rocnik JL, Okabe R, Yu JC, Lee BH, Giese N, Schenkein DP, et al. Roles of tyrosine 589 and 591 in STAT5 activation and transformationmediated by FLT3-ITD. Blood 2006;108:1339-45.
51. Neumann M, Heesch S, Schlee C, Schwartz S,Gokbuget N, Hoelzer D, et al. Whole-exome sequencing in adult ETP-ALL reveals a high rate of DNMT3A mutations. Blood 2013;121:4749-52.
52. Rawlings JS, Rosler KM, Harrison DA. The JAK/STAT signaling pathway. J Cell Sci 2004;117(Pt 8):1281-3.