Differential signaling networks of Bcr-Abl p210 and p190 kinases in leukemia cells defined by functional proteomics

Leukemia

Volumn 31, Issue 7, 2017, Pages 1502-1512

  Reckel, S ^a   Hamelin, R ^a   Georgeon, S ^a   Armand, F ^a   Jolliet, Q ^a   Chiappe, D ^a   Moniatte, M ^a   Hantschel, O ^a  

^a EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; CLATHRIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN P190; PROTEOME; STAT5 PROTEIN; TYROSINE;

ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOCYTOSIS; FUNCTIONAL PROTEOMICS; HUMAN; HUMAN CELL; LEUKEMIA CELL; MOLECULARLY TARGETED THERAPY; PHOSPHOPROTEOMICS; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE STUDY; VALIDATION STUDY; ENZYMOLOGY; LEUKEMIA; PHOSPHORYLATION; PHYSIOLOGY; PROCEDURES; SIGNAL TRANSDUCTION;

FUSION PROTEINS, BCR-ABL; HUMANS; LEUKEMIA; PHOSPHORYLATION; PROTEOMICS; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR;

EID: 85013652601     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2017.36     Document Type: Article

References (44)

1. O'Hare T, Zabriskie MS, Eiring AM, Deininger MW. Pushing the limits of targeted therapy in chronic myeloid leukaemia. Nat Rev Cancer 2012; 12: 513-526.
2. Wong S, Witte ON. The BCR-ABL story: bench to bedside and back. Annu Rev Immunol 2004; 22: 247-306.
3. Deininger MW, Goldman JM, Melo JV. The molecular biology of chronic myeloid leukemia. Blood 2000; 96: 3343-3356.
4. Hantschel O. Structure, regulation, signaling, and targeting of abl kinases in cancer. Genes Cancer 2012; 3: 436-446.
5. Gambacorti-Passerini C, Antolini L, Mahon F-X, Guilhot F, Deininger M, Fava C et al. Multicenter independent assessment of outcomes in chronic myeloid leukemia patients treated with imatinib. J Natl Cancer Inst 2011; 103: 553-561.
6. Fielding AK. How I treat Philadelphia chromosome positive acute lymphoblastic leukaemia. Blood 2010; 116: 3409-3417.
7. Rousselot P, Coude MM, Gokbuget N, Gambacorti Passerini C, Hayette S, Cayuela JM et al. Dasatinib and low-intensity chemotherapy in elderly patients with Philadelphia chromosome-positive ALL. Blood 2016; 128: 774-782.
8. Mullighan CG, Downing JR. Genome-wide profiling of genetic alterations in acute lymphoblastic leukemia: recent insights and future directions. Leukemia 2009; 23: 1209-1218.
9. Wong S, Witte ON. Modeling Philadelphia chromosome positive leukemias. Oncogene 2001; 20: 5644-5659.
10. Van Etten RA. Studying the pathogenesis of BCR-ABL+ leukemia in mice. Oncogene 2002; 21: 8643-8651.
11. Li S, Ilaria RL Jr, Million RP, Daley GQ, Van Etten RA. The P190, P210, and P230 forms of the BCR/ABL oncogene induce a similar chronic myeloid leukemia-like syndrome in mice but have different lymphoid leukemogenic activity. J Exp Med 1999; 189: 1399-1412.
12. Kovacic B, Hoelbl A, Litos G, Alacakaptan M, Schuster C, Fischhuber KM et al. Diverging fates of cells of origin in acute and chronic leukaemia. EMBO Mol Med 2012; 4: 283-297.
13. Hantschel O, Warsch W, Eckelhart E, Kaupe I, Grebien F, Wagner K-U et al. BCR-ABL uncouples canonical JAK2-STAT5 signaling in chronic myeloid leukemia. Nat Chem Biol 2012; 8: 285-293.
14. Okuda K, Golub TR, Gilliland DG, Griffin JD. p210BCR/ABL, p190BCR/ABL, and TEL/ABL activate similar signal transduction pathways in hematopoietic cell lines. Oncogene 1996; 13: 1147-1152.
15. Lugo TG, Pendergast AM, Muller AJ, Witte ON. Tyrosine kinase activity and transformation potency of bcr-abl oncogene products. Science 1990; 247: 1079-1082.
16. Ilaria RL Jr, Van Etten RA. The SH2 domain of P210BCR/ABL is not required for the transformation of hematopoietic factor-dependent cells. Blood 1995; 86: 3897-3904.
17. Brehme M, Hantschel O, Colinge J, Kaupe I, Planyavsky M, Kocher T et al. Charting the molecular network of the drug target Bcr-Abl. Proc Natl Acad Sci USA 2009; 106: 7414-7419.
18. Titz B, Low T, Komisopoulou E, Chen SS, Rubbi L, Graeber TG. The proximal signaling network of the BCR-ABL1 oncogene shows a modular organization. Oncogene 2010; 29: 5895-5910.
19. Cutler J, Tahir R, Sreenivasamurthy SK, Mitchell C, Renuse S, Nirujogi RS. Differential signaling through p190 and p210 BCR-ABL fusion proteins revealed by interactome and phosphoproteome analysis. Leukemia 2017.
20. Varjosalo M, Sacco R, Stukalov A, van Drogen A, Planyavsky M, Hauri S et al. Interlaboratory reproducibility of large-scale human protein-complex analysis by standardized AP-MS. Nat Methods 2013; 10: 307-314.
21. Burckstummer T, Bennett KL, Preradovic A, Schutze G, Hantschel O, Superti-Furga G et al. An efficient tandem affinity purification procedure for interaction proteomics in mammalian cells. Nat Methods 2006; 3: 1013-1019.
22. Schiff-Maker L, Burns MC, Konopka JB, Clark S, Witte ON, Rosenberg N. Monoclonal antibodies specific for v-abl- and c-abl-encoded molecules. J Virol 1986; 57: 1182-1186.
23. Kettenbach AN, Gerber SA. Rapid and reproducible single-stage phosphopeptide enrichment of complex peptide mixtures: application to general and phosphotyrosine-specific phosphoproteomics experiments. Anal Chem 2011; 83: 7635-7644.
24. Vizcaino JA, Csordas A, del-Toro N, Dianes JA, Griss J, Lavidas I et al. update of the PRIDE database and its related tools. Nucleic Acids Res 2016; 44: D447-D456.
25. Warmuth M, Kim S, Gu XJ, Xia G, Adrian F. Ba/F3 cells and their use in kinase drug discovery. Curr Opin Oncol 2007; 19: 55-60.
26. Hantschel O, Superti-Furga G. Regulation of the c-Abl and Bcr-Abl tyrosine kinases. Nat Rev Mol Cell Biol 2004; 5: 33-44.
27. De Keersmaecker K, Versele M, Cools J, Superti-Furga G, Hantschel O. Intrinsic differences between the catalytic properties of the oncogenic NUP214-ABL1 and BCR-ABL1 fusion protein kinases. Leukemia 2008; 22: 2208-2216.
28. Ren R. Mechanisms of BCR-ABL in the pathogenesis of chronic myelogenous leukaemia. Nat Rev Cancer 2005; 5: 172-183.
29. Shuai K, Horvath CM, Huang LH, Qureshi SA, Cowburn D, Darnell JE Jr. Interferon activation of the transcription factor Stat91 involves dimerization through SH2-phosphotyrosyl peptide interactions. Cell 1994; 76: 821-828.
30. 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.
31. Heisterkamp N, Voncken JW, Senadheera D, Gonzalez-Gomez I, Reichert A, Haataja L et al. Reduced oncogenicity of p190 Bcr/Abl F-actin-binding domain mutants. Blood 2000; 96: 2226-2232.
32. Wertheim JA, Perera SA, Hammer DA, Ren R, Boettiger D, Pear WS. Localization of BCR-ABL to F-actin regulates cell adhesion but does not attenuate CML development. Blood 2003; 102: 2220-2228.
33. Hantschel O, Wiesner S, Guttler T, Mackereth CD, Rix LL, Mikes Z et al. Structural basis for the cytoskeletal association of Bcr-Abl/c-Abl. Mol Cell 2005; 19: 461-473.
34. Mikhailik A, Ford B, Keller J, Chen Y, Nassar N, Carpino N. A phosphatase activity of Sts-1 contributes to the suppression of TCR signaling. Mol Cell 2007; 27: 486-497.
35. Neculai D, Neculai AM, Verrier S, Straub K, Klumpp K, Pfitzner E et al. Structure of the unphosphorylated STAT5a dimer. J Biol Chem 2005; 280: 40782-40787.
36. Fahrenkamp D, Li J, Ernst S, Schmitz-Van de Leur H, Chatain N, Kuster A et al. Intramolecular hydrophobic interactions are critical mediators of STAT5 dimerization. Sci Rep 2016; 6: 35454.
37. Hoelbl A, Schuster C, Kovacic B, Zhu B, Wickre M, Hoelzl MA et al. Stat5 is indispensable for the maintenance of bcr/abl-positive leukaemia. EMBO Mol Med 2010; 2: 98-110.
38. Warsch W, Kollmann K, Eckelhart E, Fajmann S, Cerny-Reiterer S, Holbl A et al. High STAT5 levels mediate imatinib resistance and indicate disease progression in chronic myeloid leukemia. Blood 2011; 117: 3409-3420.
39. Hu Y, Liu Y, Pelletier S, Buchdunger E, Warmuth M, Fabbro D et al. Requirement of Src kinases Lyn, Hck and Fgr for BCR-ABL1-induced B-lymphoblastic leukemia but not chronic myeloid leukemia. Nat Genet 2004; 36: 453-461.
40. Wu J, Meng F, Kong LY, Peng Z, Ying Y, Bornmann WG et al. Association between imatinib-resistant BCR-ABL mutation-negative leukemia and persistent activation of LYN kinase. J Natl Cancer Inst 2008; 100: 926-939.
41. Ptasznik A, Nakata Y, Kalota A, Emerson SG, Gewirtz AM. Short interfering RNA (siRNA) targeting the Lyn kinase induces apoptosis in primary, and drug-resistant, BCR-ABL1(+) leukemia cells. Nat Med 2004; 10: 1187-1189.
42. Yu G, Smithgall TE, Glazer RI. K562 leukemia cells transfected with the human c-fes gene acquire the ability to undergo myeloid differentiation. J Biol Chem 1989; 264: 10276-10281.
43. Roux KJ, Kim DI, Burke B. BioID: a screen for protein-protein interactions. Curr Protoc Protein Sci 2013; 74, Unit 19.23.1-19.34.14.
44. Varnaite R, MacNeill SA. Meet the neighbors: mapping local protein interactomes by proximity-dependent labeling with BioID. Proteomics 2016; 16: 2503-2518.