Centrosomal targeting of tyrosine kinase activity does not enhance oncogenicity in chronic myeloproliferative disorders

Leukemia

Volumn 26, Issue 4, 2012, Pages 728-735

  Bochtler, T ^a,b   Kirsch, M ^a,b   Maier, B ^a,b   Bachmann, J ^c   Klingmuller U ^c   Anderhub, S ^a,b   Ho, A D ^b   Kramer A ^a,b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c GERMAN CANCER RESEARCH CENTER   (Germany)

Author keywords

centrosome; chronic myeloproliferative disorder; PDGFR; tyrosine kinase

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 1; HYBRID PROTEIN; IMATINIB; JANUS KINASE 2; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ARTICLE; CARCINOGENICITY; CENTROSOME; CHRONIC DISEASE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MOUSE; MYELOPROLIFERATIVE DISORDER; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CENTROSOME; CHRONIC DISEASE; HUMANS; MYELOPROLIFERATIVE DISORDERS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; RECOMBINANT FUSION PROTEINS; TYROSINE;

EID: 84859627950     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2011.283     Document Type: Article

References (48)

1. Delhommeau F, Pisani DF, James C, Casadevall N, Constantinescu S, Vainchenker W. Oncogenic mechanisms in myeloproliferative disorders. Cell Mol Life Sci 2006; 63: 2939-2953. (Pubitemid 46072300)
2. De Keersmaecker K, Cools J. Chronic myeloproliferative disorders: a tyrosine kinase tale. Leukemia 2006; 20: 200-205. (Pubitemid 43148653)
3. Macdonald D, Cross NC. Chronic myeloproliferative disorders: the role of tyrosine kinases in pathogenesis, diagnosis and therapy. Pathobiology 2007; 74: 81-88. (Pubitemid 46985280)
4. Reiter A, Invernizzi R, Cross NC, Cazzola M. Molecular basis of myelodysplastic/myeloproliferative neoplasms. Haematologica 2009; 94: 1634-1638.
5. Tefferi A, Gilliland DG. Oncogenes in myeloproliferative disorders. Cell Cycle 2007; 6: 550-566. (Pubitemid 46440428)
6. Roumiantsev S, Krause DS, Neumann CA, Dimitri CA, Asiedu F, Cross NC et al. Distinct stem cell myeloproliferative/T lymphoma syndromes induced by ZNF198-FGFR1 and BCR-FGFR1 fusion genes from 8p11 translocations. Cancer Cell 2004; 5: 287-298. (Pubitemid 38402120)
7. Guasch G, Ollendorff V, Borg JP, Birnbaum D, Pebusque MJ. 8p12 stem cell myeloproliferative disorder: the FOP-fibroblast growth factor receptor 1 fusion protein of the t(6;8) translocation induces cell survival mediated by mitogen-activated protein kinase and phosphatidylinositol 3-kinase/Akt/mTOR pathways. Mol Cell Biol 2001; 21: 8129-8142. (Pubitemid 33051802)
8. Guasch G, Mack GJ, Popovici C, Dastugue N, Birnbaum D, Rattner JB et al. FGFR1 is fused to the centrosome-associated protein CEP110 in the 8p12 stem cell myeloproliferative disorder with t(8;9)(p12;q33). Blood 2000; 95: 1788-1796. (Pubitemid 30120844)
9. Walz C, Chase A, Schoch C, Weisser A, Schlegel F, Hochhaus A et al. The t(8;17)(p11;q23) in the 8p11 myeloproliferative syndrome fuses MYO18A to FGFR1. Leukemia 2005; 19: 1005-1009. (Pubitemid 40862012)
10. Reiter A, Walz C, Watmore A, Schoch C, Blau I, Schlegelberger B et al. The t(8;9)(p22;p24) is a recurrent abnormality in chronic and acute leukemia that fuses PCM1 to JAK2. Cancer Res 2005; 65: 2662-2667. (Pubitemid 40490065)
11. Murati A, Gelsi-Boyer V, Adelaide J, Perot C, Talmant P, Giraudier S et al. PCM1-JAK2 fusion in myeloproliferative disorders and acute erythroid leukemia with t(8;9) translocation. Leukemia 2005; 19: 1692-1696. (Pubitemid 43090425)
12. Bousquet M, Quelen C, De Mas V, Duchayne E, Roquefeuil B, Delsol G et al. The t(8;9)(p22;p24) translocation in atypical chronic myeloid leukaemia yields a new PCM1-JAK2 fusion gene. Oncogene 2005; 24: 7248-7252. (Pubitemid 41679286)
13. Walz C, Curtis C, Schnittger S, Schultheis B, Metzgeroth G, Schoch C et al. Transient response to imatinib in a chronic eosinophilic leukemia associated with ins(9;4)(q33;q12q25) and a CDK5RAP2-PDGFRA fusion gene. Genes Chromosomes Cancer 2006; 45: 950-956. (Pubitemid 44360182)
14. Wilkinson K, Velloso ER, Lopes LF, Lee C, Aster JC, Shipp MA et al. Cloning of the t(1;5)(q23;q33) in a myeloproliferative disorder associated with eosinophilia: involvement of PDGFRB and response to imatinib. Blood 2003; 102: 4187-4190. (Pubitemid 37487006)
15. Vizmanos JL, Novo FJ, Roman JP, Baxter EJ, Lahortiga I, Larrayoz MJ et al. NIN, a gene encoding a CEP110-like centrosomal protein, is fused to PDGFRB in a patient with a t(5;14)(q33;q24) and an imatinib-responsive myeloproliferative disorder. Cancer Res 2004; 64: 2673-2676. (Pubitemid 38500599)
16. Abe A, Emi N, Tanimoto M, Terasaki H, Marunouchi T, Saito H. Fusion of the platelet-derived growth factor receptor beta to a novel gene CEV14 in acute myelogenous leukemia after clonal evolution. Blood 1997; 90: 4271-4277. (Pubitemid 27508432)
17. Grand FH, Burgstaller S, Kuhr T, Baxter EJ, Webersinke G, Thaler J et al. p53-Binding protein 1 is fused to the platelet-derived growth factor receptor beta in a patient with a t(5;15)(q33;q22) and an imatinib-responsive eosinophilic myeloproliferative disorder. Cancer Res 2004; 64: 7216-7219. (Pubitemid 39372054)
18. La Starza R, Rosati R, Roti G, Gorello P, Bardi A, Crescenzi B et al. A new NDE1/PDGFRB fusion transcript underlying chronic myelomonocytic leukaemia in Noonan Syndrome. Leukemia 2007; 21: 830-833. (Pubitemid 46444578)
19. Luders J, Stearns T. Microtubule-organizing centres: a re-evaluation. Nat Rev Mol Cell Biol 2007; 8: 161-167. (Pubitemid 46432528)
20. Doxsey S, Zimmerman W, Mikule K. Centrosome control of the cell cycle. Trends Cell Biol 2005; 15: 303-311. (Pubitemid 40805326)
21. Kramer A, Mailand N, Lukas C, Syljuasen RG, Wilkinson CJ, Nigg EA et al. Centrosome-associated Chk1 prevents premature activation of cyclin-B-Cdk1 kinase. Nat Cell Biol 2004; 6: 884-891. (Pubitemid 39207253)
22. Nigg EA. Centrosome aberrations: cause or consequence of cancer progression? Nat Rev Cancer 2002; 2: 815-825. (Pubitemid 37328900)
23. Pihan GA, Purohit A, Wallace J, Knecht H, Woda B, Quesenberry P et al. Centrosome defects and genetic instability in malignant tumors. Cancer Res 1998; 58: 3974-3985. (Pubitemid 28405657)
24. Neben K, Giesecke C, Schweizer S, Ho AD, Kramer A. Centrosome aberrations in acute myeloid leukemia are correlated with cytogenetic risk profile. Blood 2003; 101: 289-291. (Pubitemid 36025920)
25. Giehl M, Fabarius A, Frank O, Hochhaus A, Hafner M, Hehlmann R et al. Centrosome aberrations in chronic myeloid leukemia correlate with stage of disease and chromosomal instability. Leukemia 2005; 19: 1192-1197. (Pubitemid 40946003)
26. Delaval B, Lelievre H, Birnbaum D. Myeloproliferative disorders: the centrosome connection. Leukemia 2005; 19: 1739-1744. (Pubitemid 41486150)
27. Delaval B, Letard S, Lelievre H, Chevrier V, Daviet L, Dubreuil P et al. Oncogenic tyrosine kinase of malignant hemopathy targets the centrosome. Cancer Res 2005; 65: 7231-7240. (Pubitemid 41161254)
28. Lelievre H, Chevrier V, Tassin AM, Birnbaum D. Myeloproliferative disorder FOP-FGFR1 fusion kinase recruits phosphoinositide-3 kinase and phospholipase Cgamma at the centrosome. Mol Cancer 2008; 7: 30.
29. Mikolajka A, Yan X, Popowicz GM, Smialowski P, Nigg EA, Holak TA. Structure of the N-terminal domain of the FOP (FGFR1OP) protein and implications for its dimerization and centrosomal localization. J Mol Biol 2006; 359: 863-875. (Pubitemid 43831933)
30. Gillingham AK, Munro S. The PACT domain, a conserved centrosomal targeting motif in the coiled-coil proteins AKAP450 and pericentrin. EMBO Rep 2000; 1: 524-529.
31. Graser S, Stierhof YD, Lavoie SB, Gassner OS, Lamla S, Le Clech M et al. Cep164, a novel centriole appendage protein required for primary cilium formation. J Cell Biol 2007; 179: 321-330. (Pubitemid 350004895)
32. Delgehyr N, Sillibourne J, Bornens M. Microtubule nucleation and anchoring at the centrosome are independent processes linked by ninein function. J Cell Sci 2005; 118 (Pt 8): 1565-1575. (Pubitemid 40691885)
33. Schwaller J, Anastasiadou E, Cain D, Kutok J, Wojiski S, Williams IR et al. H4(D10S170), a gene frequently rearranged in papillary thyroid carcinoma, is fused to the platelet-derived growth factor receptor beta gene in atypical chronic myeloid leukemia with t(5;10)(q33;q22). Blood 2001; 97: 3910-3918.
34. Baron U, Freundlieb S, Gossen M, Bujard H. Co-regulation of two gene activities by tetracycline via a bidirectional promoter. Nucleic Acids Res 1995; 23: 3605-3606.
35. Pfeifer AC, Kaschek D, Bachmann J, Klingmuller U, Timmer J. Model-based extension of high-throughput to high-content data. BMC Syst Biol 2010; 4: 106.
36. Chen CH, Howng SL, Cheng TS, Chou MH, Huang CY, Hong YR. Molecular characterization of human ninein protein: two distinct subdomains required for centrosomal targeting and regulating signals in cell cycle. Biochem Biophys Res Commun 2003; 308: 975-983. (Pubitemid 36976554)
37. Bond J, Roberts E, Springell K, Lizarraga SB, Scott S, Higgins J et al. A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size. Nat Genet 2005; 37: 353-355.
38. Fong KW, Choi YK, Rattner JB, Qi RZ. CDK5RAP2 is a pericentriolar protein that functions in centrosomal attachment of the gamma-tubulin ring complex. Mol Biol Cell 2008; 19: 115-125. (Pubitemid 351186138)
39. Stover EH, Chen J, Folens C, Lee BH, Mentens N, Marynen P et al. Activation of FIP1L1-PDGFRalpha requires disruption of the juxtamembrane domain of PDGFRalpha and is FIP1L1-independent. Proc Natl Acad Sci USA 2006; 103: 8078-8083. (Pubitemid 43801055)
40. Carroll M, Tomasson MH, Barker GF, Golub TR, Gilliland DG. The TEL/platelet-derived growth factor beta receptor (PDGF beta R) fusion in chronic myelomonocytic leukemia is a transforming protein that self-associates and activates PDGF beta R kinase-dependent signaling pathways. Proc Natl Acad Sci USA 1996; 93: 14845-14850.
41. Giehl M, Fabarius A, Frank O, Erben P, Zheng C, Hafner M et al. Expression of the p210BCR-ABL oncoprotein drives centrosomal hypertrophy and clonal evolution in human U937 cells. Leukemia 2007; 21: 1971-1976. (Pubitemid 47299972)
42. Fabarius A, Giehl M, Frank O, Spiess B, Zheng C, Muller MC et al. Centrosome aberrations after nilotinib and imatinib treatment in vitro are associated with mitotic spindle defects and genetic instability. Br J Haematol 2007; 138: 369-373. (Pubitemid 47035400)
43. Fabarius A, Giehl M, Rebacz B, Kramer A, Frank O, Haferlach C et al. Centrosome aberrations and G1 phase arrest after in vitro and in vivo treatment with the SRC/ABL inhibitor dasatinib. Haematologica 2008; 93: 1145-1154.
44. He Y, Wertheim JA, Xu L, Miller JP, Karnell FG, Choi JK et al. The coiled-coil domain and Tyr177 of bcr are required to induce a murine chronic myelogenous leukemia-like disease by bcr/abl. Blood 2002; 99: 2957-2968. (Pubitemid 34525386)
45. Bischof D, Pulford K, Mason DY, Morris SW. Role of the nucleophosmin (NPM) portion of the non-Hodgkin's lymphoma-associated NPM-anaplastic lymphoma kinase fusion protein in oncogenesis. Mol Cell Biol 1997; 17: 2312-2325. (Pubitemid 27133318)
46. Xiao S, McCarthy JG, Aster JC, Fletcher JA. ZNF198-FGFR1 transforming activity depends on a novel proline-rich ZNF198 oligomerization domain. Blood 2000; 96: 699-704. (Pubitemid 30463394)
47. Jackson CC, Medeiros LJ, Miranda RN. 8p11 myeloproliferative syndrome: a review. Hum Pathol 2010; 41: 461-476.
48. Kasyapa C, Gu TL, Nagarajan L, Polakiewicz R, Cowell JK. Phosphorylation of the SSBP2 and ABL proteins by the ZNF198-FGFR1 fusion kinase seen in atypical myeloproliferative disorders as revealed by phosphopeptide-specific MS. Proteomics 2009; 9: 3979-3988.