Stable interference of EWS-FLI1 in an Ewing sarcoma cell line impairs IGF-1/IGF-1R signalling and reveals TOPK as a new target

British Journal of Cancer

Volumn 101, Issue 1, 2009, Pages 80-90

  Herrero Martin D ^a,h   Osuna, D ^a   Ordoez J L ^a   Sevillano, V ^a   Martins, A S ^a   Mackintosh, C ^a   Campos, M ^a   Madoz Grpide, J ^a,e   Otero Motta, A P ^a   Caballero, G ^a   Amaral, A T ^a   Wai, D H ^b   Braun, Y ^c   Eisenacher, M ^d,f   Schaefer, K L ^c   Poremba, C ^c,g   De Alava, E ^a  

^a Centro de Investigacion del Cancer   (Spain)

^b CHILDREN S HOSPITAL LOS ANGELES   (United States)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d UNIVERSITY OF MÜNSTER   (Germany)

^e UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^f RUHR UNIVERSITY BOCHUM   (Germany)

^g Institute of Pathology   (Germany)

^h Hospital UniversitarioFundación Jiménez Díaz   (Spain)

Author keywords

Ewing sarcoma; EWS FLII; IGF I IGF IR; Stable shRNAi model; TOPK

Indexed keywords

OLIGONUCLEOTIDE; PROTEIN KINASE; RNA BINDING PROTEIN EWS; SMALL INTERFERING RNA; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; T LYMPHOKINE ACTIVATED KILLER CELL ORIGINATED PROTEIN KINASE; TRANSCRIPTION FACTOR FLI 1; UNCLASSIFIED DRUG; EWS FLI FUSION PROTEIN; EWS-FLI FUSION PROTEIN; ONCOPROTEIN; PDZ BINDING KINASE; PDZ-BINDING KINASE; PROTEIN SERINE THREONINE KINASE; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; EWING SARCOMA; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; TUMOR GROWTH; ANIMAL; BIOSYNTHESIS; CELL MOTION; DRUG ANTAGONISM; ENZYMOLOGY; GENETICS; METABOLISM; MOUSE MUTANT; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL MOVEMENT; DOWN-REGULATION; FEMALE; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MICE; MICE, INBRED NOD; MICE, SCID; ONCOGENE PROTEINS, FUSION; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR, IGF TYPE 1; RNA INTERFERENCE; SARCOMA, EWING'S; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 67649862045     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6605104     Document Type: Article

References (43)

1. Abe Y, Matsumoto S, Kito K, Ueda N (2000) Cloning and expression of a novel MAPKK-like protein kinase, lymphokine-activated killer T-cell- originated protein kinase, specifically expressed in the testis and activated lymphoid cells. J Biol Chem 275: 21525-21531
2. Abe Y, Takeuchi T, Kagawa-Miki L, Ueda N, Shigemoto K, Yasukawa M, Kito K (2007) A mitotic kinase TOPK enhances Cdkl/cyclin Bl-dependent phosphorylation of PRC1 and promotes cytokinesis. J Mol Biol 370: 231-245
3. Amsellem V, Kryszke MH, Hervy M, Subra F, Amman R, Leh H, Brachet-Ducos C, Auclair C (2005) The actin cytoskeleton-associated protein zyxin acts as a tumour suppressor in Ewing tumour cells. Exp Cell Res 304: 443-456
4. Ayllon V, O'Connor R (2007) PBK/TOPK promotes tumour cell proliferation through p38 MAPK activity and regulation of the DNA damage response. Oncogene 26: 3451-3461
5. Benini S, Perbal B, Zambelli D, Colombo MP, Manara MC, Serra M, Parenza M, Martinez V, Picci P, Scotlandi K (2005) In Ewing's sarcoma CCN3(NOV) inhibits proliferation while promoting migration and invasion of the same cell type. Oncogene 24: 4349-4361
6. Brummelkamp TR, Bernards R, Agami R (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science 296: 550-553
7. Carrillo J, Garcia-Aragoncillo E, Azorin D, Agra N, Sastre A, Gonzalez- Mediero I, Garcia-Miguel P, Pestana A, Gallego S, Segura D, Alonso J (2007) Cholecystokinin down-regulation by RNA interference impairs Ewing tumour growth. Clin Cancer Res 13: 2429-2440
8. Dauphinot L, De Oliveira C, Melot T, Sevenet N, Thomas V, Weissman BE, Delattre O (2001) Analysis of the expression of cell cycle regulators in Ewing cell lines: EWS-FLI-1 modulates p57KIP2and c-Myc expression. Oncogene 20:3258-3265
9. Delattre O, Zucman J, Plougastel B, Desmaze C, Melot T, Peter M, Kovar H, Joubert I, de Jong P, Rouleau G, Aurias A, Thomas G (1992) Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours. Nature 359:162 - 165
10. Deneen B, Denny CT (2001) Loss of p16 pathways stabilizes EWS/FLI1 expression and complements EWS/FLI1 mediated transformation. Oncogene 20:6731 - 6741
11. Dougherty JD, Garcia AD, Nakano I, Livingstone M, Norris B, Polakiewicz R, Wexler EM, Sofroniew MV, Kornblum HI, Geschwind DH (2005) PBK/TOPK, a proliferating neural progenitor-specific mitogen-activated protein kinase kinase. J Neurosci 25:10773 - 10785
12. Gangwal K, Lessnick SL (2008) Microsatellites are EWS/FLI response elements: genomic 'junk' is EWS/FLI's treasure. Cell Cycle 7: 3127-3132
13. Garcia-Echeverria C, Pearson MA, Marti A, Meyer T, Mestan J, Zimmermann J, Gao J, Brueggen J, Capraro HG, Cozens R, Evans DB, Fabbro D,Furet P, Porta DG, Liebetanz J, Martiny-Baron G, Ruetz S, Hofmann F (2004) In vivo antitumour activity of NVP-AEW541-A novel, potent, and selective inhibitor of the IGF-IR kinase. Cancer Cell 5:231 - 239
14. Guan H, Zhou Z, Wang H, Jia SF, Liu W, Kleinerman ES (2005) A small interfering RNA targeting vascular endothelial growth factor inhibits Ewing's sarcoma growth in a xenograft mouse model. Clin Cancer Res 11: 2662-2669
15. Kinsey M, Smith R, Lessnick SL (2006) NR0B1 is required for the oncogenic phenotype mediated by EWS/FLI in Ewing's sarcoma. Mol Cancer Res 4: 851 - 859
16. Kovar H (2005) Context matters: the hen or egg problem in Ewing's sarcoma. Semin Cancer Biol 15: 189-196
17. 53owth arrest in primary human fibroblasts. Cancer Cell 1: 393-401
18. Martins AS, Mackintosh C, Martin DH, Campos M, Hernandez T, Ordonez JL, de Alava E (2006) Insulin-like growth factor I receptor pathway inhibition by ADW742, alone or in combination with imatinib, doxorubicin, or vincristine, is a novel therapeutic approach in Ewing tumour. Clin Cancer Res 12: 3532-3540
19. Martins AS, Ordonez JL, Garcia-Sanchez A, Herrero D, Sevillano V, Osuna D, Mackintosh C, Caballero G, Otero AP, Poremba C, Madoz-Gurpide J, de Alava E (2008) A pivotal role for heat shock protein 90 in Ewing sarcoma resistance to anti-insulin-like growth factor 1 receptor treatment: in vitro and in vivo study. Cancer Res 68:6260-6270
20. Matsunobu T, Tanaka K, Nakamura T, Nakatani F, Sakimura R, Hanada M, Li X, Okada T, Oda Y, Tsuneyoshi M, Iwamoto Y (2006) The possible role of EWS-Fli1 in evasion of senescence in Ewing family tumours. Cancer Res 66:803 - 811
21. May WA, Arvand A, Thompson AD, Braun BS, Wright M, Denny CT (1997) EWS/FLI1-induced manic fringe renders NIH 3T3 cells tumourigenic. Nat Genet 17: 495-497
22. Mendiola M, Carrillo J, Garcia E, Lalli E, Hernandez T, de Alava E, Tirode F, Delattre O, Garcia-Miguel P, Lopez-Barea F, Pestana A, Alonso J (2006) The orphan nuclear receptor DAX1 is up-regulated by the EWS/FLI1 oncoprotein and is highly expressed in Ewing tumours. Int J Cancer 118:1381-1389
23. Nandi A, Tidwell M, Karp J, Rapoport AP (2004) Protein expression of PDZ-binding kinase is up-regulated in hematologic malignancies and strongly down-regulated during terminal differentiation of HL-60 leukemic cells. Blood Cells Mol Dis 32:240-245
24. Nandi AK, Rapoport AP (2006) Expression of PDZ-binding kinase (PBK) is regulated by cell cycle-specific transcription factors E2F and CREB/ATF. Leuk Res 30:437-447
25. Oh SM, Zhu F, Cho YY, Lee KW, Kang BS, Kim HG, Zykova T, Bode AM, Dong Z (2007) T-lymphokine-activated killer cell-originated protein kinase functions as a positive regulator of c-Jun-NH2-kinase 1 signaling and H-Ras-induced cell transformation. Cancer Res 67:5186- 5194
26. Owen LA, Lessnick SL (2006) Identification of target genes in their native cellular context: an analysis of EWS/FLI in Ewing's sarcoma. Cell Cycle 5: 2049-2053
27. Park JH, Lin ML, Nishidate T, Nakamura Y, Katagiri T (2006) PDZ-binding kinase/T-LAK cell-originated protein kinase, a putative cancer/testis antigen with an oncogenic activity in breast cancer. Cancer Res 66: 9186-9195
28. Prieur A, Tirode F, Cohen P, Delattre O (2004) EWS/FLI-1 silencing and gene profiling of Ewing cells reveal downstream oncogenic pathways and a crucial role for repression of insulin-like growth factor binding protein 3. Mol Cell Biol 24:7275-7283
29. Scotlandi K, Benini S, Nanni P, Lollini PL, Nicoletti G, Landuzzi L, Serra M, Manara MC, Picci P, Baldini N (1998) Blockage of insulin-like growth factor-I receptor inhibits the growth of Ewing's sarcoma in athymic mice. Cancer Res 58:4127-4131
30. Scotlandi K, Benini S, Sarti M, Serra M, Lollini PL, Maurici D, Picci P, Manara MC, Baldini N (1996) Insulin-like growth factor I receptor- diated circuit in Ewing's sarcoma/peripheral neuroectodermal tumour: a possible therapeutic target. Cancer Res 56:4570- 4574
31. Sekyi-Otu A, Bell RS, Ohashi C, Pollak M, Andrulis IL (1995) Insulin-like growth factor 1 (IGF-1) receptors, IGF-1, and IGF-2 are expressed in primary human sarcomas. Cancer Res 55:129 - 134
32. Sharp PA (1999) RNAi and double-strand RNA. Genes Dev 13:139-141
33. Siligan C, Ban J, Bachmaier R, Spahn L, Kreppel M, Schaefer KL, Poremba C, Aryee DN, Kovar H (2005) EWS-FLI1 target genes recovered from Ewing's sarcoma chromatin. Oncogene 24:2512 - 2524
34. Simons-Evelyn M, Bailey-Dell K, Toretsky JA, Ross DD, Fenton R, Kalvakolanu D, Rapoport AP (2001) PBK/TOPK is a novel mitotic kinase which is upregulated in Burkitt's lymphoma and other highly proliferative malignant cells. Blood Cells Mol Dis 27:825 - 829
35. Smith R, Owen LA, Trem DJ, Wong JS, Whangbo JS, Golub TR, Lessnick SL (2006) Expression profiling of EWS/FLI identifies NKX2.2 as a critical target gene in Ewing's sarcoma. Cancer Cell 9:405 - 416
36. Sorensen PH, Lessnick SL, Lopez-Terrada D, Liu XF, Triche TJ, Denny CT (1994) A second Ewing's sarcoma translocation, t(21;22), fuses the EWS gene to another ETS-family transcription factor, ERG. Nat Genet 6:146-151
37. Stegmaier K, Wong JS, Ross KN, Chow KT, Peck D, Wright RD, Lessnick SL, Kung AL, Golub TR (2007) Signature-based small molecule screening identifies cytosine arabinoside as an EWS/FLI modulator in Ewing sarcoma. PLoS Med 4:e122
38. Thompson AD, Teitell MA, Arvand A, Denny CT (1999) Divergent Ewing's sarcoma EWS/ETS fusions confer a common tumourigenic phenotype on NIH3T3 cells. Oncogene 18:5506-5513
39. Tijsterman M, Ketting RF, Plasterk RH (2002) The genetics of RNA silencing. Annu Rev Genet 36:489- 519
40. Zhu F, Zykova TA, Kang BS, Wang Z, Ebeling MC, Abe Y, Ma WY, Bode AM, Dong Z (2007) Bidirectional signals transduced by TOPK-ERK interaction increase tumourigenesis of HCT116 colorectal cancer cells. Gastroenterology 133:219- 231
41. Zupanska A, Adach A, Dziembowska M, Kaminska B (2007) Alternative pathway of transcriptional induction of p21WAF1/Cip1 by cyclosporine A in p53-deficient human glioblastoma cells. Cell Signal 19: 1268-1278
42. Zwerner JP, Guimbellot J, May WA (2003) EWS/FLI function varies in different cellular backgrounds. Exp Cell Res 290:414 - 419
43. Zykova TA, Zhu F, Lu C, Higgins L, Tatsumi Y, Abe Y, Bode AM, Dong Z (2006) Lymphokine-activated killer T-cell-originated protein kinase phosphorylation of histone H2AX prevents arsenite-induced apoptosis in RPMI7951 melanoma cells. Clin Cancer Res 12:6884- 6893