TLS/FUS, a pro-oncogene involved in multiple chromosomal translocations, is a novel regulator of BCR/ABL-mediated leukemogenesis

EMBO Journal

Volumn 17, Issue 15, 1998, Pages 4442-4455

  Perrotti, Danilo ^a   Bonatti, Silvia ^c   Trotta, Rossana ^a   Martinez, Robert ^a   Skorski, Tomasz ^a   Salomoni, Paolo ^a   Grassilli, Emanuela ^a   Iozzo, Renato V ^a   Cooper, Denise R ^b   Calabretta, Bruno ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c NONE

Author keywords

ABL; BCR; FUS; Leukemogenesis; TLS; Zinc finger protein

Indexed keywords

BCR ABL PROTEIN; CYTOKINE RECEPTOR; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 3 RECEPTOR; ONCOPROTEIN; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; LEUKEMOGENESIS; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; CELL DIFFERENTIATION; CELL DIVISION; DNA-BINDING PROTEINS; FUSION PROTEINS, BCR-ABL; GENE EXPRESSION REGULATION, NEOPLASTIC; GROWTH SUBSTANCES; HEMATOPOIETIC STEM CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; LEUKEMIA, MYELOID; MICE; MICE, INBRED ICR; MICE, SCID; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENES; RIBONUCLEOPROTEINS; RNA-BINDING PROTEIN FUS; SIGNAL TRANSDUCTION; TRANSLOCATION, GENETIC; TUMOR CELLS, CULTURED;

ANIMALIA;

EID: 0032479980     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.15.4442     Document Type: Article

References (61)

1. Aman, P. et al. (1996) Expression patterns of the human sarcoma-associated genes FUS and EWS and the genomic structure of FUS. Genomics, 37, 1-8.
2. Askew, D.S., Ashmun, R.A., Simmons, B.C. and Cleveland, J.L. (1991) Constitutive c-myc expression in an IL-3-dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene, 6, 1915-1922.
3. Bellon, T., Perrotti, D. and Calabretta, B. (1997) Granulocytic differentiation of normal hematopoietic precursor cells induced by transcription factor PU.1 correlates with negative regulation of the c-myb promoter. Blood, 90, 1828-1839.
4. Bertolotti, A., Lutz, Y., Heard, D.J., Chambon, P. and Tora, L. (1996) hTAF (II)68, a novel RNA/ssDNA-binding protein with homology to the pro-oncoproteins FUS and EWS is associated with both TFIID and RNA polymerase II. EMBO J., 15, 5022-5031.
5. Calvio, C., Neubauer, G., Mann, M. and Lamond, A.I. (1995) Identification of hnRNP P2 as FUS using electrospray mass spectrometry. RNA, 1, 724-733.
6. Chalfant, C.E., Ohno, S., Konno, Y., Fisher, A.R., Bisnant, L.D., Watson, J.E. and Cooper, D.R. (1996) A carboxy-terminal deletion mutant of protein kinase CβII inhibits insulin-stimulated 2-deoxyglucose uptake in L6 rat skeletal muscle cells. Mol. Endocrinol. 10, 1273-1281.
7. Chen, P., Xie, H. and Wells, A. (1996) Mitogenic signaling from the EGF receptor is attenuated by a phospholipase C-γ/protein kinase C feedback mechanism. Mol. Biol. Cell, 7, 871-881.
8. Cortez, D., Kadlec, L. and Pendergast, A.M. (1995) Structural and signaling requirements for BCR/ABL-mediated transformation and inhibition of apoptosis. Mol. Cell. Biol., 15, 5531-5541.
9. Courey, A.J. and Tjian, R. (1988) Analysis of Sp1 in vivo reveals multiple transcriptional domains, including a novel glutamine-rich activation motif. Cell, 55, 887-898.
10. Crozat, A., Aman, P., Mandahl, N. and Ron, D. (1993) Fusion of CHOP to a novel RNA-binding protein in human myxoid liposarcoma. Nature, 363, 640-644.
11. BCR/ABL gene of the Philadelphia chromosome. Science, 247, 824-830.
12. Dekker, L.V. and Parker, P.J. (1994) Protein kinase C: a question of specificity. Trends Biol. Sci., 19, 73-77.
13. Downward, J. (1994) Signal transduction. Regulating S6 kinase. Nature, 371, 378-379.
14. Dudley, D.T., Pang, L., Decker, S.J., Bridges, A.J. and Saltiel, A. (1995) A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl Acad. Sci. USA, 92, 7686-7689.
15. Evans, C.A., Lord, J.M., Owen-Lynch, P.J., Johnson, G., Dive, C. and Whetton, A.D. (1995) Suppression of apoptosis by v-ABL protein tyrosine kinase is associated with nuclear translocation and activation of protein kinase C in an interleukin-3-dependent haemopoietic cell line. J. Cell Sci., 108, 2591-2598.
16. Friedman, A.D. (1996) GADD153/CHOP, a DNA damage-inducible protein, reduced CAAT/enhancer binding protein activities and increased apoptosis in 32D c13 myeloid cells. Cancer Res., 56, 3250-3256.
17. Fukunaga, R., Ishizaka-Ikeda, E., Seto, Y. and Nagata, S. (1990) Expression cloning of a receptor for murine granulocyte colony-stimulating factor. Cell, 61, 341-350.
18. Fung, P.A., Labrecque, R. and Pederson, T. (1997) RNA-dependent phosphorylation of a nuclear RNA binding protein. Proc. Natl Acad. Sci. USA, 94, 1064-1068.
19. Goga, A., McLaughlin, J., Afar, D.E.H., Saffran, D.C. and Witte, O.N. (1995) Alternative signals to RAS for hematopoietic transformation by the BCR/ABL oncogene. Cell, 82, 981-988.
20. Göriach, M., Burd, C.G. and Dreyfuss, G. (1994) The determinants of RNA-binding specificity of the heterogeneous nuclear ribonucleoprotein C proteins. J. Biol. Chem., 269, 23074-23078.
21. +ALL involve GTPase-activating protein, phospholipase C-γ1 and phosphatidylinositol 3′-kinase. Leukemia, 8, 115-120.
22. Hackl, W. and Luhrmann, R. (1996) Molecular cloning and subcellular localisation of the snRNP-associated protein 69KD, a structural homologue of the proto-oncoproteins TLS and EWS with RNA and DNA-binding properties. J. Mol. Biol., 264, 843-851.
23. Heisterkamp, N., Jenster, G., ten Hoeve, J., Zovich, D., Pattengale, P.K.X. and Groffen, J. (1990) Acute leukaemia in bcr/abl transgenic mice. Nature, 344, 251-253.
24. Immanuel, D., Zinszner, H. and Ron, D. (1995) Association of SARFH (sarcoma-associated RNA-binding fly homologue) with regions of chromatin transcribed by RNA polymerase II. Mol. Cell. Biol., 15, 4562-4571.
25. Kadonaga, J.T. and Tjian, R. (1986) Affinity purification of sequence-specific DNA binding proteins. Proc. Natl Acad. Sci. USA, 83, 5889-5893.
26. Karin, M. and Hunter, T. (1995) Transcriptional control by protein phosphorylation: signal transmission from the cell surface to the nucleus. Curr. Biol., 5, 747-757.
27. Kato, J.Y. and Sherr, C.J. (1993) Inhibition of granulocyte differentiation by G1 cyclins D2 and D3 but not D1. Proc. Natl Acad. Sci. USA, 90, 11513-11517.
28. Ladanyi, M. (1995) The emerging molecular genetics of sarcoma translocations. Diagn. Mol. Pathol. 4, 162-173.
29. Lugo, T.G., Pendergast, A.M., Muller, A.J. and Witte, O.N. (1990) Tyrosine kinase activity and transformation potency of bcr-abl oncogene products. Science, 247, 1079-1082.
30. Matulonis, U., Salgia, R., Okuda, K., Druker, B. and Griffin, J.D. (1993) Interleukin-3 and p210 BCR/ABL activate both unique and overlapping pathways of signal transduction in a factor-dependent myeloid cell line. Exp. Hematol., 21, 1460-1466.
31. Maxon, M.E. and Tjian, R. (1994) Transcriptional activity of transcription factor IIE is dependent on zinc binding. Proc. Natl Acad. Sci. USA, 91, 9529-9533.
32. Mayrand, S.H., Dwen, P. and Pederson, T. (1993) Serine/threonine phosphorylation regulates binding of C hnRNP proteins to pre-mRNA. Proc. Natl Acad. Sci. USA, 90, 7764-7768.
33. McLaughlin, J., Chianese, E. and Witte, O.N. (1987) In vitro transformation of immature hematopoietic cells by the P210 BCR/ABL oncogene product of the Philadelphia chromosome. Proc. Natl Acad Sci USA 84, 6558-6562.
34. Morohoshi, F., Arai, K., Takahashi, E.I., Tanigami, A. and Ohki, M. (1996) Cloning and mapping of a human RBP56 gene encoding a putative RNA binding protein similar to FUS/TLS and EWS proteins. Genomics, 38, 51-57.
35. Morishita, K., Parganas, E., Matsugi, T. and Ihle, J.N. (1992) Expression of the Evi-1 zinc finger gene in 32Dc13 myeloid cells blocks granulocytic differentiation in response to granulocyte colony-stimulating factor. Mol. Cell. Biol., 12, 183-189.
36. Morris, J.F., Hromas, R. and Rausher, T.J., III (1994) Characterization of the DNA-binding properties of the myeloid zinc finger protein MZF1: two independent DNA-binding domains recognize two DNA consensus sequences with a common G-rich core. Mol. Cell. Biol., 11, 6166-6176.
37. Panagopoulos, I., Mandahl, N., Mitelman, F. and Aman, P. (1995) Two distinct FUS breakpoint clusters in myxoid liposarcoma and acute myeloid leukemia with the translocations t (12;16) and t (16; 21). Oncogene, 11, 1133-1137.
38. Pear, W.S., Nolan, G.P., Scott, M.L. and Baltimore, D. (1993) Production of high-liter helper free retroviruses by transient transfection. Proc. Natl Acad. Sci. USA, 90, 8392-8396.
39. Perrotti, D., Melotti, P., Skorski, T., Casella, I., Peschle, C. and Calabretta, B. (1995) Overexpression of the zinc finger protein MZF1 inhibits hematopoietic development from embryonic stem cells: correlation with negative regulation of CD34 and c-myb promoter activity. Mol. Cell. Biol., 15, 6075-6087.
40. Perrotti, D., Bellon, T., Trotta, R., Martinez, R. and Calabretta, B. (1996) A cell proliferation-dependent multiprotein complex NC-3A positively regulates the CD34 promoter via a TCATTT-containing element. Blood, 88, 3336-3348.
41. Pinol-Roma, S. and Dreyfuss, G. (1993) Cell cycle-regulated phosphorylation of the pre-mRNA-binding (heterogeneous nuclear ribonucleoprotein) C proteins. Mol. Cell. Biol., 13, 5762-5770.
42. Powis, G. et al. (1994) Wortmannin, a patent and specific inhibitor of phosphatidylinositol-2-kinase. Cancer Res., 54, 2419-2423.
43. Prasad, D.D., Ouchida, M., Lee, L., Rao, V.N. and Reddy, E.S. (1994) FUS fusion domain of FUS-erg chimeric protein resulting from the t (16;21) chromosomal translocation in human myeloid leukemia functions as a transcriptional activation domain. Oncogene, 9, 3717-3729.
44. Rabbitts, T.H., Forster, A., Larson, R. and Nathan, P. (1993) Fusion of the dominant negative transcription regulator CHOP with a novel gene FUS by translocation t (12:16) in malignant liposarcoma. Nature Genet., 4, 175-180.
45. Raitano, A.B., Halpern, J.R., Hambuch, T.M. and Sawyers, C.L. (1995) The Bcr-Abl leukemia oncogene activates Jun kinase and requires Jun for transformation. Proc. Natl Acad. Sci. USA, 92, 11746-11750.
46. Ron, D. (1997) TLS-CHOP and the role of RNA-binding proteins in oncogenic transformation. Curr. Top. Microbiol. Immunol., 220, 131-142.
47. Sawyers, C.L., Callahan, W. and Witte, O.N. (1992) Dominant negative MYC blocks transformation by ABL oncogenes. Cell. 70, 901-910.
48. Sawyers, C.L., McLaughlin, J. and Witte, O.N. (1995) Genetic requirement of Ras in the transformation of fibroblasts and hematopoietic cells by the BCR/ABL oncogene. J. Exp. Med., 181, 307-313.
49. Shimizu, K., Ichikawa, H., Tojo, A., Kaneko, Y., Maseki, N., Hayashi, Y., Ohira, M., Asano, S. and Ohki, M. (1993) An ets-related gene, ERG, is rearranged in human myeloid leukemia with t (16;21) chromosomal translocation. Proc. Natl Acad. Sci. USA, 90, 10280-10284.
50. Skorski, T., Nieborowska-Skorska, M., Szczylik, C., Kanakaraj, P., Perrotti, D., Zon, G., Gewirtz, A., Perussia, B. and Calabretta, B. (1995) C-RAF-1 serine/threonine kinase is required in BCR/ABL-dependent and normal hematopoiesis. Cancer Res., 55, 2275-2278.
51. Skorski, T. et al. (1997) Transformation of hematopoietic cells by bcr/ abl requires activation of a PI-3k/Akt-dependent pathway. EMBO J., 16, 6151-6161.
52. Steinman, R.A. and Tweardy, D.J. (1994) Granulocyte colony-stimulating factor receptor mRNA upregulation is an immediate early marker of myeloid differentiation and exhibits dysfunctional regulation in leukemic cells. Blood, 83, 119-127.
53. Tamaoki, T. (1991) Use and specificity of staurosporine, UCN-01 and calphostin C as protein kinase inhibitors. Methods Enzymol., 201, 340-347.
54. Teale, B., Singh, S., Khanna, K.K., Findik, D. and Lavin, M.F. (1992) Purification and characterization of a DNA-binding protein activated by ionizing radiation. J. Biol. Chem., 267, 10295-10301
55. Tenen, D.G., Hromas, R., Licht, J.D. and Zhang, D.E. (1997) Transcription factors, normal and myeloid development and leukemia. Blood, 90, 489-519.
56. Tkatch, L.S., Rubin, K.A., Ziegler, S.F. and Tweardy, D.J. (1995) Modulation of human G-CSF receptor mRNA and protein in normal and leukemic myeloid cells by G-CSF and retinoic acid. J. Leuk. Biol., 57, 964-971.
57. Waterhouse, N. et al. (1996) Heteronuclear ribonucleoproteins c1 and c2, components of the spliceosome, are specific targets of interleukin 1-beta-converting enzyme-like proteases in apoptosis. J. Biol. Chem., 271, 29335-29341.
58. Yi, H., Fujimura, Y., Ouchida, M., Prasad, D.D., Rao, V.N. and Reddy, E.S. (1997) Inhibition of apoptosis by normal and aberrant Fli-1 and ERG proteins involved in human solid tumors and leukemias. Oncogene, 14, 1259-1268.
59. Zinszner, H., Albalat, R. and Ron, D. (1994) A novel effector domain from the RNA-binding protein TLS or EWS is required for oncogenic transformation by CHOP. Genes Dev., 8, 2513-2526.
60. Zinszner, H., Immanuel, D., Yin, Y., Liang, F.X. and Ron, D. (1997a) A topogenic role for the oncogenic N-terminus of TLS: nucleolar localization when transcription is inhibited. Oncogene, 14, 451-461.
61. Zinszner, H., Sok, J., Immanuel, D., Yin, Y. and Ron, D. (1997b) TLS (FUS) binds RNA in vivo and engages in nucleo-cytoplasmic shuttling. J. Cell Sci., 110, 1741-1750.