LMO T-cell translocation oncogenes typify genes activated by chromosomal translocations that alter transcription and developmental processes

Genes and Development

Volumn 12, Issue 17, 1998, Pages 2651-2657

  Rabbitts, Terence H ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BURKITT LYMPHOMA; CANCER GROWTH; CHROMOSOME TRANSLOCATION 14; CHROMOSOME TRANSLOCATION 8; GENETIC LINKAGE; GROWTH REGULATION; HEMATOPOIESIS; HUMAN; LEUKEMOGENESIS; LYMPHOCYTE PROLIFERATION; PRIORITY JOURNAL; PROTO ONCOGENE; REVIEW; T CELL LEUKEMIA; TRANSCRIPTION REGULATION;

EID: 0032168564     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.17.2651     Document Type: Review

References (65)

1. Adams, J.M. and S. Cory. 1991. Transgenic models of tumor development. Science 254: 1161-1167.
2. Agulnick, A.D., M. Taira, J.J. Breen, T. Tanaka, I.B. Dawid, and H. Westphal. 1996. Functional and physical interaction of Ldb1, a novel LIM domain binding factor, with the LIM homeodomain protein Lhx1/Xlim-1. Nature 384: 270-272.
3. Aplan P.D., C.A. Jones, D.S. Chervinsky, X.F. Zhao, M.K. Ellsworth, C. Wu, E.A. McGuire, and K.W. Gross. 1997. An scl gene product lacking the transactivation domain induces bony abnormalities and cooperates with LMO1 to generate T-cell malignancies in transgenic mice. EMBO J. 16: 2408-2419.
4. Bach, I., C. Carriere, H.P. Ostendorff, B. Andersen, and M.G. Rosenfeld. 1997. A family of LIM domain-associated cofactors confer transcriptional synergism between LIM and Otx homeodomain proteins. Genes & Dev. 11: 1370-1380.
5. Bain, G., I. Engel, E.C.R. Maandag, H.P.J. Te Riele, J.R. Voland, L.L. Shart, J. Chun, B. Huey, D. Pinkel, and C. Murre. 1997. E2A deficiency leads to abnormalities in αβ T-cell development and to rapid development of T-cell lymphomas. Mol. Cell. Biol. 17: 4782-4791.
6. Begley, C.G., P.D. Aplan, M.P. Davey, K. Nakahara, K. Tchorz, J. Kurtzberg, M.S. Hershfield, B.F. Haynes, D.I. Cohen, T.A. Waldmann, and I.R. Kirsch. 1989a. Chromosomal translocation in a human leukemic stem-cell line disrupts the T-cell antigen receptor δ-chain diversity region and results in a previously unreported fusion transcript. Proc. Natl. Acad. Sci. 86: 2031-2035.
7. Begley, C.G., P.D. Aplan, S.M. Denning, B.F. Haynes, T.A. Waldmann, and I.R. Kirsch. 1989b. The gene SCL is expressed during early hematopoiesis and encodes a differentiation-related DNA-binding motif. Proc. Natl. Acad. Sci. 86: 10128-10132.
8. Bernard, O., P. Guglielmi, P. Jonveaux, D. Cherif, S. Gisselbrecht, M. Mauchauffe, R. Berger, C.-J. Larson, and D. Mathieu-Mahul. 1989. Two distinct mechanisms for the SCL gene activation in the t(1;14) translocation of T-cell leukemias. Genes Chromosomes Cancer 1: 194-210.
9. Boehm, T., R. Baer, I. Lavenir, A. Forster, J.J. Waters, E. Nacheva, and T.H. Rabbitts. 1988. The mechanism of chromosomal translocation t(11;14) involving the T-cell receptor Cδ locus on human chromosome 14q11 and a transcribed region of chromosome 11p15. EMBO J. 7: 385-394.
10. Boehm, T., L. Foroni, Y. Kaneko, M.P. Perutz, and T.H. Rabbitts. 1991. The rhombotin family of cysteine-rich LIM-domain oncogenes: Distinct members are involved in T-cell translocations to human chromosomes 11p15 and 11p13. Proc. Natl. Acad. Sci. 88: 4367-4371.
11. Boehm, T., L. Foroni, M. Kennedy, and T.H. Rabbitts. 1990a. The rhombotin gene belongs to a class of trancriptional regulators with a potential novel protein dimerisation motif. Oncogene 5: 1103-1105.
12. Boehm, T., J.M. Greenberg, L. Buluwela, I. Lavenir, A. Forster, and T.H. Rabbitts. 1990b. An unusual structure of a putative T cell oncogene which allows production of similar proteins from distinct mRNAs. EMBO J. 9: 857-868.
13. Chen, Q., J.-T. Cheng, L.-H. Tsai, N. Schneider, G. Buchanan, A. Carroll, W. Crist, B. Ozanne, M.J. Siciliano, and R. Baer. 1990a. The tal gene undergoes chromosome translocation in T cell leukemia and potentially encodes a helix-loop-helix protein. EMBO J. 9: 415-424.
14. Chen, Q., C.Y.-C. Yang, J. Tsan, Y. Xia, A.H. Ragab, S.C. Peiper, A. Carroll, and R. Baer. 1990b. Coding sequences of the tal-1 gene are disrupted by the chromosome translocation in human T cell leukemia. J. Exp. Med. 172: 1403-1408.
15. Cleary, M.L. 1991. Oncogenic conversion of transcription factors by chromosomal translocations. Cell 66: 619-622.
16. Corral, J., I. Lavenir. H. Impey, A.J. Warren, A. Forster, T.A. Larson, S. Bell, A.N.J. McKenzie, G. King, and T.H. Rabbitts. 1996. An Mll-Af9 fusion gene made by homologous recombination causes acute leukemia in chimeric mice: A method to create fusion oncogenes. Cell 85: 853-861.
17. Croce., C.M., M. Shander, J. Martinis, L. Cicurel, G.G. D'Ancona, T.W. Dolby, and H. Koprowski. 1979. Chromosomal location of the genes for human immunoglobulin heavy chains. Proc. Natl. Acad. Sci. 76: 3416-3417.
18. Dube, I.D., S. Kamel-Reid, C.C. Yuan, M. Lu, X. Wu, G. Corpus, S.C. Raimondi, W.M. Crist, A.J. Carroll, J. Minowada, and J.B. Baker. 1991. A novel human homeobox gene lies at the chromosome 10 breakpoint in lymphoid neoplasias with chromosomal translocation t(10;14). Blood 78: 2996-3003.
19. Finger, L.R., R.C. Harvey, R.C.A. Moore, L.C. Showe, and C.M. Croce. 1986. A common mechanism of chromosomal translocation in T-and B-cell neoplasia. Science 234: 982-984.
20. Finger, L.R., J. Kagan, G. Christopher, J. Kurtzberg, M.S. Hershfield, P.C. Nowell, and C.M. Croce. 1989. Involvement of the TCL5 gene on human chromosome 1 in T-cell leukemia and melanoma. Proc. Natl. Acad. Sci. 86: 5039-5043.
21. Fisch, P., T. Boehm, I. Lavenir. T. Larson, J. Arno, A. Forster, and T.H. Rabbitts. 1992. T-cell acute lymphoblastic lymphoma induced in transgenic mice by the RBTN1 and RBTN2 LIM-domain genes. Oncogene 7: 2389-2397.
22. Foroni, L., T. Boehm, L. White, A. Forster, P. Sherrington, X.B. Liao, C.I. Brannan, N.A. Jenkins, N.G. Copeland, and T.H. Rabbitts. 1992. The rhombotin gene family encode related LIM-domain proteins whose differing expression suggests multiple roles in mouse development. J. Mol. Biol. 226: 747-761.
23. Grutz, G., K. Bucher, I. Lavenir. R. Larson, T. Larson, and T.H. Rabbitts. 1998. The oncogenic LIM-protein Lmo2 forms part of a DNA-binding complex specifically in immature T cells. EMBO J. 17: 4594-4605.
24. Hatano, M., C.W.M. Roberts, M. Minden, W.M. Crist, and S.J. Korsmeyer. 1991. Deregulation of a homeobox gene, HOX11, by the t(10;14) in T cell leukemia. Science 253: 79-82.
25. Hobart, M.J., T.H. Rabbitts. P.N. Goodfellow, E. Solomon, S. Chambers, N. Spurr, and S. Povey. 1981. Immunoglobulin heavy chain genes in humans are located on chromosome 14. Ann. Hum. Genet. 45: 331-335.
26. Hsu, H.-L., J.-T. Cheng, Q. Chen, and R. Baer. 1991. Enhancer-binding activity of the tal-1 oncoprotein in association with the E47/E12 helix-loop-helix proteins. Mol. Cell. Biol. 11: 3037-3042.
27. Hsu, H.-L., L. Huang, J.T. Tsan, W. Funk, W.E. Wright, J.-S. Hu, R.E. Kingston, and R. Baer. 1994. Preferred sequences for DNA recognition by the TAL1 helix-loop-helix proteins. Mol Cell. Biol. 14: 1256-1265.
28. Jurata, L.W., D.A. Kenny, and G.N. Gill. 1996. Nuclear LIM interactor, a rhombotin and LIM homeodomain interacting protein, is expressed early in neuronal development. Proc. Natl. Acad. Sci. 93: 11693-11698.
29. Kennedy, M.A., R. Gonzalez-Sarmiento, U.R. Kees, F. Lampert, N. Dear, T. Boehm, and T.H. Rabbitts. 1991. HOX11, a homeobox-containing T-cell oncogene on human chromosome 10q24. Proc. Natl. Acad. Sci. 88: 8900-8904.
30. Larson, R., P. Fisch, T. Larson, I. Lavenir. T. Langford, G. King, and T.H. Rabbitts. 1994. T cell tumors with disparate phenotypes develop with long latency in mice transgenic for rbtn2. Oncogene 9: 3675-3681.
31. Larson, R.C., H. Osada, T.A. Larson, I. Lavenir, and T.H. Rabbitts. 1995. The oncogenic LIM protein Rhtn2 causes thymic developmental aberrations that precede malignancy in transgenic mice. Oncogene 11: 853-862.
32. Larson, R.C., I. Lavenir. T.A. Larson, R. Baer, A.J. Warren, I. Wadman, K. Nottage, and T.H. Rabbitts. 1996. Protein dimerisation between Lmo2 (Rbtn2) and Tall alters thymocyte development and potentiates T cell tumorigenesis in transgenic mice. EMBO J. 15: 1021-1027.
33. Look, A.T. 1997. Oncogenic transcription factors in the human acute leukemias. Science 278: 1059-1065.
34. Lu, M., Z. Gong, W. Shen, and A.D. Ho. 1991. The tcl-3 proto-oncogene altered by chromosomal translocation in T-cell leukemia codes for a homeobox protein. EMBO J. 10: 2905-2910.
35. Malcolm, S., P. Barton, C. Murphy, M.A. Ferguson-Smith, D.L. Bentley, and T.H. Rabbitts. 1982. Localisation of human immunoglobulin κ light chain variable region genes to the short arm of chromosome 2 by in situ hybridization. Proc. Natl. Acad. Sci. 79: 4957-4961.
36. Manolov, G. and Y. Manolov. 1972. Marker band in one chromosome 14 from Burkitt's lymphoma. Nature 237: 33-34.
37. McGuire, E.A., R.D. Hockett, K.M. Pollock, M.F. Bartholdi, S.J. O'Brien, and S.J. Korsmeyer. 1989. The t(11:14)(p15;q11) in a T-cell acute lymphoblastic leukemia cell line activates multiple transcripts, including Ttg-1, a gene encoding a potential zinc finger protein. Mol. Cel. Biol. 9: 2124-2132.
38. McGuire, E.A., C.E. Rintoul, G.M. Sclar, and S.J. Korsmeyer. 1992. Thymic overexpression of Ttg-1 in transgenic mice results in T-cell acute lymphoblastic leukemia/lymphoma. Mol. Cell. Biol. 12: 4186-4196.
39. Neale, G.A., J.E. Rehg, and R.M. Goorha. 1995. Ectopic expression of rhombotin-2 causes selective expansion of the thymus and T-cell tumors in transgenic mice. Blood 86: 3060-3071.
40. Nowell, P.C. and D.A. Hungerford. 1960. A minute chromosome in human granulocytic leukemia. Science 132: 1497-1500.
41. Osada, H., G. Grutz, H. Axelson, A. Forster, and T.H. Rabbitts. 1995. Association of erythroid transcription factors: Complexes involving the LIM protein RBTN2 and the zinc-finger protein GATA1. Proc. Natl. Acad. Sci. 92: 9585-9589.
42. Perez-Alvarado, G.C., C. Miles, J.W. Michelsen, H.A. Louis, D.R. Winge, M.C. Beckerle, and M.F. Summers. 1994. Structure of the carboxy-terminal LIM domain from the cysteine rich protein CRP. Nature Struct. Biol. 1: 388-398.
43. Pevny, L., M.C. Simon, E. Robertson, W.H. Klein, S.-F. Tsai, V. D'Agati, S.H. Orkin, and F. Costantini. 1991. Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature 349: 257-260.
44. Porcher, C., W. Swat, K. Rockwell, Y. Fujiwara, F.W. Alt, and S.H. Orkin. 1996. The T cell leukemia oncoprotein SC1/tal-1 is essential for development of all hematopoietic lineages. Cell 86: 47-57.
45. Rabbitts. T.H. 1991. Translocations, master genes, and differences between the origins of acute and chronic leukemias. Cell 67: 641-644.
46. _. 1994. Chromosomal translocations in human cancer. Nature 372: 143-149.
47. Robb, L., J.E.J. Rasko, M.L. Bath, A. Strasser, and C.G. Begley. 1995. scl, a gene frequently activated in human T cell leukemia, does not induce lymphomas in transgenic mice. Oncogene 10: 205-209.
48. Robb, L., N.J. Elwood, A.G. Elefanty, F. Kontgen, R. Li, L.D. Barnet, and C.G. Begley. 1996. The scl gene product is required for the generation of all hematopoietic lineages in the adult mouse. EMBO J. 15: 4123-4129.
49. Rowley, J.D. 1973. A new consistent chromosomal abnormality in chronic myelogeneous leukemia identified by quinaurine fluorescence and giemsa staining. Nature 243: 290-293.
50. Royer-Pokora, B., U. Loos, and W.-D. Ludwig. 1991. TTG-2, a new gene encoding a cysteine-rich protein with the LIM motif, is overexpressed in acute T-cell leukemia with the t(11;14)(p13;q11). Oncogene 6: 1887-1893.
51. Sanchez-Garcia, I. and T.H. Rabbitts. 1994. Transcriptional activation by TAL1 and FUS-CHOP proteins expressed in acute malignacies as a result of chromosomal abnormalities. Proc. Natl. Acad. Sci. 91: 7869-7873.
52. Sanchez-Garcia, I., Y. Kaneko, R. Gonzalez-Sarmiento, K. Campbell, L. White, T. Boehm, and T.H. Rabbitts. 1991. A study of chromosome 11p13 translocations involving TCRβ and TCRδ in human T cell leukemia. Oncogene 6: 577-582.
53. Schmeichel, K.L. and M.C. Beckerle. 1994. The LIM domain is a modular protein-binding interface. Cell 79: 211-219.
54. Shivdasani, R.A., E. Mayer, and S.H. Orkin. 1995. Absence of blood formation in mice lacking the T-cell leukemia oncoprotein tal-1/SCL. Nature 373: 432-434.
55. Shoresh, M., S. Orgad, O. Shmueli, R. Werczberger, D. Gelbaum, S. Abiri, and D. Segal. 1998. Overexpression Beadex mutations and loss-of-function heldup-a mutations in Drosophila affect the 3′ regulatory and coding components, respectively of the Dlmo gene. Genetics (in press).
56. Valge-Archer, V.E., H. Osada, A.J. Warren, A. Forster, J. Li, R. Baer, and T.H. Rabbitts. 1994. The LIM protein RBTN2 and the bHLH protein TAL1 are present in a complex in erythroid cells. Proc. Natl. Acad. Sci. 91: 8617-8621.
57. Valge-Archer, V., A. Foster, and T.H. Rabbitts. 1988. The LMO1 and LDB1 proteins interact in human T cell acute leukaemia with the chromosomal translocation t(11;14)(p15;q11). Oncogene (in press).
58. Wadman, I., J. Li, R.O. Bash, A. Forster, H. Osada, T.H. Rabbitts. and R. Baer. 1994a. Specific in vivo association between the bHLH and LIM proteins implicated in human T cell leukemia. EMBO J. 13: 4831-4839.
59. Wadman, I.A., H.-L. Hsu, M.H. Cobb, and R. Baer. 1994b. The MAP kinase phosphorylation site of TAL1 occurs within a transcriptional activation domain. Oncogene 9: 3713-3716.
60. Wadman, I.A., H. Osada, G.G. Grutz, A.D. Agulnick, H. Westphal, A. Forster, and T.H. Rabbitts. 1997. The LIM-only protein Lmo2 is a bridging molecule assembling an erythroid, DNA-binding complex which includes the TAL1, E47, GATA-1 and Ldb1/NLI proteins. EMBO J. 16: 3145-3157.
61. Warren, A.J., W.H. Colledge, M.B.L. Carlton, M.J. Evans, A.J.H. Smith, and T.H. Rabbitts. 1994. The oncogenic cysteine-rich LIM domain protein rbtn2 is essential for erythroid development. Cell 78: 45-58.
62. Yamada, Y., A.W. Warren, C. Dobson, A. Forster, R. Pannell, and T.H. Rabbitts. 1998. The T cell leukemia LIM protein Lmo2 is necessary for adult mouse hematopoiesis. Proc. Natl. Acad. Sci. 95: 3890-3895.
63. Yan, W., A.Z. Young, V.C. Soares, R. Kelley, R. Benezra, and Y. Zhuang. 1997. High incidence of T-cell tumors in E2A-null mice and E2A/Id1 double-knockout mice. Mol. Cell. Biol. 17: 7317-7327.
64. Zech, L., U. Hagland, K. Nilsson, and G. Klein. 1976. Characteristic chromosomal abnormalities in biopsies and lymphoid cell lines from patients with Burkitt's and nonBurkitt's lymphomas. Int. J. Cancer 17: 47-56.
65. Zhu, T.-H., J. Bodem, E. Keppel, R. Paro, and B. Royer-Pokora. 1995. A single ancestral gene of the human LIM domain oncogene family LMO in Drosophila: Characterisation of the Drosophila Dlmo gene. Oncogene 11: 1283-1290.