The nuclear oncoprotein TLX1/HOX11 associates with pericentromeric satellite 2 DNA in leukemic T-cells

Leukemia

Volumn 20, Issue 2, 2006, Pages 304-312

  Heidari, M ^a,c   Rice, K L ^a,d   Phillips, J K ^a   Kees, U R ^b   Greene, W K ^a  

^a MURDOCH UNIVERSITY   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Hetechromatin; Homeodomain; Pericentromic; Satellite 2 DNA; T cell luekemia; TXL1

Indexed keywords

DNA BINDING PROTEIN; NUCLEAR PROTEIN; ONCOPROTEIN; PROTEIN HOX11; PROTEIN TLX1; SATELLITE DNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL IMMORTALIZATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA SEQUENCE; GENOME; HETEROCHROMATIN; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; ORGANOGENESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SPLEEN; T CELL LEUKEMIA; T LYMPHOCYTE;

EID: 31444441854     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/sj.leu.2404071     Document Type: Article

References (65)

1. Dear TN, Sanchez-Garcia I, Rabbitts TH. The HOX11 gene encodes a DNA-binding nuclear transcription factor belonging to a distinct family of homeobox genes. Proc Natl Acad Sci USA 1993; 90: 4431-4435.
2. Cheng SH, Mak TW. Molecular characterization of three murine HOX11-related homeobox genes, Tlx-1, -2, and -3, and restricted expression of Tlx-1 during embryogenesis. Dev Growth Differ 1993; 35: 655-663.
3. Shirasawa S, Yunker AMR, Roth KA, Brown GA, Horning S, Korsmeyer SJ. Enx (Hox11L1)-deficient mice develop myenteric neuronal hyperplasia and megacolon. Nat Med 1997; 3: 646-650.
4. Shirasawa S, Arata A, Onimaru H, Roth KA, Brown GA, Horning S et al. Rnx deficiency results in congenital central hypoventilation. Nat Genet 2000; 24: 287-290.
5. Cheng L, Arata A, Mizuguchi R, Qian Y, Karunaratne A, Gray PA et al. Tlx3 and Tlx1 are post-mitotic selector genes determining glutamatergic over GABAergic cell fates. Nat Neurosci 2004; 7: 510-517.
6. Hatano M, Roberts CWM, Minden M, Crist WM, Korsmeyer SJ. Deregulation of a homeobox gene, HOX11, by the t(10;14) in T-cell leukemia. Science 1991; 253: 79-82.
7. Kennedy MA, Gonzalez-Sarmiento R, Kees UR, Lampert F, Dear N, Boehm T et al. HOX11, a homeobox-containing T-cell oncogene on human chromosome 10q24. Proc Natl Acad Sci USA 1991; 88: 8900-8904.
8. Dube ID, Kamel-Reid S, Yuan CC, Lu M, Wu X, Corpus G et al. A novel human homeobox gene lies at the chromosome 10 breakpoint in lymphoid neoplasias with chromosomal translocation t(10;14). Blood 1991; 78: 2996-3003.
9. Roberts CWM, Shutter JR, Korsmeyer SJ. Hox11 controls the genesis of the spleen. Nature 1994; 368: 747-749.
10. Dear TN, Colledge WH, Carlton MBL, Lavenir I, Larson T, Smith AJH et al. The Hox11 gene is essential for cell survival during spleen development. Development 1995; 121: 2909-2915.
11. Kanzler B, Dear TN. Hox11 acts cell autonomously in spleen development and its absence results in altered cell fate of mesenchymal spleen precursors. Dev Biol 2001; 234: 231-243.
12. Ferrando AA, Neuberg DS, Staunton J, Loh ML, Huard C, Raimondi SC et al. Gene expression signatures define novel oncogenic pathways in T-cell acute lymphoblastic leukemia. Cancer Cell 2002; 1: 75-87.
13. Kees UR, Heerema NA, Kumar R, Watt PM, Baker DL, La MK et al. Expression of HOX11 in childhood T-lineage acute lymphoblastic leukaemia can occur in the absence of cytogenetic aberration at 10q24: A study from the Children's Cancer Group (CCG). Leukemia 2003; 17: 887-893.
14. Bernard OA, Busson-LeConiat M, Ballerini P, Mauchauffe M, Della Valle V, Monni R et al. A new recurrent and specific cryptic translocation, t(5;14)(q35;q32), is associated with expression of the Hox11L2 gene in T acute lymphoblastic leukaemia. Leukemia 2001; 15: 1495-1504.
15. Mauvieux L, Leymarie V, Helias C, Perrusson N, Falkenrodt A, Lioure B et al. High incidence of Hox11L2 expression in children with T-ALL. Leukemia 2002; 16: 2417-2422.
16. Hawley RG, Fong AZ, Lu M, Hawley TS. The HOX11 homeobox-containing gene of human leukemia immortalizes murine hematopoietic precursors. Oncogene 1994; 9: 1-12.
17. Hough MR, Reis MD, Singaraja R, Bryce DM, Kamel-Reid S, Dardick I et al. A model for spontaneous B-lineage lymphomas in IgHμ-HOX11 transgenic mice. Proc Natl Acad Sci USA 1998; 95: 13853-13858.
18. Keller G, Wall C, Fong AZ, Hawley TS, Hawley RG. Overexpression of HOX11 leads to the immortalization of embryonic precursors with both primitive and definitive hematopoietic potential. Blood 1998; 92: 877-887.
19. Greene WK, Ford J, Dixon D, Tilbrook PA, Watt PM, Klinken SP et al. Enforced expression of HOX11 is associated with an immature phenotype in J2E erythroid cells. Br J Haematol 2002; 118: 909-917.
20. Zhang N, Shen W, Hawley RG, Lu M. HOX11 interacts with CTF1 and mediates hematopoietic precursor cell immortalization. Oncogene 1999; 18: 2273-2279.
21. Allen TD, Zhu Y-X, Hawley TS, Hawley RG. TALE homeoproteins as HOX11-interacting partners in T-cell leukemia. Leuk Lymphoma 2000; 39: 241-256.
22. Greene WK, Bahn S, Masson N, Rabbitts TH. The T-cell oncogenic protein HOX11 activates Aldh1 expression in NIH 3T3 cells but represses its expression in mouse spleen development. Mol Cell Biol 1998; 18: 7030-7037.
23. Koehler K, Franz T, Dear TN. Hox11 is required to maintain normal Wt1 mRNA levels in the developing spleen. Dev Dyn 2000; 218: 201-206.
24. Hoffmann K, Dixon DN, Greene WK, Ford J, Taplin R, Kees UR. A microarray model system identifies potential new target genes of the proto-oncogene HOX11. Genes Chromosomes Cancer 2004; 41: 309-320.
25. Tang S, Breitman ML. The optimal binding sequence of the Hox11 protein contains a predicted recognition core motif. Nucleic Acids Res 1995; 23: 1928-1935.
26. Shimizu H, Kang M, Iitsuka Y, Ichinose M, Tokuhisa T, Hatano M. Identification of an optimal Ncx binding sequence required for transcriptional activation. FEBS Lett 2000; 475: 170-174.
27. Minowada J. Leukemia cell lines. Cancer Rev 1988; 10: 1-18.
28. Kees UR, Ford J, Price PJ, Meyer BF, Herrmann RP. PER-117: A new human ALL cell line with an immature thymic phenotype. Leuk Res 1987; 11: 489-498.
29. Kinzler KW, Vogelstein B. Whole genome PCR: Application to the identification of sequences bound by gene regulatory proteins. Nucleic Acids Res 1989; 17: 3645-3653.
30. Harris SE, Winchester CL, Johnson KJ. Functional analysis of the homeodomain protein SIX5. Nucleic Acids Res 2000; 28: 1871-1878.
31. Heidari M, Rice KL, Kees UR, Greene WK. Expression and purification of the human homeodomain oncoprotein HOX11. Protein Expresssion Purif 2002; 25: 313-318.
32. Weinmann AS, Bartley SM, Zhang T, Zhang MQ, Farnham PJ. Use of chromatin immunoprecipitation to clone novel E2F target promoters. Mol Cell Biol 2001; 21: 6820-6832.
33. Jeanpierre M. Human satellites 2 and 3. Ann Genet 1994; 37: 163-171.
34. 2-terminal 50 amino acids. Mol Cell Biol 1998; 18: 3502-3508.
35. Masumoto H, Nakano M, Ohzeki J. The role of CENP-B and alpha-satellite DNA: De novo assembly and epigenetic maintenance of human centromeres. Chromosome Res 2004; 12: 543-556.
36. Alcobia I, Dilao R, Parreira L. Spatial associations of centromeres in the nuclei of hematopoietic cells: Evidence for cell-type-specific organizational patterns. Blood 2000; 95: 1608-1615.
37. Beil M, Durschmied D, Paschke S, Schreiner B, Nolte U, Bruel A et al. Spatial distribution patterns of interphase centromeres during retinoic acid-induced differentiation of promyelocytic leukemia cells. Cytometry 2002; 47: 217-225.
38. Brown KE, Guest SS, Smale ST, Hahm K, Merkenschlager M, Fisher AG. Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell 1997; 91: 845-854.
39. Cobb BS, Morales-Alcelay S, Kleiger G, Brown KE, Fisher AG, Smale ST. Targeting of Ikaros to pericentromeric heterochromatin by direct DNA binding. Genes Dev 2000; 14: 2146-2160.
40. Zhang N, Shen W, Ho AD, Lu M. Three distinct domains in the HOX11 homeobox oncoprotein are required for optimal transactivation. Oncogene 1996; 13: 1781-1787.
41. Owens BM, Zhu YX, Suen TC, Wang PX, Greenblatt JF, Goss PE et al. Specific homeodomain-DNA interactions are required for HOX11-mediated transformation. Blood 2003; 101: 4966-4974.
42. Therkelsen AJ, Nielsen A, Kolvraa S. Localisation of the classical DNA satellites on human chromosomes as determined by primed in situ labelling (PRINS). Hum Genet 1997; 100: 322-326.
43. Hansen RS, Wijmenga C, Luo P, Stanek AM, Canfield TK, Weemaes CM et al. The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome. Proc Natl Acad Sci USA 1999; 96: 14412-14417.
44. Hahm K, Cobb BS, McCarty AS, Brown KE, Klug CA, Lee R et al. Helios, a T cell-restricted Ikaros family member that quantitatively associates with Ikaros at centromeric heterochromatin. Genes Dev 1998; 12: 782-796.
45. Tang QQ, Lane MD. Activation and centromeric localization of CCAAT/ enhancer-binding proteins during the mitotic clonal expansion of adipocyte differentiation. Genes Dev 1999; 13:2231-2241.
46. Francastel C, Magis W, Groudine M. Nuclear relocation of a transactivator subunit precedes target gene activation. Proc Natl Acad Sci USA 2001; 98: 12120-12125.
47. Matsuda E, Agata Y, Sugai M, Katakai T, Gonda H, Shimizu A. Targeting of Kruppel-associated box-containing zinc finger proteins to centromeric heterochromatin. Implication for the gene silencing mechanisms. J Biol Chem 2001; 276: 14222-14229.
48. Jolly C, Konecny L, Grady DL, Kutskova YA, Cotto JJ, Morimoto RI et al. In vivo binding of active heat shock transcription factor 1 to human chromosome 9 heterochromatin during stress. J Cell Biol 2002; 156: 775-781.
49. Shestakova EA, Mansuroglu Z, Mokrani H, Ghinea N, Bonnefoy E. Transcription factor YY1 associates with pericentromeric gamma-satellite DNA in cycling but not in quiescent (G0) cells. Nucleic Acids Res 2004; 32: 4390-4399.
50. Cai M, Davis RW. Yeast centromere binding protein CBF1, of the helix-loop-helix protein family, is required for chromosome stability and methionine prototrophy. Cell 1990; 61: 437-446.
51. Stoyan T, Gloeckner G, Diekmann S, Carbon J. Multifunctional centromere binding factor 1 is essential for chromosome segregation in the human pathogenic yeast Candida glabrata. Mol Cell Biol 2001; 21: 4875-4888.
52. Dernburg AF, Broman KW, Fung JC, Marshall WF, Philips J, Agard DA et al. Perturbation of nuclear architecture by long-distance chromosome interactions. Cell 1996; 85: 745-759.
53. Francastel C, Walters MC, Groudine M, Martin DIK. A functional enhancer suppresses silencing of a transgene and prevents its localization close to centromeric heterochromatin. Cell 1999; 99: 259-269.
54. Csink AK, Bounoutas A, Griffith ML, Sabl JF, Sage BT. Differential gene silencing by trans-heterochromatin in Drosophila melanogaster. Genetics 2002; 160: 257-269.
55. Wen J, Huang S, Pack SD, Yu X, Brandt SJ, Noguchi CT. Tal1/SCL binding to pericentromeric DNA represses transcription. J Biol Chem 2005; 280: 12956-12966.
56. Brown KE, Baxter J, Graf D, Merkenschlager M, Fisher AG. Dynamic repositioning of genes in the nucleus of lymphocytes preparing for cell division. Mol Cell 1999; 3: 207-217.
57. Gasser SM. Positions of potential: Nuclear organization and gene expression. Cell 2001; 104: 639-642.
58. Fisher AG, Merkenschlager M. Gene silencing, cell fate and nuclear organisation. Curr Opinion Genetics Dev 2002; 12: 193-197.
59. Carmo-Fonseca M. The contribution of nuclear compartmentalization to gene regulation. Cell 2002; 108: 513-521.
60. Trinh LA, Ferrini R, Cobb BS, Weinmann AS, Hahm K, Ernst P et al. Down-regulation of TDT transcription in CD4(+)CD8(+) thymocytes by Ikaros proteins in direct competition with an Ets activator. Genes Dev 2001; 15: 1817-1832.
61. Sabbattini P, Lundgren M, Georgiou A, Chow C, Warnes G, Dillon N. Binding of Ikaros to the lambda5 promoter silences transcription through a mechanism that does not require heterochromatin formation. EMBO J 2001; 20: 2812-2822.
62. Suh E, Chen L, Taylor J, Traber PG. A homeodomain protein related to caudal regulates intestine-specific gene transcription. Mol Cell Biol 1994; 14: 7340-7351.
63. Jacobson EM, Li P, Leon-del-Rio A, Rosenfeld MG, Aggarwal AK. Structure of Pit-1 POU domain bound to DNA as a dimer: Unexpected arrangement and flexibility. Genes Dev 1997; 11: 198-212.
64. Kasahara H, Usheva A, Ueyama T, Aoki H, Horikoshi N, Izumo S. Characterization of homo- and heterodimerization of cardiac Csx/Nkx2.5 homeoprotein. J Biol Chem 2001; 276: 4570-4580.
65. Quirk J, Brown P. Hesx1 homeodomain protein represses transcription as a monomer and antagonises transactivation of specific sites as a homodimer. J Mol Endocrinol 2002; 28: 193-205.