Conditional MLL-CBP targets GMP and models therapy-related myeloproliferative disease

EMBO Journal

Volumn 24, Issue 2, 2005, Pages 368-381

  Wang, Jing ^a   Iwasaki, Hiromi ^b   Krivtsov, Andrei ^c   Febbo, Phillip G ^b   Thorner, Aaron R ^b   Ernst, Patricia ^a   Anastasiadou, Erna ^d,g   Kutok, Jeffery L ^b   Kogan, Scott C ^e   Zinkel, Sandra S ^a   Fisher, Jill K ^a   Hess, Jay L ^f   Golub, Todd R ^b   Armstrong, Scott A ^c   Akashi, Koichi ^b   Korsmeyer, Stanley J ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g BIOMEDICAL RESEARCH FOUNDATION   (Greece)

Author keywords

Granulocyte macrophage progenitors; Leukemogenesis; MLL CBP; Myeloproliferative disease

Indexed keywords

ETHYLNITROSOUREA; HYBRID PROTEIN; MIXED LINEAGE LEUKEMIA PROTEIN;

ACUTE LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CHROMOSOME REARRANGEMENT; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; GAMMA RADIATION; GENE; GENE MUTATION; HEMATOPOIESIS; LEUKEMOGENESIS; MLL GENE; MOUSE; MYELOPROLIFERATIVE DISORDER; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RECEPTOR UPREGULATION; UNINDEXED SEQUENCE;

ANIMALS; CREB-BINDING PROTEIN; DNA-BINDING PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MYELOID-LYMPHOID LEUKEMIA PROTEIN; MYELOPROLIFERATIVE DISORDERS; NUCLEAR PROTEINS; PROTO-ONCOGENES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 13444311619     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600521     Document Type: Article

References (43)

1. Afonja O, Smith Jr JE, Cheng DM, Goldenberg AS, Amorosi E, Shímamoto T, Nakamura S, Ohyashiki K, Ohyashiki J, Toyama K, Takeshita K (2000) MEIS1 and HOXA7 genes in human acute myeloid leukemia. Leuk Res 24: 849-855
2. Armstrong SA, Staunton JE, Silverman LB, Pieters R, den Boer ML, Minden MD, Sallan SE, Lander ES, Golub TR, Korsmeyer SJ (2002) MLL translocations specify a distinct gene expression profile that distinguishes a unique leukemia. Nat Genet 30: 41-47
3. Ayton PM, Cleary ML (2003) Transformation of myeloid progenitors by MLL oncoproteins is dependent on Hoxa7 and Hoxa9. Genes Dev 17: 2298-2307
4. Bannister AJ, Kouzarides T (1996) The CBP co-activator is a histone acetyltransferase. Nature 384: 641-643
5. Behm FG, Raimondi SC, Frestedt JL, Liu Q, Crist WM, Downing JR, Rivera GK, Kersey JH, Pui CH (1996) Rearrangement of the MLL gene confers a poor prognosis in childhood acute lymphoblastic leukemia, regardless of presenting age. Blood 87: 2870-2877
6. Blobel GA, Nakajima T, Eckner R, Montminy M, Orkin SH (1998) CREB-binding protein cooperates with transcription factor GATA-1 and is required for erythroid differentiation. Proc Natl Acad Sci USA 95: 2061-2066
7. Borrow J, Shearman AM, Stanton Jr VP, Becher R, Collins T, Williams AJ, Dube I, Katz F, Kwong YL, Morris C, Ohyashiki K, Toyama K, Rowley J, Housman DE (1996) The t(7;11)(p15;p15) translocation in acute myeloid leukaemia fuses the genes for nucleoporin NUP98 and class I homeoprotein HOXA9. Nat Genet 12: 159-167
8. Boyes J, Byfield P, Nakatani Y, Ogryzko V (1998) Regulation of activity of the transcription factor GATA-1 by acetylation. Nature 396: 594-598
9. Breuer M, Slebos R, Verbeek S, van Lohuizen M, Wientjens E, Berns A (1989) Very high frequency of lymphoma induction by a chemical carcinogen in pim-1 transgenic mice. Nature 340: 61-63
10. Buchberg AM, Bedigian HG, Jenkins NA, Copelami NG (1990) Evi-2, a common integration site involved in rnurine myeloid leukmogenesis. Mol Cell Biol 10: 4658-4666
11. Caslini C, Alarcon AS, Hess JL, Tanaka R, Murti KG, Biondi A (2000) The amino terminus targets the mixed lineage leukemia (MLL) protein to the nucleolus, nuclear matrix and mitolic chromosomal scaffolds. Leukemia 14: 1898-1908
12. Corral J, Lavenir I, Impey H, Warren AJ, Forster A. Larson TA, Bell S, McKenzie AN, King G, Rabbitts TH (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
13. Debernardi S, Lillington DM, Chaplin T, Tomlinson S, Amess J, Rohatiner A, Lister TA, Young BD (2003) Genome-wide analysis of acute myeloid leukemia with normal karyotype reveals a unique pattern of homeobox gene expression distinct from those with translocation-mediated fusion events. Genes Chromosomes Cancer 37: 149-158
14. Dobson CL, Warren AJ, Pannell R, Forster A, Lavenir I, Corral J, Smith AJ, Rabbitts TH (1999) The mll-AF9 gene fusion in mice controls myeloproliferation and specifies acute myeloid leukaemogenesis. EMBO J 18: 3564-3574
15. Dorsam ST, Ferrell CM, Dorsam GP, Derynck MK, Vijapurkar U, Khodabakhsh D, Pau B, Bernstein H, Haqq CM, Largman C, Lawrence HJ (2004) The transcriptome of the leukemogenic homeoprotein HOXA9 in human hematopoietic cells. Blood 103: 1676-1684
16. Ernst P, Wang J, Huang M, Goodman RH, Korsmeyer SJ (2001) MLL and CREB bind cooperatively to the nuclear coactivator CREB-binding protein. Mol Cell Biol 21: 2249-2258
17. Felix CA, Hosler MR, Winick NJ, Masterson M, Wilson AE, Lange BJ (1995) ALL-1 gene rearrangements in DNA topoisomerase II inhibitor-related leukemia in children. Blood 85: 3250-3256
18. Ghannam G, Takeda A, Camarata T, Moore MA, Viale A, Yaseen NR (2004) The oncogene Nup98-HOXA9 induces gene transcription in myeloid cells. J Biol Chem 279: 866-875
19. Gu W, Roeder RG (1997) Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90: 595-606
20. Higuchi M, O'Brien D, Kumaravelu P, Lenny N, Yeoh EJ, Downing JR (2002) Expression of a conditional AML1-ETO oncogene bypasses embryonic lethality and establishes a murine model of human t(8;21) acute myeloid leukemia. Cancer Cell 1: 63-74
21. Hunger SP, Tkachuk DC, Amylon MD, Link MP, Carroll AJ, Welborn JL, Willman CL, Cleary ML (1993) HRX involvement in de novo and secondary leukemias with diverse chromosome 11q23 abnormalities. Blood 81: 3197-3203
22. Kogan SC, Ward JM, Anver MR, Berman JJ, Brayton C, Cardiff RD, Carter JS, de Coronado S, Downing JR, Fredrickson TN, Haines DC, Harris AW, Harris NL, Hiai H, Jaffe ES, MacLennan IC, Pandolfi PP, Pattengale PK, Perkins AS, Simpson RM, Tuttle MS, Wong JF, Morse III HC (2002) Bethesda proposals for classification of nonlymphoid hematopoietic neoplasms in mice. Blood 100: 238-245
23. Kroon E, Krosl J, Thorsteinsdottir U, Baban S, Buchberg AM, Sauvageau G (1998) Hoxa9 transforms primary bone marrow cells through specific collaboration with Meisla but not Pbx1b. EMBO J 17: 3714-3725
24. Kumar AR, Hudson WA, Chen W, Nishiuchi R, Yao Q, Kersey JH (2004) Hoxa9 influences the phenotype but not the incidence of Mll-AF9 fusion gene leukemia. Blood 103: 1823-1828
25. Kwok RP, Lundblad JR, Chrivia JC, Richards JP, Bachinger HP, Brennan RG, Roberts SG, Green MR, Goodman RH (1994) Nuclear protein CBP is a coactivator for the transcription factor CREB [see comments]. Nature 370: 223-226
26. Lasko M, Sauer B, Mosinger B, Lee EJ, Manning RW, Yu S-H, Mulder KL, Westphal H (1992) Targeted oncogene activation by site-specific recombination in transgenic mice. Proc Natl Acad Sci USA 89: 6232-6236
27. Lavau C, Du C, Thirman M, Zeleznik-Le N (2000) Chromatin-related properties of CBP fused to MLL generate a myelodysplastic-like syndrome that evolves into myeloid leukemia. EMBO J 19: 4655-4664
28. Magli MC, Barba P, Celetti A, De Vita G, Cillo C, Boncinelli E (1991) Coordinate regulation of HOX genes in human hematopoietic cells. Proc Natl Acad Sci USA 88: 6348-6352
29. Magli MC, Largman C, Lawrence HJ (1997) Effects of HOX homeobox genes in blood cell differentiation. J Cell Physiol 173:168-177
30. Munoz L, Nomdedeu JF, Villamor N, Guardia R, Colomer D, Ribera JM, Torres JP, Berlanga JJ, Fernandez C, Llorente A, Queipo de Llano MP, Sanchez JM, Brunet S, Sierra J (2003) Acute myeloid leukemia with MLL rearrangements: clinicobiological features, prognostic impact and value of flow cytometry in the detection of residual leukemic cells. Leukemia 17: 76-82
31. Nakamura T, Largaespada DA, Shaughnessy Jr JD, Jenkins NA, Copeland NG (1996) Cooperative activation of Hoxa and Pbx1-related genes in murine myeloid leukaemias (see comments). Nat Genet 12: 149-153
32. Rabbitts TH (1994) Chromosomal translocations in human cancer. Nature 372: 143-149
33. Rowley JD, Reshmi S, Sobulo O, Musvee T, Anastasi J, Raimondi S, Schneider NR, Barredo JC, Cantu ES, Schlegelberger B, Behm F, Doggett NA, Borrow J, Zeleznik-Le N (1997) All patients with the T(11;16)(q23;p13.3) that involves MLL and CBP have treatment-related hematologic disorders. Blood 90: 535-541
34. Shen WF, Largman C, Lowney P, Corral JC, Detmer K, Hauser CA, Simonitch TA, Hack FM, Lawrence HJ (1989) Lineage-restricted expression of homeobox-containing genes in human hematopoietic cell lines. Proc Natl Acad Sci USA 86: 8536-8540
35. So CW, Karsunky H, Passegue E, Cozzio A, Weissman IL, Cleary ML (2003) MLL-GAS7 transforms multipotent hematopoietic progenitors and induces mixed lineage leukemias in mice. Cancer Cell 3: 161-171
36. Sobulo OM, Borrow J, Tomek R, Reshmi S, Harden A, Schlegelberger B, Housman D, Doggett NA, Rowley JD, Zeleznik-Le NJ (1997) MLL is fused to CBP, a histone acetyltransferase, in therapy-related acute myeloid leukemia with a t(11;16)(q23;p13.3). Proc Natl Acad Sci USA 94: 8732-8737
37. Spangrude GJ, Heimfeld S, Weissman IL (1988) Purification and characterization of mouse hematopoietic stem cells. Science 241: 58-62
38. Super HJ, McCabe NR, Thirman MJ, Larson RA, Le Beau MM, Pedersen-Bjergaard J, Philip P, Diaz MO, Rowley JD (1993) Rearrangements of the MLL gene in therapy-related acute myeloid leukemia in patients previously treated with agents targeting DNA-topoisomerase II. Blood 82: 3705-3711
39. Taki T, Sako M, Tsuchida M, Hayashi Y (1997) The t(11;16) (q23;p13) translocation in myelodysplastic syndrome fuses the MLL gene to the CBP gene. Blood 89: 3945-3950
40. Van Orden K, Giebler HA, Lemasson I, Gonzales M, Nyborg JK (1999) Binding of p53 to the KIX domain of CREB binding protein. A potential link to human T-cell leukemia virus, type I-associated leukemogenesis. J Biol Chem 274: 26321-26328
41. Yeoh EJ, Ross ME, Shurtleff SA, Williams WK, Patel D, Mahfouz R, Behm FG, Raimondi SC, Relling MV, Patel A, Cheng C, Campana D, Wilkins D, Zhou X, Li J, Liu H, Pui CH, Evans WE, Naeve C, Wong L, Downing JR (2002) Classification, subtype discovery, and prediction of outcome in pediatric acute lymphoblastic leukemia by gene expression profiling. Cancer Cell 1: 133-143
42. Yu BD, Hanson RD, Hess JL, Horning SE, Korsmeyer SJ (1998) MLL, a mammalian trithorax-group gene, functions as a transcriptional maintenance factor in morphogenesis. Proc Natl Acad Sci USA 95: 10632-10636
43. Yu BD, Hess JL, Horning SE, Brown GA, Korsmeyer SJ (1995) Altered Hox expression and segmental identity in Mll-mutant mice. Nature 378: 505-508