Aleukemia fusion protein attenuates the spindle checkpoint and promotes aneuploidy

Blood

Volumn 109, Issue 9, 2007, Pages 3963-3971

  Boyapati, Anita ^a   Yan, Ming ^a   Peterson, Luke F ^a   Biggs, Joseph R ^a   Le Beau, Michelle M ^b   Zhang, Dong Er ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b SECTION OF HEMATOLOGY ONCOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUB1 RELATED PROTEIN; HYBRID PROTEIN; NOCODAZOLE; PROTEIN AML1 ETO; UNCLASSIFIED DRUG; AML1 ETO FUSION PROTEIN, HUMAN; AML1-ETO FUSION PROTEIN, HUMAN; ANTINEOPLASTIC AGENT; BUB1 SPINDLE CHECKPOINT PROTEIN; CELL CYCLE PROTEIN; ONCOPROTEIN; PROTEIN KINASE; SPAG5 PROTEIN, HUMAN; TRANSCRIPTION FACTOR RUNX1;

ACUTE GRANULOCYTIC LEUKEMIA; ANEUPLOIDY; ARTICLE; CELL CYCLE ARREST; CHROMOSOME ABERRATION; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MITOSIS; PRIORITY JOURNAL; ANIMAL; BIOSYNTHESIS; CELL CYCLE; CELL STRAIN K 562; CHROMOSOME 21; CHROMOSOME 8; DRUG EFFECT; GENE TRANSLOCATION; GENETICS; METABOLISM; MOUSE;

ANEUPLOIDY; ANIMALS; ANTINEOPLASTIC AGENTS; CELL CYCLE; CELL CYCLE PROTEINS; CHROMOSOMES, HUMAN, PAIR 21; CHROMOSOMES, HUMAN, PAIR 8; CORE BINDING FACTOR ALPHA 2 SUBUNIT; HUMANS; K562 CELLS; LEUKEMIA, MYELOCYTIC, ACUTE; MICE; NOCODAZOLE; ONCOGENE PROTEINS, FUSION; PROTEIN KINASES; TRANSLOCATION, GENETIC;

EID: 34247378186     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-09-045583     Document Type: Article

References (62)

1. Miyoshi H, Shimizu K, Kozu T, et al. t(8;21) breakpoints on chromosome 21 in acute myeloid leukemia are clustered within a limited region of a single gene, AML1. Proc Natl Acad Sci U S A. 1991;88:10431-10434.
2. Yergeau DA, Hetherington CJ, Wang Q, et al. Embryonic lethality and impairment of haematopoiesis in mice heterozygous for an AML1-ETO fusion gene. Nat Genet. 1997;15:303-306.
3. Okuda T, Cai Z, Yang S, et al. Expression of a knocked-in AML1-ETO leukemia gene inhibits the establishment of normal definitive hematopoiesis and directly generates dysplastic hematopoietic progenitors. Blood. 1998;91:3134-3143.
4. Okuda T, van DJ, Hiebert SW, Grosveld G, Downing JR. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell. 1996;84:321-330.
5. Wang Q, Stacy T, Miller JD, et al. The CBFbeta subunit is essential for CBFalpha2 (AML1) function in vivo. Cell. 1996;87:697-708.
6. Rhoades KL, Hetherington CJ, Harakawa N, et al. Analysis of the role of AML1-ETO in leukemogenesis, using an inducible transgenic mouse model. Blood. 2000;96:2108-2115.
7. Yuan Y, Zhou L, Miyamoto T, et al. AML1-ETO expression is directly involved in the development of acute myeloid leukemia in the presence of additional mutations. Proc Natl Acad Sci U SA. 2001;98:10398-10403.
8. Fenske TS, Pengue G, Mathews V, et al. Stem cell expression of the AML1/ETO fusion protein induces a myeloproliferative disorder in mice. Proc Natl Acad Sci U S A. 2004;101:15184-15189.
9. Schwieger M, Lohler J, Friel J, et al. AML1-ETO inhibits maturation of multiple lymphohematopoietic lineages and induces myeloblast transformation in synergy with ICSBP deficiency. J Exp Med. 2002;196:1227-1240.
10. de Guzman CG, Warren AJ, Zhang Z, et al. Hematopoietic stem cell expansion and distinct myeloid developmental abnormalities in a murine model of the AML1-ETO translocation. Mol Cell Biol. 2002;22:5506-5517.
11. Higuchi M, O'Brien D, Kumaravelu P, et al. 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. 2002;1:63-74.
12. Yan M, Burel SA, Peterson LF, et al. Deletion of an AML1-ETO C-terminal NcoR/SMRT-interacting region strongly induces leukemia development. Proc Natl Acad Sci U S A. 2004;101:17186-17191.
13. Yan M, Kanbe E, Peterson LF, et al. A previously unidentified alternatively spliced isoform of t(8;21) transcript promotes leukemogenesis. Nat Med. 2006;12:945-949.
14. Mertens F, Johansson B, Mitelman F. Age- and gender-related heterogeneity of cancer chromosome aberrations. Cancer Genet Cytogenet. 1993;70:6-11.
15. Johnson PR, Yin JA. Prognostic factors in elderly patients with acute myeloid leukaemia. Leuk Lymphoma. 1994;16:51-56.
16. Herens C, Brasseur E, Jamar M, et al. Loss of the Y chromosome in bone marrow cells: results on 1907 consecutive cases of leukaemia and preleukaemia. Clin Lab Haematol. 1999;21:17-20.
17. Haferlach T, Bennett JM, Loffler H, et al. Acute myeloid leukemia with translocation (8;21): cytomorphology, dysplasia and prognostic factors in 41 cases: AML Cooperative Group and ECOG. Leuk Lymphoma. 1996;23:227-234.
18. Heim S, Mitelman F. Secondary chromosome aberrations in the acute leukemias. Cancer Genet Cytogenet. 1986;22:331-338.
19. Chen FJ, Yang AD, Fei HB. A chromosome study on 97 cases of acute nonlymphocytic leukemia M2. J Tongji Med Univ. 1994;14:35-37.
20. Rege K, Swansbury GJ, Atra AA, et al. Disease features in acute myeloid leukemia with t(8; 21)(q22;q22): influence of age, secondary karyotype abnormalities, CD19 status, and extramedullary leukemia on survival. Leuk Lymphoma. 2000;40:67-77.
21. Groupe Francais de Cytogenetique Hematologique. Acute myelogenous leukemia with an 8;21 translocation. Cancer Genet Cytogenet. 1990;44:169-179.
22. Lai YY, Qiu JY, Jiang B, et al. Characteristics and prognostic factors of acute myeloid leukemia with t (8; 21) (q22; q22). Zhongguo Shi Yan Xue Ye Xue Za Zhi. 2005;13:733-740.
23. Asou H, Tashiro S, Hamamoto K, et al. Establishment of a human acute myeloid leukemia cell line (Kasumi-1) with 8;21 chromosome translocation. Blood. 1991;77:2031-2036.
24. Matozaki S, Nakagawa T, Kawaguchi R, et al. Establishment of a myeloid leukaemic cell line (SKNO-1) from a patient with t(8;21) who acquired monosomy 17 during disease progression. Br J Haematol. 1995;89:805-811.
25. Neben K, Giesecke C, Schweizer S, Ho AD, Kramer A. Centrosome aberrations in acute myeloid leukemia are correlated with cytogenetic risk profile. Blood. 2003;101:289-291.
26. Bharadwaj R, Yu H. The spindle checkpoint, aneuploidy, and cancer. Oncogene. 2004;23:2016-2027.
27. Michel LS, Liberal V, Chatterjee A, et al. MAD2 haplo-insufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature. 2001;409:355-359.
28. Kops GJ, Foltz DR, Cleveland DW. Lethality to human cancer cells through massive chromosome loss by inhibition of the mitotic checkpoint. Proc Natl Acad Sci U S A. 2004;101:8699-8704.
29. Michel L, az-Rodriguez E, Narayan G, et al. Complete loss of the tumor suppressor MAD2 causes premature cyclin B degradation and mitotic failure in human somatic cells. Proc Natl Acad Sci U S A. 2004;101:4459-4464.
30. Dai W, Wang Q, Liu T, et al. Slippage of mitotic arrest and enhanced tumor development in mice with BubR1 haploinsufficiency. Cancer Res. 2004;64:440-445.
31. Cohen-Fix O, Peters JM, Kirschner MW, Koshland D. Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev. 1996;10:3081-3093.
32. Zou H, McGarry TJ, Bernal T, Kirschner MW. Identification of a vertebrate sister-chromatid separation inhibitor involved in transformation and tumorigenesis. Science. 1999;285:418-422.
33. Uhlmann F, Wernic D, Poupart MA, Koonin EV, Nasmyth K. Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell. 2000;103:375-386.
34. Rieder CL, Maiato H. Stuck in division or passing through: what happens when cells cannot satisfy the spindle assembly checkpoint. Dev Cell. 2004;7:637-651.
35. Karasuyama H, Melchers F. Establishment of mouse cell lines which constitutively secrete large quantities of interleukin 2, 3, 4 or 5, using modified cDNA expression vectors. Eur J Immunol. 1988;18:97-104.
36. Li S, Ilaria RL Jr, Million RP, Daley GQ, Van Etten RA. The P190, P210, and P230 forms of the BCR/ABL oncogene induce a similar chronic myeloid leukemia-like syndrome in mice but have different lymphoid leukemogenic activity. J Exp Med. 1999;189:1399-1412.
37. Amann JM, Nip J, Strom DK, et al. ETO, a target of t(8;21) in acute leukemia, makes distinct contacts with multiple histone deacetylases and binds mSin3A through its oligomerization domain. Mol Cell Biol. 2001;21:6470-6483.
38. Burel SA, Harakawa N, Zhou L, et al. Dichotomy of AML1-ETO functions: growth arrest versus block of differentiation. Mol Cell Biol. 2001;21:5577-5590.
39. Kops GJ, Weaver BA, Cleveland DW. On the road to cancer: aneuploidy and the mitotic checkpoint. Nat Rev Cancer. 2005;5:773-785.
40. Song WJ, Sullivan MG, Legare RD, et al. Haplo-insufficiency of CBFA2 causes familial thrombocytopenia with propensity to develop acute myelogenous leukaemia. Nat Genet. 1999;23:166-175.
41. Michaud J, Wu F, Osato M, et al. In vitro analyses of known and novel RUNX1/AML1 mutations in dominant familial platelet disorder with predisposition to acute myelogenous leukemia: implications for mechanisms of pathogenesis. Blood. 2002;99:1364-1372.
42. Naumann S, Reutzel D, Speicher M, Decker HJ. Complete karyotype characterization of the K562 cell line by combined application of G-banding, multiplex-fluorescence in situ hybridization, fluorescence in situ hybridization, and comparative genomic hybridization. Leuk Res. 2001;25:313-322.
43. Ciosk R, Zachariae W, Michaelis C, et al. An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast. Cell 1998;93:1067-1076.
44. Waizenegger I, Gimenez-Abian JF, Wernic D, Peters JM. Regulation of human separase by securin binding and autocleavage. Curr Biol. 2002;12:1368-1378.
45. Zou H, Stemman O, Anderson JS, Mann M, Kirschner MW. Anaphase specific auto-cleavage of separase. FEBS Lett. 2002;528:246-250.
46. Chestukhin A, Pfeffer C, Milligan S, DeCaprio JA, Pellman D. Processing, localization, and requirement of human separase for normal anaphase progression. Proc Natl Acad Sci U S A. 2003;100:4574-4579.
47. Zhang J, Hug BA, Huang EY, et al. Oligomerization of ETO is obligatory for corepressor interaction. Mol Cell Biol. 2001;21:156-163.
48. Hildebrand D, Tiefenbach J, Heinzel T, Grez M, Maurer AB. Multiple regions of ETO cooperate in transcriptional repression. J Biol Chem. 2001;276:9889-9895.
49. Tang Z, Bharadwaj R, Li B, Yu H. Mad2-Independent inhibition of APCCdc20 by the mitotic checkpoint protein BubR1. Dev Cell. 2001;1:227-237.
50. Kasai T, Iwanaga Y, Iha H, Jeang KT. Prevalent loss of mitotic spindle checkpoint in adult T-cell leukemia confers resistance to microtubule inhibitors. J Biol Chem. 2002;277:5187-5193.
51. Bhalla K, Huang Y, Tang C, et al. Characterization of a human myeloid leukemia cell line highly resistant to taxol. Leukemia. 1994;8:465-475.
52. Lutterbach B, Sun D, Schuetz J, Hiebert SW. The MYND motif is required for repression of basal transcription from the multidrug resistance 1 promoter by the t(8;21) fusion protein. Mol Cell Biol. 1998;18:3604-3611.
53. Bergstralh DT, Ting JP. Microtubule stabilizing agents: their molecular signaling consequences and the potential for enhancement by drug combination. Cancer Treat Rev. 2006;32:166-179.
54. Fujiwara T, Bandi M, Nitta M, et al. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature. 2005;437:1043-1047.
55. Castedo M, Perfettini JL, Roumier T, et al. Cell death by mitotic catastrophe: a molecular definition. Oncogene. 2004;23:2825-2837.
56. Fischbach NA, Rozenfeld S, Shen W, et al. HOXB6 overexpression in murine bone marrow immortalizes a myelomonocytic precursor in vitro and causes hematopoietic stem cell expansion and acute myeloid leukemia in vivo. Blood. 2005;105:1456-1466.
57. Luo H, Li Q, O'Neal J, et al. c-Myc rapidly induces acute myeloid leukemia in mice without evidence of lymphoma-associated antiapoptotic mutations. Blood. 2005;106:2452-2461.
58. Rosenbauer F, Wagner K, Kutok JL, et al. Acute myeloid leukemia induced by graded reduction of a lineage-specific transcription factor, PU.1. Nat Genet. 2004;36:624-630.
59. Le Beau MM, Bitts S, Davis EM, Kogan SC. Recurring chromosomal abnormalities in leukemia in PML-RARA transgenic mice parallel human acute promyelocytic leukemia. Blood. 2002;99:2985-2991.
60. Wang Z, Yu R, Melmed S. Mice lacking pituitary tumor transforming gene show testicular and splenic hypoplasia, thymic hyperplasia, thrombocytopenia, aberrant cell cycle progression, and premature centromere division. Mol Endocrinol. 2001;15:1870-1879.
61. Jallepalli PV, Waizenegger IC, Bunz F, et al. Securin is required for chromosomal stability in human cells. Cell. 2001;105:445-457.
62. Pfleghaar K, Heubes S, Cox J, Stemmann O, Speicher MR. Securin is not required for chromosomal stability in human cells. PLoSBiol. 2005;3:e416.