Therapy-related acute myeloid leukemia-like MLL rearrangements are induced by etoposide in primary human CD34+ cells and remain stable after clonal expansion

Blood

Volumn 105, Issue 5, 2005, Pages 2124-2131

  Libura, Jolanta ^b   Slater, Diana J ^b   Felix, Carolyn A ^b   Richardson, Christine ^a  

^a Columbia University College of Physicians and Surgeons ^*  (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; DNA TOPOISOMERASE (ATP HYDROLYSING); ETOPOSIDE; MIXED LINEAGE LEUKEMIA PROTEIN; DNA BINDING PROTEIN; MLL PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ACUTE GRANULOCYTIC LEUKEMIA; ARTICLE; CARCINOGENESIS; CELL ISOLATION; CELL PROLIFERATION; CELL REGENERATION; CHROMOSOME REARRANGEMENT; GENE CLUSTER; GENE DELETION; GENE DUPLICATION; GENE EXPRESSION; GENE INSERTION; GENE REARRANGEMENT; GENE TRANSLOCATION; GENOMIC INSTABILITY; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; INVERSE POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; ACUTE DISEASE; CELL CLONE; CELL CULTURE; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; FETUS BLOOD; GENETICS; HEMATOPOIETIC STEM CELL; MYELOID LEUKEMIA; PATHOLOGY; PROTO ONCOGENE; SECOND CANCER;

ACUTE DISEASE; ANTIGENS, CD34; CELL PROLIFERATION; CELLS, CULTURED; CLONE CELLS; DNA-BINDING PROTEINS; ETOPOSIDE; FETAL BLOOD; GENE REARRANGEMENT; HEMATOPOIETIC STEM CELLS; HUMANS; LEUKEMIA, MYELOID; MYELOID-LYMPHOID LEUKEMIA PROTEIN; NEOPLASMS, SECOND PRIMARY; PROTO-ONCOGENES; TRANSCRIPTION FACTORS; TRANSLOCATION, GENETIC;

EID: 14944354802     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2004-07-2683     Document Type: Article

References (83)

1. Rouse J, Jackson SP. Interfaces between the detection, signaling, and repair of DMA damage. Science. 2002;297:547-551.
2. Khanna KK, Jackson SP. DMA double-strand breaks: signaling, repair and the cancer connection. Nat Genet. 2001;27:247-254.
3. Abraham RT. Cell cycle checkpoint signalling through the ATM and ATR kinases. Genes Dev. 2001;15:2177-2196.
4. Osheroff N, Corbett A, Robinson M. Mechanism of action of topoisomerase ll-targeted antineo-plastic drugs. Adv Pharmacol. 1994;29B:105-126.
5. Clifford B, Beljin M, Stark GR, Taylor WR. G2 arrest in response to topoisomerase II inhibitors: the role of p53. Cancer Res. 2003;63:4074-4081.
6. Rouet P, Smih F, Jasin M. Expression of a site-specific endonuclease stimulates homologous recombination in mammalian cells. Proc Natl Acad Sci USA. 1994;91:6064-6068.
7. Rouet P, Smih F, Jasin M. Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol Cell Biol. 1994;14:8096-8106.
8. Liang F, Man M, Romanienko PJ, Jasin M. Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc Natl Acad Sci U S A. 1998;95:5172-5177.
9. Moynahan ME, Jasin M. Loss of heterozygosity induced by a chromosomal double-strand break. Proc Natl Acad Sci USA. 1997;94:8988-8993.
10. Johnson RD, Jasin M. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J. 2000;19: 3398-3407.
11. Richardson C, Jasin M. Frequent chromosomal translocations induced by DNA double-strand breaks. Nature. 2000;405:697-700.
12. Richardson C, Moynahan ME, Jasin M. Doublestrand break repair by interchromosomal recombination: suppression of chromosomal translocations. Gene Dev. 1998;12:3831-3842.
13. Antonarakis P, Krawczak M, Cooper DN. The nature and mechanisms of human gene mutation: the genetic basis of human cancer. Vogelstein B, Kinzler KW, eds. New York, NY: McGraw-Hill; 2002:7-42.
14. Jeffs AR, Benjes SM, Smith TL, Sowerby SJ. Morris CM. The BCR gene recombines preferentially with Alu elements in complex BCR-ABL translocations of chronic myeloid leukaemia. Hum Mol Genet. 1998;7:767-776.
15. Ferguson DO, Sekiguchi JM, Chang S, et al. The nonhomologous end-joining pathway of DMA repair is required for genomic stability and the suppression of translocations. Proc Natl Acad Sci USA. 2000;97:6630-6633.
16. Super HJ, McCabe NR.Thirman MJ, etal. Rearrangements of the MIL gene in therapy-related acute myeloid leukemia in patients previously treated with agents targeting DNA-topoisomerase II. Blood. 1993;82:3705-3711.
17. Pedersen-Bjergaard J, Rowley JD. The balanced and the unbalanced chromosome aberrations of acute myeloid leukemia may develop in different ways and may contribute differently to malignant transformation. Blood. 1994;83:2780-2786.
18. Ernst P. Fisher JK, Avery W, Wade S, Foy D, Korsmeyer SJ. Definitive hematopoiesis requires the mixed-lineage leukemia gene. Dev Cell. 2004;6:437-443.
19. Hess JL, Yu BD, Li B, Hanson RD, Korsmeyer SJ. Defects in yolk sac hematopoiesis in mil-null embryos. Blood. 1997;90:1799-1806.
20. Yu BD, Hanson RD, Hess JL, Horning SE, Korsmeyer SJ. MLL, a mammalian trithorax-group gene, functions as a transcriptional maintenance factor in morphogenesis. Proc Natl Acad Sci USA. 1998;95:10632-10636.
21. Thirman MJ, Gill HJ, Burnett RC, et al. Rearrangement of the MLL gene in acute lymphoblastic and acute myeloid leukemias with 11q23 chromosomal translocations. N Engl J Med. 1993; 329:909-914.
22. Gu Y, Alder H, Nakamura T, et al. Sequence analysis of the breakpoint cluster region in the ALL-1 gene involved in acute leukemia. Cancer Res. 1994;54:2326-2330.
23. Ziemin-van der Poel S, McCabe NR, Gill HJ, et al. Identification of a gene MLL, that spans the breakpoint in 11q23 translocations associated with human leukemias. Proc Natl Acad Sci USA. 1991;88:10735-10739.
24. Seeker-Walker L. General report on the European Union Concerted Action Workshop on 11q23, London, UK, May 1997. Leukemia. 1998;12:776-778.
25. Felix CA, Walker AH, Lange BJ, et al. Association of CYP3A4 genotype with treatment-related leukemia. Proc Natl Acad Sci U S A. 1998;95:13176-13181.
26. Maraschin J, Dutrillaux B, Aurias A. Chromosome aberrations induced by etoposide (VP-16) are not random. Int J Cancer. 1990;46:808-812.
27. Ratain MJ, Rowley JD. Therapy-related acute myeloid leukemia secondary to inhibitors of topoisomerase II: from the bedside to the target genes. Ann Oncol. 1992;3:107-111.
28. Domer PH, Head DR, Renganathan N, Raimondi SC, Yang E, Atlas M. Molecular analysis of 13 cases of MLL/11q23 secondary acute leukemia and identification of topoisomerase II consensus-binding sequences near the chromosomal break-point of a secondary leukemia with the t(4;11). Leukemia. 1995;9:1305-1312.
29. Spitzner J, Muller M. A consensus sequence for cleavage by vertebrate DMA topoisomerase II. Nucleic Acids Res. 1988;16:5533-5556.
30. Aplan PD, Chervinsky DS, Stanulla M, Burhans WC. Site-specific DMA cleavage within the MLL breakpoint cluster region induced by topoisomerase II inhibitors. Blood. 1996;87:2649-2658.
31. Strissel PL, Strick R, Rowley JD, Zeleznik-Le NJ. An in vivo topoisomerase II cleavage site and a DNase I hypersensitive site colocalize nearexon 9 in the MLL breakpoint cluster region. Blood. 1998;92:3793-3803.
32. Whitmarsh RJ, Saginario C, Zhuo Y, et al. Reciprocal DMA topoisomerase II cleavage events at 5'-TATTA-3' sequences in MLL and AF-9 create homologous single-stranded overhangs that anneal to form der(11) and der(9) genomic breakpoint junctions in treatment-related AML without further processing. Oncogene. 2003;22:8448-8459.
33. Lovett BD, Lo Nigro L. Rappaport EF. et al. Nearprecise interchromosomal recombination and functional DMA topoisomerase II cleavage sites at MLL and AF-4 genomic breakpoints in treatment-related acute lymphoblastic leukemia with t(4:11) translocation. Proc Natl Acad Sci U S A. 2001;98: 9802-9807.
34. Lovett BD, Strumberg D. Blair IA, et al. Etoposide metabolites enhance DNA topoisomerase II cleavage near leukemia-associated MLL translocation breakpoints. Biochemistry. 2001;40:1159-1170.
35. + cell model for drug-induced and native DMA topoisomerase II cleavage of MLL in treatment-related leukemia [abstract]. Blood. 2003; 102:845a.
36. Stanulla M, Wang J, Chervinsky DS, Thandla S, Aplan PD. DNA cleavage within the MLL breakpoint cluster region is a specific event which occurs as part of higher-order chromatm fragmentation during the initial stages of apoptosis. Mol Cell Biol. 1997;17:4070-4079.
37. Ishii E, Eguchi M, Eguchi-Lshimae M, et al. In vitro cleavage of the MLL gene by topoisomerase II inhibitor (etoposide) in normal cord and peripheral blood mononuclear cells. Int J Hematol. 2002;76:74-79.
38. Betti CJ, Villalobos MJ, Diaz MO, Vaughan AT. Apoptotic triggers initiate translocations within the MLL gene involving the nonhomologous end joining repair system. Cancer Res. 2001;61:4550-4555.
39. Betti CJ, Villalobos MJ, Diaz MO, Vaughan AT. Apoptotic stimuli initiate MLL-AF9 translocations that are transcribed in cells capable of division. Cancer Res. 2003;63:1377-1381.
40. Ploski J, Aplan PD. Characterization of DNA fragmentation events caused by genotoxic and non-genotoxic agents. Mut Research. 2001;473:169-180.
41. Vaughan AT, Betti CJ, Villalobos JM. Surviving apoptosis. Apoptosis. 2002;7:173-177.
42. Bonnet D, Dick J. Human acute myeloid leukemia is organized as a hierarchy that originates from primitive hematopoietic cell. Nat Med. 1997;3: 730-737.
43. Bernard OA, Berger R. Molecular basis of 11q23 rearrangements in hematopoietic malignant proliferations. Genes Chromosomes Cancer. 1995; 13:75-85.
44. Reichel M, Gillert E, Angermuller S, et al. Biased distribution of chromosomal breakpoints involving the MLL gene in infants versus children and adults with t(4,11) ALL. Oncogene. 2001;20: 2900-2907.
45. Rowley JD, Oiney HJ. International workshop on the relationship of prior therapy to balanced chromosome aberrations in therapy-related myelodysplastic syndromes and acute leukemia: overview report. Genes Chromosomes Cancer. 2002; 33:331-345.
46. Langer T, Metzler M, Reinhardt D, et al. Analysis of t(9;11) chromosomal breakpoint sequences in childhood acute leukemia', almost identical MLL breakpoints in therapy-related AML after treatment without etoposides. Genes Chromosomes Cancer. 2003;36:393-401.
47. Megonigal MD, Rappaport EF, Wilson RB, et al. Panhandle PCR for cDNA: a rapid method for isolation of MLL fusion transcripts involving unknown partner genes. Proc Natl Acad Sci U S A. 2000;97:9597-9602.
48. Raffini LJ, Slater DJ, Rappaport EF, et al. Panhandle and reverse-panhandle PCR enable cloning of der(11) and der(other) genomic breakpoint junctions of MLL translocations and identify complex translocation of MLL, AF-4, and CDK6. Proc Natl Acad Sci USA. 2002;99:4568-4573.
49. Eguchi M, Eguchi-Lshimae M, Seto M, et al. GPHN, a novel partner gene fused to MLL in a leukemia with t(11;14)(q23;q24). Genes Chromosomes Cancer. 2001;32:212-221.
50. Lewis I, Almeida-Porada G, Du J, et al. Umbilical cord blood cells capable of engrafting in primary, secondary and tertiary xenogeneic hosts are preserved after ex vivo culture in a noncontact system. Blood. 2001;97:3441-3449.
51. Hardman J, Limbird L, Goodman Oilman A. Pharmacological Basis of Therapeutics. 10th ed. New York, NY: Mc-Graw Hill; 2001.
52. Blanco J, Edick J, Relling MV. Etoposide induces chimeric MLL gene fusions. FASEB J. 2003;18: 173-180.
53. Lin F-L, Sperle K, Sternberg N. Model for homologous recombination during transfer of DNA into mouse L cells: role for DNA ends in the recombination process. Mol Cell Biol. 1984;4:1020-1034.
54. Strout MP, Marcucci G, Bloomfield CD, Caligiuri MA. The partial tandem duplication of ALL1 (MIL) is consistently generated by Alu-mediated homologous recombination in acute myeloid leukemia. Proc Natl Acad Sci U S A. 1998;95:2390-2395.
55. Schnittger S, Kinkelin U, Schoch C, et al. Screening for MLL tandem duplication in 387 unselected patients with AMI identify a prognostically unfavorable subset of AML Leukemia. 2000;14:796-804.
56. Pegram LD, Megonigal MD, Lange BJ, et al. t(3;11) translocation in treatment-related acute myeloid leukemia fuses MLL with the GMPS (GUANOSINE 5' MONOPHOSPHATE SYNTHETASE) gene. Blood. 2000;96:4360-4362.
57. Hillion J, Le Coniat M, Jonveaux P, Berger R, Bernard OA. AF6q21, a novel partner of the MLL gene in t(6;11)(q21;q23), defines a forkhead transcriptional factor subfamily. Blood. 1997;90:3714-3719.
58. Strehl S, Borkhardt A, Slany R, Fuchs DE, Konig M, Haas O. The human LASP1 gene is fused to MLL in an acute myeloid leukemia with 1(11:17) (q23:q21). Oncogene. 2001;22:157-160.
59. Ono R, Taki T, Taketani T, et al. SEPTIN6, a human homologue to mouse Septin6, is fused to MLL in infant acute myeloid leukemia with complex chromosomal abnormalities involving 11q23 and Xq24. Cancer Res. 2002;62:333-337.
60. Felix CA, Megonigal MD, Chervinsky DS, et al. Association of germline p53 mutation with MLL segmental jumping translocation m treatment-related leukemia. Blood. 1998;91:4451-4456.
61. Slater DJ, Hilgenfeld E, Rappaport EF, et al. MLL-SEPTIN6 fusion recurs in novel translocation of chromosomes 3, X, and 11 in infant acute myelomonocytic leukaemia and in t(X;11) in infant acute myeloid leukaemia, and MLL genomic breakpoint in complex MLL-SEPTIN6 rearrangement is a DNA topoisomerase II cleavage site. Oncogene. 2002;21:4706-4714.
62. Calabrese G, Fantasia D, Morizio E, et al. Chromosome 11 rearrangements and specific MLL amplification revealed by spectral karyotyping in a patient with refractory anaemia with excess of blasts (RAEB). Br J Haematol. 2003;122:760-763.
63. Pantelias GE, Maillie HD. Direct analysis of radiation-induced chromosome fragments and rings in unstimulated human peripheral blood lymphocytes by means of the premature chromosome condensation technique. Mutat Res. 1985;149: 67-72.
64. Cornforth MN, Bedford JS. Ionizing radiation damage and its early development in chromosomes. Adv Rad Biol. 1993;17:423-496.
65. Dimartino JF, Cleary ML. Mil rearrangements in haematological malignancies: lessons from clinical and biological studies. Br J Haematol. 1999; 106:614-626.
66. Megonigal MD, Rappaport EF, Jones DH, et al. Panhandle PCR strategy to amplify MLL genomic breakpoints in treatment-related leukemias. Proc Natl Acad Sci U S A. 1997;94:11583-11588.
67. Eguchi-Lshimae M. Eguchi M, Ishii E, et al. Breakage and fusion of the TEL (ETV6) gene in immature B lymphocytes induced by apoptogenic signals. Blood. 2001;97:737-743.
68. Whitman SP, Strout MP, Marcucci G, et al. The partial nontandem duplication of the MLL (ALL1) gene is a novel rearrangement that generates three distinct fusion transcripts in B-cell acute lymphoblastic leukemia. Cancer Res. 2001;61: 59-63.
69. Schichman SA, Caligiuri MA, Strout MP, et al. ALL-1 tandem duplication in acute myeloid leukemia with a normal karyotype involves homologous recombination between Alu elements. Cancer Res. 1994;54:4277-4280.
70. Richardson C, Jasin M. Coupled homologous and nonhomologous repair of a double-strand break preserves genomic integrity in mammalian cells. Mol Cell Biol. 2000;20:9068-9075.
71. Boehden G, Restle A, Marschalek R, Stocking C, Wiesmuller L Recombination at chromosomal sequences involved in leukemogenic rearrangements is differentially regulated by p53. Carcinogenesis. 2004;25:1305-1313.
72. van Gent DC, Hoeijmakers JH, Kanaar R. Chromosomal stability and the DNA double-stranded break connection. Nat Rev Genet. 2001;2:196-206.
73. Stark JM, Hu P, Pierce AJ, Moynahan ME, Ellis N, Jasin M. ATP hydrolysis by mammalian RAD51 has a key role during homology-directed DNA repair. J Biol Chem. 2002;277:20185-20194.
74. Baumann P, Benson FE, West SC. Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell. 1996;87:757-766.
75. Ivanov EL, Sugawara N, Fishman-Lobell J, Haber JE. Genetic requirements for the single-strand annealing pathway of double-strand break repair in Saccharomyces cerevisiae. Genetics. 1996; 142:693-704.
76. Xia SJ, Shammas MA, Shmookler Reis RJ. Elevated recombination in immortal human cells is mediated by HsRAD51 recombinase. Mol Cell Biol. 1997;17:7151-7158.
77. Richardson C, Stark J, Ommundsen M, Jasin M. Rad51 over-expression promotes aberrant double-strand break repair pathways and genome instability. Oncogene. 2004;23:546-553.
78. Flygare J, Falt S, Ottervald J, et al. Effects of HsRad51 overexpression on cell proliferation, cell cycle progression, and apoptosis. Exp Cell Res. 2001;268:61-69.
79. Lambert S, Lopez BS. Characterization of mammalian RAD51 double strand break repair using non-lethal dominant-negative forms. EMBO J. 2000;19:3090-3099.
80. Raderschall E, Stout K, Freier S, Suckow V, Schweiger S, Haaf T. Elevated levels of Rad51 recombination protein in tumor cells. Cancer Res. 2002;62:219-225.
81. Wang ZM, Chen ZP, Xu ZY, et al. In vitro evidence for homologous recombinational repair in resistance to melphalan. J Natl Cancer Inst. 2001;93:1473-1478.
82. Bello VE, Aloyz RS, Christodoulopoulos G, Panascl LC. Homologous recombinational repair vis-a-vis chlorambucil resistance in chronic lymphocytic leukemia. Biochem Pharmacol. 2002;63: 1585-1588.
83. Hansen LT, Lundin C, Spang-Thomsen M, Petersen LN, Helleday T. The role of RAD51 in etoposide (VP16) resistance in small cell lung cancer. Int J Cancer. 2003;105:472-479.