Etoposide and illegitimate DNA double-strand break repair in the generation of MLL translocations: New insights and new questions

DNA Repair

Volumn 5, Issue 9-10, 2006, Pages 1109-1118

  Sung, P A ^a   Libura, J ^a   Richardson, C ^a,b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b University of North Carolina at Charlotte   (United States)

Author keywords

11q23 rearrangements; AML; DSB; Etoposide; MLL; Recombination; Therapy related leukemia; Translocation

Indexed keywords

ALKYLATING AGENT; ANTHRAQUINONE DERIVATIVE; ANTINEOPLASTIC AGENT; BIMOLANE; BIOFLAVONOID; DAUNORUBICIN; DOUBLE STRANDED DNA; DOXORUBICIN; EPIRUBICIN; ETOPOSIDE; LAXATIVE; MITOXANTRONE; MIXED LINEAGE LEUKEMIA PROTEIN; PESTICIDE; PLATINUM DERIVATIVE; PODOPHYLLIN; RAZOXANE; TENIPOSIDE;

ARTICLE; BREAST CANCER; CANCER CHEMOTHERAPY; CARCINOGENESIS; CHROMOSOME TRANSLOCATION; DNA REPAIR; DNA STRAND BREAKAGE; GENE DELETION; GENE DUPLICATION; GENE EXPRESSION; GENE LOCUS; GENE REARRANGEMENT; GENE SEQUENCE; GENETIC RECOMBINATION; GENOTOXICITY; HEMATOPOIESIS; HOMOLOGOUS RECOMBINATION; HUMAN; LARYNX CANCER; LEUKEMIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; SEQUENCE ANALYSIS;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; CHROMOSOME BREAKAGE; CHROMOSOMES, HUMAN, PAIR 11; DNA DAMAGE; DNA REPAIR; DNA TOPOISOMERASES, TYPE II; ETOPOSIDE; HUMANS; LEUKEMIA, MYELOCYTIC, ACUTE; LEUKEMIA, MYELOID, ACUTE; MODELS, GENETIC; MYELOID-LYMPHOID LEUKEMIA PROTEIN; SENSITIVITY AND SPECIFICITY; TOPOISOMERASE II INHIBITORS;

EID: 33747882412     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2006.05.018     Document Type: Article

References (94)

1. Elliott B., and Jasin M. Double-strand breaks and translocations in cancer. Cell. Mol. Life Sci. 59 (2002) 373-385
2. van Gent D.C., Hoeijmakers J.H., and Kanaar R. Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2 (2001) 196-206
3. Felix C.A. Leukemias related to treatment with DNA topoisomerase II inhibitors. Med. Pediatr. Oncol. 36 (2001) 525-535
4. Lightfoot T.J., and Roman E. Causes of childhood leukaemia and lymphoma. Toxicol. Appl. Pharmacol. 199 (2004) 104-117
5. Ross J.A. Maternal diet and infant leukemia: a role for DNA topoisomerase II inhibitors?. Int. J. Cancer Suppl. 11 (1998) 26-28
6. Ross J.A., Potter J.D., Reaman G.H., Pendergrass T.W., and Robison L.L. Maternal exposure to potential inhibitors of DNA topoisomerase II and infant leukemia (United States): a report from the Children's Cancer Group. Cancer Causes Control 7 (1996) 581-590
7. Spector L.G., Xie Y., Robison L.L., Heerema N.A., Hilden J.M., Lange B., Felix C.A., Davies S.M., Slavin J., Potter J.D., Blair C.K., Reaman G.H., and Ross J.A. Maternal diet and infant leukemia: the DNA topoisomerase II inhibitor hypothesis: a report from the children's oncology group. Cancer Epidemiol. Biomarkers Prev. 14 (2005) 651-655
8. Alexander F.E., Patheal S.L., Biondi A., Brandalise S., Cabrera M.E., Chan L.C., Chen Z., Cimino G., Cordoba J.C., Gu L.J., Hussein H., Ishii E., Kamel A.M., Labra S., Magalhaes I.Q., Mizutani S., Petridou E., de Oliveira M.P., Yuen P., Wiemels J.L., and Greaves M.F. Transplacental chemical exposure and risk of infant leukemia with MLL gene fusion. Cancer Res. 61 (2001) 2542-2546
9. Strick R., Strissel P.L., Borgers S., Smith S.L., and Rowley J.D. Dietary bioflavonoids induce cleavage in the MLL gene and may contribute to infant leukemia. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 4790-4795
10. Wiemels J.L., Cazzaniga G., Daniotti M., Eden O.B., Addison G.M., Masera G., Saha V., Biondi A., and Greaves M.F. Prenatal origin of acute lymphoblastic leukaemia in children. Lancet 354 (1999) 1499-1503
11. Wiemels J.L., Xiao Z., Buffler P.A., Maia A.T., Ma X., Dicks B.M., Smith M.T., Zhang L., Feusner J., Wiencke J., Pritchard-Jones K., Kempski H., and Greaves M. In utero origin of t(8; 21) AML1-ETO translocations in childhood acute myeloid leukemia. Blood 99 (2002) 3801-3805
12. Gu Y., Alder H., Nakamura T., Schichman S.A., Prasad R., Canaani O., Saito H., Croce C.M., and Canaani E. Sequence analysis of the breakpoint cluster region in the ALL-1 gene involved in acute leukemia. Cancer Res. 54 (1994) 2326-2330
13. Bernard O.A., and Berger R. Molecular basis of 11q23 rearrangements in hematopoietic malignant proliferations. Genes Chromosomes Cancer 13 (1995) 75-85
14. Daser A., and Rabbitts T.H. The versatile mixed lineage leukaemia gene MLL and its many associations in leukaemogenesis. Semin. Cancer Biol. 15 (2005) 175-188
15. Broeker P.L., Super H.G., Thirman M.J., Pomykala H., Yonebayashi Y., Tanabe S., Zeleznik-Le N., and Rowley J.D. Distribution of 11q23 breakpoints within the MLL breakpoint cluster region in de novo acute leukemia and in treatment-related acute myeloid leukemia: correlation with scaffold attachment regions and topoisomerase II consensus binding sites. Blood 87 (1996) 1912-1922
16. Domer P.H., Head D.R., Renganathan N., Raimondi S.C., Yang E., and Atlas M. Molecular analysis of 13 cases of MLL/11q23 secondary acute leukemia and identification of topoisomerase II consensus-binding sequences near the chromosomal breakpoint of a secondary leukemia with the t(4; 11). Leukemia 9 (1995) 1305-1312
17. Edelmann L., Spiteri E., Koren K., Pulijaal V., Bialer M.G., Shanske A., Goldberg R., and Morrow B.E. AT-rich palindromes mediate the constitutional t(11; 22) translocation. Am. J. Hum. Genet. 68 (2001) 1-13
18. Negrini M., Felix C.A., Martin C., Lange B.J., Nakamura T., Canaani E., and Croce C.M. Potential topoisomerase II DNA-binding sites at the breakpoints of a t(9; 11) chromosome translocation in acute myeloid leukemia. Cancer Res. 53 (1993) 4489-4492
19. Schichman S.A., Caligiuri M.A., Gu Y., Strout M.P., Canaani E., Bloomfield C.D., and Croce C.M. ALL-1 partial duplication in acute leukemia. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 6236-6239
20. Schichman S.A., Caligiuri M.A., Strout M.P., Carter S.L., Gu Y., Canaani E., Bloomfield C.D., and Croce C.M. ALL-1 tandem duplication in acute myeloid leukemia with a normal karyotype involves homologous recombination between Alu elements. Cancer Res. 54 (1994) 4277-4280
21. Sperry A.O., Blasquez V.C., and Garrard W.T. Dysfunction of chromosomal loop attachment sites: illegitimate recombination linked to matrix association regions and topoisomerase II. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 5497-5501
22. Stanulla M., Wang J., Chervinsky D.S., Thandla S., and Aplan P.D. DNA cleavage within the MLL breakpoint cluster region is a specific event which occurs as part of higher-order chromatin fragmentation during the initial stages of apoptosis. Mol. Cell. Biol. 17 (1997) 4070-4079
23. Strissel P.L., Strick R., Rowley J.D., and Zeleznik-Le N.J. An in vivo topoisomerase II cleavage site and a DNase I hypersensitive site colocalize near exon 9 in the MLL breakpoint cluster region. Blood 92 (1998) 3793-3803
24. Dong S., Geng J.P., Tong J.H., Wu Y., Cai J.R., Sun G.L., Chen S.R., Wang Z.Y., Larsen C.J., Berger R., et al. Breakpoint clusters of the PML gene in acute promyelocytic leukemia: primary structure of the reciprocal products of the PML-RARA gene in a patient with t(15; 17). Genes Chromosomes Cancer 6 (1993) 133-139
25. Mistry A.R., Felix C.A., Whitmarsh R.J., Mason A., Reiter A., Cassinat B., Parry A., Walz C., Wiemels J.L., Segal M.R., Ades L., Blair I.A., Osheroff N., Peniket A.J., Lafage-Pochitaloff M., Cross N.C., Chomienne C., Solomon E., Fenaux P., and Grimwade D. DNA topoisomerase II in therapy-related acute promyelocytic leukemia. N. Engl. J. Med. 352 (2005) 1529-1538
26. Chissoe S.L., Bodenteich A., Wang Y.F., Wang Y.P., Burian D., Clifton S.W., Crabtree J., Freeman A., Iyer K., Jian L., et al. Sequence and analysis of the human ABL gene, the BCR gene, and regions involved in the Philadelphia chromosomal translocation. Genomics 27 (1995) 67-82
27. Jeffs A.R., Benjes S.M., Smith T.L., Sowerby S.J., and Morris C.M. The BCR gene recombines preferentially with Alu elements in complex BCR-ABL translocations of chronic myeloid leukaemia. Hum. Mol. Genet. 7 (1998) 767-776
28. Jeffs A.R., Wells E., and Morris C.M. Nonrandom distribution of interspersed repeat elements in the BCR and ABL1 genes and its relation to breakpoint cluster regions. Genes Chromosomes Cancer 32 (2001) 144-154
29. Zucman-Rossi J., Legoix P., Victor J.M., Lopez B., and Thomas G. Chromosome translocation based on illegitimate recombination in human tumors. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 11786-11791
30. Elliott B., Richardson C., and Jasin M. Chromosomal translocation mechanisms at intronic alu elements in mammalian cells. Mol. Cell 17 (2005) 885-894
31. Richardson C., and Jasin M. Frequent chromosomal translocations induced by DNA double-strand breaks. Nature 405 (2000) 697-700
32. Richardson C., Stark J., Ommundsen M., and Jasin M. Rad51 over-expression promotes aberrant double-strand break repair pathways and genome instability. Oncogene 23 (2004) 546-553
33. Weinstock D.M., Elliott B., and Jasin M. A model of oncogenic rearrangements: differences between chromosomal translocation mechanisms and simple double-strand break repair. Blood 107 (2006) 777-780
34. Osheroff N., Corbett A., and Robinson M. Mechanism of action of topoisomerase II-targeted antineoplastic drugs. Adv. Pharmacol. 29B (1994) 105-126
35. Clifford B., Beljin M., Stark G.R., and Taylor W.R. G2 arrest in response to topoisomerase II inhibitors: the role of p53. Cancer Res. 63 (2003) 4074-4081
36. Pedersen-Bjergaard J., and Philip P. Two different classes of therapy-related and de-novo acute myeloid leukemia?. Cancer Genet. Cytogenet. 55 (1991) 119-124
37. Pedersen-Bjergaard J., and Rowley J.D. The balanced and the unbalanced chromosome aberrations of acute myeloid leukemia may develop in different ways and may contribute differently to malignant transformation. Blood 83 (1994) 2780-2786
38. Philpott N.J., Elebute M.O., Powles R., Treleaven J.G., Gore M., Dainton M.G., Min T., Swansbury G.J., and Catovsky D. Platinum agents and secondary myeloid leukaemia: two cases treated only with platinum-based drugs. Br. J. Haematol. 93 (1996) 884-887
39. Felix C.A. Secondary leukemias induced by topoisomerase-targeted drugs. Biochim. Biophys. Acta 1400 (1998) 233-255
40. Super H.J., McCabe N.R., Thirman M.J., Larson R.A., Le Beau M.M., Pedersen-Bjergaard J., Philip P., Diaz M.O., and Rowley J.D. Rearrangements of the MLL gene in therapy-related acute myeloid leukemia in patients previously treated with agents targeting DNA-topoisomerase II. Blood 82 (1993) 3705-3711
41. Ratain M.J., and Rowley J.D. Therapy-related acute myeloid leukemia secondary to inhibitors of topoisomerase II: from the bedside to the target genes. Ann. Oncol. 3 (1992) 107-111
42. Heyn R., Khan F., Ensign L.G., Donaldson S.S., Ruymann F., Smith M.A., Vietti T., and Maurer H.M. Acute myeloid leukemia in patients treated for rhabdomyosarcoma with cyclophosphamide and low-dose etoposide on Intergroup Rhabdomyosarcoma Study III: an interim report. Med. Pediatr. Oncol. 23 (1994) 99-106
43. Chaudhary U.B., and Haldas J.R. Long-term complications of chemotherapy for germ cell tumours. Drugs 63 (2003) 1565-1577
44. Kollmannsberger C., Beyer J., Droz J.P., Harstrick A., Hartmann J.T., Biron P., Flechon A., Schoffski P., Kuczyk M., Schmoll H.J., Kanz L., and Bokemeyer C. Secondary leukemia following high cumulative doses of etoposide in patients treated for advanced germ cell tumors. J. Clin. Oncol. 16 (1998) 3386-3391
45. Kollmannsberger C., Hartmann J.T., Kanz L., and Bokemeyer C. Therapy-related malignancies following treatment of germ cell cancer. Int. J. Cancer 83 (1999) 860-863
46. Nichols G., de Castro K., Wei L.X., Griffin M., Lin N., Oratzi A., Murty V.V., Troxel A., Vahdat L., and Hesdorffer C. Therapy-related myelodysplastic syndrome after autologous stem cell transplantation for breast cancer. Leukemia 16 (2002) 1673-1679
47. Nowrousian M.R., Waschke S., Bojko P., Welt A., Schuett P., Ebeling P., Flasshove M., Moritz T., Schuette J., and Seeber S. Impact of chemotherapy regimen and hematopoietic growth factor on mobilization and collection of peripheral blood stem cells in cancer patients. Ann. Oncol. 14 Suppl. 1 (2003) i29-i36
48. Pectasides D., Skarlos D., Dimopoulos A.M., Farmakis D., Pectasides M., Fountzilas G., and Aravantinos G. Two cycles of carboplatin-based adjuvant chemotherapy for high-risk clinical stage I and stage IM non-seminomatous germ cell tumours of the testis: a HECOG trial. Anticancer Res. 23 (2003) 4239-4244
49. Smith R.E., Bryant J., DeCillis A., and Anderson S. Acute myeloid leukemia and myelodysplastic syndrome after doxorubicin-cyclophosphamide adjuvant therapy for operable breast cancer: the National Surgical Adjuvant Breast and Bowel Project Experience. J. Clin. Oncol. 21 (2003) 1195-1204
50. Tallman M.S., Gray R., Robert N.J., LeMaistre C.F., Osborne C.K., Vaughan W.P., Gradishar W.J., Pisansky T.M., Fetting J., Paietta E., and Lazarus H.M. Conventional adjuvant chemotherapy with or without high-dose chemotherapy and autologous stem-cell transplantation in high-risk breast cancer. N. Engl. J. Med. 349 (2003) 17-26
51. Weldon C.B., Jaffe B.M., and Kahn M.J. Therapy-induced leukemias and myelodysplastic syndromes after breast cancer treatment: an underemphasized clinical problem. Ann. Surg. Oncol. 9 (2002) 738-744
52. Aplan P.D., Chervinsky D.S., Stanulla M., and Burhans W.C. Site-specific DNA cleavage within the MLL breakpoint cluster region induced by topoisomerase II inhibitors. Blood 87 (1996) 2649-2658
53. Lovett B.D., Lo Nigro L., Rappaport E.F., Blair I.A., Osheroff N., Zheng N., Megonigal M.D., Williams W.R., Nowell P.C., and Felix C.A. Near-precise interchromosomal recombination and functional DNA 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. 98 (2001) 9802-9807
54. Lovett B.D., Strumberg D., Blair I.A., Pang S., Burden D.A., Megonigal M.D., Rappaport E.F., Rebbeck T.R., Osheroff N., Pommier Y.G., and Felix C.A. Etoposide metabolites enhance DNA topoisomerase II cleavage near leukemia-associated MLL translocation breakpoints. Biochemistry 40 (2001) 1159-1170
55. Whitmarsh R.J., Saginario C., Zhuo Y., Hilgenfeld E., Rappaport E.F., Megonigal M.D., Carroll M., Liu M., Osheroff N., Cheung N.K., Slater D.J., Ried T., Knutsen T., Blair I.A., and Felix C.A. Reciprocal DNA 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 22 (2003) 8448-8459
56. Ng A., Taylor G.M., and Eden O.B. Genotoxicity of etoposide: greater susceptibility of MLL than other target genes. Cancer Genet. Cytogenet. 164 (2006) 164-167
57. Saginario C., Whitmarsh R.J., Raffini L.J., and CA F. Human CD34+ model for drug-induced and native DNA topoisomerasell cleavage of MLL in treatment related leukemia. Blood (2003) 845A
58. Stanulla M., Chhalliyil P., Wang J., Jani-Sait S.N., and Aplan P.D. Mechanisms of MLL gene rearrangement: site-specific DNA cleavage within the breakpoint cluster region is independent of chromosomal context. Hum. Mol. Genet. 10 (2001) 2481-2491
59. Adachi Y., Kas E., and Laemmli U.K. Preferential, cooperative binding of DNA topoisomerase II to scaffold-associated regions. Embo J. 8 (1989) 3997-4006
60. Kas E., Poljak L., Adachi Y., and Laemmli U.K. A model for chromatin opening: stimulation of topoisomerase II and restriction enzyme cleavage of chromatin by distamycin. Embo J. 12 (1993) 115-126
61. Stanulla M., Wang J., Chervinsky D.S., and Aplan P.D. Topoisomerase II inhibitors induce DNA double-strand breaks at a specific site within the AML1 locus. Leukemia 11 (1997) 490-496
62. Betti C.J., Villalobos M.J., Diaz M.O., and Vaughan A.T. Apoptotic triggers initiate translocations within the MLL gene involving the nonhomologous end joining repair system. Cancer Res. 61 (2001) 4550-4555
63. Betti C.J., Villalobos M.J., Diaz M.O., and Vaughan A.T. Apoptotic stimuli initiate MLL-AF9 translocations that are transcribed in cells capable of division. Cancer Res. 63 (2003) 1377-1381
64. Ploski J.E., and Aplan P.D. Characterization of DNA fragmentation events caused by genotoxic and non-genotoxic agents. Mutat. Res. 473 (2001) 169-180
65. Vaughan A.T., Betti C.J., and Villalobos M.J. Surviving apoptosis. Apoptosis 7 (2002) 173-177
66. Blanco J.G., Edick M.J., and Relling M.V. Etoposide induces chimeric Mil gene fusions. FASEB J. 18 (2004) 173-175
67. Libura J., Slater D.J., Felix C.A., and Richardson C. Therapy-related acute myeloid leukemia-like MLL rearrangements are induced by etoposide in primary human CD34+ cells and remain stable after clonal expansion. Blood 105 (2005) 2124-2131
68. Megonigal M.D., Rappaport E.F., Wilson R.B., Jones D.H., Whitlock J.A., Ortega J.A., Slater D.J., Nowell P.C., and Felix C.A. Panhandle PCR for cDNA: a rapid method for isolation of MLL fusion transcripts involving unknown partner genes. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 9597-9602
69. Meyer C., Schneider B., Reichel M., Angermueller S., Strehl S., Schnittger S., Schoch C., Jansen M.W., van Dongen J.J., Pieters R., Haas O.A., Dingermann T., Klingebiel T., and Marschalek R. Diagnostic tool for the identification of MLL rearrangements including unknown partner genes. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 449-454
70. Raffini L.J., Slater D.J., Rappaport E.F., Lo Nigro L., Cheung N.K., Biegel J.A., Nowell P.C., Lange B.J., and Felix C.A. 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. U.S.A. 99 (2002) 4568-4573
71. Reichel M., Gilert E., Nilson I., Siegler G., Greil J., Fey G.H., and Marschalek R. Fine structure of translocations breakpoints in leukemic blasts with chromosomal translocation t(4; 11): the DNA damage-repair model of translocation. Oncogene 17 (1998) 3035-3044
72. Libura J., Ward M., Przybylski G., and Richardson C. Etoposide-initiated MLL rearrangments detected at high frequency in human primitive hematopoietic stem cells with in vitro and in vivo long-term repopulating potential. Blood (2005)
73. Hardman J., Limbird L., and Goodman A. Gilman Pharmacolgical Basis of Therapeutics (2001), Mc-Graw Hill
74. Richardson C., and Jasin M. Coupled homologous and nonhomologous repair of a double-strand break preserves genomic integrity in mammalian cells. Mol. Cell. Biol. 20 (2000) 9068-9075
75. Strout M.P., Marcucci G., Bloomfield C.D., and Caligiuri M.A. The partial tandem duplication of ALL1 (MLL) is consistently generated by Alu-mediated homologous recombination in acute myeloid leukemia. Proc. Natl. Acad. Sci. 95 (1998) 2390-2395
76. Maraschin J., Dutrillaux B., and Aurias A. Chromosome aberrations induced by etoposide (VP-16) are not random. Int. J. Cancer 46 (1990) 808-812
77. Martensson S., Nygren J., Osheroff N., and Hammarsten O. Activation of the DNA-dependent protein kinase by drug-induced and radiation-induced DNA strand breaks. Radiat. Res. 160 (2003) 291-301
78. Richardson C. RAD51, genomic stability, and tumorigenesis. Cancer Lett. 218 (2005) 127-139
79. Slupianek A., Schmutte C., Tombline G., Nieborowska-Skorska M., Hoser G., Nowicki M.O., Pierce A.J., Fishel R., and Skorski T. BCR/ABL regulates mammalian RecA homologs, resulting in drug resistance. Mol. Cell 8 (2001) 795-806
80. Pierce A.J., Hu P., Han M., Ellis N., and Jasin M. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 15 (2001) 3237-3242
81. Pierce A.J., and Jasin M. NHEJ deficiency and disease. Mol. Cell 8 (2001) 1160-1161
82. Gillert E., Leis T., Repp R., Reichel M., Hosch A., Breitenlohner I., Angermuller S., Borkhardt A., Harbott J., Lampert F., Griesinger F., Greil J., Fey G.H., and Marschalek R. A DNA damage repair mechanism is involved in the origin of chromosomal translocations (4; 11) in primary leukemic cells. Oncogene 18 (1999) 4663-4671
83. Onno M., Nakamura T., Hillova J., and Hill M. Rearrangement of the human tre oncogene by homologous recombination between Alu repeats of nucleotide sequences from two different chromosomes. Oncogene 7 (1992) 2519-2523
84. Antonarkis P., Krawczak M., and Cooper D.N. The nature and mechanisms of human gene mutation. In: Vogelstein B., and Kinsler K. (Eds). The Genetic Basis of Human Cancer (2002), Mc-Graw Hill, New York 7-42
85. Collis S.J., Schwaninger J.M., Ntambi A.J., Keller T.W., Nelson W.G., Dillehay L.E., and Deweese T.L. Evasion of early cellular response mechanisms following low level radiation-induced DNA damage. J. Biol. Chem. 279 (2004) 49624-49632
86. Pellicciari C., Bottone M.G., Schaack V., Manfredi A.A., and Barni S. Etoposide at different concentrations may open different apoptotic pathways in thymocytes. Eur. J. Histochem. 40 (1996) 289-298
87. Skov K., Zhou H., and Marples B. The effect of two topoisomerase inhibitors on low-dose hypersensitivity and increased radioresistance in Chinese hamster V79 cells. Radiat. Res. 138 (1994) S117-S120
88. Nakada S., Katsuki Y., Imoto I., Yokoyama T., Nagasawa M., Inazawa J., and Mizutani S. Early G2/M checkpoint failure as a molecular mechanism underlying etoposide-induced chromosomal aberrations. J. Clin. Invest. 116 (2006) 80-89
89. Moneypenny C.G., Shao J., Song Y., and Gallagher E.P. MLL rearrangements are induced by low doses of etoposide in human fetal hematopoietic stem cells. Carcinogenesis (2005)
90. Oguchi K., Takagi M., Tsuchida R., Taya Y., Ito E., Isoyama K., Ishii E., Zannini L., Delia D., and Mizutani S. Missense mutation and defective function of ATM in a childhood acute leukemia patient with MLL gene rearrangement. Blood 101 (2003) 3622-3627
91. Codrington R., Pannell R., Forster A., Drynan L.F., Daser A., Lobato N., Metzler M., and Rabbitts T.H. The Ews-ERG fusion protein can initiate neoplasia from lineage-committed haematopoietic cells. PLoS Biol. 3 (2005) e242
92. Richardson C., Moynahan M.E., and Jasin M. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 12 (1998) 3831-3842
93. Ng A., Taylor G.M., Wynn R.F., and Eden O.B. Effects of topoisomerase 2 inhibitors on the MLL gene in children receiving chemotherapy: a prospective study. Leukemia 19 (2005) 253-259
94. Ayene I.S., Ford L.P., and Koch C.J. Ku protein targeting by Ku70 small interfering RNA enhances human cancer cell response to topoisomerase II inhibitor and gamma radiation. Mol. Cancer Ther. 4 (2005) 529-536