Molecular genetics of B-precursor acute lymphoblastic leukemia

Journal of Clinical Investigation

Volumn 122, Issue 10, 2012, Pages 3407-3415

  Mullighan, Charles G ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BCR ABL PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; CYTOKINE RECEPTOR; CYTOKINE RECEPTOR LIKE FACTOR 2; IMATINIB; IMMUNOGLOBULIN HEAVY CHAIN; JANUS KINASE; JANUS KINASE 2; MIXED LINEAGE LEUKEMIA PROTEIN; STAT PROTEIN; TRANSCRIPTION FACTOR 7 LIKE 1; TRANSCRIPTION FACTOR ETV6; TRANSCRIPTION FACTOR PAX5; TRANSCRIPTION FACTOR RUNX1; UNCLASSIFIED DRUG;

ACUTE LYMPHOBLASTIC LEUKEMIA; ADD ON THERAPY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BONE MARROW CELL; CANCER CHEMOTHERAPY; CANCER PATIENT; CANCER PROGNOSIS; CHROMOSOME; CHROMOSOME 21; CHROMOSOME TRANSLOCATION; CLINICAL TRIAL (TOPIC); CYTOGENETICS; DIMERIZATION; EVENT FREE SURVIVAL; FLUORESCENCE IN SITU HYBRIDIZATION; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FREQUENCY; GENE OVEREXPRESSION; GENE REARRANGEMENT; GENE SEQUENCE; GENETIC VARIABILITY; HEMATOPOIESIS; HUMAN; INTRACHROMOSOMAL AMPLIFICATION OF CHROMOSOME 21; LEUKEMIA RELAPSE; LYMPHOID CELL; MOLECULAR GENETICS; NONHUMAN; PHILADELPHIA CHROMOSOME POSITIVE CELL; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN PROTEIN INTERACTION; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION; TREATMENT RESPONSE;

ADULT; ANIMALS; B-LYMPHOCYTES; CELL LINEAGE; CHILD; CLONE CELLS; GENE EXPRESSION PROFILING; GENETIC PREDISPOSITION TO DISEASE; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MICE, KNOCKOUT; NEOPLASM PROTEINS; ONCOGENE PROTEINS, FUSION; PRECURSOR B-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROGNOSIS; RISK; TRANSLOCATION, GENETIC;

EID: 84867145464     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI61203     Document Type: Review

References (125)

1. Pui CH, Robison LL, Look AT. Acute lymphoblastic leukaemia. Lancet. 2008;371(9617):1030-1043. (Pubitemid 351389536)
2. Harrison CJ. Cytogenetics of paediatric and adolescent acute lymphoblastic leukaemia. Br J Haematol. 2009;144(2):147-156.
3. Harrison CJ, Foroni L. Cytogenetics and molecular genetics of acute lymphoblastic leukemia. Rev Clin Exp Hematol. 2002;6(2):91-113.
4. Nachman JB, et al. Outcome of treatment in children with hypodiploid acute lymphoblastic leukemia. Blood. 2007;110(4):1112-1115. (Pubitemid 47281405)
5. Shurtleff SA, et al. TEL/AML1 fusion resulting from a cryptic t(12;21) is the most common genetic lesion in pediatric ALL and defines a subgroup of patients with an excellent prognosis. Leukemia. 1995;9(12):1985-1989. (Pubitemid 26023779)
6. Bohlander SK. ETV6: a versatile player in leukemogenesis. Semin Cancer Biol. 2005;15(3):162-174.
7. Okuda T, van Deursen J, 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(2):321-330. (Pubitemid 26042836)
8. Song WJ, et al. Haploinsufficiency of CBFA2 causes familial thrombocytopenia with propensity to develop acute myelogenous leukaemia. Nat Genet. 1999;23(2):166-175.
9. Roumier C, Fenaux P, Lafage M, Imbert M, Eclache V, Preudhomme C. New mechanisms of AML1 gene alteration in hematological malignancies. Leukemia. 2003;17(1):9-16. (Pubitemid 36175882)
10. Zhang J, et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature. 2012;481(7380):157-163.
11. Wang LC, Kuo F, Fujiwara Y, Gilliland DG, Golub TR, Orkin SH. Yolk sac angiogenic defect and intraembryonic apoptosis in mice lacking the Ets-related factor TEL. EMBO J. 1997;16(14):4374-4383. (Pubitemid 27298190)
12. Hiebert SW, et al. The t(12;21) translocation converts AML-1B from an activator to a repressor of transcription. Mol Cell Biol. 1996;16(4):1349-1355. (Pubitemid 26095605)
13. Torrano V, Procter J, Cardus P, Greaves M, Ford AM. ETV6-RUNX1 promotes survival of early B lineage progenitor cells via a dysregulated erythropoietin receptor. Blood. 2011;118(18):4910-4918.
14. Andreasson P, Schwaller J, Anastasiadou E, Aster J, Gilliland DG. The expression of ETV6/CBFA2 (TEL/AML1) is not sufficient for the transformation of hematopoietic cell lines in vitro or the induction of hematologic disease in vivo. Cancer Genet Cytogenet. 2001;130(2):93-104. (Pubitemid 33033225)
15. Morrow M, Horton S, Kioussis D, Brady HJ, Williams O. TEL-AML1 promotes development of specific hematopoietic lineages consistent with preleukemic activity. Blood. 2004;103(10):3890-3896. (Pubitemid 38596310)
16. Wiemels JL, et al. Prenatal origin of acute lymphoblastic leukaemia in children. Lancet. 1999; 354(9189):1499-1503. (Pubitemid 29502102)
17. Mullighan CG, et al. Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature. 2007;446(7137):758-764. (Pubitemid 46582031)
18. Parker H, et al. The complex genomic profile of ETV6-RUNX1 positive acute lymphoblastic leukemia highlights a recurrent deletion of TBL1XR1. Genes Chromosomes Cancer. 2008;47(12):1118-1125.
19. Kuiper RP, et al. High-resolution genomic profiling of childhood ALL reveals novel recurrent genetic lesions affecting pathways involved in lymphocyte differentiation and cell cycle progression. Leukemia. 2007;21(6):1258-1266. (Pubitemid 46831815)
20. Bateman CM, et al. Acquisition of genome-wide copy number alterations in monozygotic twins with acute lymphoblastic leukemia. Blood. 2010;115(17):3553- 3558.
21. Hunger SP. Chromosomal translocations involving the E2A gene in acute lymphoblastic leukemia: clinical features and molecular pathogenesis. Blood. 1996;87(4):1211-1224. (Pubitemid 26056883)
22. Zhuang Y, Soriano P, Weintraub H. The helix-loop-helix gene E2A is required for B cell formation. Cell. 1994;79(5):875-884. (Pubitemid 24371977)
23. Bain G, et al. E2A deficiency leads to abnormalities in alphabeta T-cell development and to rapid development of T-cell lymphomas. Mol Cell Biol. 1997;17(8):4782-4791. (Pubitemid 27318153)
24. Sanyal M, et al. B-cell development fails in the absence of the Pbx1 proto-oncogene. Blood. 2007;109(10):4191-4199. (Pubitemid 46743383)
25. Lu Q, Kamps MP. Heterodimerization of Hox proteins with Pbx1 and oncoprotein E2a-Pbx1 generates unique DNA-binding specifities at nucleotides predicted to contact the N-terminal arm of the Hox homeodomain--demonstration of Hox-dependent targeting of E2a-Pbx1 in vivo. Oncogene. 1997;14(1):75-83. (Pubitemid 27042957)
26. Inaba T, et al. Fusion of the leucine zipper gene HLF to the E2A gene in human acute B-lineage leukemia. Science. 1992;257(5069):531-534.
27. de Boer J, et al. The E2A-HLF oncogenic fusion protein acts through Lmo2 and Bcl-2 to immortalize hematopoietic progenitors. Leukemia. 2011;25(2):321-330.
28. Heltemes-Harris LM, et al. Ebf1 or Pax5 haploinsufficiency synergizes with STAT5 activation to initiate acute lymphoblastic leukemia. J Exp Med. 2011;208(6):1135-1149.
29. Ribeiro RC, Abromowitch M, Raimondi SC, Murphy SB, Behm F, Williams DL. Clinical and biologic hallmarks of the Philadelphia chromosome in childhood acute lymphoblastic leukemia. Blood. 1987;70(4):948-953. (Pubitemid 18022366)
30. Melo JV. The diversity of BCR-ABL fusion proteins and their relationship to leukemia phenotype. Blood. 1996;88(7):2375-2384. (Pubitemid 26327486)
31. Van Etten RA. Studying the pathogenesis of BCR-ABL+ leukemia in mice. Oncogene. 2002;21(56):8643-8651. (Pubitemid 36084196)
32. Duy C, et al. BCL6 enables Ph+ acute lymphoblastic leukaemia cells to survive BCR-ABL1 kinase inhibition. Nature. 2011;473(7347):384-388.
33. Mullighan CG, et al. BCR-ABL1 lymphoblastic leukaemia is characterized by the deletion of Ikaros. Nature. 2008;453(7191):110-114. (Pubitemid 351630327)
34. Iacobucci I, et al. Identification and molecular characterization of recurrent genomic deletions on 7p12 in the IKZF1 gene in a large cohort of BCR-ABL1-positive acute lymphoblastic leukemia patients: on behalf of Gruppo Italiano Malattie Ematologiche dell'Adulto Acute Leukemia Working Party (GIMEMA AL WP). Blood. 2009;114(10):2159-2167.
35. Georgopoulos K, et al. The Ikaros gene is required for the development of all lymphoid lineages. Cell. 1994;79(1):143-156. (Pubitemid 24309520)
36. Molnar A, Georgopoulos K. The Ikaros gene encodes a family of functionally diverse zinc finger DNA-binding proteins. Mol Cell Biol. 1994;14(12):8292-8303.
37. Virely C, et al. Haploinsufficiency of the IKZF1 (IKAROS) tumor suppressor gene cooperates with BCR-ABL in a transgenic model of acute lymphoblastic leukemia. Leukemia. 2010;24(6):1200-1204.
38. Crist W, et al. Philadelphia chromosome positive childhood acute lymphoblastic leukemia: clinical and cytogenetic characteristics and treatment outcome. A Pediatric Oncology Group study. Blood. 1990;76(3):489-494. (Pubitemid 20251814)
39. Arico M, et al. Clinical outcome of children with newly diagnosed Philadelphia chromosome-positive acute lymphoblastic leukemia treated between 1995 and 2005. J Clin Oncol. 2010;28(31):4755-4761.
40. Druker BJ, et al. Activity of a specific inhibitor of the BCR-ABL tyrosine kinase in the blast crisis of chronic myeloid leukemia and acute lymphoblastic leukemia with the Philadelphia chromosome. N Engl J Med. 2001;344(14):1038-1042. (Pubitemid 32267973)
41. Druker BJ, et al. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med. 2001;344(14):1031-1037. (Pubitemid 32267972)
42. Schultz KR, et al. Improved early event-free survival with imatinib in Philadelphia chromosomepositive acute lymphoblastic leukemia: a children's oncology group study. J Clin Oncol. 2009;27(31):5175-5181.
43. Pfeifer H, et al. Prevalence and dynamics of bcr-abl kinase domain mutations during imatinib treatment differ in patients with newly diagnosed and recurrent bcr-abl positive acute lymphoblastic leukemia. Leukemia. 2012;26(7):1475-1481.
44. Chen CS, et al. Molecular rearrangements on chromosome 11q23 predominate in infant acute lymphoblastic leukemia and are associated with specific biologic variables and poor outcome. Blood. 1993;81(9):2386-2393.
45. Pui CH, et al. 11q23/MLL rearrangement confers a poor prognosis in infants with acute lymphoblastic leukemia. J Clin Oncol. 1994;12(5):909-915.
46. Pui CH, Kane JR, Crist WM. Biology and treatment of infant leukemias. Leukemia. 1995;9(5):762-769.
47. Pui CH, et al. Secondary acute myeloid leukemia in children treated for acute lymphoid leukemia. N Engl J Med. 1989;321(3):136-142. (Pubitemid 19180676)
48. Chessels JM, Swansbury GJ, Reeves B, Bailey CC, Richards SM. Cytogenetics and prognosis in childhood lymphoblastic leukaemia: results of MRC UKALL X. Medical Research Council Working Party in Childhood Leukaemia. Br J Haematol. 1997;99(1):93-100. (Pubitemid 27461333)
49. Moorman AV, et al. Karyotype is an independent prognostic factor in adult acute lymphoblastic leukemia (ALL): analysis of cytogenetic data from patients treated on the Medical Research Council (MRC) UKALLXII/Eastern Cooperative Oncology Group (ECOG) 2993 trial. Blood. 2007;109(8):3189-3197. (Pubitemid 46572503)
50. Meyer C, et al. The MLL recombinome of acute leukemias. Leukemia. 2006;20(5):777-784.
51. Chessells JM, et al. Clinical features, cytogenetics and outcome in acute lymphoblastic and myeloid leukaemia of infancy: report from the MRC Childhood Leukaemia working party. Leukemia. 2002;16(5):776-784. (Pubitemid 34537548)
52. Moorman AV, et al. No prognostic effect of additional chromosomal abnormalities in children with acute lymphoblastic leukemia and 11q23 abnormalities. Leukemia. 2005;19(4):557-563. (Pubitemid 40521160)
53. Ziemin-van der Poel S, McCabe NR, Gill HJ, Espinosa R. Identification of a gene, MLL, that spans the breakpoint in 11q23 translocations associated with human leukemias. Proc Natl Acad Sci U S A. 1991;88(23):10735-10739. (Pubitemid 21915912)
54. Milne TA, et al. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol Cell. 2002;10(5):1107-1117. (Pubitemid 35453828)
55. Bardini M, et al. DNA copy-number abnormalities do not occur in infant ALL with t(4;11)/MLL-AF4. Leukemia. 2010;24(1):169-176.
56. Andersson AK, et al. Whole genome sequence analysis of 22 MLL rearranged infant acute lymphoblastic leukemias reveals remarkably few somatic mutations: a report from the St. Jude Children's Research Hospital - Washington University Pediatric Cancer Genome Project. ASH Annual Meeting Abstracts. 2011;118:69.
57. Armstrong SA, et al. MLL translocations specify a distinct gene expression profile that distinguishes a unique leukemia. Nat Genet. 2002;30(1):41-47.
58. Faber J, et al. HOXA9 is required for survival in human MLL-rearranged acute leukemias. Blood. 2009;113(11):2375-2385.
59. Armstrong SA, et al. Inhibition of FLT3 in MLL. Validation of a therapeutic target identified by gene expression based classification. Cancer Cell. 2003;3(2):173-183. (Pubitemid 37443389)
60. Stubbs MC, et al. MLL-AF9 and FLT3 cooperation in acute myelogenous leukemia: development of a model for rapid therapeutic assessment. Leukemia. 2008;22(1):66-77.
61. Stumpel DJ, et al. Specific promoter methylation identifies different subgroups of MLL-rearranged infant acute lymphoblastic leukemia, influences clinical outcome, and provides therapeutic options. Blood. 2009;114(27):5490- 5498.
62. Stumpel DJ, et al. Hypermethylation of specific microRNA genes in MLL-rearranged infant acute lymphoblastic leukemia: major matters at a micro scale. Leukemia. 2011;25(3):429-439.
63. Krivtsov AV, et al. H3K79 methylation profiles define murine and human MLL-AF4 leukemias. Cancer Cell. 2008;14(5):355-368.
64. Yan L, et al. Clinical, immunophenotypic, cytogenetic, and molecular genetic features in 117 adult patients with mixed-phenotype acute leukemia defined by WHO-2008 classification [published online ahead of print May 11, 2012]. Haematologica. doi:10.3324/haematol.2012.064485.
65. Jo SY, Granowicz EM, Maillard I, Thomas D, Hess JL. Requirement for Dot1l in murine postnatal hematopoiesis and leukemogenesis by MLL translocation. Blood. 2011;117(18):4759-4768.
66. Daigle SR, et al. Selective killing of mixed lineage leukemia cells by a potent small-molecule DOT1L inhibitor. Cancer Cell. 2011;20(1):53-65.
67. Schafer E, et al. Promoter hypermethylation in MLL-r infant acute lymphoblastic leukemia: biology and therapeutic targeting. Blood. 2010;115(23):4798-4809.
68. Milani L, et al. DNA methylation for subtype classification and prediction of treatment outcome in patients with childhood acute lymphoblastic leukemia. Blood. 2010;115(6):1214-1225.
69. Dyer MJ, et al. Immunoglobulin heavy chain (IGH) locus chromosomal translocations in B-cell precursor acute lymphoblastic leukemia (BCP-ALL): rare clinical curios or potent genetic drivers? Blood. 2010;115(8):1490-1499.
70. Klapproth K, Wirth T. Advances in the understanding of MYC-induced lymphomagenesis. Br J Haematol. 2010;149(4):484-497.
71. Russell LJ, et al. Deregulated expression of cytokine receptor gene, CRLF2, is involved in lymphoid transformation in B-cell precursor acute lymphoblastic leukemia. Blood. 2009;114(13):2688-2698.
72. Mullighan CG, et al. Rearrangement of CRLF2 in B-progenitor- and Down syndrome-associated acute lymphoblastic leukemia. Nat Genet. 2009;41(11):1243-1246.
73. Yoda A, et al. Functional screening identifies CRLF2 in precursor B-cell acute lymphoblastic leukemia. Proc Natl Acad Sci U S A. 2010;107(1):252-257.
74. Harvey RC, et al. Rearrangement of CRLF2 is associated with mutation of JAK kinases, alteration of IKZF1, Hispanic/Latino ethnicity, and a poor outcome in pediatric B-progenitor acute lymphoblastic leukemia. Blood. 2010;115(26):5312-5321.
75. Hertzberg L, et al. Down syndrome acute lymphoblastic leukemia: a highly heterogeneous disease in which aberrant expression of CRLF2 is associated with mutated JAK2: a report from the iBFM Study Group. Blood. 2010;115(5):1006-1017.
76. Bercovich D, et al. Mutations of JAK2 in acute lymphoblastic leukaemias associated with Down's syndrome. Lancet. 2008;372(9648):1484-1492.
77. Mullighan CG, et al. JAK mutations in high-risk childhood acute lymphoblastic leukemia. Proc Natl Acad Sci U S A. 2009;106(23):9414-9418.
78. Cario G, et al. Presence of the P2RY8-CRLF2 rearrangement is associated with a poor prognosis in non-high-risk precursor B-cell acute lymphoblastic leukemia in children treated according to the ALLBFM 2000 protocol. Blood. 2010;115(26):5393-5397.
79. Shochat C, et al. Gain-of-function mutations in interleukin-7 receptor-alpha (IL7R) in childhood acute lymphoblastic leukemias. J Exp Med. 2011;208(5):901-908.
80. Zenatti PP, et al. Oncogenic IL7R gain-of-function mutations in childhood T-cell acute lymphoblastic leukemia. Nat Genet. 2011;43(10):932-939.
81. Mullighan CG, et al. Deletion of IKZF1 and prognosis in acute lymphoblastic leukemia. N Engl J Med. 2009;360(5):470-480.
82. Den Boer ML, et al. A subtype of childhood acute lymphoblastic leukaemia with poor treatment outcome: a genome-wide classification study. Lancet Oncol. 2009;10(2):125-134.
83. Loh ML, et al. A BCR-ABL1-like gene expression profile confers a poor prognosis in patients with high-risk acute lymphoblastic leukemia (HR-ALL): a report from Children's Oncology Group (COG) AALL0232. ASH Annual Meeting Abstracts. 2011;118:743.
84. Roberts KG, et al. Genetic alterations activating kinase and cytokine receptor signaling in high rish acute lymphoblastic leukemia. Cancer Cell. 2012;22(2):153-166.
85. Harewood L, et al. Amplification of AML1 on a duplicated chromosome 21 in acute lymphoblastic leukemia: a study of 20 cases. Leukemia. 2003;17(3):547-553. (Pubitemid 36395648)
86. Robinson HM, Harrison CJ, Moorman AV, Chudoba I, Strefford JC. Intrachromosomal amplification of chromosome 21 (iAMP21) may arise from a breakage-fusion-bridge cycle. Genes Chromosomes Cancer. 2007;46(4):318-326.
87. Inukai T, et al. Clinical significance of early T-cell precursor acute lymphoblastic leukaemia: results of the Tokyo Children's Cancer Study Group Study L99-15. Br J Haematol. 2012;156(3):358-365.
88. Attarbaschi A, et al. Minimal residual disease values discriminate between low and high relapse risk in children with B-cell precursor acute lymphoblastic leukemia and an intrachromosomal amplification of chromosome 21: the Austrian and German acute lymphoblastic leukemia Berlin-Frankfurt-Munster (ALL-BFM) trials. J Clin Oncol. 2008;26(18):3046-3050.
89. Harrison CJ, et al. Three distinct subgroups of hypodiploidy in acute lymphoblastic leukaemia. Br J Haematol. 2004;125(5):552-559. (Pubitemid 38747956)
90. Holmfeldt L, et al. Genome-wide analysis of genetic alterations in hypodiploid acute lymphoblastic leukemia identifies a high frequency of mutations targeting the IKAROS gene family and Ras signaling. ASH Annual Meeting Abstracts. 2010;116:411.
91. Mullighan CG. Single nucleotide polymorphism microarray analysis of genetic alterations in cancer. Methods Mol Biol. 2011;730:235-258.
92. Yeoh EJ, et al. Classification, subtype discovery, and prediction of outcome in pediatric acute lymphoblastic leukemia by gene expression profiling. Cancer Cell. 2002;1(2):133-143.
93. Bousquet M, et al. A novel PAX5-ELN fusion protein identified in B-cell acute lymphoblastic leukemia acts as a dominant negative on wild-type PAX5. Blood. 2007;109(8):3417-3423. (Pubitemid 46572531)
94. Nebral K, et al. Incidence and diversity of PAX5 fusion genes in childhood acute lymphoblastic leukemia. Leukemia. 2009;23(1):134-143.
95. Iacobucci I, et al. The PAX5 gene is frequently rearranged in BCR-ABL1-positive acute lymphoblastic leukemia but is not associated with outcome. A report on behalf of the GIMEMA Acute Leukemia Working Party. Haematologica. 2010;95(10):1683-1690.
96. Kuiper RP, et al. IKZF1 deletions predict relapse in uniformly treated pediatric precursor B-ALL. Leukemia. 2010;24(7):1258-1264.
97. Kawamata N, et al. Molecular allelokaryotyping of pediatric acute lymphoblastic leukemias by high-resolution single nucleotide polymorphism oligonucleotide genomic microarray. Blood. 2008;111(2):776-784.
98. Yamamoto T, et al. PTPN11, RAS and FLT3 mutations in childhood acute lymphoblastic leukemia. Leuk Res. 2006;30(9):1085-1089. (Pubitemid 44037090)
99. Paulsson K, et al. Mutations of FLT3, NRAS, KRAS, and PTPN11 are frequent and possibly mutually exclusive in high hyperdiploid childhood acute lymphoblastic leukemia. Genes Chromosomes Cancer. 2008;47(1):26-33. (Pubitemid 350191461)
100. Zhang J, et al. Key pathways are frequently mutated in high-risk childhood acute lymphoblastic leukemia: a report from the Children's Oncology Group. Blood. 2011;118(11):3080-3087.
101. Raimondi SC, Pui CH, Head DR, Rivera GK, Behm FG. Cytogenetically different leukemic clones at relapse of childhood acute lymphoblastic leukemia. Blood. 1993;82(2):576-580. (Pubitemid 23206124)
102. Maloney KW, McGavran L, Odom LF, Hunger SP. Acquisition of p16(INK4A) and p15(INK4B) gene abnormalities between initial diagnosis and relapse in children with acute lymphoblastic leukemia. Blood. 1999;93(7):2380-2385. (Pubitemid 29153642)
103. Irving JA, Minto L, Bailey S, Hall AG. Loss of heterozygosity and somatic mutations of the glucocorticoid receptor gene are rarely found at relapse in pediatric acute lymphoblastic leukemia but may occur in a subpopulation early in the disease course. Cancer Res. 2005;65(21):9712-9718. (Pubitemid 41541447)
104. Mullighan CG, et al. Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science. 2008;322(5906):1377-1380. (Pubitemid 352775249)
105. Yang JJ, et al. Genome-wide copy number profiling reveals molecular evolution from diagnosis to relapse in childhood acute lymphoblastic leukemia. Blood. 2008;112(10):4178-4183.
106. van Delft FW, et al. Clonal origins of relapse in ETV6-RUNX1 acute lymphoblastic leukemia. Blood. 2011;117(23):6247-6254.
107. Kawamata N, et al. Molecular allelokaryotyping of relapsed pediatric acute lymphoblastic leukemia. Int J Oncol. 2009;34(6):1603-1612.
108. Kuster L, et al. ETV6/RUNX1-positive relapses evolve from an ancestral clone and frequently acquire deletions of genes implicated in glucocorticoid signaling. Blood. 2011;117(9):2658-2667.
109. Szczepanski T, et al. Late recurrence of childhood T-cell acute lymphoblastic leukemia frequently represents a second leukemia rather than a relapse: first evidence for genetic predisposition. J Clin Oncol. 2011;29(12):1643-1649.
110. Notta F, et al. Evolution of human BCR-ABL1 lymphoblastic leukaemia-initiating cells. Nature. 2011;469(7330):362-367.
111. Anderson K, et al. Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature. 2011;469(7330):356-361.
112. Mullighan CG, et al. CREBBP mutations in relapsed acute lymphoblastic leukaemia. Nature. 2011;471(7337):235-239.
113. Goodman RH, Smolik S. CBP/p300 in cell growth, transformation, and development. Genes Dev . 2000;14(13):1553-1577. (Pubitemid 30460905)
114. Inthal A, et al. CREBBP HAT domain mutations prevail in relapse cases of high hyperdiploid childhood acute lymphoblastic leukemia [published online ahead of print March 5, 2012]. Leukemia. doi:10.1038/leu.2012.60.
115. Pasqualucci L, et al. Inactivating mutations of acetyltransferase genes in B-cell lymphoma. Nature. 2011;471(7337):189-195.
116. Hof J, et al. Mutations and deletions of the TP53 gene predict nonresponse to treatment and poor outcome in first relapse of childhood acute lymphoblastic leukemia. J Clin Oncol. 2011;29(23):3185-3193.
117. Koppen IJ, Hermans FJ, Kaspers GJ. Folate related gene polymorphisms and susceptibility to develop childhood acute lymphoblastic leukaemia. Br J Haematol. 2010;148(1):3-14.
118. Trevino LR, et al. Germline genomic variants associated with childhood acute lymphoblastic leukemia. Nat Genet. 2009;41(9):1001-1005.
119. Papaemmanuil E, et al. Loci on 7p12.2, 10q21.2 and 14q11.2 are associated with risk of childhood acute lymphoblastic leukemia. Nat Genet. 2009;41(9):1006-1010.
120. Lahoud MH, et al. Gene targeting of Desrt, a novel ARID class DNA-binding protein, causes growth retardation and abnormal development of reproductive organs. Genome Res. 2001;11(8):1327-1334. (Pubitemid 32771539)
121. Pui CH, et al. Treating childhood acute lymphoblastic leukemia without cranial irradiation. N Engl J Med. 2009;360(26):2730-2741.
122. Pui CH, et al. Results of therapy for acute lymphoblastic leukemia in black and white children. JAMA. 2003;290(15):2001-2007. (Pubitemid 37430582)
123. Jeha S, et al. Increased risk for CNS relapse in pre-B cell leukemia with the t(1;19)/TCF3-PBX1. Leukemia. 2009;23(8):1406-1409.
124. Mullighan CG, et al. ERG deletions define a novel subtype of B-progenitor acute lymphoblastic leukemia. ASH Annual Meeting Abstracts. 2007;110:691.
125. Martinelli G, et al. IKZF1 (Ikaros) deletions in BCR-ABL1-positive acute lymphoblastic leukemia are associated with short disease-free survival and high rate of cumulative incidence of relapse: a GIMEMA AL WP report. J Clin Oncol. 2009;27(31):5202-5207.