Genome-wide profiling of genetic alterations in acute lymphoblastic leukemia: Recent insights and future directions

Leukemia

Volumn 23, Issue 7, 2009, Pages 1209-1218

  Mullighan, C G ^a   Downing, J R ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYCLIN DEPENDENT KINASE INHIBITOR 2B; GENOMIC DNA; IKAROS TRANSCRIPTION FACTOR; MIXED LINEAGE LEUKEMIA PROTEIN; RAG1 PROTEIN; TRANSCRIPTION FACTOR ETV6; TRANSCRIPTION FACTOR PAX5; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR TAL1;

ACUTE LYMPHOBLASTIC LEUKEMIA; B LYMPHOCYTE DIFFERENTIATION; BACTERIAL ARTIFICIAL CHROMOSOME; CANCER CLASSIFICATION; CANCER DIAGNOSIS; CANCER GENETICS; CARCINOGENESIS; CELL MATURATION; DNA HYBRIDIZATION; DNA MICROARRAY; GENE INTERACTION; GENE MUTATION; GENE NUMBER; GENETIC EPIGENESIS; GENETIC REGULATION; GENETIC RISK; GENOME ANALYSIS; HETEROZYGOSITY LOSS; HIGH RISK PATIENT; HUMAN; LEUKEMIA RELAPSE; MOLECULAR GENETICS; NUCLEOTIDE BINDING SITE; PRE B LYMPHOCYTE; PRE T LYMPHOCYTE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN DNA BINDING; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; UNIPARENTAL DISOMY;

EID: 67650882506     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2009.18     Document Type: Review

References (113)

1. Pui CH, Robison LL, Look AT. Acute lymphoblastic leukaemia. Lancet 2008; 371: 1030-1043.
2. Pui CH, Sandlund JT, Pei D, Campana D, Rivera GK, Ribeiro RC et al Improved outcome for children with acute lymphoblastic leukemia: results of Total Therapy Study XIIIB at St Jude Children's Research Hospital. Blood 2004; 104: 2690-2696.
3. Rowe JM, Buck G, Burnett AK, Chopra R, Wiernik PH, Richards SM et al Induction therapy for adults with acute lymphoblastic leukemia: results of more than 1500 patients from the international ALL trial: MRC UKALL XII/ECOG E2993. Blood 2005; 106: 3760-3767.
4. Gleissner B, Gokbuget N, Bartram CR, Janssen B, Rieder H, Janssen JW et al. Leading prognostic relevance of the BCR-ABL translocation in adult acute B-lineage lymphoblastic leukemia: A prospective study of the German Multicenter Trial Group and confirmed polymerase chain reaction analysis. Blood 2002; 99: 1536-1543.
5. Fielding AK, Richards SM, Chopra R, Lazarus HM, Litzow MR, Buck G et al. Outcome of 609 adults after relapse of acute lymphoblastic leukemia (ALL); an MRC UKALL12/ECOG 2993 study. Blood 2007; 109 944-950.
6. Einsiedel HG, von Stackelberg A, Hartmann R, Fengler R, Schrappe M, Janka-Schaub G et al. Long-term outcome in children with relapsed ALL by risk-stratified salvage therapy: Results of trial acute lymphoblastic leukemia-relapse study of the Berlin-Frankfurt-Munster Group 87. J Clin Oncol 2005; 23: 7942-7950.
7. Rivera GK, Zhou Y, Hancock ML, Gajjar A, Rubnitz J, Ribeiro RC et al Bone marrow recurrence after initial intensive treatment for childhood acute lymphoblastic leukemia. Cancer 2005; 103: 368-376.
8. Harrison CJ, Foroni L. Cytogenetics and molecular genetics of acute lymphoblastic leukemia. Rev Clin Exp Hematol 2002; 6: 91-113.
9. Pui CH, Relling MV, Downing JR. Acute lymphoblastic leukemia. N Engl J Med 2004; 350: 1535-1548.
10. Raimondi SC. Cytogenetics of acute leukemias. In: Pui CH (ed). Childhood Leukemias, 2nd edn. Cambridge University Press: Cambridge, 2006, pp 235-271.
11. Graux C, Cools J, Michaux L, Vandenberghe P, Hagemeijer A. Cytogenetics and molecular genetics of T-cell acute lymphoblastic leukemia: From thymocyte to lymphoblast. Leukemia 2006; 20: 1496-1510.
12. Harrison CJ. Cytogenetics of paediatric and adolescent acute lymphoblastic leukaemia. Br J Haematol 2009; 144: 147-156.
13. 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: 93-104.
14. Williams RT, Roussel MF, Sherr CJ. Arf gene loss enhances oncogenicity and limits imatinib response in mouse models of Bcr-Abl-induced acute lymphoblastic leukemia. Proc Natl Acad Sci USA 2006; 103: 6688-6693.
15. Hebert J, Cayuela JM, Berkeley J, Sigaux F. Candidate tumor-suppressor genes MTS1 (p16INK4A) and MTS2 (p15INK4B) display frequent homozygous deletions in primary cells from Tbut not from B-cell lineage acute lymphoblastic leukemias. Blood 1994; 84: 4038-4044.
16. Ogawa S, Hangaishi A, Miyawaki S, Hirosawa S, Miura Y, Takeyama K et al. Loss of the cyclin-dependent kinase 4-inhibitor (p16; MTS1) gene is frequent in and highly specific to lymphoid tumors in primary human hematopoietic malignancies. Blood 1995; 86: 1548-1556.
17. Okuda T, Shurtleff SA, Valentine MB, Raimondi SC, Head DR, Behm F et al. Frequent deletion of p16INK4a/MTS1 and p15INK4b/MTS2 in pediatric acute lymphoblastic leukemia. Blood 1995; 85: 2321-2330.
18. Weng AP, Ferrando AA, Lee W, Morris JPt, Silverman LB, Sanchez-Irizarry C et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 2004; 306: 269-271.
19. Davies JJ, Wilson IM, Lam WL. Array CGH technologies and their applications to cancer genomes. Chromosome Res 2005; 13: 237-248.
20. Wang Y, Armstrong SA. Genome-wide SNP analysis in cancer: Leukemia shows the way. Cancer Cell 2007; 11: 308-309.
21. Pinkel D, Albertson DG. Comparative genomic hybridization. Annu Rev Genomics Hum Genet 2005; 6: 331-354.
22. Larramendy ML, Huhta T, Heinonen K, Vettenranta K, Mahlamaki E, Riikonen P et al. DNA copy number changes in childhood acute lymphoblastic leukemia. Haematologica 1998; 83: 890-895.
23. Larramendy ML, Huhta T, Vettenranta K, El-Rifai W, Lundin J, Pakkala S et al. Comparative genomic hybridization in childhood acute lymphoblastic leukemia. Leukemia 1998; 12: 1638-1644.
24. Huhta T, Vettenranta K, Heinonen K, Kanerva J, Larramendy ML, Mahlamaki E et al. Comparative genomic hybridization and conventional cytogenetic analyses in childhood acute myeloid leukemia. Leuk Lymphoma 1999; 35: 311-315.
25. Schoumans J, Johansson B, Corcoran M, Kuchinskaya E, Golovleva I, Grander D et al. Characterisation of dic(9;20)(p11-13;q11) in childhood B-cell precursor acute lymphoblastic leukaemia by tiling resolution array-based comparative genomic hybridisation reveals clustered breakpoints at 9p13.2 and 20q11.2. Br J Haematol 2006; 135: 492-499.
26. Strefford JC, van Delft FW, Robinson HM, Worley H, Yiannikouris O, Selzer R et al. Complex genomic alterations and gene expression in acute lymphoblastic leukemia with intrachromosomal amplification of chromosome 21. Proc Natl Acad Sci USA 2006; 103: 8167-8172.
27. van Vlierberghe P, Meijerink JP, Lee C, Ferrando AA, Look AT, van Wering ER et al. A new recurrent 9q34 duplication in pediatric T-cell acute lymphoblastic leukemia. Leukemia 2006; 20: 1245-1253.
28. Davidsson J, Andersson A, Paulsson K, Heidenblad M, Isaksson M, Borg A et al. Tiling resolution array comparative genomic hybridization, expression and methylation analyses of dup(1q) in Burkitt lymphomas and pediatric high hyperdiploid acute lymphoblastic leukemias reveal clustered near-centromeric breakpoints and overexpression of genes in 1q22-32.3. Hum Mol Genet 2007; 16: 2215-2225.
29. Kuchinskaya E, Nordgren A, Heyman M, Schoumans J, Corcoran M, Staaf J et al. Tiling-resolution array-CGH reveals the pattern of DNA copy number alterations in acute lymphoblastic leukemia with 21q amplification: The result of telomere dysfunction and breakage/fusion/ breakage cycles? Leukemia 2007; 21: 1327-1330.
30. Lundin C, Heidenblad M, Strombeck B, Borg A, Hovland R, Heim S et al Tiling resolution array CGH of dic(7;9)(p11 approximately 13;p11 approximately 13) in B-cell precursor acute lymphoblastic leukemia reveals clustered breakpoints at 7p11.2 approximately 12.1 and 9p13.1. Cytogenet Genome Res 2007; 118: 13-18.
31. Strefford JC, Worley H, Barber K, Wright S, Stewart AR, Robinson HM et al. Genome complexity in acute lymphoblastic leukemia is revealed by array-based comparative genomic hybridization. Oncogene 2007; 26: 4306-4318.
32. Jalali GR, An Q, Konn ZJ, Worley H, Wright SL, Harrison CJ et al. Disruption of ETV6 in intron 2 results in upregulatory and insertional events in childhood acute lymphoblastic leukaemia. Leukemia 2008; 22: 114-123.
33. Kuchinskaya E, Heyman M, Nordgren A, Schoumans J, Staaf J, Borg A et al. Array-CGH reveals hidden gene dose changes in children with acute lymphoblastic leukaemia and a normal or failed karyotype by G-banding. Br J Haematol 2008; 140: 572-577.
34. Rabin KR, Man TK, Yu A, Folsom MR, Zhao YJ, Rao PH et al. Clinical utility of array comparative genomic hybridization for detection of chromosomal abnormalities in pediatric acute lymphoblastic leukemia. Pediatr Blood Cancer 2008; 51: 171-177.
35. Steinemann D, Cario G, Stanulla M, Karawajew L, Tauscher M, Weigmann A et al. Copy number alterations in childhood acute lymphoblastic leukemia and their association with minimal residual disease. Genes Chromosomes Cancer 2008; 47: 471-480.
36. Hehir-Kwa JY, Egmont-Petersen M, Janssen IM, Smeets D, van Kessel AG, Veltman JA. Genome-wide copy number profiling on high-density bacterial artificial chromosomes, single-nucleotide polymorphisms, and oligonucleotide microarrays: A platform comparison based on statistical power analysis. DNA Res 2007; 14: 1-11.
37. Lo KC, Bailey D, Burkhardt T, Gardina P, Turpaz Y, Cowell JK. Comprehensive analysis of loss of heterozygosity events in glioblastoma using the 100 K SNP mapping arrays and comparison with copy number abnormalities defined by BAC array comparative genomic hybridization. Genes Chromosomes Cancer 2008; 47: 221-237.
38. Mullighan CG, Goorha S, Radtke I, Miller CB, Coustan-Smith E, Dalton JD et al. Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature 2007; 446: 758-764.
39. Xavier RJ, Rioux JD. Genome-wide association studies: A new window into immune-mediated diseases. Nat Rev Immunol 2008; 8: 631-643.
40. Matsuzaki H, Dong S, Loi H, Di X, Liu G, Hubbell E et al. Genotyping over 100 000 SNPs on a pair of oligonucleotide arrays. Nat Methods 2004; 1: 109-111.
41. Peiffer DA, Le JM, Steemers FJ, Chang W, Jenniges T, Garcia F et al High-resolution genomic profiling of chromosomal aberrations using Infinium whole-genome genotyping. Genome Res 2006; 16: 1136-1148.
42. Lilljebjorn H, Heidenblad M, Nilsson B, Lassen C, Horvat A, Heldrup J et al. Combined high-resolution array-based comparative genomic hybridization and expression profiling of ETV6/RUNX1-positive acute lymphoblastic leukemias reveal a high incidence of cryptic Xq duplications and identify several putative target genes within the commonly gained region. Leukemia 2007; 21: 2137-2144.
43. Irving JA, Bloodworth L, Bown NP, Case MC, Hogarth LA, Hall AG. Loss of heterozygosity in childhood acute lymphoblastic leukemia detected by genome-wide microarray single nucleotide polymorphism analysis. Cancer Res 2005; 65: 3053-3058.
44. Kuiper RP, Schoenmakers EF, van Reijmersdal SV, Hehir-Kwa JY, van Kessel AG, van Leeuwen FN 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: 1258-1266.
45. Mullighan CG, Miller CB, Phillips LA, Dalton JD, Ma J, Radtke I et al. BCR-ABL1 lymphoblastic leukaemia is characterized by the deletion of Ikaros. Nature 2008; 453: 110-114.
46. Kawamata N, Ogawa S, Zimmermann M, Kato M, Sanada M, Hemminki K et al Molecular allelokaryotyping of pediatric acute lymphoblastic leukemias by high-resolution single nucleotide polymorphism oligonucleotide genomic microarray. Blood 2008; 111: 776-784.
47. Kawamata N, Ogawa S, Zimmermann M, Niebuhr B, Stocking C, Sanada M et al. Cloning of genes involved in chromosomal translocations by high-resolution single nucleotide polymorphism genomic microarray. Proc Natl Acad Sci USA 2008; 105: 11921-11926.
48. Bungaro S, Dell'Orto MC, Zangrando A, Basso D, Gorletta T, Lo Nigro L et al. Integration of genomic and gene expression data of childhood ALL without known aberrations identifies subgroups with specific genetic hallmarks. Genes Chromosomes Cancer 2009; 48: 22-38.
49. Pounds SB, Cheng C, Mullighan CG, Raimondi SC, Shurtleff SA, Downing JR. Reference alignment of SNP microarray signals for copy number analysis of tumors. Bioinformatics 2009; 25: 315-321.
50. Olshen AB, Venkatraman ES, Lucito R, Wigler M. Circular binary segmentation for the analysis of array-based DNA copy number data. Biostatistics 2004; 5: 557-572.
51. Greaves MF, Wiemels J. Origins of chromosome translocations in childhood leukaemia. Nat Rev Cancer 2003; 3: 639-649.
52. Nutt SL, Heavey B, Rolink AG, Busslinger M. Commitment to the B-lymphoid lineage depends on the transcription factor Pax5. Nature 1999; 401: 556-562.
53. Nutt SL, Eberhard D, Horcher M, Rolink AG, Busslinger M. Pax5 determines the identity of B cells from the beginning to the end of B-lymphopoiesis. Int Rev Immunol 2001; 20: 65-82.
54. Busslinger M. Transcriptional control of early B cell development. Annu Rev Immunol 2004; 22: 55-79.
55. Nutt SL, Kee BL. The transcriptional regulation of B cell lineage commitment. Immunity 2007; 26: 715-725.
56. Cazzaniga G, Daniotti M, Tosi S, Giudici G, Aloisi A, Pogliani E et al. The paired box domain gene PAX5 is fused to ETV6/TEL in an acute lymphoblastic leukemia case. Cancer Res 2001; 61: 4666-4670.
57. Strehl S, Konig M, Dworzak MN, Kalwak K, Haas OA. PAX5/ETV6 fusion defines cytogenetic entity dic(9;12)(p13;p13). Leukemia 2003; 17: 1121-1123.
58. Warming S, Liu P, Suzuki T, Akagi K, Lindtner S, Pavlakis GN et al Evi3, a common retroviral integration site in murine B-cell lymphoma, encodes an EBFAZ-related Kruppel-like zinc finger protein. Blood 2003; 101: 1934-1940.
59. Bond HM, Mesuraca M, Carbone E, Bonelli P, Agosti V, Amodio N et al Early hematopoietic zinc finger protein (EHZF), the human homolog to mouse Evi3, is highly expressed in primitive human hematopoietic cells. Blood 2004; 103: 2062-2070.
60. Bohlander SK. ETV6: A versatile player in leukemogenesis. Semin Cancer Biol 2005; 15: 162-174.
61. Wlodarska I, Veyt E, De Paepe P, Vandenberghe P, Nooijen P, Theate I et al. FOXP1, a gene highly expressed in a subset of diffuse large B-cell lymphoma, is recurrently targeted by genomic aberrations. Leukemia 2005; 19: 1299-1305.
62. Hu H, Wang B, Borde M, Nardone J, Maika S, Allred L et al. Foxp1 is an essential transcriptional regulator of B cell development. Nat Immunol 2006; 7: 819-826.
63. Nebral K, Konig M, Harder L, Siebert R, Haas OA, Strehl S. Identification of PML as novel PAX5 fusion partner in childhood acute lymphoblastic leukaemia. Br J Haematol 2007; 139: 269-274.
64. Bousquet M, Broccardo C, Quelen C, Meggetto F, Kuhlein E, Delsol G 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: 3417-3423.
65. An Q, Wright SL, Konn ZJ, Matheson E, Minto L, Moorman AV et al. Variable breakpoints target PAX5 in patients with dicentric chromosomes: a model for the basis of unbalanced translocations in cancer. Proc Natl Acad Sci USA 2008; 105: 17050-17054.
66. Nebral K, Denk D, Attarbaschi A, Konig M, Mann G, Haas OA et al. Incidence and diversity of PAX5 fusion genes in childhood acute lymphoblastic leukemia. Leukemia 2009; 23: 134-143.
67. Mullighan CG, Su X, Zhang J, Radtke I, Phillips LA, Miller CB et al Deletion of IKZF1 and Prognosis in Acute Lymphoblastic Leukemia. N Engl J Med 2009; 360: 470-480.
68. Mullighan CG, Miller CB, Radtke I, Phillips LA, Dalton J, Ma J et al. BCR-ABL1 lymphoblastic leukaemia is characterized by the deletion of Ikaros. Nature 2008; 453: 110-114.
69. Hu Y, Liu Y, Pelletier S, Buchdunger E, Warmuth M, Fabbro D et al. Requirement of Src kinases Lyn, Hck and Fgr for BCR-ABL1-induced β-lymphoblastic leukemia but not chronic myeloid leukemia. Nat Genet 2004; 36: 453-461.
70. Miller CB, Mullighan CG, Su X, Ma J, Wang M, Zhang J et al. Pax5 haploinsufficiency cooperates with BCR-ABL1 to induce acute lymphoblastic leukemia [abstract]. Blood 2008; 112: P 114.
71. Urbanek P, Wang ZQ, Fetka I, Wagner EF, Busslinger M. Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP. Cell 1994; 79: 901-912.
72. Dang J, Mullighan CG, Phillips LA, Mehta P, Downing JR. Retroviral and chemical mutagenesis identifies Pax5 as a tumor suppressor in B-progenitor acute lymphoblastic leukemia [abstract]. Blood 2008; 112: 256-257.
73. Ferrando AA, Neuberg DS, Staunton J, Loh ML, Huard C, Raimondi SC et al. Gene expression signatures define novel oncogenic pathways in T cell acute lymphoblastic leukemia. Cancer Cell 2002; 1: 75-87.
74. Graux C, Cools J, Melotte C, Quentmeier H, Ferrando A, Levine R et al Fusion of NUP214 to ABL1 on amplified episomes in T-cell acute lymphoblastic leukemia. Nat Genet 2004; 36: 1084-1089.
75. Van Vlierberghe P, van Grotel M, Beverloo HB, Lee C, Helgason T, Buijs-Gladdines J et al. The cryptic chromosomal deletion del(11)(p12p13) as a new activation mechanism of LMO2 in pediatric T-cell acute lymphoblastic leukemia. Blood 2006; 108: 3520-3529.
76. Maser RS, Choudhury B, Campbell PJ, Feng B, Wong KK, Protopopov A et al. Chromosomally unstable mouse tumours have genomic alterations similar to diverse human cancers. Nature 2007; 447: 966-971.
77. Palomero T, Sulis ML, Cortina M, Real PJ, Barnes K, Ciofani M et al. Mutational loss of PTEN induces resistance to NOTCH1 inhibition in T-cell leukemia. Nat Med 2007; 13: 1203-1210.
78. O'Neil J, Grim J, Strack P, Rao S, Tibbitts D, Winter C et al. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to gamma-secretase inhibitors. J Exp Med 2007; 204 1813-1824.
79. Clappier E, Cuccuini W, Kalota A, Crinquette A, Cayuela JM, Dik WA et al. The C-MYB locus is involved in chromosomal translocation and genomic duplications in human T-cell acute leukemia (T-ALL), the translocation defining a new T-ALL subtype in very young children. Blood 2007; 110 1251-1261.
80. Lahortiga I, De Keersmaecker K, Van Vlierberghe P, Graux C, Cauwelier B, Lambert F et al. Duplication of the MYB oncogene in T cell acute lymphoblastic leukemia. Nat Genet 2007; 39: 593-595.
81. Van Vlierberghe P, van Grotel M, Tchinda J, Lee C, Beverloo HB, van der Spek PJ et al. The recurrent SET-NUP214 fusion as a new HOXA activation mechanism in pediatric T-cell acute lymphoblastic leukemia. Blood 2008; 111: 4668-4680.
82. Fugmann SD, Lee AI, Shockett PE, Villey IJ, Schatz DG. The RAG proteins and V(D)J recombination: Complexes, ends, and transposition. Annu Rev Immunol 2000; 18: 495-527.
83. Kitagawa Y, Inoue K, Sasaki S, Hayashi Y, Matsuo Y, Lieber MR et al. Prevalent involvement of illegitimate V(D)J recombination in chromosome 9p21 deletions in lymphoid leukemia. J Biol Chem 2002; 277: 46289-46297.
84. Raghavan M, Smith LL, Lillington DM, Chaplin T, Kakkas I, Molloy G et al. Segmental uniparental disomy is a commonly acquired genetic event in relapsed acute myeloid leukemia. Blood 2008; 112: 814-821.
85. Mullighan CG, Radtke I, Ma J, Shurtleff SA, Downing JR. High-resolution SNP array profiling of relapsed acute leukemia identifies genomic abnormalities distinct from those present at diagnosis [abstract]. Blood 2007; 110: 234.
86. Beroukhim R, Lin M, Park Y, Hao K, Zhao X, Garraway LA et al. Inferring loss-of-heterozygosity from unpaired tumors using highdensity oligonucleotide SNP arrays. PLoS Comput Biol 2006; 2: E41.
87. Goldman JM, Melo JV. Chronic myeloid leukemia - advances in biology and new approaches to treatment. N Engl J Med 2003; 349: 1451-1464.
88. 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: 948-953.
89. Melo JV. The diversity of BCR-ABL fusion proteins and their relationship to leukemia phenotype. Blood 1996; 88: 2375-2384.
90. Huntly BJ, Shigematsu H, Deguchi K, Lee BH, Mizuno S, Duclos N et al MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell 2004; 6: 587-596.
91. Savona M, Talpaz M. Getting to the stem of chronic myeloid leukaemia. Nat Rev Cancer 2008; 8: 341-350.
92. Melo JV, Barnes DJ. Chronic myeloid leukaemia as a model of disease evolution in human cancer. Nat Rev Cancer 2007; 7: 441-453.
93. Mullighan CG, Radtke I, Zhang J, Phillips LA, Su X, Ma J et al. Genome-wide analysis of genetic alterations in chronic myeloid leukemia [abstract]. Blood 2008; 2008: 397-398.
94. Reynaud D, Demarco IA, Reddy KL, Schjerven H, Bertolino E, Chen Z et al. Regulation of B cell fate commitment and immunoglobulin heavy-chain gene rearrangements by Ikaros. Nat Immunol 2008; 9: 927-936.
95. Molnar A, Georgopoulos K. The Ikaros gene encodes a family of functionally diverse zinc finger DNA-binding proteins. Mol Cell Biol 1994; 14: 8292-8303.
96. Sun L, Crotty ML, Sensel M, Sather H, Navara C, Nachman J et al. Expression of dominant-negative Ikaros isoforms in T-cell acute lymphoblastic leukemia. Clin Cancer Res 1999; 5: 2112-2120.
97. Sun L, Goodman PA, Wood CM, Crotty ML, Sensel M, Sather H et al. Expression of aberrantly spliced oncogenic ikaros isoforms in childhood acute lymphoblastic leukemia. J Clin Oncol 1999; 17: 3753-3766.
98. Sun L, Heerema N, Crotty L, Wu X, Navara C, Vassilev A et al. Expression of dominant-negative and mutant isoforms of the antileukemic transcription factor Ikaros in infant acute lymphoblastic leukemia. Proc Natl Acad Sci USA 1999; 96: 680-685.
99. Nakase K, Ishimaru F, Avitahl N, Dansako H, Matsuo K, Fujii K et al. Dominant negative isoform of the Ikaros gene in patients with adult B-cell acute lymphoblastic leukemia. Cancer Res 2000; 60: 4062-4065.
100. Nishii K, Kita K, Miwa H, Shikami M, Taniguchi M, Usui E et al. Expression of B cell-associated transcription factors in B-cell precursor acute lymphoblastic leukemia cells: Association with PU.1 expression, phenotype, and immunogenotype. Int J Hematol 2000; 71: 372-378.
101. Olivero S, Maroc C, Beillard E, Gabert J, Nietfeld W, Chabannon C et al. Detection of different Ikaros isoforms in human leukaemias using real-time quantitative polymerase chain reaction. Br J Haematol 2000; 110: 826-830.
102. Takanashi M, Yagi T, Imamura T, Tabata Y, Morimoto A, Hibi S et al Expression of the Ikaros gene family in childhood acute lymphoblastic leukaemia. Br J Haematol 2002; 117: 525-530.
103. Klein F, Feldhahn N, Herzog S, Sprangers M, Mooster JL, Jumaa H et al. BCR-ABL1 induces aberrant splicing of IKAROS and lineage infidelity in pre-B lymphoblastic leukemia cells. Oncogene 2006; 25: 1118-1124.
104. Mullighan CG, Phillips LA, Su X, Ma J, Miller CB, Shurtleff SA et al Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science 2008; 322: 1377-1380.
105. Mullighan CG, Phillips LA, Kiedrowski LA, Ma J, Williams RT, Shurtleff SA et al. Ultra-high resolution genomic analysis of genomic alterations in high-risk acute lymphoblastic leukemia [abstract]. Blood 2008; 112: 715.
106. Moorman AV, Harrison CJ, Buck GA, Richards SM, Secker-Walker LM, Martineau M 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: 3189-3197.
107. Paulsson K, Cazier JB, Macdougall F, Stevens J, Stasevich I, Vrcelj N et al. Microdeletions are a general feature of adult and adolescent acute lymphoblastic leukemia: Unexpected similarities with pediatric disease. Proc Natl Acad Sci USA 2008; 105: 6708-6713.
108. Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet 2007; 8: 286-298.
109. Shendure J, Ji H. Next-generation DNA sequencing. Nat Biotechnol 2008; 26: 1135-1145.
110. Ley TJ, Mardis ER, Ding L, Fulton B, McLellan MD, Chen K et al. DNA sequencing of a cytogenetically normal acute myeloid leukaemia genome. Nature 2008; 456: 66-72.
111. Campbell PJ, Stephens PJ, Pleasance ED, O'Meara S, Li H, Santarius T et al. Identification of somatically acquired rearrangements in cancer using genome-wide massively parallel paired-end sequencing. Nat Genet 2008; 40: 722-729.
112. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008; 5: 621-628.
113. Shendure J. The beginning of the end for microarrays? Nat Methods 2008; 5: 585-587.