Application of genomics for risk stratification of childhood acute lymphoblastic leukaemia: From bench to bedside?

British Journal of Haematology

Volumn 151, Issue 2, 2010, Pages 119-131

  Izraeli, Shai ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

childhood acute lymphoblastic leukaemia; genomics; risk stratification

Indexed keywords

COMPLEMENTARY DNA;

ACUTE LYMPHOBLASTIC LEUKEMIA; CANCER RISK; CHILDHOOD CANCER; CHROMOSOME ABERRATION; COMPARATIVE GENOMIC HYBRIDIZATION; DNA MICROARRAY; GENE EXPRESSION; GENOMICS; METHYLATION; MULTIPLEX LIGATION DEPENDENT PROBE AMPLIFICATION; PRIORITY JOURNAL; PROGNOSIS; REAL TIME POLYMERASE CHAIN REACTION; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM;

CHILD; GENE EXPRESSION PROFILING; GENOMICS; HUMANS; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROGNOSIS; RISK ASSESSMENT;

EID: 77957346554     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2010.08312.x     Document Type: Review

References (77)

1. Armstrong, S.A., Staunton, J.E., Silverman, L.B., Pieters, R., den Boer, M.L., Minden, M.D., Sallan, S.E., Lander, E.S., Golub, T.R. Korsmeyer, S.J. (2002) MLL translocations specify a distinct gene expression profile that distinguishes a unique leukaemia. Nature Genetics, 30, 41 47.
2. Armstrong, S.A., Kung, A.L., Mabon, M.E., Silverman, L.B., Stam, R.W., Den Boer, M.L., Pieters, R., Kersey, J.H., Sallan, S.E., Fletcher, J.A., Golub, T.R., Griffin, J.D. Korsmeyer, S.J. (2003) Inhibition of FLT3 in MLL. Validation of a therapeutic target identified by gene expression based classification. Cancer Cell, 3, 173 183.
3. Attarbaschi, A., Mann, G., Panzer-Grumayer, R., Rottgers, S., Steiner, M., Konig, M., Csinady, E., Dworzak, M.N., Seidel, M., Janousek, D., Moricke, A., Reichelt, C., Harbott, J., Schrappe, M., Gadner, H. Haas, O.A. (2008) Minimal residual disease values discriminate between low and high relapse risk in children with B-cell precursor acute lymphoblastic leukaemia and an intrachromosomal amplification of chromosome 21: the Austrian and German acute lymphoblastic leukaemia Berlin-Frankfurt-Munster (ALL-BFM) trials. Journal of Clinical Oncology, 26, 3046 3050.
4. Basso, G., Veltroni, M., Valsecchi, M.G., Dworzak, M.N., Ratei, R., Silvestri, D., Benetello, A., Buldini, B., Maglia, O., Masera, G., Conter, V., Arico, M., Biondi, A. Gaipa, G. (2009) Risk of relapse of childhood acute lymphoblastic leukaemia is predicted by flow cytometric measurement of residual disease on day 15 bone marrow. Journal of Clinical Oncology, 27, 5168 5174.
5. Bercovich, D., Ganmore, I., Scott, L.M., Wainreb, G., Birger, Y., Elimelech, A., Shochat, C., Cazzaniga, G., Biondi, A., Basso, G., Cario, G., Schrappe, M., Stanulla, M., Strehl, S., Haas, O.A., Mann, G., Binder, V., Borkhardt, A., Kempski, H., Trka, J., Bielorei, B., Avigad, S., Stark, B., Smith, O., Dastugue, N., Bourquin, J.P., Tal, N.B., Green, A.R. Izraeli, S. (2008) Mutations of JAK2 in acute lymphoblastic leukaemias associated with Down's syndrome. Lancet, 372, 1484 1492.
6. Bhojwani, D., Kang, H., Menezes, R.X., Yang, W., Sather, H., Moskowitz, N.P., Min, D.J., Potter, J.W., Harvey, R., Hunger, S.P., Seibel, N., Raetz, E.A., Pieters, R., Horstmann, M.A., Relling, M.V., den Boer, M.L., Willman, C.L. Carroll, W.L. (2008) Gene expression signatures predictive of early response and outcome in high-risk childhood acute lymphoblastic leukaemia: a Children's Oncology Group Study [corrected]. Journal of Clinical Oncology, 26, 4376 4384.
7. Bonapace, L., Bornhauser, B.C., Schmitz, M., Cario, G., Ziegler, U., Niggli, F.K., Schafer, B.W., Schrappe, M., Stanulla, M. Bourquin, J.P. (2010) Induction of autophagy-dependent necroptosis is required for childhood acute lymphoblastic leukaemia cells to overcome glucocorticoid resistance. Journal of Clinical Investigation, 120, 1310 1323.
8. Borowitz, M.J., Devidas, M., Hunger, S.P., Bowman, W.P., Carroll, A.J., Carroll, W.L., Linda, S., Martin, P.L., Pullen, D.J., Viswanatha, D., Willman, C.L., Winick, N. Camitta, B.M. (2008) Clinical significance of minimal residual disease in childhood acute lymphoblastic leukaemia and its relationship to other prognostic factors: a Children's Oncology Group study. Blood, 111, 5477 5485.
9. Breit, S., Stanulla, M., Flohr, T., Schrappe, M., Ludwig, W.D., Tolle, G., Happich, M., Muckenthaler, M.U. Kulozik, A.E. (2006) Activating NOTCH1 mutations predict favorable early treatment response and long-term outcome in childhood precursor T-cell lymphoblastic leukaemia. Blood, 108, 1151 1157.
10. Bungaro, S., Dell'Orto, M.C., Zangrando, A., Basso, D., Gorletta, T., Lo Nigro, L., Leszl, A., Young, B.D., Basso, G., Bicciato, S., Biondi, A., te Kronnie, G. Cazzaniga, G. (2009) Integration of genomic and gene expression data of childhood ALL without known aberrations identifies subgroups with specific genetic hallmarks. Genes, Chromosomes and Cancer, 48, 22 38.
11. Buonamici, S., Trimarchi, T., Ruocco, M.G., Reavie, L., Cathelin, S., Mar, B.G., Klinakis, A., Lukyanov, Y., Tseng, J.C., Sen, F., Gehrie, E., Li, M., Newcomb, E., Zavadil, J., Meruelo, D., Lipp, M., Ibrahim, S., Efstratiadis, A., Zagzag, D., Bromberg, J.S., Dustin, M.L. Aifantis, I. (2009) CCR7 signalling as an essential regulator of CNS infiltration in T-cell leukaemia. Nature, 459, 1000 1004.
12. Cario, G., Stanulla, M., Fine, B.M., Teuffel, O., Neuhoff, N.V., Schrauder, A., Flohr, T., Schafer, B.W., Bartram, C.R., Welte, K., Schlegelberger, B. Schrappe, M. (2005) Distinct gene expression profiles determine molecular treatment response in childhood acute lymphoblastic leukaemia. Blood, 105, 821 826.
13. Cario, G., Izraeli, S., Teichert, A., Rhein, P., Skokowa, J., Moricke, A., Zimmermann, M., Schrauder, A., Karawajew, L., Ludwig, W.D., Welte, K., Schunemann, H.J., Schlegelberger, B., Schrappe, M. Stanulla, M. (2007) High interleukin-15 expression characterizes childhood acute lymphoblastic leukaemia with involvement of the CNS. Journal of Clinical Oncology, 25, 4813 4820.
14. Cario, G., Zimmermann, M., Romey, R., Gesk, S., Vater, I., Harbott, J., Schrauder, A., Moericke, A., Izraeli, S., Akasaka, T., Dyer, M.J., Siebert, R., Schrappe, M. Stanulla, M. (2010) Presence of the P2RY8-CRLF2 rearrangement is associated with a poor prognosis in non-high-risk precursor B-cell acute lymphoblastic leukaemia in children treated according to the ALL-BFM 2000 protocol. Blood. DOI
15. Cheng, Q., Yang, W., Raimondi, S.C., Pui, C.H., Relling, M.V. Evans, W.E. (2005) Karyotypic abnormalities create discordance of germline genotype and cancer cell phenotypes. Nature Genetics, 37, 878 882.
16. Conter, V., Bartram, C.R., Valsecchi, M.G., Schrauder, A., Panzer-Grumayer, R., Moricke, A., Arico, M., Zimmermann, M., Mann, G., De Rossi, G., Stanulla, M., Locatelli, F., Basso, G., Niggli, F., Barisone, E., Henze, G., Ludwig, W.D., Haas, O.A., Cazzaniga, G., Koehler, R., Silvestri, D., Bradtke, J., Parasole, R., Beier, R., van Dongen, J.J., Biondi, A. Schrappe, M. (2010) Molecular response to treatment redefines all prognostic factors in children and adolescents with B-cell precursor acute lymphoblastic leukaemia: results in 3184 patients of the AIEOP-BFM ALL 2000 study. Blood, 115, 3206 3214.
17. Coustan-Smith, E., Ribeiro, R.C., Stow, P., Zhou, Y., Pui, C.H., Rivera, G.K., Pedrosa, F. Campana, D. (2006) A simplified flow cytometric assay identifies children with acute lymphoblastic leukaemia who have a superior clinical outcome. Blood, 108, 97 102.
18. Coustan-Smith, E., Mullighan, C.G., Onciu, M., Behm, F.G., Raimondi, S.C., Pei, D., Cheng, C., Su, X., Rubnitz, J.E., Basso, G., Biondi, A., Pui, C.H., Downing, J.R. Campana, D. (2009) Early T-cell precursor leukaemia: a subtype of very high-risk acute lymphoblastic leukaemia. The Lancet Oncology, 10, 147 156.
19. Davidsen, M.L., Dalhoff, K. Schmiegelow, K. (2008) Pharmacogenetics influence treatment efficacy in childhood acute lymphoblastic leukaemia. Journal of Pediatric Hematology/Oncology, 30, 831 849.
20. Davidsson, J., Lilljebjorn, H., Andersson, A., Veerla, S., Heldrup, J., Behrendtz, M., Fioretos, T. Johansson, B. (2009) The DNA methylome of pediatric acute lymphoblastic leukaemia. Human Molecular Genetics, 18, 4054 4065.
21. Den Boer, M.L., van Slegtenhorst, M., De Menezes, R.X., Cheok, M.H., Buijs-Gladdines, J.G., Peters, S.T., Van Zutven, L.J., Beverloo, H.B., Van der Spek, P.J., Escherich, G., Horstmann, M.A., Janka-Schaub, G.E., Kamps, W.A., Evans, W.E. Pieters, R. (2009) A subtype of childhood acute lymphoblastic leukaemia with poor treatment outcome: a genome-wide classification study. Lancet Oncol, 10, 125 134.
22. Flotho, C., Coustan-Smith, E., Pei, D., Cheng, C., Song, G., Pui, C.H., Downing, J.R. Campana, D. (2007) A set of genes that regulate cell proliferation predicts treatment outcome in childhood acute lymphoblastic leukaemia. Blood, 110, 1271 1277.
23. Gefen, N., Binder, V., Zaliova, M., Linka, Y., Morrow, M., Novosel, A., Edry, L., Hertzberg, L., Shomron, N., Williams, O., Trka, J., Borkhardt, A. Izraeli, S. (2010) Hsa-mir-125b-2 is highly expressed in childhood ETV6/RUNX1 (TEL/AML1) leukaemias and confers survival advantage to growth inhibitory signals independent of p53. Leukaemia, 24, 89 96.
24. Greaves, M. (2009) Darwin and evolutionary tales in leukaemia. The Ham-Wasserman Lecture. Hematology/American Society of Hematology. Education Program, 3 12.
25. Haferlach, T., Kohlmann, A., Wieczorek, L., Basso, G., Kronnie, G.T., Bene, M.C., De Vos, J., Hernandez, J.M., Hofmann, W.K., Mills, K.I., Gilkes, A., Chiaretti, S., Shurtleff, S.A., Kipps, T.J., Rassenti, L.Z., Yeoh, A.E., Papenhausen, P.R., Liu, W.M., Williams, P.M. Foa, R. (2010) Clinical utility of microarray-based gene expression profiling in the diagnosis and subclassification of leukaemia: report from the International Microarray Innovations in Leukaemia Study Group. Journal of Clinical Oncology, 28, 2529 2537.
26. Hahn, C.K., Berchuck, J.E., Ross, K.N., Kakoza, R.M., Clauser, K., Schinzel, A.C., Ross, L., Galinsky, I., Davis, T.N., Silver, S.J., Root, D.E., Stone, R.M., DeAngelo, D.J., Carroll, M., Hahn, W.C., Carr, S.A., Golub, T.R., Kung, A.L. Stegmaier, K. (2009) Proteomic and genetic approaches identify Syk as an AML target. Cancer Cell, 16, 281 294.
27. Harvey, R.C., Mullighan, C.G., Chen, I.M., Wharton, W., Mikhail, F.M., Carroll, A.J., Kang, H., Liu, W., Dobbin, K.K., Smith, M.A., Carroll, W.L., Devidas, M., Bowman, W.P., Camitta, B.M., Reaman, G.H., Hunger, S.P., Downing, J.R. Willman, C.L. (2010) 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 leukaemia. Blood, DOI
28. Heerema, N.A., Sather, H.N., Sensel, M.G., Zhang, T., Hutchinson, R.J., Nachman, J.B., Lange, B.J., Steinherz, P.G., Bostrom, B.C., Reaman, G.H., Gaynon, P.S. Uckun, F.M. (2000) Prognostic impact of trisomies of chromosomes 10, 17, and 5 among children with acute lymphoblastic leukaemia and high hyperdiploidy (> 50 chromosomes). Journal of Clinical Oncology, 18, 1876 1887.
29. Hertzberg, L., Betts, D.R., Raimondi, S.C., Schafer, B.W., Notterman, D.A., Domany, E. Izraeli, S. (2007) Prediction of chromosomal aneuploidy from gene expression data. Genes, Chromosomes and Cancer, 46, 75 86.
30. Hertzberg, L., Vendramini, E., Ganmore, I., Cazzaniga, G., Schmitz, M., Chalker, J., Shiloh, R., Iacobucci, I., Shochat, C., Zeligson, S., Cario, G., Stanulla, M., Strehl, S., Russell, L.J., Harrison, C.J., Bornhauser, B., Yoda, A., Rechavi, G., Bercovich, D., Borkhardt, A., Kempski, H., Te Kronnie, G., Bourquin, J.P., Domany, E. Izraeli, S. (2010) Down syndrome acute lymphoblastic leukaemia, a highly heterogeneous disease in which aberrant expression of CRLF2 is associated with mutated JAK2: a report from the International BFM Study Group. Blood, 115, 1006 1017.
31. Hoffmann, K., Firth, M.J., Beesley, A.H., de Klerk, N.H. Kees, U.R. (2006) Translating microarray data for diagnostic testing in childhood leukaemia. BMC Cancer, 6, 229.
32. Holleman, A., Cheok, M.H., den Boer, M.L., Yang, W., Veerman, A.J., Kazemier, K.M., Pei, D., Cheng, C., Pui, C.H., Relling, M.V., Janka-Schaub, G.E., Pieters, R. Evans, W.E. (2004) Gene-expression patterns in drug-resistant acute lymphoblastic leukaemia cells and response to treatment. New England Journal of Medicine, 351, 533 542.
33. Holleman, A., den Boer, M.L., de Menezes, R.X., Cheok, M.H., Cheng, C., Kazemier, K.M., Janka-Schaub, G.E., Gobel, U., Graubner, U.B., Evans, W.E. Pieters, R. (2006) The expression of 70 apoptosis genes in relation to lineage, genetic subtype, cellular drug resistance, and outcome in childhood acute lymphoblastic leukaemia. Blood, 107, 769 776.
34. Iacobucci, I., Storlazzi, C.T., Cilloni, D., Lonetti, A., Ottaviani, E., Soverini, S., Astolfi, A., Chiaretti, S., Vitale, A., Messa, F., Impera, L., Baldazzi, C., D'Addabbo, P., Papayannidis, C., Lonoce, A., Colarossi, S., Vignetti, M., Piccaluga, P.P., Paolini, S., Russo, D., Pane, F., Saglio, G., Baccarani, M., Foa, R. Martinelli, G. (2009) Identification and molecular characterization of recurrent genomic deletions on 7p12 in the IKZF1 gene in a large cohort of BCR-ABL1-positive acute lymphoblastic leukaemia patients: on behalf of Gruppo Italiano Malattie Ematologiche dell'Adulto Acute Leukaemia Working Party (GIMEMA AL WP). Blood, 114, 2159 2167.
35. Jeha, S., Pei, D., Raimondi, S.C., Onciu, M., Campana, D., Cheng, C., Sandlund, J.T., Ribeiro, R.C., Rubnitz, J.E., Howard, S.C., Downing, J.R., Evans, W.E., Relling, M.V. Pui, C.H. (2009) Increased risk for CNS relapse in pre-B cell leukaemia with the t(1;19)/TCF3-PBX1. Leukaemia, 23, 1406 1409.
36. Kager, L., Cheok, M., Yang, W., Zaza, G., Cheng, Q., Panetta, J.C., Pui, C.H., Downing, J.R., Relling, M.V. Evans, W.E. (2005) Folate pathway gene expression differs in subtypes of acute lymphoblastic leukaemia and influences methotrexate pharmacodynamics. Journal of Clinical Investigation, 115, 110 117.
37. Kang, H., Chen, I.M., Wilson, C.S., Bedrick, E.J., Harvey, R.C., Atlas, S.R., Devidas, M., Mullighan, C.G., Wang, X., Murphy, M., Ar, K., Wharton, W., Borowitz, M.J., Bowman, W.P., Bhojwani, D., Carroll, W.L., Camitta, B.M., Reaman, G.H., Smith, M.A., Downing, J.R., Hunger, S.P. Willman, C.L. (2010) Gene expression classifiers for relapse-free survival and minimal residual disease improve risk classification and outcome prediction in pediatric B-precursor acute lymphoblastic leukaemia. Blood, 115, 1394 1405.
38. Kawamata, N., Ogawa, S., Zimmermann, M., Niebuhr, B., Stocking, C., Sanada, M., Hemminki, K., Yamatomo, G., Nannya, Y., Koehler, R., Flohr, T., Miller, C.W., Harbott, J., Ludwig, W.D., Stanulla, M., Schrappe, M., Bartram, C.R. Koeffler, H.P. (2008) Cloning of genes involved in chromosomal translocations by high-resolution single nucleotide polymorphism genomic microarray. Proceedings of the National Academy of Sciences of the United States of America, 105, 11921 11926.
39. Kerst, G., Kreyenberg, H., Roth, C., Well, C., Dietz, K., Coustan-Smith, E., Campana, D., Koscielniak, E., Niemeyer, C., Schlegel, P.G., Muller, I., Niethammer, D. Bader, P. (2005) Concurrent detection of minimal residual disease (MRD) in childhood acute lymphoblastic leukaemia by flow cytometry and real-time PCR. British Journal of Haematology, 128, 774 782.
40. Kohlmann, A., Schoch, C., Schnittger, S., Dugas, M., Hiddemann, W., Kern, W. Haferlach, T. (2004) Pediatric acute lymphoblastic leukaemia (ALL) gene expression signatures classify an independent cohort of adult ALL patients. Leukaemia, 18, 63 71.
41. Kohlmann, A., Kipps, T.J., Rassenti, L.Z., Downing, J.R., Shurtleff, S.A., Mills, K.I., Gilkes, A.F., Hofmann, W.K., Basso, G., Dell'orto, M.C., Foa, R., Chiaretti, S., De Vos, J., Rauhut, S., Papenhausen, P.R., Hernandez, J.M., Lumbreras, E., Yeoh, A.E., Koay, E.S., Li, R., Liu, W.M., Williams, P.M., Wieczorek, L. Haferlach, T. (2008) An international standardization programme towards the application of gene expression profiling in routine leukaemia diagnostics: the Microarray Innovations in Leukaemia study prephase. British Journal of Haematology, 142, 802 807.
42. Larson Gedman, A., Chen, Q., Kugel Desmoulin, S., Ge, Y., LaFiura, K., Haska, C.L., Cherian, C., Devidas, M., Linda, S.B., Taub, J.W. Matherly, L.H. (2009) The impact of NOTCH1, FBW7 and PTEN mutations on prognosis and downstream signaling in pediatric T-cell acute lymphoblastic leukaemia: a report from the Children's Oncology Group. Leukaemia, 23, 1417 1425.
43. Ley, T.J., Mardis, E.R., Ding, L., Fulton, B., McLellan, M.D., Chen, K., Dooling, D., Dunford-Shore, B.H., McGrath, S., Hickenbotham, M., Cook, L., Abbott, R., Larson, D.E., Koboldt, D.C., Pohl, C., Smith, S., Hawkins, A., Abbott, S., Locke, D., Hillier, L.W., Miner, T., Fulton, L., Magrini, V., Wylie, T., Glasscock, J., Conyers, J., Sander, N., Shi, X., Osborne, J.R., Minx, P., Gordon, D., Chinwalla, A., Zhao, Y., Ries, R.E., Payton, J.E., Westervelt, P., Tomasson, M.H., Watson, M., Baty, J., Ivanovich, J., Heath, S., Shannon, W.D., Nagarajan, R., Walter, M.J., Link, D.C., Graubert, T.A., DiPersio, J.F. Wilson, R.K. (2008) DNA sequencing of a cytogenetically normal acute myeloid leukaemia genome. Nature, 456, 66 72.
44. Li, Z., Zhang, W., Wu, M., Zhu, S., Gao, C., Sun, L., Zhang, R., Qiao, N., Xue, H., Hu, Y., Bao, S., Zheng, H. Han, J.D. (2009) Gene expression-based classification and regulatory networks of pediatric acute lymphoblastic leukaemia. Blood, 114, 4486 4493.
45. Lugthart, S., Cheok, M.H., den Boer, M.L., Yang, W., Holleman, A., Cheng, C., Pui, C.H., Relling, M.V., Janka-Schaub, G.E., Pieters, R. Evans, W.E. (2005) Identification of genes associated with chemotherapy crossresistance and treatment response in childhood acute lymphoblastic leukaemia. Cancer Cell, 7, 375 386.
46. Mansour, M.R., Sulis, M.L., Duke, V., Foroni, L., Jenkinson, S., Koo, K., Allen, C.G., Gale, R.E., Buck, G., Richards, S., Paietta, E., Rowe, J.M., Tallman, M.S., Goldstone, A.H., Ferrando, A.A. Linch, D.C. (2009) Prognostic implications of NOTCH1 and FBXW7 mutations in adults with T-cell acute lymphoblastic leukaemia treated on the MRC UKALLXII/ECOG E2993 protocol. Journal of Clinical Oncology, 27, 4352 4356.
47. Martinelli, G., Iacobucci, I., Storlazzi, C.T., Vignetti, M., Paoloni, F., Cilloni, D., Soverini, S., Vitale, A., Chiaretti, S., Cimino, G., Papayannidis, C., Paolini, S., Elia, L., Fazi, P., Meloni, G., Amadori, S., Saglio, G., Pane, F., Baccarani, M. Foa, R. (2009) IKZF1 (Ikaros) deletions in BCR-ABL1-positive acute lymphoblastic leukaemia are associated with short disease-free survival and high rate of cumulative incidence of relapse: a GIMEMA AL WP report. Journal of Clinical Oncology, 27, 5202 5207.
48. Mi, S., Lu, J., Sun, M., Li, Z., Zhang, H., Neilly, M.B., Wang, Y., Qian, Z., Jin, J., Zhang, Y., Bohlander, S.K., Le Beau, M.M., Larson, R.A., Golub, T.R., Rowley, J.D. Chen, J. (2007) MicroRNA expression signatures accurately discriminate acute lymphoblastic leukaemia from acute myeloid leukaemia. Proceedings of the National Academy of Sciences of the United States of America, 104, 19971 19976.
49. Milani, L., Lundmark, A., Kiialainen, A., Nordlund, J., Flaegstad, T., Forestier, E., Heyman, M., Jonmundsson, G., Kanerva, J., Schmiegelow, K., Soderhall, S., Gustafsson, M.G., Lonnerholm, G. Syvanen, A.C. (2010) DNA methylation for subtype classification and prediction of treatment outcome in patients with childhood acute lymphoblastic leukaemia. Blood, 115, 1214 1225.
50. Moorman, A.V., Richards, S.M., Martineau, M., Cheung, K.L., Robinson, H.M., Jalali, G.R., Broadfield, Z.J., Harris, R.L., Taylor, K.E., Gibson, B.E., Hann, I.M., Hill, F.G., Kinsey, S.E., Eden, T.O., Mitchell, C.D. Harrison, C.J. (2003) Outcome heterogeneity in childhood high-hyperdiploid acute lymphoblastic leukaemia. Blood, 102, 2756 2762.
51. Moorman, A.V., Richards, S.M., Robinson, H.M., Strefford, J.C., Gibson, B.E., Kinsey, S.E., Eden, T.O., Vora, A.J., Mitchell, C.D. Harrison, C.J. (2007) Prognosis of children with acute lymphoblastic leukaemia (ALL) and intrachromosomal amplification of chromosome 21 (iAMP21). Blood, 109, 2327 2330.
52. Moos, P.J., Raetz, E.A., Carlson, M.A., Szabo, A., Smith, F.E., Willman, C., Wei, Q., Hunger, S.P. Carroll, W.L. (2002) Identification of gene expression profiles that segregate patients with childhood leukaemia. Clinical Cancer Research, 8, 3118 3130.
53. Mullighan, C.G. Downing, J.R. (2009a) Genome-wide profiling of genetic alterations in acute lymphoblastic leukaemia: recent insights and future directions. Leukaemia, 23, 1209 1218.
54. Mullighan, C.G. Downing, J.R. (2009b) Global genomic characterization of acute lymphoblastic leukaemia. Seminars in Hematology, 46, 3 15.
55. Mullighan, C.G., Goorha, S., Radtke, I., Miller, C.B., Coustan-Smith, E., Dalton, J.D., Girtman, K., Mathew, S., Ma, J., Pounds, S.B., Su, X., Pui, C.H., Relling, M.V., Evans, W.E., Shurtleff, S.A. Downing, J.R. (2007) Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature, 446, 758 764.
56. Mullighan, C.G., Miller, C.B., Radtke, I., Phillips, L.A., Dalton, J., Ma, J., White, D., Hughes, T.P., Le Beau, M.M., Pui, C.H., Relling, M.V., Shurtleff, S.A. Downing, J.R. (2008) BCR-ABL1 lymphoblastic leukaemia is characterized by the deletion of Ikaros. Nature, 453, 110 114.
57. Mullighan, C.G., Su, X., Zhang, J., Radtke, I., Phillips, L.A., Miller, C.B., Ma, J., Liu, W., Cheng, C., Schulman, B.A., Harvey, R.C., Chen, I.M., Clifford, R.J., Carroll, W.L., Reaman, G., Bowman, W.P., Devidas, M., Gerhard, D.S., Yang, W., Relling, M.V., Shurtleff, S.A., Campana, D., Borowitz, M.J., Pui, C.H., Smith, M., Hunger, S.P., Willman, C.L. Downing, J.R. (2009a) Deletion of IKZF1 and prognosis in acute lymphoblastic leukaemia. New England Journal of Medicine, 360, 470 480.
58. Mullighan, C.G., Collins-Underwood, J.R., Phillips, L.A., Loudin, M.G., Liu, W., Zhang, J., Ma, J., Coustan-Smith, E., Harvey, R.C., Willman, C.L., Mikhail, F.M., Meyer, J., Carroll, A.J., Williams, R.T., Cheng, J., Heerema, N.A., Basso, G., Pession, A., Pui, C.H., Raimondi, S.C., Hunger, S.P., Downing, J.R., Carroll, W.L. Rabin, K.R. (2009b) Rearrangement of CRLF2 in B-progenitor- and Down syndrome-associated acute lymphoblastic leukaemia. Nature Genetics, 41, 1243 1246.
59. Papaemmanuil, E., Hosking, F.J., Vijayakrishnan, J., Price, A., Olver, B., Sheridan, E., Kinsey, S.E., Lightfoot, T., Roman, E., Irving, J.A., Allan, J.M., Tomlinson, I.P., Taylor, M., Greaves, M. Houlston, R.S. (2009) Loci on 7p12.2, 10q21.2 and 14q11.2 are associated with risk of childhood acute lymphoblastic leukaemia. Nature Genetics, 41, 1006 1010.
60. Peck, D., Crawford, E.D., Ross, K.N., Stegmaier, K., Golub, T.R. Lamb, J. (2006) A method for high-throughput gene expression signature analysis. Genome Biology, 7, R61.
61. Relling, M.V., Pui, C.H., Cheng, C. Evans, W.E. (2006) Thiopurine methyltransferase in acute lymphoblastic leukaemia. Blood, 107, 843 844.
62. Roman-Gomez, J., Agirre, X., Jimenez-Velasco, A., Arqueros, V., Vilas-Zornoza, A., Rodriguez-Otero, P., Martin-Subero, I., Garate, L., Cordeu, L., San Jose-Eneriz, E., Martin, V., Castillejo, J.A., Bandres, E., Calasanz, M.J., Siebert, R., Heiniger, A., Torres, A. Prosper, F. (2009) Epigenetic regulation of microRNAs in acute lymphoblastic leukaemia. Journal of Clinical Oncology, 27, 1316 1322.
63. Ross, M.E., Zhou, X., Song, G., Shurtleff, S.A., Girtman, K., Williams, W.K., Liu, H.C., Mahfouz, R., Raimondi, S.C., Lenny, N., Patel, A. Downing, J.R. (2003) Classification of pediatric acute lymphoblastic leukaemia by gene expression profiling. Blood, 102, 2951 2959.
64. Rothman, R., Trakhtenbrot, L., Bielorai, B., Izraeli, S., Ishoev, G., Amariglio, N., Rechavi, G. Toren, A. (2005) Co-existence of multiple subclones in TEL-AML1 at diagnosis of acute lymphoblastic leukaemia in association with submicroscopic deletion of AML1. British Journal Haematology, 129, 491 498.
65. Russell, L.J., Capasso, M., Vater, I., Akasaka, T., Bernard, O.A., Calasanz, M.J., Chandrasekaran, T., Chapiro, E., Gesk, S., Griffiths, M., Guttery, D.S., Haferlach, C., Harder, L., Heidenreich, O., Irving, J., Kearney, L., Nguyen-Khac, F., Machado, L., Minto, L., Majid, A., Moorman, A.V., Morrison, H., Rand, V., Strefford, J.C., Schwab, C., Tonnies, H., Dyer, M.J., Siebert, R. Harrison, C.J. (2009) Deregulated expression of cytokine receptor gene, CRLF2, is involved in lymphoid transformation in B-cell precursor acute lymphoblastic leukaemia. Blood, 114, 2688 2698.
66. Schotte, D., Chau, J.C., Sylvester, G., Liu, G., Chen, C., van der Velden, V.H., Broekhuis, M.J., Peters, T.C., Pieters, R. den Boer, M.L. (2009) Identification of new microRNA genes and aberrant microRNA profiles in childhood acute lymphoblastic leukaemia. Leukaemia, 23, 313 322.
67. Schultz, K.R., Bowman, W.P., Aledo, A., Slayton, W.B., Sather, H., Devidas, M., Wang, C., Davies, S.M., Gaynon, P.S., Trigg, M., Rutledge, R., Burden, L., Jorstad, D., Carroll, A., Heerema, N.A., Winick, N., Borowitz, M.J., Hunger, S.P., Carroll, W.L. Camitta, B. (2009) Improved early event-free survival with imatinib in Philadelphia chromosome-positive acute lymphoblastic leukaemia: a children's oncology group study. Journal of Clinical Oncology, 27, 5175 5181.
68. Staal, F.J., Cario, G., Cazzaniga, G., Haferlach, T., Heuser, M., Hofmann, W.K., Mills, K., Schrappe, M., Stanulla, M., Wingen, L.U., van Dongen, J.J. Schlegelberger, B. (2006) Consensus guidelines for microarray gene expression analyses in leukaemia from three European leukaemia networks. Leukaemia, 20, 1385 1392.
69. Stanulla, M. Schrappe, M. (2009) Treatment of childhood acute lymphoblastic leukaemia. Seminars in Hematology, 46, 52 63.
70. Stanulla, M., Schaeffeler, E., Flohr, T., Cario, G., Schrauder, A., Zimmermann, M., Welte, K., Ludwig, W.D., Bartram, C.R., Zanger, U.M., Eichelbaum, M., Schrappe, M. Schwab, M. (2005) Thiopurine methyltransferase (TPMT) genotype and early treatment response to mercaptopurine in childhood acute lymphoblastic leukaemia. JAMA, 293, 1485 1489.
71. Steinemann, D., Cario, G., Stanulla, M., Karawajew, L., Tauscher, M., Weigmann, A., Gohring, G., Ludwig, W.D., Harbott, J., Radlwimmer, B., Bartram, C., Lichter, P., Schrappe, M. Schlegelberger, B. (2008) Copy number alterations in childhood acute lymphoblastic leukaemia and their association with minimal residual disease. Genes, Chromosomes and Cancer, 47, 471 480.
72. Wei, G., Twomey, D., Lamb, J., Schlis, K., Agarwal, J., Stam, R.W., Opferman, J.T., Sallan, S.E., den Boer, M.L., Pieters, R., Golub, T.R. Armstrong, S.A. (2006) Gene expression-based chemical genomics identifies rapamycin as a modulator of MCL1 and glucocorticoid resistance. Cancer Cell, 10, 331 342.
73. Yang, J.J., Cheng, C., Yang, W., Pei, D., Cao, X., Fan, Y., Pounds, S.B., Neale, G., Trevino, L.R., French, D., Campana, D., Downing, J.R., Evans, W.E., Pui, C.H., Devidas, M., Bowman, W.P., Camitta, B.M., Willman, C.L., Davies, S.M., Borowitz, M.J., Carroll, W.L., Hunger, S.P. Relling, M.V. (2009) Genome-wide interrogation of germline genetic variation associated with treatment response in childhood acute lymphoblastic leukaemia. JAMA, 301, 393 403.
74. Yeoh, E.J., Ross, M.E., Shurtleff, S.A., Williams, W.K., Patel, D., Mahfouz, R., Behm, F.G., Raimondi, S.C., Relling, M.V., Patel, A., Cheng, C., Campana, D., Wilkins, D., Zhou, X., Li, J., Liu, H., Pui, C.H., Evans, W.E., Naeve, C., Wong, L. Downing, J.R. (2002) Classification, subtype discovery, and prediction of outcome in pediatric acute lymphoblastic leukaemia by gene expression profiling. Cancer Cell, 1, 133 143.
75. Yoda, A., Yoda, Y., Chiaretti, S., Bar-Natan, M., Mani, K., Rodig, S.J., West, N., Xiao, Y., Brown, J.R., Mitsiades, C., Sattler, M., Kutok, J.L., DeAngelo, D.J., Wadleigh, M., Piciocchi, A., Dal Cin, P., Bradner, J.E., Griffin, J.D., Anderson, K.C., Stone, R.M., Ritz, J., Foa, R., Aster, J.C., Frank, D.A. Weinstock, D.M. (2010) Functional screening identifies CRLF2 in precursor B-cell acute lymphoblastic leukaemia. Proceedings of the National Academy of Sciences of the United States of America, 107, 252 257.
76. Yoshida, T., Ng, S.Y., Zuniga-Pflucker, J.C. Georgopoulos, K. (2006) Early hematopoietic lineage restrictions directed by Ikaros. Nature Immunology, 7, 382 391.
77. Zhu, Y.M., Zhao, W.L., Fu, J.F., Shi, J.Y., Pan, Q., Hu, J., Gao, X.D., Chen, B., Li, J.M., Xiong, S.M., Gu, L.J., Tang, J.Y., Liang, H., Jiang, H., Xue, Y.Q., Shen, Z.X., Chen, Z. Chen, S.J. (2006) NOTCH1 mutations in T-cell acute lymphoblastic leukaemia: prognostic significance and implication in multifactorial leukemogenesis. Clinical Cancer Research, 12, 3043 3049.