Mutations in the BCR-ABL1 Kinase Domain and Elsewhere in Chronic Myeloid Leukemia

Clinical Lymphoma, Myeloma and Leukemia

Volumn 15, Issue S, 2015, Pages S120-S128

  Soverini, Simona ^a   De Benedittis, Caterina ^a   Mancini, Manuela ^a   Martinelli, Giovanni ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

BCR ABL1 mutations; Dasatinib; Imatinib; Nilotinib; Tyrosine kinase inhibitor

Indexed keywords

PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; ANTINEOPLASTIC AGENT; BCR ABL PROTEIN; BCR-ABL1 FUSION PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR;

ARTICLE; ASXL1 GENE; BCR ABL1 FUSION GENE; CANCER GROWTH; CHROMOSOME ABERRATION; CHROMOSOME TRANSLOCATION; CHRONIC MYELOID LEUKEMIA; COMPARATIVE GENOMIC HYBRIDIZATION; DNMT3A GENE; EXOME; EZH2 GENE; FUSION GENE; GATA 2 GENE; GENE MUTATION; GENETIC SCREENING; GOLD STANDARD; HUMAN; IDH1 GENE; IDH2 GENE; IKZF1 GENE; NEXT GENERATION SEQUENCING; NPM1 GENE; ONCOGENE; ONCOGENE K RAS; ONCOGENE N RAS; PATHOGENESIS; PROTEIN DOMAIN; RB1 GENE; RUNX1 GENE; SINGLE NUCLEOTIDE POLYMORPHISM; TET2 GENE; TUMOR SUPPRESSOR GENE; WT1 GENE; ANIMAL; ANTAGONISTS AND INHIBITORS; ENZYMOLOGY; GENETICS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MUTATION; PROTEIN TERTIARY STRUCTURE;

ANIMALS; ANTINEOPLASTIC AGENTS; FUSION PROTEINS, BCR-ABL; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MUTATION; PROTEIN KINASE INHIBITORS; PROTEIN STRUCTURE, TERTIARY;

EID: 84939610115     PISSN: 21522650     EISSN: 21522669     Source Type: Journal    
DOI: 10.1016/j.clml.2015.02.035     Document Type: Review

References (104)

1. C.L. Sawyers Chronic myeloid leukemia N Engl J Med 340 1999 1330 1340
2. P.C. Nowell, and D.A. Hungerford Chromosome studies on normal and leukemic human leukocytes J Natl Cancer Inst 25 1960 85 109
3. J.D. Rowley Letter: a new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining Nature 243 1973 290 293
4. B. Vogelstein, and K.W. Kinzler The multistep nature of cancer Trends Genet 9 1993 138 141
5. P.J. Fialkow, P.J. Martin, V. Najfeld, G.K. Penfold, R.J. Jacobson, and J.A. Hansen Evidence for a multistep pathogenesis of chronic myelogenous leukemia Blood 58 1981 158 163
6. W.H. Raskind, A.M. Ferraris, V. Najfeld, R.J. Jacobson, J.W. Moohr, and P.J. Fialkow Further evidence for the existence of a clonal Ph-negative stage in some cases of Ph-positive chronic myelocytic leukemia Leukemia 7 1993 1163 1167
7. C. Biernaux, M. Loos, A. Sels, G. Huez, and P. Stryckmans Detection of major bcr-abl gene expression at a very low level in blood cells of some healthy individuals Blood 86 1995 3118 3122
8. S. Bose, M. Deininger, J. Gora-Tybor, J.M. Goldman, and J.V. Melo The presence of typical and atypical BCR-ABL fusion genes in leukocytes of normal individuals: biologic significance and implications for the assessment of minimal residual disease Blood 92 1998 3362 3367
9. J. Song, D. Mercer, X. Hu, H. Liu, and M.M. Li Common leukemia- and lymphoma-associated genetic aberrations in healthy individuals J Mol Diagn 13 2011 213 219
10. G.Q. Daley, R.A. Van Etten, and D. Baltimore Induction of chronic myelogenous leukemia in mice by the P210bcr/abl gene of the Philadelphia chromosome Science 247 1990 824 830
11. M.A. Kelliher, J. McLaughlin, O.N. Witte, and N. Rosenberg Induction of a chronic myelogenous leukemia-like syndrome in mice with v-abl and BCR/ABL Proc Natl Acad Sci U S A 87 1990 6649 6653
12. A.G. Elefanty, I.K. Hariharan, and S. Cory BCR-ABL, the hallmark of chronic myeloid leukaemia in man, induces multiple haemopoietic neoplasms in mice EMBO J 9 1990 1069 1078
13. S. Soverini, G. Martinelli, I. Iacobucci, and M. Baccarani Imatinib mesylate for the treatment of chronic myeloid leukemia Expert Rev Anticancer Ther 8 2008 853 864
14. A. Fabarius, A. Leitner, A. Hochhaus, and et al. Impact of additional cytogenetic aberrations at diagnosis on prognosis of CML: long-term observation of 1151 patients from the randomized CML Study IV Blood 118 2011 6760 6768
15. S. Luatti, F. Castagnetti, G. Marzocchi, and et al. Additional chromosomal abnormalities in Philadelphia-positive clone: adverse prognostic influence on frontline imatinib therapy: a GIMEMA Working Party on CML analysis Blood 120 2012 761 767
16. G. Marzocchi, F. Castagnetti, S. Luatti, and et al. Variant Philadelphia translocations: molecular-cytogenetic characterization and prognostic influence on frontline imatinib therapy, a GIMEMA Working Party on CML analysis Blood 117 2011 6793 6800
17. S. Soverini, G. Martinelli, G. Rosti, I. Iacobucci, and M. Baccarani Advances in treatment of chronic myeloid leukemia with tyrosine kinase inhibitors: the evolving role of Bcr-Abl mutations and mutational analysis Pharmacogenomics 13 2012 1271 1284
18. P. Neviani Genetic events other than BCR-ABL1 Curr Hematol Malig Rep 9 2014 24 32
19. B. Johansson, T. Fioretos, and F. Mitelman Cytogenetic and molecular genetic evolution of chronic myeloid leukemia Acta Haematol 107 2002 76 94
20. S. Soverini, S. Branford, F.E. Nicolini, and et al. Implications of BCR-ABL1 kinase domain-mediated resistance in chronic myeloid leukemia Leuk Res 38 2014 10 20
21. M.E. Gorre, M. Mohammed, K. Ellwood, and et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification Science 293 2001 876 880
22. S. Soverini, G. Rosti, I. Iacobucci, M. Baccarani, and G. Martinelli Choosing the best second-line tyrosine kinase inhibitor in imatinib-resistant chronic myeloid leukemia patients harboring Bcr-Abl kinase domain mutations: how reliable is the IC(5)(0)? Oncologist 16 2011 868 876
23. S. Soverini, S. Colarossi, A. Gnani, and et al. Resistance to dasatinib in Philadelphia-positive leukemia patients and the presence or the selection of mutations at residues 315 and 317 in the BCR-ABL kinase domain Haematologica 92 2007 401 404
24. S. Soverini, G. Martinelli, S. Colarossi, and et al. Presence or the emergence of a F317L BCR-ABL mutation may be associated with resistance to dasatinib in Philadelphia chromosome-positive leukemia J Clin Oncol 24 2006 e51 e52
25. S. Soverini, G. Martinelli, S. Colarossi, and et al. Second-line treatment with dasatinib in patients resistant to imatinib can select novel inhibitor-specific BCR-ABL mutants in Ph+ ALL Lancet Oncol 8 2007 273 274
26. T. Hughes, G. Saglio, S. Branford, and et al. Impact of baseline BCR-ABL mutations on response to nilotinib in patients with chronic myeloid leukemia in chronic phase J Clin Oncol 27 2009 4204 4210
27. M.C. Muller, J.E. Cortes, D.W. Kim, and et al. Dasatinib treatment of chronic-phase chronic myeloid leukemia: analysis of responses according to preexisting BCR-ABL mutations Blood 114 2009 4944 4953
28. J. Cortes, E. Jabbour, H. Kantarjian, and et al. Dynamics of BCR-ABL kinase domain mutations in chronic myeloid leukemia after sequential treatment with multiple tyrosine kinase inhibitors Blood 110 2007 4005 4011
29. E. Jabbour, D. Jones, H.M. Kantarjian, and et al. Long-term outcome of patients with chronic myeloid leukemia treated with second-generation tyrosine kinase inhibitors after imatinib failure is predicted by the in vitro sensitivity of BCR-ABL kinase domain mutations Blood 114 2009 2037 2043
30. J.S. Khorashad, D. Milojkovic, P. Mehta, and et al. In vivo kinetics of kinase domain mutations in CML patients treated with dasatinib after failing imatinib Blood 111 2008 2378 2381
31. M.S. Zabriskie, C.A. Eide, S.K. Tantravahi, and et al. BCR-ABL1 compound mutations combining key kinase domain positions confer clinical resistance to ponatinib in Ph chromosome-positive leukemia Cancer Cell 26 2014 428 442
32. S. Redaelli, R. Piazza, R. Rostagno, and et al. Activity of bosutinib, dasatinib, and nilotinib against 18 imatinib-resistant BCR/ABL mutants J Clin Oncol 27 2009 469 471
33. J.E. Cortes, H.M. Kantarjian, T.H. Brummendorf, and et al. Safety and efficacy of bosutinib (SKI-606) in chronic phase Philadelphia chromosome-positive chronic myeloid leukemia patients with resistance or intolerance to imatinib Blood 118 2011 4567 4576
34. T. O'Hare, W.C. Shakespeare, X. Zhu, and et al. AP24534, a pan-BCR-ABL inhibitor for chronic myeloid leukemia, potently inhibits the T315I mutant and overcomes mutation-based resistance Cancer Cell 16 2009 401 412
35. J.E. Cortes, H. Kantarjian, N.P. Shah, and et al. Ponatinib in refractory Philadelphia chromosome-positive leukemias N Engl J Med 367 2012 2075 2088
36. S. Soverini, A. Hochhaus, F.E. Nicolini, and et al. BCR-ABL kinase domain mutation analysis in chronic myeloid leukemia patients treated with tyrosine kinase inhibitors: recommendations from an expert panel on behalf of European LeukemiaNet Blood 118 2011 1208 1215
37. M. Baccarani, M.W. Deininger, G. Rosti, and et al. European LeukemiaNet recommendations for the management of chronic myeloid leukemia: 2013 Blood 122 2013 872 884
38. D.C. Koboldt, K.M. Steinberg, D.E. Larson, R.K. Wilson, and E.R. Mardis The next-generation sequencing revolution and its impact on genomics Cell 155 2013 27 38
39. R.K. Thomas, E. Nickerson, J.F. Simons, and et al. Sensitive mutation detection in heterogeneous cancer specimens by massively parallel picoliter reactor sequencing Nat Med 12 2006 852 855
40. W. Qin, P. Kozlowski, B.E. Taillon, and et al. Ultra deep sequencing detects a low rate of mosaic mutations in tuberous sclerosis complex Hum Genet 127 2010 573 582
41. S. Gianella, W. Delport, M.E. Pacold, and et al. Detection of minority resistance during early HIV-1 infection: natural variation and spurious detection rather than transmission and evolution of multiple viral variants J Virol 85 2011 8359 8367
42. I. Vandenbroucke, H. Van Marck, P. Verhasselt, and et al. Minor variant detection in amplicons using 454 massive parallel pyrosequencing: experiences and considerations for successful applications Biotechniques 51 2011 167 177
43. S.Y. Ko, H.B. Oh, C.W. Park, H.C. Lee, and J.E. Lee Analysis of hepatitis B virus drug-resistant mutant haplotypes by ultra-deep pyrosequencing Clin Microbiol Infect 18 2012 E404 E411
44. C.A. Milbury, M. Correll, J. Quackenbush, R. Rubio, and G.M. Makrigiorgos COLD-PCR enrichment of rare cancer mutations prior to targeted amplicon resequencing Clin Chem 58 2012 580 589
45. L. Gong, Y. Han, L. Chen, and et al. Comparison of next-generation sequencing and clone-based sequencing in analysis of hepatitis B virus reverse transcriptase quasispecies heterogeneity J Clin Microbiol 51 2013 4087 4094
46. S. Soverini, C. De Benedittis, K. Machova Polakova, and et al. Unraveling the complexity of tyrosine kinase inhibitor-resistant populations by ultra-deep sequencing of the BCR-ABL kinase domain Blood 122 2013 1634 1648
47. K. Machova Polakova, V. Kulvait, A. Benesova, and et al. Next-generation deep sequencing improves detection of BCR-ABL1 kinase domain mutations emerging under tyrosine kinase inhibitor treatment of chronic myeloid leukemia patients in chronic phase J Cancer Res Clin Oncol November 4, 2014 Published online
48. B. Hanfstein, M.C. Muller, S. Kreil, and et al. Dynamics of mutant BCR-ABL-positive clones after cessation of tyrosine kinase inhibitor therapy Haematologica 96 2011 360 366
49. S. Soverini, C. De Benedittis, K. Machova Polakova, and et al. Ultra deep sequencing (UDS) allows more sensitive detection of tyrosine kinase inhibitor (TKI)-resistant BCR-ABL mutations that would influence therapeutic decision at the time of switchover to second- or third-line therapy Blood 122 2013 abstract #380
50. N.P. Shah, B.J. Skaggs, S. Branford, and et al. Sequential ABL kinase inhibitor therapy selects for compound drug-resistant BCR-ABL mutations with altered oncogenic potency J Clin Invest 117 2007 2562 2569
51. J.S. Khorashad, T.W. Kelley, P. Szankasi, and et al. BCR-ABL1 compound mutations in tyrosine kinase inhibitor-resistant CML: frequency and clonal relationships Blood 121 2013 489 498
52. D.L. Gibbons, S. Pricl, P. Posocco, and et al. Molecular dynamics reveal BCR-ABL1 polymutants as a unique mechanism of resistance to PAN-BCR-ABL1 kinase inhibitor therapy Proc Natl Acad Sci U S A 111 2014 3550 3555
53. W.T. Parker, S.R. Phillis, D.T. Yeung, T.P. Hughes, H.S. Scott, and S. Branford Many BCR-ABL1 compound mutations reported in chronic myeloid leukemia patients may actually be artifacts due to PCR-mediated recombination Blood 124 2014 153 155
54. I. Kinde, J. Wu, N. Papadopoulos, K.W. Kinzler, and B. Vogelstein Detection and quantification of rare mutations with massively parallel sequencing Proc Natl Acad Sci U S A 108 2011 9530 9535
55. M.W. Schmitt, S.R. Kennedy, J.J. Salk, E.J. Fox, J.B. Hiatt, and L.A. Loeb Detection of ultra-rare mutations by next-generation sequencing Proc Natl Acad Sci U S A 109 2012 14508 14513
56. T. Skorski Genetic mechanisms of chronic myeloid leukemia blastic transformation Curr Hematol Malig Rep 7 2012 87 93
57. E. Bolton-Gillespie, M. Schemionek, H.U. Klein, and et al. Genomic instability may originate from imatinib-refractory chronic myeloid leukemia stem cells Blood 121 2013 4175 4183
58. N. Hosoya, M. Sanada, Y. Nannya, and et al. Genomewide screening of DNA copy number changes in chronic myelogenous leukemia with the use of high-resolution array-based comparative genomic hybridization Genes Chromosomes Cancer 45 2006 482 494
59. D. Brazma, C. Grace, J. Howard, and et al. Genomic profile of chronic myelogenous leukemia: Imbalances associated with disease progression Genes Chromosomes Cancer 46 2007 1039 1050
60. J. Boultwood, J. Perry, A. Pellagatti, and et al. Frequent mutation of the polycomb-associated gene ASXL1 in the myelodysplastic syndromes and in acute myeloid leukemia Leukemia 24 2010 1062 1065
61. D. Nowak, S. Ogawa, M. Muschen, and et al. SNP array analysis of tyrosine kinase inhibitor-resistant chronic myeloid leukemia identifies heterogeneous secondary genomic alterations Blood 115 2010 1049 1053
62. J. Huh, Y.C. Mun, C.M. Seong, and W.S. Chung Single nucleotide polymorphism array-based karyotyping shows sequential genomic changes from monosomy to copy-neutral loss of heterozygosity of chromosome 7 and 20q deletion within a balanced translocation t(14;20) in AML Cancer Genet 204 2011 682 686
63. V.S. Nadarajan, C.L. Phan, C.H. Ang, and et al. Identification of copy number alterations by array comparative genomic hybridization in patients with late chronic or accelerated phase chronic myeloid leukemia treated with imatinib mesylate Int J Hematol 93 2011 465 473
64. X. Lu, X. Wang, Y. Kim, R. Zhang, S. Li, and J.Y. Lee Acquired genomic copy number changes in CML patients with the Philadelphia chromosome (Ph+) Cancer Genet 205 2012 513 518
65. S.T. Lee, Y. Ji, H.J. Kim, and et al. Sequential array comparative genomic hybridization analysis identifies copy number changes during blastic transformation of chronic myeloid leukemia Leuk Res 36 2012 418 421
66. N. Mori, M. Wada, J. Yokota, and et al. Mutations of the p53 tumour suppressor gene in haematologic neoplasms Br J Haematol 81 1992 235 240
67. A. Neubauer, M. He, C.A. Schmidt, D. Huhn, and E.T. Liu Genetic alterations in the p53 gene in the blast crisis of chronic myelogenous leukemia: analysis by polymerase chain reaction based techniques Leukemia 7 1993 593 600
68. A. Serra, A. Guerrasio, G. Gaidano, and et al. Molecular defects associated with the acute phase CML Leuk Lymphoma 11 suppl 1 1993 25 28
69. S. Peller, R. Yona, Y. Kopilova, and et al. Molecular alterations in the TP53 gene of peripheral blood cells of patients with chronic myeloid leukemia Genes Chromosomes Cancer 21 1998 2 7
70. H.G. Ahuja, P.S. Jat, A. Foti, M. Bar-Eli, and M.J. Cline Abnormalities of the retinoblastoma gene in the pathogenesis of acute leukemia Blood 78 1991 3259 3268
71. Z. Beck, A. Kiss, F.D. Toth, and et al. Alterations of P53 and RB genes and the evolution of the accelerated phase of chronic myeloid leukemia Leuk Lymphoma 38 2000 587 597
72. C. Roche-Lestienne, L. Deluche, S. Corm, and et al. RUNX1 DNA-binding mutations and RUNX1-PRDM16 cryptic fusions in BCR-ABL+ leukemias are frequently associated with secondary trisomy 21 and may contribute to clonal evolution and imatinib resistance Blood 111 2008 3735 3741
73. H. Sill, J.M. Goldman, and N.C. Cross Homozygous deletions of the p16 tumor-suppressor gene are associated with lymphoid transformation of chronic myeloid leukemia Blood 85 1995 2013 2016
74. A. Serra, E. Gottardi, F. Della Ragione, G. Saglio, and A. Iolascon Involvement of the cyclin-dependent kinase-4 inhibitor (CDKN2) gene in the pathogenesis of lymphoid blast crisis of chronic myelogenous leukaemia Br J Haematol 91 1995 625 629
75. A. Iolascon, F. Della Ragione, L. Giordani, A. Serra, G. Saglio, and M.F. Faienza Expression of cell cycle regulatory genes in chronic myelogenous leukemia Haematologica 83 1998 771 777
76. M.A. Haidar, X.B. Cao, T. Manshouri, and et al. p16INK4A and p15INK4B gene deletions in primary leukemias Blood 86 1995 311 315
77. H. Nakayama, F. Ishimaru, N. Avitahl, and et al. Decreases in Ikaros activity correlate with blast crisis in patients with chronic myelogenous leukemia Cancer Res 59 1999 3931 3934
78. C.G. Mullighan, C.B. Miller, I. Radtke, and et al. BCR-ABL1 lymphoblastic leukaemia is characterized by the deletion of Ikaros Nature 453 2008 110 114
79. H.G. Wendel, E. de Stanchina, E. Cepero, and et al. Loss of p53 impedes the antileukemic response to BCR-ABL inhibition Proc Natl Acad Sci U S A 103 2006 7444 7449
80. R.T. Williams, and C.J. Sherr The INK4-ARF (CDKN2A/B) locus in hematopoiesis and BCR-ABL-induced leukemias Cold Spring Harb Symp Quant Biol 73 2008 461 467
81. C.G. Mullighan, R.T. Williams, J.R. Downing, and C.J. Sherr Failure of CDKN2A/B (INK4A/B-ARF)-mediated tumor suppression and resistance to targeted therapy in acute lymphoblastic leukemia induced by BCR-ABL Genes Dev 22 2008 1411 1415
82. B. Calabretta, and D. Perrotti The biology of CML blast crisis Blood 103 2004 4010 4022
83. R.T. Williams, M.F. Roussel, and C.J. Sherr Arf gene loss enhances oncogenicity and limits imatinib response in mouse models of Bcr-Abl-induced acute lymphoblastic leukemia Proc Natl Acad Sci U S A 103 2006 6688 6693
84. L.J. Zhao, Y.Y. Wang, G. Li, and et al. Functional features of RUNX1 mutants in acute transformation of chronic myeloid leukemia and their contribution to inducing murine full-blown leukemia Blood 119 2012 2873 2882
85. K. Mitani, S. Ogawa, T. Tanaka, and et al. Generation of the AML1-EVI-1 fusion gene in the t(3;21)(q26;q22) causes blastic crisis in chronic myelocytic leukemia EMBO J 13 1994 504 510
86. M. Kurokawa, S. Ogawa, T. Tanaka, and et al. The AML1/Evi-1 fusion protein in the t(3;21) translocation exhibits transforming activity on Rat1 fibroblasts with dependence on the Evi-1 sequence Oncogene 11 1995 833 840
87. R. Toydemir, L. Rowe, M. Hibbard, M. Salama, and S. Shetty Cytogenetic and molecular characterization of double inversion 3 associated with a cryptic BCR-ABL1 rearrangement and additional genetic changes Cancer Genet Cytogenet 201 2010 81 87
88. A. De Weer, B. Poppe, B. Cauwelier, and et al. EVI1 activation in blast crisis CML due to juxtaposition to the rare 17q22 partner region as part of a 4-way variant translocation t(9;22) BMC Cancer 8 2008 193
89. K. Shimada, A. Tomita, Y. Minami, and et al. CML cells expressing the TEL/MDS1/EVI1 fusion are resistant to imatinib-induced apoptosis through inhibition of BAD, but are resensitized with ABT-737 Exp Hematol 40 2012 724 737.e2
90. I. Iacobucci, C.T. Storlazzi, D. Cilloni, and 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 114 2009 2159 2167
91. L. Wang, A. Howarth, and R.E. Clark Ikaros transcripts Ik6/10 and levels of full-length transcript are critical for chronic myeloid leukaemia blast crisis transformation Leukemia 28 2014 1745 1747
92. I. Joshi, T. Yoshida, N. Jena, and et al. Loss of Ikaros DNA-binding function confers integrin-dependent survival on pre-B cells and progression to acute lymphoblastic leukemia Nat Immunol 15 2014 294 304
93. T.A. Schwickert, H. Tagoh, S. Gultekin, and et al. Stage-specific control of early B cell development by the transcription factor Ikaros Nat Immunol 15 2014 283 293
94. S.J. Zhang, L.Y. Ma, Q.H. Huang, and et al. Gain-of-function mutation of GATA-2 in acute myeloid transformation of chronic myeloid leukemia Proc Natl Acad Sci U S A 105 2008 2076 2081
95. S.J. Zhang, J.Y. Shi, and J.Y. Li GATA-2 L359 V mutation is exclusively associated with CML progression but not other hematological malignancies and GATA-2 P250A is a novel single nucleotide polymorphism Leuk Res 33 2009 1141 1143
96. S. Soverini, J. Score, I. Iacobucci, and et al. IDH2 somatic mutations in chronic myeloid leukemia patients in blast crisis Leukemia 25 2011 178 181
97. V. Grossmann, A. Kohlmann, M. Zenger, and et al. A deep-sequencing study of chronic myeloid leukemia patients in blast crisis (BC-CML) detects mutations in 76.9% of cases Leukemia 25 2011 557 560
98. H. Makishima, A.M. Jankowska, M.A. McDevitt, and et al. CBL, CBLB, TET2, ASXL1, and IDH1/2 mutations and additional chromosomal aberrations constitute molecular events in chronic myelogenous leukemia Blood 117 2011 e198 e206
99. L.I. Shlush, S. Zandi, A. Mitchell, and et al. Identification of pre-leukaemic haematopoietic stem cells in acute leukaemia Nature 506 2014 328 333
100. L. Busque, J.P. Patel, M.E. Figueroa, and et al. Recurrent somatic TET2 mutations in normal elderly individuals with clonal hematopoiesis Nat Genet 44 2012 1179 1181
101. M. Xie, C. Lu, J. Wang, and et al. Age-related mutations associated with clonal hematopoietic expansion and malignancies Nat Med 20 2014 1472 1478
102. A. Kohlmann, H.U. Klein, S. Weissmann, and et al. The Interlaboratory RObustness of Next-generation sequencing (IRON) study: a deep sequencing investigation of TET2, CBL and KRAS mutations by an international consortium involving 10 laboratories Leukemia 25 2011 1840 1848
103. A. Kohlmann, G. Martinelli, M. Alikian, and et al. The Interlaboratory Robustness Of Next-Generation Sequencing (IRON) Study Phase II: Deep-Sequencing Analyses Of Hematological Malignancies Performed In 8,867 Cases By An International Network Involving 27 Laboratories Blood 122 2013 abstract #743
104. S. Soverini, T. Ernst, A. Kohlmann, and et al. Sensitivity, reproducibility and clinical utility of next-generation sequencing (NGS) for BCR-ABL1 kinase domain mutation screening: results from the CML work package of the Iron-II (Interlaboratory RObustness Of Next-Generation Sequencing) International Study Blood 122 2013 abstract #3284