Tyrosine kinase fusion genes in pediatric BCR-ABL1-like acute lymphoblastic leukemia

Oncotarget

Volumn 8, Issue 3, 2017, Pages 4618-4628

  Boer, Judith M ^a   Steeghs, Elisabeth M P ^a   Marchante, João R M ^a   Boeree, Aurélie ^a   Beaudoin, James J ^a   Beverloo, H Berna ^b,c   Kuiper, Roland P ^d   Escherich, Gabriele ^e   van der Velden, Vincent H J ^b   van der Schoot, C Ellen ^f   de Groot Kruseman, Hester A ^c   Pieters, Rob ^c,g   den Boer, Monique L ^a,c  

^a SOPHIA CHILDREN S HOSPITAL   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c Dutch Childhood Oncology Group DCOG   (Netherlands)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^e German Cooperative Study Group for Childhood Acute Lymphoblastic Leukemia (COALL)   (Germany)

^f UNIVERSITY OF AMSTERDAM   (Netherlands)

^g Department of Radiation Oncology   (Netherlands)

Author keywords

BCR ABL1 like; Minimal residual disease; Pediatric B cell precursor acute lymphoblastic leukemia; Tyrosine kinase fusion

Indexed keywords

PROTEIN TYROSINE KINASE; ARG TYROSINE KINASE; BCR ABL PROTEIN; BCR-ABL1 FUSION PROTEIN, HUMAN; IKAROS TRANSCRIPTION FACTOR; IKZF1 PROTEIN, HUMAN; JAK2 PROTEIN, HUMAN; JANUS KINASE 2; ONCOPROTEIN; RCSD1 PROTEIN, HUMAN; SIGNAL PEPTIDE; TELOMERIC REPEAT BINDING FACTOR 2; TERF2 PROTEIN, HUMAN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; B LYMPHOCYTE; BCR ABL1 GENE; CANCER MORTALITY; CANCER PROGNOSIS; CANCER RECURRENCE; CHILD; COHORT ANALYSIS; CONTROLLED STUDY; CRLF2 GENE; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; FUSION GENE; GENE; GENE DELETION; GENE EXPRESSION; GENE FUSION; GENE MUTATION; GENE OVEREXPRESSION; HIGH RISK POPULATION; HUMAN; HUMAN CELL; IKZF1 GENE; MAJOR CLINICAL STUDY; MALE; PEDIATRICS; POLYMERASE CHAIN REACTION SYSTEM; PROTEIN EXPRESSION; RCSD1 ABL2 GENE; RECURRENCE RISK; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SANGER SEQUENCING; SEX DIFFERENCE; TERF2 JAK2 GENE; TREATMENT RESPONSE; ADOLESCENT; DNA MICROARRAY; GENETICS; GERMANY; MUTATION; NETHERLANDS; YOUNG ADULT;

ADOLESCENT; COHORT STUDIES; FEMALE; FUSION PROTEINS, BCR-ABL; GENE DELETION; GERMANY; HUMANS; IKAROS TRANSCRIPTION FACTOR; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JANUS KINASE 2; MALE; MUTATION; NETHERLANDS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ONCOGENE PROTEINS, FUSION; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEIN-TYROSINE KINASES; TELOMERIC REPEAT BINDING PROTEIN 2; YOUNG ADULT;

EID: 85011955178     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.13492     Document Type: Article

References (32)

1. Biondi A, Schrappe M, De Lorenzo P, Castor A, Lucchini G, Gandemer V, Pieters R, Stary J, Escherich G, Campbell M, Li CK, Vora A, Arico M, et al. Imatinib after induction for treatment of children and adolescents with Philadelphiachromosome-positive acute lymphoblastic leukaemia (EsPhALL): a randomised, open-label, intergroup study. Lancet Oncol. 2012; 13:936-945.
2. Schultz KR, Carroll A, Heerema NA, Bowman WP, Aledo A, Slayton WB, Sather H, Devidas M, Zheng HW, Davies SM, Gaynon PS, Trigg M, Rutledge R, et al. Long-term follow-up of imatinib in pediatric Philadelphia chromosome-positive acute lymphoblastic leukemia: Children's Oncology Group study AALL0031. Leukemia. 2014; 28:1467-1471.
3. Den Boer ML, van Slegtenhorst M, De Menezes RX, Cheok MH, Buijs-Gladdines JG, Peters ST, Van Zutven LJ, Beverloo HB, Van der Spek PJ, Escherich G, Horstmann MA, Janka-Schaub GE, Kamps WA, et al. A subtype of childhood acute lymphoblastic leukaemia with poor treatment outcome: a genome-wide classification study. Lancet Oncol. 2009; 10:125-134.
4. Mullighan CG, Su X, Zhang J, Radtke I, Phillips LA, Miller CB, Ma J, Liu W, Cheng C, Schulman BA, Harvey RC, Chen IM, Clifford RJ, et al. Deletion of IKZF1 and prognosis in acute lymphoblastic leukemia. N Engl J Med. 2009; 360:470-480.
5. Van der Veer A, Waanders E, Pieters R, Willemse ME, Van Reijmersdal SV, Russel LJ, Harrison CJ, Evans WE, Van der Velden VHJ, Hoogerbrugge PM, Van Leeuwen F, Escherich G, Horstmann MA, et al. Independent prognostic value of BCR-ABL1-like signature and IKZF1 deletion, but not high CRLF2 expression, in children with B-cell precursor ALL. Blood. 2013; 122:2622-2629.
6. Roberts KG, Li Y, Payne-Turner D, Harvey RC, Yang YL, Pei D, McCastlain K, Ding L, Lu C, Song G, Ma J, Becksfort J, Rusch M, et al. Targetable kinase-activating lesions in Ph-like acute lymphoblastic leukemia. N Engl J Med. 2014; 371:1005-1015.
7. Roberts KG, Morin RD, Zhang J, Hirst M, Zhao Y, Su X, Chen SC, Payne-Turner D, Churchman ML, Harvey RC, Chen X, Kasap C, Yan C, et al. Genetic alterations activating kinase and cytokine receptor signaling in highrisk acute lymphoblastic leukemia. Cancer Cell. 2012; 22:153-166.
8. Izraeli S. Beyond Philadelphia: 'Ph-like' B cell precursor acute lymphoblastic leukemias-diagnostic challenges and therapeutic promises. Curr Opin Hematol. 2014; 21:289-296.
9. Imamura T, Kiyokawa N, Kato M, Imai C, Okamoto Y, Yano M, Ohki K, Yamashita Y, Kodama Y, Saito A, Mori M, Ishimaru S, Deguchi T, et al. Characterization of pediatric Philadelphia-negative B-cell precursor acute lymphoblastic leukemia with kinase fusions in Japan. Blood Cancer J. 2016; 6:e419.
10. Schwab C, Ryan SL, Chilton L, Elliott A, Murray J, Richardson S, Wragg C, Moppett J, Cummins M, Tunstall O, Parker CA, Saha V, Goulden N, et al. EBF1-PDGFRB fusion in pediatric B-cell precursor acute lymphoblastic leukemia (BCP-ALL): genetic profile and clinical implications. Blood. 2016; 127:2214-2218.
11. Zaliova M, Moorman AV, Cazzaniga G, Stanulla M, Harvey RC, Roberts KG, Heatley SL, Loh ML, Konopleva M, Chen IM, Zimmermannova O, Schwab C, Smith O, et al. Characterization of leukemias with ETV6-ABL1 fusion. Haematologica. 2016; 101:1082-1093.
12. Soler G, Radford-Weiss I, Ben-Abdelali R, Mahlaoui N, Ponceau JF, Macintyre EA, Vekemans M, Bernard OA, Romana SP. Fusion of ZMIZ1 to ABL1 in a B-cell acute lymphoblastic leukaemia with a t(9;10)(q34;q22.3) translocation. Leukemia. 2008; 22:1278-1280.
13. Ernst T, Score J, Deininger M, Hidalgo-Curtis C, Lackie P, Ershler WB, Goldman JM, Cross NC, Grand F. Identification of FOXP1 and SNX2 as novel ABL1 fusion partners in acute lymphoblastic leukaemia. Br J Haematol. 2011; 153:43-46.
14. Zhou X, Edmonson MN, Wilkinson MR, Patel A, Wu G, Liu Y, Li Y, Zhang Z, Rusch MC, Parker M, Becksfort J, Downing JR, Zhang J. Exploring genomic alteration in pediatric cancer using ProteinPaint. Nature Genetics. 2015; 48:4-6.
15. Steeghs EMP, Jerchel IS, de Goffau-Nobel W, Hoogkamer AQ, Boer JM, Boeree A, van de Ven C, Koudijs MJ, Cuppen E, De Groot-Kruseman HA, Horstmann MA, Pieters R, Den Boer ML. JAK2 aberrations in childhood precursor B cell acute lymphoblastic leukemia. Submitted.
16. Boer JM, Marchante JRM, Evans WE, Horstmann MA, Escherich G, Pieters R, Den Boer ML. BCR-ABL1-Like Cases in Pediatric Acute Lymphoblastic Leukemia: a Comparison Between DCOG/Erasmus MC and COG/St. Jude Signatures. Haematologica 2015; 100:e354-357.
17. Escherich G, Zur Stadt U, Alawi M, Horstmann M. Rapid capture targeted next generation sequencing (NGS) for detection of genomic kinase-and cytokine receptor rearrangements in B-precursor acute lymphoblastic leukemia. Annual Meeting Abstracts Blood. 2015; 126:2609.
18. Kuiper RP, Van Reijmersdal SV, Simonis M, Yu J, Sonneveld E, Scheijen B, Boer JM, Boeree A, Klous P, Hoogerbrugge P, Yilmaz M, Van Leeuwen FN, Den Boer ML, et al. Targeted locus amplification & next generation sequencing for the detection of recurrent and novel gene fusions for improved treatment decisions in pediatric acute lymphoblastic leukemia. Annual Meeting Abstracts Blood. 2015; 126:696.
19. Roberts KG, Pei D, Campana D, Payne-Turner D, Li Y, Cheng C, Sandlund JT, Jeha S, Easton J, Becksfort J, Zhang J, Coustan-Smith E, Raimondi SC, et al. Outcomes of Children With BCR-ABL1-Like Acute Lymphoblastic Leukemia Treated With Risk-Directed Therapy Based on the Levels of Minimal Residual Disease. Journal of Clinical Oncology. 2014; 32:3012-3020.
20. Weston BW, Hayden MA, Roberts KG, Bowyer S, Hsu J, Fedoriw G, Rao KW, Mullighan CG. Tyrosine Kinase Inhibitor Therapy Induces Remission in a Patient With Refractory EBF1-PDGFRB-Positive Acute Lymphoblastic Leukemia. Journal of Clinical Oncology. 2013; 31:e413-416.
21. Lengline E, Beldjord K, Dombret H, Soulier J, Boissel N, Clappier E. Successful tyrosine kinase inhibitor therapy in a refractory B-cell precursor acute lymphoblastic leukemia with EBF1-PDGFRB fusion. Haematologica. 2013; 98:e146-148.
22. Kamps WA, van der Pal-de Bruin KM, Veerman AJ, Fiocco M, Bierings M, Pieters R. Long-term results of Dutch Childhood Oncology Group studies for children with acute lymphoblastic leukemia from 1984 to 2004. Leukemia. 2010; 24:309-319.
23. Escherich G, Horstmann MA, Zimmermann M, Janka-Schaub GE, Grp CS. Cooperative study group for childhood acute lymphoblastic leukaemia (COALL): long-term results of trials 82, 85, 89, 92 and 97. Leukemia. 2010; 24:298-308.
24. Escherich G, Zimmermann M, Janka-Schaub G. Doxorubicin or daunorubicin given upfront in a therapeutic window are equally effective in children with newly diagnosed acute lymphoblastic leukemia. A randomized comparison in trial CoALL 07-03. Pediatr Blood Cancer. 2013; 60:254-257.
25. Den Boer ML, Harms DO, Pieters R, Kazemier KM, Göbel U, Körholz D, Graubner U, Haas RJ, Jorch NJ, Spaar HJ, Kaspers GJL, Kamps WA, Van der Does-Van den Berg A, et al. Patient stratification based on prednisolone-vincristineasparaginase resistance profiles in children with acute lymphoblastic leukemia. J Clin Oncol. 2003; 21:3262-3268.
26. de Vree PJ, de Wit E, Yilmaz M, van de Heijning M, Klous P, Verstegen MJ, Wan Y, Teunissen H, Krijger PH, Geeven G, Eijk PP, Sie D, Ylstra B, et al. Targeted sequencing by proximity ligation for comprehensive variant detection and local haplotyping. Nat Biotechnol. 2014; 32:1019-1025.
27. van de Wiel MA, Kim KI, Vosse SJ, van Wieringen WN, Wilting SM, Ylstra B. CGHcall: calling aberrations for array CGH tumor profiles. Bioinformatics. 2007; 23:892-894.
28. van Houte BP, Binsl TW, Hettling H, Pirovano W, Heringa J. CGHnormaliter: an iterative strategy to enhance normalization of array CGH data with imbalanced aberrations. BMC Genomics. 2009; 10:401.
29. Boer JM, Koenders JE, van der Holt B, Exalto C, Sanders MA, Cornelissen JJ, Valk PJ, den Boer ML, Rijneveld AW. Expression profiling of adult acute lymphoblastic leukemia identifies a BCR-ABL1-like subgroup characterized by high non-response and relapse rates. Haematologica. 2015; 100:e261-264.
30. Gray RJ. cmprsk: Subdistribution Analysis of Competing Risks. R package version 22-6 2013; http://CRAN.Rproject. org/package=cmprsk.
31. De Wreede LC, Fiocco M, Putter H. mstate: An R Package for the Analysis of Competing Risks and Multi-State Models. J Stat Softw. 2011; 38:1-30.
32. Therneau T. A Package for Survival Analysis in S. R package version 236-12. 2012.