Genomic and transcriptional landscape of P2RY8-CRLF2-positive childhood acute lymphoblastic leukemia

Leukemia

Volumn 31, Issue 7, 2017, Pages 1491-1501

  Vesely, C ^a   Frech, C ^a   Eckert, C ^b   Cario, G ^c   Mecklenbrauker A ^a   Zur Stadt, U ^d   Nebral, K ^a   Kraler, F ^a   Fischer, S ^a   Attarbaschi, A ^e   Schuster, M ^f   Bock, C ^f   Cave H ^g   Von Stackelberg, A ^b   Schrappe, M ^c   Horstmann, M A ^d   Mann, G ^e   Haas, O A ^a,e   Panzer Grumayer R ^a  

^a CHILDREN'S CANCER RESEARCH INSTITUTE   (Austria)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^d UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^e MEDICAL UNIVERSITY OF VIENNA   (Austria)

^f ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^g INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYCLIN DEPENDENT KINASE INHIBITOR 2B; JANUS KINASE 1; JANUS KINASE 2; PROTEIN KINASE SYK; RAS PROTEIN; STAT PROTEIN; TRANSCRIPTION FACTOR ETV6; TRANSCRIPTION FACTOR PAX5; CRLF2 PROTEIN, HUMAN; CYTOKINE RECEPTOR; IKAROS TRANSCRIPTION FACTOR; IKZF1 PROTEIN, HUMAN; JANUS KINASE; P2RY8 PROTEIN, HUMAN; PURINERGIC P2Y RECEPTOR;

ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL HYPOXIA; CHILD; CHILDHOOD LEUKEMIA; CLINICAL ARTICLE; CLINICAL TRIAL (TOPIC); CONTROLLED STUDY; CRLF2 GENE; DRUG RESISTANCE; EBF1 GENE; FEMALE; FOCAL ADHESION; GENE; GENE DELETION; GENE MUTATION; GENETIC HETEROGENEITY; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; IKZF1 GENE; IKZF3 GENE; LEUKEMIA RELAPSE; LEUKEMOGENESIS; LYMPHOID CELL; MALE; MOLECULAR CLONING; MULTIPLEX LIGATION DEPENDENT PROBE AMPLIFICATION; MUTATIONAL ANALYSIS; P2RY8 GENE; PRESCHOOL CHILD; PRIORITY JOURNAL; SCHOOL CHILD; SINGLE NUCLEOTIDE POLYMORPHISM; STEM CELL; WHOLE EXOME SEQUENCING; ADOLESCENT; GENE DOSAGE; GENE FUSION; GENETIC TRANSCRIPTION; GENETICS; GENOMICS; INFANT; PHYSIOLOGY; TUMOR SUPPRESSOR GENE;

ADOLESCENT; CHILD; CHILD, PRESCHOOL; GENE DOSAGE; GENE FUSION; GENES, TUMOR SUPPRESSOR; GENOMICS; HUMANS; IKAROS TRANSCRIPTION FACTOR; INFANT; JANUS KINASES; POLYMORPHISM, SINGLE NUCLEOTIDE; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; RECEPTORS, CYTOKINE; RECEPTORS, PURINERGIC P2Y; STAT TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 85008313637     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2016.365     Document Type: Article

References (60)

1. Hunger SP, Mullighan CG. Redefining ALL classification: toward detecting highrisk ALL and implementing precision medicine. Blood 2015; 125: 3977-3987.
2. Russell LJ, Capasso M, Vater I, Akasaka T, Bernard OA, Calasanz MJ et al. Deregulated expression of cytokine receptor gene, CRLF2, is involved in lymphoid transformation in B-cell precursor acute lymphoblastic leukemia. Blood 2009; 114: 2688-2698.
3. Mullighan CG, Collins-Underwood JR, Phillips LA, Loudin MG, Liu W, Zhang J et al. Rearrangement of CRLF2 in B-progenitor- and down syndrome-associated acute lymphoblastic leukemia. Nat Genet 2009; 41: 1243-1246.
4. Hertzberg L, Vendramini E, Ganmore I, Cazzaniga G, Schmitz M, Chalker J 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 International BFM Study Group. Blood 2010; 115: 1006-1017.
5. Chen IM, Harvey RC, Mullighan CG, Gastier-Foster J, Wharton W, Kang H et al. Outcome modeling with CRLF2, IKZF1, JAK, and minimal residual disease in pediatric acute lymphoblastic leukemia: a Children's Oncology Group study. Blood 2012; 119: 3512-3522.
6. Yoda A, Yoda Y, Chiaretti S, Bar-Natan M, Mani K, Rodig SJ et al. Functional screening identifies CRLF2 in precursor B-cell acute lymphoblastic leukemia. Proc Natl Acad Sci USA 2010; 107: 252-257.
7. Tsai AG, Yoda A, Weinstock DM, Lieber MR. t(X;14)(p22;q32)/t(Y;14)(p11;q32) CRLF2-IGH translocations from human B-lineage ALLs involve CpG-type breaks at CRLF2, but CRLF2/P2RY8 intrachromosomal deletions do not. Blood 2010; 116: 1993-1994.
8. Ensor HM, Schwab C, Russell LJ, Richards SM, Morrison H, Masic D et al. Demographic, clinical, and outcome features of children with acute lymphoblastic leukemia and CRLF2 deregulation: results from the MRC ALL97 clinical trial. Blood 2011; 117: 2129-2136.
9. Morak M, Attarbaschi A, Fischer S, Nassimbeni C, Grausenburger R, Bastelberger S et al. Small sizes and indolent evolutionary dynamics challenge the potential role of P2RY8-CRLF2-harboring clones as main relapse-driving force in childhood ALL. Blood 2012; 120: 5134-5142.
10. Harvey RC, Mullighan CG, Chen IM, Wharton W, Mikhail FM, Carroll AJ 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: 5312-5321.
11. Harvey RC, Mullighan CG, Wang X, Dobbin KK, Davidson GS, Bedrick EJ et al. Identification of novel cluster groups in pediatric high-risk B-precursor acute lymphoblastic leukemia with gene expression profiling: correlation with genomewide DNA copy number alterations, clinical characteristics, and outcome. Blood 2010; 116: 4874-4884.
12. Palmi C, Vendramini E, Silvestri D, Longinotti G, Frison D, Cario G et al. Poor prognosis for P2RY8-CRLF2 fusion but not for CRLF2 over-expression in children with intermediate risk B-cell precursor acute lymphoblastic leukemia. Leukemia 2012; 26: 2245-2253.
13. Cario G, Zimmermann M, Romey R, Gesk S, Vater I, Harbott J 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 ALL-BFM 2000 protocol. Blood 2010; 115: 5393-5397.
14. Attarbaschi A, Morak M, Cario G, Cazzaniga G, Ensor HM, te Kronnie T et al. Treatment outcome of CRLF2-rearranged childhood acute lymphoblastic leukaemia: a comparative analysis of the AIEOP-BFM and UK NCRI-CCLG study groups. Br J Haematol 2012; 158: 772-777.
15. Georgopoulos K. Haematopoietic cell-fate decisions, chromatin regulation and ikaros. Nat Rev Immunol 2002; 2: 162-174.
16. 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.
17. 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.
18. Boer JM, van der Veer A, Rizopoulos D, Fiocco M, Sonneveld E, de Groot-Kruseman HA et al. Prognostic value of rare IKZF1 deletion in childhood B-cell precursor acute lymphoblastic leukemia: an international collaborative study. Leukemia 2016; 30: 32-38.
19. Clappier E, Grardel N, Bakkus M, Rapion J, De Moerloose B, Kastner P et al. IKZF1 deletion is an independent prognostic marker in childhood B-cell precursor acute lymphoblastic leukemia, and distinguishes patients benefiting from pulses during maintenance therapy: results of the EORTC Children's Leukemia Group study 58951. Leukemia 2015; 29: 2154-2161.
20. Dorge P, Meissner B, Zimmermann M, Moricke A, Schrauder A, Bouquin JP et al. IKZF1 deletion is an independent predictor of outcome in pediatric acute lymphoblastic leukemia treated according to the ALL-BFM 2000 protocol. Haematologica 2013; 98: 428-432.
21. Palmi C, Lana T, Silvestri D, Savino A, Kronnie GT, Conter V et al. Impact of IKZF1 deletions on IKZF1 expression and outcome in Philadelphia chromosome negative childhood BCP-ALL. Reply to 'incidence and biological significance of IKZF1/Ikaros gene deletions in pediatric Philadelphia chromosome negative and Philadelphia chromosome positive B-cell precursor acute lymphoblastic leukemia'. Haematologica 2013; 98: e164-e165.
22. Asai D, Imamura T, Suenobu S, Saito A, Hasegawa D, Deguchi T et al. IKZF1 deletion is associated with a poor outcome in pediatric B-cell precursor acute lymphoblastic leukemia in Japan. Cancer Med 2013; 2: 412-419.
23. Buitenkamp TD, Pieters R, Gallimore NE, van der Veer A, Meijerink JP, Beverloo HB et al. Outcome in children with Down's syndrome and acute lymphoblastic leukemia: role of IKZF1 deletions and CRLF2 aberrations. Leukemia 2012; 26: 2204-2211.
24. Den Boer ML, van Slegtenhorst M, De Menezes RX, Cheok MH, Buijs-Gladdines JG, Peters ST et al. A subtype of childhood acute lymphoblastic leukaemia with poor treatment outcome: a genome-wide classification study. Lancet Oncol 2009; 10: 125-134.
25. van der Veer A, Zaliova M, Mottadelli F, De Lorenzo P, Te Kronnie G, Harrison CJ et al. IKZF1 status as a prognostic feature in BCR-ABL1-positive childhood ALL. Blood 2014; 123: 1691-1698.
26. Roberts KG, Morin RD, Zhang J, Hirst M, Zhao Y, Su X et al. Genetic alterations activating kinase and cytokine receptor signaling in high-risk acute lymphoblastic leukemia. Cancer Cell 2012; 22: 153-166.
27. Churchman ML, Low J, Qu C, Paietta EM, Kasper LH, Chang Y et al. Efficacy of retinoids in IKZF1-mutated BCR-ABL1 acute lymphoblastic leukemia. Cancer Cell 2015; 28: 343-356.
28. Iacobucci I, Iraci N, Messina M, Lonetti A, Chiaretti S, Valli E et al. IKAROS deletions dictate a unique gene expression signature in patients with adult B-cell acute lymphoblastic leukemia. PLoS One 2012; 7: e40934.
29. von Stackelberg A, Seeger K, Henze G, Eckert C. Clinical significance of minimal residual disease in childhood acute lymphoblastic leukemia after first relapse. Leukemia 2004; 18: 1727-1728.
30. Malinowska-Ozdowy K, Frech C, Schonegger A, Eckert C, Cazzaniga G, Stanulla M et al. KRAS and CREBBP mutations: a relapse-linked malicious liaison in childhood high hyperdiploid acute lymphoblastic leukemia. Leukemia 2015; 29: 1656-1667.
31. Mullighan CG, Zhang J, Harvey RC, Collins-Underwood JR, Schulman BA, Phillips LA et al. JAK mutations in high-risk childhood acute lymphoblastic leukemia. Proc Natl Acad Sci USA 2009; 106: 9414-9418.
32. Izraeli S, Shochat C, Tal N, Geron I. Towards precision medicine in childhood leukemia-insights from mutationally activated cytokine receptor pathways in acute lymphoblastic leukemia. Cancer Lett 2014; 352: 15-20.
33. Sakaguchi H, Okuno Y, Muramatsu H, Yoshida K, Shiraishi Y, Takahashi M et al. Exome sequencing identifies secondary mutations of SETBP1 and JAK3 in juvenile myelomonocytic leukemia. Nat Genet 2013; 45: 937-941.
34. Bains T, Heinrich MC, Loriaux MM, Beadling C, Nelson D, Warrick A et al. Newly described activating JAK3 mutations in T-cell acute lymphoblastic leukemia. Leukemia 2012; 26: 2144-2146.
35. Degryse S, de Bock CE, Cox L, Demeyer S, Gielen O, Mentens N et al. JAK3 mutants transform hematopoietic cells through JAK1 activation, causing T-cell acute lymphoblastic leukemia in a mouse model. Blood 2014; 124: 3092-3100.
36. Shochat C, Tal N, Bandapalli OR, Palmi C, Ganmore I, te Kronnie G et al. Gain-offunction mutations in interleukin-7 receptor-alpha (IL7R) in childhood acute lymphoblastic leukemias. J Exp Med 2011; 208: 901-908.
37. Nikolaev SI, Garieri M, Santoni F, Falconnet E, Ribaux P, Guipponi M et al. Frequent cases of RAS-mutated Down syndrome acute lymphoblastic leukaemia lack JAK2 mutations. Nat Commun 2014; 5: 4654.
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. Topka S, Vijai J, Walsh MF, Jacobs L, Maria A, Villano D et al. Germline ETV6 mutations confer susceptibility to acute lymphoblastic leukemia and thrombocytopenia. PLoS Genet 2015; 11: e1005262.
40. Olsson L, Albitar F, Castor A, Behrendtz M, Biloglav A, Paulsson K et al. Cooperative genetic changes in pediatric B-cell precursor acute lymphoblastic leukemia with deletions or mutations of IKZF1. Genes Chromosomes Cancer 2015; 54: 315-325.
41. Olsson L, Johansson B. Ikaros and leukaemia. Br J Haematol 2015; 169: 479-491.
42. Mullighan CG, Zhang J, Kasper LH, Lerach S, Payne-Turner D, Phillips LA et al. CREBBP mutations in relapsed acute lymphoblastic leukaemia. Nature 2011; 471: 235-239.
43. Mar BG, Bullinger LB, McLean KM, Grauman PV, Harris MH, Stevenson K et al. Mutations in epigenetic regulators including SETD2 are gained during relapse in paediatric acute lymphoblastic leukaemia. Nat Commun 2014; 5: 3469.
44. Zhu X, He F, Zeng H, Ling S, Chen A, Wang Y et al. Identification of functional cooperative mutations of SETD2 in human acute leukemia. Nat Genet 2014; 46: 287-293.
45. Marke R, Havinga J, Cloos J, Demkes M, Poelmans G, Yuniati L et al. Tumor suppressor IKZF1 mediates glucocorticoid resistance in B-cell precursor acute lymphoblastic leukemia. Leukemia 2015; 30: 1599-1603.
46. Schwickert TA, Tagoh H, Gultekin S, Dakic A, Axelsson E, Minnich M et al. Stagespecific control of early B cell development by the transcription factor Ikaros. Nat Immunol 2014; 15: 283-293.
47. Joshi I, Yoshida T, Jena N, Qi X, Zhang J, Van Etten RA et al. Loss of Ikaros DNA-binding function confers integrin-dependent survival on pre-B cells and progression to acute lymphoblastic leukemia. Nat Immunol 2014; 15: 294-304.
48. Heizmann B, Kastner P, Chan S. Ikaros is absolutely required for pre-B cell differentiation by attenuating IL-7 signals. J Exp Med 2013; 210: 2823-2832.
49. 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.
50. Kuiper RP, Waanders E, van der Velden VH, van Reijmersdal SV, Venkatachalam R, Scheijen B et al. IKZF1 deletions predict relapse in uniformly treated pediatric precursor B-ALL. Leukemia 2010; 24: 1258-1264.
51. Xavier AC, Ge Y, Taub J. Unique clinical and biological features of leukemia in Down syndrome children. Expert Rev Hematol 2010; 3: 175-186.
52. Buitenkamp TD, Izraeli S, Zimmermann M, Forestier E, Heerema NA, van den Heuvel-Eibrink MM et al. Acute lymphoblastic leukemia in children with Down syndrome: a retrospective analysis from the Ponte di Legno study group. Blood 2014; 123: 70-77.
53. van Bodegom D, Zhong J, Kopp N, Dutta C, Kim MS, Bird L et al. Differences in signaling through the B-cell leukemia oncoprotein CRLF2 in response to TSLP and through mutant JAK2. Blood 2012; 120: 2853-2863.
54. Roll JD, Reuther GW. CRLF2 and JAK2 in B-progenitor acute lymphoblastic leukemia: a novel association in oncogenesis. Cancer Res 2010; 70: 7347-7352.
55. Tasian SK, Doral MY, Borowitz MJ, Wood BL, Chen IM, Harvey RC et al. Aberrant STAT5 and PI3K/mTOR pathway signaling occurs in human CRLF2-rearranged B-precursor acute lymphoblastic leukemia. Blood 2012; 120: 833-842.
56. Maude SL, Tasian SK, Vincent T, Hall JW, Sheen C, Roberts KG et al. Targeting JAK1/2 and mTOR in murine xenograft models of Ph-like acute lymphoblastic leukemia. Blood 2012; 120: 3510-3518.
57. Steelman LS, Abrams SL, Whelan J, Bertrand FE, Ludwig DE, Basecke J et al. Contributions of the Raf/MEK/ERK, PI3K/PTEN/Akt/mTOR and Jak/STAT pathways to leukemia. Leukemia 2008; 22: 686-707.
58. Greaves M, Maley CC. Clonal evolution in cancer. Nature 2012; 481: 306-313.
59. Park SY, Wolfram P, Canty K, Harley B, Nombela-Arrieta C, Pivarnik G et al. Focal adhesion kinase regulates the localization and retention of pro-B cells in bone marrow microenvironments. J Immunol 2013; 190: 1094-1102.
60. Dupuis A, Gaub MP, Legrain M, Drenou B, Mauvieux L, Lutz P et al. Biclonal and biallelic deletions occur in 20% of B-ALL cases with IKZF1 mutations. Leukemia 2013; 27: 503-507.