The mutational landscape in pediatric acute lymphoblastic leukemia deciphered by whole genome sequencing

Human Mutation

Volumn 36, Issue 1, 2015, Pages 118-128

  Lindqvist, Carl Mårten ^a   Nordlund, Jessica ^a   Ekman, Diana ^b   Johansson, Anna ^a   Moghadam, Behrooz Torabi ^a   Raine, Amanda ^a   Övernäs, Elin ^a   Dahlberg, Johan ^a   Wahlberg, Per ^a   Henriksson, Niklas ^a   Abrahamsson, Jonas ^c,h   Frost, Britt Marie ^d,h   Grandér, Dan ^e   Heyman, Mats ^f,h   Larsson, Rolf ^a   Palle, Josefine ^a,d,h   Söderhäll, Stefan ^f,h   Forestier, Erik ^g,h   Lönnerholm, Gudmar ^d,h   Syvänen, Ann Christine ^a   Berglund, Eva C ^a   more..

^a UPPSALA UNIVERSITY   (Sweden)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c QUEEN SILVIA CHILDREN'S HOSPITAL   (Sweden)

^d UNIVERSITY CHILDREN S HOSPITAL   (Sweden)

^e KAROLINSKA INSTITUTE   (Sweden)

^f KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^g UMEÅ UNIVERSITY   (Sweden)

^h Nordic Society of Pediatric Hematology and Oncology   (Sweden)

Author keywords

Acute lymphoblastic leukemia; Clonal heterogeneity; RNA sequencing; Whole genome sequencing

Indexed keywords

DNA BINDING PROTEIN; KIF1B PROTEIN, HUMAN; KINESIN; MDK PROTEIN, HUMAN; MLL2 PROTEIN, HUMAN; NERVE GROWTH FACTOR; TUMOR PROTEIN;

ACUTE LYMPHOBLASTIC LEUKEMIA; CHILD; DNA SEQUENCE; FEMALE; GENETICS; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN GENOME; INFANT; MALE; MUTATION; PRESCHOOL CHILD; PROCEDURES; SEQUENCE ANALYSIS;

CHILD; CHILD, PRESCHOOL; DNA-BINDING PROTEINS; FEMALE; GENOME, HUMAN; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INFANT; KINESIN; MALE; MUTATION; NEOPLASM PROTEINS; NERVE GROWTH FACTORS; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, RNA;

EID: 84920094708     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.22719     Document Type: Article

References (62)

1. Al-Shehhi H, Konn ZJ, Schwab CJ, Erhorn A, Barber KE, Wright SL, Gabriel AS, Harrison CJ, Moorman AV. 2013. Abnormalities of the der(12)t(12;21) in ETV6-RUNX1 acute lymphoblastic leukemia. Genes Chromosomes Cancer 52:202-213.
2. Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, Bignell GR, Bolli N, Borg A, Borresen-Dale AL, Boyault S, Burkhardt B, et al. 2013. Signatures of mutational processes in human cancer. Nature 500:415-421.
3. Atak ZK, Gianfelici V, Hulselmans G, De Keersmaecker K, Devasia AG, Geerdens E, Mentens N, Chiaretti S, Durinck K, Uyttebroeck A, Vandenberghe P, Wlodarska I, et al. 2013. Comprehensive analysis of transcriptome variation uncovers known and novel driver events in T-cell acute lymphoblastic leukemia. PLoS Genet 9:e1003997.
4. Berglund EC, Lindqvist CM, Hayat S, Overnas E, Henriksson N, Nordlund J, Wahlberg P, Forestier E, Lonnerholm G, Syvanen AC. 2013. Accurate detection of subclonal single nucleotide variants in whole genome amplified and pooled cancer samples using HaloPlex target enrichment. BMC Genomics 14:856.
5. Bernstein BE, Stamatoyannopoulos JA, Costello JF, Ren B, Milosavljevic A, Meissner A, Kellis M, Marra MA, Beaudet AL, Ecker JR, Farnham PJ, Hirst M, et al. 2010. The NIH Roadmap Epigenomics Mapping Consortium. Nat Biotechnol 28:1045-1048.
6. Boeva V, Zinovyev A, Bleakley K, Vert JP, Janoueix-Lerosey I, Delattre O, Barillot E. 2011. Control-free calling of copy number alterations in deep-sequencing data using GC-content normalization. Bioinformatics 27:268-269.
7. Bousquet M, Broccardo C, Quelen C, Meggetto F, Kuhlein E, Delsol G, Dastugue N, Brousset P. 2007. A novel PAX5-ELN fusion protein identified in B-cell acute lymphoblastic leukemia acts as a dominant negative on wild-type PAX5. Blood 109:3417-3423.
8. Boyle AP, Hong EL, Hariharan M, Cheng Y, Schaub MA, Kasowski M, Karczewski KJ, Park J, Hitz BC, Weng S, Cherry JM, Snyder M. 2012. Annotation of functional variation in personal genomes using RegulomeDB. Genome Res 22:1790-1797.
9. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, et al. 2011. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43:491-498.
10. Gonzalez-Perez A, Lopez-Bigas N. 2012. Functional impact bias reveals cancer drivers. Nucleic Acids Res 40:e169.
11. Guo C, Chen LH, Huang Y, Chang CC, Wang P, Pirozzi CJ, Qin X, Bao X, Greer PK, McLendon RE, Yan H, Keir ST, et al. 2013. KMT2D maintains neoplastic cell proliferation and global histone H3 lysine 4 monomethylation. Oncotarget 4:2144-2153.
12. Henrich KO, Schwab M, Westermann F. 2012. 1p36 tumor suppression-a matter of dosage? Cancer Res 72:6079-6088.
13. Hidaka H, Yagasaki H, Takahashi Y, Hama A, Nishio N, Tanaka M, Yoshida N, Villalobos IB, Wang Y, Xu Y, Horibe K, Chen S, et al. 2007. Increased midkine gene expression in childhood B-precursor acute lymphoblastic leukemia. Leuk Res 31:1045-1051.
14. Holmfeldt L, Wei L, Diaz-Flores E, Walsh M, Zhang J, Ding L, Payne-Turner D, Churchman M, Andersson A, Chen SC, McCastlain K, Becksfort J, et al. 2013. The genomic landscape of hypodiploid acute lymphoblastic leukemia. Nat Genet 45:242-252.
15. Jan M, Majeti R. 2013. Clonal evolution of acute leukemia genomes. Oncogene 32:135-140.
16. Kent WJ. 2002. BLAT-the BLAST-like alignment tool. Genome Res 12:656-664.
17. Khurana E, Fu Y, Colonna V, Mu XJ, Kang HM, Lappalainen T, Sboner A, Lochovsky L, Chen J, Harmanci A, Das J, Abyzov A, et al. 2013. Integrative annotation of variants from 1092 humans: application to cancer genomics. Science 342:1235587.
18. Kircher M, Witten DM, Jain P, O'Roak BJ, Cooper GM, Shendure J. 2014. A general framework for estimating the relative pathogenicity of human genetic variants. Nat Genet 46:310-315.
19. Krohn A, Seidel A, Burkhardt L, Bachmann F, Mader M, Grupp K, Eichenauer T, Becker A, Adam M, Graefen M, Huland H, Kurtz S, et al. 2013. Recurrent deletion of 3p13 targets multiple tumour suppressor genes and defines a distinct subgroup of aggressive ERG fusion-positive prostate cancers. J Pathol 231:130-141.
20. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. 2009. Circos: an information aesthetic for comparative genomics. Genome Res 19:1639-1645.
21. Landau DA, Carter SL, Getz G, Wu CJ. 2014. Clonal evolution in hematological malignancies and therapeutic implications. Leukemia 28:34-43.
22. Larson DE, Harris CC, Chen K, Koboldt DC, Abbott TE, Dooling DJ, Ley TJ, Mardis ER, Wilson RK, Ding L. 2012. SomaticSniper: identification of somatic point mutations in whole genome sequencing data. Bioinformatics 28:311-317.
23. Lawrence MS, Stojanov P, Polak P, Kryukov GV, Cibulskis K, Sivachenko A, Carter SL, Stewart C, Mermel CH, Roberts SA, Kiezun A, Hammerman PS, et al. 2013. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 499:214-218.
24. Le Noir S, Ben Abdelali R, Lelorch M, Bergeron J, Sungalee S, Payet-Bornet D, Villarese P, Petit A, Callens C, Lhermitte L, Baranger L, Radford-Weiss I, et al. 2012. Extensive molecular mapping of TCRalpha/delta- and TCRbeta-involved chromosomal translocations reveals distinct mechanisms of oncogene activation in T-ALL. Blood 120:3298-3309.
25. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760.
26. Liang DC, Shih LY, Fu JF, Li HY, Wang HI, Hung IJ, Yang CP, Jaing TH, Chen SH, Liu HC. 2006. K-Ras mutations and N-Ras mutations in childhood acute leukemias with or without mixed-lineage leukemia gene rearrangements. Cancer 106:950-956.
27. Lilljebjorn H, Rissler M, Lassen C, Heldrup J, Behrendtz M, Mitelman F, Johansson B, Fioretos T. 2012. Whole-exome sequencing of pediatric acute lymphoblastic leukemia. Leukemia 26:1602-1607.
28. Lilljebjorn H, Soneson C, Andersson A, Heldrup J, Behrendtz M, Kawamata N, Ogawa S, Koeffler HP, Mitelman F, Johansson B, Fontes M, Fioretos T. 2010. The correlation pattern of acquired copy number changes in 164 ETV6/RUNX1-positive childhood acute lymphoblastic leukemias. Hum Mol Genet 19:3150-3158.
29. Lowe CB, Kellis M, Siepel A, Raney BJ, Clamp M, Salama SR, Kingsley DM, Lindblad-Toh K, Haussler D. 2011. Three periods of regulatory innovation during vertebrate evolution. Science 333:1019-1024.
30. Mangum DS, Downie J, Mason CC, Jahromi MS, Joshi D, Rodic V, Muschen M, Meeker N, Trede N, Frazer JK, Zhou Y, Cheng C, et al. 2014. VPREB1 deletions occur independent of lambda light chain rearrangement in childhood acute lymphoblastic leukemia. Leukemia 28:216-220.
31. Marculescu R, Vanura K, Le T, Simon P, Jager U, Nadel B. 2003. Distinct t(7;9)(q34;q32) breakpoints in healthy individuals and individuals with T-ALL. Nat Genet 33:342-344.
32. Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing. EMBnet.journal 17:10-12.
33. Mayrhofer M, Dilorenzo S, Isaksson A. 2013. Patchwork: allele-specific copy number analysis of whole-genome sequenced tumor tissue. Genome Biol 14:R24.
34. McLaren W, Pritchard B, Rios D, Chen Y, Flicek P, Cunningham F. 2010. Deriving the consequences of genomic variants with the Ensembl API and SNP Effect Predictor. Bioinformatics 26:2069-2070.
35. Meyer JA, Wang J, Hogan LE, Yang JJ, Dandekar S, Patel JP, Tang Z, Zumbo P, Li S, Zavadil J, Levine RL, Cardozo T, et al. 2013. Relapse-specific mutations in NT5C2 in childhood acute lymphoblastic leukemia. Nat Genet 45:290-294.
36. Mullighan C, Downing J. 2008. Ikaros and acute leukemia. Leuk Lymphoma 49:847-849.
37. Mullighan CG. 2013. Genomic characterization of childhood acute lymphoblastic leukemia. Semin Hematol 50:314-324.
38. Mullighan CG, Goorha S, Radtke I, Miller CB, Coustan-Smith E, Dalton JD, Girtman K, Mathew S, Ma J, Pounds SB, Su X, Pui CH, et al. 2007. Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature 446:758-764.
39. Nordlund J, Backlin CL, Wahlberg P, Busche S, Berglund EC, Eloranta ML, Flaegstad T, Forestier E, Frost BM, Harila-Saari A, Heyman M, Jonsson OG, et al. 2013. Genome-wide signatures of differential DNA methylation in pediatric acute lymphoblastic leukemia. Genome Biol 14:r105.
40. Papaemmanuil E, Rapado I, Li Y, Potter NE, Wedge DC, Tubio J, Alexandrov LB, Van Loo P, Cooke SL, Marshall J, Martincorena I, Hinton J, et al. 2014. RAG-mediated recombination is the predominant driver of oncogenic rearrangement in ETV6-RUNX1 acute lymphoblastic leukemia. Nat Genet 46:116-125.
41. Pleasance ED, Stephens PJ, O'Meara S, McBride DJ, Meynert A, Jones D, Lin ML, Beare D, Lau KW, Greenman C, Varela I, Nik-Zainal S, et al. 2010. A small-cell lung cancer genome with complex signatures of tobacco exposure. Nature 463:184-190.
42. Pui CH, Carroll WL, Meshinchi S, Arceci RJ. 2011. Biology, risk stratification, and therapy of pediatric acute leukemias: an update. J Clin Oncol 29:551-565.
43. 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, et al. 2012. Genetic alterations activating kinase and cytokine receptor signaling in high-risk acute lymphoblastic leukemia. Cancer Cell 22:153-166.
44. Schmiegelow K, Forestier E, Hellebostad M, Heyman M, Kristinsson J, Soderhall S, Taskinen M. 2010. Long-term results of NOPHO ALL-92 and ALL-2000 studies of childhood acute lymphoblastic leukemia. Leukemia 24:345-354.
45. Shaffer LG, McGowan-Jordan J, Schmid M, editors. 2013. ISCN (2013): An international system for human cytogenetic nomenclature. Basel: S. Karger.
46. Stams WA, den Boer ML, Beverloo HB, Meijerink JP, van Wering ER, Janka-Schaub GE, Pieters R. 2005. Expression levels of TEL, AML1, and the fusion products TEL-AML1 and AML1-TEL versus drug sensitivity and clinical outcome in t(12;21)-positive pediatric acute lymphoblastic leukemia. Clin Cancer Res 11:2974-2980.
47. Tamborero D, Gonzalez-Perez A, Lopez-Bigas N. 2013. OncodriveCLUST: exploiting the positional clustering of somatic mutations to identify cancer genes. Bioinformatics 29:2238-2244.
48. The Cancer Genome Atlas Research Network. 2013. Genomic and Epigenomic Landscapes of Adult De Novo Acute Myeloid Leukemia. N Engl J Med 368:2059-2074.
49. Thorvaldsdottir H, Robinson JT, Mesirov JP. 2013. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14:178-192.
50. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562-578.
51. Tzoneva G, Perez-Garcia A, Carpenter Z, Khiabanian H, Tosello V, Allegretta M, Paietta E, Racevskis J, Rowe JM, Tallman MS, Paganin M, Basso G, et al. 2013. Activating mutations in the NT5C2 nucleotidase gene drive chemotherapy resistance in relapsed ALL. Nat Med 19:368-371.
52. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA. 2007. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35(Web Server issue):W71-W74.
53. Van Loo P, Nordgard SH, Lingjaerde OC, Russnes HG, Rye IH, Sun W, Weigman VJ, Marynen P, Zetterberg A, Naume B, Perou CM, Borresen-Dale AL, et al. 2010. Allele-specific copy number analysis of tumors. Proc Natl Acad Sci USA 107:16910-1695.
54. Wang K, Li M, Hakonarson H. 2010. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38:e164.
55. Weng AP, Ferrando AA, Lee W, Morris JPt, Silverman LB, Sanchez-Irizarry C, Blacklow SC, Look AT, Aster JC. 2004. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306:269-271.
56. Vinagre J, Almeida A, Populo H, Batista R, Lyra J, Pinto V, Coelho R, Celestino R, Prazeres H, Lima L, Melo M, da Rocha AG, et al. 2013. Frequency of TERT promoter mutations in human cancers. Nat Commun 4:2185.
57. Winandy S, Wu P, Georgopoulos K. 1995. A dominant mutation in the Ikaros gene leads to rapid development of leukemia and lymphoma. Cell 83:289-299.
58. Wojcik H, Griffiths E, Staggs S, Hagman J, Winandy S. 2007. Expression of a non-DNA-binding Ikaros isoform exclusively in B cells leads to autoimmunity but not leukemogenesis. Eur J Immunol 37:1022-1032.
59. Wright DD, Sefton BM, Kamps MP. 1994. Oncogenic activation of the Lck protein accompanies translocation of the LCK gene in the human HSB2 T-cell leukemia. Mol Cell Biol 14:2429-2437.
60. Xi R, Hadjipanayis AG, Luquette LJ, Kim TM, Lee E, Zhang J, Johnson MD, Muzny DM, Wheeler DA, Gibbs RA, Kucherlapati R, Park PJ. 2011. Copy number variation detection in whole-genome sequencing data using the Bayesian information criterion. Proc Natl Acad Sci USA 108:E1128-E1136.
61. Zhang J, Ding L, Holmfeldt L, Wu G, Heatley SL, Payne-Turner D, Easton J, Chen X, Wang J, Rusch M, Lu C, Chen SC, et al. 2012. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481:157-163.
62. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol 9:R137.