Deregulation of DUX4 and ERG in acute lymphoblastic leukemia

Nature Genetics

Volumn 48, Issue 12, 2016, Pages 1481-1489

  Zhang, Jinghui ^a   McCastlain, Kelly ^a   Yoshihara, Hiroki ^a   Xu, Beisi ^a   Chang, Yunchao ^a   Churchman, Michelle L ^a   Wu, Gang ^a   Li, Yongjin ^a   Wei, Lei ^a   Iacobucci, Ilaria ^a   Liu, Yu ^a   Qu, Chunxu ^a   Wen, Ji ^a   Edmonson, Michael ^a   Payne Turner, Debbie ^a   Kaufmann, Kerstin B ^b   Takayanagi, Shin Ichiro ^b,c   Wienholds, Erno ^b   Waanders, Esmé ^a,d   Ntziachristos, Panagiotis ^e,v   Bakogianni, Sofia ^e   Wang, Jingjing ^e   Aifantis, Iannis ^e,f   Roberts, Kathryn G ^a   Ma, Jing ^a   Song, Guangchun ^a   Easton, John ^a   Mulder, Heather L ^a   Chen, Xiang ^a   Newman, Scott ^a   Ma, Xiaotu ^a   Rusch, Michael ^a   Gupta, Pankaj ^a   Boggs, Kristy ^a   Vadodaria, Bhavin ^a   Dalton, James ^a   Liu, Yanling ^a   Valentine, Marcus L ^a   Ding, Li ^g   Lu, Charles ^g   Fulton, Robert S ^g   Fulton, Lucinda ^g   Tabib, Yashodhan ^g   Ochoa, Kerri ^g   Devidas, Meenakshi ^h   Pei, Deqing ^a   Cheng, Cheng ^a   Yang, Jun ^a   Evans, William E ^a   Relling, Mary V ^a   Pui, Ching Hon ^a   Jeha, Sima ^a   Harvey, Richard C ⁱ   Chen, I Ming L ⁱ   Willman, Cheryl L ⁱ   Marcucci, Guido ^j   Bloomfield, Clara D ^k   Kohlschmidt, Jessica ^k   Mrózek, Krzysztof ^k   Paietta, Elisabeth ^l   Tallman, Martin S ^m   Stock, Wendy ⁿ   Foster, Matthew C ^o   Racevskis, Janis ^p   Rowe, Jacob M ^q   Luger, Selina ^r   Kornblau, Steven M ^s   Shurtleff, Sheila A ^a   Raimondi, Susana C ^a   Mardis, Elaine R ^g   Wilson, Richard K ^g   Dick, John E ^b   Hunger, Stephen P ^t   Loh, Mignon L ^u   Downing, James R ^a   Mullighan, Charles G ^a   more..

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b PRINCESS MARGARET HOSPITAL   (Canada)

^c KYOWA HAKKO KOGYO CO LTD   (Japan)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^g WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

ⁱ UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^j CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^k OHIO STATE UNIVERSITY   (United States)

^l ALBERT EINSTEIN CANCER CENTER   (United States)

^m MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

ⁿ UNIVERSITY OF CHICAGO MEDICAL CENTER   (United States)

^o UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^p ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^q SHAARE ZEDEK MEDICAL CENTER   (Israel)

^r UNIVERSITY OF PENNSYLVANIA   (United States)

^s UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^t UNIVERSITY OF PENNSYLVANIA   (United States)

^u UNIVERSITY OF CALIFORNIA   (United States)

^v NORTHWESTERN UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DUX4; TRANSCRIPTION FACTOR ERG; UNCLASSIFIED DRUG; DUX4 PROTEIN, HUMAN; ERG PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; ISOPROTEIN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ADOLESCENT; ADULT; ANIMAL CELL; ARTICLE; CELL CYCLE REGULATION; CHROMOSOME; CONTROLLED STUDY; DNA BINDING; EXON; FEMALE; GENE CONTROL; GENE DELETION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENE REARRANGEMENT; HUMAN; HUMAN CELL; IMMUNOBLOTTING; INTRON; LEUKEMIA CELL; LEUKEMOGENESIS; MOUSE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; TRANSACTIVATION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; TUMOR XENOGRAFT; WHOLE EXOME SEQUENCING; CELL TRANSFORMATION; GENE EXPRESSION REGULATION; GENETICS; PATHOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; CELL TRANSFORMATION, NEOPLASTIC; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REARRANGEMENT; HOMEODOMAIN PROTEINS; HUMANS; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEIN ISOFORMS; TRANSCRIPTIONAL REGULATOR ERG; YOUNG ADULT;

EID: 84992387949     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3691     Document Type: Article

References (58)

1. Hunger, S.P. & Mullighan, C.G. Acute lymphoblastic leukemia in children. N. Engl. J. Med. 373, 1541-1552 (2015
2. Mullighan, C.G. Genomic characterization of childhood acute lymphoblastic leukemia. Semin. Hematol. 50, 314-324 (2013
3. Yeoh, E.J. et al. Classification, subtype discovery, and prediction of outcome in pediatric acute lymphoblastic leukemia by gene expression profiling. Cancer Cell 1, 133-143 (2002
4. Harvey, R.C. et al. Identification of novel cluster groups in pediatric high-risk B-precursor acute lymphoblastic leukemia with gene expression profiling: correlation with genome-wide DNA copy number alterations, clinical characteristics, and outcome. Blood 116, 4874-4884 (2010
5. Mullighan, C.G. et al. Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature 446, 758-764 (2007
6. Reddy, E.S. & Rao, V.N. ERG, an ETS-related gene, codes for sequence-specific transcriptional activators. Oncogene 6, 2285-2289 (1991
7. Bartel, F.O., Higuchi, T. & Spyropoulos, D.D. Mouse models in the study of the Ets family of transcription factors. Oncogene 19, 6443-6454 (2000
8. Kruse, E.A. et al. Dual requirement for the ETS transcription factors Fli-1 and Erg in hematopoietic stem cells and the megakaryocyte lineage. Proc. Natl. Acad. Sci. USA 106, 13814-13819 (2009
9. Loughran, S.J. et al. The transcription factor Erg is essential for definitive hematopoiesis and the function of adult hematopoietic stem cells. Nat. Immunol. 9, 810-819 (2008
10. Salek-Ardakani, S. et al. ERG is a megakaryocytic oncogene. Cancer Res. 69, 4665-4673 (2009
11. Rainis, L. et al. The proto-oncogene ERG in megakaryoblastic leukemias. Cancer Res. 65, 7596-7602 (2005
12. Ng, A.P. et al. Trisomy of Erg is required for myeloproliferation in a mouse model of Down syndrome. Blood 115, 3966-3969 (2010
13. Tomlins, S.A. et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 310, 644-648 (2005
14. Prasad, D.D., Ouchida, M., Lee, L., Rao, V.N. & Reddy, E.S. TLS/FUS fusion domain of TLS/FUS-ERG chimeric protein resulting from the t(16;21) chromosomal translocation in human myeloid leukemia functions as a transcriptional activation domain. Oncogene 9, 3717-3729 (1994
15. Marcucci, G. et al. Overexpression of the ETS-related gene, ERG, predicts a worse outcome in acute myeloid leukemia with normal karyotype: a Cancer and Leukemia Group B study. J. Clin. Oncol. 23, 9234-9242 (2005
16. Rao, V.N., Papas, T.S. & Reddy, E.S. ERG, a human ETS-related gene on chromosome 21: alternative splicing, polyadenylation, and translation. Science 237, 635-639 (1987
17. Dixit, M. et al. DUX4, a candidate gene of facioscapulohumeral muscular dystrophy, encodes a transcriptional activator of PITX1. Proc. Natl. Acad. Sci. USA 104, 18157-18162 (2007
18. Italiano, A. et al. High prevalence of CIC fusion with double-homeobox (DUX4) transcription factors in EWSR1-negative undifferentiated small blue round cell sarcomas. Genes Chromosom. Cancer 51, 207-218 (2012
19. Kawamura-Saito, M. et al. Fusion between CIC and DUX4 up-regulates PEA3 family genes in Ewing-like sarcomas with t(4;19)(q35;q13) translocation. Hum. Mol. Genet. 15, 2125-2137 (2006
20. Yasuda, T. et al. Recurrent DUX4 fusions in B cell acute lymphoblastic leukemia of adolescents and young adults. Nat. Genet. 48, 569-574 (2016
21. van der Veer, A. et al. IKZF1 status as a prognostic feature in BCR-ABL1-positive childhood ALL. Blood 123, 1691-1698 (2014
22. Mullighan, C.G. et al. Deletion of IKZF1 and prognosis in acute lymphoblastic leukemia. N. Engl. J. Med. 360, 470-480 (2009
23. Young, J.M. et al. DUX4 binding to retroelements creates promoters that are active in FSHD muscle and testis. PLoS Genet. 9, e1003947 (2013
24. Zou, J. et al. The oncogenic TLS-ERG fusion protein exerts different effects in hematopoietic cells and fibroblasts. Mol. Cell. Biol. 25, 6235-6246 (2005
25. Carmichael, C.L. et al. Hematopoietic overexpression of the transcription factor Erg induces lymphoid and erythro-megakaryocytic leukemia. Proc. Natl. Acad. Sci. USA 109, 15437-15442 (2012
26. Russell, L.J. et al. Deregulated expression of cytokine receptor gene, CRLF2, is involved in lymphoid transformation in B-cell precursor acute lymphoblastic leukemia. Blood 114, 2688-2698 (2009
27. Mullighan, C.G. et al. Rearrangement of CRLF2 in B-progenitor-And Down syndrome-Associated acute lymphoblastic leukemia. Nat. Genet. 41, 1243-1246 (2009
28. Iacobucci, I. et al. Truncating erythropoietin receptor rearrangements in acute lymphoblastic leukemia. Cancer Cell 29, 186-200 (2016
29. Russell, L.J. et al. IGH@ translocations are prevalent in teenagers and young adults with acute lymphoblastic leukemia and are associated with a poor outcome. J. Clin. Oncol. 32, 1453-1462 (2014
30. Zaliova, M. et al. ERG deletion is associated with CD2 and attenuates the negative impact of IKZF1 deletion in childhood acute lymphoblastic leukemia. Leukemia 28, 182-185 (2014
31. Clappier, E. et al. An intragenic ERG deletion is a marker of an oncogenic subtype of B-cell precursor acute lymphoblastic leukemia with a favorable outcome despite frequent IKZF1 deletions. Leukemia 28, 70-77 (2014
32. Lilljebjörn, H. et al. Identification of ETV6-RUNX1-like and DUX4-rearranged subtypes in paediatric B-cell precursor acute lymphoblastic leukaemia. Nat. Commun. 7, 11790 (2016
33. Roberts, K.G. et al. Targetable kinase-Activating lesions in Ph-like acute lymphoblastic leukemia. N. Engl. J. Med. 371, 1005-1015 (2014
34. Zhou, X. et al. Exploring genomic alteration in pediatric cancer using ProteinPaint. Nat. Genet. 48, 4-6 (2016
35. Holmfeldt, L. et al. The genomic landscape of hypodiploid acute lymphoblastic leukemia. Nat. Genet. 45, 242-252 (2013
36. Zhang, J. et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481, 157-163 (2012
37. Anders, S., Pyl, P.T. & Huber, W. HTSeq-A Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166-169 (2015
38. Smyth, G.K. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3 (2004
39. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289-300 (1995
40. Buenrostro, J.D., Giresi, P.G., Zaba, L.C., Chang, H.Y. & Greenleaf, W.J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213-1218 (2013
41. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008
42. Shultz, L.D. et al. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R?null mice engrafted with mobilized human hemopoietic stem cells. J. Immunol. 174, 6477-6489 (2005
43. Kneissl, S. et al. Measles virus glycoprotein-based lentiviral targeting vectors that avoid neutralizing antibodies. PLoS One 7, e46667 (2012
44. Churchman, M.L. et al. Efficacy of retinoids in IKZF1-mutated BCR-ABL1 acute lymphoblastic leukemia. Cancer Cell 28, 343-356 (2015
45. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009
46. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009
47. Kharchenko, P.V., Tolstorukov, M.Y. & Park, P.J. Design and analysis of ChIP-seq experiments for DNA-binding proteins. Nat. Biotechnol. 26, 1351-1359 (2008
48. Robinson, J.T. et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24-26 (2011
49. Bailey, T.L. & Gribskov, M. Combining evidence using P-values: application to sequence homology searches. Bioinformatics 14, 48-54 (1998
50. Bailey, T.L. et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37, W202-W208 (2009
51. Mathelier, A. et al. JASPAR 2016: a major expansion and update of the open-Access database of transcription factor binding profiles. Nucleic Acids Res. 44D1, D110-D115 (2016
52. Mullighan, C.G. et al. BCR-ABL1 lymphoblastic leukaemia is characterized by the deletion of Ikaros. Nature 453, 110-114 (2008
53. Kamijo, T. et al. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91, 649-659 (1997
54. Mantel, N. Evaluation of survival data and two new rank order statistics arising in its consideration. Cancer Chemother. Rep. 50, 163-170 (1966
55. Peto, R. et al. Design and analysis of randomized clinical trials requiring prolonged observation of each patient. II. Analysis and examples. Br. J. Cancer 35, 1-39 (1977
56. Gray, R.J. A class of K-sample tests for comparing the cumulative incidence of a competing risk. Ann. Stat. 16, 1141-1154 (1988
57. Fine, J.P. & Gray, R.J. A proportional hazards model for the subdistribution of a competing risk. J. Am. Stat. Assoc. 94, 496-509 (1999
58. R Development Core Team. R. A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2009).