APOBEC signature mutation generates an oncogenic enhancer that drives LMO1 expression in T-ALL

Leukemia

Volumn 31, Issue 10, 2017, Pages 2057-2064

  Li, Z ^a   Abraham, B J ^b   Berezovskaya, A ^a   Farah, N ^c   Liu, Y ^d   Leon, T ^c   Fielding, A ^c   Tan, S H ^e,f   Sanda, T ^e,f   Weintraub, A S ^b   Li, B ^g,h   Shen, S ^g,h   Zhang, J ^d   Mansour, M R ^c   Young, R A ^b,i   Look, A T ^a,j  

^a HARVARD MEDICAL SCHOOL   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

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

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^f Dept Medicine Endocrinol Diabet   (Singapore)

^g SHANGHAI CHILDREN S MEDICAL CENTER   (China)

^h SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

ⁱ MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^j BOSTON CHILDREN S HOSPITAL   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B MRNA EDITING ENZYME CATALYTIC POLYPEPTIDE LIKE; CYTIDINE DEAMINASE; 5' UNTRANSLATED REGION; DNA; DNA BINDING PROTEIN; LIM PROTEIN; LMO1 PROTEIN, HUMAN; PROTEIN C MYB; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTOME; TUMOR PROTEIN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE FREQUENCY; GENE MUTATION; GENE TRANSLOCATION; HUMAN; HUMAN CELL; HUMAN TISSUE; LMO1 GENE; LUCIFERASE ASSAY; LYMPHOID CELL; ONCOGENE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; SOMATIC MUTATION; TRANSCRIPTION INITIATION SITE; 5' UNTRANSLATED REGION; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CHILD; ENHANCER REGION; GENE EXPRESSION REGULATION; GENETICS; JURKAT CELL LINE; METABOLISM; NUCLEOTIDE SEQUENCE; ONCOGENE MYB; POINT MUTATION; RNA INTERFERENCE; TUMOR CELL LINE;

5' UNTRANSLATED REGIONS; APOBEC DEAMINASES; BASE SEQUENCE; BINDING SITES; CELL LINE, TUMOR; CHILD; CHROMATIN IMMUNOPRECIPITATION; DNA, NEOPLASM; DNA-BINDING PROTEINS; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, LEUKEMIC; GENES, MYB; HUMANS; JURKAT CELLS; LIM DOMAIN PROTEINS; NEOPLASM PROTEINS; POINT MUTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTO-ONCOGENE PROTEINS C-MYB; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 85016122906     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2017.75     Document Type: Article

References (42)

1. Wheeler DA, Wang L. From human genome to cancer genome: the first decade. Genome Res 2013; 23: 1054-1062
2. Khurana E, Fu Y, Chakravarty D, Demichelis F, Rubin MA, Gerstein M. Role of noncoding sequence variants in cancer. Nat Rev Genet 2016; 17: 93-108
3. Horn S, Figl A, Rachakonda PS, Fischer C, Sucker A, Gast A, et al. TERT promoter mutations in familial and sporadic melanoma. Science 2013; 339: 959-961
4. Huang FW, Hodis E, Xu MJ, Kryukov GV, Chin L, Garraway LA. Highly recurrent TERT promoter mutations in human melanoma. Science 2013; 339: 957-959
5. Mansour MR, Abraham BJ, Anders L, Berezovskaya A, Gutierrez A, Durbin AD, et al. Oncogene regulation. An oncogenic super-enhancer formed through somatic mutation of a noncoding intergenic element. Science 2014; 346: 1373-1377
6. Navarro JM, Touzart A, Pradel LC, Loosveld M, Koubi M, Fenouil R, et al. Site-and allele-specific polycomb dysregulation in T-cell leukaemia. Nat Commun 2015; 6: 6094
7. Matthews JM, Lester K, Joseph S, Curtis DJ. LIM-domain-only proteins in cancer. Nat Rev Cancer 2013; 13: 111-122
8. Rabbitts TH. LMO T-cell translocation oncogenes typify genes activated by chromosomal translocations that alter transcription and developmental processes. Genes Dev 1998; 12: 2651-2657
9. Boehm T, Foroni L, Kennedy M, Rabbitts TH. The rhombotin gene belongs to a class of transcriptional regulators with a potential novel protein dimerisation motif. Oncogene 1990; 5: 1103-1105
10. Chambers J, Rabbitts TH. LMO2 at 25 years: a paradigm of chromosomal translocation proteins. Open Biol 2015; 5: 150062
11. Chervinsky DS, Zhao XF, Lam DH, Ellsworth M, Gross KW, Aplan PD. Disordered T-cell development and T-cell malignancies in SCL LMO1 double-transgenic mice: parallels with E2A-deficient mice. Mol Cell Biol 1999; 19: 5025-5035
12. Sanda T, Lawton LN, Barrasa MI, Fan ZP, Kohlhammer H, Gutierrez A, et al. Core transcriptional regulatory circuit controlled by the TAL1 complex in human T cell acute lymphoblastic leukemia. Cancer Cell 2012; 22: 209-221
13. Ferrando AA, Herblot S, Palomero T, Hansen M, Hoang T, Fox EA, et al. Biallelic transcriptional activation of oncogenic transcription factors in T-cell acute lymphoblastic leukemia. Blood 2004; 103: 1909-1911
14. Herblot S, Steff AM, Hugo P, Aplan PD, Hoang T. SCL and LMO1 alter thymocyte differentiation: inhibition of E2A-HEB function and pre-T alpha chain expression. Nat Immunol 2000; 1: 138-144
15. Boehm T, Baer R, Lavenir I, Forster A, Waters JJ, Nacheva E, et al. The mechanism of chromosomal translocation t(11; 14) involving the T-cell receptor C delta locus on human chromosome 14q11 and a transcribed region of chromosome 11p15. EMBO J 1988; 7: 385-394
16. Boehm T, Buluwela L, Williams D, White L, Rabbitts TH. A cluster of chromosome 11p13 translocations found via distinct D-D and D-D-J rearrangements of the human T cell receptor delta chain gene. EMBO J 1988; 7: 2011-2017
17. McGuire EA, Hockett RD, Pollock KM, Bartholdi MF, O'Brien SJ, Korsmeyer SJ. The t(11; 14)(p15; q11) in a T-cell acute lymphoblastic leukemia cell line activates multiple transcripts, including Ttg-1, a gene encoding a potential zinc finger protein. Mol Cell Biol 1989; 9: 2124-2132
18. Asnafi V, Beldjord K, Libura M, Villarese P, Millien C, Ballerini P, et al. Age-related phenotypic and oncogenic differences in T-cell acute lymphoblastic leukemias may reflect thymic atrophy. Blood 2004; 104: 4173-4180
19. Ferrando AA, Neuberg DS, Staunton J, Loh ML, Huard C, Raimondi SC, et al. Gene expression signatures define novel oncogenic pathways in T cell acute lymphoblastic leukemia. Cancer Cell 2002; 1: 75-87
20. Oram SH, Thoms J, Sive JI, Calero-Nieto FJ, Kinston SJ, Schutte J, et al. Bivalent promoter marks and a latent enhancer may prime the leukaemia oncogene LMO1 for ectopic expression in T-cell leukaemia. Leukemia 2013; 27: 1348-1357
21. Hume MA, Barrera LA, Gisselbrecht SS, Bulyk ML. UniPROBE, update 2015: new tools and content for the online database of protein-binding microarray data on protein-DNA interactions. Nucleic Acids Res 2015; 43: D117-D122
22. Newburger DE, Bulyk ML. UniPROBE: an online database of protein binding microarray data on protein-DNA interactions. Nucleic Acids Res 2009; 37: D77-D82
23. Kulakovskiy IV, Vorontsov IE, Yevshin IS, Soboleva AV, Kasianov AS, Ashoor H, et al. HOCOMOCO: expansion and enhancement of the collection of transcription factor binding sites models. Nucleic Acids Res 2016; 44: D116-D125
24. Hnisz D, Weintraub AS, Day DS, Valton AL, Bak RO, Li CH, et al. Activation of proto-oncogenes by disruption of chromosome neighborhoods. Science 2016; 351: 1454-1458
25. Anderson NM, Harrold I, Mansour MR, Sanda T, McKeown M, Nagykary N, et al. BCL2-specific inhibitor ABT-199 synergizes strongly with cytarabine against the early immature LOUCY cell line but not more-differentiated T-ALL cell lines. Leukemia 2014; 28: 1145-1148
26. Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, et al. Signatures of mutational processes in human cancer. Nature 2013; 500: 415-421
27. Burns MB, Temiz NA, Harris RS. Evidence for APOBEC3B mutagenesis in multiple human cancers. Nat Genet 2013; 45: 977-983
28. Seita J, Sahoo D, Rossi DJ, Bhattacharya D, Serwold T, Inlay MA, et al. Gene Expression Commons: an open platform for absolute gene expression profiling. PLoS One 2012; 7: e40321
29. Swanton C, McGranahan N, Starrett GJ, Harris RS. APOBEC Enzymes: Mutagenic Fuel for Cancer Evolution and Heterogeneity. Cancer Discov 2015; 5: 704-712
30. Larson RC, Lavenir I, Larson TA, Baer R, Warren AJ, Wadman I, et al. Protein dimerization between Lmo2 (Rbtn2) and Tal1 alters thymocyte development and potentiates T cell tumorigenesis in transgenic mice. EMBO J 1996; 15: 1021-1027
31. Valge-Archer VE, Osada H, Warren AJ, Forster A, Li J, Baer R, et al. The LIM protein RBTN2 and the basic helix-loop-helix protein TAL1 are present in a complex in erythroid cells. Proc Natl Acad Sci USA 1994; 91: 8617-8621
32. Coustan-Smith E, Mullighan CG, Onciu M, Behm FG, Raimondi SC, Pei D, et al. Early T-cell precursor leukaemia: a subtype of very high-risk acute lymphoblastic leukaemia. Lancet Oncol 2009; 10: 147-156
33. Gutierrez A, Dahlberg SE, Neuberg DS, Zhang J, Grebliunaite R, Sanda T, et al. Absence of biallelic TCRgamma deletion predicts early treatment failure in pediatric T-cell acute lymphoblastic leukemia. J Clin Oncol 2010; 28: 3816-3823
34. Oldridge DA, Wood AC, Weichert-Leahey N, Crimmins I, Sussman R, Winter C, et al. Genetic predisposition to neuroblastoma mediated by a LMO1 super-enhancer polymorphism. Nature 2015; 528: 418-421
35. Palii CG, Pasha R, Brand M. Lentiviral-mediated knockdown during ex vivo erythropoiesis of human hematopoietic stem cells. J Vis Exp 2011. doi: 10.3791/2813
36. Helleday T, Eshtad S, Nik-Zainal S. Mechanisms underlying mutational signatures in human cancers. Nat Rev Genet 2014; 15: 585-598
37. Roberts SA, Lawrence MS, Klimczak LJ, Grimm SA, Fargo D, Stojanov P, et al. An APOBEC cytidine deaminase mutagenesis pattern is widespread in human cancers. Nat Genet 2013; 45: 970-976
38. Henderson S, Fenton T. APOBEC3 genes: retroviral restriction factors to cancer drivers. Trends Mol Med 2015; 21: 274-284
39. Nik-Zainal S, Davies H, Staaf J, Ramakrishna M, Glodzik D, Zou X, et al. Landscape of somatic mutations in 560 breast cancer whole-genome sequences. Nature 2016; 534: 47-54
40. Gregory TR. Synergy between sequence and size in large-scale genomics. Nat Rev Genet 2005; 6: 699-708
41. Kwiatkowski N, Zhang T, Rahl PB, Abraham BJ, Reddy J, Ficarro SB, et al. Targeting transcription regulation in cancer with a covalent CDK7 inhibitor. Nature 2014; 511: 616-620
42. Loven J, Hoke HA, Lin CY, Lau A, Orlando DA, Vakoc CR, et al. Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell 2013; 153: 320-334