A NOTCH1-driven MYC enhancer promotes T cell development, transformation and acute lymphoblastic leukemia

Nature Medicine

Volumn 20, Issue 10, 2014, Pages 1130-1137

  Herranz, Daniel ^a   Ambesi Impiombato, Alberto ^a   Palomero, Teresa ^a,b   Schnell, Stephanie A ^a   Belver, Laura ^a   Wendorff, Agnieszka A ^a   Xu, Luyao ^a   Castillo Martin, Mireia ^c   Llobet Navás, David ^c   Cordon Cardo, Carlos ^c   Clappier, Emmanuelle ^d,e   Soulier, Jean ^d,e   Ferrando, Adolfo A ^a,b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b NewYork Presbyterian Hospital   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d INSERM   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MYC PROTEIN; NOTCH1 RECEPTOR; NOTCH1 PROTEIN, HUMAN; NOTCH1 PROTEIN, MOUSE;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL POPULATION; CELL TRANSFORMATION; CHROMOSOME DUPLICATION; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; ENHANCER REGION; FEMALE; GENE AMPLIFICATION; GENE CONTROL; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; T LYMPHOCYTE; THYMOCYTE; TRANSCRIPTION INITIATION SITE; UPREGULATION; ANIMAL; C57BL MOUSE; CANCER STEM CELL; CYTOLOGY; GENETICS; JURKAT CELL LINE; LYMPHOPOIESIS; METABOLISM; ONCOGENE; ONCOGENE MYC; PATHOLOGY; TUMOR CELL LINE;

MUS;

ANIMALS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; ENHANCER ELEMENTS, GENETIC; FEMALE; GENE AMPLIFICATION; GENES, MYC; HUMANS; JURKAT CELLS; LYMPHOPOIESIS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOPLASTIC STEM CELLS; ONCOGENES; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; RECEPTOR, NOTCH1; T-LYMPHOCYTES;

EID: 84921628643     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3665     Document Type: Article

References (60)

1. Van Vlierberghe, P. & Ferrando, A. The molecular basis of T cell acute lymphoblastic leukemia. J. Clin. Invest. 122, 3398-3406 (2012).
2. Ferrando, A.A. et al. Gene expression signatures define novel oncogenic pathways in T cell acute lymphoblastic leukemia. Cancer Cell 1, 75-87 (2002).
3. De Keersmaecker, K. et al. The TLX1 oncogene drives aneuploidy in T cell transformation. Nat. Med. 16, 1321-1327 (2010).
4. Della Gatta, G. et al. Reverse engineering of TLX oncogenic transcriptional networks identifies RUNX1 as tumor suppressor in T-ALL. Nat. Med. 18, 436-440 (2012).
5. Sanda, T. et al. Core transcriptional regulatory circuit controlled by the TAL1 complex in human T cell acute lymphoblastic leukemia. Cancer Cell 22, 209-221 (2012).
6. Weng, A.P. et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306, 269-271 (2004).
7. Tzoneva, G. & Ferrando, A.A. Recent advances on NOTCH signaling in T-ALL. Curr. Top. Microbiol. Immunol. 360, 163-182 (2012).
8. Koch, U. & Radtke, F. Mechanisms of T cell development and transformation. Annu. Rev. Cell Dev. Biol. 27, 539-562 (2011).
9. Radtke, F. et al. Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity 10, 547-558 (1999).
10. Schroeter, E.H., Kisslinger, J.A. & Kopan, R. Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 393, 382-386 (1998).
11. Jarriault, S. et al. Signalling downstream of activated mammalian Notch. Nature 377, 355-358 (1995).
12. Palomero, T. et al. NOTCH1 directly regulates c-MYC and activates a feed-forward-loop transcriptional network promoting leukemic cell growth. Proc. Natl. Acad. Sci. USA 103, 18261-18266 (2006).
13. Zhang, J. et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481, 157-163 (2012).
14. Watson, I.R., Takahashi, K., Futreal, P.A. & Chin, L. Emerging patterns of somatic mutations in cancer. Nat. Rev. Genet. 14, 703-718 (2013).
15. Weng, A.P. et al. c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/lymphoma. Genes Dev. 20, 2096-2109 (2006).
16. Sharma, V.M. et al. Notch1 contributes to mouse T-cell leukemia by directly inducing the expression of c-myc. Mol. Cell. Biol. 26, 8022-8031 (2006).
17. Palomero, T. et al. CUTLL1, a novel human T-cell lymphoma cell line with t(7;9) rearrangement, aberrant NOTCH1 activation and high sensitivity to γ-secretase inhibitors. Leukemia 20, 1279-1287 (2006).
18. Wang, H. et al. Genome-wide analysis reveals conserved and divergent features of Notch1/RBPJ binding in human and murine T-lymphoblastic leukemia cells. Proc. Natl. Acad. Sci. USA 108, 14908-14913 (2011).
19. Ashworth, T.D. et al. Deletion-based mechanisms of Notch1 activation in T-ALL: key roles for RAG recombinase and a conserved internal translational start site in Notch1. Blood 116, 5455-5464 (2010).
20. Lovén, J. et al. Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell 153, 320-334 (2013).
21. He, T.C. et al. Identification of c-MYC as a target of the APC pathway. Science 281, 1509-1512 (1998).
22. Sulis, M.L. et al. NOTCH1 extracellular juxtamembrane expansion mutations in T-ALL. Blood 112, 733-740 (2008).
23. Pear, W.S. et al. Exclusive development of T cell neoplasms in mice transplanted with bone marrow expressing activated Notch alleles. J. Exp. Med. 183, 2283-2291 (1996).
24. Ferrando, A.A. The role of NOTCH1 signaling in T-ALL. Hematology Am. Soc. Hematol. Educ. Program 353-361 (2009).
25. Hnisz, D. et al. Super-enhancers in the control of cell identity and disease. Cell 155, 934-947 (2013).
26. Amundadottir, L.T. et al. A common variant associated with prostate cancer in European and African populations. Nat. Genet. 38, 652-658 (2006).
27. Easton, D.F. et al. Genome-wide association study identifies novel breast cancer susceptibility loci. Nature 447, 1087-1093 (2007).
28. Haiman, C.A. et al. Multiple regions within 8q24 independently affect risk for prostate cancer. Nat. Genet. 39, 638-644 (2007).
29. Haiman, C.A. et al. A common genetic risk factor for colorectal and prostate cancer. Nat. Genet. 39, 954-956 (2007).
30. Kiemeney, L.A. et al. Sequence variant on 8q24 confers susceptibility to urinary bladder cancer. Nat. Genet. 40, 1307-1312 (2008).
31. Jia, L. et al. Functional enhancers at the gene-poor 8q24 cancer-linked locus. PLoS Genet. 5, e1000597 (2009).
32. Pomerantz, M.M. et al. The 8q24 cancer risk variant rs6983267 shows long-range interaction with MYC in colorectal cancer. Nat. Genet. 41, 882-884 (2009).
33. Wright, J.B., Brown, S.J. & Cole, M.D. Upregulation of c-MYC in cis through a large chromatin loop linked to a cancer risk-associated single-nucleotide polymorphism in colorectal cancer cells. Mol. Cell. Biol. 30, 1411-1420 (2010).
34. Sur, I.K. et al. Mice lacking a Myc enhancer that includes human SNP rs6983267 are resistant to intestinal tumors. Science 338, 1360-1363 (2012).
35. Shi, J. et al. Role of SWI/SNF in acute leukemia maintenance and enhancer-mediated Myc regulation. Genes Dev. 27, 2648-2662 (2013).
36. Dose, M. et al. c-Myc mediates pre-TCR-induced proliferation but not developmental progression. Blood 108, 2669-2677 (2006).
37. Athineos, D. & Sansom, O.J. Myc heterozygosity attenuates the phenotypes of APC deficiency in the small intestine. Oncogene 29, 2585-2590 (2010).
38. Sansom, O.J. et al. Myc deletion rescues Apc deficiency in the small intestine. Nature 446, 676-679 (2007).
39. Nie, Z. et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 151, 68-79 (2012).
40. Lin, C.Y. et al. Transcriptional amplification in tumor cells with elevated c-Myc. Cell 151, 56-67 (2012).
41. Lovén, J. et al. Revisiting global gene expression analysis. Cell 151, 476-482 (2012).
42. Zippo, A. et al. Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138, 1122-1136 (2009).
43. Real, P.J. et al. γ-secretase inhibitors reverse glucocorticoid resistance in T cell acute lymphoblastic leukemia. Nat. Med. 15, 50-58 (2009).
44. Clappier, E. et al. Clonal selection in xenografted human T cell acute lymphoblastic leukemia recapitulates gain of malignancy at relapse. J. Exp. Med. 208, 653-661 (2011).
45. Soulier, J. et al. HOXA genes are included in genetic and biologic networks defining human acute T-cell leukemia (T-ALL). Blood 106, 274-286 (2005).
46. Clappier, E. et al. NOTCH1 and FBXW7 mutations have a favorable impact on early response to treatment, but not on outcome, in children with T-cell acute lymphoblastic leukemia (T-ALL) treated on EORTC trials 58881 and 58951. Leukemia 24, 2023-2031 (2010).
47. Palomero, T. et al. Mutational loss of PTEN induces resistance to NOTCH1 inhibition in T-cell leukemia. Nat. Med. 13, 1203-1210 (2007).
48. Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576-589 (2010).
49. Encode Project Consortium. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol. 9, e1001046 (2011).
50. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
51. Blanchette, M. et al. Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res. 14, 708-715 (2004).
52. Simonis, M. et al. High-resolution identification of balanced and complex chromosomal rearrangements by 4C technology. Nat. Methods 6, 837-842 (2009).
53. Guo, K. et al. Disruption of peripheral leptin signaling in mice results in hyperleptinemia without associated metabolic abnormalities. Endocrinology 148, 3987-3997 (2007).
54. Byers, S.L., Wiles, M.V., Dunn, S.L. & Taft, R.A. Mouse estrous cycle identification tool and images. PLoS ONE 7, e35538 (2012).
55. Chiang, M.Y. et al. Leukemia-associated NOTCH1 alleles are weak tumor initiators but accelerate K-ras-initiated leukemia. J. Clin. Invest. 118, 3181-3194 (2008).
56. Kim, Y.H. et al. Combined microarray analysis of small cell lung cancer reveals altered apoptotic balance and distinct expression signatures of MYC family gene amplification. Oncogene 25, 130-138 (2006).
57. Zeller, K.I., Jegga, A.G., Aronow, B.J., O'Donnell, K.A. & Dang, C.V. An integrated database of genes responsive to the Myc oncogenic transcription factor: identification of direct genomic targets. Genome Biol. 4, R69 (2003).
58. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102, 15545-15550 (2005).
59. Huang da, W., Sherman, B.T. & Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
60. Hu, Y. & Smyth, G.K. ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J. Immunol. Methods 347, 70-78 (2009).