MYB-QKI rearrangements in angiocentric glioma drive tumorigenicity through a tripartite mechanism

Nature Genetics

Volumn 48, Issue 3, 2016, Pages 273-282

  Bandopadhayay, Pratiti ^a,b,c   Ramkissoon, Lori A ^a   Jain, Payal ^d,e   Bergthold, Guillaume ^a,f   Wala, Jeremiah ^a,b,c   Zeid, Rhamy ^a,c   Schumacher, Steven E ^a,b   Urbanski, Laura ^a   O'Rourke, Ryan ^a,b   Gibson, William J ^a,b,c   Pelton, Kristine ^a   Ramkissoon, Shakti H ^a,c,g,h   Han, Harry J ^d,e   Zhu, Yuankun ^d,e   Choudhari, Namrata ^d,e   Silva, Amanda ^a,d,e   Boucher, Katie ^d,e   Henn, Rosemary E ^d,e   Kang, Yun Jee ^a   Knoff, David ^a   Paolella, Brenton R ^a,b,c   Gladden Young, Adrianne ^b   Varlet, Pascale ⁱ   Pages, Melanie ⁱ   Horowitz, Peleg M ^a,g   Federation, Alexander ^a,c   Malkin, Hayley ^a   Tracy, Adam A ^b   Seepo, Sara ^b   Ducar, Matthew ^a,g   Van Hummelen, Paul ^a   Santi, Mariarita ^d,e   Buccoliero, Anna Maria ^j   Scagnet, Mirko ^j   Bowers, Daniel C ^k   Giannini, Caterina ^l   Puget, Stephanie ^m   Hawkins, Cynthia ⁿ   Tabori, Uri ⁿ   Klekner, Almos ^o   Bognar, Laszlo ^o   Burger, Peter C ^p   Eberhart, Charles ^p   Rodriguez, Fausto J ^p   Hill, D Ashley ^q   Mueller, Sabine ^r   Haas Kogan, Daphne A ^g,r,s   Phillips, Joanna J ^r   Santagata, Sandro ^a,c,g,h   Stiles, Charles D ^a   Bradner, James E ^a,b,c   Jabado, Nada ^t,u   Goren, Alon ^b   Grill, Jacques ^f   Ligon, Azra H ^g   Goumnerova, Liliana ^a,c,h   Waanders, Angela J ^d,e   Storm, Phillip B ^d,e   Kieran, Mark W ^a,c   Ligon, Keith L ^a,b,c,g,h   Beroukhim, Rameen ^a,b,c,g   Resnick, Adam C ^d,e   more..

^a DANA FARBER CANCER INSTITUTE   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f CNRS   (France)

^g BRIGHAM AND WOMEN S HOSPITAL   (United States)

^h BOSTON CHILDREN S HOSPITAL   (United States)

ⁱ CENTRE HOSPITALIER SAINTE ANNE   (France)

^j UNIVERSITY OF FLORENCE   (Italy)

^k UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^l MAYO CLINIC   (United States)

^m HÔPITAL NECKER ENFANTS MALADES   (France)

ⁿ HOSPITAL FOR SICK CHILDREN   (Canada)

^o UNIVERSITY OF DEBRECEN   (Hungary)

^p JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^q CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^r UNIVERSITY OF CALIFORNIA   (United States)

^s UNIVERSITY OF CALIFORNIA   (United States)

^t MONTREAL CHILDREN S HOSPITAL   (Canada)

^u MCGILL UNIVERSITY   (Canada)

more..

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN MYB; PROTEIN QKI; RNA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; ONCOPROTEIN; QKI PROTEIN, HUMAN; RNA BINDING PROTEIN;

3T3 CELL LINE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CARCINOGENICITY; CONTROLLED STUDY; EMBRYO; ENHANCER REGION; FEMALE; GENE ACTIVATION; GENE FUSION; GENE REARRANGEMENT; GENE TRANSLOCATION; GENETIC ANALYSIS; GLIOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RNA SEQUENCE; TUMOR SUPPRESSOR GENE; BIOSYNTHESIS; CHILD; COMPARATIVE GENOMIC HYBRIDIZATION; EXOME; GENE EXPRESSION REGULATION; GENETICS; HIGH THROUGHPUT SEQUENCING; META ANALYSIS; MUTATION; PATHOLOGY; TUMOR CELL LINE;

CARCINOGENESIS; CELL LINE, TUMOR; CHILD; COMPARATIVE GENOMIC HYBRIDIZATION; EXOME; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REARRANGEMENT; GLIOMA; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MUTATION; ONCOGENE PROTEINS V-MYB; ONCOGENE PROTEINS, FUSION; RNA-BINDING PROTEINS;

EID: 84959547851     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3500     Document Type: Article

References (67)

1. Ramkissoon L.A., et al. Genomic analysis of diffuse pediatric low-grade gliomas identifies recurrent oncogenic truncating rearrangements in the transcription factor MYBL1. Proc. Natl. Acad. Sci. USA 110, 8188-8193 (2013
2. Zhang J., et al. Whole-genome sequencing identifies genetic alterations in pediatric low-grade gliomas. Nat. Genet. 45, 602-612 (2013
3. Wang M., et al. Monomorphous angiocentric glioma: a distinctive epileptogenic neoplasm with features of infiltrating astrocytoma and ependymoma. J. Neuropathol. Exp. Neurol. 64, 875-881 (2005
4. Lellouch-Tubiana A., et al. Angiocentric neuroepithelial tumor (ANET): a new epilepsy-related clinicopathological entity with distinctive MRI. Brain Pathol. 15, 281-286 (2005
5. Jones D.T.W., et al. Recurrent somatic alterations of FGFR1 and NTRK2 in pilocytic astrocytoma. Nat. Genet. 45, 927-932 (2013
6. Klempnauer K.H., Bonifer C., & Sippel A.E. Identification and characterization of the protein encoded by the human c-myb proto-oncogene. EMBO J. 5, 1903-1911 (1986
7. Klempnauer K.H., Gonda T.J., & Bishop J.M. Nucleotide sequence of the retroviral leukemia gene v-myb and its cellular progenitor c-myb: the architecture of a transduced oncogene. Cell 31, 453-463 (1982
8. Ness S.A., Marknell A., & Graf T. The v-myb oncogene product binds to and activates the promyelocyte-specific mim-1 gene. Cell 59, 1115-1125 (1989
9. Sakura H., et al. Delineation of three functional domains of the transcriptional activator encoded by the c-myb protooncogene. Proc. Natl. Acad. Sci. USA 86, 5758-5762 (1989
10. Gonda T.J., Buckmaster C., & Ramsay R.G. Activation of c-myb by carboxy-terminal truncation: relationship to transformation of murine haemopoietic cells in vitro. EMBO J. 8, 1777-1783 (1989
11. Hu Y.L., Ramsay R.G., Kanei-Ishii C., Ishii S., & Gonda T.J. Transformation by carboxyl-deleted Myb reflects increased transactivating capacity and disruption of a negative regulatory domain. Oncogene 6, 1549-1553 (1991
12. Press R.D., Reddy E.P., & Ewert D.L. Overexpression of C-terminally but not N-terminally truncated Myb induces fibrosarcomas: a novel nonhematopoietic target cell for the myb oncogene. Mol. Cell. Biol. 14, 2278-2290 (1994
13. Grässer F.A., Graf T., & Lipsick J.S. Protein truncation is required for the activation of the c-myb proto-oncogene. Mol. Cell. Biol. 11, 3987-3996 (1991
14. GTEx Consortium. The Genotype-Tissue Expression (GTEx) project. Nat. Genet. 45, 580-585 (2013
15. Malaterre J., et al. c-Myb is required for neural progenitor cell proliferation and maintenance of the neural stem cell niche in adult brain. Stem Cells 26, 173-181 (2008
16. Friedrich V.L. Jr. The myelin deficit in quacking mice. Brain Res. 82, 168-172 (1974
17. Yin D., et al. High-resolution genomic copy number profiling of glioblastoma multiforme by single nucleotide polymorphism DNA microarray. Mol. Cancer Res. 7, 665-677 (2009
18. Zhao Y., et al. The tumor suppressing effects of QKI-5 in prostate cancer: a novel diagnostic and prognostic protein. Cancer Biol. Ther. 15, 108-118 (2014
19. Bian Y., et al. Downregulation of tumor suppressor QKI in gastric cancer and its implication in cancer prognosis. Biochem. Biophys. Res. Commun. 422, 187-193 (2012
20. Zack T.I., et al. Pan-cancer patterns of somatic copy number alteration. Nat. Genet. 45, 1134-1140 (2013
21. Wu J., Zhou L., Tonissen K., Tee R., & Artzt K. The quaking I-5 protein (QKI-5) has a novel nuclear localization signal and shuttles between the nucleus and the cytoplasm. J. Biol. Chem. 274, 29202-29210 (1999
22. Gao R., et al. A unifying gene signature for adenoid cystic cancer identifies parallel MYB-dependent and MYB-independent therapeutic targets. Oncotarget 5, 12528-12542 (2014
23. Mansour M.R., et al. An oncogenic super-enhancer formed through somatic mutation of a noncoding intergenic element. Science 346, 1373-1377 (2014
24. Northcott P.A., et al. Enhancer hijacking activates GFI1 family oncogenes in medulloblastoma. Nature 511, 428-434 (2014
25. ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012
26. Menzel S., et al. The HBS1L-MYB intergenic region on chromosome 6q23.3 influences erythrocyte, platelet, and monocyte counts in humans. Blood 110, 3624-3626 (2007
27. Bachoo R.M., et al. Epidermal growth factor receptor and Ink4a/Arf: convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis. Cancer Cell 1, 269-277 (2002
28. Wang Y., Vogel G., Yu Z., & Richard S. The QKI-5 and QKI-6 RNA binding proteins regulate the expression of microRNA 7 in glial cells. Mol. Cell. Biol. 33, 1233-1243 (2013
29. Chen A.-J., et al. STAR RNA-binding protein Quaking suppresses cancer via stabilization of specific miRNA. Genes Dev. 26, 1459-1472 (2012
30. Ji S., et al. miR-574-5p negatively regulates Qki6/7 to impact β-catenin/Wnt signalling and the development of colorectal cancer. Gut 62, 716-726 (2013
31. Bandopadhayay P., et al. BET bromodomain inhibition of MYC-amplified medulloblastoma. Clin. Cancer Res. 20, 912-925 (2014
32. Delmore J.E., et al. BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 146, 904-917 (2011
33. Chipumuro E., et al. CDK7 inhibition suppresses super-enhancer-linked oncogenic transcription in MYCN-driven cancer. Cell 159, 1126-1139 (2014
34. D'Alfonso T.M., et al. MYB-NFIB gene fusion in adenoid cystic carcinoma of the breast with special focus paid to the solid variant with basaloid features. Hum. Pathol. 45, 2270-2280 (2014
35. Persson M., et al. Recurrent fusion of MYB and NFIB transcription factor genes in carcinomas of the breast and head and neck. Proc. Natl. Acad. Sci. USA 106, 18740-18744 (2009
36. Stephens P.J., et al. Whole exome sequencing of adenoid cystic carcinoma. J. Clin. Invest. 123, 2965-2968 (2013
37. Danan-Gotthold M., et al. Identification of recurrent regulated alternative splicing events across human solid tumors. Nucleic Acids Res. 43, 5130-5144 (2015
38. Conn S.J., et al. The RNA binding protein quaking regulates formation of circRNAs. Cell 160, 1125-1134 (2015
39. Lu W., et al. QKI impairs self-renewal and tumorigenicity of oral cancer cells via repression of SOX2. Cancer Biol. Ther. 15, 1174-1184 (2014
40. Crompton B.D., et al. The genomic landscape of pediatric Ewing sarcoma. Cancer Discov. 4, 1326-1341 (2014
41. Kieran M.W., et al. Absence of oncogenic canonical pathway mutations in aggressive pediatric rhabdoid tumors. Pediatr. Blood Cancer 59, 1155-1157 (2012
42. Beroukhim R., et al. Assessing the significance of chromosomal aberrations in cancer: methodology and application to glioma. Proc. Natl. Acad. Sci. USA 104, 20007-20012 (2007
43. Li H., & Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009
44. McKenna A., et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303 (2010
45. Chiang D.Y., et al. High-resolution mapping of copy-number alterations with massively parallel sequencing. Nat. Methods 6, 99-103 (2009
46. Beroukhim R., et al. The landscape of somatic copy-number alteration across human cancers. Nature 463, 899-905 (2010
47. Cibulskis K., et al. Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat. Biotechnol. 31, 213-219 (2013
48. Robinson J.T., et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24-26 (2011
49. Lawrence M.S., et al. Discovery and saturation analysis of cancer genes across 21 tumour types. Nature 505, 495-501 (2014
50. Drier Y., et al. Somatic rearrangements across cancer reveal classes of samples with distinct patterns of DNA breakage and rearrangement-induced hypermutability. Genome Res. 23, 228-235 (2013
51. Chapman M.A., et al. Initial genome sequencing and analysis of multiple myeloma. Nature 471, 467-472 (2011
52. Torres-García W., et al. PRADA: pipeline for RNA sequencing data analysis. Bioinformatics 30, 2224-2226 (2014
53. Craig J.M., et al. DNA fragmentation simulation method (FSM) and fragment size matching improve aCGH performance of FFPE tissues. PLoS One 7, e38881 (2012
54. Firestein R., et al. CDK8 is a colorectal cancer oncogene that regulates β-catenin activity. Nature 455, 547-551 (2008
55. Bergthold G., et al. Expression profiles of 151 pediatric low-grade gliomas reveal molecular differences associated with location and histological subtype. Neuro-oncol. 17, 1486-1496 (2015
56. Sievert A.J., et al. Paradoxical activation and RAF inhibitor resistance of BRAF protein kinase fusions characterizing pediatric astrocytomas. Proc. Natl. Acad. Sci. USA 110, 5957-5962 (2013
57. Reynolds B.A., & Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707-1710 (1992
58. Bolstad B.M., Irizarry R.A., Astrand M., & Speed T.P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185-193 (2003
59. Gould J., Getz G., Monti S., Reich M., & Mesirov J.P. Comparative gene marker selection suite. Bioinformatics 22, 1924-1925 (2006
60. Garber M., et al. A high-throughput chromatin immunoprecipitation approach reveals principles of dynamic gene regulation in mammals. Mol. Cell 47, 810-822 (2012
61. Etchegaray J.-P., et al. The histone deacetylase SIRT6 controls embryonic stem cell fate via TET-mediated production of 5-hydroxymethylcytosine. Nat. Cell Biol. 17, 545-557 (2015
62. Bengtsen M., et al. c-Myb binding sites in haematopoietic chromatin landscapes. PLoS One 10, e0133280 (2015
63. 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
64. Quintana A.M., Liu F., O'Rourke J.P., & Ness S.A. Identification and regulation of c-Myb target genes in MCF-7 cells. BMC Cancer 11, 30 (2011
65. Zhao L., et al. Integrated genome-wide chromatin occupancy and expression analyses identify key myeloid pro-differentiation transcription factors repressed by Myb. Nucleic Acids Res. 39, 4664-4679 (2011
66. Zhu J., et al. Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell 152, 642-654 (2013
67. Chapuy B., et al. Discovery and characterization of super-enhancer-associated dependencies in diffuse large B cell lymphoma. Cancer Cell 24, 777-790 (2013