Whole-genome sequencing identifies genetic alterations in pediatric low-grade gliomas

Nature Genetics

Volumn 45, Issue 6, 2013, Pages 602-612

  Zhang, Jinghui ^a   Wu, Gang ^a   Miller, Claudia P ^a   Tatevossian, Ruth G ^a   Dalton, James D ^a   Tang, Bo ^a   Orisme, Wilda ^a   Punchihewa, Chandanamali ^a   Parker, Matthew ^a   Qaddoumi, Ibrahim ^a   Boop, Fredrick A ^a   Lu, Charles ^b   Kandoth, Cyriac ^b   Ding, Li ^b   Lee, Ryan ^a   Huether, Robert ^a   Chen, Xiang ^a   Hedlund, Erin ^a   Nagahawatte, Panduka ^a   Rusch, Michael ^a   Boggs, Kristy ^a   Cheng, Jinjun ^a   Becksfort, Jared ^a   Ma, Jing ^a   Song, Guangchun ^a   Li, Yongjin ^a   Wei, Lei ^a   Wang, Jianmin ^a   Shurtleff, Sheila ^a   Easton, John ^a   Zhao, David ^a   Fulton, Robert S ^b   Fulton, Lucinda L ^b   Dooling, David J ^b   Vadodaria, Bhavin ^a   Mulder, Heather L ^a   Tang, Chunlao ^a   Ochoa, Kerri ^b   Mullighan, Charles G ^a   Gajjar, Amar ^a   Kriwacki, Richard ^a   Sheer, Denise ^c   Gilbertson, Richard J ^a   Mardis, Elaine R ^b   Wilson, Richard K ^b   Downing, James R ^a   Baker, Suzanne J ^a   Ellison, David W ^a   more..

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

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; FIBROBLAST GROWTH FACTOR RECEPTOR 1; PROTEIN MYB; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 1;

ARTICLE; ASTROCYTE; ASTROCYTOMA; AUTOPHOSPHORYLATION; CHILDHOOD CANCER; COHORT ANALYSIS; CONTROLLED STUDY; GENE; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENE MUTATION; GLIOMA; HIGH THROUGHPUT SEQUENCING; HUMAN; MAJOR CLINICAL STUDY; MYBL1 GENE; PILOCYTIC ASTROCYTOMA; PRIORITY JOURNAL;

ADOLESCENT; ANIMALS; BASE SEQUENCE; BRAIN NEOPLASMS; CHILD; CHILD, PRESCHOOL; FEMALE; GENE DUPLICATION; GENE REARRANGEMENT; GENES, MYB; GENOME-WIDE ASSOCIATION STUDY; GLIOMA; HUMANS; INFANT; MALE; MICE; MICE, NUDE; MOLECULAR SEQUENCE DATA; MUTATION; NEOPLASM GRADING; NEOPLASM TRANSPLANTATION; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS B-RAF; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTOME;

MUS MUSCULUS;

EID: 84878723078     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.2611     Document Type: Article

References (75)

1. Armstrong, G.T. et al. Survival and long-term health and cognitive outcomes after low-grade glioma. Neuro-oncol. 13, 223-234 (2011).
2. Arora, R.S. et al. Age-incidence patterns of primary CNS tumors in children, adolescents, and adults in England. Neuro-oncol. 11, 403-413 (2009).
3. Qaddoumi, I., Sultan, I. & Gajjar, A. Outcome and prognostic features in pediatric gliomas: a review of 6212 cases from the Surveillance, Epidemiology, and End Results database. Cancer 115, 5761-5770 (2009).
4. Bouffet, E. et al. Phase II study of weekly vinblastine in recurrent or refractory pediatric low-grade glioma. J. Clin. Oncol. 30, 1358-1363 (2012).
5. Duffner, P.K., Cohen, M.E., Myers, M.H. & Heise, H.W. Survival of children with brain tumors: SEER Program, 1973-1980. Neurology 36, 597-601 (1986).
6. Fisher, P.G. et al. Outcome analysis of childhood low-grade astrocytomas. Pediatr. Blood Cancer 51, 245-250 (2008).
7. Gajjar, A. et al. Low-grade astrocytoma: a decade of experience at St. Jude Children's Research Hospital. J. Clin. Oncol. 15, 2792-2799 (1997).
8. Gnekow, A.K. et al. Long-term follow-up of the multicenter, multidisciplinary treatment study HIT-LGG-1996 for low-grade glioma in children and adolescents of the German Speaking Society of Pediatric Oncology and Hematology. Neuro-oncol. 14, 1265-1284 (2012).
9. Merchant, T.E., Conklin, H.M., Wu, S., Lustig, R.H. & Xiong, X. Late effects of conformal radiation therapy for pediatric patients with low-grade glioma: prospective evaluation of cognitive, endocrine, and hearing deficits. J. Clin. Oncol. 27, 3691-3697 (2009).
10. Stokland, T. et al. A multivariate analysis of factors determining tumor progression in childhood low-grade glioma: a population-based cohort study (CCLG CNS9702). Neuro-oncol. 12, 1257-1268 (2010).
11. Forshew, T. et al. Activation of the ERK/MAPK pathway: a signature genetic defect in posterior fossa pilocytic astrocytomas. J. Pathol. 218, 172-181 (2009).
12. Jones, D.T. et al. Tandem duplication producing a novel oncogenic BRAF fusion gene defines the majority of pilocytic astrocytomas. Cancer Res. 68, 8673-8677 (2008).
13. Pfister, S. et al. BRAF gene duplication constitutes a mechanism of MAPK pathway activation in low-grade astrocytomas. J. Clin. Invest. 118, 1739-1749 (2008).
14. Sievert, A.J. et al. Duplication of 7q34 in pediatric low-grade astrocytomas detected by high-density single-nucleotide polymorphism-based genotype arrays results in a novel BRAF fusion gene. Brain Pathol. 19, 449-458 (2009).
15. Listernick, R., Charrow, J. & Gutmann, D.H. Intracranial gliomas in neurofibromatosis type 1. Am. J. Med. Genet. 89, 38-44 (1999).
16. Listernick, R., Ferner, R.E., Liu, G.T. & Gutmann, D.H. Optic pathway gliomas in neurofibromatosis-1: controversies and recommendations. Ann. Neurol. 61, 189-198 (2007).
17. DeClue, J.E. et al. Abnormal regulation of mammalian p21ras contributes to malignant tumor growth in von Recklinghausen (type 1) neurofibromatosis. Cell 69, 265-273 (1992).
18. Dias-Santagata, D. et al. BRAF V600E mutations are common in pleomorphic xanthoastrocytoma: diagnostic and therapeutic implications. PLoS ONE 6, e17948 (2011).
19. Lin, A. et al. BRAF alterations in primary glial and glioneuronal neoplasms of the central nervous system with identification of 2 novel KIAA1549:BRAF fusion variants. J. Neuropathol. Exp. Neurol. 71, 66-72 (2012).
20. Schindler, G. et al. Analysis of BRAF V600E mutation in 1,320 nervous system tumors reveals high mutation frequencies in pleomorphic xanthoastrocytoma, ganglioglioma and extra-cerebellar pilocytic astrocytoma. Acta Neuropathol. 121, 397-405 (2011).
21. Tatevossian, R.G. et al. MAPK pathway activation and the origins of pediatric low-grade astrocytomas. J. Cell Physiol. 222, 509-514 (2010).
22. Tatevossian, R.G. et al. MYB upregulation and genetic aberrations in a subset of pediatric low-grade gliomas. Acta Neuropathol. 120, 731-743 (2010).
23. Stephens, P.J. et al. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144, 27-40 (2011).
24. Louis, D.N. et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 114, 97-109 (2007).
25. Pollack, I.F. The role of surgery in pediatric gliomas. J. Neurooncol. 42, 271-288 (1999).
26. Wisoff, J.H. et al. Primary neurosurgery for pediatric low-grade gliomas: a prospective multi-institutional study from the Children's Oncology Group. Neurosurgery 68, 1548-1554, discussion 1554-1555 (2011).
27. Louis, D.N. Molecular pathology of malignant gliomas. Annu. Rev. Pathol. 1, 97-117 (2006).
28. Ohgaki, H. & Kleihues, P. Genetic profile of astrocytic and oligodendroglial gliomas. Brain Tumor Pathol. 28, 177-183 (2011).
29. Riemenschneider, M.J., Jeuken, J.W., Wesseling, P. & Reifenberger, G. Molecular diagnostics of gliomas: state of the art. Acta Neuropathol. 120, 567-584 (2010).
30. Cin, H. et al. Oncogenic FAM131B-BRAF fusion resulting from 7q34 deletion comprises an alternative mechanism of MAPK pathway activation in pilocytic astrocytoma. Acta Neuropathol. 121, 763-774 (2011).
31. Jones, D.T. et al. Oncogenic RAF1 rearrangement and a novel BRAF mutation as alternatives to KIAA1549:BRAF fusion in activating the MAPK pathway in pilocytic astrocytoma. Oncogene 28, 2119-2123 (2009).
32. Ciesielski, M.J. & Fenstermaker, R.A. Oncogenic epidermal growth factor receptor mutants with tandem duplication: gene structure and effects on receptor function. Oncogene 19, 810-820 (2000).
33. Lin, W.M. et al. Modeling genomic diversity and tumor dependency in malignant melanoma. Cancer Res. 68, 664-673 (2008).
34. Rand, V. et al. Sequence survey of receptor tyrosine kinases reveals mutations in glioblastomas. Proc. Natl. Acad. Sci. USA 102, 14344-14349 (2005).
35. Singh, D. et al. Transforming fusions of FGFR and TACC genes in human glioblastoma. Science 337, 1231-1235 (2012).
36. Li, F., Zhai, Y.P., Tang, Y.M., Wang, L.P. & Wan, P.J. Identification of a novel partner gene, TPR, fused to FGFR1 in 8p11 myeloproliferative syndrome. Genes Chromosom. Cancer 51, 890-897 (2012).
37. Turner, N. et al. FGFR1 amplification drives endocrine therapy resistance and is a therapeutic target in breast cancer. Cancer Res. 70, 2085-2094 (2010).
38. Turner, N. & Grose, R. Fibroblast growth factor signalling: from development to cancer. Nat. Rev. Cancer 10, 116-129 (2010).
39. 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).
40. Schwartzentruber, J. et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 482, 226-231 (2012).
41. Sturm, D. et al. Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell 22, 425-437 (2012).
42. Wu, G. et al. Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat. Genet. 44, 251-253 (2012).
43. Müller, W., Afra, D. & Schroder, R. Supratentorial recurrences of gliomas. Morphological studies in relation to time intervals with astrocytomas. Acta Neurochir. (Wien) 37, 75-91 (1977).
44. Okamoto, Y. et al. Population-based study on incidence, survival rates, and genetic alterations of low-grade diffuse astrocytomas and oligodendrogliomas. Acta Neuropathol. 108, 49-56 (2004).
45. Peraud, A., Kreth, F.W., Wiestler, O.D., Kleihues, P. & Reulen, H.J. Prognostic impact of TP53 mutations and P53 protein overexpression in supratentorial WHO grade II astrocytomas and oligoastrocytomas. Clin. Cancer Res. 8, 1117-1124 (2002).
46. Pollack, I.F., Claassen, D., al-Shboul, Q., Janosky, J.E. & Deutsch, M. Low-grade gliomas of the cerebral hemispheres in children: an analysis of 71 cases. J. Neurosurg. 82, 536-547 (1995).
47. Jones, D.T. et al. Adult grade II diffuse astrocytomas are genetically distinct from and more aggressive than their paediatric counterparts. Acta Neuropathol. 121, 753-761 (2011).
48. Korshunov, A. et al. Combined molecular analysis of BRAF and IDH1 distinguishes pilocytic astrocytoma from diffuse astrocytoma. Acta Neuropathol. 118, 401-405 (2009).
49. Parsons, D.W. et al. An integrated genomic analysis of human glioblastoma multiforme. Science 321, 1807-1812 (2008).
50. von Deimling, A., Korshunov, A. & Hartmann, C. The next generation of glioma biomarkers: MGMT methylation, BRAF fusions and IDH1 mutations. Brain Pathol. 21, 74-87 (2011).
51. Yan, H. et al. IDH1 and IDH2 mutations in gliomas. N. Engl. J. Med. 360, 765-773 (2009).
52. Ohgaki, H. et al. Genetic pathways to glioblastoma: a population-based study. Cancer Res. 64, 6892-6899 (2004).
53. Ohgaki, H. & Kleihues, P. Genetic pathways to primary and secondary glioblastoma. Am. J. Pathol. 170, 1445-1453 (2007).
54. Bettegowda, C. et al. Mutations in CIC and FUBP1 contribute to human oligodendroglioma. Science 333, 1453-1455 (2011).
55. Yip, S. et al. Concurrent CIC mutations, IDH mutations, and 1p/19q loss distinguish oligodendrogliomas from other cancers. J. Pathol. 226, 7-16 (2012).
56. Flaherty, K.T. et al. Improved survival with MEK inhibition in BRAF-mutated melanoma. N. Engl. J. Med. 367, 107-114 (2012).
57. Katoh, M. Genetic alterations of FGF receptors: an emerging field in clinical cancer diagnostics and therapeutics. Expert Rev. Anticancer Ther. 10, 1375-1379 (2010).
58. Ren, M., Qin, H., Ren, R. & Cowell, J.K. Ponatinib suppresses the development of myeloid and lymphoid malignancies associated with FGFR1 abnormalities. Leukemia 27, 32-40 (2013).
59. Zhang, J. et al. A novel retinoblastoma therapy from genomic and epigenetic analyses. Nature 481, 329-334 (2012).
60. Zhang, J. et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481, 157-163 (2012).
61. Wang, J. et al. CREST maps somatic structural variation in cancer genomes with base-pair resolution. Nat. Methods 8, 652-654 (2011).
62. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
63. McPherson, A. et al. deFuse: an algorithm for gene fusion discovery in tumor RNA-Seq data. PLoS Comput. Biol. 7, e1001138 (2011).
64. Mullighan, C.G. et al. CREBBP mutations in relapsed acute lymphoblastic leukaemia. Nature 471, 235-239 (2011).
65. Zhang, J. et al. SNPdetector: a software tool for sensitive and accurate SNP detection. PLoS Comput. Biol. 1, e53 (2005).
66. Downing, J.R. et al. The Pediatric Cancer Genome Project. Nat. Genet. 44, 619-622 (2012).
67. Dees, N.D. et al. MuSiC: identifying mutational significance in cancer genomes. Genome Res. 22, 1589-1598 (2012).
68. Edmonson, M.N. et al. Bambino: a variant detector and alignment viewer for next-generation sequencing data in the SAM/BAM format. Bioinformatics 27, 865-866 (2011).
69. Mullighan, C.G. Single nucleotide polymorphism microarray analysis of genetic alterations in cancer. Methods Mol. Biol. 730, 235-258 (2011).
70. Persons, D.A. et al. Enforced expression of the GATA-2 transcription factor blocks normal hematopoiesis. Blood 93, 488-499 (1999).
71. Bajenaru, M.L. et al. Astrocyte-specific inactivation of the neurofibromatosis 1 gene (NF1) is insufficient for astrocytoma formation. Mol. Cell Biol. 22, 5100-5113 (2002).
72. Endersby, R., Zhu, X., Hay, N., Ellison, D.W. & Baker, S.J. Nonredundant functions for Akt isoforms in astrocyte growth and gliomagenesis in an orthotopic transplantation model. Cancer Res. 71, 4106-4116 (2011).
73. Jonkers, J. et al. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat. Genet. 29, 418-425 (2001).
74. Ellison, D.W. et al. Definition of disease-risk stratification groups in childhood medulloblastoma using combined clinical, pathologic, and molecular variables. J. Clin. Oncol. 29, 1400-1407 (2011).
75. Tang, B. et al. Characterization of signal transduction through the TCR-ζ chain following T cell stimulation with analogue peptides of type II collagen 260-267. J. Immunol. 160, 3135-3142 (1998).