Comprehensive genomic analysis of malignant pleural mesothelioma identifies recurrent mutations, gene fusions and splicing alterations

Nature Genetics

Volumn 48, Issue 4, 2016, Pages 407-416

  Bueno, Raphael ^a   Stawiski, Eric W ^b   Goldstein, Leonard D ^b   Durinck, Steffen ^b   De Rienzo, Assunta ^a   Modrusan, Zora ^b   Gnad, Florian ^b   Nguyen, Thong T ^b   Jaiswal, Bijay S ^b   Chirieac, Lucian R ^a   Sciaranghella, Daniele ^a   Dao, Nhien ^a   Gustafson, Corinne E ^a   Munir, Kiara J ^a   Hackney, Jason A ^b   Chaudhuri, Amitabha ^c   Gupta, Ravi ^c   Guillory, Joseph ^b   Toy, Karen ^b   Ha, Connie ^b   Chen, Ying Jiun ^b   Stinson, Jeremy ^b   Chaudhuri, Subhra ^b   Zhang, Na ^b   Wu, Thomas D ^b   Sugarbaker, David J ^d   De Sauvage, Frederic J ^b   Richards, William G ^a   Seshagiri, Somasekar ^b   more..

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b GENENTECH INC   (United States)

^c Narayana Health City ^*  (India)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN P53; RNA HELICASE; TRANSCRIPTOME; ISOPROTEIN; ONCOPROTEIN; PHOSPHOPROTEIN; SF3B1 PROTEIN, HUMAN; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ARTICLE; CONTROLLED STUDY; EXOME; GENE; GENE FUSION; GENE MUTATION; HISTONE METHYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; PLEURA MESOTHELIOMA; PRIORITY JOURNAL; RNA SEQUENCE; SF3B1 GENE; TRAF7 GENE; WILD TYPE; ALTERNATIVE RNA SPLICING; DNA MUTATIONAL ANALYSIS; GENETICS; KAPLAN MEIER METHOD; LUNG TUMOR; MESOTHELIOMA; META ANALYSIS; METABOLISM; MORTALITY; MUTATION; PLEURA TUMOR; PROPORTIONAL HAZARDS MODEL; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR CELL LINE;

ALTERNATIVE SPLICING; CELL LINE, TUMOR; DNA MUTATIONAL ANALYSIS; EXOME; HUMANS; KAPLAN-MEIER ESTIMATE; LUNG NEOPLASMS; MESOTHELIOMA; MUTATION; ONCOGENE PROTEINS, FUSION; PHOSPHOPROTEINS; PLEURAL NEOPLASMS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROPORTIONAL HAZARDS MODELS; PROTEIN ISOFORMS; RIBONUCLEOPROTEIN, U2 SMALL NUCLEAR;

EID: 84959205080     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3520     Document Type: Article

References (100)

1. Bueno, R. Multimodality treatments in the management of malignant pleural mesothelioma: an update. Hematol. Oncol. Clin. North Am. 19, 1089-1097, vii (2005
2. Rudd, R. Asbestos and the lung. Medicine 36, 261-264 (2008
3. Carbone, M., et al. Malignant mesothelioma: facts, myths, and hypotheses. J. Cell. Physiol. 227, 44-58 (2012
4. Frank, A.L., & Joshi, T.K. The global spread of asbestos. Ann. Glob. Health 80, 257-262 (2014
5. Christoph, D.C., & Eberhardt, W.E. Systemic treatment of malignant pleural mesothelioma: new agents in clinical trials raise hope of relevant improvements. Curr. Opin. Oncol. 26, 171-181 (2014
6. Bueno R., et al. Pleural biopsy: a reliable method for determining the diagnosis but not subtype in mesothelioma. Ann. Thorac. Surg. 78, 1774-1776 (2004
7. Sugarbaker, D.J., Richards, W.G., & Bueno, R. Extrapleural pneumonectomy in the treatment of epithelioid malignant pleural mesothelioma: novel prognostic implications of combined N1 and N2 nodal involvement based on experience in 529 patients. Ann. Surg. 260, 577-580, discussion 580-582 (2014
8. Baldini E.H., et al. Updated patterns of failure after multimodality therapy for malignant pleural mesothelioma. J. Thorac. Cardiovasc. Surg. 149, 1374-1381 (2015
9. Remon, J., Reguart, N., Corral, J., & Lianes, P. Malignant pleural mesothelioma: new hope in the horizon with novel therapeutic strategies. Cancer Treat. Rev. 41, 27-34 (2015
10. Dong L., et al. Differentially expressed alternatively spliced genes in malignant pleural mesothelioma identified using massively parallel transcriptome sequencing. BMC Med. Genet. 10, 149 (2009
11. Bueno R., et al. Second generation sequencing of the mesothelioma tumor genome. PLoS One 5, e10612 (2010
12. Bott M., et al. The nuclear deubiquitinase BAP1 is commonly inactivated by somatic mutations and 3p21.1 losses in malignant pleural mesothelioma. Nat. Genet. 43, 668-672 (2011
13. Guo, G., et al. Whole-exome sequencing reveals frequent genetic alterations in BAP1, NF2, CDKN2A, and CUL1 in malignant pleural mesothelioma. Cancer Res. 75, 264-269 (2015
14. Bianchi A.B., et al. High frequency of inactivating mutations in the neurofibromatosis type 2 gene (NF2) in primary malignant mesotheliomas. Proc. Natl. Acad. Sci. USA 92, 10854-10858 (1995
15. Cheng J.Q., et al. p16 alterations and deletion mapping of 9p21-p22 in malignant mesothelioma. Cancer Res. 54, 5547-5551 (1994
16. Alexandrov, L.B., Nik-Zainal, S., Wedge, D.C., Campbell, P.J., & Stratton, M.R. Deciphering signatures of mutational processes operative in human cancer. Cell Reports 3, 246-259 (2013
17. Testa J.R., et al. Germline BAP1 mutations predispose to malignant mesothelioma. Nat. Genet. 43, 1022-1025 (2011
18. Travis, W.D., Brambilla, E., Müller-Hermelink, H.K., & Harris, C.C WHO Classification of Tumors of the Lung, Pleura, Thymus and Heart (IARC Press 2004
19. Henderson, D.W., Reid, G., Kao, S.C., van Zandwijk, N., & Klebe, S. Challenges and controversies in the diagnosis of mesothelioma: Part 1. Cytology-only diagnosis, biopsies, immunohistochemistry, discrimination between mesothelioma and reactive mesothelial hyperplasia, and biomarkers. J. Clin. Pathol. 66, 847-853 (2013
20. Gordon G.J., et al. Using gene expression ratios to predict outcome among patients with mesothelioma. J. Natl. Cancer Inst. 95, 598-605 (2003
21. Gordon G.J., et al. Identification of novel candidate oncogenes and tumor suppressors in malignant pleural mesothelioma using large-scale transcriptional profiling. Am. J. Pathol. 166, 1827-1840 (2005
22. Pass H.I., et al. Gene expression profiles predict survival and progression of pleural mesothelioma. Clin. Cancer Res. 10, 849-859 (2004
23. López-Ríos F., et al. Global gene expression profiling of pleural mesotheliomas: overexpression of aurora kinases and P16/CDKN2A deletion as prognostic factors and critical evaluation of microarray-based prognostic prediction. Cancer Res. 66, 2970-2979 (2006
24. de Reyniès A., et al. Molecular classification of malignant pleural mesothelioma: identification of a poor prognosis subgroup linked to the epithelial-To-mesenchymal transition. Clin. Cancer Res. 20, 1323-1334 (2014
25. Kanamori-Katayama M., et al. LRRN4 and UPK3B are markers of primary mesothelial cells. PLoS One 6, e25391 (2011
26. Lamouille, S., Xu, J., & Derynck, R. Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol. 15, 178-196 (2014
27. Moon H.J., et al. MCF-7 cells expressing nuclear associated lysyl oxidase-like 2 (LOXL2) exhibit an epithelial-To-mesenchymal transition (EMT) phenotype and are highly invasive in vitro. J. Biol. Chem. 288, 30000-30008 (2013
28. Durinck S., et al. Spectrum of diverse genomic alterations define non-clear cell renal carcinoma subtypes. Nat. Genet. 47, 13-21 (2015
29. Forbes S.A., et al. COSMIC (the Catalogue of Somatic Mutations in Cancer): a resource to investigate acquired mutations in human cancer. Nucleic Acids Res. 38, D652-D657 (2010
30. Cancer Genome Atlas Research Network. Integrated genomic characterization of papillary thyroid carcinoma. Cell 159 676-690 (2014
31. Cancer Genome Atlas Research Network. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N. Engl. J. Med. 368 2059-2074 (2013
32. Nik-Zainal S., et al. Mutational processes molding the genomes of 21 breast cancers. Cell 149, 979-993 (2012
33. Benedetti, S., Nuvoli, B., Catalani, S., & Galati, R. Reactive oxygen species a double-edged sword for mesothelioma. Oncotarget 6, 16848-16865 (2015
34. Pfeifer, G.P. Mutagenesis at methylated CpG sequences. Curr. Top. Microbiol. Immunol. 301, 259-281 (2006
35. Ng, P.C., & Henikoff, S. Accounting for human polymorphisms predicted to affect protein function. Genome Res. 12, 436-446 (2002
36. Ramensky, V., Bork, P., & Sunyaev, S. Human non-synonymous SNPs: server and survey. Nucleic Acids Res. 30, 3894-3900 (2002
37. González-Pérez, A., & López-Bigas, N. Improving the assessment of the outcome of nonsynonymous SNVs with a consensus deleteriousness score, Condel. Am. J. Hum. Genet. 88, 440-449 (2011
38. Kan Z., et al. Diverse somatic mutation patterns and pathway alterations in human cancers. Nature 466, 869-873 (2010
39. Altomare D.A., et al. A mouse model recapitulating molecular features of human mesothelioma. Cancer Res. 65, 8090-8095 (2005
40. Shukla, S., et al. Methylation silencing of ULK2, an autophagy gene, is essential for astrocyte transformation and tumor growth. J. Biol. Chem. 289, 22306-22318 (2014
41. Qian, C., & Zhou, M.M. SET domain protein lysine methyltransferases: structure, specificity and catalysis. Cell. Mol. Life Sci. 63, 2755-2763 (2006
42. Lawrence M.S., et al. Discovery and saturation analysis of cancer genes across 21 tumour types. Nature 505, 495-501 (2014
43. Robinson G., et al. Novel mutations target distinct subgroups of medulloblastoma. Nature 488, 43-48 (2012
44. Pugh T.J., et al. Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 488, 106-110 (2012
45. Jones D.T., et al. Dissecting the genomic complexity underlying medulloblastoma. Nature 488, 100-105 (2012
46. Jiang L., et al. Exome sequencing identifies somatic mutations of DDX3X in natural killer/T-cell lymphoma. Nat. Genet. 47, 1061-1066 (2015
47. Van Petegem, F. Ryanodine receptors: allosteric ion channel giants. J. Mol. Biol. 427, 31-53 (2015
48. Liu Z., et al. Candidate tumour suppressor CCDC19 regulates miR-184 direct targeting of c-Myc thereby suppressing cell growth in non-small cell lung cancers. J. Cell. Mol. Med. 18, 1667-1679 (2014
49. Clark, V.E., et al. Genomic analysis of non-NF2 meningiomas reveals mutations in TRAF7, KLF4, AKT1, and SMO. Science 339, 1077-1080 (2013
50. Yu W., et al. First somatic mutation of E2F1 in a critical DNA binding residue discovered in well-differentiated papillary mesothelioma of the peritoneum. Genome Biol. 12, R96 (2011
51. Jean, D., Daubriac, J., Le Pimpec-Barthes, F., Galateau-Salle, F., & Jaurand, M.C. Molecular changes in mesothelioma with an impact on prognosis and treatment. Arch. Pathol. Lab. Med. 136, 277-293 (2012
52. Wolff, S., et al. SMK-1, an essential regulator of DAF-16-mediated longevity. Cell 124, 1039-1053 (2006
53. Durinck S., et al. Temporal dissection of tumorigenesis in primary cancers. Cancer Discov. 1, 137-143 (2011
54. Klijn C., et al. A comprehensive transcriptional portrait of human cancer cell lines. Nat. Biotechnol. 33, 306-312 (2015
55. Oltean, S., & Bates, D.O. Hallmarks of alternative splicing in cancer. Oncogene 33, 5311-5318 (2014
56. GTEx Consortium. The Genotype-Tissue Expression (GTEx) pilot analysis: multitissue gene regulation in humans. Science 348 648-660 (2015
57. Franz, W.M., Berger, P., & Wang, J.Y. Deletion of an N-Terminal regulatory domain of the c-Abl tyrosine kinase activates its oncogenic potential. EMBO J. 8, 137-147 (1989
58. Yoshida, K., & Ogawa, S. Splicing factor mutations and cancer. Wiley Interdiscip. Rev. RNA 5, 445-459 (2014
59. DeBoever C., et al. Transcriptome sequencing reveals potential mechanism of cryptic 3' splice site selection in SF3B1-mutated cancers. PLoS Comput. Biol. 11, e1004105 (2015
60. Furney S.J., et al. SF3B1 mutations are associated with alternative splicing in uveal melanoma. Cancer Discov. 3, 1122-1129 (2013
61. Rodrigues L.U., et al. Coordinate loss of MAP3K7 and CHD1 promotes aggressive prostate cancer. Cancer Res. 75, 1021-1034 (2015
62. Bonnal, S., Vigevani, L., & Valcárcel, J. The spliceosome as a target of novel antitumour drugs. Nat. Rev. Drug Discov. 11, 847-859 (2012
63. Cazzola, M., Rossi, M., & Malcovati, L. Biologic and clinical significance of somatic mutations of SF3B1 in myeloid and lymphoid neoplasms. Blood 121, 260-269 (2013
64. Ujiie H., et al. The tumoral and stromal immune microenvironment in malignant pleural mesothelioma: a comprehensive analysis reveals prognostic immune markers. OncoImmunology 4, e1009285 (2015
65. Cornelissen R., et al. Ratio of intratumoral macrophage phenotypes is a prognostic factor in epithelioid malignant pleural mesothelioma. PLoS One 9, e106742 (2014
66. Toung, J.M., Morley, M., Li, M., & Cheung, V.G. RNA-sequence analysis of human B-cells. Genome Res. 21, 991-998 (2011
67. King, J.E., Thatcher, N., Pickering, C.A., & Hasleton, P.S. Sensitivity and specificity of immunohistochemical markers used in the diagnosis of epithelioid mesothelioma: a detailed systematic analysis using published data. Histopathology 48, 223-232 (2006
68. Chaouche-Mazouni, S., et al. Claudin 3, 4, and 15 expression in solid tumors of lung adenocarcinoma versus malignant pleural mesothelioma. Ann. Diagn. Pathol. 19, 193-197 (2015
69. Miyanaga A., et al. Hippo pathway gene mutations in malignant mesothelioma: revealed by RNA and targeted exon sequencing. J. Thorac. Oncol. 10, 844-851 (2015
70. Richards W.G., et al. A microaliquoting technique for precise histological annotation and optimization of cell content in frozen tissue specimens. Biotech. Histochem. 82, 189-197 (2007
71. Morgan, M., et al. ShortRead: a Bioconductor package for input, quality assessment and exploration of high-Throughput sequence data. Bioinformatics 25, 2607-2608 (2009
72. Li, H., & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009
73. DePristo M.A., et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491-498 (2011
74. Saunders C.T., et al. Strelka: accurate somatic small-variant calling from sequenced tumor-normal sample pairs. Bioinformatics 28, 1811-1817 (2012
75. Sherry S.T., et al. dbSNP: the NCBI database of genetic variation. Nucleic Acids Res. 29, 308-311 (2001
76. Fu, W., et al. Analysis of 6, 515 exomes reveals the recent origin of most human protein-coding variants. Nature 493, 216-220 (2013
77. Cerami E., et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2, 401-404 (2012
78. Gao J., et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci. Signal. 6, pl1 (2013
79. Rudin C.M., et al. Comprehensive genomic analysis identifies SOX2 as a frequently amplified gene in small-cell lung cancer. Nat. Genet. 44, 1111-1116 (2012
80. Peifer M., et al. Integrative genome analyses identify key somatic driver mutations of small-cell lung cancer. Nat. Genet. 44, 1104-1110 (2012
81. Brunet, J.P., Tamayo, P., Golub, T.R., & Mesirov, J.P. Metagenes and molecular pattern discovery using matrix factorization. Proc. Natl. Acad. Sci. USA 101, 4164-4169 (2004
82. Dees N.D., et al. MuSiC: identifying mutational significance in cancer genomes. Genome Res. 22, 1589-1598 (2012
83. Lawrence M.S., et al. Mutational heterogeneity in cancer and the search for new cancer-Associated genes. Nature 499, 214-218 (2013
84. Wu, T.D., & Nacu, S. Fast and SNP-Tolerant detection of complex variants and splicing in short reads. Bioinformatics 26, 873-881 (2010
85. Robinson, M.D., McCarthy, D.J., & Smyth, G.K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010
86. Anders, S., & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010
87. Vogelstein B., et al. Cancer genome landscapes. Science 339, 1546-1558 (2013
88. Ritchie M.E., et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015
89. Wu, T.D., & Watanabe, C.K. GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21, 1859-1875 (2005
90. Greenman C.D., et al. PICNIC: an algorithm to predict absolute allelic copy number variation with microarray cancer data. Biostatistics 11, 164-175 (2010
91. Tibshirani, R., & Wang, P. Spatial smoothing and hot spot detection for CGH data using the fused lasso. Biostatistics 9, 18-29 (2008
92. Mermel C.H., et al. GISTIC2.0 facilitates sensitive and confident localization of the targets of focal somatic copy-number alteration in human cancers. Genome Biol. 12, R41 (2011
93. Boegel S., et al. HLA typing from RNA-Seq sequence reads. Genome Med. 4, 102 (2012
94. Vita R., et al. The immune epitope database (IEDB) 3.0. Nucleic Acids Res. 43, D405-D412 (2015
95. Johnston R.J., et al. The immunoreceptor TIGIT regulates antitumor and antiviral CD8+ T cell effector function. Cancer Cell 26, 923-937 (2014
96. Love, M.I., Huber, W., & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014
97. Croft, D., et al. Reactome: a database of reactions, pathways and biological processes. Nucleic Acids Res. 39, D691-D697 (2011
98. Milacic M., et al. Annotating cancer variants and anti-cancer therapeutics in reactome. Cancers (Basel) 4, 1180-1211 (2012
99. 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
100. Anders, S., Reyes, A., & Huber, W. Detecting differential usage of exons from RNA-seq data. Genome Res. 22, 2008-2017 (2012