Transposon mutagenesis identifies genetic drivers of Braf V600E melanoma

Nature Genetics

Volumn 47, Issue 5, 2015, Pages 486-495

  Mann, Michael B ^a,b   Black, Michael A ^c   Jones, Devin J ^a   Ward, Jerrold M ^b,j   Yew, Christopher Chin Kuan ^b,k   Newberg, Justin Y ^a   Dupuy, Adam J ^d   Rust, Alistair G ^e,l   Bosenberg, Marcus W ^f   Mcmahon, Martin ^g,h   Print, Cristin G ⁱ   Copeland, Neal G ^a,b   Jenkins, Nancy A ^a,b  

^a HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^c UNIVERSITY OF OTAGO   (New Zealand)

^d UNIVERSITY OF IOWA   (United States)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^f YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ UNIVERSITY OF AUCKLAND   (New Zealand)

^j Global VetPathology   (United States)

^k National Heart Research Institute Singapore   (Singapore)

^l INSTITUTE OF CANCER RESEARCH   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; NETRIN; PHOSPHATIDYLINOSITOL 3 KINASE; RNA; B RAF KINASE; BRAF PROTEIN, HUMAN; CEP350 PROTEIN, HUMAN; MICROTUBULE PROTEIN; NUCLEAR PROTEIN; TRANSPOSON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; GENE; GENE MUTATION; GENETICS; HUMAN; METASTATIC MELANOMA; MOUSE; MUTAGENESIS; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; TRANSPOSON; TUMOR GENE; TUMOR SUPPRESSOR GENE; 129 MOUSE; ANIMAL; C3H MOUSE; C57BL MOUSE; CANCER TRANSPLANTATION; EXOME; FEMALE; GENE FREQUENCY; GENE REGULATORY NETWORK; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; MALE; MELANOMA; MISSENSE MUTATION; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; SECONDARY; SKIN TUMOR; TRANSGENIC MOUSE; TUMOR CELL LINE;

MUS;

ANIMALS; CELL LINE, TUMOR; DNA TRANSPOSABLE ELEMENTS; EXOME; FEMALE; GENE FREQUENCY; GENE REGULATORY NETWORKS; GENES, TUMOR SUPPRESSOR; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MALE; MELANOMA; MICE, 129 STRAIN; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC; MICROTUBULE PROTEINS; MUTAGENESIS; MUTATION, MISSENSE; NEOPLASM TRANSPLANTATION; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS B-RAF; SKIN NEOPLASMS;

EID: 84929132642     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3275     Document Type: Article

References (98)

1. Chin, L., Garraway, L.A. & Fisher, D.E. Malignant melanoma: genetics and therapeutics in the genomic era. Genes Dev. 20, 2149-2182 (2006
2. Yokoyama, S. et al. A novel recurrent mutation in MITF predisposes to familial and sporadic melanoma. Nature 480, 99-103 (2011
3. Robles-Espinoza, C.D. et al. POT1 loss-of-function variants predispose to familial melanoma. Nat. Genet. 46, 478-481 (2014
4. Trigueros-Motos, L. Mutations in POT1 predispose to familial cutaneous malignant melanoma. Clin. Genet. 86, 217-218 (2014
5. Nazarian, R. et al. Melanomas acquire resistance to B-RAFV600E inhibition by RTK or N-RAS upregulation. Nature 468, 973-977 (2010
6. Wilmott, J.S. et al. BRAFV600E protein expression and outcome from BRAF inhibitor treatment in BRAFV600E metastatic melanoma. Br. J. Cancer 108, 924-931 (2013
7. Flaherty, K.T., Yasothan, U. & Kirkpatrick, P. Vemurafenib. Nat. Rev. Drug Discov. 10, 811-812 (2011
8. Damsky, W.E. et al. β-catenin signaling controls metastasis in Braf-Activated Pten-deficient melanomas. Cancer Cell 20, 741-754 (2011
9. Dankort, D. et al. BrafV600E cooperates with Pten loss to induce metastatic melanoma. Nat. Genet. 41, 544-552 (2009
10. Tran, S.L. et al. Absence of distinguishing senescence traits in human melanocytic nevi. J. Invest. Dermatol. 132, 2226-2234 (2012
11. Barretina, J. et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483, 603-607 (2012
12. Berger, M.F. et al. Melanoma genome sequencing reveals frequent PREX2 mutations. Nature 485, 502-506 (2012
13. Hodis, E. et al. A landscape of driver mutations in melanoma. Cell 150, 251-263 (2012
14. Krauthammer, M. et al. Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma. Nat. Genet. 44, 1006-1014 (2012
15. Nikolaev, S.I. et al. Exome sequencing identifies recurrent somatic MAP2K1 and MAP2K2 mutations in melanoma. Nat. Genet. 44, 133-139 (2012
16. Pleasance, E.D. et al. A comprehensive catalogue of somatic mutations from a human cancer genome. Nature 463, 191-196 (2010
17. Prickett, T.D. et al. Analysis of the tyrosine kinome in melanoma reveals recurrent mutations in ERBB4. Nat. Genet. 41, 1127-1132 (2009
18. Prickett, T.D. et al. Exon capture analysis of G protein-coupled receptors identifies activating mutations in GRM3 in melanoma. Nat. Genet. 43, 1119-1126 (2011
19. Stark, M.S. et al. Characterization of the melanoma miRNAome by deep sequencing. PLoS ONE 5, e9685 (2010
20. Stark, M.S. et al. Frequent somatic mutations in MAP3K5 and MAP3K9 in metastatic melanoma identified by exome sequencing. Nat. Genet. 44, 165-169 (2012
21. Turajlic, S. et al. Whole genome sequencing of matched primary and metastatic acral melanomas. Genome Res. 22, 196-207 (2012
22. Wei, X. et al. Exome sequencing identifies GRIN2A as frequently mutated in melanoma. Nat. Genet. 43, 442-446 (2011
23. Howell, P.M. Jr. et al. Epigenetics in human melanoma. Cancer Control 16, 200-218 (2009
24. Sigalotti, L. et al. Epigenetics of human cutaneous melanoma: setting the stage for new therapeutic strategies. J. Transl. Med. 8, 56 (2010
25. Yancovitz, M. et al. Intra- and inter-tumor heterogeneity of BRAFV600E mutations in primary and metastatic melanoma. PLoS ONE 7, e29336 (2012
26. Dankort, D. et al. A new mouse model to explore the initiation, progression, and therapy of BRAFV600E-induced lung tumors. Genes Dev. 21, 379-384 (2007
27. Bosenberg, M. et al. Characterization of melanocyte-specific inducible Cre recombinase transgenic mice. Genesis 44, 262-267 (2006
28. Dupuy, A.J., Akagi, K., Largaespada, D.A., Copeland, N.G. & Jenkins, N.A. Mammalian mutagenesis using a highly mobile somatic Sleeping Beauty transposon system. Nature 436, 221-226 (2005
29. Dupuy, A.J. et al. A modified Sleeping Beauty transposon system that can be used to model a wide variety of human cancers in mice. Cancer Res. 69, 8150-8156 (2009
30. Starr, T.K. et al. A transposon-based genetic screen in mice identifies genes altered in colorectal cancer. Science 323, 1747-1750 (2009
31. Copeland, N.G. & Jenkins, N.A. Harnessing transposons for cancer gene discovery. Nat. Rev. Cancer 10, 696-706 (2010
32. March, H.N. et al. Insertional mutagenesis identifies multiple networks of cooperating genes driving intestinal tumorigenesis. Nat. Genet. 43, 1202-1209 (2011
33. Uren, A.G. et al. Large-scale mutagenesis in p19ARF- and p53-deficient mice identifies cancer genes and their collaborative networks. Cell 133, 727-741 (2008
34. Brett, B.T. et al. Novel molecular and computational methods improve the accuracy of insertion site analysis in Sleeping Beauty-induced tumors. PLoS ONE 6, e24668 (2011
35. Mann, K.M. et al. Sleeping Beauty mutagenesis reveals cooperating mutations and pathways in pancreatic adenocarcinoma. Proc. Natl. Acad. Sci. USA 109, 5934-5941 (2012
36. Karreth, F.A. et al. In vivo identification of tumor- suppressive PTEN ceRNAs in an oncogenic BRAF-induced mouse model of melanoma. Cell 147, 382-395 (2011
37. Ni, T.K., Landrette, S.F., Bjornson, R.D., Bosenberg, M.W. & Xu, T. Low-copy piggyBac transposon mutagenesis in mice identifies genes driving melanoma. Proc. Natl. Acad. Sci. USA 110, E3640-E3649 (2013
38. Davoli, T. et al. Cumulative haploinsufficiency and triplosensitivity drive aneuploidy patterns and shape the cancer genome. Cell 155, 948-962 (2013
39. Solimini, N.L. et al. Recurrent hemizygous deletions in cancers may optimize proliferative potential. Science 337, 104-109 (2012
40. McFadden, D.G. et al. Genetic and clonal dissection of murine small cell lung carcinoma progression by genome sequencing. Cell 156, 1298-1311 (2014
41. Liu, G., Aronovich, E.L., Cui, Z., Whitley, C.B. & Hackett, P.B. Excision of Sleeping Beauty transposons: parameters and applications to gene therapy. J. Gene Med. 6, 574-583 (2004
42. Futreal, P.A. et al. A census of human cancer genes. Nat. Rev. Cancer 4, 177-183 (2004
43. Swanton, C. Intratumor heterogeneity: evolution through space and time. Cancer Res. 72, 4875-4882 (2012
44. Shitashige, M. et al. Traf2- and Nck-interacting kinase is essential for Wnt signaling and colorectal cancer growth. Cancer Res. 70, 5024-5033 (2010
45. Lelièvre, H., Chevrier, V., Tassin, A.M. & Birnbaum, D. Myeloproliferative disorder FOP-FGFR1 fusion kinase recruits phosphoinositide-3 kinase and phospholipase C? at the centrosome. Mol. Cancer 7, 30 (2008
46. Nan, H. et al. Genome-wide association study identifies nidogen 1 (NID1) as a susceptibility locus to cutaneous nevi and melanoma risk. Hum. Mol. Genet. 20, 2673-2679 (2011
47. Amos, C.I. et al. Genome-wide association study identifies novel loci predisposing to cutaneous melanoma. Hum. Mol. Genet. 20, 5012-5023 (2011
48. Barrett, J.H. et al. Genome-wide association study identifies three new melanoma susceptibility loci. Nat. Genet. 43, 1108-1113 (2011
49. Bishop, D.T. et al. Genome-wide association study identifies three loci associated with melanoma risk. Nat. Genet. 41, 920-925 (2009
50. Brown, K.M. et al. Common sequence variants on 20q11.22 confer melanoma susceptibility. Nat. Genet. 40, 838-840 (2008
51. Falchi, M. et al. Genome-wide association study identifies variants at 9p21 and 22q13 associated with development of cutaneous nevi. Nat. Genet. 41, 915-919 (2009
52. Macgregor, S. et al. Genome-wide association study identifies a new melanoma susceptibility locus at 1q21.3. Nat. Genet. 43, 1114-1118 (2011
53. Teerlink, C. et al. A unique genome-wide association analysis in extended Utah high-risk pedigrees identifies a novel melanoma risk variant on chromosome arm 10q. Hum. Genet. 131, 77-85 (2012
54. Sabatino, M. et al. Conservation of genetic alterations in recurrent melanoma supports the melanoma stem cell hypothesis. Cancer Res. 68, 122-131 (2008
55. Brunner, A.L. et al. Transcriptional profiling of lncRNAs and novel transcribed regions across a diverse panel of archived human cancers. Genome Biol. 13, R75 (2012
56. Khaitan, D. et al. The melanoma-upregulated long noncoding RNA SPRY4-IT1 modulates apoptosis and invasion. Cancer Res. 71, 3852-3862 (2011
57. Derrien, T. et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 22, 1775-1789 (2012
58. Harrow, J. et al. GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res. 22, 1760-1774 (2012
59. Harrow, J. et al. GENCODE: producing a reference annotation for ENCODE. Genome Biol. 7 (suppl.), S4.1-S4.9 (2006
60. Akavia, U.D. et al. An integrated approach to uncover drivers of cancer. Cell 143, 1005-1017 (2010
61. Lin, W.M. et al. Modeling genomic diversity and tumor dependency in malignant melanoma. Cancer Res. 68, 664-673 (2008
62. Xing, F. et al. Concurrent loss of the PTEN and RB1 tumor suppressors attenuates RAF dependence in melanomas harboring V600EBRAF. Oncogene 31, 446-457 (2012
63. Sanchez-Garcia, F., Akavia, U.D., Mozes, E. & Pe'er, D. JISTIC: identification of significant targets in cancer. BMC Bioinformatics 11, 189 (2010
64. Huang, D.W. et al. DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res. 35, W169-W175 (2007
65. Kanehisa, M. & Goto, S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27-30 (2000
66. Araki, H., Knapp, C., Tsai, P. & Print, C.P. GeneSetDB: a comprehensive meta-database, statistical and visualisation framework for gene set analysis. FEBS Open Bio 2, 76-82 (2012
67. Biankin, A.V. et al. Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes. Nature 491, 399-405 (2012
68. Sanz-Moreno, V. et al. Rac activation and inactivation control plasticity of tumor cell movement. Cell 135, 510-523 (2008
69. Bogunovic, D. et al. Immune profile and mitotic index of metastatic melanoma lesions enhance clinical staging in predicting patient survival. Proc. Natl. Acad. Sci. USA 106, 20429-20434 (2009
70. Le Clech, M. Role of CAP350 in centriolar tubule stability and centriole assembly. PLoS ONE 3, e3855 (2008
71. Patel, H., Truant, R., Rachubinski, R.A. & Capone, J.P. Activity and subcellular compartmentalization of peroxisome proliferator-Activated receptor a are altered by the centrosome-Associated protein CAP350. J. Cell Sci. 118, 175-186 (2005
72. Lim, J. et al. A protein-protein interaction network for human inherited ataxias and disorders of Purkinje cell degeneration. Cell 125, 801-814 (2006
73. Vandamme, J., Völkel, P., Rosnoblet, C., Le Faou, P. & Angrand, P.O. Interaction proteomics analysis of Polycomb proteins defines distinct PRC1 complexes in mammalian cells. Mol. Cell. Proteomics 10, M110.002642 (2011
74. Danielsen, J.M. et al. Mass spectrometric analysis of lysine ubiquitylation reveals promiscuity at site level. Mol. Cell. Proteomics 10, M110.003590 (2010
75. Hutchins, J.R. et al. Systematic analysis of human protein complexes identifies chromosome segregation proteins. Science 328, 593-599 (2010
76. Varjosalo, M. et al. The protein interaction landscape of the human CMGC kinase group. Cell Rep. 3, 1306-1320 (2013
77. Emanuele, M.J. et al. Global identification of modular cullin-RING ligase substrates. Cell 147, 459-474 (2011
78. Udeshi, N.D. et al. Methods for quantification of in vivo changes in protein ubiquitination following proteasome and deubiquitinase inhibition. Mol. Cell. Proteomics 11, 148-159 (2012
79. Woods, N.T. et al. Charting the landscape of tandem BRCT domain-mediated protein interactions. Sci. Signal. 5, rs6 (2012
80. Bandyopadhyay, S. et al. A human MAP kinase interactome. Nat. Methods 7, 801-805 (2010
81. Wagner, S.A. et al. A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol. Cell. Proteomics 10, M111.013284 (2011
82. Glatter, T., Wepf, A., Aebersold, R. & Gstaiger, M. An integrated workflow for charting the human interaction proteome: insights into the PP2A system. Mol. Syst. Biol. 5, 237 (2009
83. Kim, W. et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 44, 325-340 (2011
84. Yan, X., Habedanck, R. & Nigg, E.A. A complex of two centrosomal proteins, CAP350 and FOP, cooperates with EB1 in microtubule anchoring. Mol. Biol. Cell 17, 634-644 (2006
85. Stites, E.C. The response of cancers to BRAF inhibition underscores the importance of cancer systems biology. Sci. Signal. 5, pe46 (2012
86. Azmi, A.S., Wang, Z., Philip, P.A., Mohammad, R.M. & Sarkar, F.H. Proof of concept: network and systems biology approaches aid in the discovery of potent anticancer drug combinations. Mol. Cancer Ther. 9, 3137-3144 (2010
87. Collier, L.S., Carlson, C.M., Ravimohan, S., Dupuy, A.J. & Largaespada, D.A. Cancer gene discovery in solid tumours using transposon-based somatic mutagenesis in the mouse. Nature 436, 272-276 (2005
88. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009
89. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009
90. Koboldt, D.C. et al. VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res. 22, 568-576 (2012
91. R Development Core Team R.: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2008, 2013
92. Wang, K., Li, M. & Hakonarson, H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 38, e164 (2010
93. Knüppel, R., Dietze, P., Lehnberg, W., Frech, K. & Wingender, E. TRANSFAC retrieval program: a network model database of eukaryotic transcription regulating sequences and proteins. J. Comput. Biol. 1, 191-198 (1994
94. Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504 (2003
95. Irizarry, R.A. et al. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15 (2003
96. Harrington, D.P. & Fleming, T.R. A class of rank test procedures for censored survival data. Biometrika 69, 553-566 (1982
97. Spandidos, A., Wang, X., Wang, H. & Seed, B. PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res. 38, D792-D799 (2010
98. Henare, K. et al. Dissection of stromal and cancer cell-derived signals in melanoma xenografts before and after treatment with DMXAA. Br. J. Cancer 106, 1134-1147 (2012