|
|
Identification of cancer gene fusions based on advanced analysis of the human genome or transcriptome |
Lu Wang() |
Department of Pathology, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA |
|
|
Abstract Many gene fusions have been recognized as important diagnostic and/or prognostic markers in human malignancies. In recent years, novel gene fusions have been identified in cases without prior knowledge of the genetic background. Accompanied by a powerful computational data analysis method, new genome-wide screening approaches were used to detect cryptic genomic aberrations. This review focused on advanced genome-wide screening approaches in fusion gene identification, such as microarray-based approaches, next-generation sequencing, and NanoString nCounter gene expression system. The fundamental rationale and strategy for fusion gene identification using each biotech platform are also discussed.
|
Keywords
gene fusion
cancer
microarray
next-generation sequencing
NanoString nCounter system
|
Corresponding Author(s):
Wang Lu,Email:wangL1@mskcc.org
|
Issue Date: 05 September 2013
|
|
1 |
Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, Varambally S, Cao X, Tchinda J, Kuefer R, Lee C, Montie JE, Shah RB, Pienta KJ, Rubin MA, Chinnaiyan AM. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005; 310(5748): 644–648 doi: 10.1126/science.1117679 pmid:16254181
|
2 |
Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, Fujiwara S, Watanabe H, Kurashina K, Hatanaka H, Bando M, Ohno S, Ishikawa Y, Aburatani H, Niki T, Sohara Y, Sugiyama Y, Mano H. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 2007; 448(7153): 561–566 doi: 10.1038/nature05945 pmid:17625570
|
3 |
Druker BJ, Tamura S, Buchdunger E, Ohno S, Segal GM, Fanning S, Zimmermann J, Lydon NB. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med 1996; 2(5): 561–566 doi: 10.1038/nm0596-561 pmid:8616716
|
4 |
Kantarjian H, Sawyers C, Hochhaus A, Guilhot F, Schiffer C, Gambacorti-Passerini C, Niederwieser D, Resta D, Capdeville R, Zoellner U, Talpaz M, Druker B, Goldman J, O’Brien SG, Russell N, Fischer T, Ottmann O, Cony-Makhoul P, Facon T, Stone R, Miller C, Tallman M, Brown R, Schuster M, Loughran T, Gratwohl A, Mandelli F, Saglio G, Lazzarino M, Russo D, Baccarani M, Morra E; International STI571 CML Study Group.. Hematologic and cytogenetic responses to imatinib mesylate in chronic myelogenous leukemia. N Engl J Med 2002; 346(9): 645–652 doi: 10.1056/NEJMoa011573 pmid:11870241
|
5 |
Druker BJ, Guilhot F, O’Brien SG, Gathmann I, Kantarjian H, Gattermann N, Deininger MW, Silver RT, Goldman JM, Stone RM, Cervantes F, Hochhaus A, Powell BL, Gabrilove JL, Rousselot P, Reiffers J, Cornelissen JJ, Hughes T, Agis H, Fischer T, Verhoef G, Shepherd J, Saglio G, Gratwohl A, Nielsen JL, Radich JP, Simonsson B, Taylor K, Baccarani M, So C, Letvak L, Larson RA; IRIS Investigators. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med 2006; 355(23): 2408–2417 doi: 10.1056/NEJMoa062867 pmid:17151364
|
6 |
Ou SH, Bazhenova L, Camidge DR, Solomon BJ, Herman J, Kain T, Bang YJ, Kwak EL, Shaw AT, Salgia R, Maki RG, Clark JW, Wilner KD, Iafrate AJ. Rapid and dramatic radiographic and clinical response to an ALK inhibitor (crizotinib, PF02341066) in an ALK translocation-positive patient with non-small cell lung cancer. J Thorac Oncol 2010; 5(12): 2044–2046 doi: 10.1097/JTO.0b013e318200f9ff pmid:21102269
|
7 |
Shaw AT, Yeap BY, Solomon BJ, Riely GJ, Gainor J, Engelman JA, Shapiro GI, Costa DB, Ou SH, Butaney M, Salgia R, Maki RG, Varella-Garcia M, Doebele RC, Bang YJ, Kulig K, Selaru P, Tang Y, Wilner KD, Kwak EL, Clark JW, Iafrate AJ, Camidge DR. Effect of crizotinib on overall survival in patients with advanced non-small-cell lung cancer harbouring ALK gene rearrangement: a retrospective analysis. Lancet Oncol 2011; 12(11): 1004–1012 doi: 10.1016/S1470-2045(11)70232-7 pmid:21933749
|
8 |
Mitelman F, Johansson B, Mertens F. Fusion genes and rearranged genes as a linear function of chromosome aberrations in cancer. Nat Genet 2004; 36(4): 331–334 doi: 10.1038/ng1335 pmid:15054488
|
9 |
Mitelman F, Johansson B, Mertens F. The impact of translocations and gene fusions on cancer causation. Nat Rev Cancer 2007; 7(4): 233–245 doi: 10.1038/nrc2091 pmid:17361217
|
10 |
Volik S, Zhao S, Chin K, Brebner JH, Herndon DR, Tao Q, Kowbel D, Huang G, Lapuk A, Kuo WL, Magrane G, De Jong P, Gray JW, Collins C. End-sequence profiling: sequence-based analysis of aberrant genomes. Proc Natl Acad Sci USA 2003; 100(13): 7696–7701 doi: 10.1073/pnas.1232418100 pmid:12788976
|
11 |
Tuzun E, Sharp AJ, Bailey JA, Kaul R, Morrison VA, Pertz LM, Haugen E, Hayden H, Albertson D, Pinkel D, Olson MV, Eichler EE. Fine-scale structural variation of the human genome. Nat Genet 2005; 37(7): 727–732 doi: 10.1038/ng1562 pmid:15895083
|
12 |
Ruan Y, Ooi HS, Choo SW, Chiu KP, Zhao XD, Srinivasan KG, Yao F, Choo CY, Liu J, Ariyaratne P, Bin WG, Kuznetsov VA, Shahab A, Sung WK, Bourque G, Palanisamy N, Wei CL. Fusion transcripts and transcribed retrotransposed loci discovered through comprehensive transcriptome analysis using Paired-End diTags (PETs). Genome Res 2007; 17(6): 828–838 doi: 10.1101/gr.6018607 pmid:17568001
|
13 |
Cerveira N, Ribeiro FR, Peixoto A, Costa V, Henrique R, Jerónimo C, Teixeira MR. TMPRSS2-ERG gene fusion causing ERG overexpression precedes chromosome copy number changes in prostate carcinomas and paired HGPIN lesions. Neoplasia 2006; 8(10): 826–832 doi: 10.1593/neo.06427 pmid:17032499
|
14 |
Hermans KG, van Marion R, van Dekken H, Jenster G, van Weerden WM, Trapman J. TMPRSS2:ERG fusion by translocation or interstitial deletion is highly relevant in androgen-dependent prostate cancer, but is bypassed in late-stage androgen receptor-negative prostate cancer. Cancer Res 2006; 66(22): 10658–10663 doi: 10.1158/0008-5472.CAN-06-1871 pmid:17108102
|
15 |
Iljin K, Wolf M, Edgren H, Gupta S, Kilpinen S, Skotheim RI, Peltola M, Smit F, Verhaegh G, Schalken J, Nees M, Kallioniemi O. TMPRSS2 fusions with oncogenic ETS factors in prostate cancer involve unbalanced genomic rearrangements and are associated with HDAC1 and epigenetic reprogramming. Cancer Res 2006; 66(21): 10242–10246 doi: 10.1158/0008-5472.CAN-06-1986 pmid:17079440
|
16 |
Soller MJ, Isaksson M, Elfving P, Soller W, Lundgren R, Panagopoulos I. Confirmation of the high frequency of the TMPRSS2/ERG fusion gene in prostate cancer. Genes Chromosomes Cancer 2006; 45(7): 717–719 doi: 10.1002/gcc.20329 pmid:16575875
|
17 |
Wang J, Cai Y, Ren C, Ittmann M. Expression of variant TMPRSS2/ERG fusion messenger RNAs is associated with aggressive prostate cancer. Cancer Res 2006; 66(17): 8347–8351 doi: 10.1158/0008-5472.CAN-06-1966 pmid:16951141
|
18 |
Han B, Mehra R, Dhanasekaran SM, Yu J, Menon A, Lonigro RJ, Wang X, Gong Y, Wang L, Shankar S, Laxman B, Shah RB, Varambally S, Palanisamy N, Tomlins SA, Kumar-Sinha C, Chinnaiyan AM. A fluorescence in situ hybridization screen for E26 transformation-specific aberrations: identification of DDX5-ETV4 fusion protein in prostate cancer. Cancer Res 2008; 68(18): 7629–7637 doi: 10.1158/0008-5472.CAN-08-2014 pmid:18794152
|
19 |
Pflueger D, Rickman DS, Sboner A, Perner S, LaFargue CJ, Svensson MA, Moss BJ, Kitabayashi N, Pan Y, de la Taille A, Kuefer R, Tewari AK, Demichelis F, Chee MS, Gerstein MB, Rubin MA. N-myc downstream regulated gene 1 (NDRG1) is fused to ERG in prostate cancer. Neoplasia 2009; 11(8): 804–811 pmid:19649210
|
20 |
Esgueva R, Perner S, J LaFargue C, Scheble V, Stephan C, Lein M, Fritzsche FR, Dietel M, Kristiansen G, Rubin MA. Prevalence of TMPRSS2-ERG and SLC45A3-ERG gene fusions in a large prostatectomy cohort. Mod Pathol 2010; 23(4): 539–546 doi: 10.1038/modpathol.2009.193 pmid:20118910
|
21 |
Rubin MA, Maher CA, Chinnaiyan AM. Common gene rearrangements in prostate cancer. J Clin Oncol 2011; 29(27): 3659–3668 doi: 10.1200/JCO.2011.35.1916 pmid:21859993
|
22 |
Laxman B, Morris DS, Yu J, Siddiqui J, Cao J, Mehra R, Lonigro RJ, Tsodikov A, Wei JT, Tomlins SA, Chinnaiyan AM. A first-generation multiplex biomarker analysis of urine for the early detection of prostate cancer. Cancer Res 2008; 68(3): 645–649 doi: 10.1158/0008-5472.CAN-07-3224 pmid:18245462
|
23 |
Nguyen PN, Violette P, Chan S, Tanguay S, Kassouf W, Aprikian A, Chen JZ. A panel of TMPRSS2:ERG fusion transcript markers for urine-based prostate cancer detection with high specificity and sensitivity. Eur Urol 2011; 59(3): 407–414 doi: 10.1016/j.eururo.2010.11.026 pmid:21144642
|
24 |
Salami SS, Schmidt F, Laxman B, Regan MM, Rickman DS, Scherr D, Bueti G, Siddiqui J, Tomlins SA, Wei JT, Chinnaiyan AM, Rubin MA, Sanda MG. Combining urinary detection of TMPRSS2:ERG and PCA3 with serum PSA to predict diagnosis of prostate cancer. Urol Oncol 2011 pmid:21600800
|
25 |
Tomlins SA, Aubin SM, Siddiqui J, Lonigro RJ, Sefton-Miller L, Miick S, Williamsen S, Hodge P, Meinke J, Blase A, Penabella Y, Day JR, Varambally R, Han B, Wood D, Wang L, Sanda MG, Rubin MA, Rhodes DR, Hollenbeck B, Sakamoto K, Silberstein JL, Fradet Y, Amberson JB, Meyers S, Palanisamy N, Rittenhouse H, Wei JT, Groskopf J, Chinnaiyan AM. Urine TMPRSS2:ERG fusion transcript stratifies prostate cancer risk in men with elevated serum PSA. Sci Transl Med 2011; 3(94): 94ra72 doi: 10.1126/scitranslmed.3001970 pmid:21813756
|
26 |
Wang L, Motoi T, Khanin R, Olshen A, Mertens F, Bridge J, Cin PD, Antonescu CR, Singer S, Hameed M, Bovee JVMG, Hogendoorn PCW, Socci N, Ladanyi M. Identification of a novel, recurrent HEY1-NCOA2 fusion in mesenchymal chondrosarcoma based on a genome-wide screen of exon-level expression data. Genes Chromosomes Cancer 2012; 51(2): 127–139 doi: 10.1002/gcc.20937 pmid:22034177
|
27 |
Jhavar S, Reid A, Clark J, Kote-Jarai Z, Christmas T, Thompson A, Woodhouse C, Ogden C, Fisher C, Corbishley C, De-Bono J, Eeles R, Brewer D, Cooper C. Detection of TMPRSS2-ERG translocations in human prostate cancer by expression profiling using GeneChip Human Exon 1.0 ST arrays. J Mol Diagn 2008; 10(1): 50–57 doi: 10.2353/jmoldx.2008.070085 pmid:18165275
|
28 |
Lin E, Li L, Guan Y, Soriano R, Rivers CS, Mohan S, Pandita A, Tang J, Modrusan Z. Exon array profiling detects EML4-ALK fusion in breast, colorectal, and non-small cell lung cancers. Mol Cancer Res 2009; 7(9): 1466–1476 doi: 10.1158/1541-7786.MCR-08-0522 pmid:19737969
|
29 |
Li F, Feng Y, Fang R, Fang Z, Xia J, Han X, Liu XY, Chen H, Liu H, Ji H. Identification of RET gene fusion by exon array analyses in “pan-negative” lung cancer from never smokers. Cell Res 2012; 22(5): 928–931 doi: 10.1038/cr.2012.27 pmid:22349463
|
30 |
Ozawa T, Brennan CW, Wang L, Squatrito M, Sasayama T, Nakada M, Huse JT, Pedraza A, Utsuki S, Yasui Y, Tandon A, Fomchenko EI, Oka H, Levine RL, Fujii K, Ladanyi M, Holland EC. PDGFRA gene rearrangements are frequent genetic events in PDGFRA-amplified glioblastomas. Genes Dev 2010; 24(19): 2205–2218 doi: 10.1101/gad.1972310 pmid:20889717
|
31 |
Kohlmann A, Grossmann V, Haferlach T. Integration of next-generation sequencing into clinical practice: are we there yet? Semin Oncol 2012; 39(1): 26–36 doi: 10.1053/j.seminoncol.2011.11.008 pmid:22289489
|
32 |
Ozsolak F, Milos PM. RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 2011; 12(2): 87–98 doi: 10.1038/nrg2934 pmid:21191423
|
33 |
Maher CA, Palanisamy N, Brenner JC, Cao X, Kalyana-Sundaram S, Luo S, Khrebtukova I, Barrette TR, Grasso C, Yu J, Lonigro RJ, Schroth G, Kumar-Sinha C, Chinnaiyan AM. Chimeric transcript discovery by paired-end transcriptome sequencing. Proc Natl Acad Sci USA 2009; 106(30): 12353–12358 doi: 10.1073/pnas.0904720106 pmid:19592507
|
34 |
Campbell PJ, Stephens PJ, Pleasance ED, O’Meara S, Li H, Santarius T, Stebbings LA, Leroy C, Edkins S, Hardy C, Teague JW, Menzies A, Goodhead I, Turner DJ, Clee CM, Quail MA, Cox A, Brown C, Durbin R, Hurles ME, Edwards PA, Bignell GR, Stratton MR, Futreal PA. Identification of somatically acquired rearrangements in cancer using genome-wide massively parallel paired-end sequencing. Nat Genet 2008; 40(6): 722–729 doi: 10.1038/ng.128 pmid:18438408
|
35 |
Palanisamy N, Ateeq B, Kalyana-Sundaram S, Pflueger D, Ramnarayanan K, Shankar S, Han B, Cao Q, Cao X, Suleman K, Kumar-Sinha C, Dhanasekaran SM, Chen YB, Esgueva R, Banerjee S, LaFargue CJ, Siddiqui J, Demichelis F, Moeller P, Bismar TA, Kuefer R, Fullen DR, Johnson TM, Greenson JK, Giordano TJ, Tan P, Tomlins SA, Varambally S, Rubin MA, Maher CA, Chinnaiyan AM. Rearrangements of the RAF kinase pathway in prostate cancer, gastric cancer and melanoma. Nat Med 2010; 16(7): 793–798 doi: 10.1038/nm.2166 pmid:20526349
|
36 |
Tanas MR, Sboner A, Oliveira AM, Erickson-Johnson MR, Hespelt J, Hanwright PJ, Flanagan J, Luo Y, Fenwick K, Natrajan R, Mitsopoulos C, Zvelebil M, Hoch BL, Weiss SW, Debiec-Rychter M, Sciot R, West RB, Lazar AJ, Ashworth A, Reis-Filho JS, Lord CJ, Gerstein MB, Rubin MA, Rubin BP. Identification of a disease-defining gene fusion in epithelioid hemangioendothelioma. Sci Transl Med 2011; 3(98): 98ra82 doi: 10.1126/scitranslmed.3002409 pmid:21885404
|
37 |
Sboner A, Habegger L, Pflueger D, Terry S, Chen DZ, Rozowsky JS, Tewari AK, Kitabayashi N, Moss BJ, Chee MS, Demichelis F, Rubin MA, Gerstein MB. FusionSeq: a modular framework for finding gene fusions by analyzing paired-end RNA-sequencing data. Genome Biol 2010; 11(10): R104 doi: 10.1186/gb-2010-11-10-r104 pmid:20964841
|
38 |
Kinsella M, Harismendy O, Nakano M, Frazer KA, Bafna V. Sensitive gene fusion detection using ambiguously mapping RNA-Seq read pairs. Bioinformatics 2011; 27(8): 1068–1075 doi: 10.1093/bioinformatics/btr085 pmid:21330288
|
39 |
McPherson A, Hormozdiari F, Zayed A, Giuliany R, Ha G, Sun MG, Griffith M, Heravi Moussavi A, Senz J, Melnyk N, Pacheco M, Marra MA, Hirst M, Nielsen TO, Sahinalp SC, Huntsman D, Shah SP. deFuse: an algorithm for gene fusion discovery in tumor RNA-Seq data. PLOS Comput Biol 2011; 7(5): e1001138 doi: 10.1371/journal.pcbi.1001138 pmid:21625565
|
40 |
Ge H, Liu K, Juan T, Fang F, Newman M, Hoeck W. FusionMap: detecting fusion genes from next-generation sequencing data at base-pair resolution. Bioinformatics 2011; 27(14): 1922–1928 doi: 10.1093/bioinformatics/btr310 pmid:21593131
|
41 |
Iyer MK, Chinnaiyan AM, Maher CA. ChimeraScan: a tool for identifying chimeric transcription in sequencing data. Bioinformatics 2011; 27(20): 2903–2904 doi: 10.1093/bioinformatics/btr467 pmid:21840877
|
42 |
Kim D, Salzberg SL. TopHat-Fusion: an algorithm for discovery of novel fusion transcripts. Genome Biol 2011; 12(8): R72 doi: 10.1186/gb-2011-12-8-r72 pmid:21835007
|
43 |
Francis RW, Thompson-Wicking K, Carter KW, Anderson D, Kees UR, Beesley AH. FusionFinder: a software tool to identify expressed gene fusion candidates from RNA-Seq data. PLoS ONE 2012; 7(6): e39987 doi: 10.1371/journal.pone.0039987 pmid:22761941
|
44 |
Benelli M, Pescucci C, Marseglia G, Severgnini M, Torricelli F, Magi A. Discovering chimeric transcripts in paired-end RNA-seq data by using EricScript. Bioinformatics 2012; 28(24): 3232–3239 doi: 10.1093/bioinformatics/bts617 pmid:23093608
|
45 |
Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, Dunaway DL, Fell HP, Ferree S, George RD, Grogan T, James JJ, Maysuria M, Mitton JD, Oliveri P, Osborn JL, Peng T, Ratcliffe AL, Webster PJ, Davidson EH, Hood L, Dimitrov K. Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol 2008; 26(3): 317–325 doi: 10.1038/nbt1385 pmid:18278033
|
46 |
Suehara Y, Arcila M, Wang L, Hasanovic A, Ang D, Ito T, Kimura Y, Drilon A, Guha U, Rusch V, Kris MG, Zakowski MF, Rizvi N, Khanin R, Ladanyi M. Identification of KIF5B-RET and GOPC-ROS1 Fusions in Lung Adenocarcinomas through a Comprehensive mRNA-Based Screen for Tyrosine Kinase Fusions. Clin Cancer Res 2012; 18(24): 6599–6608 doi: 10.1158/1078-0432.CCR-12-0838 pmid:23052255
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|