Recurrent chimeric fusion RNAs in non-cancer tissues and cells

Nucleic Acids Research

Volumn 44, Issue 6, 2016, Pages 2859-2872

  Babiceanu, Mihaela ^a,d   Qin, Fujun ^a   Xie, Zhongqiu ^a   Jia, Yuemeng ^a   Lopez, Kevin ^a   Janus, Nick ^b   Facemire, Loryn ^a   Kumar, Shailesh ^a   Pang, Yuwei ^a   Qi, Yanjun ^b   Lazar, Iulia M ^c   Li, Hui ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b University of Virginia   (United States)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^d SANOFI PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC FUSION RNA; CHIMERIC PROTEIN; PROTEIN; RNA; TRANSCRIPTOME; UNCLASSIFIED DRUG; MESSENGER RNA; SMALL INTERFERING RNA;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER INHIBITION; CANCER TISSUE; CELL DIFFERENTIATION; CELL MOTILITY; CONTROLLED STUDY; EMBRYO; FUSION GENE; GENE; GENE EXPRESSION; GENE FUNCTION; GENE SILENCING; MASS SPECTROMETRY; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PARENTAL GENE; PRIORITY JOURNAL; PROTEIN MOTIF; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA SEQUENCE; RNA SPLICING; RNA TRANSCRIPTION; ANIMAL; ANTAGONISTS AND INHIBITORS; ASTROCYTE; BIOLOGY; CYTOLOGY; FIBROBLAST; GENE FUSION; GENE LIBRARY; GENETICS; HIGH THROUGHPUT SEQUENCING; HUMAN; MESENCHYMAL STROMA CELL; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PRIMARY CELL CULTURE; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; TRANSFORMED CELL LINE;

ANIMALS; ASTROCYTES; BASE SEQUENCE; CELL LINE, TRANSFORMED; COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; FIBROBLASTS; GENE FUSION; GENE LIBRARY; GENE SILENCING; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MESENCHYMAL STROMAL CELLS; MICE; MOLECULAR SEQUENCE DATA; PRIMARY CELL CULTURE; RNA SPLICING; RNA, MESSENGER; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, RNA; SPECIES SPECIFICITY;

EID: 84963985214     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw032     Document Type: Article

References (50)

1. Rowley, J.D. (1999) The role of chromosome translocations in leukemogenesis. Semin. Hematol., 36, 59-72.
2. Heim, S. and Mitelman, F. (2008) Molecular screening for new fusion genes in cancer. Nat. Genet., 40, 685-686.
3. Chase, A., Ernst, T., Fiebig, A., Collins, A., Grand, F., Erben, P., Reiter, A., Schreiber, S. and Cross, N.C. (2010) TFG, a target of chromosome translocations in lymphoma and soft tissue tumors, fuses to GPR128 in healthy individuals. Haematologica, 95, 20-26.
4. Ren, G., Zhang, Y., Mao, X., Liu, X., Mercer, E., Marzec, J., Ding, D., Jiao, Y., Qiu, Q., Sun, Y. et al. (2014) Transcription-mediated chimeric RNAs in prostate cancer: time to revisit old hypothesis? OMICS, 18, 615-624.
5. Yoshihara, K., Wang, Q., Torres-Garcia, W., Zheng, S., Vegesna, R., Kim, H. and Verhaak, R.G. (2015) The landscape and therapeutic relevance of cancer-associated transcript fusions. Oncogene, 34, 4845-4854.
6. Stransky, N., Cerami, E., Schalm, S., Kim, J.L. and Lengauer, C. (2014) The landscape of kinase fusions in cancer. Nat. Commun., 5, 4846-4855.
7. Wu, C.S., Yu, C.Y., Chuang, C.Y., Hsiao, M., Kao, C.F., Kuo, H.C. and Chuang, T.J. (2014) Integrative transcriptome sequencing identifies trans-splicing events with important roles in human embryonic stem cell pluripotency. Genome Res., 24, 25-36.
8. Yuan, H., Qin, F., Movassagh, M., Park, H., Golden, W., Xie, Z., Zhang, P., Sklar, J. and Li, H. (2013) A chimeric RNA characteristic of rhabdomyosarcoma in normal myogenesis process. Cancer Discov., 3, 1394-1403.
9. Ma, L., Yang, S., Zhao, W., Tang, Z., Zhang, T. and Li, K. (2012) Identification and analysis of pig chimeric mRNAs using RNA sequencing data. BMC Genomics, 13, 429-439.
10. Frenkel-Morgenstern, M., Gorohovski, A., Vucenovic, D., Maestre, L. and Valencia, A. (2015) ChiTaRS 2.1-an improved database of the chimeric transcripts and RNA-Seq data with novel sense-antisense chimeric RNA transcripts. Nucleic Acids Res., 43, D68-D75.
11. Houseley, J. and Tollervey, D. (2010) Apparent non-canonical trans-splicing is generated by reverse transcriptase in vitro. PLoS One, 5, e12271.
12. McManus, C.J., Duff, M.O., Eipper-Mains, J. and Graveley, B.R. (2010) Global analysis of trans-splicing in Drosophila. Proc. Natl. Acad. Sci. U.S.A., 107, 12975-12979.
13. Isakoff, S.J., Engelman, J.A., Irie, H.Y., Luo, J., Brachmann, S.M., Pearline, R.V., Cantley, L.C. and Brugge, J.S. (2005) Breast cancer-associated PIK3CA mutations are oncogenic in mammary epithelial cells. Cancer Res., 65, 10992-11000.
14. Jia, W., Qiu, K., He, M., Song, P., Zhou, Q., Zhou, F., Yu, Y., Zhu, D., Nickerson, M.L., Wan, S. et al. (2013) SOAPfuse: an algorithm for identifying fusion transcripts from paired-end RNA-Seq data. Genome Biol., 14, R12.
15. Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., Jones, S.J. and Marra, M.A. (2009) Circos: an information aesthetic for comparative genomics. Genome Res., 19, 1639-1645.
16. Tenga, M.J. and Lazar, I.M. (2013) Proteomic snapshot of breast cancer cell cycle: G1/S transition point. Proteomics, 13, 48-60.
17. Saeed, A.I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T., Thiagarajan, M. et al. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques, 34, 374-378.
18. Fagerberg, L., Hallstrom, B.M., Oksvold, P., Kampf, C., Djureinovic, D., Odeberg, J., Habuka, M., Tahmasebpoor, S., Danielsson, A., Edlund, K. et al. (2014) Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibody-based proteomics. Mol. Cell Proteomics, 13, 397-406.
19. Sigova, A.A., Mullen, A.C., Molinie, B., Gupta, S., Orlando, D.A., Guenther, M.G., Almada, A.E., Lin, C., Sharp, P.A., Giallourakis, C.C. et al. (2013) Divergent transcription of long noncoding RNA/mRNA gene pairs in embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A., 110, 2876-2881.
20. Chen, A., Beetham, H., Black, M.A., Priya, R., Telford, B.J., Guest, J., Wiggins, G.A., Godwin, T.D., Yap, A.S. and Guilford, P.J. (2014) E-cadherin loss alters cytoskeletal organization and adhesion in non-malignant breast cells but is insufficient to induce an epithelial-mesenchymal transition. BMC Cancer, 14, 552-565.
21. Asmann, Y.W., Hossain, A., Necela, B.M., Middha, S., Kalari, K.R., Sun, Z., Chai, H.S., Williamson, D.W., Radisky, D., Schroth, G.P. et al. (2011) A novel bioinformatics pipeline for identification and characterization of fusion transcripts in breast cancer and normal cell lines. Nucleic Acids Res., 39, e100.
22. Kang, B.H., Jensen, K.J., Hatch, J.A. and Janes, K.A. (2013) Simultaneous profiling of 194 distinct receptor transcripts in human cells. Sci. Signal., 6, rs13.
23. Eden, E., Navon, R., Steinfeld, I., Lipson, D. and Yakhini, Z. (2009) GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics, 10, 1-7.
24. Li, X., Zhao, L., Jiang, H. and Wang, W. (2009) Short homologous sequences are strongly associated with the generation of chimeric RNAs in eukaryotes. J. Mol. Evol., 68, 56-65.
25. Ray, D., Kazan, H., Cook, K.B., Weirauch, M.T., Najafabadi, H.S., Li, X., Gueroussov, S., Albu, M., Zheng, H., Yang, A. et al. (2013) A compendium of RNA-binding motifs for decoding gene regulation. Nature, 499, 172-177.
26. Young, P.J., DiDonato, C.J., Hu, D., Kothary, R., Androphy, E.J. and Lorson, C.L. (2002) SRp30c-dependent stimulation of survival motor neuron (SMN) exon 7 inclusion is facilitated by a direct interaction with hTra2 beta 1. Hum. Mol. Genet., 11, 577-587.
27. Ghetti, A., Pinol-Roma, S., Michael, W.M., Morandi, C. and Dreyfuss, G. (1992) hnRNP I, the polypyrimidine tract-binding protein: distinct nuclear localization and association with hnRNAs. Nucleic Acids Res., 20, 3671-3678.
28. Bell, M., Schreiner, S., Damianov, A., Reddy, R. and Bindereif, A. (2002) p110, a novel human U6 snRNP protein and U4/U6 snRNP recycling factor. EMBO J., 21, 2724-2735.
29. Kahvejian, A., Svitkin, Y.V., Sukarieh, R., M'Boutchou, M.N. and Sonenberg, N. (2005) Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Genes Dev., 19, 104-113.
30. Moon, A.M., Stauffer, A.M., Schwindinger, W.F., Sheridan, K., Firment, A. and Robishaw, J.D. (2014) Disruption of G-protein gamma5 subtype causes embryonic lethality in mice. PLoS One, 9, e90970.
31. Nacu, S., Yuan, W., Kan, Z., Bhatt, D., Rivers, C.S., Stinson, J., Peters, B.A., Modrusan, Z., Jung, K., Seshagiri, S. et al. Deep RNA sequencing analysis of readthrough gene fusions in human prostate adenocarcinoma and reference samples. BMC Med. Genomics, 4, 11-32.
32. Plebani, R., Oliver, G.R., Trerotola, M., Guerra, E., Cantanelli, P., Apicella, L., Emerson, A., Albiero, A., Harkin, P.D., Kennedy, R.D. et al. (2013) Long-range transcriptome sequencing reveals cancer cell growth regulatory chimeric mRNA. Neoplasia, 14, 1087-1096.
33. Mitelman, F. and J.B.A.M.F.E. (2015) Mitelman Database of Chromosome Aberrations and Gene Fusions in Cancer.
34. Frattini, V., Trifonov, V., Chan, J.M., Castano, A., Lia, M., Abate, F., Keir, S.T., Ji, A.X., Zoppoli, P., Niola, F. et al. (2013) The integrated landscape of driver genomic alterations in glioblastoma. Nat. Genet., 45, 1141-1149.
35. Wen, H., Li, Y., Malek, S.N., Kim, Y.C., Xu, J., Chen, P., Xiao, F., Huang, X., Zhou, X., Xuan, Z. et al. (2012) New fusion transcripts identified in normal karyotype acute myeloid leukemia. PLoS One, 7, e51203.
36. Atak, Z.K., Gianfelici, V., Hulselmans, G., De Keersmaecker, K., Devasia, A.G., Geerdens, E., Mentens, N., Chiaretti, S., Durinck, K., Uyttebroeck, A. et al. (2013) Comprehensive analysis of transcriptome variation uncovers known and novel driver events in T-cell acute lymphoblastic leukemia. PLoS Genet., 9, e1003997.
37. Mani, R.S., Tomlins, S.A., Callahan, K., Ghosh, A., Nyati, M.K., Varambally, S., Palanisamy, N. and Chinnaiyan, A.M. (2009) Induced chromosomal proximity and gene fusions in prostate cancer. Science, 326, 1230.
38. Barbosa-Morais, N.L., Irimia, M., Pan, Q., Xiong, H.Y., Gueroussov, S., Lee, L.J., Slobodeniuc, V., Kutter, C., Watt, S., Colak, R. et al. (2013) The evolutionary landscape of alternative splicing in vertebrate species. Science, 338, 1587-1593.
39. Rabbitts, T.H. (1994) Chromosomal translocations in human cancer. Nature, 372, 143-149.
40. Rowley, J.D. (1973) Letter: a new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature, 243, 290-293.
41. Tomlins, S.A., Rhodes, D.R., Perner, S., Dhanasekaran, S.M., Mehra, R., Sun, X.W., Varambally, S., Cao, X., Tchinda, J., Kuefer, R. et al. (2005) Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science, 310, 644-648.
42. Qin, F., Song, Z., Babiceanu, M., Song, Y., Facemire, L., Singh, R., Adli, M. and Li, H. (2015) Discovery of CTCF-sensitive cis-Spliced fusion RNAs between adjacent genes in human prostate cells. PLoS Genet, 11, e1005001.
43. Liu, S., Tsai, W.H., Ding, Y., Chen, R., Fang, Z., Huo, Z., Kim, S., Ma, T., Chang, T.Y., Priedigkeit, N.M. et al. (2015) Comprehensive evaluation of fusion transcript detection algorithms and a meta-caller to combine top performing methods in paired-end RNA-Seq data. Nucleic Acids Res., doi:10.1093/nar/gkv1234.
44. Mele, M., Ferreira, P.G., Reverter, F., DeLuca, D.S., Monlong, J., Sammeth, M., Young, T.R., Goldmann, J.M., Pervouchine, D.D., Sullivan, T.J. et al. (2015) Human genomics. The human transcriptome across tissues and individuals. Science, 348, 660-665.
45. Iyer, M.K., Niknafs, Y.S., Malik, R., Singhal, U., Sahu, A., Hosono, Y., Barrette, T.R., Prensner, J.R., Evans, J.R., Zhao, S. et al. (2015) The landscape of long noncoding RNAs in the human transcriptome. Nat. Genet., 47, 199-208.
46. Gaudry, M.J., Storz, J.F., Butts, G.T., Campbell, K.L. and Hoffmann, F.G. (2014) Repeated evolution of chimeric fusion genes in the beta-globin gene family of laurasiatherian mammals. Genome Biol. Evol., 6, 1219-1234.
47. Zhang, Y., Gong, M., Yuan, H., Park, H.G., Frierson, H.F. and Li, H. (2012) Chimeric transcript generated by cis-Splicing of adjacent genes regulates prostate cancer cell proliferation. Cancer Discov., 2, 598-607.
48. Gingeras, T.R. (2009) Implications of chimaeric non-co-linear transcripts. Nature, 461, 206-211.
49. Li, H., Wang, J., Ma, X. and Sklar, J. (2009) Gene fusions and RNA trans-splicing in normal and neoplastic human cells. Cell Cycle, 8, 218-222.
50. Zaphiropoulos, P.G. (2012) Trans-splicing in higher eukaryotes: implications for cancer development? Front. Genet., 2, 92