Long non-coding RNAs in cancer: implications for personalized therapy

Springer Science and Business Media LLC - Tập 38 Số 1 - Trang 17-28 - 2015
Marianna Vitiello1, Andrea Tuccoli1, Laura Poliseno2,1
1Oncogenomics Unit, Core Research Laboratory, Istituto Toscano Tumori c/o IFC-CNR, Pisa, Italy
2Institute of Clinical Physiology, National Research Council, Pisa, Italy

Tóm tắt

Từ khóa


Tài liệu tham khảo

C. Trapnell, B.A. Williams, G. Pertea, A. Mortazavi, G. Kwan, M.J. van Baren, S.L. Salzberg, B.J. Wold, L. Pachter, Nat. Biotechnol. 28, 511–515 (2010). doi: 10.1038/nbt.1621

J. Sana, P. Faltejskova, M. Svoboda, O. Slaby, J. Transl. Med. 10, 103 (2012). doi: 10.1186/1479-5876-10-103

E.P. Consortium, B.E. Bernstein, E. Birney, I. Dunham, E.D. Green, C. Gunter, M. Snyder, Nature 489, 57–74 (2012). doi: 10.1038/nature11247

T. Derrien, R. Johnson, G. Bussotti, A. Tanzer, S. Djebali, H. Tilgner, G. Guernec, D. Martin, A. Merkel, D.G. Knowles, J. Lagarde, L. Veeravalli, X. Ruan, Y. Ruan, T. Lassmann, P. Carninci, J.B. Brown, L. Lipovich, J.M. Gonzalez, M. Thomas, C.A. Davis, R. Shiekhattar, T.R. Gingeras, T.J. Hubbard, C. Notredame, J. Harrow, R. Guigo, Genome Res. 22, 1775–1789 (2012). doi: 10.1101/gr.132159.111

L. Yang, J.E. Froberg, J.T. Lee, Trends Biochem. Sci. 39, 35–43 (2014). doi: 10.1016/j.tibs.2013.10.002

C. Ernst, C.C. Morton, Front. Cell. Neurosci. 7, 168 (2013). doi: 10.3389/fncel.2013.00168

H. Ling, M. Fabbri, G.A. Calin, Nature reviews. Drug Discov. 12, 847–865 (2013). doi: 10.1038/nrd4140

S. Djebali, C.A. Davis, A. Merkel, A. Dobin, T. Lassmann, A. Mortazavi, A. Tanzer, J. Lagarde, W. Lin, F. Schlesinger, C. Xue, G.K. Marinov, J. Khatun, B.A. Williams, C. Zaleski, J. Rozowsky, M. Roder, F. Kokocinski, R.F. Abdelhamid, T. Alioto, I. Antoshechkin, M.T. Baer, N.S. Bar, P. Batut, K. Bell, I. Bell, S. Chakrabortty, X. Chen, J. Chrast, J. Curado, T. Derrien, J. Drenkow, E. Dumais, J. Dumais, R. Duttagupta, E. Falconnet, M. Fastuca, K. Fejes-Toth, P. Ferreira, S. Foissac, M.J. Fullwood, H. Gao, D. Gonzalez, A. Gordon, H. Gunawardena, C. Howald, S. Jha, R. Johnson, P. Kapranov, B. King, C. Kingswood, O.J. Luo, E. Park, K. Persaud, J.B. Preall, P. Ribeca, B. Risk, D. Robyr, M. Sammeth, L. Schaffer, L.H. See, A. Shahab, J. Skancke, A.M. Suzuki, H. Takahashi, H. Tilgner, D. Trout, N. Walters, H. Wang, J. Wrobel, Y. Yu, X. Ruan, Y. Hayashizaki, J. Harrow, M. Gerstein, T. Hubbard, A. Reymond, S.E. Antonarakis, G. Hannon, M.C. Giddings, Y. Ruan, B. Wold, P. Carninci, R. Guigo, T.R. Gingeras, Nature 489, 101–108 (2012). doi: 10.1038/nature11233

S. van Heesch, M. van Iterson, J. Jacobi, S. Boymans, P.B. Essers, E. de Bruijn, W. Hao, A.W. Macinnes, E. Cuppen, M. Simonis, Genome Biol. 15, R6 (2014). doi: 10.1186/gb-2014-15-1-r6

A.M. Khalil, M. Guttman, M. Huarte, M. Garber, A. Raj, D. Rivea Morales, K. Thomas, A. Presser, B.E. Bernstein, A. van Oudenaarden, A. Regev, E.S. Lander, J.L. Rinn, Proc. Natl. Acad. Sci. U. S. A. 106, 11667–11672 (2009). doi: 10.1073/pnas.0904715106

J. Zhao, T.K. Ohsumi, J.T. Kung, Y. Ogawa, D.J. Grau, K. Sarma, J.J. Song, R.E. Kingston, M. Borowsky, J.T. Lee, Mol. Cell 40, 939–953 (2010). doi: 10.1016/j.molcel.2010.12.011

X. Zhou, Q. Gao, J. Wang, X. Zhang, K. Liu, Z. Duan, Gynecol. Oncol. (2014). doi: 10.1016/j.ygyno.2014.02.033

J. Wang, X. Liu, H. Wu, P. Ni, Z. Gu, Y. Qiao, N. Chen, F. Sun, Q. Fan, Nucleic Acids Res. 38, 5366–5383 (2010). doi: 10.1093/nar/gkq285

T.K. Kim, M. Hemberg, J.M. Gray, A.M. Costa, D.M. Bear, J. Wu, D.A. Harmin, M. Laptewicz, K. Barbara-Haley, S. Kuersten, E. Markenscoff-Papadimitriou, D. Kuhl, H. Bito, P.F. Worley, G. Kreiman, M.E. Greenberg, Nature 465, 182–187 (2010). doi: 10.1038/nature09033

P.P. Amaral, M.B. Clark, D.K. Gascoigne, M.E. Dinger, J.S. Mattick, Nucleic Acids Res. 39, D146–D151 (2011). doi: 10.1093/nar/gkq1138

P.J. Volders, K. Helsens, X. Wang, B. Menten, L. Martens, K. Gevaert, J. Vandesompele, P. Mestdagh, Nucleic Acids Res. 41, D246–D251 (2013). doi: 10.1093/nar/gks915

C. Park, N. Yu, I. Choi, W. Kim, S. Lee, Bioinformatics (2014). doi: 10.1093/bioinformatics/btu325

S.W. Cheetham, F. Gruhl, J.S. Mattick, M.E. Dinger, Br. J. Cancer 108, 2419–2425 (2013). doi: 10.1038/bjc.2013.233

E.A. Gibb, C.J. Brown, W.L. Lam, Mol. Cancer 10, 38 (2011). doi: 10.1186/1476-4598-10-38

N. Hauptman, D. Glavac, Int. J. Mol. Sci. 14, 4655–4669 (2013). doi: 10.3390/ijms14034655

S.A. Mitra, A.P. Mitra, T.J. Triche, Front. Genet. 3, 17 (2012). doi: 10.3389/fgene.2012.00017

H. Zhang, Z. Chen, X. Wang, Z. Huang, Z. He, Y. Chen, J Hematol Oncol 6, 37 (2013). doi: 10.1186/1756-8722-6-37

F. Lai, R. Shiekhattar, Cell Res. 24, 263–264 (2014). doi: 10.1038/cr.2014.13

C. Martin, Y. Zhang, Curr. Opin. Cell Biol. 19, 266–272 (2007). doi: 10.1016/j.ceb.2007.04.002

E.B. Zhang, R. Kong, D.D. Yin, L.H. You, M. Sun, L. Han, T.P. Xu, R. Xia, J.S. Yang, W. De, J. Chen, Oncotarget 5, 2276–2292 (2014)

J.S. Mattick, M.J. Gagen, Mol. Biol. Evol. 18, 1611–1630 (2001)

J.S. Mattick, P.P. Amaral, M.E. Dinger, T.R. Mercer, M.F. Mehler, BioEssays : News Rev Mol Cell Dev Biol 31, 51–59 (2009). doi: 10.1002/bies.080099

Y. Kotake, T. Nakagawa, K. Kitagawa, S. Suzuki, N. Liu, M. Kitagawa, Y. Xiong, Oncogene 30, 1956–1962 (2011). doi: 10.1038/onc.2010.568

T. Kawakami, C. Zhang, T. Taniguchi, C.J. Kim, Y. Okada, H. Sugihara, T. Hattori, A.E. Reeve, O. Ogawa, K. Okamoto, Oncogene 23, 6163–6169 (2004). doi: 10.1038/sj.onc.1207808

E. Yildirim, J.E. Kirby, D.E. Brown, F.E. Mercier, R.I. Sadreyev, D.T. Scadden, J.T. Lee, Cell 152, 727–742 (2013). doi: 10.1016/j.cell.2013.01.034

R.A. Gupta, N. Shah, K.C. Wang, J. Kim, H.M. Horlings, D.J. Wong, M.C. Tsai, T. Hung, P. Argani, J.L. Rinn, Y. Wang, P. Brzoska, B. Kong, R. Li, R.B. West, M.J. van de Vijver, S. Sukumar, H.Y. Chang, Nature 464, 1071–1076 (2010). doi: 10.1038/nature08975

J.L. Rinn, M. Kertesz, J.K. Wang, S.L. Squazzo, X. Xu, S.A. Brugmann, L.H. Goodnough, J.A. Helms, P.J. Farnham, E. Segal, H.Y. Chang, Cell 129, 1311–1323 (2007). doi: 10.1016/j.cell.2007.05.022

K.L. Yap, S. Li, A.M. Munoz-Cabello, S. Raguz, L. Zeng, S. Mujtaba, J. Gil, M.J. Walsh, M.M. Zhou, Mol. Cell 38, 662–674 (2010). doi: 10.1016/j.molcel.2010.03.021

D. Chen, Z. Zhang, C. Mao, Y. Zhou, L. Yu, Y. Yin, S. Wu, X. Mou, Y. Zhu, Cell. Immunol. 289, 91–96 (2014). doi: 10.1016/j.cellimm.2014.03.015

B. Payer, J.T. Lee, Annu. Rev. Genet. 42, 733–772 (2008). doi: 10.1146/annurev.genet.42.110807.091711

C. Kanduri, J. Whitehead, F. Mohammad, FEBS Lett. 583, 857–864 (2009). doi: 10.1016/j.febslet.2009.02.004

J. Feng, C. Bi, B.S. Clark, R. Mady, P. Shah, J.D. Kohtz, Genes Dev. 20, 1470–1484 (2006). doi: 10.1101/gad.1416106

L. Yang, C. Lin, C. Jin, J.C. Yang, B. Tanasa, W. Li, D. Merkurjev, K.A. Ohgi, D. Meng, J. Zhang, C.P. Evans, M.G. Rosenfeld, Nature 500, 598–602 (2013). doi: 10.1038/nature12451

V. Tripathi, J.D. Ellis, Z. Shen, D.Y. Song, Q. Pan, A.T. Watt, S.M. Freier, C.F. Bennett, A. Sharma, P.A. Bubulya, B.J. Blencowe, S.G. Prasanth, K.V. Prasanth, Mol. Cell 39, 925–938 (2010). doi: 10.1016/j.molcel.2010.08.011

M. Beltran, I. Puig, C. Pena, J.M. Garcia, A.B. Alvarez, R. Pena, F. Bonilla, A.G. de Herreros, Genes Dev. 22, 756–769 (2008). doi: 10.1101/gad.455708

K. Gumireddy, A. Li, J. Yan, T. Setoyama, G.J. Johannes, U.A. Orom, J. Tchou, Q. Liu, L. Zhang, D.W. Speicher, G.A. Calin, Q. Huang, EMBO J 32, 2672–2684 (2013). doi: 10.1038/emboj.2013.188

S. Loewer, M.N. Cabili, M. Guttman, Y.H. Loh, K. Thomas, I.H. Park, M. Garber, M. Curran, T. Onder, S. Agarwal, P.D. Manos, S. Datta, E.S. Lander, T.M. Schlaeger, G.Q. Daley, J.L. Rinn, Nat. Genet. 42, 1113–1117 (2010). doi: 10.1038/ng.710

K. Panzitt, M.M. Tschernatsch, C. Guelly, T. Moustafa, M. Stradner, H.M. Strohmaier, C.R. Buck, H. Denk, R. Schroeder, M. Trauner, K. Zatloukal, Gastroenterology 132, 330–342 (2007). doi: 10.1053/j.gastro.2006.08.026

I.J. Matouk, I. Abbasi, A. Hochberg, E. Galun, H. Dweik, M. Akkawi, Eur J Gastroenterol Hepatol 21, 688–692 (2009)

Y. Zhao, Q. Guo, J. Chen, J. Hu, S. Wang, Y. Sun, Oncol. Rep. 31, 358–364 (2014). doi: 10.3892/or.2013.2850

B.P. Lewis, C.B. Burge, D.P. Bartel, Cell 120, 15–20 (2005). doi: 10.1016/j.cell.2004.12.035

S. Das, S. Ghosal, R. Sen, J. Chakrabarti, PLoS One 9, e98965 (2014). doi: 10.1371/journal.pone.0098965

T. Gutschner, M. Hammerle, M. Eissmann, J. Hsu, Y. Kim, G. Hung, A. Revenko, G. Arun, M. Stentrup, M. Gross, M. Zornig, A.R. MacLeod, D.L. Spector, S. Diederichs, Cancer Res. 73, 1180–1189 (2013). doi: 10.1158/0008-5472.CAN-12-2850

D.A. Sartori, D.W. Chan, Curr. Opin. Oncol. (2014). doi: 10.1097/CCO.0000000000000065

J.C. Akers, D. Gonda, R. Kim, B.S. Carter, C.C. Chen, J. Neuro-Oncol. 113, 1–11 (2013). doi: 10.1007/s11060-013-1084-8

H. Tang, Z. Wu, J. Zhang, B. Su, Mol Med Rep 7, 761–766 (2013). doi: 10.3892/mmr.2012.1254

E.M. Reis, S. Verjovski-Almeida, Front. Genet. 3, 32 (2012). doi: 10.3389/fgene.2012.00032

E.A. Gibb, E.A. Vucic, K.S. Enfield, G.L. Stewart, K.M. Lonergan, J.Y. Kennett, D.D. Becker-Santos, C.E. MacAulay, S. Lam, C.J. Brown, W.L. Lam, PLoS One 6, e25915 (2011). doi: 10.1371/journal.pone.0025915

G.L. Lee, A. Dobi, S. Srivastava, Nature reviews. Urology 8, 123–124 (2011). doi: 10.1038/nrurol.2011.10

Y. Fradet, F. Saad, A. Aprikian, J. Dessureault, M. Elhilali, C. Trudel, B. Masse, L. Piche, C. Chypre, Urology 64, 311–315 (2004). doi: 10.1016/j.urology.2004.03.052 . discussion 315–316

M. Tinzl, M. Marberger, S. Horvath, C. Chypre, Eur. Urol. 46, 182–186 (2004). doi: 10.1016/j.eururo.2004.06.004 . discussion 187

S.B. Shappell, Rev Urol 10, 44–69 (2008)

S.B. Shappell, J. Fulmer, D. Arguello, B.S. Wright, J.R. Oppenheimer, M.J. Putzi, Urology 73, 363–368 (2009). doi: 10.1016/j.urology.2008.08.459

L.S. Marks, D.G. Bostwick, Rev Urol 10, 175–181 (2008)

D. Hessels, J.M. Klein Gunnewiek, I. van Oort, H.F. Karthaus, G.J. van Leenders, B. van Balken, L.A. Kiemeney, J.A. Witjes, J.A. Schalken, Eur. Urol. 44, 8–15 (2003). discussion 15–16

T. Nakagawa, H. Endo, M. Yokoyama, J. Abe, K. Tamai, N. Tanaka, I. Sato, S. Takahashi, T. Kondo, K. Satoh, Biochem. Biophys. Res. Commun. 436, 319–324 (2013). doi: 10.1016/j.bbrc.2013.05.101

H. Ono, N. Motoi, H. Nagano, E. Miyauchi, M. Ushijima, M. Matsuura, S. Okumura, M. Nishio, T. Hirose, N. Inase, Y. Ishikawa, Cancer Med (2014). doi: 10.1002/cam4.220

X.H. Liu, Z.L. Liu, M. Sun, J. Liu, Z.X. Wang, W. De, BMC Cancer 13, 464 (2013). doi: 10.1186/1471-2407-13-464

R. Kogo, T. Shimamura, K. Mimori, K. Kawahara, S. Imoto, T. Sudo, F. Tanaka, K. Shibata, A. Suzuki, S. Komune, S. Miyano, M. Mori, Cancer Res. 71, 6320–6326 (2011). doi: 10.1158/0008-5472.CAN-11-1021

M. Svoboda, J. Slyskova, M. Schneiderova, P. Makovicky, L. Bielik, M. Levy, L. Lipska, B. Hemmelova, Z. Kala, M. Protivankova, O. Vycital, V. Liska, L. Schwarzova, L. Vodickova, P. Vodicka, Carcinogenesis (2014). doi: 10.1093/carcin/bgu055

X. He, W. Bao, X. Li, Z. Chen, Q. Che, H. Wang, X.P. Wan, Int J Mol Med 33, 325–332 (2014). doi: 10.3892/ijmm.2013.1570

J. Huang, P. Ke, L. Guo, W. Wang, H. Tan, Y. Liang, S. Yao, Int J Gynecol Cancer Off J Int Gynecol Cancer Soc 24, 635–642 (2014). doi: 10.1097/IGC.0000000000000121

L. Lu, G. Zhu, C. Zhang, Q. Deng, D. Katsaros, S.T. Mayne, H.A. Risch, L. Mu, E.M. Canuto, G. Gregori, C. Benedetto, H. Yu, Breast Cancer Res. Treat. 136, 875–883 (2012). doi: 10.1007/s10549-012-2314-z

K.P. Sorensen, M. Thomassen, Q. Tan, M. Bak, S. Cold, M. Burton, M.J. Larsen, T.A. Kruse, Breast Cancer Res. Treat. 142, 529–536 (2013). doi: 10.1007/s10549-013-2776-7

X. Li, Z. Wu, Q. Mei, X. Li, M. Guo, X. Fu, W. Han, Br. J. Cancer 109, 2266–2278 (2013). doi: 10.1038/bjc.2013.548

X.B. Lv, G.Y. Lian, H.R. Wang, E. Song, H. Yao, M.H. Wang, PLoS One 8, e63516 (2013). doi: 10.1371/journal.pone.0063516

F.J. Chen, M. Sun, S.Q. Li, Q.Q. Wu, L. Ji, Z.L. Liu, G.Z. Zhou, G. Cao, L. Jin, H.W. Xie, C.M. Wang, J. Lv, W. De, M. Wu, X.F. Cao, Mol. Carcinog. 52, 908–915 (2013). doi: 10.1002/mc.21944

Z. Yang, L. Zhou, L.M. Wu, M.C. Lai, H.Y. Xie, F. Zhang, S.S. Zheng, Ann. Surg. Oncol. 18, 1243–1250 (2011). doi: 10.1245/s10434-011-1581-y

K. Kim, I. Jutooru, G. Chadalapaka, G. Johnson, J. Frank, R. Burghardt, S. Kim, S. Safe, Oncogene 32, 1616–1625 (2013). doi: 10.1038/onc.2012.193

L. Huang, L.M. Liao, A.W. Liu, J.B. Wu, X.L. Cheng, J.X. Lin, M. Zheng, Arch. Gynecol. Obstet. (2014). doi: 10.1007/s00404-014-3236-2

Y. Nie, X. Liu, S. Qu, E. Song, H. Zou, C. Gong, Cancer Sci. 104, 458–464 (2013). doi: 10.1111/cas.12092

M.C. Lai, Z. Yang, L. Zhou, Q.Q. Zhu, H.Y. Xie, F. Zhang, L.M. Wu, L.M. Chen, S.S. Zheng, Med. Oncol. 29, 1810–1816 (2012). doi: 10.1007/s12032-011-0004-z

L.H. Schmidt, T. Spieker, S. Koschmieder, S. Schaffers, J. Humberg, D. Jungen, E. Bulk, A. Hascher, D. Wittmer, A. Marra, L. Hillejan, K. Wiebe, W.E. Berdel, R. Wiewrodt, C. Muller-Tidow, J Thorac Oncol Off Publ Int Assoc Study Lung Cancer 6, 1984–1992 (2011). doi: 10.1097/JTO.0b013e3182307eac

Y. Han, Y. Liu, L. Nie, Y. Gui, Z. Cai, Urology 81, 209.e1–209.e7 (2013). doi: 10.1016/j.urology.2012.08.044

P. Ji, S. Diederichs, W. Wang, S. Boing, R. Metzger, P.M. Schneider, N. Tidow, B. Brandt, H. Buerger, E. Bulk, M. Thomas, W.E. Berdel, H. Serve, C. Muller-Tidow, Oncogene 22, 8031–8041 (2003). doi: 10.1038/sj.onc.1206928

P. Qi, M.D. Xu, S.J. Ni, X.H. Shen, P. Wei, D. Huang, C. Tan, W.Q. Sheng, X.Y. Zhou, X. Du, Mol. Carcinog. (2014). doi: 10.1002/mc.22137

Z. Hou, W. Zhao, J. Zhou, L. Shen, P. Zhan, C. Xu, C. Chang, H. Bi, J. Zou, X. Yao, R. Huang, L. Yu, J. Yan, Int. J. Biochem. Cell Biol. (2014). doi: 10.1016/j.biocel.2014.06.004

M. Sun, F.Y. Jin, R. Xia, R. Kong, J.H. Li, T.P. Xu, Y.W. Liu, E.B. Zhang, X.H. Liu, W. De, BMC Cancer 14, 319 (2014). doi: 10.1186/1471-2407-14-319

D. Shi, H. Zheng, C. Zhuo, J. Peng, D. Li, Y. Xu, X. Li, G. Cai, S. Cai, Med. Oncol. 31, 31 (2014). doi: 10.1007/s12032-014-0031-7

G. Petrovics, W. Zhang, M. Makarem, J.P. Street, R. Connelly, L. Sun, I.A. Sesterhenn, V. Srikantan, J.W. Moul, S. Srivastava, Oncogene 23, 605–611 (2004). doi: 10.1038/sj.onc.1207069

S. Chung, H. Nakagawa, M. Uemura, L. Piao, K. Ashikawa, N. Hosono, R. Takata, S. Akamatsu, T. Kawaguchi, T. Morizono, T. Tsunoda, Y. Daigo, K. Matsuda, N. Kamatani, Y. Nakamura, M. Kubo, Cancer Sci. 102, 245–252 (2011). doi: 10.1111/j.1349-7006.2010.01737.x

L. Poliseno, Sci. Signal. 5, re5 (2012). doi: 10.1126/scisignal.2002858

J.E. Karro, Y. Yan, D. Zheng, Z. Zhang, N. Carriero, P. Cayting, P. Harrrison, M. Gerstein, Nucleic Acids Res. 35, D55–D60 (2007). doi: 10.1093/nar/gkl851

J. Zhu, J.Z. Sanborn, M. Diekhans, C.B. Lowe, T.H. Pringle, D. Haussler, PLoS Comput. Biol. 3, e247 (2007). doi: 10.1371/journal.pcbi.0030247

C. Esnault, J. Maestre, T. Heidmann, Nat. Genet. 24, 363–367 (2000). doi: 10.1038/74184

N. Proudfoot, Nature 286, 840–841 (1980)

Z. Zhang, P.M. Harrison, Y. Liu, M. Gerstein, Genome Res. 13, 2541–2558 (2003). doi: 10.1101/gr.1429003

C. Ganster, A. Wernstedt, H. Kehrer-Sawatzki, L. Messiaen, K. Schmidt, N. Rahner, K. Heinimann, C. Fonatsch, J. Zschocke, K. Wimmer, Hum. Mutat. 31, 552–560 (2010). doi: 10.1002/humu.21223

J. Wang, M. Pitarque, M. Ingelman-Sundberg, Biochem. Biophys. Res. Commun. 340, 491–497 (2006). doi: 10.1016/j.bbrc.2005.12.035

N. Puget, S. Gad, L. Perrin-Vidoz, O.M. Sinilnikova, D. Stoppa-Lyonnet, G.M. Lenoir, S. Mazoyer, Am. J. Hum. Genet. 70, 858–865 (2002). doi: 10.1086/339434

B.S. Zhou, D.R. Beidler, Y.C. Cheng, Cancer Res. 52, 4280–4285 (1992)

S.A. Korneev, J.H. Park, M. O’Shea, J Neurosci Off J Soc Neurosci 19, 7711–7720 (1999)

O.H. Tam, A.A. Aravin, P. Stein, A. Girard, E.P. Murchison, S. Cheloufi, E. Hodges, M. Anger, R. Sachidanandam, R.M. Schultz, G.J. Hannon, Nature 453, 534–538 (2008). doi: 10.1038/nature06904

T. Watanabe, Y. Totoki, A. Toyoda, M. Kaneda, S. Kuramochi-Miyagawa, Y. Obata, H. Chiba, Y. Kohara, T. Kono, T. Nakano, M.A. Surani, Y. Sakaki, H. Sasaki, Nature 453, 539–543 (2008). doi: 10.1038/nature06908

X. Guo, Z. Zhang, M.B. Gerstein, D. Zheng, PLoS Comput. Biol. 5, e1000449 (2009). doi: 10.1371/journal.pcbi.1000449

M. Kandouz, A. Bier, G.D. Carystinos, M.A. Alaoui-Jamali, G. Batist, Oncogene 23, 4763–4770 (2004). doi: 10.1038/sj.onc.1207506

L. Poliseno, L. Salmena, J. Zhang, B. Carver, W.J. Haveman, P.P. Pandolfi, Nature 465, 1033–1038 (2010). doi: 10.1038/nature09144

A.C. Marques, J. Tan, S. Lee, L. Kong, A. Heger, C.P. Ponting, Genome Biol. 13, R102 (2012). doi: 10.1186/gb-2012-13-11-r102

P. Sumazin, X. Yang, H.S. Chiu, W.J. Chung, A. Iyer, D. Llobet-Navas, P. Rajbhandari, M. Bansal, P. Guarnieri, J. Silva, A. Califano, Cell 147, 370–381 (2011). doi: 10.1016/j.cell.2011.09.041

E. Betran, W. Wang, L. Jin, M. Long, Mol. Biol. Evol. 19, 654–663 (2002)

M. Katoh, M. Katoh, Int. J. Oncol. 23, 525–531 (2003)

S. Kalyana-Sundaram, C. Kumar-Sinha, S. Shankar, D.R. Robinson, Y.M. Wu, X. Cao, I.A. Asangani, V. Kothari, J.R. Prensner, R.J. Lonigro, M.K. Iyer, T. Barrette, A. Shanmugam, S.M. Dhanasekaran, N. Palanisamy, A.M. Chinnaiyan, Cell 149, 1622–1634 (2012). doi: 10.1016/j.cell.2012.04.041

S.L. Hwang, J.H. Chang, C.Y. Cheng, S.L. Howng, W.D. Sy, A.S. Lieu, C.L. Lin, K.S. Lee, Y.R. Hong, European surgical research. Europaische chirurgische Forschung. Recherches chirurgicales europeennes 37, 100–104 (2005). doi: 10.1159/000084540

M.A. Rieger, R. Ebner, D.R. Bell, A. Kiessling, J. Rohayem, M. Schmitz, A. Temme, E.P. Rieber, B. Weigle, Cancer Res. 64, 2357–2364 (2004)

J.M. Bischof, A.P. Chiang, T.E. Scheetz, E.M. Stone, T.L. Casavant, V.C. Sheffield, T.A. Braun, Hum. Mutat. 27, 545–552 (2006). doi: 10.1002/humu.20335

M. Cesana, D. Cacchiarelli, I. Legnini, T. Santini, O. Sthandier, M. Chinappi, A. Tramontano, I. Bozzoni, Cell 147, 358–369 (2011). doi: 10.1016/j.cell.2011.09.028

Y.J. Han, S.F. Ma, G. Yourek, Y.D. Park, J.G. Garcia, FASEB J Off Publ Fed Am Soc Exp Biol 25, 2305–2312 (2011). doi: 10.1096/fj.10-177808

F.A. Karreth, Y. Tay, D. Perna, U. Ala, S.M. Tan, A.G. Rust, G. DeNicola, K.A. Webster, D. Weiss, P.A. Perez-Mancera, M. Krauthammer, R. Halaban, P. Provero, D.J. Adams, D.A. Tuveson, P.P. Pandolfi, Cell 147, 382–395 (2011). doi: 10.1016/j.cell.2011.09.032

Y. Tay, L. Kats, L. Salmena, D. Weiss, S.M. Tan, U. Ala, F. Karreth, L. Poliseno, P. Provero, F. Di Cunto, J. Lieberman, I. Rigoutsos, P.P. Pandolfi, Cell 147, 344–357 (2011). doi: 10.1016/j.cell.2011.09.029

L. Wang, Z.Y. Guo, R. Zhang, B. Xin, R. Chen, J. Zhao, T. Wang, W.H. Wen, L.T. Jia, L.B. Yao, A.G. Yang, Carcinogenesis 34, 1773–1781 (2013). doi: 10.1093/carcin/bgt139

Z.J. Rutnam, W.W. Du, W. Yang, X. Yang, B.B. Yang, Nat. Commun. 5, 2914 (2014). doi: 10.1038/ncomms3914

E. Chiefari, S. Iiritano, F. Paonessa, I. Le Pera, B. Arcidiacono, M. Filocamo, D. Foti, S.A. Liebhaber, A. Brunetti, Nat. Commun. 1, 40 (2010). doi: 10.1038/ncomms1040

K. Takahashi, K. Mitsui, S. Yamanaka, Nature 423, 541–545 (2003). doi: 10.1038/nature01646

M. Zou, E.Y. Baitei, A.S. Alzahrani, F. Al-Mohanna, N.R. Farid, B. Meyer, Y. Shi, Neoplasia 11, 57–65 (2009)

H. Hayashi, T. Arao, Y. Togashi, H. Kato, Y. Fujita, M.A. De Velasco, H. Kimura, K. Matsumoto, K. Tanaka, I. Okamoto, A. Ito, Y. Yamada, K. Nakagawa, K. Nishio, Oncogene (2013). doi: 10.1038/onc.2013.547

J.M. Nigro, K.R. Cho, E.R. Fearon, S.E. Kern, J.M. Ruppert, J.D. Oliner, K.W. Kinzler, B. Vogelstein, Cell 64, 607–613 (1991)

B. Capel, A. Swain, S. Nicolis, A. Hacker, M. Walter, P. Koopman, P. Goodfellow, R. Lovell-Badge, Cell 73, 1019–1030 (1993)

S. Memczak, M. Jens, A. Elefsinioti, F. Torti, J. Krueger, A. Rybak, L. Maier, S.D. Mackowiak, L.H. Gregersen, M. Munschauer, A. Loewer, U. Ziebold, M. Landthaler, C. Kocks, F. le Noble, N. Rajewsky, Nature 495, 333–338 (2013). doi: 10.1038/nature11928

W.R. Jeck, N.E. Sharpless, Nat. Biotechnol. 32, 453–461 (2014). doi: 10.1038/nbt.2890

J.H. Li, S. Liu, H. Zhou, L.H. Qu, J.H. Yang, Nucleic Acids Res. 42, D92–D97 (2014). doi: 10.1093/nar/gkt1248

J.H. Yang, J.H. Li, P. Shao, H. Zhou, Y.Q. Chen, L.H. Qu, Nucleic Acids Res. 39, D202–D209 (2011). doi: 10.1093/nar/gkq1056

S. Ghosal, S. Das, R. Sen, P. Basak, J. Chakrabarti, Front. Genet. 4, 283 (2013). doi: 10.3389/fgene.2013.00283

J. Salzman, C. Gawad, P.L. Wang, N. Lacayo, P.O. Brown, PLoS One 7, e30733 (2012). doi: 10.1371/journal.pone.0030733

P.L. Wang, Y. Bao, M.C. Yee, S.P. Barrett, G.J. Hogan, M.N. Olsen, J.R. Dinneny, P.O. Brown, J. Salzman, PLoS One 9, e90859 (2014). doi: 10.1371/journal.pone.0090859

L.F. Thomas, P. Saetrom, Bioinformatics (2014). doi: 10.1093/bioinformatics/btu257

J. Salzman, R.E. Chen, M.N. Olsen, P.L. Wang, P.O. Brown, PLoS Genet. 9, e1003777 (2013). doi: 10.1371/journal.pgen.1003777

C. Cocquerelle, B. Mascrez, D. Hetuin, B. Bailleul, FASEB J Off Publ Fed Am Soc Exp Biol 7, 155–160 (1993)

C.E. Burd, W.R. Jeck, Y. Liu, H.K. Sanoff, Z. Wang, N.E. Sharpless, PLoS Genet. 6, e1001233 (2010). doi: 10.1371/journal.pgen.1001233

T.B. Hansen, T.I. Jensen, B.H. Clausen, J.B. Bramsen, B. Finsen, C.K. Damgaard, J. Kjems, Nature 495, 384–388 (2013). doi: 10.1038/nature11993

F.C. Tay, J.K. Lim, H. Zhu, L.C. Hin, S. Wang, Adv. Drug Deliv. Rev. (2014). doi: 10.1016/j.addr.2014.05.010

M.S. Ebert, J.R. Neilson, P.A. Sharp, Nat. Methods 4, 721–726 (2007). doi: 10.1038/nmeth1079

R.A. Dubin, M.A. Kazmi, H. Ostrer, Gene 167, 245–248 (1995)

T.B. Hansen, J. Kjems, C.K. Damgaard, Cancer Res. 73, 5609–5612 (2013). doi: 10.1158/0008-5472.CAN-13-1568

V. Scaiewicz, V. Sorin, Y. Fellig, T. Birman, A. Mizrahi, J. Galula, R. Abu-Lail, T. Shneider, P. Ohana, L. Buscail, A. Hochberg, A. Czerniak, J Oncol 2010, 178174 (2010). doi: 10.1155/2010/178174

M. Mourtada-Maarabouni, M.R. Pickard, V.L. Hedge, F. Farzaneh, G.T. Williams, Oncogene 28, 195–208 (2009). doi: 10.1038/onc.2008.373

T. Gutschner, M. Baas, S. Diederichs, Genome Res. 21, 1944–1954 (2011). doi: 10.1101/gr.122358.111

J.C. Miller, M.C. Holmes, J. Wang, D.Y. Guschin, Y.L. Lee, I. Rupniewski, C.M. Beausejour, A.J. Waite, N.S. Wang, K.A. Kim, P.D. Gregory, C.O. Pabo, E.J. Rebar, Nat. Biotechnol. 25, 778–785 (2007). doi: 10.1038/nbt1319

T.C. Pereira, I. Lopes-Cendes, Cent. Nerv. Syst. Agents Med. Chem. 12, 217–232 (2012)

E. Zorde Khvalevsky, R. Gabai, I.H. Rachmut, E. Horwitz, Z. Brunschwig, A. Orbach, A. Shemi, T. Golan, A.J. Domb, E. Yavin, H. Giladi, L. Rivkin, A. Simerzin, R. Eliakim, A. Khalaileh, A. Hubert, M. Lahav, Y. Kopelman, E. Goldin, A. Dancour, Y. Hants, S. Arbel-Alon, R. Abramovitch, A. Shemi, E. Galun, Proc. Natl. Acad. Sci. U. S. A. 110, 20723–20728 (2013). doi: 10.1073/pnas.1314307110

S.T. Crooke, Antisense Drug Technology : Principles, Strategies, and Applications (Marcel Dekker, New York, 2001)

C.M. Feldherr, D. Akin, J. Cell Biol. 111, 1–8 (1990)

N.R. Jones, M.A. Pegues, M.A. McCrory, W. Singleton, C. Bethune, B.F. Baker, D.A. Norris, R.M. Crooke, M.J. Graham, A.J. Szalai, Molecular therapy. Nucleic Acids 1, e52 (2012). doi: 10.1038/mtna.2012.44

M. Robbins, A. Judge, I. MacLachlan, Oligonucleotides 19, 89–102 (2009). doi: 10.1089/oli.2009.0180

R.G. Lee, J. Crosby, B.F. Baker, M.J. Graham, R.M. Crooke, J. Cardiovasc. Transl. Res. 6, 969–980 (2013). doi: 10.1007/s12265-013-9495-7

F. Jaschinski, T. Rothhammer, P. Jachimczak, C. Seitz, A. Schneider, K.H. Schlingensiepen, Curr. Pharm. Biotechnol. 12, 2203–2213 (2011)

V. Tripathi, Z. Shen, A. Chakraborty, S. Giri, S.M. Freier, X. Wu, Y. Zhang, M. Gorospe, S.G. Prasanth, A. Lal, K.V. Prasanth, PLoS Genet. 9, e1003368 (2013). doi: 10.1371/journal.pgen.1003368

C. Sheridan, Nat. Biotechnol. 30, 471–473 (2012). doi: 10.1038/nbt0612-471

O.C. Uhlenbeck, Nature 328, 596–600 (1987). doi: 10.1038/328596a0

L. Beigelman, J.A. McSwiggen, K.G. Draper, C. Gonzalez, K. Jensen, A.M. Karpeisky, A.S. Modak, J. Matulic-Adamic, A.B. DiRenzo, P. Haeberli et al., J Biol Chem 270, 25702–25708 (1995)

P.A. Pavco, K.S. Bouhana, A.M. Gallegos, A. Agrawal, K.S. Blanchard, S.L. Grimm, K.L. Jensen, L.E. Andrews, F.E. Wincott, P.A. Pitot, R.J. Tressler, C. Cushman, M.A. Reynolds, T.J. Parry, Clin Cancer Res Off J Am Assoc Cancer Res 6, 2094–2103 (2000)

F. Darfeuille, S. Reigadas, J.B. Hansen, H. Orum, C. Di Primo, J.J. Toulme, Biochemistry 45, 12076–12082 (2006). doi: 10.1021/bi0606344

A.D. Ellington, J.W. Szostak, Nature 346, 818–822 (1990). doi: 10.1038/346818a0

C. Tuerk, L. Gold, Science 249, 505–510 (1990)

E.W. Ng, A.P. Adamis, Ann. N. Y. Acad. Sci. 1082, 151–171 (2006). doi: 10.1196/annals.1348.062

P. Sundaram, H. Kurniawan, M.E. Byrne, J. Wower, Eur J Pharm Sci Off J Eur Fed Pharm Sci 48, 259–271 (2013). doi: 10.1016/j.ejps.2012.10.014

M.E. Davis, Mol. Pharm. 6, 659–668 (2009). doi: 10.1021/mp900015y

D. Schaffert, E. Wagner, Gene Ther. 15, 1131–1138 (2008). doi: 10.1038/gt.2008.105

Y.C. Tseng, S. Mozumdar, L. Huang, Adv. Drug Deliv. Rev. 61, 721–731 (2009). doi: 10.1016/j.addr.2009.03.003

M.R. Diaz, P.E. Vivas-Mejia, Pharmaceuticals 6, 1361–1380 (2013). doi: 10.3390/ph6111361

T. Arima, T. Matsuda, N. Takagi, N. Wake, Cancer Genet. Cytogenet. 93, 39–47 (1997)

I. Ariel, S. Ayesh, E.J. Perlman, G. Pizov, V. Tanos, T. Schneider, V.A. Erdmann, D. Podeh, D. Komitowski, A.S. Quasem, N. de Groot, A. Hochberg, Mol Pathol 50, 34–44 (1997)

I. Ariel, N. de Groot, A. Hochberg, Am. J. Med. Genet. 91, 46–50 (2000)

M.C. Smaldone, B.J. Davies, Curr. Opin. Mol. Ther. 12, 607–616 (2010)

P. Ohana, P. Schachter, B. Ayesh, A. Mizrahi, T. Birman, T. Schneider, I. Matouk, S. Ayesh, P.J. Kuppen, N. de Groot, A. Czerniak, A. Hochberg, J Gene Med 7, 366–374 (2005). doi: 10.1002/jgm.670

A. Mizrahi, A. Czerniak, T. Levy, S. Amiur, J. Gallula, I. Matouk, R. Abu-lail, V. Sorin, T. Birman, N. de Groot, A. Hochberg, P. Ohana, J. Transl. Med. 7, 69 (2009). doi: 10.1186/1479-5876-7-69

V. Sorin, P. Ohana, A. Mizrahi, I. Matouk, T. Birman, A. Hochberg, A. Czerniak, Int. J. Oncol. 39, 1407–1412 (2011). doi: 10.3892/ijo.2011.1171