Structure of noncoding RNA is a determinant of function of RNA binding proteins in transcriptional regulation

Fire A, Xu S, Montgomery MK, Kostac SA, Driver SE, Mello CC: Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998, 391: 806-811. 10.1038/35888 Filipowicz W, Bhattacharyya SN, Sonenberg N: Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?. Nat Rev Genet. 2008, 9: 102-114. Brownlee GG: Sequence of 6S RNA of E. coli. Nat New Biol. 1971, 229: 147-149. Wassarman KM, Storz G: 6S RNA regulates E. coli RNA polymerase activity. Cell. 2000, 101: 613-623. 10.1016/S0092-8674(00)80873-9 Gruber TM, Gross CA: Multiple σ subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol. 2003, 57: 441-466. 10.1146/annurev.micro.57.030502.090913 Gildehaus N, Neusser T, Wurm R, Wagner R: Studies on the function of the riboregulator 6S RNA from E. coli: RNA polymerase binding, inhibition of in vitro transcription and synthesis of RNA-directed de novo transcripts. Nucleic Acids Res. 2007, 35: 1885-1896. 10.1093/nar/gkm085 Barrick JE, Sudarsan N, Weinberg Z, Ruzzo WL, Breaker RR: 6S RNA is a widespread regulator of eubacterial RNA polymerase that resembles an open promoter. RNA. 2005, 11: 774-784. 10.1261/rna.7286705 Trotochaud AE, Wassarman KM: A highly conserved 6S RNA structure is required for regulation of transcription. Nat Struct Mol Biol. 2005, 12: 313-319. 10.1038/nsmb917 Trotochaud AE, Wassarman KM: 6S RNA function enhances long-term cell survival. J Bacteriol. 2004, 186: 4978-4985. 10.1128/JB.186.15.4978-4985.2004 Wassarman KM, Saecker RM: Synthesis-mediated release of a small RNA inhibitor of RNA polymerase. Science. 2006, 314: 1601-1603. 10.1126/science.1134830 Aleman C, Roy-Engel AM, Shaikh TH, Deininger PL: Cis-acting influences on Alu RNA levels. Nucleic Acids Res. 2000, 28: 4755-4761. 10.1093/nar/28.23.4755 Jang KL, Latchman DS: The herpes simplex virus immediate-early protein ICP27 stimulates the transcription of cellular Alu repeated sequences by increasing the activity of transcription factor TFIIIC. Biochem J. 1992, 284: 667-673. Fornace AJ Jr, Alamo I Jr, Hollander MC, Lamoreaux E: Induction of heat shock protein transcripts and B2 transcripts by various stresses in Chinese hamster cells. Exp Cell Res. 1989, 182: 61-74. 10.1016/0014-4827(89)90279-6 Allen TA, Von Kaenel S, Goodrich JA, Kugel JF: The SINE-encoded mouse B2 RNA represses mRNA transcription in response to heat shock. Nat Struct Mol Biol. 2004, 11: 816-821. 10.1038/nsmb813 Liu WM, Chu WM, Choudary PV, Schmid CW: Cell stress and translational inhibitors transiently increase the abundance of mammalian SINE transcripts. Nucleic Acids Res. 1995, 23: 1758-1765. 10.1093/nar/23.10.1758 Fornace AJ Jr, Mitchell JB: Induction of B2 RNA polymerase III transcription by heat shock: enrichment for heat shock induced sequences in rodent cells by hybridization subtraction. Nucleic Acids Res. 1986, 14: 5793-5811. 10.1093/nar/14.14.5793 Li T, Spearow J, Rubin CM, Schmid CW: Physiological stresses increase mouse short interspersed element (SINE) RNA expression in vivo. Gene. 1999, 239: 367-372. 10.1016/S0378-1119(99)00384-4 Price BD, Calderwood SK: Heat-induced transcription from RNA polymerases II and III and HSF binding activity are co-ordinately regulated by the products of the heat shock genes. J Cell Physiol. 1992, 153: 392-401. 10.1002/jcp.1041530219 White RJ, Stott D, Rigby PW: Regulation of RNA polymerase III transcription in response to Simian virus 40 transformation. EMBO J. 1990, 9: 3713-3721. Rudin CM, Thompson CB: Transcriptional activation of short interspersed elements by DNA-damaging agents. Genes Chromosomes Cancer. 2001, 30: 64-71. 10.1002/1098-2264(2000)9999:9999<::AID-GCC1066>3.0.CO;2-F Espinoza CA, Allen TA, Hieb AR, Kugel JF, Goodrich JA: B2 RNA binds directly to RNA polymerase II to repress transcript synthesis. Nat Struct Mol Biol. 2004, 11: 822-829. 10.1038/nsmb812 Kramerov DA, Vassetzky NS: Short retroposons in eukaryotic genomes. Int Rev Cytol. 2005, 247: 165-221. Espinoza CA, Goodrich JA, Kugel JF: Characterization of the structure, function, and mechanism of B2 RNA, and ncRNA repressor of RNA polymerase II transcription. RNA. 2007, 13: 583-596. 10.1261/rna.310307 Wang X, Arai S, Song X, Reichart D, Du K, Pascual G, Tempst P, Rosenfeld MG, Glass CK, Kurokawa R: Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature. 2008, 454: 126-130. 10.1038/nature06992 Crozat A, Aman P, Mandahl N, Ron D: Fusion of CHOP to a novel RNA-binding protein in human myxoid liposarcoma. Nature. 1993, 363: 640-644. 10.1038/363640a0 Zinszner H, Sok J, Immanuel D, Yin Y, Ron D: TLS (FUS) binds RNA in vivo and engages in nucleo-cytoplasmic shuttling. J Cell Sci. 1997, 110: 1741-1750. Uranishi H, Tetsuka T, Yamashita M, Asamitsu K, Shimizu M, Itoh M, Okamoto T: Involvement of the pro-oncoprotein TLS (translocated in liposarcoma) in nuclear factor-kappaB p65-mediated transcription as a coactivator. J Biol Chem. 2001, 276: 13395-133401. 10.1074/jbc.M011176200 Ron D: TLS-CHOP and the role of RNA-binding proteins in oncogenic transformation. Curr Top Microbiol Immunol. 1997, 220: 131-142. 10.1007/978-3-642-60479-9_8 Bertrand P, Akhmedov AT, Delacote F, Durrbach A, Lopez BS: Human POMp75 is identified as the pro-oncoprotein TLS/FUS: both POMp75 and POMp75 and POMp100 DNA homologous pairing activities are associated to cell proliferation. Oncogene. 1999, 18: 4515-4521. 10.1038/sj.onc.1203048 Chrivia JC, Kwok RP, Lamb N, Hagiwara M, Montminy MR, Goodman RH: Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature. 1993, 365: 855-859. 10.1038/365855a0 Kurokawa R, Kalafus D, Ogliastro MH, Kioussi C, Xu L, Torchia J, Rosenfeld MG, Glass CK: Differential use of CREB binding protein-coactivator complexes. Science. 1998, 279: 700-703. 10.1126/science.279.5351.700 Ogryzko VV, Schiltz RL, Russanova V, Howard BH, Nakanani Y: The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell. 1996, 87: 953-959. 10.1016/S0092-8674(00)82001-2 Bannister AJ, Kouzarides T: The CBP co-activator is a histone acetyltransferase. Nature. 1996, 384: 641-643. 10.1038/384641a0 Lerga A, Hallier M, Delva L, Orvain C, Gallais I, Marie J, Moreau-Gachelin F: Identification of an RNA Binding Specificity for the Potential Splicing Factor TLS. J Biol Chem. 2001, 276: 6807-6816. 10.1074/jbc.M008304200 Xu Y, Kaminaga K, Komiyama M: G-quadruplex formation by human telomeric repeats-containing RNA in Na+ solution. J Am Chem Soc. 2008, 130: 11179-11184. 10.1021/ja8031532 Martadinata H, Phan AT: Structure of propeller-type parallel-stranded RNA G-quadruplexes, formed by human telomeric RNA sequences in K+ solution. J Am Chem Soc. 2009, 131: 2570-2578. 10.1021/ja806592z Xu Y, Suzuki Y, Ito K, Komiyama M: Telomeric repeat-containing RNA structure in living cells. Proc Natl Acad Sci USA. 2010, 107: 14579-14584. 10.1073/pnas.1001177107 Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J: Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science. 2007, 318: 798-801. 10.1126/science.1147182 Schoeftner S, Blasco MA: Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat Cell Biol. 2008, 10: 228-236. 10.1038/ncb1685 Redon S, Reichenbach P, Lingner J: The non-coding RNA TERRA is a natural ligand and direct inhibitor of human telomerase. Nucleic Acids Res. 2010, 38: 5797-5806. 10.1093/nar/gkq296 Deng Z, Norseen J, Wiedmer A, Riethman H, Lieberman PM: TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol Cell. 2009, 35: 403-413. 10.1016/j.molcel.2009.06.025 Takahama K, Kino K, Arai S, Kurokawa R, Oyoshi T: Identification of RNA binding specificity for the TET-family proteins. Nucleic Acids Symp Ser. 2008, 52: 213-214. 10.1093/nass/nrn108 Dejardin J, Kingston RE: Purification of proteins associated with specific genomic loci. Cell. 2009, 136: 175-186. 10.1016/j.cell.2008.11.045 LaBranch H, Dupuis S, Ben-David Y, Bani MR, Wellinger RJ, Chabot B: Telomere elongation by hnRNP A1 and a derivative that interacts with telomeric repeats and telomerase. Nat Genet. 1998, 19: 199-202. 10.1038/575 Lopez de Silanes I, Stagno d'Alcontres M, Blasco MA: TERRA transcripts are bound by a complex array of RNA-binding proteins. Nat Commun. 2010, 1: 33. Flynn RL, Centore RC, O'Sullivan RJ, Rai R, Tse A, Songyang Z, Chang S, Karlseder J, Zou L: TERRA and hnRNPA1 orchestrate an RPA-to POT1 switch on telomeric single-stranded DNA. Nautre. 2011, 471: 532-536. May WA, Denny CT: Biology of EWS/FLI and related fusion genes in Ewing's sarcoma and primitive neuroectodermal tumor. Curr Top Microbiol Immunol. 1997, 220: 143-150. 10.1007/978-3-642-60479-9_9 Rauscher FJ III: Chromosome translocation-mediated conversion of a tumor suppressor gene into a dominant oncogene: fusion of EWS1 to WT1 in desmoplastic small round cell tumors. Curr Top Microbiol Immunol. 1997, 220: 151-162. 10.1007/978-3-642-60479-9_10 Brown AD, Lopez-Terrada D, Denny C, Lee KA: Promoters containing ATF-binding sites are de-regulated in cells that express the EWS/ATF1 ontogeny. Oncogene. 1995, 10: 1749-1756. Fujimura Y, Ohno T, Siddique H, Lee L, Rao VN, Reddy ES: The EWS-ATF-1 gene involved in malignant melanoma of soft parts with t(12;22) chromosome translocation, encodes a constitutive transcriptional activator. Oncogene. 1996, 12: 159-167. May WA, Lessnick SL, Braun BS, Klemsz M, Lewis BC, Lunsford LB, Hromas R, Denny CT: The Ewing's sarcoma EWS/FLI-1 fusion gene encodes a more potent transcriptional activator and is a more powerful transforming gene than FLI-1. Mol Cell Biol. 1993, 13: 7393-7398. Ohno T, Rao VN, Reddy ES: EWS/Fli-1 chimeric protein is a transcriptional activator. Cancer Res. 1993, 53: 5859-5863. Ohno T, Ouchida M, Lee L, Gatalica Z, Rao VN, Reddy ES: The EWS gene, involved in Ewing family of tumors, malignant melanoma of soft parts and desmoplastic small round cell tumors, codes for an RNA binding protein with novel regulatory domains. Oncogene. 1994, 9: 3087-3097. Sanchez-Garcia I, Rabbitts TH: Transcriptional activation by TAL1 and FUS-CHOP proteins in aute malignancies as a result of chromosomal abnormalities. Proc Natl Acad Sci USA. 1994, 91: 7869-7873. 10.1073/pnas.91.17.7869 Pan S, Ming KY, Dunn TA, Li KK, Lee KA: The EWS/ATF1 fusion protein contains a dispersed activation domain that functions directly. Oncogene. 1998, 16: 1625-1631. 10.1038/sj.onc.1201671 Petermann R, Mossier BM, Aryee DN, Khazak V, Golemis EA, Kover H: Oncogenic EWS-Fli1 interacts with hsRPB7, a subunit of human RNA polymerase II. Oncogene. 1998, 17: 603-610. 10.1038/sj.onc.1201964 Delattre O, Zucman J, Plougastel B, Desmaze C, Melot T, Peter M, Kovar H, Joubert I, de Jong P, Rouleau G, Aurias A, Thomas G: Gene fusion with an ETS DNA-binding caused by chromosome translocation in human tumours. Nature. 1992, 359: 162-165. 10.1038/359162a0 Li KK, Lee KA: Transcription activation by the Ewing's Sarcoma (EWS) oncogene can be cis-repression by the EWS RNA-binding domain. J Biol Chem. 2000, 275: 23053-23058. 10.1074/jbc.M002961200 Alex D, Lee KA: RGG-boxes of the EWS oncoprotein repress a range of transcriptional activation domains. Nucleic Acids Res. 2005, 33: 1323-1331. 10.1093/nar/gki270 Takahama K, Kino K, Arai S, Kurokawa R, Oyoshi T: Identification of Ewing's sarcoma protein as a G-quadruplex DNA-and RNA-binding protein. FEBS J. 2011, 278: 988-998. 10.1111/j.1742-4658.2011.08020.x Takahama K, Sugimoto C, Arai S, Kurokawa R, Oyoshi T: Loop lengths of G-quadruplex structures affect the G-quadruplex DNA binding selectivity of the RGG motif in Ewing's Sarcoma. Biochemistry. 2011, 50: 5369-5378. 10.1021/bi2003857 Araya N, Hiraga H, Kako K, Arao Y, Kato S, Fukamizu A: Transcriptional down-regulation through nuclear exclusion of EWS methylated by PRMT1. Biochem Biophys Res Commun. 2005, 329: 653-660. 10.1016/j.bbrc.2005.02.018 Burd CG, Dreyfuss G: Conserved structures and diversity of functions of RNA-binding proteins. Science. 1994, 265: 615-621. 10.1126/science.8036511 Law WJ, Cann KL, Hicks GG: TLS, EWS and TAF15: a model for transcriptional integration of gene expression. Brief Funct Genomic Proteomic. 2006, 5: 8-14. 10.1093/bfgp/ell015 Rossow KL, Janknecht R: The Ewing's sarcoma gene product functions as a transcriptional activator. Cancer Res. 2001, 61: 2690-2695.