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Long Noncoding RNAs as Targets and Regulators of Nuclear Receptors

  • Charles E. Foulds
  • Anil K. Panigrahi
  • Cristian Coarfa
  • Rainer B. Lanz
  • Bert W. O’MalleyEmail author
Chapter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 394)

Abstract

Intensive research has been directed at the discovery, biogenesis, and expression patterns of long noncoding RNAs , yet their biochemical functions have remained elusive for the most part. Nuclear receptors that interpret signaling mediated by small molecule hormones play a role in regulating the expression of some long noncoding RNAs. More importantly, these RNAs have also been shown to effect hormone-affected gene transcription regulated by the nuclear receptors. In this chapter, we summarize the current knowledge that has been acquired on hormonal signaling inducing expression of long noncoding RNAs and how they then may act in trans or in cis to modulate gene transcription. We highlight a few of these noncoding RNA molecules in terms of how they may impact hormone-driven cancers. Future directions critical for moving this field forward are presented, with a clear emphasis on the need for better biochemical approaches to address the mechanism of action of these exciting RNAs.

Keywords

Androgen Receptor Progesterone Receptor Glucocorticoid Receptor LNCaP Cell Mineralocorticoid Receptor 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Adriaenssens E, Lottin S, Dugimont T, Fauquette W, Coll J, Dupouy JP, Boilly B, Curgy JJ (1999) Steroid hormones modulate H19 gene expression in both mammary gland and uterus. Oncogene 18(31):4460–4473. doi: 10.1038/sj.onc.1202819 PubMedCrossRefGoogle Scholar
  2. Agoulnik IU, Weigel NL (2009) Coactivator selective regulation of androgen receptor activity. Steroids 74(8):669–674. doi: 10.1016/j.steroids.2009.02.007 PubMedPubMedCentralCrossRefGoogle Scholar
  3. Amaral PP, Dinger ME, Mercer TR, Mattick JS (2008) The eukaryotic genome as an RNA machine. Science 319(5871):1787–1789. doi: 10.1126/science.1155472 PubMedCrossRefGoogle Scholar
  4. Andersson R, Gebhard C, Miguel-Escalada I, Hoof I, Bornholdt J, Boyd M, Chen Y, Zhao X, Schmidl C, Suzuki T, Ntini E, Arner E, Valen E, Li K, Schwarzfischer L, Glatz D, Raithel J, Lilje B, Rapin N, Bagger FO, Jorgensen M, Andersen PR, Bertin N, Rackham O, Burroughs AM, Baillie JK, Ishizu Y, Shimizu Y, Furuhata E, Maeda S, Negishi Y, Mungall CJ, Meehan TF, Lassmann T, Itoh M, Kawaji H, Kondo N, Kawai J, Lennartsson A, Daub CO, Heutink P, Hume DA, Jensen TH, Suzuki H, Hayashizaki Y, Muller F, Forrest AR, Carninci P, Rehli M, Sandelin A (2014) An atlas of active enhancers across human cell types and tissues. Nature 507(7493):455–461. doi: 10.1038/nature12787 PubMedCrossRefGoogle Scholar
  5. Arieti F, Gabus C, Tambalo M, Huet T, Round A, Thore S (2014) The crystal structure of the Split End protein SHARP adds a new layer of complexity to proteins containing RNA recognition motifs. Nucleic Acids Res 42(10):6742–6752. doi: 10.1093/nar/gku277 PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136(2):215–233. doi: 10.1016/j.cell.2009.01.002 PubMedPubMedCentralCrossRefGoogle Scholar
  7. Batista PJ, Molinie B, Wang J, Qu K, Zhang J, Li L, Bouley DM, Lujan E, Haddad B, Daneshvar K, Carter AC, Flynn RA, Zhou C, Lim KS, Dedon P, Wernig M, Mullen AC, Xing Y, Giallourakis CC, Chang HY (2014) m(6)A RNA Modification Controls Cell Fate Transition in Mammalian Embryonic Stem Cells. Cell Stem Cell 15(6):707–719. doi: 10.1016/j.stem.2014.09.019 PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bejerano G, Pheasant M, Makunin I, Stephen S, Kent WJ, Mattick JS, Haussler D (2004) Ultraconserved elements in the human genome. Science 304(5675):1321–1325. doi: 10.1126/science.1098119 PubMedCrossRefGoogle Scholar
  9. Berteaux N, Lottin S, Adriaenssens E, Van Coppenolle F, Leroy X, Coll J, Dugimont T, Curgy JJ (2004) Hormonal regulation of H19 gene expression in prostate epithelial cells. J Endocrinol 183(1):69–78. doi: 10.1677/joe.1.05696 PubMedCrossRefGoogle Scholar
  10. Bhan A, Hussain I, Ansari KI, Kasiri S, Bashyal A, Mandal SS (2013) Antisense transcript long noncoding RNA (lncRNA) HOTAIR is transcriptionally induced by estradiol. J Mol Biol 425(19):3707–3722. doi: 10.1016/j.jmb.2013.01.022 PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bhan A, Hussain I, Ansari KI, Bobzean SA, Perrotti LI, Mandal SS (2014) Bisphenol-A and diethylstilbestrol exposure induces the expression of breast cancer associated long noncoding RNA HOTAIR in vitro and in vivo. J Steroid Biochem Molecul Biol 141:160–170. doi: 10.1016/j.jsbmb.2014.02.002 CrossRefGoogle Scholar
  12. Bhartiya D, Pal K, Ghosh S, Kapoor S, Jalali S, Panwar B, Jain S, Sati S, Sengupta S, Sachidanandan C, Raghava GP, Sivasubbu S, Scaria V (2013) lncRNome: a comprehensive knowledgebase of human long noncoding RNAs. Database: J Biol Databases Curation, bat034. doi: 10.1093/database/bat034
  13. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, Thurman RE, Kuehn MS, Taylor CM, Neph S, Koch CM, Asthana S, Malhotra A, Adzhubei I, Greenbaum JA, Andrews RM, Flicek P, Boyle PJ, Cao H, Carter NP, Clelland GK, Davis S, Day N, Dhami P, Dillon SC, Dorschner MO, Fiegler H, Giresi PG, Goldy J, Hawrylycz M, Haydock A, Humbert R, James KD, Johnson BE, Johnson EM, Frum TT, Rosenzweig ER, Karnani N, Lee K, Lefebvre GC, Navas PA, Neri F, Parker SC, Sabo PJ, Sandstrom R, Shafer A, Vetrie D, Weaver M, Wilcox S, Yu M, Collins FS, Dekker J, Lieb JD, Tullius TD, Crawford GE, Sunyaev S, Noble WS, Dunham I, Denoeud F, Reymond A, Kapranov P, Rozowsky J, Zheng D, Castelo R, Frankish A, Harrow J, Ghosh S, Sandelin A, Hofacker IL, Baertsch R, Keefe D, Dike S, Cheng J, Hirsch HA, Sekinger EA, Lagarde J, Abril JF, Shahab A, Flamm C, Fried C, Hackermuller J, Hertel J, Lindemeyer M, Missal K, Tanzer A, Washietl S, Korbel J, Emanuelsson O, Pedersen JS, Holroyd N, Taylor R, Swarbreck D, Matthews N, Dickson MC, Thomas DJ, Weirauch MT, Gilbert J, Drenkow J, Bell I, Zhao X, Srinivasan KG, Sung WK, Ooi HS, Chiu KP, Foissac S, Alioto T, Brent M, Pachter L, Tress ML, Valencia A, Choo SW, Choo CY, Ucla C, Manzano C, Wyss C, Cheung E, Clark TG, Brown JB, Ganesh M, Patel S, Tammana H, Chrast J, Henrichsen CN, Kai C, Kawai J, Nagalakshmi U, Wu J, Lian Z, Lian J, Newburger P, Zhang X, Bickel P, Mattick JS, Carninci P, Hayashizaki Y, Weissman S, Hubbard T, Myers RM, Rogers J, Stadler PF, Lowe TM, Wei CL, Ruan Y, Struhl K, Gerstein M, Antonarakis SE, Fu Y, Green ED, Karaoz U, Siepel A, Taylor J, Liefer LA, Wetterstrand KA, Good PJ, Feingold EA, Guyer MS, Cooper GM, Asimenos G, Dewey CN, Hou M, Nikolaev S, Montoya-Burgos JI, Loytynoja A, Whelan S, Pardi F, Massingham T, Huang H, Zhang NR, Holmes I, Mullikin JC, Ureta-Vidal A, Paten B, Seringhaus M, Church D, Rosenbloom K, Kent WJ, Stone EA, Batzoglou S, Goldman N, Hardison RC, Haussler D, Miller W, Sidow A, Trinklein ND, Zhang ZD, Barrera L, Stuart R, King DC, Ameur A, Enroth S, Bieda MC, Kim J, Bhinge AA, Jiang N, Liu J, Yao F, Vega VB, Lee CW, Ng P, Yang A, Moqtaderi Z, Zhu Z, Xu X, Squazzo S, Oberley MJ, Inman D, Singer MA, Richmond TA, Munn KJ, Rada-Iglesias A, Wallerman O, Komorowski J, Fowler JC, Couttet P, Bruce AW, Dovey OM, Ellis PD, Langford CF, Nix DA, Euskirchen G, Hartman S, Urban AE, Kraus P, Van Calcar S, Heintzman N, Kim TH, Wang K, Qu C, Hon G, Luna R, Glass CK, Rosenfeld MG, Aldred SF, Cooper SJ, Halees A, Lin JM, Shulha HP, Xu M, Haidar JN, Yu Y, Iyer VR, Green RD, Wadelius C, Farnham PJ, Ren B, Harte RA, Hinrichs AS, Trumbower H, Clawson H, Hillman-Jackson J, Zweig AS, Smith K, Thakkapallayil A, Barber G, Kuhn RM, Karolchik D, Armengol L, Bird CP, de Bakker PI, Kern AD, Lopez-Bigas N, Martin JD, Stranger BE, Woodroffe A, Davydov E, Dimas A, Eyras E, Hallgrimsdottir IB, Huppert J, Zody MC, Abecasis GR, Estivill X, Bouffard GG, Guan X, Hansen NF, Idol JR, Maduro VV, Maskeri B, McDowell JC, Park M, Thomas PJ, Young AC, Blakesley RW, Muzny DM, Sodergren E, Wheeler DA, Worley KC, Jiang H, Weinstock GM, Gibbs RA, Graves T, Fulton R, Mardis ER, Wilson RK, Clamp M, Cuff J, Gnerre S, Jaffe DB, Chang JL, Lindblad-Toh K, Lander ES, Koriabine M, Nefedov M, Osoegawa K, Yoshinaga Y, Zhu B, de Jong PJ (2007) Identification and analysis of functional elements in 1 % of the human genome by the ENCODE pilot project. Nature 447(7146):799–816Google Scholar
  14. Bolton EM, Tuzova AV, Walsh AL, Lynch T, Perry AS (2014) Noncoding RNAs in prostate cancer: the long and the short of it. Clin Cancer Res: Off J Am Assoc Cancer Res 20(1):35–43. doi: 10.1158/1078-0432.CCR-13-1989
  15. Bonasio R, Shiekhattar R (2014) Regulation of Transcription by Long Noncoding RNAs. Annu Rev Genet 48:433–455. doi: 10.1146/annurev-genet-120213-092323 PubMedPubMedCentralCrossRefGoogle Scholar
  16. Brannan CI, Dees EC, Ingram RS, Tilghman SM (1990) The product of the H19 gene may function as an RNA. Mol Cell Biol 10(1):28–36PubMedPubMedCentralCrossRefGoogle Scholar
  17. Brown CJ, Lafreniere RG, Powers VE, Sebastio G, Ballabio A, Pettigrew AL, Ledbetter DH, Levy E, Craig IW, Willard HF (1991) Localization of the X inactivation centre on the human X chromosome in Xq13. Nature 349(6304):82–84. doi: 10.1038/349082a0 PubMedCrossRefGoogle Scholar
  18. Caretti G, Schiltz RL, Dilworth FJ, Di Padova M, Zhao P, Ogryzko V, Fuller-Pace FV, Hoffman EP, Tapscott SJ, Sartorelli V (2006) The RNA helicases p68/p72 and the noncoding RNA SRA are coregulators of MyoD and skeletal muscle differentiation. Dev Cell 11(4):547–560. doi: 10.1016/j.devcel.2006.08.003 PubMedCrossRefGoogle Scholar
  19. Carlile TM, Rojas-Duran MF, Zinshteyn B, Shin H, Bartoli KM, Gilbert WV (2014) Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells. Nature 515(7525):143–146. doi: 10.1038/nature13802 PubMedPubMedCentralCrossRefGoogle Scholar
  20. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, Kodzius R, Shimokawa K, Bajic VB, Brenner SE, Batalov S, Forrest AR, Zavolan M, Davis MJ, Wilming LG, Aidinis V, Allen JE, Ambesi-Impiombato A, Apweiler R, Aturaliya RN, Bailey TL, Bansal M, Baxter L, Beisel KW, Bersano T, Bono H, Chalk AM, Chiu KP, Choudhary V, Christoffels A, Clutterbuck DR, Crowe ML, Dalla E, Dalrymple BP, de Bono B, Della Gatta G, di Bernardo D, Down T, Engstrom P, Fagiolini M, Faulkner G, Fletcher CF, Fukushima T, Furuno M, Futaki S, Gariboldi M, Georgii-Hemming P, Gingeras TR, Gojobori T, Green RE, Gustincich S, Harbers M, Hayashi Y, Hensch TK, Hirokawa N, Hill D, Huminiecki L, Iacono M, Ikeo K, Iwama A, Ishikawa T, Jakt M, Kanapin A, Katoh M, Kawasawa Y, Kelso J, Kitamura H, Kitano H, Kollias G, Krishnan SP, Kruger A, Kummerfeld SK, Kurochkin IV, Lareau LF, Lazarevic D, Lipovich L, Liu J, Liuni S, McWilliam S, Madan Babu M, Madera M, Marchionni L, Matsuda H, Matsuzawa S, Miki H, Mignone F, Miyake S, Morris K, Mottagui-Tabar S, Mulder N, Nakano N, Nakauchi H, Ng P, Nilsson R, Nishiguchi S, Nishikawa S, Nori F, Ohara O, Okazaki Y, Orlando V, Pang KC, Pavan WJ, Pavesi G, Pesole G, Petrovsky N, Piazza S, Reed J, Reid JF, Ring BZ, Ringwald M, Rost B, Ruan Y, Salzberg SL, Sandelin A, Schneider C, Schonbach C, Sekiguchi K, Semple CA, Seno S, Sessa L, Sheng Y, Shibata Y, Shimada H, Shimada K, Silva D, Sinclair B, Sperling S, Stupka E, Sugiura K, Sultana R, Takenaka Y, Taki K, Tammoja K, Tan SL, Tang S, Taylor MS, Tegner J, Teichmann SA, Ueda HR, van Nimwegen E, Verardo R, Wei CL, Yagi K, Yamanishi H, Zabarovsky E, Zhu S, Zimmer A, Hide W, Bult C, Grimmond SM, Teasdale RD, Liu ET, Brusic V, Quackenbush J, Wahlestedt C, Mattick JS, Hume DA, Kai C, Sasaki D, Tomaru Y, Fukuda S, Kanamori-Katayama M, Suzuki M, Aoki J, Arakawa T, Iida J, Imamura K, Itoh M, Kato T, Kawaji H, Kawagashira N, Kawashima T, Kojima M, Kondo S, Konno H, Nakano K, Ninomiya N, Nishio T, Okada M, Plessy C, Shibata K, Shiraki T, Suzuki S, Tagami M, Waki K, Watahiki A, Okamura-Oho Y, Suzuki H, Kawai J, Hayashizaki Y (2005) The transcriptional landscape of the mammalian genome. Science 309(5740):1559–1563. doi: 10.1126/science.1112014
  21. Cech TR (2002) Ribozymes, the first 20 years. Biochem Soc Trans 30(Pt 6):1162–1166. doi: 10.1042/bst0301162
  22. Cech TR, Steitz JA (2014) The noncoding RNA revolution-trashing old rules to forge new ones. Cell 157(1):77–94. doi: 10.1016/j.cell.2014.03.008 PubMedCrossRefGoogle Scholar
  23. Chakravarty D, Sboner A, Nair SS, Giannopoulou E, Li R, Hennig S, Mosquera JM, Pauwels J, Park K, Kossai M, MacDonald TY, Fontugne J, Erho N, Vergara IA, Ghadessi M, Davicioni E, Jenkins RB, Palanisamy N, Chen Z, Nakagawa S, Hirose T, Bander NH, Beltran H, Fox AH, Elemento O, Rubin MA (2014) The oestrogen receptor alpha-regulated lncRNA NEAT1 is a critical modulator of prostate cancer. Nat Commun 5:5383. doi: 10.1038/ncomms6383 PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cheng W, Zhang Z, Wang J (2013) Long noncoding RNAs: new players in prostate cancer. Cancer Lett 339(1):8–14. doi: 10.1016/j.canlet.2013.07.008 PubMedCrossRefGoogle Scholar
  25. Chu C, Qu K, Zhong FL, Artandi SE, Chang HY (2011) Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol Cell 44(4):667–678. doi: 10.1016/j.molcel.2011.08.027 PubMedPubMedCentralCrossRefGoogle Scholar
  26. Chung S, Nakagawa H, Uemura M, Piao L, Ashikawa K, Hosono N, Takata R, Akamatsu S, Kawaguchi T, Morizono T, Tsunoda T, Daigo Y, Matsuda K, Kamatani N, Nakamura Y, Kubo M (2011) Association of a novel long non-coding RNA in 8q24 with prostate cancer susceptibility. Cancer Sci 102(1):245–252. doi: 10.1111/j.1349-7006.2010.01737.x PubMedCrossRefGoogle Scholar
  27. Cooper C, Guo J, Yan Y, Chooniedass-Kothari S, Hube F, Hamedani MK, Murphy LC, Myal Y, Leygue E (2009) Increasing the relative expression of endogenous non-coding Steroid Receptor RNA Activator (SRA) in human breast cancer cells using modified oligonucleotides. Nucleic Acids Res 37(13):4518–4531. doi: 10.1093/nar/gkp441 PubMedPubMedCentralCrossRefGoogle Scholar
  28. Core LJ, Waterfall JJ, Lis JT (2008) Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322(5909):1845–1848. doi: 10.1126/science.1162228 PubMedPubMedCentralCrossRefGoogle Scholar
  29. Crea F, Watahiki A, Quagliata L, Xue H, Pikor L, Parolia A, Wang Y, Lin D, Lam WL, Farrar WL, Isogai T, Morant R, Castori-Eppenberger S, Chi KN, Helgason CD (2014) Identification of a long non-coding RNA as a novel biomarker and potential therapeutic target for metastatic prostate cancer. Oncotarget 5(3):764–774PubMedPubMedCentralCrossRefGoogle Scholar
  30. Cui Z, Ren S, Lu J, Wang F, Xu W, Sun Y, Wei M, Chen J, Gao X, Xu C, Mao JH (2013) The prostate cancer-up-regulated long noncoding RNA PlncRNA-1 modulates apoptosis and proliferation through reciprocal regulation of androgen receptor. Urologic Oncol 31(7):1117–1123. doi: 10.1016/j.urolonc.2011.11.030 CrossRefGoogle Scholar
  31. de Kok JB, Verhaegh GW, Roelofs RW, Hessels D, Kiemeney LA, Aalders TW, Swinkels DW, Schalken JA (2002) DD3(PCA3), a very sensitive and specific marker to detect prostate tumors. Cancer Res 62(9):2695–2698PubMedGoogle Scholar
  32. De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, Tusi BK, Muller H, Ragoussis J, Wei CL, Natoli G (2010) A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol 8(5):e1000384. doi: 10.1371/journal.pbio.1000384 PubMedPubMedCentralCrossRefGoogle Scholar
  33. Ding X, Zhu L, Ji T, Zhang X, Wang F, Gan S, Zhao M, Yang H (2014) Long intergenic non-coding RNAs (LincRNAs) identified by RNA-seq in breast cancer. PLoS ONE 9(8):e103270. doi: 10.1371/journal.pone.0103270 PubMedPubMedCentralCrossRefGoogle Scholar
  34. Dinger ME, Gascoigne DK, Mattick JS (2011) The evolution of RNAs with multiple functions. Biochimie 93(11):2013–2018. doi: 10.1016/j.biochi.2011.07.018 PubMedCrossRefGoogle Scholar
  35. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, Xue C, Marinov GK, Khatun J, Williams BA, Zaleski C, Rozowsky J, Roder M, Kokocinski F, Abdelhamid RF, Alioto T, Antoshechkin I, Baer MT, Bar NS, Batut P, Bell K, Bell I, Chakrabortty S, Chen X, Chrast J, Curado J, Derrien T, Drenkow J, Dumais E, Dumais J, Duttagupta R, Falconnet E, Fastuca M, Fejes-Toth K, Ferreira P, Foissac S, Fullwood MJ, Gao H, Gonzalez D, Gordon A, Gunawardena H, Howald C, Jha S, Johnson R, Kapranov P, King B, Kingswood C, Luo OJ, Park E, Persaud K, Preall JB, Ribeca P, Risk B, Robyr D, Sammeth M, Schaffer L, See LH, Shahab A, Skancke J, Suzuki AM, Takahashi H, Tilgner H, Trout D, Walters N, Wang H, Wrobel J, Yu Y, Ruan X, Hayashizaki Y, Harrow J, Gerstein M, Hubbard T, Reymond A, Antonarakis SE, Hannon G, Giddings MC, Ruan Y, Wold B, Carninci P, Guigo R, Gingeras TR (2012) Landscape of transcription in human cells. Nature 489(7414):101–108. doi: 10.1038/nature11233 PubMedPubMedCentralCrossRefGoogle Scholar
  36. Dominissini D, Moshitch-Moshkovitz S, Schwartz S, Salmon-Divon M, Ungar L, Osenberg S, Cesarkas K, Jacob-Hirsch J, Amariglio N, Kupiec M, Sorek R, Rechavi G (2012) Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485(7397):201–206. doi: 10.1038/nature11112 PubMedCrossRefGoogle Scholar
  37. Emberley E, Huang GJ, Hamedani MK, Czosnek A, Ali D, Grolla A, Lu B, Watson PH, Murphy LC, Leygue E (2003) Identification of new human coding steroid receptor RNA activator isoforms. Biochem Biophys Res Commun 301(2):509–515. doi: 10.1016/S0006-291X(02)03070-X PubMedCrossRefGoogle Scholar
  38. Evans RM, Mangelsdorf DJ (2014) Nuclear Receptors, RXR, and the Big Bang. Cell 157(1):255–266. doi: 10.1016/j.cell.2014.03.012 PubMedPubMedCentralCrossRefGoogle Scholar
  39. Fang B, Everett LJ, Jager J, Briggs E, Armour SM, Feng D, Roy A, Gerhart-Hines Z, Sun Z, Lazar MA (2014) Circadian enhancers coordinate multiple phases of rhythmic gene transcription in vivo. Cell 159(5):1140–1152. doi: 10.1016/j.cell.2014.10.022 PubMedPubMedCentralCrossRefGoogle Scholar
  40. Ferreira LB, Palumbo A, de Mello KD, Sternberg C, Caetano MS, de Oliveira FL, Neves AF, Nasciutti LE, Goulart LR, Gimba ER (2012) PCA3 noncoding RNA is involved in the control of prostate-cancer cell survival and modulates androgen receptor signaling. BMC Cancer 12:507. doi: 10.1186/1471-2407-12-507 PubMedPubMedCentralCrossRefGoogle Scholar
  41. Foulds CE, Tsimelzon A, Long W, Le A, Tsai SY, Tsai MJ, O’Malley BW (2010) Research resource: expression profiling reveals unexpected targets and functions of the human steroid receptor RNA activator (SRA) gene. Mol Endocrinol 24(5):1090–1105. doi: 10.1210/me.2009-0427 PubMedPubMedCentralCrossRefGoogle Scholar
  42. Foulds CE, Feng Q, Ding C, Bailey S, Hunsaker TL, Malovannaya A, Hamilton RA, Gates LA, Zhang Z, Li C, Chan D, Bajaj A, Callaway CG, Edwards DP, Lonard DM, Tsai SY, Tsai MJ, Qin J, O’Malley BW (2013) Proteomic analysis of coregulators bound to ERalpha on DNA and nucleosomes reveals coregulator dynamics. Mol Cell 51(2):185–199. doi: 10.1016/j.molcel.2013.06.007 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Fu X, Ravindranath L, Tran N, Petrovics G, Srivastava S (2006) Regulation of apoptosis by a prostate-specific and prostate cancer-associated noncoding gene, PCGEM1. DNA Cell Biol 25(3):135–141. doi: 10.1089/dna.2006.25.135 PubMedCrossRefGoogle Scholar
  44. Gabory A, Jammes H, Dandolo L (2010) The H19 locus: role of an imprinted non-coding RNA in growth and development. BioEssays: News Rev Mol Cell Dev Biol 32(6):473–480. doi: 10.1002/bies.200900170 CrossRefGoogle Scholar
  45. Gong C, Maquat LE (2015) Affinity purification of long noncoding RNA-protein complexes from formaldehyde cross-linked mammalian cells. Methods Mol Biol 1206:81–86. doi: 10.1007/978-1-4939-1369-5_7 PubMedCrossRefGoogle Scholar
  46. Goodrich JA, Kugel JF (2009) From bacteria to humans, chromatin to elongation, and activation to repression: The expanding roles of noncoding RNAs in regulating transcription. Crit Rev Biochem Mol Biol 44(1):3–15. doi: 10.1080/10409230802593995 PubMedPubMedCentralCrossRefGoogle Scholar
  47. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, Wang Y, Brzoska P, Kong B, Li R, West RB, van de Vijver MJ, Sukumar S, Chang HY (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464(7291):1071–1076. doi: 10.1038/nature08975 PubMedPubMedCentralCrossRefGoogle Scholar
  48. Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, Cabili MN, Jaenisch R, Mikkelsen TS, Jacks T, Hacohen N, Bernstein BE, Kellis M, Regev A, Rinn JL, Lander ES (2009) Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458(7235):223–227. doi: 10.1038/nature07672 PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hagege H, Klous P, Braem C, Splinter E, Dekker J, Cathala G, de Laat W, Forne T (2007) Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat Protoc 2(7):1722–1733. doi: 10.1038/nprot.2007.243 PubMedCrossRefGoogle Scholar
  50. Hah N, Kraus WL (2014) Hormone-regulated transcriptomes: lessons learned from estrogen signaling pathways in breast cancer cells. Mol Cell Endocrinol 382(1):652–664. doi: 10.1016/j.mce.2013.06.021 PubMedCrossRefGoogle Scholar
  51. Hah N, Danko CG, Core L, Waterfall JJ, Siepel A, Lis JT, Kraus WL (2011) A rapid, extensive, and transient transcriptional response to estrogen signaling in breast cancer cells. Cell 145(4):622–634. doi: 10.1016/j.cell.2011.03.042 PubMedPubMedCentralCrossRefGoogle Scholar
  52. Hah N, Murakami S, Nagari A, Danko CG, Kraus WL (2013) Enhancer transcripts mark active estrogen receptor binding sites. Genome Res 23(8):1210–1223. doi: 10.1101/gr.152306.112 PubMedPubMedCentralCrossRefGoogle Scholar
  53. Hansji H, Leung EY, Baguley BC, Finlay GJ, Askarian-Amiri ME (2014) Keeping abreast with long non-coding RNAs in mammary gland development and breast cancer. Frontiers Genet 5:379. doi: 10.3389/fgene.2014.00379 CrossRefGoogle Scholar
  54. Hatchell EC, Colley SM, Beveridge DJ, Epis MR, Stuart LM, Giles KM, Redfern AD, Miles LE, Barker A, MacDonald LM, Arthur PG, Lui JC, Golding JL, McCulloch RK, Metcalf CB, Wilce JA, Wilce MC, Lanz RB, O’Malley BW, Leedman PJ (2006) SLIRP, a small SRA binding protein, is a nuclear receptor corepressor. Mol Cell 22(5):657–668. doi: 10.1016/j.molcel.2006.05.024 PubMedCrossRefGoogle Scholar
  55. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang X, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M, Ren B (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459(7243):108–112. doi: 10.1038/nature07829 PubMedPubMedCentralCrossRefGoogle Scholar
  56. Hessels D, Schalken JA (2009) The use of PCA3 in the diagnosis of prostate cancer. Nat Rev Urol 6(5):255–261. doi: 10.1038/nrurol.2009.40 PubMedCrossRefGoogle Scholar
  57. Ho TT, Zhou N, Huang J, Koirala P, Xu M, Fung R, Wu F, Mo YY (2014) Targeting non-coding RNAs with the CRISPR/Cas9 system in human cell lines. Nucleic Acids Res. doi: 10.1093/nar/gku1198 Google Scholar
  58. Honig A, Auboeuf D, Parker MM, O’Malley BW, Berget SM (2002) Regulation of alternative splicing by the ATP-dependent DEAD-box RNA helicase p72. Mol Cell Biol 22(16):5698–5707PubMedPubMedCentralCrossRefGoogle Scholar
  59. Hsieh CL, Fei T, Chen Y, Li T, Gao Y, Wang X, Sun T, Sweeney CJ, Lee GS, Chen S, Balk SP, Liu XS, Brown M, Kantoff PW (2014) Enhancer RNAs participate in androgen receptor-driven looping that selectively enhances gene activation. Proc Natl Acad Sci USA 111(20):7319–7324. doi: 10.1073/pnas.1324151111 PubMedPubMedCentralCrossRefGoogle Scholar
  60. Hube F, Velasco G, Rollin J, Furling D, Francastel C (2011) Steroid receptor RNA activator protein binds to and counteracts SRA RNA-mediated activation of MyoD and muscle differentiation. Nucleic Acids Res 39(2):513–525. doi: 10.1093/nar/gkq833 PubMedPubMedCentralCrossRefGoogle Scholar
  61. Hudson WH, Pickard MR, de Vera IM, Kuiper EG, Mourtada-Maarabouni M, Conn GL, Kojetin DJ, Williams GT, Ortlund EA (2014) Conserved sequence-specific lincRNA-steroid receptor interactions drive transcriptional repression and direct cell fate. Nat Commun 5:5395. doi: 10.1038/ncomms6395 PubMedPubMedCentralCrossRefGoogle Scholar
  62. Huet T, Miannay FA, Patton JR, Thore S (2014) Steroid receptor RNA activator (SRA) modification by the human pseudouridine synthase 1 (hPus1p): RNA binding, activity, and atomic model. PLoS ONE 9(4):e94610. doi: 10.1371/journal.pone.0094610 PubMedPubMedCentralCrossRefGoogle Scholar
  63. Hung CL, Wang LY, Yu YL, Chen HW, Srivastava S, Petrovics G, Kung HJ (2014) A long noncoding RNA connects c-Myc to tumor metabolism. Proc Natl Acad Sci USA. doi: 10.1073/pnas.1415669112 Google Scholar
  64. Janowski BA, Corey DR (2010) Minireview: Switching on progesterone receptor expression with duplex RNA. Mol Endocrinol 24(12):2243–2252. doi: 10.1210/me.2010-0067 PubMedPubMedCentralCrossRefGoogle Scholar
  65. Jiang YJ, Bikle DD (2014) lncRNA profiling reveals new mechanism for VDR protection against skin cancer formation. The Journal of steroid biochemistry and molecular biology 144(Pt A):87–90. doi: 10.1016/j.jsbmb.2013.11.018
  66. Jung C, Mittler G, Oswald F, Borggrefe T (2013) RNA helicase Ddx5 and the noncoding RNA SRA act as coactivators in the Notch signaling pathway. Biochim Biophys Acta 5:1180–1189. doi: 10.1016/j.bbamcr.2013.01.032
  67. Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, Stadler PF, Hertel J, Hackermuller J, Hofacker IL, Bell I, Cheung E, Drenkow J, Dumais E, Patel S, Helt G, Ganesh M, Ghosh S, Piccolboni A, Sementchenko V, Tammana H, Gingeras TR (2007) RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316(5830):1484–1488. doi: 10.1126/science.1138341 PubMedCrossRefGoogle Scholar
  68. Kawashima H, Takano H, Sugita S, Takahara Y, Sugimura K, Nakatani T (2003) A novel steroid receptor co-activator protein (SRAP) as an alternative form of steroid receptor RNA-activator gene: expression in prostate cancer cells and enhancement of androgen receptor activity. Biochem J 369(Pt 1):163–171. doi: 10.1042/BJ20020743 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Kelly VR, Xu B, Kuick R, Koenig RJ, Hammer GD (2010) Dax1 up-regulates Oct4 expression in mouse embryonic stem cells via LRH-1 and SRA. Mol Endocrinol 24(12):2281–2291. doi: 10.1210/me.2010-0133 PubMedPubMedCentralCrossRefGoogle Scholar
  70. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, Wu J, Harmin DA, Laptewicz M, Barbara-Haley K, Kuersten S, Markenscoff-Papadimitriou E, Kuhl D, Bito H, Worley PF, Kreiman G, Greenberg ME (2010) Widespread transcription at neuronal activity-regulated enhancers. Nature 465(7295):182–187. doi: 10.1038/nature09033 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Kino T, Hurt DE, Ichijo T, Nader N, Chrousos GP (2010) Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor. Sci Signal 3(107):ra8. doi:10.1126/scisignal.2000568Google Scholar
  72. Lam MT, Cho H, Lesch HP, Gosselin D, Heinz S, Tanaka-Oishi Y, Benner C, Kaikkonen MU, Kim AS, Kosaka M, Lee CY, Watt A, Grossman TR, Rosenfeld MG, Evans RM, Glass CK (2013) Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription. Nature 498(7455):511–515. doi: 10.1038/nature12209 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Lam MT, Li W, Rosenfeld MG, Glass CK (2014) Enhancer RNAs and regulated transcriptional programs. Trends Biochem Sci 39(4):170–182. doi: 10.1016/j.tibs.2014.02.007 PubMedPubMedCentralCrossRefGoogle Scholar
  74. Lanz RB, McKenna NJ, Onate SA, Albrecht U, Wong J, Tsai SY, Tsai MJ, O’Malley BW (1999) A steroid receptor coactivator, SRA, functions as an RNA and is present in an SRC-1 complex. Cell 97(1):17–27. doi: 10.1016/S0092-8674(00)80711-4 PubMedCrossRefGoogle Scholar
  75. Lanz RB, Razani B, Goldberg AD, O’Malley BW (2002) Distinct RNA motifs are important for coactivation of steroid hormone receptors by steroid receptor RNA activator (SRA). Proc Natl Acad Sci USA 99(25):16081–16086. doi: 10.1073/pnas.192571399 PubMedPubMedCentralCrossRefGoogle Scholar
  76. Lanz RB, Chua SS, Barron N, Soder BM, DeMayo F, O’Malley BW (2003) Steroid receptor RNA activator stimulates proliferation as well as apoptosis in vivo. Mol Cell Biol 23(20):7163–7176PubMedPubMedCentralCrossRefGoogle Scholar
  77. Leygue E, Dotzlaw H, Watson PH, Murphy LC (1999) Expression of the steroid receptor RNA activator in human breast tumors. Cancer Res 59(17):4190–4193PubMedGoogle Scholar
  78. Li L, Chang HY (2014) Physiological roles of long noncoding RNAs: insight from knockout mice. Trends Cell Biol 24(10):594–602. doi: 10.1016/j.tcb.2014.06.003 PubMedPubMedCentralCrossRefGoogle Scholar
  79. Li S, Mason CE (2014) The pivotal regulatory landscape of RNA modifications. Annu Rev Genomics Hum Genet 15:127–150. doi: 10.1146/annurev-genom-090413-025405 PubMedCrossRefGoogle Scholar
  80. Li W, Notani D, Ma Q, Tanasa B, Nunez E, Chen AY, Merkurjev D, Zhang J, Ohgi K, Song X, Oh S, Kim HS, Glass CK, Rosenfeld MG (2013) Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature 498(7455):516–520. doi: 10.1038/nature12210 PubMedPubMedCentralCrossRefGoogle Scholar
  81. Liu N, Pan T (2015) RNA epigenetics. Transl Res: J Lab Clin Med 165(1):28–35. doi: 10.1016/j.trsl.2014.04.003 CrossRefGoogle Scholar
  82. Liu S, Sheng L, Miao H, Saunders TL, MacDougald OA, Koenig RJ, Xu B (2014a) SRA gene knockout protects against diet-induced obesity and improves glucose tolerance. J Biol Chem 289(19):13000–13009. doi: 10.1074/jbc.M114.564658 PubMedPubMedCentralCrossRefGoogle Scholar
  83. Liu Z, Merkurjev D, Yang F, Li W, Oh S, Friedman MJ, Song X, Zhang F, Ma Q, Ohgi KA, Krones A, Rosenfeld MG (2014b) Enhancer activation requires trans-recruitment of a mega transcription factor complex. Cell 159(2):358–373. doi: 10.1016/j.cell.2014.08.027 PubMedPubMedCentralCrossRefGoogle Scholar
  84. Lonard DM, O’Malley BW (2005) Expanding functional diversity of the coactivators. Trends Biochem Sci 30(3):126–132. doi: 10.1016/j.tibs.2005.01.001 PubMedCrossRefGoogle Scholar
  85. Lonard DM, O’Malley BW (2006) The expanding cosmos of nuclear receptor coactivators. Cell 125(3):411–414. doi: 10.1016/j.cell.2006.04.021 PubMedCrossRefGoogle Scholar
  86. Lonard DM, O’Malley BW (2007) Nuclear receptor coregulators: judges, juries, and executioners of cellular regulation. Mol Cell 27(5):691–700. doi: 10.1016/j.molcel.2007.08.012 PubMedCrossRefGoogle Scholar
  87. Louro R, Nakaya HI, Amaral PP, Festa F, Sogayar MC, da Silva AM, Verjovski-Almeida S, Reis EM (2007) Androgen responsive intronic non-coding RNAs. BMC Biol 5:4. doi: 10.1186/1741-7007-5-4 PubMedPubMedCentralCrossRefGoogle Scholar
  88. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schutz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P, Evans RM (1995) The nuclear receptor superfamily: the second decade. Cell 83(6):835–839PubMedCrossRefGoogle Scholar
  89. Marin-Bejar O, Huarte M (2015) RNA pulldown protocol for in vitro detection and identification of RNA-associated proteins. Methods Mol Biol 1206:87–95. doi: 10.1007/978-1-4939-1369-5_8 PubMedCrossRefGoogle Scholar
  90. McKay DB, Xi L, Barthel KK, Cech TR (2014) Structure and function of steroid receptor RNA activator protein, the proposed partner of SRA noncoding RNA. J Mol Biol 426(8):1766–1785. doi: 10.1016/j.jmb.2014.01.006 PubMedPubMedCentralCrossRefGoogle Scholar
  91. McKenna NJ, O’Malley BW (2002) Combinatorial control of gene expression by nuclear receptors and coregulators. Cell 108(4):465–474PubMedCrossRefGoogle Scholar
  92. Mourtada-Maarabouni M, Pickard MR, Hedge VL, Farzaneh F, Williams GT (2009) GAS5, a non-protein-coding RNA, controls apoptosis and is downregulated in breast cancer. Oncogene 28(2):195–208. doi: 10.1038/onc.2008.373 PubMedCrossRefGoogle Scholar
  93. Murphy LC, Simon SL, Parkes A, Leygue E, Dotzlaw H, Snell L, Troup S, Adeyinka A, Watson PH (2000) Altered expression of estrogen receptor coregulators during human breast tumorigenesis. Cancer Res 60(22):6266–6271PubMedGoogle Scholar
  94. Novikova IV, Hennelly SP, Sanbonmatsu KY (2012) Structural architecture of the human long non-coding RNA, steroid receptor RNA activator. Nucleic Acids Res 40(11):5034–5051. doi: 10.1093/nar/gks071 PubMedPubMedCentralCrossRefGoogle Scholar
  95. Ottaviani S, de Giorgio A, Harding V, Stebbing J, Castellano L (2014) Noncoding RNAs and the control of hormonal signaling via nuclear receptor regulation. J Mol Endocrinol 53(2):R61–R70. doi: 10.1530/JME-14-0134 PubMedCrossRefGoogle Scholar
  96. Petrovics G, Zhang W, Makarem M, Street JP, Connelly R, Sun L, Sesterhenn IA, Srikantan V, Moul JW, Srivastava S (2004) Elevated expression of PCGEM1, a prostate-specific gene with cell growth-promoting function, is associated with high-risk prostate cancer patients. Oncogene 23(2):605–611. doi: 10.1038/sj.onc.1207069 PubMedCrossRefGoogle Scholar
  97. Pickard MR, Mourtada-Maarabouni M, Williams GT (2013) Long non-coding RNA GAS5 regulates apoptosis in prostate cancer cell lines. Biochimica et biophysica acta 1832(10):1613–1623. doi: 10.1016/j.bbadis.2013.05.005
  98. Plank JL, Dean A (2014) Enhancer function: mechanistic and genome-wide insights come together. Mol Cell 55(1):5–14. doi: 10.1016/j.molcel.2014.06.015 PubMedCrossRefGoogle Scholar
  99. Prensner JR, Chinnaiyan AM (2011) The emergence of lncRNAs in cancer biology. Cancer Discov 1(5):391–407. doi: 10.1158/2159-8290.CD-11-0209 PubMedPubMedCentralCrossRefGoogle Scholar
  100. Prensner JR, Iyer MK, Balbin OA, Dhanasekaran SM, Cao Q, Brenner JC, Laxman B, Asangani IA, Grasso CS, Kominsky HD, Cao X, Jing X, Wang X, Siddiqui J, Wei JT, Robinson D, Iyer HK, Palanisamy N, Maher CA, Chinnaiyan AM (2011) Transcriptome sequencing across a prostate cancer cohort identifies PCAT-1, an unannotated lincRNA implicated in disease progression. Nat Biotechnol 29(8):742–749. doi: 10.1038/nbt.1914 PubMedPubMedCentralCrossRefGoogle Scholar
  101. Prensner JR, Iyer MK, Sahu A, Asangani IA, Cao Q, Patel L, Vergara IA, Davicioni E, Erho N, Ghadessi M, Jenkins RB, Triche TJ, Malik R, Bedenis R, McGregor N, Ma T, Chen W, Han S, Jing X, Cao X, Wang X, Chandler B, Yan W, Siddiqui J, Kunju LP, Dhanasekaran SM, Pienta KJ, Feng FY, Chinnaiyan AM (2013) The long noncoding RNA SChLAP1 promotes aggressive prostate cancer and antagonizes the SWI/SNF complex. Nat Genet 45(11):1392–1398. doi: 10.1038/ng.2771 PubMedPubMedCentralCrossRefGoogle Scholar
  102. Prensner JR, Chen W, Han S, Iyer MK, Cao Q, Kothari V, Evans JR, Knudsen KE, Paulsen MT, Ljungman M, Lawrence TS, Chinnaiyan AM, Feng FY (2014a) The Long Non-Coding RNA PCAT-1 Promotes Prostate Cancer Cell Proliferation through cMyc. Neoplasia 16(11):900–908. doi: 10.1016/j.neo.2014.09.001 PubMedPubMedCentralCrossRefGoogle Scholar
  103. Prensner JR, Chen W, Iyer MK, Cao Q, Ma T, Han S, Sahu A, Malik R, Wilder-Romans K, Navone N, Logothetis CJ, Araujo JC, Pisters LL, Tewari AK, Canman CE, Knudsen KE, Kitabayashi N, Rubin MA, Demichelis F, Lawrence TS, Chinnaiyan AM, Feng FY (2014b) PCAT-1, a long noncoding RNA, regulates BRCA2 and controls homologous recombination in cancer. Cancer Res 74(6):1651–1660. doi: 10.1158/0008-5472.CAN-13-3159 PubMedPubMedCentralCrossRefGoogle Scholar
  104. Prensner JR, Sahu A, Iyer MK, Malik R, Chandler B, Asangani IA, Poliakov A, Vergara IA, Alshalalfa M, Jenkins RB, Davicioni E, Feng FY, Chinnaiyan AM (2014c) The IncRNAs PCGEM1 and PRNCR1 are not implicated in castration resistant prostate cancer. Oncotarget 5(6):1434–1438PubMedPubMedCentralCrossRefGoogle Scholar
  105. Qiu J, Ye L, Ding J, Feng W, Zhang Y, Lv T, Wang J, Hua K (2014) Effects of oestrogen on long noncoding RNA expression in oestrogen receptor alpha-positive ovarian cancer cells. J Steroid Biochem Molecul Biol 141:60–70. doi: 10.1016/j.jsbmb.2013.12.017 CrossRefGoogle Scholar
  106. Quinodoz S, Guttman M (2014) Long noncoding RNAs: an emerging link between gene regulation and nuclear organization. Trends Cell Biol 24(11):651–663. doi: 10.1016/j.tcb.2014.08.009 PubMedPubMedCentralCrossRefGoogle Scholar
  107. Redfern AD, Colley SM, Beveridge DJ, Ikeda N, Epis MR, Li X, Foulds CE, Stuart LM, Barker A, Russell VJ, Ramsay K, Kobelke SJ, Hatchell EC, Payne C, Giles KM, Messineo A, Gatignol A, Lanz RB, O’Malley BW, Leedman PJ (2013) RNA-induced silencing complex (RISC) Proteins PACT, TRBP, and Dicer are SRA binding nuclear receptor coregulators. Proc Natl Acad Sci USA 110(16):6536–6541. doi: 10.1073/pnas.1301620110 PubMedPubMedCentralCrossRefGoogle Scholar
  108. Romanuik TL, Wang G, Morozova O, Delaney A, Marra MA, Sadar MD (2010) LNCaP Atlas: gene expression associated with in vivo progression to castration-recurrent prostate cancer. BMC Med Genomics 3:43. doi: 10.1186/1755-8794-3-43 PubMedPubMedCentralCrossRefGoogle Scholar
  109. Ronnau CG, Verhaegh GW, Luna-Velez MV, Schalken JA (2014) Noncoding RNAs as novel biomarkers in prostate cancer. BioMed Res Int 2014:591703. doi: 10.1155/2014/591703 PubMedPubMedCentralCrossRefGoogle Scholar
  110. Schwartz JC, Younger ST, Nguyen NB, Hardy DB, Monia BP, Corey DR, Janowski BA (2008) Antisense transcripts are targets for activating small RNAs. Nat Struct Mol Biol 15(8):842–848. doi: 10.1038/nsmb.1444 PubMedPubMedCentralCrossRefGoogle Scholar
  111. Sharp PA (2009) The centrality of RNA. Cell 136(4):577–580. doi: 10.1016/j.cell.2009.02.007 PubMedCrossRefGoogle Scholar
  112. Shi Y, Downes M, Xie W, Kao HY, Ordentlich P, Tsai CC, Hon M, Evans RM (2001) Sharp, an inducible cofactor that integrates nuclear receptor repression and activation. Genes Dev 15(9):1140–1151. doi: 10.1101/gad.871201 PubMedPubMedCentralCrossRefGoogle Scholar
  113. Shore AN, Rosen JM (2014) Regulation of mammary epithelial cell homeostasis by lncRNAs. Int J Biochem Cell Biol 54:318–330. doi: 10.1016/j.biocel.2014.03.012 PubMedPubMedCentralCrossRefGoogle Scholar
  114. Sorensen KP, Thomassen M, Tan Q, Bak M, Cold S, Burton M, Larsen MJ, Kruse TA (2013) Long non-coding RNA HOTAIR is an independent prognostic marker of metastasis in estrogen receptor-positive primary breast cancer. Breast Cancer Res Treat 142(3):529–536. doi: 10.1007/s10549-013-2776-7 PubMedCrossRefGoogle Scholar
  115. Srikantan V, Zou Z, Petrovics G, Xu L, Augustus M, Davis L, Livezey JR, Connell T, Sesterhenn IA, Yoshino K, Buzard GS, Mostofi FK, McLeod DG, Moul JW, Srivastava S (2000) PCGEM1, a prostate-specific gene, is overexpressed in prostate cancer. Proc Natl Acad Sci USA 97(22):12216–12221. doi: 10.1073/pnas.97.22.12216 PubMedPubMedCentralCrossRefGoogle Scholar
  116. Su X, Malouf GG, Chen Y, Zhang J, Yao H, Valero V, Weinstein JN, Spano JP, Meric-Bernstam F, Khayat D, Esteva FJ (2014) Comprehensive analysis of long non-coding RNAs in human breast cancer clinical subtypes. Oncotarget 5(20):9864–9876PubMedPubMedCentralCrossRefGoogle Scholar
  117. Sun H, Wang G, Peng Y, Zeng Y, Zhu QN, Li TL, Cai JQ, Zhou HH, Zhu YS (2015) H19 lncRNA mediates 17β-estradiol-induced cell proliferation in MCF-7 breast cancer cells. Oncol Rep. 2015 Jun;33(6):3045–52. doi: 10.3892/or.2015.3899
  118. Sun M, Kraus WL (2013) Minireview: Long noncoding RNAs: new “links” between gene expression and cellular outcomes in endocrinology. Mol Endocrinol 27(9):1390–1402. doi: 10.1210/me.2013-1113 PubMedPubMedCentralCrossRefGoogle Scholar
  119. Sun M, Kraus WL (2014) From discovery to function: the expanding roles of long non-coding rnas in physiology and disease. Endocr Rev, er20141034. doi: 10.1210/er.2014-1034
  120. Sun M, Gadad SS, Kim DS, Kraus WL (2015) Discovery, Annotation, and Functional Analysis of Long Noncoding RNAs Controlling Cell-Cycle Gene Expression and Proliferation in Breast Cancer Cells. Mol Cell. Jul 28. pii: S1097–2765(15)00495-5. doi: 10.1016/j.molcel.2015.06.023
  121. Takayama K, Horie-Inoue K, Katayama S, Suzuki T, Tsutsumi S, Ikeda K, Urano T, Fujimura T, Takagi K, Takahashi S, Homma Y, Ouchi Y, Aburatani H, Hayashizaki Y, Inoue S (2013) Androgen-responsive long noncoding RNA CTBP1-AS promotes prostate cancer. EMBO J 32(12):1665–1680. doi: 10.1038/emboj.2013.99 PubMedPubMedCentralCrossRefGoogle Scholar
  122. Trevino LS, Weigel NL (2013) Phosphorylation: a fundamental regulator of steroid receptor action. Trends Endocrinol Metab TEM 24(10):515–524. doi: 10.1016/j.tem.2013.05.008 PubMedCrossRefGoogle Scholar
  123. Tsai MJ, O’Malley BW (1994) Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu Rev Biochem 63:451–486. doi: 10.1146/annurev.bi.63.070194.002315 PubMedCrossRefGoogle Scholar
  124. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY (2010) Long noncoding RNA as modular scaffold of histone modification complexes. Science 329(5992):689–693. doi: 10.1126/science.1192002 PubMedPubMedCentralCrossRefGoogle Scholar
  125. Ulitsky I, Bartel DP (2013) lincRNAs: genomics, evolution, and mechanisms. Cell 154(1):26–46. doi: 10.1016/j.cell.2013.06.020 PubMedPubMedCentralCrossRefGoogle Scholar
  126. Vance KW, Ponting CP (2014) Transcriptional regulatory functions of nuclear long noncoding RNAs. Trends Genet: TIG 30(8):348–355. doi: 10.1016/j.tig.2014.06.001 PubMedPubMedCentralCrossRefGoogle Scholar
  127. Vicent GP, Nacht AS, Zaurin R, Font-Mateu J, Soronellas D, Le Dily F, Reyes D, Beato M (2013) Unliganded progesterone receptor-mediated targeting of an RNA-containing repressive complex silences a subset of hormone-inducible genes. Genes Dev 27(10):1179–1197. doi: 10.1101/gad.215293.113 PubMedPubMedCentralCrossRefGoogle Scholar
  128. Volders PJ, Helsens K, Wang X, Menten B, Martens L, Gevaert K, Vandesompele J, Mestdagh P (2013) LNCipedia: a database for annotated human lncRNA transcript sequences and structures. Nucleic acids research 41(Database issue):D246–D251. doi: 10.1093/nar/gks915
  129. Walsh AL, Tuzova AV, Bolton EM, Lynch TH, Perry AS (2014) Long noncoding RNAs and prostate carcinogenesis: the missing ‘linc’? Trends Molecul Med 20(8):428–436. doi: 10.1016/j.molmed.2014.03.005 CrossRefGoogle Scholar
  130. Wang D, Garcia-Bassets I, Benner C, Li W, Su X, Zhou Y, Qiu J, Liu W, Kaikkonen MU, Ohgi KA, Glass CK, Rosenfeld MG, Fu XD (2011) Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature 474(7351):390–394. doi: 10.1038/nature10006 PubMedPubMedCentralCrossRefGoogle Scholar
  131. Wang F, Ren S, Chen R, Lu J, Shi X, Zhu Y, Zhang W, Jing T, Zhang C, Shen J, Xu C, Wang H, Wang Y, Liu B, Li Y, Fang Z, Guo F, Qiao M, Wu C, Wei Q, Xu D, Shen D, Lu X, Gao X, Hou J, Sun Y (2014) Development and prospective multicenter evaluation of the long noncoding RNA MALAT-1 as a diagnostic urinary biomarker for prostate cancer. Oncotarget 5(22):11091–11102PubMedPubMedCentralCrossRefGoogle Scholar
  132. West JA, Davis CP, Sunwoo H, Simon MD, Sadreyev RI, Wang PI, Tolstorukov MY, Kingston RE (2014) The long noncoding RNAs NEAT1 and MALAT1 bind active chromatin sites. Mol Cell 55(5):791–802. doi: 10.1016/j.molcel.2014.07.012 PubMedPubMedCentralCrossRefGoogle Scholar
  133. Willingham AT, Gingeras TR (2006) TUF love for “junk” DNA. Cell 125(7):1215–1220. doi: 10.1016/j.cell.2006.06.009 PubMedCrossRefGoogle Scholar
  134. Wilusz JE, Sunwoo H, Spector DL (2009) Long noncoding RNAs: functional surprises from the RNA world. Genes Dev 23(13):1494–1504. doi: 10.1101/gad.1800909 PubMedPubMedCentralCrossRefGoogle Scholar
  135. Xu B, Koenig RJ (2004) An RNA-binding domain in the thyroid hormone receptor enhances transcriptional activation. J Biol Chem 279(32):33051–33056. doi: 10.1074/jbc.M404930200 PubMedCrossRefGoogle Scholar
  136. Xu B, Yang WH, Gerin I, Hu CD, Hammer GD, Koenig RJ (2009) Dax-1 and steroid receptor RNA activator (SRA) function as transcriptional coactivators for steroidogenic factor 1 in steroidogenesis. Mol Cell Biol 29(7):1719–1734. doi: 10.1128/MCB.01010-08 PubMedPubMedCentralCrossRefGoogle Scholar
  137. Xu B, Gerin I, Miao H, Vu-Phan D, Johnson CN, Xu R, Chen XW, Cawthorn WP, MacDougald OA, Koenig RJ (2010) Multiple roles for the non-coding RNA SRA in regulation of adipogenesis and insulin sensitivity. PLoS ONE 5(12):e14199. doi: 10.1371/journal.pone.0014199 PubMedPubMedCentralCrossRefGoogle Scholar
  138. Yang L, Lin C, Jin C, Yang JC, Tanasa B, Li W, Merkurjev D, Ohgi KA, Meng D, Zhang J, Evans CP, Rosenfeld MG (2013) lncRNA-dependent mechanisms of androgen-receptor-regulated gene activation programs. Nature 500(7464):598–602. doi: 10.1038/nature12451 PubMedPubMedCentralCrossRefGoogle Scholar
  139. Yang L, Froberg JE, Lee JT (2014) Long noncoding RNAs: fresh perspectives into the RNA world. Trends Biochem Sci 39(1):35–43. doi: 10.1016/j.tibs.2013.10.002 PubMedPubMedCentralCrossRefGoogle Scholar
  140. Yao H, Brick K, Evrard Y, Xiao T, Camerini-Otero RD, Felsenfeld G (2010) Mediation of CTCF transcriptional insulation by DEAD-box RNA-binding protein p68 and steroid receptor RNA activator SRA. Genes Dev 24(22):2543–2555. doi: 10.1101/gad.1967810 PubMedPubMedCentralCrossRefGoogle Scholar
  141. Ye N, Wang B, Quan ZF, Cao SJ, Wen XT, Huang Y, Huang XB, Wu R, Ma XP, Yan QG (2014) Functional roles of long non-coding RNA in human breast cancer. Asian Pacific J Cancer Prev APJCP 15(15):5993–5997CrossRefGoogle Scholar
  142. Zhao X, Patton JR, Davis SL, Florence B, Ames SJ, Spanjaard RA (2004) Regulation of nuclear receptor activity by a pseudouridine synthase through posttranscriptional modification of steroid receptor RNA activator. Mol Cell 15(4):549–558. doi: 10.1016/j.molcel.2004.06.044
  143. Zhao X, Patton JR, Ghosh SK, Fischel-Ghodsian N, Shen L, Spanjaard RA (2007) Pus3p- and Pus1p-dependent pseudouridylation of steroid receptor RNA activator controls a functional switch that regulates nuclear receptor signaling. Mol Endocrinol 21(3):686–699. doi:  10.1210/me.2006-0414 PubMedCrossRefGoogle Scholar
  144. Zhao W, Luo J, Jiao S (2014a) Comprehensive characterization of cancer subtype associated long non-coding RNAs and their clinical implications. Sci Rep 4:6591. doi: 10.1038/srep06591 PubMedPubMedCentralCrossRefGoogle Scholar
  145. Zhao Z, Chen C, Liu Y, Wu C (2014b) 17beta-Estradiol treatment inhibits breast cell proliferation, migration and invasion by decreasing MALAT-1 RNA level. Biochem Biophys Res Commun 445(2):388–393. doi: 10.1016/j.bbrc.2014.02.006 PubMedCrossRefGoogle Scholar
  146. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31(13):3406–3415PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Charles E. Foulds
    • 1
  • Anil K. Panigrahi
    • 1
  • Cristian Coarfa
    • 1
  • Rainer B. Lanz
    • 1
  • Bert W. O’Malley
    • 1
    Email author
  1. 1.Department of Molecular and Cellular BiologyBaylor College of MedicineHoustonUSA

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