Expression analysis and in silico characterization of intronic long noncoding RNAs in renal cell carcinoma: Emerging functional associations

Molecular Cancer

Volumn 12, Issue 1, 2013, Pages

  Fachel, Angela A ^a   Tahira, Ana C ^a   Vilella Arias, Santiago A ^a   Maracaja Coutinho, Vinicius ^a   Gimba, Etel R P ^b,c   Vignal, Giselle M ^c   Campos, Franz S ^c   Reis, Eduardo M ^a,d   Verjovski Almeida, Sergio ^a,d  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

^c INSTITUTO NACIONAL DE CÂNCER   (Brazil)

^d Instituto Nacional de Ciencia e Tecnologia   (Brazil)

Author keywords

Antisense lncRNAs; Evolutionary lncRNA conservation; Gene expression correlation; Histone acetylation; Histone methylation; Microarray analysis; Molecular markers; Renal cell carcinoma (RCC); Unspliced intronic long noncoding RNAs

Indexed keywords

COMPLEMENTARY RNA; LONG UNTRANSLATED RNA; MESSENGER RNA; RNA POLYMERASE II;

ADULT; ARTICLE; CANCER SURVIVAL; CANCER TISSUE; CONTROLLED STUDY; CPG ISLAND; EPIGENETICS; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE LOCUS; GENE MAPPING; GENE REGULATORY NETWORK; GENETIC ASSOCIATION; HISTONE ACETYLATION; HISTONE METHYLATION; HUMAN; HUMAN TISSUE; INTRON; KIDNEY CARCINOMA; KIDNEY PARENCHYMA; LIVER; MALE; MALIGNANT TRANSFORMATION; META ANALYSIS (TOPIC); MICROARRAY ANALYSIS; MOLECULAR PATHOLOGY; NUCLEOTIDE SEQUENCE; PRIMARY TUMOR; PROMOTER REGION; PROSTATE TUMOR; RNA PROBE; RNA SEQUENCE; TRANSCRIPTION INITIATION SITE; UNINDEXED SEQUENCE;

BASE SEQUENCE; CARCINOMA, RENAL CELL; COMPUTER SIMULATION; HUMANS; INTRONS; KIDNEY NEOPLASMS; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; ORGAN SPECIFICITY; RNA, LONG NONCODING; TRANSCRIPTOME;

EID: 84887512740     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-12-140     Document Type: Article

References (101)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013, 63:11-30. 10.3322/caac.21166, 23335087.
2. Purdue MP, Moore LE, Merino MJ, Boffetta P, Colt JS, Schwartz KL, Bencko V, Davis FG, Graubard BI, Janout V, et al. An investigation of risk factors for renal cell carcinoma by histologic subtype in two case-control studies. Int J Cancer 2013, 132:2640-2647. 10.1002/ijc.27934, 23150424.
3. Eichelberg C, Junker K, Ljungberg B, Moch H. Diagnostic and prognostic molecular markers for renal cell carcinoma: a critical appraisal of the current state of research and clinical applicability. Eur Urol 2009, 55:851-863. 10.1016/j.eururo.2009.01.003, 19155123.
4. Vasudev NS, Selby PJ, Banks RE. Renal cancer biomarkers: the promise of personalized care. BMC Med 2012, 10:112. 10.1186/1741-7015-10-112, 3521191, 23016578.
5. Skubitz KM, Skubitz AP. Differential gene expression in renal-cell cancer. J Lab Clin Med 2002, 140:52-64. 10.1067/mlc.2002.125213, 12080328.
6. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, et al. Landscape of transcription in human cells. Nature 2012, 489:101-108. 10.1038/nature11233, 3684276, 22955620.
7. Kugel JF, Goodrich JA. Non-coding RNAs: key regulators of mammalian transcription. Trends Biochem Sci 2012, 37:144-151. 10.1016/j.tibs.2011.12.003, 3323709, 22300815.
8. Consortium EP, Bernstein BE, Birney E, Dunham I, Green ED, Gunter C, Snyder M. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74. 10.1038/nature11247, 3439153, 22955616.
9. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 2012, 22:1775-1789. 10.1101/gr.132159.111, 3431493, 22955988.
10. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, et al. MicroRNA expression profiles classify human cancers. Nature 2005, 435:834-838. 10.1038/nature03702, 15944708.
11. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer 2006, 6:857-866. 10.1038/nrc1997, 17060945.
12. Nakada C, Matsuura K, Tsukamoto Y, Tanigawa M, Yoshimoto T, Narimatsu T, Nguyen LT, Hijiya N, Uchida T, Sato F, et al. Genome-wide microRNA expression profiling in renal cell carcinoma: significant down-regulation of miR-141 and miR-200c. J Pathol 2008, 216:418-427. 10.1002/path.2437, 18925646.
13. Huang Y, Dai Y, Yang J, Chen T, Yin Y, Tang M, Hu C, Zhang L. Microarray analysis of microRNA expression in renal clear cell carcinoma. Eur J Surg Oncol 2009, 35:1119-1123. 10.1016/j.ejso.2009.04.010, 19443172.
14. Jung M, Mollenkopf HJ, Grimm C, Wagner I, Albrecht M, Waller T, Pilarsky C, Johannsen M, Stephan C, Lehrach H, et al. MicroRNA profiling of clear cell renal cell cancer identifies a robust signature to define renal malignancy. J Cell Mol Med 2009, 13:3918-3928. 10.1111/j.1582-4934.2009.00705.x, 19228262.
15. Chow TF, Youssef YM, Lianidou E, Romaschin AD, Honey RJ, Stewart R, Pace KT, Yousef GM. Differential expression profiling of microRNAs and their potential involvement in renal cell carcinoma pathogenesis. Clin Biochem 2010, 43:150-158. 10.1016/j.clinbiochem.2009.07.020, 19646430.
16. Juan D, Alexe G, Antes T, Liu H, Madabhushi A, Delisi C, Ganesan S, Bhanot G, Liou LS. Identification of a microRNA panel for clear-cell kidney cancer. Urology 2010, 75:835-841. 10.1016/j.urology.2009.10.033, 20035975.
17. Weng L, Wu X, Gao H, Mu B, Li X, Wang JH, Guo C, Jin JM, Chen Z, Covarrubias M, et al. MicroRNA profiling of clear cell renal cell carcinoma by whole-genome small RNA deep sequencing of paired frozen and formalin-fixed, paraffin-embedded tissue specimens. J Pathol 2010, 222:41-51.
18. Osanto S, Qin Y, Buermans HP, Berkers J, Lerut E, Goeman JJ, van Poppel H. Genome-wide microRNA expression analysis of clear cell renal cell carcinoma by next generation deep sequencing. PLoS One 2012, 7:e38298. 10.1371/journal.pone.0038298, 3380046, 22745662.
19. Fridman E, Dotan Z, Barshack I, David MB, Dov A, Tabak S, Zion O, Benjamin S, Benjamin H, Kuker H, et al. Accurate molecular classification of renal tumors using microRNA expression. J Mol Diagn 2010, 12:687-696. 10.2353/jmoldx.2010.090187, 2928434, 20595629.
20. Petillo D, Kort EJ, Anema J, Furge KA, Yang XJ, Teh BT. MicroRNA profiling of human kidney cancer subtypes. Int J Oncol 2009, 35:109-114.
21. Wu X, Weng L, Li X, Guo C, Pal SK, Jin JM, Li Y, Nelson RA, Mu B, Onami SH, et al. Identification of a 4-microRNA signature for clear cell renal cell carcinoma metastasis and prognosis. PLoS One 2012, 7:e35661. 10.1371/journal.pone.0035661, 3356334, 22623952.
22. Gutschner T, Diederichs S. The hallmarks of cancer: a long non-coding RNA point of view. RNA Biol 2012, 9:703-719. 10.4161/rna.20481, 3495743, 22664915.
23. Mitra SA, Mitra AP, Triche TJ. A central role for long non-coding RNA in cancer. Front Genet 2012, 3:17. 3279698, 22363342.
24. Reis EM, Verjovski-Almeida S. Perspectives of long non-coding RNAs in cancer diagnostics. Front Genet 2012, 3:32. 3297063, 22408643.
25. Prensner JR, Chinnaiyan AM. The emergence of lncRNAs in cancer biology. Cancer Discov 2011, 1:391-407. 10.1158/2159-8290.CD-11-0209, 3215093, 22096659.
26. Spizzo R, Almeida MI, Colombatti A, Calin GA. Long non-coding RNAs and cancer: a new frontier of translational research?. Oncogene 2012, 31:4577-4587. 10.1038/onc.2011.621, 3433647, 22266873.
27. Gibb EA, Brown CJ, Lam WL. The functional role of long non-coding RNA in human carcinomas. Mol Cancer 2011, 10:38. 10.1186/1476-4598-10-38, 3098824, 21489289.
28. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 2011, 25:1915-1927. 10.1101/gad.17446611, 3185964, 21890647.
29. Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A 2009, 106:11667-11672. 10.1073/pnas.0904715106, 2704857, 19571010.
30. Ulitsky I, Bartel DP. lincRNAs: genomics, evolution, and mechanisms. Cell 2013, 154:26-46. 10.1016/j.cell.2013.06.020, 23827673.
31. Brunner AL, Beck AH, Edris B, Sweeney RT, Zhu SX, Li R, Montgomery K, Varma S, Gilks T, Guo X, et al. Transcriptional profiling of lncRNAs and novel transcribed regions across a diverse panel of archived human cancers. Genome Biol 2012, 13:R75. 10.1186/gb-2012-13-8-r75, 22929540.
32. Prensner JR, Iyer MK, Balbin OA, Dhanasekaran SM, Cao Q, Brenner JC, Laxman B, Asangani IA, Grasso CS, Kominsky HD, et al. Transcriptome sequencing across a prostate cancer cohort identifies PCAT-1, an unannotated lincRNA implicated in disease progression. Nat Biotechnol 2011, 29:742-749. 10.1038/nbt.1914, 3152676, 21804560.
33. Ji P, Diederichs S, Wang W, Boing S, Metzger R, Schneider PM, Tidow N, Brandt B, Buerger H, Bulk E, et al. MALAT-1, a novel noncoding RNA, and thymosin beta4 predict metastasis and survival in early-stage non-small cell lung cancer. Oncogene 2003, 22:8031-8041. 10.1038/sj.onc.1206928, 12970751.
34. Lin R, Maeda S, Liu C, Karin M, Edgington TS. A large noncoding RNA is a marker for murine hepatocellular carcinomas and a spectrum of human carcinomas. Oncogene 2007, 26:851-858. 10.1038/sj.onc.1209846, 16878148.
35. Argani P, Yonescu R, Morsberger L, Morris K, Netto GJ, Smith N, Gonzalez N, Illei PB, Ladanyi M, Griffin CA. Molecular confirmation of t(6;11)(p21;q12) renal cell carcinoma in archival paraffin-embedded material using a break-apart TFEB FISH assay expands its clinicopathologic spectrum. Am J Surg Pathol 2012, 36:1516-1526. 10.1097/PAS.0b013e3182613d8f, 22892601.
36. Davis IJ, Hsi BL, Arroyo JD, Vargas SO, Yeh YA, Motyckova G, Valencia P, Perez-Atayde AR, Argani P, Ladanyi M, et al. Cloning of an alpha-TFEB fusion in renal tumors harboring the t(6;11)(p21;q13) chromosome translocation. Proc Natl Acad Sci U S A 2003, 100:6051-6056. 10.1073/pnas.0931430100, 156324, 12719541.
37. Yildirim E, Kirby JE, Brown DE, Mercier FE, Sadreyev RI, Scadden DT, Lee JT. Xist RNA is a potent suppressor of hematologic cancer in mice. Cell 2013, 152:727-742. 10.1016/j.cell.2013.01.034, 23415223.
38. St Laurent G, Shtokalo D, Tackett MR, Yang Z, Eremina T, Wahlestedt C, Urcuqui-Inchima S, Seilheimer B, McCaffrey TA, Kapranov P. Intronic RNAs constitute the major fraction of the non-coding RNA in mammalian cells. BMC Genomics 2012, 13:504. 10.1186/1471-2164-13-504, 3507791, 23006825.
39. Rearick D, Prakash A, McSweeny A, Shepard SS, Fedorova L, Fedorov A. Critical association of ncRNA with introns. Nucleic Acids Res 2011, 39:2357-2366. 10.1093/nar/gkq1080, 3064772, 21071396.
40. Nakaya HI, Amaral PP, Louro R, Lopes A, Fachel AA, Moreira YB, El-Jundi TA, da Silva AM, Reis EM, Verjovski-Almeida S. Genome mapping and expression analyses of human intronic noncoding RNAs reveal tissue-specific patterns and enrichment in genes related to regulation of transcription. Genome Biol 2007, 8:R43. 10.1186/gb-2007-8-3-r43, 1868932, 17386095.
41. Consortium EP, Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007, 447:799-816. 10.1038/nature05874, 2212820, 17571346.
42. Guil S, Soler M, Portela A, Carrere J, Fonalleras E, Gomez A, Villanueva A, Esteller M. Intronic RNAs mediate EZH2 regulation of epigenetic targets. Nat Struct Mol Biol 2012, 19:664-670. 10.1038/nsmb.2315, 22659877.
43. Beckedorff FC, Ayupe AC, Crocci-Souza R, Amaral MS, Nakaya HI, Soltys DT, Menck CF, Reis EM, Verjovski-Almeida S. The intronic long noncoding RNA ANRASSF1 recruits PRC2 to the RASSF1A promoter, reducing the expression of RASSF1A and increasing cell proliferation. PLoS Genet 2013, 9:e1003705. 10.1371/journal.pgen.1003705, 3749938, 23990798.
44. Takayama K, Horie-Inoue K, Katayama S, Suzuki T, Tsutsumi S, Ikeda K, Urano T, Fujimura T, Takagi K, Takahashi S, et al. Androgen-responsive long noncoding RNA CTBP1-AS promotes prostate cancer. EMBO J 2013, 32:1665-1680. 10.1038/emboj.2013.99, 23644382.
45. Reis EM, Nakaya HI, Louro R, Canavez FC, Flatschart AV, Almeida GT, Egidio CM, Paquola AC, Machado AA, Festa F, et al. Antisense intronic non-coding RNA levels correlate to the degree of tumor differentiation in prostate cancer. Oncogene 2004, 23:6684-6692. 10.1038/sj.onc.1207880, 15221013.
46. Tahira AC, Kubrusly MS, Faria MF, Dazzani B, Fonseca RS, Maracaja-Coutinho V, Verjovski-Almeida S, Machado MC, Reis EM. Long noncoding intronic RNAs are differentially expressed in primary and metastatic pancreatic cancer. Mol Cancer 2011, 10:141. 10.1186/1476-4598-10-141, 3225313, 22078386.
47. Silveira RA, Fachel AA, Moreira YB, De Souza CA, Costa FF, Verjovski-Almeida S, Pagnano KB. Protein-coding genes and long noncoding RNAs are differentially expressed in dasatinib-treated chronic myeloid leukemia patients with resistance to imatinib. Hematology 2013, doi:10.1179/1607845413Y.0000000094.
48. Perez DS, Hoage TR, Pritchett JR, Ducharme-Smith AL, Halling ML, Ganapathiraju SC, Streng PS, Smith DI. Long, abundantly expressed non-coding transcripts are altered in cancer. Hum Mol Genet 2008, 17:642-655.
49. Brito GC, Fachel AA, Vettore AL, Vignal GM, Gimba ER, Campos FS, Barcinski MA, Verjovski-Almeida S, Reis EM. Identification of protein-coding and intronic noncoding RNAs down-regulated in clear cell renal carcinoma. Mol Carcinog 2008, 47:757-767. 10.1002/mc.20433, 18348187.
50. Yu G, Yao W, Wang J, Ma X, Xiao W, Li H, Xia D, Yang Y, Deng K, Xiao H, et al. LncRNAs expression signatures of renal clear cell carcinoma revealed by microarray. PLoS One 2012, 7:e42377. 10.1371/journal.pone.0042377, 3412851, 22879955.
51. Dupuy A, Simon RM. Critical review of published microarray studies for cancer outcome and guidelines on statistical analysis and reporting. J Natl Cancer Inst 2007, 99:147-157. 10.1093/jnci/djk018, 17227998.
52. Takahashi M, Rhodes DR, Furge KA, Kanayama H, Kagawa S, Haab BB, Teh BT. Gene expression profiling of clear cell renal cell carcinoma: gene identification and prognostic classification. Proc Natl Acad Sci U S A 2001, 98:9754-9759. 10.1073/pnas.171209998, 55525, 11493696.
53. Liou LS, Shi T, Duan ZH, Sadhukhan P, Der SD, Novick AA, Hissong J, Skacel M, Almasan A, DiDonato JA. Microarray gene expression profiling and analysis in renal cell carcinoma. BMC Urol 2004, 4:9. 10.1186/1471-2490-4-9, 442130, 15212686.
54. Lenburg ME, Liou LS, Gerry NP, Frampton GM, Cohen HT, Christman MF. Previously unidentified changes in renal cell carcinoma gene expression identified by parametric analysis of microarray data. BMC Cancer 2003, 3:31. 10.1186/1471-2407-3-31, 317310, 14641932.
55. Jones J, Otu H, Spentzos D, Kolia S, Inan M, Beecken WD, Fellbaum C, Gu X, Joseph M, Pantuck AJ, et al. Gene signatures of progression and metastasis in renal cell cancer. Clin Cancer Res 2005, 11:5730-5739. 10.1158/1078-0432.CCR-04-2225, 16115910.
56. Higgins JP, Shinghal R, Gill H, Reese JH, Terris M, Cohen RJ, Fero M, Pollack JR, van de Rijn M, Brooks JD. Gene expression patterns in renal cell carcinoma assessed by complementary DNA microarray. Am J Pathol 2003, 162:925-932. 10.1016/S0002-9440(10)63887-4, 1868114, 12598325.
57. Gumz ML, Zou H, Kreinest PA, Childs AC, Belmonte LS, LeGrand SN, Wu KJ, Luxon BA, Sinha M, Parker AS, et al. Secreted frizzled-related protein 1 loss contributes to tumor phenotype of clear cell renal cell carcinoma. Clin Cancer Res 2007, 13:4740-4749. 10.1158/1078-0432.CCR-07-0143, 17699851.
58. Beroukhim R, Brunet JP, Di Napoli A, Mertz KD, Seeley A, Pires MM, Linhart D, Worrell RA, Moch H, Rubin MA, et al. Patterns of gene expression and copy-number alterations in von-hippel lindau disease-associated and sporadic clear cell carcinoma of the kidney. Cancer Res 2009, 69:4674-4681. 10.1158/0008-5472.CAN-09-0146, 2745239, 19470766.
59. Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, Zhang X, Wang L, Issner R, Coyne M, et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 2011, 473:43-49. 10.1038/nature09906, 3088773, 21441907.
60. Bernstein BE, Stamatoyannopoulos JA, Costello JF, Ren B, Milosavljevic A, Meissner A, Kellis M, Marra MA, Beaudet AL, Ecker JR, et al. The NIH roadmap epigenomics mapping consortium. Nat Biotechnol 2010, 28:1045-1048. 10.1038/nbt1010-1045, 3607281, 20944595.
61. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, Clawson H, Spieth J, Hillier LW, Richards S, et al. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 2005, 15:1034-1050. 10.1101/gr.3715005, 1182216, 16024819.
62. Lestrade L, Weber MJ. snoRNA-LBME-db, a comprehensive database of human H/ACA and C/D box snoRNAs. Nucleic Acids Res 2006, 34:D158-D162. 10.1093/nar/gkj002, 1347365, 16381836.
63. Kozomara A, Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011, 39:D152-D157. 10.1093/nar/gkq1027, 3013655, 21037258.
64. Kong L, Zhang Y, Ye ZQ, Liu XQ, Zhao SQ, Wei L, Gao G. CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 2007, 35:W345-W349. 10.1093/nar/gkm391, 1933232, 17631615.
65. Consortium EP. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol 2011, 9:e1001046. 10.1371/journal.pbio.1001046, 3079585, 21526222.
66. Bock C, Walter J, Paulsen M, Lengauer T. CpG island mapping by epigenome prediction. PLoS Comput Biol 2007, 3:e110. 10.1371/journal.pcbi.0030110, 1892605, 17559301.
67. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448:553-560. 10.1038/nature06008, 2921165, 17603471.
68. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. Alternative isoform regulation in human tissue transcriptomes. Nature 2008, 456:470-476. 10.1038/nature07509, 2593745, 18978772.
69. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5:621-628. 10.1038/nmeth.1226, 18516045.
70. Zhu J, Sanborn JZ, Diekhans M, Lowe CB, Pringle TH, Haussler D. Comparative genomics search for losses of long-established genes on the human lineage. PLoS Comput Biol 2007, 3:e247. 10.1371/journal.pcbi.0030247, 2134963, 18085818.
71. Gruber AR, Neubock R, Hofacker IL, Washietl S. The RNAz web server: prediction of thermodynamically stable and evolutionarily conserved RNA structures. Nucleic Acids Res 2007, 35:W335-W338. 10.1093/nar/gkm222, 1933143, 17452347.
72. Molinaro AM, Simon R, Pfeiffer RM. Prediction error estimation: a comparison of resampling methods. Bioinformatics 2005, 21:3301-3307. 10.1093/bioinformatics/bti499, 15905277.
73. Slaby O, Redova M, Poprach A, Nekvindova J, Iliev R, Radova L, Lakomy R, Svoboda M, Vyzula R. Identification of MicroRNAs associated with early relapse after nephrectomy in renal cell carcinoma patients. Genes Chromosomes Cancer 2012, 51:707-716. 10.1002/gcc.21957, 22492545.
74. Mourtada-Maarabouni M, Pickard MR, Hedge VL, Farzaneh F, Williams GT. GAS5, a non-protein-coding RNA, controls apoptosis and is downregulated in breast cancer. Oncogene 2009, 28:195-208. 10.1038/onc.2008.373, 18836484.
75. Pickard MR, Mourtada-Maarabouni M, Williams GT. Long non-coding RNA GAS5 regulates apoptosis in prostate cancer cell lines. Biochim Biophys Acta 2013, 1832:1613-1623. 10.1016/j.bbadis.2013.05.005, 23676682.
76. Qiao HP, Gao WS, Huo JX, Yang ZS. Long non-coding RNA GAS5 functions as a tumor suppressor in renal cell carcinoma. Asian Pac J Cancer Prev 2013, 14:1077-1082. 10.7314/APJCP.2013.14.2.1077, 23621190.
77. Bertozzi D, Iurlaro R, Sordet O, Marinello J, Zaffaroni N, Capranico G. Characterization of novel antisense HIF-1alpha transcripts in human cancers. Cell Cycle 2011, 10:3189-3197. 10.4161/cc.10.18.17183, 21897117.
78. Beckedorff FC, Amaral MS, Deocesano-Pereira C, Verjovski-Almeida S. Long non-coding RNAs and their implications in cancer epigenetics. Biosci Rep 2013, 33:667-675.
79. Redrup L, Branco MR, Perdeaux ER, Krueger C, Lewis A, Santos F, Nagano T, Cobb BS, Fraser P, Reik W. The long noncoding RNA Kcnq1ot1 organises a lineage-specific nuclear domain for epigenetic gene silencing. Development 2009, 136:525-530. 10.1242/dev.031328, 2685953, 19144718.
80. Yang F, Huo XS, Yuan SX, Zhang L, Zhou WP, Wang F, Sun SH. Repression of the long noncoding RNA-LET by histone deacetylase 3 contributes to hypoxia-mediated metastasis. Mol Cell 2013, 49:1083-1096. 10.1016/j.molcel.2013.01.010, 23395002.
81. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009, 459:108-112. 10.1038/nature07829, 2910248, 19295514.
82. Mercer TR, Dinger ME, Mattick JS. Long non-coding RNAs: insights into functions. Nat Rev Genet 2009, 10:155-159. 10.1038/nrg2521, 19188922.
83. Louro R, Smirnova AS, Verjovski-Almeida S. Long intronic noncoding RNA transcription: expression noise or expression choice?. Genomics 2009, 93:291-298. 10.1016/j.ygeno.2008.11.009, 19071207.
84. Wang KC, Chang HY. Molecular mechanisms of long noncoding RNAs. Mol Cell 2011, 43:904-914. 10.1016/j.molcel.2011.08.018, 3199020, 21925379.
85. Louro R, El-Jundi T, Nakaya HI, Reis EM, Verjovski-Almeida S. Conserved tissue expression signatures of intronic noncoding RNAs transcribed from human and mouse loci. Genomics 2008, 92:18-25. 10.1016/j.ygeno.2008.03.013, 18495418.
86. Pang KC, Frith MC, Mattick JS. Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of function. Trends Genet 2006, 22:1-5. 10.1016/j.tig.2005.10.003, 16290135.
87. Dinger ME, Amaral PP, Mercer TR, Pang KC, Bruce SJ, Gardiner BB, Askarian-Amiri ME, Ru K, Solda G, Simons C, et al. Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res 2008, 18:1433-1445. 10.1101/gr.078378.108, 2527704, 18562676.
88. Brentani H, Caballero OL, Camargo AA, da Silva AM, da Silva WA, Dias Neto E, Grivet M, Gruber A, Guimaraes PE, Hide W, et al. The generation and utilization of a cancer-oriented representation of the human transcriptome by using expressed sequence tags. Proc Natl Acad Sci U S A 2003, 100:13418-13423. 10.1073/pnas.1233632100, 263829, 14593198.
89. Wang E, Miller LD, Ohnmacht GA, Liu ET, Marincola FM. High-fidelity mRNA amplification for gene profiling. Nat Biotechnol 2000, 18:457-459. 10.1038/74546, 10748532.
90. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003, 19:185-193. 10.1093/bioinformatics/19.2.185, 12538238.
91. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 2001, 98:5116-5121. 10.1073/pnas.091062498, 33173, 11309499.
92. van 't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002, 415:530-536. 10.1038/415530a, 11823860.
93. Golub TR, Slonim DK, Tamayo P, Huard C, Gaasenbeek M, Mesirov JP, Coller H, Loh ML, Downing JR, Caligiuri MA, et al. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 1999, 286:531-537. 10.1126/science.286.5439.531, 10521349.
94. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45. 10.1093/nar/29.9.e45, 55695, 11328886.
95. Maere S, Heymans K, Kuiper M. BiNGO: a cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 2005, 21:3448-3449. 10.1093/bioinformatics/bti551, 15972284.
96. Segal E, Friedman N, Koller D, Regev A. A module map showing conditional activity of expression modules in cancer. Nat Genet 2004, 36:1090-1098. 10.1038/ng1434, 15448693.
97. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842. 10.1093/bioinformatics/btq033, 2832824, 20110278.
98. Kodzius R, Kojima M, Nishiyori H, Nakamura M, Fukuda S, Tagami M, Sasaki D, Imamura K, Kai C, Harbers M, et al. CAGE: cap analysis of gene expression. Nat Methods 2006, 3:211-222. 10.1038/nmeth0306-211, 16489339.
99. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111. 10.1093/bioinformatics/btp120, 2672628, 19289445.
100. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010, 28:511-515. 10.1038/nbt.1621, 3146043, 20436464.
101. Marques AC, Ponting CP. Catalogues of mammalian long noncoding RNAs: modest conservation and incompleteness. Genome Biol 2009, 10:R124. 10.1186/gb-2009-10-11-r124, 3091318, 19895688.