Genome mapping and expression analyses of human intronic noncoding RNAs reveal tissue-specific patterns and enrichment in genes related to regulation of transcription

Genome Biology

Volumn 8, Issue 3, 2007, Pages

  Nakaya, Helder I ^a   Amaral, Paulo P ^a   Louro, Rodrigo ^a   Lopes, André ^a   Fachel, Angela A ^a   Moreira, Yuri B ^a   El Jundi, Tarik A ^a   da Silva, Aline M ^a   Reis, Eduardo M ^a   Verjovski Almeida, Sergio ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

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

ARTICLE; BIOINFORMATICS; CANCER CELL CULTURE; CONTROLLED STUDY; DNA MICROARRAY; ENZYME INHIBITION; EXON; EXPRESSED SEQUENCE TAG; GENE EXPRESSION; GENE LOCUS; GENE MAPPING; GENETIC CORRELATION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRON; KIDNEY; LIVER; MALE; NONHUMAN; PROSTATE; PROSTATE CARCINOMA; RNA SYNTHESIS; RNA TRANSCRIPTION; STATISTICAL SIGNIFICANCE; TISSUE SPECIFICITY; TRANSCRIPTION REGULATION; GENE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GENOME; GENOMICS; METHODOLOGY; TISSUE DISTRIBUTION;

GENE EXPRESSION REGULATION; GENES; GENOME, HUMAN; GENOMICS; HUMANS; INTRONS; RNA, UNTRANSLATED; TISSUE DISTRIBUTION; TRANSCRIPTION, GENETIC;

EID: 34250189924     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2007-8-3-r43     Document Type: Article

References (68)

1. Reis EM Ojopi EP Alberto FL Rahal P Tsukumo F Mancini UM Guimaraes GS Thompson GM Camacho C Miracca E Large-scale transcriptome analyses reveal new genetic marker candidates of head, neck, and thyroid cancer. Cancer Res 2005, 65:1693-1699 10.1158/0008-5472.CAN-04-3506 15753364
2. Ferguson DA Chiang JT Richardson JA Graff J eXPRESSION: An in silico tool to predict patterns of gene expression. Gene Expr Patterns 2005, 5:619-628 10.1016/j.modgep.2005.03.003 15939374
3. Gupta S Zink D Korn B Vingron M Haas SA Genome wide identification and classification of alternative splicing based on EST data. Bioinformatics 2004, 20:2579-2585 10.1093/bioinformatics/bth288 15117759
4. Thanaraj TA Clark F Muilu J Conservation of humanalternative splice events in mouse. Nucleic Acids Res 2003, 31:2544-2552 156037 12736303 10.1093/nar/gkg355
5. Kan Z Rouchka EC Gish WR States DJ Gene structure prediction and alternative splicing analysis using genomically aligned ESTs. Genome Res 2001, 11:889-900 311065 11337482 10.1101/gr.155001
6. Modrek B Lee CJ Alternative splicing in the human, mouse and rat genomes is associated with an increased frequency of exon creation and/or loss. Nat Genet 2003, 34:177-180 10.1038/ng1159 12730695
7. Shendure J Church GM Computational discovery of sense-antisense transcription in the human and mouse genomes. Genome Biol 2002, 3 research0044.1 0044.14 10.1186/gb-2002-3-9-research0044
8. Yelin R Dahary D Sorek R Levanon EY Goldstein O Shoshan A Diber A Biton S Tamir Y Khosravi R Widespread occurrence of antisense transcription in the human genome. Nat Biotechnol 2003, 21:379-386 10.1038/nbt808 12640466
9. Chen J Sun M Kent WJ Huang X Xie H Wang W Zhou G Shi RZ Rowley JD Over 20% of human transcripts might form sense-antisensepairs. Nucleic Acids Res 2004, 32:4812-4820 519112 15356298 10.1093/nar/gkh818
10. Okazaki Y Furuno M Kasukawa T Adachi J Bono H Kondo S Nikaido I Osato N Saito R Suzuki H Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 2002, 420:563-573 10.1038/ nature01266 12466851
11. International Human Genome Sequencing Consortium Finishing the euchromatic sequence of the human genome. Nature 2004, 431:931-945 10.1038/nature03001 15496913
12. Scherer SW Cheung J MacDonald JR Osborne LR Nakabayashi K Herbrick JA Carson AR Parker-Katiraee L Skaug J Khaja R Human chromosome 7: DNA sequence and biology. Science 2003, 300:767-772 10.1126/science.1083423 12690205
13. Pang KC Stephen S Engstrom PG Tajul-Arifin K Chen W Wahlestedt C Lenhard B Hayashizaki Y Mattick JS RNAdb - a comprehensive mammalian noncoding RNA database. Nucleic Acids Res 2005, 33(Database):D125-D130 540043 15608161
14. Griffiths-Jones S Moxon S Marshall M Khanna A Eddy SR Bateman A Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res 2005, 33(Database):D121-124 540035 15608160
15. Goodrich JA Kugel JF Non-coding-RNA regulators of RNA polymerase II transcription. Nat Rev Mol Cell Biol 2006, 7:612-616 10.1038/nrm1946 16723972
16. Khochbin S Lawrence JJ An antisense RNA involved in p53 mRNA maturation in murine erythroleukemia cells induced to differentiate. EMBO J 1989, 8:4107-4114 401592 2480234
17. Yan MD Hong CC Lai GM Cheng AL Lin YW Chuang SE Identification and characterization of a novel gene Saf transcribed from the opposite strand of Fas. Hum Mol Genet 2005, 14:1465-1474 10.1093/hmg/ddi156 15829500
18. Krystal GW Armstrong BC Battey JF N-myc mRNA forms anRNA-RNA duplex with endogenous antisense transcripts. Mol Cell Biol 1990, 10:4180-4191 360949 1695323
19. Reis EM Nakaya HI Louro R Canavez FC Flatschart AV Almeida GT Egidio CM Paquola AC Machado AA Festa F 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
20. Du T Zamore PD microPrimer: The biogenesis and function of microRNA. Development 2005, 132:4645-4652 10.1242/dev.02070 16224044
21. Kiss T Small nucleolar RNAs: An abundant group of noncoding RNAs with diverse cellular functions. Cell 2002, 109:145-148 10.1016/ S0092-8674(02)00718-3 12007400
22. Lu J Getz G Miska EA Alvarez-Saavedra E Lamb J Peck D Sweet-Cordero A Ebert BL Mak RH Ferrando AA MicroRNA expression profiles classify human cancers. Nature 2005, 435:834-838 10.1038/nature03702 15944708
23. Kravchenko JE Rogozin IB Koonin EV Chumakov PM Transcription of mammalian messenger RNAs by a nuclear RNA polymerase of mitochondrial origin. Nature 2005, 436:735-739 1352165 16079853 10.1038/nature03848
24. Dahary D Elroy-Stein O Sorek R Naturally occurring antisense: transcriptional leakage or real overlap? Genome Res 2005, 15:364-368 551562 15710751 10.1101/gr.3308405
25. Kiyosawa H Yamanaka I Osato N Kondo S Hayashizaki Y Antisense transcripts with FANTOM2 clone set and their implications for gene regulation. Genome Res 2003, 13:1324-1334 403655 12819130 10.1101/ gr.982903
26. Iseli C Jongeneel CV Bucher P ESTScan: A program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol 1999, 138-148 10786296
27. Rodriguez A Griffiths-Jones S Ashurst JL Bradley A Identification of mammalian microRNA host genes and transcription units. Genome Res 2004, 14:1902-1910 524413 15364901 10.1101/gr.2722704
28. The snoRNABase http://www-snorna.biotoul.fr/
29. Griffiths-Jones S The microRNA Registry. Nucleic Acids Res 2004, 32(Database):D109-111 308757 14681370 10.1093/nar/gkh023
30. Bertone P Stolc V Royce TE Rozowsky JS Urban AE Zhu X Rinn JL Tongprasit W Samanta M Weissman S Global identification of human transcribed sequences with genome tiling arrays. Science 2004, 306:2242-2246 10.1126/ science.1103388 15539566
31. Hughes TR Mao M Jones AR Burchard J Marton MJ Shannon KW Lefkowitz SM Ziman M Schelter JM Meyer MR Expression profiling using microarrays fabricated by an ink-jet oligonucleotide synthesizer. Nat Biotechnol 2001, 19:342-347 10.1038/86730 11283592
32. Kampa D Cheng J Kapranov P Yamanaka M Brubaker S Cawley S Drenkow J Piccolboni A Bekiranov S Helt G Novel RNAs identified from an in-depth analysis of the transcriptome of human chromosomes 21 and 22. Genome Res 2004, 14:331-342 353210 14993201 10.1101/gr.2094104
33. Kapranov P Drenkow J Cheng J Long J Helt G Dike S Gingeras TR Examples of the complex architecture of the human transcriptome revealed by RACE and high-density tiling arrays. Genome Res 2005, 15:987-997 1172043 15998911 10.1101/gr.3455305
34. Sun BK Deaton AM Lee JT A transient heterochromatic state in Xist preempts X inactivation choice without RNA stabilization. Mol Cell 2006, 21:617-628 10.1016/j.molcel.2006.01.028 16507360
35. 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
36. Tusher VG Tibshirani R Chu G Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001, 98:5116-5121 33173 11309499 10.1073/pnas.091062498
37. Golub TR Slonim DK Tamayo P Huard C Gaasenbeek M Mesirov JP Coller H Loh ML Downing JR Caligiuri MA 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
38. Cheng J Kapranov P Drenkow J Dike S Brubaker S Patel S Long J Stern D Tammana H Helt G Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution. Science 2005, 308:1149-1154 10.1126/ science.1108625 15790807
39. Vinogradov AE Compactness of human housekeeping genes: Selection for economy or genomic design? Trends Genet 2004, 20:248-253 10.1016/ j.tig.2004.03.006 15109779
40. Vinogradov AE "Genome design" model: Evidence from conserved intronic sequence in human-mouse comparison. Genome Res 2006, 16:347-354 1415212 16461636 10.1101/gr.4318206
41. Cancer Genome Anatomy Project (CGAP) http://cgap.nci.nih.gov/
42. Cawley S Bekiranov S Ng HH Kapranov P Sekinger EA Kampa D Piccolboni A Sementchenko V Cheng J Williams AJ Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 2004, 116:499-509 10.1016/ S0092-8674(04)00127-8 14980218
43. Reis EM Louro R Nakaya HI Verjovski-Almeida S As antisense RNA gets intronic. Omics 2005, 9:2-12 10.1089/omi.2005.9.2 15805775
44. Mattick JS Makunin IV Non-coding RNA. Hum Mol Genet 2006, 15(Suppl 1):R17-29 10.1093/hmg/ddl046
45. Sanchez-Elsner T Gou D Kremmer E Sauer F Noncoding RNAs of trithorax response elements recruit Drosophila Ash1 to Ultrabithorax. Science 2006, 311:1118-1123 10.1126/science.1117705 16497925
46. Mayer C Schmitz KM Li J Grummt I Santoro R Intergenic transcripts regulate the epigenetic state of rRNA genes. Mol Cell 2006, 22:351-361 10.1016/j.molcel.2006.03.028 16678107
47. Hill AE Hong JS Wen H Teng L McPherson DT McPherson SA Levasseur DN Sorscher EJ Micro-RNA-like effects of complete intronic sequences. Front Biosci 2006, 11:1998-2006 10.2741/1941 16368574
48. Bruno IG Jin W Cote GJ Correction of aberrant FGFR1 alternative RNA splicing through targeting of intronic regulatory elements. Hum Mol Genet 2004, 13:2409-2420 10.1093/hmg/ddh272 15333583
49. De Angelis FG Sthandier O Berarducci B Toso S Galluzzi G Ricci E Cossu G Bozzoni I Chimeric snRNA molecules carrying antisense sequences against the splice junctions of exon 51 of the dystrophinpre-mRNA induce exon skipping and restoration of a dystrophin synthesis in Delta 48-50 DMD cells. Proc Natl Acad Sci USA 2002, 99:9456-9461 123162 12077324 10.1073/ pnas.142302299
50. McClorey G Fletcher S Wilton S Splicing intervention for Duchenne muscular dystrophy. Curr Opin Pharmacol 2005, 5:529-534 10.1016/ j.coph.2005.06.001 16085461
51. Johnson JM Castle J Garrett-Engele P Kan Z Loerch PM Armour CD Santos R Schadt EE Stoughton R Shoemaker DD Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 2003, 302:2141-2144 10.1126/science.1090100 14684825
52. Clark F Thanaraj TA Categorization and characterization of transcript-confirmed constitutively and alternatively spliced introns and exons from human. Hum Mol Genet 2002, 11:451-464 10.1093/hmg/ 11.4.451 11854178
53. Prescott EM Proudfoot NJ Transcriptional collision between convergent genes in budding yeast. Proc Natl Acad Sci USA 2002, 99:8796-8801 124378 12077310 10.1073/pnas.132270899
54. Martens JA Laprade L Winston F Intergenic transcription is required to repress the Saccharomyces cerevisiae SER3 gene. Nature 2004, 429:571-574 10.1038/nature02538 15175754
55. Geirsson A Lynch RJ Paliwal I Bothwell AL Hammond GL Human trophoblast noncoding RNA suppresses CIITA promoter III activity in murine B-lymphocytes. Biochem Biophys Res Commun 2003, 301:718-724 10.1016/ S0006-291X(03)00028-7 12565840
56. Willingham AT Orth AP Batalov S Peters EC Wen BG Aza-Blanc P Hogenesch JB Schultz PG A strategy for probing the function of noncoding RNAs finds a repressor of NFAT. Science 2005, 309:1570-1573 10.1126/ science.1115901 16141075
57. Mattick JS RNA regulation: A new genetics? Nat Rev Genet 2004, 5:316-323 10.1038/nrg1321 15131654
58. Kapranov P Cawley SE Drenkow J Bekiranov S Strausberg RL Fodor SP Gingeras TR Large-scale transcriptional activity in chromosomes 21 and 22. Science 2002, 296:916-919 10.1126/science.1068597 11988577
59. Rinn JL Euskirchen G Bertone P Martone R Luscombe NM Hartman S Harrison PM Nelson FK Miller P Gerstein M The transcriptional activity of human chromosome 22. Genes Dev 2003, 17:529-540 195998 12600945 10.1101/ gad.1055203
60. Bejerano G Pheasant M Makunin I Stephen S Kent WJ Mattick JS Haussler D Ultraconserved elements in the human genome. Science 2004, 304:1321-1325 10.1126/science.1098119 15131266
61. Sironi M Menozzi G Comi GP Cagliani R Bresolin N Pozzoli U Analysis of intronic conserved elements indicates that functional complexity might represent a major source of negative selection on non-coding sequences. Hum Mol Genet 2005, 14:2533-2546 10.1093/hmg/ddi257 16037065
62. Pollard KS Salama SR Lambert N Lambot MA Coppens S Pedersen JS Katzman S King B Onodera C Siepel A An RNA gene expressed during cortical development evolved rapidly in humans. Nature 2006, 443:167-172 10.1038/ nature05113 16915236
63. Rigoutsos I Huynh T Miranda K Tsirigos A McHardy A Platt D Short blocks from the noncoding parts of the human genome have instances within nearly all known genes and relate to biological processes. Proc Natl Acad Sci USA 2006, 103:6605-6610 1447521 16636294 10.1073/pnas.0601688103
64. Simons C Pheasant M Makunin IV Mattick JS Transposon-free regions in mammalian genomes. Genome Res 2006, 16:164-172 1361711 16365385 10.1101/ gr.4624306
65. UCSC Genome Browser http://genome.ucsc.edu
66. Peixoto BR Vencio RZ Egidio CM Mota-Vieira L Verjovski-Almeida S Reis EM Evaluation of reference-based two-color methods for measurement of gene expression ratios using spotted cDNA microarrays. BMC Genomics 2006, 7:35 1402275 16504121 10.1186/1471-2164-7-35
67. The R Project for Statistical Computing http://www.r-project.org
68. Shannon P Markiel A Ozier O Baliga NS Wang JT Ramage D Amin N Schwikowski B Ideker T Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res 2003, 13:2498-2504 403769 14597658 10.1101/gr.1239303