Regulated post-transcriptional RNA cleavage diversifies the eukaryotic transcriptome

Genome Research

Volumn 20, Issue 12, 2010, Pages 1639-1650

  Mercer, Tim R ^a   Dinger, Marcel E ^a   Bracken, Cameron P ^b,c   Kolle, Gabriel ^a   Szubert, Jan M ^b   Korbie, Darren J ^a   Askarian Amiri, Marjan E ^a   Gardiner, Brooke B ^a   Goodall, Gregory J ^b,c   Grimmond, Sean M ^a   Mattick, John S ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b CENTRE FOR CANCER BIOLOGY   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; RNA; RNA POLYMERASE II; TRANSCRIPTOME;

ARTICLE; EUKARYOTE; EXON; GENE EXPRESSION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA CAPPING; RNA CLEAVAGE; RNA SEQUENCE; RNA TRANSCRIPTION; RNA TRANSLATION; TRANSCRIPTION REGULATION;

EPIGENESIS, GENETIC; EUKARYOTA; GENE EXPRESSION PROFILING; GENETIC VARIATION; PEPTIDE HYDROLASES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA;

EUKARYOTA;

EID: 78650051452     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.112128.110     Document Type: Article

References (70)

1. Ahsan B, Saito TL, Hashimoto S, Muramatsu K, Tsuda M, Sasaki A, Matsushima K, Aigaki T, Morishita S. 2009. MachiBase: A Drosophila melanogaster 59-end mRNA transcription database. Nucleic Acids Res 37: D49-D53.
2. Andersson R, Enroth S, Rada-Iglesias A, Wadelius C, Komorowski J. 2009. Nucleosomes are well positioned in exons and carry characteristic histone modifications. Genome Res 19: 1732-1741.
3. Babiarz JE, Ruby JG, Wang Y, Bartel DP, Blelloch R. 2008. Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs. Genes Dev 22: 2773-2785.
4. Badger JH, Olsen GJ. 1999. CRITICA: Coding region identification tool invoking comparative analysis. Mol Biol Evol 16: 512-524.
5. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP. 2008. The impact of microRNAs on protein output. Nature 455: 64-71.
6. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. 2009. MEME SUITE: Tools for motif discovery and searching. Nucleic Acids Res 37: W202-W208.
7. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837. (Pubitemid 46802390)
8. Carninci P. 2006. Tagging mammalian transcription complexity. Trends Genet 22: 501-510.
9. Carninci P, Waki K, Shiraki T, Konno H, Shibata K, Itoh M, Aizawa K, Arakawa T, Ishii Y, Sasaki D, et al. 2003. Targeting a complex transcriptome: The construction of the mouse full-length cDNA encyclopedia. Genome Res 13: 1273-1289.
10. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, et al. 2005. The transcriptional landscape of the mammalian genome. Science 309: 1559-1563.
11. Carninci P, Sandelin A, Lenhard B, Katayama S, Shimokawa K, Ponjavic J, Semple CA, Taylor MS, Engstrom PG, Frith MC, et al. 2006. Genome-wide analysis of mammalian promoter architecture and evolution. Nat Genet 38: 626-635.
12. Cerritelli SM, Crouch RJ. 2009. Ribonuclease H: The enzymes in eukaryotes. FEBS J 276: 1494-1505.
13. Cheng J, Kapranov P, Drenkow J, Dike S, Brubaker S, Patel S, Long J, Stern D, Tammana H, Helt G, et al. 2005. Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution. Science 308: 1149-1154.
14. Chooniedass-Kothari S, Emberley E, Hamedani MK, Troup S, Wang X, Czosnek A, Hube F, Mutawe M, Watson PH, Leygue E. 2004. The steroid receptor RNA activator is the first functional RNA encoding a protein. FEBS Lett 566: 43-47.
15. Clayton C, Shapira M. 2007. Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol Biochem Parasitol 156: 93-101.
16. Cloonan N, Forrest AR, Kolle G, Gardiner BB, Faulkner GJ, Brown MK, Taylor DF, Steptoe AL, Wani S, Bethel G, et al. 2008. Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat Methods 5: 613-619.
17. Cloonan N, Xu Q, Faulkner GJ, Taylor DF, Tang DT, Kolle G, Grimmond SM. 2009. RNA-MATE: A recursive mapping strategy for high-throughput RNA-sequencing data. Bioinformatics 25: 2615-2616.
18. Cole SL, Vassar R. 2008. BACE1 structure and function in health and Alzheimer's disease. Curr Alzheimer Res 5: 100-120.
19. Core LJ, Waterfall JJ, Lis JT. 2008. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322: 1845-1848.
20. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: A sequence logo generator. Genome Res 14: 1188-1190.
21. Czech B, Malone CD, Zhou R, Stark A, Schlingeheyde C, Dus M, Perrimon N, Kellis M, Wohlschlegel JA, Sachidanandam R, et al. 2008. An endogenous small interfering RNA pathway in Drosophila. Nature 453: 798-802.
22. Dinger ME, Pang KC, Mercer TR, Mattick JS. 2008. Differentiating protein-coding and noncoding RNA: Challenges and ambiguities. PLoS Comput Biol 4: e1000176. doi: 10.1371/journal.pcbi.1000176.
23. Eisen MB, Spellman PT, Brown PO, Botstein D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci 95: 14863-14868.
24. Ender C, Krek A, Friedlander MR, Beitzinger M, Weinmann L, Chen W, Pfeffer S, Rajewsky N, Meister G. 2008. A human snoRNA with microRNA-like functions. Mol Cell 32: 519-528.
25. Fejes-Toth K, Sotirova V, Sachidanandam R, Assaf G, Hannon G, Kapranov P, Foissac S, Willingham A, Duttagupta R, Dumais E, et al. 2009. Posttranscriptional processing generates a diversity of 5′-modified long and short RNAs. Nature 457: 1028-1032.
26. German MA, Luo S, Schroth G, Meyers BC, Green PJ. 2009. Construction of parallel analysis of RNA ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome. Nat Protoc 4: 356-362.
27. Glazov EA, Cottee PA, Barris WC, Moore RJ, Dalrymple BP, Tizard ML. 2008. A microRNA catalog of the developing chicken embryo identified by a deep sequencing approach. Genome Res 18: 957-964.
28. Gu M, Lima CD. 2005. Processing the message: Structural insights into capping and decapping mRNA. Curr Opin Struct Biol 15: 99-106.
29. Hashimoto S, Suzuki Y, Kasai Y, Morohoshi K, Yamada T, Sese J, Morishita S, Sugano S, Matsushima K. 2004. 59-End SAGE for the analysis of transcriptional start sites. Nat Biotechnol 22: 1146-1149.
30. Hasselblatt P, Hockenjos B, Thoma C, Blum HE, Offensperger WB. 2005. Translation of stable hepadnaviral mRNA cleavage fragments induced by the action of phosphorothioate-modified antisense oligodeoxynucleotides. Nucleic Acids Res 33: 114-125.
31. Jiao Y, Riechmann JL, Meyerowitz EM. 2008. Transcriptome-wide analysis of uncapped mRNAs in Arabidopsis reveals regulation of mRNA degradation. Plant Cell 20: 2571-2585.
32. Kapranov P, Cawley SE, Drenkow J, Bekiranov S, Strausberg RL, Fodor SP, Gingeras TR. 2002. Large-scale transcriptional activity in chromosomes 21 and 22. Science 296: 916-919.
33. Kapranov P, Drenkow J, Cheng J, Long J, Helt G, Dike S, Gingeras TR. 2005. Examples of the complex architecture of the human transcriptome revealed by RACE and high-density tiling arrays. Genome Res 15: 987-997.
34. Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, Stadler PF, Hertel J, Hackermuller J, Hofacker IL, et al. 2007. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316: 1484-1488.
35. Karginov FV, Cheloufl S, Chong MMW, Stark A, Smith AD, Hannon GJ. 2010. Diverse endonucleolytic cleavage sites in the mammalian transcriptome depend upon microRNAs, Drosha, and additional nucleases. Mol Cell 38: 781-788.
36. 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: 163-171.
37. Kozak M. 1999. Initiation of translation in prokaryotes and eukaryotes. Gene 234: 187-208.
38. Kozak M. 2005. Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene 361: 13-37.
39. Kuhn RM, Karolchik D, Zweig AS, Wang T, Smith KE, Rosenbloom KR, Rhead B, Raney BJ, Pohl A, Pheasant M, et al. 2009. The UCSC Genome Browser Database: Update 2009. Nucleic Acids Res 37: D755-D761.
40. Laslett AL, Grimmond S, Gardiner B, Stamp L, Lin A, Hawes SM, Wormald S, Nikolic-Paterson D, Haylock D, Pera MF. 2007. Transcriptional analysis of early lineage commitment in human embryonic stem cells. BMC Dev Biol 7: 12. doi: 10.1186/1471-213X-7-12.
41. Le Hir H, Izaurralde E, Maquat LE, Moore MJ. 2000. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon- exon junctions. EMBO J 19: 6860-6869.
42. Le Hir H, Gatfield D, Izaurralde E, Moore MJ. 2001. The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J 20: 4987-4997.
43. Lin H, Zhang Z, Zhang MQ, Ma B, Li M. 2008. ZOOM! Zillions of oligos mapped. Bioinformatics 24: 2431-2437.
44. Maeda N, Kasukawa T, Oyama R, Gough J, Frith M, Engstrom PG, Lenhard B, Aturaliya RN, Batalov S, Beisel KW, et al. 2006. Transcript annotation in FANTOM3: Mouse gene catalog based on physical cDNAs. PLoS Genet 2: e62. doi: 10.1371/journal.pgen.0020062.
45. Mangus DA, Evans MC, Jacobson A. 2003. Poly(A)-binding proteins: Multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol 4: 223. doi: 10.1186/gb-2003-4-7-223.
46. Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS. 2008. Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci 105: 716-721.
47. Miura F, Kawaguchi N, Sese J, Toyoda A, Hattori M, Morishita S, Ito T. 2006. A large-scale full-length cDNA analysis to explore the budding yeast transcriptome. Proc Natl Acad Sci 103: 17846-17851.
48. Moore MJ, Proudfoot NJ. 2009. Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136: 688-700.
49. Nahkuri S, Taft RJ, Mattick JS. 2009. Nucleosomes are preferentially positioned at exons in somatic and sperm cells. Cell Cycle 8: 3420-3424.
50. Okamura K, Lai EC. 2008. Endogenous small interfering RNAs in animals. Nat Rev Mol Cell Biol 9: 673-678.
51. Okazaki Y, Furuno M, Kasukawa T, Adachi J, Bono H, Kondo S, Nikaido I, Osato N, Saito R, Suzuki H, et al. 2002. Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 420: 563-573.
52. Otsuka Y, Kedersha NL, Schoenberg DR. 2009. Identification of a cytoplasmic complex that adds a cap onto 5′-monophosphate RNA. Mol Cell Biol 29: 2155-2167.
53. Parkhomchuk D, Borodina T, Amstislavskiy V, Banaru M, Hallen L, Krobitsch S, Lehrach H, Soldatov A. 2009. Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res 37: e123. doi: 10.1093/nar/gkp596.
54. Pruitt KD, Tatusova T, Maglott DR. 2007. NCBI reference sequences (RefSeq): A curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 35: D61-D65.
55. Ruby JG, Jan C, Player C, Axtell MJ, Lee W, Nusbaum C, Ge H, Bartel DP. 2006. Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 127: 1193-1207.
56. Ruby JG, Jan CH, Bartel DP. 2007. Intronic microRNA precursors that bypass Drosha processing. Nature 448: 83-86.
57. Saida F, Odaert B. 2007. RNA recognition and cleavage by sequence-specific endoribonucleases. Protein Pept Lett 14: 103-111.
58. Scarpulla RC. 2008. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev 88: 611-638.
59. Schoenberg DR, Maquat LE. 2009. Re-capping the message. Trends Biochem Sci 34: 435-442.
60. Schwartz S, Meshorer E, Ast G. 2009. Chromatin organization marks exon- intron structure. Nat Struct Mol Biol 16: 990-995.
61. Snider L, Asawachaicharn A, Tyler AE, Geng LN, Petek LM, Maves L, Miller DG, Lemmers RJ, Winokur ST, Tawil R, et al. 2009. RNA transcripts, miRNA-sized fragments and proteins produced from D4Z4 units: New candidates for the pathophysiology of facioscapulohumeral dystrophy. Hum Mol Genet 18: 2414-2430.
62. Spies N, Nielsen CB, Padgett RA, Burge CB. 2009. Biased chromatin signatures around polyadenylation sites and exons. Mol Cell 36: 245-254.
63. Steiger MA, Decker CJ. 2001. New twists in understanding the fate of antisense oligodeoxynucleotide mRNA targets. Mol Cell 8: 732-733.
64. Suzuki H, Forrest AR, van Nimwegen E, Daub CO, Balwierz PJ, Irvine KM, Lassmann T, Ravasi T, Hasegawa Y, de Hoon MJ, et al. 2009. The transcriptional network that controls growth arrest and differentiation in a human myeloid leukemia cell line. Nat Genet 41: 553-562.
65. Taft RJ, Glazov EA, Cloonan N, Simons C, Stephen S, Faulkner GJ, Lassmann T, Forrest AR, Grimmond SM, Schroder K, et al. 2009. Tiny RNAs associated with transcription start sites in animals. Nat Genet 41: 572-578.
66. Thoma C, Hasselblatt P, Kock J, Chang SF, Hockenjos B, Will H, Hentze MW, Blum HE, von Weizsacker F, Offensperger WB. 2001. Generation of stable mRNA fragments and translation of N-truncated proteins induced by antisense oligodeoxynucleotides. Mol Cell 8: 865-872.
67. Tilgner H, Nikolaou C, Althammer S, Sammeth M, Beato M, Valcarcel J, Guigo R. 2009. Nucleosome positioning as a determinant of exon recognition. Nat Struct Mol Biol 16: 996-1001.
68. Valen E, Pascarella G, Chalk A, Maeda N, Kojima M, Kawazu C, Murata M, Nishiyori H, Lazarevic D, Motti D, et al. 2009. Genome-wide detection and analysis of hippocampus core promoters using Deep CAGE. Genome Res 19: 255-265.
69. Walsh CT, Garneau-Tsodikova S, Gatto GJ Jr. 2005. Protein post-translational modifications: The chemistry of proteome diversifications. Angew Chem Int Ed Engl 44: 7342-7372.
70. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. 2008. Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476.