Human cells contain natural double-stranded RNAs with potential regulatory functions

Nature Structural and Molecular Biology

Volumn 22, Issue 1, 2015, Pages 89-97

  Portal, Maximiliano M ^a   Pavet, Valeria ^a   Erb, Cathie ^a   Gronemeyer, Hinrich ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; NUCLEAR PROTEIN; RAN PROTEIN; RCC1 PROTEIN; RIBONUCLEASE III; RNA LIGASE; SINGLE STRANDED RNA; TRANSFER RNA; UNCLASSIFIED DRUG; PROTEIN BINDING;

ARTICLE; BINDING COMPETITION; CELL CYCLE; CELL DEATH; CELL VIABILITY; CELLULAR DISTRIBUTION; CHROMOSOME 8; CHROMOSOME REARRANGEMENT; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DISEASE PREDISPOSITION; EXOSOME; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GEL MOBILITY SHIFT ASSAY; GENE ONTOLOGY; HELA CELL LINE; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MITOSIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN RNA BINDING; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA CONFORMATION; RNA DEGRADATION; RNA INTERFERENCE; RNA PROCESSING; RNA SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; WESTERN BLOTTING; ANIMAL; CELL LINE; CELL NUCLEUS; CHEMISTRY; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS;

MAMMALIA;

ANIMALS; CELL CYCLE; CELL LINE; CELL NUCLEUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEIN BINDING; RNA, DOUBLE-STRANDED; SEQUENCE ANALYSIS, DNA;

EID: 84925286852     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2934     Document Type: Article

References (74)

1. Simons, R.W. Naturally occurring antisense RNA control: a brief review. Gene 72, 35-44 (1988).
2. Wagner, E.G. & Simons, R.W. Antisense RNA control in bacteria, phages, and plasmids. Annu. Rev. Microbiol. 48, 713-742 (1994).
3. Farnham, P.J., Abrams, J.M. & Schimke, R.T. Opposite-strand RNAs from the 5′ flanking region of the mouse dihydrofolate reductase gene. Proc. Natl. Acad. Sci. USA 82, 3978-3982 (1985).
4. Volloch, V. Cytoplasmic synthesis of globin RNA in differentiated murine erythroleukemia cells: possible involvement of RNA-dependent RNA polymerase. Proc. Natl. Acad. Sci. USA 83, 1208-1212 (1986).
5. Williams, T. & Fried, M. A mouse locus at which transcription from both DNA strands produces mRNAs complementary at their 3′ ends. Nature 322, 275-279 (1986).
6. Katayama, S. et al. Antisense transcription in the mammalian transcriptome. Science 309, 1564-1566 (2005).
7. Munroe, S.H. & Lazar, M.A. Inhibition of c-erbA mRNA splicing by a naturally occurring antisense RNA. J. Biol. Chem. 266, 22083-22086 (1991).
8. Hastings, M.L., Milcarek, C., Martincic, K., Peterson, M.L. & Munroe, S.H. Expression of the thyroid hormone receptor gene, erbAalpha, in B lymphocytes: alternative mRNA processing is independent of differentiation but correlates with antisense RNA levels. Nucleic Acids Res. 25, 4296-4300 (1997).
9. Borsani, G. et al. Characterization of a murine gene expressed from the inactive X chromosome. Nature 351, 325-329 (1991).
10. Yu, W. et al. Epigenetic silencing of tumour suppressor gene p15 by its antisense RNA. Nature 451, 202-206 (2008).
11. Li, L.C. et al. Small dsRNAs induce transcriptional activation in human cells. Proc. Natl. Acad. Sci. USA 103, 17337-17342 (2006).
12. Bühler, M. & Moazed, D. Transcription and RNAi in heterochromatic gene silencing. Nat. Struct. Mol. Biol. 14, 1041-1048 (2007).
13. Sleutels, F., Zwart, R. & Barlow, D.P. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 415, 810-813 (2002).
14. Nagano, T. et al. The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science 322, 1717-1720 (2008).
15. Pandey, R.R. et al. Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol. Cell 32, 232-246 (2008).
16. Watanabe, T. et al. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453, 539-543 (2008).
17. Tam, O.H. et al. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453, 534-538 (2008).
18. Matsui, K. et al. Natural antisense transcript stabilizes inducible nitric oxide synthase messenger RNA in rat hepatocytes. Hepatology 47, 686-697 (2008).
19. Ebralidze, A.K. et al. PU.1 expression is modulated by the balance of functional sense and antisense RNAs regulated by a shared cis-regulatory element. Genes Dev. 22, 2085-2092 (2008).
20. Faghihi, M.A. et al. Evidence for natural antisense transcript-mediated inhibition of microRNA function. Genome Biol. 11, R56 (2010).
21. Yin, W., Rossin, A., Clifford, J.L. & Gronemeyer, H. Co-resistance to retinoic acid and TRAIL by insertion mutagenesis into RAM. Oncogene 25, 3735-3744 (2006).
22. Kiemeney, L.A. et al. Sequence variant on 8q24 confers susceptibility to urinary bladder cancer. Nat. Genet. 40, 1307-1312 (2008).
23. Radtke, I. et al. Genomic analysis reveals few genetic alterations in pediatric acute myeloid leukemia. Proc. Natl. Acad. Sci. USA 106, 12944-12949 (2009).
24. Schoemaker, M.J. et al. Interaction between 5 genetic variants and allergy in glioma risk. Am. J. Epidemiol. 171, 1165-1173 (2010).
25. Shete, S. et al. Genome-wide association study identifies five susceptibility loci for glioma. Nat. Genet. 41, 899-904 (2009).
26. Simon, M. et al. Genetic risk profiles identify different molecular etiologies for glioma. Clin. Cancer Res. 16, 5252-5259 (2010).
27. Tomlinson, I. et al. A genome-wide association scan of tag SNPs identifies a susceptibility variant for colorectal cancer at 8q24.21. Nat. Genet. 39, 984-988 (2007).
28. Jenkins, R.B. et al. A low-frequency variant at 8q24.21 is strongly associated with risk of oligodendroglial tumors and astrocytomas with IDH1 or IDH2 mutation. Nat. Genet. 44, 1122-1125 (2012).
29. Guttman, M. & Rinn, J.L. Modular regulatory principles of large non-coding RNAs. Nature 482, 339-346 (2012).
30. Memczak, S. et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495, 333-338 (2013).
31. Mercer, T.R. et al. Targeted RNA sequencing reveals the deep complexity of the human transcriptome. Nat. Biotechnol. 30, 99-104 (2012).
32. Fletcher, O. & Houlston, R.S. Architecture of inherited susceptibility to common cancer. Nat. Rev. Cancer 10, 353-361 (2010).
33. Greenman, C. et al. Patterns of somatic mutation in human cancer genomes. Nature 446, 153-158 (2007).
34. Levin, J.Z. et al. Targeted next-generation sequencing of a cancer transcriptome enhances detection of sequence variants and novel fusion transcripts. Genome Biol. 10, R115 (2009).
35. Hahn, W.C. et al. Creation of human tumour cells with defined genetic elements. Nature 400, 464-468 (1999).
36. Perocchi, F., Xu, Z., Clauder-Munster, S. & Steinmetz, L.M. Antisense artifacts in transcriptome microarray experiments are resolved by actinomycin D. Nucleic Acids Res. 35, e128 (2007).
37. Belostotsky, D. Exosome complex and pervasive transcription in eukaryotic genomes. Curr. Opin. Cell Biol. 21, 352-358 (2009).
38. Flynt, A.S., Greimann, J.C., Chung, W.J., Lima, C.D. & Lai, E.C. MicroRNA biogenesis via splicing and exosome-mediated trimming in Drosophila. Mol. Cell 38, 900-907 (2010).
39. Yang, J.S. & Lai, E.C. Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol. Cell 43, 892-903 (2011).
40. Czech, B. & Hannon, G.J. Small RNA sorting: matchmaking for Argonautes. Nat. Rev. Genet. 12, 19-31 (2011).
41. Djuranovic, S., Nahvi, A. & Green, R. A parsimonious model for gene regulation by miRNAs. Science 331, 550-553 (2011).
42. Clarke, P.R. & Zhang, C. Spatial and temporal coordination of mitosis by Ran GTPase. Nat. Rev. Mol. Cell Biol. 9, 464-477 (2008).
43. Li, H.Y., Ng, W.P., Wong, C.H., Iglesias, P.A. & Zheng, Y. Coordination of chromosome alignment and mitotic progression by the chromosome-based Ran signal. Cell Cycle 6, 1886-1895 (2007).
44. Moore, J.D. The Ran-GTPase and cell-cycle control. BioEssays 23, 77-85 (2001).
45. Huang, S., Mayeda, A., Krainer, A.R. & Spector, D.L. RCC1 and nuclear organization. Mol. Biol. Cell 8, 1143-1157 (1997).
46. Hutchins, J.R. et al. Phosphorylation regulates the dynamic interaction of RCC1 with chromosomes during mitosis. Curr. Biol. 14, 1099-1104 (2004).
47. Joseph, J., Liu, S.T., Jablonski, S.A., Yen, T.J. & Dasso, M. The RanGAP1-RanBP2 complex is essential for microtubule-kinetochore interactions in vivo. Curr. Biol. 14, 611-617 (2004).
48. Hashizume, C., Kobayashi, A. & Wong, R.W. Down-modulation of nucleoporin RanBP2/Nup358 impaired chromosomal alignment and induced mitotic catastrophe. Cell Death Dis. 4, e854 (2013).
49. Joseph, J., Tan, S.H., Karpova, T.S., McNally, J.G. & Dasso, M. SUMO-1 targets RanGAP1 to kinetochores and mitotic spindles. J. Cell Biol. 156, 595-602 (2002).
50. Ho, C.Y., Wong, C.H. & Li, H.Y. Perturbation of the chromosomal binding of RCC1, Mad2 and survivin causes spindle assembly defects and mitotic catastrophe. J. Cell. Biochem. 105, 835-846 (2008).
51. Vakifahmetoglu, H., Olsson, M. & Zhivotovsky, B. Death through a tragedy: mitotic catastrophe. Cell Death Differ. 15, 1153-1162 (2008).
52. Morris, K.V. & Mattick, J.S. The rise of regulatory RNA. Nat. Rev. Genet. 15, 423-437 (2014).
53. Lee, J.T., Davidow, L.S. & Warshawsky, D. Tsix, a gene antisense to Xist at the X-inactivation centre. Nat. Genet. 21, 400-404 (1999).
54. Carninci, P. et al. The transcriptional landscape of the mammalian genome. Science 309, 1559-1563 (2005).
55. Fedoroff, N., Wellauer, P.K. & Wall, R. Intermolecular duplexes in heterogeneous nuclear RNA from HeLa cells. Cell 10, 597-610 (1977).
56. Calvet, J.P. & Pederson, T. Secondary structure of heterogeneous nuclear RNA: two classes of double-stranded RNA in native ribonucleoprotein. Proc. Natl. Acad. Sci. USA 74, 3705-3709 (1977).
57. White, E., Schlackow, M., Kamieniarz-Gdula, K., Proudfoot, N.J. & Gullerova, M. Human nuclear Dicer restricts the deleterious accumulation of endogenous double- stranded RNA. Nat. Struct. Mol. Biol. 21, 552-559 (2014).
58. Tian, B., Bevilacqua, P.C., Diegelman-Parente, A. & Mathews, M.B. The double- stranded-RNA-binding motif: interference and much more. Nat. Rev. Mol. Cell Biol. 5, 1013-1023 (2004).
59. Weber, F., Kochs, G. & Haller, O. Inverse interference: how viruses fight the interferon system. Viral Immunol. 17, 498-515 (2004).
60. Laudet, V. & Gronemeyer, H. The Nuclear Receptor Factsbook (Academic Press, San Diego, 2002).
61. Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515 (2010).
62. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S.L. Ultrafast and memory-efficient alignmeFnt of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
63. Hummel, M., Bonnin, S., Lowy, E. & Roma, G. TEQC: an R package for quality control in target capture experiments. Bioinformatics 27, 1316-1317 (2011).
64. Quinlan, A.R. & Hall, I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842 (2010).
65. Karolchik, D. et al. The UCSC Table Browser data retrieval tool. Nucleic Acids Res. 32, D493-D496 (2004).
66. Karolchik, D. et al. The UCSC Genome Browser database: 2014 update. Nucleic Acids Res. 42, D764-D770 (2014).
67. Karro, J.E. et al. Pseudogene.org: a comprehensive database and comparison platform for pseudogene annotation. Nucleic Acids Res. 35, D55-D60 (2007).
68. Mituyama, T. et al. The Functional RNA Database 3.0: databases to support mining and annotation of functional RNAs. Nucleic Acids Res. 37, D89-D92 (2009).
69. Moison, C., Arimondo, P.B. & Guieysse-Peugeot, A.L. Commercial reverse transcriptase as source of false-positive strand-specific RNA detection in human cells. Biochimie 93, 1731-1737 (2011).
70. Griffiths-Jones, S. The microRNA Registry. Nucleic Acids Res. 32, D109-D111 (2004).
71. Mi, H. & Thomas, P. PANTHER pathway: an ontology-based pathway database coupled with data analysis tools. Methods Mol. Biol. 563, 123-140 (2009).
72. Mi, H. et al. PANTHER version 7: improved phylogenetic trees, orthologs and collaboration with the Gene Ontology Consortium. Nucleic Acids Res. 38, D204-D210 (2010).
73. Raj, A. & Tyagi, S. Detection of individual endogenous RNA transcripts in situ using multiple singly labeled probes. Methods Enzymol. 472, 365-386 (2010).
74. Kimura, H. & Cook, P.R. Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J. Cell Biol. 153, 1341-1353 (2001).