Home LiteratureArticle Details
PMID: 23498938 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Review

Long noncoding RNAs: cellular address codes in development and disease.

Cell ·Vol. 152 ·No. 6 ·2013-03-14 ·Pages 1298-307

Batista PJ, Chang HY

Abstract

In biology as in real estate, location is a cardinal organizational principle that dictates the accessibility and flow of informational traffic. An essential question in nuclear organization is the nature of the address code--how objects are placed and later searched for and retrieved. Long noncoding RNAs (lncRNAs) have emerged as key components of the address code, allowing protein complexes, genes, and chromosomes to be trafficked to appropriate locations and subject to proper activation and deactivation. lncRNA-based mechanisms control cell fates during development, and their dysregulation underlies some human disorders caused by chromosomal deletions and translocations.

MeSH Terms
Animals Cell Nucleus/chemistry,genetics Disease/genetics Gene Expression Regulation Humans RNA, Long Noncoding/chemistry,genetics,metabolism
Chemicals
RNA, Long Noncoding
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Batista Pedro J
Howard Hughes Medical Institute and Program in Epithelial Biology, Stanford University School of Medicine, Stanford, CA 94305, USA.
Chang Howard Y
References (102)
102 references, click to expand
  1. Small noncoding differentially methylated copy-number variants, including lncRNA genes, cause a lethal lung developmental disorder.
    Genome Res. 2013 Jan;23(1):23-33 PMID: 23034409
  2. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression.
    Genome Res. 2012 Sep;22(9):1775-89 PMID: 22955988
  3. Direct visualization of the co-transcriptional assembly of a nuclear body by noncoding RNAs.
    Nat Cell Biol. 2011 Jan;13(1):95-101 PMID: 21170033
  4. Intergenic transcription through a polycomb group response element counteracts silencing.
    Genes Dev. 2005 Mar 15;19(6):697-708 PMID: 15741315
  5. Genome-wide measurement of RNA folding energies.
    Mol Cell. 2012 Oct 26;48(2):169-81 PMID: 22981864
  6. Molecular mechanisms of long noncoding RNAs.
    Mol Cell. 2011 Sep 16;43(6):904-14 PMID: 21925379
  7. A long ncRNA links copy number variation to a polycomb/trithorax epigenetic switch in FSHD muscular dystrophy.
    Cell. 2012 May 11;149(4):819-31 PMID: 22541069
  8. uPM3, a new molecular urine test for the detection of prostate cancer.
    Urology. 2004 Aug;64(2):311-5; discussion 315-6 PMID: 15302485
  9. The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin.
    Science. 2008 Dec 12;322(5908):1717-20 PMID: 18988810
  10. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles.
    Mol Cell. 2009 Mar 27;33(6):717-26 PMID: 19217333
  11. Lessons from X-chromosome inactivation: long ncRNA as guides and tethers to the epigenome.
    Genes Dev. 2009 Aug 15;23(16):1831-42 PMID: 19684108
  12. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses.
    Genes Dev. 2011 Sep 15;25(18):1915-27 PMID: 21890647
  13. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression.
    Proc Natl Acad Sci U S A. 2009 Jul 14;106(28):11667-72 PMID: 19571010
  14. Control of somatic tissue differentiation by the long non-coding RNA TINCR.
    Nature. 2013 Jan 10;493(7431):231-5 PMID: 23201690
  15. The selective elimination of messenger RNA underlies the mitosis-meiosis switch in fission yeast.
    Proc Jpn Acad Ser B Phys Biol Sci. 2010;86(8):788-97 PMID: 20948174
  16. Set3 HDAC mediates effects of overlapping noncoding transcription on gene induction kinetics.
    Cell. 2012 Sep 14;150(6):1158-69 PMID: 22959268
  17. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response.
    Cell. 2010 Aug 6;142(3):409-19 PMID: 20673990
  18. Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution.
    Cell. 2009 Apr 17;137(2):356-68 PMID: 19379699
  19. Long noncoding RNAs with enhancer-like function in human cells.
    Cell. 2010 Oct 1;143(1):46-58 PMID: 20887892
  20. Clinical utility of prostate carcinoma molecular diagnostic tests.
    Rev Urol. 2008 Winter;10(1):44-69 PMID: 18470278
  21. ncRNA- and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs.
    Cell. 2011 Nov 11;147(4):773-88 PMID: 22078878
  22. Mediator and cohesin connect gene expression and chromatin architecture.
    Nature. 2010 Sep 23;467(7314):430-5 PMID: 20720539
  23. MEN epsilon/beta nuclear-retained non-coding RNAs are up-regulated upon muscle differentiation and are essential components of paraspeckles.
    Genome Res. 2009 Mar;19(3):347-59 PMID: 19106332
  24. Intergenic transcription and transinduction of the human beta-globin locus.
    Genes Dev. 1997 Oct 1;11(19):2494-509 PMID: 9334315
  25. Organization of intracellular reactions with rationally designed RNA assemblies.
    Science. 2011 Jul 22;333(6041):470-4 PMID: 21700839
  26. Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs.
    Genome Res. 2007 May;17(5):556-65 PMID: 17387145
  27. Genome-wide identification of polycomb-associated RNAs by RIP-seq.
    Mol Cell. 2010 Dec 22;40(6):939-53 PMID: 21172659
  28. Immobilization of proteins in the nucleolus by ribosomal intergenic spacer noncoding RNA.
    Mol Cell. 2012 Jan 27;45(2):147-57 PMID: 22284675
  29. Malat1 is not an essential component of nuclear speckles in mice.
    RNA. 2012 Aug;18(8):1487-99 PMID: 22718948
  30. Long noncoding RNAs in C. elegans.
    Genome Res. 2012 Dec;22(12):2529-40 PMID: 22707570
  31. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes.
    Cell. 2011 Nov 11;147(4):789-802 PMID: 22056041
  32. Landscape of transcription in human cells.
    Nature. 2012 Sep 6;489(7414):101-8 PMID: 22955620
  33. Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation.
    Mol Cell. 2008 Oct 24;32(2):232-46 PMID: 18951091
  34. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits.
    Proc Natl Acad Sci U S A. 2009 Jun 9;106(23):9362-7 PMID: 19474294
  35. Long noncoding RNAs are rarely translated in two human cell lines.
    Genome Res. 2012 Sep;22(9):1646-57 PMID: 22955977
  36. Loss of the abundant nuclear non-coding RNA MALAT1 is compatible with life and development.
    RNA Biol. 2012 Aug;9(8):1076-87 PMID: 22858678
  37. A triple helix stabilizes the 3' ends of long noncoding RNAs that lack poly(A) tails.
    Genes Dev. 2012 Nov 1;26(21):2392-407 PMID: 23073843
  38. Inhibition of natural antisense transcripts in vivo results in gene-specific transcriptional upregulation.
    Nat Biotechnol. 2012 Mar 25;30(5):453-9 PMID: 22446693
  39. Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution.
    Cell. 2011 Dec 23;147(7):1537-50 PMID: 22196729
  40. The hallmarks of cancer: a long non-coding RNA point of view.
    RNA Biol. 2012 Jun;9(6):703-19 PMID: 22664915
  41. Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis.
    Genome Res. 2012 Mar;22(3):577-91 PMID: 22110045
  42. Intergenic transcripts regulate the epigenetic state of rRNA genes.
    Mol Cell. 2006 May 5;22(3):351-61 PMID: 16678107
  43. Flowering time control: another window to the connection between antisense RNA and chromatin.
    Trends Genet. 2012 Sep;28(9):445-53 PMID: 22785023
  44. DD3PCA3 RNA analysis in urine--a new perspective for detecting prostate cancer.
    Eur Urol. 2004 Aug;46(2):182-6; discussion 187 PMID: 15245811
  45. RNA mimics of green fluorescent protein.
    Science. 2011 Jul 29;333(6042):642-6 PMID: 21798953
  46. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis.
    Nature. 2010 Apr 15;464(7291):1071-6 PMID: 20393566
  47. Transcriptional profiling of long non-coding RNAs and novel transcribed regions across a diverse panel of archived human cancers.
    Genome Biol. 2012 Aug 28;13(8):R75 PMID: 22929540
  48. A large fraction of extragenic RNA pol II transcription sites overlap enhancers.
    PLoS Biol. 2010 May 11;8(5):e1000384 PMID: 20485488
  49. The dynamic architecture of Hox gene clusters.
    Science. 2011 Oct 14;334(6053):222-5 PMID: 21998387
  50. Noncoding transcription within the Igh distal V(H) region at PAIR elements affects the 3D structure of the Igh locus in pro-B cells.
    Proc Natl Acad Sci U S A. 2012 Oct 16;109(42):17004-9 PMID: 23027941
  51. Intronic RNAs mediate EZH2 regulation of epigenetic targets.
    Nat Struct Mol Biol. 2012 Jun 03;19(7):664-70 PMID: 22659877
  52. Transcription of two long noncoding RNAs mediates mating-type control of gametogenesis in budding yeast.
    Cell. 2012 Sep 14;150(6):1170-81 PMID: 22959267
  53. Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat.
    Nature. 2012 Nov 15;491(7424):454-7 PMID: 23064229
  54. Repression of the human dihydrofolate reductase gene by a non-coding interfering transcript.
    Nature. 2007 Feb 8;445(7128):666-70 PMID: 17237763
  55. Experimental validation of the regulated expression of large numbers of non-coding RNAs from the mouse genome.
    Genome Res. 2006 Jan;16(1):11-9 PMID: 16344565
  56. Chromosome territories.
    Cold Spring Harb Perspect Biol. 2010 Mar;2(3):a003889 PMID: 20300217
  57. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression.
    Nature. 2011 Apr 7;472(7341):120-4 PMID: 21423168
  58. Catalogues of mammalian long noncoding RNAs: modest conservation and incompleteness.
    Genome Biol. 2009;10(11):R124 PMID: 19895688
  59. HELLP babies link a novel lincRNA to the trophoblast cell cycle.
    J Clin Invest. 2012 Nov;122(11):4003-11 PMID: 23093777
  60. Positional information and patterning revisited.
    J Theor Biol. 2011 Jan 21;269(1):359-65 PMID: 21044633
  61. Spatial partitioning of the regulatory landscape of the X-inactivation centre.
    Nature. 2012 Apr 11;485(7398):381-5 PMID: 22495304
  62. Poly(A) tail recognition by a viral RNA element through assembly of a triple helix.
    Science. 2010 Nov 26;330(6008):1244-7 PMID: 21109672
  63. Deep sequencing of subcellular RNA fractions shows splicing to be predominantly co-transcriptional in the human genome but inefficient for lncRNAs.
    Genome Res. 2012 Sep;22(9):1616-25 PMID: 22955974
  64. Extensive and coordinated transcription of noncoding RNAs within cell-cycle promoters.
    Nat Genet. 2011 Jun 05;43(7):621-9 PMID: 21642992
  65. Systematic reconstruction of RNA functional motifs with high-throughput microfluidics.
    Nat Methods. 2012 Dec;9(12):1192-4 PMID: 23142872
  66. lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3' UTRs via Alu elements.
    Nature. 2011 Feb 10;470(7333):284-8 PMID: 21307942
  67. Genome regulation by long noncoding RNAs.
    Annu Rev Biochem. 2012;81:145-66 PMID: 22663078
  68. Nucleation of nuclear bodies by RNA.
    Nat Cell Biol. 2011 Feb;13(2):167-73 PMID: 21240286
  69. Biogenesis of nuclear bodies.
    Cold Spring Harb Perspect Biol. 2010 Dec;2(12):a000711 PMID: 21068152
  70. The long noncoding RNA, Jpx, is a molecular switch for X chromosome inactivation.
    Cell. 2010 Oct 29;143(3):390-403 PMID: 21029862
  71. RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3.
    Cell. 2012 Feb 17;148(4):664-78 PMID: 22325148
  72. Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes.
    Genes Dev. 2010 Oct 15;24(20):2264-9 PMID: 20952535
  73. The lncRNA Malat1 is dispensable for mouse development but its transcription plays a cis-regulatory role in the adult.
    Cell Rep. 2012 Jul 26;2(1):111-23 PMID: 22840402
  74. Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions.
    Mol Cell. 2011 Nov 18;44(4):667-78 PMID: 21963238
  75. RNA elimination machinery targeting meiotic mRNAs promotes facultative heterochromatin formation.
    Science. 2012 Jan 6;335(6064):96-100 PMID: 22144463
  76. Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription.
    Nature. 2008 Jul 3;454(7200):126-30 PMID: 18509338
  77. Long noncoding RNAs with snoRNA ends.
    Mol Cell. 2012 Oct 26;48(2):219-30 PMID: 22959273
  78. Long noncoding RNA as modular scaffold of histone modification complexes.
    Science. 2010 Aug 6;329(5992):689-93 PMID: 20616235
  79. Formation of triple-helical structures by the 3'-end sequences of MALAT1 and MENβ noncoding RNAs.
    Proc Natl Acad Sci U S A. 2012 Nov 20;109(47):19202-7 PMID: 23129630
  80. Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: functional role of a nuclear noncoding RNA.
    Mol Cell. 2009 Aug 28;35(4):467-78 PMID: 19716791
  81. A misplaced lncRNA causes brachydactyly in humans.
    J Clin Invest. 2012 Nov;122(11):3990-4002 PMID: 23093776
  82. Conservation of a triple-helix-forming RNA stability element in noncoding and genomic RNAs of diverse viruses.
    Cell Rep. 2012 Jul 26;2(1):26-32 PMID: 22840393
  83. Widespread transcription at neuronal activity-regulated enhancers.
    Nature. 2010 May 13;465(7295):182-7 PMID: 20393465
  84. A ncRNA modulates histone modification and mRNA induction in the yeast GAL gene cluster.
    Mol Cell. 2008 Dec 5;32(5):685-95 PMID: 19061643
  85. Topological domains in mammalian genomes identified by analysis of chromatin interactions.
    Nature. 2012 Apr 11;485(7398):376-80 PMID: 22495300
  86. Targeting nuclear RNA for in vivo correction of myotonic dystrophy.
    Nature. 2012 Aug 2;488(7409):111-5 PMID: 22859208
  87. Finishing the euchromatic sequence of the human genome.
    Nature. 2004 Oct 21;431(7011):931-45 PMID: 15496913
  88. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals.
    Nature. 2009 Mar 12;458(7235):223-7 PMID: 19182780
  89. Intergenic transcription is required to repress the Saccharomyces cerevisiae SER3 gene.
    Nature. 2004 Jun 3;429(6991):571-4 PMID: 15175754
  90. The noncoding RNA Mistral activates Hoxa6 and Hoxa7 expression and stem cell differentiation by recruiting MLL1 to chromatin.
    Mol Cell. 2011 Sep 16;43(6):1040-6 PMID: 21925392
  91. Selective elimination of messenger RNA prevents an incidence of untimely meiosis.
    Nature. 2006 Jul 6;442(7098):45-50 PMID: 16823445
  92. The inactive X chromosome adopts a unique three-dimensional conformation that is dependent on Xist RNA.
    Genes Dev. 2011 Jul 1;25(13):1371-83 PMID: 21690198
  93. Airn transcriptional overlap, but not its lncRNA products, induces imprinted Igf2r silencing.
    Science. 2012 Dec 14;338(6113):1469-72 PMID: 23239737
  94. Beyond the sequence: cellular organization of genome function.
    Cell. 2007 Feb 23;128(4):787-800 PMID: 17320514
  95. Inheritance of silent rDNA chromatin is mediated by PARP1 via noncoding RNA.
    Mol Cell. 2012 Mar 30;45(6):790-800 PMID: 22405650
  96. Paraspeckles are subpopulation-specific nuclear bodies that are not essential in mice.
    J Cell Biol. 2011 Apr 4;193(1):31-9 PMID: 21444682
  97. LincRNA-p21 suppresses target mRNA translation.
    Mol Cell. 2012 Aug 24;47(4):648-55 PMID: 22841487
  98. MENepsilon/beta noncoding RNAs are essential for structural integrity of nuclear paraspeckles.
    Proc Natl Acad Sci U S A. 2009 Feb 24;106(8):2525-30 PMID: 19188602
  99. Noncoding transcripts in sense and antisense orientation regulate the epigenetic state of ribosomal RNA genes.
    Cold Spring Harb Symp Quant Biol. 2010;75:357-64 PMID: 21502405
  100. Meiosis-specific noncoding RNA mediates robust pairing of homologous chromosomes in meiosis.
    Science. 2012 May 11;336(6082):732-6 PMID: 22582262
  101. lincRNAs act in the circuitry controlling pluripotency and differentiation.
    Nature. 2011 Aug 28;477(7364):295-300 PMID: 21874018
  102. The genomic binding sites of a noncoding RNA.
    Proc Natl Acad Sci U S A. 2011 Dec 20;108(51):20497-502 PMID: 22143764
Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
DOI
10.1016/j.cell.2013.02.012
Published
2013-03-14
Pages
1298-307
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC3651923
Subset
IM
Grants
NCI NIH HHS · R01 CA118750 · United States
NHGRI NIH HHS · R01 HG004361 · United States
Howard Hughes Medical Institute · United States
External Links
PubMed source DOI: 10.1016/j.cell.2013.02.012 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2