Technologies to probe functions and mechanisms of long noncoding RNAs

Thousands of long noncoding RNAs (lncRNAs) have been discovered, but their functional characterization has been slowed by a limited set of research tools. Here we review emerging RNA-centric methods to interrogate the intrinsic structure of lncRNAs as well as their genomic localization and biochemical partners. Understanding these technologies, including their advantages and caveats, and developing them in the future will be essential to progress from description to comprehension of the myriad roles of lncRNAs.

[1]  Harold G. Craighead,et al.  High-throughput binding characterization of RNA aptamer selections using a microplate-based multiplex microcolumn device , 2014, Analytical and Bioanalytical Chemistry.

[2]  N. Brockdorff,et al.  The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. , 2010, Developmental cell.

[3]  Michael Y Tolstorukov,et al.  The long noncoding RNAs NEAT1 and MALAT1 bind active chromatin sites. , 2014, Molecular cell.

[4]  Richard Bonneau,et al.  The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. , 2012, Molecular cell.

[5]  Howard Y. Chang,et al.  Control of somatic tissue differentiation by the long non-coding RNA TINCR , 2012, Nature.

[6]  E. Lander,et al.  The Xist lncRNA Exploits Three-Dimensional Genome Architecture to Spread Across the X Chromosome , 2013, Science.

[7]  C. Zurla,et al.  Quantifying RNA–protein interactions in situ using modified-MTRIPs and proximity ligation , 2012, Nucleic acids research.

[8]  H. Le Hir,et al.  Transcriptome-wide identification of RNA binding sites by CLIP-seq. , 2013, Methods.

[9]  Cole Trapnell,et al.  Multiplexed RNA structure characterization with selective 2′-hydroxyl acylation analyzed by primer extension sequencing (SHAPE-Seq) , 2011, Proceedings of the National Academy of Sciences.

[10]  Y. Zhang,et al.  In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features , 2013, Nature.

[11]  Zhonghan Li,et al.  The long noncoding RNA THRIL regulates TNFα expression through its interaction with hnRNPL , 2013, Proceedings of the National Academy of Sciences.

[12]  L. Stanton,et al.  The long noncoding RNA RMST interacts with SOX2 to regulate neurogenesis. , 2013, Molecular cell.

[13]  Lin Yang,et al.  Long noncoding RNAs: fresh perspectives into the RNA world. , 2014, Trends in biochemical sciences.

[14]  Howard Y. Chang,et al.  Long Noncoding RNAs: Cellular Address Codes in Development and Disease , 2013, Cell.

[15]  K. Weeks,et al.  Exploring RNA structural codes with SHAPE chemistry. , 2011, Accounts of chemical research.

[16]  Manolis Kellis,et al.  Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo , 2013, Nature.

[17]  J. Mcneil,et al.  XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure , 1996, The Journal of cell biology.

[18]  P. Trang,et al.  Nuclease footprint analyses of the interactions between RNase P ribozyme and a model mRNA substrate. , 1999, Nucleic acids research.

[19]  D. Tollervey,et al.  Mapping the miRNA interactome by cross-linking ligation and sequencing of hybrids (CLASH) , 2014, Nature Protocols.

[20]  B. S. Baker,et al.  The rox1 and rox2 RNAs are essential components of the compensasome, which mediates dosage compensation in Drosophila. , 1999, Molecular cell.

[21]  Howard Y. Chang,et al.  Revealing long noncoding RNA architecture and functions using domain-specific chromatin isolation by RNA purification , 2014, Nature Biotechnology.

[22]  Edith Heard,et al.  Fifty years of X-inactivation research , 2011, Development.

[23]  M. Rosenfeld,et al.  Brd4 and JMJD6-Associated Anti-Pause Enhancers in Regulation of Transcriptional Pause Release , 2013, Cell.

[24]  A. Spence,et al.  Epigenetic Licensing of Germline Gene Expression by Maternal RNA in C. elegans , 2011, Science.

[25]  F. Regnier,et al.  Quantification in proteomics through stable isotope coding: a review. , 2004, Journal of proteome research.

[26]  Howard Y. Chang,et al.  Systematic reconstruction of RNA functional motifs with high-throughput microfluidics , 2012, Nature Methods.

[27]  Robert C. Wolpert,et al.  A Review of the , 1985 .

[28]  P. Brown,et al.  The Yeast Rab GTPase Ypt1 Modulates Unfolded Protein Response Dynamics by Regulating the Stability of HAC1 RNA , 2012, PLoS genetics.

[29]  Julius B. Lucks,et al.  A modular strategy for engineering orthogonal chimeric RNA transcription regulators , 2013, Nucleic acids research.

[30]  Howard Y. Chang,et al.  Genome regulation by long noncoding RNAs. , 2012, Annual review of biochemistry.

[31]  B Lucks Julius,et al.  プライマー伸長塩基配列決定法(SHAPE‐Seq)を用いて分析した選択的2′‐ヒドロキシルアシル化による多重RNA構造の特徴化 , 2011 .

[32]  T. Cech,et al.  Defining the inside and outside of a catalytic RNA molecule. , 1989, Science.

[33]  D. S. Gross,et al.  Chromatin , 2020, Definitions.

[34]  Phillip D Zamore,et al.  Sequence-Specific Inhibition of Small RNA Function , 2004, PLoS biology.

[35]  Norman E. Davey,et al.  Insights into RNA Biology from an Atlas of Mammalian mRNA-Binding Proteins , 2012, Cell.

[36]  P. Sharp,et al.  Affinity chromatography of splicing complexes: U2, U5, and U4 + U6 small nuclear ribonucleoprotein particles in the spliceosome. , 1986, Science.

[37]  Qiangfeng Cliff Zhang,et al.  Landscape and variation of RNA secondary structure across the human transcriptome , 2014, Nature.

[38]  O. Uhlenbeck,et al.  Sequence-specific interaction of R17 coat protein with its ribonucleic acid binding site. , 1983, Biochemistry.

[39]  Adam P Arkin,et al.  Versatile RNA-sensing transcriptional regulators for engineering genetic networks , 2011, Proceedings of the National Academy of Sciences.

[40]  Timur Zhiyentayev,et al.  Single-cell in situ RNA profiling by sequential hybridization , 2014, Nature Methods.

[41]  C. Glass,et al.  Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation , 2013, Nature.

[42]  S. Blackshaw,et al.  Profiling the Human Protein-DNA Interactome Reveals ERK2 as a Transcriptional Repressor of Interferon Signaling , 2009, Cell.

[43]  M. Disney,et al.  Promoter-Bound Trinucleotide Repeat mRNA Drives Epigenetic Silencing in Fragile X Syndrome , 2014, Science.

[44]  Grzegorz Kudla,et al.  A pre-ribosomal RNA interaction network involving snoRNAs and the Rok1 helicase , 2014, RNA.

[45]  Michael P Snyder,et al.  SeqFold: Genome-scale reconstruction of RNA secondary structure integrating high-throughput sequencing data , 2013, Genome research.

[46]  P. Becker,et al.  ATP-dependent roX RNA remodeling by the helicase maleless enables specific association of MSL proteins. , 2013, Molecular cell.

[47]  T. Pan Probing RNA Structure by Lead Cleavage , 2000, Current protocols in nucleic acid chemistry.

[48]  Howard Y. Chang,et al.  Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. , 2011, Molecular cell.

[49]  Robert Tibshirani,et al.  Genome-wide measurement of RNA folding energies. , 2012, Molecular cell.

[50]  P. Sharp,et al.  RNA Bind-n-Seq: quantitative assessment of the sequence and structural binding specificity of RNA binding proteins. , 2014, Molecular cell.

[51]  Howard Y. Chang,et al.  Genome-wide mapping of RNA structure using nuclease digestion and high-throughput sequencing , 2013, Nature Protocols.

[52]  David Tollervey,et al.  Cross-linking, ligation, and sequencing of hybrids reveals RNA–RNA interactions in yeast , 2011, Proceedings of the National Academy of Sciences.

[53]  Michael F. Lin,et al.  Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals , 2009, Nature.

[54]  Brad A Chapman,et al.  The genomic binding sites of a noncoding RNA , 2011, Proceedings of the National Academy of Sciences.

[55]  E. Lander,et al.  Development and Applications of CRISPR-Cas9 for Genome Engineering , 2014, Cell.

[56]  Steven Busan,et al.  RNA motif discovery by SHAPE and mutational profiling (SHAPE-MaP) , 2014, Nature Methods.

[57]  Howard Y. Chang,et al.  Quantitative analysis of RNA-protein interactions on a massively parallel array for mapping biophysical and evolutionary landscapes , 2014, Nature Biotechnology.

[58]  Philip D. Gregory,et al.  Translating Dosage Compensation to Trisomy 21 , 2013, Nature.

[59]  Karissa Y. Sanbonmatsu,et al.  Structural architecture of the human long non-coding RNA, steroid receptor RNA activator , 2012, Nucleic acids research.

[60]  Robert E. Kingston,et al.  Purification of Proteins Associated with Specific Genomic Loci , 2009, Cell.

[61]  J. Steitz,et al.  Association of Argonaute proteins and microRNAs can occur after cell lysis. , 2012, RNA.

[62]  R. Kurokawa,et al.  Long Noncoding RNAs , 2015, Springer Japan.

[63]  David R. Kelley,et al.  Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre , 2014, Nature Structural &Molecular Biology.

[64]  Howard Y. Chang,et al.  RNA SHAPE analysis in living cells. , 2013, Nature chemical biology.

[65]  S. Blackshaw,et al.  The long noncoding RNA Six3OS acts in trans to regulate retinal development by modulating Six3 activity , 2011, Neural Development.

[66]  Sarah K. Bowman,et al.  High-resolution Xist binding maps reveal 2-step spreading during X-inactivation , 2013, Nature.

[67]  Rolf Backofen,et al.  Tandem stem-loops in roX RNAs act together to mediate X chromosome dosage compensation in Drosophila. , 2013, Molecular cell.

[68]  Gisela Schnapp,et al.  One-step affinity purification protocol for human telomerase , 1998, Nucleic Acids Res..

[69]  R. Russell,et al.  DMS footprinting of structured RNAs and RNA–protein complexes , 2007, Nature Protocols.

[70]  P. Tsang,et al.  A Prader–Willi locus lncRNA cloud modulates diurnal genes and energy expenditure , 2013, Human molecular genetics.

[71]  Keith W. Vance,et al.  The long non-coding RNA Paupar regulates the expression of both local and distal genes , 2014, The EMBO journal.

[72]  Howard Y. Chang,et al.  Genome-wide measurement of RNA secondary structure in yeast , 2010, Nature.

[73]  Howard Y. Chang,et al.  Long Noncoding RNA as Modular Scaffold of Histone Modification Complexes , 2010, Science.

[74]  Scott A. Rifkin,et al.  Imaging individual mRNA molecules using multiple singly labeled probes , 2008, Nature Methods.

[75]  C. Rossetto,et al.  KSHV PAN RNA Associates with Demethylases UTX and JMJD3 to Activate Lytic Replication through a Physical Interaction with the Virus Genome , 2012, PLoS pathogens.

[76]  K. Collins,et al.  RNA-based affinity purification reveals 7SK RNPs with distinct composition and regulation. , 2007, RNA.