Promoter analysis reveals globally differential regulation of human long non-coding RNA and protein-coding genes

Alam, Tanvir; Medvedeva, Yulia A.; Jia, Hui; Brown, James B.; Lipovich, Leonard; Bajic, Vladimir B.; Mantovani, Roberto

doi:10.1371/journal.pone.0109443

Promoter analysis reveals globally differential regulation of human long non-coding RNA and protein-coding genes

Journal Article · Thu Oct 02 00:00:00 EDT 2014 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0109443· OSTI ID:1212466

Alam, Tanvir ^[1]; Medvedeva, Yulia A. ^[1]; Jia, Hui ^[2]; Brown, James B. ^[3]; Lipovich, Leonard ^[4]; Bajic, Vladimir B. ^[1]; Mantovani, Roberto ^[5]

King Abdullah University of Science and Technology (KAUST), Thuwal (Saudi Arabia)
Wayne State Univ., Detroit, MI (United States). Center for Molecular Medicine and Genetics.
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Department of Genome Dynamics, Life Sciences Division.
Wayne State Univ., Detroit, MI (United States). Center for Molecular Medicine and Genetics and Dept. of Neurology.
Universita` degli Studi di Milano (Italy)

Transcriptional regulation of protein-coding genes is increasingly well-understood on a global scale, yet no comparable information exists for long non-coding RNA (lncRNA) genes, which were recently recognized to be as numerous as protein-coding genes in mammalian genomes. We performed a genome-wide comparative analysis of the promoters of human lncRNA and protein-coding genes, finding global differences in specific genetic and epigenetic features relevant to transcriptional regulation. These two groups of genes are hence subject to separate transcriptional regulatory programs, including distinct transcription factor (TF) proteins that significantly favor lncRNA, rather than coding-gene, promoters. We report a specific signature of promoter-proximal transcriptional regulation of lncRNA genes, including several distinct transcription factor binding sites (TFBS). Experimental DNase I hypersensitive site profiles are consistent with active configurations of these lncRNA TFBS sets in diverse human cell types. TFBS ChIP-seq datasets confirm the binding events that we predicted using computational approaches for a subset of factors. For several TFs known to be directly regulated by lncRNAs, we find that their putative TFBSs are enriched at lncRNA promoters, suggesting that the TFs and the lncRNAs may participate in a bidirectional feedback loop regulatory network. Accordingly, cells may be able to modulate lncRNA expression levels independently of mRNA levels via distinct regulatory pathways. Our results also raise the possibility that, given the historical reliance on protein-coding gene catalogs to define the chromatin states of active promoters, a revision of these chromatin signature profiles to incorporate expressed lncRNA genes is warranted in the future.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: National Institute of Health; USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1212466

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 10 Vol. 9; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (79)

MacroRNA underdogs in a microRNA world: Evolutionary, regulatory, and biomedical significance of mammalian long non-protein-coding RNA Lipovich, Leonard; Johnson, Rory; Lin, Chin-Yo Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1799, Issue 9 https://doi.org/10.1016/j.bbagrm.2010.10.001	journal	September 2010
Nkx2.2 antisense RNA overexpression enhanced oligodendrocytic differentiation Tochitani, Shiro; Hayashizaki, Yoshihide Biochemical and Biophysical Research Communications, Vol. 372, Issue 4 https://doi.org/10.1016/j.bbrc.2008.05.127	journal	August 2008
Searching Chromatin for Stem Cell Identity Buszczak, Michael; Spradling, Allan C. Cell, Vol. 125, Issue 2 https://doi.org/10.1016/j.cell.2006.04.004	journal	April 2006
Long Noncoding RNAs with Enhancer-like Function in Human Cells Ørom, Ulf Andersson; Derrien, Thomas; Beringer, Malte Cell, Vol. 143, Issue 1 https://doi.org/10.1016/j.cell.2010.09.001	journal	October 2010
CpG islands - ‘A rough guide’ Illingworth, Robert S.; Bird, Adrian P. FEBS Letters, Vol. 583, Issue 11 https://doi.org/10.1016/j.febslet.2009.04.012	journal	April 2009
Profiling of human CD4+ T-cell subsets identifies the TH2-specific noncoding RNA GATA3-AS1 Zhang, Huan; Nestor, Colm E.; Zhao, Shuli Journal of Allergy and Clinical Immunology, Vol. 132, Issue 4 https://doi.org/10.1016/j.jaci.2013.05.033	journal	October 2013
Polycomb group protein-mediated repression of transcription Morey, Lluís; Helin, Kristian Trends in Biochemical Sciences, Vol. 35, Issue 6 https://doi.org/10.1016/j.tibs.2010.02.009	journal	June 2010
LncRNAs have a say in protein translation Huarte, Maite Cell Research, Vol. 23, Issue 4 https://doi.org/10.1038/cr.2012.169	journal	December 2012
Transcriptome genetics using second generation sequencing in a Caucasian population Montgomery, Stephen B.; Sammeth, Micha; Gutierrez-Arcelus, Maria Nature, Vol. 464, Issue 7289 https://doi.org/10.1038/nature08903	journal	March 2010
Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis Gupta, Rajnish A.; Shah, Nilay; Wang, Kevin C. Nature, Vol. 464, Issue 7291 https://doi.org/10.1038/nature08975	journal	April 2010
Mapping and analysis of chromatin state dynamics in nine human cell types Ernst, Jason; Kheradpour, Pouya; Mikkelsen, Tarjei S. Nature, Vol. 473, Issue 7345 https://doi.org/10.1038/nature09906	journal	March 2011
The accessible chromatin landscape of the human genome Thurman, Robert E.; Rynes, Eric; Humbert, Richard Nature, Vol. 489, Issue 7414 https://doi.org/10.1038/nature11232	journal	September 2012
DNMT1-interacting RNAs block gene-specific DNA methylation Di Ruscio, Annalisa; Ebralidze, Alexander K.; Benoukraf, Touati Nature, Vol. 503, Issue 7476 https://doi.org/10.1038/nature12598	journal	October 2013
Combinatorial patterns of histone acetylations and methylations in the human genome Wang, Zhibin; Zang, Chongzhi; Rosenfeld, Jeffrey A. Nature Genetics, Vol. 40, Issue 7 https://doi.org/10.1038/ng.154	journal	June 2008
The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells Loh, Yuin-Han; Wu, Qiang; Chew, Joon-Lin Nature Genetics, Vol. 38, Issue 4 https://doi.org/10.1038/ng1760	journal	March 2006
Balanced gene regulation by an embryonic brain ncRNA is critical for adult hippocampal GABA circuitry Bond, Allison M.; VanGompel, Michael J. W.; Sametsky, Evgeny A. Nature Neuroscience, Vol. 12, Issue 8 https://doi.org/10.1038/nn.2371	journal	July 2009
A census of human transcription factors: function, expression and evolution Vaquerizas, Juan M.; Kummerfeld, Sarah K.; Teichmann, Sarah A. Nature Reviews Genetics, Vol. 10, Issue 4 https://doi.org/10.1038/nrg2538	journal	April 2009
Molecular basis of histone H3K36me3 recognition by the PWWP domain of Brpf1 Vezzoli, Alessandro; Bonadies, Nicolas; Allen, Mark D. Nature Structural & Molecular Biology, Vol. 17, Issue 5 https://doi.org/10.1038/nsmb.1797	journal	April 2010
Combined Analysis of MicroRNome and 3′-UTRome Reveals a Species-specific Regulation of Progesterone Receptor Expression in the Endometrium of Rhesus Monkey Liu, Ji-Long; Liang, Xiao-Huan; Su, Ren-Wei Journal of Biological Chemistry, Vol. 287, Issue 17 https://doi.org/10.1074/jbc.m111.301275	journal	February 2012
A unification of mosaic structures in the human genome Lercher, Martin J.; Urrutia, Araxi O.; Pavlíček, Adam Human Molecular Genetics, Vol. 12, Issue 19 https://doi.org/10.1093/hmg/ddg251	journal	October 2003
GenBank Benson, D. A.; Boguski, M. S.; Lipman, D. J. Nucleic Acids Research, Vol. 25, Issue 1 https://doi.org/10.1093/nar/25.1.1	journal	January 1997
Transcription-coupled deposition of histone modifications during MHC class II gene activation Rybtsova, Natalia; Leimgruber, Elisa; Seguin-Estévez, Queralt Nucleic Acids Research, Vol. 35, Issue 10 https://doi.org/10.1093/nar/gkm214	journal	May 2007
Integrative analysis of the human cis -antisense gene pairs, miRNAs and their transcription regulation patterns Grinchuk, Oleg V.; Jenjaroenpun, Piroon; Orlov, Yuriy L. Nucleic Acids Research, Vol. 38, Issue 2 https://doi.org/10.1093/nar/gkp954	journal	November 2009
Involvement of argonaute proteins in gene silencing and activation by RNAs complementary to a non-coding transcript at the progesterone receptor promoter Chu, Yongjun; Yue, Xuan; Younger, Scott T. Nucleic Acids Research, Vol. 38, Issue 21 https://doi.org/10.1093/nar/gkq648	journal	July 2010
HIstome--a relational knowledgebase of human histone proteins and histone modifying enzymes Khare, S. P.; Habib, F.; Sharma, R. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1125	journal	December 2011
HOCOMOCO: a comprehensive collection of human transcription factor binding sites models Kulakovskiy, Ivan V.; Medvedeva, Yulia A.; Schaefer, Ulf Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1089	journal	November 2012
EMdeCODE: a novel algorithm capable of reading words of epigenetic code to predict enhancers and retroviral integration sites and to identify H3R2me1 as a distinctive mark of coding versus non-coding genes Santoni, Federico Andrea Nucleic Acids Research, Vol. 41, Issue 3 https://doi.org/10.1093/nar/gks1214	journal	December 2012
Long non-coding RNA identification over mouse brain development by integrative modeling of chromatin and genomic features Lv, Jie; Liu, Hongbo; Huang, Zhijun Nucleic Acids Research, Vol. 41, Issue 22 https://doi.org/10.1093/nar/gkt818	journal	September 2013
Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses Cabili, M. N.; Trapnell, C.; Goff, L. Genes & Development, Vol. 25, Issue 18 https://doi.org/10.1101/gad.17446611	journal	September 2011
A double take on bivalent promoters Voigt, P.; Tee, W. -W.; Reinberg, D. Genes & Development, Vol. 27, Issue 12 https://doi.org/10.1101/gad.219626.113	journal	June 2013
The GENCODE v7 catalog of human long noncoding RNAs: Analysis of their gene structure, evolution, and expression Derrien, T.; Johnson, R.; Bussotti, G. Genome Research, Vol. 22, Issue 9 https://doi.org/10.1101/gr.132159.111	journal	September 2012
Long noncoding RNAs are rarely translated in two human cell lines Banfai, B.; Jia, H.; Khatun, J. Genome Research, Vol. 22, Issue 9 https://doi.org/10.1101/gr.134767.111	journal	September 2012
GENCODE: The reference human genome annotation for The ENCODE Project Harrow, J.; Frankish, A.; Gonzalez, J. M. Genome Research, Vol. 22, Issue 9 https://doi.org/10.1101/gr.135350.111	journal	September 2012
Annotation of functional variation in personal genomes using RegulomeDB Boyle, A. P.; Hong, E. L.; Hariharan, M. Genome Research, Vol. 22, Issue 9 https://doi.org/10.1101/gr.137323.112	journal	September 2012
Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors Wang, J.; Zhuang, J.; Iyer, S. Genome Research, Vol. 22, Issue 9 https://doi.org/10.1101/gr.139105.112	journal	September 2012
Abundant novel transcriptional units and unconventional gene pairs on human chromosome 22 Lipovich, L. Genome Research, Vol. 16, Issue 1 https://doi.org/10.1101/gr.3883606	journal	December 2005
Noncoding RNA Gas5 Is a Growth Arrest- and Starvation-Associated Repressor of the Glucocorticoid Receptor Kino, T.; Hurt, D. E.; Ichijo, T. Science Signaling, Vol. 3, Issue 107 https://doi.org/10.1126/scisignal.2000568	journal	February 2010
Transcriptional Regulatory Elements in the Human Genome Maston, Glenn A.; Evans, Sara K.; Green, Michael R. Annual Review of Genomics and Human Genetics, Vol. 7, Issue 1 https://doi.org/10.1146/annurev.genom.7.080505.115623	journal	September 2006
Histone H3 Lysine 9 Methylation and HP1γ Are Associated with Transcription Elongation through Mammalian Chromatin. Vakoc, Christopher R.; Mandat, Sean A.; Olenschock, Ben A. Blood, Vol. 106, Issue 11 https://doi.org/10.1182/blood.v106.11.1734.1734	journal	November 2005
Screening non-coding RNAs in transcriptomes from neglected species using PORTRAIT: case study of the pathogenic fungus Paracoccidioides brasiliensis Arrial, Roberto T.; Togawa, Roberto C.; Brigido, Marcelo de M. BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-239	journal	August 2009
Intergenic, gene terminal, and intragenic CpG islands in the human genome Medvedeva, Yulia A.; Fridman, Marina V.; Oparina, Nina J. BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-48	journal	January 2010
Human genes with CpG island promoters have a distinct transcription-associated chromatin organization Vavouri, Tanya; Lehner, Ben Genome Biology, Vol. 13, Issue 11 https://doi.org/10.1186/gb-2012-13-11-r110	journal	January 2012
Regulation of neural macroRNAs by the transcriptional repressor REST Johnson, R.; Teh, C. H. -L.; Jia, H. RNA, Vol. 15, Issue 1 https://doi.org/10.1261/rna.1127009	journal	November 2008
Genome-wide computational identification and manual annotation of human long noncoding RNA genes Jia, H.; Osak, M.; Bogu, G. K. RNA, Vol. 16, Issue 8 https://doi.org/10.1261/rna.1951310	journal	June 2010
Orphan CpG Islands Identify Numerous Conserved Promoters in the Mammalian Genome Illingworth, Robert S.; Gruenewald-Schneider, Ulrike; Webb, Shaun PLoS Genetics, Vol. 6, Issue 9 https://doi.org/10.1371/journal.pgen.1001134	journal	September 2010
Activity-Dependent Human Brain Coding/Noncoding Gene Regulatory Networks Lipovich, Leonard; Dachet, Fabien; Cai, Juan Genetics, Vol. 192, Issue 3 https://doi.org/10.1534/genetics.112.145128	journal	September 2012
Mutations and Binding Sites of Human Transcription Factors Kamanu, Frederick Kinyua; Medvedeva, Yulia A.; Schaefer, Ulf Frontiers in Genetics, Vol. 3 https://doi.org/10.3389/fgene.2012.00100	journal	January 2012
Sense-antisense gene pairs: sequence, transcription, and structure are not conserved between human and mouse Wood, Emily J.; Chin-Inmanu, Kwanrutai; Jia, Hui Frontiers in Genetics, Vol. 4 https://doi.org/10.3389/fgene.2013.00183	journal	January 2013
Long and noncoding RNAs (lnc-RNAs) determine androgen receptor dependent gene expression in prostate cancer growth in vivo Pestell, RichardG; Yu, Zuoren Asian Journal of Andrology, Vol. 16, Issue 2 https://doi.org/10.4103/1008-682x.122364	journal	January 2014
HOX antisense lincRNA HOXA-AS2 is an apoptosis repressor in all Trans retinoic acid treated NB4 promyelocytic leukemia cells : lincRNA HOXA-AS2 suppresses apoptosis in NB4 cells Zhao, Hang; Zhang, Xueqing; Frazão, Josias Brito Journal of Cellular Biochemistry, Vol. 114, Issue 10 https://doi.org/10.1002/jcb.24586	journal	August 2013
The human genome-wide distribution of DNA palindromes Lu, Le; Jia, Hui; Dröge, Peter Functional & Integrative Genomics, Vol. 7, Issue 3 https://doi.org/10.1007/s10142-007-0047-6	journal	March 2007
A Steroid Receptor Coactivator, SRA, Functions as an RNA and Is Present in an SRC-1 Complex Lanz, Rainer B.; McKenna, Neil J.; Onate, Sergio A. Cell, Vol. 97, Issue 1 https://doi.org/10.1016/S0092-8674(00)80711-4	journal	April 1999
A Bivalent Chromatin Structure Marks Key Developmental Genes in Embryonic Stem Cells Bernstein, Bradley E.; Mikkelsen, Tarjei S.; Xie, Xiaohui Cell, Vol. 125, Issue 2 https://doi.org/10.1016/j.cell.2006.02.041	journal	April 2006
Ribosome Profiling Provides Evidence that Large Noncoding RNAs Do Not Encode Proteins Guttman, Mitchell; Russell, Pamela; Ingolia, Nicholas T. Cell, Vol. 154, Issue 1 https://doi.org/10.1016/j.cell.2013.06.009	journal	July 2013
Histone H3 Lysine 9 Methylation and HP1γ Are Associated with Transcription Elongation through Mammalian Chromatin Vakoc, Christopher R.; Mandat, Sean A.; Olenchock, Benjamin A. Molecular Cell, Vol. 19, Issue 3 https://doi.org/10.1016/j.molcel.2005.06.011	journal	August 2005
Regional differences in gene expression and promoter usage in aged human brains Pardo, Luba M.; Rizzu, Patrizia; Francescatto, Margherita Neurobiology of Aging, Vol. 34, Issue 7 https://doi.org/10.1016/j.neurobiolaging.2013.01.005	journal	July 2013
Initial sequencing and analysis of the human genome Lander, Eric S.; Linton, Lauren M. Nature, Vol. 409, Issue 6822, p. 860-921 https://doi.org/10.1038/35057062	journal	February 2001
Tsix, a gene antisense to Xist at the X-inactivation centre Lee, Jeannie; Davidow, Lance S.; Warshawsky, David Nature Genetics, Vol. 21, Issue 4 https://doi.org/10.1038/7734	journal	April 1999
Genome-wide analysis of ETS-family DNA-binding in vitro and in vivo Wei, Gong-Hong; Badis, Gwenael; Berger, Michael F. The EMBO Journal, Vol. 29, Issue 13 https://doi.org/10.1038/emboj.2010.106	journal	June 2010
lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3′ UTRs via Alu elements Gong, Chenguang; Maquat, Lynne E. Nature, Vol. 470, Issue 7333 https://doi.org/10.1038/nature09701	journal	February 2011
An integrated encyclopedia of DNA elements in the human genome No authors listed Nature, Vol. 489, Issue 7414, p. 57-74 https://doi.org/10.1038/nature11247	journal	September 2012
Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat Carrieri, Claudia; Cimatti, Laura; Biagioli, Marta Nature, Vol. 491, Issue 7424 https://doi.org/10.1038/nature11508	journal	October 2012
lncRNA-dependent mechanisms of androgen-receptor-regulated gene activation programs Yang, Liuqing; Lin, Chunru; Jin, Chunyu Nature, Vol. 500, Issue 7464 https://doi.org/10.1038/nature12451	journal	August 2013
The evolution of lncRNA repertoires and expression patterns in tetrapods Necsulea, Anamaria; Soumillon, Magali; Warnefors, Maria Nature, Vol. 505, Issue 7485 https://doi.org/10.1038/nature12943	journal	January 2014
Activating gene expression in mammalian cells with promoter-targeted duplex RNAs Janowski, Bethany A.; Younger, Scott T.; Hardy, Daniel B. Nature Chemical Biology, Vol. 3, Issue 3 https://doi.org/10.1038/nchembio860	journal	January 2007
Genome-wide analysis of mammalian promoter architecture and evolution Carninci, Piero; Sandelin, Albin; Lenhard, Boris Nature Genetics, Vol. 38, Issue 6 https://doi.org/10.1038/ng1789	journal	April 2006
Mapping and quantifying mammalian transcriptomes by RNA-Seq Mortazavi, Ali; Williams, Brian A.; McCue, Kenneth Nature Methods, Vol. 5, Issue 7, p. 621-628 https://doi.org/10.1038/nmeth.1226	journal	May 2008
X-chromosome inactivation: a hypothesis linking ontogeny and phylogeny Huynh, Khanh D.; Lee, Jeannie T. Nature Reviews Genetics, Vol. 6, Issue 5 https://doi.org/10.1038/nrg1604	journal	April 2005
A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters Saxonov, S.; Berg, P.; Brutlag, D. L. Proceedings of the National Academy of Sciences, Vol. 103, Issue 5 https://doi.org/10.1073/pnas.0510310103	journal	January 2006
Combined Analysis of MicroRNome and 3′-UTRome Reveals a Species-specific Regulation of Progesterone Receptor Expression in the Endometrium of Rhesus Monkey Liu, Ji-Long; Liang, Xiao-Huan; Su, Ren-Wei Journal of Biological Chemistry, Vol. 287, Issue 17 https://doi.org/10.1074/jbc.M111.301275	journal	February 2012
CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine Kong, Lei; Zhang, Yong; Ye, Zhi-Qiang Nucleic Acids Research, Vol. 35, Issue suppl_2 https://doi.org/10.1093/nar/gkm391	journal	July 2007
Systematic Localization of Common Disease-Associated Variation in Regulatory DNA Maurano, M. T.; Humbert, R.; Rynes, E. Science, Vol. 337, Issue 6099 https://doi.org/10.1126/science.1222794	journal	September 2012
Highly scalable ab initio genomic motif identification Marchand, Benoît; Bajic, Vladimir B.; Kaushik, Dinesh K. Proceedings of 2011 International Conference for High Performance Computing, Networking, Storage and Analysis on - SC '11 https://doi.org/10.1145/2063384.2063459	conference	January 2011
iSeeRNA: identification of long intergenic non-coding RNA transcripts from transcriptome sequencing data Sun, Kun; Chen, Xiaona; Jiang, Peiyong BMC Genomics, Vol. 14, Issue S2 https://doi.org/10.1186/1471-2164-14-S2-S7	journal	February 2013
Modeling gene expression using chromatin features in various cellular contexts Dong, Xianjun; Greven, Melissa C.; Kundaje, Anshul Genome Biology, Vol. 13, Issue 9 https://doi.org/10.1186/gb-2012-13-9-r53	journal	January 2012
An epigenetic road map for histone lysine methylation Lachner, M. Journal of Cell Science, Vol. 116, Issue 11 https://doi.org/10.1242/jcs.00493	journal	June 2003
Conserved long noncoding RNAs transcriptionally regulated by Oct4 and Nanog modulate pluripotency in mouse embryonic stem cells Sheik Mohamed, J.; Gaughwin, P. M.; Lim, B. RNA, Vol. 16, Issue 2 https://doi.org/10.1261/rna.1441510	journal	December 2009
Distinguishing Protein-Coding from Non-Coding RNAs through Support Vector Machines Liu, Jinfeng; Gough, Julian; Rost, Burkhard PLoS Genetics, Vol. 2, Issue 4 https://doi.org/10.1371/journal.pgen.0020029	journal	January 2006
Complex Loci in Human and Mouse Genomes Engström, Pär G.; Suzuki, Harukazu; Ninomiya, Noriko PLoS Genetics, Vol. 2, Issue 4 https://doi.org/10.1371/journal.pgen.0020047	journal	January 2006

Cited By (33)

Long non-coding antisense RNA KRT7-AS is activated in gastric cancers and supports cancer cell progression by increasing KRT7 expression Huang, B.; Song, J. H.; Cheng, Y. Oncogene, Vol. 35, Issue 37 https://doi.org/10.1038/onc.2016.25	journal	February 2016
A MAFG-lncRNA axis links systemic nutrient abundance to hepatic glucose metabolism Pradas-Juni, Marta; Hansmeier, Nils R.; Link, Jenny C. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14323-y	journal	January 2020
A Comprehensive Characterization of the Function of LincRNAs in Transcriptional Regulation Through Long-Range Chromatin Interactions Cai, Liuyang; Chang, Huidan; Fang, Yaping Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep36572	journal	November 2016
EpiFactors: a comprehensive database of human epigenetic factors and complexes Medvedeva, Yulia A.; Lennartsson, Andreas; Ehsani, Rezvan Database, Vol. 2015 https://doi.org/10.1093/database/bav067	journal	January 2015
HOCOMOCO: expansion and enhancement of the collection of transcription factor binding sites models Kulakovskiy, Ivan V.; Vorontsov, Ilya E.; Yevshin, Ivan S. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1249	journal	November 2015
Discriminative identification of transcriptional responses of promoters and enhancers after stimulus Kleftogiannis, Dimitrios; Kalnis, Panos; Arner, Erik Nucleic Acids Research https://doi.org/10.1093/nar/gkw1015	journal	October 2016
lncRNAs in development and disease: from functions to mechanisms Delás, M. Joaquina; Hannon, Gregory J. Open Biology, Vol. 7, Issue 7 https://doi.org/10.1098/rsob.170121	journal	July 2017
Long Noncoding RNAs as Biomarkers in Cancer Bolha, Luka; Ravnik-Glavač, Metka; Glavač, Damjan Disease Markers, Vol. 2017 https://doi.org/10.1155/2017/7243968	journal	January 2017
Detection of long non–coding RNA homology, a comparative study on alignment and alignment–free metrics Noviello, Teresa M. R.; Di Liddo, Antonella; Ventola, Giovanna M. BMC Bioinformatics, Vol. 19, Issue 1 https://doi.org/10.1186/s12859-018-2441-6	journal	November 2018
Coordinate regulation of long non-coding RNAs and protein-coding genes in germ-free mice Dempsey, Joseph; Zhang, Angela; Cui, Julia Yue BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-5235-3	journal	November 2018
Cancer subtypes classification using long non-coding RNA Flippot, Ronan; Malouf, Gabriel G.; Su, Xiaoping Oncotarget, Vol. 7, Issue 33 https://doi.org/10.18632/oncotarget.10213	journal	June 2016
Single nucleotide polymorphisms in ZNRD1-AS1 increase cancer risk in an Asian population Wang, Ping-Yu; Li, Jing-Hua; Liu, Yue-Mei Oncotarget, Vol. 8, Issue 6 https://doi.org/10.18632/oncotarget.14334	journal	December 2016
Analysis of Genomic Sequence Motifs for Deciphering Transcription Factor Binding and Transcriptional Regulation in Eukaryotic Cells Boeva, Valentina Frontiers in Genetics, Vol. 7 https://doi.org/10.3389/fgene.2016.00024	journal	February 2016
Practical Guidance in Genome-Wide RNA:DNA Triple Helix Prediction Matveishina, Elena; Antonov, Ivan; Medvedeva, Yulia A. International Journal of Molecular Sciences, Vol. 21, Issue 3 https://doi.org/10.3390/ijms21030830	journal	January 2020
History, Discovery, and Classification of lncRNAs Jarroux, Julien; Morillon, Antonin; Pinskaya, Marina Advances in Experimental Medicine and Biology https://doi.org/10.1007/978-981-10-5203-3_1	book	January 2017
High-throughput annotation of full-length long noncoding RNAs with capture long-read sequencing Lagarde, Julien; Uszczynska-Ratajczak, Barbara; Carbonell, Silvia Nature Genetics, Vol. 49, Issue 12 https://doi.org/10.1038/ng.3988	journal	November 2017
Computational identification of putative lincRNAs in mouse embryonic stem cell Liu, Hui; Lyu, Jie; Liu, Hongbo Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep34892	journal	October 2016
Prediction of lncRNAs and their interactions with nucleic acids: benchmarking bioinformatics tools Antonov, Ivan V.; Mazurov, Evgeny; Borodovsky, Mark Briefings in Bioinformatics, Vol. 20, Issue 2 https://doi.org/10.1093/bib/bby032	journal	April 2018
Characterization and identification of long non-coding RNAs based on feature relationship Wang, Guangyu; Yin, Hongyan; Li, Boyang Bioinformatics, Vol. 35, Issue 17 https://doi.org/10.1093/bioinformatics/btz008	journal	January 2019
Modeling the relationship of epigenetic modifications to transcription factor binding Liu, Liang; Jin, Guangxu; Zhou, Xiaobo Nucleic Acids Research, Vol. 43, Issue 8 https://doi.org/10.1093/nar/gkv255	journal	March 2015
HOCOMOCO: towards a complete collection of transcription factor binding models for human and mouse via large-scale ChIP-Seq analysis Kulakovskiy, Ivan V.; Vorontsov, Ilya E.; Yevshin, Ivan S. Nucleic Acids Research, Vol. 46, Issue D1 https://doi.org/10.1093/nar/gkx1106	journal	November 2017
Long Non-Coding RNAs: A Novel Paradigm for Toxicology Dempsey, Joseph L.; Cui, Julia Yue Toxicological Sciences, Vol. 155, Issue 1 https://doi.org/10.1093/toxsci/kfw203	journal	November 2016
Chromatin environment, transcriptional regulation, and splicing distinguish lincRNAs and mRNAs Mele, Marta; Mattioli, Kaia; Mallard, William Genome Research https://doi.org/10.1101/088484	journal	November 2016
High-throughput annotation of full-length long noncoding RNAs with Capture Long-Read Sequencing Lagarde, Julien; Uszczynska-Ratajczak, Barbara; Carbonell, Silvia Nature Genetics https://doi.org/10.1101/105064	journal	October 2017
Characterization and identification of long non-coding RNAs based on feature relationship Wang, Guangyu; Yin, Hongyan; Li, Boyang Bioinformatics https://doi.org/10.1101/327882	journal	May 2018
Chromatin environment, transcriptional regulation, and splicing distinguish lincRNAs and mRNAs Melé, Marta; Mattioli, Kaia; Mallard, William Genome Research, Vol. 27, Issue 1 https://doi.org/10.1101/gr.214205.116	journal	December 2016
ASSA: Fast identification of statistically significant interactions between long RNAs Antonov, Ivan; Marakhonov, Andrey; Zamkova, Maria Journal of Bioinformatics and Computational Biology, Vol. 16, Issue 01 https://doi.org/10.1142/s0219720018400012	journal	February 2018
The bright side of dark matter: lncRNAs in cancer Evans, Joseph R.; Feng, Felix Y.; Chinnaiyan, Arul M. Journal of Clinical Investigation, Vol. 126, Issue 8 https://doi.org/10.1172/jci84421	journal	August 2016
Preservation of methylated CpG dinucleotides in human CpG islands Panchin, Alexander Y.; Makeev, Vsevolod J.; Medvedeva, Yulia A. Biology Direct, Vol. 11, Issue 1 https://doi.org/10.1186/s13062-016-0113-x	journal	March 2016
lncRNAs in development and disease: from functions to mechanisms Delás, M. Joaquina; Hannon, Gregory Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.17108	text	January 2017
Long Non-Coding RNA as the Newest Perspective Biomarkers in Cancer Beylerli, O. A.; Beylerli, A. T.; Gareev, I. F. Innovative medicine of Kuban, Vol. 14, Issue 2 https://doi.org/10.35401/2500-0268-2019-14-2-76-83	journal	June 2019
Induction of a Long Noncoding RNA Transcript, NR_045064, Promotes Defense Gene Transcription and Facilitates Intestinal Epithelial Cell Responses against Cryptosporidium Infection Li, Min; Gong, Ai-Yu; Zhang, Xin-Tian The Journal of Immunology, Vol. 201, Issue 12 https://doi.org/10.4049/jimmunol.1800566	journal	November 2018
High-throughput annotation of full-length long noncoding RNAs with capture long-read sequencing. Lagarde, Julien; Uszczynska-Ratajczak, Barbara; Carbonell, Silvia Nature America https://doi.org/10.7892/boris.116920	text	January 2017

Similar Records

Identification and positional distribution analysis of transcription factor binding sites for genes from the wheat fl-cDNA sequences

Journal Article · Fri Jun 02 20:00:00 EDT 2017 · Bioscience, Biotechnology, and Biochemistry · OSTI ID:1770454

Genome-wide de Novo Prediction of Proximal and Distal Tissue-Specific Enhancers

Journal Article · Wed Nov 02 23:00:00 EST 2005 · Genome Research, N/A, N/A, January 7, 2007, pp. 1 · OSTI ID:899445

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
DNA methylation
DNA transcription
chromatin
gene expression
gene regulation
long non-coding RNAs
sequence motif analysis
transcription factors

Promoter analysis reveals globally differential regulation of human long non-coding RNA and protein-coding genes

Citation Formats

References (79)

Cited By (33)

Similar Records

Related Subjects