Database, Vol. 2013, Article ID bat034, doi:10.

1093/database/bat034
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Original article
lncRNome: a comprehensive knowledgebase
of human long noncoding RNAs
Deeksha Bhartiya1,y, Koustav Pal2,y, Sourav Ghosh3, Shruti Kapoor3, Saakshi Jalali1,
Bharat Panwar4, Sakshi Jain2, Satish Sati3, Shantanu Sengupta3, Chetana Sachidanandan3,
Gajendra Pal Singh Raghava4, Sridhar Sivasubbu3 and Vinod Scaria1,*
1
GN Ramachandran Knowledge Center for Genome Informatics, CSIR Institute of Genomics and Integrative Biology, Mall Road, Delhi 110007, India,
2
CSIR Open Source Drug Discovery Unit, Council of Scientific and Industrial Research, Anusandhan Bhavan, Delhi 110001, India, 3Genomics and

Downloaded from http://database.oxfordjournals.org/ by guest on February 6, 2014

Molecular Medicine, CSIR Institute of Genomics and Integrative Biology, Mall Road, Delhi 110007, India and 4Bioinformatics Centre, CSIR Institute
of Microbial Technology, Sector 39-A, Chandigarh 160036, India

*Corresponding author: Tel: +91 9650466002; Fax: +91 11 27667471; Email: [email protected]
y
These authors contributed equally to this work.

Submitted 17 October 2012; Revised 8 April 2013; Accepted 11 April 2013

Citation details: Bhartiya,D., Pal,K., Ghosh,S., et al. lncRNome: a comprehensive knowledgebase of human long noncoding RNAs. Database (2013)
Vol. 2013: article ID bat034; doi:10.1093/database/bat034.

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The advent of high-throughput genome scale technologies has enabled us to unravel a large amount of the previously
unknown transcriptionally active regions of the genome. Recent genome-wide studies have provided annotations of a
large repertoire of various classes of noncoding transcripts. Long noncoding RNAs (lncRNAs) form a major proportion of
these novel annotated noncoding transcripts, and presently known to be involved in a number of functionally distinct
biological processes. Over 18 000 transcripts are presently annotated as lncRNA, and encompass previously annotated
classes of noncoding transcripts including large intergenic noncoding RNA, antisense RNA and processed pseudogenes.
There is a significant gap in the resources providing a stable annotation, cross-referencing and biologically relevant infor-
mation. lncRNome has been envisioned with the aim of filling this gap by integrating annotations on a wide variety of
biologically significant information into a comprehensive knowledgebase. To the best of our knowledge, lncRNome is one
of the largest and most comprehensive resources for lncRNAs.
Database URL: http://genome.igib.res.in/lncRNome
.............................................................................................................................................................................................................................................................................................

The noncoding RNA transcripts have been classified into a

Introduction number of subclasses, with the most popular classification
The availability of technology to annotate transcriptomes being based on their size, such as the class of small noncod-
at the genome-scale and single-nucleotide resolution has in ing RNAs, which include the well-annotated microRNAs
the recent years provided a new outlook at the transcribed (miRNAs) (6), small nucleolar RNAs (snoRNAs), long noncod-
regions within the Human genome (1–3). Contrary to the ing RNAs (lncRNAs) and so on.
popular belief, a large number of genomic loci have been Long noncoding RNAs (lncRNAs), by definition, are tran-
presently annotated to be transcriptionally active (4). scripts that are >200 nucleotides in length and do not have
Many of these regions do not have the potential to the potential to encode for proteins exceeding lengths of
encode for functional proteins and thus constitute a class 30 amino acids (7, 8). Transcriptome annotation in recent
of transcripts, popularly annotated as noncoding RNA (5). years has significantly expanded the repertoire of lncRNAs,

.............................................................................................................................................................................................................................................................................................
ß The Author(s) 2013. Published by Oxford University Press.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/
licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly
cited. Page 1 of 6
(page number not for citation purposes)
Original article Database, Vol. 2013, Article ID bat034, doi:10.1093/database/bat034
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not just in humans, but also in other model systems like per the needs of a user. To this end, the structure was
mouse (9) and zebrafish (10, 11). Although noncoding tran- designed following consultation with a number of experi-
scripts with >200 nucleotide lengths have been clubbed mental and computational biologists. We created the data-
together in a general classification of lncRNAs, the mem- base to serve as a comprehensive, user-friendly and
bers of this class have significant differences in their biolo- biologically relevant knowledgebase on human lncRNAs
gical function, genomic loci and regulation. This class built on MySQL 5.6 and having a PHP-based web interface.
includes previously known classes of ncRNAs including the In brief, each lncRNA gene has a single page with
large intergenic noncoding RNA, transcribed pseudogenes, basic linkouts to other relevant databases, annotation sets
antisense transcripts and several others, including the and relevant categories of information linked in tabs. Five
annotated classes of functionally distinct transcripts such categories of information are presently available linked
as Xist, which is involved in X inactivation (12) and Hotair with each lncRNA, which includes (i) General Information,
(13), involved in epigenetic regulation. (ii) Sequence and Structure, (iii) Interactions and Processing,
Functionally, the lncRNA class encompasses a wide var- (iv) Variations and Conservation and (v) Epigenetic
iety of distinct functions like X-chromosome inactivation, Modifications. These categories are connected to the
modulation of chromatin structure, regulation of transcrip- genome browser along with the conservation scores of all
tional and posttranscriptional processes and epigenetic lncRNA transcripts (Supplementary File S1).
modifications (14). The biological function of lncRNAs is The category ‘General Information’ hosts information

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modulated through interaction with other biomolecules like the gene name, Ensembl gene ID, gene type, gene
in the cell, such as DNA, RNA and proteins (15). Recent status, Ensembl transcript ID, transcript name, transcript
evidence has also indicated putative regulatory roles type, transcript status, chromosome, strand and genomic
for smaller RNAs processed from lncRNAs, as well as loci, all of which have been fetched from Gencode release
for lncRNAs themselves that harbor regulatory motifs 12 (http://www.gencodegenes.org) (34). The gene names
(16, 17). lncRNAs could be regulated in a different way were used to map the HGNC ID, Refseq ID, Havana gene
than protein-coding genes (18). Recent evidence also sug- ID, Havana transcript ID, NCBI ID and chromosomal loci
gests the role of lncRNAs in several diseases including a from HUGO Gene Nomenclature Committee website (35).
number of cancers like lung cancers, colorectal and blood The length was calculated using the genomic loci. The
neoplasia (7, 19). Candidate lncRNAs like NEAT2 and details about lncRNA description, disease associations,
MALAT1 have been studied in detail with their relations interactions, overexpression and references were manually
with metastasis in cancers (20–22). Additional candidates curated through literature. The alternate transcripts were
like ANRIL have been implicated in diseases like atheroscler- derived using in-house scripts and all lncRNAs were pro-
osis, (23, 24) while a number of candidate genome-wide vided stable internal IDs.
association loci map to regions presently annotated as The lncRNA sequences were downloaded from UCSC
lncRNA genes (25). It has been also suggested that a con- Genome Browser Database (36), and the structures were
ceptual understanding of lncRNA as a function of the bio- predicted using RNAfold version 1.8.5. Both the parenthesis
logical interactions would help to understand disease structure and the minimum free energy structure predicted
processes and develop potential drug targets (26). using the default parameters have been provided.
There are several comprehensive databases for other The third category comprises lncRNA interactions with
ncRNAs like miRNAs (27–30), snoRNAs (31); however, proteins and other RNAs, lncRNA processing, predicted
there is a paucity of such databases integrating biologically open reading frames (ORFs) and various motifs. The data-
significant annotations for lncRNAs. Although there are base hosts 937 quadruplex and 40 hairpins motifs present in
lncRNA databases coming up like lncRNAdb (32), lncRNAs. Both the motifs have been predicted using tools
NONCODE (33), etc., the extent of lncRNA annotations developed ‘in-house’, Quadfinder (37) and HairpinFetcher,
still remains stringent. lncRNome has been formulated to respectively. It also hosts 3716 miRNA binding sites on
integrate annotations on a wide variety of biologically sig- lncRNA. More than 10 000 binding sites for nine other pro-
nificant information into a comprehensive knowledgebase. teins, which have been summarized in the section ‘Datasets
To the best of our knowledge, lncRNome is one of the and Features’, have been provided. These datasets have
largest catalogs for lncRNAs till date, and is available been mapped using PAR-CLIP (38) and CLIP-Seq datasets
online at the URL: http://genome.igib.res.in/lncRNome. as described in the later sections. There are 6808 predicted
protein-binding sites also provided in the database, which
were predicted using Support Vector Machine–based evalu-
Database design and architecture ation of interaction propensities. The 1692 small RNA
The lncRNome database has been designed keeping in processing sites have also been provided as described in
mind both experimental and computational biologists, so the sections below. The fourth category consists of
as to provide ready access to biologically relevant data as 345 351 genomic variations mapped to lncRNAs. The

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Database, Vol. 2013, Article ID bat034, doi:10.1093/database/bat034 Original article
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database of single nucleotide polymorphisms (dbSNP) transcripts (36). RNA structures were computed using
SNPs were downloaded from UCSC genome browser and RNAfold with default parameters, which is part of the
mapped to lncRNAs. Conservation scores of 66 573 sites Vienna RNA package version 1.8.5. Our group has previ-
within lncRNAs have been provided in this category. The ously suggested the presence of G-quadruplex motifs in
fifth category provides 11 790 epigenetic marks in the pro- lncRNAs that could have potential regulatory functions
moters of lncRNAs. The datasets were downloaded from (39). To enable researchers to further take up experiments
the NIH Human Epigenome Roadmap project and in this area, predictions of potential G-quadruplex forming
mapped to lncRNA promoters. The detailed methods are motifs in entire lncRNA transcripts predicted using
available as Supplementary methods. Quadfinder have been included (37), as well as potential
The database also features a comprehensive search hairpin structures in the lncRNA have been identified
option, which enables users to search through lncRNome using HairpinFetcher.
using different keywords, such as, lncRNA names, Ensembl
IDs, known targets, SNPs, diseases, etc. In addition, a separ- lncRNA processing
ate browse option also allows users to browse the database A recent study conducted by our lab has pointed to a subset
through either using the chromosome numbers or different of lncRNAs, which could be potentially processed to small
lncRNA biotypes. The database also features a genome RNAs having downstream regulatory functions by having a
browser, which can be used to browse through the dual transcriptional output (40). The same analysis was

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genome for representative features and also provides a replicated on the present large datasets of lncRNAs. In
visual representation of the associated genomic annota- brief, smallRNA clusters were derived from DeepBase (41),
tions available within the database mentioned above a comprehensive database of smallRNA annotations
along with the conservation scores of lncRNAs. derived from smallRNA sequencing experiments available
in the public domain and overlaid on the lncRNA annota-
tions to derive information on potential lncRNAs that could
Datasets and features be processed to smallRNAs.
Long noncoding RNA annotations Protein-RNA interactions
lncRNA annotations were derived from Gencode release 12 Recent high-throughput experimental methods for analysis
(http://www.gencodegenes.org) (34), which consists of of interactions through pull down and sequencing tech-
11 790 lncRNA genes and 18 855 transcripts. The lncRNAs niques have provided critical insights into the landscape
transcripts are classified into 10 different biotypes, the stat- of protein–RNA interactions in the human genome (42).
istics of which has been provided in the Figure 1. In add- One of the major datasets of protein–RNA interactions is
ition, the datasets of lncRNAs and their HGNC IDs were derived from PAR-CLIP (38) experiments for Argonaute
derived from the Human Gene Nomenclature Committee (Ago) proteins, which are critical components of the RISC
website (35), which consisted of 1073 lncRNAs. Additional machinery involved in miRNA targeting. A comprehensive
mappings were derived for 99 human lncRNAs from mapping of potential Ago binding sites in the lncRNA tran-
lncRNAdb and from literature through manual curation scriptome is provided by mapping the reads to the human
and overlapped with each other based on genomic coord- transcriptome. Experimental datasets also exist for other
inates (Figure 2). A stable internal ID is also provided for proteins including IGF2BP2, IGF2BP3, IGF2P1, PTB, PUM2,
easy access and to enable cross-referencing between the QKI, TNRC6A, TNRC6B and TNRC6C, which have also been
different IDs regularly used by different sequence data- mapped to the lncRNA transcripts. Because the number of
bases. The consensus IDs forms the primary reference key experimental datasets for protein–RNA interactions is
within lncRNome and has also been used to reference al- scarce, we also incorporated a computational prediction
ternate transcript isoforms. Wherever appropriate, all method involving Support Vector Machine–based predic-
lncRNAs have also been linked back to relevant databases tion of residues in RNA, which could have probable propen-
such as Ensembl, HGNC and NCBI for quick cross-reference. sity to interact with proteins (Panwar and Raghava 2012,
The manual annotation of the functionally characterized unpublished results).
lncRNAs is provided, which includes information about the
disease associations, expression and functional significance. Genomic variations and conservation
The annotations are collected from literature surveys and Genome-wide association studies in the recent past have
manual curations. suggested disease associations, which could be modulated
by lncRNAs (43). In addition, a number of genomic loci pre-
Sequence and structure and motifs viously shown to be associated with diseases have now
The lncRNA sequences were downloaded from UCSC been indicated to fall within lncRNA gene loci. To facilitate
Genome Browser using genomic locations of individual further in-depth analysis and experimental validation of

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Original article Database, Vol. 2013, Article ID bat034, doi:10.1093/database/bat034
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Figure 1. Distribution of Gencode release 12 lncRNAs according to different biotypes.

effect of variations on lncRNA, we have included a compre- Conclusions and future

hensive mapping of genomic variations in lncRNA loci. In
brief, the variations corresponding to dbSNP 135 were
perspectives
downloaded (44) and mapped to respective genomic loca- lncRNome is designed to primarily serve as an evidence-
tions of lncRNAs. In addition, disease associated variations based resource of lncRNAs and their functionality in
were derived from the NIH Catalog of published genome- humans. To this end, we have provided stable reference
wide association studies and mapped to respective rsIDs. IDs for lncRNA genes and alternate transcript isoforms of
The PhastCons conservation scores were downloaded from a gene with cross-references to other sequence and anno-
UCSC and the genomic loci were mapped to lncRNAs (45). tation databases to ensure interoperability and stable
referencing. The knowledge base integrates biologically
Epigenetic modifications oriented datasets and resources on lncRNA and manual an-
notations wherever applicable with the aim of providing a
A recent report from our group suggests that the pro-
one-stop solution for annotation information on lncRNAs.
moters of lncRNAs could be potentially regulated by mech-
The interface allows an easy access to various features of
anisms that are distinct from protein-coding genes
lncRNAs comprised within five categories and their suble-
supporting the role of lncRNAs in epigenetic regulation of
vels (Supplementary Figure S1). The category ‘General’ pro-
genes. To capture the epigenetic marks, in terms of DNA
vides all the basic annotations of each lncRNA including
methylation and histone marks, we have provided a com-
genomic loci, the associated diseases and various linkouts.
prehensive access to epigenetic marks in the promoters of
The sequences and the predicted structure of the lncRNA
lncRNAs. Briefly the raw datasets were downloaded from
are provided in the category ‘Sequence and Structure’. The
the NIH Human Epigenome Roadmap project and mapped
lncRNA structures are poorly understood and it becomes
and analyzed as described in Sati et al. (46). The epigenetic
indispensable to characterize the structures to elucidate
marks are also available for browsing through the genome
the structure–function relationships. Specific lncRNA struc-
browser. The datasets and genomic mappings are compiled
tures are essential for binding to proteins, RNA and other
in Table 1.
biomolecules, and to have a better mechanistic insight of
lncRNA function, elucidation of its structure becomes
Predicted peptides important. lncRNome provides information of various hair-
The open reading frames were predicted for all the pin and quadruplex motifs in lncRNAs found to be essen-
lncRNAs using the Sixpack (http://www.ebi.ac.uk/Tools/st/ tial for regulation of a lot of biological processes. Both
emboss_sixpack/) tool from EMBOSS. The tool translates experimental and prediction datasets on RNA–protein
the given sequence in six frames and peptides starting interactions have been provided for lncRNAs revealing var-
with Methionine and with length 10 amino acids. ious protein and RNA interacting partners of lncRNAs

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Database, Vol. 2013, Article ID bat034, doi:10.1093/database/bat034 Original article
.............................................................................................................................................................................................................................................................................................

availability of a large number of transcriptome sequencing

datasets in public domain, lncRNome in the present form
has many gaps. The primary gap being the paucity of infor-
mation on expression of lncRNAs in different tissues. With
the availability of genome-wide transcriptome annotation
of many tissues in the public domain, we would enrich the
database with this information. We intend to collaborate
with other international consortiums to enable cross-
linking and sharing of resources seamlessly. In future, we
envisage the database to be available as a community-
curated and semantically linked interoperable data
resource.

Supplementary Data
Supplementary data are available at Database Online.

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Figure 2. Comparison of annotations between other data-
bases/datasets on long noncoding RNAs.
Acknowledgements
The authors acknowledge Dr V. Sabareesh, Dr Harleen Kaur
Table 1. Total fields in the database along with the genomic and Ms Ayesha Pasha for reviewing the manuscript. D.B.
loci mapped
and S.S. acknowledge a Senior Research fellowship from
Serial No. Database fields Total genomic CSIR, and S.K. acknowledges support through a Junior
loci mapped Research fellowship from CSIR. The authors acknowledge
the funding for this work from the Council of Scientific
1 Total lncRNAs 18 855
and Industrial Research (CSIR), India through the project
2 Hairpins 40
GENCODE-C (BSC00123).
3 Methylation and histone 11 790
modifications Conflict of interest. None declared.
4 miRNA binding sites 3716
5 Quadruplexes 937
6 Predicted protein-binding 6808 References
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