Published online 5 November 2007 Nucleic Acids Research, 2008, Vol. 36, Database issue D57–D62
UTRome.org: a platform for 3’UTR biology in
Marco Mangone, Philip MacMenamin, Charles Zegar, Fabio Piano and Kristin C. Gunsalus*
Department of Biology and Center for Genomics and Systems Biology, New York University, 100 Washington
Square East, New York, NY 10003, USA
Received August 16, 2007; Revised October 11, 2007; Accepted October 16, 2007
widely recognized as important post-transcriptional
regulatory regions of mRNAs. RNA-binding proteins
and small non-coding RNAs such as microRNAs
(miRNAs) bind to functional elements within 3’UTRs
to influence mRNA stability, translation and locali-
zation. These interactions play many important roles
in development, metabolism and disease. However,
genomes, 3’UTRs and their functional elements are
not well defined. Comprehensive and accurate
functional elements is thus critical. We have devel-
oped an open-access database, available at http://
www.UTRome.org, to provide a rich and compre-
hensive resource for 3’UTR biology in the well-
system Caenorhabditis elegans. UTRome.org com-
bines data from public repositories and a large-
scale effort we are undertaking to characterize
3’UTRs and their functional elements in C. elegans,
including 3’UTR sequences, graphical displays,
predicted and validated functional elements, sec-
ondary structure predictions and detailed data from
our cloning pipeline. UTRome.org will grow sub-
stantially over time to encompass individual 3’UTR
isoforms for the majority of genes, new and revised
functional elements, and in vivo data on 3’UTR
function as they become available. The UTRome
database thus represents a powerful tool to better
understand the biology of 3’UTRs.
of3’UTRs and their
Three-prime untranslated regions (30UTRs) are untrans-
lated portions of mRNAs located at the 30flanking end of
open reading frames (ORFs). These regions are implicated
in post-transcriptional regulation of gene activity through
interaction with regulatory RNA-binding proteins and
small non-coding RNAs such as miRNAs, which can
influence protein activity by altering mRNA stability,
translational efficiency or localization (1–6). Regulation at
the level of 30UTRs, by both regulatory proteins and small
RNAs, plays essential roles in diverse developmental and
metabolic processes and is also implicated in disease (1–6).
miRNAs, which bind to short complementary sequences
in 30UTRs of metazoans, represent one of the best studied
families of 30UTR regulators (4,5). Based on bioinformatic
analysis of predicted miRNA-binding sites in 30UTRs, it
has been proposed that each miRNA controls a network
of proteins in vivo, and that collectively thousands of
transcripts are likely to be regulated by miRNAs (7).
Due to the critical role that 30UTRs play in living cells,
it is important to study these regions in detail to uncover
and characterize as many embedded regulatory elements
as possible. However, 30UTRs are still incompletely
annotated in metazoan genomes, including humans (7).
Even in Caenorhabditis elegans, one of the best annotated
metazoan genomes, only about half of known transcripts
have an annotated 30UTR (8,9). Recent studies indicate
that a substantial proportion of characterized transcripts
in humans and other species experience alternative
splicing of a terminal exon or alternative polyadenlyation
(polyA) site usage (10–12). For example, careful curation
of mRNA sequence data shows that at least one-third of
genes analyzed in human, mouse and Arabidopsis, and
over 10% in C. elegans, express transcripts that share a
terminal exon but use different polyA signal (PAS) sites,
resulting in 30UTRs of different lengths [(12); D. and
J. Thierry-Mieg, personal communication]. Both 30UTR
isoforms and regulation can vary in a tissue-specific
manner (13,14), and a significant fraction of predicted
miRNA target sites in human genes are located in
alternative UTR segments (15). These studies suggest
that heterogeneity and combinatorial control of 30UTR
isoforms are likely to play a more significant role in
regulation of gene activity than previously appreciated.
The authors wish it to be known that, in their opinion, the first two authors should be regarded as joint First Authors.
*To whom correspondence should be addressed. Tel: +1 212 998 8236; Fax: +1 212 995 4015; Email: firstname.lastname@example.org
? 2007 The Author(s)
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/
by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Increased interest in 30UTRs has spawned several new
resources focused on 30UTRs and their functional
elements, such as UTRdb and UTRsite (16), PACdb
(17), Poly_A db (18), PicTar (19), TargetScan (20) and
miRanda (21), which use cross-species alignments and
EST data to predict or highlight elements within UTRs
that may have a functional role in RNA maturation or
post-transcriptional gene regulation. However, only some
of these contain data specific for C. elegans and none are
dedicated as a comprehensive archive for all aspects of
30UTR biology within a specific tractable model system.
We have therefore developed a database focused on
UTRome.org, intended as a comprehensive resource for
30UTR biology in C. elegans. The design and implementa-
tion we have established for UTRome.org could easily be
adapted for the analysis of 30UTRs in other species,
The UTRome database provides up-to-date information
on 30UTR structures and functional elements for every
C. elegans mRNA based on combined data from public
repositories such as WormBase (8,9) and continuously
updated results from an ongoing high-throughput pipeline
we have developed to define 30UTRs and their isoforms
(Figure 1A). Information about functional elements
within 30UTRs currently includes computationally pre-
dicted miRNA-binding sites [derived from the PicTar
(19,22) and MiRanda (21) algorithms], putative PAS sites
[computed based on Ref. (23)], and predicted secondary
structures [using the MFOLD algorithm (24)]. For each
30UTR, users can view or download secondary structure
prediction diagrams and browse graphical coordinate-
based displays illustrating gene models, 30UTR products
from our cloning pipeline, previously annotated evidence
for 30UTRs from ESTs and mRNAs, putative PAS sites
and predicted or validated miRNA-binding sites. We also
provide a detailed description of data produced by our
cloning pipeline, including status of cloning and annota-
tion, ABI trace files, BLAT (25) and BLAST (26)
alignments to the genome, and annotated agarose gel
images of RT-PCR products used for cloning. As new
data become available, UTRome.org will grow substan-
tially over time to encompass individual isoforms for the
majority of genes, improved predictions for miRNA-
binding sites based on updated 30UTR annotations and
additional sequenced genomes, and results from in vivo
analyses of 30UTR structure and function, including
of specific functional
DESIGN AND IMPLEMENTATION
UTRome.org uses an Apache web server and a collection
of Perl CGI scripts coupled to a MySQL database
to provide an intuitive user interface for 30UTR data.
The main UTRome database schema archives sequence
and functional informationon30UTRs andtheir
corresponding genes, coding sequences (CDSs) and
functional elements. It also serves as an electronic lab
notebook to track all stages of our in-house 30UTR
cloning and annotation pipeline: from initial RT-PCR
through generation of first-pass UTR sequence tags
(USTs) based on automated BLAT and BLAST analysis,
final sequence verification of 30UTRs, and annotation of
functional elements (a full description of this pipeline will
be published elsewhere). A second light-weight GFF
database (27) stores coordinate-based data for generating
graphical displays of sequence-based annotations, which
are generated dynamically using Bio::DB::GFF (part of
BioPerl, http://www.bioperl.org) and the Generic Genome
Browser (GBrowse) (27). An automated set of scripts
generates first-pass annotations from our cloning pipeline
from batches of raw sequence traces using BLAT and
BLAST and deposits the raw sequence data, USTs, and
validated 30UTR sequences into the database on an
ongoing basis. Data are extracted from external data
sources using Perl scripts [e.g. from WormBase’s AceDB
engine (28,29)] and imported using Perl or MySQL scripts.
The UTRome database currently contains a compre-
hensive collection of all ?26000C. elegans transcripts
from WormBase release WS180 and 30UTR sequence
annotations from our cloning pipeline. All coordinate-
based data will be updated regularly and synchronized
with each new WormBase freeze. The entire UTRome.org
database and data processing framework could easily be
adapted for any other organism by coupling the system to
data import protocols compatible with different public
repositories [e.g. FlyBase (30), etc.].
The Welcome page contains a query box in the top right
corner (mirrored in each page of the website), which lets
the user search for a specific 30UTR or for multiple
30UTRs using wildcards. The accompanying pull-down
menu allows users to search across the entire genome
(‘UTRome & Genome’) or to limit queries to genes
targeted by our cloning pipeline (‘UTRome Only’).
A productive search returns a comprehensive list of
genes and 30UTRs matching the query (Figure 1C). For
each gene in the result list, we provide general information
such as the Cosmid ID, Locus name, Chromosome and
a brief description (accessible by mousing over any Gene
or 30UTR). The first column indicates whether the
corresponding gene is targeted by our pipeline (blue if in
the UTRome project, empty otherwise). If the 30UTR has
been annotated by WormBase or the annotation from
UTRome has been finalized, we indicate its length in base
pairs. For 30UTRs in our cloning pipeline, we assign a
color-coded flag (green, orange or red circles) as an
indicator of confidence as to whether a given UST is a
bona fide 30UTR for the targeted gene. These preliminary
annotations will be updated to final curation status on an
ongoing basis as the project evolves. At the bottom of this
and every page in on the website, we include a menu bar
Nucleic Acids Research, 2008, Vol. 36, Databaseissue
Figure 1. Overview of UTRome.org. The UTRome database integrates diverse information on C. elegans 30UTRs. (A) Data on 30UTR boundaries
and predicted or experimentally validated functional elements, collected from multiple database sources or analyzed using various computational
algorithms, are displayed in a series of user-friendly web pages. (B) ‘Locus Information’ page: a sample snapshot of aggregated data. (C) Results
returned for the query ‘lin’ in a search limited to genes targeted by the UTRome project. (D) ‘ABI trace files’ page: a Java applet shows sequence
traces for a UST including part of the polyA tail. (E) Excerpt from a ‘Gel’ page: PCR products from a 96-well cloning experiment indicate evidence
for multiple 30UTR isoforms in well H4 (automatically highlighted by a green box). (F) ‘MFOLD’ page: secondary structure prediction for a 30UTR
showing putative stem-loop structure.
Nucleic Acids Research, 2008, Vol. 36, Database issueD59
containing links to protocols, batch downloads, a tour of
the site, a FAQ page and email for feedback.
Browsing 3’UTR data
Each gene or 30UTR present in the database can be
browsed by clicking on its hyperlink in the Results list,
which brings the user to a tabbed menu of data display
options for the selected gene or 30UTR. The set of tabs
opens by default on a ‘Locus Information’ page provid-
ing general information for the given gene or 30UTR
(Figure 1B): a gene description, a list of alternate 30UTR
isoforms for this gene (if any), 30UTR sequence in FASTA
format (if annotated), a graphical display of the locus
along withannotated functional
separate tables listing the miRNAs predicted to target
the gene [hyperlinked to their corresponding records at
miRBase (31)], external miRNA–target prediction sites
providing more detailed data and sequence alignments
[PicTar (19), and TargetScan (20)], and links to other
WormGenes (12), WorfDB (32), Promoterome (33) and
N-Browse (19)]. Mousing over any of these links displays
a brief description of the external resource. The graphical
display shows the transcript model(s) for the given gene
and, if available, previously mapped ESTs and mRNAs
(from WormBase), predicted miRNA-binding sites (from
both PicTar and miRanda), and sequence conservation
with the C. briggsae genome. Additional conservation
tracks will be included in future releases. A link to a local
installation of GBrowse allows the user to study the region
in more detail if desired, including zooming in to the
nucleotide level. A web form near the bottom of the page
allows users to submit (anonymously, if desired) com-
ments, suggestions or requests (e.g. for inclusion of
additional data) to the database administrator.
A second tab labeled ‘Fold’ links to a webpage dis-
playing the predicted secondary structure for the 30UTR
region of the corresponding transcript (Figure 1F),
calculated using the MFOLD algorithm (24). Secondary
structures in RNA molecules may influence the accessi-
bility of sequence-specific recognition motifs by factors
such as miRNAs and can also serve as structural features
recognized by some RNA-binding proteins (6). Although
MFOLD predictions are not experimentally validated,
they represent a valuable starting point to model the
interaction of the given 30UTR with RNA-binding factors.
Taken together, these resources provide a powerful tool to
study C. elegans 30UTRs by synthesizing all the publicly
available information for 30UTRs genome-wide.
If the given 30UTR has been cloned by our group,
additional options will appear in the tabbed menu bar at
the top of the page: ‘UTR cloning’, ‘ABI trace file’, ‘Gel’
and ‘Plate’. The ‘UTR cloning’ page provides detailed
cloning information and a graphical interpretation of new
30UTR annotations produced by our pipeline (Figure 2
shows several examples). Here a brief description of the
gene is followed by a ‘Cloning status’ table, which includes
the sequence of the primer used for cloning, its melting
temperature (Tm) and the contiguous length of the best
BLAT alignment of the UST to the C. elegans genome for
the 30UTR clone of interest. The next panel, ‘30UTR
bioinformatic analysis’, contains a computer-generated
summary of the first-pass annotation from our pipeline,
indicating cloning progress and UST quality (e.g. whether
the sequence contains a poly-A tail, aligns at the expected
locus, and contains portions of the primer used for
RT-PCR). A human-curated summary is also included
when further manual analysis has been performed. The
third panel, ‘Picture’, provides a graphical depiction of the
30UTR region of the transcript along the chromosome.
Color-coded tracks show BLAT and WU-BLAST align-
ments of the UST to the genome in the vicinity of the
given transcript: ‘Green’ glyphs represent USTs that
passed our internal quality-control tests, ‘Orange’ glyphs
indicate USTs that have been partially validated and ‘Red’
glyphs depict USTs that failed our validation tests and
have been re-submitted to the cloning pipeline. Also
displayed are PicTar and miRanda predictions for
miRNA-binding sites, any putative PAS motifs, ESTs
and mRNA evidence that support the current transcript
models, and conservation with C. briggsae. Additional
data on functional elements and sequence conservation
will be incorporated as new data become available. This
‘Picture’ panel thus provides a comprehensive snapshot of
the 30UTR and any known or predicted functional
elements within it.
The remaining three tabs document raw data for
30UTRs in our cloning pipeline. First, the ‘ABI trace file’
page (Figure 1D) allows the user either to view the
chromatogram produced by the ABI sequencer corre-
sponding to the given UST, or to download it in SCF
format. The chromatogram is rendered graphically using a
Java applet, which enables the user to browse the entire
sequence trace from 50to 30, to extract the sequence in
FASTA format, and view comments produced by the ABI
sequencer. This page enables interactive access to the raw
sequence data and its inspection at a great level of detail.
Similarly, the ‘Gel’ page (Figure 1E) shows an agarose
gel image containing the PCR bands for a set of 96 cloned
USTs, with the UST of interest highlighted for easy
reference. This raw data can provide information about
30UTR heterogeneity since additional bands could indi-
cate the presence of multiple, previously undocumented,
isoforms in the original mini-pool. We are following up on
all such cases to isolate individual alternative 30UTR
isoforms. Finally, the ‘Plate’ page, designed for internal
use, features cloning information such as plate coordinates
corresponding to the frozen stocks and barcode informa-
tion for the various stages in the cloning pipeline.
One of the primary goals of the UTRome database is to
provide continuous improvements to the comprehensive
annotation of 30UTRs and their functional elements in
C. elegans. Part of this mission is to provide an interface
for our cloning pipeline for curation and quality control,
and ultimately to use our data to improve the 30UTR
annotations in genomic repositories like WormBase.
As part of the modENCODE Consortium, an initiative
Nucleic Acids Research, 2008, Vol. 36, Databaseissue
from the National Human Genome Research Institute
(NHGRI) to provide genome-wide characterization of
sequence-based functional elements in the C. elegans
and Drosophila melanogaster genomes (see http://www.
modencode.org), we have been tasked to generate high-
quality 30UTR annotations for one-third of the C. elegans
validated 30UTRs) from this set will also flow into the
modENCODE Data Coordination Center (DCC) data-
base (to be hosted at http://www.modencode.org). We are
continuously updating the UTRome database with new
30UTR data from our cloning pipeline and plan to extend
the project to the entire genome of C. elegans. We have
also prototyped an in vivo pipeline, using fluorescent
reporter constructs, to identify functional elements med-
iating post-transcriptional gene regulation within cloned
30UTRs (19). We plan to extend and scale up this
approach using the library of 30UTR clones we are
currently generating and to incorporate these data into the
UTRome database. Over the next few years, we also
anticipate a new influx of data for C. elegans on expression
patterns of miRNAs, 30UTR isoforms, and improved
prediction of functional elements, which we envision
incorporating into the UTRome along with additional
analysis tools. Our vision for UTRome.org is to provide a
comprehensive resource to access and analyze these data,
Figure 2. Experimental analysis of 30UTRs. Three examples of USTs from our cloning pipeline aligned to the C. elegans genome using BLAT and
WU-BLAST algorithms. (A) Validation of previously annotated 30UTR: the length of the UST produced by our pipeline matches that of the
annotated 30UTR for transcript C03D6.4. (B) New experimental 30UTR evidence for a transcript with no previous experimental support (C07H4.1).
The UST contains a putative polyA addition site and a polyA tail, suggesting a true end for this 30UTR, and overlaps several predicted miRNA-
binding sites. (C) Improved 30UTR annotation: evidence for a longer alternate 30UTR isoform for a gene with a short previously annotated 30UTR
(C05D10.3). The UST sequence overlaps the 30UTR of another transcript (C05D10.1a) in the opposite orientation. miRNA-binding sites have been
predicted for C05D10.1 but not for C05D10.3. If both genes are transcribed simultaneously, these overlapping transcripts could potentially lead to
the production of double-stranded RNA and endogenous small interfering RNAs (siRNAs). In all panels, putative polyA signal and miRNA-binding
sites are indicated in green or red for transcripts oriented left-to-right or right-to-left, respectively.
Nucleic Acids Research, 2008, Vol. 36, Database issueD61
thus greatly enhancing our overall understanding of Download full-text
30UTR biology and helping the scientific community
achieve a better understanding of the mechanisms used
by cells to control post-transcriptional gene regulation in
this and other organisms.
We thank Danielle and Jean Thierry-Mieg for sharing
statistics on alternative transcript isoforms and insightful
discussions on sequence curation, Ravi Sachidanandam
for kindly providing us with the TraceView Java applet,
Michael Zuker for suggestions on how to install and
configure MFOLD, Victor Chistyakov for help with the
AJAX auto-suggest feature, Nikolaus Rajewsky and his
research group for fruitful collaborations on 30UTR
biology, Kevin Chen for helpful comments on the manu-
script, and the modENCODE Consortium for propelling
this project forward. This work was supported by grants
from the National Human Genome Research Institute
(R21HG003971 and 1U01HG004276). Funding to pay the
Open Access publication charges for this article was
provided by NHGRI award 1U01HG004276.
Conflict of interest statement. None declared.
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