Abstract
Although transcriptional and posttranscriptional events are detected in RNA-Seq data from second-generation sequencing, full-length mRNA isoforms are not captured. On the other hand, third-generation sequencing, which yields much longer reads, has current limitations of lower raw accuracy and throughput. Here, we combine second-generation sequencing and third-generation sequencing with a custom-designed method for isoform identification and quantification to generate a high-confidence isoform dataset for human embryonic stem cells (hESCs). We report 8,084 RefSeq-annotated isoforms detected as full-length and an additional 5,459 isoforms predicted through statistical inference. Over one-third of these are novel isoforms, including 273 RNAs from gene loci that have not previously been identified. Further characterization of the novel loci indicates that a subset is expressed in pluripotent cells but not in diverse fetal and adult tissues; moreover, their reduced expression perturbs the network of pluripotency-associated genes. Results suggest that gene identification, even in well-characterized human cell lines and tissues, is likely far from complete.
Keywords
PacBio
alternative splicing
hESC transcriptome
isoform discovery
lncNRA
MeSH Terms
Alternative Splicing/genetics
Embryonic Stem Cells/chemistry,metabolism
Gene Expression Profiling/methods
High-Throughput Nucleotide Sequencing/methods
Humans
Male
Protein Isoforms/genetics
Transcriptome/genetics
Chemicals
Protein Isoforms
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Au Kin Fai
Department of Statistics and Department of Health Research and Policy, Stanford University, Stanford, CA 94305.
Sebastiano Vittorio
Afshar Pegah Tootoonchi
Durruthy Jens Durruthy
Lee Lawrence
Williams Brian A
van Bakel Harm
Schadt Eric E
Reijo-Pera Renee A
Underwood Jason G
Wong Wing Hung
References (32)
32 references, click to expand
-
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
-
Rapid cDNA sequencing (expressed sequence tags) from a directionally cloned human infant brain cDNA library.
Nat Genet. 1993 Aug;4(4):373-80
PMID: 8401585
-
Landscape of transcription in human cells.
Nature. 2012 Sep 6;489(7414):101-8
PMID: 22955620
-
Detection of splice junctions from paired-end RNA-seq data by SpliceMap.
Nucleic Acids Res. 2010 Aug;38(14):4570-8
PMID: 20371516
-
An integrated encyclopedia of DNA elements in the human genome.
Nature. 2012 Sep 6;489(7414):57-74
PMID: 22955616
-
Ensembl 2011.
Nucleic Acids Res. 2011 Jan;39(Database issue):D800-6
PMID: 21045057
-
Sparse linear modeling of next-generation mRNA sequencing (RNA-Seq) data for isoform discovery and abundance estimation.
Proc Natl Acad Sci U S A. 2011 Dec 13;108(50):19867-72
PMID: 22135461
-
Simultaneous isoform discovery and quantification from RNA-seq.
Stat Biosci. 2013 May 1;5(1):100-118
PMID: 23888185
-
Consensus folding of aligned sequences as a new measure for the detection of functional RNAs by comparative genomics.
J Mol Biol. 2004 Sep 3;342(1):19-30
PMID: 15313604
-
Improving PacBio long read accuracy by short read alignment.
PLoS One. 2012;7(10):e46679
PMID: 23056399
-
Identifiability of isoform deconvolution from junction arrays and RNA-Seq.
Bioinformatics. 2009 Dec 1;25(23):3056-9
PMID: 19762346
-
Nuclear RNA sequencing of the mouse erythroid cell transcriptome.
PLoS One. 2012;7(11):e49274
PMID: 23209567
-
Structured RNAs in the ENCODE selected regions of the human genome.
Genome Res. 2007 Jun;17(6):852-64
PMID: 17568003
-
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation.
Nat Biotechnol. 2010 May;28(5):511-5
PMID: 20436464
-
The UCSC Known Genes.
Bioinformatics. 2006 May 1;22(9):1036-46
PMID: 16500937
-
Statistical inferences for isoform expression in RNA-Seq.
Bioinformatics. 2009 Apr 15;25(8):1026-32
PMID: 19244387
-
GENCODE: producing a reference annotation for ENCODE.
Genome Biol. 2006;7 Suppl 1:S4.1-9
PMID: 16925838
-
Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps.
Nature. 2009 Jul 23;460(7254):479-86
PMID: 19536157
-
HITS-CLIP yields genome-wide insights into brain alternative RNA processing.
Nature. 2008 Nov 27;456(7221):464-9
PMID: 18978773
-
NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy.
Nucleic Acids Res. 2012 Jan;40(Database issue):D130-5
PMID: 22121212
-
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
-
Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling.
Science. 2009 Apr 10;324(5924):218-23
PMID: 19213877
-
Widespread RNA and DNA sequence differences in the human transcriptome.
Science. 2011 Jul 1;333(6038):53-8
PMID: 21596952
-
RNAz 2.0: improved noncoding RNA detection.
Pac Symp Biocomput. 2010;:69-79
PMID: 19908359
-
RNA-Seq: a revolutionary tool for transcriptomics.
Nat Rev Genet. 2009 Jan;10(1):57-63
PMID: 19015660
-
TopHat: discovering splice junctions with RNA-Seq.
Bioinformatics. 2009 May 1;25(9):1105-11
PMID: 19289445
-
Monitoring early differentiation events in human embryonic stem cells by massively parallel signature sequencing and expressed sequence tag scan.
Stem Cells Dev. 2004 Dec;13(6):694-715
PMID: 15684837
-
Mapping and quantifying mammalian transcriptomes by RNA-Seq.
Nat Methods. 2008 Jul;5(7):621-8
PMID: 18516045
-
RNPomics: defining the ncRNA transcriptome by cDNA library generation from ribonucleo-protein particles.
Nucleic Acids Res. 2010 Jun;38(10):e113
PMID: 20150415
-
MapSplice: accurate mapping of RNA-seq reads for splice junction discovery.
Nucleic Acids Res. 2010 Oct;38(18):e178
PMID: 20802226
-
Fast and reliable prediction of noncoding RNAs.
Proc Natl Acad Sci U S A. 2005 Feb 15;102(7):2454-9
PMID: 15665081
-
Mind the gap: upgrading genomes with Pacific Biosciences RS long-read sequencing technology.
PLoS One. 2012;7(11):e47768
PMID: 23185243