Variation in alternative splicing across human tissues.
paper
Cited
Public
- Authors
- Yeo, Gene; Holste, Dirk; Kreiman, Gabriel; Burge, Christopher B
- Year
- 2004
- Journal
- Genome biology
- PMID
- 15461793
- DOI
- 10.1186/gb-2004-5-10-r74
- PMCID
- PMC545594
BACKGROUND: Alternative pre-mRNA splicing (AS) is widely used by higher eukaryotes to generate different protein isoforms in specific cell or tissue types. To compare AS events across human tissues, we analyzed the splicing patterns of genomically aligned expressed sequence tags (ESTs) derived from libraries of cDNAs from different tissues. RESULTS: Controlling for differences in EST coverage among tissues, we found that the brain and testis had the highest levels of exon skipping. The most pronounced differences between tissues were seen for the frequencies of alternative 3' splice site and alternative 5' splice site usage, which were about 50 to 100% higher in the liver than in any other human tissue studied. Quantifying differences in splice junction usage, the brain, pancreas, liver and the peripheral nervous system had the most distinctive patterns of AS. Analysis of available microarray expression data showed that the liver had the most divergent pattern of expression of serine-arginine protein and heterogeneous ribonucleoprotein genes compared to the other human tissues studied, possibly contributing to the unusually high frequency of alternative splice site usage seen in liver. Sequence motifs enriched in alternative exons in genes expressed in the brain, testis and liver suggest specific splicing factors that may be important in AS regulation in these tissues. CONCLUSIONS: This study distinguishes the human brain, testis and liver as having unusually high levels of AS, highlights differences in the types of AS occurring commonly in different tissues, and identifies candidate cis-regulatory elements and trans-acting factors likely to have important roles in tissue-specific AS in human cells.
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| Novel isoforms of the bovine Nuclear factor I/X (CCAAT-binding transcription factor) transcript products and their diverse expression profiles. | Zhou Y et al. | β | 2014 | β |
| Novel mutations causing biotinidase deficiency in individuals identified by newborn screening in Michigan including an unique intronic mutation that alters mRNA expression of the biotinidase gene. | Li H et al. | β | 2014 | β |
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| Targeting SR proteins improves SMN expression in spinal muscular atrophy cells. | Wee CD et al. | β | 2014 | β |
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| A comprehensive characterization of the nuclear microRNA repertoire of post-mitotic neurons. | Khudayberdiev SA et al. | β | 2013 | β |
| Alternative splice variants in TIM barrel proteins from human genome correlate with the structural and evolutionary modularity of this versatile protein fold. | Ochoa-Leyva A et al. | β | 2013 | β |
| Alternative splicing: functional diversity among voltage-gated calcium channels and behavioral consequences. | Lipscombe D et al. | β | 2013 | β |
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| Drift and conservation of differential exon usage across tissues in primate species. | Reyes A et al. | β | 2013 | β |
| Dynamic expression pattern of neuro-oncological ventral antigen 1 (Nova1) in the rat brain after focal cerebral ischemia/reperfusion insults. | Li H et al. | β | 2013 | β |
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| Pleiotropic and isoform-specific functions for Pitx2 in superior colliculus and hypothalamic neuronal development. | Waite MR et al. | β | 2013 | β |
| Reactivation of fetal splicing programs in diabetic hearts is mediated by protein kinase C signaling. | Verma SK et al. | β | 2013 | β |
| RNA-Seq analysis of the parietal cortex in Alzheimer's disease reveals alternatively spliced isoforms related to lipid metabolism. | Mills JD et al. | β | 2013 | β |
| RNA-seq characterization of spinal cord injury transcriptome in acute/subacute phases: a resource for understanding the pathology at the systems level. | Chen K et al. | β | 2013 | β |
| SASD: the Synthetic Alternative Splicing Database for identifying novel isoform from proteomics. | Zhang F et al. | β | 2013 | β |
| The application of proteomic approaches to the study of mammalian spermatogenesis and sperm function. | Macleod G et al. | β | 2013 | β |
| The developing xylem transcriptome and genome-wide analysis of alternative splicing in Populus trichocarpa (black cottonwood) populations. | Bao H et al. | β | 2013 | β |
| The mechanism of alternative splicing of the X-linked NDUFB11 gene of the respiratory chain complex I, impact of rotenone treatment in neuroblastoma cells. | Panelli D et al. | β | 2013 | β |
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| Transcriptional and post-transcriptional regulation of Drosophila germline stem cells and their differentiating progeny. | White-Cooper H et al. | β | 2013 | β |
| Transcriptome analyses of the human retina identify unprecedented transcript diversity and 3.5 Mb of novel transcribed sequence via significant alternative splicing and novel genes. | Farkas MH et al. | β | 2013 | β |
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| Emerging Roles of Alternative Pre-mRNA Splicing Regulation in Neuronal Development and Function. | Norris AD et al. | β | 2012 | β |
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| Mammalian tissues defective in nonsense-mediated mRNA decay display highly aberrant splicing patterns. | Weischenfeldt J et al. | β | 2012 | β |
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| SpliceDisease database: linking RNA splicing and disease. | Wang J et al. | β | 2012 | β |
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| Theory on the coupled stochastic dynamics of transcription and splice-site recognition. | Murugan R et al. | β | 2012 | β |
| The RNA recognition motif protein RBM11 is a novel tissue-specific splicing regulator. | Pedrotti S et al. | β | 2012 | β |
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| Detection of KIAA1549-BRAF fusion transcripts in formalin-fixed paraffin-embedded pediatric low-grade gliomas. | Tian Y et al. | β | 2011 | β |
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| Conserved alternative splicing and expression patterns of arthropod N-cadherin. | Hsu SN et al. | β | 2009 | β |
| CUGBP2 directly interacts with U2 17S snRNP components and promotes U2 snRNA binding to cardiac troponin T pre-mRNA. | Goo YH et al. | β | 2009 | β |
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| Differential splicing using whole-transcript microarrays. | Robinson MD et al. | β | 2009 | β |
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| Functional and evolutionary insights into human brain development through global transcriptome analysis. | Johnson MB et al. | β | 2009 | β |
| Functional role for senataxin, defective in ataxia oculomotor apraxia type 2, in transcriptional regulation. | Suraweera A et al. | β | 2009 | β |
| GarlicESTdb: an online database and mining tool for garlic EST sequences. | Kim DW et al. | β | 2009 | β |
| Genetics of motor neuron disorders: new insights into pathogenic mechanisms. | Dion PA et al. | β | 2009 | β |
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| Genomic landscape of developing male germ cells. | Lee TL et al. | β | 2009 | β |
| Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. | Kim KK et al. | β | 2009 | β |
| Lymphocytes from P2X7-deficient mice exhibit enhanced P2X7 responses. | Taylor SR et al. | β | 2009 | β |
| Sperm cell proteomics. | Oliva R et al. | β | 2009 | β |
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| The germ cell nuclear proteins hnRNP G-T and RBMY activate a testis-specific exon. | Liu Y et al. | β | 2009 | β |
| Als2 mRNA splicing variants detected in KO mice rescue severe motor dysfunction phenotype in Als2 knock-down zebrafish. | Gros-Louis F et al. | β | 2008 | β |
| Alternative isoform regulation in human tissue transcriptomes. | Wang ET et al. | β | 2008 | β |
| Analysis of the human testis proteome by mass spectrometry and bioinformatics. | Guo X et al. | β | 2008 | β |
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| Comparative analysis of sequence features involved in the recognition of tandem splice sites. | Bortfeldt R et al. | β | 2008 | β |
| Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. | Pan Q et al. | β | 2008 | β |
| Global analysis of aberrant pre-mRNA splicing in glioblastoma using exon expression arrays. | Cheung HC et al. | β | 2008 | β |
| Inactive forms of the catalytic subunit of protein kinase A are expressed in the brain of higher primates. | Larsen AC et al. | β | 2008 | β |
| Low conservation and species-specific evolution of alternative splicing in humans and mice: comparative genomics analysis using well-annotated full-length cDNAs. | Takeda J et al. | β | 2008 | β |
| Prediction of alternatively skipped exons and splicing enhancers from exon junction arrays. | Kechris K et al. | β | 2008 | β |
| Prediction of human miRNAs using tissue-selective motifs in 3' UTRs. | Chang YM et al. | β | 2008 | β |
| Strategies for identifying RNA splicing regulatory motifs and predicting alternative splicing events. | Holste D et al. | β | 2008 | β |
| Testicular development and spermatogenesis: harvesting the postgenomics bounty. | Rolland AD et al. | β | 2008 | β |
| The impact of multiple splice sites in human L1 elements. | Belancio VP et al. | β | 2008 | β |
| Tissue-specific splicing factor gene expression signatures. | Grosso AR et al. | β | 2008 | β |
| Aberrant termination of reproduction-related TMEM30C transcripts in the hominoids. | Osada N et al. | β | 2007 | β |
| A detailed transcript-level probe annotation reveals alternative splicing based microarray platform differences. | Lee JC et al. | β | 2007 | β |
| Age and gender-dependent alternative splicing of P/Q-type calcium channel EF-hand. | Chang SY et al. | β | 2007 | β |
| Alternative splicing events identified in human embryonic stem cells and neural progenitors. | Yeo GW et al. | β | 2007 | β |
| Alternative splicing in cancer: noise, functional, or systematic? | Skotheim RI et al. | β | 2007 | β |
| A new advance in alternative splicing databases: from catalogue to detailed analysis of regulation of expression and function of human alternative splicing variants. | de la Grange P et al. | β | 2007 | β |
| A new genetic disorder in mitochondrial fatty acid beta-oxidation: ACAD9 deficiency. | He M et al. | β | 2007 | β |
| An intronic signal for alternative splicing in the human genome. | Havlioglu N et al. | β | 2007 | β |
| Characterising alternate splicing and tissue specific expression in the chicken from ESTs. | Tang H et al. | β | 2007 | β |
| Cloning and embryonic expression patterns of the chicken CELF family. | Brimacombe KR et al. | β | 2007 | β |
| Comparative genomics and evolution of alternative splicing: the pessimists' science. | Artamonova II et al. | β | 2007 | β |
| Discovery and analysis of evolutionarily conserved intronic splicing regulatory elements. | Yeo GW et al. | β | 2007 | β |
| Discovery of tissue-specific exons using comprehensive human exon microarrays. | Clark TA et al. | β | 2007 | β |
| Functional coordination of alternative splicing in the mammalian central nervous system. | Fagnani M et al. | β | 2007 | β |
| Gene discovery and transcript analyses in the corn smut pathogen Ustilago maydis: expressed sequence tag and genome sequence comparison. | Ho EC et al. | β | 2007 | β |
| Genome-wide detection of testis- and testicular cancer-specific alternative splicing. | He C et al. | β | 2007 | β |
| Global analysis of alternative splicing differences between humans and chimpanzees. | Calarco JA et al. | β | 2007 | β |
| Heritability of alternative splicing in the human genome. | Kwan T et al. | β | 2007 | β |
| Identification of differentially regulated splice variants and novel exons in glial brain tumors using exon expression arrays. | French PJ et al. | β | 2007 | β |
| Regulation of transcription of the RNA splicing factor hSlu7 by Elk-1 and Sp1 affects alternative splicing. | Alberstein M et al. | β | 2007 | β |
| The impact of alternative splicing in vivo: mouse models show the way. | MΓΆrΓΆy T et al. | β | 2007 | β |
| The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. | Makeyev EV et al. | β | 2007 | β |
| The testis-specific human protein RBMY recognizes RNA through a novel mode of interaction. | Skrisovska L et al. | β | 2007 | β |
| Three male germline-specific aldolase A isozymes are generated by alternative splicing and retrotransposition. | Vemuganti SA et al. | β | 2007 | β |
| Three novel ABCC5 splice variants in human retina and their role as regulators of ABCC5 gene expression. | Stojic J et al. | β | 2007 | β |
| Alternatively spliced Robo2 isoforms in zebrafish and rat. | Dalkic E et al. | β | 2006 | β |
| Alternative RNA splicing regulation in the testis. | Elliott DJ et al. | β | 2006 | β |
| Alternative splicing: new insights from global analyses. | Blencowe BJ | β | 2006 | β |
| An expectation-maximization algorithm for probabilistic reconstructions of full-length isoforms from splice graphs. | Xing Y et al. | β | 2006 | β |
| ASPIC: a web resource for alternative splicing prediction and transcript isoforms characterization. | CastrignanΓ² T et al. | β | 2006 | β |
| BodyMap-Xs: anatomical breakdown of 17 million animal ESTs for cross-species comparison of gene expression. | Ogasawara O et al. | β | 2006 | β |
| Comprehensive analysis of alternative splicing in rice and comparative analyses with Arabidopsis. | Campbell MA et al. | β | 2006 | β |
| Critical appraisal of DNA microarrays in psychiatric genomics. | Mirnics K et al. | β | 2006 | β |
| Data analysis of alternative splicing microarrays. | Cuperlovic-Culf M et al. | β | 2006 | β |
| Defective splicing, disease and therapy: searching for master checkpoints in exon definition. | Buratti E et al. | β | 2006 | β |
| Djinn Lite: a tool for customised gene transcript modelling, annotation-data enrichment and exploration. | Teber ET et al. | β | 2006 | β |
| General and specific functions of exonic splicing silencers in splicing control. | Wang Z et al. | β | 2006 | β |
| Generation of neuronal variability and complexity. | Muotri AR et al. | β | 2006 | β |
| HOLLYWOOD: a comparative relational database of alternative splicing. | Holste D et al. | β | 2006 | β |
| In silico and in vivo splicing analysis of MLH1 and MSH2 missense mutations shows exon- and tissue-specific effects. | Lastella P et al. | β | 2006 | β |
| LINE-1 RNA splicing and influences on mammalian gene expression. | Belancio VP et al. | β | 2006 | β |
| Maps, codes, and sequence elements: can we predict the protein output from an alternatively spliced locus? | Sharma S et al. | β | 2006 | β |
| Microarray analysis of alternative splicing. | Cuperlovic-Culf M et al. | β | 2006 | β |
| Model of stimulation-responsive splicing and strategies in identification of immunogenic isoforms of tumor antigens and autoantigens. | Yang F et al. | β | 2006 | β |
| Prediction of mRNA polyadenylation sites by support vector machine. | Cheng Y et al. | β | 2006 | β |
| Splicing regulation in neurologic disease. | Licatalosi DD et al. | β | 2006 | β |
| The effects of multiple features of alternatively spliced exons on the K(A)/K(S) ratio test. | Chen FC et al. | β | 2006 | β |
| TISA: tissue-specific alternative splicing in human and mouse genes. | Noh SJ et al. | β | 2006 | β |
| A combinatorial code for splicing silencing: UAGG and GGGG motifs. | Han K et al. | β | 2005 | β |
| ASePCR: alternative splicing electronic RT-PCR in multiple tissues and organs. | Kim N et al. | β | 2005 | β |
| Biased alternative polyadenylation in human tissues. | Zhang H et al. | β | 2005 | β |
| Comparison of splice sites in mammals and chicken. | Abril JF et al. | β | 2005 | β |
| Diversification of stem cell molecular repertoire by alternative splicing. | Pritsker M et al. | β | 2005 | β |
| Editing efficiency of a Drosophila gene correlates with a distant splice site selection. | Agrawal R et al. | β | 2005 | β |
| Evolutionarily conserved and diverged alternative splicing events show different expression and functional profiles. | Kan Z et al. | β | 2005 | β |
| Extraction of transcript diversity from scientific literature. | Shah PK et al. | β | 2005 | β |
| FAST DB: a website resource for the study of the expression regulation of human gene products. | de la Grange P et al. | β | 2005 | β |
| GMAP: a genomic mapping and alignment program for mRNA and EST sequences. | Wu TD et al. | β | 2005 | β |
| High-throughput alternative splicing quantification by primer extension and matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. | McCullough RM et al. | β | 2005 | β |
| Human netrin-G1 isoforms show evidence of differential expression. | Meerabux JM et al. | β | 2005 | β |
| Interpretation of shotgun proteomic data: the protein inference problem. | Nesvizhskii AI et al. | β | 2005 | β |
| Non-EST based prediction of exon skipping and intron retention events using Pfam information. | Hiller M et al. | β | 2005 | β |
| Protein modularity of alternatively spliced exons is associated with tissue-specific regulation of alternative splicing. | Xing Y et al. | β | 2005 | β |
| Recognition of unknown conserved alternatively spliced exons. | Ohler U et al. | β | 2005 | β |
| Substitution rate and structural divergence of 5'UTR evolution: comparative analysis between human and cynomolgus monkey cDNAs. | Osada N et al. | β | 2005 | β |
| The mRNA encoding tauCstF-64 is expressed ubiquitously in mouse tissues. | Huber Z et al. | β | 2005 | β |
| Transcriptome analysis of human gastric cancer. | Oh JH et al. | β | 2005 | β |
| Understanding alternative splicing: towards a cellular code. | Matlin AJ et al. | β | 2005 | β |
| Up-regulation of the ubiquitous alternative splicing factor Tra2beta causes inclusion of a germ cell-specific exon. | Venables JP et al. | β | 2005 | β |
| Systematic identification and analysis of exonic splicing silencers. | Wang Z et al. | β | 2004 | β |