Global Patterns of Tissue-Specific Alternative Polyadenylation in Drosophila
We analyzed the usage and consequences of alternative cleavage and polyadenylation (APA) in Drosophila melanogaster by using >1 billion reads of stranded mRNA-seq across a variety of dissected tissues. Beyond demonstrating that a majority of fly transcripts are subject to APA, we observed broad t...
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| Published in | Cell reports (Cambridge) Vol. 1; no. 3; pp. 277 - 289 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
29.03.2012
Elsevier |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2211-1247 2211-1247 |
| DOI | 10.1016/j.celrep.2012.01.001 |
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| Abstract | We analyzed the usage and consequences of alternative cleavage and polyadenylation (APA) in Drosophila melanogaster by using >1 billion reads of stranded mRNA-seq across a variety of dissected tissues. Beyond demonstrating that a majority of fly transcripts are subject to APA, we observed broad trends for 3′ untranslated region (UTR) shortening in the testis and lengthening in the central nervous system (CNS); the latter included hundreds of unannotated extensions ranging up to 18 kb. Extensive northern analyses validated the accumulation of full-length neural extended transcripts, and in situ hybridization indicated their spatial restriction to the CNS. Genes encoding RNA binding proteins (RBPs) and transcription factors were preferentially subject to 3′ UTR extensions. Motif analysis indicated enrichment of miRNA and RBP sites in the neural extensions, and their termini were enriched in canonical cis elements that promote cleavage and polyadenylation. Altogether, we reveal broad tissue-specific patterns of APA in Drosophila and transcripts with unprecedented 3′ UTR length in the nervous system.
[Display omitted]
► >1 billion stranded RNA-seq reads generated across a panel of Drosophila tissues ► Broad trends of 3′ UTR shortening in testis and lengthening in CNS observed ► CNS 3′ UTR extensions subject 100 s of genes to tissue-specific posttranscriptional control ► CNS 3′ UTR extensions enriched for genes encoding nucleic-acid-binding proteins
Alternative cleavage and polyadenylation is a widespread mechanism that generates 3′ UTR diversity. Using stranded mRNA-seq in Drosophila, Lai and colleagues uncover global trends for 3′ UTR shortening in the testis and lengthening in the CNS. Their extensive experimental validation demonstrates the extraordinary length of many previously unannotated 3′ UTR extensions and their CNS-specific expression. Enrichment of miRNA target sites and RNA binding protein sites in these extended 3′ UTRs suggests important regulatory roles for these extensions in the CNS. |
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| AbstractList | We analyzed the usage and consequences of alternative cleavage and polyadenylation (APA) in Drosophila melanogaster by using >1 billion reads of stranded mRNA-seq across a variety of dissected tissues. Beyond demonstrating that a majority of fly transcripts are subject to APA, we observed broad trends for 3' untranslated region (UTR) shortening in the testis and lengthening in the central nervous system (CNS); the latter included hundreds of unannotated extensions ranging up to 18 kb. Extensive northern analyses validated the accumulation of full-length neural extended transcripts, and in situ hybridization indicated their spatial restriction to the CNS. Genes encoding RNA binding proteins (RBPs) and transcription factors were preferentially subject to 3' UTR extensions. Motif analysis indicated enrichment of miRNA and RBP sites in the neural extensions, and their termini were enriched in canonical cis elements that promote cleavage and polyadenylation. Altogether, we reveal broad tissue-specific patterns of APA in Drosophila and transcripts with unprecedented 3' UTR length in the nervous system. We analyzed the usage and consequences of alternative cleavage and polyadenylation (APA) in Drosophila melanogaster by using >1 billion reads of stranded mRNA-seq across a variety of dissected tissues. Beyond demonstrating that a majority of fly transcripts are subject to APA, we observed broad trends for 3′ untranslated region (UTR) shortening in the testis and lengthening in the central nervous system (CNS); the latter included hundreds of unannotated extensions ranging up to 18 kb. Extensive northern analyses validated the accumulation of full-length neural extended transcripts, and in situ hybridization indicated their spatial restriction to the CNS. Genes encoding RNA binding proteins (RBPs) and transcription factors were preferentially subject to 3′ UTR extensions. Motif analysis indicated enrichment of miRNA and RBP sites in the neural extensions, and their termini were enriched in canonical cis elements that promote cleavage and polyadenylation. Altogether, we reveal broad tissue-specific patterns of APA in Drosophila and transcripts with unprecedented 3′ UTR length in the nervous system. We analyzed the usage and consequences of alternative cleavage and polyadenylation (APA) in Drosophila melanogaster by using >1 billion reads of stranded mRNA-seq across a variety of dissected tissues. Beyond demonstrating that a majority of fly transcripts are subject to APA, we observed broad trends for 3′ untranslated region (UTR) shortening in the testis and lengthening in the central nervous system (CNS); the latter included hundreds of unannotated extensions ranging up to 18 kb. Extensive northern analyses validated the accumulation of full-length neural extended transcripts, and in situ hybridization indicated their spatial restriction to the CNS. Genes encoding RNA binding proteins (RBPs) and transcription factors were preferentially subject to 3′ UTR extensions. Motif analysis indicated enrichment of miRNA and RBP sites in the neural extensions, and their termini were enriched in canonical cis elements that promote cleavage and polyadenylation. Altogether, we reveal broad tissue-specific patterns of APA in Drosophila and transcripts with unprecedented 3′ UTR length in the nervous system. We analyzed the usage and consequences of alternative cleavage and polyadenylation (APA) in Drosophila melanogaster by using >1 billion reads of stranded mRNA-seq across a variety of dissected tissues. Beyond demonstrating that a majority of fly transcripts are subject to APA, we observed broad trends for 3′ untranslated region (UTR) shortening in the testis and lengthening in the central nervous system (CNS); the latter included hundreds of unannotated extensions ranging up to 18 kb. Extensive northern analyses validated the accumulation of full-length neural extended transcripts, and in situ hybridization indicated their spatial restriction to the CNS. Genes encoding RNA binding proteins (RBPs) and transcription factors were preferentially subject to 3′ UTR extensions. Motif analysis indicated enrichment of miRNA and RBP sites in the neural extensions, and their termini were enriched in canonical cis elements that promote cleavage and polyadenylation. Altogether, we reveal broad tissue-specific patterns of APA in Drosophila and transcripts with unprecedented 3′ UTR length in the nervous system. [Display omitted] ► >1 billion stranded RNA-seq reads generated across a panel of Drosophila tissues ► Broad trends of 3′ UTR shortening in testis and lengthening in CNS observed ► CNS 3′ UTR extensions subject 100 s of genes to tissue-specific posttranscriptional control ► CNS 3′ UTR extensions enriched for genes encoding nucleic-acid-binding proteins Alternative cleavage and polyadenylation is a widespread mechanism that generates 3′ UTR diversity. Using stranded mRNA-seq in Drosophila, Lai and colleagues uncover global trends for 3′ UTR shortening in the testis and lengthening in the CNS. Their extensive experimental validation demonstrates the extraordinary length of many previously unannotated 3′ UTR extensions and their CNS-specific expression. Enrichment of miRNA target sites and RNA binding protein sites in these extended 3′ UTRs suggests important regulatory roles for these extensions in the CNS. We analyzed the usage and consequences of alternative cleavage and polyadenylation (APA) in Drosophila melanogaster by using >1 billion reads of stranded mRNA-seq across a variety of dissected tissues. Beyond demonstrating that a majority of fly transcripts are subject to APA, we observed broad trends for 3' untranslated region (UTR) shortening in the testis and lengthening in the central nervous system (CNS); the latter included hundreds of unannotated extensions ranging up to 18 kb. Extensive northern analyses validated the accumulation of full-length neural extended transcripts, and in situ hybridization indicated their spatial restriction to the CNS. Genes encoding RNA binding proteins (RBPs) and transcription factors were preferentially subject to 3' UTR extensions. Motif analysis indicated enrichment of miRNA and RBP sites in the neural extensions, and their termini were enriched in canonical cis elements that promote cleavage and polyadenylation. Altogether, we reveal broad tissue-specific patterns of APA in Drosophila and transcripts with unprecedented 3' UTR length in the nervous system.We analyzed the usage and consequences of alternative cleavage and polyadenylation (APA) in Drosophila melanogaster by using >1 billion reads of stranded mRNA-seq across a variety of dissected tissues. Beyond demonstrating that a majority of fly transcripts are subject to APA, we observed broad trends for 3' untranslated region (UTR) shortening in the testis and lengthening in the central nervous system (CNS); the latter included hundreds of unannotated extensions ranging up to 18 kb. Extensive northern analyses validated the accumulation of full-length neural extended transcripts, and in situ hybridization indicated their spatial restriction to the CNS. Genes encoding RNA binding proteins (RBPs) and transcription factors were preferentially subject to 3' UTR extensions. Motif analysis indicated enrichment of miRNA and RBP sites in the neural extensions, and their termini were enriched in canonical cis elements that promote cleavage and polyadenylation. Altogether, we reveal broad tissue-specific patterns of APA in Drosophila and transcripts with unprecedented 3' UTR length in the nervous system. |
| Author | Eads, Brian D. Lai, Eric C. Miura, Pedro Celniker, Susan E. Eisman, Robert C. May, Gemma Westholm, Jakub O. Carlson, Joe Brown, James B. Shenker, Sol Duff, Michael O. Kaufman, Thomas Cherbas, Peter Andrews, Justen Graveley, Brenton R. Smibert, Peter Zhang, Dayu |
| AuthorAffiliation | 2 Department of Genetics and Developmental Biology, University of Connecticut Health Center, Farmington, CT 06030-6403, USA 3 Center for Genomics and Bioinformatics, Indiana University, Bloomington, IN 47405, USA 1 Department of Developmental Biology, Sloan-Kettering Institute, New York, NY 10065, USA 5 Department of Genome Dynamics, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA 4 Department of Biology, Indiana University, Bloomington, IN 47405, USA |
| AuthorAffiliation_xml | – name: 2 Department of Genetics and Developmental Biology, University of Connecticut Health Center, Farmington, CT 06030-6403, USA – name: 1 Department of Developmental Biology, Sloan-Kettering Institute, New York, NY 10065, USA – name: 4 Department of Biology, Indiana University, Bloomington, IN 47405, USA – name: 5 Department of Genome Dynamics, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA – name: 3 Center for Genomics and Bioinformatics, Indiana University, Bloomington, IN 47405, USA |
| Author_xml | – sequence: 1 givenname: Peter surname: Smibert fullname: Smibert, Peter organization: Department of Developmental Biology, Sloan-Kettering Institute, New York, NY 10065, USA – sequence: 2 givenname: Pedro surname: Miura fullname: Miura, Pedro organization: Department of Developmental Biology, Sloan-Kettering Institute, New York, NY 10065, USA – sequence: 3 givenname: Jakub O. surname: Westholm fullname: Westholm, Jakub O. organization: Department of Developmental Biology, Sloan-Kettering Institute, New York, NY 10065, USA – sequence: 4 givenname: Sol surname: Shenker fullname: Shenker, Sol organization: Department of Developmental Biology, Sloan-Kettering Institute, New York, NY 10065, USA – sequence: 5 givenname: Gemma surname: May fullname: May, Gemma organization: Department of Genetics and Developmental Biology, University of Connecticut Health Center, Farmington, CT 06030-6403, USA – sequence: 6 givenname: Michael O. surname: Duff fullname: Duff, Michael O. organization: Department of Genetics and Developmental Biology, University of Connecticut Health Center, Farmington, CT 06030-6403, USA – sequence: 7 givenname: Dayu surname: Zhang fullname: Zhang, Dayu organization: Center for Genomics and Bioinformatics, Indiana University, Bloomington, IN 47405, USA – sequence: 8 givenname: Brian D. surname: Eads fullname: Eads, Brian D. organization: Department of Biology, Indiana University, Bloomington, IN 47405, USA – sequence: 9 givenname: Joe surname: Carlson fullname: Carlson, Joe organization: Department of Genome Dynamics, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA – sequence: 10 givenname: James B. surname: Brown fullname: Brown, James B. organization: Department of Genome Dynamics, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA – sequence: 11 givenname: Robert C. surname: Eisman fullname: Eisman, Robert C. organization: Department of Biology, Indiana University, Bloomington, IN 47405, USA – sequence: 12 givenname: Justen surname: Andrews fullname: Andrews, Justen organization: Department of Biology, Indiana University, Bloomington, IN 47405, USA – sequence: 13 givenname: Thomas surname: Kaufman fullname: Kaufman, Thomas organization: Department of Biology, Indiana University, Bloomington, IN 47405, USA – sequence: 14 givenname: Peter surname: Cherbas fullname: Cherbas, Peter organization: Center for Genomics and Bioinformatics, Indiana University, Bloomington, IN 47405, USA – sequence: 15 givenname: Susan E. surname: Celniker fullname: Celniker, Susan E. email: celniker@fruitfly.org organization: Department of Genome Dynamics, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA – sequence: 16 givenname: Brenton R. surname: Graveley fullname: Graveley, Brenton R. email: graveley@neuron.uchc.edu organization: Department of Genetics and Developmental Biology, University of Connecticut Health Center, Farmington, CT 06030-6403, USA – sequence: 17 givenname: Eric C. surname: Lai fullname: Lai, Eric C. email: laie@mskcc.org organization: Department of Developmental Biology, Sloan-Kettering Institute, New York, NY 10065, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22685694$$D View this record in MEDLINE/PubMed |
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| Snippet | We analyzed the usage and consequences of alternative cleavage and polyadenylation (APA) in Drosophila melanogaster by using >1 billion reads of stranded... We analyzed the usage and consequences of alternative cleavage and polyadenylation (APA) in Drosophila melanogaster by using >1 billion reads of stranded... |
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| SubjectTerms | 3' Untranslated Regions - genetics Animals Base Sequence Blotting, Northern Conserved Sequence - genetics DNA-Binding Proteins - metabolism Drosophila melanogaster Drosophila melanogaster - embryology Drosophila melanogaster - genetics Embryo, Nonmammalian - metabolism Gene Expression Regulation, Developmental Genes, Insect - genetics In Situ Hybridization Male Molecular Sequence Data Neurons - cytology Neurons - metabolism Nucleotide Motifs - genetics Organ Specificity - genetics Poly A - metabolism Polyadenylation - genetics Protein Isoforms - genetics Protein Isoforms - metabolism Reproducibility of Results RNA, Messenger - genetics RNA, Messenger - metabolism Sequence Analysis, RNA Testis - metabolism Transcriptome - genetics |
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| Title | Global Patterns of Tissue-Specific Alternative Polyadenylation in Drosophila |
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