Genome-wide Analysis of Drosophila Circular RNAs Reveals Their Structural and Sequence Properties and Age-Dependent Neural Accumulation

Westholm, Jakub O.; Miura, Pedro; Olson, Sara; Shenker, Sol; Joseph, Brian; Sanfilippo, Piero; Celniker, Susan E.; Graveley, Brenton R.; Lai, Eric C.

doi:10.1016/j.celrep.2014.10.062

Title: Genome-wide Analysis of Drosophila Circular RNAs Reveals Their Structural and Sequence Properties and Age-Dependent Neural Accumulation

Abstract

Circularization was recently recognized to broadly expand transcriptome complexity. Here, we exploit massive Drosophila total RNA-sequencing data, >5 billion paired-end reads from >100 libraries covering diverse developmental stages, tissues, and cultured cells, to rigorously annotate >2,500 fruit fly circular RNAs. These mostly derive from back-splicing of protein-coding genes and lack poly(A) tails, and the circularization of hundreds of genes is conserved across multiple Drosophila species. We elucidate structural and sequence properties of Drosophila circular RNAs, which exhibit commonalities and distinctions from mammalian circles. Notably, Drosophila circular RNAs harbor >1,000 well-conserved canonical miRNA seed matches, especially within coding regions, and coding conserved miRNA sites reside preferentially within circularized exons. Finally, we analyze the developmental and tissue specificity of circular RNAs and note their preferred derivation from neural genes and enhanced accumulation in neural tissues. Interestingly, circular isoforms increase substantially relative to linear isoforms during CNS aging and constitute an aging biomarker.

Authors:: Westholm, Jakub O.; Miura, Pedro; Olson, Sara; Shenker, Sol; Joseph, Brian; Sanfilippo, Piero; Celniker, Susan E.; Graveley, Brenton R.; Lai, Eric C.

Publication Date:: Mon Dec 01 00:00:00 EST 2014

Research Org.:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE; National Institutes of Health (NIH)

OSTI Identifier:: 1227570

Alternate Identifier(s):: OSTI ID: 1207947

Grant/Contract Number:: U54-HG006994; R01-GM95296; R01-GM083300; 1004721; R01-NS083833; AC02-05CH11231

Resource Type:: Published Article

Journal Name:: Cell Reports

Additional Journal Information:: Journal Name: Cell Reports Journal Volume: 9 Journal Issue: 5; Journal ID: ISSN 2211-1247

Publisher:: Elsevier

Country of Publication:: Netherlands

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Westholm, Jakub O., Miura, Pedro, Olson, Sara, Shenker, Sol, Joseph, Brian, Sanfilippo, Piero, Celniker, Susan E., Graveley, Brenton R., and Lai, Eric C. Genome-wide Analysis of Drosophila Circular RNAs Reveals Their Structural and Sequence Properties and Age-Dependent Neural Accumulation.  Netherlands: N. p., 2014. 
Web.  doi:10.1016/j.celrep.2014.10.062.

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                    Westholm, Jakub O., Miura, Pedro, Olson, Sara, Shenker, Sol, Joseph, Brian, Sanfilippo, Piero, Celniker, Susan E., Graveley, Brenton R., & Lai, Eric C. Genome-wide Analysis of Drosophila Circular RNAs Reveals Their Structural and Sequence Properties and Age-Dependent Neural Accumulation.  Netherlands.  https://doi.org/10.1016/j.celrep.2014.10.062

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                    Westholm, Jakub O., Miura, Pedro, Olson, Sara, Shenker, Sol, Joseph, Brian, Sanfilippo, Piero, Celniker, Susan E., Graveley, Brenton R., and Lai, Eric C. Mon .  
"Genome-wide Analysis of Drosophila Circular RNAs Reveals Their Structural and Sequence Properties and Age-Dependent Neural Accumulation".  Netherlands.  https://doi.org/10.1016/j.celrep.2014.10.062.

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@article{osti_1227570,

  title        = {Genome-wide Analysis of Drosophila Circular RNAs Reveals Their Structural and Sequence Properties and Age-Dependent Neural Accumulation},

  author       = {Westholm, Jakub O. and Miura, Pedro and Olson, Sara and Shenker, Sol and Joseph, Brian and Sanfilippo, Piero and Celniker, Susan E. and Graveley, Brenton R. and Lai, Eric C.},

  abstractNote = {Circularization was recently recognized to broadly expand transcriptome complexity. Here, we exploit massive Drosophila total RNA-sequencing data, >5 billion paired-end reads from >100 libraries covering diverse developmental stages, tissues, and cultured cells, to rigorously annotate >2,500 fruit fly circular RNAs. These mostly derive from back-splicing of protein-coding genes and lack poly(A) tails, and the circularization of hundreds of genes is conserved across multiple Drosophila species. We elucidate structural and sequence properties of Drosophila circular RNAs, which exhibit commonalities and distinctions from mammalian circles. Notably, Drosophila circular RNAs harbor >1,000 well-conserved canonical miRNA seed matches, especially within coding regions, and coding conserved miRNA sites reside preferentially within circularized exons. Finally, we analyze the developmental and tissue specificity of circular RNAs and note their preferred derivation from neural genes and enhanced accumulation in neural tissues. Interestingly, circular isoforms increase substantially relative to linear isoforms during CNS aging and constitute an aging biomarker.},

  doi          = {10.1016/j.celrep.2014.10.062},

  journal      = {Cell Reports},

  number       = 5,

  volume       = 9,

  place        = {Netherlands},

  year         = {Mon Dec 01 00:00:00 EST 2014},

  month        = {Mon Dec 01 00:00:00 EST 2014}

}

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Title: Genome-wide Analysis of Drosophila Circular RNAs Reveals Their Structural and Sequence Properties and Age-Dependent Neural Accumulation

Abstract

Citation Formats

circRNA Biogenesis Competes with Pre-mRNA Splicing journal, October 2014

Circular RNAs are a large class of animal RNAs with regulatory potency journal, February 2013

Widespread and extensive lengthening of 3' UTRs in the mammalian brain journal, March 2013

STAR: ultrafast universal RNA-seq aligner journal, October 2012

The intervening sequence of the ribosomal RNA precursor is converted to a circular RNA in isolated nuclei of tetrahymena journal, February 1981

Biological basis for restriction of microRNA targets to the 3′ untranslated region in mammalian mRNAs journal, February 2009

Deep annotation of Drosophila melanogaster microRNAs yields insights into their processing, modification, and emergence journal, December 2010

Using FlyAtlas to identify better Drosophila melanogaster models of human disease journal, May 2007

Neural-specific elongation of 3' UTRs during Drosophila development journal, September 2011

MicroRNA Targeting Specificity in Mammals: Determinants beyond Seed Pairing journal, July 2007

Noncanonical RNAs From Transcripts of the Drosophila muscleblind Gene journal, May 2006

Global Patterns of Tissue-Specific Alternative Polyadenylation in Drosophila journal, March 2012

Cell-Type Specific Features of Circular RNA Expression journal, September 2013

Expanded identification and characterization of mammalian circular RNAs journal, July 2014

Mis-splicing yields circular RNA molecules. journal, January 1993

The developmental transcriptome of Drosophila melanogaster journal, December 2010

Complementary Sequence-Mediated Exon Circularization journal, September 2014

Global analysis of trans-splicing in Drosophila journal, July 2010

Circular RNAs are abundant, conserved, and associated with ALU repeats journal, December 2012

Gene Ontology: tool for the unification of biology journal, May 2000

Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs journal, December 2007

Scrambled exons journal, February 1991

Diversity and dynamics of the Drosophila transcriptome journal, March 2014

Detecting and characterizing circular RNAs journal, May 2014

Natural RNA circles function as efficient microRNA sponges journal, February 2013

Identification of Functional Elements and Regulatory Circuits by Drosophila modENCODE journal, December 2010

Regulation of Vertebrate Nervous System Alternative Splicing and Development by an SR-Related Protein journal, September 2009

Diversity of miRNAs, siRNAs, and piRNAs across 25 Drosophila cell lines journal, July 2014

Transcriptome-wide discovery of circular RNAs in Archaea journal, December 2011

Post-transcriptional exon shuffling events in humans can be evolutionarily conserved and abundant journal, September 2011

Conserved microRNA targeting in Drosophila is as widespread in coding regions as in 3'UTRs journal, August 2010

The regulatory activity of microRNA* species has substantial influence on microRNA and 3′ UTR evolution journal, March 2008

Circular RNAs Are the Predominant Transcript Isoform from Hundreds of Human Genes in Diverse Cell Types journal, February 2012

A computational analysis of sequence features involved in recognition of short introns journal, September 2001

Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. journal, November 1976

Circular transcripts of the testis-determining gene Sry in adult mouse testis journal, June 1993

circRNA Biogenesis Competes with Pre-mRNA Splicing
journal, October 2014

Circular RNAs are a large class of animal RNAs with regulatory potency
journal, February 2013

Widespread and extensive lengthening of 3' UTRs in the mammalian brain
journal, March 2013

STAR: ultrafast universal RNA-seq aligner
journal, October 2012

The intervening sequence of the ribosomal RNA precursor is converted to a circular RNA in isolated nuclei of tetrahymena
journal, February 1981

Biological basis for restriction of microRNA targets to the 3′ untranslated region in mammalian mRNAs
journal, February 2009

Deep annotation of Drosophila melanogaster microRNAs yields insights into their processing, modification, and emergence
journal, December 2010

Using FlyAtlas to identify better Drosophila melanogaster models of human disease
journal, May 2007

Neural-specific elongation of 3' UTRs during Drosophila development
journal, September 2011

MicroRNA Targeting Specificity in Mammals: Determinants beyond Seed Pairing
journal, July 2007

Noncanonical RNAs From Transcripts of the Drosophila muscleblind Gene
journal, May 2006

Global Patterns of Tissue-Specific Alternative Polyadenylation in Drosophila
journal, March 2012

Cell-Type Specific Features of Circular RNA Expression
journal, September 2013

Expanded identification and characterization of mammalian circular RNAs
journal, July 2014

Mis-splicing yields circular RNA molecules.
journal, January 1993

The developmental transcriptome of Drosophila melanogaster
journal, December 2010

Complementary Sequence-Mediated Exon Circularization
journal, September 2014

Global analysis of trans-splicing in Drosophila
journal, July 2010

Circular RNAs are abundant, conserved, and associated with ALU repeats
journal, December 2012

Gene Ontology: tool for the unification of biology
journal, May 2000

Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs
journal, December 2007

Scrambled exons
journal, February 1991

Diversity and dynamics of the Drosophila transcriptome
journal, March 2014

Detecting and characterizing circular RNAs
journal, May 2014

Natural RNA circles function as efficient microRNA sponges
journal, February 2013

Identification of Functional Elements and Regulatory Circuits by Drosophila modENCODE
journal, December 2010

Regulation of Vertebrate Nervous System Alternative Splicing and Development by an SR-Related Protein
journal, September 2009

Diversity of miRNAs, siRNAs, and piRNAs across 25 Drosophila cell lines
journal, July 2014

Transcriptome-wide discovery of circular RNAs in Archaea
journal, December 2011

Post-transcriptional exon shuffling events in humans can be evolutionarily conserved and abundant
journal, September 2011

Conserved microRNA targeting in Drosophila is as widespread in coding regions as in 3'UTRs
journal, August 2010

The regulatory activity of microRNA* species has substantial influence on microRNA and 3′ UTR evolution
journal, March 2008

Circular RNAs Are the Predominant Transcript Isoform from Hundreds of Human Genes in Diverse Cell Types
journal, February 2012

A computational analysis of sequence features involved in recognition of short introns
journal, September 2001

Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures.
journal, November 1976

Circular transcripts of the testis-determining gene Sry in adult mouse testis
journal, June 1993