Natural RNA circles function as efficient microRNA sponges
Abstract
MicroRNAs (miRNAs) are important post-transcriptional regulators of gene expression that act by direct base pairing to target sites within untranslated regions of messenger RNAs. Recently, miRNA activity has been shown to be affected by the presence of miRNA sponge transcripts, the so-called competing endogenous RNA in humans and target mimicry in plants. We previously identified a highly expressed circular RNA (circRNA) in human and mouse brain. Here we show that this circRNA acts as a miR-7 sponge; we term this circular transcript ciRS-7 (circular RNA sponge for miR-7). ciRS-7 contains more than 70 selectively conserved miRNA target sites, and it is highly and widely associated with Argonaute (AGO) proteins in a miR-7-dependent manner. Although the circRNA is completely resistant to miRNA-mediated target destabilization, it strongly suppresses miR-7 activity, resulting in increased levels of miR-7 targets. In the mouse brain, we observe overlapping co-expression of ciRS-7 and miR-7, particularly in neocortical and hippocampal neurons, suggesting a high degree of endogenous interaction. We further show that the testis-specific circRNA, sex-determining region Y (Sry), serves as a miR-138 sponge, suggesting that miRNA sponge effects achieved by circRNA formation are a general phenomenon. This study serves as the first, to our knowledge, functional analysis of a naturally expressed circRNA.
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Decreased circCDR1-AS levels lead to downregulation of mRNAs targeted by miR-7.
“As decreased circCDR1-AS levels lead to downregulation of mRNAs targeted by miR-7 [621]”
From Molecular and cellular mechanisms underlying the pathogenesis of Alzheimer’s disease (2020) · cites this paper as [621]
CircRNAs participate in the development of diseases by regulating gene expression at several levels, such as regulating mRNA splicing and transcription, interacting with RNA-binding proteins (RBPs), and acting as miRNA sponges.
“Independent of the mechanism of synthesis, circRNAs participate in the development of diseases by regulating gene expression at several levels, such as regulating mRNA splicing and transcription, interacting with RNA-binding proteins (RBPs), and acting as miRNA sponges [14].”
From Circular RNAs in depression: Biogenesis, function, expression, and therapeutic potential (2021) · cites this paper as [14]
CircRNAs act as miRNA sponges by binding and inhibiting miRNAs, thereby regulating target gene expression at transcriptional and post-transcriptional levels.
“Similar to competitive endogenous RNA (ceRNA), circRNAs act as sponges to bind and inhibit the activity of miRNAs [14], thus regulating the expression of target genes at the transcriptional and post-transcriptional levels through destabilization and translational silencing of mRNAs [15].”
From Circular RNAs in depression: Biogenesis, function, expression, and therapeutic potential (2021) · cites this paper as [14]
CDR1as circRNA acts as a miR-7 sponge and is named ciRS-7; ciRS-7 contains more than 70 selectively conserved miRNA target sites.
“Hansen et al. have shown that the human cerebellar degeneration-related protein 1 antisense (CDR1as) circRNA acts as a miR-7 sponge and named this circular transcript circular RNA sponge for miR-7 (ciRS-7).CiRS-7 contains more than 70 selectively conserved miRNA target sites [14].”
From Circular RNAs in depression: Biogenesis, function, expression, and therapeutic potential (2021) · cites this paper as [14]
CircRNAs may act as miRNA sponges by interacting with RBPs, and regulating mRNA transcription, splicing, and translation.
“CircRNAs may act as miRNA sponges by interacting with RBPs, and regulating mRNA transcription, splicing, and translation [14,41,51].”
From Circular RNAs in depression: Biogenesis, function, expression, and therapeutic potential (2021) · cites this paper as [14]
CiRS-7 is abundantly expressed in the mammalian brain, where it increases the translation of the miR-7 target mRNA.
“CiRS-7 is abundantly expressed in the mammalian brain [49,62], where it increases the translation of the miR-7 target mRNA [14,49].”
From Circular RNAs in depression: Biogenesis, function, expression, and therapeutic potential (2021) · cites this paper as [14]
The circRNA of human CDR1as/ciRS-7 is a miR-7 sponge, harbors 74 binding sites for miR-7, and binds to the argonaute (AGO) protein in a miR-7-dependent manner; this allows it to participate in the initiation and progression of PD.
“Interestingly, the circRNA of human CDR1as/ciRS-7 is a miR-7 sponge, which harbors 74 binding sites for miR-7 and is able to bind to the argonaute (AGO) protein in a miR-7-dependent manner.Binding to the AGO protein allows the circRNA of human CDR1as/ciRS-7 to participate in the initiation and progression of PD [14,70].”
From Circular RNAs in depression: Biogenesis, function, expression, and therapeutic potential (2021) · cites this paper as [14]
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- Authors
- Hansen, T. B., Jensen, T. I., Clausen, B. H., Bramsen, J. B., Finsen, B., Damgaard, C. K., & Kjems, J.
- Affiliations
- Aarhus University (DK)
- University of Southern Denmark (DK)
- Corresponding author
- Hansen, Thomas B.
- Kjems, Jørgen
- ORCID
- Venue
- Nature
- Published
- 2013-02-27
- Volume
- 495
- Issue
- 7441
- Pages
- 384-388
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2064165694
- Cited by
- 7,985
- References
- 28
- Citations by year
- 2026: 292 · 2025: 453 · 2024: 708 · 2023: 735 · 2022: 1053 · 2021: 1220 · 2020: 1044 · 2019: 791 · 2018: 598 · 2017: 398 · 2016: 230 · 2015: 189 · 2014: 163 · 2013: 96 · 2012: 1
- FWCI
- 101.31
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- University of Southern Denmark Research Portal (University of Southern Denmark) (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Natur og Univers, Det Frie Forskningsråd
- Lundbeckfonden (R83-2011-8232)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Circular RNAs in diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Keywords
- circular RNA, ciRS-7, microRNA sponge, miR-7, competing endogenous RNA, post-transcriptional regulation, Argonaute proteins, microRNA binding sites, SRY, miR-138, testis, brain neurons, hippocampus, neocortex
- MeSH terms
- RNA, Circular, Animals, Brain, Gene Expression Regulation, HeLa Cells, Humans, Male, Mice, Inbred C57BL, RNA, MicroRNAs, Mice, Sex-Determining Region Y Protein, HEK293 Cells, Argonaute Proteins
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